Translocation of the papillomavirus L2/vDNA complex across the limiting membrane requires the onset of mitosis

PLoS Pathogens

Volumn 13, Issue 5, 2017, Pages

  Calton, Christine M ^a   Bronnimann, Matthew P ^b   Manson, Ariana R ^c   Li, Shuaizhi ^b   Chapman, Janice A ^a   Suarez Berumen, Marcela ^c   Williamson, Tatum R ^c   Molugu, Sudheer K ^d   Bernal, Ricardo A ^d   Campos, Samuel K ^a,b,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c The University of Arizona   (United States)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; BINDING PROTEIN; CYCLOPHILIN; FURIN; GAMMA SECRETASE; LUCIFERASE; SMALL INTERFERING RNA; CAPSID PROTEIN; L2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; VIRUS DNA;

ACIDIFICATION; ARTICLE; BIOTINYLATION; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL SYNCHRONIZATION; CHROMATIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FLOW CYTOMETRY; GENE MUTATION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; KERATINOCYTE; LUCIFERASE ASSAY; MITOSIS; PAPILLOMAVIRIDAE; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SANGER SEQUENCING; SITE DIRECTED MUTAGENESIS; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; CELL CYCLE CHECKPOINT; CELL LINE; CELL NUCLEUS; ENDOSOME; GENETICS; HUMAN PAPILLOMAVIRUS TYPE 16; METABOLISM; MUTATION; PAPILLOMAVIRUS INFECTION; PHYSIOLOGY; TRANS GOLGI NETWORK; TRANSPORT AT THE CELLULAR LEVEL; VIRAL TROPISM; VIRION; VIROLOGY; VIRUS ENTRY; VIRUS GENOME;

BIOLOGICAL TRANSPORT; CAPSID PROTEINS; CELL CYCLE CHECKPOINTS; CELL LINE; CELL NUCLEUS; DNA, VIRAL; ENDOSOMES; GENOME, VIRAL; HUMAN PAPILLOMAVIRUS 16; HUMANS; KERATINOCYTES; MITOSIS; MUTATION; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; TRANS-GOLGI NETWORK; VIRAL TROPISM; VIRION; VIRUS INTERNALIZATION;

EID: 85020196790     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006200     Document Type: Article

References (67)

1. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, et al. The biology and life-cycle of human papillomaviruses. Vaccine. 2012;30Suppl 5:F55–70. Epub 2012/12/05.
2. Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, et al. Global burden of human papillomavirus and related diseases. Vaccine. 2012;30Suppl 5:F12–23. Epub 2012/12/05.
3. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT, et al. Arrangement of L2 within the papillomavirus capsid. Journal of virology. 2008;82(11):5190–7. Epub 2008/03/28. doi: 10.1128/JVI.02726-07 18367526
4. Favre M, Breitburd F, Croissant O, Orth G, Chromatin-like structures obtained after alkaline disruption of bovine and human papillomaviruses. Journal of virology. 1977;21(3):1205–9. Epub 1977/03/01. 191643
5. Day PM, Roden RB, Lowy DR, Schiller JT, The papillomavirus minor capsid protein, L2, induces localization of the major capsid protein, L1, and the viral transcription/replication protein, E2, to PML oncogenic domains. Journal of virology. 1998;72(1):142–50. Epub 1998/01/07. 9420209
6. Holmgren SC, Patterson NA, Ozbun MA, Lambert PF, The minor capsid protein L2 contributes to two steps in the human papillomavirus type 31 life cycle. Journal of virology. 2005;79(7):3938–48. Epub 2005/03/16. doi: 10.1128/JVI.79.7.3938-3948.2005 15767396
7. Ishii Y, Ozaki S, Tanaka K, Kanda T, Human papillomavirus 16 minor capsid protein L2 helps capsomeres assemble independently of intercapsomeric disulfide bonding. Virus genes. 2005;31(3):321–8. Epub 2005/09/22. doi: 10.1007/s11262-005-3250-3 16175337
8. Day PM, Baker CC, Lowy DR, Schiller JT, Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(39):14252–7. Epub 2004/09/24. doi: 10.1073/pnas.0404229101 15383670
9. Broutian TR, Brendle SA, Christensen ND, Differential binding patterns to host cells associated with particles of several human alphapapillomavirus types. The Journal of general virology. 2010;91(Pt 2):531–40. Epub 2009/10/23. doi: 10.1099/vir.0.012732-0 19846678
10. Cerqueira C, Liu Y, Kuhling L, Chai W, Hafezi W, van Kuppevelt TH, et al. Heparin increases the infectivity of Human Papillomavirus type 16 independent of cell surface proteoglycans and induces L1 epitope exposure. Cellular microbiology. 2013;15(11):1818–36. Epub 2013/04/23. doi: 10.1111/cmi.12150 23601855
11. Culp TD, Cladel NM, Balogh KK, Budgeon LR, Mejia AF, Christensen ND, Papillomavirus particles assembled in 293TT cells are infectious in vivo. Journal of virology. 2006;80(22):11381–4. Epub 2006/09/01. doi: 10.1128/JVI.01328-06 16943284
12. Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, Day PM, Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. Journal of virology. 2009;83(5):2067–74. Epub 2008/12/17. doi: 10.1128/JVI.02190-08 19073722
13. Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM, The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(48):20458–63. Epub 2009/11/19. doi: 10.1073/pnas.0908502106 19920181
14. Richards KF, Bienkowska-Haba M, Dasgupta J, Chen XS, Sapp M, Multiple heparan sulfate binding site engagements are required for the infectious entry of human papillomavirus type 16. Journal of virology. 2013;87(21):11426–37. Epub 2013/08/24. doi: 10.1128/JVI.01721-13 23966387
15. Cerqueira C, Samperio Ventayol P, Vogeley C, Schelhaas M, Kallikrein-8 Proteolytically Processes Human Papillomaviruses in the Extracellular Space To Facilitate Entry into Host Cells. Journal of virology. 2015;89(14):7038–52. Epub 2015/05/01. doi: 10.1128/JVI.00234-15 25926655
16. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT, Mechanisms of human papillomavirus type 16 neutralization by l2 cross-neutralizing and l1 type-specific antibodies. Journal of virology. 2008;82(9):4638–46. Epub 2008/02/29. doi: 10.1128/JVI.00143-08 18305047
17. Day PM, Schelhaas M, Concepts of papillomavirus entry into host cells. Current opinion in virology. 2014;4:24–31. Epub 2014/02/15. doi: 10.1016/j.coviro.2013.11.002 24525291
18. Schelhaas M, Shah B, Holzer M, Blattmann P, Kuhling L, Day PM, et al. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS pathogens. 2012;8(4):e1002657. Epub 2012/04/27. doi: 10.1371/journal.ppat.1002657 22536154
19. Muller KH, Spoden GA, Scheffer KD, Brunnhofer R, De Brabander JK, Maier ME, et al. Inhibition by cellular vacuolar ATPase impairs human papillomavirus uncoating and infection. Antimicrobial agents and chemotherapy. 2014;58(5):2905–11. Epub 2014/03/13. doi: 10.1128/AAC.02284-13 24614368
20. Smith JL, Campos SK, Wandinger-Ness A, Ozbun MA, Caveolin-1-dependent infectious entry of human papillomavirus type 31 in human keratinocytes proceeds to the endosomal pathway for pH-dependent uncoating. Journal of virology. 2008;82(19):9505–12. Epub 2008/08/01. doi: 10.1128/JVI.01014-08 18667513
21. Grassel L, Fast LA, Scheffer KD, Boukhallouk F, Spoden GA, Tenzer S, et al. The CD63-Syntenin-1 Complex Controls Post-Endocytic Trafficking of Oncogenic Human Papillomaviruses. Scientific reports. 2016;6:32337. Epub 2016/09/01. doi: 10.1038/srep32337 27578500
22. Bienkowska-Haba M, Williams C, Kim SM, Garcea RL, Sapp M, Cyclophilins facilitate dissociation of the human papillomavirus type 16 capsid protein L1 from the L2/DNA complex following virus entry. Journal of virology. 2012;86(18):9875–87. Epub 2012/07/05. doi: 10.1128/JVI.00980-12 22761365
23. Day PM, Thompson CD, Schowalter RM, Lowy DR, Schiller JT, Identification of a role for the trans-Golgi network in human papillomavirus 16 pseudovirus infection. Journal of virology. 2013;87(7):3862–70. Epub 2013/01/25. doi: 10.1128/JVI.03222-12 23345514
24. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, Kuruvilla L, et al. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(18):7452–7. Epub 2013/04/10. doi: 10.1073/pnas.1302164110 23569269
25. Zhang W, Kazakov T, Popa A, DiMaio D, Vesicular trafficking of incoming human papillomavirus 16 to the Golgi apparatus and endoplasmic reticulum requires gamma-secretase activity. mBio. 2014;5(5):e01777–14. Epub 2014/09/18. doi: 10.1128/mBio.01777-14 25227470
26. Ishii Y, Nakahara T, Kataoka M, Kusumoto-Matsuo R, Mori S, Takeuchi T, et al. Identification of TRAPPC8 as a host factor required for human papillomavirus cell entry. PloS one. 2013;8(11):e80297. Epub 2013/11/19. doi: 10.1371/journal.pone.0080297 24244674
27. Bergant M, Banks L, SNX17 facilitates infection with diverse papillomavirus types. Journal of virology. 2013;87(2):1270–3. Epub 2012/11/02. doi: 10.1128/JVI.01991-12 23115288
28. Bergant Marusic M, Ozbun MA, Campos SK, Myers MP, Banks L, Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17. Traffic. 2012;13(3):455–67. Epub 2011/12/14. doi: 10.1111/j.1600-0854.2011.01320.x 22151726
29. Popa A, Zhang W, Harrison MS, Goodner K, Kazakov T, Goodwin EC, et al. Direct binding of retromer to human papillomavirus type 16 minor capsid protein L2 mediates endosome exit during viral infection. PLoS pathogens. 2015;11(2):e1004699. Epub 2015/02/19. doi: 10.1371/journal.ppat.1004699 25693203
30. Pim D, Broniarczyk J, Bergant M, Playford MP, Banks L, A Novel PDZ Domain Interaction Mediates the Binding between Human Papillomavirus 16 L2 and Sorting Nexin 27 and Modulates Virion Trafficking. Journal of virology. 2015;89(20):10145–55. Epub 2015/07/24. doi: 10.1128/JVI.01499-15 26202251
31. Aydin I, Weber S, Snijder B, Samperio Ventayol P, Kuhbacher A, Becker M, et al. Large Scale RNAi Reveals the Requirement of Nuclear Envelope Breakdown for Nuclear Import of Human Papillomaviruses. PLoS pathogens. 2014;10(5):e1004162. Epub 2014/05/31. doi: 10.1371/journal.ppat.1004162 24874089
32. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF, Establishment of human papillomavirus infection requires cell cycle progression. PLoS pathogens. 2009;5(2):e1000318. Epub 2009/02/28. doi: 10.1371/journal.ppat.1000318 19247434
33. Broniarczyk J, Massimi P, Bergant M, Banks L, Human Papillomavirus Infectious Entry and Trafficking Is a Rapid Process. Journal of virology. 2015;89(17):8727–32. Epub 2015/06/13. doi: 10.1128/JVI.00722-15 26063434
34. Aydin I, Villalonga-Planells R, Greune L, Bronnimann MP, Calton CM, Becker M, et al. A central region in the minor capsid protein of papillomaviruses facilitates viral genome tethering and membrane penetration for mitotic nuclear entry. PLoS pathogens. 2017;13(5):e1006308.
35. DiGiuseppe S, Luszczek W, Keiffer TR, Bienkowska-Haba M, Guion LG, Sapp MJ, Incoming human papillomavirus type 16 genome resides in a vesicular compartment throughout mitosis. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(22):6289–94. Epub 2016/05/18. doi: 10.1073/pnas.1600638113 27190090
36. Barker DF, Campbell AM, The birA gene of Escherichia coli encodes a biotin holoenzyme synthetase. Journal of molecular biology. 1981;146(4):451–67. Epub 1981/03/15. 7024555
37. DiGiuseppe S, Bienkowska-Haba M, Hilbig L, Sapp M, The nuclear retention signal of HPV16 L2 protein is essential for incoming viral genome to transverse the trans-Golgi network. Virology. 2014;458–459:93–105. Epub 2014/06/15. doi: 10.1016/j.virol.2014.04.024 24928042
38. Howard PK, Shaw J, Otsuka AJ, Nucleotide sequence of the birA gene encoding the biotin operon repressor and biotin holoenzyme synthetase functions of Escherichia coli. Gene. 1985;35(3):321–31. Epub 1985/01/01. 3899863
39. Beckett D, Kovaleva E, Schatz PJ, A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein science: a publication of the Protein Society. 1999;8(4):921–9. Epub 1999/04/22.
40. Parrott MB, Adams KE, Mercier GT, Mok H, Campos SK, Barry MA, Metabolically biotinylated adenovirus for cell targeting, ligand screening, and vector purification. Molecular therapy: the journal of the American Society of Gene Therapy. 2003;8(4):688–700. Epub 2003/10/08.
41. Schatz PJ, Use of peptide libraries to map the substrate specificity of a peptide-modifying enzyme: a 13 residue consensus peptide specifies biotinylation in Escherichia coli. Bio/technology. 1993;11(10):1138–43. Epub 1993/10/01. 7764094
42. Bronnimann MP, Calton CM, Chiquette SF, Li S, Lu M, Chapman JA, et al. Furin Cleavage of L2 During Papillomavirus Infection: Minimal Dependence on Cyclophilins. Journal of virology. 2016. Epub 2016/04/29.
43. Cerqueira C, Schelhaas M, Principles of polyoma- and papillomavirus uncoating. Medical microbiology and immunology. 2012;201(4):427–36. Epub 2012/09/25. doi: 10.1007/s00430-012-0262-1 23001401
44. Richards RM, Lowy DR, Schiller JT, Day PM, Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(5):1522–7. Epub 2006/01/25. doi: 10.1073/pnas.0508815103 16432208
45. Campos SK, Chapman JA, Deymier MJ, Bronnimann MP, Ozbun MA, Opposing effects of bacitracin on human papillomavirus type 16 infection: enhancement of binding and entry and inhibition of endosomal penetration. Journal of virology. 2012;86(8):4169–81. Epub 2012/02/22. doi: 10.1128/JVI.05493-11 22345461
46. Stebelska K, Dubielecka PM, Sikorski AF, The effect of PS content on the ability of natural membranes to fuse with positively charged liposomes and lipoplexes. The Journal of membrane biology. 2005;206(3):203–14. Epub 2006/02/04. doi: 10.1007/s00232-005-0793-0 16456715
47. Wattiaux R, Jadot M, Warnier-Pirotte MT, Wattiaux-De Coninck S, Cationic lipids destabilize lysosomal membrane in vitro. FEBS letters. 1997;417(2):199–202. Epub 1997/12/12. 9395295
48. Bronnimann MP, Chapman JA, Park CK, Campos SK, A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection. Journal of virology. 2013;87(1):464–73. Epub 2012/10/26. doi: 10.1128/JVI.01539-12 23097431
49. DiGiuseppe S, Keiffer TR, Bienkowska-Haba M, Luszczek W, Guion LG, Muller M, et al. Topography of the Human Papillomavirus Minor Capsid Protein L2 during Vesicular Trafficking of Infectious Entry. Journal of virology. 2015;89(20):10442–52. Epub 2015/08/08. doi: 10.1128/JVI.01588-15 26246568
50. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 1997;106(6):348–60. Epub 1998/01/10. 9362543
51. Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA, Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. Journal of cell science. 1998;111 (Pt 23):3497–506. Epub 1998/11/13.
52. Colanzi A, Corda D, Mitosis controls the Golgi and the Golgi controls mitosis. Current opinion in cell biology. 2007;19(4):386–93. Epub 2007/08/11. doi: 10.1016/j.ceb.2007.06.002 17689238
53. Colanzi A, Hidalgo Carcedo C, Persico A, Cericola C, Turacchio G, Bonazzi M, et al. The Golgi mitotic checkpoint is controlled by BARS-dependent fission of the Golgi ribbon into separate stacks in G2. The EMBO journal. 2007;26(10):2465–76. Epub 2007/04/14. doi: 10.1038/sj.emboj.7601686 17431394
54. Marsh MP, Campos SK, Baker ML, Chen CY, Chiu W, Barry MA, Cryoelectron microscopy of protein IX-modified adenoviruses suggests a new position for the C terminus of protein IX. Journal of virology. 2006;80(23):11881–6. Epub 2006/09/22. doi: 10.1128/JVI.01471-06 16987967
55. Cervigni RI, Bonavita R, Barretta ML, Spano D, Ayala I, Nakamura N, et al. JNK2 controls fragmentation of the Golgi complex and the G2/M transition through phosphorylation of GRASP65. Journal of cell science. 2015;128(12):2249–60. Epub 2015/05/08. doi: 10.1242/jcs.164871 25948586
56. Sutterlin C, Hsu P, Mallabiabarrena A, Malhotra V, Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell. 2002;109(3):359–69. Epub 2002/05/23. 12015985
57. Corda D, Barretta ML, Cervigni RI, Colanzi A, Golgi complex fragmentation in G2/M transition: An organelle-based cell-cycle checkpoint. IUBMB life. 2012;64(8):661–70. Epub 2012/06/26. doi: 10.1002/iub.1054 22730233
58. Valente C, Colanzi A, Mechanisms and Regulation of the Mitotic Inheritance of the Golgi Complex. Frontiers in cell and developmental biology. 2015;3:79. Epub 2016/01/07. doi: 10.3389/fcell.2015.00079 26734607
59. Champion L, Linder MI, Kutay U, Cellular Reorganization during Mitotic Entry. Trends in cell biology. 2016. Epub 2016/08/17.
60. Guttler T, Madl T, Neumann P, Deichsel D, Corsini L, Monecke T, et al. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nature structural & molecular biology. 2010;17(11):1367–76. Epub 2010/10/26.
61. Jabbour M, Campbell EM, Fares H, Lybarger L, Discrete domains of MARCH1 mediate its localization, functional interactions, and posttranscriptional control of expression. Journal of immunology. 2009;183(10):6500–12. Epub 2009/11/03.
62. Roux KJ, Kim DI, Raida M, Burke B, A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. The Journal of cell biology. 2012;196(6):801–10. Epub 2012/03/14. doi: 10.1083/jcb.201112098 22412018
63. Buck CB, Pastrana DV, Lowy DR, Schiller JT, Efficient intracellular assembly of papillomaviral vectors. Journal of virology. 2004;78(2):751–7. Epub 2003/12/25. doi: 10.1128/JVI.78.2.751-757.2004 14694107
64. Gordon VM, Klimpel KR, Arora N, Henderson MA, Leppla SH, Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infection and immunity. 1995;63(1):82–7. Epub 1995/01/01. 7806387
65. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE, Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. The Journal of cell biology. 1988;106(3):761–71. Epub 1988/03/01. 2450098
66. Campos SK, Ozbun MA, Two highly conserved cysteine residues in HPV16 L2 form an intramolecular disulfide bond and are critical for infectivity in human keratinocytes. PloS one. 2009;4(2):e4463. Epub 2009/02/14. doi: 10.1371/journal.pone.0004463 19214230
67. Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT, Maturation of papillomavirus capsids. Journal of virology. 2005;79(5):2839–46. Epub 2005/02/15. doi: 10.1128/JVI.79.5.2839-2846.2005 15709003