Papillomavirus virus-like particles activate the PI3-kinase pathway via alpha-6 beta-4 integrin upon binding

Virology

Volumn 352, Issue 2, 2006, Pages 319-328

  Fothergill, Thomas ^a   McMillan, Nigel A J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Akt; FKHR and GSK3 ; Integrin; Papillomavirus; PI3 kinase; VLP

Indexed keywords

ALPHA6BETA4 INTEGRIN; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; TRANSCRIPTION FACTOR FKHR; VIRUS ENZYME;

ARTICLE; CELL COUNT; CELL INTERACTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPILLOMA VIRUS; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS PARTICLE; VIRUS STRAIN;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BASE SEQUENCE; BINDING SITES; BOVINE PAPILLOMAVIRUS 1; CATTLE; CELL CYCLE; CELL LINE; ENZYME ACTIVATION; FORKHEAD TRANSCRIPTION FACTORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INTEGRIN ALPHA6BETA4; MAP KINASE SIGNALING SYSTEM; PAPILLOMAVIRIDAE; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VIRION;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 33747067917     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.05.002     Document Type: Article

References (67)

1. Alessi D.R., James S.R., Downes C.P., Holmes A.B., Gaffney P.R., Reese C.B., and Cohen P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 7 4 (1997) 261-269
2. Basso A.D., Solit D.B., Chiosis G., Giri B., Tsichlis P., and Rosen N. Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J. Biol. Chem. 277 42 (2002) 39858-39866
3. Bosch F.X., Manos M.M., Munoz N., Sherman M., Jansen A.M., Peto J., Schiffman M.H., Moreno V., Kurman R., Shah K.V., and Group I.S. Prevalence of human papillomavirus in cervical cancer. A worldwide perspective. J. Natl. Cancer Inst. 87 (1995) 796-802
4. Bousarghin L., Touze A., Combita-Rojas A.L., and Coursaget P. Positively charged sequences of human papillomavirus type 16 capsid proteins are sufficient to mediate gene transfer into target cells via the heparan sulfate receptor. J. Gen. Virol. 84 Pt. 1 (2003) 157-164
5. Bousarghin L., Touze A., Yvonnet B., and Coursaget P. Positively charged synthetic peptides from structural proteins of papillomaviruses abrogate human papillomavirus infectivity. J. Med. Virol. 73 3 (2004) 474-480
6. Boyle K.A., Pietropaolo R.L., and Compton T. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol. Cell. Biol. 19 5 (1999) 3607-3613
7. Brazil D.P., and Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26 11 (2001) 657-664
8. Briand G., Barbeau B., and Tremblay M. Binding of HIV-1 to its receptor induces tyrosine phosphorylation of several CD4-associated proteins, including the phosphatidylinositol 3-kinase. Virology 228 2 (1997) 171-179
9. Burgering B.M., and Coffer P.J. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376 6541 (1995) 599-602
10. Christensen N.D., and Kreider J.W. Monoclonal antibody neutralization of BPV-1. Virus Res. 28 2 (1993) 195-202
11. Combita A.L., Touze A., Bousarghin L., Sizaret P.Y., Munoz N., and Coursaget P. Gene transfer using human papillomavirus pseudovirions varies according to virus genotype and requires cell surface heparan sulfate. FEMS Microbiol. Lett. 204 1 (2001) 183-188
12. Darr C.D., Mauser A., and Kenney S. Epstein-Barr virus immediate-early protein BRLF1 induces the lytic form of viral replication through a mechanism involving phosphatidylinositol-3 kinase activation. J. Virol. 75 13 (2001) 6135-6142
13. Davis C.B., Dikic I., Unutmaz D., Hill C.M., Arthos J., Siani M.A., Thompson D.A., Schlessinger J., and Littman D.R. Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J. Exp. Med. 186 10 (1997) 1793-1798
14. Derksen P.W., Keehnen R.M., Evers L.M., van Oers M.H., Spaargaren M., and Pals S.T. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 99 4 (2002) 1405-1410
15. Drobni P., Mistry N., McMillan N., and Evander M. Carboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310 1 (2003) 163-172
16. Erlenhoefer C., Wurzer W.J., Loffler S., Schneider-Schaulies S., ter Meulen V., and Schneider-Schaulies J. CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J. Virol. 75 10 (2001) 4499-4505
17. Evander M., Frazer I.H., Payne E., Qi Y.M., Hengst K., and McMillan N.A. Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J. Virol. 71 3 (1997) 2449-2456
18. Fausch S.C., Da Silva D.M., Rudolf M.P., and Kast W.M. Human papillomavirus virus-like particles do not activate Langerhans cells: a possible immune escape mechanism used by human papillomaviruses. J. Immunol. 169 6 (2002) 3242-3249
19. Fruman D.A., and Cantley L.C. Phosphoinositide 3-kinase in immunological systems. Semin. Immunol. 14 1 (2002) 7-18
20. Fukao T., and Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol. 24 7 (2003) 358-363
21. Giroglou T., Florin L., Schafer F., Streeck R.E., and Sapp M. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75 3 (2001) 1565-1570
22. Guha M., and Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277 35 (2002) 32124-32132
23. Helin E., Vainionpaa R., Hyypia T., Julkunen I., and Matikainen S. Measles virus activates NF-kappa B and STAT transcription factors and production of IFN-alpha/beta and IL-6 in the human lung epithelial cell line A549. Virology 290 1 (2001) 1-10
24. Howley P.M. Papillomaviridae: the viruses and their replication. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields' Virology. 3rd ed. vol. 2 (1996), Lippincott-Raven Publishers, Philadelphia 2045-2076 2 vols
25. Johnson R.A., Wang X., Ma X.L., Huong S.M., and Huang E.S. Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J. Virol. 75 13 (2001) 6022-6032
26. Joyce J.G., Tung J.S., Przysiecki C.T., Cook J.C., Lehman E.D., Sands J.A., Jansen K.U., and Keller P.M. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. [in process citation]. J. Biol. Chem. 274 9 (1999) 5810-5822
27. Kikkawa Y., Sanzen N., Fujiwara H., Sonnenberg A., and Sekiguchi K. Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J. Cell Sci. 113 Pt. 5 (2000) 869-876
28. Li E., Stupack D., Klemke R., Cheresh D.A., and Nemerow G.R. Adenovirus endocytosis via alpha-V integrin requires phosphoinositide-3-OH kinase. J. Virol. 72 3 (1998) 2055-2061
29. Liang J., and Slingerland J.M. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2 4 (2003) 339-345
30. Mainiero F., Murgia C., Wary K.K., Curatola A.M., Pepe A., Blumemberg M., Westwick J.K., Der C.J., and Giancotti F.G. The coupling of a6b4 integrin to Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J. 16 9 (1997) 2365-2375
31. McMillan N.A., Payne E., Frazer I.H., and Evander M. Expression of the alpha6 integrin confers papillomavirus binding upon receptor-negative B-cells. Virology 261 2 (1999) 271-279
32. Muller M., Gissmann L., Cristiano R.J., Sun X.Y., Frazer I.H., Jenson A.B., Alonso A., Zentgraf H., and Zhou J. Papillomavirus capsid binding and uptake by cells from different tissues and species. J. Virol. 69 2 (1995) 948-954
33. Nadler S.T., Stoehr J.P., Rabaglia M.E., Schueler K.L., Birnbaum M.J., and Attie A.D. Normal Akt/PKB with reduced PI3K activation in insulin-resistant mice. Am. J. Physiol.: Endocrinol. Metab. 281 6 (2001) E1249-E1254
34. Naranatt P.P., Akula S.M., Zien C.A., Krishnan H.H., and Chandran B. Kaposi's sarcoma-associated herpesvirus induces the phosphatidylinositol 3-kinase-PKC-zeta-MEK-ERK signaling pathway in target cells early during infection: implications for infectivity. J. Virol. 77 2 (2003) 1524-1539
35. Nicholson K.M., and Anderson N.G. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 14 5 (2002) 381-395
36. Okkenhaug K., Bilancio A., Farjot G., Priddle H., Sancho S., Peskett E., Pearce W., Meek S.E., Salpekar A., Waterfield M.D., Smith A.J., and Vanhaesebroeck B. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 297 5583 (2002) 1031-1034
37. Patterson N.A., Smith J.L., and Ozbun M.A. Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J. Virol. 79 11 (2005) 6838-6847
38. Payne E., Bowles M.R., Don A., Hancock J.F., and McMillan N.A. Human papillomavirus type 6b virus-like particles are able to activate the Ras-MAP kinase pathway and induce cell proliferation. J. Virol. 75 9 (2001) 4150-4157
39. Popik W., and Pitha P.M. Early activation of mitogen-activated protein kinase kinase, extracellular signal-regulated kinase, p38 mitogen-activated protein kinase, and c-Jun N-terminal kinase in response to binding of simian immunodeficiency virus to Jurkat T cells expressing CCR5 receptor. Virology 252 1 (1998) 210-217
40. Popik W., Hesselgesser J.E., and Pitha P.M. Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates expression of inflammatory genes and activates the MEK/ERK signaling pathway. J. Virol. 72 8 (1998) 6406-6413
41. Qi Y.M., Peng S.W., Hengst K., Evander M., Park D.S., Zhou J., and Frazer I.H. Epithelial cells display separate receptors for Papillomavirus VLPs and for soluble L1 capsid protein. Virology 216 (1996) 35-45
42. Querbes W., Benmerah A., Tosoni D., Di Fiore P.P., and Atwood W.J. A JC virus-induced signal is required for infection of glial cells by a clathrin- and eps15-dependent pathway. J. Virol. 78 1 (2004) 250-256
43. Roden R.B., Kirnbauer R., Jenson A.B., Lowy D.R., and Schiller J.T. Interaction of papillomaviruses with the cell surface. J. Virol. 68 11 (1994) 7260-7266
44. Roden R.B.S., Hubbert N.L., Kirnbauer R., Christensen N.D., Lowy D.R., and Schiller J.T. Assessment of the serological relatedness of genital human papillomaviruses by hemagglutination inhibition. J. Virol. 70 5 (1996) 3298-3301
45. Roden R.B.S., Armstrong A., Haderer P., Christensen N.D., Hubbert N.L., Lowy D.R., Schiller J.T., and Kirnbauer R. Characterization of a human papillomavirus type 16 variant-dependent neutralizing epitope. J. Virol. 71 8 (1997) 6247-6252
46. Scheid M.P., and Woodgett J.R. PKB/AKT: functional insights from genetic models. Nat. Rev., Mol. Cell Biol. 2 10 (2001) 760-768
47. Scheid M.P., and Woodgett J.R. Unravelling the activation mechanisms of protein kinase B/Akt. FEBS Lett. 546 1 (2003) 108-112
48. Selinka H.C., Giroglou T., and Sapp M. Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299 2 (2002) 279-287
49. Selinka H.C., Giroglou T., Nowak T., Christensen N.D., and Sapp M. Further evidence that papillomavirus capsids exist in two distinct conformations. J. Virol. 77 24 (2003) 12961-12967
50. Shafti-Keramat S., Handisurya A., Kriehuber E., Meneguzzi G., Slupetzky K., and Kirnbauer R. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol. 77 24 (2003) 13125-13135
51. Shih W.L., Kuo M.L., Chuang S.E., Cheng A.L., and Doong S.L. Hepatitis B virus X protein inhibits transforming growth factor-beta-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 275 33 (2000) 25858-25864
52. Stahl S., Weitzman S., and Jones J.C. The role of laminin-5 and its receptors in mammary epithelial cell branching morphogenesis. J. Cell Sci. 110 Pt. 1 (1997) 55-63
53. Stokoe D., Stephens L.R., Copeland T., Gaffney P.R., Reese C.B., Painter G.F., Holmes A.B., McCormick F., and Hawkins P.T. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277 5325 (1997) 567-570
54. Street A., Macdonald A., McCormick C., and Harris M. Hepatitis C virus NS5A-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular beta-catenin and stimulation of beta-catenin-responsive transcription. J. Virol. 79 8 (2005) 5006-5016
55. Sugano N., Chen W., Roberts M.L., and Cooper N.R. Epstein-Barr virus binding to CD21 activates the initial viral promoter via NF-kappaB induction. J. Exp. Med. 186 5 (1997) 731-737
56. Swart R., Ruf I.K., Sample J., and Longnecker R. Latent membrane protein 2A-mediated effects on the phosphatidylinositol 3-kinase/Akt pathway. J. Virol. 74 22 (2000) 10838-10845
57. Tang K., Nie D., Cai Y., and Honn K.V. The beta4 integrin subunit rescues A431 cells from apoptosis through a PI3K/Akt kinase signaling pathway. Biochem. Biophys. Res. Commun. 264 1 (1999) 127-132
58. Viscidi R.P., Ahdieh-Grant L., Clayman B., Fox K., Massad L.S., Cu-Uvin S., Shah K.V., Anastos K.M., Squires K.E., Duerr A., Jamieson D.J., Burk R.D., Klein R.S., Minkoff H., Palefsky J., Strickler H., Schuman P., Piessens E., and Miotti P. Serum immunoglobulin G response to human papillomavirus type 16 virus-like particles in human immunodeficiency virus (HIV)-positive and risk-matched HIV-negative women. J. Infect. Dis. 187 2 (2003) 194-205
59. Volpers C., Unckell F., Schirmacher P., Streeck R.E., and Sapp M. Binding and internalization of human papillomavirus type 33 virus-like particles by eukaryotic cells. J. Virol. 69 6 (1995) 3258-3264
60. Weaver V.M., Lelievre S., Lakins J.N., Chrenek M.A., Jones J.C., Giancotti F., Werb Z., and Bissell M.J. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2 3 (2002) 205-216
61. Weissman D., Rabin R.L., Arthos J., Rubbert A., Dybul M., Swofford R., Venkatesan S., Farber J.M., and Fauci A.S. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature 389 6654 (1997) 981-985
62. Whitman M., Kaplan D.R., Schaffhausen B., Cantley L., and Roberts T.M. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315 6016 (1985) 239-242
63. Williams D.L., Li C., Ha T., Ozment-Skelton T., Kalbfleisch J.H., Preiszner J., Brooks L., Breuel K., and Schweitzer J.B. Modulation of the phosphoinositide 3-kinase pathway alters innate resistance to polymicrobial sepsis. J. Immunol. 172 1 (2004) 449-456
64. Yano S., Tokumitsu H., and Soderling T.R. Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396 6711 (1998) 584-587
65. Yao R., and Cooper G.M. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267 5206 (1995) 2003-2006
66. Yoon C.S., Kim K.D., Park S.N., and Cheong S.W. alpha (6) Integrin is the main receptor of human papillomavirus type 16 vlp. Biochem. Biophys. Res. Commun. 283 3 (2001) 668-673
67. Zur Hausen H. Molecular pathogenesis of cancer of the cervix and its causation by specific human papillomavirus types. Curr. Top. Microbiol. Immunol. 186 (1994) 131-156