Risk of squamous cell skin cancer after organ transplant associated with antibodies to cutaneous papillomaviruses, polyomaviruses, and TMC6/8 (EVER1/2) variants

Cancer Medicine

Volumn 3, Issue 5, 2014, Pages 1440-1447

  Madeleine, Margaret M ^a,b   Carter, Joseph J ^a   Johnson, Lisa G ^a   Wipf, Gregory C ^a   Davis, Connie ^c   Berg, Daniel ^b   Nelson, Karen ^d   Daling, Janet R ^a,b   Schwartz, Stephen M ^a,b   Galloway, Denise A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d PUGET SOUND BLOOD CENTER   (United States)

Author keywords

Cutaneous human papillomavirus; Epidemiology; Organ transplant; Polyomavirus; Squamous cell skin cancer

Indexed keywords

ALLELE; ANTIBODY DETECTION; ARTICLE; BETAPAPILLOMAVIRUS; BLOOD SAMPLING; CANCER RISK; CASE CONTROL STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GRAFT RECIPIENT; HISTOPATHOLOGY; HUMAN; IMMUNOASSAY; MAJOR CLINICAL STUDY; ORGAN TRANSPLANTATION; PAPILLOMA VIRUS; POLYOMA VIRUS; PRIORITY JOURNAL; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SQUAMOUS CELL CARCINOMA; TMC6 GENE; TMC8 GENE; VIRUS LIKE AGENT; ADVERSE EFFECTS; CARCINOMA, SQUAMOUS CELL; CLASSIFICATION; COMPLICATION; GENETIC VARIATION; GENETICS; GENOTYPE; ODDS RATIO; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTION; RISK; SKIN NEOPLASMS;

CARCINOMA, SQUAMOUS CELL; CASE-CONTROL STUDIES; GENETIC VARIATION; GENOTYPE; HUMANS; ODDS RATIO; ORGAN TRANSPLANTATION; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; RISK; SKIN NEOPLASMS;

EID: 84991491909     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.280     Document Type: Article

References (56)

1. Engels, E. A., R. M. Pfeiffer, J. F. Jr Fraumeni, B. L. Kasiske, A. K. Israni, J. J. Snyder, et al. 2011. Spectrum of cancer risk among US solid organ transplant recipients. JAMA 306:1891-1901.
2. Euvrard, S., J. Kanitakis, and A. Claudy. 2003. Skin cancers after organ transplantation. N. Engl. J. Med. 348:1681-1691.
3. Bouwes Bavinck, J. N., B. A. De, B. J. Vermeer, M. M. Hartevelt, F. J. van der Woude, F. H. Claas, et al. 1993. Sunlight, keratotic skin lesions and skin cancer in renal transplant recipients. Br. J. Dermatol. 129:242-249.
4. Jensen, P., S. Hansen, B. Moller, T. Leivestad, P. Pfeffer, O. Geiran, et al. 1999. Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimens. J. Am. Acad. Dermatol. 40:177-186.
5. Lindelof, B., B. Sigurgeirsson, H. Gabel, and R. S. Stern. 2000. Incidence of skin cancer in 5356 patients following organ transplantation. Br. J. Dermatol. 143:513-519.
6. Arron, S. T., J. G. Ruby, E. Dybbro, D. Ganem, and J. L. Derisi. 2011. Transcriptome sequencing demonstrates that human papillomavirus is not active in cutaneous squamous cell carcinoma. J. Invest. Dermatol. 131:1745-1753.
7. Berg, D., and C. C. Otley. 2002. Skin cancer in organ transplant recipients: epidemiology, pathogenesis, and management. J. Am. Acad. Dermatol. 47:1-17.
8. Euvrard, S., J. Kanitakis, E. Decullier, A. C. Butnaru, N. Lefrancois, P. Boissonnat, et al. 2006. Subsequent skin cancers in kidney and heart transplant recipients after the first squamous cell carcinoma. Transplantation 81:1093-1100.
9. Orth, G. 2005. Human papillomaviruses associated with epidermodysplasia verruciformis in non-melanoma skin cancers: guilty or innocent? J. Invest. Dermatol. 125:xii-xiii.
10. Pfister, H. 2003. Chapter 8: human papillomavirus and skin cancer. J. Natl. Cancer Inst. Monogr. 2003:52-56.
11. Ramoz, N., A. Taieb, L. A. Rueda, L. S. Montoya, B. Bouadjar, M. Favre, et al. 2000. Evidence for a nonallelic heterogeneity of epidermodysplasia verruciformis with two susceptibility loci mapped to chromosome regions 2p21-p24 and 17q25. J. Invest. Dermatol. 114:1148-1153.
12. Lazarczyk, M., P. Cassonnet, C. Pons, Y. Jacob, and M. Favre. 2009. The EVER proteins as a natural barrier against papillomaviruses: a new insight into the pathogenesis of human papillomavirus infections. Microbiol. Mol. Biol. Rev. 73:348-370.
13. Proby, C. M., C. A. Harwood, R. E. Neale, A. C. Green, S. Euvrard, L. Naldi, et al. 2011. A case-control study of betapapillomavirus infection and cutaneous squamous cell carcinoma in organ transplant recipients. Am. J. Transplant. 11:1498-1508.
14. Harwood, C. A., T. Surentheran, J. M. McGregor, P. J. Spink, I. M. Leigh, J. Breuer, et al. 2000. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J. Med. Virol. 61:289-297.
15. Reuschenbach, M., T. Tran, F. Faulstich, W. Hartschuh, S. Vinokurova, M. Kloor, et al. 2011. High-risk human papillomavirus in non-melanoma skin lesions from renal allograft recipients and immunocompetent patients. Br. J. Cancer 104:1334-1341.
16. Feng, H., M. Shuda, Y. Chang, and P. S. Moore. 2008. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319:1096-1100.
17. Sihto, H., H. Kukko, V. Koljonen, R. Sankila, T. Bohling, and H. Joensuu. 2009. Clinical factors associated with Merkel cell polyomavirus infection in Merkel cell carcinoma. J. Natl. Cancer Inst. 101:938-945.
18. Rollison, D. E., A. R. Giuliano, J. L. Messina, N. A. Fenske, B. S. Cherpelis, V. K. Sondak, et al. 2012. Case-control study of Merkel cell polyomavirus infection and cutaneous squamous cell carcinoma. Cancer Epidemiol. Biomarkers Prev. 21:74-81.
19. Ridd, K., S. Yu, and B. C. Bastian. 2009. The presence of polyomavirus in non-melanoma skin cancer in organ transplant recipients is rare. J. Invest. Dermatol. 129:250-252.
20. Moens, U., M. Ludvigsen, and G. M. Van. 2011. Human polyomaviruses in skin diseases. Patholog. Res. Int. 2011:123491.
21. Casabonne, D., A. Lally, L. Mitchell, K. M. Michael, T. Waterboer, M. Pawlita, et al. 2009. A case-control study of cutaneous squamous cell carcinoma among Caucasian organ transplant recipients: the role of antibodies against human papillomavirus and other risk factors. Int. J. Cancer 125:1935-1945.
22. Madeleine, M. M., L. G. Johnson, J. R. Daling, S. M. Schwartz, J. J. Carter, D. Berg, et al. 2013. Cohort profile: the skin cancer after organ transplant study. Int. J. Epidemiol. 42:1669-1677.
23. Sehr, P., M. Muller, R. Hopfl, A. Widschwendter, and M. Pawlita. 2002. HPV antibody detection by ELISA with capsid protein L1 fused to glutathione S-transferase. J. Virol. Methods 106:61-70.
24. Waterboer, T., P. Sehr, K. M. Michael, S. Franceschi, J. D. Nieland, T. O. Joos, et al. 2005. Multiplex human papillomavirus serology based on in situ-purified glutathione s-transferase fusion proteins. Clin. Chem. 51:1845-1853.
25. Orozco, J. J., J. J. Carter, L. A. Koutsky, and D. A. Galloway. 2005. Humoral immune response recognizes a complex set of epitopes on human papillomavirus type 6 L1 capsomers. J. Virol. 79:9503-9514.
26. Carter, J. J., K. G. Paulson, G. C. Wipf, D. Miranda, M. M. Madeleine, L. G. Johnson, et al. 2009. Association of Merkel cell polyomavirus-specific antibodies with Merkel cell carcinoma. J. Natl. Cancer Inst. 101:1510-1522.
27. Edlund, C. K., W. H. Lee, D. Li, D. J. Van Den Berg, and D. V. Conti. 2008. Snagger: a user-friendly program for incorporating additional information for tagSNP selection. BMC Bioinformatics 9:174.
28. Ludbrook, J. 1998. Multiple comparison procedures updated. Clin. Exp. Pharmacol. Physiol. 25:1032-1037.
29. Dworkin, A. M., S. Y. Tseng, D. C. Allain, O. H. Iwenofu, S. B. Peters, and A. E. Toland. 2009. Merkel cell polyomavirus in cutaneous squamous cell carcinoma of immunocompetent individuals. J. Invest. Dermatol. 129:2868-2874.
30. Reisinger, D. M., J. D. Shiffer, A. B. Jr Cognetta, Y. Chang, and P. S. Moore. 2010. Lack of evidence for basal or squamous cell carcinoma infection with Merkel cell polyomavirus in immunocompetent patients with Merkel cell carcinoma. J. Am. Acad. Dermatol. 63:400-403.
31. zur Hausen, H. 2000. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J. Natl. Cancer Inst. 92:690-698.
32. Weissenborn, S. J., I. Nindl, K. Purdie, C. Harwood, C. Proby, J. Breuer, et al. 2005. Human papillomavirus-DNA loads in actinic keratoses exceed those in non-melanoma skin cancers. J. Invest. Dermatol. 125:93-97.
33. Cornet, I., V. Bouvard, M. S. Campo, M. Thomas, L. Banks, L. Gissmann, et al. 2012. Comparative analysis of transforming properties of E6 and E7 from different beta human papillomavirus types. J. Virol. 86:2366-2370.
34. Caldeira, S., I. Zehbe, R. Accardi, I. Malanchi, W. Dong, M. Giarre, et al. 2003. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 77:2195-2206.
35. Accardi, R., W. Dong, A. Smet, R. Cui, A. Hautefeuille, A. S. Gabet, et al. 2006. Skin human papillomavirus type 38 alters p53 functions by accumulation of deltaNp73. EMBO Rep. 7:334-340.
36. Howie, H. L., J. I. Koop, J. Weese, K. Robinson, G. Wipf, L. Kim, et al. 2011. Beta-HPV 5 and 8 E6 promote p300 degradation by blocking AKT/p300 association. PLoS Pathog. 7:e1002211.
37. Giampieri, S., and A. Storey. 2004. Repair of UV-induced thymine dimers is compromised in cells expressing the E6 protein from human papillomaviruses types 5 and 18. Br. J. Cancer 90:2203-2209.
38. Struijk, L., E. van der Meijden, S. Kazem, S. J. Ter, F. R. de Gruijl, R. D. Steenbergen, et al. 2008. Specific betapapillomaviruses associated with squamous cell carcinoma of the skin inhibit UVB-induced apoptosis of primary human keratinocytes. J. Gen. Virol. 89:2303-2314.
39. Underbrink, M. P., H. L. Howie, K. M. Bedard, J. I. Koop, and D. A. Galloway. 2008. E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J. Virol. 82:10408-10417.
40. Muschik, D., I. Braspenning-Wesch, E. Stockfleth, F. Rosl, T. G. Hofmann, and I. Nindl. 2011. Cutaneous HPV23 E6 prevents p53 phosphorylation through interaction with HIPK2. PLoS ONE 6:e27655.
41. Giampieri, S., R. Garcia-Escudero, J. Green, and A. Storey. 2004. Human papillomavirus type 77 E6 protein selectively inhibits p53-dependent transcription of proapoptotic genes following UV-B irradiation. Oncogene 23:5864-5870.
42. Viarisio, D., K. Mueller-Decker, U. Kloz, B. Aengeneyndt, A. Kopp-Schneider, H. J. Grone, et al. 2011. E6 and E7 from beta HPV38 cooperate with ultraviolet light in the development of actinic keratosis-like lesions and squamous cell carcinoma in mice. PLoS Pathog. 7:e1002125.
43. Chow, L. T., S. S. Reilly, T. R. Broker, and L. B. Taichman. 1987. Identification and mapping of human papillomavirus type 1 RNA transcripts recovered from plantar warts and infected epithelial cell cultures. J. Virol. 61:1913-1918.
44. de Koning, M., W. Quint, L. Struijk, B. Kleter, P. Wanningen, L. J. van Doorn, et al. 2006. Evaluation of a novel highly sensitive, broad-spectrum PCR-reverse hybridization assay for detection and identification of beta-papillomavirus DNA. J. Clin. Microbiol. 44:1792-1800.
45. Waterboer, T., D. Abeni, F. Sampogna, A. Rother, C. Masini, P. Sehr, et al. 2008. Serological association of beta and gamma human papillomaviruses with squamous cell carcinoma of the skin. Br. J. Dermatol. 159:457-459.
46. Andersson, K., T. Waterboer, R. Kirnbauer, K. Slupetzky, T. Iftner, E. M. de Villiers, et al. 2008. Seroreactivity to cutaneous human papillomaviruses among patients with nonmelanoma skin cancer or benign skin lesions. Cancer Epidemiol. Biomarkers Prev. 17:189-195.
47. Bouwes Bavinck, J. N., R. E. Neale, D. Abeni, S. Euvrard, A. C. Green, C. A. Harwood, et al. 2010. Multicenter study of the association between betapapillomavirus infection and cutaneous squamous cell carcinoma. Cancer Res. 70:9777-9786.
48. Karagas, M. R., T. Waterboer, Z. Li, H. H. Nelson, K. M. Michael, J. N. Bavinck, et al. 2010. Genus beta human papillomaviruses and incidence of basal cell and squamous cell carcinomas of skin: population based case-control study. BMJ 341:c2986.
49. Plasmeijer, E. I., N. Pandeya, P. O'Rourke, M. Pawlita, T. Waterboer, M. C. Feltkamp, et al. 2011. The Association between cutaneous squamous cell carcinoma and betapapillomavirus seropositivity: a cohort study. Cancer Epidemiol. Biomarkers Prev. 20:1171-1177.
50. Paradisi, A., T. Waterboer, F. Sampogna, S. Tabolli, S. Simoni, M. Pawlita, et al. 2011. Seropositivity for human papillomavirus and incidence of subsequent squamous cell and basal cell carcinomas of the skin in patients with a previous nonmelanoma skin cancer. Br. J. Dermatol. 165:782-791.
51. Andersson, K., K. M. Michael, T. Luostarinen, T. Waterboer, R. Gislefoss, T. Hakulinen, et al. 2012. Prospective study of human papillomavirus seropositivity and risk of nonmelanoma skin cancer. Am. J. Epidemiol. 175:685-695.
52. Patel, A. S., M. R. Karagas, M. Pawlita, T. Waterboer, and H. H. Nelson. 2008. Cutaneous human papillomavirus infection, the EVER2 gene and incidence of squamous cell carcinoma: a case-control study. Int. J. Cancer 122:2377-2379.
53. Sampogna, F., J. N. Bavinck, M. Pawlita, D. Abeni, C. A. Harwood, C. M. Proby, et al. 2012. Factors associated with the seroprevalence of 26 cutaneous and two genital human papillomavirus types in organ transplant patients. J. Gen. Virol. 93:165-174.
54. Weissenborn, S. J., M. N. de Koning, U. Wieland, W. G. Quint, and H. J. Pfister. 2009. Intrafamilial transmission and family-specific spectra of cutaneous betapapillomaviruses. J. Virol. 83:811-816.
55. Scheurlen, W., L. Gissmann, G. Gross, and H. zur Hausen. 1986. Molecular cloning of two new HPV types (HPV 37 and HPV 38) from a keratoacanthoma and a malignant melanoma. Int. J. Cancer 37:505-510.
56. de Villiers, E. M., C. Fauquet, T. R. Broker, H. U. Bernard, and H. H. Zur. 2004. Classification of papillomaviruses. Virology 324:17-27.