Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Virology Journal
Published in: Virology Journal 1/2008

Open Access 01-12-2008 | Research

The evolution of human influenza A viruses from 1999 to 2006: A complete genome study

Authors: Karoline Bragstad, Lars P Nielsen, Anders Fomsgaard

Published in: Virology Journal | Issue 1/2008

Login to get access

Abstract

Background

Knowledge about the complete genome constellation of seasonal influenza A viruses from different countries is valuable for monitoring and understanding of the evolution and migration of strains. Few complete genome sequences of influenza A viruses from Europe are publicly available at the present time and there have been few longitudinal genome studies of human influenza A viruses. We have studied the evolution of circulating human H3N2, H1N1 and H1N2 influenza A viruses from 1999 to 2006, we analysed 234 Danish human influenza A viruses and characterised 24 complete genomes.

Results

H3N2 was the prevalent strain in Denmark during the study period, but H1N1 dominated the 2000–2001 season. H1N2 viruses were first observed in Denmark in 2002–2003. After years of little genetic change in the H1N1 viruses the 2005–2006 season presented H1N1 of greater variability than before. This indicates that H1N1 viruses are evolving and that H1N1 soon is likely to be the prevalent strain again. Generally, the influenza A haemagglutinin (HA) of H3N2 viruses formed seasonal phylogenetic clusters. Different lineages co-circulating within the same season were also observed. The evolution has been stochastic, influenced by small "jumps" in genetic distance rather than constant drift, especially with the introduction of the Fujian-like viruses in 2002–2003. Also evolutionary stasis-periods were observed which might indicate well fit viruses. The evolution of H3N2 viruses have also been influenced by gene reassortments between lineages from different seasons. None of the influenza genes were influenced by strong positive selection pressure. The antigenic site B in H3N2 HA was the preferred site for genetic change during the study period probably because the site A has been masked by glycosylations. Substitutions at CTL-epitopes in the genes coding for the neuraminidase (NA), polymerase acidic protein (PA), matrix protein 1 (M1), non-structural protein 1 (NS1) and especially the nucleoprotein (NP) were observed. The N-linked glycosylation pattern varied during the study period and the H3N2 isolates from 2004 to 2006 were highly glycosylated with ten predicted sequons in HA, the highest amount of glycosylations observed in this study period.

Conclusion

The present study is the first to our knowledge to characterise the evolution of complete genomes of influenza A H3N2, H1N1 and H1N2 isolates from Europe over a time period of seven years from 1999 to 2006. More precise knowledge about the circulating strains may have implications for predicting the following season strains and thereby better matching the vaccine composition.
Appendix
Available only for authorised users
Literature
1.
2.
Lin YP, Gregory V, Bennett M, Hay A: Recent changes among human influenza viruses. Virus Research 2004, 103: 47-52. 10.1016/j.virusres.2004.02.011CrossRefPubMed
3.
Paget WJ, Meerhoff TJ, Goddard NL: Mild to moderate influenza activity in Europe and the detection of novel A(H1N2) and B viruses during the winter of 2001-02. Euro Surveill 2002, 7: 147-157.PubMed
4.
Ellis JS, Alvarez-Aguero A, Gregory V, Lin YP, Hay A, Zambon MC: Influenza AH1N2 viruses, United Kingdom, 2001-02 influenza season. Emerg Infect Dis 2003, 9: 304-310.PubMedCentralCrossRefPubMed
5.
Chi SX, Bolar TV, Zhao P, Tam JS, Rappaport R, Cheng S: Molecular Evolution of Human Influenza A/H3N2 Virus in Asia adn Europe from 2001 to 2003. Journal of Clinical Microbiology 2005, 43: 6130-6132. 10.1128/JCM.43.12.6130-6132.2005PubMedCentralCrossRefPubMed
6.
Barr IG, Komadina N, Hurt A, Iannello C, Tomasov R, Shaw R, Durrant C, Sjogren H, Hampson AW: An Influenza A (H3) Reassortant Was Epidemic in Australia and New Zealand in 2003. J Med Virol 2005, 76: 391-397. 10.1002/jmv.20374CrossRefPubMed
7.
Ghedin E, Sengamalay NA, Shumway M, Zaborsky J, Feldblyum T, Subbu V, Spiro DJ, Sitz J, Koo H, Bolotov P, Dernovoy D, Tatusova T, Bao Y, St George K, Taylor J, Lipman DJ, Fraser CM, Taubenberger JK, Salzberg SL: Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 2005, 437: 1162-1166. 10.1038/nature04239CrossRefPubMed
8.
9.
Macken C, Lu H, Goodman J, Boykin L: The value of a database in surveillance and vaccine selection. In Options for the Control of Influenza IV. Edited by: Osterhaus A, Cox N and Hampson AW. Amsterdam: Elsevier Science; 2001:103-106.
10.
Hardy CT, Young SA, Webster RG, Naeve CW, Owens RJ: Egg fluids and cells of the chorioallantoic membrane of embryonated chicken eggs can select different variants of influenza A (H3N2) viruses. Virology 1995, 211: 302-306. 10.1006/viro.1995.1405CrossRefPubMed
11.
Suzuki Y: Natural Selection on the Influenza Virus Genome. Mol Biol Evol 2006, 23: 1902-1911. 10.1093/molbev/msl050CrossRefPubMed
12.
Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A: Human memory CTL response specific for influenza A virus is broad and multispecific. Hum Immunol 2000, 61: 438-452. 10.1016/S0198-8859(00)00105-1CrossRefPubMed
13.
Fanning TG, Reid AH, Taubenberger JK: Influenza A Virus Neuraminidase: Regions of the Protein Potentially Involved in Virus-Host Interactions. Virology 2000, 276: 417-423. 10.1006/viro.2000.0578CrossRefPubMed
14.
Wang M, Lamberth K, Harndahl M, Roder G, Stryhn A, Larsen MV, Nielsen M, Lundegaard C, Tang ST, Dziegiel MH, Rosenkvist J, Pedersen AE, Buus S, Claesson MH, Lund O: CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 2007, 25: 2823-2831. 10.1016/j.vaccine.2006.12.038CrossRefPubMed
15.
DiBrino M, Tsuchida T, Turner RV, Parker KC, Coligan JE, Biddison WE: HLA-A1 and HLA-A3 T cell epitopes derived from influenza virus proteins predicted from peptide binding motifs. J Immunol 1993, 151: 5930-5935.PubMed
16.
Guo HC, Jardetzky TS, Garrett TP, Lane WS, Strominger JL, Wiley DC: Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature 1992, 360: 364-366. 10.1038/360364a0CrossRefPubMed
17.
Berkhoff EG, Geelhoed-Mieras MM, Fouchier RA, Osterhaus AD, Rimmelzwaan GF: Assessment of the extent of variation in influenza A virus cytotoxic T-lymphocyte epitopes by using virus-specific CD8+ T-cell clones. J Gen Virol 2007, 88: 530-535. 10.1099/vir.0.82120-0CrossRefPubMed
18.
DiBrino M, Parker KC, Margulies DH, Shiloach J, Turner RV, Biddison WE, Coligan JE: The HLA-B14 peptide binding site can accommodate peptides with different combinations of anchor residues. J Biol Chem 1994, 269: 32426-32434.PubMed
19.
Vartdal F, Johansen BH, Friede T, Thorpe CJ, Stevanovic S, Eriksen JE, Sletten K, Thorsby E, Rammensee HG, Sollid LM: The peptide binding motif of the disease associated HLA-DQ (alpha 1* 0501, beta 1* 0201) molecule. Eur J Immunol 1996, 26: 2764-2772. 10.1002/eji.1830261132CrossRefPubMed
20.
Rohrlich PS, Cardinaud S, Firat H, Lamari M, Briand P, Escriou N, Lemonnier FA: HLA-B*0702 transgenic, H-2KbDb double-knockout mice: phenotypical and functional characterization in response to influenza virus. Int Immunol 2003, 15: 765-772. 10.1093/intimm/dxg073CrossRefPubMed
21.
Bright RA, Medina MJ, Xu X, Perez-Oronoz G, Wallis TR, Davis XM, Povinelli L, Cox NJ, Klimov AI: Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 2005, 366: 1175-1181. 10.1016/S0140-6736(05)67338-2CrossRefPubMed
22.
Hay AJ, Zambon MC, Wolstenholme AJ, Skehel JJ, Smith MH: Molecular basis of resistance of influenza A viruses to amantadine. J Antimicrob Chemother 1986, 18 Suppl B: 19-29.PubMed
23.
Jameson J, Cruz J, Terajima M, Ennis FA: Human CD8+ and CD4+ T lymphocyte memory to influenza A viruses of swine and avian species. J Immunol 1999, 162: 7578-7583.PubMed
24.
DiBrino M, Parker KC, Margulies DH, Shiloach J, Turner RV, Biddison WE, Coligan JE: Identification of the peptide binding motif for HLA-B44, one of the most common HLA-B alleles in the Caucasian population. Biochemistry 1995, 34: 10130-10138. 10.1021/bi00032a005CrossRefPubMed
25.
Gregory V, Bennett M, Orkhan MH, Al Hajjar S, Varsano N, Mendelson E, Zambon M, Ellis J, Hay A, Lin YP: Emergence of Influenza A H1N2 Reassortant Viruses in the Human Population during 2001. Virology 2002, 300: 1-7. 10.1006/viro.2002.1513CrossRefPubMed
26.
Xu X, Smith CB, Mungall BA, Lindstrom SE, Hall HE, Subbarao K, Cox NJ, Klimov A: Intercontinental circulation of human influenza A(H1N2) reassortant viruses during the 2001-2002 influenza season. J Infect Dis 2002, 186: 1490-1493. 10.1086/344738CrossRefPubMed
27.
Lindstrom SE, Hiromoto Y, Nerome R, Omoe K, Sugita S, Yamazaki Y, Takahashi T, Nerome K: Phylogenetic analysis of the entire genome of influenza A (H3N2) viruses from Japan: evidence for genetic reassortment of the six internal genes. J Virol 1998, 72: 8021-8031.PubMedCentralPubMed
28.
Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, St George K, Grenfell B T, Salzberg SL, Fraser CM, Lipman DJ, Taubenberger JK: Whole-genome analysis of human influenza A virus reveales multiple persistent lineages and reassortment among recent H3N2 viruses. In PLoS Biology. Volume 3. Plos Biol; 2005:1579-1589. 10.1371/journal.pbio.0030300
29.
Centers for Disease Control and Prevention (CDC): Preliminary assessment of the effectiveness of the 2003-04 inactivated influenza vaccine--Colorado, December 2003. MMWR Morb Mortal Wkly Rep 2004, 53: 8-11.
30.
Gulati U, Wu W, Gulati S, Kumari K, Waner JL, Air GM: Mismatched hemagglutinin and neuraminidase specificities in recent human H3N2 influenza viruses. Virology 2005, 339: 12-20. 10.1016/j.virol.2005.05.009CrossRefPubMed
31.
Daum LT, Canas LC, Smith CB, Klimov A, Huff W, Barnes W, Lohman KL: Genetic and antigenic analysis of the first A/New Caledonia/20/99-like H1N1 influenza isolates reported in the Americas. Emerg Infect Dis 2002, 8: 408-412.PubMedCentralCrossRefPubMed
32.
Organization WH: Recommended composition of influenza virus vaccines for use in the 2000-2001 season. Wkly Epidemiol Rec 2000, 61-68.
33.
Wiley DC, Wilson IA, Skehel JJ: Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981, 289: 373-378. 10.1038/289373a0CrossRefPubMed
34.
Wang ML, Skehel JJ, Wiley DC: Comparative Analyses of the Specificities of Anti-Influenza Hemagglutinin Antibodies in Human Sera. J Virol 1985, 57: 124-128.
35.
Lambkin R, McLain L, Jones SE, Aldridge SL, Dimmock NJ: Neutralization escape mutants of type A influenza virus are readily selected by antisera from mice immunized with whole virus: a possible mechanism for antigenic drift. J Gen Virol 1994, 75: 3493-3502.CrossRefPubMed
36.
Yohannes K, Roche P, Hampson A, Miller M, Spencer J: Annual report of the National Influenza Surveillance Scheme, 2003. Commun Dis Intell 2004, 28: 160-168.
37.
Jin H, Zhou H, Liu H, Chan W, Adhikary L, Mahmood K, Lee MS, Kemble G: Two residues in the hemagglutinin of A/Fujian/411/02-like influenza viruses are responsible for antigenic drift from A/Panama/2007/99. Virology 2005, 336: 113-119. 10.1016/j.virol.2005.03.010CrossRefPubMed
38.
Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA: Mapping the Antigenic and Genetic Evolution of Influenza Virus. Science 2004, 305: 371-376. 10.1126/science.1097211CrossRefPubMed
39.
40.
Wilson IA, Cox NJ: Structural Basis of Immune Recognition of Influenza Virus Hemagglutinin. Annual Review of Immunology 1990, 8: 737-787. 10.1146/annurev.iy.08.040190.003513CrossRefPubMed
41.
Gulati U, Hwang CC, Venkatramani L, Gulati S, Stray SJ, Lee JT, Laver WG, Bochkarev A, Zlotnick A, Air GM: Antibody epitopes on the neuraminidase of a recent H3N2 influenza virus (A/Memphis/31/98). J Virol 2002, 76: 12274-12280. 10.1128/JVI.76.23.12274-12280.2002PubMedCentralCrossRefPubMed
42.
Tisdale M: Monitoring of viral susceptibility: new challenges with the development of influenza NA inhibitors. Rev Med Virol 2000, 10: 45-55. 10.1002/(SICI)1099-1654(200001/02)10:1<45::AID-RMV265>3.0.CO;2-RCrossRefPubMed
43.
Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y: Resistant influenza A viruses in children treated with oseltamivir: descriptive study. The Lancet 2004, 364: 759-765. 10.1016/S0140-6736(04)16934-1CrossRef
44.
Ilyushina NA, Govorkova EA, Webster RG: Detection of amantadine-resistant variants among avian influenza viruses isolated in North America and Asia. Virology 2005, 341: 102-106. 10.1016/j.virol.2005.07.003CrossRefPubMed
45.
Suzuki H, Saito R, Masuda H, Oshitani H, Sato M, Sato I: Emergence of amantadine-resistant influenza A viruses: epidemiological study. J Infect Chemother 2003, 9: 195-200. 10.1007/s10156-003-0262-6CrossRefPubMed
46.
Gubareva LV, Kaiser L, Hayden FG: Influenza virus neuraminidase inhibitors. Lancet 2000, 355: 827-835. 10.1016/S0140-6736(99)11433-8CrossRefPubMed
47.
Ives JA, Carr JA, Mendel DB, Tai CY, Lambkin R, Kelly L, Oxford JS, Hayden FG, Roberts NA: The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antiviral Res 2002, 55: 307-317. 10.1016/S0166-3542(02)00053-0CrossRefPubMed
48.
Bui HH, Peters B, Assarsson E, Mbawuike I, Sette A: Ab and T cell epitopes of influenza A virus, knowledge and opportunities. Proc Natl Acad Sci U S A 2007, 104: 246-251. 10.1073/pnas.0609330104PubMedCentralCrossRefPubMed
49.
Townsend AR, Skehel JJ: The influenza A virus nucleoprotein gene controls the induction of both subtype specific and cross-reactive cytotoxic T cells. J Exp Med 1984, 160: 552-563. 10.1084/jem.160.2.552CrossRefPubMed
50.
Winter G, Fields S: The structure of the gene encoding the nucleoprotein of human influenza virus A/PR/8/34. Virology 1981, 114: 423-428. 10.1016/0042-6822(81)90223-3CrossRefPubMed
51.
Abed Y, Goyette N, Boivin G: Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob Agents Chemother 2005, 49: 556-559. 10.1128/AAC.49.2.556-559.2005PubMedCentralCrossRefPubMed
52.
Bright RA, Shay DK, Shu B, Cox NJ, Klimov A: Adamantane Reasistance Among Influenza A Viruses Isolated Early During the 2005-2006 Influenza Season in the United States. JAMA 2006, 295: 891-894. 10.1001/jama.295.8.joc60020CrossRefPubMed
53.
Barr IG, Hurt AC, Iannello P, Tomasov C, Deed N, Komadina N: Increased adamantane resistance in influenza A(H3) viruses in Australia and neighbouring countries in 2005. Antiviral Res 2007, 73: 112-117. 10.1016/j.antiviral.2006.08.002CrossRefPubMed
54.
Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S: Hemagglutinin Residues of Recent Human A(H3N2) Influenza Viruses That Contribute to the Inability to Agglutinate Chicken Erythrocytes. Virology 2001, 289: 74-85. 10.1006/viro.2001.1121CrossRefPubMed
55.
Mochalova L, Gambaryan A, Romanova J, Tuzikov A, Chinarev A, Katinger D, Katinger H, Egorov A, Bovin N: Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryonated eggs. Virology 2003, 313: 473-480. 10.1016/S0042-6822(03)00377-5CrossRefPubMed
56.
Lu B, Zhou H, Ye D, Kemble G, Jin H: Improvement of Influenza A/Fujian/411/02 (H3N2) Virus Growth in Embryonated Chicken Eggs by Balancing the Hemagglutinin and Neuraminidase Activities, Using Reverse Genetics. J Virol 2005, 79: 6763-6771. 10.1128/JVI.79.11.6763-6771.2005PubMedCentralCrossRefPubMed
57.
Lu B, Zhou H, Chan W, Kemble G, Jin H: Single amino acid substitutions in the hemagglutinin of influenza A/Singapore/21/04 (H3N2) increase virus growth in embryonated chicken eggs. Vaccine 2006, 24: 6691-6693. 10.1016/j.vaccine.2006.05.062CrossRefPubMed
58.
Abe Y, Takashita E, Sugawara K, Matsuzaki Y, Muraki Y, Hongo S: Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J Virol 2004, 78: 9605-9611. 10.1128/JVI.78.18.9605-9611.2004PubMedCentralCrossRefPubMed
59.
60.
Xu X, Cox NJ, Bender CA, Regnery HL, Shaw MW: Genetic variation in neuraminidase genes of influenza A (H3N2) viruses. Virology 1996, 224: 175-183. 10.1006/viro.1996.0519CrossRefPubMed
61.
Wolf YI, Viboud C, Holmes EC, Koonin EV, Lipman DJ: Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biol Direct 2006, 1: 34. 10.1186/1745-6150-1-34PubMedCentralCrossRefPubMed
62.
Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J, George KS, Griesemer SB, Ghedi E, Sengamalay NA, Spiro DJ, Volkov I, Grenfell BT, Lipman DJ, Taubenberger JK, Holmes EC: Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus. PLoS Pathog 2006, 2: e125. 10.1371/journal.ppat.0020125PubMedCentralCrossRefPubMed
63.
Bush RM, Fitch WM, Bender CA, Cox NJ: Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol Biol Evol 1999, 16: 1457-1465.CrossRefPubMed
64.
Bragstad K, Jorgensen PH, Handberg KJ, Fomsgaard A: Genome characterisation of the newly discovered avian influenza A H5N7 virus subtype combination. Arch Virol 2006.
65.
Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR: Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 2001, 146: 2275-2289. 10.1007/s007050170002CrossRefPubMed
66.
Bragstad K, Jorgensen PH, Handberg KJ, Mellergaard S, Corbet S, Fomsgaard A: New avian influenza A virus subtype combination H5N7 identified in Danish mallard ducks. Virus Res 2005, 109: 181-190. 10.1016/j.virusres.2004.12.004CrossRefPubMed
67.
68.
69.
Swafford DL: Phylogenetic Analysis Using Parsimony, PAUP. Sinauer Associates, Inc. Publishers; 2003.
70.
Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21: 2531-2533. 10.1093/bioinformatics/bti320CrossRefPubMed
71.
Suzuki Y, Gojobori T: A method for detecting positive selection at single amino acid sites. Mol Biol Evol 1999, 16: 1315-1328.CrossRefPubMed
72.
Pond SL, Frost SD, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21: 676-679. 10.1093/bioinformatics/bti079CrossRefPubMed
73.
Kosakovsky Pond SL, Frost SDW: Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection. Mol Biol Evol 2005, 22: 1208-1222. 10.1093/molbev/msi105CrossRefPubMed
74.
75.
Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, Kuiken C, Korber B: Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 2004, 14: 1229-1246. 10.1093/glycob/cwh106CrossRefPubMed
76.
77.
78.
Air GM, Els MC, Brown LE, Laver WG, Webster RG: Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. Virology 1985, 145: 237-248. 10.1016/0042-6822(85)90157-6CrossRefPubMed
79.
Caton AJ, Brownlee GG, Yewdell JW, Gerhard W: The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982, 31: 417-427. 10.1016/0092-8674(82)90135-0CrossRefPubMed
80.
Colman PM, Varghese JN, Laver WG: Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 1983, 303: 41-44. 10.1038/303041a0CrossRefPubMed
81.
Fanning TG, Taubenberger JK: Phylogenetically important regions of the Influenza A H1 hemagglutinin protein. Virus Research 1999, 65: 33-42. 10.1016/S0168-1702(99)00098-2CrossRefPubMed
82.
Wiley DC, Skehel JJ: The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem 1987, 56: 365-394. 10.1146/annurev.bi.56.070187.002053CrossRefPubMed
83.
84.
Air GM, Laver WG: The neuraminidase of influenza virus. Proteins 1989, 6: 341-356. 10.1002/prot.340060402CrossRefPubMed
Metadata
Title
The evolution of human influenza A viruses from 1999 to 2006: A complete genome study
Authors
Karoline Bragstad
Lars P Nielsen
Anders Fomsgaard
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2008
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-5-40

Other articles of this Issue 1/2008

Virology Journal 1/2008 Go to the issue

Research

Functional characterization of the vaccinia virus I5 protein

Hypothesis

Stone age diseases and modern AIDS

Short report

Modeling the effects of drug resistant influenza virus in a pandemic

Research

Ex vivo promoter analysis of antiviral heat shock cognate 70B gene in Anopheles gambiae

Short report

Epitope characterization of the protective monoclonal antibody VN04-2 shows broadly neutralizing activity against highly pathogenic H5N1

Short report

Molecular profiling of T-helper immune genes during dengue virus infection
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits