Journal Article
. 2020 Mar; 18:2.
doi: 10.1186/s12953-020-00158-4.

Comprehensive analysis of the cardiac proteome in a rat model of myocardial ischemia-reperfusion using a TMT-based quantitative proteomic strategy

Sun Ha Lim 1 Jongwon Lee 1 Mee-Jung Han 2 
Affiliations
  • PMID: 32165865
  •     45 References

Abstract

Background: Traditional studies of the cardiac proteome have mainly investigated in an animal model by two-dimensional gel electrophoresis (2-DE). However, the results have not been of satisfactory quality for an understanding of the underlying mechanism. Recent quantitative proteomic methods have been improved to overcome these limitations. To comprehensively study the cardiac proteome in a rat model of ischemia-reperfusion (IR), we developed a tandem mass tag (TMT)-based quantitative proteomic strategy. Furthermore, using this strategy, we examined the molecular mechanisms underlying the prevention of myocardial infarction by the intake of Triticum aestivum L. extract (TALE), a representative dietary fiber grain.

Methods: Cardiac proteomes were analyzed by 2-DE as a gel-based approach, and TMT labeling coupled with two-dimensional liquid chromatography (2D-LC) and tandem mass spectrometry (MS/MS) as a non-gel-based quantitative approach. Additionally, gene ontology annotation was conducted by PANTHER database. Several proteins of interest were verified by a Western blot analysis.

Results: Total 641 proteins were identified commonly from two independent MS datasets using 2D-LC MS/MS. Among these, we identified 151 IR-related proteins that were differentially expressed between the sham-operation group and IR group, comprising 62 up-regulated proteins and 89 down-regulated proteins. Most of the reduced proteins were involved in metabolic processes. In addition, 57 of the IR-related proteins were affected by TALE intake, representing 25 up-regulated proteins and 32 down-regulated proteins. In particular, TALE intake leads to a switch in metabolism to reduce the loss of high-energy phosphates and the accumulation of harmful catabolites (especially reactive oxygen species (ROS)) and to maintain cytoskeleton balance, leading to a reduction in cardiac IR injury.

Conclusions: Our study provides a comprehensive proteome map of IR-related proteins and potential target proteins and identifies mechanisms implicated in the prevention of myocardial infarction by TALE intake in a rat IR model.

Keywords: Cardiac proteome; Dietary fiber; Ischemia; Myocardial infarction; Quantitative proteomics; TMT labeling; Triticum aestivum.

Postconditioning: reduction of reperfusion-induced injury.
Zhi-Qing Zhao, Jakob Vinten-Johansen.
Cardiovasc Res, 2006 Mar 21; 70(2). PMID: 16545349
Review.
Dietary fibre intake and risk of cardiovascular disease: systematic review and meta-analysis.
Diane E Threapleton, Darren C Greenwood, +6 authors, Victoria J Burley.
BMJ, 2013 Dec 21; 347. PMID: 24355537    Free PMC article.
Highly Cited. Systematic Review.
Systematic comparison of label-free, metabolic labeling, and isobaric chemical labeling for quantitative proteomics on LTQ Orbitrap Velos.
Zhou Li, Rachel M Adams, +3 authors, Chongle Pan.
J Proteome Res, 2011 Dec 23; 11(3). PMID: 22188275
Highly Cited.
Plant-based foods containing cell wall polysaccharides rich in specific active monosaccharides protect against myocardial injury in rat myocardial infarction models.
Sun Ha Lim, Yaesil Kim, +4 authors, Jongwon Lee.
Sci Rep, 2016 Dec 09; 6. PMID: 27929093    Free PMC article.
Sub-proteomic fractionation, iTRAQ, and OFFGEL-LC-MS/MS approaches to cardiac proteomics.
Chad M Warren, David L Geenen, +2 authors, R John Solaro.
J Proteomics, 2010 Apr 17; 73(8). PMID: 20394843    Free PMC article.
Novel therapeutic strategies for ischemic heart disease.
Adam J Perricone, Richard S Vander Heide.
Pharmacol Res, 2014 Sep 07; 89. PMID: 25193582    Free PMC article.
Review.
Cardiovascular remodelling in coronary artery disease and heart failure.
Gerd Heusch, Peter Libby, +4 authors, Lionel Opie.
Lancet, 2014 May 17; 383(9932). PMID: 24831770    Free PMC article.
Highly Cited. Review.
Simvastatin reduces myocardial infarct size via increased nitric oxide production in normocholesterolemic rabbits.
Narentuoya Bao, Hiroaki Ushikoshi, +11 authors, Shinya Minatoguchi.
J Cardiol, 2009 Jan 27; 53(1). PMID: 19167645
Neuroprotective effects of Triticum aestivum L. against beta-amyloid-induced cell death and memory impairments.
Jung-Hee Jang, Chang-Yul Kim, +5 authors, Jongwon Lee.
Phytother Res, 2009 May 15; 24(1). PMID: 19441012
Biochemical dysfunction in heart mitochondria exposed to ischaemia and reperfusion.
Giancarlo Solaini, David A Harris.
Biochem J, 2005 Aug 20; 390(Pt 2). PMID: 16108756    Free PMC article.
Review.
Overview: the maturing of proteomics in cardiovascular research.
Jennifer E Van Eyk.
Circ Res, 2011 Feb 22; 108(4). PMID: 21335431    Free PMC article.
Review.
Myocardial ischemia: current concepts and future perspectives.
Hiroaki Shimokawa, Satoshi Yasuda.
J Cardiol, 2008 Oct 17; 52(2). PMID: 18922380
Review.
Apple pectin, a dietary fiber, ameliorates myocardial injury by inhibiting apoptosis in a rat model of ischemia/reperfusion.
Sun Ha Lim, Mi Young Kim, Jongwon Lee.
Nutr Res Pract, 2014 Aug 12; 8(4). PMID: 25110558    Free PMC article.
Proteomic analysis of right and left cardiac ventricles under aerobic conditions and after ischemia/reperfusion.
Virgilio J J Cadete, Han-bin Lin, +2 authors, Grzegorz Sawicki.
Proteomics, 2012 Jun 12; 12(14). PMID: 22685060
Neuroproteome changes after ischemia/reperfusion injury and tissue plasminogen activator administration in rats: a quantitative iTRAQ proteomics study.
Zamir Merali, Meah MingYang Gao, +3 authors, Andrea Kassner.
PLoS One, 2014 Jun 01; 9(5). PMID: 24879061    Free PMC article.
Can Co-Activation of Nrf2 and Neurotrophic Signaling Pathway Slow Alzheimer's Disease?
Kelsey E Murphy, Joshua J Park.
Int J Mol Sci, 2017 Jun 01; 18(6). PMID: 28561773    Free PMC article.
Review.
Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction.
Noriyuki Kioka, Kazumitsu Ueda, Teruo Amachi.
Cell Struct Funct, 2002 Apr 09; 27(1). PMID: 11937713
Review.
The physiological role of cardiac cytoskeleton and its alterations in heart failure.
Vasco Sequeira, Louise L A M Nijenkamp, Jessica A Regan, Jolanda van der Velden.
Biochim Biophys Acta, 2013 Jul 19; 1838(2). PMID: 23860255
Review.
Elucidation of thioredoxin target protein networks in mouse.
Cexiong Fu, Changgong Wu, +4 authors, Hong Li.
Mol Cell Proteomics, 2009 May 07; 8(7). PMID: 19416943    Free PMC article.
Cross Talk between Two Antioxidant Systems, Thioredoxin and DJ-1: Consequences for Cancer.
Prahlad V Raninga, Giovanna Di Trapani, Kathryn F Tonissen.
Oncoscience, 2015 Jan 17; 1(1). PMID: 25593990    Free PMC article.
Review.
Large-scale analysis of the yeast proteome by multidimensional protein identification technology.
M P Washburn, D Wolters, J R Yates.
Nat Biotechnol, 2001 Mar 07; 19(3). PMID: 11231557
Highly Cited.
Intravenous administration of adenosine triphosphate disodium during primary percutaneous coronary intervention attenuates the transient rapid improvement of myocardial wall motion, not myocardial stunning, shortly after recanalization in acute anterior myocardial infarction.
Takehito Tokuyama, Tadamichi Sakuma, +12 authors, Yasuhiko Hayashi.
J Cardiol, 2009 Sep 29; 54(2). PMID: 19782267
Proteomic studies on protective effects of salvianolic acids, notoginsengnosides and combination of salvianolic acids and notoginsengnosides against cardiac ischemic-reperfusion injury.
Qing-Xi Yue, Fu-Bo Xie, +6 authors, De-An Guo.
J Ethnopharmacol, 2011 Sep 10; 141(2). PMID: 21903157
Deciphering Clostridium tyrobutyricum Metabolism Based on the Whole-Genome Sequence and Proteome Analyses.
Joungmin Lee, Yu-Sin Jang, +2 authors, Sang Yup Lee.
mBio, 2016 Jun 16; 7(3). PMID: 27302759    Free PMC article.
YADA: a tool for taking the most out of high-resolution spectra.
Paulo C Carvalho, Tao Xu, +3 authors, John R Yates.
Bioinformatics, 2009 Aug 18; 25(20). PMID: 19684088    Free PMC article.
Metabolic adaptation to a disruption in oxygen supply during myocardial ischemia and reperfusion is underpinned by temporal and quantitative changes in the cardiac proteome.
Xin Li, Fatih Arslan, +7 authors, Siu Kwan Sze.
J Proteome Res, 2012 Feb 23; 11(4). PMID: 22352837
Effect of duration of ischemia on myocardial proteome in ischemia/reperfusion injury.
Justyna Fert-Bober, Rasphal S Basran, Jolanta Sawicka, Grzegorz Sawicki.
Proteomics, 2008 Jun 20; 8(12). PMID: 18563752
Models, Regulations, and Functions of Microtubule Severing by Katanin.
Debasish Kumar Ghosh, Debdeep Dasgupta, Abhishek Guha.
ISRN Mol Biol, 2012 Jan 01; 2012. PMID: 27335666    Free PMC article.
Review.
DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics.
David L Tabb, W Hayes McDonald, John R Yates.
J Proteome Res, 2003 Mar 20; 1(1). PMID: 12643522    Free PMC article.
Highly Cited.
Reperfusion therapy for acute myocardial infarction: Concepts and controversies from inception to acceptance.
Klaus Peter Rentrop, Frederick Feit.
Am Heart J, 2015 Nov 07; 170(5). PMID: 26542507
Review.
Water extract of Triticum aestivum L. and its components demonstrate protective effect in a model of vascular dementia.
Hyung Soo Han, Jung-Hee Jang, +6 authors, Jongwon Lee.
J Med Food, 2010 Jun 05; 13(3). PMID: 20521983
Metabolic Modulators in Heart Disease: Past, Present, and Future.
Gary D Lopaschuk.
Can J Cardiol, 2017 Mar 11; 33(7). PMID: 28279520
Highly Cited. Review.
Two-dimensional differential gel electrophoresis of rat heart proteins in ischemia and ischemia-reperfusion.
Jun Sakai, Hironori Ishikawa, +3 authors, Masaharu Kanaoka.
Methods Mol Biol, 2006 Dec 19; 357. PMID: 17172676
Characterization of the molecular mechanisms underlying increased ischemic damage in the aldehyde dehydrogenase 2 genetic polymorphism using a human induced pluripotent stem cell model system.
Antje D Ebert, Kazuki Kodo, +12 authors, Joseph C Wu.
Sci Transl Med, 2014 Sep 26; 6(255). PMID: 25253673    Free PMC article.
Comparative analysis of envelope proteomes in Escherichia coli B and K-12 strains.
Mee-Jung Han, Sang Yup Lee, Soon Ho Hong.
J Microbiol Biotechnol, 2012 Apr 27; 22(4). PMID: 22534293
The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy.
Fedik Rahimov, Louis M Kunkel.
J Cell Biol, 2013 May 15; 201(4). PMID: 23671309    Free PMC article.
Highly Cited. Review.
Gelsolin: the tail of a molecular gymnast.
Shalini Nag, Mårten Larsson, Robert C Robinson, Leslie D Burtnick.
Cytoskeleton (Hoboken), 2013 Jun 12; 70(7). PMID: 23749648
Review.
Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data.
Alan D Lopez, Colin D Mathers, +2 authors, Christopher J L Murray.
Lancet, 2006 May 30; 367(9524). PMID: 16731270
Highly Cited.
Complement factor H binds malondialdehyde epitopes and protects from oxidative stress.
David Weismann, Karsten Hartvigsen, +12 authors, Christoph J Binder.
Nature, 2011 Oct 08; 478(7367). PMID: 21979047    Free PMC article.
Highly Cited.
Methanol Extract of Cassia mimosoides var. nomame Attenuates Myocardial Injury by Inhibition of Apoptosis in a Rat Model of Ischemia-Reperfusion.
Sun Ha Lim, Jongwon Lee.
Prev Nutr Food Sci, 2012 Sep 01; 17(3). PMID: 24471081    Free PMC article.
The interactome of LIM domain proteins: the contributions of LIM domain proteins to heart failure and heart development.
Amy Li, Fredrik Ponten, Cristobal G dos Remedios.
Proteomics, 2012 Jan 19; 12(2). PMID: 22253135
Review.
The nebulin repeat protein Lasp regulates I-band architecture and filament spacing in myofibrils.
Isabelle Fernandes, Frieder Schöck.
J Cell Biol, 2014 Aug 13; 206(4). PMID: 25113030    Free PMC article.
Characterization of breast cancer interstitial fluids by TmT labeling, LTQ-Orbitrap Velos mass spectrometry, and pathway analysis.
Cinzia Raso, Carlo Cosentino, +11 authors, John R Yates.
J Proteome Res, 2012 May 09; 11(6). PMID: 22563702    Free PMC article.
Dietary fiber intake and reduced risk of coronary heart disease in US men and women: the National Health and Nutrition Examination Survey I Epidemiologic Follow-up Study.
Lydia A Bazzano, Jiang He, +3 authors, National Health and Nutrition Examination Survey I Epidemiologic Follow-up Study.
Arch Intern Med, 2003 Sep 10; 163(16). PMID: 12963562
Mitochondria as a drug target in ischemic heart disease and cardiomyopathy.
Andrew M Walters, George A Porter, Paul S Brookes.
Circ Res, 2012 Oct 16; 111(9). PMID: 23065345    Free PMC article.
Highly Cited. Review.