Effect of Aerobic Exercise on Protein Expression in Muscle of Obese Mexican Adolescents: A Proteomic and Bioinformatic Analysis — Oak Academic Publishing
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Effect of Aerobic Exercise on Protein Expression in Muscle of Obese Mexican Adolescents: A Proteomic and Bioinformatic Analysis
Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
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Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
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Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
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Departmento de Ciencias Aplicadas al Trabajo, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
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Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
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Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
1 Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
2 Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
3 Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
4 Departmento de Ciencias Aplicadas al Trabajo, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
5 Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
6 Departmento de Ciencias Médicas, División de Ciencias de la Salud, Universidad de Guanajuato, León, México
The beneficial effects of exercise have been recognized for many years yet the molecular mechanisms by which exercise show benefits on health are still elusive. A combination of experimental and bioinformatics approaches can be an invaluable tool to increase the cellular understanding of the molecular mechanisms that underlie the aerobic exercise in obese adolescents. Muscle skeletal proteins were separated by 2D-PAGE and changes in protein expression were revealed by ImageMaster 2D Platinum analysis software. Proteins with expression changes after aerobic exercise were identified by comparison with 2D maps from SWISS-2DPAGE and interactions of proteins were analyzed with STRING and DAVID databases. After aerobic exercise, all participants decreased glucose, insulin, total cholesterol, body mass index and waist circumference. Proteomic differential analysis revealed 10 overexpressed proteins after aerobic training, which correspond to carbonic anhydrase III, beta enolase, creatine kinase, ATP synthase beta subunit, aldolase A, glyceraldehyde-3-phosphate dehydrogenase, triosephosphate isomerase, pyruvate kinase, lactate dehydrogenase and adenylate kinase. Exercise increased glycolysis and oxidative phosphorylation pathways, which is likely to be regulated by ubiquitin c protein. In conclusion, our analysis suggested that obese adolescents show changes in their body mass index, waist circumference and serum glucose after aerobic exercise through improved protein expression patterns that aid, especially, glucose metabolism and increase the oxidative phosphorylation. The most likely explanation for the observed pattern is that ubiquitin c protein keeps the glycolytic enzymes bound within skeletal muscle, obtaining a non-degradative role in cell signaling.
KeywordsGlycolysisOxidative PhosphorylationUbiquitin C ProteinProteomicsExercise
Weinstein, A.R., Sesso, H.D., Lee, I.M., Cook, N.R., Manson, J.E., Buring, J.E. and Gaziano, J.M. (2004) Relationship of Physical Activity vs Body Mass Index with Type 2 Diabetes in Women. The Journal of the American Medical Association, 292, 1188-1194. http://dx.doi.org/10.1001/jama.292.10.1188
Civitarese, A.E. and Ravussin, E. (2008) Mitochondrial Energetics and Insulin Resistance. Endocrinology, 149, 950954. http://dx.doi.org/10.1210/en.2007-1444
Winder, W.W. and Hardie, D.G. (1999) AMP-Activated Protein Kinase, a Metabolic Master Switch: Possible Roles in Type 2 Diabetes. The American Journal of Physiology, 277, E1-10.
Short, K.R., Vittone, J.L., Bigelow, M.L., Proctor, D.N., Rizza, R.A., Coenen-Schimke, J.M. and Nair, K.S. (2003) Impact of Aerobic Exercise Training on Age-Related Changes in Insulin Sensitivity and Muscle Oxidative Capacity. Diabetes, 52, 1888-1896. http://dx.doi.org/10.2337/diabetes.52.8.1888
Lee, S., Kuk, J.L., Davidson, L.E., Hudson, R., Kilpatrick, K., Graham, T.E. and Ross, R. (2005) Exercise without Weight Loss Is an Effective Strategy for Obesity Reduction in Obese Individuals with and without Type 2 Diabetes. Journal of Applied Physiology, 99, 1220-1225. http://dx.doi.org/10.1152/japplphysiol.00053.2005
Ross, R., Janssen, I., Dawson, J., Kungl, A.M., Kuk, J.L., Wong, S.L., Nguyen-Duy, T.B., Lee, S., Kilpatrick, K. and Hudson, R. (2004) Exercise-Induced Reduction in Obesity and Insulin Resistance in Women: A Randomized Controlled Trial. Obesity Research, 12, 789-798. http://dx.doi.org/10.1038/oby.2004.95
Ferguson, M.A., Gutin, B., Le, N.A., Karp, W., Litaker, M., Humphries, M., Okuyama, T., Riggs, S. and Owens, S. (1999) Effects of Exercise Training and Its Cessation on Components of the insulin Resistance Syndrome in Obese Children. International Journal of Obesity and Related Metabolic Disorders, 23, 889-895. http://dx.doi.org/10.1038/sj.ijo.0800968
Macias-Cervantes, M.H., Malacara, J.M., Garay-Sevilla, M.E. and Diaz-Cisneros, F.J. (2009) Effect of Recreational Physical Activity on Insulin Levels in Mexican/Hispanic Children. European Journal of Pediatrics, 168, 1195-1202. http://dx.doi.org/10.1007/s00431-008-0907-7
LeBlanc, P.J., Peters, S.J., Tunstall, R.J., Cameron-Smith, D. and Heigenhauser, G.J. (2004) Effects of Aerobic Training on Pyruvate Dehydrogenase and Pyruvate Dehydrogenase Kinase in Human Skeletal Muscle. The Journal of Physiology, 557, 559-570. http://dx.doi.org/10.1113/jphysiol.2003.058263
Park, H., Kaushik, V.K., Constant, S., Prentki, M., Przybytkowski, E., Ruderman, N.B. and Saha, A.K. (2002) Coordinate Regulation of Malonyl-CoA Decarboxylase, Snglycerol-3-Phosphate Acyltransferase, and Acetyl-CoA Carboxylase by AMP-Activated Protein Kinase in Rat Tissues in Response to Exercise. The Journal of Biological Chemistry, 277, 32571-32577. http://dx.doi.org/10.1074/jbc.M201692200
Green, H.J., Bombardier, E.B., Duhamel, T.A., Holloway, G.P., Tupling, A.R. and Ouyang, J. (2008) Acute Responses in Muscle Mitochondrial and Cytosolic Enzyme Activities during Heavy Intermittent Exercise. Journal of Applied Physiology, 104, 931-937. http://dx.doi.org/10.1152/japplphysiol.01151.2007
Hittel, D.S., Hathout, Y. and Hoffman, E.P. (2007) Proteomics and Systems Biology in Exercise and Sport Sciences Research. Exercise and Sport Sciences Reviews, 35, 5-11. http://dx.doi.org/10.1097/jes.0b013e31802d744a
Cole, T.J., Bellizzi, M.C., Flegal, K.M. and Dietz, W.H. (2000) Establishing a Standard Definition for Child Overweight and Obesity Worldwide: International Survey. BMJ, 320, 1240-1243. http://dx.doi.org/10.1136/bmj.320.7244.1240
Rosas, M., Pastelin, G., Vargas-Alarcon, G., Martinez-Reding, J., Lomeli, C., Mendoza-Gonzalez, C., Lorenzo, J.A., Mendez, A., Franco, M., Sanchez-Lozada, L.G., Verdejo, J., Sanchez, N., Ruiz, R., Ferez-Santander, S.M., Attie, F., (2008) Clinical Guidelines for Detection, Prevention, Diagnosis and Treatment of Systemic Arterial Hypertension in Mexico. Archivos de Cardiologia de Mexico, 78, S2-5-57.
Jackson, A.S. and Pollock, M.L. (1985) Practical Assessment of Body Composition. Physician Sport Medicine, 13, 76-90.
Pollock, M.L., Bohannon, R.L., Cooper, K.H., Ayres, J.J., Ward, A., White, S.R. and Linnerud, A.C. (1976) A Comparative Analysis of Four Protocols for Maximal Treadmill Stress Testing. American Heart Journal, 92, 39-46. http://dx.doi.org/10.1016/S0002-8703(76)80401-2
Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., Lin, J., Minguez, P., Bork, P., von Mering, C. and Jensen, L.J. (2013) STRING v9.1: Protein-Protein Interaction Networks, with Increased Coverage and Integration. Nucleic Acids Research, 41, D808-815. http://dx.doi.org/10.1093/nar/gks1094
Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and Integrative Analysis of Large Gene Lists Using DAVID Bioinformatics Resources. Nature Protocols, 4, 44-57.
Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Bioinformatics Enrichment Tools: Paths toward the Comprehensive Functional Analysis of Large Gene Lists. Nucleic Acids Research, 37, 1-13. http://dx.doi.org/10.1093/nar/gkn923
Komander, D. (2009) The Emerging Complexity of Protein Ubiquitination. Biochemical Society Transactions, 37, 937953. http://dx.doi.org/10.1042/BST0370937
Hody, S., Leprince, P., Sergeant, K., Renaut, J., Croisier, J.L., Wang, F. and Rogister, B. (2011) Human Muscle Proteome Modifications after Acute or Repeated Eccentric Exercises. Medicine and Science in Sports and Exercise, 43, 2281-2296. http://dx.doi.org/10.1249/MSS.0b013e318222edf3
Egan, B., Dowling, P., O’Connor, P. L., Henry, M., Meleady, P., Zierath, J. R. and O’Gorman, D.J. (2011) 2-D DIGE Analysis of the Mitochondrial Proteome from Human Skeletal Muscle Reveals Time Course-Dependent Remodelling in Response to 14 Consecutive Days of Endurance Exercise Training. Proteomics, 11, 1413-1428. http://dx.doi.org/10.1002/pmic.201000597
Gondin, J., Brocca, L., Bellinzona, E., D’Antona, G., Maffiuletti, N. A., Miotti, D., Pellegrino, M. A., and Bottinelli, R. (2011) Neuromuscular Electrical Stimulation Training Induces Atypical Adaptations of the Human Skeletal Muscle Phenotype: A Functional and Proteomic Analysis. Journal of Applied Physiology, 110, 433-450. http://dx.doi.org/10.1152/japplphysiol.00914.2010
Shang, X., Chen, S., Ren, H., Li, Y. and Huang, H. (2009) Carbonic Anhydrase III: The New Hope for the Elimination of Exercise-Induced Muscle Fatigue. Medical Hypotheses, 72, 427-429. http://dx.doi.org/10.1016/j.mehy.2008.10.027
Janssen, E., Terzic, A., Wieringa, B. and Dzeja, P.P. (2003) Impaired Intracellular Energetic Communication in Muscles from Creatine Kinase and Adenylate Kinase (M-CK/AK1) Double Knock-Out Mice. The Journal of Biological Chemistry, 278, 30441-30449. http://dx.doi.org/10.1074/jbc.M303150200
Dzeja, P.P. and Terzic, A. (2003) Phosphotransfer Networks and Cellular Energetics. The Journal of Experimental Biology, 206, 2039-2047. http://dx.doi.org/10.1242/jeb.00426
Hojlund, K., Wrzesinski, K., Larsen, P.M., Fey, S.J., Roepstorff, P., Handberg, A., Dela, F., Vinten, J., McCormack, J. G., Reynet, C. and Beck-Nielsen, H. (2003) Proteome Analysis Reveals Phosphorylation of ATP Synthase Beta-Subunit In human Skeletal Muscle and Proteins with Potential Roles in Type 2 Diabetes. The Journal of Biological Chemistry, 278, 10436-10442. http://dx.doi.org/10.1074/jbc.M212881200
Gonzalez, B., Hernando, R. and Manso, R. (2000) Stress Proteins of 70 kDa in Chronically Exercised Skeletal Muscle. European Journal of Physiology, 440, 42-49.
Gaster, M., Staehr, P., Beck-Nielsen, H., Schroder, H.D. and Handberg, A. (2001) GLUT4 Is Reduced in Slow Muscle Fibers of Type 2 Diabetic Patients: Is Insulin Resistance in Type 2 Diabetes a Slow, Type 1 Fiber Disease? Diabetes, 50, 1324-1329. http://dx.doi.org/10.2337/diabetes.50.6.1324
Ye, Y., Blaser, G., Horrocks, M.H., Ruedas-Rama, M.J., Ibrahim, S., Zhukov, A.A., Orte, A., Klenerman, D., Jackson, S.E. and Komander, D. (2012) Ubiquitin Chain Conformation Regulates Recognition and Activity of Interacting Proteins. Nature, 492, 266-270. http://dx.doi.org/10.1038/nature11722