Re-evaluation of epidermodysplasia verruciformis: Reconciling more than 90 years of debate

Journal of the American Academy of Dermatology

Volumn 76, Issue 6, 2017, Pages 1161-1175

  Przybyszewska, Joanna ^a   Zlotogorski, Abraham ^b   Ramot, Yuval ^b  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

epidermodysplasia verruciformis; EVER1; EVER2; general verrucosis; genetics; genodermatoses; human papillomavirus; immunodeficiency; SCID; squamous cell carcinoma

Indexed keywords

B LYMPHOCYTE; BETAPAPILLOMAVIRUS; BONE MARROW CELL; CELLULAR IMMUNITY; DENDRITIC CELL; DISEASE PREDISPOSITION; ENDOTHELIUM CELL; EPIDERMODYSPLASIA VERRUCIFORMIS; GENE MUTATION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNOCOMPROMISED PATIENT; KERATINOCYTE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; VIRUS REPLICATION; WART VIRUS; GENETICS; IMMUNOLOGY; MUTATION; PAPILLOMAVIRUS INFECTION; VIROLOGY;

EPIDERMODYSPLASIA VERRUCIFORMIS; HUMANS; MUTATION; PAPILLOMAVIRUS INFECTIONS;

EID: 85011968298     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2016.12.035     Document Type: Review

References (98)

1. Orth, G., Genetics and susceptibility to human papillomaviruses: epidermodysplasia verruciformis, a disease model. Bull Acad Natl Med 194 (2010), 923–940.
2. Gaud, G., Guillemot, D., Jacob, Y., Favre, M., Vuillier, F., EVER2 protein binds TRADD to promote TNF-alpha-induced apoptosis. Cell Death Dis, 4, 2013, e499.
3. Majewski, S., Jablonska, S., Why epidermodysplasia verruciformis - a rare genetic disease - has raised such great interest. Int J Dermatol 43 (2004), 309–311.
4. Lane, J.E., Bowman, P.H., Cohen, D.J., Epidermodysplasia verruciformis. South Med J 96 (2003), 613–615.
5. Gewirtzman, A., Bartlett, B., Tyring, S., Epidermodysplasia verruciformis and human papilloma virus. Curr Opin Infect Dis 21 (2008), 141–146.
6. Burger, B., Itin, P.H., Epidermodysplasia verruciformis. Curr Probl Dermatol 45 (2014), 123–131.
7. Cubie, H.A., Diseases associated with human papillomavirus infection. Virology 445 (2013), 21–34.
8. Cardoso, J.C., Calonje, E., Cutaneous manifestations of human papillomaviruses: a review. Acta Dermatovenerol Alp Pannonica Adriat 20 (2011), 145–154.
9. Pfister, H., Biology of epidermodysplasia verruciformis-associated HPV. [in German] Hautarzt 62 (2011), 17–21.
10. Patel, T., Morrison, L.K., Rady, P., Tyring, S., Epidermodysplasia verruciformis and susceptibility to HPV. Dis Markers 29 (2010), 199–206.
11. Mertz, K.D., Schmid, M., Burger, B., et al. Detection of Merkel cell polyomavirus in epidermodysplasia-verruciformis-associated skin neoplasms. Dermatology 222:1 (2011), 87–92.
12. Kwon, E.K., Halvorson, C.R., Rady, P., et al. Merkel cell polyomavirus detection in a patient with familial epidermodysplasia verruciformis. Pediatr Dermatol 30:4 (2013), 505–507.
13. Arnold, A.W., Hofbauer, G.F., Human papillomavirus and squamous cell cancer of the skin–epidermodysplasia verruciformis-associated human papillomavirus revisited. Curr Probl Dermatol 43 (2012), 49–56.
14. Kalińska-Bienias, A., Kowalewski, C., Majewski, S., The EVER genes – the genetic etiology of carcinogenesis in epidermodysplasia verruciformis and a possible role in non-epidermodysplasia verruciformis patients. Postepy Dermatol Alergol 33:2 (2016), 75–80.
15. Fox, S.H., Elston, D.M., Epidermodysplasia verruciformis and the risk for malignancy. Cutis 98:4 (2016), E10–E12.
16. Gubinelli, E., Posteraro, P., Cocuroccia, B., Girolomoni, G., Epidermodysplasia verruciformis with multiple mucosal carcinomas treated with pegylated interferon alfa and acitretin. J Dermatolog Treat 14:3 (2003), 184–188.
17. Partridge, M.E., Pariser, R.J., Ocular and cutaneous squamous cell carcinoma in an African American man with epidermodysplasia verruciformis resulting in blindness and death. J Am Acad Dermatol 49:5 Suppl (2003), S262–S264.
18. Lutzner, M.A., Blanchet-Bardon, C., Orth, G., Clinical observations, virologic studies, and treatment trials in patients with epidermodysplasia verruciformis, a disease induced by specific human papillomaviruses. J Invest Dermatol 83:1 Suppl (1984), 18s–25s.
19. Nindl, I., Gottschling, M., Stockfleth, E., Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23:4 (2007), 247–259.
20. Termorshuizen, F., Feltkamp, M.C., Struijk, L., de Gruijl, F.R., Bavinck, J.N., van Loveren, H., Sunlight exposure and (sero)prevalence of epidermodysplasia verruciformis-associated human papillomavirus. J Invest Dermatol 122:6 (2004), 1456–1462.
21. Al Rubaie, S., Breuer, J., Inshasi, J., Al Saady, S., Fathi, I., Epidermodysplasia verruciformis with neurological manifestations. Int J Dermatol 37:10 (1998), 766–771.
22. Tanigaki, T., Endo, H., A case of epidermodysplasia verruciformis (Lewandowsky-Lutz, 1922) with skin cancer: histopathology of malignant cutaneous changes. Dermatologica 169:2 (1984), 97–101.
23. Adachi, A., Kiyono, T., Hayashi, Y., Ohashi, M., Ishibashi, M., Detection of human papillomavirus (HPV) type 47 DNA in malignant lesions from epidermodysplasia verruciformis by protocols for precise typing of related HPV DNAs. J Clin Microbiol 34:2 (1996), 369–375.
24. Yutsudo, M., Shimakage, T., Hakura, A., Human papillomavirus type 17 DNA in skin carcinoma tissue of a patient with epidermodysplasia verruciformis. Virology 144:1 (1985), 295–298.
25. Sa, N.B., Guerini, M.B., Barbato, M.T., Di Giunta, G., Nunes, D.H., Epidermodysplasia verruciformis: clinical presentation with varied forms of lesions. An Bras Dermatol 86:4 Suppl 1 (2011), S57–S60.
26. Gul, U., Kilic, A., Gonul, M., Cakmak, S.K., Bayis, S.S., Clinical aspects of epidermodysplasia verruciformis and review of the literature. Int J Dermatol 46:10 (2007), 1069–1072.
27. Jacyk, W.K., Dreyer, L., de Villiers, E.M., Seborrheic keratoses of black patients with epidermodysplasia verruciformis contain human papillomavirus DNA. Am J Dermatopathol 15:1 (1993), 1–6.
28. Kanda, R., Tanigaki, T., Kitano, Y., Yoshikawa, K., Yutsudo, M., Hakura, A., Types of human papillomavirus isolated from Japanese patients with epidermodysplasia verruciformis. Br J Dermatol 121:4 (1989), 463–469.
29. Jacyk, W.K., De Villiers, E.M., Epidermodysplasia verruciformis in Africans. Int J Dermatol 32:11 (1993), 806–810.
30. Lewandowsky, F., Lutz, W., Ein Fall einer bisher nicht beschriebenen Hauterkrankung. [in German] Arch Dermatol Syph 141 (1922), 193–203.
31. Orth, G., Host defenses against human papillomaviruses: lessons from epidermodysplasia verruciformis. Curr Top Microbiol Immunol 321 (2008), 59–83.
32. Lazarczyk, M., Pons, C., Mendoza, J.A., Cassonnet, P., Jacob, Y., Favre, M., Regulation of cellular zinc balance as a potential mechanism of EVER-mediated protection against pathogenesis by cutaneous oncogenic human papillomaviruses. J Exp Med 205:1 (2008), 35–42.
33. Zuo, Y.G., Ma, D., Zhang, Y., Qiao, J., Wang, B., Identification of a novel mutation and a genetic polymorphism of EVER1 gene in two families with epidermodysplasia verruciformis. J Dermatol Sci 44:3 (2006), 153–159.
34. Pereira de Oliveira, W.R., Carrasco, S., Neto, C.F., Rady, P., Tyring, S.K., Nonspecific cell-mediated immunity in patients with epidermodysplasia verruciformis. J Dermatol 30:3 (2003), 203–209.
35. Ramoz, N., Rueda, L.A., Bouadjar, B., Montoya, L.S., Orth, G., Favre, M., Mutations in two adjacent novel genes are associated with epidermodysplasia verruciformis. Nat Genet 32:4 (2002), 579–581.
36. Kurima, K., Peters, L.M., Yang, Y., et al. Dominant and recessive deafness caused by mutations of a novel gene, TMC1, required for cochlear hair-cell function. Nat Genet 30:3 (2002), 277–284.
37. Vreugde, S., Erven, A., Kros, C.J., et al. Beethoven, a mouse model for dominant, progressive hearing loss DFNA36. Nat Genet 30:3 (2002), 257–258.
38. Crequer, A., Picard, C., Pedergnana, V., et al. EVER2 deficiency is associated with mild T-cell abnormalities. J Clin Immunol 33:1 (2013), 14–21.
39. Majewski, S., Hunzelmann, N., Nischt, R., et al. TGF beta-1 and TNF alpha expression in the epidermis of patients with epidermodysplasia verruciformis. J Invest Dermatol 97:5 (1991), 862–867.
40. Orth, G., Genetics of epidermodysplasia verruciformis: insights into host defense against papillomaviruses. Semin Immunol 18:6 (2006), 362–374.
41. McDermott, D.F., Gammon, B., Snijders, P.J., et al. Autosomal dominant epidermodysplasia verruciformis lacking a known EVER1 or EVER2 mutation. Pediatr Dermatol 26:3 (2009), 306–310.
42. Androphy, E.J., Dvoretzky, I., Lowy, D.R., X-linked inheritance of epidermodysplasia verruciformis. Genetic and virologic studies of a kindred. Arch Dermatol 121:7 (1985), 864–868.
43. Crequer, A., Troeger, A., Patin, E., et al. Human RHOH deficiency causes T cell defects and susceptibility to EV-HPV infections. J Clin Invest 122:9 (2012), 3239–3247.
44. Crequer, A., Picard, C., Patin, E., et al. Inherited MST1 deficiency underlies susceptibility to EV-HPV infections. PLoS One, 7(8), 2012, e44010.
45. Stray-Pedersen, A., Jouanguy, E., Crequer, A., et al. Compound heterozygous CORO1A mutations in siblings with a mucocutaneous-immunodeficiency syndrome of epidermodysplasia verruciformis-HPV, molluscum contagiosum and granulomatous tuberculoid leprosy. J Clin Immunol 34:7 (2014), 871–890.
46. Horev, L., Unger, S., Molho-Pessach, V., et al. Generalized verrucosis and HPV-3 susceptibility associated with CD4 T-cell lymphopenia caused by inherited human interleukin-7 deficiency. J Am Acad Dermatol 72:6 (2015), 1082–1084.
47. Fueller, F., Kubatzky, K.F., The small GTPase RhoH is an atypical regulator of haematopoietic cells. Cell Commun Signal, 6, 2008, 6.
48. Tybulewicz, V.L., Henderson, R.B., Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 9:9 (2009), 630–644.
49. Kinashi, T., Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 5:7 (2005), 546–559.
50. Roadcap, D.W., Clemen, C.S., Bear, J.E., The role of mammalian coronins in development and disease. Subcell Biochem 48 (2008), 124–135.
51. Gao, J., Zhao, L., Wan, Y.Y., Zhu, B., Mechanism of Action of IL-7 and Its Potential Applications and Limitations in Cancer Immunotherapy. Int J Mol Sci 16:5 (2015), 10267–10280.
52. Jiang, Q., Li, W.Q., Aiello, F.B., et al. Cell biology of IL-7, a key lymphotrophin. Cytokine Growth Factor Rev 16:4-5 (2005), 513–533.
53. Ramoz, N., Rueda, L.A., Bouadjar, B., Favre, M., Orth, G., A susceptibility locus for epidermodysplasia verruciformis, an abnormal predisposition to infection with the oncogenic human papillomavirus type 5, maps to chromosome 17qter in a region containing a psoriasis locus. J Invest Dermatol 112:3 (1999), 259–263.
54. Avruch, J., Zhou, D., Fitamant, J., Bardeesy, N., Mst1/2 signalling to Yap: gatekeeper for liver size and tumour development. Br J Cancer 104:1 (2011), 24–32.
55. Schlegelmilch, K., Mohseni, M., Kirak, O., et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144:5 (2011), 782–795.
56. Tan, M.J., White, E.A., Sowa, M.E., Harper, J.W., Aster, J.C., Howley, P.M., Cutaneous beta-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling. Proc Natl Acad Sci U S A 109:23 (2012), E1473–E1480.
57. Rogers, H.D., Macgregor, J.L., Nord, K.M., et al. Acquired epidermodysplasia verruciformis. J Am Acad Dermatol 60:2 (2009), 315–320.
58. Broekaert, S.M., Ehrchen, J., Buttner, R., Pfister, H.J., Metze, D., Acquired epidermodysplasia verruciformis in an HIV-infected patient. J Dtsch Dermatol Ges 12:4 (2014), 353–355.
59. Lowe, S.M., Katsidzira, L., Meys, R., et al. Acquired epidermodysplasia verruciformis due to multiple and unusual HPV infection among vertically-infected, HIV-positive adolescents in Zimbabwe. Clin Infect Dis 54:10 (2012), e119–e123.
60. Ashida, A., Shimizu, A., Okuyama, R., Acquired epidermodysplasia verruciformis associated with human papillomavirus type 47 in a HIV-infected patient. J Dermatol 43:6 (2016), 717–718.
61. Kawai, K., Egawa, N., Kiyono, T., Kanekura, T., Epidermodysplasia-verruciformis-like eruption associated with gamma-papillomavirus infection in a patient with adult T-cell leukemia. Dermatology 219:3 (2009), 274–278.
62. Jacyk, W.K., Lechner, W., Epidermodysplasia verruciformis in lepromatous leprosy. Report of 2 cases. Dermatologica 168:4 (1984), 202–205.
63. O'Blenes, C., Pasternak, S., Issekutz, A., Gillis, J., Chowdhury, D., Finlayson, L., Epidermodysplasia verruciformis in lipoid proteinosis: case report and discussion of pathophysiology. Pediatr Dermatol 32:1 (2015), 118–121.
64. Cougoul, P., Tournier, E., Delavigne, K., Rauzy, O.B., Ysebaert, L., Sibaud, V., Acquired epidermodysplasia verruciformis, a new opportunistic infection related to bendamustine. Ann Hematol 94:6 (2015), 1071–1073.
65. Fernandez, K.H., Rady, P., Tyring, S., Stone, M.S., Acquired epidermodysplasia verruciformis in a child with atopic dermatitis. Pediatr Dermatol 31:3 (2014), 400–402.
66. Kunishige, J.H., Hymes, S.R., Madkan, V., et al. Epidermodysplasia verruciformis in the setting of graft-versus-host disease. J Am Acad Dermatol 57:5 Suppl (2007), S78–S80.
67. Holmes, C., Chong, A.H., Tabrizi, S.N., Downes, N., Nindl, I., Epidermodysplasia verruciformis-like syndrome in association with systemic lupus erythematosus. Australas J Dermatol 50:1 (2009), 44–47.
68. Koranda, F.C., Dehmel, E.M., Kahn, G., Penn, I., Cutaneous complications in immunosuppressed renal homograft recipients. JAMA 229:4 (1974), 419–424.
69. Lutzner, M.A., Orth, G., Dutronquay, V., Ducasse, M.F., Kreis, H., Crosnier, J., Detection of human papillomavirus type 5 DNA in skin cancers of an immunosuppressed renal allograft recipient. Lancet 2:8347 (1983), 422–424.
70. Lutzner, M., Croissant, O., Ducasse, M.-F., Kreis, H., Crosnier, J., Orth, G., A Potentially Oncogenic Human Papillomavirus (HPV-5) Found in Two Renal Allograft Recipients. J Investig Dermatol 75:4 (1980), 353–356.
71. Slawsky, L.D., Gilson, R.T., Hockley, A.J., Libow, L.F., Epidermodysplasia verruciformis associated with severe immunodeficiency, lymphoma, and disseminated molluscum contagiosum. J Am Acad Dermatol 27:3 (1992), 448–450.
72. Oliveira, W.R., Ferreira, G.N., Rady, P.L., Festa, C., Tyring, S.K., Epidermodysplasia verruciformis associated with myelodysplastic syndrome: an intriguing association. J Cutan Med Surg 13:6 (2009), 317–320.
73. Hohenstein, E., Rady, P.L., Hergersberg, M., et al. Epidermodysplasia verruciformis in a HIV-positive patient homozygous for the c917A–>T polymorphism in the TMC8/EVER2 gene. Dermatology 218:2 (2009), 114–118.
74. Cowan, K.R., Gonzalez Santiago, T.M., Tollefson, M.M., Acquired epidermodysplasia verruciformis in a child with the human immunodeficiency virus. Pediatr Dermatol 30:6 (2013), e252–e254.
75. Jacobelli, S., Laude, H., Carlotti, A., et al. Epidermodysplasia verruciformis in human immunodeficiency virus-infected patients: a marker of human papillomavirus-related disorders not affected by antiretroviral therapy. Arch Dermatol 147:5 (2011), 590–596.
76. Lutzner, M.A., Epidermodysplasia verruciformis. An autosomal recessive disease characterized by viral warts and skin cancer. A model for viral oncogenesis. Bull Cancer 65:2 (1978), 169–182.
77. Carre, D., Dompmartin, A., Verdon, R., et al. Epidermodysplasia verruciformis in a patient with HIV infection: no response to highly active antiretroviral therapy. Int J Dermatol 42:4 (2003), 296–300.
78. Barzegar, C., Paul, C., Saiag, P., et al. Epidermodysplasia verruciformis-like eruption complicating human immunodeficiency virus infection. Br J Dermatol 139:1 (1998), 122–127.
79. Berger, T.G., Sawchuk, W.S., Leonardi, C., Langenberg, A., Tappero, J., Leboit, P.E., Epidermodysplasia verruciformis-associated papillomavirus infection complicating human immunodeficiency virus disease. Br J Dermatol 124:1 (1991), 79–83.
80. Moore, R.L., de Schaetzen, V., Joseph, M., et al. Acquired epidermodysplasia verruciformis syndrome in HIV-infected pediatric patients: prospective treatment trial with topical glycolic acid and human papillomavirus genotype characterization. Arch Dermatol 148:1 (2012), 128–130.
81. Sri, J.C., Dubina, M.I., Kao, G.F., Rady, P.L., Tyring, S.K., Gaspari, A.A., Generalized verrucosis: a review of the associated diseases, evaluation, and treatments. J Am Acad Dermatol 66:2 (2012), 292–311.
82. Morrison, C., Eliezri, Y., Magro, C., Nuovo, G.J., The histologic spectrum of epidermodysplasia verruciformis in transplant and AIDS patients. J Cutan Pathol 29:8 (2002), 480–489.
83. Ansarin, H., Tajziehchi, L., Shaianfar, N., A case of epidermodysplasia verruciformis with squamous cell carcinomas on non-sun-exposed areas of skin. Arch Iran Med 10:2 (2007), 261–263.
84. Anadolu, R., Oskay, T., Erdem, C., Boyvat, A., Terzi, E., Gurgey, E., Treatment of epidermodysplasia verruciformis with a combination of acitretin and interferon alfa-2a. J Am Acad Dermatol 45:2 (2001), 296–299.
85. Lee, K.C., Risser, J., Bercovitch, L., What is the evidence for effective treatments of acquired epidermodysplasia verruciformis in HIV-infected patients?. Arch Dermatol 146:8 (2010), 903–905.
86. Mendes, A.D., Bittencourt Mde, J., Moure, E.R., D'Macedo, C.M., Yamaki, I.N., Araujo, D.M., Acquired epidermodysplasia verruciformis in a renal transplant recipient–case report. An Bras Dermatol 89:1 (2014), 144–146.
87. Halvorson, C.R., McClain, S., Rady, P., Tyring, S., Gaspari, A.A., Merkel cell carcinoma presenting in a young patient as a forme fruste of variant epidermodysplasia verruciformis. J Am Acad Dermatol 65:3 (2011), 667–669.
88. Zampetti, A., Giurdanella, F., Manco, S., et al. Acquired epidermodysplasia verruciformis: a comprehensive review and a proposal for treatment. Dermatol Surg 39:7 (2013), 974–980.
89. Haas, N., Fuchs, P.G., Hermes, B., Henz, B.M., Remission of epidermodysplasia verruciformis-like skin eruption after highly active antiretroviral therapy in a human immunodeficiency virus-positive patient. Br J Dermatol 145:4 (2001), 669–670.
90. Gorlin, R.J., Gelb, B., Diaz, G.A., Lofsness, K.G., Pittelkow, M.R., Fenyk, J.R. Jr., WHIM syndrome, an autosomal dominant disorder: clinical, hematological, and molecular studies. Am J Med Genet 91:5 (2000), 368–376.
91. Kawai, T., Malech, H.L., WHIM syndrome: congenital immune deficiency disease. Curr Opin Hematol 16:1 (2009), 20–26.
92. Kreuter, A., Hochdorfer, B., Brockmeyer, N.H., Altmeyer, P., Pfister, H., Wieland, U., A human papillomavirus-associated disease with disseminated warts, depressed cell-mediated immunity, primary lymphedema, and anogenital dysplasia: WILD syndrome. Arch Dermatol 144:3 (2008), 366–372.
93. Rezaei, N., Hedayat, M., Aghamohammadi, A., Nichols, K.E., Primary immunodeficiency diseases associated with increased susceptibility to viral infections and malignancies. J Allergy Clin Immunol 127:6 (2011), 1329–1341.e2 quiz 42-43.
94. Fischer, A., Severe combined immunodeficiencies (SCID). Clin Exp Immunol 122:2 (2000), 143–149.
95. Trauner, M.A., Ruben, B.S., Hatcher, S.L., Lawry, M.A., Groin eruption in an HIV-positive man: epidermodysplasia verruciformis (EDV). Arch Dermatol 138:4 (2002), 527–532.
96. Yanagi, T., Shibaki, A., Tsuji-Abe, Y., Yokota, K., Shimizu, H., Epidermodysplasia verruciformis and generalized verrucosis: the same disease?. Clin Exp Dermatol 31:3 (2006), 390–393.
97. Li, S.L., Duo, L.N., Wang, H.J., et al. Identification of LCK mutation in a family with atypical epidermodysplasia verruciformis with T-cell defects and virus-induced squamous cell carcinoma. Br J Dermatol 175 (2016), 1204–1209.
98. Tahiat, A., Badran, Y.R., Chou, J., et al. Epidermodysplasia verruciformis as a manifestation of ARTEMIS deficiency in a young adult. J Allergy Clin Immunol 139 (2017), 372–375.e4.