From: Subject: VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche : Nature Date: Tue, 16 May 2006 19:43:23 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0048_01C67920.FE3CF540" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.2869 This is a multi-part message in MIME format. ------=_NextPart_000_0048_01C67920.FE3CF540 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.nature.com/nature/journal/v438/n7069/full/nature04186.html VEGFR1-positive = haematopoietic bone marrow progenitors initiate the pre-metastatic niche = : Nature
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Nature 438, 820-827 (8 December 2005) | doi:10.1038/nature04186

VEGFR1-positive haematopoietic bone marrow progenitors = initiate the=20 pre-metastatic niche

Rosandra N. Kaplan1,2,6,10,=20 Rebecca D. Riba1,2,10,=20 Stergios Zacharoulis1,2,6,10,=20 Anna H. Bramley1,2,=20 Lo=EFc Vincent4,=20 Carla Costa1,2,=20 Daniel D. MacDonald1,2,=20 David K. Jin4,=20 Koji Shido4,=20 Scott A. Kerns1,2,=20 Zhenping Zhu8,=20 Daniel Hicklin8,=20 Yan Wu8,=20 Jeffrey L. Port5,=20 Nasser Altorki5,=20 Elisa R. Port7,=20 Davide Ruggero9,=20 Sergey V. Shmelkov1,2,4,=20 Kristian K. Jensen1,2,=20 Shahin Rafii3,4=20 and David Lyden1,2,6

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Abstract

The cellular and molecular mechanisms by which a tumour = cell=20 undergoes metastasis to a predetermined location are largely unknown. = Here we=20 demonstrate that bone marrow-derived haematopoietic progenitor cells = that=20 express vascular endothelial growth factor receptor 1 (VEGFR1; also = known as=20 Flt1) home to tumour-specific pre-metastatic sites and form cellular = clusters=20 before the arrival of tumour cells. Preventing VEGFR1 function using = antibodies=20 or by the removal of VEGFR1+ cells from the bone marrow of = wild-type=20 mice abrogates the formation of these pre-metastatic clusters and = prevents=20 tumour metastasis, whereas reconstitution with selected Id3 (inhibitor = of=20 differentiation 3)-competent VEGFR1+ cells establishes = cluster=20 formation and tumour metastasis in Id3 knockout mice. We also show that=20 VEGFR1+ cells express VLA-4 (also known as integrin 3Dalpha=2043Dbeta=201), and that tumour-specific growth factors = upregulate=20 fibronectin=97a VLA-4 ligand=97in resident fibroblasts, providing a = permissive niche=20 for incoming tumour cells. Conditioned media obtained from distinct = tumour types=20 with unique patterns of metastatic spread redirected fibronectin = expression and=20 cluster formation, thereby transforming the metastatic profile. These = findings=20 demonstrate a requirement for VEGFR1+ haematopoietic = progenitors in=20 the regulation of metastasis, and suggest that expression patterns of=20 fibronectin and VEGFR1+VLA-4+ clusters dictate=20 organ-specific tumour spread.

Bone marrow-derived cells (BMDCs) contribute to = malignant=20 transformation1,=20 tumour vascularization2,=20 3=20 and neoplastic cell migration4.=20 Previously, we identified haematopoietic progenitor cells (HPCs) = expressing=20 VEGFR1 that reside within specified niches of the bone marrow. During = the=20 angiogenic switch, these cells proliferate and mobilize to the = bloodstream along=20 with bone marrow-derived endothelial progenitor cells that express = VEGFR2 (also=20 known as Flk1), and contribute to the vascularization and growth of = specific=20 primary tumours2,=20 5.=20 These myelomonocytic VEGFR1+ cells localize to perivascular = sites,=20 thus stabilizing tumour neo-vessels2.=20 These and other tumour-associated cells enhance primary tumour = neo-angiogenesis=20 and growth, yet their precise contribution to metastasis is = unclear6,=20 7,=20 8.=20 Therefore, the aim of this study was to determine the role of = VEGFR1+=20 HPCs in the temporal and functional generation of metastasis.

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BMDCs colonize pre-metastatic sites before tumour cells

We analysed the fate of 3Dbeta=20-galactosidase-positive (3Dbeta=20-gal+) and green fluorescent protein-positive=20 (GFP+) BMDCs following intradermal primary tumour injection = in mice.=20 Animals were inoculated with either Lewis lung carcinoma (LLC) cells, = which=20 metastasize to the lungs and occasionally the liver, or B16 melanoma = cells,=20 which possess a more widely disseminated metastatic potential. After=20 irradiation, but before tumour implantation, we observed minimal 3Dbeta=20-gal+ BMDCs (mean 3Dplusminus=20 s.e.m., 0.01% 3Dplusminus=20 0.01 of cells 3Dbeta=20-gal+ per 3Dtimes=20100 objective field) or GFP+ BMDCs = in the=20 lungs. (Fig.=20 1a, b,=20 left panels). By day 14 after tumour implantation, but before the = arrival of=20 tumour cells, the extravasation and cluster formation of 3Dbeta-gal+ BMDCs (3.2% 3Dplusminus=20 1.2, P < 0.05 by Student's = t-test) or=20 GFP+ BMDCs were detected near terminal bronchioles and distal = alveoli, both common sites for future tumour metastasis (Fig.=20 1a, b,=20 left middle panels and insets). On day 16, established 3Dbeta=20-gal+ cell clusters dictated the contours of = future=20 metastatic lesions (Fig.=20 1a, right middle panel). Individual DsRed-tagged tumour cells, = associated=20 with pre-existing BMDC clusters, were visible by day 18 (Fig.=20 1b, right middle panel) and progressed to micrometastases by day 23 = (Fig.=20 1a, b,=20 right panels). 3Dbeta=20-gal+ BMDCs were maintained within = well-established tumour=20 metastases (Fig.=20 1a, right panel and inset).

Figure=20 1: Bone marrow-derived cells form the pre-metastatic=20 niche.

a, 3Dbeta=20-gal+ bone marrow cells (left panel) are rarely = observed in=20 lungs after irradiation and before LLC cell implantation (n =3D = 6). By day=20 14, 3Dbeta=20-gal+ bone marrow-derived clusters appear in the = lung=20 parenchyma (left middle panel and magnified inset of the region arrowed; = n =3D 25) and are associated with micrometastases by day 23 = (right panel,=20 arrows) and in gross metastases (right panel, inset; n =3D 12). = Also shown=20 is a cluster with associated stroma between a terminal bronchiole and = bronchial=20 vein, a common metastatic site (right middle panel). B, terminal = bronchiole; V,=20 bronchial vein. b, GFP+ bone marrow in the lungs after = irradiation and before DsRed-tagged B16 cell implantation (left panel; = n=20 =3D 6). On day 14, GFP+ (green) BMDCs are seen with no=20 DsRed+ (red) tumour cells (left middle panel and inset; = n =3D=20 12). Beginning on day 18, a few single DsRed+ B16 cells = adhere to=20 GFP+ bone marrow clusters (right middle panel), and by day = 23,=20 DsRed+ tumour cells proliferate at cluster sites (right = panel;=20 n =3D 8). DAPI stain (blue) shows cell nuclei. c, A graph = showing=20 flow cytometric data of bone marrow-derived GFP+ BMDCs and=20 DsRed+ B16 cells in the lung, and two flow diagrams on day 14 = (left=20 panel) and day 18 (right panel) (n =3D 30; error bars show = s.e.m.).=20 d, GFP+ BMDCs mobilized with B16 conditioned media, = then=20 DsRed-tagged tumour cells injected through the tail vein adhere = 24 h later=20 (right panel, arrows) compared with animals receiving media alone (left = panel;=20 P < 0.01). Inset shows proliferating tumour cells in a cluster = after=20 four days (right panel inset; n =3D 6). e, Number of = clusters per=20 3Dtimes=20100 objective field in animals with = intradermal LLC or B16=20 tumours (n =3D 12). Scale bar on top left panel applies to panels = a=20 (left, left middle, right middle, 80 3Dmicro=20m; left middle inset, 8 3Dmicro=20m; right, 20 3Dmicro=20m; right inset, 47 3Dmicro=20m), b (left, left middle, 80 3Dmicro=20m; left middle inset, 8 3Dmicro=20m; right middle, right, 40 3Dmicro=20m) and d (40 3Dmicro=20m; right inset, 20 3Dmicro=20m).

High=20 resolution image and legend (89K)

To further define the timing of tumour cell arrival, a = flow=20 cytometric study of the lungs was undertaken. Before day 8, minimal=20 GFP+ BMDCs were observed in this tissue; however, from day = 12, BMDCs=20 began migrating into the lung (Fig.=20 1c, graph and left flow cytometry panel). These GFP+ = cells=20 increased in number, and were joined by DsRed-tagged tumour cells by day = 18 (Fig.=20 1c, graph and right flow diagram). No tumour cells were detected by = flow=20 cytometry or microscopy earlier than day 16, and increasing numbers of = tumour=20 cells were identified over time (Fig.=20 1b, right panels; Fig.=20 1c; Supplementary=20 Fig. 1a). More than 95% of tumour cells co-clustered with = GFP+=20 BMDCs (97% 3Dplusminus=20 1.1; Fig.=20 1b, right panels).

Although a few tumour cells may have been undetectable = using these=20 methodologies, further experiments in mice given = B16-melanoma-conditioned media=20 (MCM) showed that this conditioning alone mobilized BMDCs that were = capable of=20 forming a pre-metastatic niche. We introduced DsRed-tagged B16 tumour = cells=20 intravenously into mice with pre-established GFP+ BMDC = clusters in=20 the lung after challenge with MCM (Fig.=20 1d, right panel) or media alone (Fig.=20 1d, left panel). MCM increased the number of tumour cells in the = lung one=20 day after tumour injection compared with media alone (141.3 3Dplusminus=20 10.2 versus 2.7 3Dplusminus=20 0.6 tumour cells per section of lung tissue, = P=20 < 0.01). Four days after tumour injection, the frequency and size of = the lung=20 nodules were augmented by MCM (207 3Dplusminus=20 5.6 versus 14 3Dplusminus=20 1.7, P < 0.01; Fig.=20 1d, right panel inset). Co-localization of DsRed-tagged tumour cells = with=20 GFP+ BMDC clusters was >93% at both time points, = indicating that=20 BMDCs assist tumour cell adhesion and proliferation. Therefore, factors = provided=20 by the primary tumour induce BMDCs to enter the bloodstream and mobilize = to=20 organ-specific pre-metastatic sites, and this migration precedes the = arrival of=20 tumour cells.

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Sites of BMDC clusters are tumour-type specific

We examined whether the type of tumour cell dictated = BMDC=20 distribution to specific pre-metastatic sites. Intradermal injection of = LLC=20 cells resulted in BMDC cluster formation limited to the lung (47.5 2.6 clusters per 3Dtimes=20100 objective field) and liver (10.8 3Dplusminus=20 1.1) with no clusters in other organs (Fig.=20 1e, left panel). In contrast, the B16 melanoma tumour cells induced = the=20 formation of BMDC clusters in multiple tissues such as the lung (103.8 = 6.9), liver (41.8 3Dplusminus=20 2.4), testis (36.6 3Dplusminus=20 3.1), spleen (25 3Dplusminus=20 3.2) and kidney (20.6 3Dplusminus=20 1.8), which are all common metastatic sites = for this=20 tumour (Fig.=20 1e, right panel). Furthermore, melanoma cells, consistent with their = more=20 aggressive metastatic nature, induced more clusters than LLC cells = (P=20 < 0.01).

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Recruited BMDCs consist of haematopoietic progenitors

We characterized the cellular and molecular composition = of=20 incorporated BMDC clusters. Clusters induced by either tumour type = expressed=20 VEGFR1 (Fig.=20 2a, right panel), and GFP+ BMDC clusters coexpressed = VEGFR1 (Fig.=20 2b, left panel), compared with little VEGFR1 in the lung after = irradiation=20 alone (Fig.=20 2a, left panel and inset). Further characterization revealed that = subsets of=20 VEGFR1+ BMDCs coexpressed the stem/progenitor cell antigens = CD133 (Fig.=20 2b, right panel), CD34 (Supplementary=20 Fig. 1b and Supplementary=20 Table) and CD117 (also known as c-Kit; Fig.=20 2c), suggesting that these cells may comprise phenotypically marked=20 VEGFR1+ HPCs and precursor cells. After primary tumour = implantation,=20 CD117-positive progenitor cells arrived in the lung before GFP-tagged = tumour=20 cells by flow cytometry (Supplementary=20 Fig. 1c), recapitulating the recruitment of BMDCs described above. = There is=20 a degree of maturational heterogeneity, with the myelomonocytic marker = CD11b=20 present on certain incorporated cells (data not shown). Early = VEGFR1+=20 bone marrow clusters lacked expression of VEGFR2 and CD31 (also known as = PECAM1;=20 Supplementary=20 Fig. 1d, left and left middle panels, respectively). VEGFR2-positive = circulating endothelial progenitor cells migrated to fully formed BMDC = clusters=20 (Supplementary=20 Fig. 1d, right panel), and coincided with the arrival of tumour = cells (Supplementary=20 Fig. 1e, graph). Thus bone marrow-derived VEGFR1+ HPCs = initiate=20 and maintain the pre-metastatic niche.

Figure=20 2: Pre-metastatic clusters are comprised of VEGFR1+=20 haematopoietic progenitors.

a, VEGFR1 staining in irradiated lung before tumour = implantation (left panel and inset; n =3D 10) and 14 days after = LLC cell=20 implantation showing clusters in the lung (right panel, arrows; n = =3D 18,=20 3.9 3Dplusminus=20 0.2% cells with VEGFR1 staining per 3Dtimes=20100 objective field, P < 0.05). = b,=20 c, Double immunofluorescence in the lung of an animal with day 14 = LLC=20 tumour. b, VEGFR1+ (red) and GFP+ (green) = bone=20 marrow cells (left panel), VEGFR1+ (red) and = CD133+=20 (green) (right panel). c, VEGFR1+ (red) and = CD117+=20 (green). d, VEGFR1+ clusters in c-Myc transgenic lymph = node at=20 day 40 of life and before tumorigenesis (middle panel and inset showing=20 VEGFR1+ cells (red)) as compared with wild-type littermate = lymph node=20 without the transgene (left panel), and day 120 c-Myc transgenic node = with=20 lymphoma (right panel). In the inset of the right panel, arrows indicate = the=20 VEGFR1+ clusters (red) surrounded by lymphoma (green) = (n =3D 6).=20 Scale bar at bottom right applies to panels a (80 3Dmicro=20m; left inset, 40 3Dmicro=20m), b (20 3Dmicro=20m), c (20 3Dmicro=20m) and d (80 3Dmicro=20m; insets, 8 3Dmicro=20m).

High=20 resolution image and legend (62K)

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BMDC clusters occur in a spontaneous tumour model

We compared these findings to those in a spontaneous = tumour model=20 using c-Myc transgenic mice. On day 40 of life, prominent = VEGFR1+=20 clusters were detected exclusively in the lymph nodes of these animals = before=20 the onset of lymphoma (145.1 3Dplusminus=20 16.4 clusters per 3Dtimes=20100 objective field; Fig.=20 2d, middle panel and inset), with no observed clusters in wild-type=20 littermates (0.4 3Dplusminus=20 0.3, P < 0.001; Fig.=20 2d, left panel). By 120 days, VEGFR1+ clusters persisted = in=20 established lymphomas (67.8 3Dplusminus=20 9.5 versus 0.7 3Dplusminus=20 0.5 in c-Myc mice versus littermates, = P <=20 0.001; Fig.=20 2d, right panel and inset). The lymphoma cells, which surrounded the = VEGFR1+ HPCs, did not express VEGFR1 (Fig.=20 2d, right panel inset).

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BMDC clusters are recruited to pre-metastasic human tissue

To validate the mouse data showing tumour-specific = formation of=20 VEGFR1+ cellular clusters, we analysed human tissues from = patients=20 with malignancy. VEGFR1+ clusters were observed in both = primary=20 tumours and metastatic tissue (Fig.=20 3, showing breast carcinoma in an axillary lymph node, lung = carcinoma and=20 oesophageal carcinoma). There were increased cellular clusters in common = sites=20 of metastasis before tumour spread, suggesting the potential of this = tissue as a=20 future site for metastasis (Fig.=20 3, showing axillary lymph node (21 3Dplusminus=20 5 clusters per 3Dtimes=20100 objective field), lung (19 3Dplusminus=20 4) and gastro-oesophageal junction (25 3Dplusminus=20 4)). In patients without malignancy, lymph = nodes and lung=20 tissue did not show VEGFR1+ clusters (Fig.=20 3b, d,=20 insets). VEGFR1+ cellular clusters expressed the = haematopoietic=20 progenitor marker c-Kit (Fig.=20 3e, f,=20 insets).

Figure=20 3: Expression of VEGFR1 in pre-metastatic human = tissue.

a=96f, Cellular clusters stained with VEGFR1 = in=20 malignant and non-malignant tissues in individuals with breast (n = =3D 15),=20 lung (n =3D 15) and gastrointestinal (n =3D 3) cancers. = Lymph node=20 with evidence of breast adenocarcinoma metastasis (a, red arrows = indicate=20 tumour) and lymph node without malignancy from same patient (b). = Primary=20 lung adenocarcinoma (c) and adjacent 'normal' lung without = neoplasm=20 (d, red arrows indicate VEGFR1+ cells). No = VEGFR1+=20 clusters were seen in lymph node (b, inset; n =3D 6) and = lung tissue=20 (d, inset; n =3D 3) from individuals without cancer. Also = shown is a=20 primary adenosquamous carcinoma of the gastro-oesophageal junction = (e),=20 and a hepatic lymph node without carcinoma (f). Insets in = e,=20 f, show co-immunofluorescence of VEGFR1 (red) and c-Kit (green). = Scale=20 bar at bottom right applies to all panels (40 3Dmicro=20m; insets, 40 3Dmicro=20m).

High=20 resolution image and legend (183K)

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Functional role for VEGFR1+ BMDCs in directing = metastasis

We assessed the potential of purified VEGFR1+ = bone=20 marrow cells to initiate pre-metastatic clusters by selectively = transplanting=20 these progenitors into irradiated mice. By day 24 after LLC tumour cell=20 implantation, control mice that received wild-type bone marrow showed = prominent=20 lung metastases and established blood vessels (Fig.=20 4a, left panel and inset). However, mice transplanted with purified=20 VEGFR1+ cells formed numerous micrometastases throughout the = lungs=20 (25 3Dplusminus=20 9 micrometastases per 3Dtimes=20100 objective field; Fig.=20 4a, middle panel) with aberrant vasculature (Fig.=20 4a, middle panel inset). In contrast, bone marrow depleted of=20 VEGFR1+ cells failed to produce pre-metastatic clusters (Fig.=20 4a, right panel; P < 0.01 by analysis of variance = (ANOVA)). These=20 results suggest that the VEGFR1+ HPCs initiating the = pre-metastatic=20 cluster can attract tumour cells.

Figure=20 4: Inhibition of homing of bone marrow cells prevents=20 metastasis.

a, VEGFR1+-selected bone marrow (R1-pos) = permits=20 micrometastasis (red arrows, middle panel) but prevents = well-vascularized large=20 metastases as seen in wild types (left panel), 24 days after LLC = implantation.=20 Insets show CD31 (endothelial marker) expression. Bone marrow depleted = of=20 VEGFR1+ cells (non-R1) abrogates both clusters and metastases = (right=20 panel) (P < 0.01 by ANOVA). The table shows the number of = clusters and=20 micrometastases per 3Dtimes=20100 objective field. *denotes that the = metastasis filled=20 the lung. (R1-pos, n =3D 4; non-R1, n =3D 4; wild type, = n =3D 6;=20 non-R1 plus wild type, n =3D 4). b, Treatment with = antibodies to=20 VEGFR1 (anti-R1) and VEGFR2 (anti-R2) in mice with LLC tumours prevents = both=20 clusters and metastases (P < 0.01 by ANOVA; for all groups, = n =3D=20 5). Arrows in the lung of the wild type denote a large LLC metastasis. = Arrows in=20 anti-R2 show a cluster, inset shows a micrometastasis within a cluster. = T,=20 tumour cells. The table shows the number of clusters and LLC = micrometastases in=20 lung per 3Dtimes=20100 objective field. *denotes that the = metastasis filled=20 the tissue. Scale bar at bottom right applies to panels a = (20 m; wild type inset, 26 3Dmicro=20m; R1-pos inset, 32 3Dmicro=20m) and b (40 3Dmicro=20m; anti-R2 inset, 20 3Dmicro=20m).

High=20 resolution image and legend (69K)

To address whether disruption of VEGFR1+ = cellular=20 cluster formation could block the metastasis of well-established = tumours, mice=20 inoculated with LLC or B16 tumour cells were treated with monoclonal = antibodies=20 against VEGFR1 and/or VEGFR2. This approach allows for selective = targeting of=20 the BMDCs, as the tumour cells do not express either VEGFR1 or VEGFR2. = By day=20 24, widespread metastases were evident in untreated mice with LLC = tumours in the=20 lung (Fig.=20 4b, left panel) or B16 tumours in the spleen (Supplementary=20 Fig. 2, left panel and inset). Anti-VEGFR1 antibody treatment = eliminated the=20 initiating clusters and completely prevented metastasis (Fig.=20 4b, left middle panel; Supplementary=20 Fig. 3; P < 0.01 by ANOVA), whereas anti-VEGFR2 antibody = did not=20 prevent the formation of VEGFR1+ clusters but limited = metastatic=20 progression (15 3Dplusminus=20 11 micrometastases per 3Dtimes=20100 objective field; Fig.=20 4b, right middle panel and inset; Supplementary=20 Fig. 3). The two antibodies combined blocked cluster formation to an = extent=20 similar to anti-VEGFR1 therapy; however, we did observe an isolated LLC = lesion=20 in the lung of one animal (Supplementary=20 Fig. 3b, inset). Collectively, these results suggest that targeting = the=20 VEGFR1+ cell cluster can prevent tumour cell adhesion, = proliferation=20 and metastatic spread.

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VLA-4, MMP9 and Id3 mediate the pre-metastatic niche

We investigated the cellular and molecular mechanisms by = which=20 migratory HPCs, through interaction with the microenvironment, form = permissive=20 pre-metastatic niches. The interaction of VLA-4 (integrin 3Dalpha=2043Dbeta=201) with its ligand fibronectin is essential for = the=20 migration of haematopoietic cells within the bone marrow9,=20 10=20 and of circulating leukocytes4,=20 11.=20 We assessed whether VEGFR1+ cells express integrins, which = may=20 facilitate the interaction of this cell type with the pre-metastatic = niche. We=20 found that VEGFR1+ HPCs at the pre-metastatic cluster express = VLA-4=20 (Fig.=20 5a, and inset showing coexpression with VEGFR1), suggesting that = VLA-4=20 allows for the adhesion of the BMDCs that form the pre-metastatic niche. = Following cluster formation, 3Dalpha=2043Dbeta=207 and 3Dalpha=2063Dbeta=204 integrins were prominently expressed within the = metastatic=20 niche (data not shown). Proteinases including matrix metalloproteinase 9 = (MMP9),=20 produced by haematopoietic cells, can serve to break down basement = membranes,=20 thus altering the local microenvironments by releasing soluble = Kit-ligand and=20 VEGF-A to support newly introduced cells that express c-Kit12,=20 13.=20 In addition, metalloproteinase expression can be enhanced through 3Dalpha=2043Dbeta=201 signalling after fibronectin binding14,=20 15.=20 MMP9 was expressed in pre-metastatic clusters, and this upregulation of = MMP9=20 expression may be a result of integrin binding and activation in=20 VEGFR1+ HPCs (Fig.=20 5b). These findings expand upon previous work demonstrating that=20 VEGFR1-mediated induction of MMP9 directed metastasis to the = lungs7.

Figure=20 5: The VLA-4/fibronectin pathway mediates cluster=20 formation.

a=96c, Wild-type mice 14 days after tumour = implantation=20 develop clusters expressing VLA-4 (inset, VEGFR1 (red) and VLA-4 = (green)), MMP9=20 and Id3 (inset, VEGFR1 (red) and Id3 (green)). d, Lung tissue in = Id3=20 knockout (KO) mice with LLC tumours given = VEGFR1+GFP+=20 BMDCs (P < 0.01 by ANOVA; n =3D 6). Green arrows show = region in=20 upper inset. Red arrows (lower inset) show the site of metastasis with=20 GFP+VEGFR1+ cells. e, Baseline fibronectin=20 expression in the wild-type lung (n =3D 6) (left panel). = Increased stromal=20 fibronectin in the peribronchial region of the pre-metastatic lung at = day three=20 (middle panel, arrows), with maximal expression on day 14 (right panel). = Insets,=20 PDGRF3Dalpha=20 expression indicates resident fibroblasts laying down = fibronectin.=20 f, Quantitative RT=96PCR reveals increased fibronectin expression = in the=20 lungs of mice with LLC tumours compared with wild type (*P < = 0.05 by=20 ANOVA; n =3D 6), and a similar earlier trend in lungs from = animals with B16=20 melanoma. Scale bar at top right applies to panels a, b, = c=20 (40 3Dmicro=20m; insets, 8 3Dmicro=20m), d (80 3Dmicro=20m; top right inset, 20 3Dmicro=20m; bottom right inset 80 3Dmicro=20m) and e (40 3Dmicro=20m; insets, 20 3Dmicro=20m).

High=20 resolution image and legend (57K)

We previously showed that upregulation of Id gene = expression is=20 critical for the mobilization of progenitors that aid the growth of = primary=20 tumours15.=20 Id3 expression was also seen within the clusters (Fig.=20 5c, and inset showing coexpression with VEGFR1). Id3 may facilitate = the=20 mobilization of VEGFR1+ cells to the pre-metastatic niche. In = addition, expression of specific integrins is regulated by Id genes, and = may be=20 responsible for BMDC and stromal cell interactions, motility and=20 recruitment16.

To confirm the functional roles of these proteins in = establishing=20 the pre-metastatic niche, we either inhibited the expression of VLA-4 = (with=20 anti-integrin 3Dalpha=204 antibodies) or studied VEGFR1+ cell cluster = formation in=20 MMP9 and Id3 knockout mice. In these models, we found reduced cluster = formation=20 (Supplementary=20 Fig. 3a=96c) and metastatic spread three weeks after tumour = implantation. We=20 also found impaired mobilization of VEGFR1+ HPCs into the = circulation=20 of Id3 knockout mice compared to wild type (654 versus 3,283=20 VEGFR1+CD11b+ cells 3Dmicro=20l-1) in response to tumour inoculation (P = < 0.01=20 by Student's t-test; Supplementary=20 Table). Decreased mobilization of HPCs may explain the reduced = metastatic=20 phenotype seen in these animals2,=20 17.

To formally examine the potential of wild-type = VEGFR1+=20 cells to restore the metastatic defect in Id3 knockout mice, = Id3-competent=20 GFP+VEGFR1+ HPCs were injected intravenously into = Id3=20 knockout tumour-bearing mice. VEGFR1+ HPCs alone = re-established=20 cluster formation and micrometastases by day 21 after tumour = implantation (Fig.=20 5d, and upper inset; Supplementary=20 Fig. 3c). Notably, the LLC metastatic lesions were associated with=20 GFP+ BMDCs (Fig.=20 5d, lower inset). These findings further emphasize the functional = role of=20 VEGFR1+ BMDCs in the establishment of clusters and=20 metastasis.

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Fibronectin upregulation supports adhesion of VLA-4+ = BMDCs

We next investigated the potential of tissue-specific = ligands to=20 support the adhesion and formation of BMDC clusters. Following the = implantation=20 of LLC tumour cells, but before the homing of the=20 VLA-4+VEGFR1+ BMDCs, increased fibronectin = expression was=20 observed from day 3 (Fig.=20 5e, middle panel; Fig.=20 5f) to day 14 (Fig.=20 5e, right panel; Fig.=20 5f) in the vicinity of the future metastatic niche, compared with = the=20 baseline level of fibronectin expression in wild-type lung (Fig.=20 5e, left panel; Fig.=20 5f). Furthermore, resident fibroblast-like stromal cells (Fig.=20 5e, left panel inset), which proliferate in response to primary = tumour (Fig.=20 5e, right panel inset), may contribute to the localized deposition = of=20 fibronectin. Melanoma cells also induced fibronectin expression in the = lung in a=20 similar fashion to that of LLC cells (Supplementary=20 Fig. 3d). Moreover, increased fibronectin expression was notable in = multiple=20 tissues exposed to MCM, such as the intestine and oviduct, consistent = with the=20 more aggressive metastatic nature of B16 cells (fibronectin expression: = P=20 < 0.05 days 3=965 and P < 0.001 days 7=969 (by ANOVA) in = oviducts (Fig.=20 6a) and intestines (Fig.=20 6b) with MCM treatment compared with mice treated with = LLC-conditioned media=20 (LCM) or wild-type mice).

Figure=20 6: Redirection of LLC metastases to atypical = sites.

a, b, By quantitative RT=96PCR analysis, = increased=20 fibronectin expression was seen in the oviduct (a) and intestine=20 (b) in mice given MCM compared with wild-type and LCM-treatment. = For=20 oviduct, *P < 0.05 at days 3=965 and **P < 0.001 for = days 7=969=20 compared with wild type, and for intestine, *P < 0.001 at days = 7=969=20 compared with wild type by ANOVA (n =3D 6). c, = ELISA assay=20 (in triplicate) for VEGF and PlGF levels in the conditioned media = (*P=20 < 0.05 when compared with L-LCM, **P < 0.01 when compared = with=20 media alone, by ANOVA). d, Transwell migration assays (in = triplicate)=20 demonstrate enhanced migration of VEGFR1+ cells to LCM and = MCM=20 (**P < 0.001 by ANOVA). e, Treatment with MCM redirects = the=20 metastatic spread of LLC to B16 melanoma metastatic sites, such as the = spleen=20 (left panel), kidney (left middle panel), intestine (right middle panel) = and=20 oviduct (right panel). Arrows denote the regions of metastatic borders, = which=20 are shown in the insets (n =3D 6). T, LLC tumour cells. Scale bar = at bottom=20 right applies to panel e (200 3Dmicro=20m; insets, 20 3Dmicro=20m).

High=20 resolution image and legend (40K)

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VEGFR1+ cells promote tumour adherence and growth

To confirm that VEGFR1+ progenitors promote = the=20 chemoattraction and attachment of circulating tumour cells, we isolated = and red=20 fluorescence-labelled (PKH26-Gl) VEGFR1+ cells from mice with = malignancy (Supplementary=20 Fig. 4). Within one hour of in vitro co-incubation with green = fluorescence-labelled (PKH2-GL) B16 or LLC cells, the HPCs aggregated,=20 proliferated (150% increase) and promoted the attachment and = proliferation of=20 the tumour cells. In contrast, preculturing VEGFR1+ HPCs with = either=20 anti-VEGFR1 or anti-VLA-4 antibodies blocked this binding affinity and = expansion=20 (Supplementary=20 Fig. 4a, middle and right panels). Using a transwell migration = assay, tumour=20 cells manifested enhanced mobility in response to bone marrow-derived=20 VEGFR1+ cells (29.6 3Dplusminus=20 1.4 tumour cells per 3Dtimes=20200 objective field) as compared to cells that = do not=20 express VEGFR1 (11.2 3Dplusminus=20 0.4) and media alone (9.9 3Dplusminus=20 0.9, P < 0.001 by ANOVA; Supplementary=20 Fig. 4b). The SDF-1/CXCR4 chemokine axis participates in homing and=20 retention of HPCs within the bone marrow18.=20 Specific tumour cell types, which express CXCR4, may also migrate in = this=20 fashion in response to local chemokine gradients19,=20 20,=20 21.=20 Within the fully formed pre-metastatic cluster containing = VEGFR1+=20 cells, fibroblasts and fibronectin (Fig.=20 1a, left middle panel), SDF-1 (also known as CXCL12) became highly = expressed=20 (Supplementary=20 Fig. 4c). We also observed CXCR4 expression in B16 melanoma and LLC = tumours=20 (Supplementary=20 Fig. 4d). These data suggest that SDF-1 may provide one pathway for=20 attracting CXCR4+ tumour cells to the pre-metastatic = niche.

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Tumour-derived conditioned media dictate metastatic patterns

To delineate the mechanism of the organ-specific = metastatic=20 potential of LLC and B16 cells, we collected culture-derived conditioned = media.=20 Similarly, but more rapidly than primary LLC cells, the intraperitoneal=20 injection of LCM generated fibronectin expression, possibly from = resident=20 fibroblasts, and BMDC cluster formation (Supplementary=20 Fig. 5a) compared with media alone (Supplementary=20 Fig. 5a, insets). MCM stimulated fibronectin expression to a greater = extent=20 in liver than LCM (Supplementary=20 Fig. 5b). MCM caused enhanced fibroblast proliferation (data not = shown) and=20 fibronectin expression with cluster formation in a wide range of organs, = as=20 shown for intestine (Fig.=20 6a, b;=20 Supplementary=20 Fig. 5b) in comparison to media (Supplementary=20 Fig. 5b, inset). We analysed LCM and MCM for variations in growth = factors to=20 account for the distinct metastatic potentials and profiles of LLC and = B16 (Fig.=20 6c). We found high levels of VEGF in both conditioned media, more = than in=20 plasma from tumour-bearing mice (Supplementary=20 Fig. 5c). However, in MCM and melanoma-derived plasma we = specifically=20 detected higher levels of placental growth factor (PlGF), which signals = though=20 VEGFR1 alone, as compared with LCM- and LLC-derived plasma (Fig.=20 6c, Supplementary=20 Fig. 5c). Furthermore, in the low-metastatic-variant of LLC, levels = of both=20 VEGF and PlGF were much lower in the conditioned media (L-LCM) and = plasma=20 compared with its more aggressive counterpart (Fig.=20 6c, Supplementary=20 Fig. 5c). In a transwell assay, LCM and MCM enhanced the migration = of=20 VEGFR1+ BMDCs most effectively when compared with the other = growth=20 factor conditions (LCM 55% 3Dplusminus=20 0.4, MCM 68.1% 3Dplusminus=20 5, media 10.8% 3Dplusminus=20 1.7, P < 0.001 by ANOVA; Fig.=20 6d). Considering these results, we questioned whether cytokines such = as PlGF=20 present in MCM were capable of redirecting LLC metastases to = non-conventional=20 metastatic sites for this tumour. MCM given before intradermal LLC = implantation,=20 and daily thereafter, resulted in the redirection of LLC metastasis from = lung to=20 those sites frequently observed in melanoma including kidney, spleen, = intestine=20 and oviduct (Fig.=20 6e). Our results demonstrate that tumour-specific chemokines and/or=20 cytokines present in conditioned media, along with the = VEGFR1+=20 cellular clusters, are another determinant in the multidimensional = programme=20 driving metastatic spread.

The precise cellular and molecular mechanisms that = dictate=20 metastasis of a specific tumour to a predetermined metastatic location = are not=20 known. Many tumours have a predilection for metastasis to specific = organs. Based=20 on the current dogma, metastatic predisposition is believed to reflect = inherent=20 molecular differences in tumour cells themselves and the potential = influence by=20 surrounding stromal cells, which include the vasculature, connective = tissue and=20 immune cells22,=20 23,=20 24,=20 25,=20 26.=20 Our results introduce the concept that tumour metastasis is initiated by = a=20 well-defined sequence of events dependent on cellular 'bookmarking' = through=20 site-specific delivery of VEGFR1+ cells to form permissive = niches=20 within target organs. Our data suggest that differences in = tumour-secreted=20 humoral factors promote metastatic spread in specific distant organs. = Within=20 days following tumour implantation, fibronectin becomes upregulated in = certain=20 locations by resident fibroblast and fibroblast-like cells within target = organs=20 that are conventional sites of metastasis, corresponding to the = particular=20 primary tumour. Simultaneously, HPCs exit the bone marrow into the = peripheral=20 circulation as previously described11.=20 As a result of the niche-specific directional cues from fibronectin,=20 VEGFR1+ HPCs, expressing VLA-4 and Id3, can traverse = established=20 endothelium to form a pre-metastatic niche before the arrival of=20 CXCR4+ tumour cells and VEGFR2+ endothelial cells. = These=20 clusters, with MMP9 production altering the microenvironment and = enhanced=20 expression of SDF-1 creating a chemokine gradient, permit the attraction = of=20 tumour cells and their incorporation into the niche, thereby developing = a=20 complete metastatic lesion. We show that inhibition by a VEGFR1 antibody = or=20 depletion of VEGFR1+ cells from the bone marrow prevents the=20 formation of pre-metastatic clusters and, therefore, metastases. = Moreover,=20 blocking either VEGFR1 or VLA-4 inhibits the binding and establishment = of the=20 haematopoietic cell clusters and tumour cells. Restoration of the = pre-metastatic=20 niche and metastasis with the introduction of wild-type = VEGFR1+ cells=20 into Id3 knockout mice suggests that the expression of Id3 induces = expression of=20 the necessary elements, including MMP9, integrins and possibly = chemokines, to=20 provide a road map for the homing of VEGFR1+ cells essential = for the=20 establishment of the pre-metastatic niche.

Much focus has been placed on the role of inflammatory = cells in=20 aiding in tumour adherence and invasion into distant organs27,=20 28,=20 29,=20 30.=20 The VEGFR1+ HPCs identified in this study show = characteristics common=20 to physiological pathways of inflammation by providing the necessary = adhesion=20 molecules, proteinases, chemokines and growth conditions to create a = conducive=20 microenvironment for engraftment of tumour cells12,=20 20,=20 31.=20 The pre-metastatic niche, however, is distinct, introducing an = undifferentiated=20 state as seen with the VEGFR1+ HPC population. This is the = first=20 direct evidence that a non-neoplastic cell population can portend a = future=20 metastatic site. Furthermore, identification of haematopoietic clusters = in human=20 tissues before evidence of tumour spread demonstrates the applicability = of=20 targeting VEGFR1 and VLA-4 to identify and prevent metastasis in the = clinical=20 setting. This concept will have a tremendous impact on tumour staging, = and may=20 alter the landscape of adjuvant chemotherapy.

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Methods

Bone marrow transplantation

Wild-type C57Bl/6 mice were lethally irradiated=20 (950 rads) and transplanted with 1 3Dtimes=20 106 3Dbeta=20-gal+ bone marrow cells (from Rosa26 mice) or 1 = 106 GFP+ bone marrow = cells (from=20 EGFP-transgenic mice, C57Bl/6-TgN(ActbEGFP)1Osb/J;=20 Jackson Laboratory)2.=20 After 4 weeks, mice were injected intradermally in the flank with either = 2 106 LLC=20 or B16=20 cells (American Type Culture Collection).

Selective bone marrow transplantation

Mice irradiated as described above received a bone = marrow=20 transplant from purified cell populations obtained as described in the = Supplementary=20 Methods.

3Dbeta=20-Galactosidase staining

Tissues and femoral bones were fixed in 4% = paraformaldehyde=20 for 4 h. The samples were stained in = 5-bromo-4-chloro-3-indolyl--d-galactoside = (X-gal) solution at=20 37 =B0C, as described32,=20 for 36 h and then embedded2.

GFP visualization

Tissues were immediately frozen in OCT=20 compound (Tissue-Tek) without fixation. Serial sections (cryostat,=20 Leica) were mounted with Vectashield containing DAPI=20 (4,6-diamidino-2-phenylindole), and visualized with an ultraviolet = fluorescent=20 microscope (Nikon Eclipse=20 E800) with a Retiga=20 camera (QImaging) through IPLab=20 version 3.65a imaging software (Scanalytics).

Immunohistochemistry

Tissues were fixed and embedded in OCT or paraffin = as=20 previously described16.=20 The following antibodies were used: VEGFR1=20 clone MF-1 (ImClone Systems) or Flt1=20 clone C-17 (Santa Cruz Biotechnology); CD31=20 SC-1506 (Santa Cruz Biotechnology); VEGFR2=20 DC101 (ImClone Systems); MMP9=20 D19557 (Oncogene); Id3=20 C-20 (Santa Cruz Biotechnology); Fibronectin=20 TV-1 (Chemicon); CD11b=20 CBRM1/5 (eBioscience); CD34=20 RAM34 (BD Pharmigen); c-Kit=20 ACK2 (eBioscience); PDGFR APA5 (BD Pharmingen); V (Chemicon); CD133=20 13A4 (eBioscience); 4/VLA-4 PS-2 (Southern Biotech); 3Dalpha=205 (CD49e, 5H10-27); 6/CD49f GoH3 (BD Pharmingen); 1 9EG7 (BD Pharmingen); 2 M18/2 (BD Pharmingen); 4 (Santa Cruz Biotechnology); 7 M293 (BD Pharmingen); SDF-1=20 79018.111 (R&D Systems); and CXCR4=20 2B11 (BD Pharmingen).

Double immunofluorescence

Tissues in OCT were post-fixed with acetone. A = double=20 immunofluorescence protocol was performed as described in the Supplementary=20 Methods.

Antibody targeting

Wild-type mice were inoculated with 2 3Dtimes=20 106 LLC or B16 cells. For blockade = of VEGFR1=20 function, mice were injected intraperitoneally every 48 h, between = day=20 7=9622, with rat=20 anti-mouse VEGFR1 antibody (MF-1, IgG1, 400 3Dmicro=20g, ImClone Systems) or VEGFR2=20 antibody (DC101, IgG1, 800 3Dmicro=20g, ImClone Systems) or both, or with IgG control antibody, = and then=20 killed on day 24.

Conditioned media assays

Conditioned media was filtered (0.22-3Dmicro=20m filter) from serum-free media cultured on B16 (MCM) or LLC = (LCM)=20 cells for 18 h, as described33.=20 Conditioned media (300 3Dmicro=20l) was injected intraperitoneally daily for nine days into = wild-type=20 mice that had received Rosa26 bone marrow transplants four weeks = earlier.=20 Tissues were stained for fibronectin=20 TV-1 (Chemicon) and 3Dbeta=20-gal. For tumour redirection studies, intraperitoneal = injections of MCM=20 (300 3Dmicro=20l) commenced two days before intradermal LLC implantation and = then=20 daily over the next 21 days. Matched control groups with and without = tumour were=20 given serum-free media. Wild-type mice were injected with MCM = (300 l) daily for seven days before tail vein = injection of B16=20 tumour cells, and then daily until killed either one or four days after=20 intravenous tumour administration. Lungs were perfused with PBS before = embedding=20 in OCT.

Migration assays

Migration of VEGFR1+ cells in response = to=20 conditioned media was measured in a transwell assay. VEGFR1+ = cells=20 were isolated as above, and 1 3Dtimes=20 105 cells suspended in serum-free = media placed=20 in the upper compartment of 5-m-pore transwells (Costar, Corning). Cells = were=20 allowed to migrate for 18 h with conditioned media or corresponding = control=20 media in the lower compartment, with the analysis of cell counts = assessed every=20 6 h using a haemocytometer and trypan blue.

Quantitative analysis of fibronectin expression

Lung tissue was homogenized with a tissue = homogenizer in=20 TriZol reagent, and RNA was extracted as described previously34.=20 Fibronectin gene expression was quantified and normalized to=20 glyceraldehyde-3-phosphate dehydrogenase (Gapdh) expression by = polymerase=20 chain reaction with reverse transcription (RT=96PCR) using TaqMan=20 gene expression assays (Applied Biosystems) as described = previously35

Chemokine assays

Conditioned media, serum-free media and plasma = obtained from=20 mice with day 14 tumours were analysed for VEGF and PlGF concentrations = by an=20 enzyme-linked immunosorbent assay (ELISA; Quantikine,=20 R&D Systems) according to the manufacturer's instructions.

Flow cytometry

Flow cytometry was performed on an entire right = lung after=20 perfusion with PBS by right-ventricular injection. The tissue was minced = into=20 small pieces, filtered with 100-=20 and 40-3Dmicro=20m filters (BD Biosciences) to form a single-cell = suspension as=20 previously described35,=20 36.

Human specimens

Human specimens include: tumour tissue, adjacent = normal=20 tissue (beyond tumour margins), distant normal tissue and lymph nodes. = Tissues=20 were embedded as described above and stained with antibodies to human VEGFR1=20 FB5 (ImClone Systems) or Flt1=20 (Calbiochem). Tissue samples were obtained and handled in accordance = with an=20 approved Institutional Review Board application.

Quantitative immunohistochemistry

Using both IPLab and Adobe Photoshop 7.0, random = 100 objective fields were analysed by = selecting a=20 standardized colour range for 3Dbeta=20-gal or immunohistochemical staining. After boundary = delineation, the=20 area under the pixelation histogram was calculated, comparing total = staining=20 area to total tissue area.

Statistical analyses

Results are expressed as mean 3Dplusminus s.e.m. Data were analysed by Student's = t-test and=20 one way analysis of variance (ANOVA) using the GraphPad Prism=20 statistical program. P values <0.05 were considered = significant. Error=20 bars depict s.e.m.

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Acknowledgments

We thank M. Barna for critical reading of the manuscript = and L.=20 Breda, S. Rivella and S. Neustein for discussions. R.N.K. is a recipient = of the=20 Laura Rosenberg Fellowship award and supported by a grant from the = American=20 Hellenic Educational Progressive Association (Fifth District) and the = LTC=20 Foundation. D.L. is supported by the Doris Duke Charitable Foundation, = the=20 Children's Blood Foundation, the Emerald Foundation, the Theodore A. = Rapp=20 Foundation and a grant from the National Cancer Institute. S.R. is an=20 investigator of the Howard Hughes Medical Institute and supported by = grants from=20 the American Cancer Society, the Leukemia and Lymphoma Society, and the = National=20 Institutes of Health.

Competing interests statement:

The authors declared no competing interests.

Supplementary=20 information accompanies this paper.

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  1. Department of Pediatrics and the Children's Blood = Foundation=20 Laboratories,
  2. Cell and Developmental Biology,
  3. Howard Hughes Medical Institute,
  4. Genetic Medicine and
  5. Surgery, Weill Cornell Medical College of Cornell = University, 1300=20 York Avenue and
  6. Department of Pediatrics and
  7. Surgery, Memorial Sloan-Kettering Cancer Center, 1233 York = Avenue,=20 New York, New York 10021, USA
  8. Imclone Systems Incorporated, New York, New York 10014, = USA
  9. Fox Chase Cancer Center, Philadelphia, Pennsylvania 19111, = USA
  10. *These authors contributed equally to this work

Correspondence to: Shahin Rafii3,4David=20 Lyden1,2,6=20 Correspondence and requests for materials should be addressed to D.L.=20 (Email: dcl2001@med.cornell.edu) or = S.R.=20 (Email: srafii@med.cornell.edu).

Received 13 May 2005; Accepted 19 August = 2005

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ISSN: 0028-0836

EISSN: 1476-4687

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normal; FONT-SIZE: 70%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #000; = PADDING-TOP: 2px; TEXT-DECORATION: none } MAP.journal-nav UL LI UL.subnav A:visited { PADDING-RIGHT: 10px; DISPLAY: block; PADDING-LEFT: 20px; FONT-WEIGHT: = normal; FONT-SIZE: 70%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #000; = PADDING-TOP: 2px; TEXT-DECORATION: none } MAP.journal-nav UL LI UL.subnav A:hover { BACKGROUND: url(/common/images/nav_dots1.gif) #fab934 no-repeat 11px = 5px; COLOR: #fff; TEXT-DECORATION: none } MAP.journal-nav UL LI UL.subnav A.on { COLOR: #fff } MAP.journal-nav UL LI UL.subnav A.on:visited { COLOR: #fff } #journalnav MAP.supplementary UL A { FONT-WEIGHT: normal; FONT-SIZE: 70% } #journalnav MAP.supplementary UL A:visited { FONT-WEIGHT: normal; FONT-SIZE: 70% } H2.society-resources { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: = 80%; PADDING-BOTTOM: 2px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: 2px; = BACKGROUND-COLOR: #fab934 } UL.society-resources { 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