Galectins regulate the inflammatory response in airway epithelial cells exposed to microbial neuraminidase by modulating the expression of SOCS1 and RIG1

Molecular Immunology

Volumn 68, Issue 2, 2015, Pages 194-202

  Nita Lazar, Mihai ^a   Banerjee, Aditi ^a   Feng, Chiguang ^a   Vasta, Gerardo R ^a  

^a UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

Author keywords

Chemokines; Cytokines; Galectin; Neuraminidase; RIG1; Signaling pathway; SOCS

Indexed keywords

GALACTOSE; GALECTIN; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RETINOIC ACID INDUCIBLE PROTEIN I; SIALIDASE; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; BACTERIAL PROTEIN; CYTOKINE; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; GALECTIN 1; GALECTIN 3; LGALS1 PROTEIN, HUMAN; RECOMBINANT PROTEIN; SOCS1 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING;

ARTICLE; CYTOKINE PRODUCTION; CYTOKINE STORM; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INFLAMMATION; INFLUENZA A VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SECRETION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; SURFACE PROPERTY; UPREGULATION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; RESPIRATORY MUCOSA; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; BACTERIAL PROTEINS; CELL LINE, TUMOR; CYTOKINES; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; EPITHELIAL CELLS; ESCHERICHIA COLI; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GALECTIN 1; GALECTIN 3; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INFLUENZA A VIRUS; JANUS KINASES; MICE; NEURAMINIDASE; PROTO-ONCOGENE PROTEINS C-AKT; RECOMBINANT PROTEINS; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING 1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84957433993     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.08.005     Document Type: Article

References (61)

1. Alonso J.M., Guiyoule A., et al. A model of meningococcal bacteremia after respiratory superinfection in influenza A virus-infected mice. FEMS Microbiol. Lett. 2003, 222(1):99-106.
2. Arimori Y., Nakamura R., et al. Type I interferon limits influenza virus-induced acute lung injury by regulation of excessive inflammation in mice. Antiviral Res. 2013, 99(3):230-237.
3. Bermejo-Martin J.F., Martin-Loeches I., et al. Host adaptive immunity deficiency in severe pandemic influenza. Crit. Care 2010, 14(5):R167.
4. Billiau A. Interferon: the pathways of discovery I. Molecular and cellular aspects. Cytokine Growth Factor Rev. 2006, 17(5):381-409.
5. Bode J.G., Ludwig S., et al. The MKK6/p38 mitogen-activated protein kinase pathway is capable of inducing SOCS3 gene expression and inhibits IL-6-induced transcription. Biol. Chem. 2001, 382(10):1447-1453.
6. Camby I., Le Mercier M., et al. Galectin-1: a small protein with major functions. Glycobiology 2006, 16(16840800):157.
7. Chen W.H., Toapanta F.R., et al. Potential role for alternatively activated macrophages in the secondary bacterial infection during recovery from influenza. Immunol. Lett. 2012, 141(2):227-234.
8. Chertow D.S., Memoli M.J. Bacterial coinfection in influenza: a grand rounds review. JAMA 2013, 309(3):275-282.
9. Choi Y.S., Park J.K., et al. Cytokine signaling-1 suppressor is inducible by IL-1beta and inhibits the catabolic effects of IL-1beta in chondrocytes: its implication in the paradoxical joint-protective role of IL-1beta. Arthritis Res. Ther. 2013, 15(6):R191.
10. Clark A.R., Dean J.L. The p38 MAPK pathway in rheumatoid arthritis: a sideways look. Open Rheumatol. J. 2012, 6:209-219.
11. Croker B.A., Kiu H., et al. SOCS regulation of the JAK/STAT signalling pathway. Semin. Cell Dev. Biol. 2008, 19(4):414-422.
12. Cross A.S., Hyun S.W., et al. NEU1 and NEU3 sialidase activity expressed in human lung microvascular endothelia: NEU1 restrains endothelial cell migration, whereas NEU3 does not. J. Biol. Chem. 2012, 287(19):15966-15980.
13. Damjanovic D., Lai R., et al. Marked improvement of severe lung immunopathology by influenza-associated pneumococcal superinfection requires the control of both bacterial replication and host immune responses. Am. J. Pathol. 2013, 183(3):868-880.
14. Davey G.M., Heath W.R., et al. SOCS1: a potent and multifaceted regulator of cytokines and cell-mediated inflammation. Tissue Antigens 2006, 67(1):1-9.
15. Ehlting C., Lai W.S., et al. Regulation of suppressor of cytokine signaling 3 (SOCS3) mRNA stability by TNF-alpha involves activation of the MKK6/p38MAPK/MK2 cascade. J. Immunol. 2007, 178(5):2813-2826.
16. Farnworth S.L., Henderson N.C., et al. Galectin-3 reduces the severity of Pneumococcal pneumonia by augmenting neutrophil function. Am. J. Pathol. 2008, 172(2):395-405.
17. Feng C., Ghosh A., et al. The galectin CvGal1 from the eastern oyster (Crassostrea virginica) binds to blood group A oligosaccharides on the hemocyte surface. J. Biol. Chem. 2013, 288(34):24394-24409.
18. Feng C., Stamatos N.M., et al. Sialyl residues modulate LPS-mediated signaling through the toll-like receptor 4 complex. PLoS One 2012, 7(4):e32359.
19. Feng C., Zhang L., et al. Neuraminidase reprograms lung tissue and potentiates lipopolysaccharide-induced acute lung injury in mice. J. Immunol. 2013, 191(9):4828-4837.
20. Fischer C., Sanchez-Ruderisch H., et al. Galectin-1 interacts with the 51 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J. Biol. Chem. 2005, 280(44):37266-37277.
21. Fletcher J., Starr R. The role of suppressors of cytokine signalling in thymopoiesis and T cell activation. Int. J. Biochem. Cell Biol. 2005, 37(9):1774-1786.
22. Fukuyama S., Kawaoka Y. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr. Opin. Immunol. 2011, 23(4):481-486.
23. Gianni T., Campadelli-Fiume G. The epithelial alphavbeta3-integrin boosts the MYD88-dependent TLR2 signaling in response to viral and bacterial components. PLoS Pathog. 2014, 10(11):e1004477.
24. Gianni T., Leoni V., et al. Alphavbeta3-integrin is a major sensor and activator of innate immunity to herpes simplex virus-1. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(48):19792-19797.
25. Gonzalez-Navajas J.M., Lee J., et al. Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 2012, 12(2):125-135.
26. Guarda G., Braun M., et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011, 34(2):213-223.
27. Ilangumaran S., Ramanathan S., et al. Regulation of the immune system by SOCS family adaptor proteins. Semin. Immunol. 2004, 16(6):351-365.
28. Kedzierski L., Linossi E.M., et al. Suppressor of cytokine signaling 4 (SOCS4) protects against severe cytokine storm and enhances viral clearance during influenza infection. PLoS Pathog. 2014, 10(5):e1004134.
29. Kiu H., Hilton D.J., et al. Mechanism of crosstalk inhibition of IL-6 signaling in response to LPS and TNFalpha. Growth Factors 2007, 25(5):319-328.
30. Koh H.S., Lee C., et al. CD7 expression and galectin-1-induced apoptosis of immature thymocytes are directly regulated by NF-kappaB upon T-cell activation. Biochem. Biophys. Res. Commun. 2008, 370(1):149-153.
31. Lillehoj E.P., Hyun S.W., et al. NEU1 sialidase expressed in human airway epithelia regulates epidermal growth factor receptor (EGFR) and MUC1 protein signaling. J. Biol. Chem. 2012, 287(11):8214-8231.
32. Luo M. Influenza virus entry. Adv. Exp. Med. Biol. 2012, 726:201-221.
33. Matsumiya T., Stafforini D.M. Function and regulation of retinoic acid-inducible gene-I. Crit. Rev. Immunol. 2010, 30(6):489-513.
34. Monsalvo A.C., Batalle J.P., et al. Severe pandemic 2009H1N1 influenza disease due to pathogenic immune complexes. Nat. Med. 2011, 17(2):195-199.
35. Naka T., Fujimoto M., et al. Negative regulation of cytokine and TLR signalings by SOCS and others. Adv. Immunol. 2005, 87:61-122.
36. Nguyen K.B., Salazar-Mather T.P., et al. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 2002, 169(8):4279-4287.
37. Nita-Lazar M., Banerjee A., et al. Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. Mol. Immunol. 2015, 65(1):1-16.
38. Pauli E.K., Schmolke M., et al. Influenza A virus inhibits type I IFN signaling via NF-kappaB-dependent induction of SOCS-3 expression. PLoS Pathog. 2008, 4(11):e1000196.
39. Perera P.Y., Mayadas T.N., et al. CD11b/CD18 acts in concert with CD14 and Toll-like receptor (TLR) 4 to elicit full lipopolysaccharide and taxol-inducible gene expression. J. Immunol. 2001, 166(1):574-581.
40. Poltorak A., He X., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282(5396):2085-2088.
41. Pothlichet J., Chignard M., et al. Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J. Immunol. 2008, 180(4):2034-2038.
42. Rabinovich G.A., Daly G., et al. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J. Exp. Med. 1999, 190(3):385-398.
43. Rabinovich G.A., Ilarregui J.M. Conveying glycan information into T-cell homeostatic programs: a challenging role for galectin-1 in inflammatory and tumor microenvironments. Immunol. Rev. 2009, 230(1):144-159.
44. Ramirez-Martinez G., Cruz-Lagunas A., et al. Seasonal and pandemic influenza H1N1 viruses induce differential expression of SOCS-1 and RIG-I genes and cytokine/chemokine production in macrophages. Cytokine 2013, 62(1):151-159.
45. Santucci L., Fiorucci S., et al. Galectin-1 suppresses experimental colitis in mice. Gastroenterology 2003, 124(5):1381-1394.
46. Sato S., Ouellet N., et al. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during Streptococcal pneumonia. J. Immunol. 2002, 168(4):1813-1822.
47. Seki M., Higashiyama Y., et al. Acute infection with influenza virus enhances susceptibility to fatal pneumonia following Streptococcus pneumoniae infection in mice with chronic pulmonary colonization with Pseudomonas aeruginosa. Clin. Exp. Immunol. 2004, 137(1):35-40.
48. Speshock J.L., Doyon-Reale N., et al. Filamentous influenza A virus infection predisposes mice to fatal septicemia following superinfection with Streptococcus pneumoniae serotype 3. Infect. Immun. 2007, 75(6):3102-3111.
49. Takeuchi O., Akira S. MDA5/RIG-I and virus recognition. Curr. Opin. Immunol. 2008, 20(1):17-22.
50. Toscano M.A., Campagna L., et al. Nuclear factor (NF)-kappaB controls expression of the immunoregulatory glycan-binding protein galectin-1. Mol. Immunol. 2011, 48(15-16):1940-1949.
51. Toscano M.A., Commodaro A.G., et al. Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2-and T regulatory-mediated anti-inflammatory responses. J. Immunol. 2006, 176(10):6323-6332.
52. Vasta G.R. Roles of galectins in infection. Nat. Rev. Microbiol. 2009, 7(6):424-438.
53. Vasta G.R., Ahmed H. Animal Lectins: A Functional View 2008, CRC Press.
54. Xu X., Zheng J., et al. Respiratory syncytial virus NS1 protein degrades STAT2 by inducing SOCS1 expression. Intervirology 2014, 57(2):65-73.
55. Yang X.X., Du N., et al. Gene expression profiles comparison between 2009 pandemic and seasonal H1N1 influenza viruses in A549 cells. Biomed. Environ. Sci. 2010, 23(4):259-266.
56. Yee N.K., Hamerman J.A. Beta(2) integrins inhibit TLR responses by regulating NF-kappaB pathway and p38 MAPK activation. Eur. J. Immunol. 2013, 43(3):779-792.
57. Yoneyama M., Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 2009, 227(1):54-65.
58. Yoo J.S., Kato H., et al. Sensing viral invasion by RIG-I like receptors. Curr. Opin. Microbiol. 2014, 20:131-138.
59. Yoshimura A., Naka T., et al. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 2007, 7(6):454-465.
60. Zimmermann S., Murray P.J., et al. Induction of suppressor of cytokine signaling-1 by toxoplasma gondii contributes to immune evasion in macrophages by blocking IFN-gamma signaling. J. Immunol. 2006, 176(3):1840-1847.
61. Zúñiga J., Torres M., et al. Inflammatory profiles in severe pneumonia associated with the pandemic influenza A/H1N1 virus isolated in Mexico City. Autoimmunity 2011, 44(7):562-570.