Furin cleavage of L2 during papillomavirus infection: Minimal dependence on cyclophilins

Journal of Virology

Volumn 90, Issue 14, 2016, Pages 6224-6234

  Bronnimann, Matthew P ^a   Calton, Christine M ^a   Chiquette, Samantha F ^a,b   Li, Shuaizhi ^a   Lu, Mingfeng ^a   Chapman, Janice A ^a   Bratton, Kristin N ^a,c   Schlegel, Angela M ^a,d   Camposa, Samuel K ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c EMORY UNIVERSITY   (United States)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLTRANSFERASE; CELL ENZYME; CYCLOPHILIN; CYSTEINE; FURIN; NEUTRALIZING ANTIBODY; CAPSID PROTEIN; EPITOPE; L2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; SMALL INTERFERING RNA;

AMINO TERMINAL SEQUENCE; ANTIBODY SCREENING; ARTICLE; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; DISULFIDE BOND; EXTRACELLULAR MATRIX; HACAT CELL; HUMAN PAPILLOMAVIRUS TYPE 16; KERATINOCYTE; MUTATIONAL ANALYSIS; NONHUMAN; PAPILLOMAVIRUS INFECTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROPIONIBACTERIUM FREUDENREICHII SHERMANII; PROTEIN CLEAVAGE; PROTEIN DOMAIN; RESIDUE ANALYSIS; VIRUS INFECTIVITY; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; VIROLOGY; VIRUS ENTRY;

AMINO ACID SEQUENCE; CAPSID PROTEINS; CYCLOPHILINS; EPITOPES; FURIN; HUMAN PAPILLOMAVIRUS 16; HUMANS; KERATINOCYTES; MUTAGENESIS, SITE-DIRECTED; MUTATION; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; VIRUS INTERNALIZATION;

EID: 84977471878     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00038-16     Document Type: Article

References (69)

1. Centers for Disease Control and Prevention. 2015. Genital HPV infection- fact sheet. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/std/hpv/stdfact-hpv.htm.
2. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, Stanley MA. 2012. The biology and life-cycle of human papillomaviruses. Vaccine 30(Suppl 5):F55-F70.
3. Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, Vignat J, Ferlay J, Bray F, Plummer M, Franceschi S. 2012. Global burden of human papillomavirus and related diseases. Vaccine 30(Suppl 5):F12-F23.
4. Buck CB, Day PM, Trus BL. 2013. The papillomavirus major capsid protein L1. Virology 445:169-174. http://dx.doi.org/10.1016/j.virol.2013.05.038.
5. Favre M, Breitburd F, Croissant O, Orth G. 1977. Chromatin-like structures obtained after alkaline disruption of bovine and human papillomaviruses. J Virol 21:1205-1209.
6. Wang JW, Roden RB. 2013. L2, the minor capsid protein of papillomavirus. Virology 445:175-186. http://dx.doi.org/10.1016/j.virol.2013.04.017.
7. Cerqueira C, Liu Y, Kuhling L, Chai W, Hafezi W, van Kuppevelt TH, Kuhn JE, Feizi T, Schelhaas M. 2013. Heparin increases the infectivity of human papillomavirus type 16 independent of cell surface proteoglycans and induces L1 epitope exposure. Cell Microbiol 15:1818-1836.
8. Richards KF, Bienkowska-Haba M, Dasgupta J, Chen XS, Sapp M. 2013. Multiple heparan sulfate binding site engagements are required for the infectious entry of human papillomavirus type 16. J Virol 87:11426- 11437. http://dx.doi.org/10.1128/JVI.01721-13.
9. Richards RM, Lowy DR, Schiller JT, Day PM. 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. http://dx.doi.org/10.1073/pnas.0508815103.
10. Schelhaas M, Shah B, Holzer M, Blattmann P, Kuhling L, Day PM, Schiller JT, Helenius A. 2012. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog 8:e1002657. http://dx.doi.org/10.1371/journal.ppat.1002657.
11. Aksoy P, Abban CY, Kiyashka E, Qiang W, Meneses PI. 2014. HPV16 infection of HaCaTs is dependent on beta4 integrin, and alpha6 integrin processing. Virology 449:45-52. http://dx.doi.org/10.1016/j.virol.2013.10.034.
12. Dziduszko A, Ozbun MA. 2013. Annexin A2 and S100A10 regulate human papillomavirus type 16 entry and intracellular trafficking in human keratinocytes. J Virol 87:7502-7515. http://dx.doi.org/10.1128/JVI.00519-13.
13. Raff AB, Woodham AW, Raff LM, Skeate JG, Yan L, Da Silva DM, Schelhaas M, Kast WM. 2013. The evolving field of human papillomavirus receptor research: a review of binding and entry. J Virol 87:6062-6072. http://dx.doi.org/10.1128/JVI.00330-13.
14. Scheffer KD, Gawlitza A, Spoden GA, Zhang XA, Lambert C, Berditchevski F, Florin L. 2013. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J Virol 87:3435-3446. http://dx.doi.org/10.1128/JVI.02906-12.
15. Spoden G, Freitag K, Husmann M, Boller K, Sapp M, Lambert C, Florin L. 2008. Clathrin- and caveolin-independent entry of human papillomavirus type 16-involvement of tetraspanin-enriched microdomains (TEMs). PLoS One 3:e3313. http://dx.doi.org/10.1371/journal.pone.0003313.
16. Spoden G, Kuhling L, Cordes N, Frenzel B, Sapp M, Boller K, Florin L, Schelhaas M. 2013. Human papillomavirus types 16, 18, and 31 share similar endocytic requirements for entry. J Virol 87:7765-7773. http://dx.doi.org/10.1128/JVI.00370-13.
17. Surviladze Z, Dziduszko A, Ozbun MA. 2012. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog 8:e1002519. http://dx.doi.org/10.1371/journal.ppat.1002519.
18. Müller KH, Spoden GA, Scheffer KD, Brunnhofer R, De Brabander JK, Maier ME, Florin L, Muller CP. 2014. Inhibition by cellular vacuolar ATPase impairs human papillomavirus uncoating and infection. Antimicrob Agents Chemother 58:2905-2911. http://dx.doi.org/10.1128/AAC.02284-13.
19. Day PM, Thompson CD, Schowalter RM, Lowy DR, Schiller JT. 2013. Identification of a role for the trans-Golgi network in human papillomavirus 16 pseudovirus infection. J Virol 87:3862-3870. http://dx.doi.org/10.1128/JVI.03222-12.
20. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, Kuruvilla L, Guie MA, Poffenberger AC, Nelson CD, Atwood WJ, DiMaio D. 2013. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc Natl Acad Sci U S A 110:7452- 7457. http://dx.doi.org/10.1073/pnas.1302164110.
21. Popa A, Zhang W, Harrison MS, Goodner K, Kazakov T, Goodwin EC, Lipovsky A, Burd CG, DiMaio D. 2015. Direct binding of retromer to human papillomavirus type 16 minor capsid protein L2 mediates endosome exit during viral infection. PLoS Pathog 11:e1004699. http://dx.doi.org/10.1371/journal.ppat.1004699.
22. Zhang W, Kazakov T, Popa A, DiMaio D. 2014. Vesicular trafficking of incoming human papillomavirus 16 to the Golgi apparatus and endoplasmic reticulum requires gamma-secretase activity. mBio 5:e01777-14. http://dx.doi.org/10.1128/mBio.01777-14.
23. Bienkowska-Haba M, Williams C, Kim SM, Garcea RL, Sapp M. 2012. Cyclophilins facilitate dissociation of the human papillomavirus type 16 capsid protein L1 from the L2/DNA complex following virus entry. J Virol 86:9875-9887. http://dx.doi.org/10.1128/JVI.00980-12.
24. DiGiuseppe S, Bienkowska-Haba M, Hilbig L, Sapp M. 2014. The nuclear retention signal of HPV16 L2 protein is essential for incoming viral genome to transverse the trans-Golgi network. Virology 458-459: 93-105.
25. Calton CM, Schlegel AM, Chapman JA, Campos SK. 2013. Human papillomavirus type 16 does not require cathepsin L or B for infection. J Gen Virol 94:1865-1869. http://dx.doi.org/10.1099/vir.0.053694-0.
26. Bergant M, Banks L. 2013. SNX17 facilitates infection with diverse papillomavirus types. J Virol 87:1270-1273. http://dx.doi.org/10.1128/JVI.01991-12.
27. Bergant Marusic M, Ozbun MA, Campos SK, Myers MP, Banks L. 2012. Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17. Traffic 13:455-467. http://dx.doi.org/10.1111/j.1600-0854.2011.01320.x.
28. Schneider MA, Spoden GA, Florin L, Lambert C. 2011. Identification of the dynein light chains required for human papillomavirus infection. Cell Microbiol 13:32-46. http://dx.doi.org/10.1111/j.1462-5822.2010.01515.x.
29. Campos SK, Chapman JA, Deymier MJ, Bronnimann MP, Ozbun MA. 2012. Opposing effects of bacitracin on human papillomavirus type 16 infection: enhancement of binding and entry and inhibition of endosomal penetration. J Virol 86:4169-4181. http://dx.doi.org/10.1128/JVI.05493-11.
30. Aydin I, Weber S, Snijder B, Samperio Ventayol P, Kuhbacher A, Becker M, Day PM, Schiller JT, Kann M, Pelkmans L, Helenius A, Schelhaas M. 2014. Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathog 10:e1004162. http://dx.doi.org/10.1371/journal.ppat.1004162.
31. Bronnimann MP, Chapman JA, Park CK, Campos SK. 2013. A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection. J Virol 87:464-473. http://dx.doi.org/10.1128/JVI.01539-12.
32. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF. 2009. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5:e1000318. http://dx.doi.org/10.1371/journal.ppat.1000318.
33. Day PM, Baker CC, Lowy DR, Schiller JT. 2004. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc Natl Acad Sci U S A 101:14252-14257. http://dx.doi.org/10.1073/pnas.0404229101.
34. Thomas G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3:753-766. http://dx.doi.org/10.1038/nrm934.
35. Nakayama K. 1997. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 327(Part 3):625-635.
36. Campos SK, Barry MA. 2006. Comparison of adenovirus fiber, protein IX, and hexon capsomeres as scaffolds for vector purification and cell targeting. Virology 349:453-462. http://dx.doi.org/10.1016/j.virol.2006.01.032.
37. Campos SK, Ozbun MA. 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. http://dx.doi.org/10.1371/journal.pone.0004463.
38. Rubio I, Seitz H, Canali E, Sehr P, Bolchi A, Tommasino M, Ottonello S, Muller M. 2011. The N-terminal region of the human papillomavirus L2 protein contains overlapping binding sites for neutralizing, crossneutralizing and non-neutralizing antibodies. Virology 409:348-359. http://dx.doi.org/10.1016/j.virol.2010.10.017.
39. Abramoff MD, Magalhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics Int 11:36-42.
40. Bienkowska-Haba M, Patel HD, Sapp M. 2009. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog 5:e1000524. http://dx.doi.org/10.1371/journal.ppat.1000524.
41. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT. 2008. Mechanisms of human papillomavirus type 16 neutralization by L2 crossneutralizing and L1 type-specific antibodies. J Virol 82:4638-4646. http://dx.doi.org/10.1128/JVI.00143-08.
42. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT, Trus BL. 2008. Arrangement of L2 within the papillomavirus capsid. J Virol 82:5190-5197. http://dx.doi.org/10.1128/JVI.02726-07.
43. Windram OP, Weber B, Jaffer MA, Rybicki EP, Shepherd DN, Varsani A. 2008. An investigation into the use of human papillomavirus type 16 virus-like particles as a delivery vector system for foreign proteins: N- and C-terminal fusion of GFP to the L1 and L2 capsid proteins. Arch Virol 153:585-589. http://dx.doi.org/10.1007/s00705-007-0025-2.
44. Parrott MB, Adams KE, Mercier GT, Mok H, Campos SK, Barry MA. 2003. Metabolically biotinylated adenovirus for cell targeting, ligand screening, and vector purification. Mol Ther 8:688-700. http://dx.doi.org/10.1016/S1525-0016(03)00213-2.
45. Christakos KJ, Chapman JA, Fane BA, Campos SK. 2016. PhiXing-it, displaying foreign peptides on bacteriophage PhiX174. Virology 488:242- 248. http://dx.doi.org/10.1016/j.virol.2015.11.021.
46. Reddy DV, Shenoy BC, Carey PR, Sonnichsen FD. 2000. High resolution solution structure of the 1.3S subunit of transcarboxylase from Propionibacterium shermanii. Biochemistry 39:2509-2516. http://dx.doi.org/10.1021/bi9925367.
47. Esko JD, Stewart TE, Taylor WH. 1985. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci U S A 82:3197-3201. http://dx.doi.org/10.1073/pnas.82.10.3197.
48. Day PM, Lowy DR, Schiller JT. 2008. Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol 82:12565-12568. http://dx.doi.org/10.1128/JVI.01631-08.
49. Chiron MF, Fryling CM, FitzGerald D. 1997. Furin-mediated cleavage of Pseudomonas exotoxin-derived chimeric toxins. J Biol Chem 272:31707- 31711. http://dx.doi.org/10.1074/jbc.272.50.31707.
50. Gordon VM, Klimpel KR, Arora N, Henderson MA, Leppla SH. 1995. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect Immun 63:82-87.
51. Wang JW, Jagu S, Kwak K, Wang C, Peng S, Kirnbauer R, Roden RB. 2014. Preparation and properties of a papillomavirus infectious intermediate and its utility for neutralization studies. Virology 449:304-316. http://dx.doi.org/10.1016/j.virol.2013.10.038.
52. Mamoor S, Onder Z, Karanam B, Kwak K, Bordeaux J, Crosby L, Roden RB, Moroianu J. 2012. The high risk HPV16 L2 minor capsid protein has multiple transport signals that mediate its nucleocytoplasmic traffic. Virology 422:413-424. http://dx.doi.org/10.1016/j.virol.2011.11.007.
53. Roden RB, Day PM, Bronzo BK, Yutzy WHt Yang Y, Lowy DR, Schiller JT. 2001. Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J Virol 75:10493-10497. http://dx.doi.org/10.1128/JVI.75.21.10493-10497.2001.
54. Sen J, Jacobs A, Jiang H, Rong L, Caffrey M. 2007. The disulfide loop of gp41 is critical to the furin recognition site of HIV gp160. Protein Sci 16:1236-1241. http://dx.doi.org/10.1110/ps.072771407.
55. Day PM, Thompson CD, Buck CB, Pang YY, Lowy DR, Schiller JT. 2007. Neutralization of human papillomavirus with monoclonal antibodies reveals different mechanisms of inhibition. J Virol 81:8784-8792. http://dx.doi.org/10.1128/JVI.00552-07.
56. Lee H, Brendle SA, Bywaters SM, Guan J, Ashley RE, Yoder JD, Makhov AM, Conway JF, Christensen ND, Hafenstein S. 2015. A cryoelectron microscopy study identifies the complete H16.V5 epitope and reveals global conformational changes initiated by binding of the neutralizing antibody fragment. J Virol 89:1428-1438. http://dx.doi.org/10.1128/JVI.02898-14.
57. Cardone G, Moyer AL, Cheng N, Thompson CD, Dvoretzky I, Lowy DR, Schiller JT, Steven AC, Buck CB, Trus BL. 2014. Maturation of the human papillomavirus 16 capsid. mBio 5:e01104-14. http://dx.doi.org/10.1128/mBio.01104-14.
58. Carter JJ, Wipf GC, Benki SF, Christensen ND, Galloway DA. 2003. Identification of a human papillomavirus type 16-specific epitope on the C-terminal arm of the major capsid protein L1. J Virol 77:11625-11632. http://dx.doi.org/10.1128/JVI.77.21.11625-11632.2003.
59. Gambhira R, Karanam B, Jagu S, Roberts JN, Buck CB, Bossis I, Alphs HH, Culp T, Christensen ND, Roden RBS. 2007. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J Virol 81:13927-13931. http://dx.doi.org/10.1128/JVI.00936-07.
60. Cameron A, Appel J, Houghten RA, Lindberg I. 2000. Polyarginines are potent furin inhibitors. J Biol Chem 275:36741-36749. http://dx.doi.org/10.1074/jbc.M003848200.
61. Sapp M, Bienkowska-Haba M. 2009. Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. FEBS J 276:7206-7216. http://dx.doi.org/10.1111/j.1742-4658.2009.07400.x.
62. Wiens ME, Smith JG. 2015. Alpha-defensin HD5 inhibits furin cleavage of human papillomavirus 16 L2 to block infection. J Virol 89:2866-2874. http://dx.doi.org/10.1128/JVI.02901-14.
63. Guan J, Bywaters SM, Brendle SA, Lee H, Ashley RE, Christensen ND, Hafenstein S. 2015. The U4 antibody epitope on human papillomavirus 16 identified by cryo-electron microscopy. J Virol 89:12108-12117. http://dx.doi.org/10.1128/JVI.02020-15.
64. Wei JX, Yang J, Sun JF, Jia LT, Zhang Y, Zhang HZ, Li X, Meng YL, Yao LB, Yang AG. 2009. Both strands of siRNA have potential to guide posttranscriptional gene silencing in mammalian cells. PLoS One 4:e5382. http://dx.doi.org/10.1371/journal.pone.0005382.
65. Worby CA, Dixon JE. 2002. Sorting out the cellular functions of sorting nexins. Nat Rev Mol Cell Biol 3:919-931. http://dx.doi.org/10.1038/nrm974.
66. Schowalter RM, Smith SE, Dutch RE. 2006. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J Virol 80:10931-10941. http://dx.doi.org/10.1128/JVI.01287-06.
67. Gordon VM, Leppla SH. 1994. Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases. Infect Immun 62:333-340.
68. Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM. 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. http://dx.doi.org/10.1073/pnas.0908502106.
69. Cerqueira C, Samperio Ventayol P, Vogeley C, Schelhaas M. 2015. Kallikrein-8 proteolytically processes human papillomaviruses in the extracellular space to facilitate entry into host cells. J Virol 89:7038-7052. http://dx.doi.org/10.1128/JVI.00234-15.