Enterocyte shedding and epithelial lining repair following ischemia of the human small intestine attenuate inflammation

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Matthijsen, Robert A ^a,b   Derikx, Joep P M ^a   Kuipers, Dian ^a   van Dam, Ronald M ^a   Dejong, Cornelis H C ^a   Buurman, Wim A ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b Infection and Immunology   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; EPITHELIAL CELL ADHESION MOLECULE; FATTY ACID BINDING PROTEIN 2; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MESSENGER RNA; MYELOPEROXIDASE; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CELL DAMAGE; CELL REGENERATION; CELLULAR STRESS RESPONSE; CLINICAL ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME RELEASE; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; INTESTINE EPITHELIUM CELL; ISCHEMIA; JEJUNUM MUCOSA; MALE; NEUTROPHIL CHEMOTAXIS; PROTEIN EXPRESSION; REPERFUSION; AGED; APOPTOSIS; EPITHELIUM; INFLAMMATION; INTESTINE CELL; METABOLISM; MIDDLE AGED; NECROSIS; PATHOLOGY; REPERFUSION INJURY; SMALL INTESTINE; WOUND HEALING;

AGED; APOPTOSIS; ENTEROCYTES; EPITHELIUM; FEMALE; HUMANS; INFLAMMATION; INTESTINE, SMALL; ISCHEMIA; LIPOPOLYSACCHARIDES; MALE; MIDDLE AGED; NECROSIS; REPERFUSION INJURY; WOUND HEALING;

EID: 70349275747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007045     Document Type: Article

References (42)

1. Derikx JPM, Matthijsen RA, de Bruïne AP, van Bijnen AA, Heineman E, et al. (2008) Rapid Reversal of Human Intestinal Ischemia-Reperfusion Induced Damage by Shedding of Injured Enterocytes and Reepithelialisation. PLoS ONE 3: e3428.
2. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357: 1121-1135.
3. de Groot H, Rauen U (2007) Ischemia-reperfusion injury: processes in pathogenetic networks: a review. Transplant Proc 39: 481-484.
4. Daemen MA, van't Veer C, Denecker G, Heemskerk VH, Wolfs TG, et al. (1999) Inhibition of apoptosis induced by ischemia-reperfusion prevents inflammation. J Clin Invest 104: 541-549.
5. Donath S, Li P, Willenbockel C, Al-Saadi N, Gross V, et al. (2006) Apoptosis repressor with caspase recruitment domain is required for cardioprotection in response to biomechanical and ischemic stress. Circulation 113: 1203-1212.
6. Yaoita H, Ogawa K, Maehara K, Maruyama Y (1998) Attenuation of ischemia/ reperfusion injury in rats by a caspase inhibitor. Circulation 97: 276-281.
7. Restifo NP (2000) Building better vaccines: how apoptotic cell death can induce inflammation and activate innate and adaptive immunity. Curr Opin Immunol 12: 597-603.
8. Hart ML, Ceonzo KA, Shaffer LA, Takahashi K, Rother RP, et al. (2005) Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J Immunol 174: 6373-6380.
9. Zhou W, Farrar CA, Abe K, Pratt JR, Marsh JE, et al. (2000) Predominant role for C5b-9 in renal ischemia/reperfusion injury. J Clin Invest 105: 1363-1371.
10. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, et al. (1983) Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67: 1016-1023.
11. Libby P, Maroko PR, Bloor CM, Sobel BE, Braunwald E (1973) Reduction of experimental myocardial infarct size by corticosteroid administration. J Clin Invest 52: 599-607.
12. Wada K, Montalto MC, Stahl GL (2001) Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 120: 126-133.
13. Litt MR, Jeremy RW, Weisman HF, Winkelstein JA, Becker LC (1989) Neutrophil depletion limited to reperfusion reduces myocardial infarct size after 90 minutes of ischemia. Evidence for neutrophil-mediated reperfusion injury. Circulation 80: 1816-1827.
14. Daemen MA, van de Ven MW, Heineman E, Buurman WA (1999) Involvement of endogenous interleukin-10 and tumor necrosis factor-alpha in renal ischemia-reperfusion injury. Transplantation 67: 792-800.
15. Frangogiannis NG, Smith CW, Entman ML (2002) The inflammatory response in myocardial infarction. Cardiovasc Res 53: 31-47.
16. Takada M, Nadeau KC, Shaw GD, Marquette KA, Tilney NL (1997) The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J Clin Invest 99: 2682-2690.
17. Lucchesi BR (1990) Modulation of leukocyte-mediated myocardial reperfusion injury. Annu Rev Physiol 52: 561-576.
18. de Vries B, Kohl J, Leclercq WK, Wolfs TG, van Bijnen AA, et al. (2003) Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils. J Immunol 170: 3883-3889.
19. Guo RF, Ward PA (2005) Role of C5a in inflammatory responses. Annu Rev Immunol 23: 821-852.
20. De Vries B, Matthijsen RA, Wolfs TG, Van Bijnen AA, Heeringa P, et al. (2003) Inhibition of complement factor C5 protects against renal ischemia-reperfusion injury: inhibition of late apoptosis and inflammation. Transplantation 75: 375-382.
21. Murohara T, Delyani JA, Albelda SM, Lefer AM (1996) Blockade of platelet endothelial cell adhesion molecule-1 protects against myocardial ischemia and reperfusion injury in cats. J Immunol 156: 3550-3557.
22. Schoenberg MH, Poch B, Younes M, Schwarz A, Baczako K, et al. (1991) Involvement of neutrophils in postischaemic damage to the small intestine. Gut 32: 905-912.
23. Ma XL, Tsao PS, Lefer AM (1991) Antibody to CD-18 exerts endothelial and cardiac protective effects in myocardial ischemia and reperfusion. J Clin Invest 88: 1237-1243.
24. Matthijsen RA, Derikx JP, Steffensen R, van Dam RM, Dejong CH, et al. (2009) Mannose-binding lectin null alleles are associated with preserved epithelial cell integrity following intestinal ischemia reperfusion in man. Mol Immunol.
25. Kanda T, Fujii H, Tani T, Murakami H, Suda T, et al. (1996) Intestinal fatty acid-binding protein is a useful diagnostic marker for mesenteric infarction in humans. Gastroenterology 110: 339-343.
26. Engelberts I, Stephens S, Francot GJ, van der Linden CJ, Buurman WA (1991) Evidence for different effects of soluble TNF-receptors on various TNF measurements in human biological fluids. Lancet 338: 515-516.
27. Vedder NB, Winn RK, Rice CL, Chi EY, Arfors KE, et al. (1990) Inhibition of leukocyte adherence by anti-CD18 monoclonal antibody attenuates reperfusion injury in the rabbit ear. Proc Natl Acad Sci U S A 87: 2643-2646.
28. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81: 1-5.
29. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, et al. (2007) The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220: 60-81.
30. Huynh ML, Fadok VA, Henson PM (2002) Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 109: 41-50.
31. Grotz MR, Deitch EA, Ding J, Xu D, Huang Q, et al. (1999) Intestinal cytokine response after gut ischemia: role of gut barrier failure. Ann Surg 229: 478-486.
32. Salvemini D, Wang ZQ, Zweier JL, Samouilov A, Macarthur H, et al. (1999) A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 286: 304-306.
33. Cuzzocrea S, De Sarro G, Costantino G, Ciliberto G, Mazzon E, et al. (1999) IL-6 knock-out mice exhibit resistance to splanchnic artery occlusion shock. J Leukoc Biol 66: 471-480.
34. Tsuruma T, Yagihashi A, Tarumi K, Hirata K (1998) Anti-rat IL-8 (CINC) monoclonal antibody administration reduces ischemia-reperfusion injury in small intestine. Transplant Proc 30: 2644-2645.
35. Matthijsen RA, Huugen D, Hoebers NT, de Vries B, Peutz-Kootstra CJ, et al. (2007) Myeloperoxidase is critically involved in the induction of organ damage after renal ischemia reperfusion. Am J Pathol 171: 1743-1752.
36. Arumugam TV, Shiels IA, Woodruff TM, Granger DN, Taylor SM (2004) The role of the complement system in ischemia-reperfusion injury. Shock 21: 401-409.
37. Laufer J, Oren R, Goldberg I, Horwitz A, Kopolovic J, et al. (2000) Cellular localization of complement C3 and C4 transcripts in intestinal specimens from patients with Crohn's disease. Clin Exp Immunol 120: 30-37.
38. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, et al. (2008) Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 9: 1179-1188.
39. Taylor CT, Colgan SP (2007) Hypoxia and gastrointestinal disease. J Mol Med 85: 1295-1300.
40. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, et al. (2000) Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 48: 285-296.
41. Cai Z, Manalo DJ, Wei G, Rodriguez ER, Fox-Talbot K, et al. (2003) Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 108: 79-85.
42. Patel A, van de Poll MC, Greve JW, Buurman WA, Fearon KC, et al. (2004) Early stress protein gene expression in a human model of ischemic preconditioning. Transplantation 78: 1479-1487.