Dissecting influenza virus pathogenesis uncovers a novel chemical approach to combat the infection

Virology

Volumn 435, Issue 1, 2013, Pages 92-101

  Oldstone, Michael B A ^a   Teijaro, John R ^a   Walsh, Kevin B ^a,b   Rosen, Hugh ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b GENENTECH INC   (United States)

Author keywords

Cytokine storm; Influenza; Pulmonary endothelial cells; S1P receptor agonist therapy; Sphingosine 1 phosphate (S1P) receptor (rec) signaling

Indexed keywords

ALPHA INTERFERON; CYM 5442; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSELTAMIVIR; RANTES; RP 002; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS SIALIDASE;

ADAPTIVE IMMUNITY; ANTIVIRAL ACTIVITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHEMOPROPHYLAXIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE STORM; DISEASE ASSOCIATION; DISEASE COURSE; DRUG MECHANISM; DRUG POTENTIATION; DRUG STRUCTURE; DRUG TARGETING; EVIDENCE BASED MEDICINE; HUMAN; IMMUNOREGULATION; INFLAMMATORY INFILTRATE; INFLUENZA; INFLUENZA A (H1N1); INFLUENZA VIRUS; INNATE IMMUNITY; LUNG ENDOTHELIUM; MORBIDITY; MORTALITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS VIRULENCE;

ANIMALS; CYTOKINES; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; ENDOTHELIAL CELLS; ENZYME INHIBITORS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; LUNG; MICE; MYCOTOXINS; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; RECEPTORS, LYSOSPHINGOLIPID; SURVIVAL RATE;

MURINAE; ORTHOMYXOVIRIDAE;

EID: 84870710094     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.09.039     Document Type: Review

References (42)

1. Ahmed R., Oldstone M.B.A., Palese P. Protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic. Nat. Immunol. 2007, 8:1188-1193.
2. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., Lew A.M., Shortman K., Heath W.R., Carbone F.R. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006, 25:153-162.
3. Arankalle V.A., Lole K.S., Arya R.P., Tripathy A.S., Ramdasi A.Y., Chadha M.S., Sangle S.A., Kadam D.B. Role of host immune response and viral load in the differential outcome of pandemic H1N1 (2009) influenza virus infection in Indian patients. PLoS One 2010, 5:e13099.
4. Baskin C.R., Bielefeldt-Ohmann H., Tumpey T.M., Sabourin P.J., Long J.P., Garcia-Sastre A., Tolnay A.E., Albrecht R.A., Pyles J.A., Olson P.H., Aicher L.D., Rosenzweig E.R., Murali-Krishna K., Clark E.A., Kotur M.S., Fornek J.L., Proll S., Palermo R.E., Sabourin C.L., Katze M.G. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3455-3460.
5. Baumgarth N., Kelso A. Functionally distinct T cells in three compartments of the respiratory tract after influenza virus infection. Eur. J. Immunol. 1996, 26:2189-2197.
6. Belz G.T., Smith C.M., Kleinert L., Reading P., Brooks A., Shortman K., Carbone F.R., Heath W.R. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8670-8675.
7. Cahalan S.M., Gonzalez-Cabrera P.J., Sarkisyan G., Nguyen N., Schaeffer M.T., Huang L., Yeager A., Clemons B., Scott F., Rosen H. Actions of a picomolar short-acting S1P1 agonist in S1P1-eGFP knock-in mice. Nat. Chem. Biol. 2011, 7:254-256.
8. Cheng X.W., Lu J., Wu C.L., Yi L.N., Xie X., Shi X.D., Fang S.S., Zan H., Kung H.F., He M.L. Three fatal cases of pandemic 2009 influenza A virus infection in Shenzhen are associated with cytokine storm. Respir. Physiol. Neurobiol. 2011, 175:185-187.
9. Chou Y.Y., Albrecht R.A., Pica N., Lowen A.C., Richt J.A., Garcia-Sastre A., Palese P., Hai R. The M segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the guinea pig model. J. Virol. 2011, 85:11235-11241.
10. Dawood F.S., Iuliano A.D., Reed C., Meltzer M.I., Shay D.K., Cheng P.Y., Bandaranayake D., Breiman R.F., Brooks W.A., Buchy P., Feikin D.R., Fowler K.B., Gordon A., Hien N.T., Horby P., Huang Q.S., Katz M.A., Krishnan A., Lal R., Montgomery J.M., Molbak K., Pebody R., Presanis A.M., Razuri H., Steens A., Tinoco Y.O., Wallinga J., Yu H., Vong S., Bresee J., Widdowson M.A. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modeling study. Lancet Infect. Dis. 2012, 9:687-695.
11. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J., Chau T.N., Hoang D.M., Chau N.V., Khanh T.H., Dong V.C., Qui P.T., Cam B.V., Ha do Q., Guan Y., Peiris J.S., Chinh N.T., Hien T.T., Farrar J. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006, 12:1203-1207.
12. Fujiwara Y., Osborne D.A., Walker M.D., Wang D.A., Bautista D.A., Liliom K., Van Brocklyn J.R., Parrill A.L., Tigyi G. Identification of the hydrophobic ligand binding pocket of the S1P1 receptor. J. Biol. Chem. 2007, 282:2374-2385.
13. Fujiwara Y., Sardar V., Tokumura A., Baker D., Murakami-Murofushi K., Parrill A.L., Tigyi G. Identification of residues responsible for ligand recognition and regioisomeric selectivity of lysophosphatidic acid receptors expressed in mammalian cells. J. Biol. Chem. 2005, 280:35038-35050.
14. Fukuyama S., Kawaoka Y. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr. Opin. Immunol. 2011, 23:481-486.
15. Hai R., Schmolke M., Varga Z.T., Manicassamy B., Wang T.T., Belser J.A., Pearce M.B., Garcia-Sastre A., Tumpey T.M., Palese P. PB1-F2 expression by the 2009 pandemic H1N1 influenza virus has minimal impact on virulence in animal models. J. Virol. 2010, 84:4442-4450.
16. Hanson M.A., Roth C.B., Jo E., Griffith M.T., Scott F.L., Reinhart G., Desale H., Clemons B., Cahalan S.M., Schuerer S.C., Sanna M.G., Han G.W., Kuhn P., Rosen H., Stevens R.C. Crystal structure of a lipid G protein-coupled receptor. Science 2012, 335:851-855.
17. Inagaki Y., Pham T.T., Fujiwara Y., Kohno T., Osborne D.A., Igarashi Y., Tigyi G., Parrill A.L. Sphingosine-1-phosphate analogue recognition and selectivity at S1P4 within the endothelial differentiation gene family of receptors. Biochem. J. 2005, 389:187-195.
18. Jo E., Sanna M.G., Gonzalez-Cabrera P.J., Thangada S., Tigyi G., Osborne D.A., Hla T., Parrill A.L., Rosen H. S1P1-selective in vivo-active agonists from high-throughput screening: off-the-shelf chemical probes of receptor interactions, signaling, and fate. Chem. Biol. 2005, 12:703-715.
19. Johnson N.P., Mueller J. Updating the accounts: global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull. Hist. Med. 2002, 76:105-115.
20. Kash J.C., Tumpey T.M., Proll S.C., Carter V., Perwitasari O., Thomas M.J., Basler C.F., Palese P., Taubenberger J.K., Garcia-Sastre A., Swayne D.E., Katze M.G. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 2006, 443:578-581.
21. Kobasa D., Jones S.M., Shinya K., Kash J.C., Copps J., Ebihara H., Hatta Y., Kim J.H., Halfmann P., Hatta M., Feldmann F., Alimonti J.B., Fernando L., Li Y., Katze M.G., Feldmann H., Kawaoka Y. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007, 445:319-323.
22. Lee N., Wong C.K., Chan P.K., Chan M.C., Wong R.Y., Lun S.W., Ngai K.L., Lui G.C., Wong B.C., Lee S.K., Choi K.W., Hui D.S. Cytokine response patterns in severe pandemic 2009 H1N1 and seasonal influenza among hospitalized adults. PLoS One 2011, 6:e26050.
23. Marcelin G., Aldridge J.R., Duan S., Ghoneim H.E., Rehg J., Marjuki H., Boon A.C., McCullers J.A., Webby R.J. Fatal outcome of pandemic H1N1 2009 influenza virus infection is associated with immunopathology and impaired lung repair, not enhanced viral burden, in pregnant mice. J. Virol. 2011, 85:11208-11219.
24. Marsolais D., Hahm B., Walsh K.B., Edelmann K.H., McGavern D.B., Hatta Y., Kawaoka Y., Rosen H., Oldstone M.B.A. A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1560-1565.
25. McGavern D., Christen U., Oldstone M.B.A. Molecular anatomy of antigen-specific CD8+ T cell engagement and synapse formation in vivo. Nat. Immunol. 2002, 3:918-925.
26. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Hughes M., Perez D.R., Donis R., Hoffmann E., Hobom G., Kawaoka Y. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9345-9350.
27. Nguyen H.T., Fry A.M., Gubareva L.V. Neuraminidase inhibitor resistance in influenza viruses and laboratory testing methods. Antivir. Ther. 2012, 17:159-173.
28. Orozovic G., Orozovic K., Lennerstrand J., Olsen B. Detection of resistance mutations to antivirals oseltamivir and zanamivir in avian influenza A viruses isolated from wild birds. PLoS One 2011, 6:e16028.
29. Parrill A.L., Baker D.L., Wang D.A., Fischer D.J., Bautista D.A., Van Brocklyn J.R., Spiegel S., Tigyi G. Structural features of EDG1 receptor-ligand complexes revealed by computational modeling and mutagenesis. Ann. N. Y. Acad. Sci. 2000, 905:330-339.
30. Parrill A.L., Wang D.A., Bautista D.L., Van Brocklyn J.R., Lorincz Z., Fischer D.J., Baker D.L., Liliom K., Spiegel S., Tigyi G. Identification of Edg1 receptor residues that recognize sphingosine-1-phosphate. J. Biol. Chem. 2000, 275:39379-39384.
31. Rosen H., Gonzalez-Cabrera P.J., Sanna M.G., Brown S. Sphingosine-1-phosphate receptor signaling. Annu. Rev. Biochem. 2009, 78:743-768.
32. Rosen H., Sanna M.G., Cahalan S.M., Gonzalez-Cabrera P.J. Tipping the gatekeeper: S1P regulation of endothelial barrier function. Trends Immunol. 2007, 28:102-107.
33. Schurer S.C., Brown S.J., Gonzalez-Cabrera P.J., Schaeffer M.T., Chapman J., Jo E., Chase P., Spicer T., Hodder P., Rosen H. Ligand-binding pocket shape differences between sphingosine-1-phosphate (S1P) receptors S1P1 and S1P3 determine efficiency of chemical probe identification by ultrahigh-throughput screening. ACS Chem. Biol. 2008, 3:486-498.
34. Scott L.J. Fingolimod: a review of its use in the management of relapsing-remitting multiple sclerosis. CNS Drugs 2011, 25:673-698.
35. Song M.S., Pascua P.N., Lee J.H., Baek Y.H., Park K.J., Kwon H.I., Park S.J., Kim C.J., Kim H., Webby R.J., Webster R.G., Choi Y.K. Virulence and genetic compabitility of polymerase reassortant viruses derived from the pandemic (H1N1) 2009 influenza virus and circulating influenza A viruses. J. Virol. 2011, 85:6275-6286.
36. Steinman R.M., Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 2006, 311:17-58.
37. Teijaro J.R., Walsh K.B., Cahalan S.M., Fremgen D.M., Roberts E., Scott F., Martinborough E., Peach R., Oldstone M.B.A., Rosen H. Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 2011, 146:980-991.
38. Walsh K.B., Teijaro J.R., Wilker P.R., Jatzek A., Fremgen D.M., Das S.C., Watanabe T., Hatta M., Shinya K., Suresh M., Kawaoka Y., Rosen H., Oldstone M.B.A Suppression of cytokine storm with a sphingosine analog provides protection against pathogenic influenza virus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:12018-12023.
39. Wang B., Dwyer D.E., Blyth C.C., Soedjono M., Shi H., Kesson A., Ratnamohan M., McPhie K., Cunningham A.L., Saksena N.K. Detection of the rapid emergence of the H275Y mutation associated with oseltamivir resistance in severe pandemic influenza virus A/H1N1 09 infections. Antivir. Res. 2010, 87:16-21.
40. Wang D.A., Lorincz Z., Bautista D.L., Liliom K., Tigyi G., Parrill A.L. A single amino acid determines lysophospholipid specificity of the S1P1 (EDG1) and LPA1 (EDG2) phospholipid growth factor receptors. J. Biol. Chem. 2001, 276:49213-49220.
41. Watanabe T., Imai M., Watanabe S., Shinya K., Hatta M., Li C., Neumann G., Ozawa M., Hanson A., Zhong G., Fukuyama S., Kawakami E., Simmons H.A., Schenkman D., Brunner K., Capuano S.V.r., Weinfurter J.T., Kilander A., Dudman S.G., Suresh M., Hungnes O., Friedrich T.C., Kawaoka Y. Characterization in vitro and in vivo of pandemic (H1N1) 2009 viruses isolated from patients. J. Virol. 2012, 86:9361-9368.
42. Zhang Y., Sun H., Fan L., Ma Y., Sun Y., Pu J., Yang J., Qiao J., Ma G., Liu J. Acute respiratory distress syndrome induced by a swine 2009 H1N1 variant in mice. PLoS One 2012, 7:e29347.