Papillomavirus infection requires γ secretase

Journal of Virology

Volumn 84, Issue 20, 2010, Pages 10661-10670

  Karanam, Balasubramanyam ^a   Peng, Shiwen ^a   Li, Tong ^a   Buck, Christopher ^b   Day, Patricia M ^b   Roden, Richard B S ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ENDO N (1,3,3) TRIMETHYLBICYCLO[2,2,1]HEPT 2 YL 4 FLUOROPHENYL SULFONAMIDE; 2 [2 (3,5 DIFLUOROPHENYL) ACETYLAMINO] N [1 METHYL 2 OXO 5 PHENYL 2,3 DIHYDRO 1H BENZO[E][1,4]DIAZEPIN 3 YL] PROPIONAMIDE; ANTIVIRUS AGENT; BATIMASTAT; BETA SECRETASE; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; MARIMASTAT; N BENZYLOXYCARBONYL LEUCINE LEUCINAL; N BENZYLOXYCARBONYL LEUCINE PHENYLALANINAL; NICASTRIN; PRESENILIN 1; UNCLASSIFIED DRUG;

ADENOVIRUS; ADENOVIRUS INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CELL NUCLEUS INCLUSION BODY; CELL VIABILITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO; ENZYME ACTIVITY; FEMALE; HUMAN PAPILLOMAVIRUS TYPE 16; IC 50; MOUSE; NONHUMAN; PAPILLOMAVIRUS INFECTION; POLYOMAVIRUS INFECTION; PRIORITY JOURNAL; VERRUCA VULGARIS; VIRUS CAPSID;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL LINE; CELLS, CULTURED; COTTONTAIL RABBIT PAPILLOMAVIRUS; ENZYME INHIBITORS; FEMALE; GENITALIA, FEMALE; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMAN PAPILLOMAVIRUS 31; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PRESENILIN-1; RABBITS;

ADENOVIRIDAE; HUMAN ECHOVIRUS 1; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; PAPILLOMAVIRIDAE; POLYOMAVIRUS;

EID: 77957193739     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01081-10     Document Type: Article

References (53)

1. Beel, A. J., and C. R. Sanders. 2008. Substrate specificity of gamma-secretase and other intramembrane proteases. Cell Mol. Life Sci. 65:1311-1334.
2. Bienkowska-Haba, M., H. D. Patel, and M. Sapp. 2009. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog. 5:e1000524.
3. Bossis, I., R. B. Roden, R. Gambhira, R. Yang, M. Tagaya, P. M. Howley, and P. I. Meneses. 2005. Interaction of tSNARE syntaxin 18 with the papillomavirus minor capsid protein mediates infection. J. Virol. 79:6723-6731.
4. Bousarghin, L., A. Touze, P. Y. Sizaret, and P. Coursaget. 2003. Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J. Virol. 77:3846-3850. (Pubitemid 36297304)
5. Buck, C. B., P. M. Day, C. D. Thompson, J. Lubkowski, W. Lu, D. R. Lowy, and J. T. Schiller. 2006. Human alpha-defensins block papillomavirus infection. Proc. Natl. Acad. Sci. U. S. A. 103:1516-1521.
6. Buck, C. B., D. V. Pastrana, D. R. Lowy, and J. T. Schiller. 2004. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78:751-757.
7. Cai, H., Y. Wang, D. McCarthy, H. Wen, D. R. Borchelt, D. L. Price, and P. C. Wong. 2001. BACE1 is the major β-secretase for generation of Aβ peptides by neurons. Nat. Neurosci. 4:233-234.
8. Campos, S. K., and M. A. Ozbun. 2009. Two highly conserved cysteine residues in HPV16 L2 form an intramolecular disulfide bond and are critical for infectivity in human keratinocytes. PLoS One 4:e4463.
9. Christensen, N. D., N. M. Cladel, and C. A. Reed. 1995. Postattachment neutralization of papillomaviruses by monoclonal and polyclonal antibodies. Virology 207:136-142.
10. Culp, T. D., L. R. Budgeon, and N. D. Christensen. 2006. Human papillomaviruses bind a basal extracellular matrix component secreted by keratinocytes which is distinct from a membrane-associated receptor. Virology 347:147-159.
11. Culp, T. D., N. M. Cladel, K. Balogh, L. R. Budgeon, A. Mejia, and N. D. Christensen. 2006. Papillomavirus particles assembled in 293TT cells are infectious in vivo. J. Virol. 80:11381-11384.
12. Davis, J. A., S. Naruse, H. Chen, C. Eckman, S. Younkin, D. L. Price, D. R. Borchelt, S. S. Sisodia, and P. C. Wong. 1998. An Alzheimer's disease-linked PS1 variant rescues the developmental abnormalities of PS1-deficient embryos. Neuron 20:603-609.
13. Day, P. M., C. C. Baker, D. R. Lowy, and J. T. Schiller. 2004. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc. Natl. Acad. Sci. U. S. A. 101:14252-14257.
14. Day, P. M., D. R. Lowy, and J. T. Schiller. 2008. Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J. Virol. 82:12565-12568.
15. Day, P. M., D. R. Lowy, and J. T. Schiller. 2003. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307:1-11.
16. Doorbar, J. 2005. The papillomavirus life cycle. J. Clin. Virol. 32(Suppl 1):S7-S15.
17. Fay, A., W. H. Yutzy IV, R. B. Roden, and J. Moroianu. 2004. The positively charged termini of L2 minor capsid protein required for bovine papillomavirus infection function separately in nuclear import and DNA binding. J. Virol. 78:13447-13454. (Pubitemid 39612744)
18. Jagu, S., B. Karanam, R. Gambhira, S. V. Chivukula, R. J. Chaganti, D. R. Lowy, J. T. Schiller, and R. B. Roden. 2009. Concatenated multitype L2 fusion proteins as candidate prophylactic pan-human papillomavirus vaccines. J. Natl. Cancer Inst. 101:782-792.
19. Johnson, K. M., R. C. Kines, J. N. Roberts, D. R. Lowy, J. T. Schiller, and P. M. Day. 2009. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J. Virol. 83:2067-2074.
20. Joyce, J. G., J. S. Tung, C. T. Przysiecki, J. C. Cook, E. D. Lehman, J. A. Sands, K. U. Jansen, and P. M. Keller. 1999. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J. Biol. Chem. 274:5810-5822.
21. Kamper, N., P. M. Day, T. Nowak, H. C. Selinka, L. Florin, J. Bolscher, L. Hilbig, J. T. Schiller, and M. Sapp. 2006. A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes. J. Virol. 80:759-768. (Pubitemid 43062888)
22. Karanam, B., S. Jagu, W. K. Huh, and R. B. Roden. 2009. Developing vaccines against minor capsid antigen L2 to prevent papillomavirus infection. Immunol. Cell Biol. 87:287-299.
23. Kim, S. H., Y. I. Yin, Y. M. Li, and S. S. Sisodia. 2004. Evidence that assembly of an active gamma-secretase complex occurs in the early compartments of the secretory pathway. J. Biol. Chem. 279:48615-48619.
24. Kines, R. C., C. D. Thompson, D. R. Lowy, J. T. Schiller, and P. M. Day. 2009. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc. Natl. Acad. Sci. U. S. A. 106:20458-20463.
25. Kirnbauer, R., F. Booy, N. Cheng, D. R. Lowy, and J. T. Schiller. 1992. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl. Acad. Sci. U. S. A. 89:12180-12184.
26. Lah, J. J., and A. I. Levey. 2000. Endogenous presenilin-1 targets to endocytic rather than biosynthetic compartments. Mol. Cell Neurosci. 16:111-126.
27. Lancaster, W. D., C. Olson, and W. Meinke. 1977. Bovine papilloma virus: presence of virus-specific DNA sequences in naturally occurring equine tumors. Proc. Natl. Acad. Sci. U. S. A. 74:524-528.
28. Li, T., G. Ma, H. Cai, D. L. Price, and P. C. Wong. 2003. Nicastrin is required for assembly of presenilin/gamma-secretase complexes to mediate Notch signaling and for processing and trafficking of beta-amyloid precursor protein in mammals. J. Neurosci. 23:3272-3277.
29. Olson, C., D. E. Gordon, M. G. Robl, and K. P. Lee. 1969. Oncogenicity of bovine papilloma virus. Arch. Environ. Health 19:827-837.
30. Parkin, D. M., and F. Bray. 2006. Chapter 2: The burden of HPV-related cancers. Vaccine 24(Suppl 3):S11-S25.
31. Pasternak, S. H., R. D. Bagshaw, M. Guiral, S. Zhang, C. A. Ackerley, B. J. Pak, J. W. Callahan, and D. J. Mahuran. 2003. Presenilin-1, nicastrin, amyloid precursor protein, and gamma-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278:26687-26694.
32. Pastrana, D. V., C. B. Buck, Y. Y. Pang, C. D. Thompson, P. E. Castle, P. C. FitzGerald, S. Kruger Kjaer, D. R. Lowy, and J. T. Schiller. 2004. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321:205-216.
33. Pastrana, D. V., Y. L. Tolstov, J. C. Becker, P. S. Moore, Y. Chang, and C. B. Buck. 2009. Quantitation of human seroresponsiveness to Merkel cell polyomavirus. PLoS Pathog. 5:e1000578.
34. Patterson, N. A., J. L. Smith, and M. A. Ozbun. 2005. Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J. Virol. 79:6838-6847.
35. Pyeon, D., P. F. Lambert, and P. Ahlquist. 2005. Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc. Natl. Acad. Sci. U. S. A. 102:9311-9316.
36. Pyeon, D., S. M. Pearce, S. M. Lank, P. Ahlquist, and P. F. Lambert. 2009. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog. 5:e1000318.
37. Ray, W. J., M. Yao, J. Mumm, E. H. Schroeter, P. Saftig, M. Wolfe, D. J. Selkoe, R. Kopan, and A. M. Goate. 1999. Cell surface presenilin-1 participates in the gamma-secretase-like proteolysis of Notch. J. Biol. Chem. 274:36801-36807.
38. Richards, R. M., D. R. Lowy, J. T. Schiller, and P. M. Day. 2006. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc. Natl. Acad. Sci. U. S. A. 103:1522-1527.
39. Roberts, J. N., C. B. Buck, C. D. Thompson, R. Kines, M. Bernardo, P. L. Choyke, D. R. Lowy, and J. T. Schiller. 2007. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat. Med. 13:857-861.
40. Roden, R. B., P. M. Day, B. K. Bronzo, W. H. t. Yutzy, Y. Yang, D. R. Lowy, and J. T. Schiller. 2001. Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J. Virol. 75:10493-10497.
41. Roden, R. B., H. L. Greenstone, R. Kirnbauer, F. P. Booy, J. Jessie, D. R. Lowy, and J. T. Schiller. 1996. In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. J. Virol. 70:5875-5883.
42. Sapp, M., and M. Bienkowska-Haba. 2009. Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. FEBS J. 276:7206-7216.
43. Sapp, M., and P. M. Day. 2009. Structure, attachment and entry of polyoma- and papillomaviruses. Virology 384:400-409.
44. Schulz, J. G., W. Annaert, J. Vandekerckhove, P. Zimmermann, B. De Strooper, and G. David. 2003. Syndecan 3 intramembrane proteolysis is presenilin/gamma-secretase-dependent and modulates cytosolic signaling. J. Biol. Chem. 278:48651-48657.
45. Shafti-Keramat, S., A. Handisurya, E. Kriehuber, G. Meneguzzi, K. Slupetzky, and R. Kirnbauer. 2003. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol. 77:13125-13135. (Pubitemid 37494308)
46. Shah, S., S. F. Lee, K. Tabuchi, Y. H. Hao, C. Yu, Q. LaPlant, H. Ball, C. E. Dann III, T. Sudhof, and G. Yu. 2005. Nicastrin functions as a gamma-secretase-substrate receptor. Cell 122:435-447.
47. Smith, J. L., S. K. Campos, and M. A. Ozbun. 2007. Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes. J. Virol. 81:9922-9931.
48. Smith, J. L., S. K. Campos, A. Wandinger-Ness, and M. A. Ozbun. 2008. Caveolin-1-dependent infectious entry of human papillomavirus type 31 in human keratinocytes proceeds to the endosomal pathway for pH-dependent uncoating. J. Virol. 82:9505-9512.
49. Struhl, G., and A. Adachi. 2000. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell 6:625-636.
50. Suga, K., A. Saito, T. Tomiyama, H. Mori, and K. Akagawa. 2005. Syntaxin 5 interacts specifically with presenilin holoproteins and affects processing of βAPP in neuronal cells. J. Neurochem. 94:425-439. (Pubitemid 40995258)
51. Vetrivel, K. S., H. Cheng, S. H. Kim, Y. Chen, N. Y. Barnes, A. T. Parent, S. S. Sisodia, and G. Thinakaran. 2005. Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J. Biol. Chem. 280:25892-25900.
52. Walboomers, J. M., M. V. Jacobs, M. M. Manos, F. X. Bosch, J. A. Kummer, K. V. Shah, P. J. Snijders, J. Peto, C. J. Meijer, and N. Muñoz. 1999. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189:12-19. (Pubitemid 29406813)
53. zur Hausen, H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2:342-350.