Identification of Susceptibility Loci for Cutaneous Squamous Cell Carcinoma

Journal of Investigative Dermatology

Volumn 136, Issue 5, 2016, Pages 930-937

  Asgari, Maryam M ^a,b   Wang, Wei ^c   Ioannidis, Nilah M ^c   Itnyre, Jacqueline ^c   Hoffmann, Thomas ^d   Jorgenson, Eric ^b   Whittemore, Alice S ^c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DIVISION OF RESEARCH   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 2;

ALLELE; ARTICLE; CONTROLLED STUDY; GENE IDENTIFICATION; GENE LOCUS; GENETIC SCREENING; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HISPANIC; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; MAJOR CLINICAL STUDY; PHENOTYPE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN CARCINOMA; SKIN PIGMENTATION; ADULT; CALIFORNIA; CARCINOMA, SQUAMOUS CELL; CASE CONTROL STUDY; CAUCASIAN; COHORT ANALYSIS; FEMALE; GENETIC PREDISPOSITION; GENETICS; MALE; MIDDLE AGED; PATHOLOGY; SKIN NEOPLASMS;

ADULT; CALIFORNIA; CARCINOMA, SQUAMOUS CELL; CASE-CONTROL STUDIES; COHORT STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; SKIN NEOPLASMS;

EID: 84978091657     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2016.01.013     Document Type: Article

References (78)

1. Amos, C.I., Wang, L.E., Lee, J.E., Gershenwald, J.E., Chen, W.V., Fang, S., et al. Genome-wide association study identifies novel loci predisposing to cutaneous melanoma. Hum Mol Genet 20 (2011), 5012–5023.
2. Andresen, P.A., Nymoen, D.A., Kjaerheim, K., Leivestad, T., Helsing, P., Susceptibility to cutaneous squamous cell carcinoma in renal transplant recipients associates with genes regulating melanogenesis independent of their role in pigmentation. Biomark Cancer 5 (2013), 41–47.
3. Banda, Y., Kvale, M.N., Hoffmann, T.J., Hesselson, S.E., Ranatunga, D., Tang, H., et al. Characterizing race/ethnicity and genetic ancestry for 100,000 subjects in the Genetic Epidemiology Research on Adult Health and Aging (GERA) cohort. Genetics 200 (2015), 1285–1295.
4. Barrett, J.H., Iles, M.M., Harland, M., Taylor, J.C., Aitken, J.F., Andresen, P.A., et al. Genome-wide association study identifies three new melanoma susceptibility loci. Nat Genet 43 (2011), 1108–1113.
5. Bastiaens, M.T., ter Huurne, J.A., Kielich, C., Gruis, N.A., Westendorp, R.G., Vermeer, B.J., et al. Melanocortin-1 receptor gene variants determine the risk of nonmelanoma skin cancer independently of fair skin and red hair. Am J Hum Genet 68 (2001), 884–894.
6. Binstock, M., Hafeez, F., Metchnikoff, C., Arron, S.T., Single-nucleotide polymorphisms in pigment genes and nonmelanoma skin cancer predisposition: a systematic review. Br J Dermatol 171 (2014), 713–721.
7. Bishop, D.T., Demenais, F., Iles, M.M., Harland, M., Taylor, J.C., Corda, E., et al. Genome-wide association study identifies three loci associated with melanoma risk. Nat Genet 41 (2009), 920–925.
8. Bouwes Bavinck, J.N., Claas, F.H., The role of HLA molecules in the development of skin cancer. Hum Immunol 41 (1994), 173–179.
9. Bouwes Bavinck, J.N., Vermeer, B.J., van der Woude, F.J., Vandenbroucke, J.P., Schreuder, G.M., Thorogood, J., et al. Relation between skin cancer and HLA antigens in renal-transplant recipients. N Engl J Med 325 (1991), 843–848.
10. Box, N.F., Duffy, D.L., Irving, R.E., Russell, A., Chen, W., Griffyths, L.R., et al. Melanocortin-1 receptor genotype is a risk factor for basal and squamous cell carcinoma. J Invest Dermatol 116 (2001), 224–229.
11. Branicki, W., Brudnik, U., Wojas-Pelc, A., Interactions between HERC2, OCA2 and MC1R may influence human pigmentation phenotype. Ann Hum Genet 73 (2009), 160–170.
12. Brown, K.M., Macgregor, S., Montgomery, G.W., Craig, D.W., Zhao, Z.Z., Iyadurai, K., et al. Common sequence variants on 20q11.22 confer melanoma susceptibility. Nat Genet 40 (2008), 838–840.
13. Cochran, W.G., The combination of estimates from different experiments. Biometrics 10 (1954), 101–129.
14. Crum, C.P., McKeon, F.D., p63 in epithelial survival, germ cell surveillance, and neoplasia. Annu Rev Pathol 5 (2010), 349–371.
15. Dessinioti, C., Tzannis, K., Sypsa, V., Nikolaou, V., Kypreou, K., Antoniou, C., et al. Epidemiologic risk factors of basal cell carcinoma development and age at onset in a Southern European population from Greece. Exp Dermatol 20 (2011), 622–626.
16. Devlin, B., Roeder, K., Genomic control for association studies. Biometrics 55 (1999), 997–1004.
17. Duffy, D.L., Iles, M.M., Glass, D., Zhu, G., Barrett, J.H., Hoiom, V., et al. IRF4 variants have age-specific effects on nevus count and predispose to melanoma. Am J Hum Genet 87 (2010), 6–16.
18. Duffy, D.L., Zhao, Z.Z., Sturm, R.A., Hayward, N.K., Martin, N.G., Montgomery, G.W., Multiple pigmentation gene polymorphisms account for a substantial proportion of risk of cutaneous malignant melanoma. J Invest Dermatol 130 (2010), 520–528.
19. Eiberg, H., Troelsen, J., Nielsen, M., Mikkelsen, A., Mengel-From, J., Kjaer, K.W., et al. Blue eye color in humans may be caused by a perfectly associated founder mutation in a regulatory element located within the HERC2 gene inhibiting OCA2 expression. Hum Genet 123 (2008), 177–187.
20. Eriksson, N., Macpherson, J.M., Tung, J.Y., Hon, L.S., Naughton, B., Saxonov, S., et al. Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet, 6, 2010, e1000993.
21. Feng, J., Zhang, X., Zhu, H., Wang, X., Ni, S., Huang, J., High expression of FoxP1 is associated with improved survival in patients with non-small cell lung cancer. Am J Clin Pathol 138 (2012), 230–235.
22. Fernandez, L.P., Milne, R.L., Pita, G., Aviles, J.A., Lazaro, P., Benitez, J., et al. SLC45A2: a novel malignant melanoma-associated gene. Hum Mutat 29 (2008), 1161–1167.
23. Gerstenblith, M.R., Shi, J., Landi, M.T., Genome-wide association studies of pigmentation and skin cancer: a review and meta-analysis. Pigment Cell Melanoma Res 23 (2010), 587–606.
24. GTEx Consortium. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348 (2015), 648–660.
25. Gudbjartsson, D.F., Sulem, P., Stacey, S.N., Goldstein, A.M., Rafnar, T., Sigurgeirsson, B., et al. ASIP and TYR pigmentation variants associate with cutaneous melanoma and basal cell carcinoma. Nat Genet 40 (2008), 886–891.
26. Guedj, M., Bourillon, A., Combadieres, C., Rodero, M., Dieude, P., Descamps, V., et al. Variants of the MATP/SLC45A2 gene are protective for melanoma in the French population. Hum Mutat 29 (2008), 1154–1160.
27. Han, J., Kraft, P., Nan, H., Guo, Q., Chen, C., Qureshi, A., et al. A genome-wide association study identifies novel alleles associated with hair color and skin pigmentation. PLoS Genet, 4, 2008, e1000074.
28. Han, J., Qureshi, A.A., Nan, H., Zhang, J., Song, Y., Guo, Q., et al. A germline variant in the interferon regulatory factor 4 gene as a novel skin cancer risk locus. Cancer Res 71 (2011), 1533–1539.
29. Hemminki, K., Zhang, H., Czene, K., Familial invasive and in situ squamous cell carcinoma of the skin. Br J Cancer 88 (2003), 1375–1380.
30. Hoffmann, T.J., Kvale, M.N., Hesselson, S.E., Zhan, Y., Aquino, C., Cao, Y., et al. Next generation genome-wide association tool: design and coverage of a high-throughput European-optimized SNP array. Genomics 98 (2011), 79–89.
31. Hoffmann, T.J., Zhan, Y., Kvale, M.N., Hesselson, S.E., Gollub, J., Iribarren, C., et al. Design and coverage of high throughput genotyping arrays optimized for individuals of East Asian, African American, and Latino race/ethnicity using imputation and a novel hybrid SNP selection algorithm. Genomics 98 (2011), 422–430.
32. Housman, T.S., Feldman, S.R., Williford, P.M., Fleischer, A.B. Jr., Goldman, N.D., Acostamadiedo, J.M., et al. Skin cancer is among the most costly of all cancers to treat for the Medicare population. J Am Acad Dermatol 48 (2003), 425–429.
33. Hu, H.H., Guedj, M., Descamps, V., Jouary, T., Bourillon, A., Ezzedine, K., et al. Assessment of tyrosinase variants and skin cancer risk in a large cohort of French subjects. J Dermatol Sci 64 (2011), 127–133.
34. Hussain, S.K., Sundquist, J., Hemminki, K., The effect of having an affected parent or sibling on invasive and in situ skin cancer risk in Sweden. J Invest Dermatol 129 (2009), 2142–2147.
35. Ibarrola-Villava, M., Hu, H.H., Guedj, M., Fernandez, L.P., Descamps, V., Basset-Seguin, N., et al. MC1R, SLC45A2 and TYR genetic variants involved in melanoma susceptibility in southern European populations: results from a meta-analysis. Eur J Cancer 48 (2012), 2183–2191.
36. Jacobs, L.C., Hamer, M.A., Gunn, D.A., Deelen, J., Lall, J.S., van Heemst, D., et al. A genome-wide association study identifies the skin color genes IRF4, MC1R, ASIP, and BNC2 influencing facial pigmented spots. J Invest Dermatol 135 (2015), 1735–1742.
37. Jacobs, L.C., Wollstein, A., Lao, O., Hofman, A., Klaver, C.C., Uitterlinden, A.G., et al. Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Hum Genet 132 (2013), 147–158.
38. Kennedy, C., ter Huurne, J., Berkhout, M., Gruis, N., Bastiaens, M., Bergman, W., et al. Melanocortin 1 receptor (MC1R) gene variants are associated with an increased risk for cutaneous melanoma which is largely independent of skin type and hair color. J Invest Dermatol 117 (2001), 294–300.
39. Kosiniak-Kamysz, A., Marczakiewicz-Lustig, A., Marcinska, M., Skowron, M., Wojas-Pelc, A., Pospiech, E., et al. Increased risk of developing cutaneous malignant melanoma is associated with variation in pigmentation genes and VDR, and may involve epistatic effects. Melanoma Res 24 (2014), 388–396.
40. Kvale, M.N., Hesselson, S., Hoffmann, T.J., Cao, Y., Chan, D., Connell, S., et al. Genotyping informatics and quality control for 100,000 subjects in the Genetic Epidemiology Research on Adult Health and Aging (GERA) cohort. Genetics 200 (2015), 1051–1060.
41. Leonard, M.K., Kommagani, R., Payal, V., Mayo, L.D., Shamma, H.N., Kadakia, M.P., DeltaNp63alpha regulates keratinocyte proliferation by controlling PTEN expression and localization. Cell Death Differ 18 (2011), 1924–1933.
42. Leonardi-Bee, J., Ellison, T., Bath-Hextall, F., Smoking and the risk of nonmelanoma skin cancer: systematic review and meta-analysis. Arch Dermatol 148 (2012), 939–946.
43. Lin, W., Qureshi, A.A., Kraft, P., Nan, H., Guo, Q., Hu, F.B., et al. ASIP genetic variants and the number of non-melanoma skin cancers. Cancer Causes Control 22 (2011), 495–501.
44. Liu, F., Visser, M., Duffy, D.L., Hysi, P.G., Jacobs, L.C., Lao, O., et al. Genetics of skin color variation in Europeans: genome-wide association studies with functional follow-up. Hum Genet 134 (2015), 823–835.
45. Maccioni, L., Rachakonda, P.S., Scherer, D., Bermejo, J.L., Planelles, D., Requena, C., et al. Variants at chromosome 20 (ASIP locus) and melanoma risk. Int J Cancer 132 (2013), 42–54.
46. Marchini, J., Howie, B., Genotype imputation for genome-wide association studies. Nat Rev Genet 11 (2010), 499–511.
47. Nan, H., Kraft, P., Hunter, D.J., Han, J., Genetic variants in pigmentation genes, pigmentary phenotypes, and risk of skin cancer in Caucasians. Int J Cancer 125 (2009), 909–917.
48. Nan, H., Kraft, P., Qureshi, A.A., Guo, Q., Chen, C., Hankinson, S.E., et al. Genome-wide association study of tanning phenotype in a population of European ancestry. J Invest Dermatol 129 (2009), 2250–2257.
49. Nan, H., Qureshi, A.A., Han, J., Melanoma susceptibility variants on chromosome 20q11.22 are associated with pigmentary traits and the risk of nonmelanoma skin cancer. Br J Dermatol 162 (2010), 461–463.
50. Nan, H., Xu, M., Kraft, P., Qureshi, A.A., Chen, C., Guo, Q., et al. Genome-wide association study identifies novel alleles associated with risk of cutaneous basal cell carcinoma and squamous cell carcinoma. Hum Mol Genet 20 (2011), 3718–3724.
51. Newton, R.A., Cook, A.L., Roberts, D.W., Leonard, J.H., Sturm, R.A., Post-transcriptional regulation of melanin biosynthetic enzymes by cAMP and resveratrol in human melanocytes. J Invest Dermatol 127 (2007), 2216–2227.
52. Palmer, J.S., Duffy, D.L., Box, N.F., Aitken, J.F., O'Gorman, L.E., Green, A.C., et al. Melanocortin-1 receptor polymorphisms and risk of melanoma: is the association explained solely by pigmentation phenotype?. Am J Hum Genet 66 (2000), 176–186.
53. Patterson, L.B., Parichy, D.M., Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet, 9, 2013, e1003561.
54. Pe'er, I., Yelensky, R., Altshuler, D., Daly, M.J., Estimation of the multiple testing burden for genomewide association studies of nearly all common variants. Genet Epidemiol 32 (2008), 381–385.
55. Pique-Regi, R., Degner, J.F., Pai, A.A., Gaffner, D.J., Gilad, Y., Pritchard, J.K., Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res 21 (2011), 447–455.
56. Poligone, B., Gilmore, E.S., Alexander, C.V., Oleksyn, D., Gillespie, K., Zhao, J., et al. PKK suppresses tumor growth and is decreased in squamous cell carcinoma of the skin. J Invest Dermatol 135 (2015), 869–876.
57. Praetorius, C., Grill, C., Stacey, S.N., Metcalf, A.M., Gorkin, D.U., Robinson, K.C., et al. A polymorphism in IRF4 affects human pigmentation through a tyrosinase-dependent MITF/TFAP2A pathway. Cell 155 (2013), 1022–1033.
58. Roewert-Huber, J., Lange-Asschenfeldt, B., Stockfleth, E., Kerl, H., Epidemiology and aetiology of basal cell carcinoma. Br J Dermatol 157:Suppl. 2 (2007), 47–51.
59. Romano, R.A., Li, H., Tummala, R., Maul, R., Sinha, S., Identification of basonuclin2, a DNA-binding zinc-finger protein expressed in germ tissues and skin keratinocytes. Genomics 83 (2004), 821–833.
60. Scherer, D., Kumar, R., Genetics of pigmentation in skin cancer—a review. Mutat Res 705 (2010), 141–153.
61. Shiels, M.S., Katki, H.A., Freedman, N.D., Purdue, M.P., Wentzensen, N., Trabert, B., et al. Cigarette smoking and variations in systemic immune and inflammation markers. J Natl Cancer Inst, 2014, 106 dju294.
62. Simeonov, D.R., Wang, X., Wang, C., Sergeev, Y., Dolinska, M., Bower, M., et al. DNA variations in oculocutaneous albinism: an updated mutation list and current outstanding issues in molecular diagnostics. Hum Mutat 34 (2013), 827–835.
63. Smyth, I.M., Wilming, L., Lee, A.W., Taylor, M.S., Gautier, P., Barlow, K., et al. Genomic anatomy of the Tyrp1 (brown) deletion complex. Proc Natl Acad Sci USA 103 (2006), 3704–3709.
64. Soejima, M., Koda, Y., Population differences of two coding SNPs in pigmentation-related genes SLC24A5 and SLC45A2. Int J Legal Med 121 (2007), 36–39.
65. Stacey, S.N., Gudbjartsson, D.F., Sulem, P., Bergthorsson, J.T., Kumar, R., Thorleifsson, G., et al. Common variants on 1p36 and 1q42 are associated with cutaneous basal cell carcinoma but not with melanoma or pigmentation traits. Nat Genet 40 (2008), 1313–1318.
66. Stacey, S.N., Sulem, P., Masson, G., Gudjonsson, S.A., Thorleifsson, G., Jakobsdottir, M., et al. New common variants affecting susceptibility to basal cell carcinoma. Nat Genet 41 (2009), 909–914.
67. Stefanaki, I., Panagiotou, O.A., Kodela, E., Gogas, H., Kypreou, K.P., Chatzinasiou, F., et al. Replication and predictive value of SNPs associated with melanoma and pigmentation traits in a Southern European case-control study. PLoS One, 8, 2013, e55712.
68. Stokowski, R.P., Pant, P.V., Dadd, T., Fereday, A., Hinds, D.A., Jarman, C., et al. A genomewide association study of skin pigmentation in a South Asian population. Am J Hum Genet 81 (2007), 1119–1132.
69. Sturm, R.A., Duffy, D.L., Zhao, Z.Z., Leite, F.P., Stark, M.S., Hayward, N.K., et al. A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue-brown eye color. Am J Hum Genet 82 (2008), 424–431.
70. Sulem, P., Gudbjartsson, D.F., Stacey, S.N., Helgason, A., Rafnar, T., Magnusson, K.P., et al. Genetic determinants of hair, eye and skin pigmentation in Europeans. Nat Genet 39 (2007), 1443–1452.
71. Valverde, P., Healy, E., Jackson, I., Rees, J.L., Thody, A.J., Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nat Genet 11 (1995), 328–330.
72. Vanhoutteghem, A., Djian, P., Basonuclins 1 and 2, whose genes share a common origin, are proteins with widely different properties and functions. Proc Natl Acad Sci USA 103 (2006), 12423–12428.
73. Visser, M., Kayser, M., Palstra, R.J., HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter. Genome Res 22 (2012), 446–455.
74. Visser, M., Palstra, R.J., Kayser, M., Human skin color is influenced by an intergenic DNA polymorphism regulating transcription of the nearby BNC2 pigmentation gene. Hum Mol Genet 23 (2014), 5750–5762.
75. Visser, M., Palstra, R.J., Kayser, M., Allele-specific transcriptional regulation of IRF4 in melanocytes is mediated by chromatin looping of the intronic rs12203592 enhancer to the IRF4 promoter. Hum Mol Genet 24 (2015), 2649–2661.
76. Yang, M.H., Lin, B.R., Chang, C.H., Chen, S.T., Lin, S.K., Kuo, M.Y., et al. Connective tissue growth factor modulates oral squamous cell carcinoma invasion by activating a miR-504/FOXP1 signalling. Oncogene 31 (2012), 2401–2411.
77. Zhang, M., Song, F., Liang, L., Nan, H., Zhang, J., Liu, H., et al. Genome-wide association studies identify several new loci associated with pigmentation traits and skin cancer risk in European Americans. Hum Mol Genet 22 (2013), 2948–2959.
78. Zhou, B., Shi, J., Whittemore, A.S., Optimal methods for meta-analysis of genome-wide association studies. Genet Epidemiol 35 (2011), 581–591.