Advertisement

Tumor Biology

, Volume 37, Issue 3, pp 3163–3171 | Cite as

XPC (A2920C), XPF (T30028C), TP53 (Arg72Pro), and GSTP1 (Ile105Val) polymorphisms in prognosis of cutaneous melanoma

  • Gabriela Vilas Bôas Gomez
  • Cristiane de Oliveira
  • José Augusto Rinck-Junior
  • Aparecida Machado de Moraes
  • Gustavo Jacob Lourenço
  • Carmen Silvia Passos Lima
Original Article

Abstract

This study aimed to evaluate whether XPC A2920C, XPF T30028C, TP53 Arg72Pro, and GSTP1 Ile105Val polymorphisms alter outcomes of cutaneous melanoma (CM) patients. DNA from 237 CM patients seen at the University of Campinas Teaching Hospital from April 2000 to February 2014 was analyzed by polymerase chain reaction and restriction fragment length polymorphism assays. The prognostic impact of genotypes of polymorphisms on progression-free survival (PFS) and overall survival (OS) of CM patients were examined using the Kaplan-Meier probability estimates and univariate and multivariate Cox regression analyses. At 60 months of follow-up, shorter PFS and OS were seen in patients with XPF CC genotype (48.9 vs. 66.7 %, P = 0.002; 77.9 vs. 83.5 %, P = 0.006, respectively) and XPF CC + TP53 ArgArg (43.6 vs. 65.9 %, P = 0.007; 71.6 vs. 84.8 %, P = 0.006, respectively) compared with those with remaining genotypes (Kaplan-Meier estimates). Patients with XPF CC (hazard ratio (HR) 2.45, P = 0.002; HR 3.77, P = 0.005) and XPF CC + TP53 ArgArg (HR 2.67, P = 0.009; HR 4.04, P = 0.03) genotypes had more chance to present tumor progression in univariate and multivariate analyses, whereas patients with XPF CC (HR 2.78, P = 0.009) and XPF CC + TP53 ArgArg (HR 3.84, P = 0.01) genotypes were under greater risk of progressing to death in univariate analysis, compared with those with the remaining genotypes. The data suggest, for the first time, that inherited abnormalities in DNA repair pathway related to XPF 30028C and TP53 Arg72Pro polymorphisms act as prognostic factors for PFS and OS of CM patients.

Keywords

Cutaneous melanoma DNA repair Survival Genetic polymorphism 

Notes

Compliance with Ethical Standards

Conflicts of interest

None

Research support

São Paulo Research Foundation (FAPESP) (grant no. 2009/12602-0, no. 2010/18904-5, and no. 2014/10042-5) funded this study. The funding source had no involvement in the design of the study, in the collection, analysis, interpretation of the data, and writing of the manuscript.

References

  1. 1.
    Mouret S, Forestier A, Douki T. The specificity of UVA-induced DNA damage in human melanocytes. Photochem Photobiol Sci. 2012;11:155–62. doi: 10.1039/c1pp05185g.CrossRefPubMedGoogle Scholar
  2. 2.
    Instituto Nacional do Câncer (INCA/2014), htp://www.inca.org.br. Accessed 10 January 2015.
  3. 3.
    Buettner PG, Leiter U, Eigentler TK, Garbe C. Development of prognostic factors and survival in cutaneous melanoma over 25 years: an analysis of the Central Malignant Melanoma Registry of the German Dermatological Society. Cancer. 2005;103:616–24. doi: 10.1002/cncr.20816.CrossRefPubMedGoogle Scholar
  4. 4.
    Spatz A, Stock N, Batist G, van Kempen LC. The biology of melanoma prognostic factors. Discov Med. 2010;10:87–93.PubMedGoogle Scholar
  5. 5.
    Woods JE, Soule EH, Creagan ET. Metastasis and death in patients with thin melanomas (less than 0.76 mm). Ann Surg. 1983;198:63–4. doi: 10.1097/00006534-198409000-00072.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Tsao H, Chin L, Garraway LA, Fisher DE. Melanoma: from mutations to medicine. Genes Dev. 2012;26:1131–55. doi: 10.1101/gad.191999.112.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Svobodová AR, Galandáková A, Sianská J, Doležal D, Ulrichová J, Vostálová J. Acute exposure to solar simulated ultraviolet radiation affects oxidative stress-related biomarkers in skin, liver and blood of hairless mice. Biol Pharm Bull. 2011;34:471–9. doi: 10.1248/bpb.34.471.CrossRefPubMedGoogle Scholar
  8. 8.
    Kraemer KH, Lee MM, Andrews AD, Lambert WC. The role of sunlight and DNA repair in melanoma and nonmelanoma skin cancer. The xeroderma pigmentosum paradigm. Arch Dermatol. 1994;130:1018–21. doi: 10.1001/archderm.1994.01690080084012.CrossRefPubMedGoogle Scholar
  9. 9.
    De Boer J, Hoeijmakers JH. Nucleotide excision repair and human syndromes. Carcinogenesis. 2000;21:453–60. doi: 10.1093/carcin/21.3.453.CrossRefPubMedGoogle Scholar
  10. 10.
    Whibley C, Pharoah PDP, Hollstein M. P53 polymorphisms: cancer implications. Nat Rev Cancer. 2009;9:95–107. doi: 10.1038/nrc2584.CrossRefPubMedGoogle Scholar
  11. 11.
    Dusinska M, Staruchova M, Horska A, Smolkova B, Collins A, Bonassi S, et al. Are glutathione S transferases involved in DNA damage signalling? Interactions with DNA damage and repair revealed from molecular epidemiology studies. Mutat Res Mol Mech Mutagen. 2012;736:130–7. doi: 10.1016/j.mrfmmm.2012.03.003.CrossRefGoogle Scholar
  12. 12.
    Laborde E. Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death. Cell Death Differ. 2010;17:1373–80. doi: 10.1038/cdd.2010.80.CrossRefPubMedGoogle Scholar
  13. 13.
    Winsey SL, Haldar NA, Marsh HP, Bunce M, Marshall SE, Harris AL, et al. A variant within the DNA repair gene XRCC3 is associated with the development of melanoma skin cancer. Cancer Res. 2000;60:5612–6.PubMedGoogle Scholar
  14. 14.
    Povey JE, Darakhshan F, Robertson K, Bisset Y, Mekky M, Rees J, et al. DNA repair gene polymorphisms and genetic predisposition to cutaneous melanoma. Carcinogenesis. 2007;28:1087–93. doi: 10.1093/carcin/bgl257.CrossRefPubMedGoogle Scholar
  15. 15.
    Oliveira C, Rinck-Junior JA, Lourenço GJ, Moraes AM, Lima CSP. Assessment of the XPC (A2920C), XPF (T30028C), TP53 (Arg72Pro) and GSTP1 (Ile105Val) polymorphisms in the risk of cutaneous melanoma. J Cancer Res Clin Oncol. 2013;139:1199–206. doi: 10.1007/s00432-013-1430-4.CrossRefPubMedGoogle Scholar
  16. 16.
    Zhu Y, Yang H, Chen Q, Lin J, Grossman HB, Dinney CP, et al. Modulation of DNA damage/DNA repair capacity by XPC polymorphisms. DNA Repair (Amst). 2008;7:141–8. doi: 10.1016/j.dnarep.2007.08.006.CrossRefGoogle Scholar
  17. 17.
    Shi TY, He J, Qiu LX, Zhu ML, Wang MY, Zhou XY, et al. Association between XPF polymorphisms and cancer risk: a meta-analysis. PLoS One 2012;7. doi: 10.1371/journal.pone.0038606.
  18. 18.
    Matlashewski GJ, Tuck S, Pim D, Lamb P, Schneider J, Crawford LV. Primary structure polymorphism at amino acid residue 72 of human p53. Mol Cell Biol. 1987;7:961–3.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Dumont P, Leu JI-J, Della Pietra AC, George DL, Murphy M. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat Genet. 2003;33:357–65. doi: 10.1038/ng1093.CrossRefPubMedGoogle Scholar
  20. 20.
    Zimniak P, Nanduri B, Pikuła S, Bandorowicz-Pikuła J, Singhal SS, Srivastava SK, et al. Naturally occurring human glutathione S-transferase GSTP1-1 isoforms with isoleucine and valine in position 104 differ in enzymic properties. Eur J Biochem. 1994;224:893–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Rigel DS, Friedman RJ, Levenstein MJ, Greenwald DI. Relationship of fluorescent lights to malignant melanoma: another view. J Dermatol Surg Oncol. 1983;9:836–8.CrossRefPubMedGoogle Scholar
  22. 22.
    Fitzpatrick TB. The validity and practicality of sun-reactive skin types I through VI. Arch Dermatol. 1988;124:869–71. doi: 10.1001/archderm.1988.01670060015008.CrossRefPubMedGoogle Scholar
  23. 23.
    Thomas NE, Kricker A, From L, Busam K, Millikan RC, Ritchey ME, et al. Associations of cumulative sun exposure and phenotypic characteristics with histologic solar elastosis. Cancer Epidemiol Biomarkers Prev. 2010;19:2932–41. doi: 10.1158/1055-9965.EPI-10-0686.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Marghoob AA, Koenig K, Bittencourt FV, Kopf AW, Bart RS. Breslow thickness and Clark level in melanoma: support for including level in Pathology Reports and in American Joint Committee on Cancer Staging. Cancer. 2000;88:589–95. doi: 10.1002/(SICI)1097-0142(20000201)88:3<589::AID-CNCR15>3.0.CO;2-I.CrossRefPubMedGoogle Scholar
  25. 25.
    Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol. 2009;27:6199–206. doi: 10.1200/JCO.2009.23.4799.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Haigh PI, DiFronzo LA, McCready DR. Optimal excision margins for primary cutaneous melanoma: a systematic review and meta-analysis. Can J Surg. 2003;46:419–26.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Nieweg OE, Roses DF, et al. Final trial report of sentinel-node biopsy versus nodal observation in melanoma. N Engl J Med. 2014;370:599–609. doi: 10.1056/NEJMoa1310460.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Mocellin S, Pasquali S, Rossi CR, Nitti D. Interferon alpha adjuvant therapy in patients with high-risk melanoma: a systematic review and meta-analysis. J Natl Cancer Inst. 2010;102:493–501. doi: 10.1093/jnci/djq009.CrossRefPubMedGoogle Scholar
  29. 29.
    Burmeister BH, Henderson MA, Ainslie J, Fisher R, Di Iulio J, Smithers BM, et al. Adjuvant radiotherapy versus observation alone for patients at risk of lymph-node field relapse after therapeutic lymphadenectomy for melanoma: a randomised trial. Lancet Oncol. 2012;13:589–97. doi: 10.1016/S1470-2045(12)70138-9.CrossRefPubMedGoogle Scholar
  30. 30.
    Sondak VK, Gibney GT. Surgical management of melanoma. Hematol Oncol Clin North Am 2014. doi: 10.1016/j.hoc.2014.02.009.
  31. 31.
    Sasse AD, Sasse EC, Clark LGO, Ulloa L, Clark OAC. Chemoimmunotherapy versus chemotherapy for metastatic malignant melanoma. Cochrane Database Syst Rev 2007:CD005413. doi: 10.1002/14651858.CD005413.pub2.
  32. 32.
    Rate WR, Solin LJ, Turrisi AT. Palliative radiotherapy for metastatic malignant melanoma: brain metastases, bone metastases, and spinal cord compression. Int J Radiat Oncol Biol Phys. 1988;15:859–64.CrossRefPubMedGoogle Scholar
  33. 33.
    Rastrelli M, Tropea S, Pigozzo J. Melanoma m1: diagnosis and therapy. In Vivo (Brooklyn). 2014;28:273–85.Google Scholar
  34. 34.
    Hu Z, Wang Y, Wang X, Liang G, Miao X, Xu Y, et al. DNA repair gene XPC genotypes/haplotypes and risk of lung cancer in a Chinese population. Int J Cancer. 2005;115:478–83. doi: 10.1002/ijc.20911.CrossRefPubMedGoogle Scholar
  35. 35.
    Honma HN, De Capitani EM, Perroud MW, Barbeiro AS, Toro IFC, Costa DB, et al. Influence of p53 codon 72 exon 4, GSTM1, GSTT1 and GSTP1*B polymorphisms in lung cancer risk in a Brazilian population. Lung Cancer. 2008;61:152–62. doi: 10.1016/j.lungcan.2007.12.014.CrossRefPubMedGoogle Scholar
  36. 36.
    Hohaus S, Di Ruscio A, Di Febo A, Massini G, D’Alo' F, Guidi F, et al. Glutathione S-transferase P1 genotype and prognosis in Hodgkin’s lymphoma. Clin Cancer Res. 2005;11:2175–9. doi: 10.1158/1078-0432.CCR-04-1250.CrossRefPubMedGoogle Scholar
  37. 37.
    Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time 1 quantitative PCR and the 2(−delta delta C(T)) method. Methods. 2001;25:402–8.CrossRefPubMedGoogle Scholar
  38. 38.
    Beiguelman B. Dinâmica dos Genes nas Famílias e Populações. Ribeirão Preto, Sociedade Brasileira de Genética. 1995;2:1–472.Google Scholar
  39. 39.
    Jekel JF, Katz DL and Elmore JG. Epidemiology, biostatistics and preventive medicine, 2nd ed, 2001;175–181.Google Scholar
  40. 40.
    Schrama D, Scherer D, Schneider M, Zapatka M, Bröcker E-B, Schadendorf D, et al. ERCC5 p.Asp1104His and ERCC2 p.Lys751Gln polymorphisms are independent prognostic factors for the clinical course of melanoma. J Invest Dermatol. 2011;131:1280–90. doi: 10.1038/jid.2011.35.CrossRefPubMedGoogle Scholar
  41. 41.
    Li C, Yin M, Wang L-E, Amos CI, Zhu D, Lee JE, et al. Polymorphisms of nucleotide excision repair genes predict melanoma survival. J Invest Dermatol. 2013;133:1813–21. doi: 10.1038/jid.2012.498.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Geer LY, Marchler-Bauer A, Geer RC, et al. The NCBI BioSystems database. Nucleic Acids Res. 2010;38:D492–6.CrossRefPubMedGoogle Scholar
  43. 43.
    Yokoi M, Masutani C, Maekawa T, Sugasawa K, Ohkuma Y, Hanaoka F. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J Biol Chem. 2000;275:9870–5. doi: 10.1074/jbc.275.13.9870.CrossRefPubMedGoogle Scholar
  44. 44.
    Zhu XD, Niedernhofer L, Kuster B, Mann M, Hoeijmakers JHJ, De Lange T. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol Cell. 2003;12:1489–98. doi: 10.1016/S1097-2765(03)00478-7.CrossRefPubMedGoogle Scholar
  45. 45.
    Cui R, Widlund HR, Feige E, Lin JY, Wilensky DL, Igras VE, et al. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell. 2007;128:853–64. doi: 10.1016/j.cell.2006.12.045.CrossRefPubMedGoogle Scholar
  46. 46.
    Cotignola J, Chou JF, Roy P, Mitra N, Busam K, Halpern AC, et al. Investigation of the effect of MDM2 SNP309 and TP53 Arg72Pro polymorphisms on the age of onset of cutaneous melanoma. J Invest Dermatol. 2012;132:1471–8. doi: 10.1038/jid.2012.15.CrossRefPubMedGoogle Scholar
  47. 47.
    Kauffmann A, Rosselli F, Lazar V, Winnepenninckx V, Mansuet-Lupo A, Dessen P, et al. High expression of DNA repair pathways is associated with metastasis in melanoma patients. Oncogene. 2008;27:565–73. doi: 10.1038/sj.onc.1210700.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2015

Authors and Affiliations

  • Gabriela Vilas Bôas Gomez
    • 1
  • Cristiane de Oliveira
    • 1
  • José Augusto Rinck-Junior
    • 1
  • Aparecida Machado de Moraes
    • 1
  • Gustavo Jacob Lourenço
    • 1
  • Carmen Silvia Passos Lima
    • 1
  1. 1.Department of Internal Medicine, Faculty of Medical SciencesUniversity of CampinasCampinasBrazil

Personalised recommendations