Structural Correlates of Rotavirus Cell Entry

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Abdelhakim, Aliaa H ^a,d   Salgado, Eric N ^a,e   Fu, Xiaofeng ^b   Pasham, Mithun ^a   Nicastro, Daniela ^b   Kirchhausen, Tomas ^a   Harrison, Stephen C ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Columbia University College of Physicians and Surgeons ^*  (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT DYE; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SIALIDASE; VIRUS PROTEIN; VIRUS RNA; CAPSID PROTEIN; VIRUS ANTIGEN; VP4 PROTEIN, ROTAVIRUS; VP7 PROTEIN, ROTAVIRUS;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN PURIFICATION; QUANTITATIVE ASSAY; ROTAVIRUS; VIRUS DOUBLE LAYERED PARTICLE; VIRUS ENTRY; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS TRANSFORMATION; ANIMAL; CELL CULTURE; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; GENETICS; IMAGE PROCESSING; KIDNEY; METABOLISM; MUTATION; PHYSIOLOGY; VIRION; VIROLOGY; VIRUS ASSEMBLY;

ROTAVIRUS;

ANIMALS; ANTIGENS, VIRAL; CAPSID PROTEINS; CELL MEMBRANE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; IMAGE PROCESSING, COMPUTER-ASSISTED; KIDNEY; MICROSCOPY, ELECTRON; MUTATION; ROTAVIRUS; VIRION; VIRUS ASSEMBLY; VIRUS INTERNALIZATION;

EID: 84907587065     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004355     Document Type: Article

References (49)

1. Danthi P, Tosteson M, Li QH, Chow M, (2003) Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus. J Virol 77: 5266–5274.
2. Dormitzer PR, Nason EB, Prasad BV, Harrison SC, (2004) Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430: 1053–1058.
3. Kim IS, Trask SD, Babyonyshev M, Dormitzer PR, Harrison SC, (2010) Effect of mutations in VP5 hydrophobic loops on rotavirus cell entry. J Virol 84: 6200–6207.
4. Estes MK, Kapikian AZ (2007) Rotaviruses. In: Knipe DM, Howley PM, editors. Fields Virology, 5th ed. Philadelphia: Lippincott, Williams & Wilkins. pp. 1918–1974.
5. Dormitzer PR, Greenberg HB, Harrison SC, (2000) Purified recombinant rotavirus VP7 forms soluble, calcium-dependent trimers. Virology 277: 420–428.
6. Chen JZ, Settembre EC, Aoki ST, Zhang X, Bellamy AR, et al. (2009) Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc Natl Acad Sci U S A 106: 10644–10648.
7. Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, et al. (2009) Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 324: 1444–1447.
8. Prasad BVV, Wang GJ, Clrex JPM, Chiu W, (1988) Three-dimensional structure of rotavirus. J Mol Biol 1998: 269–275.
9. Settembre EC, Chen JZ, Dormitzer PR, Grigorieff N, Harrison SC, (2011) Atomic model of an infectious rotavirus particle. EMBO J 30: 408–416.
10. Crawford SE, Mukherjee SK, Estes MK, Lawton JA, Shaw AL, et al. (2001) Trypsin cleavage stabilizes the rotavirus VP4 spike. J Virol 75: 6052–6061.
11. Clark SM, Roth JR, Clark ML, Barnett BB, Spendlove RS, (1981) Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J Virol 39: 816–822.
12. Espejo RT, Lopez S, Arias C, (1981) Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. J Virol 37: 156–160.
13. Rodriguez JM, Chichon FJ, Martin-Forero E, Gonzalez-Camacho F, Carrascosa JL, et al. (2014) New insights into rotavirus entry machinery: stabilization of rotavirus spike conformation is independent of trypsin cleavage. PLoS Pathog 10: e1004157.
14. Dormitzer PR, Sun ZY, Wagner G, Harrison SC, (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21: 885–897.
15. Yoder JD, Dormitzer PR, (2006) Alternative intermolecular contacts underlie the rotavirus VP5* two- to three-fold rearrangement. EMBO J 25: 1559–1568.
16. Yoder JD, Trask SD, Vo TP, Binka M, Feng N, et al. (2009) VP5* rearranges when rotavirus uncoats. J Virol 83: 11372–11377.
17. Haselhorst T, Fleming FE, Dyason JC, Hartnell RD, Yu X, et al. (2009) Sialic acid dependence in rotavirus host cell invasion. Nat Chem Biol 5: 91–93.
18. Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, et al. (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485: 256–259.
19. Martinez MA, Lopez S, Arias CF, Isa P, (2013) Gangliosides have a functional role during rotavirus cell entry. J Virol 87: 1115–1122.
20. Gutierrez M, Isa P, Sanchez-San Martin C, Perez-Vargas J, Espinosa R, et al. (2010) Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis. J Virol 84: 9161–9169.
21. Wolf M, Vo PT, Greenberg HB, (2011) Rhesus rotavirus entry into a polarized epithelium is endocytosis dependent and involves sequential VP4 conformational changes. J Virol 85: 2492–2503.
22. Trask SD, Dormitzer PR, (2006) Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J Virol 80: 11293–11304.
23. Trask SD, Kim IS, Harrison SC, Dormitzer PR, (2010) A rotavirus spike protein conformational intermediate binds lipid bilayers. J Virol 84: 1764–1770.
24. Estes MK, Graham DY, Gerba CP, Smith EM, (1979) Simian rotavirus SA11 replication in cell cultures. J Virol 31: 810–815.
25. Aoki ST, Trask SD, Coulson BS, Greenberg HB, Dormitzer PR, et al. (2011) Cross-linking of rotavirus outer capsid protein VP7 by antibodies or disulfides inhibits viral entry. J Virol 85: 10509–10517.
26. Dormitzer PR, Greenberg HB, Harrison SC, (2001) Proteolysis of monomeric recombinant rotavirus VP4 yields an oligomeric VP5* core. J Virol 75: 7339–7350.
27. Méndez E, Lopez S, Cuadras MA, Romero P, Arias CF, (1999) Entry of rotaviruses is a multistep process. Virology 263: 450–459.
28. Guerrero CA, Mendez E, Zarate S, Isa P, Lopez S, et al. (2000) Integrin alpha(v)beta(3) mediates rotavirus cell entry. Proc Natl Acad Sci U S A 97: 14644–14649.
29. Zarate S, Espinosa R, Romero P, Guerrero CA, Arias CF, et al. (2000) Integrin alpha2beta1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278: 50–54.
30. Graham KL, Halasz P, Tan Y, Hewish MJ, Takada Y, et al. (2003) Integrin-using rotaviruses bind alpha2beta1 integrin alpha2 I domain via VP4 DGE sequence and recognize alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. J Virol 77: 9969–9978.
31. Guerrero CA, Bouyssounade D, Zarate S, Isa P, Lopez T, et al. (2002) Heat shock cognate protein 70 is involved in rotavirus cell entry. J Virol 76: 4096–4102.
32. Diaz-Salinas MA, Romero P, Espinosa R, Hoshino Y, Lopez S, et al. (2013) The spike protein VP4 defines the endocytic pathway used by rotavirus to enter MA104 cells. J Virol 87: 1658–1663.
33. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, et al. (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591–605.
34. Massol RH, Boll W, Griffin AM, Kirchhausen T, (2006) A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc Natl Acad Sci U S A 103: 10265–10270.
35. Wolf M, Deal EM, Greenberg HB, (2012) Rhesus rotavirus trafficking during entry into MA104 cells is restricted to the early endosome compartment. J Virol 86: 4009–4013.
36. Silva-Ayala D, Lopez T, Gutierrez M, Perrimon N, Lopez S, et al. (2013) Genome-wide RNAi screen reveals a role for the ESCRT complex in rotavirus cell entry. Proc Natl Acad Sci U S A 110: 10270–10275.
37. Diaz-Salinas MA, Silva-Ayala D, Lopez S, Arias CF, (2014) Rotaviruses reach late endosomes and require the cation-dependent mannose-6-phosphate receptor and the activity of cathepsin proteases to enter the cell. J Virol 88: 4389–4402.
38. Kaljot KT, Shaw RD, Rubin DH, Greenberg HB, (1988) Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J Virol 62: 1136–1144.
39. Tsai B, Gilbert JM, Stehle T, Lencer W, Benjamin TL, et al. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 22: 4346–4355.
40. Hummeler K, Tomassini N, Sokol F, (1970) Morphological aspects of the uptake of simian virus 40 by permissive cells. J Virol 6: 87–93.
41. Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, et al. (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12: 11–18 sup pp 11–12.
42. Cocucci E, Aguet F, Boulant S, Kirchhausen T, (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150: 495–507.
43. Cureton DK, Massol RH, Whelan SP, Kirchhausen T, (2010) The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog 6: e1001127.
44. Harbison CE, Lyi SM, Weichert WS, Parrish CR, (2009) Early steps in cell infection by parvoviruses: host-specific differences in cell receptor binding but similar endosomal trafficking. J Virol 83: 10504–10514.
45. Mastronarde DN, (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36–51.
46. Kremer JR, Mastronarde DN, McIntosh JR, (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71–76.
47. Nicastro D, Schwartz C, Pierson J, Gaudette R, Porter ME, et al. (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313: 944–948.
48. Kalwarczyk T, Ziebacz N, Bielejewska A, Zaboklicka E, Koynov K, et al. (2011) Comparative analysis of viscosity of complex liquids and cytoplasm of mammalian cells at the nanoscale. Nano Lett 11: 2157–2163.
49. Ludert JE, Feng N, Yu JH, Broome RL, Hoshino Y, et al. (1996) Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. J Virol 70: 487–493.