Molecular Testing in Solid Tumors: An = Overview

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TABLE OF CONTENTS

[THYROID= =20 CARCINOMA...] [OLIGODE= NDROGLIOMA=20 AND...] [LUNG=20 ADENOCARCINOMA...] [CONCLUS= ION]=20 [REFERE= NCES]=20 [TAB= LES] [FI= GURES]

=A9=20 Copyright by College of American Pathologists 2008=20

Archives of Pathology and Laboratory = Medicine:=20 Vol. 132, No. 2, pp. 164=96167.

Molecular Testing in Solid Tumors: An Overview

Jennifer L. Hunt, MD, MEd

From the Department of Anatomic Pathology, Cleveland Clinic=20 Foundation, Cleveland, = Ohio

Accepted July 30, 2007

Molecular testing in anatomic pathology is going = to become=20 more and more important during the next decade as we develop assays = that can=20 aid in diagnosis, prognosis, and predicting response to therapy. The = anatomic pathologist needs to be familiar with the different assays=20 available but also needs to be able to discern which are going to = become=20 standard of care and which will not. Three different types of tumors = are=20 reviewed: thyroid cancer, oligodendroglioma, and lung carcinoma. = Molecular=20 assays that are currently in use or on the near horizon, including=20 translocation analyses for RET-PTC and = PPARγ-PAX8, point=20 mutation analysis for BRAF and epidermal growth factor = receptor, and=20 genetic loss for 1p and 19q, are = discussed.

3D"" Traditionally, pathologists have relied on the=20 hematoxylin-eosin=96stained slide to make diagnoses. Prognostic = indicators were=20 limited to those that could be seen at the light microscopic level and = included=20 such variables as surgical margin status, lymph node metastases, and = perineural=20 and angiolymphatic invasion. These tools remain at the core of pathology = practice for clinical care of patients. In the past 2 decades, the = analysis of=20 protein expression by immunohistochemical staining has become an = integral tool=20 for assessment of pathology specimens. More recently, molecular testing = is being=20 integrated into very specific areas in diagnostic pathology.

3D"" Molecular testing in anatomic pathology serves = various=20 functions. The testing can be used diagnostically to assist in = classifying or=20 subclassifying tumors or other lesions. Clinical molecular testing can = also be=20 used for prognostic purposes. Finally, testing for molecular mutational = events=20 can be performed to analyze potential to respond to therapeutic = agents.

3D"" The technologies that are used in assays for = mutational events=20 in anatomic pathology are often based on standard molecular biology = techniques=20 and assays. Many of the clinical assays rely on amplification of nucleic = acids=20 (polymerase chain reaction [PCR]) and hybridization techniques = (fluorescent in=20 situ hybridization [FISH]). Three types of tumors are discussed in this = brief=20 review, with particular emphasis on some of the specific molecular = assays that=20 are currently in use or in development for these organ systems. Several = specific=20 techniques are discussed in reference to clinical applicability in = samples from=20 the anatomic pathology laboratory.

THYROID CARCINOMA: RET-PTC, PPARγ-PAX8, AND = BRAF=20 Return= =20 to TOC

3D"" Thyroid tumors have several well-identified = molecular=20 mutations. These have given us a better understanding of pathogenesis = and now=20 are making their way into use for clinical diagnostic testing. In fact, = several=20 studies have now reported utility of molecular testing in thyroid = specimens=20 preoperatively in fine-needle aspiration samples in final pathology = diagnosis.^1,²

3D"" The 2 most common types of mutations in thyroid = cancers are=20 translocations and point mutations. Translocations, or intrachromosomal=20 rearrangements, between the RET proto-oncogene and various = partner genes=20 are found in up to 40% of papillary carcinomas.³=20 The most common partner genes are H4 (PTC1) and = ELE1=20 (PTC3) (Figure=20 1 3D"" ). These translocations, and particularly = RET-PTC3, are more=20 common in radiation-induced tumors.⁴

3D"" The other translocation that is notable in thyroid = cancers=20 occurs in follicular carcinomas. Up to 40% of follicular carcinomas = harbor a=20 translocation between the PAX8 gene and the PPARγ = gene=20 (PAX8-PPARγ).^5,⁶=20 Oncocytic carcinomas do not usually have this PAX8-PPARγ = translocation.=20 However, recent evidence has suggested that some cases of follicular = variant of=20 papillary carcinoma may harbor this translocation.⁷

3D"" Translocations can be difficult to detect in = paraffin samples.=20 Many translocation breakpoints occur in large introns and may not be = highly=20 clustered, making PCR from genomic DNA very difficult. The most common = strategy=20 for testing is to use the messenger RNA (mRNA), in which the introns are = spliced=20 out, resulting in consistent fusion of exons from the 2 different = partner genes=20 in the mRNA. Unfortunately, mRNA is not of high quality when obtained = from=20 paraffin samples, and so many of the translocation assays are designed = for fresh=20 or frozen tissue. Another testing option for translocations that has = proven to=20 be highly successful in paraffin-embedded tissues is FISH. Dual color = probes, or=20 chromosome-specific paints, will localize each chromosome involved in = the=20 translocation. After hybridization in the assay, the abnormal fusions or = breaks=20 can be identified. Finally, the overexpression of a fusion protein = driven by the=20 translocation can be detected by immunohistochemistry in certain = instances.=20 Antibodies for RET and PPARγ have been used in this way. This = approach is=20 usually the least specific because protein expression can be increased = through a=20 variety of mechanisms.

3D"" The final notable mutation in papillary carcinoma = is found in=20 the BRAF gene, which encodes for a serine threonine kinase.^8,⁹=20 This point mutation is a T-to-A transition at codon 600 (nucleotide = 1799). This=20 mutation is thought to be the most common mutation in papillary = carcinomas and=20 is estimated to be found in 40% to 60% of cases.¹⁰=20 The mutation is more frequently found in conventional and tall-cell = variant=20 tumors and is uncommon in follicular variant of papillary carcinoma.⁵=20 Point mutations can be detected by a variety of assays, most of which = are based=20 in PCR techniques. These assays include standard direct gene sequencing, = quantitative PCR, and newer platforms, such as pyrosequencing. All of = the assays=20 are fairly reliable for identifying cases with the characteristic = BRAF=20 gene mutation in papillary thyroid carcinoma.

OLIGODENDROGLIOMA AND LOSS OF 1p AND 19q Return= =20 to TOC

3D"" In brain tumors, concurrent loss of 1p and 19q is = associated=20 with oligodendroglioma differentiation.¹¹=20 This mutational profile has also been shown to correlate with responses = to=20 chemotherapy.¹²=20 By contrast, loss of heterozygosity (LOH) mutations in p53 and = p16=20 may be associated with a poor survival or with tumor progression.¹³=20 Because of the strong prognostic and diagnostic value of 1p and 19q loss = analysis, some institutions are testing oligodendrogliomas and other = primary=20 glial neoplasms for these genetic abnormalities.^14,¹⁵=20 The areas of 1p and 19q that are lost are fairly large and have been = called the=20 minimal deletion regions. Usually, multiple markers are used to = cover the=20 region (Figure=20 2 3D"" ).¹⁶

3D"" Loss of chromosomal arms can be assessed by FISH = or by PCR,=20 using an LOH analysis.¹¹=20 FISH for loss of genetic material on fixed tissue sections can be = difficult to=20 interpret because of incomplete nuclei from drop-out in tissue = sectioning.=20 However, with appropriate validation, this is an excellent diagnostic = test.

3D"" Loss of heterozygosity analysis relies on our = ability to=20 discriminate between the 2 inherited copies of a particular gene. = Polymerase=20 chain reaction=96based technologies have evolved to do this type of = assessment=20 using the polymorphisms in the human genome. These polymorphisms occur=20 frequently with an estimated periodicity of at least 1 polymorphism per = 1000=20 base pairs. Loss of heterozygosity analysis usually uses short tandem = repeat=20 polymorphisms. These are areas in the genome at which there is a short = sequence=20 of DNA that is repeated. The sequence of the repeat unit is the same = from person=20 to person, but it is repeated for a variable number of times; these=20 polymorphisms are inherited.

3D"" For PCR assays to assess for LOH, primers are = designed to=20 flank a location-specific short tandem repeat polymorphism. In a person = who is=20 heterozygous for that gene locus, the PCR amplicons will have different = lengths=20 because there are 2 copies of the gene with different numbers of repeat = units.=20 Polymerase chain reaction products of different sizes will migrate at = different=20 speeds in both gel and capillary electrophoresis analyses. In tumor = cells that=20 have lost 1 copy of a normally heterozygous short tandem repeat = polymorphism=20 (LOH), there will be only 1 PCR product.

3D"" Both LOH and FISH assays are commonly used to = detect loss of=20 1p and 19q in oligodendrogliomas. These assays provide valuable clinical = prognostic and therapeutic information.¹³

LUNG ADENOCARCINOMA AND EPIDERMAL GROWTH FACTOR RECEPTOR = Return= =20 to TOC

3D"" Lung carcinogenesis is complex and has = predominantly been=20 associated with smoking-related genetic damage. One of the common = mutations=20 found in lung cancer is a point mutation in the RAS oncogene.¹⁷=20 These mutations are often clustered in 2 different hot spots and can be = fairly=20 easily detected by direct sequencing. Many other mutations in other = genes,=20 including tumor suppressor genes, have also been described in lung=20 carcinogenesis.¹⁸=20 The recent discovery of alterations in epidermal growth factor receptor=20 (EGFR) in lung carcinomas has been intriguing, especially because = there=20 are drugs that are directed against EGFR that have become = potential=20 targeted therapies for lung carcinoma (Table=20 1 3D"" ).

3D"" Epidermal growth factor receptor is also known as=20 c-Erb-B1 and HER1. Epidermal growth factor receptor and = the=20 closely related family members HER2/neu (c-Erb-B2) and=20 Erb-B3 and Erb-B4 are all cell membrane receptors that = have=20 intrinsic tyrosine kinase activities. Epidermal growth factor receptor = is a=20 170-kd protein, 1186 amino acid transmembrane protein that has an = extracellular=20 ligand-binding domain, a transmembrane domain, and an intracellular = tyrosine=20 kinase domain. As with other oncogenes, EGFR can be assessed at = several=20 different levels: At the genomic level, we can identify mutations in the = DNA=20 sequence or copy number changes. At the mRNA level and the protein = expression=20 level, the amount of gene expression or the protein expression can be = analyzed.=20 In lung cancers, studies have detected alterations in EGFR at = each=20 level.^19,²⁰

3D"" In lung carcinomas, overexpression of EGFR by=20 immunohistochemistry is often seen. Variable results have been reported=20 regarding the prognostic significance of EGFR expression. Gene = amplification by=20 FISH has also been described in lung carcinomas, and recent reports do = suggest=20 that amplification has prognostic and therapeutic implications.^21,²²

3D"" One of the most interesting EGFR = alterations has been=20 recently described.^23=9625=20 Mutations have been found clustered in the tyrosine kinase domain of the = EGFR gene, occurring almost exclusively in lung carcinomas. They = are=20 thought to be highly specific to certain populations of patients with = specific=20 tumors: young women, never-smokers, and adenocarcinomas (Table=20 2 3D"" ).^24,²⁶

3D"" Despite much work on other types of tumors, there = have been=20 very few reports of EGFR mutations outside of lung carcinomas. = The=20 reported rates of EGFR mutation in lung cancers are variable and = are=20 obviously highly dependent on the population being tested. The = EGFR=20 mutations are clustered in the region of exons 18 to 21, which is the = area that=20 encodes the ATP-binding pocket of the tyrosine kinase domain of = EGFR. The=20 most common mutations involve exons 19 and 21, which account for more = than 95%=20 of mutations. Exon 19 mutations are deletion mutations, usually = involving=20 between 10 and 20 base pairs of the exon 19 sequence, beginning around = codon=20 746; occasional exon 19 point mutations are also seen (codon 719). Exon = 21=20 mutations are almost always point mutations, involving codon 858 with a = T-to-G=20 transversion in most cases.

3D"" The relationship between somatic EGFR = sequence=20 mutations and response to anti-EGFR therapies has been controversial. = Initial=20 reports were promising, with demonstrated tumor shrinkage and benefits = in=20 surrogate endpoints.^23,²⁵=20 It appeared that mutations in the EGFR gene were more frequent in = patients who responded to anti-EGFR therapies. However, importantly, all = of=20 these reports also acknowledge that some patients without identifiable = mutations=20 responded to anti-EGFR therapy. More recent studies have failed to = demonstrate=20 long-term benefit in survival advantages with treatment with anti-EGFR=20 therapies.^27,²⁸=20 Therefore, testing for the point mutations and deletion mutations in the = EGFR gene has not become standard practice at this time.

CONCLUSION Return= =20 to TOC

3D"" This overview provides several examples of = molecular tests in=20 different stages of clinical applicability. The life cycle of new = diagnostic=20 assays is complex. Some assays quickly and appropriately become the = standard of=20 care. Others are brought into clinical practice slowly, as needs evolve = and=20 develop. Still others show initial promising results but are abandoned = when they=20 fail to provide value in practice or when clinical management changes = over time.=20 The assays discussed provide examples that fit into each of these=20 categories.

3D"" Molecular testing in anatomic pathology will = almost certainly=20 become critical for providing optimal patient care during the next 5 to = 10=20 years. As more assays are developed that provide valuable diagnostic,=20 prognostic, and therapeutic information for patient management, anatomic = pathologists will need to be familiar with the literature to order = appropriate=20 ancillary studies. Advanced molecular assays are best interpreted in an=20 integrated fashion, with basic hematoxylin-eosin morphology and=20 immunohistochemical findings remaining an essential component of the = overall=20 diagnosis.

References Return= =20 to TOC

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2. Cohen Y,=20 Rosenbaum E, Clark DP. et al. Mutational analysis of BRAF in fine needle = aspiration biopsies of the thyroid: a potential application for the = preoperative=20 assessment of thyroid nodules. Clin Cancer Res = 2004;10:2761=962765. [PubMed=20 Citation]

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Tables Return= =20 to TOC

3D""=20 Table 1. 3D""=20 Three Most Common Anti=96Epidermal Growth Factor Receptor = Drugs Currently=20 Available and the Food and Drug Administration (FDA) Approval=20 Status

3D""=20 Table 2. 3D""=20 Epidermal Growth Factor Receptor (EGFR) Sequence Mutations in = Different=20 Populations*

Figures Return= =20 to TOC

Click on thumbnail for full-sized = image.

3D""=20 Figure 1. 3D""=20 This diagram demonstrates the RET-PTC1 rearrangement, in = which exon 1=20 of the H4 gene is fused to exons 12 to 20 of the RET=20 gene

Click on thumbnail for full-sized = image.

3D""=20 Figure 2. 3D""=20 This diagram demonstrates the approach used to select short = tandem=20 repeats covering a minimal deletion region for 1p and 19q. These short = tandem=20 repeats fall within the minimal deletion = region

The author has no relevant financial = interest in the=20 products or companies described in this article.

Presented at the Texas Society = of=20 Pathologists 86th Annual Meeting, Fort Worth, Tex, January 26=9628, = 2007.

Reprints: Jennifer L. Hunt, MD, = MEd,=20 Department of Anatomic Pathology, L25, Cleveland Clinic Foundation, 9500 = Euclid=20 Ave, Cleveland, OH 44195 (E-mail: huntj2@ccf.org)

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