Alicia GILMORE, Mustafa HITIT, Muhammet Rasit UGUR, Thu Tran Nhat DINH, Wei TAN, Dean JOUSAN, Molly NICODEMUS, Einko TOPPER, Abdullah KAYA, Erdogan MEMILI

Functional Variables of Bull Sperm Associated with Cryotolerance

The objective of this study was to ascertain sperm population and cellular characteristics as well as total antioxidant capacity in spermatozoafrom Holstein bulls with Good (11 bulls) and Poor (5 bulls) cryotolerance. Post-thaw sperm kinetics were evaluated using CASA, membraneintegrity was assessed via HOS test, and DNA fragmentation was measured using the HaloSperm kit. Data were analyzed using principalcomponent analysis. The spermatozoa from Good bulls had a higher number of cells with intact membranes (P=0.029), non-fragmented DNA(P=0.018), and post-thaw viability (P

Boğa Sperminin Kriyotolerans İle İlişkili Fonksiyonel Değişkenleri

Bu çalışmanın amacı, iyi (11 boğa) ve zayıf (5 boğa) kriyotoleransa sahip Holstein boğalardan sperm popülasyonun ve hücresel özelliklerinin yanı sıra toplam antioksidan kapasitesini belirlemektir. Dondurma çözdürme sonrası sperm kinetiği CASA kullanılarak değerlendirildi, membran bütünlüğü HOS testi ile değerlendirildi ve DNA fragmantasyonu HaloSperm kiti kullanılarak ölçüldü. Veriler, temel bileşen analizi kullanılarak değerlendirildi (PCA). İyi kriyotoleransa sahip boğalardan elde edilen spermatozoa, zayıf kriyotoleranslı boğalardan alınan sperme kıyasla daha fazla sayıda intakt membran (P=0.029), fragmente olmamış DNA’ya (P=0.018) ve dondurma çözdürme sonrası canlılığa (P

PDF

___

1. Graham JK, Kunze E, Hammerstedt RH: Analysis of sperm cell viability, acrosomal integrity, and mitochondrial function using flow cytometry. Biol. Reprod, 43 (1): 55-64, 1990. DOI: 10.1095/biolreprod43.1.55

2. Ugur MR, Saber Abdelrahman A, Evans HC, Gilmore AA, Hitit M, Arifiantini RI, Purwantara B, Kaya A, Memili E: Advances in cryopreservation of bull sperm. Front Vet Sci, 6:268, 2019. DOI: 10.3389/ fvets.2019.00268

3. Barth AD, Oko RJ: Abnormal morphology of bovine spermatozoa. (Iowa State University Press), 1989.

4. Kastelic JP, Thundathil JC: Breeding soundness evaluation and semen analysis for predicting bull fertility. Reprod Domest Anim, 43, 368-373, 2008. DOI: 10.1111/j.1439-0531.2008.01186.x

5. Nagata MPB, Egashira J, Katafuchi N, Endo K, Ogata K, Yamanaka K, Yamanouchi T, Matsuda H, Hashiyada Y, Yamashita K: Bovine sperm selection procedure prior to cryopreservation for improvement of postthawed semen quality and fertility. J Anim Sci Biotechnol, 10:91, 2019. DOI: 10.1186/s40104-019-0395-9

6. Katz DF, Diel L, Overstreet JW: Differences in the movement of morphologically normal and abnormal human seminal spermatozoa. Biol Reprod, 26 (4): 566-570, 1982. DOI: 10.1095/biolreprod26.4.566

7. Li Y, Kalo D, Zeron Y, Roth Z: Progressive motility-a potential predictive parameter for semen fertilization capacity in bovines. Zygote, 24 (1): 70- 82, 2016. DOI: 10.1017/s0967199414000720

Determinants of Sperm Freezability Research Article 8. Nadir S, Saacke RG, Bame J, Mullins J, Degelos S: Effect of freezing semen and dosage of sperm on number of accessory sperm, fertility, and embryo quality in artificially inseminated cattle. J Anim Sci, 71 (1): 199- 204. 1993. DOI: 10.2527/1993.711199x

9. Pardede BP, Supriatna I, Yudi Y, Agil M: Decreased bull fertility: agerelated changes in sperm motility and DNA fragmentation. E3S Web Conf, 151:01010, 2020. DOI: 10.1051/e3sconf/202015101010

10. Muiño R, Rivera MM, Rigau T, Rodriguez-Gil JE, Peña AI: Effect of different thawing rates on post-thaw sperm viability, kinematic parameters and motile sperm subpopulations structure of bull semen. Anim Reprod Sci, 109 (1-4): 50-64, 2008. DOI: 10.1016/j.anireprosci.2007.11.028

11. Medeiros CMO, Forell F, Oliveira ATD, Rodrigues JL: Current status of sperm cryopreservation: Why isn’t it better? Theriogenology, 57, 327- 344, 2002. DOI: 10.1016/S0093-691X(01)00674-4

12. Gunawan M, Kaiin EM, Mudita GS, Chaidir RRA: Soybean phospholipids-based extender as an alternative for bull sperm cryopreservation. IOP Conf Ser Earth Environ Sci, 478:012014, 2020. DOI: 10.1088/1755-1315/478/1/012014

13. Yoon SJ, Kwon WS, Rahman MS, Lee JS, Pang MG: A novel approach to identifying physical markers of cryo-damage in bull spermatozoa. PLoS One, 10 (5): e0126232, 2015. DOI: 10.1371/journal.pone.0126232

14. Peris-Frau P, Soler AJ, Iniesta-Cuerda M, Martín-Maestro A, Sánchez-Ajofrín I, Medina-Chávez DA, Fernández-Santos MR, Garcíaálvarez O, Maroto-Morales A, Montoro V, Garde JJ: Sperm cryodamage in ruminants: Understanding the molecular changes induced by the cryopreservation process to optimize sperm quality. Int J Mol Sci, 21 (8): 2781, 2020. DOI: 10.3390/ijms21082781

15. Khalil WA, El-Harairy MA, Zeidan AE, Hassan MA, Mohey-Elsaeed O: Evaluation of bull spermatozoa during and after cryopreservation: Structural and ultrastructural insights. Int J Vet Sci Med, 6, S49-S56, 2018. DOI: 10.1016/j.ijvsm.2017.11.001

16. Grötter LG, Cattaneo L, Marini PE, Kjelland M, and Ferré LB: Recent advances in bovine sperm cryopreservation techniques with a focus on sperm post-thaw quality optimization. Reprod Domest Anim, 54 (4): 655- 665, 2019. DOI: 10.1111/rda.13409

17. Aitken RJ, Mark AB, Brett Nixon: Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress? Asian J Androl, 17 (4): 633-639, 2015. DOI: 10.4103/1008-682X.153850

18. Diether N, Dyck MK: Male fertility evaluation using biomarkers in livestock. JSM Biomar, 3 (1): 1011, 2017.

19. Aitken RJ, De Iuliis GN: On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod, 16 (1): 3-13, 2010. DOI: 10.1093/ molehr/gap059

20. Di Santo M, Tarozzi N, Nadalini M, Borini A: Human sperm cryopreservation: Update on techniques, effect on DNA integrity, and implications for ART. Adv Urol, 2012:854837, 2012.

21. Evenson DP, Larson KL, Jost LK: Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl, 23, 25-43, 2002. DOI: 10.1002/j.1939-4640.2002.tb02599.x

22. Said TM, Gaglani A, Agarwal A: Implication of apoptosis in sperm cryoinjury. Reprod Biomed Online, 21 (4): 456-462, 2010. DOI: 10.1016/j. rbmo.2010.05.011

23. Gürler H, Malama E, Heppelmann M, Calisici O, Leiding C, Kastelic JP, Bollwein H: Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology, 86, 562-571, 2016. DOI: 10.1016/j.theriogenology. 2016.02.007

24. Ballester J, Johannisson A, Saravia F, Håård M, Gustafsson H, Bajramovic D, Rodriguez-Martinez H: Post-thaw viability of bull AIdoses with low-sperm numbers. Theriogenology, 68 (6): 934-943, 2007. DOI: 10.1016/j.theriogenology.2007.07.008

25. Ugur MR, Dinh T, Hitit M, Kaya A, Topper E, Didion B, Memili E: Amino acids of seminal plasma associated with freezability of bull sperm. Front Cell Dev Biol, 7:347, 2020. DOI: 10.3389/fcell.2019.00347

26. Pace MM, Sullivan JJ, Elliott FI, Graham EF, Coulter GH: Effects of thawing temperature, number of spermatozoa and spermatozoal quality on fertility of bovine spermatozoa packaged in. 5-ml French straws. J Anim Sci, 53, 693-701, 1981. DOI: 10.2527/jas1981.533693x

27. Garner DL, Johnson LA, Yue ST, Roth BL, Haugland RP: Dual DNA staining assessment of bovine sperm viability using sybr‐14 and propidium iodide. J Androl, 15 (6): 620-629, 1994.

28. Ibănescu I, Leiding C, Ciornei ŞG, RoŞca P, Sfartz I, Drugociu D: Differences in CASA output according to the chamber type when analyzing frozen-thawed bull sperm. Anim Reprod Sci, 166, 72-79, 2016. DOI: 10.1016/j.anireprosci.2016.01.005

29. Gadkar S, Shah CA, Sachdeva G, Samant U, Puri CP: Progesterone receptor as an indicator of sperm function. Biol Reprod, 67 (4): 1327-1336, 2002. DOI: 10.1095/biolreprod67.4.1327

30. Dogan S, Mason MC, Govindaraju A, Belser L, Kaya A, Stokes J, Rowe D, Memili E: Interrelationships between apoptosis and fertility in bull sperm. J Reprod Dev, 59 (1): 18-26, 2013. DOI: 10.1262/jrd.2012-068

31. Roychoudhury S, Sharma R, Sikka S, Agarwal A: Diagnostic application of total antioxidant capacity in seminal plasma to assess oxidative stress in male factor infertility. J Assist Reprod Genet, 33 (5): 627- 635, 2016. DOI: 10.1007/s10815-016-0677-5

32. Kumar D, Kumar PR, Singh PA, Yadav SP, Sarkar SK, Bharadwaj A, Yadav PS: Characteristics of frozen thawed semen in predicting the fertility of buffalo bulls. Indian J Anim Sci, 84, 389-392, 2014.

33. Karunakaran M, Devanathan TG: Evaluation of bull semen for fertility-associated protein, in vitro characters and fertility. J Appl Anim Res, 45 (1): 136-144, 2017. DOI: 10.1080/09712119.2015.1129343

34. Jiang XP, Zhou WM, Wang SQ, Wang W, Tang JY, Xu Z, Zhang ZX, Qin C, Wang ZJ, Zhang W: Multivariate model for predicting semen cryopreservation outcomes in a human sperm bank. Asian J Androl, 19 (4): 404-408, 2017. DOI: 10.4103/1008-682X.178488

35. Singh P, Kumar D, Kumar P, Singh I, Yadav PS: Cryopreservation and quality assessment of buffalo bull semen collected from farmer’s doorstep. Agric Res, 2 (2): 148-152, 2013. DOI: 10.1007/s40003-013-0056-8

36. Nagy Á, Polichronopoulos T, Gáspárdy A, Solti L, Cseh S: Correlation between bull fertility and sperm cell velocity parameters generated by computer-assisted semen analysis. Acta Vet Hung, 63 (3): 370-381, 2015. DOI: 10.1556/004.2015.035

37. Bollwein H, Bittner L: Impacts of oxidative stress on bovine sperm function and subsequent in vitro embryo development. Anim Reprod, 15 (Suppl. 1): 703-710, 2018. DOI: 10.21451/1984-3143-AR2018-0041

38. Morrell JM, Valeanu AS, Lundeheim N, Johannisson A: Sperm quality in frozen beef and dairy bull semen. Acta Vet Scand, 60:41, 2018. DOI: 10.1186/s13028-018-0396-2

39. Ismail NH, Osman K, Mohd Yusof FZ, Syed Mohamad SF, Jaafar FHF, Ibrahim SF: Improvement of post-thaw sperm kinematics and dna integrity of cross-bred bovine sperm by incorporating dgc as selection method prior to cryopreservation. J Agric Sci, 9 (13): 24-31, 2017. DOI: 10.5539/jas.v9n13p24

40. Sieme H, Oldenhof H, Wolkers WF: Sperm membrane behaviour during cooling and cryopreservation. Reprod Domest Anim, 50, 20-26, 2015. DOI: 10.1111/rda.12594

41. Kasimanickam R, Kasimanickam V, Thatcher CD, Nebel RL, Cassell BG: Relationships among lipid peroxidation, glutathione peroxidase, superoxide dismutase, sperm parameters, and competitive index in dairy bulls. Theriogenology, 67 (5): 1004-1012, 2007. DOI: 10.1016/j. theriogenology.2006.11.013

42. Ryu DY, Song WH, Pang WK, Yoon SJ, Rahman MS, Pang MG: Freezability biomarkers in bull epididymal spermatozoa. Sci Rep, 9:12797, 2019. DOI: 10.1038/s41598-019-49378-5

43. Nijs M, Creemers E, Cox A, Janssen M, Vanheusden E, CastroSanchez Y, Thijs H, Ombelet W: Influence of freeze-thawing on hyaluronic acid binding of human spermatozoa. Reprod Biomed, 19, 202- 206, 2009. DOI: 10.1016/S1472-6483(10)60073-9

44. Castro LS, Hamilton TRS, Mendes CM, Nichi M, Barnabe VH, Visintin JA, Assumpção MEOA: Sperm cryodamage occurs after rapid freezing phase: Flow cytometry approach and antioxidant enzymes activity at different stages of cryopreservation. J Anim Sci Biotechnol, 7:17, 2016. DOI: 10.1186/s40104-016-0076-x

45. El-Regalaty H: Effects of cryopreservation of buffalo and bovine spermatozoa on sperm dna damage and early embryonic development. J Anim Poult Prod, 8 (7): 167-172, 2017. DOI: 10.21608/jappmu. 2017.45843

46. Kumaresan A, Gupta MD, Datta TK, Morrell JM: Sperm DNA integrity and male fertility in farm animals: A review. Front Vet Sci, 7:321, 2020. DOI: 10.3389/fvets.2020.00321

47. Enciso M, Cisale H, Johnston SD, Sarasa J, Fernández JL, Gosálvez J: Major morphological sperm abnormalities in the bull are related to sperm DNA damage. Theriogenology, 76 (1): 23-32, 2011. DOI: 10.1016/j. theriogenology.2010.12.034

48. Karoui S, Díaz C, González-Marín C, Amenabar ME, Serrano M, Ugarte E, Gosálvez J, Roy R, López-Fernández C, Carabaño MJ: Is sperm DNA fragmentation a good marker for field AI bull fertility?. J Anim Sci, 90 (8): 2437-2449, 2012. DOI: 10.2527/jas.2011-4492

49. Li MW, Lloyd KCK: DNA fragmentation index (DFI) as a measure of sperm quality and fertility in mice. Sci Rep. 10:3833, 2020. DOI: 10.1038/ s41598-020-60876-9

50. Hitit M, Ugur MR, Dihn TT, Sajeev D, Kaya A, Topper E, Tan W, Memili E: Cellular and functional physiopathology of bull sperm with altered sperm freezability. Front Vet Sci, 7:581137, 2020. DOI: 10.3389/ fvets.2020.581137

51. Lewis SEM, Sterling ESL, Young IS, Thompson W: Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil Steril, 67 (1): 142-147, 1997. DOI: 10.1016/s0015- 0282(97)81871-7

52. Smith R, Vantman D, Ponce J, Escobar J, Lissi E: Andrology: Total antioxidant capacity of human seminal plasma. Hum Reprod, 11 (8): 1655- 1660, 1996. DOI: 10.1093/oxfordjournals.humrep.a019465

53. Siciliano L, Tarantino P, Longobardi F, Rago V, De Stefano C, Carpino A: Impaired seminal antioxidant capacity in human semen with hyperviscosity or oligoasthenozoospermia. J Androl, 22 (5): 798-803, 2001.

54. Bucak MN, Tuncer PB, Sarıözkan S, Baspınar N, Taspınar M, Çoyan K, Bilgili A, Peker Akalın P, Büyükleblebici S, Aydos S, Ilgaz S, Sunguroğlu A, Öztuna D: Effects of antioxidants on post-thawed bovine sperm and oxidative stress parameters: Antioxidants protect DNA integrity against cryodamage. Cryobiology, 61, 248-253, 2010. DOI: 10.1016/j.cryobiol.2010.09.001