Lack of Interferon-γ Production Despite the Presence of Interleukin-18 During Cutaneous Wound Healing

Molecular Medicine

Volumn 6, Issue 12, 2000, Pages 1016-1027

  Kämpfer, Heiko ^a   Paulukat, Jens ^a   Mühl, Heiko ^a   Wetzler, Christian ^a   Pfeilschifter, Josef ^a   Frank, Stefan ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Cutaneous Wound Repair; Injury Site; Prolonged Inflammatory Phase; RNase Protection Assay; Skin Repair

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; INTERLEUKIN 18; MESSENGER RNA; RIBONUCLEASE; RNA;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; DBA MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL DIABETES MELLITUS; FEMALE; GENETICS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE; METABOLISM; MOUSE; MUTATION; PATHOLOGY; PHENOTYPE; PROMOTER REGION; SKIN; TIME; TISSUE DISTRIBUTION; UPREGULATION; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DNA, COMPLEMENTARY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE II; INTERLEUKIN-18; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; MUTATION; PHENOTYPE; PROMOTER REGIONS (GENETICS); RIBONUCLEASES; RNA; RNA, MESSENGER; SKIN; TIME FACTORS; TISSUE DISTRIBUTION; UP-REGULATION; WOUND HEALING;

MLCS; MLOWN;

EID: 0034575279     PISSN: 10761551     EISSN: 15283658     Source Type: Journal    
DOI: 10.1007/BF03402053     Document Type: Article

References (57)

1. S.A. Jimenez B. Freundlich J. Rosenbloom Selective inhibition of human diploid fibroblast collagen synthesis by interferons J. Clin. Invest. 1984 74 1112 1116 10.1172/JCI111480 1:CAS:528:DyaL2cXls1ykurY%3D 6432846 425272
2. M.R. Duncan B. Berman Persistence of a reduced-collagen-producing phenotype in cultured scleroderma fibroblasts after short term exposure to interferons J. Clin. Invest. 1987 79 1318 1324 10.1172/JCI112956 1:CAS:528:DyaL2sXktVGms7w%3D 2437154 424374
3. M.J. Czaja F.R. Weiner M. Eghbali M. Giambrone M. Eghbali M.A. Zern Differential effects of gamma-interferon on collagen and fibronectin gene expression J. Biol. Chem. 1987 262 13348 13351 3115979 1:CAS:528:DyaL2sXlslCjtLw%3D
4. R.D. Granstein T.J. Flotte E.P. Amento Interferons and collagen production J. Invest. Dermatol. 1990 95 75 80 10.1111/1523-1747.ep12874789
5. R. Fleischmajer J.J. Perlish M. Duncan Scleroderma: a model for fibrosis Arch. Dermatol. 1983 119 957 962 10.1001/archderm.1983.01650360003004 1:STN:280:DyaL2c%2FnvVGktw%3D%3D 6360053
6. J.C. Murray S.V. Pollack S.R. Pinnell Keloids: a review J. Am. Acad. Dermatol. 1981 4 461 470 10.1016/S0190-9622(81)70048-3 1:STN:280:DyaL3M7pt1Ggug%3D%3D 7014664
7. F.W. Symington Lymphotoxin, tumor necrosis factor, and gamma interferon are cytostatic for normal human keratinocytes J. Invest. Dermatol. 1989 92 798 805 10.1111/1523-1747.ep12696816 1:CAS:528:DyaL1MXkslKiurg%3D 2470828
8. A. Scheynius J. Fransson C. Johansson H. Hammar B. Baker L. Fry H. Valsimarsson Expression of interferon-gamma receptors in normal and psoriatic skin J. Invest. Dermatol. 1992 98 255 258 10.1111/1523-1747.ep12556086 1:STN:280:DyaK387itFKlsQ%3D%3D 1531061
9. R. Hein J. Behr M. Hundgen et al. Treatment of systemic sclerosis with gamma-interferon Br. J. Dermatol. 1992 126 496 501 10.1111/j.1365-2133.1992.tb11824.x 1:STN:280:DyaK38zgsVOmsw%3D%3D 1610690
10. N. Hunzelmann S. Anders G. Fierlbeck et al. Systemic scleroderma. Multicenter trial of 1 year of treatment with recombinant interferon gamma Arch. Dermatol. 1997 13 609 613 10.1001/archderm.1997.03890410065008
11. R.D. Granstein G.F. Murphy R.J. Margolis M.H. Byrne E.P. Amento Gamma interferon inhibits collagen synthesis in vivo in the mouse J. Clin. Invest. 1987 79 1254 1258 10.1172/JCI112945 1:CAS:528:DyaL2sXitFahtrY%3D 3104404 424325
12. R.D. Granstein M.R. Deak S.L. Jacques et al. The systemic administration of gamma interferon inhibits collagen synthesis and acute inflammation in a murine skin wounding model J. Invest. Dermatol. 1989 93 18 27 10.1111/1523-1747.ep12277336 1:CAS:528:DyaL1MXltFentLw%3D 2501396
13. M. Munder M. Mallo K. Eichmann M. Modolell Murine macrophages secrete interferon-γ upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation J. Exp. Med. 1998 187 2103 2108 10.1084/jem.187.12.2103 1:CAS:528:DyaK1cXktVemur8%3D 9625771 2212367
14. S.E.M. Howie R.D. Aldridge E. McVittie R.J. Forsey C. Sands J.A.A. Hunter Epidermal keratinocyte production of interferon-γ immunoreactive protein and mRNA is an early event in allergic contact dermatitis J. Invest. Dermatol. 1996 106 1218 1223 10.1111/1523-1747.ep12348507 1:CAS:528:DyaK28XksVajsLk%3D 8752660
15. T.R. Mosmann H. Cherwinski M.W. Bond M.A. Giedlin R.L. Coffman Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J. Immunol. 1986 136 2348 2357 2419430 1:CAS:528:DyaL28XhvVClsbk%3D
16. T.R. Mosmann R.L. Coffman TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties Annu. Rev. Immunol. 1989 7 145 173 10.1146/annurev.iy.07.040189.001045 1:CAS:528:DyaL1MXit12lsbk%3D 2523712
17. R.S. Fishel A. Barbul W.E. Beschorner H.L. Wasserkrug G. Efron Lymphocyte participation in wound healing: morphologic assessment using monoclonal antibodies Ann. Surg. 1987 206 25 29 10.1097/00000658-198707000-00004 1:STN:280:DyaL2s3mvFyntw%3D%3D 2955751 1492926
18. R. Ross E.P. Benditt Wound healing and collagen formation. Fine structure in experimental scurvy J. Cell Biol. 1962 12 533 548 10.1083/jcb.12.3.533 1:CAS:528:DyaF38Xkt1GqtLk%3D 14494203 2106045
19. J.E. Efron F.L. Frankel S.A. Lazarou H.L. Wasserkrug A. Barbul Wound healing and T-lymphocytes J. Surg. Res. 1990 48 460 463 10.1016/0022-4804(90)90013-R 1:STN:280:DyaK3c3nvFaquw%3D%3D 2352421
20. H. Kämpfer U. Kalina H. Mühl J. Pfeilschifter S. Frank Counterregulation of interleukin-18 mRNA and protein expression during cutaneous wound repair in mice J. Invest. Dermatol. 1999 113 369 374 10.1046/j.1523-1747.1999.00704.x 10469336
21. D.L. Coleman Diabetes-obesity syndromes in mice Diabetes 1982 31 1 6 10.2337/diab.31.1.S1 1:STN:280:DyaL3s7jt1yltA%3D%3D 7160533
22. H. Chen O. Charlat L.A. Tartaglia et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice Cell 1996 84 491 495 10.1016/S0092-8674(00)81294-5 1:CAS:528:DyaK28XhtFWqt7s%3D 8608603
23. G.H. Lee R. Proenca J.M. Montez K.M. Carroll J.G. Darvishzadeh J.I. Lee J.M. Friedman Abnormal splicing of the leptin receptor in diabetic mice Nature 1996 379 632 635 10.1038/379632a0 1:CAS:528:DyaK28XhtFKru7o%3D 8628397
24. P. Chomczynski N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 1987 162 156 159 10.1016/0003-2697(87)90021-2 1:CAS:528:DyaL2sXitFSns7Y%3D 2440339
25. S. Werner K.G. Peters M.T. Longaker F. Fuller-Pace M.J. Banda L.T. Williams Large induction of keratinocyte growth factor expression in the dermis during wound healing Proc. Natl. Acad. Sci. USA 1992 89 6896 6900 10.1073/pnas.89.15.6896 1:CAS:528:DyaK38XlsVynt70%3D 1379725
26. P.W. Gray D.V. Goeddel Cloning and expression of murine immune interferon cDNA Proc. Natl. Acad. Sci. USA 1983 80 5842 5846 10.1073/pnas.80.19.5842 1:CAS:528:DyaL2cXmt1Orug%3D%3D 6310596
27. W. Chu D.A. Johnson P.R. Musich Molecular cloning and characterization of mouse mast cell chymases Biochem. Biophys. Acta 1992 1121 83 87 1376147 1:CAS:528:DyaK3sXktVersLc%3D
28. H. Mühl C.A. Dinarello Macrophage inflammatory protein-1 alpha production in lipopolysaccharide-stimulated human adherent blood mononuclear cells is inhibited by the nitric oxide synthase inhibitor N(G)-monomethyl-L-arginine J. Immunol. 1997 159 5063 5069 9366434
29. S. Akira The role of IL-18 in innate immunity Curr. Opin. Immunol. 2000 12 59 63 10.1016/S0952-7915(99)00051-5 1:CAS:528:DC%2BD3cXhsVOkurw%3D 10679398
30. C. Wetzler H. Kämpfer B. Stallmeyer J. Pfeilschifter S. Frank Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse: prolonged persistance of neutrophils and macrophages during the late phase of repair J. Invest. Dermatol. 2000 115 245 253 10.1046/j.1523-1747.2000.00029.x 1:CAS:528:DC%2BD3cXlvFOltLw%3D 10951242
31. P.J. Maddon S.M. Molineaux D.E. Maddon et al. Structure and expression of the human and mouse T4 genes Proc. Natl. Acad. Sci. USA 1987 84 9155 9159 10.1073/pnas.84.24.9155 1:CAS:528:DyaL1cXhvF2hsrc%3D 3501122
32. J.M. Austyn S. Gordon F4/80, a monoclonal antibody directed specifically against the mouse macrophage Eur. J. Immunol. 1981 11 805 815 10.1002/eji.1830111013 1:STN:280:DyaL38%2Fnt12jsg%3D%3D 7308288
33. H. Mizutani N. Schechter G. Lazarus R.A. Black T.S. Kuppers Rapid and specific conversion of precursor interleukin 1β (IL-1β) to an active IL-1 species by human mast cell chymase J. Exp. Med. 1991 174 821 825 10.1084/jem.174.4.821 1:CAS:528:DyaK3MXmtVGksLk%3D 1919436
34. D.J. Hazuda J. Strickler F. Kueppers P.L. Simon P.R. Young Processing of precursor interleukin 1β and inflammatory disease J. Biol. Chem. 1990 265 6318 6322 1:CAS:528:DyaK3cXktVCntr4%3D 2156847
35. U. Schonbeck F. Mach P. Libby Generation of biologically active IL-1β by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1β processing J. Immunol. 1998 161 3340 3346 1:CAS:528:DyaK1cXmsFWntbs%3D 9759850
36. P. Martin Wound healing—aiming for perfect skin regeneration Science 1997 276 75 81 10.1126/science.276.5309.75 1:CAS:528:DyaK2sXitlyqtLw%3D 9082989
37. B. Eckes M. Aumailley T. Krieg R.A.F. Clark Collagens and the reestablishment of dermal integrity The Molecular and Cellular Biology of Wound Repair 1996 New York Plenum Press 493 512
38. S. Frank M. Madlener S. Werner Transforming growth factors β1, β2, and β3 and their receptors are differentially regulated during normal and impaired wound healing J. Biol. Chem. 1996 271 10188 10193 10.1074/jbc.271.17.10188 1:CAS:528:DyaK28XisFKjsrk%3D 8626581
39. M. Shah D.M. Foreman M.W.J. Ferguson Neutralisation of TGF-β1 and TGF-β2 or exogenous addition of TGF-β3 to cutaneous rat wounds reduces scarring J. Cell Sci. 1995 108 985 1002 7542672 1:CAS:528:DyaK2MXkvFaltr4%3D
40. M.P. Welsh G.F. Odland R.A.F. Clark Temporal relationships of F-actin bundle formation, collagen and fibronectin matrix assembly, and fibronectin receptor expression to wound contraction J. Cell. Biol. 1990 110 133 145 10.1083/jcb.110.1.133
41. R.A. Ignotz J. Massague Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into extracellular matrix J. Biol. Chem. 1986 261 4337 4340 3456347 1:CAS:528:DyaL28Xhs1amur4%3D
42. A.B. Roberts M.B. Sporn R.K. Assoian et al. Transforming growth factor β: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation Proc. Natl. Acad. Sci. USA 1986 83 4167 4171 10.1073/pnas.83.12.4167 1:CAS:528:DyaL28XksFGhtL0%3D 2424019
43. M. Schäffer A. Barbul Lymphocyte function in wound healing and following injury Br. J. Surgery 1998 85 444 460 10.1046/j.1365-2168.1998.00734.x
44. R.E. Pollock G.F. Babcock M.M. Romsdahl K. Nishioka Surgical stress-mediated suppression of murine natural killer cell cytotoxicity Cancer Res. 1984 44 3888 3891 6744305 1:STN:280:DyaL2c3lvFWguw%3D%3D
45. B.A. Blazar M.L. Rodrick J.B. O’Mahony J.J. Wood P.Q. Bessey D.W. Wilmore J.A. Mannick Suppression of natural killer-cell function in humans following thermal and traumatic injury J. Clin. Immunol. 1986 6 26 36 10.1007/BF00915361 1:STN:280:DyaL287mvVOmug%3D%3D 3485653
46. L.A. DiPietro Wound healing: the role of the macrophage and other immune cells Shock 1995 4 233 240 10.1097/00024382-199510000-00001 1:STN:280:DyaK287hvVSgsg%3D%3D 8564549
47. T. Espevik I.S. Figari M.R. Shalaby G.A. Lackides G.D. Lewis H.M. Shepard M.A. Palladino Inhibition of cytokine production by cyclosporin A and transforming growth factor β. J. Exp. Med. 1987 166 571 576 10.1084/jem.166.2.571 1:CAS:528:DyaL2sXlsVKqu7Y%3D 3110354
48. A.B. Roberts Transforming growth factor-β: activity and efficacy in animal models of wound healing Wound Repair Regen. 1995 3 408 418 10.1046/j.1524-475X.1995.30405.x 1:STN:280:DC%2BD28jht1altw%3D%3D 17147652
49. S. O’Kane M.W. Ferguson Transforming growth factor βs and wound healing Int. J. Biochem. Cell Biol. 1997 29 63 78 10.1016/S1357-2725(96)00120-3 9076942
50. G.S. Sidhu D. Thaloor A.K. Singh P.N. Raghunath R.K. Maheshwari Enhanced biosynthesis of extracellular matrix proteins and TGF-β1 by polyinosinic-polycytidylic acid during cutaneous wound healing in vivo J. Cell Physiol. 1996 169 108 114 10.1002/(SICI)1097-4652(199610)169:1<108::AID-JCP11>3.0.CO;2-9 1:CAS:528:DyaK28XmtFClu74%3D 8841427
51. T. Ghayur S. Banerjee M. Hugunin et al. Caspase-1 processes IFN-γ-inducing factor and regulates LPS-induced IFN-γ production Nature 1997 386 619 623 10.1038/386619a0 1:CAS:528:DyaK2sXisFCntr0%3D 9121587
52. Y. Gu K. Kuida H. Tsutsui et al. Activation of interferon-γ inducing factor mediated by interleukin-1β converting enzyme Science 1997 275 206 209 10.1126/science.275.5297.206 1:CAS:528:DyaK2sXksFyrsQ%3D%3D 8999548
53. K. Nakamura H. Okamura M. Wada K. Nagata T. Tamura Endotoxin-induced serum factor that stimulates γ interferon production Infect. Immunol. 1989 57 590 595 1:CAS:528:DyaL1MXhtFartb0%3D
54. K. Kohno J. Kataoka T. Ohtsuki et al. IFN-γ-inducing factor (IGIF) is a co-stimulatory factor on the activation of Th1 but not Th2 cells and exerts its effects independently of IL-12 J. Immunol. 1997 158 1541 1550 9029088 1:CAS:528:DyaK2sXhtF2gtL0%3D
55. D. Robinson K. Shibuya A. Mui et al. IGIF does not drive Th1 development but synergizes with IL-12 for interferon-γ production and activates IRAK and NFκB Immunity 1997 7 571 581 10.1016/S1074-7613(00)80378-7 1:CAS:528:DyaK2sXntVWisLs%3D 9354477
56. A.J. Puren G. Fantuzzi Y. Gu M.S. Su C.A. Dinarello Interleukin-18 (IFN γ-inducing factor) induces IL-8 and IL-1β via TNF alpha production from non-CD14+ human blood mononuclear cells J. Clin. Invest. 1998 101 711 721 10.1172/JCI1379 1:CAS:528:DyaK1cXosVamtw%3D%3D 9449707 508617
57. L. Kremer L. Dupre I. Wolowczuk C. Locht In vivo immunomodulation following intradermal injection with DNA encoding IL-18 J. Immunol. 1999 163 3226 3231 10477591 1:CAS:528:DyaK1MXlvV2lsLs%3D