Distinct profiles of systemic biomarkers of oxidative stress in chronic human pathologies: Cardiovascular, psychiatric, neurodegenerative, rheumatic, infectious, neoplasmic and endocrinological diseases — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Distinct profiles of systemic biomarkers of oxidative stress in chronic human pathologies: Cardiovascular, psychiatric, neurodegenerative, rheumatic, infectious, neoplasmic and endocrinological diseases
Ge Sante et Retraite, Paris, France
,
Consultant en Statistiques, Esches, France
,
Procrelys, Maison Médicale Ambroise Paré, Lyon, France
,
Department of Metabolic Biochemistry, La Pitié Salpetriere-Charles Foix (AP-HP), Paris, France
,
école Supérieure de Physique et de Chimie Industrielles, ESPCI, Paris, France
,
Université Pierre et Marie Curie-Paris 6, Paris, France
,
Université Pierre et Marie Curie-Paris 6, Paris, France
1 Ge Sante et Retraite, Paris, France
2 Consultant en Statistiques, Esches, France
3 Procrelys, Maison Médicale Ambroise Paré, Lyon, France
4 Department of Metabolic Biochemistry, La Pitié Salpetriere-Charles Foix (AP-HP), Paris, France
5 école Supérieure de Physique et de Chimie Industrielles, ESPCI, Paris, France
6 Université Pierre et Marie Curie-Paris 6, Paris, France
7 Université Pierre et Marie Curie-Paris 6, Paris, France
Oxidative stress is involved in chronic and acute pa thologies: cardiovascular, neurodegenerative, neo plastic, inflammatory and infectious diseases. Clinical trials focused on prevention of cardiovascular and neoplastic diseases involving antioxidant supplementation have however provided predominantly negative obserations in large-scale studies. Screening of patient cohorts to assess baseline oxidative stress on the basis of a biomarker profile is decisive but lacking. For the first time, we evaluated the level of oxidative stress, testing more than 10 established biomarkers, in a comprehensive initial survey of 617 patients displaying chronic human pathologies. Multiple disease specific abnormalities were identified in plasma, whole blood and/or urine. This is the case for vitamins and oligo elements, vitamin C, vitamin E, β -carotene, se lenium, zinc and copper; endogenous antioxidants such as reduced and oxidised glutathione, thiols, urate, and glutathione peroxidase activity , and a biomarker of oxidative DNA damage (8-hydroxy-2’-deoxy guanosine). The distinct biomarker profiles suggest the involvment of multiple forms of oxidative insults which are in some way partially specific to each pathological condition. This finding is in favor of the determination of an integrated score to combine contributions of distinct biomarkers, in order to screen patients presenting elevated levels of oxidative stress.
Halliwell, B. and Gutteridge, J.M. (1989) Free radicals in biology and medicine. Clarendon Press, Oxford.
Van Lenten, B.J., Navab, M., Shih, D., Fogelman, A.M. and Lusis, A.J. (2001) The role of high-density lipoproteins in oxidation and inflammation. Trends in Cardiovascular Medicine, 11, 155-161. doi:10.1016/S1050-1738(01)00095-0
Stocker, R. and Keaney Jr., J.F. (2004) Role of oxidative modifications in atherosclerosis. Trends in Cardiovascular Medicine, 84, 1381-1478. doi:10.1152/physrev.00047.2003
Barnham, K.J., Masters, C.L. and Bush, A.I. (2004) Neurodegenerative diseases and oxidative stress. Nature Reviews Drug Discovery, 3, 205-214. doi:10.1038/nrd1330
Floyd, R.A. and Hensley, K. (2002) Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiology of Aging, 23, 795-807. doi:10.1016/S0197-4580(02)00019-2
Halliwell, B. (1999) Antioxidant defence mechanisms: From the beginning to the end (of the beginning). Free Radical Research, 31, 261-272. doi:10.1080/10715769900300841
Therond, P., Bonnefont-Rousselot, D., Davit-Spraul, A., Conti, M. and Legrand, A. (2000) Biomarkers of oxidative stress: An analytical approach. Current Opinion in Clinical Nutrition & Metabolic Care, 3, 373-384. doi:10.1097/00075197-200009000-00009
Dalle-Donne, I., Rossi, R., Colombo, R., Giustarini, D. and Milzani, A. (2006) Biomarkers of oxidative damage in human disease. Clinical Chemistry, 52, 601-623. doi:10.1373/clinchem.2005.061408
Kadiiska, M.B., Gladen, B.C., Baird, D.D., Germolec, D., Graham, L.B., Parker, C.E., Nyska, A., Wachsman, J.T., Ames, B.N., Basu, S., Brot, N., Fitzgerald, G.A., Floyd, R.A., George, M., Heinecke, J.W., Hatch, G.E., Hensley, K., Lawson, J.A., Marnett, L.J., Morrow, J.D., Murray, D.M., Plastaras, J., Roberts II, L.J., Rokach, J., Shigenaga, M.K., Sohal, R.S., Sun, J., Tice, R.R., Van Thiel, D.H., Wellner, D., Walter, P.B., Tomer, K.B., Mason, R.P. and Barrett, J.C. (2005) Biomarkers of oxidative stress study II: Are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radical Biology & Medicine, 38, 698-710. doi:10.1016/j.freeradbiomed.2004.09.017
Kadiiska, M.B., Gladen, B.C., Baird, D.D., Graham, L.B., Parker, C.E., Ames, B.N., Basu, S., Fitzgerald, G.A., Lawson, J.A., Marnett, L.J., Morrow, J.D., Murray, D.M., Plastaras, J., Roberts II, L.J., Rokach, J., Shigenaga, M.K., Sun, J., Walter, P.B., Tomer, K.B., Barrett, J.C. and Mason, R.P. (2005) Biomarkers of oxidative stress study III. Effects of the nonsteroidal anti-inflammatory agents indomethacin and meclofenamic acid on measurements of oxidative products of lipids in CCl4 poisoning. Free Radical Biology and Medicine, 38, 711-718. doi:10.1016/j.freeradbiomed.2004.10.024
Witztum, J.L. and Steinberg, D. (2001) The oxidative modification hypothesis of atherosclerosis: Does it hold for humans? Trends in Cardiovascular Medicine, 11, 93- 102. doi:10.1016/S1050-1738(01)00111-6
Heinecke, J.W. (2001) Is the emperor wearing clothes? Clinical trials of vitamin E and the LDL oxidation hypothesis. Arteriosclerosis, Thrombosis, and Vascular Biology, 21, 1261-1264. doi:10.1161/hq0801.095084
Hercberg, S., Galan, P., Preziosi, P., Bertrais, S., Mennen, L., Malvy, D., Roussel, A.M., Favier, A. and Briancon, S. (2004) The SU.VI.MAX Study: A randomized, placebocontrolled trial of the health effects of antioxidant vitamins and minerals. Archives of Internal Medicine, 164, 2335-2342. doi:10.1001/archinte.164.21.2335
Omaye, S.T., Turnbull, J.D. and Sauberlich, H.E. (1979) Selected methods for the determination of ascorbic acid in animal cells, tissues, and fluids. Methods in Enzymology, 62, 3-11. doi:10.1016/0076-6879(79)62181-X
Zhao, B., Tham, S.Y., Lu, J., Lai, M.H., Lee, L.K. and Moochhala, S.M. (2004) Simultaneous determination of vitamins C, E and beta-carotene in human plasma by high-performance liquid chromatography with photodiode-array detection. Journal of Pharmaceutical Sciences, 7, 200-204.
Sturup, S., Hayes, R.B. and Peters, U. (2005) Development and application of a simple routine method for the determination of selenium in serum by octopole reaction system ICPMS. Analytical and Bioanalytical Chemistry, 381, 686-694. doi:10.1007/s00216-004-2946-x
Tietze, F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Analytical Biochemistry, 27, 502-522. doi:10.1016/0003-2697(69)90064-5
Motchnik, P.A., Frei, B. and Ames, B.N. (1994) Measurement of antioxidants in human blood plasma. Methods in Enzymology, 234, 269-279. doi:10.1016/0076-6879(94)34094-3
Hoffman, M. (2011) Hypothesis: Hyperhomocysteinemia is an indicator of oxidant stress. Medical Hypotheses, 77, 1088-1093. doi:10.1016/j.mehy.2011.09.009
Wayner, D.D., Burton, G.W., Ingold, K.U., Barclay, L.R. and Locke, S.J. (1987) The relative contributions of vitamin E, urate, ascorbate and proteins to the total peroxyl radical-trapping antioxidant activity of human blood plasma. Biochimica et Biophysica Acta, 924, 408-419. doi:10.1016/0304-4165(87)90155-3
Balcerczyk, A., Grzelak, A., Janaszewska, A., Jakubowski, W., Koziol, S., Marszalek, M., Rychlik, B., Soszynski, M., Bilinski, T. and Bartosz, G. (2003) Thiols as major determinants of the total antioxidant capacity. Biofactors, 17, 75-82. doi:10.1002/biof.5520170108
Kuzuya, M., Ando, F., Iguchi, A. and Shimokata, H. (2002) Effect of aging on serum uric acid levels: Longitudinal changes in a large Japanese population group. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 57, M660-M664. doi:10.1093/gerona/57.10.M660
Hak, A.E. and Choi, H.K. (2008) Menopause, postmenopausal hormone use and serum uric acid levels in US women—The third national health and nutrition examination survey. Arthritis Research & Therapy, 10, R116. doi:10.1186/ar2519
Sautin, Y.Y. and Johnson, R.J. (2008) Uric acid: The oxidant-antioxidant paradox. Nucleosides, Nucleotides and Nucleic Acids, 27, 608-619. doi:10.1080/15257770802138558
Zaman, Z., Roche, S., Fielden, P., Frost, P.G., Niriella, D.C. and Cayley, A.C. (1992) Plasma concentrations of vitamins A and E and carotenoids in Alzheimer’s disease. Age Ageing, 21, 91-94. doi:10.1093/ageing/21.2.91
Schippling, S., Kontush, A., Arlt, S., Buhmann, C., Sturenburg, H.J., Mann, U., Muller-Thomsen, T. and Beisiegel, U. (2000) Increased lipoprotein oxidation in Alzheimer’s disease. Free Radical Biology & Medicine, 28, 351-360. doi:10.1016/S0891-5849(99)00247-6
Mecocci, P., Polidori, M.C., Cherubini, A., Ingegni, T., Mattioli, P., Catani, M., Rinaldi, P., Cecchetti, R., Stahl, W., Senin, U. and Beal, M.F. (2002) Lymphocyte oxidative DNA damage and plasma antioxidants in Alzheimer disease. Archives of Neurology, 59, 794-798. doi:10.1001/archneur.59.5.794
Polidori, M.C. and Mecocci, P. (2002) Plasma susceptibility to free radical-induced antioxidant consumption and lipid peroxidation is increased in very old subjects with Alzheimer disease. Journal of Alzheimer’s Disease, 4, 517-522.
Besler, H.T., Comoglu, S. and Okcu, Z. (2002) Serum levels of antioxidant vitamins and lipid peroxidation in multiple sclerosis. Nutritional Neuroscience, 5, 215-220. doi:10.1080/10284150290029205
Jimenez-Jimenez, F.J., Molina, J.A., de Bustos, F., Orti-Pareja, M., Benito-Leon, J., Tallon-Barranco, A., Gasalla, T., Porta, J. and Arenas, J. (1999) Serum levels of betacarotene, alpha-carotene and vitamin A in patients with Alzheimer’s disease. European Journal of Neurology, 6, 495-497. doi:10.1046/j.1468-1331.1999.640495.x
Buhmann, C., Arlt, S., Kontush, A., Moller-Bertram, T., Sperber, S., Oechsner, M., Stuerenburg, H.J. and Bei- siegel, U. (2004) Plasma and CSF markers of oxidative stress are increased in Parkinson’s disease and influenced by antiparkinsonian medication. Neurobiology of Disease, 15, 160-170. doi:10.1016/j.nbd.2003.10.003
Palm, R. and Hallmans, G. (1982) Zinc and copper in multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry, 45, 691-698. doi:10.1136/jnnp.45.8.691
Jimenez-Jimenez, F.J., Fernandez-Calle, P., Martinez-Vanaclocha, M., Herrero, E., Molina, J.A., Vazquez, A. and Codoceo, R. (1992) Serum levels of zinc and copper in patients with Parkinson’s disease. Journal of the Neurological Sciences, 112, 30-33. doi:10.1016/0022-510X(92)90127-7
Bush, A.I. and Strozyk, D. (2004) Serum copper: A biomarker for Alzheimer disease? Archives of Neurology, 61, 631-632. doi:10.1001/archneur.61.5.631
Tchantchou, F., Graves, M., Ortiz, D., Rogers, E. and Shea, T.B. (2004) Dietary supplementation with apple juice concentrate alleviates the compensatory increase in glutathione synthase transcription and activity that accompanies dietary and genetically-induced oxidative stress. Journal of Nutrition Health and Aging, 8, 492-496.
Maes, M., De Vos, N., Pioli, R., Demedts, P., Wauters, A., Neels, H. and Christophe, A. (2000) Lower serum vitamin E concentrations in major depression. Another marker of lowered antioxidant defenses in that illness. Journal of Affective Disorders, 58, 241-246. doi:10.1016/S0165-0327(99)00121-4
Tiemeier, H., Hofman, A., Kiliaan, A.J., Meijer, J. and Breteler, M.M. (2002) Vitamin E and depressive symptoms are not related. The Rotterdam Study. Journal of Affective Disorders, 72, 79-83. doi:10.1016/S0165-0327(01)00427-X
Bilici, M., Efe, H., Koroglu, M.A., Uydu, H.A., Bekaroglu, M. and Deger, O. (2001) Antioxidative enzyme activities and lipid peroxidation in major depression: Alterations by antidepressant treatments. Journal of Affective Disorders, 64, 43-51. doi:10.1016/S0165-0327(00)00199-3
Tarp, U., Stengaard-Pedersen, K., Hansen, J.C. and Thorling, E.B. (1992) Glutathione redox cycle enzymes and selenium in severe rheumatoid arthritis: Lack of antioxidative response to selenium supplementation in polymorphonuclear leucocytes. Annals of the Rheumatic Diseases, 51, 1044-1049. doi:10.1136/ard.51.9.1044
Hassan, M.Q., Hadi, R.A., Al-Rawi, Z.S., Padron, V.A. and Stohs, S.J. (2001) The glutathione defense system in the pathogenesis of rheumatoid arthritis. Journal of Applied Toxicology, 21, 169-173. doi:10.1002/jat.736
Surapaneni, K.M. and Venkataramana, G. (2007) Status of lipid peroxidation, glutathione, ascorbic acid, vitamin E and antioxidant enzymes in patients with osteoarthritis. Indian Journal of Medical Sciences, 61, 9-14. doi:10.4103/0019-5359.29592
Mulherin, D.M., Thurnham, D.I. and Situnayake, R.D. (1996) Glutathione reductase activity, riboflavin status, and disease activity in rheumatoid arthritis. Annals of the Rheumatic Diseases, 55, 837-840. doi:10.1136/ard.55.11.837
Honkanen, V., Konttinen, Y.T., Sorsa, T., Hukkanen, M., Kemppinen, P., Santavirta, S., Saari, H. and Westermarck, T. (1991) Serum zinc, copper and selenium in rheumatoid arthritis. Journal of Trace Elements and Electrolytes in Health and Disease, 5, 261-263.
Yazar, M., Sarban, S., Kocyigit, A. and Isikan, U.E. (2005) Synovial fluid and plasma selenium, copper, zinc, and iron concentrations in patients with rheumatoid arthritis and osteoarthritis. Biological Trace Element Research, 106, 123-132. doi:10.1385/BTER:106:2:123
Centers for Disease Control and Prevention (CDC), National Center for Health Statistics (NCHS) (2002) National Health and Nutrition Examination Survey Questionnaire. Hyattsville. http://www.cdc.gov/nchs/about/major/nhanes/nhanes01-02.htm
Jordao Jr., A.A., Silveira, S., Figueiredo, J.F. and Vannucchi, H. (1998) Urinary excretion and plasma vitamin E levels in patients with AIDS. Nutrition, 14, 423-426. doi:10.1016/S0899-9007(98)00012-4
Baum, M., Cassetti, L., Bonvehi, P., Shor-Posner, G., Lu, Y. and Sauberlich, H. (1994) Inadequate dietary intake and altered nutrition status in early HIV-1 infection. Nutrition, 10, 16-20.
Delmas-Beauvieux, M.C., Peuchant, E., Couchouron, A., Constans, J., Sergeant, C., Simonoff, M., Pellegrin, J.L., Leng, B., Conri, C. and Clerc, M. (1996) The enzymatic antioxidant system in blood and glutathione status in human immunodeficiency virus (HIV)-infected patients: Effects of supplementation with selenium or beta-caro-tene. American Journal of Clinical Nutrition, 64, 101-107.
Jahoor, F., Jackson, A., Gazzard, B., Philips, G., Sharpstone, D., Frazer, M.E. and Heird, W. (1999) Erythrocyte glutathione deficiency in symptom-free HIV infection is associated with decreased synthesis rate. American Journal of Physiology, 276, E205-E211.
Von Herbay, A., Stahl, W., Niederau, C., von Laar, J., Strohmeyer, G. and Sies, H. (1996) Diminished plasma levels of vitamin E in patients with severe viral hepatitis. Free Radical Research, 25, 461-466. doi:10.3109/10715769609149068
Jain, S.K., Pemberton, P.W., Smith, A., McMahon, R.F., Burrows, P.C., Aboutwerat, A. and Warnes, T.W. (2002) Oxidative stress in chronic hepatitis C: Not just a feature of late stage disease. Journal of Hepatology, 36, 805-811. doi:10.1016/S0168-8278(02)00060-0
Swietek, K. and Juszczyk, J. (1997) Reduced glutathione concentration in erythrocytes of patients with acute and chronic viral hepatitis. Journal of Viral Hepatitis, 4, 139-141.
Loguercio, C., Blanco, F.D., De Girolamo, V., Disalvo, D., Nardi, G., Parente, A. and Blanco, C.D. (1999) Ethanol consumption, amino acid and glutathione blood levels in patients with and without chronic liver disease. Alco- holism: Clinical and Experimental Research, 23, 1780- 1784. doi:10.1111/j.1530-0277.1999.tb04073.x
Toyokuni, S. (2008) Molecular mechanisms of oxidative stress-induced carcinogenesis: From epidemiology to oxygenomics. International Union of Biochemistry and Molecular Biology, 60, 441-447. doi:10.1002/iub.61
Gupte, A. and Mumper, R.J. (2009) Elevated copper and oxidative stress in cancer cells as a target for cancer treatment. Cancer Treatment Reviews, 35, 32-46. doi:10.1016/j.ctrv.2008.07.004
Ménézo, Y., Entezami, F., Lichtblau, I., Belloc, S., Cohen, M. and Dale, B. (2012) Oxidative stress and fertility: Incorrect assumptions and ineffective solutions? Zygote, 12, 1-11. doi:10.1017/S0967199412000263
Bjelakovic, G., Nikolova, D., Gluud, L.L., Simonetti, R.G. and Gluud, C. (2008) Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database of Systematic Reviews, 16, Article ID: CD007176.