Home LiteratureArticle Details
PMID: 21804909 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

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

Current opinion in virology ·Vol. 1 ·No. 1 ·2011-07-00 ·Pages 44-9

Moyer CL, Nemerow GR

Abstract

Significant progress has recently been obtained in our understanding of cellular entry by nonenveloped viruses (NEVs). A key step in the entry process involves the disruption or remodeling of the limiting cell membrane allowing the virus to gain access to the cellular replication machinery. Biochemical, genetic and structural data from diverse virus groups have shed light on the process of membrane penetration thereby revealing both the conservation and divergence of the mechanisms and principles governing this process. In general, membrane breach is achieved via the highly regulated spatiotemporal exposure of a virally encoded membrane lytic factor, resulting in the transfer of the viral genome or nucleocapsid into the cytosol.

MeSH Terms
Animals Cell Membrane/virology Humans Viral Proteins/genetics,metabolism Virion/genetics,physiology Virus Diseases/virology Virus Internalization Viruses/genetics
Chemicals
Viral Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Moyer Crystal L
Department of Immunology and Microbial Sciences, The Scripps Research Institute, La Jolla, CA 92037, USA.
Nemerow Glen R
References (54)
54 references, click to expand
  1. Poliovirus mutants at histidine 195 of VP2 do not cleave VP0 into VP2 and VP4.
    J Virol. 1999 Nov;73(11):9072-9 PMID: 10516013
  2. Structure of the reovirus membrane-penetration protein, Mu1, in a complex with is protector protein, Sigma3.
    Cell. 2002 Jan 25;108(2):283-95 PMID: 11832217
  3. Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus.
    J Virol. 1988 Sep;62(9):3399-406 PMID: 3404580
  4. Mammalian reovirus, a nonfusogenic nonenveloped virus, forms size-selective pores in a model membrane.
    Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16496-501 PMID: 17053074
  5. The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol.
    J Virol. 2000 Aug;74(15):7085-95 PMID: 10888649
  6. Structures and functions of parvovirus capsids and the process of cell infection.
    Curr Top Microbiol Immunol. 2010;343:149-76 PMID: 20397069
  7. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry.
    Proc Natl Acad Sci U S A. 2005 Nov 22;102(47):17148-53 PMID: 16284249
  8. VIPERdb2: an enhanced and web API enabled relational database for structural virology.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D436-42 PMID: 18981051
  9. Infectious adenovirus type 2 transport through early but not late endosomes.
    Traffic. 2008 Dec;9(12):2265-78 PMID: 18980614
  10. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2.
    J Cell Biol. 1995 Oct;131(1):111-23 PMID: 7559769
  11. N-terminal α-helix-independent membrane interactions facilitate adenovirus protein VI induction of membrane tubule formation.
    Virology. 2010 Dec 5;408(1):31-8 PMID: 20869737
  12. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment.
    Cell. 1993 Apr 23;73(2):309-19 PMID: 8477447
  13. Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking.
    J Virol. 2000 Feb;74(4):1919-30 PMID: 10644365
  14. Two distinct binding affinities of poliovirus for its cellular receptor.
    J Biol Chem. 2000 Jul 28;275(30):23089-96 PMID: 10770940
  15. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding.
    J Virol. 1990 May;64(5):1934-45 PMID: 2157861
  16. An animal virus-derived peptide switches membrane morphology: possible relevance to nodaviral transfection processes.
    Biochemistry. 1999 Apr 27;38(17):5328-36 PMID: 10220319
  17. Peptides released from reovirus outer capsid form membrane pores that recruit virus particles.
    EMBO J. 2008 Apr 23;27(8):1289-98 PMID: 18369316
  18. Entry and release of poliovirus as observed by electron microscopy of cultured cells.
    J Virol. 1969 Oct;4(4):505-13 PMID: 4309884
  19. Picornaviruses.
    Curr Top Microbiol Immunol. 2010;343:43-89 PMID: 20397067
  20. Low endocytic pH and capsid protein autocleavage are critical components of Flock House virus cell entry.
    J Virol. 2009 Sep;83(17):8628-37 PMID: 19553341
  21. 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 Jan;80(2):1015-24 PMID: 16379002
  22. A proapoptotic peptide derived from reovirus outer capsid protein {micro}1 has membrane-destabilizing activity.
    J Virol. 2011 Feb;85(4):1507-16 PMID: 21106751
  23. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization.
    J Cell Biol. 1994 Oct;127(1):257-64 PMID: 7523420
  24. Requirements for the formation of membrane pores by the reovirus myristoylated micro1N peptide.
    J Virol. 2009 Jul;83(14):7004-14 PMID: 19439475
  25. ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding.
    Mol Cell. 2005 Oct 28;20(2):289-300 PMID: 16246730
  26. Poliovirus cell entry: common structural themes in viral cell entry pathways.
    Annu Rev Microbiol. 2002;56:677-702 PMID: 12142481
  27. Flock house virus: a model system for understanding non-enveloped virus entry and membrane penetration.
    Curr Top Microbiol Immunol. 2010;343:1-22 PMID: 20407886
  28. Defect in entry and altered pathogenicity of a polyoma virus mutant blocked in VP2 myristylation.
    Virology. 1993 Jan;192(1):142-53 PMID: 8390748
  29. From touchdown to transcription: the reovirus cell entry pathway.
    Curr Top Microbiol Immunol. 2010;343:91-119 PMID: 20397070
  30. Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization.
    J Mol Biol. 2005 Jan 21;345(3):461-74 PMID: 15581891
  31. Stepwise dismantling of adenovirus 2 during entry into cells.
    Cell. 1993 Nov 5;75(3):477-86 PMID: 8221887
  32. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors.
    J Virol. 2000 Mar;74(6):2777-85 PMID: 10684294
  33. Adenovirus protein VI mediates membrane disruption following capsid disassembly.
    J Virol. 2005 Feb;79(4):1992-2000 PMID: 15681401
  34. An N-terminal domain of adenovirus protein VI fragments membranes by inducing positive membrane curvature.
    Virology. 2010 Jun 20;402(1):11-9 PMID: 20409568
  35. Release of canine parvovirus from endocytic vesicles.
    Virology. 2003 Nov 25;316(2):267-80 PMID: 14644609
  36. Adenovirus.
    Curr Top Microbiol Immunol. 2010;343:195-224 PMID: 20376613
  37. Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle.
    Virology. 1977 May 15;78(2):554-66 PMID: 194397
  38. Cryo-electron microscopy structure of an adenovirus-integrin complex indicates conformational changes in both penton base and integrin.
    J Virol. 2009 Nov;83(22):11491-501 PMID: 19726496
  39. Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways.
    J Virol. 2007 Apr;81(7):3170-80 PMID: 17229689
  40. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily.
    Cell. 1989 Mar 10;56(5):855-65 PMID: 2538245
  41. The role of the adenovirus protease on virus entry into cells.
    EMBO J. 1996 Apr 15;15(8):1766-77 PMID: 8617221
  42. Maturation cleavage required for infectivity of a nodavirus.
    J Virol. 1992 Nov;66(11):6728-34 PMID: 1404613
  43. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells.
    J Biol Chem. 2002 Jul 5;277(27):24609-17 PMID: 11986312
  44. Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus.
    J Virol. 2003 May;77(9):5266-74 PMID: 12692228
  45. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection.
    J Virol. 2002 Feb;76(4):1884-91 PMID: 11799183
  46. A lipid receptor sorts polyomavirus from the endolysosome to the endoplasmic reticulum to cause infection.
    PLoS Pathog. 2009 Jun;5(6):e1000465 PMID: 19503604
  47. Quantitative microscopy of fluorescent adenovirus entry.
    J Struct Biol. 2000 Feb;129(1):57-68 PMID: 10675297
  48. Functional genetic and biophysical analyses of membrane disruption by human adenovirus.
    J Virol. 2011 Mar;85(6):2631-41 PMID: 21209115
  49. Imaging poliovirus entry in live cells.
    PLoS Biol. 2007 Jul;5(7):e183 PMID: 17622193
  50. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo.
    PLoS Pathog. 2008 Nov;4(11):e1000208 PMID: 19008951
  51. A highly membrane-active peptide in Flock House virus: implications for the mechanism of nodavirus infection.
    Chem Biol. 1999 Jul;6(7):473-81 PMID: 10381406
  52. Membrane partitioning of the cleavage peptide in flock house virus.
    Biophys J. 2000 Feb;78(2):839-45 PMID: 10653796
  53. 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 Aug;78(16):8732-45 PMID: 15280481
  54. Proline 137 is critical for adenovirus protease encapsidation and activation but not enzyme activity.
    Virology. 1995 May 10;209(1):167-73 PMID: 7747466
Article Info
Journal
Current opinion in virology
Abbr.
Curr Opin Virol
ISSN
1879-6265
DOI
10.1016/j.coviro.2011.05.002
Published
2011-07-00
Pages
44-9
Language
English
Region
Netherlands
NLM ID
101560941
PMCID
PMC3144554
Subset
IM
Grants
NHLBI NIH HHS · R01 HL054352 · United States
NHLBI NIH HHS · R01 HL054352-17 · United States
NEI NIH HHS · R01 EY011431 · United States
NHLBI NIH HHS · HL054352 · United States
NEI NIH HHS · R01 EY011431-15 · United States
External Links
PubMed source DOI: 10.1016/j.coviro.2011.05.002 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2