Exogenous IL-6 Inhibits Acute Inflammatory Responses and Prevents Ischemia/Reperfusion Injury after Intestinal Transplantation

American Journal of Transplantation

Volumn 4, Issue 4, 2004, Pages 482-494

  Kimizuka, Kei ^a   Nakao, Atsunori ^a   Nalesnik, Michael A ^a   Demetris, Anthony J ^a   Uchiyama, Takashi ^a   Ruppert, Kris ^b   Fink, Mitchell P ^a   Stolz, Donna B ^a   Murase, Noriko ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

IL 6; Intestinal transplantation; Ischemia reperfusion injury; Polymorphonuclear neutrophiric granulocyte infiltration; Tight junction proteins

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 MUTEIN; RECOMBINANT INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNIVERSITY OF WISCONSIN SOLUTION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; COLD INJURY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG EFFICACY; EPITHELIZATION; INFLAMMATION; INTESTINE BLOOD FLOW; INTESTINE ISCHEMIA; INTESTINE TRANSPLANTATION; MALE; NEUTROPHIL; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; RAT; RAT STRAIN; REPERFUSION INJURY;

ACUTE DISEASE; ANIMALS; BLOTTING, WESTERN; CYTOKINES; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-6; INTESTINES; LUNG; MALE; MUTATION; NEUTROPHILS; ORGAN TRANSPLANTATION; ORGANIC CHEMICALS; PEROXIDASE; RATS; RATS, INBRED LEW; REPERFUSION INJURY; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 1942502273     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2004.00368.x     Document Type: Article

References (54)

1. Abu-Elmagd K, Reyes J, Bond G et al. Clinical intestinal transplantation: a decade of experience at a single center. Ann Surg 2001; 23: 404-416; 416-407 [discussion].
2. Bohlen HG. Integration of intestinal structure, function, and microvascular regulation. Microcirculation 1998; 5: 27-37.
3. Rollwagen FM, Li YY, Pacheco ND et al. Microvascular effects of oral interleukin-6 on ischemia/reperfusion in the murine small intestine. Am J Pathol 2000; 156: 1177-1182.
4. Mueller AR, Platz KP, Heckert C et al. L-arginine application improves mucosal structure after small bowel transplantation. Transplant Proc 1998; 30: 2336-2338.
5. Pritts T, Hungness E, Wang Q et al. Mucosal and enterocyte IL-6 production during sepsis and endotoxemia - role of transcription factors and regulation by the stress response. Am J Surg 2002; 183:372-383.
6. Mueller AR, Platz KP, Schirmeier A et al. L-arginine application improves graft morphology and mucosal barrier function after small bowel transplantation. Transplant Proc 2000; 32: 1275-1277.
7. Yamamoto S, Tanabe M, Wakabayashi G et al. The role of tumor necrosis factor-alpha and interleukin-1beta in ischemia-reperfusion injury of the rat small intestine. J Surg Res 2001; 99: 134-141.
8. Wang W, Smail N, Wang P et al. Increased gut permeability after hemorrhage is associated with upregulation of local and systemic IL-6. J Surg Res 1998; 79: 39-46.
9. Cicalese L, Caraceni P, Nalesnik MA et al. Oxygen free radical content and neutrophil infiltration are important determinants in mucosal injury after rat small bowel transplantation. Transplantation 1996; 62: 161-166.
10. Korthuis RJ, Grisham MB, Granger DN. Leukocyte depletion attenuates vascular injury in postischemic skeletal muscle. Am J Physiol Heart Circ Physiol 1988; 254: H823-H827.
11. Harris AG, Leiderer R, Peer F et al. Skeletal muscle microvascular and tissue injury after varying durations of ischemia. Am J Physiol Heart Circ Physiol 1996; 271: H2388-H2398.
12. Molmenti EP, Ziambaras T, Perlmutter DH. Evidence for an acute phase response in human intestinal epithelial cells. J Biol Chem 1993; 268: 14116-14124.
13. Beagley KW, Eldridge JH, Lee F et al. Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J Exp Med 1989; 169: 2133-2148.
14. Damas P, Ledoux D, Nys M et al. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 1992; 215: 356-362.
15. Farmer DG, McDiarmid SV, Kuniyoshi J et al. Intragraft expression of messenger RNA for interleukin-6 and tumor necrosis factor-alpha is a predictor of rat small intestine transplant rejection. J Surg Res 1994; 57: 138-142.
16. McDiarmid SV, Farmer DG, Kuniyoshi JS et al. The correlation of intragraft cytokine expression with rejection in rat small intestine transplantation. Transplantation 1994; 58: 690-697.
17. Ulich TR, Yin S, Guo K et al. Intratracheal injection of endotoxin and cytokines. II. Interleukin-6 and transforming growth factor beta inhibit acute inflammation. Am J Pathol 1991; 138: 1097-1101.
18. Camargo CA Jr, Madden JF, Gao W et al. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 1997; 26: 1513-1520.
19. Rollwagen FM, Li YY, Pacheco ND et al. Systemic bacteraemia following haemorrhagic shock in mice: alleviation with oral interleukin 6. Cytokine 1996; 8: 121-129.
20. Skelly SM, Tackney C, Hicklin D et al. High-level expression of a biologically active human interleukin-6 mutein. J Biotechnol 1994; 34: 79-86.
21. Muench MO, Guy Z, Moore MA. Ex vivo differentiation therapy as a method of leukemic cell purging in murine bone marrow expansion cultures. Cancer Res 1992; 52: 6576-6582.
22. Sakamoto T, Liu Z, Murase N et al. Mitosis and apoptosis in the liver of interleukin-6-deficient mice after partial hepatectomy. Hepatology 1999; 29: 403-411.
23. Yokomuro S, Tsuji H, Lunz JG 3rd et al. Growth control of human biliary epithelial cells by interleukin 6, hepatocyte growth factor, transforming growth factor beta1, and activin A: comparison of a cholangiocarcinoma cell line with primary cultures of non-neoplastic biliary epithelial cells. Hepatology 2000; 32: 26-35.
24. Terakura M, Murase N, Demetris AJ et al. Lymphoid/nonlymphoid compartmentalization of donor leukocyte chimerism in rat recipients of heart allografts, with or without adjunct bone marrow. Transplantation 1998; 66: 350-357.
25. Murase N, Demetris AJ, Kim DG et al. Rejection of multivisceral allografts in rats: a sequential analysis with comparison to isolated orthotopic small-bowel and liver grafts. Surgery 1990; 108: 880-889.
26. Mammen JM, Matthews JB. Mucosal repair in the gastrointestinal tract. Crit Care Med 2003; 31: S532-S537.
27. Lacy ER. Epithelial restitution in the gastrointestinal tract. J Clin Gastroenterol 1988; 10: S72-S77.
28. Svanes K, Ito S, Takeuchi K et al. Restitution of the surface epithelium of the in vitro frog gastric mucosa after damage with hyperosmolar sodium chloride. Morphologic and physiologic characteristics. Gastroenterology 1982; 82: 1409-1426.
29. Schmittgen TD, Zakrajsek BA, Mills AG et al. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 2000; 285: 194-204.
30. Black-Schaffer B, Gall EP, Shimizu RT et al. The pathogenesis of the intestinal lesion of deep hypothermia and a proposed relationship to that of irreversible shock, including a note on a mechanism for the normal turnover of intestinal epithelium. Surgery 1967; 61: 904-914.
31. Mueller AR, Nalesnik MA, Langrehr JM et al. Evidence that small bowel preservation causes primarily basement membrane and endothelial rather than epithelial cell injury. Transplantation 1993; 56: 1499-1504.
32. Schmeling DJ, Caty MG, Oldham KT et al. Evidence for neutrophil-related acute lung injury after intestinal ischemia-reperfusion. Surgery 1989; 106: 195-201; 201-192 [discussion].
33. Starr R, Willson TA, Viney EM et al. A family of cytokine-inducible inhibitors of signalling. Nature 1997; 387: 917-921.
34. Alexander WS. Suppressors of cytokine signalling (SOCS) in the immune system. Nat Rev Immunol 2002; 2: 410-416.
35. Barton BE, Shortall J, Jackson JV. Interleukins 6 and 11 protect mice from mortality in a staphylococcal enterotoxin-induced toxic shock model. Infect Immun 1996; 64: 714-718.
36. Meng ZH, Dyer K, Billiar TR et al. Distinct effects of systemic infusion of G-CSF vs. IL-6 on lung and liver inflammation and injury in hemorrhagic shock. Shock 2000; 14: 41-48.
37. van der Poll T, Keogh CV, Guirao X et al. Interleukin-6 gene-deficient mice show impaired defense against pneumococcal pneumonia. J Infect Dis 1997; 176: 439-444.
38. Leon LR, White AA, Kluger MJ. Role of IL-6 and TNF in thermoregulation and survival during sepsis in mice. Am J Physiol 1998; 275: R269-R277.
39. Xing Z, Gauldie J, Cox G et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest 1998; 101: 311-320.
40. Wang Q, Fang CH, Hasselgren PO. Intestinal permeability is reduced and IL-10 levels are increased in septic IL-6 knockout mice. Am J Physiol Regul Integr Comp Physiol 2001; 281: R1013-R1023.
41. Fattori E, Cappelletti M, Costa P et al. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med 1994; 180: 1243-1250.
42. Cuzzocrea S, De Sarro G, Costantino G et al. IL-6 knock-out mice exhibit resistance to splanchnic artery occlusion shock. J Leukoc Biol 1999; 66: 471-480.
43. Meng ZH, Dyer K, Billiar TR et al. Essential role for IL-6 in postresuscitation inflammation in hemorrhagic shock. Am J Physiol Cell Physiol 2001; 280: C343-C351.
44. Kopf M, Baumann H, Freer G et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994; 368: 339-342.
45. Aderka D, Maor Y, Novick D et al. Interleukin-6 inhibits the proliferation of B-chronic lymphocytic leukemia cells that is induced by tumor necrosis factor-alpha or-beta. Blood 1993; 81: 2076-2084.
46. Aderka D, Le JM, Vilcek J. IL-6 inhibits lipopolysaccharide-induced tumor necrosis factor production in cultured human monocytes, U937 cells, and in mice. J Immunol 1989; 143: 3517-3523.
47. Ohkawa F, Ikeda U, Kawasaki K et al. Inhibitory effect of interleukin-6 on vascular smooth muscle contraction. Am J Physiol 1994; 266: H898-H902.
48. Tamion F, Richard V, Lyoumi S et al. Gut ischemia and mesenteric synthesis of inflammatory cytokines after hemorrhagic or endotoxic shock. Am J Physiol 1997; 273: G314-G321.
49. Koksoy C, Kuzu MA, Ergun H et al. Intestinal ischemia and reperfusion impairs vasomotor functions of pulmonary vascular bed. Ann Surg 2000; 231: 105-111.
50. Ishii H, Ishibashi M, Takayama M et al. The role of cytokine-induced neutrophil chemoattractant-1 in neutrophil-mediated remote lung injury after intestinal ischaemia/reperfusion in rats. Respirology 2000; 5: 325-331.
51. Souza AL Jr, Poggetti RS, Fontes B et al. Gut ischemia/reperfusion activates lung macrophages for tumor necrosis factor and hydrogen peroxide production. J Trauma 2000; 49: 232-236.
52. Mazzon E, Sturniolo GC, Puzzolo D et al. Effect of stress on the paracellular barrier in the rat ileum. Gut 2002; 51: 507-513.
53. Chiu CJ, McArdle AH, Brown R et al. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 1970; 101: 478-483.
54. Park PO, Haglund U, Bulkley GB et al. The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery 1990; 107: 574-580.