Sperm Redox System Equilibrium: Implications for Fertilization and Male Fertility.
Glutathione peroxidase
Glutathione transferase
Oxidative regulation
ROS
Sperm maturation
Spermatozoa
Testis thioredoxin system
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
31
5
2022
pubmed:
1
6
2022
medline:
3
6
2022
Statut:
ppublish
Résumé
Structural and regulatory requirements of mammalian spermatozoa in both development and function make them extremely unique cells. Looking at the complexity of spermatozoon structure and its requirements for both motility and quick breakdown within the post-fertilization environment, as well as its functional needs as an extremely streamlined cell with high energy requirements, demonstrate the high importance of oxidative-reductive processes. The oxidative state of the testis and epididymis during sperm development and maturation highly influences sperm structure, with a high dependence on disulfide bond formation, facilitated by thiol mediated processes. However, once functionally active, sperm transition to a new high-risk functional paradigm requiring low levels of reactive oxygen species (ROS) while also being highly susceptible to oxidative damage due to the high proportion of polyunsaturated fatty acids within the lipid bilayer of the plasmalemma and the lack of cytosolic antioxidant defenses. This chapter highlights how glutathione and thioredoxin systems mediate the oxidative environment of the male reproductive tract and facilitate the successful development, maturation and function of mammalian spermatozoa.
Identifiants
pubmed: 35641877
doi: 10.1007/978-3-030-89340-8_15
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
345-367Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Aitken RJ, Baker MA, Nixon B. Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress? Asian J Androl. 2015;17(4):633.
pubmed: 25999358
pmcid: 4492056
doi: 10.4103/1008-682X.153850
Aitken RJ. The capacitation-apoptosis highway: oxysterols and mammalian sperm function. Biol Reprod. 2011;85(1):9–12.
pubmed: 21490245
doi: 10.1095/biolreprod.111.092528
Meister A, Larsson A. Glutathione synthetase deficiency and other disorders of the gamma-glutamyl cycle. Metab Mol Bases Inherit Dis. 1995;1:1461–95.
Meister A. Glutathione; metabolism and function via the γ-glutamyl cycle. Life Sci. 1974;15(2):177–90.
pubmed: 4620960
doi: 10.1016/0024-3205(74)90206-9
Pastore A, Federici G, Bertini E, Piemonte F. Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta. 2003;333(1):19–39.
pubmed: 12809732
doi: 10.1016/S0009-8981(03)00200-6
Meister A, Anderson ME. Glutathione. Annu Rev Biochem. 1983;52(1):711–60.
pubmed: 6137189
doi: 10.1146/annurev.bi.52.070183.003431
Sies H. Glutathione and its role in cellular functions. Free Radic Biol Med. 1999;27(9–10):916–21.
pubmed: 10569624
doi: 10.1016/S0891-5849(99)00177-X
Dickinson DA, Forman HJ. Glutathione in defense and signaling: lessons from a small thiol. Ann N Y Acad Sci. 2002;973(1):488–504.
pubmed: 12485918
doi: 10.1111/j.1749-6632.2002.tb04690.x
Grosshans K, Calvin HI. Estimation of glutathione in purified populations of mouse testis germ cells. Biol Reprod. 1985;33(5):1197–205.
pubmed: 4074809
doi: 10.1095/biolreprod33.5.1197
Teaf CM, Harbison RD, Bishop JB. Germ-cell mutagenesis and GSH depression in reproductive tissue of the F-344 rat induced by ethyl methanesulfonate. Mutat Res Lett. 1985;144(2):93–8.
doi: 10.1016/0165-7992(85)90009-0
Mushahwar IK, Koeppe RE. Free amino acids of testes. Concentrations of free amino acids in the testes of several species and the precursors of glutamate and glutamine in rat testes in vivo. Biochem J. 1973;132(3):353–9.
pubmed: 4724582
pmcid: 1177598
doi: 10.1042/bj1320353
Kochakian CD. Free amino acids of sex organs of the mouse: regulation by androgen. Am J Physiol Content. 1975;228(4):1231–5.
doi: 10.1152/ajplegacy.1975.228.4.1231
Gualtieri AF, Iwachow MA, Venara M, Rey RA, Schteingart HF. Bisphenol A effect on glutathione synthesis and recycling in testicular Sertoli cells. J Endocrinol Investig. 2011;34(5):e102–9.
doi: 10.1007/BF03347468
Li L, Seddon AP, Meister A, Risley MS. Spermatogenic cell-somatic cell interactions are required for maintenance of spermatogenic cell glutathione. Biol Reprod. 1989;40(2):317–31.
pubmed: 2720029
doi: 10.1095/biolreprod40.2.317
Den Boer PJ, Mackenbach P, Grootegoed JA. Glutathione metabolism in cultured Sertoli cells and spermatogenic cells from hamsters. Reproduction. 1989;87(1):391–400.
doi: 10.1530/jrf.0.0870391
Kaneko T, et al. The expression of glutathione reductase in the male reproductive system of rats supports the enzymatic basis of glutathione function in spermatogenesis. Eur J Biochem. 2002;269(5):1570–8.
pubmed: 11874473
doi: 10.1046/j.1432-1033.2002.02809.x
Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. Reproduction. 1987;81(2):459–69.
doi: 10.1530/jrf.0.0810459
Aruldhas MM, et al. Chronic chromium exposure-induced changes in testicular histoarchitecture are associated with oxidative stress: study in a non-human primate (Macaca radiata Geoffroy). Hum Reprod. 2005;20(10):2801–13.
pubmed: 15980013
doi: 10.1093/humrep/dei148
Paul C, Teng S, Saunders PTK. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod. 2009;80(5):913–9.
pubmed: 19144962
pmcid: 2709966
doi: 10.1095/biolreprod.108.071779
Celino FT, et al. Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase. PLoS One. 2011;6(2):e16938.
pubmed: 21364994
pmcid: 3041797
doi: 10.1371/journal.pone.0016938
Roveri A, Ursini F, Flohé L, Maiorino M. PHGPx and spermatogenesis. Biofactors. 2001;14:213–22.
pubmed: 11568459
doi: 10.1002/biof.5520140127
Potts RJ, Jefferies TM, Notarianni LJ. Antioxidant capacity of the epididymis. Hum Reprod. 1999;14(10):2513–6.
pubmed: 10527979
doi: 10.1093/humrep/14.10.2513
Colagar AH, Marzony ET. Ascorbic acid in human seminal plasma: determination and its relationship to sperm quality. J Clin Biochem Nutr. 2009;45(2):144–9.
pubmed: 19794921
pmcid: 2735625
doi: 10.3164/jcbn.08-251
Funahashi H, Cantley TC, Stumpf TT, Terlouw SL, Day BN. Use of low-salt culture medium for in vitro maturation of porcine oocytes is associated with elevated oocyte glutathione levels and enhanced male pronuclear formation after in vitro fertilization. Biol Reprod. 1994;51(March):633–9.
pubmed: 7819443
doi: 10.1095/biolreprod51.4.633
Sutovsky P, Schatten G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod. 1997;56(6):1503–12.
pubmed: 9166704
doi: 10.1095/biolreprod56.6.1503
Zuelke KA, Jeffay SC, Zucker RM, Perreault SD. Glutathione (GSH) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes, and pre-implantation stage embryos. Mol Reprod Dev. 2003;64(1):106–12.
pubmed: 12420305
doi: 10.1002/mrd.10214
Kim IH, et al. Effect of exogenous glutathione on the in vitro fertilization of bovine oocytes. Theriogenology. 1999;52(3):537–47.
pubmed: 10734387
doi: 10.1016/S0093-691X(99)00150-8
Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod. 1993;49(1):89–94.
pubmed: 8353194
doi: 10.1095/biolreprod49.1.89
Krisher RL, Bavister BD. Responses of oocytes and embryos to the culture environment. Theriogenology. 1998;49(1):103–14.
pubmed: 10732124
doi: 10.1016/S0093-691X(97)00405-6
Eppig JJ. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev. 1996;8(4):485–9.
pubmed: 8870074
doi: 10.1071/RD9960485
Furnus CC, De Matos DG, Moses DF. Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracellular glutathione level and its role on subsequent embryo development. Mol Reprod Dev. 1998;51(1):76–83.
pubmed: 9712320
doi: 10.1002/(SICI)1098-2795(199809)51:1<76::AID-MRD9>3.0.CO;2-T
de Matos DG, Furnus CC, Moses DF. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod. 1997;57(6):1420–5.
pubmed: 9408249
doi: 10.1095/biolreprod57.6.1420
de Matos DG, Furnus CC. 2000-The importance of having high glutathione.pdf. Theriogenology. 2000;53(3):761–71.
pubmed: 10735042
doi: 10.1016/S0093-691X(99)00278-2
Abeydeera LR, et al. Coculture with follicular shell pieces can enhance the developmental competence of pig oocytes after in vitro fertilization: relevance to intracellular glutathione. Theriogenology. 1998;58(9):1244–56.
Hamilton LE, et al. Sperm-borne glutathione-s-transferase omega 2 accelerates the nuclear decondensation of spermatozoa during fertilization in mice†. Biol Reprod. 2019;101(2):368–76.
pubmed: 31087045
doi: 10.1093/biolre/ioz082
Perreault SD, Wolff RA, Zirkin BR. The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol. 1984;101(1):160–7.
pubmed: 6692970
doi: 10.1016/0012-1606(84)90126-X
Furnus CC, et al. Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim Reprod Sci. 2008;109(1):88–99.
pubmed: 18242890
doi: 10.1016/j.anireprosci.2007.12.003
Curnow EC, Ryan J, Saunders D, Hayes ES. Bovine in vitro oocyte maturation as a model for manipulation of the γ-glutamyl cycle and intraoocyte glutathione. Reprod Fertil Dev. 2008;20(5):579–88.
pubmed: 18577355
doi: 10.1071/RD08041
Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol. 2005;45:51–88.
pubmed: 15822171
doi: 10.1146/annurev.pharmtox.45.120403.095857
Mannervik B, Helena Danielson U, Ketterer B. Glutathione transferases—structure and catalytic activit. Crit Rev Biochem. 1988;23(3):283–337.
doi: 10.3109/10409238809088226
Tew KD, Townsend DM. Glutathione-s-transferases as determinants of cell survival and death. Antioxid Redox Signal. 2012;17(12):1728–37.
pubmed: 22540427
pmcid: 3474190
doi: 10.1089/ars.2012.4640
Raijmakers MTM, et al. Glutathione and glutathione S-transferases A1-1 and P1-1 in seminal plasma may play a role in protecting against oxidative damage to spermatozoa. Fertil Steril. 2003;79(1):169–72.
pubmed: 12524083
doi: 10.1016/S0015-0282(02)04404-7
Hemachand T, Gopalakrishnan B, Salunke DM, Totey SM, Shaha C. Sperm plasma-membrane-associated glutathione S-transferases as gamete recognition molecules. J Cell Sci. 2002;115(10):2053–65.
pubmed: 11973347
doi: 10.1242/jcs.115.10.2053
Petit FM, Serres C, Auer J. Moonlighting proteins in sperm–egg interactions. Biochem Soc Trans. 2014;42(6):1740–3.
pubmed: 25399599
doi: 10.1042/BST20140218
Llavanera M, et al. Exploring seminal plasma GSTM3 as a quality and in vivo fertility biomarker in pigs—relationship with sperm morphology. Antioxidants. 2020;9(8) https://doi.org/10.3390/antiox9080741 .
Gopalakrishnan B, et al. Studies on glutathione S-transferases important for sperm function: evidence of catalytic activity-independent functions. Biochem J. 1998;329(2):231–41.
pubmed: 9425104
pmcid: 1219036
doi: 10.1042/bj3290231
Llavanera M, et al. Deactivation of the JNK pathway by GSTP1 is essential to maintain sperm functionality. Front Cell Dev Biol. 2021;9:627140.
pubmed: 33732696
pmcid: 7959831
doi: 10.3389/fcell.2021.627140
Hamilton LE, Acteau G, Xu W, Sutovsky P, Oko R. The developmental origin and compartmentalization of glutathione-s-transferase omega 2 isoforms in the perinuclear theca of eutherian spermatozoa. Biol Reprod. 2017;97(4):612–21.
pubmed: 29036365
pmcid: 5803777
doi: 10.1093/biolre/iox122
Protopapas N, et al. The perforatorium and postacrosomal sheath of rat spermatozoa share common developmental origins and protein constituents. Biol Reprod. 2019;100(6):1461–72.
pubmed: 30939204
pmcid: 6561862
doi: 10.1093/biolre/ioz052
Hamilton LE, et al. GSTO2 isoforms participate in the oxidative regulation of the plasmalemma in eutherian spermatozoa during capacitation. Antioxidants. 2019;8(12) https://doi.org/10.3390/antiox8120601 .
Yu B, Huang Z. Variations in antioxidant genes and male infertility. Biomed Res Int. 2015:2015.
Tirumala Vani G, et al. Role of glutathione S-transferase Mu-1 (GSTM1) polymorphism in oligospermic infertile males. Andrologia. 2010;42(4):213–7.
pubmed: 20629642
doi: 10.1111/j.1439-0272.2009.00971.x
Aydemir B, Onaran I, Kiziler AR, Alici B, Akyolcu MC. Increased oxidative damage of sperm and seminal plasma in men with idiopathic infertility is higher in patients with glutathione S-transferase Mu-1 null genotype. Asian J Androl. 2007;9(1):108–15.
pubmed: 17187162
doi: 10.1111/j.1745-7262.2007.00237.x
Finotti AC, Costa E, Bordin BM, Silva CT, Moura KK. Glutathione S-transferase M1 and T1 polymorphism in men with idiopathic infertility. Genet Mol Res. 2009;8(3):1093–8.
pubmed: 19768671
doi: 10.4238/vol8-3gmr642
Tang K, et al. Genetic polymorphisms of glutathione S-transferase M1, T1, and P1, and the assessment of oxidative damage in infertile men with varicoceles from northwestern China. J Androl. 2012;33(2):257–63.
pubmed: 21546615
doi: 10.2164/jandrol.110.012468
Wu W, et al. GSTM1 and GSTT1 null polymorphisms and male infertility risk: an updated meta-analysis encompassing 6934 subjects. Sci Rep. 2013;3(1):1–11.
Listowsky I, et al. Human testicular glutathione S-transferases: insights into tissue-specific expression of the diverse subunit classes. Chem Biol Interact. 1998;111:103–12.
pubmed: 9679547
doi: 10.1016/S0009-2797(97)00154-3
Mukhtar H, Lee IP, Bend JR. Glutathione S-transferase activities in rat and mouse sperm and human semen. Biochem Biophys Res Commun. 1978;83(3):1093–8.
pubmed: 708428
doi: 10.1016/0006-291X(78)91507-3
Yu Z, et al. Gene expression profiles in different stages of mouse spermatogenic cells during spermatogenesis. Biol Reprod. 2003;69(1):37–47.
pubmed: 12606389
doi: 10.1095/biolreprod.102.012609
Klys HS, Whillis D, Howard G, Harrison DJ. Glutathione S-transferase expression in the human testis and testicular germ cell neoplasia. Br J Cancer. 1992;66(3):589–93.
pubmed: 1355663
pmcid: 1977959
doi: 10.1038/bjc.1992.319
Yin Z-L, Dahlstrom JE, Le Couteur DG, Board PG. Immunohistochemistry of omega class glutathione S-transferase in human tissues. J Histochem Cytochem. 2001;49(8):983–7.
pubmed: 11457926
doi: 10.1177/002215540104900806
Johansson A-S, Mannervik B. Human glutathione transferase A3-3, a highly efficient catalyst of double-bond isomerization in the biosynthetic pathway of steroid hormones. J Biol Chem. 2001;276(35):33061–5.
pubmed: 11418619
doi: 10.1074/jbc.M104539200
Lantum HBM, Baggs RB, Krenitsky DM, Board PG, Anders MW. Immunohistochemical localization and activity of glutathione transferase zeta (GSTZ1–1) in rat tissues. Drug Metab Dispos. 2002;30(6):616–25.
pubmed: 12019185
doi: 10.1124/dmd.30.6.616
Li J, et al. Systematic mapping and functional analysis of a family of human Epididymal secretory sperm-located proteins*. Mol Cell Proteomics. 2010;9(11):2517–28.
pubmed: 20736409
pmcid: 2984238
doi: 10.1074/mcp.M110.001719
Papp S, Robaire B, Hermo L. Immunocytochemical localization of the Ya, Yc, Yb1, and Yb2 subunits of glutathione S-transferases in the testis and epididymis of adult rats. Microsc Res Tech. 1995;30(1):1–23.
pubmed: 7711317
doi: 10.1002/jemt.1070300102
Sun Z, Wei R, Luo G, Niu R, Wang J. Proteomic identification of sperm from mice exposed to sodium fluoride. Chemosphere. 2018;207:676–81.
pubmed: 29857199
doi: 10.1016/j.chemosphere.2018.05.153
Sun Z, et al. Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Arch Toxicol. 2018;92(1):169–80.
pubmed: 28918527
doi: 10.1007/s00204-017-2054-2
Fulcher KD, Welch JE, Klapper DG, O’Brien DA, Eddy EM. Identification of a unique μ-class glutathione S-transferase in mouse spermatogenic cells. Mol Reprod Dev. 1995;42(4):415–24.
pubmed: 8607970
doi: 10.1002/mrd.1080420407
Oko R, Sutovsky P. Biogenesis of sperm perinuclear theca and its role in sperm functional competence and fertilization. J Reprod Immunol. 2009;83(1–2):2–7.
pubmed: 19883945
doi: 10.1016/j.jri.2009.05.008
Sutovsky P, Manandhar G, Wu A, Oko R. Interactions of sperm perinuclear theca with the oocyte: implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microsc Res Tech. 2003;61(4):362–78.
pubmed: 12811742
doi: 10.1002/jemt.10350
Brigelius-Flohé R, Flohé L. Regulatory phenomena in the glutathione peroxidase superfamily. Antioxid Redox Signal. 2020;33(7):498–516.
pubmed: 31822117
doi: 10.1089/ars.2019.7905
Noblanc A, et al. Glutathione peroxidases at work on Epididymal spermatozoa: an example of the dual effect of reactive oxygen species on mammalian male fertilizing ability. J Androl. 2011;32(6):641–50.
pubmed: 21441427
doi: 10.2164/jandrol.110.012823
Drevet JR. The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol. 2006;250(1–2):70–9.
pubmed: 16427183
doi: 10.1016/j.mce.2005.12.027
Maser RL, Magenheimer BS, Calvet JP. Mouse plasma glutathione peroxidase. cDNA sequence analysis and renal proximal tubular expression and secretion. J Biol Chem. 1994;269(43):27066–73.
pubmed: 7929449
doi: 10.1016/S0021-9258(18)47126-8
Schwaab V, Faure J, Dufaure J, Drevet JR. GPx3: the plasma-type glutathione peroxidase is expressed under androgenic control in the mouse epididymis and vas deferens. Mol Reprod Dev Inc Gamete Res. 1998;51(4):362–72.
doi: 10.1002/(SICI)1098-2795(199812)51:4<362::AID-MRD2>3.0.CO;2-L
Rejraji H, Vernet P, Drevet JR. GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Mol Reprod Dev Inc Gamete Res. 2002;63(1):96–103.
doi: 10.1002/mrd.10136
de Haan JB, et al. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J Biol Chem. 1998;273(35):22528–36.
pubmed: 9712879
doi: 10.1074/jbc.273.35.22528
Morel Y, Barouki R. Repression of gene expression by oxidative stress. Biochem J. 1999;342(3):481–96.
pubmed: 10477257
pmcid: 1220487
doi: 10.1042/bj3420481
Meseguer M, et al. Effect of sperm glutathione peroxidases 1 and 4 on embryo asymmetry and blastocyst quality in oocyte donation cycles. Fertil Steril. 2006;86(5):1376–85.
pubmed: 16979635
doi: 10.1016/j.fertnstert.2006.03.053
Ursini F, Maiorino M. Lipid peroxidation and ferroptosis: the role of GSH and GPx4. Free Radic Biol Med. 2020;152(March):175–85.
pubmed: 32165281
doi: 10.1016/j.freeradbiomed.2020.02.027
Li L, et al. Ferroptosis is associated with oxygen-glucose deprivation/reoxygenation-induced Sertoli cell death. Int J Mol Med. 2018;41(5):3051–62.
pubmed: 29436589
Zhao X, et al. Inhibition of ferroptosis attenuates busulfan-induced oligospermia in mice. Toxicology. 2020;440:152489.
pubmed: 32416107
doi: 10.1016/j.tox.2020.152489
Ursini F, et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science (80-). 1999;285(5432):1393–6.
doi: 10.1126/science.285.5432.1393
Flohe L (2007) Selenium in mammalian spermiogenesis.
doi: 10.1515/BC.2007.112
Schneider M, et al. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J. 2009;23(9):3233–42.
pubmed: 19417079
doi: 10.1096/fj.09-132795
Fisher HM, Aitken RJ. Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J Exp Zool. 1997;277(5):390–400.
pubmed: 9127958
doi: 10.1002/(SICI)1097-010X(19970401)277:5<390::AID-JEZ5>3.0.CO;2-K
Shalgi R, Seligman J, Kosower NS. Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol Reprod. 1989;40(5):1037–45.
pubmed: 2765609
doi: 10.1095/biolreprod40.5.1037
Puglisi R, et al. The nuclear form of glutathione peroxidase 4 is associated with sperm nuclear matrix and is required for proper paternal chromatin decondensation at fertilization. J Cell Physiol. 2012;227(4):1420–7.
pubmed: 21618532
doi: 10.1002/jcp.22857
Pfeifer H, et al. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J. 2001;15(7):1236–8.
pubmed: 11344099
doi: 10.1096/fj.00-0655fje
Ghyselinck NB, et al. Structural organization and regulation of the gene for the androgen-dependent glutathione peroxidase-like protein specific to the mouse epididymis. Mol Endocrinol. 1993;7(2):258–72.
pubmed: 8469239
Vernet P, Faure J, Dufaure J, Drevet JR. Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase. Mol Reprod Dev Inc Gamete Res. 1997;47(1):87–98.
doi: 10.1002/(SICI)1098-2795(199705)47:1<87::AID-MRD12>3.0.CO;2-X
Chabory E, et al. Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest. 2009;119(7):2074–85.
pubmed: 19546506
pmcid: 2701883
Ahsan U, et al. Role of selenium in male reproduction—a review. Anim Reprod Sci. 2014;146(1–2):55–62.
pubmed: 24613013
doi: 10.1016/j.anireprosci.2014.01.009
Sprinker LH, Harr JR, Newberne PM, Whanger PD, Weswig PH. Selenium deficiency lesions in rats fed vitamin E supplemented rations. Nutr Rep Int. 1971;4(6):335–40.
Olson GE, Winfrey VP, NagDas SK, Hill KE, Burk RF. Selenoprotein P is required for mouse sperm development. Biol Reprod. 2005;73(1):201–11.
pubmed: 15744015
doi: 10.1095/biolreprod.105.040360
Olson GE, Winfrey VP, NagDas SK, Hill KE, Burk RF. Apolipoprotein E receptor-2 (ApoER2) mediates selenium uptake from selenoprotein P by the mouse testis. J Biol Chem. 2007;282(16):12290–7.
pubmed: 17314095
doi: 10.1074/jbc.M611403200
Kehr S, et al. X-ray fluorescence microscopy reveals the role of selenium in spermatogenesis. J Mol Biol. 2009;389(5):808–18.
pubmed: 19379757
pmcid: 2778597
doi: 10.1016/j.jmb.2009.04.024
Gladyshev VN, et al. Selenocysteine-containing Thioredoxin reductase in C. elegans. Biochem Biophys Res Commun. 1999;259(2):244–9.
pubmed: 10362494
doi: 10.1006/bbrc.1999.0765
Arnér ESJ, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem. 2000;267(20):6102–9.
pubmed: 11012661
doi: 10.1046/j.1432-1327.2000.01701.x
Su D, et al. Mammalian Selenoprotein Thioredoxin-glutathione reductase. J Biol Chem. 2005;280(28):26491–8.
pubmed: 15901730
doi: 10.1074/jbc.M503638200
Nayernia K, et al. Asthenozoospermia in mice with targeted deletion of the sperm mitochondrion-associated cysteine-rich protein ( Smcp ) gene. Mol Cell Biol. 2002;22(9):3046–52.
pubmed: 11940662
pmcid: 133774
doi: 10.1128/MCB.22.9.3046-3052.2002
Lee S, Kim SM, Lee RT. Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Antioxidants Redox Signal. 2013;18(10):1165–207.
doi: 10.1089/ars.2011.4322
Moore EC, Reichard P, Thelander L. Synthesis of Deoxyribonucleotides. October. 1964;239(10):3436–44.
Laurent T, Moore EC, Reichard P. Synthesis of Deoxyribonucleotides. October. 1964;239(10):3436–44.
Yodoi J, Tagaya Y, Masutani H, Maeda Y, Kawabe T. IL-2 receptor and Fc epsilon R2 gene activation in lymphocyte transformation: possible roles of ATL-derived factor. Princess Takamatsu Symp. 1988;19:73–86.
pubmed: 2978620
Gasdaska PY, Gasdaska JR, Cochran S, Powis G. Cloning and sequencing of a human thioredoxin reductase. FEBS Lett. 1995;373(1):5–9.
pubmed: 7589432
doi: 10.1016/0014-5793(95)01003-W
Pedrajas JR, et al. Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem. 1999;274(10):6366–73.
pubmed: 10037727
doi: 10.1074/jbc.274.10.6366
Miranda-Vizuete A, Damdimopoulos AE, Pedrajas JR, Gustafsson J-Å, Spyrou G. Human mitochondrial thioredoxin reductase. Eur J Biochem. 1999;261(2):405–12.
pubmed: 10215850
doi: 10.1046/j.1432-1327.1999.00286.x
Spyrou G, Enmark E, Miranda-Vizuete A, Gustafsson JÅ. Cloning and expression of a novel mammalian thioredoxin. J Biol Chem. 1997;272(5):2936–41.
pubmed: 9006939
doi: 10.1074/jbc.272.5.2936
Hanschmann E-M, Godoy JR, Berndt C, Hudemann C, Lillig CH. Thioredoxins, glutaredoxins, and peroxiredoxins--molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling. Antioxid Redox Signal. 2013;19(13):1539–605.
pubmed: 23397885
pmcid: 3797455
doi: 10.1089/ars.2012.4599
Clarke FM, et al. Identification of molecules involved in the ‘early pregnancy factor’ phenomenon. J Reprod Fertil. 1991;93(2):525–39.
pubmed: 1787474
doi: 10.1530/jrf.0.0930525
Salz HK, et al. The Drosophila maternal effect locus deadhead encodes a thioredoxin homolog required for female meiosis and early embryonic development. Genetics. 1994;136(3):1075–86.
pubmed: 7516301
pmcid: 1205864
doi: 10.1093/genetics/136.3.1075
Tirmarche S, Kimura S, Dubruille R, Horard B, Loppin B. Unlocking sperm chromatin at fertilization requires a dedicated egg thioredoxin in Drosophila. Nat Commun. 2016;7:135–9.
doi: 10.1038/ncomms13539
Emelyanov AV, Fyodorov DV. Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin. Genes Dev. 2016;30(24):2651–6.
pubmed: 28031247
pmcid: 5238724
doi: 10.1101/gad.290916.116
Svensson MJ, Chen JD, Pirrotta V, Larsson J. The ThioredoxinT and deadhead gene pair encode testis- and ovary-specific thioredoxins in Drosophila melanogaster. Chromosoma. 2003;112(3):133–43.
pubmed: 14579129
doi: 10.1007/s00412-003-0253-5
Jiménez A, et al. Absolute mRNA levels and transcriptional regulation of the mouse testis-specific thioredoxins. Biochem Biophys Res Commun. 2005;330(1):65–74.
pubmed: 15781233
doi: 10.1016/j.bbrc.2005.02.128
Sadek CM, et al. Characterization of human thioredoxin-like 2: a novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem. 2003;278(15):13133–42.
pubmed: 12569107
doi: 10.1074/jbc.M300369200
Jiménez A, et al. Human spermatid-specific thioredoxin-1 (Sptrx-1) is a two-domain protein with oxidizing activity. FEBS Lett. 2002;530(1–3):79–84.
pubmed: 12387870
doi: 10.1016/S0014-5793(02)03417-8
Sadek CM, et al. Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells. 2001;6(12):1077–90.
pubmed: 11737268
doi: 10.1046/j.1365-2443.2001.00484.x
Miranda-Vizuete A, et al. The mammalian testis-specific Thioredoxin system. Antioxidants Redox Signal. 2004;6(1):25–40.
doi: 10.1089/152308604771978327
Jiménez A, et al. Spermatocyte/spermatid-specific thioredoxin-3, a novel golgi apparatus-associated thioredoxin, is a specific marker of aberrant spermatogenesis. J Biol Chem. 2004;279(33):34971–82.
pubmed: 15181017
doi: 10.1074/jbc.M404192200
Yu Y, Oko R, Miranda-Vizuete A. Developmental expression of spermatid-specific thioredoxin-1 protein: transient association to the longitudinal columns of the fibrous sheath during sperm tail formation. Biol Reprod. 2002;67(5):1546–54.
pubmed: 12390887
doi: 10.1095/biolreprod.102.004838
Ogawa K, et al. Is outer arm dynein intermediate chain 1 multifunctional? Mol Biol Cell. 1996;7(12):1895–907.
pubmed: 8970153
pmcid: 276038
doi: 10.1091/mbc.7.12.1895
Sutovsky P, Navara CS, Schatten G. Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine Fertilization. Biol Reprod. 1996;55(6):1195–205.
pubmed: 8949874
doi: 10.1095/biolreprod55.6.1195
Smith TB, Baker MA, Connaughton HS, Habenicht U, Aitken RJ. Functional deletion of Txndc2 and Txndc3 increases the susceptibility of spermatozoa to age-related oxidative stress. Free Radic Biol Med. 2013;65:872–81.
pubmed: 23707457
doi: 10.1016/j.freeradbiomed.2013.05.021
Ohta E, et al. Identification and characterization of GCP16, a novel Acylated Golgi protein that interacts with GCP170*. J Biol Chem. 2003;278(51):51957–67.
pubmed: 14522980
doi: 10.1074/jbc.M310014200
Brede G, Solheim J, Stang E, Prydz H. Mutants of the protein serine kinase PSKH1 disassemble the Golgi apparatus. Exp Cell Res. 2003;291(2):299–312.
pubmed: 14644153
doi: 10.1016/j.yexcr.2003.07.009
Saitoh M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998;17(9):2596–606.
pubmed: 9564042
pmcid: 1170601
doi: 10.1093/emboj/17.9.2596
Ahlering P, et al. Sperm content of TXNDC8 reflects sperm chromatin structure, pregnancy establishment, and incidence of multiple births after ART. Syst Biol Reprod Med. 2020;66(5):311–21.
pubmed: 32851881
doi: 10.1080/19396368.2020.1801889
Buckman C, et al. Semen levels of spermatid-specific thioredoxin-3 correlate with pregnancy rates in ART couples. PLoS One. 2013;8(5):e61000.
pubmed: 23734172
pmcid: 3667087
doi: 10.1371/journal.pone.0061000
Patel-King RS, Benashski SE, Harrison A, King SM. Two functional Thioredoxins containing redox-sensitive vicinal dithiols from the Chlamydomonas outer dynein arm (∗). J Biol Chem. 1996;271(11):6283–91.
pubmed: 8626422
doi: 10.1074/jbc.271.11.6283
Roymans D, et al. Identification of the tumor metastasis suppressor Nm23-H1/Nm23-R1 as a constituent of the centrosome. Exp Cell Res. 2001;262(2):145–53.
pubmed: 11139339
doi: 10.1006/excr.2000.5087
Pinon VP-B, et al. Cytoskeletal Association of the A and B Nucleoside Diphosphate Kinases of Interphasic but not mitotic human carcinoma cell lines: specific nuclear localization of the B Subunit. Exp Cell Res. 1999;246(2):355–67.
pubmed: 9925751
doi: 10.1006/excr.1998.4318
Nickerson JA, Wells WW. The microtubule-associated nucleoside diphosphate kinase. J Biol Chem. 1984;259(18):11297–304.
pubmed: 6088539
doi: 10.1016/S0021-9258(18)90862-8
O’Flaherty C. Peroxiredoxins: hidden players in the antioxidant defence of human spermatozoa. Basic Clin Androl. 2014;24(1):1–10.
doi: 10.1186/2051-4190-24-1
Rhee SG, Woo HA. Multiple functions of Peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H2O2, and protein chaperones. Antioxid Redox Signal. 2010;15(3):781–94.
doi: 10.1089/ars.2010.3393
Chevallet M, et al. Regeneration of Peroxiredoxins during recovery after oxidative stress: only some overoxidized peroxiredoxins can be reduced during recovery after oxidative stress. J Biol Chem. 2003;278(39):37146–53.
pubmed: 12853451
doi: 10.1074/jbc.M305161200
Manandhar G, et al. Peroxiredoxin 2 and peroxidase enzymatic activity of mammalian spermatozoa. Biol Reprod. 2009;80(6):1168–77.
pubmed: 19208552
doi: 10.1095/biolreprod.108.071738
Yim SH, et al. Identification and characterization of alternatively transcribed form of peroxiredoxin IV gene that is specifically expressed in spermatids of postpubertal mouse testis. J Biol Chem. 2011;286(45):39002–12.
pubmed: 21835919
pmcid: 3234725
doi: 10.1074/jbc.M111.257220
Veal EA, et al. A 2-Cys Peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell. 2004;15(1):129–39.
pubmed: 15225554
doi: 10.1016/j.molcel.2004.06.021