Protein intrinsic disorder and influenza virulence: The 1918 H1N1 and H5N1 viruses

Virology Journal

Volumn 6, Issue , 2009, Pages

  Goh, Gerard Kian Meng ^a,d   Dunker, A Keith ^a   Uversky, Vladimir N ^a,b,c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS HEMAGGLUTININ; HEMAGGLUTININ FUSOGENIC PEPTIDE, INFLUENZA VIRUS;

AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; NONHUMAN; PROTEIN ANALYSIS; VIRUS ENTRY; VIRUS STRAIN; VIRUS VIRULENCE; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; HUMAN; INFLUENZA; INFLUENZA VIRUS A H3N2; MOLECULAR GENETICS; PATHOGENICITY; PROTEIN TERTIARY STRUCTURE; VIROLOGY; VIRULENCE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HEMAGGLUTININS, VIRAL; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; VIRULENCE;

EID: 67949091224     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-6-69     Document Type: Article

References (89)

1. GF Brooks JS Butel SA Morse, Jawetz, Melnick and Adelberg's medical microbiology 23rd edition New York: Lange/McGraw-Hill 23 2004
2. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. RA Fouchier V Munster A Wallensten TM Bestebroer S Herfst D Smith GF Rimmelzwaan B Olsen AD Osterhaus, J Virol 2005 79 2814 2822 15709000 (Pubitemid 40270559)
3. Lessons learned from reconstructing the 1918 influenza pandemic. A Garcia-Sastre RJ Whitley, J Infect Dis 2006 194 Suppl 2 S127 132 17163385
4. Evidence of an absence: the genetic origins of the 1918 pandemic influenza virus. AH Reid JK Taubenberger TG Fanning, Nat Rev Microbiol 2004 2 909 914 15494747 (Pubitemid 39561807)
5. The 1918 Spanish influenza: integrating history and biology. AH Reid JK Taubenberger TG Fanning, Microbes Infect 2001 3 81 87 11226857 (Pubitemid 32172043)
6. Influenza pandemics of the 20th century. ED Kilbourne, Emerg Infect Dis 2006 12 9 14 16494710 (Pubitemid 43143528)
7. Human illness from avian influenza H7N3, British Columbia. SA Tweed DM Skowronski ST David A Larder M Petric W Lees Y Li J Katz M Krajden R Tellier, Emerg Infect Dis 2004 10 2196 2199 15663860 (Pubitemid 39587346)
8. Update: isolation of avian influenza A(H5N1) viruses from humans Hong Kong, 19971998. MMWR Morb Mortal Wkly Rep 1998 46 1245 1247 9436713
9. Infectious disease. An avian flu jumps to people. B Wuethrich, Science 2003 299 1504 12624244
10. Avian influenza, Viet Nam update. World Health Organization, Wkly Epidemiol Rec 2005 80 233 234 16080581
11. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Y Guan KF Shortridge S Krauss RG Webster, Proc Natl Acad Sci USA 1999 96 9363 9367 10430948 (Pubitemid 29374760)
12. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. YP Lin M Shaw V Gregory K Cameron W Lim A Klimov K Subbarao Y Guan S Krauss K Shortridge, Proc Natl Acad Sci USA 2000 97 9654 9658 10920197 (Pubitemid 30650831)
13. Coiled coils in both intracellular vesicle and viral membrane fusion. JJ Skehel DC Wiley, Cell 1998 95 871 874 9875840 (Pubitemid 29019038)
14. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. JJ Skehel DC Wiley, Annu Rev Biochem 2000 69 531 569 10966468 (Pubitemid 30792219)
15. Mechanisms of viral membrane fusion and its inhibition. DM Eckert PS Kim, Annu Rev Biochem 2001 70 777 810 11395423 (Pubitemid 32662225)
16. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. DC Wiley JJ Skehel, Annu Rev Biochem 1987 56 365 394 3304138
17. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. JJ Skehel PM Bayley EB Brown SR Martin MD Waterfield JM White IA Wilson DC Wiley, Proc Natl Acad Sci USA 1982 79 968 972 6951181
18. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. J Stevens AL Corper CF Basler JK Taubenberger P Palese IA Wilson, Science 2004 303 1866 1870 14764887 (Pubitemid 38374878)
19. H+-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. P Durrer C Galli S Hoenke C Corti R Gluck T Vorherr J Brunner, J Biol Chem 1996 271 13417 13421 8662770 (Pubitemid 26185382)
20. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. IA Wilson JJ Skehel DC Wiley, Nature 1981 289 366 373 7464906
21. Structure of influenza haemagglutinin at the pH of membrane fusion. PA Bullough FM Hughson JJ Skehel DC Wiley, Nature 1994 371 37 43 8072525 (Pubitemid 24277462)
22. Evidence for H(+)-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. T Weber G Paesold C Galli R Mischler G Semenza J Brunner, J Biol Chem 1994 269 18353 18358 8034580
23. Electron microscopy of antibody complexes of influenza virus haemagglutinin in the fusion pH conformation. SA Wharton LJ Calder RW Ruigrok JJ Skehel DA Steinhauer DC Wiley, Embo J 1995 14 240 246 7835335
24. Integrating historical, clinical and molecular genetic data in order to explain the origin and virulence of the 1918 Spanish influenza virus. JK Taubenberger AH Reid TA Janczewsk TG Fanning, Philos Trans R Soc Lond B Biol Sci 2001 356 1829 11779381
25. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. D Kobasa A Takada K Shinya M Hatta P Halfmann S Theriault H Suzuki H Nishimura K Mitamura N Sugaya, Nature 2004 431 703 707 15470432 (Pubitemid 39382618)
26. The effects of the 19181919 influenza pandemic on infant and child health in Derbyshire. A Reid, Med Hist 2005 49 29 54 15730129 (Pubitemid 40144934)
27. Influenza pandemics of the 20th century. ED Kilbourne, Emerg Infect Dis 2006 12 9 14 16494710 (Pubitemid 43143528)
28. The 1918 Spanish influenza: Integrating history and biology. AH Reid JK Taubenberger TG Fanning, Microbes Infect. 2001 3 1 81 87 11226857 (Pubitemid 32172043)
29. Intrinsically disordered protein. AK Dunker JD Lawson CJ Brown RM Williams P Romero JS Oh CJ Oldfield AM Campen CM Ratliff KW Hipps, J Mol Graph Model 2001 19 26 59 11381529 (Pubitemid 32411501)
30. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. PE Wright HJ Dyson, J Mol Biol 1999 293 321 331 10550212 (Pubitemid 29516173)
31. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. PH Weinreb W Zhen AW Poon KA Conway PT Lansbury Jr, Biochemistry 1996 35 13709 13715 8901511 (Pubitemid 26363912)
32. Why are "natively unfolded" proteins unstructured under physiologic conditions? VN Uversky JR Gillespie AL Fink, Proteins 2000 41 415 427 11025552 (Pubitemid 30822417)
33. Natively unfolded human prothymosin alpha adopts partially folded collapsed conformation at acidic pH. VN Uversky JR Gillespie IS Millett AV Khodyakova AM Vasiliev TV Chernovskaya RN Vasilenko GD Kozlovskaya DA Dolgikh AL Fink, Biochemistry 1999 38 15009 15016 10555983
34. Protein disorder and the evolution of molecular recognition: theory, predictions and observations. AK Dunker E Garner S Guilliot P Romero K Albrecht J Hart Z Obradovic C Kissinger JE Villafranca, Pac Symp Biocomput 1998 473 484 9697205
35. Intrinsic disorder and protein function. AK Dunker CJ Brown JD Lawson LM Iakoucheva Z Obradovic, Biochemistry 2002 41 6573 6582 12022860 (Pubitemid 34547347)
36. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. VN Uversky CJ Oldfield AK Dunker, J Mol Recognit 2005 18 343 384 16094605 (Pubitemid 41341287)
37. Natively disordered proteins. GW Daughdrill GJ Pielak VN Uversky MS Cortese AK Dunker, Protein Folding Handbook Weinheim, Germany: Wiley-VCH, Verlag GmbH & Co. KGaA, Buchner J, Kiefhaber T, 2005 271 353
38. Flexible nets. The roles of intrinsic disorder in protein interaction networks. AK Dunker MS Cortese P Romero LM Iakoucheva VN Uversky, FEBS J 2005 272 5129 5148 16218947 (Pubitemid 41503146)
39. Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. H Xie S Vucetic LM Iakoucheva CJ Oldfield AK Dunker Z Obradovic VN Uversky, J Proteome Res 2007 6 1917 1932 17391016 (Pubitemid 46814514)
40. Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. S Vucetic H Xie LM Iakoucheva CJ Oldfield AK Dunker Z Obradovic VN Uversky, J Proteome Res 2007 6 1899 1916 17391015 (Pubitemid 46814513)
41. Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. H Xie S Vucetic LM Iakoucheva CJ Oldfield AK Dunker VN Uversky Z Obradovic, J Proteome Res 2007 6 1882 1898 17391014 (Pubitemid 46814512)
42. What does it mean to be natively unfolded? VN Uversky, Eur J Biochem 2002 269 2 12 11784292 (Pubitemid 34107333)
43. Natively unfolded proteins: a point where biology waits for physics. VN Uversky, Protein Sci 2002 11 739 756 11910019 (Pubitemid 34241284)
44. Protein folding revisited. A polypeptide chain at the folding-misfolding-nonfolding cross-roads: which way to go? VN Uversky, Cell Mol Life Sci 2003 60 1852 1871 14523548 (Pubitemid 37222583)
45. Intrinsically unstructured proteins. P Tompa, Trends Biochem Sci 2002 27 527 533 12368089 (Pubitemid 35279598)
46. Intrinsically unstructured proteins and their functions. HJ Dyson PE Wright, Nat Rev Mol Cell Biol 2005 6 197 208 15738986 (Pubitemid 40314921)
47. The interplay between structure and function in intrinsically unstructured proteins. P Tompa, FEBS Lett 2005 579 3346 3354 15943980 (Pubitemid 40804685)
48. Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity, and signaling conduits. CA Galea Y Wang SG Sivakolundu RW Kriwacki, Biochemistry 2008 47 7598 7609 18627125 (Pubitemid 352019491)
49. The unfoldomics decade: an update on intrinsically disordered proteins. AK Dunker CJ Oldfield J Meng P Romero JY Yang JW Chen V Vacic Z Obradovic VN Uversky, BMC Genomics 2008 9 Suppl 2 S1 18831774
50. Function and structure of inherently disordered proteins. AK Dunker I Silman VN Uversky JL Sussman, Curr Opin Struct Biol 2008 18 756 764 18952168
51. Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. CJ Oldfield J Meng JY Yang MQ Yang VN Uversky AK Dunker, BMC Genomics 2008 9 Suppl 1 S1 18366598
52. Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. J Gsponer ME Futschik SA Teichmann MM Babu, Science 2008 322 1365 1368 19039133 (Pubitemid 352775246)
53. Biochemistry. Controlled chaos. VN Uversky AK Dunker, Science 2008 322 1340 1341 19039128
54. TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder. A Campen RM Williams CJ Brown J Meng VN Uversky AK Dunker, Protein Pept Lett 2008 15 956 963 18991772
55. Evolutionary rate heterogeneity in proteins with long disordered regions. CJ Brown S Takayama AM Campen P Vise TW Marshall CJ Oldfield CJ Williams AK Dunker, J Mol Evol 2002 55 104 110 12165847 (Pubitemid 34634364)
56. A practical overview of protein disorder prediction methods. F Ferron S Longhi B Canard D Karlin, Proteins 2006 65 1 14 16856179 (Pubitemid 44320610)
57. Intrinsic disorder and functional proteomics. P Radivojac LM Iakoucheva CJ Oldfield Z Obradovic VN Uversky AK Dunker, Biophys J 2007 92 1439 1456 17158572 (Pubitemid 46393458)
58. Prediction of intrinsic disorder and its use in functional proteomics. VN Uversky P Radivojac LM Iakoucheva Z Obradovic AK Dunker, Methods Mol Biol 2007 408 69 92 18314578
59. Prediction of protein disorder at the domain level. Z Dosztanyi M Sandor P Tompa I Simon, Curr Protein Pept Sci 2007 8 161 171 17430197 (Pubitemid 46681753)
60. Prediction of protein disorder. Z Dosztanyi P Tompa, Methods Mol Biol 2008 426 103 115 18542859
61. Predicting protein disorder for N-, C-, and internal regions. X Li P Romero M Rani AK Dunker Z Obradovic, Genome Inform Ser Workshop Genome Inform 1999 10 30 40 11072340
62. Sequence complexity of disordered protein. P Romero Z Obradovic X Li EC Garner CJ Brown AK Dunker, Proteins 2001 42 38 48 11093259
63. Flavors of protein disorder. S Vucetic CJ Brown AK Dunker Z Obradovic, Proteins 2003 52 573 584 12910457 (Pubitemid 37034155)
64. Predicting intrinsic disorder from amino acid sequence. Z Obradovic K Peng S Vucetic P Radivojac CJ Brown AK Dunker, Proteins 2003 53 Suppl 6 566 572 14579347 (Pubitemid 37352217)
65. Protein intrinsic disorder toolbox for comparative analysis of viral proteins. GK-M Goh AK Dunker VN Uversky, BMC Genomics 2008 9 S4 18831795
66. The effects of the 19181919 influenza pandemic on infant and child health in Derbyshire. A Reid, Med Hist 2005 49 29 54 15730129 (Pubitemid 40144934)
67. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. RJ Russell SJ Gamblin LF Haire DJ Stevens B Xiao Y Ha JJ Skehel, Virology 2004 325 287 296 15246268 (Pubitemid 38902794)
68. Molecular characterization of low pathogenicity H7N3 avian influenza viruses isolated in Italy. LBB Di Trani P Cordioli M Muscillo E Vignolo A Moreno M Tollis, Avian Dis. 2004 48 2 376 383 15283425 (Pubitemid 39508874)
69. Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. H Wan E Sorrell H Song M Hossain G Ramirez-Nieto I Monne J Stevens G Cattoli I Capua L Chen, PLoS ONE 2008 3 e2923 18698430
70. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. MN Matrosovich S Krauss RG Webster, Virology 2001 281 156 162 11277689 (Pubitemid 32881133)
71. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. M Hatta P Gao P Halfmann Y Kawaoka, Science 2001 293 1840 1842 11546875 (Pubitemid 32845783)
72. H5N1 influenza: a protean pandemic threat. Y Guan LL Poon CY Cheung TM Ellis W Lim AS Lipatov KH Chan KM Sturm-Ramirez CL Cheung YH Leung, Proc Natl Acad Sci USA 2004 101 8156 8161 15148370 (Pubitemid 38698070)
73. Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. NV Kaverin IA Rudneva NA Ilyushina AS Lipatov S Krauss RG Webster, J Virol 2004 78 240 249 14671105 (Pubitemid 37549736)
74. Structure of antigenic sites on the haemagglutinin molecule of H5 avian influenza virus and phenotypic variation of escape mutants. NV Kaverin IA Rudneva NA Ilyushina NL Varich AS Lipatov YA Smirnov EA Govorkova AK Gitelman DK Lvov RG Webster, J Gen Virol 2002 83 2497 2505 12237433
75. Restoration of virulence of escape mutants of H5 and H9 influenza viruses by their readaptation to mice. I Rudneva N Ilyushina T Timofeeva R Webster N Kaverin, J Gen Virol 2005 86 2831 2838 16186239 (Pubitemid 41410475)
76. A Comparative Analysis of Viral Matrix Proteins Using Disorder Predictor. GKM Goh V Uversky AK Dunker, Virol J 2008 126 18947403
77. Protein Intrinsic Disorder Toolbox for Comparative Analysis of Viral Proteins. GKM Goh AK Dunker V Uversky, BMC Genomics. 2008 9 Suppl 2 S4 S7 18831795
78. Human infection by avian influenza A H5N1. KY Yuen SS Wong, Hong Kong Med J 2005 11 189 199 15951584 (Pubitemid 40826027)
79. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. KY Yuen PK Chan M Peiris DN Tsang TL Que KF Shortridge PT Cheung WK To ET Ho R Sung AF Cheng, Lancet 1998 351 467 471 9482437 (Pubitemid 28070092)
80. Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. PK Chan, Clin Infect Dis 2002 34 Suppl 2 S58 64 11938498
81. [Cytokine storm in avian influenza]. D Us, Mikrobiyol Bul 2008 42 365 380 18697437
82. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Y Ha DJ Stevens JJ Skehel DC Wiley, Proc Natl Acad Sci USA 2001 98 11181 11186 11562490 (Pubitemid 32928703)
83. Evidence of an absence: the genetic origins of the 1918 pandemic influenza virus. AH Reid JK Taubenberger TG Fanning, Nat Rev Microbiol 2004 2 909 914 15494747 (Pubitemid 39561807)
84. Interspecies transmission of influenza viruses. RG Webster GB Sharp EC Claas, Am J Respir Crit Care Med 1995 1995 152 S25 23
85. The structure and receptor binding properties of the 1918 influenza hemagglutinin. SJ Gamblin LF Haire RJ Russell DJ Stevens B Xiao Y Ha N Vasisht DA Steinhauer RS Daniels A Elliot, Science 2004 303 1838 1842 14764886 (Pubitemid 38374870)
86. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. YP Lin M Shaw V Gregory K Cameron W Lim A Klimov K Subbarao Y Guan S Krauss K Shortridge, Proc Natl Acad Sci USA 2000 97 9654 9658 10920197 (Pubitemid 30650831)
87. Influenza: Fatal immunity and the 1918 virus. YM Loo M Gale, Nature 2007 445 267 268 17230179
88. The Protein Data Bank. HM Berman Z Westbrook G Feng H Bhat H Weissig LN Sindyalov PE Bourne, Nucleic Acids Res 2000 28 235 242 10592235 (Pubitemid 30047768)
89. Biomolecules in the computer: Jmol to the rescue. A Herráez, Biochemistry and Molecular Biology Education 2006 34 255 261