Cardiac Phosphoproteomics During Remote Ischemic Preconditioning: a Role for the Sarcomeric Z-disk Proteins

Overview

Journal Biomed Res Int

Publisher Wiley

Specialties Biomedical Engineering
Biotechnology
General Medicine

Date 2014 May 6

PMID 24795895

Citations 13

Authors

Safa Abdul-Ghani

Kate J Heesom

Gianni D Angelini

M-Saadeh Suleiman

Affiliations

Soon will be listed here.

Abstract

Remote ischemic preconditioning (RIPC) induced by brief ischemia/reperfusion cycles of remote organ (e.g., limb) is cardioprotective. The myocardial cellular changes during RIPC responsible for this phenomenon are not currently known. The aim of this work was to identify the activation by phosphorylation of cardiac proteins following RIPC. To achieve our aim we used isobaric tandem mass tagging (TMT) and reverse phase nanoliquid chromatography tandem spectrometry using a Linear Trap Quadropole (LTQ) Orbitrap Velos mass spectrometer. Male C57/Bl6 mice were anesthetized by an intraperitoneal injection of Tribromoethanol. A cuff was placed around the hind limb and inflated at 200 mmHg to prevent blood flow as confirmed by Laser Doppler Flowmetry. RIPC was induced by 4 cycles of 5 min of limb ischemia followed by 5 min of reperfusion. Hearts were extracted for phosphoproteomics. We identified approximately 30 phosphoproteins that were differentially expressed in response to RIPC protocol. The levels of several phosphoproteins in the Z-disk of the sarcomere including phospho-myozenin-2 were significantly higher than control. This study describes and validates a novel approach to monitor the changes in the cardiac phosphoproteome following the cardioprotective intervention of RIPC and prior to index ischemia. The increased level of phosphorylated sarcomeric proteins suggests they may have a role in cardiac signaling during RIPC.

Citing Articles

Proteomics of the heart.

Karpov O, Stotland A, Raedschelders K, Chazarin B, Ai L, Murray C Physiol Rev. 2024; 104(3):931-982.

PMID: 38300522 PMC: 11381016. DOI: 10.1152/physrev.00026.2023.

Remote Ischemic Preconditioning induces Cardioprotective Autophagy and Signals through the IL-6-Dependent JAK-STAT Pathway.

Billah M, Ridiandries A, Allahwala U, Mudaliar H, Dona A, Hunyor S Int J Mol Sci. 2020; 21(5).

PMID: 32121587 PMC: 7084188. DOI: 10.3390/ijms21051692.

Perioperative Cardioprotection by Remote Ischemic Conditioning.

Cho Y, Kim W Int J Mol Sci. 2019; 20(19).

PMID: 31569468 PMC: 6801656. DOI: 10.3390/ijms20194839.

Time Series Gene Expression Profiling and Temporal Regulatory Pathway Analysis of Angiotensin II Induced Atrial Fibrillation in Mice.

Wu Y, Han X, Chen C, Zou L, Dong Z, Zhang Y Front Physiol. 2019; 10:597.

PMID: 31191333 PMC: 6548816. DOI: 10.3389/fphys.2019.00597.

Effect of Remote Ischemic Preconditioning on Troponin I in CABG.

Javaherforoosh Zadeh F, Moadeli M, Soltanzadeh M, Janatmakan F Anesth Pain Med. 2018; 7(4):e12549.

PMID: 29430406 PMC: 5797663. DOI: 10.5812/aapm.12549.

References

Vasilyev N, Williams T, Brennan M, Unzek S, Zhou X, Heinecke J . Myeloperoxidase-generated oxidants modulate left ventricular remodeling but not infarct size after myocardial infarction. Circulation. 2005; 112(18):2812-20. DOI: 10.1161/CIRCULATIONAHA.105.542340. View

Hausenloy D, Yellon D . Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res. 2008; 79(3):377-86. DOI: 10.1093/cvr/cvn114. View

Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J . Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol. 2010; 105(5):657-64. DOI: 10.1007/s00395-010-0104-5. View

Redington K, Disenhouse T, Strantzas S, Gladstone R, Wei C, Tropak M . Remote cardioprotection by direct peripheral nerve stimulation and topical capsaicin is mediated by circulating humoral factors. Basic Res Cardiol. 2012; 107(2):241. DOI: 10.1007/s00395-011-0241-5. View

Disatnik M, Buraggi G, Mochly-Rosen D . Localization of protein kinase C isozymes in cardiac myocytes. Exp Cell Res. 1994; 210(2):287-97. DOI: 10.1006/excr.1994.1041. View

Surendra H, Diaz R, Harvey K, Tropak M, Callahan J, Hinek A . Interaction of δ and κ opioid receptors with adenosine A1 receptors mediates cardioprotection by remote ischemic preconditioning. J Mol Cell Cardiol. 2013; 60:142-50. DOI: 10.1016/j.yjmcc.2013.04.010. View

Shao B, Pennathur S, Heinecke J . Myeloperoxidase targets apolipoprotein A-I, the major high density lipoprotein protein, for site-specific oxidation in human atherosclerotic lesions. J Biol Chem. 2012; 287(9):6375-86. PMC: 3307260. DOI: 10.1074/jbc.M111.337345. View

Zhou W, Zeng D, Chen R, Liu J, Yang G, Liu P . Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants. Pediatr Cardiol. 2009; 31(1):22-9. DOI: 10.1007/s00246-009-9536-9. View

Robia S, Ghanta J, Robu V, Walker J . Localization and kinetics of protein kinase C-epsilon anchoring in cardiac myocytes. Biophys J. 2001; 80(5):2140-51. PMC: 1301406. DOI: 10.1016/S0006-3495(01)76187-5. View

10.

Patel H, Moore J, Hsu A, Gross G . Cardioprotection at a distance: mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism. J Mol Cell Cardiol. 2002; 34(10):1317-23. DOI: 10.1006/jmcc.2002.2072. View

11.

Pyle W, Solaro R . At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res. 2004; 94(3):296-305. DOI: 10.1161/01.RES.0000116143.74830.A9. View

12.

Bass-Zubek A, Hobbs R, Amargo E, Garcia N, Hsieh S, Chen X . Plakophilin 2: a critical scaffold for PKC alpha that regulates intercellular junction assembly. J Cell Biol. 2008; 181(4):605-13. PMC: 2386101. DOI: 10.1083/jcb.200712133. View

13.

Geoghegan K, Varghese A, Feng X, Bessire A, Conboy J, Ruggeri R . Deconstruction of activity-dependent covalent modification of heme in human neutrophil myeloperoxidase by multistage mass spectrometry (MS(4)). Biochemistry. 2012; 51(10):2065-77. DOI: 10.1021/bi201872j. View

14.

Hepponstall M, Ignjatovic V, Binos S, Monagle P, Jones B, Cheung M . Remote ischemic preconditioning (RIPC) modifies plasma proteome in humans. PLoS One. 2012; 7(11):e48284. PMC: 3489679. DOI: 10.1371/journal.pone.0048284. View

15.

Weinbrenner C, Nelles M, Herzog N, Sarvary L, Strasser R . Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: a newly identified non-neuronal but PKC-dependent pathway. Cardiovasc Res. 2002; 55(3):590-601. DOI: 10.1016/s0008-6363(02)00446-7. View

16.

Kim N, Lee Y, Kim H, Joo H, Youm J, Park W . Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics. 2006; 6(4):1237-49. DOI: 10.1002/pmic.200500291. View

17.

Thielmann M, Wendt D, Tsagakis K, Price V, Dohle D, Pasa S . Remote ischemic preconditioning: the surgeon's perspective. J Cardiovasc Med (Hagerstown). 2012; 14(3):187-92. DOI: 10.2459/JCM.0b013e3283590df6. View

18.

Ahmed R, Mohamed E, Ashraf M, Maithili S, Nabil F, Rami R . Effect of remote ischemic preconditioning on serum troponin T level following elective percutaneous coronary intervention. Catheter Cardiovasc Interv. 2013; 82(5):E647-53. DOI: 10.1002/ccd.24825. View

19.

Serejo F, Rodrigues Jr L, da Silva Tavares K, Campos de Carvalho A, Nascimento J . Cardioprotective properties of humoral factors released from rat hearts subject to ischemic preconditioning. J Cardiovasc Pharmacol. 2007; 49(4):214-20. DOI: 10.1097/FJC.0b013e3180325ad9. View

20.

Zhang R, Zhao J, Mandveno A, Potter J . Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res. 1995; 76(6):1028-35. DOI: 10.1161/01.res.76.6.1028. View