From: Subject: Induction of Potent Antitumor Immunity by Intratumoral Injection of Interleukin 23-Transduced Dendritic Cells -- Hu et al. 66 (17): 8887 -- Cancer Research Date: Wed, 16 Jan 2008 17:55:07 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C85868.EE2C41A0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C85868.EE2C41A0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/66/17/8887 Induction of Potent Antitumor Immunity by = Intratumoral Injection of Interleukin 23-Transduced Dendritic Cells -- = Hu et al. 66 (17): 8887 -- Cancer Research 3D"Cancer 3D"
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[Cancer Research 66, 8887-8896, September 1, = 2006]
=A9 2006 American = Association=20 for Cancer Research

Immunology

Induction of Potent Antitumor Immunity by Intratumoral Injection of=20 Interleukin 23=96Transduced Dendritic Cells =

Jinwei=20 Hu1, Xiangpeng Yuan1, = Maria L.=20 Belladonna3, John M. Ong1,=20 Sebastian Wachsmann-Hogiu2, Daniel L.=20 Farkas2, Keith L. Black1 and=20 John S. Yu1

1 Maxine Dunitz Neurosurgical Institute = and=20 2 Department of Surgery, Cedars-Sinai Medical Center, Los = Angeles,=20 California and 3 Department of Experimental Medicine, = University of=20 Perugia, Perugia, Italy

Requests for reprints: John S. Yu, Maxine = Dunitz=20 Neurosurgical Institute, Cedars-Sinai Medical Center, Suite 800 East, = 8631 West=20 3rd Street, Los Angeles, CA 90048. Phone: 310-423-0845; Fax: = 310-423-0810;=20 E-mail: yuj{at}cshs.org .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
D= endritic=20 cells (DCs) are potent antigen-presenting cells that play a = critical=20 role in priming immune responses to tumor. Interleukin = (IL)-23 can=20 act directly on DC to promote immunogenic presentation of = tumor=20 peptide in vitro. Here, we evaluated the combination = of bone=20 marrow=96derived DC and IL-23 on the induction of antitumor = immunity in=20 a mouse intracranial glioma model. DCs can be transduced by = an=20 adenoviral vector coding single-chain mouse IL-23 to express = high=20 levels of bioactive IL-23. Intratumoral implantation of=20 IL-23=96expressing DCs produced a protective effect on = intracranial=20 tumor=96bearing mice. The mice consequently gained systemic = immunity=20 against the same tumor rechallenge. The protective effect of=20 IL-23=96expressing DCs was comparable with or even better = than that of=20 IL-12-expressing DCs. IL-23=96transduced DC (DC-IL-23) = treatment=20 resulted in robust intratumoral CD8+ and = CD4+=20 T-cell infiltration and induced a specific TH1-type response = to the=20 tumor in regional lymph nodes and spleen at levels greater = than those=20 of nontransduced DCs. Moreover, splenocytes from animals = treated with=20 DC-IL-23 showed heightened levels of specific CTL activity. = In=20 vivo lymphocyte depletion experiments showed that the = antitumor=20 immunity induced by DC-IL-23 was mainly dependent on = CD8+=20 T cells and that CD4+ T cells and natural killer = cells=20 were also involved. In summary, i.t. injection of DC-IL-23 = resulted=20 in significant and effective systemic antitumor immunity in=20 intracranial tumor=96bearing mice. These findings suggest a = new=20 approach to induce potent tumor-specific immunity to = intracranial=20 tumors. This approach may have therapeutic potential for = treating=20 human glioma. (Cancer Res 2006; 66(17): 8887-96)


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
References
 
D= endritic=20 cells (DCs) are specialized antigen-presenting cells that = exist=20 virtually in every tissue and can both elicit primary and = boost=20 secondary immune responses (1=964).=20 Since the identification of their role in immunogenicity (1),=20 tremendous attention has been focused on the critical role of = DCs in=20 antitumor immune responses. DCs pulsed with synthetic tumor = peptides=20 induce an effective antitumor immune response in vitro = and=20 after adoptive transfer in mice (3,=20 5,=20 6).=20 Murine DCs can efficiently present antigens associated with = whole=20 tumor cell lysates to na=EFve and primed T cells in = vitro and=20 can elicit antitumor immunity resulting in tumor regression = in=20 vivo (7,=20 8).=20 Furthermore, DCs loaded with acid-eluted tumor peptide (9)=20 or RNA (10,=20 11)=20 are also effective in inducing immunity against tumors. = However,=20 these approaches require identifying tumor-specific peptides = or=20 harvesting sufficient tissue from solid human tumors as well = as the=20 cumbersome process of ex vivo DC pulsing.

An alternative approach to eliciting tumor antigen presentation = is=20 i.t. delivery of DC to allow tumor antigen capture in situ = at=20 the tumor site. Intratumoral administration of DCs into s.c. = growing=20 murine MT-901 breast tumor showed efficient uptake of = apoptotic tumor=20 cells by DC. Local injection of DC alone can result in = regression of=20 the tumor in vivo (12).=20 Intratumoral DC vaccination in intracranial tumor=96bearing = rats=20 resulted in prolonged survival and immunity to subsequent = tumor=20 rechallenge (13).=20 Intratumoral injection with IL-12 gene=96modified DC=20 significantly suppressed the growth of established intradermal = tumor=20 and induced a strong antitumor T-cell response (14).=20 After delivery of p53 gene=96transduced DC into = established=20 skin tumors, a systemic antitumor effect was induced and = tumor=20 growth was significantly inhibited. More importantly, the = i.t.=20 injection of p53-expressing DCs has a greater effect than = s.c.=20 immunization (15).=20 Furthermore, increased numbers of DC in solid tumor masses = led to=20 induction of potent antitumor immunity in animal models (16)=20 and better prognosis in some clinical studies (17).=20

Interleukin (IL)-23 is a newly discovered cytokine, which = consists=20 of a heterodimer of IL-12 P40 subunit and a novel protein, = P19.=20 It has been shown that IL-23 acts on memory T cells and DCs=20 directly to promote IL-12 and IFN-3D{gamma}=20 = production=20 in vitro (18,=20 19).=20 Of further importance, IL-23 can act directly on CD83D{alpha}=20+=20 DC to promote immunogenic presentation of an otherwise=20 tolerogenic tumor peptide (19).=20 Recently, it has been shown that IL-23=96expressing tumor = cells exhibit=20 antitumor and antimetastatic functions in s.c. colon = carcinoma model=20 (20).=20 We recently showed that IL-23=96expressing bone = marrow=96derived neural=20 stem cells display antitumor function in an intracranial = glioma model=20 (21).=20

Based on the essential role of i.t. administration of DCs in=20 initiating antitumor immune responses and on the promoting = role=20 of IL-23 in the DC presentation of tumor antigen, we = hypothesized=20 that i.t. delivery of IL-23 gene=96transduced DC may = offer=20 an efficient means for triggering immune responses in situ=20 within tumors, particularly in intracranial tumors. = Therefore, in=20 the present study, we adenovirally transduced bone=20 marrow=96derived DCs with IL-23 and studied the antitumor = effect of=20 i.t. administration of IL-23=96expressing DC in an = intracranial tumor=20 model. We found that i.t. injection with IL-23=96transduced = DC=20 (DC-IL-23) resulted in significantly prolonged survival in=20 intracranial tumor=96bearing mice and induced a strong=20 tumor-specific T-cell immune response. The antitumor effect = induced=20 by IL-23=96expressing DCs was comparable with or even better = than that=20 induced by IL-12-expressing DCs. Furthermore, = IL-23=96expressing=20 DC=96treated survivors were resistant to subsequent = intracranial=20 rechallenge with the same tumor.


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
References
 
<= B>Cell=20 lines and animals. GL26 (murine glioma) and B16-F10 (murine=20 melanoma) were maintained in RPMI 1640 supplemented with 10%=20 heat-inactivated fetal bovine serum (FBS), 2 mmol/L L-glutamine, 5 x=20 10=965 mol/L =DF-mercaptoethanol, and antibiotics = (all from=20 Invitrogen, Gaithersgurg, MD), referred to henceforth as CM.=20 GL26-DsRed was a derivative of GL26 and was obtained by = stable=20 transfection of red-fluorescent protein into GL26 cells. Six- = to=20 eight-week-old female C57BL/6 mice were purchased from The = Jackson=20 Laboratory (Bar Harbor, ME) and housed at the animal = maintenance=20 facility of Cedars-Sinai Medical Center. The animals were = used for=20 experiments at 8 to 10 weeks of age. All of the animals used = were=20 treated in strict accordance with the Institutional Animal = Care and=20 Use Committee of Cedars-Sinai Medical Center guidelines. =

Generation of bone marrow=96derived DCs and transduction = with=20 adenoviral vectors. Erythrocyte-depleted mouse bone marrow = cells=20 from flushed marrow cavities of femurs and tibias were = cultured=20 overnight in CM to remove the adherent macrophages. = Nonadherent cells=20 were then placed in fresh CM containing 10 ng/mL granulocyte=20 macrophage colony-stimulating factor and 10 ng/mL IL-4 on day = 1. On=20 day 5, DCs were harvested by gentle pipetting and were = resuspended at=20 5 x 106/mL in CM. Three=20 milliliters of the DC suspension were overlaid onto 3 mL of = CM-14.5%=20 (w/v) metrizamide (Sigma, St. Louis, MO) solution in a 15-mL=20 centrifuge tube. The resulting gradient was centrifuged at = 2,000 rpm,=20 brake off, 4=B0C, for 15 minutes. The low-density interface=20 containing the DCs was collected by pipette aspiration. The = DCs were=20 rinsed twice with HBSS, enumerated, and resuspended in PBS = for=20 adenoviral vector transduction.

Adenoviral vectors bearing genes for single-chain mouse IL-23=20 (AdIL-23), IL-12 (AdIL-12), LacZ (AdLacZ), or a 2.4-kb = noncoding=20 stuffer DNA (AdEmpty) were constructed as previously = described=20 (21)=20 and used to transduce DCs with a centrifugal method (22).=20 Briefly, 1 x 106 = DCs were=20 suspended in 500 =B5L of PBS containing 1% FBS and then mixed = with=20 adenoviral vector that was suspended in 500 =B5L of PBS = containing 1%=20 FBS. A multiplicity of infection (MOI) of 50 was used for all = the=20 transductions except for the study to generate similar = protein=20 expression level of either IL-23 or IL-12, which had a MOI of = 50 for=20 AdIL-12 transduction and a MOI of 20 for AdIL-23 = transduction. The=20 mixtures of DCs and viral vectors were centrifuged (2,000 = x g at 37=B0C) for 2 = hours. After=20 the centrifugal transduction process, the DCs were washed = twice in=20 PBS and used for subsequent experiments.

Animal studies in vivo. C57BL/6 mice (female, 8-10 = weeks=20 old) were anesthetized with i.p. ketamine and medetomidine, = and=20 stereotactically implanted with 1 x=20 104 GL26 or GL26-DsRed glioma cells in 2.5 =B5L of = 1.2%=20 methylcellulose/PBS in the right striatum as previously = described (21).=20 Three days after tumor implantation, the mice received three=20 injections (2.5 =B5L, 1 x = 105=20 cells) of either adenovirus-transduced DCs, nontransduced = DCs, or=20 saline every 7 days with the same coordinates as the tumor=20 implantation. For brain tissue analysis, the mice were = euthanized on=20 day 7 after the first i.t. DC injection by intracordic=20 perfusion-fixation with 4% paraformaldehyde. Animal brains = were cut=20 into 40-=B5m coral sections and processed for = immunohistochemistry=20 staining. In the tumor rechallenge experiment, surviving = animals=20 were inoculated with the same tumor cells on the = contralateral=20 side of the brain from the first tumor implantation. =

In the lymphocyte depletion experiments, mice were injected = i.p.=20 with 0.5 mg of rat anti-mouse CD8 (53-6.7) and anti-CD4 = (GK1.5; both=20 from American Type Culture Collection, Rockville, MD) = monoclonal=20 antibodies or with normal rat immunoglobulin G (IgG) as = control=20 antibody in 200 =B5L of PBS 1 day before tumor implantation, = once daily=20 for the following 3 consecutive days, and then twice a week. = Natural=20 killer (NK) cells were depleted by i.p. injection of 200 =B5g = of=20 anti-NK1.1 monoclonal antibody (clone PK136, BD PharMingen, = San=20 Diego, CA) or IgG2a as control using the same schedule as = above.=20 Lymphocyte depletion was confirmed in each depletion = experiment by=20 FACScan (Becton Dickinson, San Jose, CA) analysis of = peripheral=20 blood.

Flow cytometry. For phenotype analysis of DCs, = phycoerythrin-=20 or FITC-conjugated monoclonal antibodies against murine = cell-surface=20 molecules (MHC-I, MHC-II, CD11c, CD54, CD80, CD86, and = appropriate=20 isotype control; all from BD PharMingen) were used and = cytometric=20 analysis was done with a FACScan. For the CD8+ and=20 CD4+ T-cell infiltration experiment, brain tissues = of six=20 mice were pooled and homogenized, followed by Percoll = (Amersham=20 Biosciences, Piscataway, NJ) gradient centrifugation to = isolate=20 mononuclear cells. The isolated mononuclear cells were = stained by=20 FITC-CD4 (clone GK1.5) and phycoerythrin-CD8 (clone 53-6.7)=20 antibodies (BD PharMingen) and then subjected to FACScan=20 analysis.

In vitro cytokine release assays. Lymphoid cells were=20 obtained from the draining lymph node and spleen harvested = from=20 each of two mice that had received the second i.t. injection = of=20 transduced DCs, nontransduced DCs, or saline 7 days earlier. = The=20 spleen or lymph node was pressed through sterile gauze, = rinsed,=20 treated for erythrocyte depletion, and rinsed again. These = cells=20 (2 x 106) were = cocultured with 4 x 105 = mitomycin=20 C=96treated GL26 or B16-F10 tumor cells in 24-well culture = plates for=20 36 hours. Culture supernatants were collected for = measurements=20 of murine IFN-3D{gamma}=20 and = IL-4=20 release by standard ELISA (BD PharMingen). The lower limit of = sensitivity for each assay was 31.3 and 15.6 pg/mL, = respectively. In=20 the IL-23 P40 subunit release assay, a sandwich ELISA = specific for=20 murine P40 was used as previously described (19).=20 In the IL-23 P19 and IL-12 P70 release assay, sandwich ELISA = kits=20 (eBioscience, San Diego, CA) were used according to the = instructions=20 of the manufacturer.

Cytotoxicity assays. Splenocytes were harvested as = described=20 above and pooled from two mice per group 7 days after the = second=20 i.t. injection of transduced DCs, nontransduced DCs, or = saline.=20 These cells (5 x = 106) were=20 restimulated in vitro with 5 x=20 105 mitomycin C=96treated GL26 cells in the = presence of 25=20 IU/mL recombinant human IL-2 for 5 days and used as effector=20 cells in a lactate dehydrogenase (LDH) release assay. GL26 or = B16-F10 cells (1 x = 104=20 per well) and serial dilutions of effector cells were = incubated in a=20 96-well U-bottomeded plate at 37=B0C for 5 hours. = Supernatants then=20 were analyzed with a cytotoxicity detection kit (Roche = Applied=20 Science, Indianapolis, IN) according to the instructions of = the=20 manufacturer. Results were expressed as the percentage of = specific=20 lysis. Statistical comparisons were done with paired = Student's=20 t test.

Reverse transcription-PCR. Adenoviral vector=96transduced = and=20 nontransduced DCs were harvested after 24 and 48 hours of=20 transduction. The cell pellets were subjected to total RNA = extraction=20 with a RNeasy Mini kit (Qiagen, Valencia, CA). The isolated = RNA=20 was reverse transcribed with a Bioscript kit (Bioline, Randolph, = MA)=20 and Oligo(dT)12-18 primer (Invitrogen). The PCR was = carried=20 out in a 20-=B5L reaction mixture that contained 1 =B5L = of cDNA as=20 template, specific oligonucleotide primer pairs of P19 = subunit=20 (forward, cagcagctctctcggaatct; reverse, tagaactcaggctgggcatc) = and=20 =DF-actin (forward, ggactcctatgtgggtgacg; reverse,=20 tacgaccagaggcatacagg), and Accuzyme (Bioline). The P19 was=20 concurrently amplified with internal control =DF-actin in the = same=20 reaction tube as previously described (23).=20 The amplified products were identified by agarose gel = electrophoresis=20 and ethidium bromide staining.

Trafficking study of i.t. injection of DCs. Three days = after=20 intracranial GL26 implantation, animals were randomly divided = into four groups and i.t. injected with IL-23=96 or empty=20 vector=96transduced DCs, nontransdcued DCs, or saline. Both=20 transduced and nontransduced DCs were labeled with red = fluorescent=20 cell linker (PKH26; Sigma) immediately before the i.t. = injection.=20 Briefly, the transduced or nontransduced DCs were incubated=20 with PKH26 at a concentration of 2 x=20 10-6 mol/L at room temperature for 5 minutes, = rinsed=20 extensively with HBSS, examined for viability and number by = the=20 trypan blue exclusion method, and used for injection. The = injected=20 mice were euthanized 24 hours after the injection by = intracordic=20 perfusion-fixation with 4% paraformaldehyde. The ipsilateral = deep=20 cervical lymph nodes (draining lymph nodes) were harvested = and=20 postfixed at 4=B0C, embedded in optimum cutting temperature = compound,=20 and frozen. Serial 8-=B5m sections were cut from these = samples with a=20 cryostat and examined under a fluorescent microscope. To = quantify the=20 fluorescence-positive cells, images were analyzed at a final=20 magnification of x20. = Four adjacent=20 sections were analyzed for each animal with the Zeiss = AxioVision=20 software (Carl Zeiss MicroImaging, Inc., Thornwood, NY). The = numbers=20 of fluorescence-positive cells counted in a field of x20 magnification were reported as mean = =B1 SD=20 of the experiment group.

Immunohistochemistry stainings of brain sections. = Free-floating=20 40-=B5m sections were treated with 10% donkey serum (Sigma) = for=20 30 minutes at room temperature and then stained with anti-CD4 = (rat=20 monoclonal antibody 1:50; BD PharMingen) and anti-CD8 (rat = monoclonal=20 antibody 1:100; BD PharMingen) primary antibodies and isotype = control=20 antibodies. The primary antibodies were detected with = FITC-conjugated=20 donkey anti-rat IgG (1:200; Jackson ImmunoResearch = Laboratories, West=20 Grove, PA). The sections were then counterstained with=20 4',6-diamidino-2-phenylindole before mounting. The results = were=20 evaluated under a confocal microscope. The positively stained = cells=20 were quantified by analyzing the images at a final = magnification of=20 x20. Four adjacent sections=20 containing tumor mass were analyzed for each animal with the=20 AxioVision software (Carl Zeiss). The numbers of positively=20 stained cells counted in a field of 20x=20 magnification were reported as mean =B1 SD of the experiment = group.=20 Comparisons between experiment groups were made with paired = Student's=20 t test.


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
References
 
<= B>DCs can=20 be transduced by an adenoviral vector to express high levels = of=20 biologically active IL-23. Using a centrifugal method, we = transduced murine bone marrow=96derived DCs, which were = generated in=20 vitro with granulocyte macrophage colony-stimulating = factor plus=20 IL-4, with an adenoviral vector carrying a single-chain mouse = IL-23 under the control of murine cytomegalovirus promoter,=20 AdIL-23 (21).=20 Transduction with a LacZ-expressing adenoviral vector at MOI = 50 by a=20 centrifugal method, which can efficiently introduce transgene = into DC=20 (22),=20 revealed that murine DCs could be adenovirally transduced at = 85%=20 efficiency (data not shown). This is consistent with a = previous study=20 by Nishimura et al. (22).=20 After the completion of DC transduction with AdIL-23, the=20 concentration of IL-23 P40 subunit released into the culture = medium=20 was measured by ELISA and the mRNA transcription of IL-23 P19 = subunit=20 in the cell pellet was detected by reverse transcription-PCR=20 (RT-PCR). As shown in Fig.=20 1A , accumulation of P40 was observed in cultures = of=20 AdIL-23=96transduced DCs (DC-IL-23), but not in cultures of=20 nontransduced or AdEmpty-transduced DCs (DC-Empty). RT-PCR = showed=20 that P19 mRNA was only detected in the cell pellets that were = transduced by AdIL-23, which confirmed that IL-23 expression = was only=20 achieved in the DC-IL-23 (Fig.=20 1B). The IL-23 produced by the DC-IL-23 was = confirmed to=20 be biologically active and capable of stimulating IFN-=20 production from concanavalin A blast T cells as previously = described=20 (data not shown; ref. 19).=20 To examine the effect of adenoviral transduction and exogenous = IL-23=20 expression on the DCs phenotype, various cell-surface = molecules were=20 examined by flow cytometry. AdEmpty transduction had little = effect on=20 the DC phenotype compared with nontransduced DCs. DC-IL-23 = did not=20 differ from DC-Empty or nontransduced DCs, except for = increased=20 levels of MHC-I and MHC-II molecules (Table=20 1 ).



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  		Figure 1. Transgene = expression by=20 DCs after adenovirus transduction. A, the = accumulation of=20 IL-23 P40 subunit was detected in the culture supernatant of = DC-IL-23 with ELISA. Columns, mean of triplicate=20 determinations; bars, SD. B, the mRNA = transcription of=20 IL-23 P19 subunit in cell pellets of DC-IL-23 was detected = by RT-PCR=20 [lane 1, ladder; lane 2 and 5, = DC-IL-23;=20 lane 3 and 6, DC-Empty; lane 4 and = 7,=20 nontransduced DCs (DC)]. =

 = ;

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  		Table 1. Phenotypic = characteristic=20 of adenoviral vector=96transduced DCs =

 = ;
Intratumoral=20 injections with DC-IL-23 result in prolonged survival in = intracranial=20 tumor=96bearing mice. To examine whether the DC-IL-23 = provided a=20 therapeutic benefit for brain tumor, we established gliomas = in=20 C57BL/6 mice with an intracranial implantation of 1 x 104 GL26 cells. Three days = after the=20 tumor implantation, mice were randomly divided into four = groups.=20 Each group was i.t. injected thrice with either saline,=20 DC-IL-23, DC-Empty, or nontransduced DCs, respectively, at = 7-day=20 interval (Fig.=20 2A ). As shown in Fig.=20 2B, i.t. administration of DC-IL-23 resulted in=20 significantly prolonged survival compared with DC-Empty or=20 nontransduced DCs. Approximately 80% of the DC-IL-23=96treated = mice=20 survived beyond an observed period of 120 days. DC-Empty and=20 nontransduced DC treatments led to only 20% of the mice = surviving=20 beyond 120 days. All of the saline-treated mice died within = 45 days=20 after the GL26 implantation. Statistical analysis revealed = that the=20 effect of DC-IL-23 was significantly different from that of = DC-Empty=20 or nontransduced DCs (P =3D 0.0114, DC-IL-23 versus = DC-Empty;=20 P =3D 0.0164, DC-IL-23 versus nontransduced DC; = log-rank test).=20 In addition, the effects of DC-Empty and nontransduced DCs = were=20 significantly different from that of saline (P < = 0.0001,=20 DC-Empty versus saline; P < 0.0001, nontransduced = DC versus=20 saline; log-rank test). However, there was no significant = difference=20 between the DC-Empty and nontransduced DC treatments = (P =3D=20 0.9103; log-rank test). Because IL-23 relates to IL-12 (18)=20 and it has been shown that IL-12 gene=96transduced DC=20 significantly suppressed the growth of established intradermal = tumor=20 (14),=20 we sought to compare the antitumor effect of IL-23=96expressing = DCs=20 with that of IL-12-expressing DCs in the intracranial tumor = model.=20 DCs expressing similar transgene protein levels of either = IL-23 or=20 IL-12 by adenoviral vector transduction were i.t. injected = into=20 intracranial tumor=96bearing mice with the same schedule as = described=20 in Fig.=20 2A. The DC-IL-23 treatment resulted in a similar = pattern=20 of survival benefit on the tumor-bearing mice as that of the = DC-IL-12=20 treatment (Fig.=20 2C), but this survival benefit was less than that = in Fig.=20 2B because a lower MOI for AdIL-23 transduction = was used=20 in the experiment in Fig.=20 2C. Statistical analysis revealed that the = DC-IL-23=20 treatment was not significantly different from the DC-IL-12 = treatment=20 (P =3D 0.1566, DC-IL-23 versus DC-IL-12; log-rank = test),=20 although DC-IL-23 treatment resulted in 3D~=2060% = survival rate=20 versus 3D~50% for DC-IL-12. We also compared the antitumor = effect of=20 DC transduced by either AdIL-23 or AdIL-12 with the same MOI = of 50.=20 The same MOI transduction resulted in a higher transgene = protein=20 level in DC-IL-23 than in AdIL-12-transduced DCs (DC-IL-12; = ref. 21)4=20 and, consequently, DC-IL-23 showed significantly better = antitumor=20 effect than DC-IL-12 (P =3D 0.0409, DC-IL-23 versus = DC-IL-12;=20 log-rank test; Fig.=20 2D).



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  		Figure 2. In vivo=20 experiments with intracranial tumor model. A, = experiment=20 schema shows tumor implantation, DC injection, rechallenge, = and=20 survival observation time. B, effect of DC-IL-23 on = the=20 experimental glioma in C57BL/6 mice. Kaplan-Meier survival = curve of=20 intracranial glioma=96bearing C57BL/6 mice that were = injected i.t.=20 thrice with DC-IL-23, DC-Empty, nontransduced DCs, or = saline.=20 C and D, comparison of the effects of DC-IL-23 = and=20 DC-IL-12 on experimental glioma in C57BL/6 mice. = Kaplan-Meier=20 survival curve of intracranial glioma=96bearing C57BL/6 mice = that were=20 injected i.t. thrice with adenoviral vector=96transduced DCs = that had=20 similar transgene expression levels of either IL-23 or IL-12 = (C). Kaplan-Meier survival curve of intracranial=20 glioma=96bearing C57BL/6 mice that were injected i.t. thrice = with DCs=20 that were transduced with a MOI of 50 by either AdIL-23 or = AdIL-12=20 (D). Representative of two independent experiments. =

 = ;
On=20 the basis of the known ability of IL-23 to induce proliferation = of=20 memory T cells, we sought to assess whether the i.t. injection = of=20 IL-23=96expressing DC could induce enhanced T-cell infiltration = in=20 tumor-bearing brains. Seven days after the first i.t. injection = of=20 transduced DCs, brain tissues were subjected to homogenization,=20 gradient centrifugation to isolate mononuclear cells, and = then=20 immunostaining for flow cytometry. The FACScan analysis = revealed=20 that intracranial CD8+ and CD4+ T-cell = infiltration=20 was enhanced in DC-IL-23=96treated tumor-bearing brains = compared=20 with those of DC-Empty=96, nontransduced DC=96, and = saline-treated=20 tissues (Fig.=20 3 ). Stained in situ by immunohistochemistry, = brain tumors=20 from the mice treated with DC-IL-23 showed robust = infiltration of=20 CD8+ and CD4+ T cells [Fig.=20 4A and B (a-h)]. There was = negligible=20 CD8+ and CD4+ T-cell infiltration, however,=20 within tumors from mice treated with saline [Fig.=20 4A and B (q-t)]. The treatment with = DC-Empty=20 and nontransduced DC also resulted in i.t. T-cell = infiltration, but=20 the intensity of that infiltration was significantly lower = than that=20 seen in the DC-IL-23=96treated tumors [Fig.=20 4A and B (i-p)]. Semiquantification revealed = that=20 there were 3D~104 =B1 12.75 CD8 positively stained cells identified = in=20 DC-IL-23=96treated group as compared with 35 =B1 8.21 and 31 = =B1 4.96 in=20 the DC-Empty=96 and nontransduced DC=96treated groups, = respectively. CD4=20 positively stained cells were 3D~=2082.25 = =B1 8.48 in=20 DC-IL-23=96treated group as compared with 29.75 =B1 13.45 and = 28.25 =B1=20 6.85 in the DC-Empty=96 and nontransduced DC=96treated = groups,=20 respectively. Both CD8+ and CD4+ T-cell = infiltration=20 reached significant difference (P < 0.05) for the=20 DC-IL-23=96treated group when compared with either = DC-Empty=96 or=20 nontransduced DC=96treated group.



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  		Figure 3. T-cell = infiltration=20 within the tumor-bearing brains of transduced DC=96 and = nontransduced=20 DC=96injected mice. Fluorescence-activated cell sorting = analysis=20 showed the CD8+ and CD4+ T-cell = infiltration=20 in the tumor-bearing brain tissues of mice that were i.t. = injected=20 with DC-IL-23 (A), DC-Empty (B), nontransduced = DCs=20 (C), and saline (D). DC-IL-23=96treated mice = showed=20 robust infiltration of CD8+ and CD4+ T = cells=20 compared with that of DC-Empty=96 and nontransduced = DC=96treated mice. =

 = ;



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  		Figure 4. Intratumoral = T-cell=20 infiltration after the administration of transduced and=20 nontransduced DCs. A, intracranial tumor=96bearing = mice showed=20 robust infiltration of CD8+ T cells within the = tumor=20 masses 7 days after the first i.t. injection of DC-IL-23=20 (A-H). Moderate infiltration of CD8+ T = cells=20 within the tumor masses was also observed in = DC-Empty=96treated=20 (I-L) and nontransduced DC=96treated (M-P) = mice.=20 Saline-treated mice showed negligible CD8+ T-cell = infiltration in the tumor masses (Q-T). Bar, 250 = =B5m.=20 B, intracranial tumor=96bearing mice showed robust = infiltration=20 of CD4+ T cells within the tumor masses 7 days = after the=20 first i.t. injection of DC-IL-23 (A-H). Moderate = infiltration=20 of CD4+ T cells within the tumor masses was also = observed=20 in DC-Empty=96treated (I-L) and nontransduced = DC=96treated=20 (M-P) mice. Saline-treated mice showed negligible=20 CD4+ T-cell infiltration in the tumor masses=20 (Q-T). Bar, 250 =B5m. =

 = ;
Tumor-specific=20 immune response can be identified after intratumoral = implantation of=20 DC-IL-23 into the brains of tumor-bearing mice. Because = the above=20 data showed that i.t. injection of DC-IL-23 resulted in = prolonged=20 survival and intratumoral T-cell infiltration in the brain=20 tumor=96bearing mice, we next asked whether systemic immune = responses=20 specific for the tumor were induced by i.t. injection of = DC-IL-23. To=20 address this question, deep cervical lymph nodes in the = ipsilateral=20 side of the implanted glioma (draining lymph nodes) as well = as the=20 spleen were harvested from the tumor-bearing mice 7 days = after the=20 second i.t. injection of DC-IL-23. These lymphoid cells were=20 cocultured with mitomycin C=96treated GL26 cells in = vitro and=20 IFN-3D{gamma} and IL-4 production in the culture supernatant = was=20 examined. As shown in Table=20 2 , injection with DC-Empty or nontransduced DCs enhanced = tumor-specific IFN-3D{gamma}=20 = production by=20 lymphoid cells harvested from draining lymph nodes and spleen = compared with saline injection. More importantly, i.t. = injection of=20 DC-IL-23 resulted in greater enhancement of IFN-3D{gamma}=20 = production in=20 response to GL26 restimulation by these lymphoid cells. In = contrast,=20 there was no detectable IL-4 increase in spleen and only a = slight=20 increase in draining lymph nodes. The IFN-3D{gamma}=20 was = specifically released with GL26 stimulation, but not with = syngeneic=20 B16-F10 tumor cells (data not shown). These results suggest = that i.t.=20 injected DC-IL-23 can traffic to the draining lymph node and=20 efficiently stimulate lymphocytes in situ to produce = IFN-. To=20 verify this notion, DC-IL-23, DC-Empty, and nontransduced DCs = were=20 labeled with fluorescent linker (PKH26) and injected i.t. = into brain=20 tumor=96bearing mice, and the ipsilateral deep cervical lymph = node (the=20 draining lymph node) was examined 24 hours after the = injection.=20 Numerous fluorescence-positive cells were identified in lymph = nodes=20 from animals injected with PKH26-labeled adenoviral = vector=96transduced=20 or nontransdcued DCs (Fig.=20 5 ). Quantification of the fluorescence-positive cells = revealed=20 an average of 25 =B1 2 cells per field in all the mice = injected with=20 either adenoviral vector=96transduced or nontransdcued DCs. = Spleen=20 cells from the DC-IL-23=96treated mice were also analyzed for = CTL=20 activity against tumor targets. Figure=20 6 showed the CTL activity against GL26 cells by spleen = cells from=20 mice that received saline compared with those that received=20 adenoviral vector=96transduced and nontransduced DCs. Mice = that=20 received either transduced or nontransduced DCs showed = enhanced CTL=20 activity compared with saline-injected mice. DC-IL-23 = injection=20 induced significantly higher CTL activity than did DC-Empty = or=20 nontransduced DC injection (Fig.=20 6A). Statistical analysis revealed that there were = significant differences in cytolytic activity between = DC-IL-23/GL26=20 and DC-Empty/GL26, DC/GL26, or saline/GL26 at all three=20 effector-to-target ratios (P < 0.05). Significant=20 differences in cytolytic activity were found between = saline/GL26 and=20 DC-Empty/GL26 or DC/GL26 only at effector-to-target ratios of = 30 and=20 100. Splenocytes from DC-IL-23=96treated mice lacked any = apparent CTL=20 activity against the irrelevant tumor cell B16-F10 (Fig.=20 6B), indicating that the CTL activity was tumor=20 specific.


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  		Table 2. IFN-3D{gamma}=20 and=20 IL-4 production by lymphoid cells from draining lymph nodes = and=20 spleen =

 = ;


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  		Figure 5. Intratumoral = injection of=20 transduced and nontransduced DCs migrated to the draining = lymph=20 node. Intracranial tumor=96bearing mice were injected i.t. = with=20 transduced or nontransduced DCs that were labeled with = PKH26. The=20 draining lymph nodes were harvested 24 hours after the = injection and=20 were processed for fluorescent microscope examination.=20 Fluorescence-positive cells were observed in the draining = lymph=20 nodes harvested from mice injected with DC-IL-23 (A), = DC-Empty (B), and nontransduced DCs (C). No=20 fluorescence-positive cell was observed in the draining = lymph nodes=20 harvested from mice injected with saline (D). Bar, = 250 =B5m. =

 = ;


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  		Figure 6. Tumor-specific = CTL=20 activity of spleen cells induced by i.t. injection of = DC-IL-23.=20 A, spleen cells obtained from the tumor-bearing mice = 7 days=20 after second i.t. injection of transduced DCs, nontransduced = DCs, or=20 saline were restimulated with mitomycin C=96treated GL26 = cells for 5=20 days, and the CTL activity of the resultant effector cells = was=20 measured against parental GL26 tumor target in a LDH release = assay.=20 Representative of three independent experiments. **, = P <=20 0.05, compared with either DC-Empty/GL26 or DC/GL26; *, = P=20 < 0.05, compared with saline/GL26. B, spleen cells = were=20 obtained and restimulated as described in (A) and the = CTL=20 activity of the resultant effector cells was measured = against GL26=20 and B16-F10 tumor targets in a LDH release assay. **, = P <=20 0.05, compared with B16-F10. Representative of three = independent=20 experiments. =

 = ;
We=20 also examined whether a memory protective immunity was established = by=20 the i.t. injection of DC-IL-23. DC-IL-23=96treated survivors = were=20 subjected to rechallenge with another intracranial implantation = of=20 GL26 (Fig.=20 1A). All of the rechallenged animals survived = beyond day=20 90 post rechallenge and were tumor-free at the end point of = the=20 survival study as verified by H&E staining of brain = sections. In=20 contrast, age-matched na=EFve mice were uniformly susceptible = to GL26=20 glioma challenge and died of brain tumor within 45 days of = the=20 challenge.

Involvement of CD8+, CD4+ T cells and NK = cells in=20 the antitumor effect of i.t. injection with DC-IL-23. To = identify=20 the population of T cells and NK cells involved in the = antitumor=20 immunity induced by DC-IL-23, mice were injected with = depleting=20 anti-CD8, anti-CD4, or control rat antibodies for circulating = T-cell=20 depletion or with anti-NK1.1 or control mouse antibodies for = NK cell=20 depletion. Flow cytometry showed that the injection of = antibodies=20 depleted the appropriate cell population by 95% (data not = sown). As=20 shown in Fig.=20 7A , depletion of CD8+ T cells greatly impaired = the=20 protective effect of DC-IL-23 on intracranial tumor=96bearing = mice (P =3D 0.0013, CD8 depletion versus control rat IgG;=20 log-rank test). There was no long-term survival observed in = the CD8=20 T-cell=96depleted mice. Similarly, but less significantly, = the=20 impairment of the protective effect was also observed in the = CD4=20 T-cell=96depleted mice (P =3D 0.0475, CD4 depletion = versus control=20 rat IgG; log-rank test). In NK cell=96depleted mice, DC-IL-23 = treatment=20 still had a protective effect on intracranial = tumor=96bearing=20 mice (Fig.=20 7B). However, the effect was impaired in these mice=20 compared with the mice that received control mouse IgG (P = =3D=20 0.0439, NK cell depletion versus control mouse IgG; log-rank=20 test). These data indicate that CD8+ T cells are = essential=20 for the antitumor effect conferred by i.t. injection of=20 DC-IL-23, and that CD4+ T cells and NK cells also = have=20 roles in the effect.



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  		Figure 7. Involvement of=20 CD8+, CD4+ T cells and NK cells in the = antitumor immunity induced by DC-IL-23. A, = Kaplan-Meier=20 survival curve of intracranial tumor=96bearing mice that = received=20 anti-CD8, anti-CD4 depleting antibodies or control IgG and = were=20 treated with i.t. injection of DC-IL-23. B, = Kaplan-Meier=20 survival curve of intracranial tumor=96bearing mice that = received=20 either anti-NK1.1 antibody for NK cell depletion or control = IgG and=20 were treated with i.t. injection of DC-IL-23. Representative = of=20 three independent experiments. =

 = ;

3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
References
 
I= t has=20 been reported that the presence of increased DC numbers = within solid=20 tumor masses induces effective antitumor immune responses in = animal=20 models (16)=20 and is associated with improved prognosis in clinical = patients (17).=20 In the current study, we showed that i.t. administration of = DC-IL-23=20 can induce significant and effective systemic antitumor = immune=20 responses that control the growth of experimental = intracranial=20 gliomas in immunocompetent mice, suggesting that a = gene-modified DC=20 in situ vaccine may have a broad therapeutic potential = for the=20 management of human brain tumors.

Viral vector=96mediated genetic modification of DCs to express=20 immunomodulatory proteins or tumor antigens has been = successfully=20 achieved in animal models of tumor treatment (15,=20 24,=20 25).=20 Among vectors used for transducing DC, adenoviral vector=20 represents an efficient means of inserting transgenes into DC = without=20 detrimental effects on its phenotype or function (22,=20 26,=20 27).=20 In this study, we transduced DCs with adenoviral vector = coding=20 single-chain mouse IL-23 using a centrifugal method. A = previous study=20 showed that adenoviral infection could induce maturation of = DC=20 via a nuclear factor 3D{kappa}=20B=96dependent=20 pathway (28).=20 We found, however, that the adenoviral vector itself had no=20 detrimental effect on the DC phenotype in our experimental = settings,=20 which was consistent with a study showing that infection with = adenovirus encoding an enhanced green fluorescent protein had = little=20 effect on expression of the surface markers of DCs, as well = as=20 with findings from Murakami et al.'s (15)=20 report that DC transduced by an adenoviral vector coding p53 = protein=20 or control Dl312 vector showed no apparent effect on DC=20 differentiation and activation (22).=20 These differences may be due, at least partly, to the methods = used=20 for transducing DCs. A centrifugal method, which enhances = adenovirus=20 transduction efficiency with a short infection time (22),=20 was used in our study. We also observed that IL-23 = adenovirally=20 transduced into DC increased the expression of both MHC class = I and=20 class II surface molecules. These phenotypic changes could be = due, in=20 part, to the direct effect of IL-23 or, more likely, = indirectly=20 through IFN-3D{gamma}=20 = production by=20 contaminating T cells or NK cells. In fact, DCs generated = from bone=20 marrow of IFN-3D{gamma}=20 = knockout mice=20 did not show any change in the expression level of MHC class = I and=20 class II molecules after adenoviral vector transduction (data = not=20 shown).

Treating intracranial glioma=96bearing mice with i.t. injection = of=20 DC-IL-23 resulted in profound antitumor effects with massive = T-cell=20 infiltrations. These data confirm published studies of others = (20)=20 as well as our own (21)=20 that found that IL-23 expressed by tumor cells or by neural = stem=20 cells showed antitumor effects in in vivo colon = carcinoma=20 models (20)=20 and brain tumor models (21),=20 respectively. Lymphocytes from spleen and draining lymph = nodes of=20 mice treated i.t. with DC-IL-23 displayed heightened levels = of=20 IFN-3D{gamma} secretion as well as CTL activity in a tumor-specific=20 fashion. Indeed, these responses could contribute to the = profound=20 in vivo antitumor effects that we observed. Moreover, i.t.=20 injection of DC-IL-23 resulted in robust infiltration of=20 CD8+ and CD4+ T cells within the = tumor-bearing=20 brain. These findings are of particular interest because both = cytolytic and noncytolytic tumor-specific, tumor-infiltrating = lymphocytes have been shown to mediate potent antitumor = effects in=20 vivo upon adoptive transfer (29,=20 30).=20

Evidence has shown that immature DCs can readily acquire = antigen(s)=20 via uptake of apoptotic cells, which in turn elicit MHC class = I=96restricted CTLs (31,=20 32).=20 Thus, using flow cytometry, we confirmed in each experiment = in the=20 current study that the prepared DCs have an immature = phenotype. DCs=20 delivered locally at the tumor site may phagocytose adjacent = tumor=20 cells and present tumor antigens in vivo, which could = be=20 greatly facilitated by the expression of IL-23 that is able = to act=20 directly on CD83D{alpha}=20+ DC to promote immunogenic = presentation of tumor=20 antigen. The combination of the tumor antigen presentation = ability of=20 DC and the promoting effect of IL-23 on antigen presentation=20 in situ within tumor masses may underline the superior = antitumor effect of IL-23=96expressing DCs. = IL-23=96expressing=20 DCs showed antitumor activity superior to IL-12-expressing = DCs=20 when the same MOIs of AdIL-23 and AdIL-12 transduced DCs were = injected i.t. When both IL-23=96expressing DCs and = IL-12=96expressing=20 DCs had similar transgene protein levels, IL-23=96expressing = DCs=20 showed a higher survival rate on tumor-bearing animal. These = findings=20 indicate that, under the current experimental settings, DC = with=20 AdIL-23 transduction can lead to greater transgene expression = and an=20 enhanced antitumor response against intracranial glioma.

Our in vivo lymphocyte depletion experiments showed that=20 CD8+ T cells and, to a lesser extent, = CD4+ T=20 cells and NK cells are required for the generation of the = antitumor=20 immunity conferred by IL-23=96expressing DCs. These data are = consistent=20 with our previous findings, which showed that the antiglioma=20 activity of IL-23=96expressing neural stem cells was mainly=20 dependent on CD8+ T cells, and CD4+ T = cells and=20 NK cells were also involved in the process (21).=20 However, the data are in contrast to Lo et al.'s study (20).=20 The latter study showed that the antitumor effect of = IL-23=96expressing=20 tumor cells was independent of CD4+ T cells and NK = cells.=20 These differences are probably the result of the different = tumor=20 models used in the two studies. GL26 glioma was used as an=20 intracranial brain tumor model in the current study whereas = Lo et al.=20 used a s.c. colon adenocarcinoma model. The unique = environment of the=20 central nervous system with regard to antigen presentation = and the=20 differences of immunogenicity among different tumor cell = lines may=20 underline the variability in the cellular subsets crucial to = an=20 antitumor effect.

It has been reported that IL-23 can activate macrophages to=20 produce proinflammatory cytokines, such as IL-17, which may=20 contribute to autoimmune inflammation of the brain (33=9636).=20 In our experimental model, however, we showed that IL-17 = could=20 not be detected by mRNA transcription or by protein = expression=20 in the brain of DC-IL-23=96treated mice (data not shown). = We=20 recently reported that IFN-3D{gamma}=20 = mRNA can be=20 greatly elevated in tumor-rechallenged mice that survived = previous=20 brain tumor implantation by IL-23=96expressing neural stem = cell=20 treatment. These rechallenged mice showed no demyelination or = inflammation changes, as verified by histologic analysis of = brain=20 tissue (21).=20 Indeed, in our current study, none of the mice treated with = DC-IL-23=20 showed signs of autoimmune distress (ruffled fur, weight = loss,=20 lethargy, or agitation) or histopathologic changes in the = brain (data=20 not shown). Thus, although the molecular mechanisms governing = the=20 pathways that regulate TH1-type antitumor immunity and = autoimmune=20 response by exogenous IL-23 are presently unclear, i.t. = injection of=20 IL-23=96expressing DCs results in systemic and effective = antitumor=20 activity in intracranial tumor=96bearing mice with no = detectable=20 deleterious side effects.

Taken together, in the current study, we present evidence that=20 i.t. injection with IL-23 gene=96transduced DC is = feasible,=20 mediates an effective antitumor immunity that is superior to=20 that observed with DC-Empty or nontransduced DC, or even with = DC-IL-12, and is capable of inducing substantial systemic = antitumor=20 immune responses. These data provide a preclinical rationale=20 for IL-23=96expressing DC=96based brain tumor therapy.

Note: When the present study was finished, Overwijk et al. (37)=20 reported that IL-23 is a potent vaccine adjuvant for the = induction=20 of therapeutic, tumor-specific CD8 T-cell response and = Bettelli=20 et al. (38)=20 reported that IL-23 is not the differentiation factor for the = generation of IL-17-producing T cells, whereas Langowski et = al. (39)=20 reported that IL-23 is an important molecular link between=20 tumor-promoting proinflammatory processes and the failure of = the=20 adaptive immune surveillance to infiltrate tumors.


3D"   =20 Acknowledgments =
 
Grant support:=20 NIH grants 1K23 NS02232, 1R01 NS048959, and 1R21 NS048879 = (J.S. Yu),=20 and NMRC grants 1435-04-04-GT-41387 and -43096 (D.L. = Farkas).=20

The costs of publication of this article were defrayed in part = by=20 the payment of page charges. This article must therefore be = hereby=20 marked advertisement in accordance with 18 U.S.C. = Section 1734=20 solely to indicate this fact.

We thank Dr. Scot Macdonald for the critical review of the = manuscript=20 and helpful comments, and Dr. Chris Wheeler for the = discussions.=20


3D"   =20 Footnotes
 
Note: J. Hu and X. Yuan contributed = equally to=20 this work.

4 Unpublished data. =

Received 10/ 4/05. Revised 6/ 7/06. Accepted 7/11/06.


3D"   =20 References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
3D"References
&nb= sp;

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Cancer=20 Epidemiology Biomarkers & Prevention Molecular=20 Cancer Therapeutics
Molecular=20 Cancer Research Cell Growth=20 & Differentiation
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Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_0000_01C85868.EE2C41A0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else 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quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= } else if (a>=3D0 && b>=3D0 && c>=3D0) {=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= } else {=0A= if (a>=3D0) a=3D_uFixA(_ubd.cookie,";",_ust);=0A= else a=3D_udh+"."+_uu+"."+_ust+"."+_ust+"."+_ust+".1";=0A= _ubd.cookie=3D"__utma=3D"+a+"; path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= }=0A= if (_ulink && xx && xx!=3D"" && xx!=3D"-") {=0A= xx=3D_uUES(xx);=0A= if (xx.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmx=3D"+xx+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= if (_ulink && v && v!=3D"" && v!=3D"-") {=0A= v=3D_uUES(v);=0A= if (v.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmv=3D"+v+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= _uInfo(page);=0A= _ufns=3D0;=0A= _ufno=3D0;=0A= if (!page || page=3D=3D"") _uff=3D1;=0A= }=0A= function _uInfo(page) {=0A= var p,s=3D"",dm=3D"",pg=3D_udl.pathname+_udl.search;=0A= if (page && page!=3D"") pg=3D_uES(page,1);=0A= _ur=3D_ubd.referrer;=0A= if (!_ur || _ur=3D=3D"") { _ur=3D"-"; }=0A= else {=0A= dm=3D_ubd.domain;=0A= if(_utcp && _utcp!=3D"/") dm+=3D_utcp;=0A= p=3D_ur.indexOf(dm);=0A= if ((p>=3D0) && (p<=3D8)) { _ur=3D"0"; }=0A= if (_ur.indexOf("[")=3D=3D0 && = _ur.lastIndexOf("]")=3D=3D(_ur.length-1)) { _ur=3D"-"; }=0A= }=0A= s+=3D"&utmn=3D"+_uu;=0A= if (_ufsc) s+=3D_uBInfo();=0A= if (_uctm) s+=3D_uCInfo();=0A= if (_utitle && _ubd.title && _ubd.title!=3D"") = s+=3D"&utmdt=3D"+_uES(_ubd.title);=0A= if (_udl.hostname && _udl.hostname!=3D"") = s+=3D"&utmhn=3D"+_uES(_udl.hostname);=0A= s+=3D"&utmr=3D"+_ur;=0A= s+=3D"&utmp=3D"+pg;=0A= if ((_userv=3D=3D0 || _userv=3D=3D2) && _uSP()) {=0A= var i=3Dnew Image(1,1);=0A= i.src=3D_ugifpath+"?"+"utmwv=3D"+_uwv+s;=0A= i.onload=3Dfunction() {_uVoid();}=0A= }=0A= if ((_userv=3D=3D1 || _userv=3D=3D2) && _uSP()) {=0A= var i2=3Dnew Image(1,1);=0A= = i2.src=3D_ugifpath2+"?"+"utmwv=3D"+_uwv+s+"&utmac=3D"+_uacct+"&utmcc=3D"+= _uGCS();=0A= i2.onload=3Dfunction() { _uVoid(); }=0A= }=0A= return;=0A= }=0A= function _uVoid() { return; }=0A= function _uCInfo() {=0A= if (!_ucto || _ucto=3D=3D"") { _ucto=3D"15768000"; 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