Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection

PLoS Pathogens

Volumn 11, Issue 2, 2015, Pages

  Popa, Andreea ^a   Zhang, Wei ^a   Harrison, Megan S ^a   Goodner, Kylia ^a   Kazakov, Teymur ^a   Goodwin, Edward C ^a   Lipovsky, Alex ^a   Burd, Christopher G ^a   DiMaio, Daniel ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN L2; CD8 ANTIGEN; MALTOSE BINDING PROTEIN; PLASMID VECTOR; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; L2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; PROTEIN BINDING; SMALL INTERFERING RNA; VIRUS ANTIGEN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING MOTIF; ELECTRON MICROSCOPY; ENDOSOME; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GOLGI COMPLEX; HUMAN; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; NONHUMAN; PROTEIN BINDING; VIRUS ENTRY; VIRUS INFECTION; VIRUS MUTATION; WART VIRUS; CELL LINE; CELL NUCLEUS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN PAPILLOMAVIRUS TYPE 16; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIROLOGY; VIRUS CAPSID; VIRUS RELEASE;

HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; PAPILLOMAVIRIDAE;

ANTIGENS, VIRAL; BINDING SITES; CAPSID; CAPSID PROTEINS; CELL LINE; CELL NUCLEUS; ENDOSOMES; GOLGI APPARATUS; HEK293 CELLS; HELA CELLS; HUMAN PAPILLOMAVIRUS 16; HUMANS; ONCOGENE PROTEINS, VIRAL; PROTEIN BINDING; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VIRUS INTERNALIZATION; VIRUS RELEASE;

EID: 84924362646     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004699     Document Type: Article

References (54)

1. Parkin DM, Bray F, (2006) Chapter 2: The burden of HPV-related cancers. Vaccine 24 Suppl 3: S3/11–25.
2. Liu WJ, Gissmann L, Sun XY, Kanjanahaluethai A, Muller M, et al. (1997) Sequence close to the N-terminus of L2 protein is displayed on the surface of bovine papillomavirus type 1 virions. Virology 227: 474–483. 9018146
3. Wang JW, Roden RB, (2013) L2, the minor capsid protein of papillomavirus. Virology 445: 175–186. doi: 10.1016/j.virol.2013.04.017 23689062
4. Buck CB, Trus BL, Rossmann MG, Rao VB, (2012) Chapter 18. The Papillomavirus Virion: A Machine Built to Hide Molecular Achilles’ Heels. Viral Molecular Machines, Adv Exp Med Biol 726: 403–422. doi: 10.1007/978-1-4614-0980-9_18 22297524
5. Day PM, Lowy DR, Schiller JT, (2008) Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol 82: 12565–12568. doi: 10.1128/JVI.01631-08 18829767
6. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M, (2001) Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75: 1565–1570. 11152531
7. Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, et al. (2009) Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 83: 2067–2074. doi: 10.1128/JVI.02190-08 19073722
8. Joyce JG, Tung JS, Przysiecki CT, Cook JC, Lehman ED, et al. (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. 10026203
9. Selinka HC, Giroglou T, Nowak T, Christensen ND, Sapp M, (2003) Further evidence that papillomavirus capsids exist in two distinct conformations. J Virol 77: 12961–12967. 14645552
10. 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. 16432208
11. Dasgupta J, Bienkowska-Haba M, Ortega ME, Patel HD, Bodevin S, et al. (2011) Structural basis of oligosaccharide receptor recognition by human papillomavirus. J Biol Chem 286: 2617–2624. doi: 10.1074/jbc.M110.160184 21115492
12. 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. doi: 10.1128/JVI.01721-13 23966387
13. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT, (2008) Mechanisms of human papillomavirus type 16 neutralization by L2 cross-neutralizing and L1 type-specific antibodies. J Virol 82: 4638–4646. doi: 10.1128/JVI.00143-08 18305047
14. Letian T, Tianyu Z, (2010) Cellular receptor binding and entry of human papillomavirus. Virol J 7: 2. doi: 10.1186/1743-422X-7-2 20051141
15. 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. doi: 10.1111/j.1742-4658.2009.07400.x 19878308
16. Schiller JT, Day PM, Kines RC, (2010) Current understanding of the mechanism of HPV infection. Gynecol Oncol 118: S12–17. doi: 10.1016/j.ygyno.2010.04.004 20494219
17. Schelhaas M, Shah B, Holzer M, Blattmann P, Kuhling L, et al. (2012) Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog 8: e1002657. doi: 10.1371/journal.ppat.1002657 22536154
18. Bienkowska-Haba M, Patel HD, Sapp M, (2009) Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog 5: e1000524. doi: 10.1371/journal.ppat.1000524 19629175
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. doi: 10.1128/JVI.03222-12 23345514
20. 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. doi: 10.1016/j.virol.2014.03.021 24928051
21. Laniosz V, Dabydeen SA, Havens MA, Meneses PI, (2009) Human papillomavirus type 16 infection of human keratinocytes requires clathrin and caveolin-1 and is brefeldin a sensitive. J Virol 83: 8221–8232. doi: 10.1128/JVI.00576-09 19494002
22. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, et al. (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. doi: 10.1073/pnas.1302164110 23569269
23. Smith JL, Campos SK, Wandinger-Ness A, Ozbun MA, (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. doi: 10.1128/JVI.01014-08 18667513
24. Zhang W, Kazakov T, Popa A, DiMaio D, (2014) Vesicular trafficking of incoming human papillomavirus type 16 to the Golgi apparatus and endoplasmic reticulum requires gamma-secretase activity. mBio 5: e01777–01714. doi: 10.1128/mBio.01777-14 25227470
25. Aydin I, Weber S, Snijder B, Samperio Ventayol P, Kuhbacher A, et al. (2014) Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathog 10: e1004162. doi: 10.1371/journal.ppat.1004162 24874089
26. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF, (2009) Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5: e1000318. doi: 10.1371/journal.ppat.1000318 19247434
27. 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. 15383670
28. Sapp M, Day PM, (2009) Structure, attachment and entry of polyoma- and papillomaviruses. Virology 384: 400–409. doi: 10.1016/j.virol.2008.12.022 19157477
29. 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. doi: 10.1128/JVI.00980-12 22761365
30. 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. doi: 10.1111/j.1600-0854.2011.01320.x 22151726
31. Kamper N, Day PM, Nowak T, Selinka HC, Florin L, et al. (2006) A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes. J Virol 80: 759–768. 16378978
32. Pereira R, Hitzeroth II, Rybicki EP, (2009) Insights into the role and function of L2, the minor capsid protein of papillomaviruses. Arch Virol 154: 187–197. doi: 10.1007/s00705-009-0310-3 19169853
33. Roden RB, Day PM, Bronzo BK, Yutzy WHt, Yang Y, et al. (2001) Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J Virol 75: 10493–10497. 11581419
34. 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. doi: 10.1128/JVI.01539-12 23097431
35. Seaman MN, (2012) The retromer complex—endosomal protein recycling and beyond. J Cell Sci 125: 4693–4702. doi: 10.1242/jcs.103440 23148298
36. Burd C, Cullen PJ, (2014) Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol 6.
37. Seaman MNJ, (2007) Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci 120: 2378–2389. 17606993
38. Tabuchi M, Yanatori I, Kawai Y, Kishi F, (2010) Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J Cell Sci 123: 756–766. doi: 10.1242/jcs.060574 20164305
39. Buck CB, Pastrana DV, Lowy DR, Schiller JT, (2004) Efficient intracellular assembly of papillomaviral vectors. J Virol 78: 751–757. 14694107
40. Buck CB, Pastrana DV, Lowy DR, Schiller JT, (2005) Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119: 445–462. 16350417
41. Seaman MN, (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165: 111–122. 15078902
42. Sapp M, Kraus U, Volpers C, Snijders PJ, Walboomers JM, et al. (1994) Analysis of type-restricted and cross-reactive epitopes on virus-like particles of human papillomavirus type 33 and in infected tissues using monoclonal antibodies to the major capsid protein. J Gen Virol 75: 3375–3383. 7996132
43. Gullberg M, Gustafsdottir SM, Schallmeiner E, Jarvius J, Bjarnegard M, et al. (2004) Cytokine detection by antibody-based proximity ligation. Proc Natl Acad Sci U S A 101: 8420–8424. 15155907
44. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, et al. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3: 995–1000. 17072308
45. Harrison MS, Hung CS, Liu TT, Christiano R, Walther TC, et al. (2014) A mechanism for retromer endosomal coat complex assembly with cargo. Proc Natl Acad Sci U S A 111: 267–272. doi: 10.1073/pnas.1316482111 24344282
46. Inoue T, Moore P, Tsai B, (2011) How viruses and toxins disassemble to enter host cells. Annu Rev Microbiol 65: 287–305. doi: 10.1146/annurev-micro-090110-102855 21682643
47. Moyer CL, Wiethoff CM, Maier O, Smith JG, Nemerow GR, (2011) Functional genetic and biophysical analyses of membrane disruption by human adenovirus. J Virol 85: 2631–2641. doi: 10.1128/JVI.02321-10 21209115
48. Yin W, Liu D, Liu N, Xu L, Li S, et al. (2012) SNX17 regulates Notch pathway and pancreas development through the retromer-dependent recycling of Jag1. Cell Regen 1:4 doi: 10.1186/2045-9769-1-4
49. Regberg J, Eriksson JN, Langel U, (2013) Cell-penetrating peptides: from cell cultures to in vivo applications. Front Biosci (Elite Ed) 5: 509–516. 23277006
50. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, et al. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761–771. 2450098
51. Goodwin EC, Yang E, Lee CJ, Lee HW, DiMaio D, et al. (2000) Rapid induction of senescence in human cervical carcinoma cells. Proc Natl Acad Sci U S A 97: 10978–10983. 11005870
52. Magaldi TG, Buch MHC, Murata H, Erickson KD, Garcea RL, et al. (2012) Mutations in the GM1 binding site in SV40 VP1 alter receptor usage and cellular tropism. J Virol 86: 7028–7042. doi: 10.1128/JVI.00371-12 22514351
53. Thomas MA, Lichtenstein DL, Krajcsi P, Wold WS, (2007) A real-time PCR method to rapidly titer adenovirus stocks. Methods Mol Med 130: 185–192. 17401173
54. Lipovsky A, Zhang W, Iwasaki A, DiMaio D, Tang BL, (2014) Application of the proximity-dependent assay and fluorescence imaging approaches to study viral entry pathways (in press). MiMB: Membrane Trafficking