Physical Activity and Male Reproductive Function: A New Role for Gamete Mitochondria.
Journal
Exercise and sport sciences reviews
ISSN: 1538-3008
Titre abrégé: Exerc Sport Sci Rev
Pays: United States
ID NLM: 0375434
Informations de publication
Date de publication:
01 04 2021
01 04 2021
Historique:
entrez:
15
3
2021
pubmed:
16
3
2021
medline:
21
12
2021
Statut:
ppublish
Résumé
Several studies demonstrated that some types of physical exercise might affect male reproductive potential, even though the potential mechanisms involved in the modulation of sperm quality remain poorly understood. Therefore, we propose a new role for gamete mitochondria as a key hub that coordinates molecular events related to the effects induced by physical exercise.
Identifiants
pubmed: 33720911
doi: 10.1249/JES.0000000000000245
pii: 00003677-202104000-00004
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
99-106Informations de copyright
Copyright © 2021 by the American College of Sports Medicine.
Références
Jóźków P, Rossato M. The impact of intense exercise on semen quality. Am. J. Mens Health . 2017; 11(3):654–62.
Hajizadeh Maleki B, Tartibian B, Chehrazi M. Effects of aerobic, resistance, and combined exercise on markers of male reproduction in healthy human subjects: a randomized controlled trial. J. Strength Cond. Res . 2019; 33(4):1130–45.
Amaral S, Amaral A, Ramalho-Santos J. Aging and male reproductive function: a mitochondrial perspective. Front Biosci (Schol Ed) . 2013; 5:181–97.
Meinhardt A, Wilhelm B, Seitz J. Expression of mitochondrial marker proteins during spermatogenesis. Hum. Reprod. Update . 1999; 5(2):108–19.
Ramalho-Santos J, Amaral S. Mitochondria and mammalian reproduction. Mol. Cell. Endocrinol . 2013; 379(1–2):74–84.
De Martino C, Floridi A, Marcante ML, et al. Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats. Cell Tissue Res . 1979; 196(1):1–22.
Petit JM, Ratinaud MH, Cordelli E, Spanò M, Julien R. Mouse testis cell sorting according to DNA and mitochondrial changes during spermatogenesis. Cytometry . 1995; 19(4):304–12.
Ruiz-Pesini E, Díez-Sánchez C, López-Pérez MJ, Enríquez JA. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr. Top. Dev. Biol . 2007; 77:3–19.
Smith LB, Walke WH. The regulation of spermatogenesis by androgens. Semin. Cell Dev. Biol . 2014; 30:2–13.
Demain LA, Conway GS, Newman WG. Genetics of mitochondrial dysfunction and infertility. Clin. Genet . 2017; 91(2):199–207.
Wells D. Mitochondrial DNA quantity as a biomarker for blastocyst implantation potential. Fertil. Steril . 2017; 108(5):742–7.
Durairajanayagam D, Singh D, Agarwal A, Henkel R. Causes and consequences of sperm mitochondrial dysfunction. Andrologia . 2020; e13666.
Ritchie C, Ko EY. Oxidative stress in the pathophysiology of male infertility. Andrologia . 2020; e13581.
Gaskins AJ, Mendiola J, Afeiche M, Jørgensen N, Swan SH, Chavarro JE. Physical activity and television watching in relation to semen quality in young men. Br. J. Sports Med . 2015; 49(4):265–70.
Rosety MÁ, Díaz AJ, Rosety JM, et al. Exercise improved semen quality and reproductive hormone levels in sedentary obese adults. Nutr. Hosp . 2017; 34(3):603–7.
Hajizadeh Maleki B, Tartibian B, Chehrazi M. The effects of three different exercise modalities on markers of male reproduction in healthy subjects: a randomized controlled trial. Reproduction . 2017; 153(2):157–74.
Hajizadeh Maleki B, Tartibian B. Moderate aerobic exercise training for improving reproductive function in infertile patients: a randomized controlled trial. Cytokine . 2017; 92:55–67.
Sansone A, Sansone M, Vaamonde D, et al. Sport, doping and male fertility. Reprod. Biol. Endocrinol . 2018; 16(1):114.
Safarinejad MR, Azma K, Kolahi AA. The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus-pituitary-testis axis, and semen quality: a randomized controlled study. J. Endocrinol . 2009; 200(3):259–71.
Vaamonde D, Da Silva-Grigoletto ME, García-Manso JM, Vaamonde-Lemos R, Swanson RJ, Oehninger SC. Response of semen parameters to three training modalities. Fertil. Steril . 2009; 92(6):1941–6.
Hajizadeh Maleki B, Tartibian B, Eghbali M, Asri-Rezaei S. Comparison of seminal oxidants and antioxidants in subjects with different levels of physical fitness. Andrology . 2013; 1(4):607–14.
Hajizadeh Maleki B, Tartibian B. Long-term low-to-intensive cycling training: impact on semen parameters and seminal cytokines. Clin. J. Sport Med . 2015; 25(6):535–40.
Hajizadeh Maleki B, Tartibian B, Vaamonde D. The effects of 16 weeks of intensive cycling training on seminal oxidants and antioxidants in male road cyclists. Clin. J. Sport Med . 2014; 24(4):302–7.
Verratti V, Di Giulio C, D’Angeli A, Tafuri A, Francavilla S, Pelliccione F. Sperm forward motility is negatively affected by short-term exposure to altitude hypoxia. Andrologia . 2016; 48(7):800–6.
Vaamonde D, Da Silva ME, Poblador MS, Lancho JL. Reproductive profile of physically active men after exhaustive endurance exercise. Int. J. Sports Med . 2006; 27(9):680–9.
Ibañez-Perez J, Santos-Zorrozua B, Lopez-Lopez E, et al. Impact of physical activity on semen quality among men from infertile couples. Eur. J. Obstet. Gynecol. Reprod. Biol . 2019; 237:170–4.
Kipandula W, Lampiao F. Semen profiles of young men involved as bicycle taxi cyclists in Mangochi District, Malawi: a case-control study. Malawi Med. J . 2015; 27(4):151–3.
Vaamonde D, Da Silva-Grigoletto ME, Fernandez JM, Algar-Santacruz C, García-Manso JM. Findings on sperm alterations and DNA fragmentation, nutritional, hormonal and antioxidant status in an elite triathlete, Case report. Rev. Andal. Med. Deporte . 2014; 7(4):143–8.
Vaamonde D, Algar-Santacruz C, Abbasi A, García-Manso JM. Sperm DNA fragmentation as a result of ultra-endurance exercise training in male athletes. Andrologia . 2018; 50(1).
Pelliccione F, Verratti V, D’Angeli A, et al. Physical exercise at high altitude is associated with a testicular dysfunction leading to reduced sperm concentration but healthy sperm quality. Fertil. Steril . 2011; 96(1):28–33.
Tartibian B, Maleki BH. Correlation between seminal oxidative stress biomarkers and antioxidants with sperm DNA damage in elite athletes and recreationally active men. Clin. J. Sport Med . 2012; 22(2):132–9.
Hajizadeh Maleki B, Tartibian B. Resistance exercise modulates male factor infertility through anti-inflammatory and antioxidative mechanisms in infertile men: a RCT. Life Sci . 2018; 203:150–60.
Finkler M, Lichtenberg D, Pinchuk I. The relationship between oxidative stress and exercise. J. Basic Clin. Physiol. Pharmacol . 2014; 25(1):1–11.
Powers SK, Radak Z, Ji LL. Exercise-induced oxidative stress: past, present and future. J. Physiol . 2016; 594(18):5081–92.
Mastaloudis A, Leonard SW, Traber MG. Oxidative stress in athletes during extreme endurance exercise. Free Radic. Biol. Med . 2001; 31(7):911–22.
Cooper CE, Vollaard NB, Choueiri T, Wilson MT. Exercise, free radicals and oxidative stress. Biochem. Soc. Trans . 2002; 30(2):280–5.
Bloomer RJ, Goldfarb AH, McKenzie MJ. Oxidative stress response to aerobic exercise: comparison of antioxidant supplements. Med. Sci. Sports Exerc . 2006; 38(6):1098–105.
Finaud J, Lac G, Filaire E. Oxidative stress: relationship with exercise and training. Sports Med . 2006; 36(4):327–58.
Bloomer RJ. Effect of exercise on oxidative stress biomarkers. Adv. Clin. Chem . 2008; 46:1–50.
Bloomer RJ, Goldfarb AH. Anaerobic exercise and oxidative stress: a review. Can. J. Appl. Physiol . 2004; 29(3):245–63.
Nakatani K, Komatsu M, Kato T, et al. Habitual exercise induced resistance to oxidative stress. Free Radic. Res . 2005; 39:905–11.
Schneider CD, Barp J, Ribeiro JL, Belló-Klein A, Oliveira AR. Oxidative stress after three different intensities of running. Can. J. Appl. Physiol . 2005; 30(6):723–34.
Watson TA, MacDonald-Wicks LK, Garg ML. Oxidative stress and antioxidants in athletes undertaking regular exercise training. Int. J. Sport Nutr. Exerc. Metab . 2005; 15(2):131–46.
Cakir-Atabek H, Demir S, PinarbaŞili RD, Gündüz N. Effects of different resistance training intensity on indices of oxidative stress. J. Strength Cond. Res . 2010; 24(9):2491–7.
Djordjevic D, Cubrilo D, Macura M, Barudzic N, Djuric D, Jakovljevic V. The influence of training status on oxidative stress in young male handball players. Mol. Cell. Biochem . 2011; 351(1–2):251–9.
Parker L, McGuckin TA, Leicht AS. Influence of exercise intensity on systemic oxidative stress and antioxidant capacity. Clin. Physiol. Funct. Imaging . 2014; 34(5):377–83.
Leonardo-Mendonça RC, Concepción-Huertas M, Guerra-Hernández E, Zabala M, Escames G, Acuña-Castroviejo D. Redox status and antioxidant response in professional cyclists during training. Eur. J. Sport Sci . 2014; 14(8):830–8.
Vezzoli A, Dellanoce C, Mrakic-Sposta S, et al. Oxidative stress assessment in response to ultraendurance exercise: thiols redox status and ROS production according to duration of a competitive race. Oxid. Med. Cell. Longev . 2016; 2016:6439037.
Hadžović-Džuvo A, Valjevac A, Lepara O, Pjanić S, Hadžimuratović A, Mekić A. Oxidative stress status in elite athletes engaged in different sport disciplines. Bosn. J. Basic Med. Sci . 2014; 14(2):56–62.
Park SY, Kwak YS. Impact of aerobic and anaerobic exercise training on oxidative stress and antioxidant defense in athletes. J. Exerc. Rehabil . 2016; 12(2):113–7.
Kocabaş R, Namiduru ES, Bagçeci AM, et al. The acute effects of interval exercise on oxidative stress and antioxidant status in volleyball players. J. Sports Med. Phys. Fitness . 2018; 58(4):421–7.
Radak Z, Chung HY, Koltai E, Taylor AW, Goto S. Exercise, oxidative stress and hormesis. Ageing Res. Rev . 2008; 7(1):34–42.
Pialoux V, Mounier R, Rock E, et al. Effects of the ‘live high-train low’ method on prooxidant/antioxidant balance on elite athletes. Eur. J. Clin. Nutr . 2009; 63(6):756–62.
Deminice R, Sicchieri T, Payão PO, Jordão AA. Blood and salivary oxidative stress biomarkers following an acute session of resistance exercise in humans. Int. J. Sports Med . 2010; 31(9):599–603.
Tanskanen M, Atalay M, Uusitalo A. Altered oxidative stress in overtrained athletes. J. Sports Sci . 2010; 28(3):309–17.
Sharifi G, Najafabadi AB, Ghashghaei FE. Oxidative stress and total antioxidant capacity in handball players. Adv. Biomed. Res . 2014; 3:181.
Slattery K, Bentley D, Coutts AJ. The role of oxidative, inflammatory and neuroendocrinological systems during exercise stress in athletes: implications of antioxidant supplementation on physiological adaptation during intensified physical training. Sports Med . 2015; 45(4):453–71.
Fisher-Wellman K, Bloomer RJ. Acute exercise and oxidative stress: a 30 year history. Dyn. Med . 2009; 8:1.
Powers SK, Deminice R, Ozdemir M, Yoshihara T, Bomkamp MP, Hyatt H. Exercise-induced oxidative stress: friend or foe. J. Sport Health Sci . 2020; 9(20):415–25.
Stokes KA, Gilbert KL, Hall GM, Andrews RC, Thompson D. Different responses of selected hormones to three types of exercise in young men. Eur. J. Appl. Physiol . 2013; 113(3):775–83.
Lee EC, Fragala MS, Kavouras SA, Queen RM, Pryor JL, Casa DJ. Biomarkers in sports and exercise: tracking health, performance, and recovery. J. Strength Cond. Res . 2017; 31(10):2920–37.
Vingren JL, Kraemer WJ, Ratamess NA, Anderson JM, Volek JS, Maresh CM. Testosterone physiology in resistance exercise and training: the up-stream regulatory elements. Sports Med . 2010; 40(12):1037–53.
Vaamonde D, Da Silva-Grigoletto ME, García-Manso JM, Barrera N, Vaamonde-Lemos R. Physically active men show better semen parameters and hormone values than sedentary men. Eur. J. Appl. Physiol . 2012; 112(9):3267–73.
Sato K, Iemitsu M, Katayama K, Ishida K, Kanao Y, Saito M. Responses of sex steroid hormones to different intensities of exercise in endurance athletes. Exp. Physiol . 2016; 101(1):168–75.
Herbert P, Hayes LD, Sculthorpe NF, Grace FM. HIIT produces increases in muscle power and free testosterone in male masters athletes. Endocr. Connect . 2017; 6(7):430–6.
Kraemer WJ, Fragala MS, Watson G, et al. Hormonal responses to a 160-km race across frozen Alaska. Br. J. Sports Med . 2008; 42(2):116–20.
Kupchak BR, Kraemer WJ, Hoffman MD, Phinney SD, Volek JS. The impact of an ultramarathon on hormonal and biochemical parameters in men. Wilderness Environ. Med . 2014; 25(3):278–88.
Hooper DR, Kraemer WJ, Stearns RL, et al. Evidence of the exercise-hypogonadal male condition at the 2011 Kona ironman world championships. Int. J. Sports Physiol. Perform . 2019; 14(2):170–5.
Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise: development of the “exercise-hypogonadal male condition”. Acta Physiol. Hung . 2005; 92(2):121–37.
Lane AR, Hackney AC. Reproductive dysfunction from the stress of exercise training is not gender specific: the “exercise-hypogonadal male condition”. J. Endocrinol Diabetes . 2014; 1(2):4.
Arce JC, De Souza MJ. Exercise and male factor infertility. Sports Med . 1993; 15(3):146–69.
Rovira-Llopis S, Bañuls C, de Marañon AM, et al. Low testosterone levels are related to oxidative stress, mitochondrial dysfunction and altered subclinical atherosclerotic markers in type 2 diabetic male patients. Free Radic. Biol. Med . 2017; 108:155–62.
Aitken RJ. Impact of oxidative stress on male and female germ cells: implications for fertility. Reproduction . 2020; 159(4):R189–201.
Bloomer RJ, Fisher-Wellman KH. Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake. Gend. Med . 2008; 5(3):218–28.
Guidi F, Magherini F, Gamberi T, et al. Plasma protein carbonylation and physical exercise. Mol. Biosyst . 2011; 7(3):640–50.
Shamsi MB, Venkatesh S, Kumar R, et al. Antioxidant levels in blood and seminal plasma and their impact on sperm parameters in infertile men. Indian J. Biochem. Biophys . 2010; 47(1):38–43.
Benedetti S, Tagliamonte MC, Catalani S, et al. Differences in blood and semen oxidative status in fertile and infertile men, and their relationship with sperm quality. Reprod. Biomed. Online . 2012; 25(3):300–6.
Ferramosca A, Albani D, Coppola L, Zara V. Varicocele negatively affects sperm mitochondrial respiration. Urology . 2015; 86(4):735–9.
Ferramosca A, Pinto Provenzano S, Montagna DD, Coppola L, Zara V. Oxidative stress negatively affects human sperm mitochondrial respiration. Urology . 2013; 82(1):78–83.
Nowicka-Bauer K, Nixon B. Molecular changes induced by oxidative stress that impair human sperm motility. Antioxidants (Basel) . 2020; 9(2):134.
Agarwal A, Rana M, Qiu E, AlBunni H, Bui AD, Henkel R. Role of oxidative stress, infection and inflammation in male infertility. Andrologia . 2018; 50(11):e13126.
Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril . 2003; 79(4):829–43.
Tremellen K. Oxidative stress and male infertility — a clinical perspective. Hum. Reprod. Update . 2008; 14(3):243–58.
Benkhalifa M, Ferreira YJ, Chahine H, et al. Mitochondria: participation to infertility as source of energy and cause of senescence. Int. J. Biochem. Cell Biol . 2014; 55:60–4.
Lee HC, Wei YH. Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging. Exp. Biol. Med . 2007; 232(5):592–606.
Gruber J, Schaffer S, Halliwell B. The mitochondrial free radical theory of ageing — where do we stand? Front. Biosci . 2008; 13:6554–79.
Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab . 2008; 93(8):3199–207.
Piomboni P, Focarelli R, Stendardi A, Ferramosca A, Zara V. The role of mitochondria in energy production for human sperm motility. Int. J. Androl . 2012; 35(2):109–24.
Amaral A, Lourenço B, Marques M, Ramalho-Santos J. Mitochondria functionality and sperm quality. Reproduction . 2013; 146(5):R163–74.
Ferramosca A, Zara V. Bioenergetics of mammalian sperm capacitation. Biomed. Res. Int . 2014; 2014:902953.
Moscatelli N, Lunetti P, Braccia C, et al. Comparative proteomic analysis of proteins involved in bioenergetics pathways associated with human sperm motility. Int. J. Mol. Sci . 2019; 20(12):3000.
Barbagallo F, La Vignera S, Cannarella R, Aversa A, Calogero AE, Condorelli RA. Evaluation of sperm mitochondrial function: a key organelle for sperm motility. J. Clin. Med . 2020; 9(2):363.
Di Giacomo M, Zara V, Bergamo P, Ferramosca A. Crosstalk between mitochondrial metabolism and oxidoreductive homeostasis: a new perspective for understanding the effects of bioactive dietary compounds. Nutr. Res. Rev . 2020; 33(1):90–101.
Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J. Mens. Health . 2014; 32(1):1–17.
Losano JDA, Angrimani DSR, Ferreira Leite R, Simões da Silva BDC, Barnabe VH, Nichi M. Spermatic mitochondria: role in oxidative homeostasis, sperm function and possible tools for their assessment. Zygote . 2018; 26(4):251–60.
Hoch FL. Cardiolipins and biomembrane function. Biochim. Biophys. Acta . 1992; 1113(1):71–133.
Yan LJ, Sohal RS. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl. Acad. Sci. U. S. A . 1998; 95(22):12896–901.
Lippe G, Comelli M, Mazzilis D, Sala FD, Mavelli I. The inactivation of mitochondrial F1 ATPase by H 2 O 2 is mediated by iron ions not tightly bound in the protein. Biochem. Biophys. Res. Commun . 1991; 181(2):764–70.
Yan LJ, Levine RL, Sohal RS. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U. S. A . 1997; 94(21):11168–72.
Kumar R, Venkatesh S, Kumar M, et al. Oxidative stress and sperm mitochondrial DNA mutation in idiopathic oligoasthenozoospermic men. Indian J. Biochem. Biophys . 2009; 46(2):172–7.
Venkatesh S, Deecaraman M, Kumar R, Shamsi MB, Dada R. Role of reactive oxygen species in the pathogenesis of mitochondrial DNA (mtDNA) mutations in male infertility. Indian J. Med. Res . 2009; 129(2):127–37.
Turner TT, Lysiak JJ. Oxidative stress: a common factor in testicular dysfunction. J. Androl . 2008; 29(5):488–98.
Gandini L, Lombardo F, Paoli D, et al. Study of apoptotic DNA fragmentation in human spermatozoa. Hum. Reprod . 2000; 15(4):830–9.
Nakada K, Sato A, Yoshida K, et al. Mitochondria-related male infertility. Proc. Natl. Acad. Sci. U. S. A . 2006; 103(41):15148–53.
Shabalina IG, Landreh L, Edgar D, et al. Leydig cell steroidogenesis unexpectedly escapes mitochondrial dysfunction in prematurely aging mice. FASEB J . 2015; 29(8):3274–86.
Midzak A, Rone M, Aghazadeh Y, Culty M, Papadopoulos V. Mitochondrial protein import and the genesis of steroidogenic mitochondria. Mol. Cell. Endocrinol . 2011; 336(1–2):70–9.
Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr. Rev . 2004; 25(6):947–70.
Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab. Rev . 2006; 38(1–2):171–96.
Beattie MC, Chen H, Fan J, Papadopoulos V, Miller P, Zirkin BR. Aging and luteinizing hormone effects on reactive oxygen species production and DNA damage in rat Leydig cells. Biol. Reprod . 2013; 88(4):100.
Duan T, Fan K, Chen S, et al. Role of peroxiredoxin 2 in H 2 O 2 -induced oxidative stress of primary Leydig cells. Mol. Med. Rep . 2016; 13(6):4807–13.
Meeker JD, Godfrey-Bailey L, Hauser R. Relationships between serum hormone levels and semen quality among men from an infertility clinic. J. Androl . 2007; 28(3):397–406.
Richthoff J, Spano M, Giwercman YL, et al. The impact of testicular and accessory sex gland function on sperm chromatin integrity as assessed by the sperm chromatin structure assay (SCSA). Hum. Reprod . 2002; 17(12):3162–9.
Ferramosca A, Conte A, Moscatelli N, Zara V. A high-fat diet negatively affects rat sperm mitochondrial respiration. Andrology . 2016; 4(3):520–5.
Ferramosca A, Moscatelli N, Di Giacomo M, Zara V. Dietary fatty acids influence sperm quality and function. Andrology . 2017; 5(3):423–30.
Ferramosca A, Provenzano SP, Coppola L, Zara V. Mitochondrial respiratory efficiency is positively correlated with human sperm motility. Urology . 2012; 79(4):809–14.
Moscatelli N, Spagnolo B, Pisanello M, et al. Single-cell-based evaluation of sperm progressive motility via fluorescent assessment of mitochondria membrane potential. Sci. Rep . 2017; 7(1):17931.
Starkov AA, Simonyan RA, Dedukhova V, Mansurova SE, Palamarchuk LA, Skulachev VP. Regulation of the energy coupling in mitochondria by some steroid and thyroid hormones. Biochim. Biophys. Acta . 1997; 1318(1–2):173–83.
Vaamonde D, Garcia-Manso JM, Hackney AC. Impact of physical activity and exercise on male reproductive potential: a new assessment questionnaire. Rev. Andal. Med. Deport . 2017; 10(2):79–93.
Kujala UM, Alen M, Huhtaniemi IT. Gonadotrophin-releasing hormone and human chorionic gonadotrophin tests reveal that both hypothalamic and testicular endocrine functions are suppressed during acute prolonged physical exercise. Clin. Endocrinol. (Oxf) . 1990; 33(2):219–25.
Diemer T, Allen JA, Hales KH, Hales DB. Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology . 2003; 144(7):2882–91.
Hales DB, Allen JA, Shankara T, et al. Mitochondrial function in Leydig cell steroidogenesis. Ann. N. Y. Acad. Sci . 2005; 1061:120–34.