Molecular characterization of melanoma cases in Denmark suspected of genetic predisposition

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Wadt, Karin A W ^a   Aoude, Lauren G ^b   Krogh, Lotte ^c   Sunde, Lone ^d   Bojesen, Anders ^e   Grønskov, Karen ^a,f   Wartacz, Nine ^a   Ek, Jakob ^a   Tolstrup Andersen, Morten ^a   Klarskov Andersen, Mette ^a   Borg, Åke ^g   Heegaard, Steffen ^f   Kiilgaard, Jens F ^f   Hansen, Thomas V O ^h   Klein, Kerenaftali ^b   Jönsson, Göran ^g   Drzewiecki, Krzysztof T ^h   Dunø, Morten ^a   Hayward, Nicholas K ^b   Gerdes, Anne M ^a  

^a University Hospital of Copenhagen ^*  (Denmark)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d AARHUS UNIVERSITY HOSPITAL   (Denmark)

^e LILLEBAELT HOSPITAL   (Denmark)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g LUND UNIVERSITY   (Sweden)

^h International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MELANOCORTIN 1 RECEPTOR; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; BAP1 PROTEIN, HUMAN; CDK4 PROTEIN, HUMAN; MITF PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN THIOLESTERASE;

ADULT; ARTICLE; BRCA1 ASSOCIATED PROTEIN GENE; CDKN2A GENE; CONTROLLED STUDY; CUTANEOUS MELANOMA; CYCLIN DEPENDENT KINASE 4 GENE; DENMARK; FAMILY HISTORY; GENE; GENETIC ANALYSIS; GENETIC PREDISPOSITION; GERMLINE MUTATION; HIGH RISK PATIENT; HUMAN; MAJOR CLINICAL STUDY; MELANOCORTIN RECEPTOR 1 GENE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR GENE; MUTATIONAL ANALYSIS; NEXT GENERATION SEQUENCING; PENETRANCE; UVEA MELANOMA; GENETIC SCREENING; GENETICS; MELANOMA; SKIN NEOPLASMS; STANDARDS; TUMOR GENE;

CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DENMARK; GENES, NEOPLASM; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; GERM-LINE MUTATION; HUMANS; MELANOMA; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; RECEPTOR, MELANOCORTIN, TYPE 1; SKIN NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE;

EID: 84925612085     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122662     Document Type: Article

References (67)

1. Danish Cancerregistry. Available: http://www.ssi.dk/Sundhedsdataogit/Registre/Cancerregisteret.aspx. Accessed 15 October 2014.
2. Shekar SN, Duffy DL, Youl P, Baxter AJ, Kvaskoff M, Whiteman DC, et al. A population-based study of Australian twins with melanoma suggests a strong genetic contribution to liability. J Invest Dermatol. 2009; 129: 2211-9. doi: 10.1038/jid.2009.48 PMID: 19357710
3. Fallah M, Pukkala E, Sundquist K, Tretli S, Olsen JH, Tryggvadottir L, et al. Familial melanoma by histology and age: joint data from five Nordic countries. Eur J Cancer. 2014; 50: 1176-83. doi: 10.1016/j.ejca.2013.12.023 PMID: 24461199
4. Gandini S, Sera F, Cattaruzza MS, Pasquini P, Abeni D, Boyle P, et al. Meta-analysis of risk factors for cutaneous melanoma: I. Common and atypical naevi. Eur J Cancer. 2005; 41: 28-44. PMID: 15617989
5. Gandini S, Sera F, Cattaruzza MS, Pasquini P, Picconi O, Boyle P, et al. Meta-analysis of risk factors for cutaneous melanoma: II. Sun exposure. Eur J Cancer. 2005; 41: 45-60. PMID: 15617990
6. Gandini S, Sera F, Cattaruzza MS, Pasquini P, Zanetti R, Masini C, et al. Meta-analysis of risk factors for cutaneous melanoma: III. Family history, actinic damage and phenotypic factors. Eur J Cancer. 2005; 41: 2040-59. PMID: 16125929
7. Lazovich D, Vogel RI, Berwick M, Weinstock MA, Anderson KE, Warshaw EM. Indoor tanning and risk of melanoma: a case-control study in a highly exposed population. Cancer Epidemiol Biomarkers Prev. 2010; 19: 1557-68. doi: 10.1158/1055-9965.EPI-09-1249 PMID: 20507845
8. Colantonio S, Bracken MB, Beecker J. The association of indoor tanning and melanoma in adults: systematic review and meta-analysis. J Am Acad Dermatol. 2014; 70: 847-57. doi: 10.1016/j.jaad.2013.11.050 PMID: 24629998
9. Goldstein AM, Chan M, Harland M, Hayward NK, Demenais F, Bishop DT, et al. Features associated with germline CDKN2A mutations: a GenoMEL study of melanoma-prone families from three continents. J Med Genet. 2007; 44: 99-106. PMID: 16905682
10. De Snoo FA, Hayward NK. Cutaneous melanoma susceptibility and progression genes. Cancer Lett. 2005; 230: 153-86. PMID: 16297704
11. Zuo L, Weger J, Yang Q, Goldstein AM, Tucker MA, Walker GJ, et al. Germline mutations in the p16INK4a binding domain of CDK4 in familial melanoma. Nat Genet. 1996; 12: 97-9. PMID: 8528263
12. Wiesner T, Obenauf AC, Murali R, Fried I, Griewank KG, Ulz P, et al. Germline mutations in BAP1 predispose to melanocytic tumors. Nat Genet. 2011; 43: 1018-21. doi: 10.1038/ng.910 PMID: 21874003
13. Robles-Espinoza CD, Harland M, Ramsay AJ, Aoude LG, Quesada V, Ding Z, et al. POT1 loss-of-function variants predispose to familial melanoma. Nat Genet. 2014; 46: 478-81. doi: 10.1038/ng.2947 PMID: 24686849
14. Aoude L, Pritchard A, Robles-Espinoza C, Wadt KAW, Harland M, Choi J, et al. Nonsense mutations in the shelterin complex genes ACD and TERF2IP in familial melanoma. J Natl Cancer Inst. 2014; 107.
15. Horn S, Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, et al. TERT Promoter Mutations in Familial and Sporadic Melanoma. Science (80-). 2013; 339: 959-61. doi: 10.1126/science.1230062 PMID: 23348503
16. Shi J, Yang XR, Ballew B, Rotunno M, Calista D, Fargnoli MC, et al. Rare missense variants in POT1 predispose to familial cutaneous malignant melanoma. Nat Genet. 2014; 46: 482-6. doi: 10.1038/ng.2941 PMID: 24686846
17. Puntervoll HE, Yang XR, Vetti HH, Bachmann IM, Avril MF, Benfodda M, et al. Melanoma prone families with CDK4 germline mutation: phenotypic profile and associations with MC1R variants. J Med Genet. 2013; 50: 264-70. doi: 10.1136/jmedgenet-2012-101455 PMID: 23384855
18. Ghiorzo P, Fornarini G, Sciallero S, Battistuzzi L, Belli F, Bernard L, et al. CDKN2A is the main susceptibility gene in Italian pancreatic cancer families. J Med Genet. 2012; 49: 164-70. doi: 10.1136/ jmedgenet-2011-100281 PMID: 22368299
19. Goldstein AM. Familial melanoma, pancreatic cancer and germline CDKN2A mutations. Hum Mutat. 2004; 23: 630. PMID: 15146472
20. Raimondi S, Sera F, Gandini S, Iodice S, Caini S, Maisonneuve P, et al. MC1R variants, melanoma and red hair color phenotype: a meta-analysis. Int J Cancer. 2008; 122: 2753-60. doi: 10.1002/ijc.23396 PMID: 18366057
21. Burchill SA, Ito S, Thody AJ. Effects of melanocyte-stimulating hormone on tyrosinase expression and melanin synthesis in hair follicular melanocytes of the mouse. J Endocrinol. 1993; 137: 189-95. PMID: 8326247
22. Sturm RA, Duffy DL, Box NF, Newton RA, Shepherd AG, Chen W, et al. Genetic association and cellular function of MC1R variant alleles in human pigmentation. Ann N Y Acad Sci. 2003; 994: 348-58. PMID: 12851335
23. García-Borrón JC, Abdel-Malek Z, Jiménez-Cervantes C. MC1R, the cAMP pathway, and the response to solar UV: extending the horizon beyond pigmentation. Pigment Cell Melanoma Res. 2014; 27: 699-720. doi: 10.1111/pcmr.12257 PMID: 24807163
24. Panzella L, Leone L, Greco G, Vitiello G, D'Errico G, Napolitano A, et al. Red human hair pheomelanin is a potent pro-oxidant mediating UV-independent contributory mechanisms of melanomagenesis. Pigment Cell Melanoma Res. 2014; 27: 244-52. doi: 10.1111/pcmr.12199 PMID: 24387634
25. Yokoyama S, Woods SL, Boyle GM, Aoude LG, MacGregor S, Zismann V, et al. A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature. 2011; 480: 99-103. doi: 10.1038/nature10630 PMID: 22080950
26. Bertolotto C, Lesueur F, Giuliano S, Strub T, de Lichy M, Bille K, et al. A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma. Nature; 2011; 480: 94-8. doi: 10.1038/nature10539 PMID: 22012259
27. Gudbjartsson DF, Sulem P, Stacey SN, Goldstein AM, Rafnar T, Sigurgeirsson B, et al. ASIP and TYR pigmentation variants associate with cutaneous melanoma and basal cell carcinoma. Nat Genet. 2008; 40: 886-91. doi: 10.1038/ng.161 PMID: 18488027
28. Gerstenblith MR, Shi J, Landi MT. Genome-wide association studies of pigmentation and skin cancer: a review and meta-analysis. Pigment Cell Melanoma Res. 2010; 23: 587-606. doi: 10.1111/j.1755-148X.2010.00730.x PMID: 20546537
29. Barrett JH, Iles MM, Harland M, Taylor JC, Aitken JF, Andresen PA, et al. Genome-wide association study identifies three new melanoma susceptibility loci. Nat Genet. 2011; 43: 1108-13. doi: 10.1038/ ng.959 PMID: 21983787
30. Yonekawa Y, Kim IK. Epidemiology and management of uveal melanoma. Hematol Oncol Clin North Am. 2012; 26: 1169-84. doi: 10.1016/j.hoc.2012.08.004 PMID: 23116575
31. Virgili G, Gatta G, Ciccolallo L, Capocaccia R, Biggeri A, Crocetti E, et al. Incidence of uveal melanoma in Europe. Ophthalmology. 2007; 114: 2309-15. PMID: 17498805
32. Weis E, Shah CP, Lajous M, Shields JA, Shields CL. The association between host susceptibility factors and uveal melanoma: a meta-analysis. Arch Ophthalmol. American Medical Association; 2006; 124: 54-60. PMID: 16401785
33. Wadt KAW, Aoude LG, Johansson P, Solinas A, Pritchard A, Crainic O, et al. A recurrent germline BAP1 mutation and extension of the BAP1 tumor predisposition spectrum to include basal cell carcinoma. Clin Genet. 2014; (Epub ahead of print) Available: http://www.ncbi.nlm.nih.gov/pubmed/25225168
34. Ribeiro C, Campelos S, Moura CS, Machado JC, Justino A, Parente B. Well-differentiated papillary mesothelioma: Clustering in a Portuguese family with a germline BAP1 mutation. Ann Oncol. 2013; 24: 2147-50. doi: 10.1093/annonc/mdt135 PMID: 23585512
35. Carbone M, Yang H, Pass HI, Krausz T, Testa JR, Gaudino G. BAP1 and cancer. Nat Rev Cancer. 2013; 13: 153-9. PMID: 23550303
36. Kannengiesser C, Avril M-F, Spatz A, Laud K, Lenoir GM, Bressac-de-Paillerets B. CDKN2A as a uveal and cutaneous melanoma susceptibility gene. Genes Chromosomes Cancer. 2003; 38: 265-8. PMID: 14506702
37. Abdel-Rahman MH, Pilarski R, Massengill JB, Christopher BN, Noss R, Davidorf FH. Melanoma candidate genes CDKN2A/p16/INK4A, p14ARF, and CDK4 sequencing in patients with uveal melanoma with relative high-risk for hereditary cancer predisposition. Melanoma Res. 2011; 21: 175-9. doi: 10.1097/CMR.0b013e328343eca2 PMID: 21412176
38. Easton DF, Steele L, Fields P, Ormiston W, Averill D, Daly PA, et al. Cancer risks in two large breast cancer families linked to BRCA2 on chromosome 13q12-13. Am J Hum Genet. 1997; 61: 120-8. PMID: 9245992
39. Sinilnikova OM, Egan KM, Quinn JL, Boutrand L, Lenoir GM, Stoppa-Lyonnet D, et al. Germline brca2 sequence variants in patients with ocular melanoma. Int J Cancer. 1999; 82: 325-8. PMID: 10399947
40. Lukowsky A, Schäfer-Hesterberg G, Sterry W, Voit C. Germline CDKN2A/p16 mutations are rare in multiple primary and familial malignant melanoma in German patients. J Dermatol Sci. 2008; 49: 163-5. PMID: 17890059
41. Veinalde R, Ozola A, Azarjana K, Molven A, Akslen LA, Doniòa S, et al. Analysis of Latvian familial melanoma patients shows novel variants in the noncoding regions of CDKN2A and that the CDK4 mutation R24H is a founder mutation. Melanoma Res. 2013; 23: 221-6. doi: 10.1097/CMR.0b013e3283608695 PMID: 23546221
42. Vossen RHAM, Aten E, Roos A, den Dunnen JT. High-resolution melting analysis (HRMA): more than just sequence variant screening. Hum Mutat. 2009; 30: 860-6. doi: 10.1002/humu.21019 PMID: 19418555
43. Christensen C, Bartkova J, Mistrík M, Hall A, Lange MK, Ralfkiær U, et al. A short acidic motif in ARF guards against mitochondrial dysfunction and melanoma susceptibility. Nat Commun. 2014; 5: 5348. doi: 10.1038/ncomms6348 PMID: 25370744
44. Harland M, Taylor CF, Chambers PA, Kukalizch K, Randerson-Moor JA, Gruis NA, et al. A mutation hotspot at the p14ARF splice site. Oncogene. 2005; 24: 4604-8. PMID: 15856016
45. Djursby M, Wadt K, Lorentzen H, Borg A, Gerdes A-M, Krogh L. [CDKN2A-mutation in a family with hereditary malignant melanoma.]. Ugeskr Laeger. 2014; 176.
46. Hodis E, Watson IR, Kryukov G V, Arold ST, Imielinski M, Theurillat J-P, et al. A landscape of driver mutations in melanoma. Cell. 2012; 150: 251-63. doi: 10.1016/j.cell.2012.06.024 PMID: 22817889
47. Scaini MC, Minervini G, Elefanti L, Ghiorzo P, Pastorino L, Tognazzo S, et al. CDKN2A Unclassified Variants in Familial Malignant Melanoma: Combining Functional and Computational Approaches for Their Assessment. Hum Mutat. 2014
48. Lohmueller KE, Sparsø T, Li Q, Andersson E, Korneliussen T, Albrechtsen A, et al. Whole-exome sequencing of 2,000 Danish individuals and the role of rare coding variants in type 2 diabetes. Am J Hum Genet. 2013; 93: 1072-86. doi: 10.1016/j.ajhg.2013.11.005 PMID: 24290377
49. Helgadottir H, Höiom V, Jönsson G, Tuominen R, Ingvar C, Borg A, et al. High risk of tobacco-related cancers in CDKN2A mutation-positive melanoma families. J Med Genet. 2014; 51: 545-52. doi: 10.1136/jmedgenet-2014-102320 PMID: 24935963
50. Aitken J, Welch J, Duffy D, Milligan A, Green A, Martin N, et al. CDKN2A variants in a population-based sample of Queensland families with melanoma. J Natl Cancer Inst. 1999; 91: 446-52. PMID: 10070944
51. Bishop DT, Demenais F, Goldstein AM, Bergman W, Bishop JN, Bressac-de Paillerets B, et al. Geographical variation in the penetrance of CDKN2A mutations for melanoma. J Natl Cancer Inst. 2002; 94: 894-903. PMID: 12072543
52. Aoude LG, Wadt K, Bojesen A, Crüger D, Borg A, Trent JM, et al. A BAP1 mutation in a Danish family predisposes to uveal melanoma and other cancers. PLoS One. 2013; 8: e72144. doi: 10.1371/journal. pone.0072144 PMID: 23977234
53. Wadt K, Choi J, Chung JY, Kiilgaard J, Heegaard S, Drzewiecki KT, et al. A cryptic BAP1 splice mutation in a family with uveal and cutaneous melanoma, and paraganglioma. Pigment Cell Melanoma Res. 2012; 25: 815-8. doi: 10.1111/pcmr.12006 PMID: 22889334
54. Begg CB, Orlow I, Hummer AJ, Armstrong BK, Kricker A, Marrett LD, et al. Lifetime risk of melanoma in CDKN2A mutation carriers in a population-based sample. J Natl Cancer Inst. 2005; 97: 1507-15. PMID: 16234564
55. Box NF, Duffy DL, Chen W, Stark M, Martin NG, Sturm RA, et al. MC1R genotype modifies risk of melanoma in families segregating CDKN2A mutations. Am J Hum Genet. 2001; 69: 765-73. PMID: 11500805
56. Harinck F, Kluijt I, van der Stoep N, Oldenburg RA, Wagner A, Aalfs CM, et al. Indication for CDKN2Amutation analysis in familial pancreatic cancer families without melanomas. J Med Genet. 2012; 49: 362-5. doi: 10.1136/jmedgenet-2011-100563 PMID: 22636603
57. McWilliams RR, Wieben ED, Rabe KG, Pedersen KS, Wu Y, Sicotte H, et al. Prevalence of CDKN2A mutations in pancreatic cancer patients: implications for genetic counseling. Eur J Hum Genet. 2011; 19: 472-8. doi: 10.1038/ejhg.2010.198 PMID: 21150883
58. Slater EP, Langer P, Fendrich V, Habbe N, Chaloupka B, Matthäi E, et al. Prevalence of BRCA2 and CDKN2a mutations in German familial pancreatic cancer families. Fam Cancer. 2010; 9: 335-43. doi: 10.1007/s10689-010-9329-6 PMID: 20195775
59. Njauw CNJ, Kim I, Piris A, Gabree M, Taylor M, Lane AM, et al. Germline BAP1 inactivation is preferentially associated with metastatic ocular melanoma and cutaneous-ocular melanoma families. PLoS One. 2012; 7: e35295. doi: 10.1371/journal.pone.0035295 PMID: 22545102
60. Williams PF, Olsen CM, Hayward NK, Whiteman DC. Melanocortin 1 receptor and risk of cutaneous melanoma: a meta-analysis and estimates of population burden. Int J Cancer. 2011; 129: 1730-40. doi: 10.1002/ijc.25804 PMID: 21128237
61. Hu H-H, Benfodda M, Dumaz N, Gazal S, Descamps V, Bourillon A, et al. A large french case-control study emphasizes the role of rare Mc1R variants in melanoma risk. Biomed Res Int. 2014; 925716.
62. Ghiorzo P, Pastorino L, Queirolo P, Bruno W, Tibiletti MG, Nasti S, et al. Prevalence of the E318K MITF germline mutation in Italian melanoma patients: associations with histological subtypes and family cancer history. Pigment Cell Melanoma Res. 2013; 26: 259-62. doi: 10.1111/pcmr.12047 PMID: 23167872
63. Gromowski T, Masojć B, Scott RJ, Cybulski C, Górski B, Kluźniak W, et al. Prevalence of the E318K and V320I MITF germline mutations in Polish cancer patients and multiorgan cancer risk-a populationbased study. Cancer Genet. 2014; 207: 128-32. doi: 10.1016/j.cancergen.2014.03.003 PMID: 24767713
64. Fargnoli MC, Gandini S, Peris K, Maisonneuve P, Raimondi S. MC1R variants increase melanoma risk in families with CDKN2A mutations: a meta-analysis. Eur J Cancer. 2010; 46: 1413-20. doi: 10.1016/j.ejca.2010.01.027 PMID: 20189796
65. Ghiorzo P, Bonelli L, Pastorino L, Bruno W, Barile M, Andreotti V, et al. MC1R variation and melanoma risk in relation to host/clinical and environmental factors in CDKN2A positive and negative melanoma patients. Exp Dermatol. 2012; 21: 718-20. doi: 10.1111/j.1600-0625.2012.01549.x PMID: 22804906
66. Popova T, Hebert L, Jacquemin V, Gad S, Caux-Moncoutier V, Dubois-D'Enghien C, et al. Germline BAP1 mutations predispose to renal cell carcinomas. Am J Hum Genet. 2013; 92: 974-80. doi: 10.1016/j.ajhg.2013.04.012 PMID: 23684012
67. Aitken JF, Youl P, Green A, MacLennan R, Martin NG. Accuracy of case-reported family history of melanoma in Queensland, Australia. Melanoma Res. 1996; 6: 313-7. PMID: 8873051