Protective role of p70s6K in intestinal ischemia/reperfusion injury in mice

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Ban, Kechen ^a   Kozar, Rosemary A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOSUPPRESSIVE AGENT; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; RAPAMYCIN; S6 KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; DISEASE EXACERBATION; ENTERITIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HYPOXIA; IN VITRO STUDY; INFLAMMATION; INTESTINE EPITHELIUM CELL; INTESTINE ISCHEMIA; INTESTINE MUCOSA PERMEABILITY; MALE; MOLECULAR MECHANICS; MORTALITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REOXYGENATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STOMACH PROTECTION;

ANIMALS; APOPTOSIS; CELL LINE; EPITHELIAL CELLS; IMMUNOSUPPRESSIVE AGENTS; INTESTINAL DISEASES; INTESTINAL MUCOSA; MALE; MICE; RATS; REPERFUSION INJURY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SIROLIMUS; TIME FACTORS; TOR SERINE-THREONINE KINASES;

ANIMALIA; MUS;

EID: 84864401253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041584     Document Type: Article

References (65)

1. Antonsson JB, Fiddian-Green RG, (1991) The role of the gut in shock and multiple system organ failure. Eur J Surg. 157: 3-12.
2. Pierro A, Eaton S, (2004) Intestinal ischemia reperfusion injury and multisystem organ failure. Semin Pediatr Surg. 13: 11-17.
3. Turnage RH, Kadesky KM, Myers SI, Guice KS, Oldham KT, (1996) Hepatic hypoperfusion after intestinal reperfusion. Surgery. 119: 151-160.
4. Baue AE, (2006) MOF, MODS, and SIRS: what is in a name or an acronym? Shock. 26: 438-449.
5. Granger DN, Korthuis RJ, (1995) Physiologic mechanisms of postischemic tissue injury. Annu Rev Physiol. 57: 311-332.
6. Oldenburg WA, Lau LL, Rodenberg TJ, Edmonds HJ, Burger CD, (2004) Acute mesenteric ischemia: a clinical review. Arch Intern Med. 164: 1054-1062.
7. Vollmar B, Menger MD, (2011) Intestinal ischemia/reperfusion: microcirculatory pathology and functional consequences. Langenbecks Arch Surg. 396: 13-29.
8. 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.
9. Wullschleger S, Loewith R, Hall MN, (2006) TOR signaling in growth and metabolism. Cell. 124: 471-484.
10. Hay N, Sonenberg N, (2004) Upstream and downstream of mTOR. Genes Dev. 18: 1926-1945.
11. Martin DE, Hall MN, (2005) The expanding TOR signaling network. Curr Opin Cell Biol. 17: 158-166.
12. Sarbassov DD, Ali SM, Sabatini DM, (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol. 17: 596-603.
13. Petritsch C, Beug H, Balmain A, Oft M, (2000) TGF-beta inhibits p70 S6 kinase via protein phosphatase 2A to induce G(1) arrest. Genes Dev. 14: 3093-3101.
14. Delgoffe GM, Powell JD, (2009) mTOR: taking cues from the immune microenvironment. Immunology. 127: 459-465.
15. Mills RE, Jameson JM, (2009) T cell dependence on mTOR signaling. Cell Cycle. 8: 545-548.
16. Weichhart T, Säemann MD, (2009) The multiple facets of mTOR in immunity. Trends Immunol. 30: 218-226.
17. Säemann MD, Haidinger M, Hecking M, Hörl WH, Weichhart T, (2009) The multifunctional role of mTOR in innate immunity: implications for transplant immunity. Am J Transplant. 9: 2655-2661.
18. Ma XM, Blenis J, (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol. 10: 307-318.
19. Fukatsu K, Kudsk KA, (2011) Nutrition and gut immunity. Surg Clin North Am. 91: 755-770.
20. Zhao XF, Gartenhaus RB, (2009) Phospho-p70S6K and cdc2/cdk1 as therapeutic targets for diffuse large B-cell lymphoma. Expert Opin Ther Targets. 13: 1085-1093.
21. González-Rodriguez A, Alba J, Zimmerman V, Kozma SC, Valverde AM, (2009) S6K1 deficiency protects against apoptosis in hepatocytes. Hepatology. 50: 216-229.
22. Rhoads JM, Liu Y, Niu X, Surendran S, Wu G, (2008) Arginine stimulates cdx2-transformed intestinal epithelial cell migration via a mechanism requiring both nitric oxide and phosphorylation of p70 S6 kinase. J Nutr. 138: 1652-1657.
23. Suer S, Ampasala D, Walsh MF, Basson MD, (2009) Role of ERK/mTOR signaling in TGFbeta-modulated focal adhesion kinase mRNA stability and protein synthesis in cultured rat IEC-6 intestinal epithelial cells. Cell Tissue Res. 336: 213-223.
24. Rocourt DV, Mehta VB, Besner GE, (2007) Heparin-binding EGF-like growth factor decreases inflammatory cytokine expression after intestinal ischemia/reperfusion injury. J Surg Res. 139: 269-273.
25. Swank GM, Deitch EA, (1996) Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg. 20: 411-417.
26. Yao C, Liu J, Shao L, (2011) Rapamycin inhibits the proliferation and apoptosis of gastric cancer cells by down regulating the expression of survivin. Hepatogastroenterology. 58: 1075-1080.
27. Chen B, Yuping S, Ni J, (2012) Rapamycin decreases survivin expression to induce NSCLC cell apoptosis under hypoxia through inhibiting HIF-1α induction. MOL BIOL REP. 39: 185-191.
28. Farrelly AM, Kilbride SM, Bonner C, Prehn JH, Byrne MM, (2011) Rapamycin protects against dominant negative-HNF1A-induced apoptosis in INS-1 cells. Apoptosis. 16: 1128-1137.
29. Kato H, Nakajima S, Saito Y, Takahashi S, Katoh R, et al. (2012) mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. CELL DEATH DIFFER. 19: 310-320.
30. Velagapudi C, Bhandari BS, Abboud-Werner S, Simone S, Abboud HE, et al. (2011) The tuberin/mTOR pathway promotes apoptosis of tubular epithelial cells in diabetes. J Am Soc Nephrol. 22: 262-273.
31. González-Rodriguez A, Alba J, Zimmerman V, Kozma SC, Valverde AM, (2009) S6K1 deficiency protects against apoptosis in hepatocytes. Hepatology. 50: 216-229.
32. Esposito C, Grosjean F, Torreggiani M, Esposito V, Mangione F, et al. (2011) Sirolimus prevents short-term renal changes induced by ischemia-reperfusion injury in rats. AM J NEPHROL. 33: 239-249.
33. Yang B, Jain S, Ashra SY, Furness PN, Nicholson ML, (2006) Apoptosis and caspase-3 in long-term renal ischemia/reperfusion injury in rats and divergent effects of immunosuppressants. Transplantation. 81: 1442-1450.
34. Inman SR, Davis NA, Olson KM, Lukaszek VA, McKinley MR, et al. (2003) Rapamycin preserves renal function compared with cyclosporine A after ischemia/reperfusion injury. Urology. 62: 750-754.
35. Qian J, Ren X, Wang X, Zhang P, Jones WK, et al. (2009) Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. CIRC RES. 105: 1223-1231.
36. Khan S, Salloum F, Das A, Xi L, Vetrovec GW, et al. (2006) Rapamycin confers preconditioning-like protection against ischemia-reperfusion injury in isolated mouse heart and cardiomyocytes. J Mol Cell Cardiol. 41: 256-264.
37. Arias-Diaz J, Ildefonso JA, Muñoz JJ, Zapata A, Jiménez E, (2009) Both tacrolimus and sirolimus decrease Th1/Th2 ratio, and increase regulatory T lymphocytes in the liver after ischemia/reperfusion. LAB INVEST. 89: 433-445.
38. Feitoza CQ, Gonçalves GM, Bertocchi AP, Wang PW, Damião MJ, et al. (2007) A role for HO-1 in renal function impairment in animals subjected to ischemic and reperfusion injury and treated with immunosuppressive drugs. Transplant Proc. 39: 424-426.
39. Gonçalves GM, Cenedeze MA, Feitoza CQ, de Paula CB, Marques GD, et al. (2007) The role of immunosuppressive drugs in aggravating renal ischemia and reperfusion injury. Transplant Proc. 39: 417-420.
40. Bochelen D, Rudin M, Sauter A, (1999) Calcineurin inhibitors FK506 and SDZ ASM 981 alleviate the outcome of focal cerebral ischemic/reperfusion injury. J Pharmacol Exp Ther. 288: 653-659.
41. Dubuquoy L, Rousseaux C, Thuru X, Peyrin-Biroulet L, Romano O, et al. (2006) PPARgamma as a new therapeutic target in inflammatory bowel diseases. Gut. 55: 1341-1349.
42. Finn AV, John M, Nakazawa G, Polavarapu R, Karmali V, et al. (2009) Differential healing after sirolimus, paclitaxel, and bare metal stent placement in combination with peroxisome proliferator-activator receptor gamma agonists: requirement for mTOR/Akt2 in PPARgamma activation. Circ Res. 105: 1003-1012.
43. Mendes Sdos S, Candi A, Vansteenbrugge M, Pignon MR, Bult H, et al. (2009) Microarray analyses of the effects of NF-kappaB or PI3K pathway inhibitors on the LPS-induced gene expression profile in RAW264.7 cells: synergistic effects of rapamycin on LPS-induced MMP9-overexpression. Cell Signal. 21: 1109-1122.
44. Kim JE, Chen J, (2004) Regulation of peroxisome proliferator-activated receptor-gamma activity by mammalian target of rapamycin and amino acids in adipogenesis. Diabetes. 53: 2748-2756.
45. Ban K, Kozar RA, (2008) Enteral glutamine: a novel mediator of PPARgamma in the postischemic gut. J Leukoc Biol. 84: 595-599.
46. Sato N, Kozar RA, Zou L, Weatherall JM, Attuwaybi B, et al. (2005) Peroxisome proliferator-activated receptor gamma mediates protection against cyclooxygenase-2-induced gut dysfunction in a rodent model of mesenteric ischemia/reperfusion. Shock. 24: 462-469.
47. Sato N, Moore FA, Kone BC, Zou L, Smith MA, et al. (2006) Differential induction of PPAR-gamma by luminal glutamine and iNOS by luminal arginine in the rodent postischemic small bowel. Am J Physiol Gastrointest Liver Physiol. 290: G616-623.
48. Hassoun HT, Zou L, Moore FA, Kozar RA, Weisbrodt NW, et al. (2002) Alpha-melanocyte-stimulating hormone protects against mesenteric ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol. 282: G1059-1068.
49. Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, et al. (2008) The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity. 29: 565-577.
50. Sato N, Moore FA, Smith MA, Zou L, Moore-Olufemi S, et al. (2005) Immune-enhancing enteral nutrients differentially modulate the early proinflammatory transcription factors mediating gut ischemia/reperfusion. J Trauma. 58: 455-461.
51. Fujishiro J, Pech TC, Finger TF, Praktinjo M, Stoffels B, et al. (2010) Influence of immunosuppression on alloresponse, inflammation and contractile function of graft after intestinal transplantation. Am J Transplant. 10: 1545-1555.
52. Puglisi RN, Strande L, Santos M, Schulte G, Hewitt CW, et al. (1996) Beneficial effects of cyclosporine and rapamycin in small bowel ischemic injury. J Surg Res. 65: 115-118.
53. Tsang CK, Qi H, Liu LF, Zheng XF, (2007) Targeting mammalian target of rapamycin (mTOR) for health and diseases. Drug Discov Today. 12: 112-24.
54. Laplante M, Sabatini DM, (2009) mTOR signaling at a glance. J Cell Sci. 122(Pt 20): 3589-3594.
55. Takagi H, King GL, Aiello LP, (1998) Hypoxia upregulates glucose transport activity through an adenosine-mediated increase of GLUT1 expression in retinal capillary endothelial cells. Diabetes. 47: 1480-1488.
56. Schalm SS, Blenis J, (2002) Identification of a conserved motif required for mTOR signaling. Curr Biol. 12: 632-639.
57. Shao J, Evers BM, Sheng H, (2004) Roles of phosphatidylinositol 3′-kinase and mammalian target of rapamycin/p70 ribosomal protein S6 kinase in K-Ras-mediated transformation of intestinal epithelial cells. Cancer Res. 64: 229-235.
58. Minami T, Zushi S, Shinomura Y, Matsuzawa Y, (1996) Phospholipase A2 stimulation of rat intestinal epithelial cell (IEC-6) migration. Am J Physiol. 271(4 Pt 1): G664-668.
59. Ban K, Santora R, Kozar RA, (2001) Enteral arginine modulates inhibition of AP-1/c-Jun by SP600125 in the postischemic gut. Mol Cell Biochem. 347: 191-199.
60. Paddenberg R, Stieger P, von Lilien AL, Faulhammer P, Goldenberg A, et al. (2007) Rapamycin attenuates hypoxia-induced pulmonary vascular remodeling and right ventricular hypertrophy in mice. Respir Res. 2007 8: 15.
61. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN, (1970) Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg. 101: 478-483.
62. Park PO, Haglund U, Bulkley GB, Fält K, (1990) The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery. 107: 574-580.
63. Quaedackers JS, Beuk RJ, Bennet L, Charlton A, oude Egbrink MG, et al. (2000) An evaluation of methods for grading histologic injury following ischemia/reperfusion of the small bowel. Transplant Proc. 32: 1307-1310.
64. Wattanasirichaigoon S, Menconi MJ, Delude RL, Fink MP, (1999) Lisofylline ameliorates intestinal mucosal barrier dysfunction caused by ischemia and ischemia/reperfusion. Shock. 11: 269-275.
65. Tawadrous ZS, Delude RL, Fink MP, (2002) Resuscitation from hemorrhagic shock with Ringer's ethyl pyruvate solution improves survival and ameliorates intestinal mucosal hyperpermeability in rats. Shock. 17: 473-477.