Amino acid substitutions in the E2 glycoprotein of Sindbis-like virus XJ-160 confer the ability to undergo heparan sulfate-dependent infection of mouse embryonic fibroblasts

Virology Journal

Volumn 7, Issue , 2010, Pages

  Zhu, Wuyang ^a   Fu, Shihong ^a   He, Ying ^a   Li, Jinping ^b   Liang, Guodong ^a  

^a Institute for Viral Disease Control and Prevention   (China)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLYCOPROTEIN E2; HEPARAN SULFATE; HISTIDINE; GLYCOPROTEIN E2, SINDBIS VIRUS; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; FIBROBLAST; MOUSE EMBRYO; MUTANT; NONHUMAN; SINDBIS VIRUS; SUCKLING; VIRUS CELL INTERACTION; VIRUS VIRULENCE; WILD TYPE; ALPHAVIRUS INFECTION; ANIMAL; CELL CULTURE; GENETICS; HAMSTER; METABOLISM; MOUSE; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; VIROLOGY; VIRULENCE; VIRUS ENTRY;

MUS; SINDBIS VIRUS; SINDBIS-LIKE VIRUS;

ALPHAVIRUS INFECTIONS; AMINO ACID SUBSTITUTION; ANIMALS; CELLS, CULTURED; CRICETINAE; FIBROBLASTS; HEPARITIN SULFATE; MICE; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; SINDBIS VIRUS; VIRAL ENVELOPE PROTEINS; VIRULENCE; VIRUS INTERNALIZATION;

EID: 77956472420     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-7-225     Document Type: Article

References (29)

1. Sindbis virus: a newly recognized arthropod-transmitted virus. RM Taylor HS Hurlbut TH Work JR Kingsbury TE Frothingham, Am J Trop Med Hyg 1955 4 844 846 13259009
2. Isolation of virus strains from mosquitoes collected in Queensland 1972-1976. Aust. RL Doherty JG Carley BH Kay C Filippich EN Marks CL Frazier, J Exp Biol Med Sci 1979 57 509 520 10.1038/icb.1979.52
3. The alphaviruses: gene expression, replication, and evolution. JH Strauss EG Strauss, Microbiol Rev 1994 58 491 562 7968923
4. Isolation and complete nucleotide sequence of a Chinese Sindbis-like virus. GD Liang L Li GL Zhou SH Fu QP Li FS Li HH He Q Jin Y He BQ Chen YD Hou, J Gen Virol 2000 81 1347 1351 10769078
5. Sequencing analysis of the genome of YN87448 virus, first isolated in China. GL Zhou GD Liang L Li SH Fu HL Zhang, Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 1998 12 81
6. Binding of Sindbis virus to cell surface heparan sulfate. AP Byrnes DE Griffin, J Virol 1998 72 7349 7356 9696831
7. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. WB Klimstra KD Ryman RE Johnston, J Virol 1998 72 7357 7366 9696832
8. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. KA Bernard WB Klimstra RE Johnston, Virology 2000 276 93 103 10.1006/viro.2000.0546 11021998
9. An amino acid substitution in the coding region of the E2 glycoprotein adapts Ross River virus to utilize heparan sulfate as an attachment moiety. ML Heil A Albee JH Strauss RJ Kuhn, J Virol 2001 75 6303 6309 10.1128/JVI.75.14. 6303-6309.2001 11413296
10. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. WuDunn PG Spear, J Virol 1989 63 52 58 2535752
11. Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T-cell lines. M Patel M Yanagishita G Roderiquez DC Bou-Habib T Oravecz VC Hascall MA Norcross, AIDS Res Hum Retroviruses 1993 9 167 174 10.1089/aid.1993.9.167 8096145
12. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. C Summerford RJ Samulski, J Virol 1998 72 1438 1445 9445046
13. Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. T Krusat HJ Streckert, Arch Virol 1997 142 1247 1254 10.1007/s007050050156 9229012
14. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. T Jackson FM Ellard RA Ghazaleh SM Brookes WE Blakemore AH Corteyn DI Stuart JW Newman AM King, J Virol 1996 70 5282 5287 8764038
15. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. JG Joyce JS Tung CT Przysiecki JC Cook ED Lehman JA Sands KU Jansen PM Keller, J Biol Chem 1999 274 5810 10.1074/jbc.274.9.5810 10026203
16. Interaction of E2 Glycoprotein with Heparan Sulfate Is Crucial for Cellular Infection of Sindbis Virus. W Zhu L Wang Y Yang J Jia S Fu Y He JP Li G Liang, PLoS ONE 2010 5 3 9656 10.1371/journal.pone.0009656 20300181
17. Substitutions of 169Lys and 173Thr in nonstructural protein 1 influence the infectivity and pathogenicity of XJ-160 virus. WY Zhu YL Yang SH Fu LH Wang YG Zhai Q Tang GD Liang, Arch Virol 2009 154 245 253 10.1007/s00705-008-0298-0 19118404
18. Functional analysis of secreted and transmembrane proteins critical to mouse development. KJ Mitchell KI Pinson OG Kelly J Brennan J Zupicich P Scherz PA Leighton LV Goodrich X Lu BJ Avery P Tate K Dill E Pangilinan P Wakenight M Tessier-Lavigne WC Skarnes, Nat Genet 2001 28 241 249 10.1038/90074 11431694
19. Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. JP Li F Gong Hagner-McWhirter E Forsberg M brink R Kisilevsky X Zhang U Lindahl, J Biol Chem 2003 278 28363 28366 10.1074/jbc.C300219200 12788935
20. Embryonic fibroblasts with a gene trap mutation in Ext1 produce short heparan sulfate chains. S Yamada M Busse M Ueno OG Kelly WC Skarnes K Sugahara M Kusche-Gullberg, J Biol Chem 2004 279 32134 32141 10.1074/jbc.M312624200 15161920
21. Lack of L-iduronic acid in heparan sulfate affects interaction with growth factors and cell signaling. J Jia M Maccarana X Zhang M Bespalov U Lindahl JP Li, J Biol Chem 2009 284 15942 15950 10.1074/jbc.M809577200 19336402
22. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer:the fragmin advanced malignancy outcome study (FAMOUS). AK Kakkar MN Levine Z Kadziola NR Lemoine V Low HK Patel G Rustin M Thomas M Quigley RC Williamson, J Clin Oncol 2004 22 1944 1948 10.1200/JCO.2004.10.002 15143088
23. Specificity studies on the heparin lyases from Flavobacterium heparinum. UR Desai HM Wang RJ Linhardt, Biochemistry 1993 32 8140 8145 10.1021/bi00083a012 8347612
24. Heparin-binding and patterns of virulence for two recombinant strains of Sindbis virus. JS Bear AP Byrnes DE Griffin, Virology 2006 347 183 190 10.1016/j.virol.2005.11.034 16380143
25. Large-plaque mutants of Sindbis virus show reduced binding to heparin sulfate, heightened virema, and slower clearance from circulation. AP Byrnes DE Griffin, J Virol 2000 74 644 651 10.1128/JVI.74.2.644-651.2000 10623725
26. Infection of neonatal mice with sindbis virus results in a systemic inflammatory response syndrome. WB Klimstra KD Ryman KA Bernard KB Nguyen CA Biron RE Johnston, J Virol 1999 73 10387 10398 10559357
27. Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. KD Ryman CL Gardner CW Burke KC Meier JM Thompson WB Klimstra, J Virol 2007 81 3563 3573 10.1128/JVI.02494-06 17215278
28. Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry. E Lee M Lobigs, J Virol 2000 74 8867 8875 10.1128/JVI.74.19.8867-8875.2000 10982329
29. Heparan sulfate-independent infection attenuates high-neurovirulence GDVII virus-induced encephalitis. HV Reddi AS Manoj Kumar AY Kung PD Kallio BP Schlitt HL Lipton, J Virol 2004 78 8909 8916 10.1128/JVI.78.16.8909-8916.2004 15280499