Michael T. Tetzlaff MD, PhD
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1 Molecular alterations informing the diagnosis of melanocytic tumors Michael T. Tetzlaff MD, PhD Associate Professor Department of Pathology, Section of Dermatopathology Department of Translational and Molecular Pathology The University of Texas MD Anderson Cancer Center Executive Officer Translational Research Program The Alliance for Clinical Trials
2 Disclosure In the past 12 months, I have had a financial relationship with the manufacturer(s) of the product(s) or provider(s) of the service(s) that will be discussed in my presentation. Advisory boards for Novartis, Myriad Genetics and Seattle Genetics.
3 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
4 Comparative genomic hybridization (CGH) systematically interrogates the whole genome Image courtesy of Dr. Priya Nagarajan. The relative hybridization of tumor derived probe compared to normal defines the relative composition of tumor DNA throughout the genome Gains show net green signal Losses show net red signal
5 CGH confirms widespread genomic instability in melanoma compared to nevi Applied CGH to 186 melanocytic tumors 132 Melanomas 54 Melanocytic nevi 96% of melanomas carry some Can chromosomal we exploit this copy difference aberration: between melanoma Gains or and losses nevi in in a discrete diagnostic fragments assay? of chromosomes
6 Fluorescence in situ hybridization (FISH): as a surrogate of CGH Hybridize fluorescently labeled probes: 11q13 (CCND1) 6p25 (RREB1) 6q23 (MYB) Cen6 11q13 6p25 6q23 Cen 6 Important advantage: Specifically interrogate these surrogate loci in the tumor cells. Assess tumor cell nuclei for abnormalities in the number of fluorescent signals. Geram i P et al. Am J Surg Pathology (8):
7 FISH assay as a surrogate of the genomic instability captured by CGH Cen 6 6p25 6q23 11q13 Probe Set UCSF/Northwestern Neogenomics RREB (6p25)>2 >29% >16% RREB (6p25)>CEN6 >55% >53% MYB (6q23)<CEN6 >40% >42% CCND1 (11q13)>2 >38% >19% Geram i P et al. Am J Surg Pathology (8):
8 Second generation FISH: New probes expand and improve the diagnostic utility of FISH cen9 9p21 6p25 8q24 11q13 Probe Cut-off RREB (6p25)>2 (Gain) >29% CDKN2A (9p21) Homozygous Deletion >29% MYC (8q24) >2 (Gain) >29% CCND1 (11q13)>2 (Gain) >29% Gerami P et al. Am. J. Surg Pathol (6):
9 Second generation FISH: New probes expand and improve the diagnostic utility of FISH 9p21 Cen6 Cen9 6p25 6p25 6q23 8q24 11q13 11q13 Probe Set Sensitivity Specificity FISH #1 75% 96% FISH #2 94% 98% Gerami P et al. Am. J. Surg Pathol (6):
10 FISH literature: unambiguous lesions Author Year Journal Gerami P 2009 AJSP Melanomas Tested Melanomas Positive SENSITIVITY Nevi Tested Nevi negative SPECIFICITY Type of case tested Gerami P 2010 Archives % Unambiguous MM vs Nevus Morey 2009 Pathology % % Unambiguous MM vs Nevus Newmann MD 2009 Modern Pathology % % Unambiguous MM vs Nevus Gaiser T 2010 Modern Pathology % % Unambiguous MM vs Nevus Moore MW 2011 Diagnostic Pathology % % Unambiguous MM vs Nevus Vergier B 2011 Modern Pathology % % Unambiguous MM vs Nevus Fang 2012 IJSP Unambiguous melanomas versus nevi Overall Sensitivity= 82.2% (479/583) Range: 43%-100% Overall Specificity= 95.3% (686/720) Range: 93%-100% % % Unambiguous MM vs Nevus % Metastases from these lesions Newmann MD 2009 Modern Pathology % % Lentiginous nevus of the elderly vs MM Pennachia 2012 Virchows % % Lentiginous nevus of the elderly vs MM Pouryazdanparast P 2009 AJSP % % Blue nevus-like MM vs Epithelioid Blue nevus Gammon B 2011 JCP % % Blue nevus-like MM vs Epithelioid Blue nevus Gerami P 2011 JCP % % Desmoplastic melanoma vs Desmoplastic nevus IMPORTANT LIMITATION: Most of these studies used unambiguous nevi Gerami P 2010 AJSP % % Superficial melanocytic neoplasms with pagetoid melanocytosis vs MM Gerami P 2009 AJSP % % Nevoid Melanoma vs nevus Busam KJ 2010 JCP % % Conjunctival melanoma vs Nevus % Dalton SR 2010 AJSP and unambiguous melanomas, where FISH Metastatic is MM vs nodal nevus; primary MM % % not needed. Requena 2012 Histopathology 12 (8) 7 88% 6 (5) 5 100% Spitzoid MM vs Spitzoid nevus Kiuru 2012 JCP % Sclerosing melanocytic nevus Diaz 2011 AJSP % % Spindle cell MM vs PSCN (Reed) Pouryazdanparast P 2011 AJSP % Nevus with atypical epithelioid cell component
11 FISH is less sensitive but highly specific in diagnostically challenging melanocytic lesions Author Year Journal Melanomas Tested Melanomas Positive SENSITIVITY Nevi Tested Nevi negative SPECIFICITY Type of case tested Gerami P 2009 AJSP % % DCML Vergier B 2011 Modern Pathology % % DCML For DCML: Melanoma versus Nevi Gaiser T 2010 Modern Pathology % 7 (3) 1 33% DCML Overall Sensitivity= 50.6% (43/85) Range: 43%-100% Zembowicz A 2012 Archives of Path Lab Med % % DCML Tetzlaff MT 2013 AJSP % % DCML Overall Specificity= 81.1% (167/206) Range: 33%-89% Al-Rohil 2016 Human Pathology % % DCML
12 The utility of FISH in diagnostically challenging melanocytic lesions Studied the largest series of ambiguous melanocytic tumors with clinically annotated outcomes (minimum 5 years follow-up). Histopathology versus clinical outcome Metastasis No Metastasis Favor benign 1 31 Favor melanoma Sensitivity=95% Specificity=52% FISH versus clinical outcome Metastasis No Metastasis FISH negative FISH positive 9 14 Sensitivity=43% Specificity=80% Vergier B et al. Modern Pathology :
13 The utility of FISH in diagnostically challenging melanocytic lesions Histopathologic Review FISH RESULT Metastasis No Metastasis Favor Malignant FISH NEG 8 23 n=49 FISH POS 9 9 Favor Benign FISH NEG 1 26 n=32 FISH POS 0 3 Vergier B et al. Modern Pathology :
14 Most lesions with benign morphology and benign follow-up are FISH-NEGATIVE Histopathologic Review FISH RESULT Metastasis No Metastasis Favor Malignant FISH NEG 8 23 n=49 FISH POS 9 9 Favor Benign FISH NEG 1 26 n=32 FISH POS 0 3 High specificity of FISH is reassuring in lesions where a benign diagnosis is favored Vergier B et al. Modern Pathology :
15 FISH-NEGATIVE lesions can produce metastases Histopathologic Review FISH RESULT Metastasis No Metastasis Favor Malignant FISH NEG 8 23 n=49 FISH POS 9 9 Favor Benign FISH NEG 1 26 n=32 FISH POS 0 3 FISH negative lesions produce metastasis. Vergier B et al. Modern Pathology :
16 There are FISH-POSITIVE lesions with a mostly benign morphology and follow-up Histopathologic Review FISH RESULT Metastasis No Metastasis Favor Malignant FISH NEG 8 23 n=49 FISH POS 9 9 Favor Benign FISH NEG 1 26 n=32 FISH POS 0 3 Benign lesions can be FISH positive. Vergier B et al. Modern Pathology :
17 FISH positivity correlates with worse outcome In a series of histopathologically unambiguous melanomas (n=144), compared clinical outcome between FISH+ (n=118) and FISH- (n=26) melanomas. NO correlation between FISH status and Breslow, ulceration, SLN status. Multivariate analysis: FISH+ Melanomas have increased risk for subsequent metastasis when controlled for: Age, Breslow thickness, Ulceration, SLN
18 FISH positivity correlates with worse outcome Gains at 8q24 or 11q13
19 FISH positivity correlates with worse outcome Gains at 8q24 or 11q13
20 FISH positivity correlates with worse outcome Homozygous deletion of 9p21 in Spitzoid lesions Assessed 75 Atypical Spitz Tumors by FISH (First and Second generation probes)
21 FISH positivity correlates with worse outcome Homozygous deletion of 9p21 in Spitzoid lesions Assessed 75 Atypical Spitz Tumors by FISH (First and Second generation probes) SLN- SLN+ SLNx SLN+/LN+ Death
22 FISH positivity correlates with worse outcome Homozygous deletion of 9p21 in Spitzoid lesions Assessed 75 Atypical Spitz Tumors by FISH (First and Second generation probes) SLN- SLN+ SLNx SLN+/LN+ Death
23 FISH positivity correlates with worse outcome Homozygous deletion of 9p21 in Spitzoid lesions 9p21 9/11 patients with metastasis beyond sentinel node and/or death, showed homozygous deletion of 9p21 compared to 3/64 among those in group 1.
24 FISH positivity correlates with worse outcome Homozygous deletion of 9p21 in Spitzoid lesions 9p21 9/11 patients with metastasis beyond sentinel node and/or death, showed homozygous deletion of 9p21 compared to 3/64 among those in group 1.
25 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
26 htert promoter mutations as a surrogate of clinical outcome among Spitzoid lesions Clinical Features Favorable (n=52) Unfavorable (n=4) Age (years) (P =0.03)* < (60%) 21 (40%) 0 (0%) 4 (100%) Gender (P =0.64) Female Male 30 (60%) 22 (40%) 3 (75%) 1 (25%) 56 patients with Atypical Spitz Tumor and follow-up 21/40 (50%) who underwent SLN biopsy with at least one positive SLN 9 patients with extensive nodal metastases 4 patients with hematogenous metastases who died of disease Mean follow up for remaining 52 patients=32.5 months Location (P=0.27) Lower extremity Upper extremity Face Ear Scalp Trunk Race (P=0.70) White Black Other Not specified Lesional diameter (p=0.054) 5 mm 6-10 mm >10 mm (81%) 2 (5%) 5 (14%) (43%) 23 (45%) 6 (12%) (100%) 0 (0%) 0 (0%) 0 1 (33%) 0 (0%) 2 (67%) 1
27 htert promoter mutations as a surrogate of clinical outcome among Spitzoid lesions All 4 patients who died of disease had htert promoter mutations 0/52 patients alive had TERT promoter mutations 12/49 with favorable outcome had homozygous deletion of 9p21 2/4 patients who died of disease had homozygous deletion of 9p21 All 4 had loss of p16 protein by IHC
28 htert promoter mutations as a surrogate of clinical outcome among Spitzoid lesions TERT promoter mutations are not always associated with poor prognosis in atypical spitzoid tumors. Requena C, Heidenreich B, Kumar R, Nagore E. Pigment Cell Melanoma Res htert promoter mutations Spitz/Reed Nevi (n=15) AST/SMM (n=9) 0/15 2/9 1 of 2 AST/SMMs with htert promoter mutations had positive SLN Both patients alive and without disease (60 and 66 months) htert promoter mutations as marker of bad prognosis could not be demonstrated in our series
29 Case Presentation 33 year old woman with a brown lesion on the thigh, recently enlarging and becoming darker
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34 Mart-1/Ki-67
35 FISH results 9p21 cen9 6p25 8q24 11q13
36 Final Diagnosis INVASIVE MELANOMA, CLARK LEVEL IV (AT LEAST), BRESLOW THICKNESS 0.98 MM (AT LEAST), MITOTIC FIGURES: 1/mm 2 WITH SPITZOID FEATURES 9p21 cen9
37 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
38 Germline BAP1 loss confers risk to develop melanocytic tumors with distinct morphology Two families with multiple members bearing numerous papular melanocyic neoplasms with typical Spitzoid morphology and occasional uveal melanomas. Haplotype analyses determined that affected Analyzed lesions by acgh and identified frequent Sequencing individuals analyses inherited of the same minimally maternal deleted deletions of variable portions of chromosome 3p chromosome region identified 3. The deleted mutations copy in was BAP1. always in the lesions of both families. paternal.
39 BAP1 loss also seen in sporadically occurring melanocytic tumors with distinct morphology Assessed 32 Atypical Spitz tumors by BAP1 IHC: BAP1 negative in 9/32 tumors with characteristic features: Papular lesions on the trunk Predominantly dermal Epithelioid cells Prominent TILS BRAF V600E (8/9 cases)
40 BAP1 loss also seen in sporadically occurring melanocytic tumors with distinct morphology
41 Case Presentation A 45 year-old man presented with a papular brown lesion on abdomen.
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46 BAP-1
47 BRAF-V600E
48 Final Diagnosis Combined melanocytic nevus, with features of Spitz nevus and BAP1 loss, present at tissue edges.
49 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
50 Kinase fusions are frequent in melanocytic lesions with Spitzoid morphology Different fusion partner gene Spanned the spectrum of Spitzoid neoplasia Each fusion occurred in mutually exclusive fashion of others Constitutively active kinase activity IHC+ Kinase
51 Spitzoid lesions with ALK kinase fusions have distinctive clinical and histopathologic features ALK kinase fusion lesions (n=49) Median Age Gender Anatomic Location Diagnosis ALK IHC Clinical outcome 14y (Range: y) 29 female: 20 male 26 Extremities 12 trunk 9 Head/Neck 11 Spitz nevus; 34 AST; 4 Spitzoid MM 100% positive 2 with SLN deposits (All alive; NED)
52 Spitzoid lesions characterized by many distinctive genetic abnormalities HRAS mutation and 11p amplification Homozygous deletion of 9p21 Loss of 6q23 Kinase fusions: o ALK o ROS1 o NTRK1 o BRAF o RET o MET o NTRK3 Spitzoid proliferation BAP1 loss with BRAF V600E htert promoter mutation
53 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
54 Melanoma, blue nevus type
55 Distinguishing among blue nevus-like lesions remains a challenge Location Cellularity Blue nevus Mid- to upper dermis Dendritic melanocytes with coarse pigment Cellular Blue nevus Pan-dermal Biphasic with dendritic and epithelioid melanocytes Atypical Cellular Blue nevus Pan-dermal Biphasic with dendritic and epithelioid melanocytes Melanoma, Blue nevus type Pan-dermal and may involve subcutis May contain or resemble blue nevus/cellular blue nevus Size Small (<10 mm) Can be >10 mm Can be >10 mm >10 mm Symmetry Present Present Present/Absent Usually absent Cytologic atypia Absent Absent Increased Prominent Mitotic figures Usually absent Infrequent Increased High, atypical Necrosis Absent Absent Absent Present
56 Chromosomal instability is typical of blue nevus-like melanomas Copy number changes Cellular Blue nevus Melanoma, Blue nevus type 3/17 (17%) 6/9 (67%) In comparison to cellular blue nevi, melanoma blue nevus type exhibits significant chromosomal instability
57 Chromosomal instability typical of blue nevus-like melanomas detected by FISH 100% (22/22) Blue nevi FISH negative 100% (5/5) Melanoma, blue nevus type FISH positive 90% (9/10) Blue nevus like metastases FISH positive
58 BAP1 loss and genomic instability in melanoma, blue nevus-type Loss of nuclear BAP1 IHC GNAQ mutation (Exon 5) GNA11 mutation (Exon 5) Cellular Blue nevus Melanoma, Blue nevus type 0/24 (0%) 7/11 (64%) 16/18 (89%) 1/11 (9%) 1/18 (6%) 8/11 (73%) GNAQ/GNA11 mutations in both benign and malignant blue nevus-like proliferations BAP1 loss typical in melanoma, blue nevus type Chromosomal abnormalities frequent in melanoma, blue nevus type
59 Targeted sequencing identifies mutations specific to Melanoma, blue nevus type BAP1 and SF3B1 mutated only in melanoma, blue nevus-type GNAQ/GNA11 mutations across the spectrum of blue nevus-like lesions BAP1 and SF3B1 mutated in melanoma, blue nevus type Sequencing analyses likely to be informative in diagnosis of blue nevus like lesions.
60 Molecular studies informing the diagnosis of melanocytic tumors Comparative Genomic Hybridization (CGH) Fluorescence in situ hybridization (FISH) is a surrogate of genomic instability described by CGH First generation FISH Sensitivity, specificity and pitfalls How does FISH inform our diagnosis? Second-generation FISH testing FISH and prognosis htert promoter mutations BAP1 associated Spitzoid lesions Translocation associated Spitzoid lesions Molecular alterations distinguishing Melanoma Blue nevus type Gene expression profiling as an additional ancillary test
61 Gene expression signature as an additional adjunct to inform the diagnosis N=1 N=5 N=8
62 Gene expression signature as an additional adjunct to inform the diagnosis
63 Validation of gene expression signature as an additional adjunct to inform the diagnosis Sensitivity: 91.5% Specificity: 92.5%
64 Gene expression signature correlates with clinical outcome All malignant lesions produced distant metastases and all benign lesions had >5 years follow up. Sensitivity (diagnosis of melanoma): 93.9% Specificity (diagnosis of benign): 96.2%
65 Thank you Questions Victor Prieto MD PhD Jonathan L. Curry MD Carlos A. Torres-Cabala MD Priya Nagarajan MD PhD Phyu Aung MD PhD Doina Ivan MD
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