Vascular endothelial dysfunction in Duchenne muscular dystrophy is restored by bradykinin through upregulation of eNOS and nNOS

Basic Research in Cardiology

Volumn 107, Issue 1, 2012, Pages

  Dabiré, Hubert ^a   Barthélémy, Inès ^b,c   Blanchard Gutton, Nicolas ^b,c   Sambin, Lucien ^a   Sampedrano, Carolina Carlos ^a   Gouni, Vassiliki ^a   Unterfinger, Yves ^b,c   Aguilar, Pablo ^b,c   Thibaud, Jean Laurent ^b,c   Ghaleh, Bijan ^a,c   Bizé, Alain ^a,c   Pouchelon, Jean Louis ^a,c   Blot, Stéphane ^b,c   Berdeaux, Alain ^a,c   Hittinger, Luc ^a,c   Chetboul, Valérie ^a,c   Su, Jin Bo ^a  

^a INSERM U955   (France)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Bradykinin; Duchenne muscular dystrophic cardiomyopathy; Endothelial dysfunction; Endothelial nitric oxide synthase; Neuronal nitric oxide synthase

Indexed keywords

BRADYKININ; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; CORONARY ARTERY DILATATION; DOG; DRUG MECHANISM; DUCHENNE MUSCULAR DYSTROPHY; ENDOTHELIAL DYSFUNCTION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; WESTERN BLOTTING;

ANIMALS; BLOOD PRESSURE; BRADYKININ; CAROTID ARTERIES; CYCLIC GMP; DISEASE MODELS, ANIMAL; DOGS; ENDOTHELIUM, VASCULAR; MUSCULAR DYSTROPHY, DUCHENNE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; VENTRICULAR DYSFUNCTION, LEFT;

EID: 83755172261     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-011-0240-6     Document Type: Article

References (44)

1. T Bachetti L Comini E Pasini A Cargnoni S Curello R Ferrari 2001 Ace-inhibition with quinapril modulates the nitric oxide pathway in normotensive rats J Mol Cell Cardiol 33 395 403 10.1006/jmcc.2000.1311 11181009 10.1006/jmcc.2000.1311 1:CAS:528:DC%2BD3MXht1aqtrk%3D (Pubitemid 32538997)
2. F Barbe JB Su TT Guyene B Crozatier J Ménard L Hittinger 1996 Bradykinin pathway is involved in acute hemodynamic effects of enalaprilat in dogs with heart failure Am J Physiol 270 H1985 H1992 8764248 1:CAS:528:DyaK28XktlSjtrY%3D
3. RJ Bartlett S Stockinger MM Denis WT Bartlett L Inverardi TT Le N thi Man GE Morris DJ Bogan J Metcalf-Bogan JN Kornegay 2000 In vivo targeted repair of a point mutation in the canine dystrophin gene by a chimeric RNA/DNA oligonucleotide Nat Biotechnol 18 615 622 10.1038/76448 10835598 10.1038/76448 1:CAS:528:DC%2BD3cXkt12gtLw%3D (Pubitemid 30415294)
4. HD Bauser-Heaton HG Bohlen 2007 Cerebral microvascular dilation during hypotension and decreased oxygen tension: a role for nNOS Am J Physiol Heart Circ Physiol 293 H2193 H2201 10.1152/ajpheart.00190.2007 17630350 10.1152/ajpheart.00190.2007 1:CAS:528:DC%2BD2sXht1WlurnM (Pubitemid 47605862)
5. E Bonilla CE Samitt AF Miranda AP Hays G Salviati S DiMauro LM Kunkel EP Hoffman LP Rowland 1988 Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface Cell 54 447 452 10.1016/0092-8674(88)90065-7 3042151 10.1016/0092-8674(88)90065-7 1:CAS:528:DyaL1cXlsVOnsrw%3D
6. JE Brenman DS Chao H Xia K Aldape DS Bredt 1995 Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy Cell 82 743 752 10.1016/0092-8674(95)90471-9 7545544 10.1016/0092-8674(95)90471-9 1:CAS:528:DyaK2MXotFahu7Y%3D
7. M Cerletti T Negri F Cozzi R Colpo F Andreetta D Croci KE Davies F Cornelio O Pozza G Karpati R Gilbert M Mora 2003 Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer Gene Ther 10 750 757 10.1038/sj.gt.3301941 12704413 10.1038/sj.gt.3301941 1:CAS:528:DC%2BD3sXivFGqtrY%3D (Pubitemid 36621818)
8. WJ Chang ST Iannaccone KS Lau BS Masters TJ McCabe K McMillan RC Padre MJ Spencer JG Tidball JT Stull 1996 Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy Proc Natl Acad Sci USA 93 9142 9147 8799168 10.1073/pnas.93.17.9142 1:CAS:528:DyaK28Xlt1Cntr8%3D (Pubitemid 26282032)
9. CP Cheng K Onishi N Ohte M Suzuki WC Little 1998 Functional effects of endogenous bradykinin in congestive heart failure J Am Coll Cardiol 31 1679 1686 10.1016/S0735-1097(98)00159-4 9626851 10.1016/S0735-1097(98)00159-4 1:CAS:528:DyaK1cXktV2msro%3D (Pubitemid 28273315)
10. V Chetboul C Escriou D Tessier V Richard J-L Pouchelon H Thibault F Lallemand C Thuillez S Blot G Derumeaux 2004 Tissue Doppler imaging detects early asymptomatic myocardial abnormalities in a dog model of Duchenne's cardiomyopathy Eur Heart J 25 1934 1939 10.1016/j.ehj.2004.09.007 15522473 10.1016/j.ehj.2004.09.007 (Pubitemid 39452611)
11. OZ Chi X Liu HR Weiss 2003 Effects of inhibition of neuronal nitric oxide synthase on NMDA-induced changes in cerebral blood flow and oxygen consumption Exp Brain Res 148 256 260 10.1007/s00221-002-1310-7 12520415 1:CAS:528:DC%2BD3sXhs1Kmuw%3D%3D (Pubitemid 36057013)
12. MV Cohen XM Yang GS Liu G Heusch JM Downey 2001 Acetylcholine, bradykinin, opioids, and phenylephrine, but not adenosine, trigger preconditioning by generating free radicals and opening mitochondrial K(ATP) channels Circ Res 89 273 278 10.1161/hh1501.094266 11485978 10.1161/hh1501. 094266 1:CAS:528:DC%2BD3MXmt1Clsbw%3D (Pubitemid 34132686)
13. BJ Cooper NJ Winand H Stedman BA Valentine EP Hoffman LM Kunkel MO Scott KH Fischbeck JN Kornegay RJ Avery 1988 The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs Nature 334 154 156 10.1038/334154a0 3290691 10.1038/334154a0 1:CAS:528:DyaL1cXlt1emsLc%3D
14. EM Van Craenenbroeck VY Hoymans PJ Beckers NM Possemiers K Wuyts BP Paelinck CJ Vrints VM Conraads 2010 Exercise training improves function of circulating angiogenic cells in patients with chronic heart failure Basic Res Cardiol 105 665 676 10.1007/s00395-010-0105-4 20508941 10.1007/s00395-010-0105-4
15. C Dell'Agnola Z Wang R Storb SJ Tapscott CS Kuhr SD Hauschka RS Lee GE Sale E Zellmer S Gisburne J Bogan JN Kornegay BJ Cooper TA Gooley M-T Little 2004 Hematopoietic stem cell transplantation does not restore dystrophin expression in Duchenne muscular dystrophy dogs Blood 104 4311 4318 10.1182/blood-2004-06-2247 15328150 10.1182/blood-2004-06-2247 (Pubitemid 39620188)
16. L Drelicharz V Kozlovski T Skorka S Heinze-Paluchowska A Jasinski A Gebska T Guzik R Olszanecki L Wojnar U Mende G Csanyi S Chlopicki 2008 NO and PGI(2) in coronary endothelial dysfunction in transgenic mice with dilated cardiomyopathy Basic Res Cardiol 103 417 430 10.1007/s00395-008-0723-2 18431525 10.1007/s00395-008-0723-2 1:CAS:528:DC%2BD1cXhtVOgu7vJ
17. T Ehring D Baumgart M Krajcar M Hümmelgen S Kompa G Heusch 1994 Attenuation of myocardial stunning by the ACE inhibitor ramiprilat through a signal cascade of bradykinin and prostaglandins but not nitric oxide Circulation 90 1368 1385 10.1161/01.CIR.90.3.1368 8087948 1:CAS:528:DyaK2cXmslWlu74%3D (Pubitemid 24284460)
18. P Groves S Kurz H Just H Drexler 1995 Role of endogenous bradykinin in human coronary vasomotor control Circulation 92 3424 3430 10.1161/01.CIR.92.12. 3424 8521563 1:STN:280:DyaK287gtlSgtw%3D%3D
19. G Heusch H Post MC Michel M Kelm R Schulz 2000 Endogenous nitric oxide and myocardial adaptation to ischemia Circ Res 87 146 152 10.1161/01.RES.87.2. 146 10903999 1:CAS:528:DC%2BD3cXlt1aiur8%3D (Pubitemid 30616911)
20. EP Hoffman RH Brown LM Kunkel 1987 Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 51 919 928 10.1016/0092-8674(87)90579-4 3319190 10.1016/0092-8674(87)90579-4 1:CAS:528:DyaL1cXntlWqug%3D%3D
21. JM Howell H Lochmüller A O'Hara S Fletcher BA Kakulas B Massie J Nalbantoglu G Karpati 1998 High-level dystrophin expression after adenovirus-mediated dystrophin minigene transfer to skeletal muscle of dystrophic dogs: prolongation of expression with immunosuppression Hum Gene Ther 9 629 634 9551611 10.1089/hum.1998.9.5-629 1:CAS:528:DyaK1cXit1ersbc%3D (Pubitemid 28200619)
22. A Ichihara EW Inscho JD Imig LG Navar 1998 Neuronal nitric oxide synthase modulates rat renal microvascular function Am J Physiol 274 F516 F524 9530268 1:CAS:528:DyaK1cXitVSjtr4%3D
23. A Jalowy R Schulz G Heusch 1998 AT1 receptor blockade in experimental myocardial ischemia/reperfusion Basic Res Cardiol 93 Suppl 2 85 91 9833169 10.1007/s003950050226 1:CAS:528:DyaK1cXntlWrtLc%3D (Pubitemid 28498137)
24. M Koenig EP Hoffman CJ Bertelson AP Monaco C Feener LM Kunkel 1987 Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals Cell 50 509 517 10.1016/0092-8674(87)90504-6 3607877 10.1016/0092-8674(87)90504-6 1:CAS:528:DyaL1cXltVCluw%3D%3D (Pubitemid 18098338)
25. T Miike S Sugino Y Ohtani K Taku K Yoshioka 1987 Vascular endothelial cell injury and platelet embolism in Duchenne muscular dystrophy at the preclinical stage J Neurol Sci 82 67 80 3440873 10.1016/0022-510X(87)90007-4 1:STN:280:DyaL1c7lsV2ltQ%3D%3D (Pubitemid 18001989)
26. JV Mombouli PM Vanhoutte 1995 Kinins and endothelial control of vascular smooth muscle Annu Rev Pharmacol Toxicol 35 679 705 10.1146/annurev.pa.35. 040195.003335 7598512 10.1146/annurev.pa.35.040195.003335 1:CAS:528: DyaK2MXlt1Gqsr0%3D
27. S Moncada A Higgs 1993 The l-arginine-nitric oxide pathway N Engl J Med 329 2002 2012 10.1056/NEJM199312303292706 7504210 10.1056/NEJM199312303292706 1:CAS:528:DyaK2cXhsF2ntrw%3D (Pubitemid 24015045)
28. LA Nikolaidis A Doverspike R Huerbin T Hentosz RP Shannon 2002 Angiotensin-converting enzyme inhibitors improve coronary flow reserve in dilated cardiomyopathy by a bradykinin-mediated, nitric oxide-dependent mechanism Circulation 105 2785 2790 10.1161/01.CIR.0000017433.90061.2E 12057995 10.1161/01.CIR.0000017433.90061.2E 1:CAS:528:DC%2BD38Xlt1yku78%3D (Pubitemid 34615152)
29. RM Palmer DS Ashton S Moncada 1988 Vascular endothelial cells synthesize nitric oxide from l-arginine Nature 333 664 666 10.1038/333664a0 3131684 10.1038/333664a0 1:CAS:528:DyaL1cXktlGktb8%3D
30. A Prasad S Husain W Schenke R Mincemoyer N Epstein AA Quyyumi 2000 Contribution of bradykinin receptor dysfunction to abnormal coronary vasomotion in humans J Am Coll Cardiol 36 1467 1473 10.1016/S0735-1097(00)00892-5 11079644 10.1016/S0735-1097(00)00892-5 1:CAS:528:DC%2BD3cXosFKgs7s%3D
31. M Sampaolesi S Blot G D'Antona N Granger R Tonlorenzi A Innocenzi P Mognol J-L Thibaud BG Galvez I Barthélémy L Perani S Mantero M Guttinger O Pansarasa C Rinaldi MG Cusella De Angelis Y Torrente C Bordignon R Bottinelli G Cossu 2006 Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs Nature 444 574 579 10.1038/nature05282 17108972 10.1038/nature05282 1:CAS:528:DC%2BD28Xht1KjurjO (Pubitemid 44864430)
32. M Sander B Chavoshan SA Harris ST Iannaccone JT Stull GD Thomas RG Victor 2000 Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy Proc Natl Acad Sci USA 97 13818 13823 10.1073/pnas.250379497 11087833 10.1073/pnas.250379497 1:CAS:528:DC%2BD3cXoslynsL8%3D
33. A Schäfer D Fraccarollo S Pförtsch E Loch J Neuser C Vogt J Bauersachs 2011 Clopidogrel improves endothelial function and NO bioavailability by sensitizing adenylyl cyclase in rats with congestive heart failure Basic Res Cardiol 106 485 494 10.1007/s00395-011-0153-4 21287353 10.1007/s00395-011-0153- 4
34. R Schulz M Kelm G Heusch 2004 Nitric oxide in myocardial ischemia/reperfusion injury Cardiovasc Res 61 402 413 10.1016/j.cardiores.2003. 09.019 14962472 10.1016/j.cardiores.2003.09.019 1:CAS:528:DC%2BD2cXhtFWms7k%3D (Pubitemid 38210147)
35. R Schulz H Post C Vahlhaus G Heusch 1998 Ischemic preconditioning in pigs: a graded phenomenon: its relation to adenosine and bradykinin Circulation 98 1022 1029 10.1161/01.CIR.98.10.1022 9737523 1:CAS:528:DyaK1cXmtFKqt7s%3D (Pubitemid 28446656)
36. M Seddon N Melikian R Dworakowski H Shabeeh B Jiang J Byrne B Casadei P Chowienczyk AM Shah 2009 Effects of neuronal nitric oxide synthase on human coronary artery diameter and blood flow in vivo Circulation 119 2656 2662 10.1161/CIRCULATIONAHA.108.822205 19433760 10.1161/CIRCULATIONAHA.108.822205 1:CAS:528:DC%2BD1MXmtVGrurc%3D
37. NJ Sharp JN Kornegay SD Van Camp MH Herbstreith SL Secore S Kettle WY Hung CD Constantinou MJ Dykstra AD Roses 1992 An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy Genomics 13 115 121 1577476 10.1016/0888-7543(92) 90210-J 1:CAS:528:DyaK38XisFentbs%3D
38. JB Su F Barbe B Crozatier DJ Campbell L Hittinger 1999 Increased bradykinin levels accompany the hemodynamic response to acute inhibition of angiotensin-converting enzyme in dogs with heart failure J Cardiovasc Pharmacol 34 700 710 10547087 10.1097/00005344-199911000-00012 1:CAS:528: DyaK1MXntVOht7c%3D (Pubitemid 29491733)
39. JB Su 2006 Kinins and cardiovascular diseases Curr Pharm Des 12 3423 3435 17017936 10.2174/138161206778194051 1:CAS:528:DC%2BD28XpvF2rtLw%3D (Pubitemid 44364129)
40. GD Thomas M Sander KS Lau PL Huang JT Stull RG Victor 1998 Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle Proc Natl Acad Sci USA 95 15090 15095 9844020 10.1073/pnas.95.25.15090 1:CAS:528:DyaK1cXotVGlsLg%3D (Pubitemid 29003761)
41. D Tonduangu L Hittinger B Ghaleh P Le Corvoisier L Sambin S Champagne T Badoual F Vincent A Berdeaux B Crozatier JB Su 2004 Chronic infusion of bradykinin delays the progression of heart failure and preserves vascular endothelium-mediated vasodilation in conscious dogs Circulation 109 114 119 10.1161/01.CIR.0000105726.89770.35 14662711 10.1161/01.CIR.0000105726.89770.35 1:CAS:528:DC%2BD3sXhtVWjtrjL (Pubitemid 38056031)
42. D Townsend I Turner S Yasuda J Martindale J Davis M Shillingford JN Kornegay JM Metzger 2010 Chronic administration of membrane sealant prevents severe cardiac injury and ventricular dilatation in dystrophic dogs J Clin Invest 120 1140 1150 10.1172/JCI41329 20234088 10.1172/JCI41329 1:CAS:528:DC%2BC3cXksVChsLg%3D
43. BA Valentine BJ Cooper A de Lahunta R O'Quinn JT Blue 1988 Canine X-linked muscular dystrophy. An animal model of Duchenne muscular dystrophy: clinical studies J Neurol Sci 88 69 81 3225630 10.1016/0022-510X(88)90206-7 1:STN:280:DyaL1M7ktV2jsA%3D%3D (Pubitemid 19016584)
44. R Weidenbach R Schulz P Gres M Behrends H Post G Heusch 2000 Enhanced reduction of myocardial infarct size by combined ACE inhibition and AT(1)-receptor antagonism Br J Pharmacol 131 138 144 10.1038/sj.bjp.0703544 10960080 10.1038/sj.bjp.0703544 1:CAS:528:DC%2BD3cXmsFKisb8%3D