Postconditioning with glucagon like peptide-2 reduces ischemia/reperfusion injury in isolated rat hearts: role of survival kinases and mitochondrial KATP channels (original) (raw)

References

  1. Angelone T, Filice E, Quintieri AM, Imbrogno S, Amodio N, Pasqua T, Pellegrino D, Mulè F, Cerra MC (2010) Receptor identification and physiological caracterization of glucagon-like peptide-2 in the rat heart. Nutr Metab Cardiovasc Dis 22:486–494. doi:10.1016/j.numecd.2010.07.014
    Article PubMed Google Scholar
  2. Ban K, Kim KH, Cho CK, Sauvé M, Diamandis EP, Backx PH, Drucker DJ, Husain M (2010) Glucagon-like peptide (GLP)-1(9-36)amide-mediated cytoprotection is blocked by exendin(9-39) yet does not require the known GLP-1 receptor. Endocrinology 151:1520–1531. doi:10.1210/en.2009-1197
    Article PubMed CAS Google Scholar
  3. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105:771–785. doi:10.1007/s00395-010-0124-1
    Article PubMed CAS Google Scholar
  4. Bose AK, Mocanu MM, Carr RD, Yellon DM (2005) Glucagon like peptide-1 is protective against myocardial ischemia/reperfusion injury when given either as a preconditioning mimetic or at reperfusion in an isolated rat heart model. Cardiovasc Drugs Ther 19:9–11. doi:10.1007/s10557-007-6030-6
    Article PubMed Google Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 7:248–254
    Article Google Scholar
  6. Cerra MC, De Iuri L, Angelone T, Corti A, Tota B (2006) Recombinant N-terminal fragments of chromogranin-A modulate cardiac function of the Langendorff-perfused rat heart. Basic Res Cardiol 100:1–10. doi:10.1007/s00395-005-0547-2
    Google Scholar
  7. Chance WT, Foley-Nelson T, Thomas I, Balasubramaniam A (1997) Prevention of parenteral nutrition-induced gut hypoplasia by coinfusion of glucagon-like peptide-2. Am J Physiol 273:G559–G563
    PubMed CAS Google Scholar
  8. Cohen MV, Downey JM (2011) Ischemic postconditioning: from receptor to end-effector. Antioxid Redox Signal 14:821–831. doi:10.1089/ars.2010.3318
    Article PubMed CAS Google Scholar
  9. Darling CE, Jiang R, Maynard M, Whittaker P, Vinten-Johansen J, Przyklenk K (2005) Postconditioning via stuttering reperfusion limits myocardial infarct size in rabbit hearts: role of ERK1/2. Am J Physiol Heart Circ Physiol 289:H1618–H1626. doi:10.1152/ajpheart.00055.2005
    Article PubMed CAS Google Scholar
  10. Drucker DJ (1998) Glucagon-like peptides. Diabetes 47:159–169. doi:10.1210/en.142.2.521
    Article PubMed CAS Google Scholar
  11. Dube PE, Brubaker PL (2007) Frontiers in glucagon-like peptide-2: multiple actions, multiple mediators. Am J Physiol Endocrinol Metab 293:E460–E465. doi:10.1152/ajpendo.00149.2007
    Article PubMed CAS Google Scholar
  12. Gomez L, Paillard M, Thibault H, Derumeaux G, Ovize M (2008) Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 117:2761–2768. doi:10.1161/CIRCULATIONAHA.107.755066
    Article PubMed CAS Google Scholar
  13. Guan L, Gong D, Tian N, Zou Y (2005) Uncoupling protein 2 involved in protection of glucagon-like peptide 2 in small intestine with ischemia-reperfusion injury in mice. Dig Dis Sci 50:554–560. doi:10.1007/s10620-005-2474-3
    Article PubMed CAS Google Scholar
  14. Hausenloy DJ, Baxter G, Bell R, Bøtker HE, Davidson SM, Downey J, Heusch G, Kitakaze M, Lecour S, Mentzer R, Mocanu MM, Ovize M, Schulz R, Shannon R, Walker M, Walkinshaw G, Yellon DM (2010) Translating novel strategies for cardioprotection: the Hatter Workshop recommendations. Basic Res Cardiol 105:677–686. doi:10.1007/s00395-010-0121-4
    Article PubMed Google Scholar
  15. Hausenloy DJ, Lecour S, Yellon DM (2011) Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischaemic postconditioning: two sides of the same coin. Antioxid Redox Signal 14:893–907. doi:10.1089/ars.2010.3360
    Article PubMed CAS Google Scholar
  16. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM (2005) Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288:H971–H976. doi:10.1152/ajpheart.00374.2004
    Article PubMed CAS Google Scholar
  17. Hausenloy DJ, Yellon DM (2004) New directions for protecting the heart against ischaemia-reperfusion injury: targeting the reperfusion injury salvage kinase (RISK)-pathway. Cardiovasc Res 61:448–460. doi:10.1016/j.cardiores.2003.09.024
    Article PubMed CAS Google Scholar
  18. Heusch G (2009) No risk, no cardioprotection? A critical perspective. Cardiovasc Res 84:173–175. doi:10.1093/cvr/cvp298
    Article PubMed CAS Google Scholar
  19. Heusch G, Musiolik J, Gedik N, Skyschally A (2011) Mitochondrial STAT3 activation and cardioprotection by ischemic postconditioning in pigs with regional myocardial ischemia/reperfusion. Circ Res 109:1302–1308. doi:10.1161/CIRCRESAHA.111.255604
    Article PubMed CAS Google Scholar
  20. Hönisch A, Theuring N, Ebner B, Wagner C, Strasser RH, Weinbrenner C (2010) Postconditioning with levosimendan reduces the infarct size involving the PI3 K pathway and KATP-channel activation but is independent of PDE-III inhibition. Basic Res Cardiol 105:155–167. doi:10.1007/s00395-009-0064-9
    Article PubMed Google Scholar
  21. Hoosein NM, Gurd RS (1984) Human glucagon-like peptides 1 and 2 activate rat brain adenylate cyclase. FEBS Lett 178:83–86. doi:10.1016/0014-5793(84)81245-4
    Article PubMed CAS Google Scholar
  22. Jeppesen PB, Sanguinetti EL, Buchman A, Howard L, Scolapio JS, Ziegler TR, Gregory J, Tappenden KA, Holst J, Mortensen PB (2005) Teduglutide (ALX-0600), a dipeptidyl peptidase IV resistant glucagon-like peptide 2 analogue, improves intestinal function in short bowel syndrome patients. Gut 54:1224–1231. doi:10.1136/gut.2004.061440
    Article PubMed CAS Google Scholar
  23. L’Heureux MC, Brubaker PL (2003) Glucagon-like peptide-2 and common therapeutics in a murine model of ulcerative colitis. J Pharmacol Exp Ther 306:347–354. doi:10.1124/jpet.103.051771
    Article PubMed Google Scholar
  24. Lovshin J, Estall J, Yusta B, Brown TJ, Drucker DJ (2001) Glucagon-like peptide (GLP)-2 action in the murine central nervous system is enhanced by elimination of GLP-1 receptor signaling. J Biol Chem 276:21489–21499. doi:10.1074/jbc.M009382200
    Article PubMed CAS Google Scholar
  25. Lund A, Vilsbøll T, Bagger JI, Holst JJ, Knop FK (2011) The separate and combined impact of the intestinal hormones, GIP, GLP-1, and GLP-2, on glucagon secretion in type 2 diabetes. Am J Physiol Endocrinol Metab 300:E1038–E1046. doi:10.1152/ajpendo.00665.2010
    Article PubMed CAS Google Scholar
  26. Matsubara M, Kanemoto S, Leshnower BG, Albone EF, Hinmon R, Plappert T, Gorman JH 3rd, Gorman RC (2011) Single dose GLP-1-Tf ameliorates myocardial ischemia/reperfusion injury. J Surg Res 165:38–45. doi:10.1016/j.jss.2009.03.016
    Article PubMed CAS Google Scholar
  27. Munroe DG, Gupta AK, Kooshesh F, Vyas TB, Rizkalla G, Wang H, Demchyshyn L, Yang ZJ, Kamboj RK, Chen H, McCallum K, Sumner-Smith M, Drucker DJ, Crivici A (1999) Prototypic G protein coupled receptor for the intestinotrophic factor glucagon-like peptide 2. Proc Natl Acad Sci USA 96:1569–1573. doi:10.1073/pnas.96.4.1569
    Article PubMed CAS Google Scholar
  28. Nikolaidis LA, Mankad S, Sokos GG, Miske G, Shah A, Elahi D, Shannon RP (2004) Effects of glucagon-like peptide-1 in patients with acute myocardial infarction and left ventricular dysfunction after successful reperfusion. Circulation 109:962–965. doi:10.1161/01.CIR.0000120505.91348.58
    Article PubMed CAS Google Scholar
  29. Pagliaro P, Mancardi D, Rastaldo R, Penna C, Gattullo D, Miranda KM, Feelisch M, Wink DA, Kass DA, Paolocci N (2003) Nitroxyl affords thiol-sensitive myocardial protective effects akin to early preconditioning. Free Radic Biol Med 34:33–43. doi:10.1016/S0891-5849(02)01179-6
    Article PubMed CAS Google Scholar
  30. Penna C, Alloatti G, Cappello S, Gattullo D, Berta G, Mognetti B, Losano G, Pagliaro P (2005) Platelet-activating factor induces cardioprotection in isolated rat heart akin to ischaemic preconditioning: role of phosphoinositide 3-kinase and protein kinase C activation. Am J Physiol Heart Circ Physiol 288:H2512–H2520. doi:10.1152/ajpheart.00599.2004
    Article PubMed CAS Google Scholar
  31. Penna C, Mancardi D, Raimondo S, Geuna S, Pagliaro P (2008) The paradigm of postconditioning to protect the heart. J Cell Mol Med 12:435–458. doi:10.1111/j.1582-4934.2007.00210.x
    Article PubMed CAS Google Scholar
  32. Penna C, Mancardi D, Rastaldo R, Losano G, Pagliaro P (2007) Intermittent activation of bradykinin B2 receptors and mitochondrial KATP channels trigger cardiac postconditioning through redox signaling. Cardiovasc Res 75:168–177. doi:10.1016/j.cardiores.2007.03.001
    Article PubMed CAS Google Scholar
  33. Penna C, Perrelli MG, Raimondo S, Tullio F, Merlino A, Moro F, Geuna S, Mancardi D, Pagliaro P (2009) Postconditioning induces an anti-apoptotic effect and preserves mitochondrial integrity in isolated rat hearts. Biochim Biophys Acta 1787:780–794. doi:10.1016/j.bbabio.2009.03.013
    Google Scholar
  34. Penna C, Rastaldo R, Mancardi D, Raimondo S, Cappello S, Gattullo D, Losano G, Pagliaro P (2006) Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K + channel and protein kinase C activation. Basic Res Cardiol 101:180–189. doi:10.1007/s00395-006-0584-5
    Article PubMed CAS Google Scholar
  35. Perez A, Duxbury M, Rocha FG, Ramsanahie AP, Farivar RS, Varnholt H, Ito H, Wong H, Rounds J, Zinner MJ, Whang EE, Ashley SW (2005) Glucagon-like peptide 2 is an endogenous mediator of postresection intestinal adaptation. J Parenter Enteral Nutr 29:97–101. doi:10.1177/014860710502900297
    Article CAS Google Scholar
  36. Read PA, Hoole SP, White PA, Khan FZ, O’Sullivan M, West NE, Dutka DP (2011) A pilot study to assess whether glucagon-like Peptide-1 protects the heart from ischemic dysfunction and attenuates stunning after coronary balloon occlusion in humans. Circ Cardiovasc Interv 4:266–272. doi:10.1161/CIRCINTERVENTIONS.110.960476
    Article PubMed CAS Google Scholar
  37. Schulman D, Latchman DS, Yellon DM (2002) Urocortin protects the heart from reperfusion injury via upregulation of p42/p44 MAPK signaling pathway. Am J Physiol Heart Circ Physiol 283:H1481–H1488. doi:10.1152/ajpheart.01089.2001
    PubMed CAS Google Scholar
  38. Schwartz Longacre L, Kloner RA, Arai AE, Baines CP, Bolli R, Braunwald E, Downey J, Gibbons RJ, Gottlieb RA, Heusch G, Jennings RB, Lefer DJ, Mentzer RM, Murphy E, Ovize M, Ping P, Przyklenk K, Sack MN, Vander Heide RS, Vinten-Johansen J, Yellon DM (2011) New horizons in cardioprotection: recommendations from the 2010 national heart, lung, and blood institute workshop. Circulation 124:1172–1179. doi:10.1161/CIRCULATIONAHA.111.032698
    Article PubMed Google Scholar
  39. Shi X, Li X, Wang Y, Zhang K, Zhou F, Chan L, Li D, Guan X (2011) Glucagon-like peptide-2-stimulated protein synthesis through the PI 3Kinase-dependent Akt-mTOR signaling pathway. Am J Physiol Endocrinol Metab 300:E554–E563. doi:10.1152/ajpendo.00620.2010
    Article PubMed CAS Google Scholar
  40. Simpkin JC, Yellon DM, Davidson SM, Lim SY, Wynne AM, Smith CC (2007) Apelin-13 and apelin-36 exhibit direct cardioprotective activity against ischemia-reperfusion injury. Basic Res Cardiol 102:518–528. doi:10.1007/s00395-007-0671-2
    Article PubMed CAS Google Scholar
  41. Sivaraman V, Mudalagiri NR, Di Salvo C, Kolvekar S, Hayward M, Yap J, Keogh B, Hausenloy DJ, Yellon DM (2007) Postconditioning protects human atrial muscle through the activation of the RISK pathway. Basic Res Cardiol 102:453–459. doi:10.1007/s00395-007-0664-1
    Article PubMed Google Scholar
  42. Skyschally A, van Caster P, Boengler K, Gres P, Musiolik J, Schilawa D, Schulz R, Heusch G (2009) Ischemic postconditioning in pigs: no causal role for RISK activation. Circ Res 104:15–18. doi:10.1161/CIRCRESAHA.108.186429
    Article PubMed CAS Google Scholar
  43. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G (2009) Ischemic postconditioning: experimental models and protocol algorithms. Basic Res Cardiol 104:469–483. doi:10.1007/s00395-009-0040-4
    Article PubMed Google Scholar
  44. Tamareille S, Mateus V, Ghaboura N, Jeanneteau J, Croué A, Henrion D, Furber A, Prunier F (2009) RISK and SAFE signaling pathway interactions in remote limb ischemic perconditioning in combination with local ischemic postconditioning. Basic Res Cardiol 106:1329–1339. doi:10.1007/s00395-011-0210-z
    Article Google Scholar
  45. Tang-Christensen M, Larsen PJ, Thulesen J, Romer J, Vrang N (2000) The proglucagon-derived peptide, glucagon-like peptide-2, is a neurotransmitter involved in the regulation of food intake. Nat Med 6:802–807. doi:10.1038/77535
    Article PubMed CAS Google Scholar
  46. Tsang A, Hausenloy D, Mocanu M, Yellon D (2004) Postconditioning: a form of “Modified reperfusion” protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res 95:230–232. doi:10.1161/01.RES.0000138303.76488.fe
    Article PubMed CAS Google Scholar
  47. Vinten-Johansen J, Zhao ZQ, Zatta AJ, Kin H, Halkos ME, Kerendi F (2005) Postconditioning: a new link in nature’s armor against myocardial ischemia-reperfusion injury. Basic Res Cardiol 100:295–310. doi:10.1007/s00395-005-0523-x
    Article PubMed CAS Google Scholar
  48. Yang XM, Philipp S, Downey JM, Cohen MV (2005) Postconditioning’s protection is not dependent on circulating blood factors or cells but involves adenosine receptors and requires PI3–kinase and guanylyl cyclase activation. Basic Res Cardiol 100:57–63. doi:10.1007/s00395-004-0498-4
    Article PubMed CAS Google Scholar
  49. Yang XM, Proctor JB, Cui L, Krieg T, Downey JM, Cohen MV (2004) Multiple, brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways. J Am Coll Cardiol 44:1103–1110. doi:10.1016/j.jacc.2004.05.060
    Article PubMed Google Scholar
  50. Ye Y, Perez-Polo JR, Aguilar D, Birnbaum Y (2011) The potential effects of anti-diabetic medications on myocardial ischemia-reperfusion injury. Basic Res Cardiol 106:925–952. doi:10.1007/s00395-011-0216-6
    Article PubMed CAS Google Scholar
  51. Zhang W, Zhu W, Zhang J, Li N, Li J (2008) Protective effects of glucagon-like peptide 2 on intestinal ischemia-reperfusion rats. Microsurgery 28:285–290. doi:10.1002/micr.20491
    Article PubMed CAS Google Scholar

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