Antioxidants to enhance fertility: Role of eNOS and potential benefits

Pharmacological Research

Volumn 64, Issue 5, 2011, Pages 431-437

  Visioli, Francesco ^a,b   Hagen, Tory M ^a,b  

^a IMDEA FOOD INSTITUTE   (Spain)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Erectile dysfunction; Infertility; Nitric oxide; Pre eclampsia; Reproductive health; Vascular dysfunction

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE DERIVATIVE; PHOSPHOPROTEIN PHOSPHATASE 2A; POLYPHENOL DERIVATIVE; SPHINGOMYELIN PHOSPHODIESTERASE; THIOCTIC ACID;

ADRENERGIC SYSTEM; BLOOD VESSEL TONE; CONCEPTION; DIETARY INTAKE; ENZYME PHOSPHORYLATION; GLUTATHIONE METABOLISM; HUMAN; HYPERTENSION; INFERTILITY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SPERMATOZOON; UNSPECIFIED SIDE EFFECT; VASCULAR DISEASE; VASOMOTOR DISORDER;

EID: 80054974912     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2011.06.021     Document Type: Review

References (97)

1. Gupta S, Agarwal A, Banerjee J, Alvarez JG. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstet Gynecol Surv 2007;62:335-47. (Pubitemid 46624276)
2. Desai N, Sabanegh Jr E, Kim T, Agarwal A. Free radical theory of aging: implications in male infertility. Urology 2010;75:14-9.
3. Lanzafame FM, La Vignera S, Vicari E, Calogero AE. Oxidative stress and medical antioxidant treatment in male infertility. Reprod Biomed Online 2009;19:638-59.
4. Sikka SC. Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J Androl 2004;25:5-18. (Pubitemid 38017778)
5. Zhang Q, Radisavljevic ZM, Siroky MB, Azadzoi KM. Dietary antioxidants improve arteriogenic erectile dysfunction. Int J Androl 2010.
6. Polyzos NP, Mauri D, Tsappi M, Tzioras S, Kamposioras K, Cortinovis I, et al. Combined vitamin C and E supplementation during pregnancy for preeclampsia prevention: a systematic review. Obstet Gynecol Surv 2007;62:202-6. (Pubitemid 46294789)
7. Fiore G, Capasso A. Effects of vitamin E and C on placental oxidative stress: an in vitro evidence for the potential therapeutic or prophylactic treatment of preeclampsia. Med Chem 2008;4:526-30.
8. Rumbold A, Duley L, Crowther CA, Haslam RR. Antioxidants for preventing preeclampsia. Cochrane Database Syst Rev 2008:CD004227.
9. Brune B. Nitric oxide: a short lived molecule stays alive. Pharmacol Res 2010;61:265-8.
10. Pavoine C, Pecker F. Sphingomyelinases: their regulation and roles in cardiovascular pathophysiology. Cardiovasc Res 2009;82:175-83.
11. Feng J, Damrauer SM, Lee M, Sellke FW, Ferran C, Abid MR. Endotheliumdependent coronary vasodilatation requires NADPH oxidase-derived reactive oxygen species. Arterioscler Thromb Vasc Biol 2010;30:1703-10.
12. Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, et al. Aging and endothelial function in normotensive subjects and patients with essential hypertension. Circulation 1995;91:1981-7.
13. Kubo SH, Rector TS, Bank AJ, Williams RE, Heifetz SM. Endotheliumdependent vasodilation is attenuated in patients with heart failure. Circulation 1991;84:1589-96.
14. Drexler H, Hayoz D, Munzel T, Hornig B, Just H, Brunner HR, et al. Endothelial function in chronic congestive heart failure. Am J Cardiol 1992;69:1596-601.
15. Kaiser DR, Billups K, Mason C, Wetterling R, Lundberg JL, Bank AJ. Impaired brachial artery endothelium-dependent and -independent vasodilation in men with erectile dysfunction and no other clinical cardiovascular disease. J Am Coll Cardiol 2004;43:179-84. (Pubitemid 38201141)
16. Guay AT. ED2: erectile dysfunction = endothelial dysfunction. Endocrinol Metab Clin North Am 2007;36:453-63.
17. Palumbo PJ. Metabolic risk factors, endothelial dysfunction, and erectile dysfunction in men with diabetes. Am J Med Sci 2007;334:466-80. (Pubitemid 350306466)
18. Wallis AB, Saftlas AF, Hsia J, Atrash HK. Secular trends in the rates of preeclampsia, eclampsia, and gestational hypertension, United States, 1987-2004. Am J Hypertens 2008;21:521-6. (Pubitemid 351589674)
19. Aardema MW, Oosterhof H, Timmer A, van RI, Aarnoudse JG. Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by pre-eclampsia and small for gestational age fetuses. Placenta 2001;22:405-11. (Pubitemid 32519790)
20. Aardema MW, Saro MC, Lander M, De Wolf BT, Oosterhof H, Aarnoudse JG. Second trimester Doppler ultrasound screening of the uterine arteries differentiates between subsequent normal and poor outcomes of hypertensive pregnancy: two different pathophysiological entities? Clin Sci (Lond) 2004;106:377-82. (Pubitemid 38553585)
21. Brodszki J, Lanne T, Laurini R, Strevens H, Wide-Swensson D, Marsal K. Vascular mechanical properties and endothelial function in pre-eclampsia with special reference to bilateral uterine artery notch. Acta Obstet Gynecol Scand 2008;87:154-62. (Pubitemid 351171540)
22. Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, McLachlan RI. Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum Reprod 2010;25:2415-26.
23. van der LB, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, et al. Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 2000;192:1731-44.
24. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593-615. (Pubitemid 32735142)
25. Kone BC. Protein-protein interactions controlling nitric oxide synthases. Acta Physiol Scand 2000;168:27-31. (Pubitemid 30128664)
26. Minshall RD, Sessa WC, Stan RV, Anderson RG, Malik AB. Caveolin regulation of endothelial function. Am J Physiol Lung Cell Mol Physiol 2003;285:L11179.
27. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999;399:597-601.
28. Fulton D, Babbitt R, Zoellner S, Fontana J, Acevedo L, McCabe TJ, et al. Targeting of endothelial nitric-oxide synthase to the cytoplasmic face of the Golgi complex or plasma membrane regulates Akt-versus calcium-dependent mechanisms for nitric oxide release. J Biol Chem 2004;279:30349-57. (Pubitemid 38937962)
29. Smith AR, Visioli F, Hagen TM. Plasma membrane-associated endothelial nitric oxide synthase and activity in aging rat aortic vascular endothelia markedly decline with age. Arch Biochem Biophys 2006;454:100-5. (Pubitemid 44427736)
30. Smith AR, Visioli F, Frei B, Hagen TM. Age-related changes in endothelial nitric oxide synthase phosphorylation and nitric oxide dependent vasodilation: evidence for a novel mechanism involving sphingomyelinase and ceramideactivated phosphatase 2A. Aging Cell 2006;5:391-400. (Pubitemid 44322535)
31. Zhu Y, Liao HL, Niu XL, Yuan Y, Lin T, Verna L, et al. Low density lipoprotein induces eNOS translocation to membrane caveolae: the role of RhoA activation and stress fiber formation. Biochim Biophys Acta 2003;1635:117-26. (Pubitemid 38068277)
32. Ullrich V, Bachschmid M. Superoxide as a messenger of endothelial function. Biochem Biophys Res Commun 2000;278:1-8.
33. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000;87:840-4.
34. Drew B, Leeuwenburgh C. Aging and the role of reactive nitrogen species. Ann N Y Acad Sci 2002;959:66-81. (Pubitemid 34457553)
35. Levine GN, Frei B, Koulouris SN, Gerhard MD, Keaney Jr JF, Vita JA. Ascorbic acid reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation 1996;93:1107-13. (Pubitemid 26087013)
36. Taddei S, Virdis A, Ghiadoni L, Magagna A, Salvetti A. Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. Circulation 1998;97:2222-9. (Pubitemid 28265383)
37. Gokce N, Keaney Jr JF, Frei B, Holbrook M, Olesiak M, Zachariah BJ, et al. Longterm ascorbic acid administration reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation 1999;99:3234-40. (Pubitemid 29293432)
38. Huang A, Vita JA, Venema RC, Keaney Jr JF. Ascorbic acid enhances endothelial nitric-oxide synthase activity by increasing intracellular tetrahydrobiopterin. J Biol Chem 2000;275:17399-406. (Pubitemid 30430776)
39. Heller R, Munscher-Paulig F, Grabner R, Till U. l-Ascorbic acid potentiates nitric oxide synthesis in endothelial cells. J Biol Chem 1999;274:8254-60.
40. Visioli F, Smith A, Zhang W, Keaney Jr JF, Hagen T, Frei B. Lipoic acid and vitamin C potentiate nitric oxide synthesis in human aortic endothelial cells independently of cellular glutathione status. Redox Rep 2002;7:223-7.
41. Carr A, Frei B. The role of natural antioxidants in preserving the biological activity of endothelium-derived nitric oxide. Free Radic Biol Med 2000;28: 1806-14. (Pubitemid 30628667)
42. Duffy SJ, Gokce N, Holbrook M, Huang A, Frei B, Keaney Jr JF, et al. Treatment of hypertension with ascorbic acid. Lancet 1999;354:2048-9.
43. Forman HJ, Zhang H, Rinna A. Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 2009;30:1-12.
44. Suh JH, Shenvi SV, Dixon BM, Liu H, Jaiswal AK, Liu RM, et al. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci USA 2004;101:3381-6. (Pubitemid 38338203)
45. Lavoie S, Chen Y, Dalton TP, Gysin R, Cuenod M, Steullet P, et al. Curcumin, quercetin, and tBHQ modulate glutathione levels in astrocytes and neurons: importance of the glutamate cysteine ligase modifier subunit. J Neurochem 2009;108:1410-22.
46. Shenvi SV, Smith EJ, Hagen TM. Transcriptional regulation of rat gammaglutamate cysteine ligase catalytic subunit gene is mediated through a distal antioxidant response element. Pharmacol Res 2009;60:229-36.
47. Feelisch M, Kotsonis P, Siebe J, Clement B, Schmidt HH. The soluble guanylyl cyclase inhibitor 1H- [1, 2, 4]oxadiazolo [4, 3, -a] quinoxalin-1-one is a nonselective heme protein inhibitor of nitric oxide synthase and other cytochrome P-450 enzymes involved in nitric oxide donor bioactivation. Mol Pharmacol 1999;56:243-53. (Pubitemid 29347599)
48. Ceron PI, Cremonez DC, Bendhack LM, Tedesco AC. The relaxation induced by S-nitroso-glutathione and S-nitroso-N-acetylcysteine in rat aorta is not related to nitric oxide production. J Pharmacol Exp Ther 2001;298:686-94. (Pubitemid 32673421)
49. Cornell TT, Hinkovska-Galcheva V, Sun L, Cai Q, Hershenson MB, Vanway S, et al. Ceramide-dependent PP2A regulation of TNFalpha-induced IL-8 production in respiratory epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009;296: L8849.
50. Rutkute K, Asmis RH, Nikolova-Karakashian MN. Regulation of neutral sphingomyelinase-2 by GSH: a new insight to the role of oxidative stress in aging-associated inflammation. J Lipid Res 2007;48:2443-52. (Pubitemid 350058755)
51. Martin SF, Sawai H, Villalba JM, Hannun YA. Redox regulation of neutral sphingomyelinase-1 activity in HEK293 cells through a GSH-dependent mechanism. Arch Biochem Biophys 2007;459:295-300. (Pubitemid 46367841)
52. Marchesini N, Hannun YA. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 2004;82:27-44. (Pubitemid 38580872)
53. Liu B, Andrieu-Abadie N, Levade T, Zhang P, Obeid LM, Hannun YA. Glutathione regulation of neutral sphingomyelinase in tumor necrosis factor-alpha-induced cell death. J Biol Chem 1998;273:11313-20. (Pubitemid 28204985)
54. Sen CK, Roy S, Han D, Packer L. Regulation of cellular thiols in human lymphocytes by alpha-lipoic acid: a flow cytometric analysis. Free Radic Biol Med 1997;22:1241-57. (Pubitemid 27171967)
55. Packer L. Alpha-lipoic acid: a metabolic antioxidant which regulates NF-kappa B signal transduction and protects against oxidative injury. Drug Metab Rev 1998;30:245-75. (Pubitemid 28266862)
56. Hagen TM, Vinarsky V, Wehr CM, Ames BN. (R)-alpha-lipoic acid reverses the age-associated increase in susceptibility of hepatocytes to tertbutylhydroperoxide both in vitro and in vivo. Antioxid Redox Signal 2000;2:473-83.
57. Bharat S, Cochran BC, Hsu M, Liu J, Ames BN, Andersen JK. Pre-treatment with R-lipoic acid alleviates the effects of GSH depletion in PC12 cells: implications for Parkinson's disease therapy. Neurotoxicology 2002;23:479-86. (Pubitemid 36527668)
58. Moini H, Tirosh O, Park YC, Cho KJ, Packer L. R-alpha-lipoic acid action on cell redox status, the insulin receptor, and glucose uptake in 3T3-L1 adipocytes. Arch Biochem Biophys 2002;397:384-91. (Pubitemid 34852307)
59. Smith AR, Visioli F, Frei B, Hagen TM. Lipoic acid significantly restores, in rats, the age-related decline in vasomotion. Br J Pharmacol 2008;153:1615-22. (Pubitemid 351535993)
60. Ziegler D, Reljanovic M, Mehnert H, Gries FA. Alpha-lipoic acid in the treatment of diabetic polyneuropathy in Germany: current evidence from clinical trials. Exp Clin Endocrinol Diabetes 1999;107:421-30.
61. The Local Food Nutraceutical Consortium. Understanding local Mediterranean diets: a multidisciplinary pharmacological and ethnobotanical approach. Pharmacol Res 2005;52:353-66.
62. Rossoni G, Grande S, Galli C, Visioli F. Wild artichoke prevents the ageassociated loss of vasomotor function. J Agric Food Chem 2005;53:10291-6. (Pubitemid 43081249)
63. Grande S, Bogani P, de Saizieu A, Schueler G, Galli C, Visioli F. Vasomodulating potential of Mediterranean wild plant extracts. J Agric Food Chem 2004;52:5021-6.
64. Heller R, Unbehaun A, Schellenberg B, Mayer B, Werner-Felmayer G, Werner ER. l-ascorbic acid potentiates endothelial nitric oxide synthesis via a chemical stabilization of tetrahydrobiopterin. J Biol Chem 2001;276:40-7. (Pubitemid 32050286)
65. Deka A, Vita JA. Tea and cardiovascular disease. Pharmacol Res 2011;64:136-45.
66. Heiss C, Kleinbongard P, Dejam A, Perre S, Schroeter H, Sies H, et al. Acute consumption of flavanol-rich cocoa and the reversal of endothelial dysfunction in smokers. J Am Coll Cardiol 2005;46:1276-83.
67. Pignatelli P, Di Santo S, Buchetti B, Sanguigni V, Brunelli A, Violi F. Polyphenols enhance platelet nitric oxide by inhibiting protein kinase C-dependent NADPH oxidase activation: effect on platelet recruitment. FASEB J 2006;20:1082-9. (Pubitemid 44943904)
68. Pignatelli P, Ghiselli A, Buchetti B, Carnevale R, Natella F, Germano G, et al. Polyphenols synergistically inhibit oxidative stress in subjects given red and white wine. Atherosclerosis 2006;188:77-83. (Pubitemid 44142538)
69. Hermann F, Spieker LE, Ruschitzka F, Sudano I, Hermann M, Binggeli C, et al. Dark chocolate improves endothelial and platelet function. Heart 2006;92:119-20. (Pubitemid 43021877)
70. Heidelbaugh JJ. Management of erectile dysfunction. Am Fam Physician 2010;81:305-12.
71. Duffy SJ, Keaney Jr JF, Holbrook M, Gokce N, Swerdloff PL, Frei B, et al. Short- and long-term black tea consumption reverses endothelial dysfunction in patients with coronary artery disease. Circulation 2001;104:151-6. (Pubitemid 32655830)
72. Bettuzzi S, Brausi M, Rizzi F, Castagnetti G, Peracchia G, Corti A. Chemoprevention of human prostate cancer by oral administration of green tea catechins in volunteers with high-grade prostate intraepithelial neoplasia: a preliminary report from a one-year proof-of-principle study. Cancer Res 2006;66:1234-40. (Pubitemid 43165995)
73. Richard D, Kefi K, Barbe U, Poli A, Bausero P, Visioli F. Weight and plasma lipid control by decaffeinated green tea. Pharmacol Res 2009;59:351-4.
74. Koca O, Caliskan S, Ozturk MI, Gunes M, Kilicoglu G, Karaman MI. Vasculogenic erectile dysfunction and metabolic syndrome. J Sex Med 2010.
75. Richard D, Kefi K, Barbe U, Bausero P, Visioli F. Polyunsaturated fatty acids as antioxidants. Pharmacol Res 2008;57:451-5.
76. Richard D, Wolf C, Barbe U, Kefi K, Bausero P, Visioli F. Docosahexaenoic acid down-regulates endothelial Nox 4 through a sPLA2 signalling pathway. Biochem Biophys Res Commun 2009;389:516-22.
77. Agarwal A, Said TM. Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU Int 2005;95:503-7. (Pubitemid 40311459)
78. Banfi B, Molnar G, Maturana A, Steger K, Hegedus B, Demaurex N, et al. A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 2001;276:37594-601.
79. Agarwal A, Prabakaran SA, Said TM. Prevention of oxidative stress injury to sperm. J Androl 2005;26:654-60. (Pubitemid 41476621)
80. Safarinejad MR, Hosseini SY, Dadkhah F, Asgari MA. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin Nutr 2010;29:100-5.
81. Schneider M, Forster H, Boersma A, Seiler A, Wehnes H, Sinowatz F, et al. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J 2009;23:3233-42.
82. Drevet JR. The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol 2006;250:70-9.
83. Ursini F, Heim S, Kiess M, Maiorino M, Roveri A, Wissing J, et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999;285:1393-6. (Pubitemid 29411669)
84. Chabory E, Damon C, Lenoir A, Henry-Berger J, Vernet P, Cadet R, et al. Mammalian glutathione peroxidases control acquisition and maintenance of spermatozoa integrity. J Anim Sci 2010;88:1321-31.
85. Conrad M, Schweizer U. Unveiling the molecular mechanisms behind seleniumrelated diseases through knockout mouse studies. Antioxid Redox Signal 2010;12:851-65.
86. Song GJ, Norkus EP, Lewis V. Relationship between seminal ascorbic acid and sperm DNA integrity in infertile men. Int J Androl 2006;29:569-75. (Pubitemid 44800234)
87. Colagar AH, Marzony ET. Ascorbic acid in human seminal plasma: determination and its relationship to sperm quality. J Clin Biochem Nutr 2009;45:144-9.
88. Dawson EB, Harris WA, Rankin WE, Charpentier LA, McGanity WJ. Effect of ascorbic acid on male fertility. Ann NY Acad Sci 1987;498:312-23.
89. Fraga CG, Motchnik PA, Shigenaga MK, Helbock HJ, Jacob RA, Ames BN. Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 1991;88:11003-6. (Pubitemid 21915967)
90. Bansal AK, Bilaspuri GS. Impacts of oxidative stress and antioxidants on semen functions. Vet Med Int 2010:2010.
91. Roseff SJ. Improvement in sperm quality and function with French maritime pine tree bark extract. J Reprod Med 2002;47:821-4. (Pubitemid 35222051)
92. Keskes-Ammar L, Feki-Chakroun N, Rebai T, Sahnoun Z, Ghozzi H, Hammami S, et al. Sperm oxidative stress and the effect of an oral vitamin E and selenium supplement on semen quality in infertile men. Arch Androl 2003;49:83-94. (Pubitemid 36269762)
93. Basu A, Imrhan V. Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur J Clin Nutr 2007;61:295-303. (Pubitemid 46358768)
94. Kavanaugh CJ, Trumbo PR, Ellwood KC. The U.S. Food and Drug Administration's evidence-based review for qualified health claims: tomatoes, lycopene, and cancer. J Natl Cancer Inst 2007;99:1074-85. (Pubitemid 47241392)
95. Goyal A, Chopra M, Lwaleed BA, Birch B, Cooper AJ. The effects of dietary lycopene supplementation on human seminal plasma. BJU Int 2007;99:1456-60. (Pubitemid 47164808)
96. Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod 2011.
97. Gonzales GF, Ruiz A, Gonzales C, Villegas L, Cordova A. Effect of Lepidium meyenii (maca) roots on spermatogenesis of male rats. Asian J Androl 2001;3:231-3. (Pubitemid 32936841)