Tumorigenic activity of merkel cell polyomavirus T antigens expressed in the stratified epithelium of mice

Cancer Research

Volumn 75, Issue 6, 2015, Pages 1068-1079

  Spurgeon, Megan E ^a   Cheng, Jingwei ^b,c   Bronson, Roderick T ^d   Lambert, Paul F ^a   DeCaprio, James A ^b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; CYTOKERATIN 14; TRANSCRIPTION FACTOR E2F; VIRUS T ANTIGEN; CAPSULAR POLYSACCHARIDE K14; E2F1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR E2F1;

ACANTHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DIFFERENTIATION; DNA DAMAGE; HYPERKERATOSIS; HYPERPLASIA; IN VIVO STUDY; MERKEL CELL; MERKEL CELL POLYOMAVIRUS; MERKEL CELL TUMOR; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; SKIN PAPILLOMA; SQUAMOUS EPITHELIUM CELL; TUMOR GROWTH; UNSCHEDULED DNA SYNTHESIS; VIRUS CARCINOGENESIS; ANIMAL; BACTERIAL CAPSULE; C57BL MOUSE; EPITHELIUM; FEMALE; IMMUNOLOGY; MALE; METABOLISM; PAPILLOMA; PHENOTYPE; PHYSIOLOGY; SKIN NEOPLASMS;

ANIMALS; ANTIGENS, VIRAL, TUMOR; BACTERIAL CAPSULES; E2F1 TRANSCRIPTION FACTOR; EPITHELIUM; FEMALE; MALE; MERKEL CELL POLYOMAVIRUS; MICE; MICE, INBRED C57BL; PAPILLOMA; PHENOTYPE; SKIN NEOPLASMS;

EID: 84928976319     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2425     Document Type: Article

References (47)

1. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008;319:1096-100.
2. DeCaprio JA, Garcea RL. A cornucopia of human polyomaviruses. Nat Rev Microbiol 2013;11:264-76.
3. Carter JJ, Daugherty MD, Qi X, Bheda-Malge A, Wipf GC, Robinson K, et al. Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes. Proc Natl Acad Sci U S A 2013;110:12744-9.
4. Shuda M, Feng H, Kwun HJ, Rosen ST, Gjoerup O, Moore PS, et al. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc Natl Acad Sci U S A 2008;105:16272-7.
5. Tolstov YL, Knauer A, Chen JG, Kensler TW, Kingsley LA, Moore PS, et al. Asymptomatic primary Merkel cell polyomavirus infection among adults. Emerg Infect Dis 2011;17:1371-80.
6. Chen T, Hedman L, Mattila PS, Jartti T, Ruuskanen O, Soderlund-Venermo M, et al. Serological evidence of Merkel cell polyomavirus primary infections in childhood. J Clin Virol 2011;50:125-9.
7. Viscidi RP, Rollison DE, Sondak VK, Silver B, Messina JL, Giuliano AR, et al. Age-specific seroprevalence of Merkel cell polyomavirus, BK virus, and JC virus. Clin Vaccine Immunol 2011;18:1737-43.
8. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 2010;7:509-15.
9. Maksimovic S, Nakatani M, Baba Y, Nelson AM, Marshall KL, Wellnitz SA, et al. Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 2014;509:617-21.
10. Woo SH, Stumpfova M, Jensen UB, Lumpkin EA, Owens DM. Identification of epidermal progenitors for the Merkel cell lineage. Development 2010;137:3965-71.
11. Bardot ES, Valdes VJ, Zhang J, Perdigoto CN, Nicolis S, Hearn SA, et al. Polycomb subunits Ezh1 and Ezh2 regulate the Merkel cell differentiation program in skin stem cells. EMBO J 2013;32:1990-2000.
12. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 2001;1:4.
13. Cheng J, Rozenblatt-Rosen O, Paulson KG, Nghiem P, DeCaprio JA. Merkel cell polyomavirus large T antigen has growth-promoting and inhibitory activities. J Virol 2013;87:6118-26.
14. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 2001;29:418-25.
15. Herber R, Liem A, Pitot H, Lambert PF. Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene. J Virol 1996;70:1873-81.
16. Song S, Pitot HC, Lambert PF. The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals. J Virol 1999;73:5887-93.
17. Rodig SJ, Cheng J, Wardzala J, DoRosario A, Scanlon JJ, Laga AC, et al. Improved detection suggests all Merkel cell carcinomas harbor Merkel polyomavirus. J Clin Invest 2012;122:4645-53.
18. Morrison KM, Miesegaes GR, Lumpkin EA, Maricich SM. Mammalian Merkel cells are descended from the epidermal lineage. Dev Biol 2009;336:76-83.
19. Van Keymeulen A, Mascre G, Youseff KK, Harel I, Michaux C, De Geest N, et al. Epidermal progenitors give rise to Merkel cells during embryonic development and adult homeostasis. J Cell Biol 2009;187:91-100.
20. Zambrowicz BP, Imamoto A, Fiering S, Herzenberg LA, Kerr WG, Soriano P. Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc Natl Acad Sci U S A 1997;94:3789-94.
21. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, et al. Restoration of p53 function leads to tumour regression in vivo. Nature 2007;445:661-5.
22. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
23. Vassar R, Rosenberg M, Ross S, Tyner A, Fuchs E. Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice. Proc Natl Acad Sci U S A 1989;86:1563-7.
24. Hiraiwa A, Fujita M, Nagasaka T, Adachi A, Ohashi M, Ishibashi M. Immunolocalization of hCDC47 protein in normal and neoplastic human tissues and its relation to growth. Int J Cancer 1997;74:180-4.
25. Suzuki S, Adachi A, Hiraiwa A, Ohashi M, Ishibashi M, Kiyono T. Cloning and characterization of human MCM7 promoter. Gene 1998;216:85-91.
26. Balsitis S, Dick F, Dyson N, Lambert PF. Critical roles for non-pRb targets of human papillomavirus type 16 E7 in cervical carcinogenesis. Cancer Res 2006;66:9393-400.
27. Brake T, Connor JP, Petereit DG, Lambert PF. Comparative analysis of cervical cancer in women and in a human papillomavirus-transgenic mouse model: identification of minichromosome maintenance protein 7 as an informative biomarker for human cervical cancer. Cancer Res 2003;63:8173-80.
28. Nguyen MM, Potter SJ, Griep AE. Deregulated cell cycle control in lens epithelial cells by expression of inhibitors of tumor suppressor function. Mech Dev 2002;112:101-13.
29. Ingle A, Ghim S, Joh J, Chepkoech I, Bennett Jenson A, Sundberg JP. Novel laboratory mouse papillomavirus (MusPV) infection. Vet Pathol 2011;48:500-5.
30. Arora R, Shuda M, Guastafierro A, Feng H, Toptan T, Tolstov Y, et al. Survivin is a therapeutic target in merkel cell carcinoma. Sci Transl Med 2012;4:133ra56.
31. Griffiths DA, Abdul-Sada H, Knight LM, Jackson BR, Richards K, Prescott EL, et al. Merkel cell polyomavirus small T antigen targets the NEMO adaptor protein to disrupt inflammatory signaling. J Virol 2013;87:13853-67.
32. Kwun HJ, Shuda M, Feng H, Camacho CJ, Moore PS, Chang Y. Merkel cell polyomavirus small T antigen controls viral replication and oncoprotein expression by targeting the cellular ubiquitin ligase SCFFbw7. Cell Host Microbe 2013;14:125-35.
33. Li J, Wang X, Diaz J, Tsang SH, Buck CB, You J. Merkel cell polyomavirus large T antigen disrupts host genomic integrity and inhibits cellular proliferation. J Virol 2013;87:9173-88.
34. Shahzad N, Shuda M, Gheit T, Kwun HJ, Cornet I, Saidj D, et al. The T antigen locus of Merkel cell polyomavirus downregulates human Toll-like receptor 9 expression. J Virol 2013;87:13009-19.
35. Shuda M, Kwun HJ, Feng H, Chang Y, Moore PS. Human Merkel cell polyomavirus small T antigen is an oncoprotein targeting the 4E-BP1 translation regulator. J Clin Invest 2011;121:3623-34.
36. Tsang SH, Wang X, Li J, Buck CB, You J. Host DNA damage response factors localize to merkel cell polyomavirus DNA replication sites to support efficient viral DNA replication. J Virol 2014;88:3285-97.
37. Spurgeon ME, Lambert PF. Merkel cell polyomavirus: a newly discovered human virus with oncogenic potential. Virology 2013;435:118-30.
38. Moll I, Roessler M, Brandner JM, Eispert AC, Houdek P, Moll R. Human Merkel cells-aspects of cell biology, distribution and functions. Eur J Cell Biol 2005;84:259-71.
39. Jankowski M, Kopinski P, Schwartz R, Czajkowski R. Merkel cell carcinoma: Is this a true carcinoma? Exp Dermatol 2014;31:792-4.
40. Maricich SM, Wellnitz SA, Nelson AM, Lesniak DR, Gerling GJ, Lumpkin EA, et al. Merkel cells are essential for light-touch responses. Science 2009;324:1580-2.
41. Woo SH, Ranade S, Weyer AD, Dubin AE, Baba Y, Qiu Z, et al. Piezo2 is required for Merkel-cell mechanotransduction. Nature 2014;509:622-6.
42. Ikeda R, Cha M, Ling J, Jia Z, Coyle D, Gu JG. Merkel cells transduce and encode tactile stimuli to drive Abeta-afferent impulses. Cell 2014;157:664-75.
43. Heath M, Jaimes N, Lemos B, Mostaghimi A, Wang LC, Penas PF, et al. Clinical characteristics of Merkel cell carcinoma at diagnosis in 195 patients: the AEIOU features. J Am Acad Dermatol 2008;58:375-81.
44. Hennings H, Glick AB, Lowry DT, Krsmanovic LS, Sly LM, Yuspa SH. FVB/N mice: an inbred strain sensitive to the chemical induction of squamous cell carcinomas in the skin. Carcinogenesis 1993;14:2353-8.
45. Coussens LM, Hanahan D, Arbeit JM. Genetic predisposition and parameters of malignant progression in K14-HPV16 transgenic mice. Am J Pathol 1996;149:1899-917.
46. Wakabayashi Y, Mao JH, Brown K, Girardi M, Balmain A. Promotion of Hras-induced squamous carcinomas by a polymorphic variant of the Patched gene in FVB mice. Nature 2007;445:761-5.
47. Song S, Liem A, Miller JA, Lambert PF. Human papillomavirus types 16 E6 and E7 contribute differently to carcinogenesis. Virology 2000;267:141-50.