Roles of the putative integrin-binding motif of the human metapneumovirus fusion (F) protein in cell-cell fusion, viral infectivity, and pathogenesis

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4338-4352

  Wei, Yongwei ^a,b,e   Zhang, Yu ^a,b   Cai, Hui ^a   Mirza, Anne M ^c   Iorio, Ronald M ^c   Peeples, Mark E ^d   Niewiesk, Stefan ^a   Li, Jianrong ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^e NINGBO UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPA 5 BETA 1 INTEGRIN; CD51 ANTIGEN; HUMAN METAPNEUMOVIRUS FUSION PROTEIN; HYBRID PROTEIN; INTEGRIN; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL CELL FUSION; CELL FUSION; CELL SURFACE; CONTROLLED STUDY; COTTON RAT; DOWN REGULATION; FEMALE; FUSION ACTIVITY; HISTOLOGY; IMMUNOGENICITY; MEMBRANE FUSION; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VIROGENESIS; VIRUS ENTRY; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS REPLICATION;

AMINO ACID MOTIFS; ANIMALS; FEMALE; HUMANS; INTEGRIN ALPHA5BETA1; INTEGRIN ALPHAV; METAPNEUMOVIRUS; MUTATION, MISSENSE; PARAMYXOVIRIDAE INFECTIONS; PROTEIN BINDING; RATS; SIGMODONTINAE; VIRAL FUSION PROTEINS; VIRULENCE; VIRUS INTERNALIZATION;

EID: 84897005475     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03491-13     Document Type: Article

References (57)

1. van den Hoogen BG, de Jong JC, Groen J, Kuiken T, de Groot R, Fouchier RA, Osterhaus AD. 2001. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat. Med. 7:719-724. http://dx.doi.org/10.1038/89098.
2. van den Hoogen BG, van Doornum GJ, Fockens JC, Cornelissen JJ, Beyer WE, de Groot R, Osterhaus AD, Fouchier RA. 2003. Prevalence and clinical symptoms of human metapneumovirus infection in hospitalized patients. J. Infect. Dis. 188:1571-1577. http://dx.doi.org/10.1086/379200.
3. Crowe JE, Jr. 2004. Human metapneumovirus as a major cause of human respiratory tract disease. Pediatr. Infect. Dis. J. 23:S215-S221. http://dx.doi.org/10.1097/01.inf.0000144668.81573.6d.
4. Biacchesi S, Skiadopoulos MH, Boivin G, Hanson CT, Murphy BR, Collins PL, Buchholz UJ. 2003. Genetic diversity between human metapneumovirus subgroups. Virology 315:1-9. http://dx.doi.org/10.1016/S0042-6822(03)00528-2.
5. Boivin G, Abed Y, Pelletier G, Ruel L, Moisan D, Cote S, Peret TC, Erdman DD, Anderson LJ. 2002. Virological features and clinical manifestations associated with human metapneumovirus: a new paramyxovirus responsible for acute respiratory-tract infections in all age groups. J. Infect. Dis. 186:1330-1334. http://dx.doi.org/10.1086/344319.
6. Falsey AR, Erdman D, Anderson LJ, Walsh EE. 2003. Human metapneumovirus infections in young and elderly adults. J. Infect. Dis. 187:785-790. http://dx.doi.org/10.1086/367901.
7. Govindarajan D, Buchholz UJ, Samal SK. 2006. Recovery of avian metapneumovirus subgroup C from cDNA: cross-recognition of avian and human metapneumovirus support proteins. J. Virol. 80:5790-5797. http://dx.doi.org/10.1128/JVI.00138-06.
8. Lamb RA. 1993. Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11. http://dx.doi.org/10.1006/viro.1993.1561.
9. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U. S. A. 102:9288-9293. http://dx.doi.org/10.1073/pnas.0503989102.
10. 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. U. S. A. 109:16672-16677. http://dx.doi.org/10.1073/pnas.1213802109.
11. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA. 2006. Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 103:17903-17908. http://dx.doi.org/10.1073/pnas.0608678103.
12. Lamb RA, Jardetzky TS. 2007. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436. http://dx.doi.org/10.1016/j.sbi.2007.08.016.
13. Kim YH, Donald JE, Grigoryan G, Leser GP, Fadeev AY, Lamb RA, DeGrado WF. 2011. Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc. Natl. Acad. Sci. U. S. A. 108: 20992-20997. http://dx.doi.org/10.1073/pnas.1116034108.
14. Mallipeddi SK, Samal SK. 1993. Structural difference in the fusion protein among strains of bovine respiratory syncytial virus. Vet. Microbiol. 36:359-367. http://dx.doi.org/10.1016/0378-1135(93)90102-D.
15. Pastey MK, Samal SK. 1997. Analysis of bovine respiratory syncytial virus envelope glycoproteins in cell fusion. J. Gen. Virol. 78(Pt 8):1885-1889.
16. Chaiwatpongsakorn S, Epand RF, Collins PL, Epand RM, Peeples ME. 2011. Soluble respiratory syncytial virus fusion protein in the fully cleaved, pretriggered state is triggered by exposure to low-molarity buffer. J. Virol. 85:3968-3977. http://dx.doi.org/10.1128/JVI.01813-10.
17. Schowalter RM, Smith SE, Dutch RE. 2006. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J. Virol. 80:10931-10941. http://dx.doi.org/10.1128/JVI.01287-06.
18. Schowalter RM, Chang A, Robach JG, Buchholz UJ, Dutch RE. 2009. Low-pH triggering of human metapneumovirus fusion: essential residues and importance in entry. J. Virol. 83:1511-1522. http://dx.doi.org/10.1128/JVI.01381-08.
19. Mas V, Herfst S, Osterhaus AD, Fouchier RA, Melero JA. 2011. Residues of the human metapneumovirus fusion (F) protein critical for its strainrelated fusion phenotype: implications for the virus replication cycle. J. Virol. 85:12650-12661. http://dx.doi.org/10.1128/JVI.05485-11.
20. Wei Y, Feng K, Yao X, Cai H, Li J, Mirza AM, Iorio RM, Li J. 2012. Localization of a region in the fusion protein of avian metapneumovirus that modulates cell-cell fusion. J. Virol. 86:11800-11814. http://dx.doi.org/10.1128/JVI.00232-12.
21. Biacchesi S, Skiadopoulos MH, Yang L, Lamirande EW, Tran KC, Murphy BR, Collins PL, Buchholz UJ. 2004. Recombinant human metapneumovirus lacking the small hydrophobic SH and/or attachment G glycoprotein: deletion of G yields a promising vaccine candidate. J. Virol. 78:12877-12887. http://dx.doi.org/10.1128/JVI.78.23.12877-12887.2004.
22. Herfst S, Mas V, Ver LS, Wierda RJ, Osterhaus AD, Fouchier RA, Melero JA. 2008. Low-pH-induced membrane fusion mediated by human metapneumovirus F protein is a rare, strain-dependent phenomenon. J. Virol. 82:8891-8895. http://dx.doi.org/10.1128/JVI.00472-08.
23. Cseke G, Maginnis MS, Cox RG, Tollefson SJ, Podsiad AB, Wright DW, Dermody TS, Williams JV. 2009. Integrin alphavbeta1 promotes infection by human metapneumovirus. Proc. Natl. Acad. Sci. U. S. A. 106: 1566-1571. http://dx.doi.org/10.1073/pnas.0801433106.
24. Cox RG, Livesay SB, Johnson M, Ohi MD, Williams JV. 2012. The human metapneumovirus fusion protein mediates entry via an interaction with RGD-binding integrins. J. Virol. 86:12148-12160. http://dx.doi.org/10.1128/JVI.01133-12.
25. Chang A, Masante C, Buchholz UJ, Dutch RE. 2012. Human metapneumovirus (HMPV) binding and infection are mediated by interactions between the HMPV fusion protein and heparan sulfate. J. Virol. 86:3230-3243. http://dx.doi.org/10.1128/JVI.06706-11.
26. van den Hoogen BG, Bestebroer TM, Osterhaus AD, Fouchier RA. 2002. Analysis of the genomic sequence of a human metapneumovirus. Virology 295:119-132. http://dx.doi.org/10.1006/viro.2001.1355.
27. Herfst S, de Graaf M, Schickli JH, Tang RS, Kaur J, Yang CF, Spaete RR, Haller AA, van den Hoogen BG, Osterhaus AD, Fouchier RA. 2004. Recovery of human metapneumovirus genetic lineages A and B from cloned cDNA. J. Virol. 78:8264-8270. http://dx.doi.org/10.1128/JVI.78.15.8264-8270.2004.
28. Zhang Y, Wei Y, Li J, Li J. 2012. Development and optimization of a direct plaque assay for human and avian metapneumoviruses. J. Virol. Methods 185:61-68. http://dx.doi.org/10.1016/j.jviromet.2012.05.030.
29. de Graaf M, Herfst S, Schrauwen EJ, van den Hoogen BG, Osterhaus AD, Fouchier RA. 2007. An improved plaque reduction virus neutralization assay for human metapneumovirus. J. Virol. Methods 143:169-174. http://dx.doi.org/10.1016/j.jviromet.2007.03.005.
30. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, Zhou T, Graepel KW, Kumar A, Moin S, Boyington JC, Chuang GY, Soto C, Baxa U, Bakker AQ, Spits H, Beaumont T, Zheng Z, Xia N, Ko SY, Todd JP, Rao S, Graham BS, Kwong PD. 2013. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342:592-598. http://dx.doi.org/10.1126/science.1243283.
31. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340:1113-1117. http://dx.doi.org/10.1126/science.1234914.
32. Triantafilou K, Takada Y, Triantafilou M. 2001. Mechanisms of integrinmediated virus attachment and internalization process. Crit. Rev. Immunol. 21:311-322. http://dx.doi.org/10.1615/CritRevImmunol.v21.i4.10.
33. Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ. 2006. Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J. Virol. 80: 8961-8969. http://dx.doi.org/10.1128/JVI.00843-06.
34. Berryman S, Clark S, Monaghan P, Jackson T. 2005. Early events in integrin alphavbeta6-mediated cell entry of foot-and-mouth disease virus. J. Virol. 79:8519-8534. http://dx.doi.org/10.1128/JVI.79.13.8519-8534.2005.
35. Chesnokova LS, Hutt-Fletcher LM. 2011. Fusion of Epstein-Barr virus with epithelial cells can be triggered by alphavbeta5 in addition to alphavbeta6 and alphavbeta8, and integrin binding triggers a conformational change in glycoproteins gHgL. J. Virol. 85:13214-13223. http://dx.doi.org/10.1128/JVI.05580-11.
36. Dicara D, Burman A, Clark S, Berryman S, Howard MJ, Hart IR, Marshall JF, Jackson T. 2008. Foot-and-mouth disease virus forms a highly stable, EDTA-resistant complex with its principal receptor, integrin alphavbeta6: implications for infectiousness. J. Virol. 82:1537-1546. http://dx.doi.org/10.1128/JVI.01480-07.
37. Gianni T, Campadelli-Fiume G. 2012. alphaVbeta3-integrin relocalizes nectin1 and routes herpes simplex virus to lipid rafts. J. Virol. 86:2850-2855. http://dx.doi.org/10.1128/JVI.06689-11.
38. Summerford C, Bartlett JS, Samulski RJ. 1999. AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat. Med. 5:78-82. http://dx.doi.org/10.1038/4768.
39. Lee E, Lobigs M. 2000. 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. J. Virol. 74:8867-8875. http://dx.doi.org/10.1128/JVI.74.19.8867-8875.2000.
40. van der Most RG, Corver J, Strauss JH. 1999. Mutagenesis of the RGD motif in the yellow fever virus 17D envelope protein. Virology 265:83-95. http://dx.doi.org/10.1006/viro.1999.0026.
41. Rothwangl KB, Rong L. 2009. Analysis of a conserved RGE/RGD motif in HCV E2 in mediating entry. Virol. J. 6:12. http://dx.doi.org/10.1186/1743-422X-6-12.
42. Leippert M, Beck E, Weiland F, PfaffE. 1997. Point mutations within the betaG-betaH loop of foot-and-mouth disease virus O1K affect virus attachment to target cells. J. Virol. 71:1046-1051.
43. Arnaout MA, Goodman SL, Xiong JP. 2002. Coming to grips with integrin binding to ligands. Curr. Opin. Cell Biol. 14:641-651. http://dx.doi.org/10.1016/S0955-0674(02)00371-X.
44. Hauck CR, Agerer F, Muenzner P, Schmitter T. 2006. Cellular adhesion molecules as targets for bacterial infection. Eur. J. Cell Biol. 85:235-242. http://dx.doi.org/10.1016/j.ejcb.2005.08.002.
45. Zhang L, Zhang C, Ojcius DM, Sun D, Zhao J, Lin X, Li L, Li L, Yan J. 2012. The mammalian cell entry (Mce) protein of pathogenic Leptospira species is responsible forRGDmotif-dependent infection of cells and animals. Mol. Microbiol. 83:1006-1023. http://dx.doi.org/10.1111/j.1365-2958.2012.07985.x.
46. Allaoui A, Sansonetti PJ, Menard R, Barzu S, Mounier J, Phalipon A, Parsot C. 1995. MxiG, a membrane protein required for secretion of Shigella spp. Ipa invasins: involvement in entry into epithelial cells and in intercellular dissemination. Mol. Microbiol. 17:461-470.
47. Stockbauer KE, Magoun L, Liu M, Burns EH, Jr, Gubba S, Renish S, Pan X, Bodary SC, Baker E, Coburn J, Leong JM, Musser JM. 1999. A natural variant of the cysteine protease virulence factor of group A Streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins alphavbeta3 and alphaIIbbeta3. Proc. Natl. Acad. Sci. U. S. A. 96:242-247. http://dx.doi.org/10.1073/pnas.96.1.242.
48. Barden S, Lange S, Tegtmeyer N, Conradi J, Sewald N, Backert S, Niemann HH. 2013. A helical RGD motif promoting cell adhesion: crystal structures of the Helicobacter pylori type IV secretion system pilus protein CagL. Structure 21:1931-1941. http://dx.doi.org/10.1016/j.str.2013.08.018.
49. Wen X, Krause JC, Leser GP, Cox RG, Lamb RA, Williams JV, Crowe JE, Jr, Jardetzky TS. 2012. Structure of the human metapneumovirus fusion protein with neutralizing antibody identifies a pneumovirus antigenic site. Nat. Struct. Mol. Biol. 19:461-463. http://dx.doi.org/10.1038/nsmb.2250.
50. Akula SM, Pramod NP, Wang FZ, Chandran B. 2001. Human herpesvirus 8 envelope-associated glycoprotein B interacts with heparan sulfatelike moieties. Virology 284:235-249. http://dx.doi.org/10.1006/viro.2001.0921.
51. Spear PG, Longnecker R. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185. http://dx.doi.org/10.1128/JVI.77.19.10179-10185.2003.
52. Zhang L, Bukreyev A, Thompson CI, Watson B, Peeples ME, Collins PL, Pickles RJ. 2005. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J. Virol. 79:1113-1124. http://dx.doi.org/10.1128/JVI.79.2.1113-1124.2005.
53. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. 2002. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J. Virol. 76:5654-5666. http://dx.doi.org/10.1128/JVI.76.11.5654-5666.2002.
54. Kim HW, Canchola JG, Brandt CD, Pyles G, Chanock RM, Jensen K, Parrott RH. 1969. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am. J. Epidemiol. 89:422-434.
55. Yim KC, Cragin RP, Boukhvalova MS, Blanco JC, Hamlin ME, Boivin G, Porter DD, Prince GA. 2007. Human metapneumovirus: enhanced pulmonary disease in cotton rats immunized with formalin-inactivated virus vaccine and challenged. Vaccine 25:5034-5040. http://dx.doi.org/10.1016/j.vaccine.2007.04.075.
56. Buchholz UJ, Nagashima K, Murphy BR, Collins PL. 2006. Live vaccines for human metapneumovirus designed by reverse genetics. Expert Rev. Vaccines 5:695-706. http://dx.doi.org/10.1586/14760584.5.5.695.
57. Biacchesi S, Pham QN, Skiadopoulos MH, Murphy BR, Collins PL, Buchholz UJ. 2005. Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J. Virol. 79:12608-12613. http://dx.doi.org/10.1128/JVI.79.19.12608-12613.2005.