Extracellular cathepsin K exerts antimicrobial activity and is protective against chronic intestinal inflammation in mice

Gut

Volumn 62, Issue 4, 2013, Pages 520-530

  Sina, Christian ^a   Lipinski, Simone ^a   Gavrilova, Olga ^a   Aden, Konrad ^a   Rehman, Ateequr ^a   Till, Andreas ^a   Rittger, Andrea ^b   Podschun, Rainer ^a   Meyer Hoffert, Ulf ^a   Haesler, Robert ^a   Midtling, Emilie ^a   Pütsep, Katrin ^c   McGuckin, Michael A ^d   Schreiber, Stefan ^a   Saftig, Paul ^b   Rosenstiel, Philip ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN K; DEXTRAN SULFATE; DNA 16S; INTERLEUKIN 8; MUCIN; PLACEBO; RECOMBINANT CATHEPSIN K; RECOMBINANT ENZYME; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACILLUS; BACILLUS MEGATERIUM; BACILLUS UNIFORMIS; BACTERICIDAL ACTIVITY; BACTEROIDES; BACTEROIDES DISTASONIS; BACTEROIDES FRAGILIS; BACTEROIDES OVATUS; BACTEROIDES THETAIOTAOMICRON; COLITIS; COLON MUCOSA; COLONOSCOPY; CONTROLLED STUDY; DISEASE SEVERITY; DNA FINGERPRINTING; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FECES ANALYSIS; FEMALE; GOBLET CELL; HISTOPATHOLOGY; ILEUM MUCOSA; INTESTINE FLORA; LACTOBACILLUS SALIVARIUS; MALE; MEDICAL ASSESSMENT; MOUSE; NONHUMAN; PREVOTELLA; PREVOTELLA DISIENS; PREVOTELLA INTERMEDIA; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS MITIS; TREATMENT OUTCOME;

ANIMALS; BLOTTING, WESTERN; CATHEPSIN K; COLITIS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; ENDOSCOPY, GASTROINTESTINAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84874661796     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2011-300076     Document Type: Article

References (48)

1. Dicksved J, Halfvarson J, Rosenquist M, et al. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J 2008;2:716-27. (Pubitemid 351951567)
2. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006;124:837-48. (Pubitemid 43261456)
3. Rosenstiel P, Fantini M, Brautigam K, et al. TNF-alpha and IFN-gamma regulate the expression of the NOD2 (CARD15) gene in human intestinal epithelial cells. Gastroenterology 2003;124:1001-9. (Pubitemid 36389803)
4. Rosenstiel P, Sina C, Franke A, et al. Towards a molecular risk maperecent advances on the etiology of inflammatory bowel disease. Semin Immunol 2009;21:334-45.
5. Rosenstiel P, Sina C, End C, et al. Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J Immunol 2007;178:8203-11. (Pubitemid 46898093)
6. Lipinski S, Till A, Sina C, et al. DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J Cell Sci. 2009;122:3522-30.
7. Schreiber S, Rosenstiel P, Albrecht M, et al. Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat Rev Genet 2005;6:376-88. (Pubitemid 40577181)
8. Chapman HA, Riese RJ, Shi GP. Emerging roles for cysteine proteases in human biology. Annu Rev Physiol 1997;59:63-88. (Pubitemid 27142435)
9. Colbert JD, Matthews SP, Miller G, et al. Diverse regulatory roles for lysosomal proteases in the immune response. Eur J Immunol 2009;39:2955-65.
10. Friedrichs B, Tepel C, Reinheckel T, et al. Thyroid functions of mouse cathepsins B, K, and L. J Clin Invest 2003;111:1733-45. (Pubitemid 38057754)
11. Buhling F, Waldburg N, Reisenauer A, et al. Lysosomal cysteine proteases in the lung: role in protein processing and immunoregulation. Eur Respir J 2004;23:620-8. (Pubitemid 38456008)
12. Beers C, Burich A, Kleijmeer MJ, et al. Cathepsin S controls MHC class II-mediated antigen presentation by epithelial cells in vivo. J Immunol 2005;174:1205-12.
13. Herszenyi L, Plebani M, Carraro P, et al. Impaired fibrinolysis and increased protease levels in gastric and duodenal mucosa of patients with active duodenal ulcer. Am J Gastroenterol 1997;92:843-7. (Pubitemid 27200803)
14. Sheahan K, Shuja S, Murnane MJ. Cysteine protease activities and tumor development in human colorectal carcinoma. Cancer Res 1989;49:3809-14. (Pubitemid 19197402)
15. Menzel K, Hausmann M, Obermeier F, et al. Cathepsins B, L and D in inflammatory bowel disease macrophages and potential therapeutic effects of cathepsin inhibition in vivo. Clin Exp Immunol 2006;146:169-80. (Pubitemid 44393851)
16. Vreemann A, Qu H, Mayer K, et al. Cathepsin B release from rodent intestine mucosa due to mechanical injury results in extracellular matrix damage in early posttraumatic phases. Biol Chem 2009;390:481-92.
17. Klemencic I, Carmona AK, Cezari MH, et al. Biochemical characterization of human cathepsin X revealed that the enzyme is an exopeptidase, acting as carboxymonopeptidase or carboxydipeptidase. Eur J Biochem 2000;267:5404-12.
18. Gelb BD, Shi GP, Chapman HA, et al. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 1996;273:1236-8.
19. Inaoka T, Bilbe G, Ishibashi O, et al. Molecular cloning of human cDNA for cathepsin K: novel cysteine proteinase predominantly expressed in bone. Biochem Biophys Res Commun 1995;206:89-96.
20. Buhling F, Gerber A, Hackel C, et al. Expression of cathepsin K in lung epithelial cells. Am J Respir Cell Mol Biol 1999;20:612-19. (Pubitemid 129495649)
21. Tepel C, Bromme D, Herzog V, et al. Cathepsin K in thyroid epithelial cells: sequence, localization and possible function in extracellular proteolysis of thyroglobulin. J Cell Sci 2000;24:4487-98. (Pubitemid 32117909)
22. Krueger S, Kuester D, Bernhardt A, et al. Regulation of cathepsin X overexpression in H. pylori-infected gastric epithelial cells and macrophages. J Pathol 2009;217:581-8.
23. Saftig P, Hunziker E, Wehmeyer O, et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A 1998;95:13453-8. (Pubitemid 28522993)
24. Asagiri M, Hirai T, Kunigami T, et al. Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 2008;319:624-7. (Pubitemid 351197065)
25. Siegmund B, Lehr HA, Fantuzzi G, et al. IL-1 beta-converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci U S A 2001;98:13249-54. (Pubitemid 33051348)
26. Becker C, Fantini MC, Wirtz S, et al. In vivo imaging of colitis and colon cancer development in mice using high resolution chromoendoscopy. Gut 2005;54:950-4. (Pubitemid 40873907)
27. Melton-Celsa AR, Darnell SC, O'Brien AD. Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91:H21 isolates in orally infected, streptomycin-treated mice. Infect Immun 1996;64:1569-76. (Pubitemid 26129817)
28. Fedders H, Podschun R, Leippe M. The antimicrobial peptide Ci-MAM-A24 is highly active against multidrug-resistant and anaerobic bacteria pathogenic for humans. Int J Antimicrob Agents 2010;36:264-6.
29. Ott SJ, Musfeldt M, Wenderoth DF, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004;53:685-93. (Pubitemid 38561447)
30. Guo X, Xia X, Tang R, et al. Real-time PCR quantification of the predominant bacterial divisions in the distal gut of Meishan and Landrace pigs. Anaerobe 2008;14:224-8.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 2001;25:402-8. (Pubitemid 34164012)
32. Rehman A, Sina C, Gavrilova O, et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011;60:1354-62.
33. Kos J, Sekirnik A, Premzl A, et al. Carboxypeptidases cathepsins X and B display distinct protein profile in human cells and tissues. Exp Cell Res 2005;306:103-13. (Pubitemid 40692776)
34. Foligne B, Zoumpopoulou G, Dewulf J, et al. A key role of dendritic cells in probiotic functionality. PLoS One 2007;2:e313.
35. Thorne KJ, Oliver RC, Barrett AJ. Lysis and killing of bacteria by lysosomal proteinases. Infect Immun 1976;14:555-63.
36. Johansson ME, Phillipson M, Petersson J, et al. The inner of the two Muc2 mucindependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 2008;105:15064-9.
37. Swidsinski A, Sydora BC, Doerffel Y, et al. Viscosity gradient within the mucus layer determines the mucosal barrier function and the spatial organization of the intestinal microbiota. Inflamm Bowel Dis 2007;13:963-70. (Pubitemid 47309967)
38. Meyer-Hoffert U, Hornef MW, Henriques-Normark B, et al. Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 2008;57:764-71. (Pubitemid 351716969)
39. Weinrauch Y, Drujan D, Shapiro SD, et al. Neutrophil elastase targets virulence factors of enterobacteria. Nature 2002;417:91-4. (Pubitemid 34498822)
40. Salzman NH, Hung K, Haribhai D, et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010;11:76-83.
41. Salzman NH, Ghosh D, Huttner KM, et al. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 2003;422:522-6. (Pubitemid 36433647)
42. Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 2002;160:2253-7. (Pubitemid 34663415)
43. Brix K, Dunkhorst A, Mayer K, et al. Cysteine cathepsins: cellular roadmap to different functions. Biochimie 2008;90:194-207. (Pubitemid 351172569)
44. Jordans S, Jenko-Kokalj S, Kuhl NM, et al. Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions. BMC Biochem 2009;10:23.
45. Sokol H, Lay C, Seksik P, et al. Analysis of bacterial bowel communities of IBD patients: what has it revealed? Inflamm Bowel Dis 2008;14:858-67. (Pubitemid 351898071)
46. Tai EK, Wu WK, Wong HP, et al. A new role for cathelicidin in ulcerative colitis in mice. Exp Biol Med (Maywood) 2007;232:799-808. (Pubitemid 46827822)
47. Hausmann M, Obermeier F, Schreiter K, et al. Cathepsin D is up-regulated in inflammatory bowel disease macrophages. Clin Exp Immunol 2004;136:157-67. (Pubitemid 38437778)
48. Park B, Brinkmann MM, Spooner E, et al. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat Immunol 2008;9:1407-14.