A proteomic study of plasma protein changes under extreme physical stress

Journal of Proteomics

Volumn 98, Issue , 2014, Pages 1-14

  Balfoussia, Edily ^a   Skenderi, Katerina ^b   Tsironi, Maria ^c   Anagnostopoulos, Athanasios K ^a   Parthimos, Nikolaos ^d   Vougas, Kostantinos ^a   Papassotiriou, Ioannis ^e   Tsangaris, George Th ^a   Chrousos, George P ^d  

^a BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^b HAROKOPIO UNIVERSITY   (Greece)

^c UNIVERSITY OF PELOPONNESE   (Greece)

^d UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^e AGHIA SOPHIA CHILDREN S HOSPITAL   (Greece)

Author keywords

2 DE; Endurance; Plasma; Proteomics; Spartathlon

Indexed keywords

ANTIOXIDANT; FIBRINOGEN; KININOGEN; PLASMA PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; SERUM AMYLOID P; VITAMIN D; VITRONECTIN;

ADULT; ANTICOAGULATION; ARTICLE; COMPLEMENT SYSTEM; EXERCISE; EXTREME PHYSICAL STRESS; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEOMICS; QUANTITATIVE ANALYSIS;

2-DE; ENDURANCE; PLASMA; PROTEOMICS; SPARTATHLON;

ADULT; ATHLETES; BLOOD PROTEINS; HUMANS; MALE; MIDDLE AGED; PHYSICAL EXERTION; PROTEOMICS; RUNNING; STRESS, PHYSIOLOGICAL;

EID: 84891820844     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.12.004     Document Type: Article

References (86)

1. Skenderi K.P., Tsironi M., Lazaropoulou C., Anastasiou C.A., Matalas A.L., Kanavaki I., et al. Changes in free radical generation and antioxidant capacity during ultramarathon foot race. Eur J Clin Invest 2008, 38:159-165.
2. Skenderi K.P., Kavouras S.A., Anastasiou C.A., Yiannakouris N., Matalas A.L. Exertional rhabdomyolysis during a 246-km continuous running race. Med Sci Sports Exerc 2006, 38:1054-1057.
3. Papassotiriou I., Alexiou V.G., Tsironi M., Skenderi K., Spanos A., Falagas M.E. Severe aseptic inflammation caused by long distance running (246km) does not increase procalcitonin. Eur J Clin Invest 2008, 38:276-279.
4. Bartzeliotou A.I., Margeli A.P., Tsironi M., Skenderi K., Bacoula C., Chrousos G.P., et al. Circulating levels of adhesion molecules and markers of endothelial activation in acute inflammation induced by prolonged brisk exercise. Clin Biochem 2007, 40:765-770.
5. Margeli A., Skenderi K., Tsironi M., Hantzi E., Matalas A.L., Vrettou C., et al. Dramatic elevations of interleukin-6 and acute-phase reactants in athletes participating in the ultradistance foot race spartathlon: severe systemic inflammation and lipid and lipoprotein changes in protracted exercise. J Clin Endocrinol Metab 2005, 90:3914-3918.
6. Goussetis E., Spiropoulos A., Tsironi M., Skenderi K., Margeli A., Graphakos S., et al. Spartathlon, a 246 kilometer foot race: effects of acute inflammation induced by prolonged exercise on circulating progenitor reparative cells. Blood Cells Mol Dis 2009, 42:294-299.
7. Finaud J., Lac G., Filaire E. Oxidative stress: relationship with exercise and training. Sports Med 2006, 36:327-358.
8. Mitsuishi Y., Motohashi H., Yamamoto M. The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism. Front Oncol 2012, 2:200.
9. Taguchi K., Motohashi H., Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011, 16:123-140.
10. Radak Z., Chung H.Y., Goto S. Exercise and hormesis: oxidative stress-related adaptation for successful aging. Biogerontology 2005, 6:71-75.
11. Fry R.W., Morton A.R., Keast D. Overtraining in athletes. An update. Sports Med 1991, 12:32-65.
12. Rowbottom D.G., Keast D., Goodman C., Morton A.R. The haematological, biochemical and immunological profile of athletes suffering from the overtraining syndrome. Eur J Appl Physiol 1995, 70:502-509.
13. Radak Z., Naito H., Taylor A.W., Goto S. Nitric oxide: is it the cause of muscle soreness?. Nitric Oxide 2012, 26:89-94.
14. Davies K.J., Quintanilha A.T., Brooks G.A., Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 1982, 107:1198-1205.
15. McArdle A., Dillmann W.H., Mestril R., Faulkner J.A., Jackson M.J. Overexpression of HSP70 in mouse skeletal muscle protects against muscle damage and age-related muscle dysfunction. FASEB J 2004, 18:355-357.
16. Tsangaris G.T., Karamessinis P., Kolialexi A., Garbis S.D., Antsaklis A., Mavrou A., et al. Proteomic analysis of amniotic fluid in pregnancies with Down syndrome. Proteomics 2006, 6:4410-4419.
17. Vercauteren F.G., Arckens L., Quirion R. Applications and current challenges of proteomic approaches, focusing on two-dimensional electrophoresis. Amino Acids 2007, 33:405-414.
18. Scoppetta F., Tartaglia M., Renzone G., Avellini L., Gaiti A., Scaloni A., et al. Plasma protein changes in horse after prolonged physical exercise: a proteomic study. J Proteomics 2012, 75:4494-4504.
19. Kolialexi A., Mavrou A., Spyrou G., Tsangaris G.T. Mass spectrometry-based proteomics in reproductive medicine. Mass Spectrom Rev 2008, 27:624-634.
20. Rabilloud T. Mechanisms of protein silver staining in polyacrylamide gels: a 10-year synthesis. Electrophoresis 1990, 11:785-794.
21. Chambers J.L., Christoph G.G., Krieger M., Kay L., Stroud R.M. Silver ion inhibition of serine proteases: crystallographic study of silver-trypsin. Biochem Biophys Res Commun 1974, 59:70-74.
22. Chevallet M., Luche S., Rabilloud T. Silver staining of proteins in polyacrylamide gels. Nat Protoc 2006, 1:1852-1858.
23. Mastorakos G., Pavlatou M., Diamanti-Kandarakis E., Chrousos G.P. Exercise and the stress system. Hormones (Athens) 2005, 4:73-89.
24. Reuland D.J., McCord J.M., Hamilton K.L. The Role of Nrf2 in the Attenuation of Cardiovascular Disease. Exerc Sport Sci Rev 2013, 41:162-168.
25. Warnberg J., Cunningham K., Romeo J., Marcos A. Physical activity, exercise and low-grade systemic inflammation. Proc Nutr Soc 2010, 69:400-406.
26. Fountoulakis M. Proteomics: current technologies and applications in neurological disorders and toxicology. Amino Acids 2001, 21:363-381.
27. Gorg A., Weiss W., Dunn M.J. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4:3665-3685.
28. Anderson N.L., Anderson N.G. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002, 1:845-867.
29. Smith J.E. Effects of strenuous exercise on haemostasis. Br J Sports Med 2003, 37:433-435.
30. Smith J.E., Garbutt G., Lopes P., Pedoe D.T. Effects of prolonged strenuous exercise (marathon running) on biochemical and haematological markers used in the investigation of patients in the emergency department. Br J Sports Med 2004, 38:292-294.
31. Zhou A., Huntington J.A., Pannu N.S., Carrell R.W., Read R.J. How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration. Nat Struct Biol 2003, 10:541-544.
32. Preissner K.T., Seiffert D. Role of vitronectin and its receptors in haemostasis and vascular remodeling. Thromb Res 1998, 89:1-21.
33. Houlihan L.M., Davies G., Tenesa A., Harris S.E., Luciano M., Gow A.J., et al. Common variants of large effect in F12, KNG1, and HRG are associated with activated partial thromboplastin time. Am J Hum Genet 2010, 86:626-631.
34. Li Y.H., Kuo C.H., Shi G.Y., Wu H.L. The role of thrombomodulin lectin-like domain in inflammation. J Biomed Sci 2012, 19:34.
35. Mehdi H., Nunn M., Steel D.M., Whitehead A.S., Perez M., Walker L., et al. Nucleotide sequence and expression of the human gene encoding apolipoprotein H (beta 2-glycoprotein I). Gene 1991, 108:293-298.
36. Shi W., Chong B.H., Hogg P.J., Chesterman C.N. Anticardiolipin antibodies block the inhibition by beta 2-glycoprotein I of the factor Xa generating activity of platelets. Thromb Haemost 1993, 70:342-345.
37. Schousboe I., Rasmussen M.S. Synchronized inhibition of the phospholipid mediated autoactivation of factor XII in plasma by beta 2-glycoprotein I and anti-beta 2-glycoprotein I. Thromb Haemost 1995, 73:798-804.
38. Matsuda J., Gohchi K., Kawasugi K., Gotoh M., Saitoh N., Tsukamoto M. Inhibitory activity of anti-beta 2-glycoprotein I antibody on factor Va degradation by activated-protein C and its cofactor protein S. Am J Hematol 1995, 49:89-91.
39. Yenari M.A., Liu J., Zheng Z., Vexler Z.S., Lee J.E., Giffard R.G. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci 2005, 1053:74-83.
40. Sharp F.R., Massa S.M., Swanson R.A. Heat-shock protein protection. Trends Neurosci 1999, 22:97-99.
41. Giffard R.G., Yenari M.A. Many mechanisms for hsp70 protection from cerebral ischemia. J Neurosurg Anesthesiol 2004, 16:53-61.
42. Giffard R.G., Xu L., Zhao H., Carrico W., Ouyang Y., Qiao Y., et al. Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J Exp Biol 2004, 207:3213-3220.
43. Kiang J.G., Tsokos G.C. Heat shock protein 70kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 1998, 80:183-201.
44. Garrido C., Schmitt E., Cande C., Vahsen N., Parcellier A., Kroemer G. HSP27 and HSP70: potentially oncogenic apoptosis inhibitors. Cell Cycle 2003, 2:579-584.
45. He M., Guo H., Yang X., Zhou L., Zhang X., Cheng L., et al. Genetic variations in HSPA8 gene associated with coronary heart disease risk in a Chinese population. PLoS One 2010, 5:e9684.
46. Erbse A., Mayer M.P., Bukau B. Mechanism of substrate recognition by Hsp70 chaperones. Biochem Soc Trans 2004, 32:617-621.
47. Yun J.K., McCormick T.S., Villabona C., Judware R.R., Espinosa M.B., Lapetina E.G. Inflammatory mediators are perpetuated in macrophages resistant to apoptosis induced by hypoxia. Proc Natl Acad Sci U S A 1997, 94:13903-13908.
48. de la Rosa E.J., Vega-Nunez E., Morales A.V., Serna J., Rubio E., de Pablo F. Modulation of the chaperone heat shock cognate 70 by embryonic (pro)insulin correlates with prevention of apoptosis. Proc Natl Acad Sci U S A 1998, 95:9950-9955.
49. Mosser D.D., Caron A.W., Bourget L., Meriin A.B., Sherman M.Y., Morimoto R.I., et al. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 2000, 20:7146-7159.
50. Santoro M.G. Heat shock factors and the control of the stress response. Biochem Pharmacol 2000, 59:55-63.
51. Takahashi K., Koga K., Linge H.M., Zhang Y., Lin X., Metz C.N., et al. Macrophage CD74 contributes to MIF-induced pulmonary inflammation. Respir Res 2009, 10:33.
52. Flaster H., Bernhagen J., Calandra T., Bucala R. The macrophage migration inhibitory factor-glucocorticoid dyad: regulation of inflammation and immunity. Mol Endocrinol 2007, 21:1267-1280.
53. Al-Abed Y., Metz C.N., Cheng K.F., Aljabari B., VanPatten S., Blau S., et al. Thyroxine is a potential endogenous antagonist of macrophage migration inhibitory factor (MIF) activity. Proc Natl Acad Sci U S A 2011, 108:8224-8227.
54. Opstal-van Winden A.W., Vermeulen R.C., Peeters P.H., Beijnen J.H., van Gils C.H. Early diagnostic protein biomarkers for breast cancer: how far have we come?. Breast Cancer Res Treat 2012, 134:1-12.
55. Pineiro M., Andres M., Iturralde M., Carmona S., Hirvonen J., Pyorala S., et al. ITIH4 (inter-alpha-trypsin inhibitor heavy chain 4) is a new acute-phase protein isolated from cattle during experimental infection. Infect Immun 2004, 72:3777-3782.
56. Mahler D.A., Loke J. Pulmonary dysfunction in ultramarathon runners. Yale J Biol Med 1981, 54:243-248.
57. Luisetti M., Miravitlles M., Stockley R.A. Alpha1-antitrypsin deficiency: a report from the 2nd meeting of the Alpha One International Registry, Rapallo (Genoa, Italy), 2001. Eur Respir J 2002, 20:1050-1056.
58. Lisowska-Myjak B. AAT as a diagnostic tool. Clin Chim Acta 2005, 352:1-13.
59. Neubauer O., Konig D., Wagner K.H. Recovery after an Ironman triathlon: sustained inflammatory responses and muscular stress. Eur J Appl Physiol 2008, 104:417-426.
60. Lachmann P. Genetics of the complement system. J Med Genet 1975, 12:372-377.
61. Matsuyama W., Nakagawa M., Takashima H., Muranaga F., Sano Y., Osame M. Molecular analysis of hereditary deficiency of the third component of complement (C3) in two sisters. Intern Med 2001, 40:1254-1258.
62. Conrad D.H., Carlo J.R., Ruddy S. Interaction of beta1H globulin with cell-bound C3b: quantitative analysis of binding and influence of alternative pathway components on binding. J Exp Med 1978, 147:1792-1805.
63. Weiler J.M., Daha M.R., Austen K.F., Fearon D.T. Control of the amplification convertase of complement by the plasma protein beta1H. Proc Natl Acad Sci U S A 1976, 73:3268-3272.
64. Pangburn M.K., Schreiber R.D., Muller-Eberhard H.J. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein beta1H for cleavage of C3b and C4b in solution. J Exp Med 1977, 146:257-270.
65. Robach P., Boisson R.C., Vincent L., Lundby C., Moutereau S., Gergele L., et al. Hemolysis induced by an extreme mountain ultra-marathon is not associated with a decrease in total red9Q6619 blood cell volume. Scand J Med Sci Sports 2012 Jun 5, http://dx.doi.org/10.1111/j.1600-0838.2012.01481.x.
66. Gilligan D.R., Altschule M.D., Katersky E.M. Physiological intravascular hemolysis of exercise. Hemoglobinemia and hemoglobinuria following cross-country runs. J Clin Invest 1943, 22:859-869.
67. Weight L.M., Byrne M.J., Jacobs P. Haemolytic effects of exercise. Clin Sci (Lond) 1991, 81:147-152.
68. Dang C.V. Runner's anemia. JAMA 2001, 286:714-716.
69. Wassell J. Haptoglobin: function and polymorphism. Clin Lab 2000, 46:547-552.
70. Tolosano E., Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol 2002, 21:297-306.
71. Maly M.A., Majek P., Reicheltova Z., Kotlin R., Suttnar J., Oravec M., et al. Proteomic analysis of plasma samples from acute coronary syndrome patients-the pilot study. Int J Cardiol 2012, 157:126-128.
72. Cicarelli D.D., Vieira J.E., Bensenor F.E. Comparison of C-reactive protein and serum amyloid a protein in septic shock patients. Mediators Inflamm 2008, 2008:631414.
73. Getz G.S., Reardon C.A. Paraoxonase, a cardioprotective enzyme: continuing issues. Curr Opin Lipidol 2004, 15:261-267.
74. Mackness M., Mackness B. Paraoxonase 1 and atherosclerosis: is the gene or the protein more important?. Free Radic Biol Med 2004, 37:1317-1323.
75. Fitos I., Visy J., Zsila F., Mady G., Simonyi M. Selective binding of imatinib to the genetic variants of human alpha1-acid glycoprotein. Biochim Biophys Acta 2006, 1760:1704-1712.
76. Zsila F., Iwao Y. The drug binding site of human alpha1-acid glycoprotein: insight from induced circular dichroism and electronic absorption spectra. Biochim Biophys Acta 2007, 1770:797-809.
77. Fournier T., Medjoubi N.N., Porquet D. Alpha-1-acid glycoprotein. Biochim Biophys Acta 2000, 1482:157-171.
78. Royle N.J., Irwin D.M., Koschinsky M.L., MacGillivray R.T., Hamerton J.L. Human genes encoding prothrombin and ceruloplasmin map to 11p11-q12 and 3q21-24, respectively. Somat Cell Mol Genet 1987, 13:285-292.
79. Pousset D., Piller V., Bureaud N., Piller F. High levels of ceruloplasmin in the serum of transgenic mice developing hepatocellular carcinoma. Eur J Biochem 2001, 268:1491-1499.
80. Iakovidis I., Delimaris I., Piperakis S.M. Copper and its complexes in medicine: a biochemical approach. Mol Biol Int 2011, 2011:594529.
81. Ruckman K.S., Sherman A.R. Effects of exercise on iron and copper metabolism in rats. J Nutr 1981, 111:1593-1601.
82. Renaudineau Y., Nedellec S., Berthou C., Lydyard P.M., Youinou P., Pers J.O. Role of B-cell antigen receptor-associated molecules and lipid rafts in CD5-induced apoptosis of B CLL cells. Leukemia 2005, 19:223-229.
83. Pacque P.F., Booth C.K., Ball M.J., Dwyer D.B. The effect of an ultra-endurance running race on mucosal and humoral immune function. J Sports Med Phys Fitness 2007, 47:496-501.
84. Gomme P.T., Bertolini J. Therapeutic potential of vitamin D-binding protein. Trends Biotechnol 2004, 22:340-345.
85. Chishimba L., Thickett D.R., Stockley R.A., Wood A.M. The vitamin D axis in the lung: a key role for vitamin D-binding protein. Thorax 2010, 65:456-462.
86. Speeckaert M., Huang G., Delanghe J.R., Taes Y.E. Biological and clinical aspects of the vitamin D binding protein (Gc-globulin) and its polymorphism. Clin Chim Acta 2006, 372:33-42.