The E2 protein of human papillomavirus type 8 increases the expression of matrix metalloproteinase-9 in human keratinocytes and organotypic skin cultures

Medical Microbiology and Immunology

Volumn 200, Issue 2, 2011, Pages 127-135

  Akgül, Baki ^a   García Escudero, Ramón ^b   Ekechi, Christine ^c   Steger, Gertrud ^a   Navsaria, Harshad ^c   Pfister, Herbert ^a   Storey, Alan ^d  

^a UNIVERSITY OF COLOGNE   (Germany)

^b CIEMAT   (Spain)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

E2 oncoprotein; HPV8; MMP9

Indexed keywords

ARGININE; DNA; GELATINASE B; ISOLEUCINE; LEUCINE; LYSINE; MUTANT PROTEIN; PROTEIN E2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BASEMENT MEMBRANE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVATION; EPIDERMIS CELL; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 8; KERATINOCYTE; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; REPORTER GENE; SKIN CULTURE; TRANSACTIVATION; WART VIRUS;

AMINO ACID SEQUENCE; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; MATRIX METALLOPROTEINASE 9; MOLECULAR SEQUENCE DATA; MUTATION; ONCOGENE PROTEINS, VIRAL; ORGAN CULTURE TECHNIQUES; PROMOTER REGIONS, GENETIC; SKIN; TRANS-ACTIVATORS; UP-REGULATION;

EID: 79955678029     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00430-011-0183-4     Document Type: Article

References (37)

1. DePinho RA (2000) The age of cancer. Nature 408(6809): 248-254
2. Rigel DS (2008) Cutaneous ultraviolet exposure and its relationship to the development of skin cancer. J Am Acad Dermatol 58(5 Suppl 2):S129-132
3. Rodust PM, Stockfleth E, Ulrich C, Leverkus M, Eberle J (2009) UV-induced squamous cell carcinoma - a role for antiapoptotic signalling pathways. Br J Dermatol 161(Suppl 3):107-115
4. Pfister H (2003) Chapter 8: human papillomavirus and skin cancer. J Natl Cancer Inst Monogr (31):52-56
5. Akgül B, Cooke JC, Storey A (2006) HPV-associated skin disease. J Pathol 208(2):165-175 (Pubitemid 43126110)
6. Karagas MR, Nelson HH, Sehr P, Waterboer T, Stukel TA, Andrew A, Green AC, Bavinck JN, Perry A, Spencer S, Rees JR, Mott LA, Pawlita M (2006) Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin. J Natl Cancer Inst 98(6):389-395
7. Schaper ID, Marcuzzi GP, Weissenborn SJ, Kasper HU, Dries V, Smyth N, Fuchs P, Pfister H (2005) Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res 65(4):1394-1400 (Pubitemid 40270167)
8. Akgül B, Pfefferle R, Marcuzzi GP, Zigrino P, Krieg T, Pfister H, Mauch C (2006) Expression of matrix metalloproteinase (MMP)-2, MMP-9, MMP-13, and MT1-MMP in skin tumors of human papillomavirus type 8 transgenic mice. Exp Dermatol 15(1):35-42
9. Smola-Hess S, Pahne J, Mauch C, Zigrino P, Smola H, Pfister HJ (2005) Expression of membrane type 1 matrix metalloproteinase in papillomavirus- positive cells: role of the human papillomavirus (HPV) 16 and HPV8 E7 gene products. J Gen Virol 86(Pt 5):1291-1296 (Pubitemid 40613245)
10. Akgül B, Karle P, Adam M, Fuchs PG, Pfister HJ (2003) Dual role of tumor suppressor p53 in regulation of DNA replication and oncogene E6-promoter activity of epidermodysplasia verruciformis-associated human papillomavirus type 8. Virology 308(2):279-290 (Pubitemid 36434235)
11. Hadaschik D, Hinterkeuser K, Oldak M, Pfister HJ, Smola-Hess S (2003) The Papillomavirus E2 protein binds to and synergizes with C/EBP factors involved in keratinocyte differentiation. J Virol 77(9):5253-5265 (Pubitemid 36460939)
12. Lee D, Lee B, Kim J, Kim DW, Choe J (2000) cAMP response element-binding protein-binding protein binds to human papillomavirus E2 protein and activates E2-dependent transcription. J Biol Chem 275(10):7045-7051 (Pubitemid 30146250)
13. Massimi P, Pim D, Bertoli C, Bouvard V, Banks L (1999) Interaction between the HPV-16 E2 transcriptional activator and p53. Oncogene 18(54):7748-7754 (Pubitemid 30052759)
14. Müller A, Ritzkowsky A, Steger G (2002) Cooperative activation of human papillomavirus type 8 gene expression by the E2 protein and the cellular coactivator p300. J Virol 76(21):11042-11053 (Pubitemid 35176221)
15. Peng YC, Breiding DE, Sverdrup F, Richard J, Androphy EJ (2000) AMF-1/Gps2 binds p300 and enhances its interaction with papillomavirus E2 proteins. J Virol 74(13):5872-5879 (Pubitemid 30412955)
16. Oldak M, Smola H, Aumailley M, Rivero F, Pfister H, Smola-Hess S (2004) The human papillomavirus type 8 E2 protein suppresses beta4-integrin expression in primary human keratinocytes. J Virol 78(19):10738-10746 (Pubitemid 39258399)
17. Steger G, Schnabel C, Schmidt HM (2002) The hinge region of the human papillomavirus type 8 E2 protein activates the human p21(WAF1/CIP1) promoter via interaction with Sp1. J Gen Virol 83(Pt 3):503-510 (Pubitemid 34182994)
18. Pfefferle R, Marcuzzi GP, Akgül B, Kasper HU, Schulze F, Haase I, Wickenhauser C, Pfister H (2008) The human papillomavirus type 8 E2 protein induces skin tumors in transgenic mice. J Invest Dermatol 128(9):2310-2315
19. Behren A, Simon C, Schwab RM, Loetzsch E, Brodbeck S, Huber E, Stubenrauch F, Zenner HP, Iftner T (2005) Papillomavirus E2 protein induces expression of the matrix metalloproteinase-9 via the extracellular signal-regulated kinase/activator protein-1 signaling pathway. Cancer Res 65(24):11613-11621 (Pubitemid 41821721)
20. Muhlen S, Behren A, Iftner T, Plinkert PK, Simon C (2009) AP-1 and ERK1 but not p38 nor JNK is required for CRPV early protein 2-dependent MMP-9 promoter activation in rabbit epithelial cells. Virus Res 139(1):100-105
21. Muhlen S, Behren A, Iftner T, Simon C (2010) Influence of HPV16 E2 and its localisation on the expression of matrix metalloproteinase-9. Int J Oncol 37(2):337-345
22. Purdie KJ, Sexton CJ, Proby CM, Glover MT, Williams AT, Stables JN, Leigh IM (1993) Malignant transformation of cutaneous lesions in renal allograft patients: a role for human papillomavirus. Cancer Res 53(21):5328-5333 (Pubitemid 23333407)
23. Zhang B, Ye S, Herrmann SM, Eriksson P, de Maat M, Evans A, Arveiler D, Luc G, Cambien F, Hamsten A, Watkins H, Henney AM (1999) Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation 99(14):1788-1794 (Pubitemid 29181405)
24. O'Shaughnessy RF, Akgül B, Storey A, Pfister H, Harwood CA, Byrne C (2007) Cutaneous human papillomaviruses down-regulate AKT1, whereas AKT2 up-regulation and activation associates with tumors. Cancer Res 67(17):8207-8215 (Pubitemid 47395157)
25. Akgül B, Garcia-Escudero R, Ghali L, Pfister HJ, Fuchs PG, Navsaria H, Storey A (2005) The E7 protein of cutaneous human papillomavirus type 8 causes invasion of human keratinocytes into the dermis in organotypic cultures of skin. Cancer Res 65(6):2216-2223 (Pubitemid 40490130)
26. Stubenrauch F, Pfister H (1994) Low-affinity E2-binding site mediates downmodulation of E2 transactivation of the human papillomavirus type 8 late promoter. J Virol 68(11):6959-6966 (Pubitemid 24328745)
27. Brokaw JL, Blanco M, McBride AA (1996) Amino acids critical for the functions of the bovine papillomavirus type 1 E2 transactivator. J Virol 70(1):23-29 (Pubitemid 126508764)
28. Stubenrauch F, Colbert AM, Laimins LA (1998) Transactivation by the E2 protein of oncogenic human papillomavirus type 31 is not essential for early and late viral functions. J Virol 72(10):8115-8123 (Pubitemid 28421806)
29. Hegde RS, Grossman SR, Laimins LA, Sigler PB (1992) Crystal structure at 1.7 A of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature 359(6395):505-512
30. Prakash SS, Grossman SR, Pepinsky RB, Laimins LA, Androphy EJ (1992) Amino acids necessary for DNA contact and dimerization imply novel motifs in the papillomavirus E2 trans-activator. Genes Dev 6(1):105-116
31. McPhillips MG, Oliveira JG, Spindler JE, Mitra R, McBride AA (2006) Brd4 is required for e2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J Virol 80(19):9530-9543 (Pubitemid 44435629)
32. Schweiger MR, You J, Howley PM (2006) Bromodomain protein 4 mediates the papillomavirus E2 transcriptional activation function. J Virol 80(9):4276-4285
33. Senechal H, Poirier GG, Coulombe B, Laimins LA, Archambault J (2007) Amino acid substitutions that specifically impair the transcriptional activity of papillomavirus E2 affect binding to the long isoform of Brd4. Virology 358(1):10-17 (Pubitemid 46048882)
34. Verdolini R, Amerio P, Goteri G, Bugatti L, Lucarini G, Mannello B, Filosa G, Offidani A, Brancorsini D, Biagini G, Giangiacomi M (2001) Cutaneous carcinomas and preinvasive neoplastic lesions. Role of MMP-2 and MMP-9 metalloproteinases in neoplastic invasion and their relationship with proliferative activity and p53 expression. J Cutan Pathol 28(3):120-126 (Pubitemid 32112995)
35. Dumas V, Kanitakis J, Charvat S, Euvrard S, Faure M, Claudy A (1999) Expression of basement membrane antigens and matrix metalloproteinases 2 and 9 in cutaneous basal and squamous cell carcinomas. Anticancer Res 19(4B):2929-2938 (Pubitemid 30042573)
36. Chebassier N, Leroy S, Tenaud I, Knol AC, Dreno B (2002) Overexpression of MMP-2 and MMP-9 in squamous cell carcinomas of immunosuppressed patients. Arch Dermatol Res 294(3):124-126 (Pubitemid 34591573)
37. Vermeer PD, Denker J, Estin M, Moninger TO, Keshavjee S, Karp P, Kline JN, Zabner J (2009) MMP9 modulates tight junction integrity and cell viability in human airway epithelia. Am J Physiol Lung Cell Mol Physiol 296(5):L751-L762