Inhibition of lectin-mediated innate host defences in vivo modulates disease severity during influenza virus infection

Immunology and Cell Biology

Volumn 89, Issue 3, 2011, Pages 482-491

  Tate, Michelle D ^a   Brooks, Andrew G ^a   Reading, Patrick C ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WHO COLLABORATING CENTRE FOR REFERENCE AND RESEARCH ON INFLUENZA   (Australia)

Author keywords

collectin; inflammation; influenza; innate; macrophage

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; LECTIN; MANNAN; MANNOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLYCOSYLATION; HISTOPATHOLOGY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG EDEMA; LUNG FLUID; MALE; MORTALITY; MOUSE; NONHUMAN; RAT; VIRUS NEUTRALIZATION; VIRUS PNEUMONIA; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELL LINE; DOGS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; INFLUENZA A VIRUS, H1N1 SUBTYPE; LEUKOCYTES; MACROPHAGES; MALE; MANNANS; MANNOSE-BINDING LECTIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA; PULMONARY EDEMA; RESPIRATORY SYSTEM; VIRUS REPLICATION;

MUS; ORTHOMYXOVIRIDAE;

EID: 79952814603     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2010.113     Document Type: Article

References (69)

1. Skehel JJ, Wiley DC Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 2000; 69: 531-569.
2. Wright PF, Webster RG. Fields Virology, 4th edn. Lippincott, Williams & Wilkins: Philadelphia, PA, USA, 2001.
3. Wagner R, Matrosovich M, Klenk HD. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 2002; 12: 159-166. (Pubitemid 34516947)
4. Wiley DC, Wilson IA, Skehel JJ. Structural identification of theantibody-bindingsitesof Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981; 289: 373-378. (Pubitemid 11135143)
5. Seidel W, Kunkel F, Geisler B, Garten W, Herrmann B, Dohner L et al. Intraepidemic variants of influenza virus H3 hemagglutinin differing in the number of carbohydrate sidechains. Arch Virol 1991; 120: 289-296.
6. Ohuchi M, Ohuchi R, Feldmann A, Klenk HD. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 1997; 71: 8377-8384. (Pubitemid 27446417)
7. Anders EM, Hartley CA, Jackson DC Bovine and mouse serum beta inhibitors of influenza A viruses are mannose-binding lectins. Proc Natl Acad Sci USA 1990; 87: 4485-4489.
8. Kawaoka Y, Webster RG. Interplay between carbohydrate in the stalk and the length of the connecting peptide determines the cleavability of influenza virus hemagglutinin. J Virol 1989; 63: 3296-3300. (Pubitemid 19181386)
9. Klenk HD, Wagner R, Heuer D, Wolff T. Importance of hemagglutinin glycosylation for the biological functions of influenza virus. Virus Res 2002; 82: 73-75. (Pubitemid 34273715)
10. Hartshorn KL, White MR, Voelker DR, Coburn J, Zaner K, Crouch EC Mechanism of binding of surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem J 2000; 351 (Pt 2): 449-458.
11. Hartshorn KL, White MR, Shepherd V, Reid K, Jensenius JC, Crouch EC Mechanisms of anti-influenza activity of surfactant proteins A and D: comparison with serum collectins. Am J Physiol 1997; 273: L1156-L1166.
12. Reading PC, Morey LS, Crouch EC, Anders EM. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J Virol 1997; 71: 8204-8212. (Pubitemid 27446395)
13. Tecle T, White MR, Crouch EC, Hartshorn KL. Inhibition of influenza viral neura-minidaseactivitybycollectins. Arch Virol 2007; 152: 1731-1742.
14. LeVine AM, Whitsett JA, Hartshorn KL, Crouch EC, Korfhagen TR. Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J Immunol 2001; 167: 5868-5873. (Pubitemid 33062780)
15. Vigerust DJ, Ulett KB, Boyd KL, Madsen J, Hawgood S, McCullers JA. N-linked glycosylation attenuates H3N2 influenza viruses. J Virol 2007; 81: 8593-8600. (Pubitemid 47242833)
16. Hawgood S, Brown C, Edmondson J, Stumbaugh A, Allen L, Goerke J et al. Pulmonary collectins modulate strain-specific influenza a virus infection and host responses. J Virol 2004; 78: 8565-8572. (Pubitemid 39025122)
17. Reading PC, Miller JL, Anders EM. Involvement of the mannose receptor in infection of macrophages by influenza virus. J Virol 2000; 74: 5190-5197. (Pubitemid 30313859)
18. Ikegami M, Na CL, Korfhagen TR, Whitsett JA. Surfactant protein D influences surfactant ultrastructure and uptake by alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 2005; 288: L552-L561. (Pubitemid 40229522)
19. Ikegami M, Whitsett JA, Jobe A, Ross G, Fisher J, Korfhagen T. Surfactant meta-bolism in SP-D gene-targeted mice. Am J Physiol Lung Cell Mol Physiol 2000; 279: L468-L476.
20. Korfhagen TR, Sheftelyevich V, Burhans MS, Bruno MD, Ross GF, Wert SE et al. Surfactant protein-D regulates surfactant phospholipid homeostasis in vivo. J Biol Chem 1998; 273: 28438-28443. (Pubitemid 28496149)
21. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W. Theantigenic structureof the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982; 31: 417-427. (Pubitemid 13178866)
22. Rodgers B, Mims CA. Interaction of influenza virus with mouse macrophages. Infect Immun 1981; 31: 751-757. (Pubitemid 11146258)
23. Wells MA, Albrecht P, Daniel S, Ennis FA. Host defense mechanisms against influenza virus: interaction of influenza virus with murine macrophages in vitro. Infect Immun 1978; 22: 758-762. (Pubitemid 9083962)
24. Peschke T, Bender A, Nain M, Gemsa D. Role of macrophage cytokines in influenza A virus infections. Immunobiology 1993; 189: 340-355. (Pubitemid 24001405)
25. Wijburg OL, DiNataleS, Vadolas J, van Rooijen N, Strugnell RA. Alveolar macrophages regulate the induction of primary cytotoxic T-lymphocyte responses during influenza virus infection. J Virol 1997; 71: 9450-9457. (Pubitemid 27492389)
26. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ et al. Pathogenicity of influenza viruseswith genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 2005; 79: 14933-14944. (Pubitemid 41636290)
27. Reading PC, Whitney PG, Barr DP, Smyth MJ, Brooks AG. NK cells contribute to the early clearance of HSV-1 from the lung but cannot control replication in the central nervous system following intranasal infection. Eur J Immunol 2006; 36: 897-905.
28. Stewart TS, Ballou CE. A comparison of yeast mannans and phosphomannans by acetolysis. Biochemistry 1968; 7: 1855-1863.
29. Ning ZY, Luo MY, Qi WB, Yu B, Jiao PR, Liao M. Detection of expression of influenza virus receptors in tissues of BALB/c mice by histochemistry. Vet Res Commun 2009; 33: 895-903.
30. Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG et al. Influenza virus receptor specificityand cell tropism in mouse and human airway epithelial cells. J Virol 2006; 80: 7469-7480. (Pubitemid 44092569)
31. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H et al. Aberrant innate immune response in lethal infectionof macaques withthe 1918 influenzavirus. Nature 2007; 445: 319-323. (Pubitemid 46122819)
32. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF et al. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 2002; 360: 1831-1837. (Pubitemid 35449422)
33. Xing Z, Kirpalani H, Torry D, Jordana M, Gauldie J. Polymorphonuclear leukocytes as a significant source of tumor necrosis factor-alpha in endotoxin-challenged lung tissue. Am J Pathol 1993; 143: 1009-1015. (Pubitemid 24070541)
34. Gottschalk A, Belyavin G, Biddle F. Glycoproteins as influenza virus hemagglutinin inhibitors and as cellular receptors. In Glycoproteins. Theircomposition, structure and function 1972, Edited by A. Gottschalk. 1082-1096.
35. Hartshorn KL, Sastry K, White MR, Anders EM, Super M, Ezekowitz RA et al. Human mannose-binding protein functions as an opsonin for influenza A viruses. J Clin Invest 1993; 91: 1414-1420. (Pubitemid 23127341)
36. Malhotra R, Haurum JS, Thiel S, Sim RB. Bindingof human collectins (SP-Aand MBP) to influenza virus. Biochem J 1994; 304 (Pt 2): 455-461. (Pubitemid 24368224)
37. Hartley CA, Jackson DC, Anders EM. Two distinct serum mannose-binding lectins function as beta inhibitors of influenza virus: identification of bovine serum beta inhibitor as conglutinin. J Virol 1992; 66: 4358-4363.
38. Hanaoka K, Pritchett TJ, Takasaki S, Kochibe N, Sabesan S, Paulson JC et al. 4-O-acetyl-N-acetylneuraminic acid in the N-linked carbohydrate structures of equine and guinea pig alpha 2-macroglobulins, potent inhibitors of influenza virus infection. J Biol Chem 1989; 264: 9842-9849. (Pubitemid 19159248)
39. Pritchett TJ, Paulson JC. Basis for the potent inhibition of influenza virus infection by equine and guinea pig alpha 2-macroglobulin. J Biol Chem 1989; 264: 9850-9858. (Pubitemid 19159249)
40. Hartshorn KL, Webby R, White MR, Tecle T, Pan C, Boucher S et al. Role of viral hemagglutinin glycosylation in anti-influenza activities of recombinant surfactant protein D. Respir Res 2008; 9: 65.
41. Postle AD, Mander A, Reid KB, Wang JY, Wright SM, Moustaki M et al. Deficient hydrophilic lung surfactant proteins A and D with normal surfactant phospholipid molecular species in cystic fibrosis. Am J Respir Cell Mol Biol 1999; 20: 90-98. (Pubitemid 129504846)
42. Sims MW, Tal-Singer RM, Kierstein S, Musani AI, Beers MF, Panettieri RA et al. Chronic obstructive pulmonary disease and inhaled steroids alter surfactant protein D (SP-D) levels: a cross-sectional study. Respir Res 2008; 9: 13.
43. Suzuki Y, Nagao Y, Kato H, Matsumoto M, Nerome K, Nakajima K et al. Human influenza A virus hemagglutinin distinguishes sialyloligosaccharides in membrane-associated gangliosides as its receptor which mediates the adsorption and fusion processes of virus infection. Specificity for oligosaccharides and sialic acids and the sequence to which sialic acid is attached. J Biol Chem 1986; 261: 17057-17061. (Pubitemid 17210357)
44. White MR, Crouch E, van Eijk M, Hartshorn M, Pemberton L, Tornoe I et al. Cooperative anti-influenza activities of respiratory innate immune proteins and neuraminidase inhibitor. Am J Physiol Lung Cell Mol Physiol 2005; 288: L831-L840. (Pubitemid 40547908)
45. Benne CA, Kraaijeveld CA, van Strijp JA, Brouwer E, Harmsen M, Verhoef J et al. Interactions ofsurfactant protein A with influenza Aviruses: bindingand neutralization. J Infect Dis 1995; 171: 335-341.
46. Reading PC, Bozza S, Gilbertson B, Tate M, Moretti S, Job ER et al. antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J Immunol 2008; 180: 3391-3398.
47. Gazi U, Martinez-Pomares L. Influence of the mannose receptor in host immune responses. Immunobiology 2009; 214: 554-561. Epub 2009 Jan 21.
48. Kirby AC, Raynes JG, Kaye PM. CD11b regulates recruitment of alveolar macrophages but not pulmonary dendritic cells after pneumococcal challenge. J Infect Dis 2006; 193:205-213. (Pubitemid 43113482)
49. Tate MD, Pickett DL, van Rooijen N, Brooks AG, Reading PC Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 2010; 84: 7569-7580.
50. Rojas M, Woods CR, Mora AL, Xu J, Brigham KL. Endotoxin-induced lung injury in mice: structural, functional, and biochemical responses. Am J Physiol Lung Cell Mol Physiol 2005; 288: L333-L341. (Pubitemid 40105372)
51. Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2008; 295: L379-L399.
52. Polito AJ, Proud D. Epithelia cells as regulators of airway inflammation. J Allergy Clin Immunol 1998; 102: 714-718. (Pubitemid 28543518)
53. Hippenstiel S, Opitz B, Schmeck B, Suttorp N. Lung epithelium as a sentinel and effector system in pneumonia-molecular mechanisms of pathogen recognition and signaltransduction. Respir Res 2006; 7: 97.
54. Matute-Bello G, Liles WC, Steinberg KP, Kiener PA, Mongovin S, Chi EY et al. Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS). J Immunol 1999; 163: 2217-2225. (Pubitemid 29382230)
55. Li X, Rayford H, Shu R, Zhuang J, Uhal BD. Essential roleforcathepsin D in bleomycin-induced apoptosis of alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004; 287: L46-L51. (Pubitemid 38787649)
56. Walsh JJ, Dietlein LF, Low FN, Burch GE, Mogabgab WJ. Bronchotracheal response in human influenza. Type A, Asian strain, as studied by light and electron microscopic examination of bronchoscopic biopsies. Arch Intern Med 1961; 108: 376-388.
57. Jacoby DB, Tamaoki J, Borson DB, Nadel JA. Influenza infection causes airway hyperresponsiveness by decreasing enkephalinase. J Appl Physiol 1988; 64: 2653-2658.
58. Wolk KE, Lazarowski ER, Traylor ZP, Yu EN, Jewell NA, Durbin RK et al. Influenza A virus inhibitsalveolarfluid clearance in BALB/c mice. Am J Respir Crit Care Med 2008; 178: 969-976.
59. Chen XJ, Seth S, Yue G, Kamat P, Compans RW, Guidot D et al. Influenza virus inhibits ENaCand lungfluid clearance. Am J Physiol Lung Cell Mol Physiol 2004; 287: L366-L373. (Pubitemid 38943919)
60. Basler CF, Aguilar PV. Progress in identifying virulence determinants of the 1918 H1N1 and the Southeast Asian H5N1 influenza A viruses. Antiviral Res 2008; 79: 166-178.
61. Ward AC Virulence of influenza A virus for mouse lung. Virus Genes 1997; 14: 187-194. (Pubitemid 27397054)
62. Brown EG, Bailly JE. Genetic analysis of mouse-adapted influenza A virus identifies roles for the NA, PB1, and PB2 genes in virulence. Virus Res 1999; 61: 63-76. (Pubitemid 29276873)
63. Taylor RM. Experimental infection with influenza a virus in mice: The increase in intrapulmonary virus after inoculation and the influence of various factors thereon. J Exp Med 1941; 73: 43-55.
64. Anders EM, Hartley CA, Reading PC, Ezekowitz RA. Complement-dependent neutrali-zation of influenza virus by a serum mannose-binding lectin. J Gen Virol 1994; 75 (Pt 3): 615-622. (Pubitemid 24091818)
65. Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptorspecificityof the H3 hemagglutinin based on speciesof origin. Virology 1983; 127: 361-373. (Pubitemid 13026446)
66. Crouch E, Chang D, Rust K, Persson A, Heuser J. Recombinant pulmonary surfactant protein D Post-translational modification and molecular assembly. J Biol Chem 1994; 269: 15808-15813.
67. Tate MD, Brooks AG, Reading PC The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respir Res 2008; 9: 57.
68. Tate MD, Deng YM, Jones JE, Anderson GP, Brooks AG, Reading PC Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J Immunol 2009; 183: 7441-7450.
69. Sur S, Wild JS, Choudhury BK, Sur N, Alam R, Klinman DM. Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. J Immunol 1999; 162: 6284-6293. (Pubitemid 29314994)