Design of an HA2-based escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge

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

Volumn 107, Issue 31, 2010, Pages 13701-13706

  Bommakanti, Gayathri ^a   Citron, Michael P ^b   Hepler, Robert W ^b   Callahan, Cheryl ^b   Heidecker, Gwendolyn J ^b   Najar, Tariq Ahmad ^a   Lu, Xianghan ^b   Joyce, Joseph G ^b   Shiver, John W ^b   Casimiro, Danilo R ^b   Meulen, Jan Ter ^b   Liang, Xiaoping ^b   Varadarajan, Raghavan ^a,c  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b MERCK RESEARCH LABORATORIES   (United States)

^c JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

Bacterial expression; Hemagglutinin; Protein design

Indexed keywords

ANTIGEN; MEMBRANE PROTEIN; PROTEIN HA 2; PROTEIN HA 6; UNCLASSIFIED DRUG; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; IMMUNOGENICITY; INFLUENZA VIRUS; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; ANIMAL; BAGG ALBINO MOUSE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; GENETICS; IMMUNOLOGY; INFLUENZA VIRUS A; METABOLISM; MUTATION; ORTHOMYXOVIRUS INFECTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; CIRCULAR DICHROISM; ESCHERICHIA COLI; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

EID: 77956379133     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1007465107     Document Type: Article

References (41)

1. Fan J, et al. (2004) Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22:2993-3003.
2. Horimoto T, Kawaoka Y (2005) Influenza: Lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591-600.
3. Cox MM (2005) Cell-based protein vaccines for influenza. Curr Opin Mol Ther 7:24-9.
4. Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin. Annu Rev Biochem 69:531-569.
5. Chen J, et al. (1998) Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409-417.
6. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
7. Sauter NK, et al. (1992) Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: Analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography. Biochemistry 31:9609-9621.
8. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-73.
9. Both GW, Sleigh MJ, Cox NJ, Kendal AP (1983) Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: Multiple evolutionary pathways and sequential amino acid changes at key antigenic sites. J Virol 48:52-60.
10. Wiley DC, Wilson IA, Skehel JJ (1981) Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378.
11. Gocnik M, et al. (2008) Antibodies induced by the HA2 glycopolypeptide of influenza virus haemagglutinin improve recovery from influenza A virus infection. J Gen Virol 89:958-967.
12. Smirnov YA, Lipatov AS, Gitelman AK, Class EC, Osterhaus AD (2000) Prevention and treatment of bronchopneumonia in mice caused by mouse-adapted variant of avian H5N2 influenza A virus using monoclonal antibody against conserved epitope in the HA stem region. Arch Virol 145:1733-1741.
13. Okuno Y, Matsumoto K, Isegawa Y, Ueda S (1994) Protection against the mouse-adapted A/FM/1/47 strain of influenza A virus in mice by a monoclonal antibody with cross-neutralizing activity among H1 and H2 strains. J Virol 68:517-520.
14. Ekiert DC, et al. (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251.
15. Sui J, et al. (2009) Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16:265-273.
16. Throsby M, et al. (2008) Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 3:e3942.
17. Okuno Y, Isegawa Y, Sasao F, Ueda S (1993) A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 67:2552-2558.
18. Sanchez-Fauquier A, Villanueva N, Melero JA (1987) Isolation of cross-reactive, subtype-specific monoclonal antibodies against influenza virus HA1 and HA2 hemagglutinin subunits. Arch Virol 97:251-265.
19. Chen J, et al. (1995) A soluble domain of the membrane-anchoring chain of influenza virus hemagglutinin (HA2) folds in Escherichia coli into the low-pH-induced conformation. Proc Natl Acad Sci USA 92:12205-12209.
20. Steel J, et al. (2010) Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1:e00018.
21. Sharma D, et al. (2005) Protein minimization of the gp120 binding region of human CD4. Biochemistry 44:16192-16202.
22. Godley L, et al. (1992) Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 68:635-645.
23. Lee B, Richards FM (1971) The interpretation of protein structures: Estimation of static accessibility. J Mol Biol 55:379-400.
24. Kuhlman B, et al. (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302:1364-1368.
25. Varadarajan R, et al. (2005) Characterization of gp120 and its single-chain derivatives, gp120-CD4D12 and gp120-M9: implications for targeting the CD4i epitope in human immunodeficiency virus vaccine design. J Virol 79:1713-1723.
26. Bajaj K, Chakrabarti P, Varadarajan R (2005) Mutagenesis-based definitions and probes of residue burial in proteins. Proc Natl Acad Sci USA 102:16221-16226.
27. Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823-832.
28. Mitra A, et al. (2005) High level expression of peptides and proteins using cytochrome b5 as a fusion host. Protein Expr Purif 41:84-97.
29. Joyce JG, et al. (2002) Enhancement of alpha -helicity in the HIV-1 inhibitory peptide DP178 leads to an increased affinity for human monoclonal antibody 2F5 but does not elicit neutralizing responses in vitro. Implications for vaccine design. J Biol Chem 277:45811-45820.
30. Dani VS, Ramakrishnan C, Varadarajan R (2003) MODIP revisited: Re-evaluation and refinement of an automated procedure for modeling of disulfide bonds in proteins. Protein Eng 16:187-193.
31. Wang TT, et al. (2010) Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog 6:e1000796.
32. Lim AP, et al. (2008) Neutralizing human monoclonal antibody against H5N1 influenza HA selected from a Fab-phage display library. Virol J 5:130.
33. Air GM(1981) Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc Natl Acad Sci USA 78:7639-7643.
34. Knossow M, et al. (2002) Mechanism of neutralization of influenza virus infectivity by antibodies. Virology 302:294-298.
35. Hensley SE, et al. (2009) Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326:734-736.
36. Knossow M, Skehel JJ (2006) Variation and infectivity neutralization in influenza. Immunology 119:1-7.
37. Okada J, et al. (2010) Monoclonal antibodies in man that neutralized H3N2 influenza viruses were classified into three groups with distinct strain specificity: 1968-1973, 1977-1993 and 1997-2003. Virology 397:322-330.
38. Gerhard W (2001) The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 260:171-190.
39. Prajapati RS, Indu S, Varadarajan R (2007) Identification and thermodynamic characterization of molten globule states of periplasmic binding proteins. Biochemistry 46:10339-10352.
40. Ramachandran S, Udgaonkar JB (1996) Stabilization of barstar by chemical modification of the buried cysteines. Biochemistry 35:8776-8785.
41. Sayle RA, Milner-White EJ (1995) RASMOL: Biomolecular graphics for all. Trends Biochem Sci 20:374-376.