Lipopolysaccharide-induced expression of matrix metalloproteinases in human monocytes is suppressed by IFN-γ via superinduction of ATF-3 and suppression of AP-1

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 5089-5097

  Ho, Hao H ^a,b   Antoniv, Taras T ^a   Ji, Jong Dae ^a,c   Ivashkiv, Lionel B ^a,d  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Korea University College of Medicine   (South Korea)

^d Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CYTOKINE; DNA; GAMMA INTERFERON; INTERSTITIAL COLLAGENASE; LIPOPOLYSACCHARIDE; MACROPHAGE ACTIVATING FACTOR; MATRIX METALLOPROTEINASE; RNA; STAT1 PROTEIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; ATF3 PROTEIN, HUMAN; AUTACOID; DNA BINDING PROTEIN; MMP1 PROTEIN, HUMAN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN C FOS; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA BINDING; GENE OVEREXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; RNA INTERFERENCE; BIOSYNTHESIS; CELL CULTURE; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTOR 3; CELL LINE, TUMOR; CELLS, CULTURED; DNA-BINDING PROTEINS; DOWN-REGULATION; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MACROPHAGES; MATRIX METALLOPROTEINASE 1; MONOCYTES; PROTO-ONCOGENE PROTEINS C-FOS; REPRESSOR PROTEINS; TETRADECANOYLPHORBOL ACETATE; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR AP-1;

EID: 55149096344     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.5089     Document Type: Article

References (72)

1. Gross, J., and C. M. Lapiere. 1962. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. USA 48: 1014-1022.
2. Woessner, J. F., Jr. 1991. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5: 2145-2154.
3. Chakraborti, S., M. Mandal, S. Das, A. Mandal, and T. Chakraborti. 2003. Regulation of matrix metalloproteinases: an overview. Mol. Cell. Biochem. 253: 269-285.
4. Sounni, N. E., and A. Noel. 2005. Membrane type-matrix metalloproteinases and tumor progression. Biochimie 87: 329-342.
5. Lemaitre, V., and J. D'Armiento. 2006. Matrix metalloproteinases in development and disease. Birth Defects Res. C Embryo Today 78: 1-10.
6. Vincenti, M. P., and C. E. Brinckerhoff. 2002. Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res. 4: 157-164.
7. Huntington, J. T., J. M. Shields, C. J. Der, C. A. Wyatt, U. Benbow, C. L. Slingluff, Jr., and C. E. Brinckerhoff. 2004. Overexpression of collagenase 1 (MMP-1) is mediated by the ERK pathway in invasive melanoma cells: role of BRAF mutation and fibroblast growth factor signaling. J. Biol. Chem. 279: 33168-33176.
8. McQuibban, G. A., J. H. Gong, E. M. Tam, C. A. McCulloch, I. Clark-Lewis, and C. M. Overall. 2000. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289: 1202-1206.
9. Wilson, C. L., A. J. Ouellette, D. P. Satchell, T. Ayabe, Y. S. Lopez-Boado, J. L. Stratman, S. J. Hultgren, L. M. Matrisian, and W. C. Parks. 1999. Regulation of intestinal α-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286: 113-117.
10. Powell, W. C., B. Fingleton, C. L. Wilson, M. Boothby, and L. M. Matrisian. 1999. The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis. Curr. Biol. 9: 1441-1447.
11. Hartzell, W., and S. D. Shapiro. 1999. Macrophage elastase prevents Gemella morbillorum infection and improves outcome following murine bone marrow transplantation. Chest 116: 31S-32S. (Pubitemid 29340194)
12. Lopez-Boado, Y. S., C. L. Wilson, L. V. Hooper, J. I. Gordon, S. J. Hultgren, and W. C. Parks. 2000. Bacterial exposure induces and activates matrilysin in mucosal epithelial cells. J. Cell Biol. 148: 1305-1315.
13. Corry, D. B., K. Rishi, J. Kanellis, A. Kiss, L. Z. Song Lz, J. Xu, L. Feng, Z. Werb, and F. Kheradmand. 2002. Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency. Nat. Immunol. 3: 347-353.
14. Li, Q., P. W. Park, C. L. Wilson, and W. C. Parks. 2002. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111: 635-646. (Pubitemid 35441246)
15. Haro, H., H. C. Crawford, B. Fingleton, J. R. MacDougall, K. Shinomiya, D. M. Spengler, and L. M. Matrisian. 2000. Matrix metalloproteinase-3-dependent generation of a macrophage chemoattractant in a model of herniated disc resorption. J. Clin. Invest. 105: 133-141. (Pubitemid 30054352)
16. Liu, Z., X. Zhou, S. D. Shapiro, J. M. Shipley, S. S. Twining, L. A. Diaz, R. M. Senior, and Z. Werb. 2000. The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 102: 647-655.
17. Haro, H., H. C. Crawford, B. Fingleton, K. Shinomiya, D. M. Spengler, and L. M. Matrisian. 2000. Matrix metalloproteinase-7-dependent release of tumor necrosis factor-α in a model of herniated disc resorption. J. Clin. Invest. 105: 143-150. (Pubitemid 30054353)
18. Parks, W. C., C. L. Wilson, and Y. S. Lopez-Boado. 2004. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4: 617-629. (Pubitemid 39025047)
19. Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2: 161-174. (Pubitemid 37328786)
20. Schroen, D. J., and C. E. Brinckerhoff. 1996. Nuclear hormone receptors inhibit matrix metalloproteinase (MMP) gene expression through diverse mechanisms. Gene Expression 6: 197-207.
21. Szekanecz, Z., and A. E. Koch. 2007. Macrophages and their products in rheumatoid arthritis. Curr. Opin. Rheumatol. 19: 289-295. (Pubitemid 46597469)
22. Stoll, G., and M. Bendszus. 2006. Inflammation and atherosclerosis: novel insights into plaque formation and destabilization. Stroke 37: 1923-1932. (Pubitemid 44297753)
23. Takahashi, K., M. Takeya, and N. Sakashita. 2002. Multifunctional roles of macrophages in the development and progression of atherosclerosis in humans and experimental animals. Med. Electron Microsc. 35: 179-203. (Pubitemid 36205679)
24. Boyle, J. J. 2005. Macrophage activation in atherosclerosis: pathogenesis and pharmacology of plaque rupture. Curr. Vasc. Pharmacol. 3: 63-68.
25. Libby, P. 2000. Changing concepts of atherogenesis. J. Intern. Med. 247: 349-358.
26. Shah, P. K., E. Falk, J. J. Badimon, A. Fernandez-Ortiz, A. Mailhac, G. Villareal-Levy, J. T. Fallon, J. Regnstrom, and V. Fuster. 1995. Human monocyte- derived macrophages induce collagen breakdown in fibrous caps of atherosclerotic plaques: potential role of matrix-degrading metalloproteinases and implications for plaque rupture. Circulation 92: 1565-1569.
27. Sukhova, G. K., U. Schonbeck, E. Rabkin, F. J. Schoen, A. R. Poole, R. C. Billinghurst, and P. Libby. 1999. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation 99: 2503-2509.
28. Xu, Y., L. Wang, G. Buttice, P. K. Sengupta, and B. D. Smith. 2004. Major histocompatibility class II transactivator (CIITA) mediates repression of collagen (COL1A2) transcription by interferon γ (IFN-γ). J. Biol. Chem. 279: 41319-41332. (Pubitemid 39328146)
29. Lewis, M., E. P. Amento, and E. N. Unemori. 1999. Transcriptional inhibition of stromelysin by interferon-γ in normal human fibroblasts is mediated by the AP-1 domain. J. Cell. Biochem. 72: 373-386. (Pubitemid 29047400)
30. Ma, Z., M. J. Chang, R. C. Shah, and E. N. Benveniste. 2005. Interferon-γ- activated STAT-1α suppresses MMP-9 gene transcription by sequestration of the coactivators CBP/p300. J. Leukocyte Biol. 78: 515-523. (Pubitemid 41061323)
31. Yokota, H., M. B. Goldring, and H. B. Sun. 2003. CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J. Biol. Chem. 278: 47275-47280. (Pubitemid 37452316)
32. Andrews, H. J., R. A. Bunning, C. A. Dinarello, and R. G. Russell. 1989. Modulation of human chondrocyte metabolism by recombinant human interferon γ: in-vitro effects on basal and IL-1-stimulated proteinase production, cartilage degradation and DNA synthesis. Biochim. Biophys. Acta 1012: 128-134.
33. Unemori, E. N., M. J. Bair, E. A. Bauer, and E. P. Amento. 1991. Stromelysin expression regulates collagenase activation in human fibroblasts: dissociable control of two metalloproteinases by interferon-γ. J. Biol. Chem. 266: 23477-23482.
34. Varga, J., T. Yufit, and R. R. Brown. 1995. Inhibition of collagenase and stromelysin gene expression by interferon-γ in human dermal fibroblasts is mediated in part via induction of tryptophan degradation. J. Clin. Invest. 96: 475-481.
35. Nozell, S., Z. Ma, C. Wilson, R. Shah, and E. N. Benveniste. 2004. Class II major histocompatibility complex transactivator (CIITA) inhibits matrix metalloproteinase- 9 gene expression. J. Biol. Chem. 279: 38577-38589. (Pubitemid 39296012)
36. Fenrick, R., L. Wang, J. Nip, J. M. Amann, R. J. Rooney, J. Walker-Daniels, H. C. Crawford, D. L. Hulboy, M. S. Kinch, L. M. Matrisian, and S. W. Hiebert. 2000. TEL, a putative tumor suppressor, modulates cell growth and cell morphology of ras-transformed cells while repressing the transcription of stromelysin- 1. Mol. Cell. Biol. 20: 5828-5839. (Pubitemid 30613032)
37. Barchowsky, A., D. Frleta, and M. P. Vincenti. 2000. Integration of the NF-κB and mitogen-activated protein kinase/AP-1 pathways at the collagenase-1 promoter: divergence of IL-1 and TNF-dependent signal transduction in rabbit primary synovial fibroblasts. Cytokine 12: 1469-1479. (Pubitemid 30786268)
38. Quinones, S., J. Saus, Y. Otani, E. D. Harris, Jr., and M. Kurkinen. 1989. Transcriptional regulation of human stromelysin. J. Biol. Chem. 264: 8339-8344.
39. Buttice, G., and M. Kurkinen. 1993. A polyomavirus enhancer A-binding protein- 3 site and Ets-2 protein have a major role in the 12-O- tetradecanoylphorbol- 13-acetate response of the human stromelysin gene. J. Biol. Chem. 268: 7196-7204. (Pubitemid 23105610)
40. Buttice, G., S. Quinones, and M. Kurkinen. 1991. The AP-1 site is required for basal expression but is not necessary for TPA-response of the human stromelysin gene. Nucleic Acids Res. 19: 3723-3731. (Pubitemid 21912741)
41. Bidder, M., A. P. Loewy, T. Latifi, E. P. Newberry, G. Ferguson, D. M. Willis, and D. A. Towler. 2000. Ets domain transcription factor PE1 suppresses human interstitial collagenase promoter activity by antagonizing protein-DNA interactions at a critical AP1 element. Biochemistry 39: 8917-8928. (Pubitemid 30602802)
42. Jinnin, M., H. Ihn, Y. Mimura, Y. Asano, K. Yamane, and K. Tamaki. 2005. Matrix metalloproteinase-1 up-regulation by hepatocyte growth factor in human dermal fibroblasts via ERK signaling pathway involves Ets1 and Fli1. Nucleic Acids Res. 33: 3540-3549. (Pubitemid 41430577)
43. Jayaraman, G., R. Srinivas, C. Duggan, E. Ferreira, S. Swaminathan, K. Somasundaram, J. Williams, C. Hauser, M. Kurkinen, R. Dhar, et al. 1999. p300/cAMP-responsive element-binding protein interactions with ets-1 and ets-2 in the transcriptional activation of the human stromelysin promoter. J. Biol. Chem. 274: 17342-17352. (Pubitemid 129519072)
44. Nakajima, H., Y. Hiyama, W. Tsukada, H. Warabi, S. Uchida, and S. Hirose. 1990. Effects of interferon γ on cultured synovial cells from patients with rheumatoid arthritis: inhibition of cell growth, prostaglandin E2, and collagenase release. Ann. Rheum. Dis. 49: 512-516. (Pubitemid 20225402)
45. Schroen, D. J., J. D. Chen, M. P. Vincenti, and C. E. Brinckerhoff. 1997. The nuclear receptor corepressor SMRT inhibits interstitial collagenase (MMP-1) transcription through an HRE-independent mechanism. Biochem. Biophys. Res. Commun. 237: 52-58.
46. Khan, K. M., L. R. Howe, and D. J. Falcone. 2004. Extracellular matrix-induced cyclooxygenase-2 regulates macrophage proteinase expression. J. Biol. Chem. 279: 22039-22046.
47. Zhang, Y., K. McCluskey, K. Fujii, and L. M. Wahl. 1998. Differential regulation of monocyte matrix metalloproteinase and TIMP-1 production by TNF-α, granulocyte- macrophage CSF, and IL-1 β through prostaglandin-dependent and -independent mechanisms. J. Immunol. 161: 3071-3076. (Pubitemid 28425734)
48. Lai, W. C., M. Zhou, U. Shankavaram, G. Peng, and L. M. Wahl. 2003. Differential regulation of lipopolysaccharide-induced monocyte matrix metalloproteinase (MMP)-1 and MMP-9 by p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J. Immunol. 170: 6244-6249.
49. Rubinson, D. A., C. P. Dillon, A. V. Kwiatkowski, C. Sievers, L. Yang, J. Kopinja, M. Zhang, M. T. McManus, F. B. Gertler, M. L. Scott, and L. Van Parijs. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33: 401-406. (Pubitemid 36278858)
50. Tassiulas, I., X. Hu, H. Ho, Y. Kashyap, P. Paik, Y. Hu, C. A. Lowell, and L. B. Ivashkiv. 2004. Amplification of IFN-α-induced STAT1 activation and inflammatory function by Syk and ITAM-containing adaptors. Nat. Immunol. 5: 1181-1189. (Pubitemid 39549633)
51. Sengupta, T. K., A. Chen, Z. Zhong, J. E. Darnell, Jr., and L. B. Ivashkiv. 1995. Activation of monocyte effector genes and STAT family transcription factors by inflammatory synovial fluid is independent of interferon γ. J. Exp. Med. 181: 1015-1025.
52. Hu, X., P. K. Paik, J. Chen, A. Yarilina, L. Kockeritz, T. T. Lu, J. R. Woodgett, and L. B. Ivashkiv. 2006. IFN-γ suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 24: 563-574. (Pubitemid 43728157)
53. Angel, P., I. Baumann, B. Stein, H. Delius, H. J. Rahmsdorf, and P. Herrlich. 1987. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol. Cell. Biol. 7: 2256-2266.
54. Westermarck, J., and V. M. Kahari. 1999. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13: 781-792. (Pubitemid 29220691)
55. Benbow, U., and C. E. Brinckerhoff. 1997. The AP-1 site and MMP gene regulation: what is all the fuss about? Matrix Biol. 15: 519-526. (Pubitemid 27190026)
56. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptormediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784. (Pubitemid 43090463)
57. Ramana, C. V., M. P. Gil, R. D. Schreiber, and G. R. Stark. 2002. Stat1-dependent and -independent pathways in IFN-γ-dependent signaling. Trends Immunol. 23: 96-101.
58. Ho, H. H., and L. B. Ivashkiv. 2006. Role of STAT3 in type I interferon responses: negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 281: 14111-14118.
59. Gilchrist, M., V. Thorsson, B. Li, A. G. Rust, M. Korb, K. Kennedy, T. Hai, H. Bolouri, and A. Aderem. 2006. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441: 173-178.
60. Westermarck, J., A. Seth, and V. M. Kahari. 1997. Differential regulation of interstitial collagenase (MMP-1) gene expression by ETS transcription factors. Oncogene 14: 2651-2660. (Pubitemid 27283104)
61. Oikawa, T. 2004. ETS transcription factors: possible targets for cancer therapy. Cancer Sci. 95: 626-633. (Pubitemid 39255808)
62. Schroen, D. J., and C. E. Brinckerhoff. 1996. Inhibition of rabbit collagenase (matrix metalloproteinase-1; MMP-1) transcription by retinoid receptors: evidence for binding of RARs/RXRs to the -77 AP-1 site through interactions with c-Jun. J. Cell. Physiol. 169: 320-332.
63. Benbow, U., J. L. Rutter, C. H. Lowrey, and C. E. Brinckerhoff. 1999. Transcriptional repression of the human collagenase-1 (MMP-1) gene in MDA231 breast cancer cells by all-trans-retinoic acid requires distal regions of the promoter. Br. J. Cancer 79: 221-228. (Pubitemid 29002289)
64. Tower, G. B., C. I. Coon, K. Belguise, D. Chalbos, and C. E. Brinckerhoff. 2003. Fra-1 targets the AP-1 site/2G single nucleotide polymorphism (ETS site) in the MMP-1 promoter. Eur. J. Biochem. 270: 4216-4225.
65. Newberry, E. P., D. Willis, T. Latifi, J. M. Boudreaux, and D. A. Towler. 1997. Fibroblast growth factor receptor signaling activates the human interstitial collagenase promoter via the bipartite Ets-AP1 element. Mol. Endocrinol. 11: 1129-1144.
66. Yan, C., and D. D. Boyd. 2007. Regulation of matrix metalloproteinase gene expression. J. Cell. Physiol. 211: 19-26. (Pubitemid 46363892)
67. Shapiro, S. D., E. J. Campbell, D. K. Kobayashi, and H. G. Welgus. 1990. Immune modulation of metalloproteinase production in human macrophages: selective pretranslational suppression of interstitial collagenase and stromelysin biosynthesis by interferon-γ. J. Clin. Invest. 86: 1204-1210.
68. Nguyen, J., P. Knapnougel, P. Lesavre, and B. Bauvois. 2005. Inhibition of matrix metalloproteinase-9 by interferons and TGF-β1 through distinct signalings accounts for reduced monocyte invasiveness. FEBS Lett. 579: 5487-5493. (Pubitemid 41455619)
69. Hu, X., K. H. Park-Min, H. H. Ho, and L. B. Ivashkiv. 2005. IFN-γ-primed macrophages exhibit increased CCR2-dependent migration and altered IFN-γ responses mediated by Stat1. J. Immunol. 175: 3637-3647. (Pubitemid 41292023)
70. Tsareva, S. A., R. Moriggl, F. M. Corvinus, B. Wiederanders, A. Schutz, B. Kovacic, and K. Friedrich. 2007. Signal transducer and activator of transcription 3 activation promotes invasive growth of colon carcinomas through matrix metalloproteinase induction. Neoplasia 9: 279-291.
71. Itoh, M., T. Murata, T. Suzuki, M. Shindoh, K. Nakajima, K. Imai, and K. Yoshida. 2006. Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells. Oncogene 25: 1195-1204. (Pubitemid 43297934)
72. Sharma, B., and R. V. Iozzo. 1998. Transcriptional silencing of perlecan gene expression by interferon-γ. J. Biol. Chem. 273: 4642-4646. (Pubitemid 28103209)