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Structural Insights into Rotavirus Entry

  • Javier M. RodríguezEmail author
  • Daniel LuqueEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1215)

Abstract

To initiate infection, non-enveloped viruses must recognize a target cell and penetrate the cell membrane by pore formation or membrane lysis. Rotaviruses are non-enveloped dsRNA viruses that infect the mature intestinal epithelium. They are major etiologic agents of diarrheal disease in human infants, as well as in young individuals of various avian and mammalian species. Rotavirus entry into the cell is a complex multistep process initiated by the interaction of the tip of the viral spike with glycan ligands at the cell surface, and driven by conformational changes of the proteins present in the outer protein capsid, the viral machinery for entry. This review feeds on the abundant structural information produced for rotavirus during the past 30 years and focuses on the structure and the dynamics of the rotavirus entry machinery. We survey the current models for rotavirus entry into cells.

Keywords

Structural virology Viral receptor Non-enveloped virus Rotavirus entry Structural changes Multi-layered particle Entry 

References

  1. 1.
    Lozach PY, Huotari J, Helenius A (2011) Late-penetrating viruses. Curr Opin Virol 1(1):35–43.  https://doi.org/10.1016/j.coviro.2011.05.004 CrossRefPubMedGoogle Scholar
  2. 2.
    Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124(4):729–740PubMedGoogle Scholar
  3. 3.
    Yamauchi Y, Greber UF (2016) Principles of virus uncoating: cues and the snooker ball. Traffic 17(6):569–592.  https://doi.org/10.1111/tra.12387 CrossRefPubMedGoogle Scholar
  4. 4.
    Burckhardt CJ, Greber UF (2009) Virus movements on the plasma membrane support infection and transmission between cells. PLoS Pathog 5(11):e1000621.  https://doi.org/10.1371/journal.ppat.1000621 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Greber UF (2002) Signalling in viral entry. Cell Mol Life Sci 59(4):608–626PubMedGoogle Scholar
  6. 6.
    Luisoni S, Greber UF (2016) Biology of adenovirus cell entry – receptors, pathways, mechanism. In: Curiel D (ed) Adenoviral vectors for gene therapy, 2nd edn. Academic, London, pp 27–58Google Scholar
  7. 7.
    Sieczkarski SB, Whittaker GR (2005) Viral entry. Curr Top Microbiol Immunol 285:1–23PubMedGoogle Scholar
  8. 8.
    Harrison SC (2005) Mechanism of membrane fusion by viral envelope proteins. Adv Virus Res 64:231–261.  https://doi.org/10.1016/S0065-3527(05)64007-9 CrossRefPubMedGoogle Scholar
  9. 9.
    Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4(1):67–76.  https://doi.org/10.1038/nrmicro1326 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Mas V, Melero JA (2013) Entry of enveloped viruses into host cells: membrane fusion. Subcell Biochem 68:467–487PubMedGoogle Scholar
  11. 11.
    Suomalainen M, Greber UF (2013) Uncoating of non-enveloped viruses. Curr Opin Virol 3(1):27–33.  https://doi.org/10.1016/j.coviro.2012.12.004 CrossRefPubMedGoogle Scholar
  12. 12.
    Mertens P (2004) The dsRNA viruses. Virus Res 101(1):3–13PubMedGoogle Scholar
  13. 13.
    Desselberger U (2014) Rotaviruses. Virus Res 190:75–96.  https://doi.org/10.1016/j.virusres.2014.06.016 CrossRefPubMedGoogle Scholar
  14. 14.
    Trask SD, McDonald SM, Patton JT (2012) Structural insights into the coupling of virion assembly and rotavirus replication. Nat Rev Microbiol 10(3):165–177.  https://doi.org/10.1038/nrmicro2673. nrmicro2673 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Estes MK, Greenberg HB (2013) Rotaviruses. In: Knipe DM, Howley PM, Cohen JI et al (eds) Fields virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, p 1Google Scholar
  16. 16.
    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(5933):1444–1447PubMedPubMedCentralGoogle Scholar
  17. 17.
    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.  https://doi.org/10.1016/j.jmb.2007.01.028 CrossRefPubMedGoogle Scholar
  18. 18.
    Chen JZ, Settembre EC, Aoki ST, Zhang X, Bellamy AR, Dormitzer PR, Harrison SC, Grigorieff N (2009) Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc Natl Acad Sci USA 106(26):10644–10648PubMedGoogle Scholar
  19. 19.
    Dormitzer PR, Nason EB, Prasad BV, Harrison SC (2004) Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430(7003):1053–1058PubMedPubMedCentralGoogle Scholar
  20. 20.
    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(5):885–897PubMedPubMedCentralGoogle Scholar
  21. 21.
    Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, Le Pendu J, Estes MK, Prasad BV (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485(7397):256–259.  https://doi.org/10.1038/nature10996 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hu L, Ramani S, Czako R, Sankaran B, Yu Y, Smith DF, Cummings RD, Estes MK, Venkataram Prasad BV (2015) Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus. Nat Commun 6:8346.  https://doi.org/10.1038/ncomms9346 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Liu Y, Xu S, Woodruff AL, Xia M, Tan M, Kennedy MA, Jiang X (2017) Structural basis of glycan specificity of P[19] VP8*: implications for rotavirus zoonosis and evolution. PLoS Pathog 13(11):e1006707.  https://doi.org/10.1371/journal.ppat.1006707 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    McClain B, Settembre E, Temple BR, Bellamy AR, Harrison SC (2010) X-ray crystal structure of the rotavirus inner capsid particle at 3.8 A resolution. J Mol Biol 397(2):587–599.  https://doi.org/10.1016/j.jmb.2010.01.055. S0022-2836(10)00110-5 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Prasad BV, Wang GJ, Clerx JP, Chiu W (1988) Three-dimensional structure of rotavirus. J Mol Biol 199(2):269–275PubMedGoogle Scholar
  26. 26.
    Settembre EC, Chen JZ, Dormitzer PR, Grigorieff N, Harrison SC (2011) Atomic model of an infectious rotavirus particle. EMBO J 30(2):408–416.  https://doi.org/10.1038/emboj.2010.322. emboj2010322 [pii]CrossRefPubMedGoogle Scholar
  27. 27.
    Yeager M, Dryden K, Olson N, Greenberg H, Baker T (1990) Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J Cell Biol 110(6):2133–2144PubMedGoogle Scholar
  28. 28.
    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.  https://doi.org/10.1073/pnas.0711623105. 0711623105 [pii]CrossRefPubMedGoogle Scholar
  29. 29.
    Collaborators GBDDD (2017) Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis 17(9):909–948.  https://doi.org/10.1016/S1473-3099(17)30276-1 CrossRefGoogle Scholar
  30. 30.
    Roy P (2013) Orbiviruses. In: Knipe DM, Howley PM, Cohen JI et al (eds) Fields virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, p 1Google Scholar
  31. 31.
    Dermody TS, Parker JS, Sherry B (2013) Orthoreoviruses. In: Knipe DM, Howley PM, Cohen JI et al (eds) Fields virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, p 1Google Scholar
  32. 32.
    King A, Lefkowitz EJ, Adams MJ, Carstens EB (eds) (2011) Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Academic, San DiegoGoogle Scholar
  33. 33.
    Pesavento JB, Crawford SE, Estes MK, Prasad BV (2006) Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 309:189–219PubMedGoogle Scholar
  34. 34.
    Estrozi LF, Settembre EC, Goret G, McClain B, Zhang X, Chen JZ, Grigorieff N, Harrison SC (2013) Location of the dsRNA-dependent polymerase, VP1, in rotavirus particles. J Mol Biol 425(1):124–132PubMedGoogle Scholar
  35. 35.
    Flewett TH, Bryden AS, Davies H, Woode GN, Bridger JC, Derrick JM (1974) Relation between viruses from acute gastroenteritis of children and newborn calves. Lancet 2(7872):61–63PubMedGoogle Scholar
  36. 36.
    Arnold MM, Sen A, Greenberg HB, Patton JT (2013) The battle between rotavirus and its host for control of the interferon signaling pathway. PLoS Pathog 9(1):e1003064.  https://doi.org/10.1371/journal.ppat.1003064 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Patton JT, Chen D (1999) RNA-binding and capping activities of proteins in rotavirus open cores. J Virol 73(2):1382–1391PubMedPubMedCentralGoogle Scholar
  38. 38.
    Periz J, Celma C, Jing B, Pinkney JN, Roy P, Kapanidis AN (2013) Rotavirus mRNAS are released by transcript-specific channels in the double-layered viral capsid. Proc Natl Acad Sci USA 110(29):12042–12047PubMedGoogle Scholar
  39. 39.
    McDonald SM, Patton JT (2011) Rotavirus VP2 core shell regions critical for viral polymerase activation. J Virol 85(7):3095–3105.  https://doi.org/10.1128/JVI.02360-10 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    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):2313–2320PubMedPubMedCentralGoogle Scholar
  41. 41.
    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):283–295PubMedPubMedCentralGoogle Scholar
  42. 42.
    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):1485–1497PubMedPubMedCentralGoogle Scholar
  43. 43.
    Zhang X, Jin L, Fang Q, Hui WH, Zhou ZH (2010) 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 141(3):472–482.  https://doi.org/10.1016/j.cell.2010.03.041. S0092-8674(10)00360-0 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Dormitzer PR, Greenberg HB, Harrison SC (2000) Purified recombinant rotavirus VP7 forms soluble, calcium-dependent trimers. Virology 277(2):420–428PubMedGoogle Scholar
  45. 45.
    Cohen J, Laporte J, Charpilienne A, Scherrer R (1979) Activation of rotavirus RNA polymerase by calcium chelation. Arch Virol 60(3–4):177–186PubMedGoogle Scholar
  46. 46.
    Trask SD, Dormitzer PR (2006) Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J Virol 80(22):11293–11304PubMedPubMedCentralGoogle Scholar
  47. 47.
    Chen DY, Ramig RF (1992) Determinants of rotavirus stability and density during CsCl purification. Virology 186(1):228–237PubMedGoogle Scholar
  48. 48.
    Rodriguez JM, Chichon FJ, Martin-Forero E, Gonzalez-Camacho F, Carrascosa JL, Caston JR, Luque D (2014) New insights into rotavirus entry machinery: stabilization of rotavirus spike conformation is independent of trypsin cleavage. PLoS Pathog 10(5):e1004157.  https://doi.org/10.1371/journal.ppat.1004157 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Prasad BV, Chiu W (1994) Structure of rotavirus. Curr Top Microbiol Immunol 185:9–29PubMedGoogle Scholar
  50. 50.
    Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Banyai K, Estes MK, Gentsch JR, Iturriza-Gomara M, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Patton JT, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Desselberger U, Van Ranst M (2008) Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153(8):1621–1629.  https://doi.org/10.1007/s00705-008-0155-1 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Dormitzer PR, Greenberg HB (1992) Calcium chelation induces a conformational change in recombinant herpes simplex virus-1-expressed rotavirus VP7. Virology 189(2):828–832PubMedGoogle Scholar
  52. 52.
    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(10):5389–5394PubMedGoogle Scholar
  53. 53.
    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):9969–9978PubMedPubMedCentralGoogle Scholar
  54. 54.
    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.  https://doi.org/10.1073/pnas.250299897 CrossRefPubMedGoogle Scholar
  55. 55.
    Hewish MJ, Takada Y, Coulson BS (2000) Integrins alpha2beta1 and alpha4beta1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74(1):228–236PubMedPubMedCentralGoogle Scholar
  56. 56.
    Ludert JE, Ruiz MC, Hidalgo C, Liprandi F (2002) Antibodies to rotavirus outer capsid glycoprotein VP7 neutralize infectivity by inhibiting virion decapsidation. J Virol 76(13):6643–6651PubMedPubMedCentralGoogle Scholar
  57. 57.
    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.  https://doi.org/10.1099/0022-1317-78-6-1367 CrossRefPubMedGoogle Scholar
  58. 58.
    Elaid S, Libersou S, Ouldali M, Morellet N, Desbat B, Alves ID, Lepault J, Bouaziz S (2014) A peptide derived from the rotavirus outer capsid protein VP7 permeabilizes artificial membranes. Biochim Biophys Acta 1838(8):2026–2035.  https://doi.org/10.1016/j.bbamem.2014.04.005 CrossRefPubMedGoogle Scholar
  59. 59.
    Clark SM, Roth JR, Clark ML, Barnett BB, Spendlove RS (1981) Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J Virol 39(3):816–822PubMedPubMedCentralGoogle Scholar
  60. 60.
    Estes MK, Graham DY, Mason BB (1981) Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J Virol 39(3):879–888PubMedPubMedCentralGoogle Scholar
  61. 61.
    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.  https://doi.org/10.1099/0022-1317-77-3-391 CrossRefPubMedGoogle Scholar
  62. 62.
    Li Z, Baker ML, Jiang W, Estes MK, Prasad BV (2009) Rotavirus architecture at subnanometer resolution. J Virol 83(4):1754–1766.  https://doi.org/10.1128/JVI.01855-08. JVI.01855-08 [pii]CrossRefPubMedGoogle Scholar
  63. 63.
    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(12):6200–6207PubMedPubMedCentralGoogle Scholar
  64. 64.
    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.  https://doi.org/10.1006/jmbi.2000.5238 CrossRefPubMedGoogle Scholar
  65. 65.
    Yoder JD, Dormitzer PR (2006) Alternative intermolecular contacts underlie the rotavirus VP5* two- to three-fold rearrangement. EMBO J 25(7):1559–1568.  https://doi.org/10.1038/sj.emboj.7601034 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Arias CF, Romero P, Alvarez V, Lopez S (1996) Trypsin activation pathway of rotavirus infectivity. J Virol 70(9):5832–5839PubMedPubMedCentralGoogle Scholar
  67. 67.
    Gilbert JM, Greenberg HB (1998) Cleavage of rhesus rotavirus VP4 after arginine 247 is essential for rotavirus-like particle-induced fusion from without. J Virol 72(6):5323–5327PubMedPubMedCentralGoogle Scholar
  68. 68.
    Komoto S, Wakuda M, Ide T, Niimi G, Maeno Y, Higo-Moriguchi K, Taniguchi K (2011) Modification of the trypsin cleavage site of rotavirus VP4 to a furin-sensitive form does not enhance replication efficiency. J Gen Virol 92(Pt 12):2914–2921PubMedGoogle Scholar
  69. 69.
    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):6052–6061PubMedPubMedCentralGoogle Scholar
  70. 70.
    Trask SD, Kim IS, Harrison SC, Dormitzer PR (2010) A rotavirus spike protein conformational intermediate binds lipid bilayers. J Virol 84(4):1764–1770PubMedGoogle Scholar
  71. 71.
    Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15(7):690–698PubMedPubMedCentralGoogle Scholar
  72. 72.
    Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, Wiley DC (1998) Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95(3):409–417PubMedGoogle Scholar
  73. 73.
    Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289(5796):366–373Google Scholar
  74. 74.
    Welch BD, Liu Y, Kors CA, Leser GP, Jardetzky TS, Lamb RA (2012) Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc Natl Acad Sci USA 109(41):16672–16677PubMedGoogle Scholar
  75. 75.
    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):1136–1144PubMedPubMedCentralGoogle Scholar
  76. 76.
    Abdelhakim AH, Salgado EN, Fu X, Pasham M, Nicastro D, Kirchhausen T, Harrison SC (2014) Structural correlates of rotavirus cell entry. PLoS Pathog 10(9):e1004355.  https://doi.org/10.1371/journal.ppat.1004355 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Arias CF, Silva-Ayala D, Lopez S (2015) Rotavirus entry: a deep journey into the cell with several exits. J Virol 89(2):890–893.  https://doi.org/10.1128/JVI.01787-14 CrossRefPubMedGoogle Scholar
  78. 78.
    Baker M, Prasad BV (2010) Rotavirus cell entry. Curr Top Microbiol Immunol 343:121–148.  https://doi.org/10.1007/82_2010_34 CrossRefPubMedGoogle Scholar
  79. 79.
    Lopez S, Arias CF (2004) Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12(6):271–278PubMedGoogle Scholar
  80. 80.
    Lopez S, Arias CF (2006) Early steps in rotavirus cell entry. Curr Top Microbiol Immunol 309:39–66PubMedGoogle Scholar
  81. 81.
    Zarate S, Espinosa R, Romero P, Guerrero CA, Arias CF, Lopez S (2000) Integrin alpha2beta1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278(1):50–54.  https://doi.org/10.1006/viro.2000.0660 CrossRefPubMedGoogle Scholar
  82. 82.
    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):4096–4102PubMedPubMedCentralGoogle Scholar
  83. 83.
    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.  https://doi.org/10.1128/JVI.78.20.10839-10847.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Fleming FE, Graham KL, Takada Y, Coulson BS (2011) Determinants of the specificity of rotavirus interactions with the alpha2beta1 integrin. J Biol Chem 286(8):6165–6174.  https://doi.org/10.1074/jbc.M110.142992 CrossRefPubMedGoogle Scholar
  85. 85.
    Jolly CL, Huang JA, Holmes IH (2001) Selection of rotavirus VP4 cell receptor binding domains for MA104 cells using a phage display library. J Virol Methods 98(1):41–51PubMedGoogle Scholar
  86. 86.
    Ramani S, Hu L, Venkataram Prasad BV, Estes MK (2016) Diversity in rotavirus-host glycan interactions: a “sweet” spectrum. Cell Mol Gastroenterol Hepatol 2(3):263–273.  https://doi.org/10.1016/j.jcmgh.2016.03.002 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Venkataram Prasad BV, Shanker S, Hu L, Choi JM, Crawford SE, Ramani S, Czako R, Atmar RL, Estes MK (2014) Structural basis of glycan interaction in gastroenteric viral pathogens. Curr Opin Virol 7:119–127.  https://doi.org/10.1016/j.coviro.2014.05.008 CrossRefPubMedGoogle Scholar
  88. 88.
    Varki A, Schnaar RL, Schauer R (2015) Sialic acids and other nonulosonic acids. In: rd VA, Cummings RD et al (eds) Essentials of glycobiology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 179–195.  https://doi.org/10.1101/glycobiology.3e.015 CrossRefGoogle Scholar
  89. 89.
    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.  https://doi.org/10.1099/0022-1317-80-4-943 CrossRefPubMedGoogle Scholar
  90. 90.
    Kraschnefski MJ, Scott SA, Holloway G, Coulson BS, von Itzstein M, Blanchard H (2005) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of the VP8* carbohydrate-binding protein of the human rotavirus strain Wa. Acta Crystallogr Sect F Struct Biol Cryst Commun 61(11):989–993.  https://doi.org/10.1107/S1744309105032999 CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Yu X, Guillon A, Szyczew AJ, Kiefel MJ, Coulson BS, von Itzstein M, Blanchard H (2008) Crystallization and preliminary X-ray diffraction analysis of the carbohydrate-recognizing domain (VP8*) of bovine rotavirus strain NCDV. Acta Crystallogr Sect F Struct Biol Cryst Commun 64(6):509–511.  https://doi.org/10.1107/S1744309108011949 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Ciarlet M, Ludert JE, Iturriza-Gomara M, Liprandi F, Gray JJ, Desselberger U, Estes MK (2002) Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J Virol 76(8):4087–4095PubMedPubMedCentralGoogle Scholar
  93. 93.
    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.  https://doi.org/10.1038/nchembio.134 CrossRefPubMedGoogle Scholar
  94. 94.
    Bohm R, Fleming FE, Maggioni A, Dang VT, Holloway G, Coulson BS, von Itzstein M, Haselhorst T (2015) Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat Commun 6:5907.  https://doi.org/10.1038/ncomms6907 CrossRefPubMedGoogle Scholar
  95. 95.
    Huang P, Xia M, Tan M, Zhong W, Wei C, Wang L, Morrow A, Jiang X (2012) Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J Virol 86(9):4833–4843.  https://doi.org/10.1128/JVI.05507-11 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Liu Y, Huang P, Jiang B, Tan M, Morrow AL, Jiang X (2013) Poly-LacNAc as an age-specific ligand for rotavirus P[11] in neonates and infants. PLoS One 8(11):e78113.  https://doi.org/10.1371/journal.pone.0078113 CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Liu Y, Huang P, Tan M, Liu Y, Biesiada J, Meller J, Castello AA, Jiang B, Jiang X (2012) Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. J Virol 86(18):9899–9910.  https://doi.org/10.1128/JVI.00979-12 CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Ramani S, Cortes-Penfield NW, Hu L, Crawford SE, Czako R, Smith DF, Kang G, Ramig RF, Le Pendu J, Prasad BV, Estes MK (2013) The VP8* domain of neonatal rotavirus strain G10P[11] binds to type II precursor glycans. J Virol 87(13):7255–7264.  https://doi.org/10.1128/JVI.03518-12 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Yu Y, Lasanajak Y, Song X, Hu L, Ramani S, Mickum ML, Ashline DJ, Prasad BV, Estes MK, Reinhold VN, Cummings RD, Smith DF (2014) Human milk contains novel glycans that are potential decoy receptors for neonatal rotaviruses. Mol Cell Proteomics 13(11):2944–2960.  https://doi.org/10.1074/mcp.M114.039875 CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Marionneau S, Cailleau-Thomas A, Rocher J, Le Moullac-Vaidye B, Ruvoen N, Clement M, Le Pendu J (2001) ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83(7):565–573PubMedGoogle Scholar
  101. 101.
    Yu X, Mishra R, Holloway G, von Itzstein M, Coulson BS, Blanchard H (2015) Substantial receptor-induced structural rearrangement of rotavirus VP8*: potential implications for cross-species infection. Chembiochem 16(15):2176–2181.  https://doi.org/10.1002/cbic.201500360 CrossRefPubMedGoogle Scholar
  102. 102.
    Martinez MA, Lopez S, Arias CF, Isa P (2013) Gangliosides have a functional role during rotavirus cell entry. J Virol 87(2):1115–1122.  https://doi.org/10.1128/JVI.01964-12 CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Torres-Flores JM, Silva-Ayala D, Espinoza MA, Lopez S, Arias CF (2015) The tight junction protein JAM-A functions as coreceptor for rotavirus entry into MA104 cells. Virology 475:172–178.  https://doi.org/10.1016/j.virol.2014.11.016 CrossRefPubMedGoogle Scholar
  104. 104.
    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(8):4389–4402.  https://doi.org/10.1128/JVI.03457-13 CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Gutierrez M, Isa P, Sanchez-San Martin C, Perez-Vargas J, Espinosa R, Arias CF, Lopez S (2010) Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis. J Virol 84(18):9161–9169.  https://doi.org/10.1128/JVI.00731-10 CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Sanchez-San Martin C, Lopez T, Arias CF, Lopez S (2004) Characterization of rotavirus cell entry. J Virol 78(5):2310–2318PubMedPubMedCentralGoogle Scholar
  107. 107.
    Silva-Ayala D, Lopez T, Gutierrez M, Perrimon N, Lopez S, Arias CF (2013) Genome-wide RNAi screen reveals a role for the ESCRT complex in rotavirus cell entry. Proc Natl Acad Sci USA 110(25):10270–10275.  https://doi.org/10.1073/pnas.1304932110 CrossRefPubMedGoogle Scholar
  108. 108.
    Diaz-Salinas MA, Romero P, Espinosa R, Hoshino Y, Lopez S, Arias CF (2013) The spike protein VP4 defines the endocytic pathway used by rotavirus to enter MA104 cells. J Virol 87(3):1658–1663.  https://doi.org/10.1128/JVI.02086-12 CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Fleming FE, Bohm R, Dang VT, Holloway G, Haselhorst T, Madge PD, Deveryshetty J, Yu X, Blanchard H, von Itzstein M, Coulson BS (2014) Relative roles of GM1 ganglioside, N-acylneuraminic acids, and alpha2beta1 integrin in mediating rotavirus infection. J Virol 88(8):4558–4571.  https://doi.org/10.1128/JVI.03431-13 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Li B, Ding S, Feng N, Mooney N, Ooi YS, Ren L, Diep J, Kelly MR, Yasukawa LL, Patton JT, Yamazaki H, Shirao T, Jackson PK, Greenberg HB (2017) Drebrin restricts rotavirus entry by inhibiting dynamin-mediated endocytosis. Proc Natl Acad Sci USA 114(18):E3642–E3651.  https://doi.org/10.1073/pnas.1619266114 CrossRefPubMedGoogle Scholar
  111. 111.
    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(7):4009–4013.  https://doi.org/10.1128/JVI.06667-11 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Soliman M, Seo JY, Kim DS, Kim JY, Park JG, Alfajaro MM, Baek YB, Cho EH, Kwon J, Choi JS, Kang MI, Park SI, Cho KO (2018) Activation of PI3K, Akt, and ERK during early rotavirus infection leads to V-ATPase-dependent endosomal acidification required for uncoating. PLoS Pathog 14(1):e1006820.  https://doi.org/10.1371/journal.ppat.1006820 CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    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(6):2492–2503PubMedGoogle Scholar
  114. 114.
    Yoder JD, Trask SD, Vo TP, Binka M, Feng N, Harrison SC, Greenberg HB, Dormitzer PR (2009) VP5* rearranges when rotavirus uncoats. J Virol 83(21):11372–11377.  https://doi.org/10.1128/JVI.01228-09 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Centro Nacional de Microbiología/ISCIIIMadridSpain

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