Proteomics applied to exercise physiology: A cutting-edge technology

Journal of Cellular Physiology

Volumn 227, Issue 3, 2012, Pages 885-898

  Petriz, Bernardo A ^a   Gomes, Clarissa P ^a   Rocha, Luiz A O ^a,b   Rezende, Taia M B ^a   Franco, Octávio L ^a,b,c  

^a UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

^b UNIVERSITY OF BRASILIA   (Brazil)

^c FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN; PROTEOME;

EXERCISE PHYSIOLOGY; HEART; HUMAN; ISOELECTRIC FOCUSING; MASS SPECTROMETRY; MUSCLE FUNCTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEOMICS; REVIEW; SKELETAL MUSCLE; TECHNOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ATHLETIC PERFORMANCE; EXERCISE; HUMANS; PROTEOMICS;

EID: 84155192359     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22809     Document Type: Review

References (155)

1. Aebersold R, Mann M. 2003. Mass spectrometry-based proteomics. Nature 422: 198-207.
2. Babiychuk EB, Draeger A. 2006. Biochemical characterization of detergent-resistant membranes: A systematic approach. Biochem J 397: 407-416.
3. Baicu SC, Taylor MJ. 2002. Acid-base buffering in organ preservation solutions as a function of temperature: New parameters for comparing buffer capacity and efficiency. Cryobiology 45: 33-48.
4. Bansal A, Dai Q, Chiao YA, Hakala KW, Zhang JQ, Weintraub ST, Lindsey ML. 2010. Proteomic analysis reveals late exercise effects on cardiac remodeling following myocardial infarction. J Proteomics 73: 2041-2049.
5. Bertile F, Schaeffer C, Le Maho Y, Raclot T, Van Dorsselaer A. 2009. A proteomic approach to identify differentially expressed plasma proteins between the fed and prolonged fasted states. Proteomics 9: 148-158.
6. Bhuyan AK. 2010. On the mechanism of SDS-induced protein denaturation. Biopolymers 93: 186-199.
7. Bjellqvist B, Ek K, Righetti PG, Gianazza E, Gorg A, Westermeier R, Postel W. 1982. Isoelectric focusing in immobilized pH gradients: Principle, methodology and some applications. J Biochem Biophys Methods 6: 317-339.
8. Bogdanov B, Smith RD. 2005. Proteomics by FTICR mass spectrometry: Top down and bottom up. Mass Spectrom Rev 24: 168-200.
9. Boluyt MO, Brevick JL, Rogers DS, Randall MJ, Scalia AF, Li ZB. 2006. Changes in the rat heart proteome induced by exercise training: Increased abundance of heat shock protein hsp20. Proteomics 6: 3154-3169.
10. Booth FW, Thomason DB. 1991. Molecular and cellular adaptation of muscle in response to exercise: Perspectives of various models. Physiol Rev 71: 541-585.
11. Burniston JG. 2008. Changes in the rat skeletal muscle proteome induced by moderate-intensity endurance exercise. Biochim Biophys Acta 1784: 1077-1086.
12. Burniston JG. 2009. Adaptation of the rat cardiac proteome in response to intensity-controlled endurance exercise. Proteomics 9: 106-115.
13. Byrne JC, Downes MR, O'Donoghue N, O'Keane C, O'Neill A, Fan Y, Fitzpatrick JM, Dunn M, Watson RW. 2009. 2D-DIGE as a strategy to identify serum markers for the progression of prostate cancer. J Proteome Res 8: 942-957.
14. Canas B, Pineiro C, Calvo E, Lopez-Ferrer D, Gallardo JM. 2007. Trends in sample preparation for classical and second generation proteomics. J Chromatogr A 1153: 235-258.
15. Capitanio D, Vasso M, Fania C, Moriggi M, Vigano A, Procacci P, Magnaghi V, Gelfi C. 2009. Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE. Proteomics 9: 2004-2020.
16. Castellanos-Serra L, Paz-Lago D. 2002. Inhibition of unwanted proteolysis during sample preparation: Evaluation of its efficiency in challenge experiments. Electrophoresis 23: 1745-1753.
17. Chen WQ, Diao WF, Viidik A, Skalicky M, Hoger H, Lubec G. 2008. Modulation of the hippocampal protein machinery in voluntary and treadmill exercising rats. Biochim Biophys Acta 1784: 555-562.
18. Chen X, Hess S. 2008. Adipose proteome analysis: Focus on mediators of insulin resistance. Expert Rev Proteomics 5: 827-839.
19. Chevallet M, Santoni V, Poinas A, Rouquie D, Fuchs A, Kieffer S, Rossignol M, Lunardi J, Garin J, Rabilloud T. 1998. New zwitterionic detergents improve the analysis of membrane proteins by two-dimensional electrophoresis. Electrophoresis 19: 1901-1909.
20. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ, Skinner JS. 2009. American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc 41: 1510-1530.
21. Coffey VG, Reeder DW, Lancaster GI, Yeo WK, Febbraio MA, Yaspelkis BB 3rd, Hawley JA. 2007. Effect of high-frequency resistance exercise on adaptive responses in skeletal muscle. Med Sci Sports Exerc 39: 2135-2144.
22. Collier TS, Sarkar P, Rao B, Muddiman DC. 2010. Quantitative top-down proteomics of SILAC labeled human embryonic stem cells. J Am Soc Mass Spectrom 21: 879-889.
23. Cox B, Emili A. 2006. Tissue subcellular fractionation and protein extraction for use in mass-spectrometry-based proteomics. Nat Protoc 1: 1872-1878.
24. de Roos B, Rungapamestry V, Ross K, Rucklidge G, Reid M, Duncan G, Horgan G, Toomey S, Browne J, Loscher CE, Mills KH, Roche HM. 2009. Attenuation of inflammation and cellular stress-related pathways maintains insulin sensitivity in obese type I interleukin-1 receptor knockout mice on a high-fat diet. Proteomics 9: 3244-3256.
25. Decramer S, Gonzalez de Peredo A, Breuil B, Mischak H, Monsarrat B, Bascands JL, Schanstra JP. 2008. Urine in clinical proteomics. Mol Cell Proteomics 7: 1850-1862.
26. Diffee GM. 2004. Adaptation of cardiac myocyte contractile properties to exercise training. Exerc Sport Sci Rev 32: 112-119.
27. Diffee GM, Seversen EA, Stein TD, Johnson JA. 2003. Microarray expression analysis of effects of exercise training: Increase in atrial MLC-1 in rat ventricles. Am J Physiol Heart Circ Physiol 284: H830-H837.
28. Ding Q, Vaynman S, Souda P, Whitelegge JP, Gomez-Pinilla F. 2006. Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 24: 1265-1276.
29. Donoghue P, Doran P, Wynne K, Pedersen K, Dunn MJ, Ohlendieck K. 2007. Proteomic profiling of chronic low-frequency stimulated fast muscle. Proteomics 7: 3417-3430.
30. Dulbecco R, Vogt M. 1954. Plaque formation and isolation of pure lines with poliomyelitis viruses. J Exp Med 99: 167-182.
31. Egen NB, Bliss M, Mayersohn M, Owens SM, Arnold L, Bier M. 1988. Isolation of monoclonal antibodies to phencyclidine from ascites fluid by preparative isoelectric focusing in the Rotofor. Anal Biochem 172: 488-494.
32. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. 1989. Electrospray ionization for mass spectrometry of large biomolecules. Science 246: 64-71.
33. Fenning A, Harrison G, Dwyer D, Rose'Meyer R, Brown L. 2003. Cardiac adaptation to endurance exercise in rats. Mol Cell Biochem 251: 51-59.
34. Flueck M. 2009. Plasticity of the muscle proteome to exercise at altitude. High Alt Med Biol 10: 183-193.
35. Foster LJ, de Hoog CL, Zhang Y, Zhang Y, Xie X, Mootha VK, Mann M. 2006. A mammalian organelle map by protein correlation profiling. Cell 125: 187-199.
36. Fountoulakis M, Takacs B. 2001. Effect of strong detergents and chaotropes on the detection of proteins in two-dimensional gels. Electrophoresis 22: 1593-1602.
37. Frey N, Olson EN. 2003. Cardiac hypertrophy: The good, the bad, and the ugly. Annu Rev Physiol 65: 45-79.
38. Garrels JI, McLaughlin CS, Warner JR, Futcher B, Latter GI, Kobayashi R, Schwender B, Volpe T, Anderson DS, Mesquita-Fuentes R, Payne WE. 1997. Proteome studies of Saccharomyces cerevisiae: Identification and characterization of abundant proteins. Electrophoresis 18: 1347-1360.
39. Gaziano TA, Bitton A, Anand S, Abrahams-Gessel S, Murphy A. 2010. Growing epidemic of coronary heart disease in low- and middle-income countries. Curr Probl Cardiol 35: 72-115.
40. Giada F, Biffi A, Agostoni P, Anedda A, Belardinelli R, Carlon R, Caru B, D'Andrea L, Delise P, De Francesco A, Fattirolli F, Guglielmi R, Guiducci U, Pelliccia A, Penco M, Perticone F, Thiene G, Vona M, Zeppilli P. 2008. Exercise prescription for the prevention and treatment of cardiovascular diseases: Part I. J Cardiovasc Med (Hagerstown) 9: 529-544.
41. Giometti CS, Anderson NG. 1981. Muscle protein analysis. III. Analysis of solubilized frozen-tissue sections by two-dimensional electrophoresis. Clin Chem 27: 1918-1921.
42. Giometti CS, Anderson NG, Anderson NL. 1979. Muscle protein analysis. I. High-resolution two-dimensional electrophoresis of skeletal muscle proteins for analysis of small biopsy samples. Clin Chem 25: 1877-1884.
43. Giometti CS, Barany M, Danon MJ, Anderson NG. 1980. Muscle protein analysis. II. Two-dimensional electrophoresis of normal and diseased human skeletal muscle. Clin Chem 26: 1152-1155.
44. Gomori G. 1955. Preparation of buffers for use in enzyme studies. Methods Enzymol 1: 138-146.
45. Gonzalez B, Manso R. 2004. Induction, modification and accumulation of HSP70s in the rat liver after acute exercise: Early and late responses. J Physiol 556: 369-385.
46. Gorg A, Weiss W, Dunn MJ. 2004. Current two-dimensional electrophoresis technology for proteomics. Proteomics 4: 3665-3685.
47. Graves PR, Haystead TA. 2002. Molecular biologist's guide to proteomics. Microbiol Mol Biol Rev 66: 39-63; table of contents.
48. Griffin TJ, Gygi SP, Rist B, Aebersold R, Loboda A, Jilkine A, Ens W, Standing KG. 2001. Quantitative proteomic analysis using a MALDI quadrupole time-of-flight mass spectrometer. Anal Chem 73: 978-986.
49. Grussenmeyer T, Meili-Butz S, Dieterle T, Traunecker E, Carrel TP, Lefkovits I. 2008. Quantitative proteome analysis in cardiovascular physiology and pathology. I. Data processing. J Proteome Res 7: 5211-5220.
50. Guelfi KJ, Casey TM, Giles JJ, Fournier PA, Arthur PG. 2006. A proteomic analysis of the acute effects of high-intensity exercise on skeletal muscle proteins in fasted rats. Clin Exp Pharmacol Physiol 33: 952-957.
51. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R. 1999. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17: 994-999.
52. Hamilton MT, Booth FW. 2000. Skeletal muscle adaptation to exercise: A century of progress. J Appl Physiol 88: 327-331.
53. Harmancey R, Wilson CR, Taegtmeyer H. 2008. Adaptation and maladaptation of the heart in obesity. Hypertension 52: 181-187.
54. Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, Macera CA, Heath GW, Thompson PD, Bauman A. 2007. Physical activity and public health: Updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Circulation 116: 1081-1093.
55. Hassel M, Klenk G, Frohme M. 1996. Prevention of unwanted proteolysis during extraction of proteins from protease-rich tissue. Anal Biochem 242: 274-275.
56. Hedou J, Bastide B, Page A, Michalski JC, Morelle W. 2009. Mapping of O-linked beta-N-acetylglucosamine modification sites in key contractile proteins of rat skeletal muscle. Proteomics 9: 2139-2148.
57. Henningsen R, Gale BL, Straub KM, DeNagel DC. 2002. Application of zwitterionic detergents to the solubilization of integral membrane proteins for two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2: 1479-1488.
58. Herbert B, Galvani M, Hamdan M, Olivieri E, MacCarthy J, Pedersen S, Righetti PG. 2001. Reduction and alkylation of proteins in preparation of two-dimensional map analysis: Why, when, and how? Electrophoresis 22: 2046-2057.
59. Hirsch J, Hansen KC, Burlingame AL, Matthay MA. 2004. Proteomics: Current techniques and potential applications to lung disease. Am J Physiol Lung Cell Mol Physiol 287: L1-L23.
60. Hirtz C, Chevalier F, Centeno D, Egea JC, Rossignol M, Sommerer N, de Periere D. 2005. Complexity of the human whole saliva proteome. J Physiol Biochem 61: 469-480.
61. Hojlund K, Yi Z, Hwang H, Bowen B, Lefort N, Flynn CR, Langlais P, Weintraub ST, Mandarino LJ. 2008. Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. Mol Cell Proteomics 7: 257-267.
62. Holloszy JO. 1975. Adaptation of skeletal muscle to endurance exercise. Med Sci Sports 7: 155-164.
63. Holloszy JO. 2005. Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol 99: 338-343.
64. Holloway KV, O'Gorman M, Woods P, Morton JP, Evans L, Cable NT, Goldspink DF, Burniston JG. 2009. Proteomic investigation of changes in human vastus lateralis muscle in response to interval-exercise training. Proteomics 9: 5155-5174.
65. Hoving S, Gerrits B, Voshol H, Muller D, Roberts RC, van Oostrum J. 2002. Preparative two-dimensional gel electrophoresis at alkaline pH using narrow range immobilized pH gradients. Proteomics 2: 127-134.
66. Hu S, Xie Y, Ramachandran P, Ogorzalek Loo RR, Li Y, Loo JA, Wong DT. 2005. Large-scale identification of proteins in human salivary proteome by liquid chromatography/mass spectrometry and two-dimensional gel electrophoresis-mass spectrometry. Proteomics 5: 1714-1728.
67. Ibel K, May RP, Kirschner K, Szadkowski H, Mascher E, Lundahl P. 1990. Protein-decorated micelle structure of sodium-dodecyl-sulfate-protein complexes as determined by neutron scattering. Eur J Biochem 190: 311-318.
68. Isfort RJ. 2002. Proteomic analysis of striated muscle. J Chromatogr B Analyt Technol Biomed Life Sci 771: 155-165.
69. Isfort RJ, Wang F, Greis KD, Sun Y, Keough TW, Bodine SC, Anderson NL. 2002a. Proteomic analysis of rat soleus and tibialis anterior muscle following immobilization. J Chromatogr B Analyt Technol Biomed Life Sci 769: 323-332.
70. Isfort RJ, Wang F, Greis KD, Sun Y, Keough TW, Farrar RP, Bodine SC, Anderson NL. 2002b. Proteomic analysis of rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics 2: 543-550.
71. Issaq HJ, Conrads TP, Janini GM, Veenstra TD. 2002. Methods for fractionation, separation and profiling of proteins and peptides. Electrophoresis 23: 3048-3061.
72. Jayapal KP, Sui S, Philp RJ, Kok YJ, Yap MG, Griffin TJ, Hu WS. 2010a. Multitagging proteomic strategy to estimate protein turnover rates in dynamic systems. J Proteome Res 9: 2087-2097.
73. Jiang X, Ye M, Liu G, Feng S, Cui L, Zou H. 2007. Method development of efficient protein extraction in bone tissue for proteome analysis. J Proteome Res 6: 2287-2294.
74. Kaletas BK, van der Wiel IM, Stauber J, Guzel C, Kros JM, Luider TM, Heeren RM. 2009. Sample preparation issues for tissue imaging by imaging MS. Proteomics 9: 2622-2633.
75. Karas M, Hillenkamp F. 1988. Laser desorption ionization of proteins with molecular masses exceeding 10, 000 daltons. Anal Chem 60: 2299-2301.
76. Kavazis AN, Alvarez S, Talbert E, Lee Y, Powers SK. 2009. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol Heart Circ Physiol 297: H144-H152.
77. Klose J. 1975. Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 26: 231-243.
78. Kolch W, Mischak H, Pitt AR. 2005. The molecular make-up of a tumour: Proteomics in cancer research. Clin Sci (Lond) 108: 369-383.
79. Lanne B, Potthast F, Hoglund A, Brockenhuus von Lowenhielm H, Nystrom AC, Nilsson F, Dahllof B. 2001. Thiourea enhances mapping of the proteome from murine white adipose tissue. Proteomics 1: 819-828.
80. le Maire M, Champeil P, Moller JV. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta 1508: 86-111.
81. Li RX, Zhou H, Li SJ, Sheng QH, Xia QC, Zeng R. 2005. Prefractionation of proteome by liquid isoelectric focusing prior to two-dimensional liquid chromatography mass spectrometric identification. J Proteome Res 4: 1256-1264.
82. Liebler DC. 2002. Proteomic approaches to characterize protein modifications: New tools to study the effects of environmental exposures. Environ Health Perspect 110: 3-9.
83. Lima LC, Assis GV, Hiyane W, Almeida WS, Arsa G, Baldissera V, Campbell CS, Simoes HG. 2008. Hypotensive effects of exercise performed around anaerobic threshold in type 2 diabetic patients. Diabetes Res Clin Pract 81: 216-222.
84. Longhurst JC, Kelly AR, Gonyea WJ, Mitchell JH. 1981. Chronic training with static and dynamic exercise: Cardiovascular adaptation, and response to exercise. Circ Res 48: I171-I178.
85. Lopez JL. 2007. Two-dimensional electrophoresis in proteome expression analysis. J Chromatogr B Analyt Technol Biomed Life Sci 849: 190-202.
86. Luche S, Santoni V, Rabilloud T. 2003. Evaluation of nonionic and zwitterionic detergents as membrane protein solubilizers in two-dimensional electrophoresis. Proteomics 3: 249-253.
87. Marwick TH, Hordern MD, Miller T, Chyun DA, Bertoni AG, Blumenthal RS, Philippides G, Rocchini A. 2009. Exercise training for type 2 diabetes mellitus: Impact on cardiovascular risk: A scientific statement from the American Heart Association. Circulation 119: 3244-3262.
88. Mayr M, Mayr U, Chung YL, Yin X, Griffiths JR, Xu Q. 2004. Vascular proteomics: Linking proteomic and metabolomic changes. Proteomics 4: 3751-3761.
89. McAlpin CR, Cox CR, Matyi SA, Voorhees KJ. 2010. Enhanced matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis of bacteriophage major capsid proteins with beta-mercaptoethanol pretreatment. Rapid Commun Mass Spectrom 24: 11-14.
90. Moller B, Posch S. 2009. Robust features for 2-DE gel image registration. Electrophoresis 30: 4137-4148.
91. Moritz RL, Ji H, Schutz F, Connolly LM, Kapp EA, Speed TP, Simpson RJ. 2004a. A proteome strategy for fractionating proteins and peptides using continuous free-flow electrophoresis coupled off-line to reversed-phase high-performance liquid chromatography. Anal Chem 76: 4811-4824.
92. Moritz RL, Ji H, Schutz F, Connolly LM, Kapp EA, Speed TP, Simpson RJ. 2004b. A proteome strategy for fractionating proteins and peptides using continuous free-flow electrophoresis coupled off-line to reversed-phase high-performance liquid chromatography. Anal Chem 76: 4811-4824.
93. Murakami U, Uchida K. 1985. Contents of myofibrillar proteins in cardiac, skeletal, and smooth muscles. J Biochem 98: 187-197.
94. Nader GA, Esser KA. 2001. Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90: 1936-1942.
95. Nichols GA, Bell TJ, Pedula KL, O'Keeffe-Rosetti M. 2010. Medical care costs among patients with established cardiovascular disease. Am J Manag Care 16: e86-e93.
96. Novotny MV, Soini HA, Mechref Y. 2008. Biochemical individuality reflected in chromatographic, electrophoretic and mass-spectrometric profiles. J Chromatogr B Analyt Technol Biomed Life Sci 866: 26-47.
97. O'Connell K, Gannon J, Doran P, Ohlendieck K. 2007. Proteomic profiling reveals a severely perturbed protein expression pattern in aged skeletal muscle. Int J Mol Med 20: 145-153.
98. O'Donovan G, Blazevich AJ, Boreham C, Cooper AR, Crank H, Ekelund U, Fox KR, Gately P, Giles-Corti B, Gill JM, Hamer M, McDermott I, Murphy M, Mutrie N, Reilly JJ, Saxton JM, Stamatakis E. 2010. The ABC of Physical Activity for Health: A consensus statement from the British Association of Sport and Exercise Sciences. J Sports Sci 28: 573-591.
99. O'Farrell PH. 1975. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021.
100. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. 2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1: 376-386.
101. Ong SE, Kratchmarova I, Mann M. 2003. Properties of 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J Proteome Res 2: 173-181.
102. Patton WF. 2002. Detection technologies in proteome analysis. J Chromatogr B Analyt Technol Biomed Life Sci 771: 3-31.
103. Pesavento JJ, Bullock CR, LeDuc RD, Mizzen CA, Kelleher NL. 2008. Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J Biol Chem 283: 14927-14937.
104. Phanstiel D, Brumbaugh J, Berggren WT, Conard K, Feng X, Levenstein ME, McAlister GC, Thomson JA, Coon JJ. 2008. Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells. Proc Natl Acad Sci USA 105: 4093-4098.
105. Piec I, Listrat A, Alliot J, Chambon C, Taylor RG, Bechet D. 2005. Differential proteome analysis of aging in rat skeletal muscle. Faseb J 19: 1143-1145.
106. Pieper R, Gatlin CL, McGrath AM, Makusky AJ, Mondal M, Seonarain M, Field E, Schatz CR, Estock MA, Ahmed N, Anderson NG, Steiner S. 2004. Characterization of the human urinary proteome: A method for high-resolution display of urinary proteins on two-dimensional electrophoresis gels with a yield of nearly 1400 distinct protein spots. Proteomics 4: 1159-1174.
107. Powers SK, Quindry JC, Kavazis AN. 2008. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 44: 193-201.
108. Quadroni M, James P. 1999. Proteomics and automation. Electrophoresis 20: 664-677.
109. Rabilloud T. 1998. Use of thiourea to increase the solubility of membrane proteins in two-dimensional electrophoresis. Electrophoresis 19: 758-760.
110. Rabilloud T. 2009. Detergents and chaotropes for protein solubilization before two-dimensional electrophoresis. Methods Mol Biol 528: 259-267.
111. Rabilloud T, Adessi C, Giraudel A, Lunardi J. 1997. Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 18: 307-316.
112. Rao PV, Reddy AP, Lu X, Dasari S, Krishnaprasad A, Biggs E, Roberts CT, Nagalla SR. 2009. Proteomic identification of salivary biomarkers of type-2 diabetes. J Proteome Res 8: 239-245.
113. Reisinger V, Eichacker LA. 2006. Analysis of membrane protein complexes by blue native PAGE. Proteomics 6: 6-15.
114. Reisinger V, Eichacker LA. 2008. Solubilization of membrane protein complexes for blue native PAGE. J Proteomics 71: 277-283.
115. Richardson MR, Lai X, Dixon JL, Sturek M, Witzmann FA. 2009. Diabetic dyslipidemia and exercise alter the plasma low-density lipoproteome in Yucatan pigs. Proteomics 9: 2468-2483.
116. Roe MR, Griffin TJ. 2006. Gel-free mass spectrometry-based high throughput proteomics: Tools for studying biological response of proteins and proteomes. Proteomics 6: 4678-4687.
117. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ. 2004. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
118. Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA. 2009. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One 4: e5610.
119. Satta D, Schapira G, Chafey P, Righetti PG, Wahrmann JP. 1984. Solubilization of plasma membranes in anionic, non-ionic and zwitterionic surfactants for iso-dalt analysis: A critical evaluation. J Chromatogr 299: 57-72.
120. Schenk S, Schoenhals GJ, de Souza G, Mann M. 2008. A high confidence, manually validated human blood plasma protein reference set. BMC Med Genomics 1: 41.
121. Schmid GM, Converset V, Walter N, Sennitt MV, Leung KY, Byers H, Ward M, Hochstrasser DF, Cawthorne MA, Sanchez JC. 2004. Effect of high-fat diet on the expression of proteins in muscle, adipose tissues, and liver of C57BL/6 mice. Proteomics 4: 2270-2282.
122. Schott P, Asif AR, Graf C, Toischer K, Hasenfuss G, Kogler H. 2008. Myocardial adaptation of energy metabolism to elevated preload depends on calcineurin activity: A proteomic approach. Basic Res Cardiol 103: 232-243.
123. Schreiweis MA, Butler JP, Kulkarni NH, Knierman MD, Higgs RE, Halladay DL, Onyia JE, Hale JE. 2007. A proteomic analysis of adult rat bone reveals the presence of cartilage/chondrocyte markers. J Cell Biochem 101: 466-476.
124. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K. 2003. Resistance of cell membranes to different detergents. Proc Natl Acad Sci USA 100: 5795-5800.
125. Seo Y, Lee K, Park K, Bae K, Choi I. 2006. A proteomic assessment of muscle contractile alterations during unloading and reloading. J Biochem 139: 71-80.
126. Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Boucherie H, Mann M. 1996a. Linking genome and proteome by mass spectrometry: Large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 93: 14440-14445.
127. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860.
128. Shevchenko A, Wilm M, Vorm O, Mann M. 1996b. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
129. Short KR, Vittone JL, Bigelow ML, Proctor DN, Coenen-Schimke JM, Rys P, Nair KS. 2005. Changes in myosin heavy chain mRNA and protein expression in human skeletal muscle with age and endurance exercise training. J Appl Physiol 99: 95-102.
130. Sun B, Wang JH, Lv YY, Zhu SS, Yang J, Ma JZ. 2008. Proteomic adaptation to chronic high intensity swimming training in the rat heart. Comp Biochem Physiol Part D Genom Proteom 3: 108-117.
131. Svensson M, Boren M, Skold K, Falth M, Sjogren B, Andersson M, Svenningsson P, Andren PE. 2009. Heat stabilization of the tissue proteome: A new technology for improved proteomics. J Proteome Res 8: 974-981.
132. Svensson M, Skold K, Nilsson A, Falth M, Nydahl K, Svenningsson P, Andren PE. 2007. Neuropeptidomics: MS applied to the discovery of novel peptides from the brain. Anal Chem 79: 15-16, 18-21.
133. Thongboonkerd V, Klein JB, Arthur JM. 2003. Proteomic identification of a large complement of rat urinary proteins. Nephron Exp Nephrol 95: e69-e78.
134. Tong Y, Hara A, Komatsu M, Tanaka N, Kamijo Y, Gonzalez FJ, Aoyama T. 2005. Suppression of expression of muscle-associated proteins by PPARalpha in brown adipose tissue. Biochem Biophys Res Commun 336: 76-83.
135. Trott D, McManus CA, Martin JL, Brennan B, Dunn MJ, Rose ML. 2009. Effect of phosphorylated hsp27 on proliferation of human endothelial and smooth muscle cells. Proteomics 9: 3383-3394.
136. Unlu M, Morgan ME, Minden JS. 1997. Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071-2077.
137. Vercauteren FG, Arckens L, Quirion R. 2007. Applications and current challenges of proteomic approaches, focusing on two-dimensional electrophoresis. Amino Acids 33: 405-414.
138. Verrills NM. 2006. Clinical proteomics: Present and future prospects. Clin Biochem Rev 27: 99-116.
139. Walker JMea. 2005. The proteomics protocols handbook. 999 Riverview Drive S, editor. Totowa, New Jersey: Humana Press Inc.
140. Warren CM, Geenen DL, Helseth DL Jr, Xu H, Solaro RJ. 2010. Sub-proteomic fractionation, iTRAQ, and OFFGEL-LC-MS/MS approaches to cardiac proteomics. J Proteomics 73: 1551-1561.
141. Warren CM, Greaser ML. 2003. Method for cardiac myosin heavy chain separation by sodium dodecyl sulfate gel electrophoresis. Anal Biochem 320: 149-151.
142. Westermeier R. 2004. Isoelectric focusing. Methods Mol Biol 244: 225-232.
143. Westermeier R, Marouga R. 2005. Protein detection methods in proteomics research. Biosci Rep 25: 19-32.
144. Westermeier R, Postel W, Weser J, Gorg A. 1983. High-resolution two-dimensional electrophoresis with isoelectric focusing in immobilized pH gradients. J Biochem Biophys Methods 8: 321-330.
145. Wilkins MR, Pasquali C, Appel RD, Ou K, Golaz O, Sanchez JC, Yan JX, Gooley AA, Hughes G, Humphery-Smith I, Williams KL, Hochstrasser DF. 1996. From proteins to proteomes: Large scale protein identification by two-dimensional electrophoresis and amino acid analysis. Biotechnology (NY) 14: 61-65.
146. Xu X, Wan W, Ji L, Lao S, Powers AS, Zhao W, Erikson JM, Zhang JQ. 2008. Exercise training combined with angiotensin II receptor blockade limits post-infarct ventricular remodelling in rats. Cardiovasc Res 78: 523-532.
147. Yamaguchi W, Fujimoto E, Higuchi M, Tabata I. 2010. A DIGE proteomic analysis for high-intensity exercise-trained rat skeletal muscle. J Biochem 148: 327-333.
148. Yang KD, Chang WC, Chuang H, Wang PW, Liu RT, Yeh SH. 2010. Increased complement factor H with decreased factor B determined by proteomic differential displays as a biomarker of tai chi chuan exercise. Clin Chem 56: 127-131.
149. Yates JR 3rd, Carmack E, Hays L, Link AJ, Eng JK. 1999. Automated protein identification using microcolumn liquid chromatography-tandem mass spectrometry. Methods Mol Biol 112: 553-569.
150. Yu H, Meng Y, Wang LS, Jin X, Gao LF, Zhou L, Ji K, Li Y, Zhao LJ, Chen GQ, Zhao XJ, Yang B. 2009. Differential protein expression in heart in UT-B null mice with cardiac conduction defects. Proteomics 9: 504-511.
151. Yuan Q, Fontenele-Neto JD, Fricker LD. 2004. Effect of voluntary exercise on genetically obese Cpefat/fat mice: Quantitative proteomics of serum. Obes Res 12: 1179-1188.
152. Zheng YZ, Foster LJ. 2009. Biochemical and proteomic approaches for the study of membrane microdomains. J Proteomics 72: 12-22.
153. Zhou G, Li H, DeCamp D, Chen S, Shu H, Gong Y, Flaig M, Gillespie JW, Hu N, Taylor PR, Emmert-Buck MR, Liotta LA, Petricoin EF 3rd, Zhao Y. 2002. 2D differential in-gel electrophoresis for the identification of esophageal scans cell cancer-specific protein markers. Mol Cell Proteomics 1: 117-124.
154. Zimmerli LU, Schiffer E, Zurbig P, Good DM, Kellmann M, Mouls L, Pitt AR, Coon JJ, Schmieder RE, Peter KH, Mischak H, Kolch W, Delles C, Dominiczak AF. 2008. Urinary proteomic biomarkers in coronary artery disease. Mol Cell Proteomics 7: 290-298.
155. Zuo X, Speicher DW. 2000. A method for global analysis of complex proteomes using sample prefractionation by solution isoelectrofocusing prior to two-dimensional electrophoresis. Anal Biochem 284: 266-278.