Calcium-Dependent Rubella Virus Fusion Occurs in Early Endosomes

Journal of Virology

Volumn 90, Issue 14, 2016, Pages 6303-6313

  Dubé, Mathieu ^a,b   Etienne, Loïc ^a   Fels, Maximilian ^a   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL PROTEIN; GLYCOPROTEIN E1; LIPOSOME; VIRUS FUSION PROTEIN;

ARTICLE; CALCIUM BINDING; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; CHELATION; CONTROLLED STUDY; ENDOSOME; LIPOSOME MEMBRANE; MOLECULAR INTERACTION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN REFOLDING; RESIDUE ANALYSIS; RUBELLA VIRUS; VIRUS CELL INTERACTION; VIRUS ENTRY; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; GENETICS; MEMBRANE FUSION; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN CONFORMATION; RUBELLA; VERO CELL LINE; VIROLOGY; VIRUS ASSEMBLY;

ANIMALS; CALCIUM; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; ENDOSOMES; HYDROGEN-ION CONCENTRATION; LIPOSOMES; MEMBRANE FUSION; MUTATION; PROTEIN CONFORMATION; RUBELLA; RUBELLA VIRUS; VERO CELLS; VIRAL FUSION PROTEINS; VIRUS ASSEMBLY; VIRUS INTERNALIZATION;

EID: 84977553601     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00634-16     Document Type: Article

References (57)

1. Hobman TC. 2013. Rubella virus, p 687-711. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Lee JY, Bowden DS. 2000. Rubella virus replication and links to teratogenicity. Clin Microbiol Rev 13:571-587. http://dx.doi.org/10.1128/CMR.13.4.571-587.2000.
3. Frey TK. 1994. Molecular biology of rubella virus. Adv Virus Res 44:69-160. http://dx.doi.org/10.1016/S0065-3527(08)60328-0.
4. Cooper LZ. 1985. The history and medical consequences of rubella. Rev Infect Dis 7(Suppl 1):S2-S10. http://dx.doi.org/10.1093/clinids/7.Supplement_1.S2.
5. WHO. 2015. Rubella fact sheet no. 367. WHO, Geneva, Switzerland.
6. Andrus JK, de Quadros CA, Solorzano CC, Periago MR, Henderson DA. 2011. Measles and rubella eradication in the Americas. Vaccine 29(Suppl 4):D91-D96. http://dx.doi.org/10.1016/j.vaccine.2011.04.059.
7. Kuhn RJ. 2013. Togaviridae, p 629-650. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
8. Kee SH, Cho EJ, Song JW, Park KS, Baek LJ, Song KJ. 2004. Effects of endocytosis inhibitory drugs on rubella virus entry into VeroE6 cells. Microbiol Immunol 48:823-829. http://dx.doi.org/10.1111/j.1348-0421.2004.tb03614.x.
9. Petruzziello R, Orsi N, Macchia S, Rieti S, Frey TK, Mastromarino P. 1996. Pathway of rubella virus infectious entry into Vero cells. J Gen Virol 77:303-308. http://dx.doi.org/10.1099/0022-1317-77-2-303.
10. Katow S, Sugiura A. 1988. Low pH-induced conformational change of rubella virus envelope proteins. J Gen Virol 69:2797-2807. http://dx.doi.org/10.1099/0022-1317-69-11-2797.
11. Battisti AJ, Yoder JD, Plevka P, Winkler DC, Prasad VM, Kuhn RJ, Frey TK, Steven AC, Rossmann MG. 2012. Cryo-electron tomography of rubella virus. J Virol 86:11078 -11085. http://dx.doi.org/10.1128/JVI.01390-12.
12. Mangala Prasad V, Willows SD, Fokine A, Battisti AJ, Sun S, Plevka P, Hobman TC, Rossmann MG. 2013. Rubella virus capsid protein structure and its role in virus assembly and infection. Proc Natl Acad Sci U S A 110:20105-20110. http://dx.doi.org/10.1073/pnas.1316681110.
13. Katow S, Sugiura A. 1985. Antibody response to individual rubella virus proteins in congenital and other rubella virus infections. J Clin Microbiol 21:449-451.
14. Waxham MN, Wolinsky JS. 1985. A model of the structural organization of rubella virions. Rev Infect Dis 7(Suppl 1):S133-S139. http://dx.doi.org/10.1093/clinids/7.Supplement_1.S133.
15. Cong H, Jiang Y, Tien P. 2011. Identification of the myelin oligodendrocyte glycoprotein as a cellular receptor for rubella virus. J Virol 85:11038-11047. http://dx.doi.org/10.1128/JVI.05398-11.
16. Qiu Z, Yao J, Cao H, Gillam S. 2000. Mutations in the E1 hydrophobic domain of rubella virus impair virus infectivity but not virus assembly. J Virol 74:6637- 6642. http://dx.doi.org/10.1128/JVI.74.14.6637-6642.2000.
17. DuBois RM, Vaney MC, Tortorici MA, Kurdi RA, Barba-Spaeth G, Krey T, Rey FA. 2013. Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature 493:552-556. http://dx.doi.org/10.1038/nature11741.
18. Dube M, Rey FA, Kielian M. 2014. Rubella virus: first calcium-requiring viral fusion protein. PLoS Pathog 10:e1004530. http://dx.doi.org/10.1371/journal.ppat.1004530.
19. Kielian M. 2014. Mechanisms of virus membrane fusion proteins. Annu Rev Virol 1:171-189. http://dx.doi.org/10.1146/annurev-virology-031413-085521.
20. Harrison SC. 2015. Viral membrane fusion. Virology 479-480:498-507. http://dx.doi.org/10.1016/j.virol.2015.03.043.
21. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM. 2008. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15:1024-1030. http://dx.doi.org/10.1038/nsmb.1484.
22. Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220. http://dx.doi.org/10.1126/science.1126548.
23. Roche S, Bressanelli S, Rey FA, Gaudin Y. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191. http://dx.doi.org/10.1126/science.1127683.
24. Yao J, Gillam S. 1999. Mutational analysis, using a full-length rubella virus cDNA clone, of rubella virus E1 transmembrane and cytoplasmic domains required for virus release. J Virol 73:4622-4630.
25. Glomb-Reinmund S, Kielian M. 1998. fus-1, a pH shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J Virol 72:4281-4287.
26. Liljestrom P, Lusa S, Huylebroeck D, Garoff H. 1991. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J Virol 65:4107-4113.
27. Zheng A, Umashankar M, Kielian M. 2010. In vitro and in vivo studies identify important features of dengue virus pr-E protein interactions. PLoS Pathog 6:e1001157. http://dx.doi.org/10.1371/journal.ppat.1001157.
28. Kielian M, Jungerwirth S, Sayad KU, DeCandido S. 1990. Biosynthesis, maturation, and acid activation of the Semliki Forest virus fusion protein. J Virol 64:4614-4624.
29. Stiasny K, Kiermayr S, Holzmann H, Heinz FX. 2006. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J Virol 80:9557-9568. http://dx.doi.org/10.1128/JVI.00080-06.
30. Chatterjee PK, Vashishtha M, Kielian M. 2000. Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion. J Virol 74:1623-1631. http://dx.doi.org/10.1128/JVI.74.4.1623-1631.2000.
31. Chanel-Vos C, Kielian M. 2004. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J Virol 78:13543-13552. http://dx.doi.org/10.1128/JVI.78.24.13543-13552.2004.
32. Ooi YS, Stiles KM, Liu CY, Taylor GM, Kielian M. 2013. Genome-wide RNAiscreen identifies novel host proteins required for alphavirus entry. PLoS Pathog 9:e1003835. http://dx.doi.org/10.1371/journal.ppat.1003835.
33. Feng Y, Press B, Wandinger-Ness A. 1995. Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131:1435-1452. http://dx.doi.org/10.1083/jcb.131.6.1435.
34. Ho YP, Yang MW, Chen LT, Yang YC. 2007. Relative calcium-binding strengths of amino acids determined using the kinetic method. Rapid Commun Mass Spectrom 21:1083-1089. http://dx.doi.org/10.1002/rcm.2927.
35. Kuo W, Herrick DZ, Ellena JF, Cafiso DS. 2009. The calcium-dependent and calcium-independent membrane binding of synaptotagmin 1: two modes of C2B binding. J Mol Biol 387:284-294. http://dx.doi.org/10.1016/j.jmb.2009.01.064.
36. DeKruyff RH, Bu X, Ballesteros A, Santiago C, Chim YL, Lee HH, Karisola P, Pichavant M, Kaplan GG, Umetsu DT, Freeman GJ, Casasnovas JM. 2010. T cell/transmembrane, Ig, and mucin-3 allelic variants differentially recognize phosphatidylserine and mediate phagocytosis of apoptotic cells. J Immunol 184:1918-1930. http://dx.doi.org/10.4049/jimmunol.0903059.
37. Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Kobayashi T, Gruenberg J. 2002. Separation and characterization of late endosomal membrane domains. J Biol Chem 277:32157-32164. http://dx.doi.org/10.1074/jbc.M202838200.
38. Umashankar M, Sanchez-San Martin C, Liao M, Reilly B, Guo A, Taylor G, Kielian M. 2008. Differential cholesterol binding by class II fusion proteins determines membrane fusion properties. J Virol 82:9245-9253. http://dx.doi.org/10.1128/JVI.00975-08.
39. + chelators. J Cereb Blood Flow Metab 14:911-923. http://dx.doi.org/10.1038/jcbfm.1994.122.
40. Tsien RY. 1981. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527-528. http://dx.doi.org/10.1038/290527a0.
41. Tsien RY. 1980. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19:2396-2404. http://dx.doi.org/10.1021/bi00552a018.
42. Mercer J, Schelhaas M, Helenius A. 2010. Virus entry by endocytosis. Annu Rev Biochem 79:803-833. http://dx.doi.org/10.1146/annurev-biochem-060208-104626.
43. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, Zerial M. 1994. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13:1287-1296.
44. Sieczkarski SB, Whittaker GR. 2003. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333-343. http://dx.doi.org/10.1034/j.1600-0854.2003.00090.x.
45. Zaitseva E, Yang ST, Melikov K, Pourmal S, Chernomordik LV. 2010. Dengue virus ensures its fusion in late endosomes using compartmentspecific lipids. PLoS Pathog 6:e1001131. http://dx.doi.org/10.1371/journal.ppat.1001131.
46. Gerasimenko JV, Tepikin AV, Petersen OH, Gerasimenko OV. 1998. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol 8:1335-1338. http://dx.doi.org/10.1016/S0960-9822(07)00565-9.
47. Cheung G, Cousin MA. 2013. Synaptic vesicle generation from activitydependent bulk endosomes requires calcium and calcineurin. J Neurosci 33:3370-3379. http://dx.doi.org/10.1523/JNEUROSCI.4697-12.2013.
48. Leventis PA, Grinstein S. 2010. The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407-427. http://dx.doi.org/10.1146/annurev.biophys.093008.131234.
49. van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112-124. http://dx.doi.org/10.1038/nrm2330.
50. Richard AS, Zhang A, Park SJ, Farzan M, Zong M, Choe H. 2015. Virion-associated phosphatidylethanolamine promotes TIM1-mediated infection by Ebola, dengue, and West Nile viruses. Proc Natl Acad Sci U S A 112:14682-14687. http://dx.doi.org/10.1073/pnas.1508095112.
51. Nalefski EA, Falke JJ. 1996. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375-2390. http://dx.doi.org/10.1002/pro.5560051201.
52. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709-712. http://dx.doi.org/10.1038/nature09555.
53. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708. http://dx.doi.org/10.1038/nature09546.
54. Wallin M, Ekstrom M, Garoff H. 2004. Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J 23:54-65. http://dx.doi.org/10.1038/sj.emboj.7600012.
55. Haynes JI, II, Chang D, Consigli RA. 1993. Mutations in the putative calcium-binding domain of polyomavirus VP1 affect capsid assembly. J Virol 67:2486-2495.
56. Dormitzer PR, Greenberg HB, Harrison SC. 2000. Purified recombinant rotavirus VP7 forms soluble, calcium-dependent trimers. Virology 277: 420-428. http://dx.doi.org/10.1006/viro.2000.0625.
57. DeLano WL. 2002. The PyMOL user's manual. DeLano Scientific, San Carlos, CA.