Interferon regulatory factor-1 in flagellin-induced reprogramming: Potential protective role of CXCL10 in cornea innate defense against pseudomonas aeruginosa infection

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 12, 2013, Pages 7510-7521

  Yoon, Gi Sang ^a   Dong, Chen ^b   Gao, Nan ^b   Kumar, Ashok ^a,b   Standiford, Theodore J ^c   Yu, Fu Shin X ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cell reprogramming; CXCL10; Inflammation; IRF1; Toll like receptors

Indexed keywords

CXCL2 CHEMOKINE; FLAGELLIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 2;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA PERFORATION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNATE IMMUNITY; KERATITIS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEAR REPROGRAMMING; OPTICAL DENSITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PSEUDOMONAS INFECTION; REAL TIME POLYMERASE CHAIN REACTION; SERODIAGNOSIS; SLIT LAMP; WESTERN BLOTTING;

CELL REPROGRAMMING; CXCL10; INFLAMMATION; IRF1; TOLL-LIKE RECEPTORS;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHEMOKINE CXCL10; CHEMOKINE CXCL2; COLONY COUNT, MICROBIAL; CORNEAL ULCER; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIUM, CORNEAL; EYE INFECTIONS, BACTERIAL; FLAGELLIN; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84887836128     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12453     Document Type: Article

References (67)

1. Ueta M, Kinoshita S. Innate immunity of the ocular surface. Brain Res Bull. 2010; 81: 219-228.
2. Santaolalla R, Fukata M, Abreu MT. Innate immunity in the small intestine. Curr Opin Gastroenterol. 2011; 27: 125-131.
3. Schaible B, Schaffer K, Taylor CT. Hypoxia, innate immunity and infection in the lung. Respir Physiol Neurobiol. 2010; 174: 235-243.
4. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011; 34: 637-650.
5. Nish S, Medzhitov R. Host defense pathways: role of redundancy and compensation in infectious disease phenotypes. Immunity. 2011; 34: 629-636.
6. Bals R, Hiemstra PS. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur Respir J. 2004; 23: 327-333.
7. Song J, Abraham SN. Innate and adaptive immune responses in the urinary tract. Eur J Clin Invest. 2008; 38(suppl 2): 21-28.
8. Kumar A, Yu FS. Toll-like receptors and corneal innate immunity. Curr Mol Med. 2006; 6: 327-337.
9. Yu FS, Hazlett LD. Toll-like receptors and the eye. Invest Ophthalmol Vis Sci. 2006; 47: 1255-1263.
10. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology. 2004; 126: 1054-1070.
11. Kobayashi K, Hernandez LD, Galan JE, Janeway CA Jr, Medzhitov R, Flavell RA. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell. 2002; 110: 191-202.
12. Gingras S, Parganas E, de Pauw A, Ihle JN, Murray PJ. Reexamination of the role of suppressor of cytokine signaling 1 (SOCS1) in the regulation of toll-like receptor signaling. J Biol Chem. 2004; 279: 54702-54707.
13. Liew FY, Liu H, Xu D. A novel negative regulator for IL-1 receptor and Toll-like receptor 4. Immunol Lett. 2005; 96: 27-31.
14. Feterowski C, Novotny A, Kaiser-Moore S, et al. Attenuated pathogenesis of polymicrobial peritonitis in mice after TLR2 agonist pre-treatment involves ST2 up-regulation. Int Immunol. 2005; 17: 1035-1046.
15. Fan H, Cook JA. Molecular mechanisms of endotoxin tolerance. J Endotoxin Res. 2004; 10: 71-84.
16. Nahid MA, Satoh M, Chan EK. MicroRNA in TLR signaling and endotoxin tolerance. Cell Mol Immunol. 2011: 8: 388-403.
17. Biswas SK, Lopez-Collazo E. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 2009; 30: 475-487.
18. Cavaillon JM, Adib-Conquy M. Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis. Crit Care. 2006; 10: 233.
19. O'Neill LA, Bowie AG. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat Rev Immunol. 2007; 7: 353-364.
20. Gao N, Kumar A, Guo H, Wu X, Wheater M, Yu FS. Topical flagellin-mediated innate defense against Candida albicans keratitis. Invest Ophthalmol Vis Sci. 2011; 52: 3074-3082.
21. Gao N, Kumar A, Jyot J, Yu FS. Flagellin-induced corneal antimicrobial peptide production and wound repair involve a novel NF-kappaB-independent and EGFR-dependent pathway. PLoS One. 2010; 5: e9351.
22. Kumar A, Gao N, Standiford TJ, Gallo RL, Yu FS. Topical flagellin protects the injured corneas from Pseudomonas aeruginosa infection. Microbes Infect. 2010; 12: 978-989.
23. Kumar A, Hazlett LD, Yu FS. Flagellin suppresses the inflammatory response and enhances bacterial clearance in a murine model of Pseudomonas aeruginosa keratitis. Infect Immun. 2008; 76: 89-96.
24. Kumar A, Yin J, Zhang J, Yu FS. Modulation of corneal epithelial innate immune response to pseudomonas infection by flagellin pretreatment. Invest Ophthalmol Vis Sci. 2007; 48: 4664-4670.
25. Burdelya LG, Krivokrysenko VI, Tallant TC, et al. An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science. 2008; 320: 226-230.
26. Vijay-Kumar M, Aitken JD, Sanders CJ, et al. Flagellin treatment protects against chemicals, bacteria, viruses, and radiation. J Immunol. 2008; 180: 8280-8285.
27. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Flavell RA, Pamer EG. Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J Infect Dis. 2010; 201: 534-543.
28. Jarchum I, Liu M, Lipuma L, Pamer EG. Toll-like receptor-5 stimulation protects mice from acute Clostridium difficile colitis. Infect Immun. 2011; 79: 1498-1503.
29. Miao EA, Alpuche-Aranda CM, Dors M, et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol. 2006; 7: 569-575.
30. Miao EA, Andersen-Nissen E, Warren SE, Aderem A. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol. 2007; 29: 275-288.
31. Uematsu S, Akira S. Immune responses of TLR5({thorn}) lamina propria dendritic cells in enterobacterial infection. J Gastroenterol. 2009; 44: 803-811.
32. Carvalho FA, Aitken JD, Gewirtz AT, Vijay-Kumar M. TLR5 activation induces secretory interleukin-1 receptor antagonist (sIL-1Ra) and reduces inflammasome-associated tissue damage. Mucosal Immunol. 2010; 4: 102-111.
33. Campodonico VL, Llosa NJ, Grout M, Doring G, Maira-Litran T, Pier GB. Evaluation of flagella and flagellin of Pseudomonas aeruginosa as vaccines. Infect Immun. 2010; 78: 746-755.
34. Prince A. Flagellar activation of epithelial signaling. Am J Respir Cell Mol Biol. 2006; 34: 548-551.
35. Li G, Domenico J, Jia Y, Lucas JJ, Gelfand EW. NF-kappaBdependent induction of cathelicidin-related antimicrobial peptide in murine mast cells by lipopolysaccharide. Int Arch Allergy Immunol. 2009; 150: 122-132.
36. Pistolic J, Cosseau C, Li Y, et al. Host defence peptide LL-37 induces IL-6 expression in human bronchial epithelial cells by activation of the NF-kappaB signaling pathway. J Innate Immun. 2009; 1: 254-267.
37. Huang X, Barrett RP, McClellan SA, Hazlett LD. Silencing Tolllike receptor-9 in Pseudomonas aeruginosa keratitis. Invest Ophthalmol Vis Sci. 2005; 46: 4209-4216.
38. Zhang J, Xu K, Ambati B, Yu FS. Toll-like receptor 5-mediated corneal epithelial inflammatory responses to Pseudomonas aeruginosa flagellin. Invest Ophthalmol Vis Sci. 2003; 44: 4247-4254.
39. Kumar A, Zhang J, Yu FS. Toll-like receptor 2-mediated expression of beta-defensin-2 in human corneal epithelial cells. Microbes Infect. 2006; 8: 380-389.
40. Stirnweiss A, Ksienzyk A, Klages K, et al. IFN regulatory factor-1 bypasses IFN-mediated antiviral effects through viperin gene induction. J Immunol. 2010; 184: 5179-5185.
41. Zaheer RS, Proud D. Human rhinovirus-induced epithelial production of CXCL10 is dependent upon IFN regulatory factor-1. Am J Respir Cell Mol Biol 2010; 43: 413-421.
42. Koetzler R, Zaheer RS, Newton R, Proud D. Nitric oxide inhibits IFN regulatory factor 1 and nuclear factor-kappaB pathways in rhinovirus-infected epithelial cells. J Allergy Clin Immunol. 2009; 124: 551-557.
43. Zaheer RS, Proud D. Human rhinovirus-induced epithelial production of CXCL10 is dependent upon IFN regulatory factor-1. Am J Respir Cell Mol Biol. 2010; 43: 413-421.
44. Gao N, Yin J, Yoon GS, Mi QS, Yu FS. Dendritic cell-epithelium interplay is a determinant factor for corneal epithelial wound repair. Am J Pathol. 2011; 179: 2243-2253.
45. Souza-Fonseca-Guimaraes F, Adib-Conquy M, Cavaillon JM. Natural killer (NK) cells in antibacterial innate immunity: angels or devils? Mol Med. 2012; 18: 270-285.
46. Lighvani S, Huang X, Trivedi PP, Swanborg RH, Hazlett LD. Substance P regulates natural killer cell interferon-gamma production and resistance to Pseudomonas aeruginosa infection. Eur J Immunol. 2005; 35: 1567-1575.
47. Hazlett LD, Li Q, Liu J, McClellan S, Du W, Barrett RP. NKT cells are critical to initiate an inflammatory response after Pseudomonas aeruginosa ocular infection in susceptible mice. J Immunol. 2007; 179: 1138-1146.
48. Colonna M. TLR pathways and IFN-regulatory factors: to each its own. Eur J Immunol. 2007; 37: 306-309.
49. Honda K, Taniguchi T. Toll-like receptor signaling and IRF transcription factors. IUBMB Life. 2006; 58: 290-295.
50. Savitsky D, Tamura T, Yanai H, Taniguchi T. Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol Immunother. 2010; 59: 489-510.
51. Battistini A. Interferon regulatory factors in hematopoietic cell differentiation and immune regulation. J Interferon Cytokine Res. 2009; 29: 765-780.
52. Aly S, Mages J, Reiling N, et al. Mycobacteria-induced granuloma necrosis depends on IRF-1. J Cell Mol Med. 2009; 13: 2069-2082.
53. Yamada H, Mizuno S, Sugawara I. Interferon regulatory factor 1 in mycobacterial infection. Microbiol Immunol. 2002; 46: 751-760.
54. Cole AM, Ganz T, Liese AM, Burdick MD, Liu L, Strieter RM. Cutting edge: IFN-inducible ELR-CXC chemokines display defensin-like antimicrobial activity. J Immunol. 2001; 167: 623-627.
55. Cao W, Liu YJ. Innate immune functions of plasmacytoid dendritic cells. Curr Opin Immunol. 2007; 19: 24-30.
56. Mohan K, Cordeiro E, Vaci M, McMaster C, Issekutz TB. CXCR3 is required for migration to dermal inflammation by normal and in vivo activated T cells: differential requirements by CD4 and CD8 memory subsets. Eur J Immunol. 2005; 35: 1702-1711.
57. Cole AM, Ganz T, Liese AM, Burdick MD, Liu L, Strieter RM. Cutting edge: IFN-inducible ELR-CXC chemokines display defensin-like antimicrobial activity. J Immunol. 2001; 167: 623-627.
58. Alarcon I, Kwan L, Yu C, Evans DJ, Fleiszig SM. Role of the corneal epithelial basement membrane in ocular defense against Pseudomonas aeruginosa. Infect Immun. 2009; 77: 3264-3271.
59. Alarcon I, Tam C, Mun JJ, LeDue J, Evans DJ, Fleiszig SM. Factors impacting corneal epithelial barrier function against Pseudomonas aeruginosa traversal. Invest Ophthalmol Vis Sci. 2011; 52: 1368-1377.
60. Augustin DK, Heimer SR, Tam C, et al. Role of defensins in corneal epithelial barrier function against Pseudomonas aeruginosa traversal. Infect Immun. 2011; 79: 595-605.
61. Huang LC, Petkova TD, Reins RY, Proske RJ, McDermott AM. Multifunctional roles of human cathelicidin (LL-37) at the ocular surface. Invest Ophthalmol Vis Sci. 2006; 47: 2369-2380.
62. Gao N, Sang Yoon G, Liu X, et al. Genome-wide transcriptional analysis of differentially expressed genes in flagellin-pretreated mouse corneal epithelial cells in response to Pseudomonas aeruginosa: involvement of S100A8/A9. Mucosal Immunol. 2013; 6: 993-1005.
63. Quaranta MG, Napolitano A, Sanchez M, Giordani L, Mattioli B, Viora M. HIV-1 Nef impairs the dynamic of DC/NK crosstalk: different outcome of CD56(dim) and CD56(bright) NK cell subsets. FASEB J. 2007; 21: 2323-2334.
64. Goodridge JP, Lathbury LJ, John E, Charles AK, Christiansen FT, Witt CS. The genotype of the NK cell receptor, KIR2DL4, influences INFgamma secretion by decidual natural killer cells. Mol Hum Reprod. 2009; 15: 489-497.
65. Schoenborn JR, Wilson CB. Regulation of interferon-c during innate and adaptive immune responses. Adv Immunol. 2007; 96: 41-101.
66. Hazlett LD. Corneal response to Pseudomonas aeruginosa infection. Prog Retin Eye Res. 2004; 23: 1-30.
67. Yu FS, Cornicelli MD, Kovach MA, et al. Flagellin stimulates protective lung mucosal immunity: role of cathelicidin-related antimicrobial peptide. J Immunol. 2010; 185: 1142-1149.