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Rotavirus Cell Entry

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Cell Entry by Non-Enveloped Viruses

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 343))

Abstract

Infecting nearly every child by age five, rotaviruses are the major causative agents of severe gastroenteritis in young children. While much is known about the structure of these nonenveloped viruses and their components, the exact mechanism of viral cell entry is still poorly understood. A consensus opinion that appears to be emerging from recent studies is that rotavirus cell entry involves a series of complex and coordinated events following proteolytic priming of the virus. Rotaviruses attach to the cell through sialic acid containing receptors, with integrins and Hsc70 acting as postattachment receptors, all localized on lipid rafts. Unlike other endocytotic mechanisms, this internalization pathway appears to be independent of clathrin or caveola. Equally complex and coordinated is the fascinating structural gymnastics of the VP4 spikes that are implicated in facilitating optimal interface between viral and host components. While these studies only begin to capture the basic cellular, molecular, and structural mechanisms of cell entry, the unusual features they have uncovered and many intriguing questions they have raised undoubtedly will prompt further investigations.

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References

  • Angel J, Franco MA, Greenberg HB (2007) Rotavirus vaccines: recent developments and future considerations. Nat Rev Microbiol 5(7):529–539

    PubMed  CAS  Google Scholar 

  • Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, Dormitzer PR (2009) Structure of rotavirus outer layer protein VP7 bound with a neutralizing Fab. Science 324:1444–1447

    Google Scholar 

  • Arias CF, Romero P, Alvarez V, Lopez S (1996) Trypsin activation pathway of rotavirus infectivity. J Virol 70(9):5832–5839

    PubMed  CAS  Google Scholar 

  • Banda K, Kang G, Varki A (2009) ‘Sialidase sensitivity’ of rotaviruses revisited. Nat Chem Biol 5(2):71–72

    PubMed  CAS  Google Scholar 

  • Bass DM, Baylor MR, Chen C, Mackow EM, Bremont M, Greenberg HB (1992) Liposome-mediated transfection of intact viral particles reveals that plasma membrane penetration determines permissivity of tissue culture cells to rotavirus. J Clin Invest 90(6):2313–2320

    PubMed  CAS  Google Scholar 

  • Bass DM, Baylor M, Chen C, Upadhyayula U (1995) Dansylcadaverine and cytochalasin D enhance rotavirus infection of murine L cells. Virology 212(2):429–437

    PubMed  CAS  Google Scholar 

  • Blanchard H, Yu X, Coulson BS, von Itzstein M (2007) Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8*). J Mol Biol 367(4):1215–1226

    PubMed  CAS  Google Scholar 

  • Blutt SE, Conner ME (2007) Rotavirus: to the gut and beyond! Curr Opin Gastroenterol 23(1):39–43

    PubMed  Google Scholar 

  • Charpilienne A, Abad MJ, Michelangeli F, Alvarado F, Vasseur M, Cohen J, Ruiz MC (1997) Solubilized and cleaved VP7, the outer glycoprotein of rotavirus, induces permeabilization of cell membrane vesicles. J Gen Virol 78(Pt 6):1367–1371

    PubMed  CAS  Google Scholar 

  • Chemello ME, Aristimuno OC, Michelangeli F, Ruiz MC (2002) Requirement for vacuolar H+-ATPase activity and Ca2+ gradient during entry of rotavirus into MA104 cells. J Virol 76(24):13083–13087

    PubMed  CAS  Google Scholar 

  • Ciarlet M, Estes MK (1999) Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. J Gen Virol 80(Pt 4):943–948

    PubMed  CAS  Google Scholar 

  • Ciarlet M, Estes MK (2001) Interactions between rotavirus and gastrointestinal cells. Curr Opin Microbiol 4(4):435–441

    PubMed  CAS  Google Scholar 

  • Ciarlet M, Crawford SE, Cheng E, Blutt SE, Rice DA, Bergelson JM, Estes MK (2002) VLA-2 (alpha2beta1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J Virol 76(3):1109–1123

    PubMed  CAS  Google Scholar 

  • Cohen J (1977) Ribonucleic acid polymerase activity associated with purified calf rotavirus. J Gen Virol 36(3):395–402

    PubMed  CAS  Google Scholar 

  • Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422(6927):37–44

    PubMed  CAS  Google Scholar 

  • Coulson BS, Londrigan SL, Lee DJ (1997) Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc Natl Acad Sci USA 94:5389–5394

    PubMed  CAS  Google Scholar 

  • Crawford SE, Mukherjee SK, Estes MK, Lawton JA, Shaw AL, Ramig RF, Prasad BV (2001) Trypsin cleavage stabilizes the rotavirus VP4 spike. J Virol 75(13):6052–6061

    PubMed  CAS  Google Scholar 

  • Cuadras MA, Greenberg HB (2003) Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo. Virology 313(1):308–321

    PubMed  CAS  Google Scholar 

  • Cuadras MA, Arias CF, Lopez S (1997) Rotaviruses induce an early membrane permeabilization of MA104 cells and do not require a low intracellular Ca2+ concentration to initiate their replication cycle. J Virol 71(12):9065–9074

    PubMed  CAS  Google Scholar 

  • Cunliffe NA, Bresee JS, Gentsch JR, Glass RI, Hart CA (2002) The expanding diversity of rotaviruses. Lancet 359(9307):640–641

    PubMed  Google Scholar 

  • Delorme C, Brussow H, Sidoti J, Roche N, Karlsson KA, Neeser JR, Teneberg S (2001) Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J Virol 75(5):2276–2287

    PubMed  CAS  Google Scholar 

  • Denisova E, Dowling W, LaMonica R, Shaw R, Scarlata S, Ruggeri F, Mackow ER (1999) Rotavirus capsid protein VP5* permeabilizes membranes. J Virol 73(4):3147–3153

    PubMed  CAS  Google Scholar 

  • Dimitrov DS (2004) Virus entry: molecular mechanisms and biomedical applications. Nat Rev Microbiol 2(2):109–122

    PubMed  Google Scholar 

  • Dormitzer PR (2008) Rotavirus cell entry. In: Patton J (ed) Segmented double-stranded RNA viruses – structure and molecular biology. Caister/Academic, Norfolk, pp 189–214

    Google Scholar 

  • Dormitzer PR, Greenberg HB, Harrison SC (2000) Purified recombinant rotavirus VP7 forms soluble, calcium-dependent trimers. Virology 277(2):420–428

    PubMed  CAS  Google Scholar 

  • Dormitzer PR, Sun ZY, Blixt O, Paulson JC, Wagner G, Harrison SC (2002a) Specificity and affinity of sialic acid binding by the rhesus rotavirus VP8* core. J Virol 76(20):10512–10517

    PubMed  CAS  Google Scholar 

  • Dormitzer PR, Sun ZY, Wagner G, Harrison SC (2002b) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21(5):885–897

    PubMed  CAS  Google Scholar 

  • Dormitzer PR, Nason EB, Prasad BV, Harrison SC (2004) Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430(7003):1053–1058

    PubMed  CAS  Google Scholar 

  • Estes MK, Kapikian AZ (2006) Rotaviruses. In: Knipe PMHDM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed) Fields virology, vol 2. Lippincott Williams & Wilkins/Wolters Kluwer, Philadelphia, pp 1917–1974, 2 vols

    Google Scholar 

  • Estes MK, Morris AP (1999) A viral enterotoxin. A new mechanism of virus-induced pathogenesis. Adv Exp Med Biol 473:73–82

    PubMed  CAS  Google Scholar 

  • Estes MK, Graham DY, Mason BB (1981) Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J Virol 39(3):879–888

    PubMed  CAS  Google Scholar 

  • Falconer MM, Gilbert JM, Roper AM, Greenberg HB, Gavora JS (1995) Rotavirus-induced fusion from without in tissue culture cells. J Virol 69(9):5582–5591

    PubMed  CAS  Google Scholar 

  • Feng N, Lawton JA, Gilbert J, Kuklin N, Vo P, Prasad BV, Greenberg HB (2002) Inhibition of rotavirus replication by a non-neutralizing, rotavirus VP6-specific IgA mAb. J Clin Invest 109(9):1203–1213

    PubMed  CAS  Google Scholar 

  • Fiore L, Greenberg HB, Mackow ER (1991) The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin. Virology 181(2):553–563

    PubMed  CAS  Google Scholar 

  • Fukudome K, Yoshie O, Konno T (1989) Comparison of human, simian, and bovine rotaviruses for requirement of sialic acid in hemagglutination and cell adsorption. Virology 172(1):196–205

    PubMed  CAS  Google Scholar 

  • Fukuhara N, Yoshie O, Kitaoka S, Konno T (1988) Role of VP3 in human rotavirus internalization after target cell attachment via VP7. J Virol 62(7):2209–2218

    PubMed  CAS  Google Scholar 

  • Gajardo R, Vende P, Poncet D, Cohen J (1997) Two proline residues are essential in the calcium-binding activity of rotavirus VP7 outer capsid protein. J Virol 71(3):2211–2216

    PubMed  CAS  Google Scholar 

  • Gavrilovskaya IN, Brown EJ, Ginsberg MH, Mackow ER (1999) Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J Virol 73(5):3951–3959

    PubMed  CAS  Google Scholar 

  • Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, Jain V, Cunliffe NA, Nakagomi O, Kirkwood CD, Fischer TK, Parashar UD, Bresee JS, Jiang B, Glass RI (2005) Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis 192(Suppl 1):S146–S159

    PubMed  Google Scholar 

  • Gouet P, Diprose JM, Grimes JM, Malby R, Burroughs JN, Zientara S, Stuart DI, Mertens PP (1999) The highly ordered double-stranded RNA genome of bluetongue virus revealed by crystallography. Cell 97(4):481–490

    PubMed  CAS  Google Scholar 

  • Graham KL, Halasz P, Tan Y, Hewish MJ, Takada Y, Mackow ER, Robinson MK, Coulson BS (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(18):9969–9978

    PubMed  CAS  Google Scholar 

  • Greenberg HB, Estes MK (2009) Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136:1939–1951

    PubMed  CAS  Google Scholar 

  • Grimes JM, Jakana J, Ghosh M, Basak AK, Roy P, Chiu W, Stuart DI, Prasad BV (1997) An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure 5(7):885–893

    PubMed  CAS  Google Scholar 

  • Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Zientara S, Mertens PCP, Stuart DI (1998) The atomic structure of the bluetongue virus core. Nature 395:470–478

    PubMed  CAS  Google Scholar 

  • Gualtero DF, Guzman F, Acosta O, Guerrero CA (2007) Amino acid domains 280–297 of VP6 and 531–554 of VP4 are implicated in heat shock cognate protein hsc70-mediated rotavirus infection. Arch Virol 152(12):2183–2196

    PubMed  CAS  Google Scholar 

  • Guerrero CA, Mendez E, Zarate S, Isa P, Lopez S, Arias CF (2000) Integrin alpha(v)beta(3) mediates rotavirus cell entry. Proc Natl Acad Sci USA 97(26):14644–14649

    PubMed  CAS  Google Scholar 

  • Guerrero CA, Bouyssounade D, Zarate S, Isa P, Lopez T, Espinosa R, Romero P, Mendez E, Lopez S, Arias CF (2002) Heat shock cognate protein 70 is involved in rotavirus cell entry. J Virol 76(8):4096–4102

    PubMed  CAS  Google Scholar 

  • Haselhorst T, Fleming FE, Dyason JC, Hartnell RD, Yu X, Holloway G, Santegoets K, Kiefel MJ, Blanchard H, Coulson BS, von Itzstein M (2009) Sialic acid dependence in rotavirus host cell invasion. Nat Chem Biol 5(2):91–93

    PubMed  CAS  Google Scholar 

  • Hewish MJ, Takada Y, Coulson BS (2000) Integrins alpha2beta1 and alpha4beta1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74(1):228–236

    PubMed  CAS  Google Scholar 

  • Hill CL, Booth TF, Prasad BV, Grimes JM, Mertens PP, Sutton GC, Stuart DI (1999) The structure of a cypovirus and the functional organization of dsRNA viruses. Nat Struct Biol 6(6):565–568

    PubMed  CAS  Google Scholar 

  • Hogle JM (2002) Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu Rev Microbiol 56:677–702

    PubMed  CAS  Google Scholar 

  • Hyser JM, Estes MK (2009) Rotavirus vaccines and pathogenesis: 2008. Curr Opin Gastroenterol 25(1):36–43

    PubMed  Google Scholar 

  • Isa P, Realpe M, Romero P, Lopez S, Arias CF (2004) Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 322(2):370–381

    PubMed  CAS  Google Scholar 

  • Isa P, Arias CF, Lopez S (2006) Role of sialic acids in rotavirus infection. Glycoconj J 23(1–2):27–37

    PubMed  CAS  Google Scholar 

  • Kaljot KT, Shaw RD, Rubin DH, Greenberg HB (1988) Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J Virol 62(4):1136–1144

    PubMed  CAS  Google Scholar 

  • Keljo DJ, Smith AK (1988) Characterization of binding of simian rotavirus SA-11 to cultured epithelial cells. J Pediatr Gastroenterol Nutr 7(2):249–256

    PubMed  CAS  Google Scholar 

  • Keljo DJ, Kuhn M, Smith A (1988) Acidification of endosomes is not important for the entry of rotavirus into the cell. J Pediatr Gastroenterol Nutr 7(2):257–263

    PubMed  CAS  Google Scholar 

  • Konno T, Suzuki H, Kitaoka S, Sato T, Fukuhara N, Yoshie O, Fukudome K, Numazaki Y (1993) Proteolytic enhancement of human rotavirus infectivity. Clin Infect Dis 16(Suppl 2):S92–S97

    PubMed  Google Scholar 

  • Kraschnefski MJ, Bugarcic A, Fleming FE, Yu X, von Itzstein M, Coulson BS, Blanchard H (2009) Effects on sialic acid recognition of amino acid mutations in the carbohydrate-binding cleft of the rotavirus spike protein. Glycobiology 19(3):194–200

    PubMed  CAS  Google Scholar 

  • Krishnan T, Sen A, Choudhury JS, Das S, Naik TN, Bhattacharya SK (1999) Emergence of adult diarrhoea rotavirus in Calcutta, India. Lancet 353(9150):380–381

    PubMed  CAS  Google Scholar 

  • Lawton JA, Estes MK, Prasad BV (1997a) Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat Struct Biol 4(2):118–121

    PubMed  CAS  Google Scholar 

  • Lawton JA, Zeng CQ, Mukherjee SK, Cohen J, Estes MK, Prasad BV (1997b) Three-dimensional structural analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer. J Virol 71(10):7353–7360

    PubMed  CAS  Google Scholar 

  • Lawton JA, Estes MK, Prasad BV (1999) Comparative structural analysis of transcriptionally competent and incompetent rotavirus-antibody complexes. Proc Natl Acad Sci USA 96(10):5428–5433

    PubMed  CAS  Google Scholar 

  • Lawton JA, Estes MK, Prasad BV (2000) Mechanism of genome transcription in segmented dsRNA viruses. Adv Virus Res 55:185–229

    PubMed  CAS  Google Scholar 

  • Li Z, Baker ML, Jiang W, Estes MK, Prasad BV (2009) Rotavirus architecture at subnanometer resolution. J Virol 83(4):1754–1766

    PubMed  CAS  Google Scholar 

  • Liemann S, Chandran K, Baker TS, Nibert ML, Harrison SC (2002) Structure of the reovirus membrane-penetration protein, Mu1, in a complex with is protector protein, Sigma3. Cell 108(2):283–295

    PubMed  CAS  Google Scholar 

  • Liprandi F, Moros Z, Gerder M, Ludert JE, Pujol FH, Ruiz MC, Michelangeli F, Charpilienne A, Cohen J (1997) Productive penetration of rotavirus in cultured cells induces coentry of the translation inhibitor alpha-sarcin. Virology 237(2):430–438

    PubMed  CAS  Google Scholar 

  • Lopez S, Arias CF (2004) Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12(6):271–278

    PubMed  CAS  Google Scholar 

  • Lopez S, Arias CF (2006) Early steps in rotavirus cell entry. Curr Top Microbiol Immunol 309:39–66

    PubMed  CAS  Google Scholar 

  • Lorrot M, Vasseur M (2006) Rotavirus NSP4 114-135 peptide has no direct, specific effect on chloride transport in rabbit brush-border membrane. Virol J 3:94

    PubMed  Google Scholar 

  • Ludert JE, Michelangeli F, Gil F, Liprandi F, Esparza J (1987) Penetration and uncoating of rotaviruses in cultured cells. Intervirology 27(2):95–101

    PubMed  CAS  Google Scholar 

  • Ludert JE, Krishnaney AA, Burns JW, Vo PT, Greenberg HB (1996) Cleavage of rotavirus VP4 in vivo. J Gen Virol 77(Pt 3):391–395

    PubMed  CAS  Google Scholar 

  • Mackow ER (2002) Human group B and C rotaviruses, 2nd edn. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL (eds) Infections of the gastrointestinal tract. Lippincott Williams & Wilkins, Philadelphia, pp 879–902

    Google Scholar 

  • Mackow ER, Shaw RD, Matsui SM, Vo PT, Dang MN, Greenberg HB (1988) The rhesus rotavirus gene encoding protein VP3: location of amino acids involved in homologous and heterologous rotavirus neutralization and identification of a putative fusion region. Proc Natl Acad Sci USA 85(3):645–649

    PubMed  CAS  Google Scholar 

  • Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, Pothier P, Prasad BV, Cohen J, Rey FA (2001) Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. EMBO J 20(7):1485–1497

    PubMed  CAS  Google Scholar 

  • Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gomara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82(7):3204–3219

    PubMed  CAS  Google Scholar 

  • McClain B, Settembre E, Temple BR, Bellamy AR, Harrison SC (2010). X-ray crystal structure of rotavirus inner capsid particle at 3.8 A resolution. J. Mol. Biol. 397:587–599

    Google Scholar 

  • Mendez E, Arias CF, Lopez S (1993) Binding to sialic acids is not an essential step for the entry of animal rotaviruses to epithelial cells in culture. J Virol 67(9):5253–5259

    PubMed  CAS  Google Scholar 

  • Mendez E, Lopez S, Cuadras MA, Romero P, Arias CF (1999) Entry of rotaviruses is a multistep process. Virology 263(2):450–459

    PubMed  CAS  Google Scholar 

  • Mertens PPC, Attoui H, Duncan R, Dermody TS (2005) Reoviridae. In: Ball LA (ed) Virus taxonomy. Eighth report of the international committee on taxonomy of viruses. Elsevier/Academic, London, pp 447–454

    Google Scholar 

  • Monnier N, Higo-Moriguchi K, Sun ZY, Prasad BV, Taniguchi K, Dormitzer PR (2006) High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J Virol 80(3):1513–1523

    PubMed  CAS  Google Scholar 

  • Nakagawa A, Miyazaki N, Taka J, Naitow H, Ogawa A, Fujimoto Z, Mizuno H, Higashi T, Watanabe Y, Omura T, Cheng RH, Tsukihara T (2003) The atomic structure of rice dwarf virus reveals the self-assembly mechanism of component proteins. Structure 11(10):1227–1238

    PubMed  CAS  Google Scholar 

  • Nandi P, Charpilienne A, Cohen J (1992) Interaction of rotavirus particles with liposomes. J Virol 66(6):3363–3367

    PubMed  CAS  Google Scholar 

  • Nason EL, Samal SK, Venkataram Prasad BV (2000) Trypsin-induced structural transformation in aquareovirus. J Virol 74(14):6546–6555

    PubMed  CAS  Google Scholar 

  • Nason EL, Rothagel R, Mukherjee SK, Kar AK, Forzan M, Prasad BV, Roy P (2004) Interactions between the inner and outer capsids of bluetongue virus. J Virol 78(15):8059–8067

    PubMed  CAS  Google Scholar 

  • Nejmeddine M, Trugnan G, Sapin C, Kohli E, Svensson L, Lopez S, Cohen J (2000) Rotavirus spike protein VP4 is present at the plasma membrane and is associated with microtubules in infected cells. J Virol 74(7):3313–3320

    PubMed  CAS  Google Scholar 

  • Parashar UD, Glass RI (2009) Rotavirus vaccines – early success, remaining questions. N Engl J Med 360(11):1063–1065

    PubMed  CAS  Google Scholar 

  • Parashar UD, Gibson CJ, Bresse JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12(2):304–306

    PubMed  Google Scholar 

  • Penaranda ME, Cubitt WD, Sinarachatanant P, Taylor DN, Likanonsakul S, Saif L, Glass RI (1989a) Group C rotavirus infections in patients with diarrhea in Thailand, Nepal, and England. J Infect Dis 160(3):392–397

    PubMed  CAS  Google Scholar 

  • Penaranda ME, Ho MS, Fang ZY, Dong H, Bai XS, Duan SC, Ye WW, Estes MK, Echeverria P, Hung T et al (1989b) Seroepidemiology of adult diarrhea rotavirus in China, 1977 to 1987. J Clin Microbiol 27(10):2180–2183

    PubMed  CAS  Google Scholar 

  • Pesavento JB, Crawford SE, Roberts E, Estes MK, Prasad BV (2005) pH-Induced conformational change of the rotavirus VP4 spike: implications for cell entry and antibody neutralization. J Virol 79(13):8572–8580

    PubMed  CAS  Google Scholar 

  • Pesavento JB, Crawford SE, Estes MK, Prasad BV (2006) Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 309:189–219

    PubMed  CAS  Google Scholar 

  • Petrie BL, Graham DY, Estes MK (1981) Identification of rotavirus particle types. Intervirology 16(1):20–28

    PubMed  CAS  Google Scholar 

  • Prasad BV, Wang GJ, Clerx JP, Chiu W (1988) Three-dimensional structure of rotavirus. J Mol Biol 199(2):269–275

    PubMed  CAS  Google Scholar 

  • Prasad BV, Burns JW, Marietta E, Estes MK, Chiu W (1990) Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy. Nature 343(6257):476–479

    PubMed  CAS  Google Scholar 

  • Prasad BV, Rothnagel R, Zeng CQ, Jakana J, Lawton JA, Chiu W, Estes MK (1996) Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382(6590):471–473

    PubMed  CAS  Google Scholar 

  • Quan CM, Doane FW (1983) Ultrastructural evidence for the cellular uptake of rotavirus by endocytosis. Intervirology 20(4):223–231

    PubMed  CAS  Google Scholar 

  • Ramig RF (1997) Genetics of the rotaviruses. Annu Rev Microbiol 51:225–255

    PubMed  CAS  Google Scholar 

  • Ramig RF (2004) Pathogenesis of intestinal and systemic rotavirus infection. J Virol 78(19):10213–10220

    PubMed  CAS  Google Scholar 

  • Ramig RF (2007) Systemic rotavirus infection. Expert Rev Anti Infect Ther 5(4):591–612

    PubMed  CAS  Google Scholar 

  • Reinisch KM, Nibert ML, Harrison SC (2000) Structure of the reovirus core at 3.6 A resolution. Nature 404(6781):960–967

    PubMed  CAS  Google Scholar 

  • Ruiz MC, Alonso-Torre SR, Charpilienne A, Vasseur M, Michelangeli F, Cohen J, Alvarado F (1994) Rotavirus interaction with isolated membrane vesicles. J Virol 68(6):4009–4016

    PubMed  CAS  Google Scholar 

  • Ruiz MC, Abad MJ, Charpilienne A, Cohen J, Michelangeli F (1997) Cell lines susceptible to infection are permeabilized by cleaved and solubilized outer layer proteins of rotavirus. J Gen Virol 78(Pt 11):2883–2893

    PubMed  CAS  Google Scholar 

  • Saif LJ, Jiang B (1994) Nongroup A rotaviruses of humans and animals. Curr Top Microbiol Immunol 185:339–371

    PubMed  CAS  Google Scholar 

  • Sanchez-San Martin C, Lopez T, Arias CF, Lopez S (2004) Characterization of rotavirus cell entry. J Virol 78(5):2310–2318

    PubMed  CAS  Google Scholar 

  • Sanekata T, Ahmed MU, Kader A, Taniguchi K, Kobayashi N (2003) Human group B rotavirus infections cause severe diarrhea in children and adults in Bangladesh. J Clin Microbiol 41(5):2187–2190

    PubMed  CAS  Google Scholar 

  • Santos N, Hoshino Y (2005) Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15(1):29–56

    PubMed  Google Scholar 

  • Sapin C, Colard O, Delmas O, Tessier C, Breton M, Enouf V, Chwetzoff S, Ouanich J, Cohen J, Wolf C, Trugnan G (2002) Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J Virol 76(9):4591–4602

    PubMed  CAS  Google Scholar 

  • Sen A, Kobayashi N, Das S, Krishnan T, Bhattacharya SK, Naik TN (2001) The evolution of human group B rotaviruses. Lancet 357(9251):198–199

    PubMed  CAS  Google Scholar 

  • Shaw AL, Rothnagel R, Chen D, Ramig RF, Chiu W, Prasad BV (1993) Three-dimensional visualization of the rotavirus hemagglutinin structure. Cell 74(4):693–701

    PubMed  CAS  Google Scholar 

  • Shaw AL, Samal SK, Subramanian K, Prasad BV (1996) The structure of aquareovirus shows how the different geometries of the two layers of the capsid are reconciled to provide symmetrical interactions and stabilization. Structure 4(8):957–967

    PubMed  CAS  Google Scholar 

  • Simons K, Ehehalt R (2002) Cholesterol, lipid rafts, and disease. J Clin Invest 110(5):597–603

    PubMed  CAS  Google Scholar 

  • Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569

    PubMed  CAS  Google Scholar 

  • Stewart PL, Nemerow GR (2007) Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol 15(11):500–507

    PubMed  CAS  Google Scholar 

  • Suzuki H, Kitaoka S, Konno T, Sato T, Ishida N (1985) Two modes of human rotavirus entry into MA 104 cells. Arch Virol 85(1–2):25–34

    PubMed  CAS  Google Scholar 

  • Svensson L (1992) Group C rotavirus requires sialic acid for erythrocyte and cell receptor binding. J Virol 66(9):5582–5585

    PubMed  CAS  Google Scholar 

  • Taniguchi K, Urasawa S (1995) Diversity in rotavirus genomes. Semin Virol 6(2):123–131

    CAS  Google Scholar 

  • Tihova M, Dryden KA, Bellamy AR, Greenberg HB, Yeager M (2001) Localization of membrane permeabilization and receptor binding sites on the VP4 hemagglutinin of rotavirus: implications for cell entry. J Mol Biol 314(5):985–992

    PubMed  CAS  Google Scholar 

  • Trask SD, Dormitzer PR (2006) Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J Virol 80(22):11293–11304

    PubMed  CAS  Google Scholar 

  • Triantafilou K, Takada Y, Triantafilou M (2001) Mechanisms of integrin-mediated virus attachment and internalization process. Crit Rev Immunol 21(4):311–322

    PubMed  CAS  Google Scholar 

  • Tucker AW, Haddix AC, Bresee JS, Holman RC, Parashar UD, Glass RI (1998) Cost-effectiveness analysis of a rotavirus immunization program for the United States. JAMA 279(17):1371–1376

    PubMed  CAS  Google Scholar 

  • Willoughby RE, Yolken RH, Schnaar RL (1990) Rotaviruses specifically bind to the neutral glycosphingolipid asialo-GM1. J Virol 64(10):4830–4835

    PubMed  CAS  Google Scholar 

  • Yeager M, Dryden KA, Olson NH, Greenberg HB, Baker TS (1990) Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J Cell Biol 110(6):2133–2144

    PubMed  CAS  Google Scholar 

  • Yeager M, Berriman JA, Baker TS, Bellamy AR (1994) Three-dimensional structure of the rotavirus haemagglutinin VP4 by cryo-electron microscopy and difference map analysis. EMBO J 13(5):1011–1018

    PubMed  CAS  Google Scholar 

  • Yoder JD, Dormitzer PR (2006) Alternative intermolecular contacts underlie the rotavirus VP5* two- to three-fold rearrangement. EMBO J 25(7):1559–1568

    PubMed  CAS  Google Scholar 

  • Yolken RH, Willoughby R, Wee SB, Miskuff R, Vonderfecht S (1987) Sialic acid glycoproteins inhibit in vitro and in vivo replication of rotaviruses. J Clin Invest 79(1):148–154

    PubMed  CAS  Google Scholar 

  • Zarate S, Espinosa R, Romero P, Guerrero CA, Arias CF, Lopez S (2000a) Integrin alpha2beta1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278(1):50–54

    PubMed  CAS  Google Scholar 

  • Zarate S, Espinosa R, Romero P, Mendez E, Arias CF, Lopez S (2000b) The VP5 domain of VP4 can mediate attachment of rotaviruses to cells. J Virol 74(2):593–599

    PubMed  CAS  Google Scholar 

  • Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez KO, Camacho-Nuez M, Arias CF, Lopez S (2003) Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J Virol 77(13):7254–7260

    PubMed  CAS  Google Scholar 

  • Zarate S, Romero P, Espinosa R, Arias CF, Lopez S (2004) VP7 mediates the interaction of rotaviruses with integrin alphavbeta3 through a novel integrin-binding site. J Virol 78(20):10839–10847

    PubMed  CAS  Google Scholar 

  • Zhang H, Zhang J, Yu X, Lu X, Zhang Q, Jakana J, Chen DH, Zhang X, Zhou ZH (1999) Visualization of protein-RNA interactions in cytoplasmic polyhedrosis virus. J Virol 73(2):1624–1629

    PubMed  CAS  Google Scholar 

  • Zhang X, Walker SB, Chipman PR, Nibert ML, Baker TS (2003) Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 A. Nat Struct Biol 10(12):1011–1018

    PubMed  CAS  Google Scholar 

  • Zhang X, Settembre E, Xu C, Dormitzer PR, Bellamy R, Harrison SC, Grigorieff N (2008) Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc Natl Acad Sci USA 105(6):1867–1872

    PubMed  CAS  Google Scholar 

  • Zhou YJ, Burns JW, Morita Y, Tanaka T, Estes MK (1994) Localization of rotavirus VP4 neutralization epitopes involved in antibody-induced conformational changes of virus structure. J Virol 68(6):3955–3964

    PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the support from NIH grants AI36040 and RR002250, National Science Foundation IIS-0705474, and Robert Welch foundation (Q 1279). We thank Mary Estes and Sue Crawford for useful discussions and critical reading of the manuscript.

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Correspondence to B. V. Venkataram Prasad .

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Baker, M., Prasad, B.V.V. (2010). Rotavirus Cell Entry. In: Johnson, J. (eds) Cell Entry by Non-Enveloped Viruses. Current Topics in Microbiology and Immunology, vol 343. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2010_34

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