Optimized addition of nitric oxide compounds in semen extender improves post-thaw seminal attributes of Murrah buffaloes.

Publisher: Springer Country of Publication: United States NLM ID: 1277355 Publication Model: Electronic Cited Medium: Internet ISSN: 1573-7438 (Electronic) Linking ISSN: 00494747 NLM ISO Abbreviation: Trop Anim Health Prod Subsets: MEDLINE

Publication: 2005- : Heidelberg : Springer
Original Publication: Edinburgh, Livingstone.

Bison* ; Semen Preservation*/veterinary ; Semen Preservation*/methods; Male ; Animals ; Semen ; Semen Analysis/veterinary ; Buffaloes/physiology ; Nitric Oxide/pharmacology ; NG-Nitroarginine Methyl Ester/pharmacology ; Sperm Motility ; Cryoprotective Agents/pharmacology ; Spermatozoa ; Cryopreservation/veterinary

Semen dilution and cryopreservation alter the homogeneity of seminal plasma, resulting in a non-physiological redox milieu and consequently poor sperm functionality. Considering the concentration-specific bimodal action of nitric oxide (NO) in the regulation of sperm functions, cryopreservation media supplemented with optimized concentrations can improve the semen attributes. The present study aimed to evaluate the effect of adding an optimized concentration of sodium nitroprusside (SNP) and N-nitro-L-arginine methyl ester (L-NAME) in an extender on in vitro semen quality. An aliquot of semen samples (n = 32) from Murrah buffalo bulls (n = 8) was divided into control (C) and treatment (T-I: SNP in extender at 1 µmol/L; T-II: L-NAME in extender at 10 µmol/L). Fresh semen quality parameters showed no significant difference at 0 h except for the structural integrity in the T-II group. Post-thaw semen quality parameters and sperm kinematics using computer-aided sperm analysis (CASA) revealed significantly higher (p < 0.05) cryoresistance in the treatment groups. Viability, acrosome integrity, and membrane integrity were significantly higher (p < 0.05) in both treatment groups; however, the results were pervasive in T-II. Lower abnormal spermatozoa were observed in both T-I and T-II. SNP supplementation led to a significant rise (p < 0.05) in NO, whereas L-NAME reduced the NO concentration in post-thawed samples, which was directly correlated with different sperm functionality and associated biomarkers viz. total antioxidant capacity (TAC) and thiobarbituric acid reactive substance (TBARS). It was concluded that the cryopreservation media supplemented with SNP and L-NAME at 1 µmol/L and 10 µmol/L, respectively, lower the cryo-damage and improve post-thaw seminal attributes.
(© 2023. The Author(s), under exclusive licence to Springer Nature B.V.)

Agarwal, A., Virk, G., Ong, C., & Du Plessis, S. S. (2014). Effect of oxidative stress on male reproduction. The World Journal of Men's Health, 32(1), 1-17.
Aitken, A., Banasazczyk, S., Dentith, M., Lindsay, M., Shragge, J., Piña-Varas, P., Annetts, D., Austin, J., Ley-Cooper, Y., Monday, T., & Yuan, H. (2015). A major geophysical experiment in the Capricorn Orogeny, Western Australia. ASEG Extended Abstracts, 2015(1), 1-5.
Al-Ebady, A. S. (2012). Effect of adding L. arginine on some parameters of bull sperms after freezing in liquid nitrogen (-196ºC). Al-Qadisiyah Journal of Veterinary Medicine Sciences, 11(2), 156-161.
Ambrosini, A., Zolese, G., Ambrosi, S., Ragni, L., Tiano, L., Littarru, G., Bertoli, E., Mantero, F., Boscaro, M. & Balercia, G. (2006).Oleoylethanolamide protects human sperm cells from oxidation stress: studies on cases of idiopathic infertility. Biology of Reproduction, 74(4), 659-665.
Andrabi, S. M. H. (2009). Factors affecting the quality of cryopreserved buffalo (Bubalusbubalis) bull spermatozoa. Reproduction in Domestic Animals, 44(3), 552-569.
Bahmanzadeh, M., Abolhassani, F., Amidi, F., Ejtemaiemehr Sh., Salehi M., & Abbasi M. (2008). The effects of nitric oxide synthase inhibitor (L-NAME) on epididymal sperm count, motility, and morphology in varicocelized rat. DARU, 16(1).
Balercia, G., Moretti, S., Vignini, A., Magagnini, M., Mantero, F., Boscaro, M., Ricciardo‐Lamonica, G., & Mazzanti, L. (2004). Role of nitric oxide concentrations on human sperm motility. Journal of Andrology, 25(2), 245-249.
Bisla, A., Rautela, R., Yadav, V., Singh, P., Kumar, A., Ghosh, S., Kumar, A., Bag, S., Kumar, B. & Srivastava, N. (2020). Nano‐purification of raw semen minimises oxidative stress with improvement in post‐thaw quality of buffalo spermatozoa. Andrologia, 52(9), e13709.
Blom, E. (1950). A one-minute live-dead sperm stain by means of eosin-nigrosin. Fertility and Sterility, 1, 176-177.
Bolaños, J. P., Delgado-Esteban, M., Herrero-Mendez, A., Fernandez-Fernandez, S., & Almeida, A. (2008). Regulation of glycolysis and pentose–phosphate pathway by nitric oxide: Impact on neuronal survival. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1777(7-8), 789-793.
Buzadzic, B., Vucetic, M., Jankovic, A., Stancic, A., Korac, A., Korac, B., & Otasevic, V. (2015). New insights into male (in) fertility: the importance of NO. British Journal of Pharmacology, 172(6), 1455-1467.
Castro, L. S., Hamilton, T. R. S., Mendes, C. M., Nichi, M., Barnabe, V. H., Visintin, J. A., & Assumpção, M. E. O. A. (2016). Sperm cryodamage occurs after rapid freezing phase: flow cytometry approach and antioxidant enzymes activity at different stages of cryopreservation. Journal of Animal Science and Biotechnology, 7(1), 17.
de Andrade, A. F., Arruda, R. P., Torres, M. A., Pieri, N. C., Leite, T. G., Celeghini, E. C. C., Oliveira, L.Z., Gardés, T.P., Bussiere, M.C.C., & Silva, D. F. (2018). Nitric oxide in frozen-thawed equine sperm: Effects on motility, membrane integrity and sperm capacitation. Animal Reproduction Science, 195, 176-184.
Doshi, S. B., Khullar, K., Sharma, R. K., & Agarwal, A. (2012). Role of reactive nitrogen species in male infertility. Reproductive Biology and Endocrinology, 10(1), 1-11.
Emamverdi, M., Zhandi, M., ZareShahneh, A., Sharafi, M., & Akbari‐Sharif, A. (2013). Optimization of Ram semen cryopreservation using a chemically defined soybean lecithin‐based extender. Reproduction in Domestic Animals, 48(6), 899-904.
Forouzanfar, M., Sharafi, M., Hosseini, S. M., Ostadhosseini, S., Hajian, M., Hosseini, L., Abedi, P., Nili, N., Rahmani, H.R. & Nasr-Esfahani, M. H. (2010). In vitro comparison of egg yolk–based and soybean lecithin–based extenders for cryopreservation of ram semen. Theriogenology, 73(4), 480-487.
Francavilla, F., Santucci, R., Macerola, B., Ruvolo, G., & Romano, R. (2000). Nitric oxide synthase inhibition in human sperm affects sperm-oocyte fusion but not zonapellucida binding. Biology of Reproduction, 63(2), 425-429.
Gibb, Z., Lambourne, S. R., & Aitken, R. J. (2014). The paradoxical relationship between stallion fertility and oxidative stress. Biology of reproduction, 91(3), 77-1.
Gibb, Z., Griffin, R. A., Aitken, R. J., & De Iuliis, G. N. (2020). Functions and effects of reactive oxygen species in male fertility. Animal Reproduction Science, 220, 106456.
Hancock, J. L. (1951). A staining technique for the study of temperature-shock in semen. Nature, 167(4243), 323-324.
Hancock, J. L. (1952). The morphology of bull spermatozoa. Journal of Experimental Biology, 29(3), 445-453.
Hancock, J. T., & Neill, S. J. (2019). Nitric oxide: its generation and interactions with other reactive signaling compounds. Plants, 8(2), 41.
Harrison, R. A. P. (2004). Rapid PKA‐catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Molecular Reproduction and Development: Incorporating Gamete Research, 67(3), 337-352.
Jeyendran, R. S., Van der Ven, H. H., Perez-Pelaez, M., Crabo, B. G., & Zaneveld, L. J. D. (1984). Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. Reproduction, 70(1), 219-228.
Joly, G. A., Ayres, M., Chelly, F., & Kilbourn, R. G. (1994). Effects of NG-methyl-L-arginine, NG-nitro-L-arginine, and aminoguanidine on constitutive and inducible nitric oxide synthase in rat aorta. Biochemical and Biophysical Research Communications, 199(1), 147-154.
Khodaei, H., Chamani, M., Mahdavi, B., & Akhondi, A. A. (2016). Effects of adding sodium nitroprusside to semen diluents on motility, viability and lipid peroxidation of sperm in holstein bulls. International Journal of Fertility and Sterility, 9(4), 521.
Kothari, S., Thompson, A., Agarwal, A., & du Plessis, S. S. (2010). Free radicals: their beneficial and detrimental effects on sperm function. Indian Journal of Experimental Biology, 48(5), 425-435.
Kumar, A., Prasad, J. K., Srivastava, N., & Ghosh, S. K. (2019). Strategies to minimize various stress-related freeze–thaw damages during conventional cryopreservation of mammalian spermatozoa. Biopreservation and Biobanking, 17(6), 603-612.
Leal, A. C. M. S., Caldas-Bussiere, M. C., de Carvalho, C. P., Viana, K. S., & Quirino, C. R. (2009). Role of nitric oxide on quality of freshly ejaculated bull spermatozoa during heparin-induced in vitro capacitation. Animal Reproduction Science, 116(1-2), 38-49.
Len, J. S., Koh, W. S. D., & Tan, S. X. (2019). The roles of reactive oxygen species and antioxidants in cryopreservation. Bioscience Reports, 39(8).
Lone, S. A., Prasad, J. K., Ghosh, S. K., Das, G. K., Kumar, N., Balamurugan, B., Katiyar, R., & Verma, M. R. (2016). Effect of cholesterol loaded cyclodextrin (CLC) on lipid peroxidation and reactive oxygen species levels during cryopreservation of buffalo (Bubalusbubalis) spermatozoa. Asian Pacific Journal of Reproduction, 5(6), 476-480.
Makker, K., Agarwal, A., & Sharma, R. (2009). Oxidative stress & male infertility. Indian Journal of Medical Research, 129(4), 357.
Martinez-Alborcia, M. J., Valverde, A., Parrilla, I., Vazquez, J. M., Martinez, E. A., & Roca, J. (2012). Detrimental effects of non-functional spermatozoa on the freezability of functional spermatozoa from boar ejaculate. PLoS One, 7(5), e36550.
Miraglia, E., Rullo, M. L., Bosia, A., Massobrio, M., Revelli, A., & Ghigo, D. (2007). Stimulation of the nitric oxide/cyclic guanosine monophosphate signaling pathway elicits human sperm chemotaxis in vitro. Fertility and Sterility, 87(5), 1059-1063.
Miraglia, E., De Angelis, F., Gazzano, E., Hassanpour, H., Bertagna, A., Aldieri, E., Revelli, A., & Ghigo, D. (2011). Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway. Reproduction, 141(1), 47-54.
Mughal, D. H., Ijaz, A., Yousaf, M. S., Wadood, F., & Farooq, U. (2017). Cryopreservation of buffalo (Bubalusbubalis) semen-limitations and expectations. Buffalo Bulletin, 36(1), 1-14.
Nash, K. M., Rockenbauer, A., & Villamena, F. A. (2012). Reactive nitrogen species reactivities with nitrones: theoretical and experimental studies. Chemical Research in Toxicology, 25(8), 1581-1597.
Naskar, S. (2018). Impact of Oxidative Stress and Antioxidants on Sperm Quality in Murrah Bulls (Masters dissertation, NDRI, Karnal).
Ortega Ferrusola, C., Gonzalez Fernandez, L., Macias Garcia, B., Salazar-Sandoval, C., Morillo Rodriguez, A., Rodríguez Martinez, H., Tapia, J. A. & Pena, F. J. (2009). Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biology of Reproduction, 81(6), 1106-1111.
Otasevic, V., Korac, A., Vucetic, M., Macanovic, B., Garalejic, E., Ivanovic-Burmazovic, I., Filipovic, M.R., Buzadzic, B., Stancic, A., Jankovic, A. & Korac, B. (2013). Is manganese (II) pentaazamacrocyclic superoxide dismutase mimic beneficial for human sperm mitochondria function and motility?. Antioxidants and Redox Signaling, 18(2), 170-178.
Ozer Kaya, S., Kandemir, F. M., Gur, S., Erisir, M., Benzer, F., Kaya, E., Turk, G. & Sonmez, M. (2020). Evaluation of the role of L‐arginine on spermatological parameters, seminal plasma nitric oxide levels and arginase enzyme activities in rams. Andrologia, 52(1), e13439.
Pacher, P., Beckman, J. S., & Liaudet, L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiological Reviews, 87(1), 315-424.
Panth, S. (2017). Reactive Nitrogen Species as Biomarker of Semen Quality in Crossbred Cattle Bulls (Masters Dissertation, NDRI, Karnal).
Rahman, M. S., Kwon, W. S., Lee, J. S., Kim, J., Yoon, S. J., Park, Y. J., You, Y.A., Hwang, S., & Pang, M. G. (2014). Sodium nitroprusside suppresses male fertility in vitro. Andrology, 2(6), 899-909.
Ramya, T., Misro, M. M., Sinha, D., Nandan, D., & Mithal, S. (2011). Altered levels of seminal nitric oxide, nitric oxide synthase, and enzymatic antioxidants and their association with sperm function in infertile subjects. Fertility and Sterility, 95(1), 135-140.
Roca, J., Martinez-Alborcia, M. J., Gil, M. A., Parrilla, I., & Martinez, E. A. (2013). Dead spermatozoa in raw semen samples impair in vitro fertilization outcomes of frozen-thawed spermatozoa. Fertility and Sterility, 100(3), 875-881.
Rodriguez, P. C., O’flaherty, C. M., Beconi, M. T., & Beorlegui, N. B. (2005). Nitric oxide-induced capacitation of cryopreserved bull spermatozoa and assessment of participating regulatory pathways. Animal Reproduction Science, 85(3-4), 231-242.
Rosselli, M., Dubey, R. K., Imthurn, B., Macas, E., & Keller, P. J. (1995). Andrology: effects of nitric oxide on human spermatozoa: evidence that nitric oxide decreases sperm motility and induces sperm toxicity. Human Reproduction, 10(7), 1786-1790.
Roy, S. C., & Atreja, S. K. (2008). Tyrosine phosphorylation of a 38‐kDa capacitation‐associated buffalo (Bubalus bubalis) sperm protein is induced by L‐arginine and regulated through a cAMP/PKA‐independent pathway. International Journal of Andrology, 31(1), 12-24.
Santos, M. V. D. O., da Silva, A. M., Praxedes, É. A., Borges, A. A., TelesFilho, A. C. D. A., Souza‐Junior, J. B. F., Bertini, L.M., Silva, A.R., & Pereira, A. F. (2019). Antioxidant effects of the essential oil of Syzygiumaromaticum on bovine epididymal spermatozoa. Andrologia, 51(11), e13448.
Semenova, A. V., Tomilova, I. K., Panikratov, K. D., Kadykova, E. L., & Basharin, A. V. (2005). The role of nitric oxide in fertility disorders in men. Urologiia (Moscow, Russia: 1999), (6), 31-36.
Sharafi, M., Zhandi, M., Shahverdi, A., & Shakeri, M. (2015). Beneficial effects of nitric oxide induced mild oxidative stress on post-thawed bull semen quality. International Journal of Fertility and Sterility, 9(2), 230.
Srivastava, S., Desai, P., Coutinho, E., & Govil, G. (2006). Mechanism of action of L-arginine on the vitality of spermatozoa is primarily through increased biosynthesis of nitric oxide. Biology of Reproduction, 74(5), 954-958.
Stochmal, L. S. E. (2000). Effect of sodium nitroprusside on mouse sperm migration in vitro. Archives of andrology, 45(1), 29-33.
Thundathil, J., de Lamirande, E., & Gagnon, C. (2003). Nitric oxide regulates the phosphorylation of the threonine-glutamine-tyrosine motif in proteins of human spermatozoa during capacitation. Biology of Reproduction, 68(4), 1291-1298.
Tomlinson, M. J., East, S. J., Barratt, C. L. R., Bolton, A. E., & Cooke, I. D. (1992). Preliminary communication: possible role of reactive nitrogen intermediates in leucocyte‐mediated sperm dysfunction. American Journal of Reproductive Immunology, 27(1‐2), 89-92.
Ugur, M. R., Saber Abdelrahman, A., Evans, H. C., Gilmore, A. A., Hitit, M., Arifiantini, R. I., Purwantara, B., Kaya, A., & Memili, E. (2019). Advances in cryopreservation of bull sperm. Frontiers in Veterinary Science, 6, 268.
Upadhyay, V. R., Ramesh, V., Dewry, R. K., Yadav, D. K., & Ponraj, P. (2022). Bimodal interplay of reactive oxygen and nitrogen species in physiology and pathophysiology of bovine sperm function. Theriogenology, 187, 82-94.
Upadhyay, V. R., Ramesh, V., Dewry, R. K., Kumar, G., Raval, K., & Patoliya, P. (2021a). Implications of cryopreservation on structural and functional attributes of bovine spermatozoa: An overview. Andrologia, e14154.
Upadhyay, V. R., Roy, A. K., Pandita, S., Kshetrimayum, D., Patoliya, P., Raval, K., Dewry, R. K., Sarita, S. & Nath, S. (2021b). Deciphering dose and time dependent effect of supplementing SNP and L-NAME in extender on progressive motility of Murrah bull spermatozoa. The Indian Journal of Animal Sciences, 91(11).
Vidya, G., Garg, S. P., Rawekar, A. T., Deshpande, V. K., Biswas, D. A., Sawane, M. V., & Akarte, A. N. (2011). Effect of Oxidative stress on sperm quality in Leukocytospermic infertile men. Biomedical Research (0970–938X), 22(3).
Vucetic, M., Otasevic, V., Korac, A., Stancic, A., Jankovic, A., Markelic, M., Golic, I., Velickovic, K., Buzadzic, B., & Korac, B. (2011). Interscapular brown adipose tissue metabolic reprogramming during cold acclimation: Interplay of HIF-1α and AMPKα. Biochimica et Biophysica Acta (BBA)-General Subjects, 1810(12), 1252-1261.
Wu, T. P., Huang, B. M., Tsai, H. C., Lui, M. C., & Liu, M. Y. (2004). Effects of nitric oxide on human spermatozoa activity, fertilization and mouse embryonic development. Archives of Andrology, 50(3), 173-179.

Keywords: Cryo-injury; N-nitro-L-arginine methyl ester (L-NAME); Semen; Sodium nitroprusside (SNP)

31C4KY9ESH (Nitric Oxide)
V55S2QJN2X (NG-Nitroarginine Methyl Ester)
0 (Cryoprotective Agents)

Date Created: 20230126 Date Completed: 20230130 Latest Revision: 20230202

20240628

10.1007/s11250-023-03474-x

36702975