Targeted next generation sequencing reveals unique mutation profile of primary melanocytic tumors of the central nervous system

Journal of Neuro-Oncology

Volumn 127, Issue 3, 2016, Pages 435-444

  van de Nes, Johannes ^a   Gessi, Marco ^b   Sucker, Antje ^a   Möller, Inga ^a   Stiller, Mathias ^a   Horn, Susanne ^a   Scholz, Simone L ^a   Pischler, Carina ^h   Stadtler, Nadine ^a   Schilling, Bastian ^a   Zimmer, Lisa ^a   Hillen, Uwe ^a   Scolyer, Richard A ^d,f,g   Buckland, Michael E ^e,f   Lauriola, Libero ⁱ   Pietsch, Torsten ^b   Waha, Andreas ^b   Schadendorf, Dirk ^a   Murali, Rajmohan ^c   Griewank, Klaus G ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d Departments of Tissue Pathology and Diagnostic Oncology   (Australia)

^e ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^f UNIVERSITY OF SYDNEY   (Australia)

^g MELANOMA INSTITUTE AUSTRALIA   (Australia)

^h MEDICAL UNIVERSITY OF GRAZ   (Austria)

ⁱ CATHOLIC UNIVERSITY   (Italy)

Author keywords

BAP1; GNA11; GNAQ; Melanocytoma

Indexed keywords

ARID1A GENE; ARTICLE; BAP1 GENE; BRAF GENE; CANCER DIAGNOSIS; CANCER GRADING; CANCER PROGNOSIS; CENTRAL NERVOUS SYSTEM PRIMARY MELANOCYTIC TUMOR; CENTRAL NERVOUS SYSTEM TUMOR; CHROMOSOME 3; CUTANEOUS MELANOMA; GENE; GENE MUTATION; GENETIC ANALYSIS; GNA11 GENE; GNAQ GENE; HUMAN; HUMAN TISSUE; MELANOCYTOSIS; METASTASIS; NEXT GENERATION SEQUENCING; NF1 GENE; ONCOGENE N RAS; PIK3CA GENE; PRIMARY TUMOR; RAC1 GENE; UVEA MELANOMA; ADOLESCENT; ADULT; AGED; CANCER STAGING; COPY NUMBER VARIATION; ENZYME IMMUNOASSAY; FEMALE; FOLLOW UP; GENETICS; HIGH THROUGHPUT SEQUENCING; MALE; MELANOMA; MENINGIOMA; MIDDLE AGED; MUTATION; PATHOLOGY; PROCEDURES; PROGNOSIS; SKIN TUMOR; TUMOR RECURRENCE; YOUNG ADULT;

BAP1 PROTEIN, HUMAN; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN THIOLESTERASE;

ADOLESCENT; ADULT; AGED; BIOMARKERS, TUMOR; CENTRAL NERVOUS SYSTEM NEOPLASMS; DNA COPY NUMBER VARIATIONS; FEMALE; FOLLOW-UP STUDIES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MELANOMA; MENINGEAL NEOPLASMS; MIDDLE AGED; MUTATION; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PROGNOSIS; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE; YOUNG ADULT;

EID: 84953432675     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-015-2052-2     Document Type: Article

References (32)

1. Goldgeier MH, Klein LE, Klein-Angerer S, Moellmann G, Nordlund JJ (1984) The distribution of melanocytes in the leptomeninges of the human brain. J Invest Dermatol 82:235–238
2. Wadasadawala T, Trivedi S, Gupta T, Epari S, Jalali R (2010) The diagnostic dilemma of primary central nervous system melanoma. J Clin Neurosci Off J Neurosurg Soc Australia 17:1014–1017. doi:10.1016/j.jocn.2009.12.020
3. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, Nickerson E, Auclair D, Li L, Place C, Dicara D, Ramos AH, Lawrence MS, Cibulskis K, Sivachenko A, Voet D, Saksena G, Stransky N, Onofrio RC, Winckler W, Ardlie K, Wagle N, Wargo J, Chong K, Morton DL, Stemke-Hale K, Chen G, Noble M, Meyerson M, Ladbury JE, Davies MA, Gershenwald JE, Wagner SN, Hoon DS, Schadendorf D, Lander ES, Gabriel SB, Getz G, Garraway LA, Chin L (2012) A landscape of driver mutations in melanoma. Cell 150:251–263. doi:10.1016/j.cell.2012.06.024
4. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, Cheng E, Davis MJ, Goh G, Choi M, Ariyan S, Narayan D, Dutton-Regester K, Capatana A, Holman EC, Bosenberg M, Sznol M, Kluger HM, Brash DE, Stern DF, Materin MA, Lo RS, Mane S, Ma S, Kidd KK, Hayward NK, Lifton RP, Schlessinger J, Boggon TJ, Halaban R (2012) Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 44:1006–1014. doi:10.1038/ng.2359
5. Van Raamsdonk CD, Griewank KG, Crosby MB, Garrido MC, Vemula S, Wiesner T, Obenauf AC, Wackernagel W, Green G, Bouvier N, Sozen MM, Baimukanova G, Roy R, Heguy A, Dolgalev I, Khanin R, Busam K, Speicher MR, O’Brien J, Bastian BC (2010) Mutations in GNA11 in uveal melanoma. New Engl J Med 363:2191–2199. doi:10.1056/NEJMoa1000584
6. Harbour JW, Onken MD, Roberson ED, Duan S, Cao L, Worley LA, Council ML, Matatall KA, Helms C, Bowcock AM (2010) Frequent mutation of BAP1 in metastasizing uveal melanomas. Science 330:1410–1413. doi:10.1126/science.1194472
7. Harbour JW, Roberson ED, Anbunathan H, Onken MD, Worley LA, Bowcock AM (2013) Recurrent mutations at codon 625 of the splicing factor SF3B1 in uveal melanoma. Nat Genet. doi:10.1038/ng.2523
8. Martin M, Masshofer L, Temming P, Rahmann S, Metz C, Bornfeld N, van de Nes J, Klein-Hitpass L, Hinnebusch AG, Horsthemke B, Lohmann DR, Zeschnigk M (2013) Exome sequencing identifies recurrent somatic mutations in EIF1AX and SF3B1 in uveal melanoma with disomy 3. Nat Genet 45:933–936. doi:10.1038/ng.2674
9. Küsters-Vandevelde HV, Klaasen A, Küsters B, Groenen PJ, van Engen-van Grunsven IA, van Dijk MR, Reifenberger G, Wesseling P, Blokx WA (2010) Activating mutations of the GNAQ gene: a frequent event in primary melanocytic neoplasms of the central nervous system. Acta Neuropathol 119:317–323. doi:10.1007/s00401-009-0611-3
10. Murali R, Wiesner T, Rosenblum MK, Bastian BC (2012) GNAQ and GNA11 mutations in melanocytomas of the central nervous system. Acta Neuropathol 123:457–459. doi:10.1007/s00401-012-0948-x
11. Gessi M, van de Nes J, Griewank K, Barresi V, Buckland ME, Kirfel J, Caltabiano R, Hammes J, Lauriola L, Pietsch T, Waha A (2014) Absence of TERT promoter mutations in primary melanocytic tumors of the central nervous system. Neuropathol Appl Neurobiol. doi:10.1111/nan.12138
12. Horn S, Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, Kadel S, Moll I, Nagore E, Hemminki K, Schadendorf D, Kumar R (2013) TERT promoter mutations in familial and sporadic melanoma. Science 339:959–961. doi:10.1126/science.1230062
13. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA (2013) Highly recurrent TERT promoter mutations in human melanoma. Science 339:957–959. doi:10.1126/science.1229259
14. Griewank KG, Murali R, Schilling B, Scholz S, Sucker A, Song M, Susskind D, Grabellus F, Zimmer L, Hillen U, Steuhl KP, Schadendorf D, Westekemper H, Zeschnigk M (2013) TERT promoter mutations in ocular melanoma distinguish between conjunctival and uveal tumours. Br J Cancer 109:497–501. doi:10.1038/bjc.2013.312
15. Gessi M, Hammes J, Lauriola L, Dorner E, Kirfel J, Kristiansen G, Muehlen A, Denkhaus D, Waha A, Pietsch T (2013) GNA11 and N-RAS mutations: alternatives for MAPK pathway activating GNAQ mutations in primary melanocytic tumours of the central nervous system. Neuropathol Appl Neurobiol 39:417–425. doi:10.1111/j.1365-2990.2012.01288.x
16. Küsters-Vandevelde HV, Küsters B, van Engen-van Grunsven AC, Groenen PJ, Wesseling P, Blokx WA (2015) Primary melanocytic tumors of the central nervous system: a review with focus on molecular aspects. Brain Pathol 25:209–226. doi:10.1111/bpa.12241
17. Küsters-Vandevelde HV, van Engen-van Grunsven IA, Coupland SE, Lake SL, Rijntjes J, Pfundt R, Küsters B, Wesseling P, Blokx WA, Groenen PJ (2014) Mutations in G protein encoding genes and chromosomal alterations in primary leptomeningeal melanocytic neoplasms. POR, Pathology oncology research. doi:10.1007/s12253-014-9841-3
18. Thomas S, Putter C, Weber S, Bornfeld N, Lohmann DR, Zeschnigk M (2012) Prognostic significance of chromosome 3 alterations determined by microsatellite analysis in uveal melanoma: a long-term follow-up study. Br J Cancer 106:1171–1176. doi:10.1038/bjc.2012.54
19. Ehlers JP, Worley L, Onken MD, Harbour JW (2008) Integrative genomic analysis of aneuploidy in uveal melanoma. Clin Cancer Res Off J Am Assoc Cancer Res 14:115–122. doi:10.1158/1078-0432.CCR-07-1825
20. Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, Kutzner H, Cho KH, Aiba S, Brocker EB, LeBoit PE, Pinkel D, Bastian BC (2005) Distinct sets of genetic alterations in melanoma. New Engl J Med 353:2135–2147. doi:10.1056/NEJMoa050092
21. Griewank K, Westekemper H, Murali R, Mach M, Schilling B, Wiesner T, Schimming T, Livingstone E, Sucker A, Grabellus F, Metz C, Susskind D, Hillen U, Speicher MR, Woodman SE, Steuhl KP, Schadendorf D (2013) Conjunctival melanomas harbor BRAF and NRAS mutations and copy number changes similar to cutaneous and mucosal melanomas. Clin Cancer Res Off J Am Assoc Cancer Res. doi:10.1158/1078-0432.CCR-13-0163
22. Koelsche C, Hovestadt V, Jones DT, Capper D, Sturm D, Sahm F, Schrimpf D, Adeberg S, Bohmer K, Hagenlocher C, Mechtersheimer G, Kohlhof P, Muhleisen H, Beschorner R, Hartmann C, Braczynski AK, Mittelbronn M, Buslei R, Becker A, Grote A, Urbach H, Staszewski O, Prinz M, Hewer E, Pfister SM, von Deimling A, Reuss DE (2015) Melanotic tumors of the nervous system are characterized by distinct mutational, chromosomal and epigenomic profiles. Brain Pathol 25:202–208. doi:10.1111/bpa.12228
23. Brat DJ, Giannini C, Scheithauer BW, Burger PC (1999) Primary melanocytic neoplasms of the central nervous systems. Am J Surg Pathol 23:745–754
24. Murali R, Chandramohan R, Moller I, Scholz SL, Berger M, Huberman K, Viale A, Pirun M, Socci ND, Bouvier N, Bauer S, Artl M, Schilling B, Schimming T, Sucker A, Schwindenhammer B, Grabellus F, Speicher MR, Schaller J, Hillen U, Schadendorf D, Mentzel T, Cheng DT, Wiesner T, Griewank KG (2015) Targeted massively parallel sequencing of angiosarcomas reveals frequent activation of the mitogen activated protein kinase pathway. Oncotarget 6:36041–36052
25. Wiesner T, Obenauf AC, Murali R, Fried I, Griewank KG, Ulz P, Windpassinger C, Wackernagel W, Loy S, Wolf I, Viale A, Lash AE, Pirun M, Socci ND, Rutten A, Palmedo G, Abramson D, Offit K, Ott A, Becker JC, Cerroni L, Kutzner H, Bastian BC, Speicher MR (2011) Germline mutations in BAP1 predispose to melanocytic tumors. Nat Genet 43:1018–1021. doi:10.1038/ng.910
26. Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, Vivanco I, Lee JC, Huang JH, Alexander S, Du J, Kau T, Thomas RK, Shah K, Soto H, Perner S, Prensner J, Debiasi RM, Demichelis F, Hatton C, Rubin MA, Garraway LA, Nelson SF, Liau L, Mischel PS, Cloughesy TF, Meyerson M, Golub TA, Lander ES, Mellinghoff IK, Sellers WR (2007) Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci USA 104:20007–20012. doi:10.1073/pnas.0710052104
27. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, Reich M, Winckler W, Lawrence MS, Weir BA, Tanaka KE, Chiang DY, Bass AJ, Loo A, Hoffman C, Prensner J, Liefeld T, Gao Q, Yecies D, Signoretti S, Maher E, Kaye FJ, Sasaki H, Tepper JE, Fletcher JA, Tabernero J, Baselga J, Tsao MS, Demichelis F, Rubin MA, Janne PA, Daly MJ, Nucera C, Levine RL, Ebert BL, Gabriel S, Rustgi AK, Antonescu CR, Ladanyi M, Letai A, Garraway LA, Loda M, Beer DG, True LD, Okamoto A, Pomeroy SL, Singer S, Golub TR, Lander ES, Getz G, Sellers WR, Meyerson M (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463:899–905. doi:10.1038/nature08822
28. Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R, Getz G (2011) GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol 12:R41. doi:10.1186/gb-2011-12-4-r41
29. Curtin JA, Busam K, Pinkel D, Bastian BC (2006) Somatic activation of KIT in distinct subtypes of melanoma. Journal of clinical oncology. Off J Am Soc Clin Oncol 24:4340–4346. doi:10.1200/JCO.2006.06.2984
30. Daniels AB, Lee JE, MacConaill LE, Palescandolo E, Van Hummelen P, Adams SM, DeAngelis MM, Hahn WC, Gragoudas ES, Harbour JW, Garraway LA, Kim IK (2012) High throughput mass spectrometry-based mutation profiling of primary uveal melanoma. Invest Ophthalmol Vis Sci 53:6991–6996. doi:10.1167/iovs.12-10427
31. Griewank KG, van de Nes J, Schilling B, Moll I, Sucker A, Kakavand H, LE Haydu, Asher M, Zimmer L, Hillen U, Thompson JF, Scolyer RA, Schadendorf D, Murali R (2014) Genetic and clinico-pathologic analysis of metastatic uveal melanoma. Modern pathology. Off J United States Can Acad Pathol 27:175–183. doi:10.1038/modpathol.2013.138
32. Prescher G, Bornfeld N, Hirche H, Horsthemke B, Jöckel KH, Becher R (1996) Prognostic implications of monosomy 3 in uveal melanoma. Lancet 347:1222–1225