Trappin-2/elafin modulate innate immune responses of human endometrial epithelial cells to polyI:C

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Drannik, Anna G ^a   Nag, Kakon ^a   Yao, Xiao Dan ^a   Henrick, Bethany M ^a   Sallenave, Jean Michel ^b,c,d   Rosenthal, Kenneth L ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b INSTITUT PASTEUR   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; ELAFIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; INTERLEUKIN 8; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; SERINE; TRAPPIN 2 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PI3 PROTEIN, HUMAN; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; ELAFIN GENE; ENDOMETRIUM; EPITHELIUM CELL; FEMALE GENITAL SYSTEM; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; INNATE IMMUNITY; NUCLEOTIDE SEQUENCE; PROTEIN PHOSPHORYLATION; TRAPPIN 2 GENE; VESICULAR STOMATITIS VIRUS; VIRUS ATTACHMENT; VIRUS REPLICATION; CELL LINE; CHEMISTRY; CYTOLOGY; FEMALE; IMMUNOLOGY; PHYSIOLOGY; RHABDOVIRUS INFECTION; VIROLOGY;

CELL LINE; ELAFIN; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERLEUKIN-6; INTERLEUKIN-8; NF-KAPPA B; RHABDOVIRIDAE INFECTIONS; RNA, VIRAL; VESICULOVIRUS; VIRUS REPLICATION;

EID: 84860192608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035866     Document Type: Article

References (90)

1. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, et al. (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 6: e1000852.
2. Wira CR, Grant-Tschudy KS, Crane-Godreau MA, (2005) Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am J Reprod Immunol 53: 65-76.
3. Samuel CE, (2001) Antiviral actions of interferons. Clin Microbiol Rev 14: 778-809, table of contents.
4. Yoneyama M, Fujita T, (2010) Recognition of viral nucleic acids in innate immunity. Rev Med Virol 20: 4-22.
5. Erhart W, Alkasi O, Brunke G, Wegener F, Maass N, et al. (2011) Induction of human beta-defensins and psoriasin in vulvovaginal human papillomavirus-associated lesions. J Infect Dis 204: 391-399.
6. Ghosh M, Shen Z, Fahey JV, Cu-Uvin S, Mayer K, et al. (2010) Trappin-2/Elafin: a novel innate anti-human immunodeficiency virus-1 molecule of the human female reproductive tract. Immunology 129: 207-219.
7. Bingle CD, Vyakarnam A, (2008) Novel innate immune functions of the whey acidic protein family. Trends Immunol 29: 444-453.
8. Drannik AG, Henrick BM, Rosenthal KL, (2011) War and peace between WAP and HIV: role of SLPI, trappin-2, elafin and ps20 in susceptibility to HIV infection. Biochem Soc Trans 39: 1427-1432.
9. Schalkwijk J, Chang A, Janssen P, De Jongh GJ, Mier PD, (1990) Skin-derived antileucoproteases (SKALPs): characterization of two new elastase inhibitors from psoriatic epidermis. Br J Dermatol 122: 631-641.
10. Sallenave JM, (2010) Secretory leukocyte protease inhibitor and elafin/trappin-2: versatile mucosal antimicrobials and regulators of immunity. Am J Respir Cell Mol Biol 42: 635-643.
11. Moreau T, Baranger K, Dade S, Dallet-Choisy S, Guyot N, et al. (2008) Multifaceted roles of human elafin and secretory leukocyte proteinase inhibitor (SLPI), two serine protease inhibitors of the chelonianin family. Biochimie 90: 284-295.
12. Drenth J, Low BW, Richardson JS, Wright CS, (1980) The toxin-agglutinin fold. A new group of small protein structures organized around a four-disulfide core. J Biol Chem 255: 2652-2655.
13. Piletz JE, Heinlen M, Ganschow RE, (1981) Biochemical characterization of a novel whey protein from murine milk. J Biol Chem 256: 11509-11516.
14. Tsunemi M, Matsuura Y, Sakakibara S, Katsube Y, (1996) Crystal structure of an elastase-specific inhibitor elafin complexed with porcine pancreatic elastase determined at 1.9 A resolution. Biochemistry 35: 11570-11576.
15. Schalkwijk J, Wiedow O, Hirose S, (1999) The trappin gene family: proteins defined by an N-terminal transglutaminase substrate domain and a C-terminal four-disulphide core. Biochem J 340 (Pt 3): 569-577.
16. Nara K, Ito S, Ito T, Suzuki Y, Ghoneim MA, et al. (1994) Elastase inhibitor elafin is a new type of proteinase inhibitor which has transglutaminase-mediated anchoring sequence termed "cementoin". J Biochem 115: 441-448.
17. Guyot N, Bergsson G, Butler MW, Greene CM, Weldon S, et al. (2010) Functional study of elafin cleaved by Pseudomonas aeruginosa metalloproteinases. Biol Chem 391: 705-716.
18. Guyot N, Zani ML, Berger P, Dallet-Choisy S, Moreau T, (2005) Proteolytic susceptibility of the serine protease inhibitor trappin-2 (pre-elafin): evidence for tryptase-mediated generation of elafin. Biol Chem 386: 391-399.
19. Guyot N, Zani ML, Maurel MC, Dallet-Choisy S, Moreau T, (2005) Elafin and its precursor trappin-2 still inhibit neutrophil serine proteinases when they are covalently bound to extracellular matrix proteins by tissue transglutaminase. Biochemistry 44: 15610-15618.
20. Simpson AJ, Wallace WA, Marsden ME, Govan JR, Porteous DJ, et al. (2001) Adenoviral augmentation of elafin protects the lung against acute injury mediated by activated neutrophils and bacterial infection. J Immunol 167: 1778-1786.
21. Bellemare A, Vernoux N, Morin S, Gagne SM, Bourbonnais Y, (2010) Structural and antimicrobial properties of human pre-elafin/trappin-2 and derived peptides against Pseudomonas aeruginosa. BMC Microbiol 10: 253.
22. Simpson AJ, Maxwell AI, Govan JR, Haslett C, Sallenave JM, (1999) Elafin (elastase-specific inhibitor) has anti-microbial activity against gram-positive and gram-negative respiratory pathogens. FEBS Lett 452: 309-313.
23. Wilkinson TS, Dhaliwal K, Hamilton TW, Lipka AF, Farrell L, et al. (2009) Trappin-2 promotes early clearance of Pseudomonas aeruginosa through CD14-dependent macrophage activation and neutrophil recruitment. Am J Pathol 174: 1338-1346.
24. Baranger K, Zani ML, Chandenier J, Dallet-Choisy S, Moreau T, (2008) The antibacterial and antifungal properties of trappin-2 (pre-elafin) do not depend on its protease inhibitory function. Febs J 275: 2008-2020.
25. Henriksen PA, Hitt M, Xing Z, Wang J, Haslett C, et al. (2004) Adenoviral gene delivery of elafin and secretory leukocyte protease inhibitor attenuates NF-kappa B-dependent inflammatory responses of human endothelial cells and macrophages to atherogenic stimuli. J Immunol 172: 4535-4544.
26. Butler MW, Robertson I, Greene CM, O'Neill SJ, Taggart CC, et al. (2006) Elafin prevents lipopolysaccharide-induced AP-1 and NF-kappaB activation via an effect on the ubiquitin-proteasome pathway. J Biol Chem 281: 34730-34735.
27. Roghanian A, Williams SE, Sheldrake TA, Brown TI, Oberheim K, et al. (2006) The antimicrobial/elastase inhibitor elafin regulates lung dendritic cells and adaptive immunity. Am J Respir Cell Mol Biol 34: 634-642.
28. McMichael JW, Roghanian A, Jiang L, Ramage R, Sallenave JM, (2005) The antimicrobial antiproteinase elafin binds to lipopolysaccharide and modulates macrophage responses. Am J Respir Cell Mol Biol 32: 443-452.
29. Iqbal SM, Ball TB, Levinson P, Maranan L, Jaoko W, et al. (2009) Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition. Aids 23: 1669-1677.
30. King AE, Paltoo A, Kelly RW, Sallenave JM, Bocking AD, et al. (2007) Expression of natural antimicrobials by human placenta and fetal membranes. Placenta 28: 161-169.
31. King AE, Critchley HO, Sallenave JM, Kelly RW, (2003) Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation. J Clin Endocrinol Metab 88: 4426-4431.
32. Sallenave JM, Marsden MD, Ryle AP, (1992) Isolation of elafin and elastase-specific inhibitor (ESI) from bronchial secretions. Evidence of sequence homology and immunological cross-reactivity. Biol Chem Hoppe Seyler 373: 27-33.
33. Wiedow O, Schroder JM, Gregory H, Young JA, Christophers E, (1990) Elafin: an elastase-specific inhibitor of human skin. Purification, characterization, and complete amino acid sequence. J Biol Chem 265: 14791-14795.
34. Schalkwijk J, de Roo C, de Jongh GJ, (1991) Skin-derived antileukoproteinase (SKALP), an elastase inhibitor from human keratinocytes. Purification and biochemical properties. Biochim Biophys Acta 1096: 148-154.
35. Simpson AJ, Cunningham GA, Porteous DJ, Haslett C, Sallenave JM, (2001) Regulation of adenovirus-mediated elafin transgene expression by bacterial lipopolysaccharide. Hum Gene Ther 12: 1395-1406.
36. Pfundt R, Wingens M, Bergers M, Zweers M, Frenken M, et al. (2000) TNF-alpha and serum induce SKALP/elafin gene expression in human keratinocytes by a p38 MAP kinase-dependent pathway. Arch Dermatol Res 292: 180-187.
37. Sallenave JM, Shulmann J, Crossley J, Jordana M, Gauldie J, (1994) Regulation of secretory leukocyte proteinase inhibitor (SLPI) and elastase-specific inhibitor (ESI/elafin) in human airway epithelial cells by cytokines and neutrophilic enzymes. Am J Respir Cell Mol Biol 11: 733-741.
38. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA, (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
39. Nazli A, Yao XD, Smieja M, Rosenthal KL, Ashkar AA, et al. (2009) Differential induction of innate anti-viral responses by TLR ligands against Herpes simplex virus, type 2, infection in primary genital epithelium of women. Antiviral Res 81: 103-112.
40. Schaefer TM, Fahey JV, Wright JA, Wira CR, (2005) Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J Immunol 174: 992-1002.
41. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
42. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, et al. (2005) Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175: 2851-2858.
43. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
44. Bauer CM, Dewitte-Orr SJ, Hornby KR, Zavitz CC, Lichty BD, et al. (2008) Cigarette smoke suppresses type I interferon-mediated antiviral immunity in lung fibroblast and epithelial cells. J Interferon Cytokine Res 28: 167-179.
45. Wathelet MG, Lin CH, Parekh BS, Ronco LV, Howley PM, et al. (1998) Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol Cell 1: 507-518.
46. Maniatis T, Falvo JV, Kim TH, Kim TK, Lin CH, et al. (1998) Structure and function of the interferon-beta enhanceosome. Cold Spring Harb Symp Quant Biol 63: 609-620.
47. Mossman KL, Macgregor PF, Rozmus JJ, Goryachev AB, Edwards AM, et al. (2001) Herpes simplex virus triggers and then disarms a host antiviral response. J Virol 75: 750-758.
48. Paladino P, Cummings DT, Noyce RS, Mossman KL, (2006) The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I. J Immunol 177: 8008-8016.
49. Lin R, Heylbroeck C, Pitha PM, Hiscott J, (1998) Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol 18: 2986-2996.
50. Ashkar AA, Yao XD, Gill N, Sajic D, Patrick AJ, et al. (2004) Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J Infect Dis 190: 1841-1849.
51. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, et al. (2006) Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. Aids 20: 73-83.
52. Lester RT, Yao XD, Ball TB, McKinnon LR, Kaul R, et al. (2008) Toll-like receptor expression and responsiveness are increased in viraemic HIV-1 infection. Aids 22: 685-694.
53. Rebbapragada A, Wachihi C, Pettengell C, Sunderji S, Huibner S, et al. (2007) Negative mucosal synergy between Herpes simplex type 2 and HIV in the female genital tract. Aids 21: 589-598.
54. Lieber M, Smith B, Szakal A, Nelson-Rees W, Todaro G, (1976) A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 17: 62-70.
55. Sallenave JM, Xing Z, Graham F, Gauldie J, (1997) In vivo adenovirus-mediated expression of human pre-elafin, a potent neutrophil elastase inhibitor. Chest 111: 128S-129S.
56. Sallenave JM, Xing Z, Simpson AJ, Graham FL, Gauldie J, (1998) Adenovirus-mediated expression of an elastase-specific inhibitor (elafin): a comparison of different promoters. Gene Ther 5: 352-360.
57. Bett AJ, Haddara W, Prevec L, Graham FL, (1994) An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc Natl Acad Sci U S A 91: 8802-8806.
58. Vandermeeren M, Daneels G, Bergers M, van Vlijmen-Willems I, Pol A, et al. (2001) Development and application of monoclonal antibodies against SKALP/elafin and other trappin family members. Arch Dermatol Res 293: 343-349.
59. Sakurai H, Kawabata K, Sakurai F, Nakagawa S, Mizuguchi H, (2008) Innate immune response induced by gene delivery vectors. Int J Pharm 354: 9-15.
60. Dogusan Z, Garcia M, Flamez D, Alexopoulou L, Goldman M, et al. (2008) Double-stranded RNA induces pancreatic beta-cell apoptosis by activation of the toll-like receptor 3 and interferon regulatory factor 3 pathways. Diabetes 57: 1236-1245.
61. Hobbs DS, Pestka S, (1982) Purification and characterization of interferons from a continuous myeloblastic cell line. J Biol Chem 257: 4071-4076.
62. Noyce RS, Collins SE, Mossman KL, (2006) Identification of a novel pathway essential for the immediate-early, interferon-independent antiviral response to enveloped virions. J Virol 80: 226-235.
63. McAlhany SJ, Ayala GE, Frolov A, Ressler SJ, Wheeler TM, et al. (2004) Decreased stromal expression and increased epithelial expression of WFDC1/ps20 in prostate cancer is associated with reduced recurrence-free survival. Prostate 61: 182-191.
64. Alvarez R, Reading J, King DF, Hayes M, Easterbrook P, et al. (2008) WFDC1/ps20 is a novel innate immunomodulatory signature protein of human immunodeficiency virus (HIV)-permissive CD4+ CD45RO+ memory T cells that promotes infection by upregulating CD54 integrin expression and is elevated in HIV type 1 infection. J Virol 82: 471-486.
65. Alam SR, Newby DE, Henriksen PA, (2012) Role of the endogenous elastase inhibitor, elafin, in cardiovascular injury: From epithelium to endothelium. Biochem Pharmacol 83: 695-704.
66. Vergnolle N SJ-M, Langella P, Bermudez-Humaran L, (2011) Recombinant probiotic bacteria for the prevention and treatment of Inflammatory Bowel Disease (IBD) and Irritable Bowel Syndrome (IBS).
67. Shaw L, Wiedow O, (2011) Therapeutic potential of human elafin. Biochem Soc Trans 39: 1450-1454.
68. McElvaney NG, Doujaiji B, Moan MJ, Burnham MR, Wu MC, et al. (1993) Pharmacokinetics of recombinant secretory leukoprotease inhibitor aerosolized to normals and individuals with cystic fibrosis. Am Rev Respir Dis 148: 1056-1060.
69. Zani ML, Tanga A, Saidi A, Serrano H, Dallet-Choisy S, et al. (2011) SLPI and trappin-2 as therapeutic agents to target airway serine proteases in inflammatory lung diseases: current and future directions. Biochem Soc Trans 39: 1441-1446.
70. Motta JP, Magne L, Descamps D, Rolland C, Squarzoni-Dale C, et al. (2011) Modifying the protease, antiprotease pattern by elafin overexpression protects mice from colitis. Gastroenterology 140: 1272-1282.
71. Fahey JV, Bodwell JE, Hickey DK, Ghosh M, Muia MN, et al. (2011) New approaches to making the microenvironment of the female reproductive tract hostile to HIV. Am J Reprod Immunol 65: 334-343.
72. Ma G, Greenwell-Wild T, Lei K, Jin W, Swisher J, et al. (2004) Secretory leukocyte protease inhibitor binds to annexin II, a cofactor for macrophage HIV-1 infection. J Exp Med 200: 1337-1346.
73. MasCasullo V, Fam E, Keller MJ, Herold BC, (2005) Role of mucosal immunity in preventing genital herpes infection. Viral Immunol 18: 595-606.
74. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, et al. (2003) Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. Aids 17: F39-48.
75. Rapista A, Ding J, Benito B, Lo YT, Neiditch MB, et al. (2011) Human defensins 5 and 6 enhance HIV-1 infectivity through promoting HIV attachment. Retrovirology 8: 45.
76. Hazrati E, Galen B, Lu W, Wang W, Ouyang Y, et al. (2006) Human alpha- and beta-defensins block multiple steps in herpes simplex virus infection. J Immunol 177: 8658-8666.
77. Semple F, MacPherson H, Webb S, Cox SL, Mallin LJ, et al. (2011) Human beta-defensin 3 affects the activity of pro-inflammatory pathways associated with MyD88 and TRIF. Eur J Immunol 41: 3291-3300.
78. Hasan M, Ruksznis C, Wang Y, Leifer CA, (2011) Antimicrobial peptides inhibit polyinosinic-polycytidylic Acid-induced immune responses. J Immunol 187: 5653-5659.
79. Zapata W, Rodriguez B, Weber J, Estrada H, Quinones-Mateu ME, et al. (2008) Increased levels of human beta-defensins mRNA in sexually HIV-1 exposed but uninfected individuals. Curr HIV Res 6: 531-538.
80. Steinstraesser L, Tippler B, Mertens J, Lamme E, Homann HH, et al. (2005) Inhibition of early steps in the lentiviral replication cycle by cathelicidin host defense peptides. Retrovirology 2: 2.
81. Harty RN, Pitha PM, Okumura A, (2009) Antiviral activity of innate immune protein ISG15. J Innate Immun 1: 397-404.
82. Guo J, Peters KL, Sen GC, (2000) Induction of the human protein P56 by interferon, double-stranded RNA, or virus infection. Virology 267: 209-219.
83. Terenzi F, Hui DJ, Merrick WC, Sen GC, (2006) Distinct induction patterns and functions of two closely related interferon-inducible human genes, ISG54 and ISG56. J Biol Chem 281: 34064-34071.
84. Li Y, Li C, Xue P, Zhong B, Mao AP, et al. (2009) ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc Natl Acad Sci U S A 106: 7945-7950.
85. Lester RT, Yao XD, Ball TB, McKinnon LR, Omange WR, et al. (2009) HIV-1 RNA dysregulates the natural TLR response to subclinical endotoxemia in Kenyan female sex-workers. PLoS One 4: e5644.
86. McLaren PJ, Ball TB, Wachihi C, Jaoko W, Kelvin DJ, et al. (2010) HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. J Infect Dis 202 (Suppl 3): S339-344.
87. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
88. Taggart CC, Cryan SA, Weldon S, Gibbons A, Greene CM, et al. (2005) Secretory leucoprotease inhibitor binds to NF-kappaB binding sites in monocytes and inhibits p65 binding. J Exp Med 202: 1659-1668.
89. Mulligan MS, Lentsch AB, Huber-Lang M, Guo RF, Sarma V, et al. (2000) Anti-inflammatory effects of mutant forms of secretory leukocyte protease inhibitor. Am J Pathol 156: 1033-1039.
90. Pham CT, (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 6: 541-550.