Biophysical characterization of HRC peptide analogs interaction with heptad repeat regions of the SARS-coronavirus Spike fusion protein core

Journal of Structural Biology

Volumn 155, Issue 2, 2006, Pages 162-175

  Yan, Zhe ^a   Tripet, Brian ^a   Hodges, Robert S ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Coiled coil; Coronavirus (CoV); Heptad repeat regions (HRN and HRC); SARS CoV; Severe acute respiratory syndrome (SARS); Six helix bundle state; Spike protein

Indexed keywords

HRC PEPTIDE; HYBRID PROTEIN; LACTAM; PEPTIDE DERIVATIVE; PROTEIN INHIBITOR; SPIKE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA HELIX; ARTICLE; CORRELATION ANALYSIS; ELECTRICITY; HYDROPHOBICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

AMINO ACID SEQUENCE; BINDING SITES; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN DENATURATION; REPETITIVE SEQUENCES, AMINO ACID; SARS VIRUS; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE; TEMPERATURE; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

SARS CORONAVIRUS;

EID: 33747802391     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2006.03.024     Document Type: Article

References (39)

1. Bianchi E., Finotto M., Ingallinella P., Hrin R., Carella A.V., Hou X.S., Schleif W.A., Miller M.D., Geleziunas R., and Pessi A. Covalent stabilization of coiled coils of the HIV gp41 N region yields extremely potent and broad inhibitors of viral infection. Proc. Natl. Acad. Sci. USA 102 (2005) 12903-12908
2. Bosch B.J., Martina B.E., Van Der Zee R., Lepault J., Haijema B.J., Versluis C., Heck A.J., De Groot R., Osterhaus A.D., and Rottier P.J. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. USA 101 (2004) 8455-8460
3. Bosch B.J., van der Zee R., de Haan C.A., and Rottier P.J. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77 (2003) 8801-8811
4. Chakrabartty A., Kortemme T., and Baldwin R.L. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci. 3 (1994) 843-852
5. Chan D.C., Chutkowski C.T., and Kim P.S. Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target. Proc. Natl. Acad. Sci. USA 95 (1998) 15613-15917
6. Chan D.C., and Kim P.S. HIV entry and its inhibition. Cell 93 (1998) 681-684
7. Duquerroy S., Vigouroux A., Rottier P.J., Rey F.A., and Bosch B.J. Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology 335 (2005) 276-285
8. Eckert D.M., and Kim P.S. Design of potent inhibitors of HIV-1 entry from the gp41 N-peptide region. Proc. Natl. Acad. Sci. USA 98 (2001) 11187-11192
9. Eckert D.M., and Kim P.S. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70 (2001) 777-810
10. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., Luo S.W., Li P.H., Zhang L.J., Guan Y.J., Butt K.M., Wong K.L., Chan K.W., Lim W., Shortridge K.F., Yuen K.Y., Peiris J.S., and Poon L.L. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302 (2003) 276-278
11. Hakansson-McReynolds S., Jiang S., Rong L., and Caffrey M. Solution structure of the SARS-coronavirus HR2 domain in the prefusion state. J. Biol. Chem. 281 (2006) 11965-11971
12. Hartley D.M., and Smith D.L. Uncertainty in SARS epidemiology. Lancet 362 (2003) 170-171
13. Holmes K.V. Structural biology. Adaptation of SARS coronavirus to humans. Science 309 (2005) 1822-1823
14. Houston Jr. M.E., Gannon C.L., Kay C.M., and Hodges R.S. Lactam bridge stabilization of alpha-helical peptides: ring size, orientation and positional effects. J. Pept. Sci. 1 (1995) 274-282
15. Houston Jr. M.E., Wallace A., Bianchi E., Pessi A., and Hodges R.S. Use of a conformationally restricted secondary structural element to display peptide libraries: a two-stranded alpha-helical coiled-coil stabilized by lactam bridges. J. Mol. Biol. 262 (1996) 270-282
16. Ingallinella P., Bianchi E., Finotto M., Cantoni G., Eckert D.M., Supekar V.M., Bruckmann C., Carfi A., and Pessi A. Structural characterization of the fusion-active complex of severe acute respiratory syndrome (SARS) coronavirus. Proc. Natl. Acad. Sci. USA 101 (2004) 8709-8714
17. Kates S.A., Daniels S.B., and Albericio F. Automated allyl cleavage for continuous-flow synthesis of cyclic and branched peptides. Anal. Biochem. 212 (1993) 303-310
18. LaBonte J., Lebbos J., and Kirkpatrick P. Enfuvirtide. Nat. Rev. Drug Discov. 2 (2003) 345-346
19. Lee D.L., Ivaninskii S., Burkhard P., and Hodges R.S. Unique stabilizing interactions identified in the two-stranded alpha-helical coiled-coil: crystal structure of a cortexillin I/GCN4 hybrid coiled-coil peptide. Protein Sci. 12 (2003) 1395-1405
20. Li F., Li W., Farzan M., and Harrison S.C. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309 (2005) 1864-1868
21. Liu S., Xiao G., Chen Y., He Y., Niu J., Escalante C.R., Xiong H., Farmar J., Debnath A.K., Tien P., and Jiang S. Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet 363 (2004) 938-947
22. Lu M., Blacklow S.C., and Kim P.S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2 (1995) 1075-1082
23. Normile D. Infectious diseases. Mounting lab accidents raise SARS fears. Science 304 (2004) 659-661
24. Normile D. Infectious diseases. Second lab accident fuels fears about SARS. Science 303 (2004) 26
25. O'Neil K.T., and DeGrado W.F. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250 (1990) 646-651
26. Root M.J., Kay M.S., and Kim P.S. Protein design of an HIV-1 entry inhibitor. Science 291 (2001) 884-888
27. Skehel J.J., and Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69 (2000) 531-569
28. Spaan W., Cavanagh D., and Horzinek M.C. Coronaviruses: structure and genome expression. J. Gen. Virol. 69 Pt 12 (1988) 2939-2952
29. Supekar V.M., Bruckmann C., Ingallinella P., Bianchi E., Pessi A., and Carfi A. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc. Natl. Acad. Sci. USA 101 (2004) 17958-17963
30. Tripet B., Howard M.W., Jobling M., Holmes R.K., Holmes K.V., and Hodges R.S. Structural characterization of the SARS-coronavirus spike S fusion protein core. J. Biol. Chem. 279 (2004) 20836-20849
31. Tripet, B., Kao, D., Jeffers, S., Holmes, K., Hodges, R., 2006. Template-based HRC antigens elicit neutralizing antibodies to the SARS-CoV. J. Struct. Biol. (in press).
32. Tripet B., Wagschal K., Lavigne P., Mant C.T., and Hodges R.S. Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil: 20 amino acid substitutions in position "d". J. Mol. Biol. 300 (2000) 377-402
33. Wagschal K., Tripet B., and Hodges R.S. De novo design of a model peptide sequence to examine the effects of single amino acid substitutions in the hydrophobic core on both stability and oligomerization state of coiled-coils. J. Mol. Biol. 285 (1999) 785-803
34. Wagschal K., Tripet B., Lavigne P., Mant C., and Hodges R.S. The role of position a in determining the stability and oligomerization state of alpha-helical coiled coils: 20 amino acid stability coefficients in the hydrophobic core of proteins. Protein Sci. 8 (1999) 2312-2329
35. Xu Y., Lou Z., Liu Y., Pang H., Tien P., Gao G.F., and Rao Z. Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 279 (2004) 49414-49419
36. Xu Y., Zhu J., Liu Y., Lou Z., Yuan F., Cole D.K., Ni L., Su N., Qin L., Li X., Bai Z., Bell J.I., Pang H., Tien P., Gao G.F., and Rao Z. Characterization of the heptad repeat regions, HR1 and HR2, and design of a fusion core structure model of the spike protein from severe acute respiratory syndrome (SARS) coronavirus. Biochemistry 43 (2004) 14064-14071
37. Yuan K., Yi L., Chen J., Qu X., Qing T., Rao X., Jiang P., Hu J., Xiong Z., Nie Y., Shi X., Wang W., Ling C., Yin X., Fan K., Lai L., Ding M., and Deng H. Suppression of SARS-CoV entry by peptides corresponding to heptad regions on spike glycoprotein. Biochem. Biophys. Res. Commun. 319 (2004) 746-752
38. Zhou N.E., Kay C.M., and Hodges R.S. The role of interhelical ionic interactions in controlling protein folding and stability. De novo designed synthetic two-stranded alpha-helical coiled-coils. J. Mol. Biol. 237 (1994) 500-512
39. Zhu J., Xiao G., Xu Y., Yuan F., Zheng C., Liu Y., Yan H., Cole D.K., Bell J.I., Rao Z., Tien P., and Gao G.F. Following the rule: formation of the 6-helix bundle of the fusion core from severe acute respiratory syndrome coronavirus spike protein and identification of potent peptide inhibitors. Biochem. Biophys. Res. Commun. 319 (2004) 283-288