Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 26, 2011, Pages 10696-10701

  Peng, Guiqing ^a   Sun, Dawei ^a   Rajashankar, Kanagalaghatta R ^b   Qian, Zhaohui ^c   Holmes, Kathryn V ^c   Li, Fang ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Carcinoembryonic antigen related cell adhesion molecule 1 binding by coronaviruses; Coronavirus evolution; Galectin like N terminal domain of coronavirus spike proteins; Sugar binding by coronaviruses

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CORE PROTEIN; GALECTIN; VIRUS RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; CORONAVIRUS; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; HYDROPHOBICITY; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; VIRUS IMMUNITY; VIRUS MORPHOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CARCINOEMBRYONIC ANTIGEN; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RECEPTORS, VIRUS; SEQUENCE HOMOLOGY, AMINO ACID;

BOVINE CORONAVIRUS; CORONAVIRUS; MURINAE; MURINE HEPATITIS VIRUS;

EID: 79960567167     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1104306108     Document Type: Article

References (45)

1. Delmas B, et al. (1992) Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:417-420.
2. Yeager CL, et al. (1992) Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-422.
3. Delmas B, Gelfi J, Sjöström H, Noren O, Laude H (1993) Further characterization of aminopeptidase-N as a receptor for coronaviruses. Adv Exp Med Biol 342:293-298.
4. Dveksler GS, et al. (1991) Cloning of the mouse hepatitis virus (MHV) receptor: Expression in human and hamster cell lines confers susceptibility toMHV. J Virol 65:6881-6891.
5. Williams RK, Jiang GS, Holmes KV (1991) Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci USA 88:5533-5536. (Pubitemid 21914779)
6. Hofmann H, et al. (2005) Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc Natl Acad Sci USA 102:7988-7993. (Pubitemid 40781050)
7. Li WH, et al. (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
8. Schwegmann-Wessels C, Herrler G (2006) Sialic acids as receptor determinants for coronaviruses. Glycoconj J 23:51-58.
9. Krempl C, Schultze B, Laude H, Herrler G (1997) Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J Virol 71:3285-3287. (Pubitemid 27121569)
10. Schultze B, et al. (1996) Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity. J Virol 70:5634-5637. (Pubitemid 26240741)
11. Cavanagh D, Davis PJ (1986) Coronavirus IBV: Removal of spike glycopolypeptide S1 by urea abolishes infectivity and haemagglutination but not attachment to cells. J Gen Virol 67:1443-1448.
12. Schultze B, Cavanagh D, Herrler G (1992) Neuraminidase treatment of avian infectious bronchitis coronavirus reveals a hemagglutinating activity that is dependent on sialic acid-containing receptors on erythrocytes. Virology 189:792-794.
13. Schultze B, Gross HJ, Brossmer R, Herrler G (1991) The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J Virol 65:6232-6237.
14. Künkel F, Herrler G (1993) Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 195:195-202.
15. Bowden TA, Crispin M, Jones EY, Stuart DI (2010) Shared paramyxoviral glycoprotein architecture is adapted for diverse attachment strategies. Biochem Soc Trans 38:1349-1355.
16. Overbaugh J, Miller AD, Eiden MV (2001) Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol Mol Biol Rev 65:371-389. (Pubitemid 32881711)
17. Bosch BJ, van der Zee R, de Haan CAM, Rottier PJM (2003) The coronavirus spike protein is a class I virus fusion protein: Structural and functional characterization of the fusion core complex. J Virol 77:8801-8811. (Pubitemid 36936092)
18. Godet M, Grosclaude J, Delmas B, Laude H (1994) Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J Virol 68:8008-8016. (Pubitemid 24362689)
19. Breslin JJ, et al. (2003) Human coronavirus 229E: Receptor binding domain and neutralization by soluble receptor at 37 degrees C. J Virol 77:4435-4438. (Pubitemid 36350983)
20. Hofmann H, et al. (2006) Highly conserved regions within the spike proteins of human coronaviruses 229E and NL63 determine recognition of their respective cellular receptors. J Virol 80:8639-8652. (Pubitemid 44384874)
21. Lin HX, et al. (2008) Identification of residues in the receptor-binding domain (RBD) of the spike protein of human coronavirus NL63 that are critical for the RBD-ACE2 receptor interaction. J Gen Virol 89:1015-1024.
22. Wong SK, Li WH, Moore MJ, Choe H, Farzan M (2004) A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J Biol Chem 279:3197-3201. (Pubitemid 38140552)
23. Wu K, Li WK, Peng G, Li F (2009) Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc Natl Acad Sci USA 106:19970-19974.
24. Li F, Li WH, Farzan M, Harrison SC (2005) Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:1864-1868. (Pubitemid 41325098)
25. Kubo H, Yamada YK, Taguchi F (1994) Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J Virol 68:5403-5410. (Pubitemid 24258552)
26. Beauchemin N, et al. (1999) Redefined nomenclature for members of the carcino-embryonic antigen family. Exp Cell Res 252:243-249. (Pubitemid 29530255)
27. Godfraind C, et al. (1995) Tissue and cellular distribution of an adhesion molecule in the carcinoembryonic antigen family that serves as a receptor for mouse hepatitis virus. Lab Invest 73:615-627.
28. Wessner DR, et al. (1998) Mutational analysis of the virus and monoclonal antibody binding sites in MHVR, the cellular receptor of the murine coronavirus mouse hepatitis virus strain A59. J Virol 72:1941-1948. (Pubitemid 28100747)
29. Ohtsuka N, Yamada YK, Taguchi F (1996) Difference in virus-binding activity of two distinct receptor proteins for mouse hepatitis virus. J Gen Virol 77:1683-1692. (Pubitemid 26278746)
30. Tan KM, et al. (2002) Crystal structure of murine sCEACAM1a[1,4]: A coronavirus receptor in the CEA family. EMBO J 21:2076-2086.
31. Compton SR, Stephensen CB, Snyder SW, Weismiller DG, Holmes KV (1992) Coronavirus species specificity: Murine coronavirus binds to a mouse-specific epitope on its carcinoembryonic antigen-related receptor glycoprotein. J Virol 66:7420-7428.
32. Zeng QH, Langereis MA, van Vliet ALW, Huizinga EG, de Groot RJ (2008) Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci USA 105:9065-9069.
33. Langereis MA, van Vliet ALW, Boot W, de Groot RJ (2010) Attachment of mouse hepatitis virus to O-acetylated sialic acid is mediated by hemagglutinin-esterase and not by the spike protein. J Virol 84:8970-8974.
34. Yokomori K, Banner LR, Lai MMC (1991) Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses. Virology 183:647-657.
35. Li WK, Li F (2011) Cross-crystal averaging with search models to improve molecular replacement phases. Structure 19:155-161.
36. Thackray LB, Turner BC, Holmes KV (2005) Substitutions of conserved amino acids in the receptor-binding domain of the spike glycoprotein affect utilization of murine CEACAM1a by the murine coronavirus MHV-A59. Virology 334:98-110. (Pubitemid 40320738)
37. Leparc-Goffart I, et al. (1997) Altered pathogenesis of a mutant of the murine coronavirus MHV-A59 is associated with a Q159L amino acid substitution in the spike protein. Virology 239:1-10. (Pubitemid 28027065)
38. Dormitzer PR, Sun ZYJ, Wagner G, Harrison SC (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21:885-897. (Pubitemid 34206162)
39. Seetharaman J, et al. (1998) X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution. J Biol Chem 273:13047-13052. (Pubitemid 28246869)
40. Holm L, Sander C (1998) Touring protein fold space with Dali/FSSP. Nucleic Acids Res 26:316-319. (Pubitemid 28291549)
41. Bowden TA, et al. (2008) Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15:567-572. (Pubitemid 351799140)
42. Santiago C, Celma ML, Stehle T, Casasnovas JM (2010) Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat Struct Mol Biol 17:124-129.
43. Bellizzi JJ, Widom J, Kemp CW, Clardy J (1999) Producing selenomethionine-labeled proteins with a baculovirus expression vector system. Structure 7:R263-R267. (Pubitemid 29529871)
44. Qian ZH, Wang HZ, Empig C, Anderson WF, Albritton LM (2004) Complementation of a binding-defective retrovirus by a host cell receptor mutant. J Virol 78:5766-5772. (Pubitemid 38661664)
45. Taguchi F, Ikeda T, Shida H (1992) Molecular cloning and expression of a spike protein of neurovirulent murine coronavirus JHMV variant cl-2. J Gen Virol 73:1065-1072.