SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway

Cell Research

Volumn 18, Issue 2, 2008, Pages 290-301

  Wang, Hongliang ^a   Yang, Peng ^a   Liu, Kangtai ^a   Guo, Feng ^a   Zhang, Yanli ^a   Zhang, Gongyi ^b   Jiang, Chengyu ^a  

^a TSINGHUA UNIVERSITY   (China)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

Angiotensin converting enzyme 2 (ACE2); Endocytosis; Lipid rafts; Severe Acute Respiratory Syndrome Coronavirus (SARS CoV)

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CALCIUM BINDING PROTEIN; CAV1 PROTEIN, HUMAN; CAVEOLIN 1; CLATHRIN; DIPEPTIDYL CARBOXYPEPTIDASE; EPS15 PROTEIN, HUMAN; MEMBRANE PROTEIN; PHOSPHOPROTEIN; SIGNAL PEPTIDE; SPIKE GLYCOPROTEIN, CORONAVIRUS; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ARTICLE; CAVEOLA; CELL LINE; ENDOCYTOSIS; ENDOSOME; GENETICS; HUMAN; METABOLISM; PATHOGENICITY; PH; PROTEIN TRANSPORT; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIROLOGY; VIRUS ENTRY;

CALCIUM-BINDING PROTEINS; CAVEOLAE; CAVEOLIN 1; CELL LINE; CLATHRIN; ENDOCYTOSIS; ENDOSOMES; HUMANS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE GLYCOPROTEINS; PEPTIDYL-DIPEPTIDASE A; PHOSPHOPROTEINS; PROTEIN TRANSPORT; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

CORONAVIRUS; SARS CORONAVIRUS;

EID: 38849114449     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2008.15     Document Type: Article

References (45)

1. Drosten C, Gunther S, Preiser W, et al. Identification of a novel Coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 2003; 348:1967-1976.
2. Ksiazek TG, Erdman D, Goldsmith CS, et al. A novel Coronavirus associated with severe acute respiratory syndrome. NEngl J Med 2003;348:1953-1966.
3. Pelkmans L, Helenius A. Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 2003; 15:414-422.
4. Sieczkarski SB, Whittaker GR. Dissecting virus entry via endocytosis. J Gen Virol 2002; 83:1535-1545.
5. Fackler OT, Peterlin BM. Endocytic entry of HIV-1. Curr Biol 2000;10:1005-1008.
6. Matlin KS, Reggio H, Helenius A, Simons K. Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 1981; 91:601-613.
7. Sieczkarski SB, Whittaker GR. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 2002; 76:10455-10464.
8. Nunes-Correia I, Eulalio A, Nir S, Pedroso de Lima MC. Caveolae as an additional route for influenza virus endocytosis in MDCK cells. Cell Mol Biol Lett 2004; 9:47-60.
9. Ng ML, Tan SH, See EE, Ooi EE, Ling AE. Early events of SARS Coronavirus infection in vero cells. J Med Virol 2003; 71:323-331.
10. Qinfen Z, Jinming C, Xiaojun H, et al. The life cycle of SARS Coronavirus in Vero E6 cells. J Med Virol 2004; 73:332-337.
11. Simmons G, Reeves JD, Rennekamp AJ, Amberg SM, Piefer AJ, Bates P. Characterization of severe acute respiratory syndromeassociated Coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc Natl Acad Sci USA 2004; 101:4240-4245.
12. Yang ZY, Huang Y, Ganesh L, et al. pH-dependent entry of severe acute respiratory syndrome Coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J Virol 2004; 78:5642-5650.
13. Huang IC, Bosch BJ, Li F, et al. SARS Coronavirus, but not human Coronavirus NL63, utilizes cathepsin L to infect ACE2expressing cells. J Biol Chem 2006; 281:3198-3203.
14. Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P. Inhibitors of cathepsin L prevent severe acute respiratory syndrome Coronavirus entry. Proc Natl Acad Sci USA 2005;102:11876-11881.
15. Moore MJ, Dorfman T, Li W, et al. Retroviruses pseudotyped with the severe acute respiratory syndrome Coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J Virol 2004; 78:10628-10635.
16. Kuba K, Imai Y, Rao S, et al. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat Med 2005; 11:875-879.
17. Ray RB, Basu A, Steele R, et al. Ebola virus glycoprotein-mediated anoikis of primary human cardiac microvascular endothelial cells. Virology 2004; 321:181-188.
18. Blanchard E, Belouzard S, Goueslain L, et al. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 2006; 80:6964-6972.
19. Codran A, Royer C, Jaeck D, et al. Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependentendocytosis. J Gen Wra/2006; 87:2583-2593.
20. Empig CJ, Goldsmith MA. Association of the caveola vesicular system with cellular entry by filoviruses. J Virol 2002; 76:5266-5270.
21. Dautry-Varsat A. Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 1986; 68:375-381.
22. Dautry-Varsat A, Ciechanover A, Lodish HF. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci USA 1983; 80:2258-2262.
23. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983; 97:329-339.
24. Wang LH, Rothberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 1993; 123:1107-1117.
25. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A. Inhibition of clathrin-coated pit assembly by an Eps 15 mutant. J Cell Sci 1999; 112 Part 9:1303-1311.
26. Benmerah A, Poupon V, Cerf-Bensussan N, Dautry-Varsat A. Mapping of Eps15 domains involved in its targeting to clathrincoated pits. J Biol Chem 2000; 275:3288-3295.
27. Stan RV. Structure of caveolae. Biochim Biophys Acta 2005; 1746:334-348.
28. Orlandi PA, Fishman PH. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 1998; 141:905-915.
29. Sanchez-San Martin C, Lopez T, Arias CF, Lopez S. Characterization of rotavirus cell entry. J Virol 2004; 78:2310-2318.
30. Lanzrein M, Schlegel A, Kempf C. Entry and uncoating of enveloped viruses. Biochem J 1994; 302 (Part 2):313-320.
31. Cantin C, Holguera J, Ferreira L, Villar E, Munoz-Barroso I. Newcastle disease virus may enter cells by caveolae-mediated endocytosis. J Gen Virol 2007; 88:559-569.
32. Li GM, Li YG, Yamate M, Li SM, Ikuta K. Lipid rafts play an important role in the early stage of severe acute respiratory syndrome-coronavirus life cycle. Microbes Infect 2007; 9:96-102.
33. Cinatl J Jr, Hoever G, Morgenstern B, et al. Infection of cultured intestinal epithelial cells with severe acute respiratory syndrome Coronavirus. Cell Mol Life Sci 2004; 61:2100-2112.
34. Mossel EC, Huang C, Narayanan K, Makino S, Tesh RB, Peters CJ. Exogenous ACE2 expression allows refractory cell lines to support severe acute respiratory syndrome Coronavirus replication. J Virol 2005; 79:3846-3850.
35. Mirre C, Monlauzeur L, Garcia M, Delgrossi MH, Le Bivic A. Detergent-resistant membrane microdomains from Caco-2 cells do not contain caveolin. Am J Physiol 1996; 271:C887-C894.
36. Inoue Y, Tanaka N, Tanaka Y, et al. Clathrin-dependent entry of SARS Coronavirus into target cells expressing cytoplasmic tail-deleted ACE2. J Virol 2007; 81:8722-8729.
37. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis GJ, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS Coronavirus. A first step in understanding SARS pathogenesis. J Pathol 2004; 203:631-637.
38. Popik W, Alee TM, Au WC. Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. J Virol 2002; 76:4709-4722.
39. Manes S, del Real G, Martinez AC. Pathogens: raft hijackers. Nat Rev 2003; 3:557-568.
40. Shigeta S, Yamase T. Current status of anti-SARS agents. Antivir Chem Chemother 2005; 16:23-31.
41. Kliger Y, Levanon EY, Gerber D. From genome to antivirals: SARS as a test tube. Drug Disc Today 2005; 10:345-352.
42. Negre D, Mangeot PE, Duisit G, et al. Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther2000; 7:1613-1623.
43. Kohler G, Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975; 256:495-497.
44. Kee SH, Cho EJ, Song JW, Park KS, Baek U, Song KJ. Effects of endocytosis inhibitory drugs on rubella virus entry into VeroE6 cells. Microbiol Immunol 2004; 48:823-829.
45. Meertens L, Bertaux C, Dragic T. Hepatitis Cvirus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J Virol 2006; 80:11571-11578.