Morg1 heterozygous mice are protected from acute renal ischemia-reperfusion injury

American Journal of Physiology - Renal Physiology

Volumn 297, Issue 5, 2009, Pages

  Hammerschmidt, Elke ^a   Loeffler, Ivone ^a   Wolf, Gunter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Chemokine expression; HIF 1 ; HIF 2 ; Hypoxia; Ischemic renal failure; Renal inflammation

Indexed keywords

ERYTHROPOIETIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL HYDROXYLASE 3; PROTEIN MORG 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; HETEROZYGOSITY; KIDNEY ISCHEMIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RENAL PROTECTION; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE;

EID: 70350705956     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00204.2009     Document Type: Article

References (48)

1. Abuelo JG. Normotensive ischemic acute renal failure. N Engl J Med 357: 797-805, 2007.
2. Alderliesten, de Graauw M A, Oldenampsen J, Qin Y, Pont C, van Buren L, van de Water B. Extracellular signal-regulated kinase activation during renal ischemia/reperfusion mediates focal adhesion dissolution and renal injury. Am J Pathol 171: 452-462, 2007. (Pubitemid 47344678)
3. Asselman M, Verhulst A, Van Ballegooijen ES, Bangma CH, Verkoelen CF, De Broe ME. Hyaluronan is apically secreted and expressed by proliferating or regenerating renal tubular cells. Kidney Int 68: 71-83, 2005. (Pubitemid 43181365)
4. Barrilli A, Molinas S, Petrini G, Menacho M, Elias MM. Losartan reverses fibrotic changes in cortical renal tissue induced by ischemia or ischemia-reperfusion without changes in renal function. Mol Cell Biochem 260: 161-170, 2004. (Pubitemid 39127584)
5. Beck-Schimmer B, Oertli B, Pasch T, Wüthrich RP. Hyaluronan induces monocyte chemoattractant protein-1 expression in renal tubular epithelial cells. J Am Soc Nephrol 9: 2283-2290, 1998. (Pubitemid 28543806)
6. Bernhardt WM, Câmpean V, Kany S, Jürgensen JS, Weidemann A, Warnecke C, Arend M, Klaus S, Günzler V, Amann K, Willam C, Wiesener MS, Eckardt KU. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 17: 1970-1978, 2006.
7. Bishop T, Galagher D, Pascual A, Lygate CA, de Bono JP, Nicholls LG, Ortega-Saenz P, Oster H, Wijeyekoon B, Sutherland AI, Grosfeld A, Aragones J, Schnieder M, van Geyte K, Teixeira D, Diez-Juan A, Lopez-Barneo J, Channon KM, Maxwell PH, Pugh CW, Davies AM, Carmeliet P, Ratcliffe PJ. Abnormal sympathoadrenal development and systemic hypotension in PHD3 -/- mice. Mol Cell Biol 28: 3386-3400, 2008. (Pubitemid 351657101)
8. Broekema M, Harmsen MC, van Luyn MJA, Koerts JA, Petersen AH, van Kooten TG, van Goor H, Navis G, Popa ER. Bone marrow-derived myofibroblasts contribute to the renal interstitial myofibroblast population and produce procallagen I after ischemia/reperfusion in rats. J Am Soc Nephrol 18: 165-175, 2007. (Pubitemid 46053430)
9. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622, 2009.
10. Capecchi MR. Altering the genome by homologous recombination. Science 244: 1288-1292, 1989.
11. Göransson V, Johnsson C, Jacobson A, Heldin P, Hällgren R, Hansell P. Renal hyaluronan accumulation and hyaluronan synthase expression after ischemia-reperfusion injury in the rat. Nephrol Dial Transplant 19: 823-830, 2004. (Pubitemid 38455652)
12. Hill P, Shukla D, Tran MG, Aragones J, Cook HT, Carmeliet P, Maxwell PH. Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 19: 39-46, 2008.
13. Hopfer U, Hopfer H, Jablonski K, Stahl RAK, Wolf G. The novel WD-repeat protein Morg1 acts as a molecular scaffold for hypoxia-inducible factor prolyl hydroxylase 3 (PHD3). J Biol Chem 281: 8645-8655, 2006. (Pubitemid 43847969)
14. Jo SK, Sung SA, Cho WY, Go KJ, Kim HK. Macrophage contribute to the initiation of ischaemic acute renal failure in rats. Nephrol Dial Transplant 21: 1231-1239, 2006.
15. Joyeux-Faure M. Cellular protection by erythropoietin: new therapeutic implications? J Pharmacol Exp Ther 323: 759-762, 2007. (Pubitemid 350146047)
16. Kuhlicke J, Frick JS, Morote-Garcia JC, Rosenberger P, Eltzschig HK. Hypoxia inducible factor (HIF-1) coordinates induction of Toll-like receptors TLR2 and TLR6 during hypoxia. PloS ONE 12: e1364, 2007. (Pubitemid 351753480)
17. Li L, Yi F, Sundy CM, Chen L, Hilliker ML, Donley DK, Muldoon DB, Li PL. Expression and actions of HIF prolyl-4-hydroxylase in the rat kidney. Am J Physiol Renal Physiol 292: F207-F216, 2007. (Pubitemid 46105261)
18. Li L, Xiong Y, Qu Y, Mao M, Mu W, Wang H, Mu D. The requirement of extracellular signal-related protein kinase pathway in the activation of hypoxia inducible factor 1α in the developing rat brain after hypoxiaischemia. Acta Neuropathol 115: 297-303, 2008.
19. Matsumoto M, Makino Y, Tanaka T, Tanaka H, Ishizaka N, Noiri E, Fujita T, Nangaku M. Induction of renoprotective gene expression by cobalt ameliorates ischemic injury of the kidney in rats. J Am Soc Nephrol 14: 1825-1832, 2003.
20. Menke J, Iwata Y, Rabacal WA, Basu R, Yeung YG, Humphreys BD, Wada T, Schwarting A, Stanley ER, Kelley VR. CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. J Clin Invest 119: 2330-2342, 2009.
21. Menne J, Park JK, Shushakova N, Mengel M, Meier M, Fliser D. The continuous erythropoietin receptor activator affects different pathways of diabetic renal injury. J Am Soc Nephrol 18: 2046-2053, 2007. (Pubitemid 47041070)
22. Miyazawa S, Watanabe H, Miyaji C, Hotta O, Abo T. Leukocyte accumulation and changes in extra-renal organs during renal ischemia reperfusion in mice. J Lab Clin Med 139: 269-278, 2002. (Pubitemid 34577478)
23. Mole DR, Ratcliffe PJ. Cellular oxygen sensing in health and disease. Pediatr Nephrol 23: 681-694, 2008.
24. Nangaku M, Eckardt KU. Hypoxia and the HIF system in the kidney disease. J Mol Med 85: 1325-1330, 2007. (Pubitemid 50004091)
25. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 17: 17-25, 2006. (Pubitemid 39274273)
26. Pombo CM, Bonventre JV, Avruch J, Woodgett JR, Kyriakis JM, Force T. The stress-activated protein kinases are major c-jun amino-terminal kinases activated by ischemia and reperfusion. J Biol Chem 269: 26546-26551, 1994. (Pubitemid 24328483)
27. Prakash J, de Borst MH, Lacombe M, Opdam F, Klok PA, van Goor H, Meijer DKF, Moolenaar F, Poelstra K, Kok RJ. Inhibition of renal Rho kinase attenuates ischemia/reperfusion-induced injury. J Am Soc Nephrol 19: 2086-2097, 2008.
28. Rankin EB, Biju MP, Liu Q, Unger TL, Rha J, Johnson RS, Simon MC, Kieth B, Haase VH. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 117: 1068-1077, 2007. (Pubitemid 46556763)
29. Rantanen K, Pursiheimo J, Högel H, Himanen V, Metzen E, Jaakkola PM. Prolyl hydroxylase PHD3 activates oxygen-depedent protein aggregation. Mol Biol Cell 19: 2231-2240, 2008.
30. Richard DE, Berra E, Gothié E, Roux D, Pouysségur J. p42/44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J Biol Chem 274: 32631-32637, 1999. (Pubitemid 129535289)
31. Rose S, Stillman IE. Acute tubular necrosis is a syndrome of physiologic and pathologic dissociation. J Am Soc Nephrol 19: 871-875, 2008.
32. Rosenberger C, Griethe W, Gruber G, Wiesener M, Frei U, Bachmann S, Eckardt KU. Cellular responses to hypoxia after segmental infarction. Kidney Int 64: 874-886, 2003. (Pubitemid 37013823)
33. Rosenberger C, Heyman SN, Rosen S, Shina A, Goldfarb M, Griethe W, Frei U, Reinke P, Bachmann S, Eckardt KU. Up-regulation of HIF in experimental acute renal failure: evidence for a protective transcriptional response to hypoxia. Kidney Int 67: 531-542, 2005. (Pubitemid 40139845)
34. Rosenberger C, Rosen S, Heymann SN. Renal parenchymal oxygenation and hypoxia adaptation in acute kidney injury. Clin Exp Pharmacol Physiol 33: 980-988, 2006. (Pubitemid 44427322)
35. Salahudeen AK, Haider N, Jenkins J, Joshi M, Patel H, Huang H, Yang M, Zhe H. Antiapoptotic properties of erythropoiesis-stimulating proteins in models of cisplatin-induced acute kidney injury. Am J Physiol Renal Physiol 294: F1354-F1365, 2008.
36. Sandovici M, Henning RH, van Goor H, Helfrich W, de Zeeuw D, Deelman LE. Systemic gene therapy with interleukin-13 attenuates renal ischemia-reperfusion injury. Kidney Int 73: 1364-1373, 2008. (Pubitemid 351770490)
37. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Götte M, Malle E, Schaefer RM, Gröne HJ. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115: 2223-2233, 2005. (Pubitemid 41134165)
38. Schödeöl J, Klanke B, Weidemann A, Buchholz B, Berhardt W, Bertog M, Amann K, Korbmacher C, Wiesener M, Warnecke C, Kurtz A, Eckardt KU, Willam C. HIF-prolyl hydroxylases in the rat kidney. Am J Pathol 174: 1663-1674, 2009.
39. Serviddio G, Romano AD, Gesualdo L, Tamborra R, Di Palma AM, Rollo T, Altomare E, Vendemiale G. Postconditioning is an effective strategy to reduce renal ischaemia/reperfusion injury. Nephrol Dial Transplant 23: 1504-1512, 2008. (Pubitemid 351767728)
40. Szwarc I, Soullier S, Gayrard N, Mejean C, Mourad G, Argiles A. Ischemic postconditioning prevents ischemic acute renal failure. Transplan Proc 39: 2554-2556, 2007. (Pubitemid 47588390)
41. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor α levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol 26: 8336-8346, 2006. (Pubitemid 44748568)
42. Vomastek T, Schaeffer HJ, Tarcsafalvi A, Smolkin ME, Bissonette EA, Weber MJ. Modular construction of a signaling scaffold: MORG1 interacts with components of the ERK cascade and links ERK signaling to specific agonists. Proc Natl Acad Sci USA 101: 6981-6986, 2004. (Pubitemid 38596429)
43. Weidemann A, Bernhardt WM, Klanke B, Daniel C, Buchholz B, Câmpean V, Amann K, Warnecke C, Wiesener MS, Eckardt KU, Willam C. HIF activation, protects from acute kidney injury. J Am Soc Nephrol 19: 486-494, 2008. (Pubitemid 351355392)
44. Weigel PH, DeAngeelis PL. Hyaluronan synthases; a decade-plus of novel glycosyltransferases. J Biol Chem 282: 3677-36781, 2007.
45. Wolf G, Bohlender J, Bondeva T, Roger T, Thaiss F, Wenzel UO. Angiotensin II upregulates Toll-like receptor 4 on mesangial cells. J Am Soc Nephrol 17: 1585-1593, 2006. (Pubitemid 43794661)
46. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban S. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 117: 2847-2859, 2007. (Pubitemid 47529615)
47. Yamada K, Miwa T, Liu J, Nangaku M, Song WC. Critical protection from renal ischemia reperfusion injury by CD55 and CD59. J Immunol 172: 3869-3875, 2004. (Pubitemid 38337974)
48. Yin JL, Shackel NA, Zekry A, McGuinness PH, Richards C, Putten KV, McCaughan GW, Eris JM, Bishop GA. Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with the fluorogenic probes or SYBR green I. Immunol Cell Biol 79: 213-221, 2001. (Pubitemid 32522168)