PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Atroshchenko M.M., Medvedev D.V. Biochemical markers of stallion sperm quality (review) Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2023, Vol. 58, № 2, p. 249-259.
(how to cite this article)

doi: 10.15389/agrobiology.2023.2.249eng

UDC: 636.1:612.616.2:577.1

 

BIOCHEMICAL MARKERS OF STALLION SPERM QUALITY (review)

M.M. Atroshchenko ✉, D.V. Medvedev

All-Russian Research Institute for Horse Breeding, Divovo, Rybnoe District, Ryazan Province, 391105 Russia, e-mail atromiks-77@mail.ru (✉ corresponding author), meddmit@mail.ru

ORCID:
Atroshchenko M.M. orcid.org/0000-0001-6023-0332
Medvedev D.V. orcid.org/0000-0002-0627-7348

Final revision received September 7, 2022,
Accepted October 6, 2022

Seminal plasma is a multicomponent fluid that serves as a vehicle for delivering spermatozoa to the oocyte. This fluid transports male gametes and provides their protection and nutrition during further movement in the female genital tract (T.R. Talluri et al., 2017). Thereby, understanding the effect of the components of seminal plasma on reproductive cells, as well as the search for markers of cryo-resistance and sperm fertility is undoubtedly interesting for researchers. Because stallion sperm lifespan, capacitation capacity, and fertility vary widely between individuals, it is important for horse breeding to investigate the factors that influence these parameters. The purpose of our review is to analyze current publications on the study of biochemical markers that characterize sperm quality and to consider methods for determining reactive oxygen species and oxidative stress products in spermatozoa and seminal plasma. Metabolites of seminal plasma, enzymes activity in it, indicators of oxidative stress and antioxidant defense system can serve as biochemical markers of sperm quality (S. Pesch et al., 2006). To ensure motility, spermatozoa need a large amount of ATP. Monosaccharides and organic acids such as lactate, pyruvate, citrate, succinate are good energy substrates for these cells. This gives rise to interest in them as markers of fertility (C.R. Darr et al., 2016; E.B. Menezes et al., 2019; M.F. Lay et al., 2001). The concentration of nitric oxide (II) metabolites is another promising indicator for assessing the quality of stallions sperm, since it plays an important role in the regulation of sperm motility and capacitation and the fertilization process (M.B. Herrero et al., 2000; P.T. Goud et al., 2008; F. Francavilla et al., 2000). Among enzymes of seminal plasma, lactate dehydrogenase, alanine and aspartate aminosferases, γ-glutamyl transpeptidase are of interest. While semen analysis is considered the gold standard for diagnosing male fertility, it cannot detect the molecular abnormalities that are responsible for unexplained cases of male infertility. Currently, oxidative stress is considered one of the main causes of such phenomena. It damages sperm proteins, lipids and DNA, which in turn leads to poor embryo implantation and a decrease in pregnancy rates. In this review, the main producers of free radicals in sperm and the antioxidant defense system of male gametes as well as methods for the determination of reactive oxygen species and end products of oxidative stress in spermatozoa and seminal plasma are considered (A. Agarwal et al., 2003; S. Bisht et al., 2017; H. Sies, 2018). Based on the literature data, it was concluded that biochemical markers, such as seminal plasma metabolites, enzyme activity in it, and indicators of oxidative stress, have significant potential for characterizing stallion sperm quality.

Keywords: stallions, fertility, spermatozoa, seminal plasma, oxidative stress, enzymes, metabolites.  

 

REFERENCES

  1. Talluri T.R., Mal G., Ravi S.K. Biochemical components of seminal plasma and their correlation to the fresh seminal characteristics in Marwari stallions and Poitou jacks. Veterenary World, 2017, 10(2): 214-220 (doi: 10.14202/vetworld.2017.214-220).
  2. Juyena N.S., Stelletta C. Seminal plasma: an essential attribute to spermatozoa. Journal of Andrology, 2012, 33(4): 536-551 (doi: 10.2164/jandrol.110.012583).
  3. Tvrda E., Sikeli P., Lukacova J., Massanyi P., Lukac N. Mineral nutrients and male fertility. Journal of Microbiology, Biotechnology and Food Sciences, 2013, 3(1): 1-14.
  4. Velho A.L.C., Menezes E., Dinh T., Kaya A., Topper E., Moura A.A.,  Memili E. Metabolomic markers of fertility in bull seminal plasma. PLoS ONE, 2018, 13(4): e0195279 CrossRef
  5. Mann T. Biochemistry of stallion semen. Journal of reproduction and fertility. Supplement, 1975, 23: 47-52.
  6. Darr C.R., Varner D.D., Teague S., Cortopassi G.A., Datta S., Meyers S.A. Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial function, motility, and ROS production. Biology of Reproduction, 2016, 95(2): 1-11 CrossRef
  7. Menezes E.B., Velho A.L.C., Santos F., Dinh T., Kaya A., Topper E., Moura A.A., Memili E. Uncovering sperm metabolome to discover biomarkers for bull fertility. BMC Genomics, 2019, 20(1): 714 CrossRef
  8. Lay M.F., Richardson M.E., Boone W.R., Bodine A.B., Thurston R.J. Seminal plasma and IVF potential. Biochemical constituents of seminal plasma of males from in vitro fertilization couples. Journal of Assisted Reproduction and Genetics, 2001, 18(3): 144-150 CrossRef
  9. Mann T. The Biochemistry of semen and of the male reproductive tract. Medical Journal of Australia, 1965, 1(18): 652-653 CrossRef
  10. Paventi G., Lessard C., Bailey J.L., Passarella S. In boar sperm capacitation L-lactate and succinate, but not pyruvate and citrate, contribute to the mitochondrial membrane potential increase as monitored via safranine O fluorescence. Biochemical and Biophysical Research Communications, 2015, 462(3): 257-262 CrossRef
  11. Herrero M.B., Gagnon C. Nitric oxide: a novel mediator of sperm function. Journal of Andrology, 2001, 22: 349-356.
  12. Roselli M., Keller P.J., Dubey R.K. Role of nitric oxide in the biology physiology and pathophysiology of reproduction. Human Reproduction Update, 1998, 4(1): 3-24 CrossRef
  13. Balercia G., Moretti S., Vignini A., Magagnini M., Mantero F., Boscaro M., Riccardo-Lamonica G., Mazzanti L. Role of nitric oxide concentrations on human sperm motility. Journal of Andrology, 2004, 25(2): 245-249 CrossRef
  14. Vignini A., Nanetti L., Buldreghini E., Moroni C., Ricciardo Lamonina G., Mantero F., Boscaro M., Mazzanti L., Balercia G. The production of peroxynitrite by human spermatozoa may affect sperm motility through the formation of protein nitrotyrosine. Fertility and Sterility, 2006, 85(4): 947-953 CrossRef
  15. Herrero M.B., Chatterjee S., Lefièvre L., de Lamirande E., Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radical Biology and Medicine, 2000, 29(6): 522-536 CrossRef
  16. Goud P.T., Goud A.P., Diamond M.P., Gonik M.P., Abu-Soud H. Nitric oxide extends the oocyte temporal window for optimal fertilization. Free Radical Biology and Medicine, 2008, 45(4): 453-459 doi: CrossRef
  17. Francavilla F., Santucci R., Macerola B., Ruvolo G., Romano R. Nitric oxide synthase inhibition in human sperm affects sperm-oocyte fusion but not zona pellucida binding. Biology of Reproduction, 2000, 63(2): 425-429 CrossRef
  18. Miraglia E., De Angelis F., Gazzano E., Hassanpour H., Bertagna A., Aldieri E., Revelli A., Ghigo D. Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway. Reproduction, 2011, 141(1): 47-54 CrossRef
  19. Khan F.A., Sholtz E.L., Chenier T.S. The nitric oxide system in equine reproduction: surrent status and future directions. Journal of Equine Veterinary Science, 2015, 35(6): 481-487 CrossRef
  20. Ha T.Y., Kim H.S., Shin T. Expression of constitutive endothelial, neuronal and inducible nitric oxide synthase in the testis and epididymis of horse. Journal of Veterinary Medical Science, 2004, 66(4): 351-356 CrossRef
  21. Ortega Ferrusola C., González Fernández L., Macías García B., Salazar-Sandoval C., Morillo Rodríguez A., Rodríguez Martinez H., Tapia J.A., Peña F.J. Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biology of Reproduction, 2009, 81: 1106-1111 CrossRef
  22. Eghbali M., Alavi-Shoushtari S.M., Asri-Rezaei S., Ansari M.H.K. Effects of the seminal plasm iron and lead content on semen quality of water buffalo (Bubalus bubalis) bulls. Veterinary Research Forum, 2010, 1(3): 142-148.
  23. Pesch S., Bergmann M., Bostedt H. Determination of some enzymes and macro and microelements in stallion seminal plasma and their correlations to semen quality. Theriogenology, 2006, 66(2): 307-313 CrossRef
  24. El-Bishbishy H.A., Aly H.A.A., El-Shafey M. Lipoic acid mitigates bisphenol A-induced testicular mitochondrial toxicity in rats. Environmental Health, 2013, 29(10): 875-887 CrossRef
  25. Bucci D., Isani G., Giaretta E., Spinaci M., Tamanini C., Ferlizza E., Galeati G. Alkaline phosphatase in boar sperm function. Andrology, 2014, 2(1): 100-106 CrossRef
  26. Katila T. In vitro evaluation of frozen-thawed stallion semen: a review. Acta Veterinaria Scandinavica, 2001, 42(2): 199-217 CrossRef
  27. O’Flaherty C., Breininger E., Beorlegui N., Beconi M.T. Acrosome reaction of bovine spermatozoa: role of reactive oxygen species and lactate dehydrogenase C4. Biochimica and Biophysica Acta — General Subjects, 2005, 1726(1): 96-101 CrossRef
  28. Agarwal Y.P., Vanha-Perttula T. Glutation, L-glutamic acid and γ-glutamil transpeptidase in the bull reproductive tissues. International Journal of Andrology, 1988, 11(2): 123-131 CrossRef
  29. Pizzol D., Ferlin A., Garolla A., Lenzi A., Bertoldo A., Foresta C. Genetic and molecular diagnostics of male infertility in the clinical practice. Frontiers in Bioscience-Landmark, 2014, 19: 291-303 CrossRef
  30. Ramya T., Misro M.M., Sinha D., Nandan D. Sperm function and seminal oxidative stress as tools to identify sperm pathologies in infertile men. Fertility and Sterility, 2010, 93(1): 297-300 CrossRef
  31. Agarwal A., Saleh R.A., Bedaiwy M.A. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertility and Sterility, 2003, 79(4): 829-843 CrossRef
  32. Bisht S., Faiq M., Tolahunase M., Dada R. Oxidative stress and male infertility. Nature Reviews Urology, 2017, 14(8): 470-485 CrossRef
  33. Sies H. On the history of oxidative stress: Concept and some aspects of current development. Current Opinion in Toxicology, 2018, 7(2): 122-126 CrossRef
  34. Bansal A.K., Bilaspuri G.S. Impacts of oxidative stress and antioxidants on semen functions. Veterinary Medicine International, 2010, 2011: 686137 CrossRef
  35. Kumar N., Singh A.K. Reactive oxygen species in seminal plasma as a cause of male infertility. Journal of Gynecology Obstetrics and Human Reproduction, 2018, 47: 565-572 CrossRef
  36. Miranda-Vilela A.L., Alves P.C., Akimoto A.K., Pereira L.C., Nazare Klautau-Guimaraes M.D., Grisolia C.K. The effect of hydrogen peroxide-induced oxidative stress on leukocytes depends on age and physical training in healthy human subjects carrying the same genotypes of antioxidant enzymes’ gene polymorphisms. American Journal of Human Biology, 2010, 22(6): 807-812 CrossRef
  37. Breitbart H. Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Molecular and Cellular Endocrinology, 2002, 187(2): 139-144 CrossRef
  38. Khosrowbeygi A., Zarghami N. Fatty acid composition of human spermatozoa and seminal plasma levels of oxidative stress biomarkers in subfertile males. Prostaglandins, Leukotrienes & Essential Fatty Acids, 2007, 77(2): 117-121 CrossRef
  39. Garrido N., Meseguer M., Simon C., Pellicer A., Remohi J. Pro-oxidative and antioxidative imbalance in human semen and its relation with male fertility. Asian Journal of Andrology, 2004, 6(1): 59-65.
  40. Henkel R.R. Leukocytes and oxidative stress: dilemma for sperm function and male fertility. Asian Journal of Andrology, 2011, 13(1): 43-52 CrossRef
  41. Saleh R.A., Agarwal A., Kandirali E., Sharma R.K., Thomas A.J., Nada E.A, Evenson D.P., Alvarez J.G. Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertility and Sterility, 2002, 78(6): 1215-1224 CrossRef
  42. Lobascio A.M., De Felici M., Anibaldi M., Greco P., Minasi M.G., Greco E. Involvement of seminal leukocytes, reactive oxygen species, and sperm mitochondrial membrane potential in the DNA damage of the human spermatozoa. Andrology, 2015, 3(2): 265-270 CrossRef
  43. Peña F.J., O’Flaherty C., Ortiz Rodríguez J.M., Martín Cano F.E., Gaitskell-Phillips G.L., Gil M.C., Ortega Ferrusola C. Redox regulation and oxidative stress: the particular case of the stallion spermatozoa. Antioxidants, 2019, 8(11): 567 CrossRef
  44. Keating J., Grundy C.E., Fivey P.S., Elliott M., Robinson J. Investigation of the association between the presence of cytoplasmic residues on the human sperm midpiece and defective sperm function. Journal of Reproduction and Fertility, 1997, 110(1): 71-77 CrossRef
  45. Zini A., Defreitas G., Freeman M., Hechter S., Jarvi K. Varicocele is associated with abnormal retention of cytoplasmic droplets by human spermatozoa. Fertility and Sterility, 2000, 74(3): 461-464 CrossRef
  46. Sabeti P., Pourmasumi S., Rahiminia T., Akyash F., Talebi A.R. Etiologies of sperm oxidative stress. International Journal of Reproductive Biomedicine, 2016, 14(4): 231-240.
  47. Bollwein H., Fuchs I., Koess C. Interrelationship between plasma membrane integrity, mitochondrial membrane potential and DNA fragmentation in cryopreserved bovine spermatozoa. Reproduction in Domestic Animals, 2008, 43(2): 189-195 CrossRef
  48. Agarwal A., Gupta S., Sharma R.K. Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology, 2005, 3: 28 CrossRef
  49. Catalán J., Yánez-Ortiz I., Tvarijonaviciute A., González-Aróstegui L.G., Rubio C.P., Barranco I., Yeste M., Miró J. Seminal plasma antioxidants are related to sperm cryotolerance in the horse. Antioxidants,2022, 11(7): 1279 CrossRef
  50. Papas M., Catalán, J., Fernandez-Fuertes B., Arroyo L., Bassols A., Miró J., Yeste M. Specific activity of superoxide dismutase in stallion seminal plasma is related to sperm cryotolerance. Antioxidants, 2019, 8(11): 539 CrossRef
  51. Miriyala S., Holley A.K., St Clair D.K. Mitochondrial superoxide dismutase — signals of distinction. Anti-Cancer Agents in Medicinal Chemistry, 2011, 11(2): 181-190 CrossRef
  52. Obal D., Dai S., Keith R., Dimova N., Kingery J., Zheng Y-T., Zweier J., Velayutham M., Prabhu S.D., Li Q., Conklin D., Yang D., Bhatnagar A., Bolli R., Rokosh G. Cardiomyocyte-restricted overexpression of extracellular superoxide dismutase increases nitric oxide bioavailability and reduces infarct size after ischemia/reperfusion. Basic Research in Cardiology, 2012, 107(6): 305 CrossRef
  53. Kowalowka M., Wysocki P., Fraser L., Strzezek J. Extracellular superoxide dismutase of boar seminal plasma. Reproduction in Domestic Animals, 2008, 43(4): 490-496 CrossRef
  54. Bucak M.N., Ateşşahin A., Varişli O., Yüce A., Tekin N., Akçay A. The influence of trehalose, taurine, cysteamine and hyaluronan on ram semen. Microscopic and oxidative stress parameters after freeze-thawing process. Theriogenology, 2007, 67(5): 1060-1067 CrossRef
  55. Del Prete C., Stout T., Montagnaro S., Pagnini U., Uccello M., Florio P., Ciani F., Tafuri S., Palumbo V., Pasolini M.P., Cocchia N., Henning H. Combined addition of superoxide dismutase, catalase and glutathione peroxidase improves quality of cooled stored stallion semen. Animal Reproduction Science, 2019, 210: 106195 CrossRef
  56. Margis R., Dunand C., Teixeira F.K., Margis-Pinheiro M. Glutathione peroxidase family — an evolutionary overview. The FEBS Journal, 2008, 275(15): 3959-3970 CrossRef
  57. Sanocka D., Kurpisz M. Reactive oxygen species and sperm cells. Reproductive Biology and Endocrinology, 2004, 2: 12-26 CrossRef
  58. Chatterjee S., Gagnon C. Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Molecular Reproduction and Development, 2001, 59(4): 451-458 CrossRef
  59. Wang Y., Sharma R.K., Agarwal A. Effect of cryopreservation and sperm concentration on lipid peroxidation in human semen. Urology, 1997, 50(3): 409-413 CrossRef
  60. Dalle-Donne I., Rossi R., Giustarini D., Milzani A., Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta, 2003, 329(1-2): 23-38 CrossRef
  61. Dubinina E.E., Burmistrov S.O., Khodov D.A., Porotov I.G. Voprosy meditsinskoy khimii, 1995, 41(1): 24-26 (in Russ.).
  62. Agarwal A., Majzoub A. Laboratory tests for oxidative stress. Indian Journal of Urology, 2017, 33(3): 199-206 CrossRef
  63. Allamaneni S.S., Agarwal A., Nallella K.P., Sharma R.K., Thomas Jr. A.J., Sikka S.C. Characterization of oxidative stress status by evaluation of reactive oxygen species levels in whole semen and isolated spermatozoa. Fertility and Sterility, 2005, 83(3): 800-803 CrossRef
  64. Eruslanov E., Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods in Molecular Biology, 2010, 594: 57-72 CrossRef

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)