Coronavirus and influenza virus proteolytic priming takes place in tetraspanin-enriched membrane microdomains

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 6093-6104

  Earnest, James T ^a   Hantak, Michael P ^a   Park, Jung Eun ^a   Gallagher, Tom ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD9 ANTIGEN; TETRASPANIN; PEPTIDE HYDROLASE; VIRUS FUSION PROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CORONAVIRIDAE; EMBRYO; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PARTICLE; ANIMAL; CHEMISTRY; INFLUENZA A VIRUS; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ATTACHMENT;

CORONAVIRUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ANIMALS; CORONAVIRUS; HUMANS; INFLUENZA A VIRUS; MEMBRANE MICRODOMAINS; PEPTIDE HYDROLASES; PROTEOLYSIS; RECEPTORS, VIRUS; TETRASPANINS; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84929648708     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00543-15     Document Type: Article

References (69)

1. Millet JK, Whittaker GR. 2014. Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci U S A 111:15214-15219. http://dx.doi.org/10.1073/pnas.1407087111.
2. Kido H, Yokogoshi Y, Sakai K, Tashiro M, Kishino Y, Fukutomi A, Katunuma N. 1992. Isolation and characterization of a novel trypsin-like protease found in rat bronchiolar epithelial Clara cells. A possible activator of the viral fusion glycoprotein. J Biol Chem 267:13573-13579.
3. Bertram S, Heurich A, Lavender H, Gierer S, Danisch S, Perin P, Lucas JM, Nelson PS, Pohlmann S, Soilleux EJ. 2012. Influenza and SARScoronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts. PLoS One 7:e35876. http://dx.doi.org/10.1371/journal.pone.0035876.
4. Zhirnov OP, Klenk HD, Wright PF. 2011. Aprotinin and similar protease inhibitors as drugs against influenza. Antiviral Res 92:27-36. http://dx.doi.org/10.1016/j.antiviral.2011.07.014.
5. Bugge TH, Antalis TM, Wu Q. 2009. Type II transmembrane serine proteases. J Biol Chem 284:23177-23181. http://dx.doi.org/10.1074/jbc.R109.021006.
6. Glowacka I, Bertram S, Muller MA, Allen P, Soilleux E, Pfefferle S, Steffen I, Tsegaye TS, He Y, Gnirss K, Niemeyer D, Schneider H, Drosten C, Pohlmann S. 2011. Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response. J Virol 85:4122-4134. http://dx.doi.org/10.1128/JVI.02232-10.
7. Shulla A, Heald-Sargent T, Subramanya G, Zhao J, Perlman S, Gallagher T. 2011. A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol 85:873-882. http://dx.doi.org/10.1128/JVI.02062-10.
8. Shirato K, Kawase M, Matsuyama S. 2013. Middle East respiratory syndrome coronavirus infection mediated by the transmembrane serine protease TMPRSS2. J Virol 87:12552-12561. http://dx.doi.org/10.1128/JVI.01890-13.
9. Gierer S, Bertram S, Kaup F, Wrensch F, Heurich A, Kramer-Kuhl A, Welsch K, Winkler M, Meyer B, Drosten C, Dittmer U, von Hahn T, Simmons G, Hofmann H, Pohlmann S. 2013. The spike protein of the emerging betacoronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2, and is targeted by neutralizing antibodies. J Virol 87:5502-5511. http://dx.doi.org/10.1128/JVI.00128-13.
10. Bertram S, Dijkman R, Habjan M, Heurich A, Gierer S, Glowacka I, Welsch K, Winkler M, Schneider H, Hofmann-Winkler H, Thiel V, Pohlmann S. 2013. TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J Virol 87:6150-6160. http://dx.doi.org/10.1128/JVI.03372-12.
11. Kawase M, Shirato K, Matsuyama S, Taguchi F. 2009. Proteasemediated entry via the endosome of human coronavirus 229E. J Virol 83:712-721. http://dx.doi.org/10.1128/JVI.01933-08.
12. Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P. 2005. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci U S A 102:11876-11881. http://dx.doi.org/10.1073/pnas.0505577102.
13. Bottcher E, Matrosovich T, Beyerle M, Klenk HD, Garten W, Matrosovich M. 2006. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J Virol 80: 9896-9898. http://dx.doi.org/10.1128/JVI.01118-06.
14. Hatesuer B, Bertram S, Mehnert N, Bahgat MM, Nelson PS, Pohlman S, Schughart K. 2013. Tmprss2 is essential for influenza H1N1 virus pathogenesis in mice. PLoS Pathog 9:e1003774. http://dx.doi.org/10.1371/journal.ppat.1003774.
15. Bottcher-Friebertshauser E, Freuer C, Sielaff F, Schmidt S, Eickmann M, Uhlendorff J, Steinmetzer T, Klenk HD, Garten W. 2010. Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors. J Virol 84:5605-5614. http://dx.doi.org/10.1128/JVI.00140-10.
16. Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E. 2009. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420:133-154. http://dx.doi.org/10.1042/BJ20082422.
17. Yanez-Mo M, Barreiro O, Gordon-Alonso M, Sala-Valdes M, Sanchez-Madrid F. 2009. Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19:434-446. http://dx.doi.org/10.1016/j.tcb.2009.06.004.
18. van Spriel AB, Figdor CG. 2010. The role of tetraspanins in the pathogenesis of infectious diseases. Microbes Infect 12:106-112. http://dx.doi.org/10.1016/j.micinf.2009.11.001.
19. Le Naour F, Andre M, Boucheix C, Rubinstein E. 2006. Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts. Proteomics 6:6447-6454. http://dx.doi.org/10.1002/pmic.200600282.
20. Rana S, Claas C, Kretz CC, Nazarenko I, Zoeller M. 2011. Activationinduced internalization differs for the tetraspanins CD9 and Tspan8: impact on tumor cell motility. Int J Biochem Cell Biol 43:106-119. http://dx.doi.org/10.1016/j.biocel.2010.10.002.
21. Ono M, Hakomori S. 2004. Glycosylation defining cancer cell motility and invasiveness. Glycoconj J 20:71-78. http://dx.doi.org/10.1023/B:GLYC.0000018019.22070.7d.
22. Andre M, Le Caer JP, Greco C, Planchon S, El Nemer W, Boucheix C, Rubinstein E, Chamot-Rooke J, Le Naour F. 2006. Proteomic analysis of the tetraspanin web using LC-ESI-MS/MS and MALDI-FTICR-MS. Proteomics 6:1437-1449. http://dx.doi.org/10.1002/pmic.200500180.
23. He J, Sun E, Bujny MV, Kim D, Davidson MW, Zhuang X. 2013. Dual function of CD81 in influenza virus uncoating and budding. PLoS Pathog 9:e1003701. http://dx.doi.org/10.1371/journal.ppat.1003701.
24. Konig R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, Bhattacharyya S, Alamares JG, Tscherne DM, Ortigoza MB, Liang Y, Gao Q, Andrews SE, Bandyopadhyay S, De Jesus P, Tu BP, Pache L, Shih C, Orth A, Bonamy G, Miraglia L, Ideker T, Garcia-Sastre A, Young JA, Palese P, Shaw ML, Chanda SK. 2010. Human host factors required for influenza virus replication. Nature 463:813-817. http://dx.doi.org/10.1038/nature08699.
25. Nguyen EK, Nemerow GR, Smith JG. 2010. Direct evidence from singlecell analysis that human alpha-defensins block adenovirus uncoating to neutralize infection. J Virol 84:4041-4049. http://dx.doi.org/10.1128/JVI.02471-09.
26. Rumschlag-Booms E, Guo Y, Wang J, Caffrey M, Rong L. 2009. Comparative analysis between a low pathogenic and a high pathogenic influenza H5 hemagglutinin in cell entry. Virol J 6:76. http://dx.doi.org/10.1186/1743-422X-6-76.
27. Thorp EB, Gallagher TM. 2004. Requirements for CEACAMs and cholesterol during murine coronavirus cell entry. J Virol 78:2682-2692. http://dx.doi.org/10.1128/JVI.78.6.2682-2692.2004.
28. Campbell EM, Perez O, Melar M, Hope TJ. 2007. Labeling HIV-1 virions with two fluorescent proteins allows identification of virions that have productively entered the target cell. Virology 360:286-293. http://dx.doi.org/10.1016/j.virol.2006.10.025.
29. Heaton NS, Levya-Grado VH, Tan GS, Eggink D, Hai R, Palese P. 2013. In vivo bioluminescent imaging of influenza A virus infection and characterization of novel cross-protective monoclonal antibodies. J Virol 87: 8272-8281. http://dx.doi.org/10.1128/JVI.00969-13.
30. Szretter KJ, Balish AL, Katz JM. 2006. Influenza: propagation, quantification, and storage. Curr Protoc Microbiol Chapter 15:Unit 15G.1. http://dx.doi.org/10.1002/0471729256.mc15g01s3.
31. Shulla A, Gallagher T. 2009. Role of spike protein endodomains in regulating coronavirus entry. J Biol Chem 284:32725-32734. http://dx.doi.org/10.1074/jbc.M109.043547.
32. 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. http://dx.doi.org/10.1016/j.jviromet.2010.08.006.
33. Barlan A, Zhao J, Sarkar MK, Li K, McCray PB, Jr, Perlman S, Gallagher T. 2014. Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J Virol 88:4953-4961. http://dx.doi.org/10.1128/JVI.00161-14.
34. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, Pascale S, Scarselli E, Cortese R, Nicosia A, Cosset F-L. 2003. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278:41624-41630. http://dx.doi.org/10.1074/jbc.M305289200.
35. Scheffer KD, Gawlitza A, Spoden GA, Zhang XA, Lambert C, Berditchevski F, Florin L. 2013. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J Virol 87:3435-3446. http://dx.doi.org/10.1128/JVI.02906-12.
36. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-422. http://dx.doi.org/10.1038/357420a0.
37. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254. http://dx.doi.org/10.1038/nature12005.
38. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454. http://dx.doi.org/10.1038/nature02145.
39. Ziyyat A, Rubinstein E, Monier-Gavelle F, Barraud V, Kulski O, Prenant M, Boucheix C, Bomsel M, Wolf JP. 2006. CD9 controls the formation of clusters that contain tetraspanins and the integrin alpha 6 beta 1, which are involved in human and mouse gamete fusion. J Cell Sci 119:416-424. http://dx.doi.org/10.1242/jcs.02730.
40. Matsuyama S, Nagata N, Shirato K, Kawase M, Takeda M, Taguchi F. 2010. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J Virol 84:12658-12664. http://dx.doi.org/10.1128/JVI.01542-10.
41. Runge KE, Evans JE, He ZY, Gupta S, McDonald KL, Stahlberg H, Primakoff P, Myles DG. 2007. Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 304:317-325. http://dx.doi.org/10.1016/j.ydbio.2006.12.041.
42. Symeonides M, Lambele M, Roy NH, Thali M. 2014. Evidence showing that tetraspanins inhibit HIV-1-induced cell-cell fusion at a post-hemifusion stage. Viruses 6:1078-1090. http://dx.doi.org/10.3390/v6031078.
43. Okamoto T, Iwata S, Yamazaki H, Hatano R, Komiya E, Dang NH, Ohnuma K, Morimoto C. 2014. CD9 negatively regulates CD26 expression and inhibits CD26-mediated enhancement of invasive potential of malignant mesothelioma cells. PLoS One 9:e86671. http://dx.doi.org/10.1371/journal.pone.0086671.
44. Claas C, Stipp CS, Hemler ME. 2001. Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J Biol Chem 276:7974-7984. http://dx.doi.org/10.1074/jbc.M008650200.
45. Dveksler GS, Pensiero MN, Cardellichio CB, Williams RK, Jiang GS, Holmes KV, Dieffenbach CW. 1991. Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J Virol 65:6881-6891.
46. Sala-Valdes M, Ursa A, Charrin S, Rubinstein E, Hemler ME, Sanchez-Madrid F, Yanez-Mo M. 2006. EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrinradixin-moesin proteins. J Biol Chem 281:19665-19675. http://dx.doi.org/10.1074/jbc.M602116200.
47. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ, II, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ. 1991. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 266:19599-19610.
48. Cannon KS, Cresswell P. 2001. Quality control of transmembrane domain assembly in the tetraspanin CD82. EMBO J 20:2443-2453. http://dx.doi.org/10.1093/emboj/20.10.2443.
49. Toledo MS, Suzuki E, Handa K, Hakomori S. 2005. Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J Biol Chem 280:16227-16234. http://dx.doi.org/10.1074/jbc.M413713200.
50. Bourboulia D, Stetler-Stevenson WG. 2010. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 20:161-168. http://dx.doi.org/10.1016/j.semcancer.2010.05.002.
51. Heurich A, Hofmann-Winkler H, Gierer S, Liepold T, Jahn O, Pohlmann S. 2014. TMPRSS2 and ADAM17 cleave ACE2 differentially and only proteolysis by TMPRSS2 augments entry driven by the severe acute respiratory syndrome coronavirus spike protein. J Virol 88:1293-1307. http://dx.doi.org/10.1128/JVI.02202-13.
52. Lin B, Ferguson C, White JT, Wang S, Vessella R, True LD, Hood L, Nelson PS. 1999. Prostate-localized and androgen-regulated expression of the membrane-bound serine protease TMPRSS2. Cancer Res 59:4180-4184.
53. Qiu Z, Hingley ST, Simmons G, Yu C, Das Sarma J, Bates P, Weiss SR. 2006. Endosomal proteolysis by cathepsins is necessary for murine coronavirus mouse hepatitis virus type 2 spike-mediated entry. J Virol 80: 5768-5776. http://dx.doi.org/10.1128/JVI.00442-06.
54. Kim TS, Heinlein C, Hackman RC, Nelson PS. 2006. Phenotypic analysis of mice lacking the Tmprss2-encoded protease. Mol Cell Biol 26:965-975. http://dx.doi.org/10.1128/MCB.26.3.965-975.2006.
55. Sales KU, Hobson JP, Wagenaar-Miller R, Szabo R, Rasmussen AL, Bey A, Shah MF, Molinolo AA, Bugge TH. 2011. Expression and genetic loss of function analysis of the HAT/DESC cluster proteases TMPRSS11A and HAT. PLoS One 6:e23261. http://dx.doi.org/10.1371/journal.pone.0023261.
56. Hemler ME. 2005. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6:801-811. http://dx.doi.org/10.1038/nrm1736.
57. Dietrich C, Volovyk ZN, Levi M, Thompson NL, Jacobson K. 2001. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proc Natl Acad Sci U S A 98:10642-10647. http://dx.doi.org/10.1073/pnas.191168698.
58. Wang Y, Murakami Y, Yasui T, Wakana S, Kikutani H, Kinoshita T, Maeda Y. 2013. Significance of GPI-anchored protein enrichment in lipid rafts for the control of autoimmunity. J Biol Chem 288:25490-25499. http://dx.doi.org/10.1074/jbc.M113.492611.
59. Brown DA, London E. 2000. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J Biol Chem 275:17221-17224. http://dx.doi.org/10.1074/jbc.R000005200.
60. Gomez-Mouton C, Abad JL, Mira E, Lacalle RA, Gallardo E, Jimenez-Baranda S, Illa I, Bernad A, Manes S, Martinez AC. 2001. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad SciUSA 98:9642-9647. http://dx.doi.org/10.1073/pnas.171160298.
61. Charrin S, Manié S, Thiele C, Billard M, Gerlier D, Boucheix C, Rubinstein E. 2003. A physical and functional link between cholesterol and tetraspanins. Eur J Immunol 33:2479-2489. http://dx.doi.org/10.1002/eji.200323884.
62. Nomura R, Kiyota A, Suzaki E, Kataoka K, Ohe Y, Miyamoto K, Senda T, Fujimoto T. 2004. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J Virol 78:8701-8708. http://dx.doi.org/10.1128/JVI.78.16.8701-8708.2004.
63. Sun X, Whittaker GR. 2003. Role for influenza virus envelope cholesterol in virus entry and infection. J Virol 77:12543-12551. http://dx.doi.org/10.1128/JVI.77.23.12543-12551.2003.
64. Kawase M, Shirato K, van der Hoek L, Taguchi F, Matsuyama S. 2012. Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry. J Virol 86:6537-6545. http://dx.doi.org/10.1128/JVI.00094-12.
65. Bahgat MM, Blazejewska P, Schughart K. 2011. Inhibition of lung serine proteases in mice: a potentially new approach to control influenza infection. Virol J 8:27. http://dx.doi.org/10.1186/1743-422X-8-27.
66. Owsianka AM, Timms JM, Tarr AW, Brown RJ, Hickling TP, Szwejk A, Bienkowska-Szewczyk K, Thomson BJ, Patel AH, Ball JK. 2006. Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 80:8695-8704. http://dx.doi.org/10.1128/JVI.00271-06.
67. Lee KK, Pessi A, Gui L, Santoprete A, Talekar A, Moscona A, Porotto M. 2011. Capturing a fusion intermediate of influenza hemagglutinin with a cholesterol-conjugated peptide, a new antiviral strategy for influenza virus. J Biol Chem 286:42141-42149. http://dx.doi.org/10.1074/jbc.M111.254243.
68. Bosch BJ, Martina BE, Van Der Zee R, Lepault J, Haijema BJ, Versluis C, Heck AJ, De Groot R, Osterhaus AD, Rottier PJ. 2004. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc Natl Acad Sci U S A 101:8455-8460. http://dx.doi.org/10.1073/pnas.0400576101.
69. Lu L, Liu Q, Zhu Y, Chan KH, Qin L, Li Y, Wang Q, Chan JF, Du L, Yu F, Ma C, Ye S, Yuen KY, Zhang R, Jiang S. 2014. Structure-based discovery of Middle East respiratory syndrome coronavirus fusion inhibitor. Nat Commun 5:3067. http://dx.doi.org/10.1038/ncomms4067.