Literature DB >> 21834687

Disruption of caveolae blocks ischemic preconditioning-mediated S-nitrosylation of mitochondrial proteins.

Junhui Sun1, Mark J Kohr, Tiffany Nguyen, Angel M Aponte, Patricia S Connelly, Shervin G Esfahani, Marjan Gucek, Mathew P Daniels, Charles Steenbergen, Elizabeth Murphy.   

Abstract

AIMS: Nitric oxide (NO) and protein S-nitrosylation (SNO) play important roles in ischemic preconditioning (IPC)-induced cardioprotection. Mitochondria are key regulators of preconditioning, and most proteins showing an increase in SNO with IPC are mitochondrial. The aim of this study was to address how IPC transduces NO/SNO signaling to mitochondria in the heart.
RESULTS: In this study using Langendorff perfused mouse hearts, we found that IPC-induced cardioprotection was blocked by treatment with either N-nitro-L-arginine methyl ester (L-NAME, a constitutive NO synthase inhibitor), ascorbic acid (a reducing agent to decompose SNO), or methyl-?-cyclodextrin (M?CD, a cholesterol sequestering agent to disrupt caveolae). IPC not only activated AKT/eNOS signaling but also led to translocation of eNOS to mitochondria. M?CD treatment disrupted caveolar structure, leading to dissociation of eNOS from caveolin-3 and blockade of IPC-induced activation of the AKT/eNOS signaling pathway. A significant increase in mitochondrial SNO was found in IPC hearts compared to perfusion control, and the disruption of caveolae by M?CD treatment not only abolished IPC-induced cardioprotection, but also blocked the IPC-induced increase in SNO. INNOVATION: These results provide mechanistic insight into how caveolae/eNOS/NO/SNO signaling mediates cardioprotection induced by IPC.
CONCLUSION: Altogether these results suggest that caveolae transduce eNOS/NO/SNO cardioprotective signaling in the heart.

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Year:  2011        PMID: 21834687      PMCID: PMC3218381          DOI: 10.1089/ars.2010.3844

Source DB:  PubMed          Journal:  Antioxid Redox Signal        ISSN: 1523-0864            Impact factor:   8.401


  41 in total

1.  Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells.

Authors:  Nikolaos A Maniatis; Viktor Brovkovych; Scott E Allen; Theresa A John; Ayesha N Shajahan; Chinnaswamy Tiruppathi; Stephen M Vogel; Randal A Skidgel; Asrar B Malik; Richard D Minshall
Journal:  Circ Res       Date:  2006-09-14       Impact factor: 17.367

Review 2.  Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies.

Authors:  Michael V Cohen; Xi-Ming Yang; James M Downey
Journal:  Cardiovasc Res       Date:  2005-12-27       Impact factor: 10.787

Review 3.  Preconditioning: the mitochondrial connection.

Authors:  Elizabeth Murphy; Charles Steenbergen
Journal:  Annu Rev Physiol       Date:  2007       Impact factor: 19.318

Review 4.  The multiple faces of caveolae.

Authors:  Robert G Parton; Kai Simons
Journal:  Nat Rev Mol Cell Biol       Date:  2007-03       Impact factor: 94.444

5.  Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking.

Authors:  Yasuko Iwakiri; Ayano Satoh; Suvro Chatterjee; Derek K Toomre; Cecile M Chalouni; David Fulton; Roberto J Groszmann; Vijay H Shah; William C Sessa
Journal:  Proc Natl Acad Sci U S A       Date:  2006-12-14       Impact factor: 11.205

6.  Nitric oxide synthase in cardiac sarcoplasmic reticulum.

Authors:  K Y Xu; D L Huso; T M Dawson; D S Bredt; L C Becker
Journal:  Proc Natl Acad Sci U S A       Date:  1999-01-19       Impact factor: 11.205

Review 7.  Caveolae and lipid rafts: G protein-coupled receptor signaling microdomains in cardiac myocytes.

Authors:  Paul A Insel; Brian P Head; Rennolds S Ostrom; Hemal H Patel; James S Swaney; Chih-Min Tang; David M Roth
Journal:  Ann N Y Acad Sci       Date:  2005-06       Impact factor: 5.691

8.  Protection of adult rat cardiac myocytes from ischemic cell death: role of caveolar microdomains and delta-opioid receptors.

Authors:  Hemal H Patel; Brian P Head; Heidi N Petersen; Ingrid R Niesman; Diane Huang; Garrett J Gross; Paul A Insel; David M Roth
Journal:  Am J Physiol Heart Circ Physiol       Date:  2006-02-24       Impact factor: 4.733

Review 9.  The ubiquitous role of nitric oxide in cardioprotection.

Authors:  Steven P Jones; Roberto Bolli
Journal:  J Mol Cell Cardiol       Date:  2005-11-08       Impact factor: 5.000

Review 10.  Caveolins and the regulation of endothelial nitric oxide synthase in the heart.

Authors:  Olivier Feron; Jean-Luc Balligand
Journal:  Cardiovasc Res       Date:  2006-03-01       Impact factor: 10.787

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  35 in total

Review 1.  Sarcolemmal dependence of cardiac protection and stress-resistance: roles in aged or diseased hearts.

Authors:  Louise E See Hoe; Lauren T May; John P Headrick; Jason N Peart
Journal:  Br J Pharmacol       Date:  2016-09-09       Impact factor: 8.739

2.  Sarcolemmal cholesterol and caveolin-3 dependence of cardiac function, ischemic tolerance, and opioidergic cardioprotection.

Authors:  Louise E See Hoe; Jan M Schilling; Emiri Tarbit; Can J Kiessling; Anna R Busija; Ingrid R Niesman; Eugene Du Toit; Kevin J Ashton; David M Roth; John P Headrick; Hemal H Patel; Jason N Peart
Journal:  Am J Physiol Heart Circ Physiol       Date:  2014-07-25       Impact factor: 4.733

3.  Netrin-1 abrogates ischemia/reperfusion-induced cardiac mitochondrial dysfunction via nitric oxide-dependent attenuation of NOX4 activation and recoupling of NOS.

Authors:  Kin Lung Siu; Christopher Lotz; Peipei Ping; Hua Cai
Journal:  J Mol Cell Cardiol       Date:  2014-07-24       Impact factor: 5.000

4.  Power Grid Protection of the Muscle Mitochondrial Reticulum.

Authors:  Brian Glancy; Lisa M Hartnell; Christian A Combs; Armel Femnou; Junhui Sun; Elizabeth Murphy; Sriram Subramaniam; Robert S Balaban
Journal:  Cell Rep       Date:  2017-04-18       Impact factor: 9.423

Review 5.  S-nitrosylation: specificity, occupancy, and interaction with other post-translational modifications.

Authors:  Alicia M Evangelista; Mark J Kohr; Elizabeth Murphy
Journal:  Antioxid Redox Signal       Date:  2013-01-04       Impact factor: 8.401

Review 6.  Signaling epicenters: the role of caveolae and caveolins in volatile anesthetic induced cardiac protection.

Authors:  Yousuke T Horikawa; Yasuo M Tsutsumi; Hemal H Patel; David M Roth
Journal:  Curr Pharm Des       Date:  2014       Impact factor: 3.116

7.  Postconditioning leads to an increase in protein S-nitrosylation.

Authors:  Guang Tong; Angel M Aponte; Mark J Kohr; Charles Steenbergen; Elizabeth Murphy; Junhui Sun
Journal:  Am J Physiol Heart Circ Physiol       Date:  2014-01-17       Impact factor: 4.733

8.  Cardioprotective Role of Caveolae in Ischemia-Reperfusion Injury.

Authors:  Junhui Sun; Tiffany Nguyen; Mark J Kohr; Elizabeth Murphy
Journal:  Transl Med (Sunnyvale)       Date:  2013-09-16

9.  Pivotal role of mTORC2 and involvement of ribosomal protein S6 in cardioprotective signaling.

Authors:  Toshiyuki Yano; Marcella Ferlito; Angel Aponte; Atsushi Kuno; Tetsuji Miura; Elizabeth Murphy; Charles Steenbergen
Journal:  Circ Res       Date:  2014-02-20       Impact factor: 17.367

10.  Essential role of nitric oxide in acute ischemic preconditioning: S-nitros(yl)ation versus sGC/cGMP/PKG signaling?

Authors:  Junhui Sun; Angel M Aponte; Mark J Kohr; Guang Tong; Charles Steenbergen; Elizabeth Murphy
Journal:  Free Radic Biol Med       Date:  2012-09-16       Impact factor: 7.376

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