Pkd2 mesenteric vessels exhibit a primary defect in endothelium-dependent vasodilatation restored by rosiglitazone

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 1, 2013, Pages

  Brookes, Zoë L S ^a   Ruff, Lewis ^a   Upadhyay, Viralkumar S ^b   Huang, Linghong ^a   Prasad, Sony ^a   Solanky, Tirupa ^a   Nauli, Surya M ^b   Ong, Albert C M ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Autosomal dominant polycystic kidney disease; Ischemia reperfusion injury; Nitric oxide; Peroxisome proliferator activated receptor; Polycystic kidney disease 2

Indexed keywords

ACETYLCHOLINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PEROXYNITRITE; PHENYLEPHRINE; POLYCYSTIN 2; POTASSIUM CHLORIDE; ROSIGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CELL STIMULATION; CONTROLLED STUDY; DRUG EFFICACY; ENDOTHELIUM DEPENDENT VASODILATATION; HEART MUSCLE ISCHEMIA; HYPERTENSION; IN VIVO STUDY; KIDNEY FAILURE; MALE; MESENTERY BLOOD VESSEL; MOUSE; MYOGRAPHY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASODILATATION; VENULE;

ANIMALS; ANTIOXIDANTS; ARTERIOLES; CALCIUM; CAPILLARY PERMEABILITY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENOTYPE; HETEROZYGOTE; HYPERTENSION; MALE; MESENTERY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; MYOGRAPHY; NITRIC OXIDE; OXIDATIVE STRESS; PEROXYNITROUS ACID; PHENOTYPE; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; PPAR GAMMA; RENAL INSUFFICIENCY; REPERFUSION INJURY; SUPEROXIDES; THIAZOLIDINEDIONES; TIME FACTORS; TRPP CATION CHANNELS; VASODILATION; VASODILATOR AGENTS; VENULES;

EID: 84871914247     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01102.2011     Document Type: Article

References (42)

1. AbouAlaiwi WA, Takahashi M, Mell BR, Jones TJ, Ratnam S, Kolb RJ, Nauli SM. Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 104: 860-869, 2009.
2. Bagi Z, Koller A, Kaley G. PPAR γ activation, by reducing oxidative stress, increases NO bioavailability in coronary arterioles of mice with Type 2 diabetes. Am J Physiol Heart Circ Physiol 286: H742-H748, 2004.
3. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624, 1990.
4. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol Cell Physiol 271: C1424-C1437, 1996.
5. Boulter C, Mulroy S, Webb S, Fleming S, Brindle K, Sandford R. Cardiovascular, skeletal, and renal defects in mice with a targeted disruption of the Pkd1 gene. Proc Natl Acad Sci USA 98: 12174-12179, 2001.
6. Boyle JG, Logan PJ, Ewart MA, Reihill JA, Ritchie SA, Connell JMC, Cleland SJ, Salt IP. Rosiglitazone stimulates nitric oxide synthesis in human aortic endothelial cells via AMP-activated protein kinase. J Biol Chem 283: 11210-11217, 2008.
7. Brookes ZL, Kaufman S. Myogenic responses and compliance of mesenteric and splenic vasculature in the rat. Am J Physiol Regul Integr Comp Physiol 284: R1604-R1610, 2003.
8. Brookes ZL, Stedman EN, Guerrini R, Lawton BK, Calo G, Lambert DG. Proinflammatory and vasodilator effects of nociceptin/orphanin FQ in the rat mesenteric microcirculation are mediated by histamine. Am J Physiol Heart Circ Physiol 293: H2977-H2985, 2007.
9. Calnek DS, Mazzella L, Roser S, Roman J, Hart CM. Peroxisome proliferator-activated receptor gamma ligands increase release of nitric oxide from endothelial cells. Arterioscler Thromb Vasc Biol 23: 52-57, 2003.
10. Chang MY, Parker E, El Nahas M, Haylor JL, Ong AC. Endothelin B receptor blockade accelerates disease progression in a murine model of autosomal dominant polycystic kidney disease. J Am Soc Nephrol 18: 560-569, 2007.
11. Chang MY, Parker E, Ibrahim S, Shortland JR, Nahas ME, Haylor JL, Ong AC. Haploinsufficiency of Pkd2 is associated with increased tubular cell proliferation and interstitial fibrosis in two murine Pkd2 models. Nephrol Dial Transplant 21: 2078-2084, 2006.
12. Charleston C, Puana R, McAllister RK, Hunter FA, Childs EW. Morphine sulfate attenuates hemorrhagic shock-induced hyperpermeability. Anesth Analg 103: 156-161, 2006.
13. Clough G, Michel CC, Phillips ME. Inflammatory changes in permeability and ultrastructure of single vessels in the frog mesenteric microcirculation. J Physiol 395: 99-114, 1988.
14. Gao Z, Joseph E, Ruden DM, Lu X. Drosophila Pkd2 is haploid- insufficient for mediating optimal smooth muscle contractility. J Biol Chem 279: 14225-14231, 2004.
15. Harrington LS, Carrier MJ, Gallagher N, Gilroy D, Garland CJ, Mitchell JA. Elucidation of the temporal relationship between endothelial-derived NO and EDHF in mesenteric vessels. Am J Physiol Heart Circ Physiol 293: H1682-H1688, 2007.
16. Hwang J, Kleinhenz DJ, Rupnow HL, Campbell AG, Thule PM, Sutliff RL, Hart CM. The PPAR ligand, rosiglitazone, reduces vascular oxidative stress and NADPH oxidase expression in diabetic mice. Vascul Pharmacol 46: 456-462, 2007.
17. Kawanabe Y, Takahashi M, Jin X, Abdul-Majeed S, Nauli AM, Sari Y, Nauli SM. Cilostazol prevents endothelin-induced smooth muscle constriction and proliferation. PLos One 7: e44476, 2012.
18. Kim K, Drummond I, Ibraghimov-Beskrovnaya O, Klinger K, Arnaout MA. Polycystin 1 is required for the structural integrity of blood vessels. Proc Natl Acad Sci USA 97: 1731-1736, 2000.
19. Kurbegovic A, Cote O, Couillard M, Ward CJ, Harris PC, Trudel M. Pkd1 transgenic mice: adult model of polycystic kidney disease with extrarenal and renal phenotypes. Hum Mol Genet 19: 1174-1189, 2010.
20. Lantinga-van Leeuwen IS, Dauwerse JG, Baelde HJ, Leonhard WN, van de Wal A, Ward CJ, Verbeek S, Deruiter MC, Breuning MH, de Heer E, Peters DJ. Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease. Hum Mol Genet 13: 3069-3077, 2004.
21. Mansart A, Ruff LJ, Ariaans MP, Ross JJ, Reilly CS, Brown NJ, Kaufman S, Brookes ZL. Constriction of rat extra-splenic veins to lipopolysaccharide involves endothelin-1. Naunyn Schmiedebergs Arch Pharmacol 381: 555-562, 2010.
22. Mao Z, Ong AC. Peroxisome proliferator-activated receptor gamma agonists in kidney disease-future promise, present fears. Nephron Clin Pract 112: c230-c241, 2009.
23. McGown CC, Brown NJ, Hellewell PG, Reilly CS, Brookes ZL. Beneficial microvascular and anti-inflammatory effects of pravastatin during sepsis involve nitric oxide synthase III. Br J Anaesth 104: 183-190, 2010.
24. Merta M, Reiterova J, Rysava R, Tesar V, Zavada J, Jachymova M, Zima T. Role of endothelin and nitric oxide in the pathogenesis of arterial hypertension in autosomal dominant polycystic kidney disease. Physiol Res 52: 433-437, 2003.
25. Mindham MA, Mayes PA. The fuel of the spleen. Studies using a new method for perfusing the rat spleen with whole blood. Biochem J 263: 325-332, 1989.
26. Morel N, Vandenberg G, Ahrabi AK, Caron N, Desjardins F, Balligand JL, Horie S, Devuyst O. PKD1 haploinsufficiency is associated with altered vascular reactivity and abnormal calcium signaling in the mouse aorta. Pflügers Arch 457: 845-856, 2009.
27. Muto S, Aiba A, Saito Y, Nakao K, Nakamura K, Tomita K, Kitamura T, Kurabayashi M, Nagai R, Higashihara E, Harris PC, Katsuki M, Horie S. Pioglitazone improves the phenotype and molecular defects of a targeted Pkd1 mutant. Hum Mol Genet 11: 1731-1742, 2002.
28. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J. Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 117: 1161-1171, 2008.
29. Ong AC, Harris PC. Molecular pathogenesis of ADPKD: The polycystin complex gets complex. Kidney Int 67: 1234-1247, 2005.
30. Ong AC, Ward CJ, Butler RJ, Biddolph S, Bowker C, Torra R, Pei Y, Harris PC. Coordinate expression of the autosomal dominant polycystic kidney disease proteins, polycystin-2 and polycystin-1, in normal and cystic tissue. Am J Pathol 154: 1721-1729, 1999.
31. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J, Blum M, Dworniczak B. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12: 938-943, 2002.
32. Prasad S, McDaid JP, Tam FW, Haylor JL, Ong AC. Pkd2 dosage influences cellular repair responses following ischemia-reperfusion injury. Am J Pathol 175: 1493-1503, 2009.
33. Qian Q, Hunter LW, Du H, Ren Q, Han Y, Sieck GC. Pkd2 / vascular smooth muscles develop exaggerated vasocontraction in response to phenylephrine stimulation. J Am Soc Nephrol 18: 485-493, 2007.
34. Qian Q, Hunter LW, Li M, Marin-Padilla M, Prakash YS, Somlo S, Harris PC, Torres VE, Sieck GC. Pkd2 haploinsufficiency alters intra- cellular calcium regulation in vascular smooth muscle cells. Hum Mol Genet 12: 1875-1880, 2003.
35. Reed RA, Mattai J, Shipley GG. Interaction of cholera toxin with ganglioside GM1 receptors in supported lipid monolayers. Biochemistry 26: 824-832, 1987.
36. Torres VE, Harris PC, Pirson Y. Autosomal dominant polycystic kidney disease. Lancet 369: 1287-1301, 2007.
37. Wang D, Iversen J, Strandgaard S. Contractility and endothelium- dependent relaxation of resistance vessels in polycystic kidney disease rats. J Vasc Res 36: 502-509, 1999.
38. Wang D, Iversen J, Strandgaard S. Endothelium-dependent relaxation of small resistance vessels is impaired in patients with autosomal dominant polycystic kidney disease. J Am Soc Nephrol 11: 1371-1376, 2000.
39. Wang D, Iversen J, Wilcox CS, Strandgaard S. Endothelial dysfunction and reduced nitric oxide in resistance arteries in autosomal-dominant polycystic kidney disease. Kidney Int 64: 1381-1388, 2003.
40. Wang P, Zweier JL. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J Biol Chem 271: 29223-29230, 1996.
41. Wu G, D'Agati V, Cai Y, Markowitz G, Park JH, Reynolds DM, Maeda Y, Le TC, Hou H Jr, Kucherlapati R, Edelmann W, Somlo S. Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell 93: 177-188, 1998.
42. Wu G, Markowitz GS, Li L, D'Agati VD, Factor SM, Geng L, Tibara S, Tuchman J, Cai Y, Park JH, van Adelsberg J, Hou H Jr, Kucherlapati R, Edelmann W, Somlo S. Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat Genet 24: 75-78, 2000.