Matrix metalloproteinase 13 modulates intestinal epithelial barrier integrity in inflammatory diseases by activating TNF

EMBO Molecular Medicine

Volumn 5, Issue 7, 2013, Pages 1000-1016

  Vandenbroucke, Roosmarijn E ^a,b   Dejonckheere, Eline ^a,b   Van Hauwermeiren, Filip ^a,b   Lodens, Sofie ^a,b   De Rycke, Riet ^a,b   Van Wonterghem, Elien ^a,b   Staes, An ^a,b   Gevaert, Kris ^a,b   López Otin, Carlos ^c   Libert, Claude ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

Author keywords

IBD; Intestinal permeability; Matrix metalloproteinase; Sepsis; Tumour necrosis factor

Indexed keywords

COLLAGENASE 3; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE PERMEABILITY; COLITIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENDOTOXEMIA; FEMALE; GOBLET CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; INTESTINE EPITHELIUM CELL; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPSIS; TANDEM MASS SPECTROMETRY; TIGHT JUNCTION;

EID: 84880026950     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201202100     Document Type: Article

References (83)

1. Ailenberg M, Sefton MV (2009) Effect of a matrix metalloproteinase sequestering biomaterial on Caco-2 epithelial cell barrier integrity in vitro. Acta Biomater 5: 1898-1904
2. Albanese CT, Cardona M, Smith SD, Watkins S, Kurkchubasche AG, Ulman I, Simmons RL, Rowe MI (1994) Role of intestinal mucus in transepithelial passage of bacteria across the intact ileum in vitro. Surgery 116: 76-82
3. Asara JM, Zhang X, Zheng B, Christofk HH, Wu N, Cantley LC (2006) In-gel stable-isotope labeling (ISIL): a strategy for mass spectrometry-based relative quantification. J Proteome Res 5: 155-163
4. Balzan S, de Almeida Quadros C, de Cleva R, Zilberstein B, Cecconello I (2007) Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol 22: 464-471
5. Brown SJ, Mayer L (2007) The immune response in inflammatory bowel disease. Am J Gastroenterol 102: 2058-2069
6. Burrage PS, Mix KS, Brinckerhoff CE (2006) Matrix metalloproteinases: role in arthritis. Front Biosci 11: 529-543
7. Cantaluppi V, Assenzio B, Pasero D, Romanazzi GM, Pacitti A, Lanfranco G, Puntorieri V, Martin EL, Mascia L, Monti G, et al (2008) Polymyxin-B hemoperfusion inactivates circulating proapoptotic factors. Intensive Care Med 34: 1638-1645
8. Carrico CJ, Meakins JL, Marshall JC, Fry D, Maier RV (1986) Multiple-organ-failure syndrome. Arch Surg 121: 196-208
9. Cauwe B, Opdenakker G (2010) Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol 45: 351-423
10. Cauwe B, Van den Steen PE, Opdenakker G (2007) The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit Rev Biochem Mol Biol 42: 113-185
11. Chandler S, Cossins J, Lury J, Wells G (1996) Macrophage metalloelastase degrades matrix and myelin proteins and processes a tumour necrosis factor-alpha fusion protein. Biochem Biophys Res Commun 228: 421-429
12. Cruz DN, Perazella MA, Bellomo R, de Cal M, Polanco N, Corradi V, Lentini P, Nalesso F, Ueno T, Ranieri VM, et al (2007) Effectiveness of polymyxin B-immobilized fiber column in sepsis: a systematic review. Crit Care 11: R47
13. Cruz DN, Antonelli M, Fumagalli R, Foltran F, Brienza N, Donati A, Malcangi V, Petrini F, Volta G, Bobbio Pallavicini FM, et al (2009) Early use of polymyxin B hemoperfusion in abdominal septic shock: the EUPHAS randomized controlled trial. JAMA 301: 2445-2452
14. de Aquino SG, Guimaraes MR, Stach-Machado DR, da Silva JA, Spolidorio LC, Rossa C Jr (2009) Differential regulation of MMP-13 expression in two models of experimentally induced periodontal disease in rats. Arch Oral Biol 54: 609-617
15. Decock J, Thirkettle S, Wagstaff L, Edwards DR (2011) Matrix metalloproteinases: protective roles in cancer. J Cell Mol Med 15: 1254-1265
16. Deitch EA, Berg R (1987) Bacterial translocation from the gut: a mechanism of infection. J Burn Care Rehabil 8: 475-482
17. Dejager L, Pinheiro I, Dejonckheere E, Libert C (2011) Cecal ligation and puncture: the gold standard model for polymicrobial sepsis? Trends Microbiol 19: 198-208
18. Dejonckheere E, Vandenbroucke RE, Libert C (2011) Matrix metalloproteinase8 has a central role in inflammatory disorders and cancer progression. Cytokine Growth Factor Rev 22: 73-81
19. Dharmani P, Leung P, Chadee K (2011) Tumor necrosis factor-alpha and Muc2 mucin play major roles in disease onset and progression in dextran sodium sulphate-induced colitis. PLoS ONE 6: e25058
20. Dorman G, Cseh S, Hajdu I, Barna L, Konya D, Kupai K, Kovacs L, Ferdinandy P (2010) Matrix metalloproteinase inhibitors: a critical appraisal of design principles and proposed therapeutic utility. Drugs 70: 949-964
21. d'Ortho MP, Will H, Atkinson S, Butler G, Messent A, Gavrilovic J, Smith B, Timpl R, Zardi L, Murphy G (1997) Membrane-type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur J Biochem 250: 751-757
22. Faries PL, Simon RJ, Martella AT, Lee MJ, Machiedo GW (1998) Intestinal permeability correlates with severity of injury in trauma patients. J Trauma 44: 1031-1035 (discussion 1035-1036)
23. Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17: 375-412
24. Fink MP (2003) Intestinal epithelial hyperpermeability: update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr Opin Crit Care 9: 143-151
25. Fukuda H, Mochizuki S, Abe H, Okano HJ, Hara-Miyauchi C, Okano H, Yamaguchi N, Nakayama M, D'Armiento J, Okada Y (2011) Host-derived MMP-13 exhibits a protective role in lung metastasis of melanoma cells by local endostatin production. Br J Cancer 105: 1615-1624
26. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements JM, Crimmin M, Davidson AH, Drummond AH, Galloway WA, Gilbert R, et al (1995) Matrix metalloproteinases and processing of pro-TNF-alpha. J Leukoc Biol 57: 774-777
27. Gitter AH, Bendfeldt K, Schmitz H, Schulzke JD, Bentzel CJ, Fromm M (2000) Epithelial barrier defects in HT-29/B6 colonic cell monolayers induced by tumor necrosis factor-alpha. Ann N Y Acad Sci 915: 193-203
28. Hartenstein B, Dittrich BT, Stickens D, Heyer B, Vu TH, Teurich S, Schorpp-Kistner M, Werb Z, Angel P (2006) Epidermal development and wound healing in matrix metalloproteinase 13-deficient mice. J Invest Dermatol 126: 486-496
29. He F, Peng J, Deng XL, Yang LF, Camara AD, Omran A, Wang GL, Wu LW, Zhang CL, Yin F (2012) Mechanisms of tumor necrosis factor-alpha-induced leaks in intestine epithelial barrier. Cytokine 59: 264-272
30. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, Taupin D, Thornton DJ, Png CW, Crockford TL, Cornall RJ, et al (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54
31. Helsens K, Colaert N, Barsnes H, Muth T, Flikka K, Staes A, Timmerman E, Wortelkamp S, Sickmann A, Vandekerckhove J, et al (2010) ms_lims, a simple yet powerful open source laboratory information management system for MS-driven proteomics. Proteomics 10: 1261-1264
32. Huet E, Vallee B, Delbe J, Mourah S, Pruliere-Escabasse V, Tremouilleres M, Kadomatsu K, Doan S, Baudouin C, Menashi S, et al (2011) EMMPRIN modulates epithelial barrier function through a MMP-mediated occludin cleavage: implications in dry eye disease. Am J Pathol 179: 1278-1286
33. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101: 17192-17197
34. Iwaya H, Maeta K, Hara H, Ishizuka S (2012) Mucosal permeability is an intrinsic factor in susceptibility to dextran sulfate sodium-induced colitis in rats. Exp Biol Med (Maywood) 237: 451-460
35. John LJ, Fromm M, Schulzke JD (2011) Epithelial barriers in intestinal inflammation. Antioxid Redox Signal 15: 1255-1270
36. Kaser A, Flak MB, Tomczak MF, Blumberg RS (2011) The unfolded protein response and its role in intestinal homeostasis and inflammation. Exp Cell Res 317: 2772-2779
37. Kerensky TA, Gottlieb AB, Yaniv S, Au SC (2012) Etanercept: efficacy and safety for approved indications. Expert Opin Drug Safety 11: 121-139
38. Killar L, White J, Black R, Peschon J (1999) Adamalysins. A family of metzincins including TNF-alpha converting enzyme (TACE). Ann N Y Acad Sci 878: 442-452
39. Kitagawa H, Takeda F, Kohei H (1986) A simple method for estimation of gastric mucus and effects of antiulcerogenic agents on the decrease in mucus during water-immersion stress in rats. Arzneimittelforschung 36: 1240-1244
40. Le Gall SM, Bobe P, Reiss K, Horiuchi K, Niu XD, Lundell D, Gibb DR, Conrad D, Saftig P, Blobel CP (2009) ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol Biol Cell 20: 1785-1794
41. Lesuffleur T, Porchet N, Aubert JP, Swallow D, Gum JR, Kim YS, Real FX, Zweibaum A (1993) Differential expression of the human mucin genes MUC1 to MUC5 in relation to growth and differentiation of different mucus-secreting HT-29 cell subpopulations. J Cell Sci 106: 771-783
42. Li Q, Zhang Q, Zhang M, Wang C, Zhu Z, Li N, Li J (2008) Effect of n-3 polyunsaturated fatty acids on membrane microdomain localization of tight junction proteins in experimental colitis. FEBS J 275: 411-420
43. Li Q, Zhang Q, Wang C, Liu X, Li N, Li J (2009) Disruption of tight junctions during polymicrobial sepsis in vivo. J Pathol 218: 210-221
44. Lieberman JM, Sacchettini J, Marks C, Marks WH (1997) Human intestinal fatty acid binding protein: report of an assay with studies in normal volunteers and intestinal ischemia. Surgery 121: 335-342
45. Lu DY, Yu WH, Yeh WL, Tang CH, Leung YM, Wong KL, Chen YF, Lai CH, Fu WM (2009) Hypoxia-induced matrix metalloproteinase-13 expression in astrocytes enhances permeability of brain endothelial cells. J Cell Physiol 220: 163-173
46. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286: G367-G376
47. Ma TY, Boivin MA, Ye D, Pedram A, Said HM (2005) Mechanism of TNF-{alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol 288: G422-G430
48. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR II, Raleigh DR, Guan Y, Watson AJ, Montrose MH, et al (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126
49. McElroy SJ, Prince LS, Weitkamp JH, Reese J, Slaughter JC, Polk DB (2011) Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: a potential role in neonatal necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 301: G656-G666
50. McGuckin MA, Linden SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265-278
51. Mueller C, Corazza N, Trachsel-Loseth S, Eugster HP, Buhler-Jungo M, Brunner T, Imboden MA (1999) Noncleavable transmembrane mouse tumor necrosis factor-alpha (TNFalpha) mediates effects distinct from those of wild-type TNFalpha in vitro and in vivo. J Biol Chem 274: 38112-38118
52. Murthy S, Flanigan A, Coppola D, Buelow R (2002) RDP58, a locally active TNF inhibitor, is effective in the dextran sulphate mouse model of chronic colitis. Inflamm Res 51: 522-531
53. Myers KJ, Murthy S, Flanigan A, Witchell DR, Butler M, Murray S, Siwkowski A, Goodfellow D, Madsen K, Baker B (2003) Antisense oligonucleotide blockade of tumor necrosis factor-alpha in two murine models of colitis. J Pharmacol Exp Ther 304: 411-424
54. Niessen CM (2007) Tight junctions/adherens junctions: basic structure and function. J Invest Dermatol 127: 2525-2532
55. Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW, Innis-Whitehouse W, Eastburn KK, Madara JL (2000) Tight junctions are membrane microdomains. J Cell Sci 113: 1771-1781
56. Ocampo SM, Romero C, Avino A, Burgueno J, Gassull MA, Bermudez J, Eritja R, Fernandez E, Perales JC (2012) Functionally enhanced siRNA targeting TNFalpha attenuates DSS-induced colitis and TLR-mediated immunostimulation in mice. Mol Ther 20: 382-390
57. Overall CM, Blobel CP (2007) In search of partners: linking extracellular proteases to substrates. Nat Rev Mol Cell Biol 8: 245-257
58. Overall CM, Lopez-Otin C (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2: 657-672
59. Rath T, Roderfeld M, Graf J, Wagner S, Vehr AK, Dietrich C, Geier A, Roeb E (2006) Enhanced expression of MMP-7 and MMP-13 in inflammatory bowel disease: a precancerous potential? Inflamm Bowel Dis 12: 1025-1035
60. Rath T, Roderfeld M, Halwe JM, Tschuschner A, Roeb E, Graf J (2010) Cellular sources of MMP-7, MMP-13 and MMP-28 in ulcerative colitis. Scand J Gastroenterol 45: 1186-1196
61. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA (2009) Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc 4: 31-36
62. Schmitz H, Fromm M, Bentzel CJ, Scholz P, Detjen K, Mankertz J, Bode H, Epple HJ, Riecken EO, Schulzke JD (1999) Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci 112: 137-146
63. Shukla A, Barrett TF, Nakayama KI, Nakayama K, Mossman BT, Lounsbury KM (2006) Transcriptional up-regulation of MMP12 and MMP13 by asbestos occurs via a PKCdelta-dependent pathway in murine lung. FASEB J 20: 997-999
64. Smirnova MG, Kiselev SL, Birchall JP, Pearson JP (2001) Up-regulation of mucin secretion in HT29-MTX cells by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-6. Eur Cytokine Netw 12: 119-125
65. Staes A, Impens F, Van Damme P, Ruttens B, Goethals M, Demol H, Timmerman E, Vandekerckhove J, Gevaert K (2011) Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat Protoc 6: 1130-1141
66. Swank GM, Deitch EA (1996) Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg 20: 411-417
67. Takaishi H, Kimura T, Dalal S, Okada Y, D'Armiento J (2008) Joint diseases and matrix metalloproteinases: a role for MMP-13. Curr Pharm Biotechnol 9: 47-54
68. Tam EM, Morrison CJ, Wu YI, Stack MS, Overall CM (2004) Membrane protease proteomics: isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates. Proc Natl Acad Sci USA 101: 6917-6922
69. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809
70. Umeda K, Ikenouchi J, Katahira-Tayama S, Furuse K, Sasaki H, Nakayama M, Matsui T, Tsukita S, Furuse M (2006) ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126: 741-754
71. Van der Sluis M, De Koning BAE, De Bruijn ACJM, Velcich A, Meijerink JPP, Van Goudoever JB, Buller HA, Dekker J, Van Seuningen I, Renes IB, et al (2006) Muc2-deficient mice spontaneously develop colitis, indicating that Muc2 is critical for colonic protection. Gastroenterology 131: 117-129
72. Van Hauwermeiren F, Vandenbroucke RE, Libert C (2011) Treatment of TNF mediated diseases by selective inhibition of soluble TNF or TNFR1. Cytokine Growth Factor Rev 22: 311-319
73. Vandenbroucke RE, Dejager L, Libert C (2011a) The first MMP in sepsis. EMBO Mol Med 3: 367-369
74. Vandenbroucke RE, Dejonckheere E, Libert C (2011b) A therapeutic role for matrix metalloproteinase inhibitors in lung diseases? Eur Respir J 38: 1200-1214
75. Vandenbroucke RE, Dejonckheere E, Van Lint P, Demeestere D, Van Wonterghem E, Vanlaere I, Puimege L, Van Hauwermeiren F, De Rycke R, Mc Guire C, et al (2012) Matrix metalloprotease 8-dependent extracellular matrix cleavage at the blood-CSF barrier contributes to lethality during systemic inflammatory diseases. J Neurosci 32: 9805-9816
76. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034
77. Vanlaere I, Libert C (2009) Matrix metalloproteinases as drug targets in infections caused by gram-negative bacteria and in septic shock. Clin Microbiol Rev 22: 224-239 Table of Contents
78. Vizoso FJ, Gonzalez LO, Corte MD, Corte MG, Bongera M, Martinez A, Martin A, Andicoechea A, Gava RR (2006) Collagenase-3 (MMP-13) expression by inflamed mucosa in inflammatory bowel disease. Scand J Gastroenterol 41: 1050-1055
79. Williams KL, Fuller CR, Dieleman LA, DaCosta CM, Haldeman KM, Sartor RB, Lund PK (2001) Enhanced survival and mucosal repair after dextran sodium sulfate-induced colitis in transgenic mice that overexpress growth hormone. Gastroenterology 120: 925-937
80. Wlodarska M, Finlay BB (2010) Host immune response to antibiotic perturbation of the microbiota. Mucosal Immunol 3: 100-103
81. Wu MH, Lo JF, Kuo CH, Lin JA, Lin YM, Chen LM, Tsai FJ, Tsai CH, Huang CY, Tang CH (2012) Endothelin-1 promotes MMP-13 production and migration in human chondrosarcoma cells through FAK/PI3K/Akt/mTOR pathways. J Cell Physiol 227: 3016-3026
82. Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV, Merlin D (2009) Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS ONE 4: e6073
83. Zitka O, Kukacka J, Krizkova S, Huska D, Adam V, Masarik M, Prusa R, Kizek R (2010) Matrix metalloproteinases. Curr Med Chem 17: 3751-3768