Mutational analysis of Lassa virus glycoprotein highlights regions required for alpha-dystroglycan utilization

Journal of Virology

Volumn 91, Issue 18, 2017, Pages

  Acciani, Marissa ^a   Alston, Jacob T ^a   Zhao, Guohui ^a   Reynolds, Hayley ^a   Ali, Afroze M ^a   Xu, Brian ^a   Brindley, Melinda A ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Arenavirus; Receptor binding; Virus entry

Indexed keywords

DYSTROGLYCAN; GLYCOPROTEIN GP1, LASSA VIRUS; LAMP1 PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MUTANT PROTEIN; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR;

CELL LINE; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; HUMAN; LASSA VIRUS; METABOLISM; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; VESICULOVIRUS; VIRUS ENTRY;

CELL LINE; DNA MUTATIONAL ANALYSIS; DYSTROGLYCANS; HUMANS; LASSA VIRUS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MUTAGENESIS, INSERTIONAL; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; RECEPTORS, VIRUS; RECOMBINANT PROTEINS; TRANSDUCTION, GENETIC; VESICULOVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 85028312482     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00574-17     Document Type: Article

References (59)

1. Frame JD, Baldwin JM, Jr, Gocke DJ, Troup JM. 1970. Lassa fever, a new virus disease of man from West Africa. I. Clinical description and pathological findings. Am J Trop Med Hyg 19:670-676
2. Gunther S, Lenz O. 2004. Lassa virus. Crit Rev Clin Lab Sci 41:339-390. https://doi.org/10.1080/10408360490497456
3. Mofolorunsho KC. 2016. Outbreak of lassa fever in Nigeria: measures for prevention and control. Pan Afr Med J 23:210. https://doi.org/10.11604/ pamj.2016.23.210.8923
4. Fichet-Calvet E, Rogers DJ. 2009. Risk maps of Lassa fever in West Africa. PLoS Negl Trop Dis 3:e388. https://doi.org/10.1371/journal.pntd.0000388
5. Ogbu O, Ajuluchukwu E, Uneke CJ. 2007. Lassa fever in West African sub-region: an overview. J Vector Borne Dis 44:1-11
6. Monath TP, Newhouse VF, Kemp GE, Setzer HW, Cacciapuoti A. 1974. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science 185:263-265. https://doi.org/10.1126/ science.185.4147.263
7. Olayemi A, Cadar D, Magassouba N, Obadare A, Kourouma F, Oyeyiola A, Fasogbon S, Igbokwe J, Rieger T, Bockholt S, Jerome H, Schmidt-Chanasit J, Garigliany M, Lorenzen S, Igbahenah F, Fichet JN, Ortsega D, Omilabu S, Gunther S, Fichet-Calvet E. 2016. New hosts of the Lassa virus. Sci Rep 6:25280. https://doi.org/10.1038/srep25280
8. Ajayi NA, Ukwaja KN, Ifebunandu NA, Nnabu R, Onwe FI, Asogun DA. 2014. Lassa fever-full recovery without ribavarin treatment: a case report. Afr Health Sci 14:1074-1077. https://doi.org/10.4314/ahs.v14i4.40
9. Yun NE, Walker DH. 2012. Pathogenesis of Lassa fever. Viruses 4:2031-2048. https://doi.org/10.3390/v4102031
10. Burri DJ, Pasqual G, Rochat C, Seidah NG, Pasquato A, Kunz S. 2012. Molecular characterization of the processing of arenavirus envelope glycoprotein precursors by subtilisin kexin isozyme-1/site-1 protease. J Virol 86:4935-4946. https://doi.org/10.1128/JVI.00024-12
11. Kunz S, Edelmann KH, de la Torre JC, Gorney R, Oldstone MB. 2003. Mechanisms for lymphocytic choriomeningitis virus glycoprotein cleavage, transport, and incorporation into virions. Virology 314:168-178. https://doi.org/10.1016/S0042-6822(03)00421-5
12. Beyer WR, Popplau D, Garten W, von Laer D, Lenz O. 2003. Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J Virol 77:2866-2872. https://doi.org/10.1128/JVI.77.5.2866-2872.2003
13. Lenz O, Ter Meulen J, Klenk HD, Seidah NG, Garten W. 2001. The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc Natl Acad Sci U S A 98:12701-12705. https://doi.org/ 10.1073/pnas.221447598
14. Bederka LH, Bonhomme CJ, Ling EL, Buchmeier MJ. 2014. Arenavirus stable signal peptide is the keystone subunit for glycoprotein complex organization. mBio 5:e02063. https://doi.org/10.1128/mBio.02063-14
15. Messina EL, York J, Nunberg JH. 2012. Dissection of the role of the stable signal peptide of the arenavirus envelope glycoprotein in membrane fusion. J Virol 86:6138-6145. https://doi.org/10.1128/JVI.07241-11
16. Eichler R, Lenz O, Strecker T, Garten W. 2003. Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length. FEBS Lett 538: 203-206. https://doi.org/10.1016/S0014-5793(03)00160-1
17. Briknarova K, Thomas CJ, York J, Nunberg JH. 2011. Structure of a zinc-binding domain in the Junin virus envelope glycoprotein. J Biol Chem 286:1528-1536. https://doi.org/10.1074/jbc.M110.166025
18. York J, Nunberg JH. 2007. A novel zinc-binding domain is essential for formation of the functional Junin virus envelope glycoprotein complex. J Virol 81:13385-13391. https://doi.org/10.1128/JVI.01785-07
19. York J, Nunberg JH. 2006. Role of the stable signal peptide of Junin arenavirus envelope glycoprotein in pH-dependent membrane fusion. J Virol 80:7775-7780. https://doi.org/10.1128/JVI.00642-06
20. Jae LT, Raaben M, Herbert AS, Kuehne AI, Wirchnianski AS, Soh TK, Stubbs SH, Janssen H, Damme M, Saftig P, Whelan SP, Dye JM, Brummelkamp TR. 2014. Virus entry. Lassa virus entry requires a triggerinduced receptor switch. Science 344:1506-1510. https://doi.org/10.1126/science.1252480
21. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, Ravkov EV, Nichol ST, Compans RW, Campbell KP, Oldstone MB. 1998. Identification of alphadystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079-2081. https://doi.org/10.1126/ science.282.5396.2079
22. Hastie KM, Igonet S, Sullivan BM, Legrand P, Zandonatti MA, Robinson JE, Garry RF, Rey FA, Oldstone MB, Saphire EO. 2016. Crystal structure of the prefusion surface glycoprotein of the prototypic arenavirus LCMV. Nat Struct Mol Biol 23:513-521. https://doi.org/10.1038/nsmb.3210
23. Igonet S, Vaney MC, Vonrhein C, Bricogne G, Stura EA, Hengartner H, Eschli B, Rey FA. 2011. X-ray structure of the arenavirus glycoprotein GP2 in its postfusion hairpin conformation. Proc Natl Acad Sci U S A 108: 19967-19972. https://doi.org/10.1073/pnas.1108910108
24. Eschli B, Quirin K, Wepf A, Weber J, Zinkernagel R, Hengartner H. 2006. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J Virol 80:5897-5907. https://doi.org/10.1128/JVI.00008-06
25. Shimojima M, Stroher U, Ebihara H, Feldmann H, Kawaoka Y. 2012. Identification of cell surface molecules involved in dystroglycanindependent Lassa virus cell entry. J Virol 86:2067-2078. https://doi.org/ 10.1128/JVI.06451-11
26. Goncalves AR, Moraz ML, Pasquato A, Helenius A, Lozach PY, Kunz S. 2013. Role of DC-SIGN in Lassa virus entry into human dendritic cells. J Virol 87:11504-11515. https://doi.org/10.1128/JVI.01893-13
27. Rojek JM, Sanchez AB, Nguyen NT, de la Torre JC, Kunz S. 2008. Different mechanisms of cell entry by human-pathogenic Old World and New World arenaviruses. J Virol 82:7677-7687. https://doi.org/10.1128/JVI.00560-08
28. Oppliger J, Torriani G, Herrador A, Kunz S. 2016. Lassa virus cell entry via dystroglycan involves an unusual pathway of macropinocytosis. J Virol https://doi.org/10.1128/JVI.00257-16
29. Nunberg JH, York J. 2012. The curious case of arenavirus entry, and its inhibition. Viruses 4:83-101. https://doi.org/10.3390/v4010083
30. Cohen-Dvashi H, Israeli H, Shani O, Katz A, Diskin R. 2016. Role of LAMP1 binding and pH sensing by the spike complex of Lassa virus. J Virol 90:10329-10338. https://doi.org/10.1128/JVI.01624-16
31. Li S, Sun Z, Pryce R, Parsy ML, Fehling SK, Schlie K, Siebert CA, Garten W, Bowden TA, Strecker T, Huiskonen JT. 2016. Acidic pH-induced confor-mations and LAMP1 binding of the Lassa virus glycoprotein spike. PLoS Pathog 12:e1005418. https://doi.org/10.1371/journal.ppat.1005418
32. Hastie KM, Zandonatti MA, Kleinfelter LM, Heinrich ML, Rowland MM, Chandran K, Branco LM, Robinson JE, Garry RF, Saphire EO. 2017. Structural basis for antibody-mediated neutralization of Lassa virus. Science 356:923-928. https://doi.org/10.1126/science.aam7260
33. Cohen-Dvashi H, Cohen N, Israeli H, Diskin R. 2015. Molecular mechanism for LAMP1 recognition by Lassa virus. J Virol 89:7584-7592. https:// doi.org/10.1128/JVI.00651-15
34. Bonhomme CJ, Capul AA, Lauron EJ, Bederka LH, Knopp KA, Buchmeier MJ. 2011. Glycosylation modulates arenavirus glycoprotein expression and function. Virology 409:223-233. https://doi.org/10.1016/j.virol.2010.10.011
35. Eichler R, Lenz O, Garten W, Strecker T. 2006. The role of single N-glycans in proteolytic processing and cell surface transport of the Lassa virus glycoprotein GP-C. Virol J 3:41. https://doi.org/10.1186/1743-422X-3-41
36. Jae LT, Raaben M, Riemersma M, van Beusekom E, Blomen VA, Velds A, Kerkhoven RM, Carette JE, Topaloglu H, Meinecke P, Wessels MW, Lefeber DJ, Whelan SP, van Bokhoven H, Brummelkamp TR. 2013. Deciphering the glycosylome of dystroglycanopathies using haploid screens for Lassa virus entry. Science 340:479-483. https://doi.org/10.1126/science.1233675
37. Gallagher P, Henneberry J, Wilson I, Sambrook J, Gething MJ. 1988. Addition of carbohydrate side chains at novel sites on influenza virus hemagglutinin can modulate the folding, transport, and activity of the molecule. J Cell Biol 107:2059-2073. https://doi.org/10.1083/jcb.107.6.2059
38. Tsuchiya E, Sugawara K, Hongo S, Matsuzaki Y, Muraki Y, Li ZN, Nakamura K. 2002. Effect of addition of new oligosaccharide chains to the globular head of influenza A/H2N2 virus haemagglutinin on the intracellular transport and biological activities of the molecule. J Gen Virol 83:1137-1146. https://doi.org/10.1099/0022-1317-83-5-1137
39. Paal T, Brindley MA, St Clair C, Prussia A, Gaus D, Krumm SA, Snyder JP, Plemper RK. 2009. Probing the spatial organization of measles virus fusion complexes. J Virol 83:10480-10493. https://doi.org/10.1128/JVI.01195-09
40. Radoshitzky SR, Longobardi LE, Kuhn JH, Retterer C, Dong L, Clester JC, Kota K, Carra J, Bavari S. 2011. Machupo virus glycoprotein determinants for human transferrin receptor 1 binding and cell entry. PLoS One 6:e21398. https://doi.org/10.1371/journal.pone.0021398
41. Zavorotinskaya T, Albritton LM. 1999. A hydrophobic patch in ecotropic murine leukemia virus envelope protein is the putative binding site for a critical tyrosine residue on the cellular receptor. J Virol 73: 10164-10172
42. Apte-Sengupta S, Navaratnarajah CK, Cattaneo R. 2013. Hydrophobic and charged residues in the central segment of the measles virus hemagglutinin stalk mediate transmission of the fusion-triggering signal. J Virol 87:10401-10404. https://doi.org/10.1128/JVI.01547-13
43. Bae Y, Kingsman SM, Kingsman AJ. 1997. Functional dissection of the Moloney murine leukemia virus envelope protein gp70. J Virol 71: 2092-2099
44. Wang WK, Dudek T, Essex M, Lee TH. 1999. Hypervariable region 3 residues of HIV type 1 gp120 involved in CCR5 coreceptor utilization: therapeutic and prophylactic implications. Proc Natl Acad Sci U S A 96:4558-4562. https://doi.org/10.1073/pnas.96.8.4558
45. Johnson DE, Ostrowski P, Jaumouille V, Grinstein S. 2016. The position of lysosomes within the cell determines their luminal pH. J Cell Biol 212: 677-692. https://doi.org/10.1083/jcb.201507112
46. Cosset FL, Marianneau P, Verney G, Gallais F, Tordo N, Pecheur EI, Ter Meulen J, Deubel V, Bartosch B. 2009. Characterization of Lassa virus cell entry and neutralization with Lassa virus pseudoparticles. J Virol 83: 3228-3237. https://doi.org/10.1128/JVI.01711-08
47. Klewitz C, Klenk HD, Ter Meulen J. 2007. Amino acids from both N-terminal hydrophobic regions of the Lassa virus envelope glycoprotein GP-2 are critical for pH-dependent membrane fusion and infectivity. J Gen Virol 88:2320-2328. https://doi.org/10.1099/vir.0.82950-0
48. Andersen KG, Shapiro BJ, Matranga CB, Sealfon R, Lin AE, Moses LM, Folarin OA, Goba A, Odia I, Ehiane PE, Momoh M, England EM, Winnicki S, Branco LM, Gire SK, Phelan E, Tariyal R, Tewhey R, Omoniwa O, Fullah M, Fonnie R, Fonnie M, Kanneh L, Jalloh S, Gbakie M, Saffa S, Karbo K, Gladden AD, Qu J, Stremlau M, Nekoui M, Finucane HK, Tabrizi S, Vitti JJ, Birren B, Fitzgerald M, McCowan C, Ireland A, Berlin AM, Bochicchio J, Tazon-Vega B, Lennon NJ, Ryan EM, Bjornson Z, Milner DA, Jr, Lukens AK, Broodie N, Rowland M, Heinrich M, Akdag M, Schieffelin JS, Levy D, Akpan H, Bausch DG, Rubins K, McCormick JB, Lander ES, Günther S, Hensley L, Okogbenin S, Viral Hemorrhagic Fever Consortium, Schaffner SF, Okokhere PO, Khan SH, Grant DS, Akpede GO, Asogun DA, Gnirke A, Levin JZ, Happi CT, Garry RF, Sabeti PC. 2015. Clinical sequencing uncovers origins and evolution of Lassa virus. Cell 162:738-750. https:// doi.org/10.1016/j.cell.2015.07.020
49. Kunz S. 2009. Receptor binding and cell entry of Old World arenaviruses reveal novel aspects of virus-host interaction. Virology 387:245-249. https://doi.org/10.1016/j.virol.2009.02.042
50. Sullivan BM, Emonet SF, Welch MJ, Lee AM, Campbell KP, de la Torre JC, Oldstone MB. 2011. Point mutation in the glycoprotein of lymphocytic choriomeningitis virus is necessary for receptor binding, dendritic cell infection, and long-term persistence. Proc Natl Acad Sci U S A 108: 2969-2974. https://doi.org/10.1073/pnas.1019304108
51. Sevilla N, Kunz S, Holz A, Lewicki H, Homann D, Yamada H, Campbell KP, de La Torre JC, Oldstone MB. 2000. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 192:1249-1260. https://doi.org/10.1084/jem.192.9.1249
52. Kunz S, Sevilla N, Rojek JM, Oldstone MB. 2004. Use of alternative receptors different than alpha-dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325:432-445. https://doi.org/ 10.1016/j.virol.2004.05.009
53. Teng MN, Borrow P, Oldstone MB, de la Torre JC. 1996. A single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with the ability to cause growth hormone deficiency syndrome. J Virol 70:8438-8443
54. Smelt SC, Borrow P, Kunz S, Cao W, Tishon A, Lewicki H, Campbell KP, Oldstone MB. 2001. Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor alpha-dystroglycan correlate with viral tropism and disease kinetics. J Virol 75:448-457. https://doi.org/10.1128/JVI.75.1.448-457.2001
55. Ono N, Tatsuo H, Hidaka Y, Aoki T, Minagawa H, Yanagi Y. 2001. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75:4399-4401. https://doi.org/10.1128/JVI.75.9.4399-4401.2001
56. Robinson JE, Hastie KM, Cross RW, Yenni RE, Elliott DH, Rouelle JA, Kannadka CB, Smira AA, Garry CE, Bradley BT, Yu H, Shaffer JG, Boisen ML, Hartnett JN, Zandonatti MA, Rowland MM, Heinrich ML, Martinez-Sobrido L, Cheng B, de la Torre JC, Andersen KG, Goba A, Momoh M, Fullah M, Gbakie M, Kanneh L, Koroma VJ, Fonnie R, Jalloh SC, Kargbo B, Vandi MA, Gbetuwa M, Ikponmwosa O, Asogun DA, Okokhere PO, Follarin OA, Schieffelin JS, Pitts KR, Geisbert JB, Kulakoski PC, Wilson RB, Happi CT, Sabeti PC, Gevao SM, Khan SH, Grant DS, Geisbert TW, Saphire EO, Branco LM, Garry RF. 2016. Most neutralizing human monoclonal antibodies target novel epitopes requiring both Lassa virus glycoprotein subunits. Nat Commun 7:11544. https://doi.org/10.1038/ncomms11544
57. Lefrancois L, Lyles DS. 1982. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. I. Analysis of neutralizing epitopes with monoclonal antibodies. Virology 121:157-167
58. Whitt MA. 2010. Generation of VSV pseudotypes using recombinant DeltaG-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines. J Virol Methods 169:365-374. https://doi.org/10.1016/j.jviromet.2010.08.006
59. Imperiali M, Thoma C, Pavoni E, Brancaccio A, Callewaert N, Oxenius A. 2005. O Mannosylation of alpha-dystroglycan is essential for lymphocytic choriomeningitis virus receptor function. J Virol 79:14297-14308. https://doi.org/10.1128/JVI.79.22.14297-14308.2005