Estrogen prevents intestinal inflammation after trauma-hemorrhage via downregulation of angiotensin II and angiotensin II subtype I receptor

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 5, 2008, Pages

  Chen, Jianguo ^a   Yang, Shaolong ^a   Hu, Shunhua ^a   Choudhry, Mashkoor A ^a   Bland, Kirby I ^a   Chaudry, Irshad H ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

Chemokines; Cytokines; Estrogen receptor antagonist; Myeloperoxidase; Shock

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN RECEPTOR; APELIN RECEPTOR; CHEMOKINE; ESTRADIOL; ESTROGEN; FULVESTRANT; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; LOSARTAN; MYELOPEROXIDASE; PROTEIN CINC1; PROTEIN CINC3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENTERITIS; ENZYME ACTIVITY; ENZYME REGULATION; INTESTINAL BLEEDING; INTESTINE BLOOD FLOW; INTESTINE INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANGIOTENSIN II; ANIMALS; CYTOKINES; DOWN-REGULATION; ESTRADIOL; HEMORRHAGE; INFLAMMATION; MALE; PEROXIDASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1;

EID: 57349192786     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90443.2008     Document Type: Article

References (48)

1. Anthuber M, Farkas S, Rihl M, Menger MD, Schildberg FW, Jauch KW, Messmer K. Angiotensin-converting enzyme inhibition by enalapril: a novel approach to reduce ischemia/reperfusion damage after experimental liver transplantation. Hepatology 25: 648-651, 1997.
2. Ba ZF, Shimizu T, Szalay L, Bland KI, Chaudry IH. Gender differences in small intestinal perfusion following trauma hemorrhage: the role of endothelin-1. Am J Physiol Gastrointest Liver Physiol 288: G860-G865, 2005.
3. Cheng ZJ, Vapaatalo H, Mervaala E. Angiotensin II and vascular inflammation. Med Sci Monit 11: RA194-RA205, 2005.
4. Collard CD, Gelman S. Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 94: 1133-1138, 2001.
5. Engelhorn T, Goerike S, Doerfler A, Okorn C, Forsting M, Heusch G, Schulz R. The angiotensin II type 1-receptor blocker candesartan increases cerebral blood flow, reduces infarct size, and improves neurologic outcome after transient cerebral ischemia in rats. J Cereb Blood Flow Metab 24: 467-474, 2004.
6. Erickson RH, Yoon BC, Koh DY, Kim DH, Kim YS. Dietary induction of angiotensin-converting enzyme in proximal and distal rat small intestine. Am J Physiol Gastrointest Liver Physiol 281: G1221-G1227, 2001.
7. Fink MP. Gastrointestinal mucosal injury in experimental models of shock, trauma, and sepsis. Crit Care Med 19: 627-641, 1991.
8. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115: 182-205, 1998.
9. Griendling KK, Murphy TJ, Alexander RW. Molecular biology of the renin-angiotensin system. Circulation 87: 1816-1828, 1993.
10. Harrison DG, Cai H, Landmesser U, Griendling KK. Interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease. J Renin Angiotensin Aldosterone Syst 4: 51-61, 2003.
11. Hartmann M, Montgomery A, Jonsson K, Haglund U. Tissue oxygenation in hemorrhagic shock measured as transcutaneous oxygen tension, subcutaneous oxygen tension, and gastrointestinal intramucosal pH in pigs. Crit Care Med 19: 205-210, 1991.
12. Homma H, Hoy E, Xu DZ, Lu Q, Feinman R, Deitch EA. The female intestine is more resistant than the male intestine to gut injury and inflammation when subjected to conditions associated with shock states. Am J Physiol Gastrointest Liver Physiol 288: G466-G472, 2005.
13. Hong HJ, Liu JC, Chan P, Juan SH, Loh SH, Lin JG, Cheng TH. 17beta-estradiol downregulates angiotensin-II-induced endothelin-1 gene expression in rat aortic smooth muscle cells. J Biomed Sci 11: 27-36, 2004.
14. Konstam MA. Administration of captopril following MI reduced the incidence of ischemia-related events. Evid Based Cardiovasc Med 2: 21, 1998.
15. Kuebler JF, Toth B, Yokoyama Y, Bland KI, Rue LW 3rd, Chaudry IH. Alpha1-acid-glycoprotein protects against trauma-hemorrhagic shock. J Surg Res 119: 21-28, 2004.
16. Malech HL, Gallin JI. Current concepts: immunology. Neutrophils in human diseases. N Engl J Med 317: 687-694, 1987.
17. Masuko H, Jin MB, Horiuchi H, Suzuki T, Taniguchi M, Shimamura T, Fukai M, Magata S, Ogata K, Ishikawa H, Fujita M, Nagashima K, Furukawa H, Todo S. Protective effect of angiotensin II type I receptor antagonist, CV-11974, on ischemia and reperfusion injury of the liver. Transplantation 71: 1034-1039, 2001.
18. Meldrum KK, Meldrum DR, Meng X, Ao L, Harken AH. TNFalpha-dependent bilateral renal injury is induced by unilateral renal ischemia-reperfusion. Am J Physiol Heart Circ Physiol 282: H540-H546, 2002.
19. Moore FA. The role of the gastrointestinal tract in postinjury multiple organ failure. Am J Surg 178: 449-453, 1999.
20. Nakagawa H, Komorita N, Shibata F, Ikesue A, Konishi K, Fujioka M, Kato H. Identification of cytokine-induced neutrophil chemoattractants (CINC), rat GRO/CINC-2 alpha and CINC-2 beta, produced by granulation tissue in culture: purification, complete amino acid sequences and characterization. Biochem J 301: 545-550, 1994.
21. Nickenig G, Strehlow K, Wassmann S, Baumer AT, Albory K, Sauer H, Bohm M. Differential effects of estrogen and progesterone on AT(1) receptor gene expression in vascular smooth muscle cells. Circulation 102: 1828-1833, 2000.
22. Olanders K, Sun Z, Borjesson A, Dib M, Andersson E, Lasson A, Ohlsson T, Andersson R. The effect of intestinal ischemia and reperfusion injury on ICAM-1 expression, endothelial barrier function, neutrophil tissue influx, and protease inhibitor levels in rats. Shock 18: 86-92, 2002.
23. Padmanabhan N, Padmanabhan S, Connell JM. Genetic basis of cardiovascular disease - the renin-angiotensin-aldosterone system as a paradigm. J Renin Angiotensin Aldosterone Syst 1: 316-324, 2000.
24. Peitzman AB, Billiar TR, Harbrecht BG, Kelly E, Udekwu AO, Simmons RL. Hemorrhagic shock. Curr Probl Surg 32: 925-1002, 1995.
25. Piqueras L, Kubes P, Alvarez A, O'Connor E, Issekutz AC, Esplugues JV, Sanz MJ. Angiotensin II induces leukocyte-endothelial cell interactions in vivo via AT(1) and AT(2) receptor-mediated P-selectin upregulation. Circulation 102: 2118-2123, 2000.
26. Pueyo ME, Gonzalez W, Nicoletti A, Savoie F, Arnal JF, Michel JB. Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. Arterioscler Thromb Vasc Biol 20: 645-651, 2000.
27. Przyklenk K, Kloner RA. "Cardioprotection" by ACE-inhibitors in acute myocardial ischemia and infarction? (Review). Basic Res Cardiol 88, Suppl 1: 139-154, 1993.
28. Reilly PM, Bulkley GB. Vasoactive mediators and splanchnic perfusion. Crit Care Med 21: S55-S68, 1993.
29. Riaz AA, Wang Y, Schramm R, Sato T, Menger MD, Jeppsson B, Thorlacius H. Role of angiotensin II in ischemia/reperfusion-induced leukocyte-endothelium interactions in the colon. FASEB J 18: 881-883, 2004.
30. Richard DE, Berra E, Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem 275: 26765-26771, 2000.
31. Rodriguez P, Heyman M, Candalh C, Blaton MA, Bouchaud C. Tumour necrosis factor-alpha induces morphological and functional alterations of intestinal HT29 cl.19A cell monolayers. Cytokine 7: 441-448, 1995.
32. Ruiz-Ortega M, Lorenzo O, Ruperez M, Blanco J, Egido J. Systemic infusion of angiotensin II into normal rats activates nuclear factor-kappaB and AP-1 in the kidney: role of AT(1) and AT(2) receptors. Am J Pathol 158: 1743-1756, 2001.
33. Russell DH, Barreto JC, Klemm K, Miller TA. Hemorrhagic shock increases gut macromolecular permeability in the rat. Shock 4: 50-55, 1995.
34. Samy TS, Schwacha MG, Cioffi WG, Bland KI, Chaudry IH. Androgen and estrogen receptors in splenic T lymphocytes: effects of flutamide and trauma-hemorrhage. Shock 14: 465-470, 2000.
35. Schinke M, Doods HN, Ganten D, Wienen W, Entzeroth M. Characterization of rat intestinal angiotensin II receptors. Eur J Pharmacol 204: 165-170, 1991.
36. Schulz R, Heusch G. Angiotensin II type 1 receptors in cerebral ischaemia-reperfusion: initiation of inflammation. J Hypertens Suppl 24: S123-S129, 2006.
37. Schunkert H, Danser AH, Hense HW, Derkx FH, Kurzinger S, Riegger GA. Effects of estrogen replacement therapy on the renin-angiotensin system in postmenopausal women. Circulation 95: 39-45, 1997.
38. Shibata F, Konishi K, Kato H, Komorita N, al Mokdad M, Fujioka M, Nakagawa H. Recombinant production and biological properties of rat cytokine-induced neutrophil chemoattractants, GRO/CINC-2 alpha, CINC-2 beta and CINC-3. Eur J Biochem 231: 306-311, 1995.
39. Singh G, Chaudry KI, Morrison MH, Chaudry IH. Tumor necrosis factor depresses gut absorptive function. Circ Shock 39: 279-284, 1993.
40. Souza DG, Bertini R, Vieira AT, Cunha FQ, Poole S, Allegretti M, Colotta F, Teixeira MM. Repertaxin, a novel inhibitor of rat CXCR2 function, inhibits inflammatory responses that follow intestinal ischaemia and reperfusion injury. Br J Pharmacol 143: 132-142, 2004.
41. Takagi T, Yoshida N, Isozaki Y, Shimozawa M, Katada K, Manabe H, Hanada O, Kokura S, Ichikawa H, Naito Y, Okanoue T, Yoshikawa T. CV-11974, angiotensin II type I receptor antagonist, protects against ischemia-reperfusion injury of the small intestine in rats. Eur J Pharmacol 535: 283-290, 2006.
42. Vaday GG, Franitza S, Schor H, Hecht I, Brill A, Cahalon L, Hershkoviz R, Lider O. Combinatorial signals by inflammatory cytokines and chemokines mediate leukocyte interactions with extracellular matrix. J Leukoc Biol 69: 885-892, 2001.
43. Xu Y, Kumar D, Dyck JR, Ford WR, Clanachan AS, Lopaschuk GD, Jugdutt BI. AT(1) and AT(2) receptor expression and blockade after acute ischemia-reperfusion in isolated working rat hearts. Am J Physiol Heart Circ Physiol 282: H1206-H1215, 2002.
44. Yang S, Zheng R, Hu S, Ma Y, Choudhry MA, Messina JL, Rue LW 3rd, Bland KI, Chaudry IH. Mechanism of cardiac depression after trauma-hemorrhage: increased cardiomyocyte IL-6 and effect of sex steroids on IL-6 regulation and cardiac function. Am J Physiol Heart Circ Physiol 287: H2183-H2191, 2004.
45. Yilmaz EN, Vahl AC, van Rij GL, Vink GQ, Brom HL, Rauwerda JA. The effect of inhibition of renin-angiotensin system by valsartan during hypovolemic shock and low flow sigmoideal ischaemia in pigs. Cardiovasc Surg 11: 45-51, 2003.
46. Yu HP, Hsieh YC, Suzuki T, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH. Mechanism of the nongenomic effects of estrogen on intestinal myeloperoxidase activity following trauma-hemorrhage: upregulation of the PI-3K/Akt pathway. J Leukoc Biol 82: 774-780, 2007.
47. Yu HP, Chaudry IH. The role of estrogen and receptor agonists in maintaining organ function following trauma-hemorrhage. Shock. In press.
48. Yusof M, Kamada K, Gaskin FS, Korthuis RJ. Angiotensin II mediates postischemic leukocyte-endothelial interactions: role of calcitonin generelated peptide. Am J Physiol Heart Circ Physiol 292: H3032-H3037, 2007.