Viral weapons of membrane destruction: Variable modes of membrane penetration by non-enveloped viruses

Current Opinion in Virology

Volumn 1, Issue 1, 2011, Pages 44-49

  Moyer, Crystal L ^a   Nemerow, Glen R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; CHAPERONE; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; MARCKS PROTEIN; PHOSPHOLIPASE; VIRUS PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CYTOSOL; ENDOSOME; MEMBRANE DAMAGE; MOLECULAR MECHANICS; NONENVELOPED VIRUS; NONHUMAN; PROTEIN PROCESSING; RECEPTOR BINDING; SIGNAL TRANSDUCTION; VIRUS ENVELOPE; VIRUS GENOME; VIRUS NUCLEOCAPSID; VIRUS PARTICLE; VIRUS TYPING;

EID: 79960439011     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2011.05.002     Document Type: Article

References (54)

1. Hogle JM: Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu Rev Microbiol 2002, 56:677-702. (Pubitemid 35217471)
2. Gallagher TM, Rueckert RR: Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus. J Virol 1988, 62:3399-3406.
3. Bong DT, Steinem C, Janshoff A, Johnson JE, Reza Ghadiri M: A highly membrane-active peptide in flock house virus: implications for the mechanism of nodavirus infection. Chem Biol 1999, 6:473-481. (Pubitemid 29311484)
4. Schneemann A, Zhong W, Gallagher TM, Rueckert RR: Maturation cleavage required for infectivity of a nodavirus. J Virol 1992, 66:6728-6734.
5. Gastaldelli M, Imelli N, Boucke K, Amstutz B, Meier O, Greber UF: Infectious adenovirus type 2 transport through early but not late endosomes. Traffic 2008, 9:2265-2278.
6. Nakano MY, Greber UF: Quantitative microscopy of fluorescent adenovirus entry. J Struct Biol 2000, 129:57-68. (Pubitemid 30130157)
7. Greber UF, Webster P, Weber J, Helenius A: The role of the adenovirus protease on virus entry into cells. EMBO J 1996, 15:1766-1777. (Pubitemid 26119212)
8. Rancourt C, Keyvani-Amineh H, Sircar S, Labrecque P, Weber JM: Proline 137 is critical for adenovirus protease encapsidation and activation but not enzyme activity. Virology 1995, 209:167-173.
9. Hindiyeh M, Li QH, Basavappa R, Hogle JM, Chow M: Poliovirus mutants at histidine 195 of vp2 do not cleave vp0 into vp2 and vp4. J Virol 1999, 73:9072-9079. (Pubitemid 29487060)
10. Greber UF, Willetts M, Webster P, Helenius A: Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75:477-486. (Pubitemid 23335073)
11. Nakano MY, Boucke K, Suomalainen M, Stidwill RP, Greber UF: The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol 2000, 74:7085-7095. (Pubitemid 30470693)
12. Smith JG, Wiethoff CM, Stewart PL, Nemerow GR: Adenovirus. Curr Top Microbiol Immunol 2010, 343:195-224.
13. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR: Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73:309-319. (Pubitemid 23123309)
14. Lindert S, Silvestry M, Mullen TM, Nemerow GR, Stewart PL: Cryo-electron microscopy structure of an adenovirus-integrin complex indicates conformational changes in both penton base and integrin. J Virol 2009, 83:11491-11501.
15. Wickham TJ, Filardo EJ, Cheresh DA, Nemerow GR: Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J Cell Biol 1994, 127:257-264.
16. Mendelsohn CL, Wimmer E, Racaniello VR: Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily Cell 1989, 56:855-865. (Pubitemid 19082521)
17. McDermott BM Jr, Rux AH, Eisenberg RJ, Cohen GH, Racaniello VR: Two distinct binding affinities of poliovirus for its cellular receptor. J Biol Chem 2000, 275:23089-23096. (Pubitemid 30646200)
18. Fricks CE, Hogle JM: Cell-induced conformational change in poliovirus: externalization of the amino terminus of vp1 is responsible for liposome binding. J Virol 1990, 64:1934-1945. (Pubitemid 20148434)
19. Danthi P, Tosteson M, Li QH, Chow M: Genome delivery and ion channel properties are altered in vp4 mutants of poliovirus. J Virol 2003, 77:5266-5274. (Pubitemid 36460940)
20. De Sena J, Mandel B: Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle. Virology 1977, 78:554-566. (Pubitemid 8115902)
21. Bartlett JS, Wilcher R, Samulski RJ: Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 2000, 74:2777-2785. (Pubitemid 30117589)
22. Parker JS, Parrish CR: Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrinmediated endocytosis, followed by slower intracellular trafficking. J Virol 2000, 74:1919-1930. (Pubitemid 30434051)
23. Vihinen-Ranta M, Wang D, Weichert WS, Parrish CR: The vp1 nterminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J Virol 2002, 76:1884-1891. (Pubitemid 34094635)
24. Farr GA, Zhang LG, Tattersall P: Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci USA 2005, 102:17148-17153. (Pubitemid 41692698)
25. Mani B, Baltzer C, Valle N, Almendral JM, Kempf C, Ros C: Low ph-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the vp1 n-terminal sequence (n-vp1), n-vp2 cleavage, and uncoating of the full-length genome. J Virol 2006, 80:1015-1024. (Pubitemid 43062912)
26. Qian M, Cai D, Verhey KJ, Tsai B: A lipid receptor sorts •• polyomavirus from the endolysosome to the endoplasmic reticulum to cause infection. PLoS Pathog 2009, 5:e1000465. Qian et al. characterize the factors governing polyomavirus subcellular trafficking following virus internalization. Elegant live cell microscopy indicated polyomavirus trafficks through endolysosomal compartments, and biochemical analyses provide evidence that infection is dependent upon exposure to low pH in these compartments. Furthermore, the authors show that sorting of polyomavirus to the ER is mediated by the viral receptor, ganglioside GD1a.
27. Odegard A, Banerjee M, Johnson JE: Flock house virus: a model system for understanding non-enveloped virus entry and membrane penetration. Curr Top Microbiol Immunol 2010, 343:1-22.
28. Odegard AL, Kwan MH, Walukiewicz HE, Banerjee M, Schneemann A, Johnson JE: Low endocytic ph and capsid protein autocleavage are critical components of flock house virus cell entry. J Virol 2009, 83:8628-8637.
29. Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC: Structure of the reovirus membrane-penetration protein, mu1, in a complex with is protector protein, sigma3. Cell 2002, 108:283-295. (Pubitemid 34161147)
30. Ebert DH, Deussing J, Peters C, Dermody TS: Cathepsin l and cathepsin b mediate reovirus disassembly in murine fibroblast cells. J Biol Chem 2002, 277:24609-24617. (Pubitemid 34951989)
31. Danthi P, Guglielmi KM, Kirchner E, Mainou B, Stehle T, Dermody TS: From touchdown to transcription: the reovirus cell entry pathway. Curr Top Microbiol Immunol 2010, 343:91-119.
32. Nibert ML, Odegard AL, Agosto MA, Chandran K, Schiff LA: Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J Mol Biol 2005, 345:461-474. (Pubitemid 39575917)
33. Magnuson B, Rainey EK, Benjamin T, Baryshev M, Mkrtchian S, Tsai B: Erp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol Cell 2005, 20:289-300. (Pubitemid 41484173)
34. Sahli R, Freund R, Dubensky T, Garcea R, Bronson R, Benjamin T: Defect in entry and altered pathogenicity of a polyoma virus mutant blocked in vp2 myristylation. Virology 1993, 192:142-153.
35. Wiethoff CM, Wodrich H, Gerace L, Nemerow GR: Adenovirus protein vi mediates membrane disruption following capsid disassembly. J Virol 2005, 79:1992-2000. (Pubitemid 40204556)
36. Moyer CL, Wiethoff CM, Maier O, Smith JG, Nemerow GR: Functional genetic and biophysical analyses of membrane disruption by human adenovirus. J Virol 2011, 85:2631-2641.
37. Maier O, Galan DL, Wodrich H, Wiethoff CM: An n-terminal domain of adenovirus protein vi fragments membranes by inducing positive membrane curvature. Virology 2010, 402:11-19. Maier et al. use biophysical techniques to investigate the interaction of AdV protein VI with model membranes, and find that VI probably perturbs membrane structure via induction of positive curvature. These studies present a possible mechanism for protein VI-mediated endosome rupture during AdV cellular entry.
38. Maier O, Wiethoff CM: N-terminal alpha-helix-independent membrane interactions facilitate adenovirus protein vi induction of membrane tubule formation. Virology 2010, 408:31-38.
39. Prchla E, Plank C, Wagner E, Blaas D, Fuchs R: Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J Cell Biol 1995, 131:111-123.
40. Janshoff A, Bong DT, Steinem C, Johnson JE, Ghadiri MR: An animal virus-derived peptide switches membrane morphology: possible relevance to nodaviral transfection processes. Biochemistry 1999, 38:5328-5336.
41. Bong DT, Janshoff A, Steinem C, Ghadiri MR: Membrane partitioning of the cleavage peptide in flock house virus. Biophys J 2000, 78:839-845. (Pubitemid 30211841)
42. Tuthill TJ, Groppelli E, Hogle JM, Rowlands DJ: Picornaviruses. Curr Top Microbiol Immunol 2010, 343:43-89.
43. Dunnebacke TH, Levinthal JD, Williams RC: Entry and release of poliovirus as observed by electron microscopy of cultured cells. J Virol 1969, 4:505-513.
44. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, •• Hogle JM: Imaging poliovirus entry in live cells. PLoS Biol 2007, 5:e183. Using live-cell microscopy and dual-fluorescent labeling, Brandenburg et al. detail the subcellular trafficking of both the RNA genome and protein capsid during poliovirus cell entry. This technique discriminates between productive and non-productive infections, thus circumventing inherent issues of bulk-analysis.
45. Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, Nibert ML: Putative autocleavage of outer capsid protein micro1, allowing release of myristoylated peptide micro1n during particle uncoating, is critical for cell entry by reovirus. J Virol 2004, 78:8732-8745. (Pubitemid 39025138)
46. Agosto MA, Ivanovic T, Nibert ML: Mammalian reovirus, a nonfusogenic nonenveloped virus, forms size-selective pores in a model membrane. Proc Natl Acad Sci USA 2006, 103:16496-16501. (Pubitemid 44715224)
47. Ivanovic T, Agosto MA, Zhang L, Chandran K, Harrison SC, • Nibert ML: Peptides released from reovirus outer capsid form membrane pores that recruit virus particles. EMBO J 2008, 27:1289-1298. Reovirus membrane penetration is mediated by μ1N, which forms pores in membranes. Ivanovic and colleagues show that once formed, these pores recruit virus particles, thus suggesting a possible mechanistic link between membrane penetration and viral transport to the cytoplasm. (Pubitemid 351574754)
48. Zhang L, Agosto MA, Ivanovic T, King DS, Nibert ML, Harrison SC: Requirements for the formation of membrane pores by the reovirus myristoylated micro1n peptide. J Virol 2009, 83:7004-7014.
49. Parrish CR: Structures and functions of parvovirus capsids and the process of cell infection. Curr Top Microbiol Immunol 2010, 343:149-176.
50. Suikkanen S, Antila M, Jaatinen A, Vihinen-Ranta M, Vuento M: Release of canine parvovirus from endocytic vesicles. Virology 2003, 316:267-280. (Pubitemid 37468530)
51. Kim JW, Lyi SM, Parrish CR, Parker JS: A proapoptotic peptide derived from reovirus outer capsid protein {micro}1 has membrane-destabilizing activity. J Virol 2011, 85:1507-1516.
52. Fejer G, Drechsel L, Liese J, Schleicher U, Ruzsics Z, Imelli N, • Greber UF, Keck S, Hildenbrand B, Krug A et al: Key role of splenic myeloid dcs in the ifn-alphabeta response to adenoviruses in vivo. PLoS Pathog 2008, 4:e1000208. Fejer et al. show that the interferon response to AdV in vivo is primarily mediated by spleic myeloid dendritic cells. Furthermore, the authors provide compelling evidence that the pro-inflammatory response to AdV infection is linked to the endosome penetration step of cell entry, thus suggesting a novel mechanism for innate immune sensing of viral infection.
53. Zhu J, Huang X, Yang Y: Innate immune response to adenoviral vectors is mediated by both toll-like receptor-dependent and - independent pathways. J Virol 2007, 81:3170-3180. (Pubitemid 46456626)
54. Carrillo-Tripp M, Shepherd CM, Borelli IA, Venkataraman S, Lander G, Natarajan P, Johnson JE, Brooks CL 3rd, Reddy VS: Viperdb2: an enhanced and web api enabled relational database for structural virology. Nucleic Acids Res 2009, 37:D436-442.