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Flow Cytometric Examination of The Interaction Between Drone Sperm (Apis Mellifera Anatoliaca) and Insulin in Soybean Lecithin-Based Cryopreservation Extenders

Year 2024, Volume: 43 Issue: 1, 46 - 54, 02.09.2024

Mehmed Berk Toker , Ahmet Aktar , Selvinar Seven-çakmak , İbrahim Çakmak , Mustafa Akkaşoğlu , Selim Alçay

https://doi.org/10.30782/jrvm.1420188

Abstract

This study was conducted to evaluate the effects of different doses of insulin (5, 10, and 15 IU) added to soybean lecithin-based drone sperm freezing extenders on sperm parameters through flow cytometry or microscopic examinations. Samples obtained from sexually mature bees were pooled to eliminate individual variation. The freezing process was organized with three insulin supplemented doses and one insulin-free control group, and the method was implemented as planned. Thawed samples were evaluated for motility, plasma membrane (hypo-osmotic swelling test), and DNA integrity (TUNEL assay) using a phase-contrast microscope with fluorescent attachment. Additionally, acrosomal integrity (PNA-FITC), nitric oxide levels (DAF-2/DA), and mitochondrial membrane potential (JC-1) were investigated using a flow cytometer. As expected, all sperm parameters were affected by the freezing process inherently, however, the insulin-supplemented experimental groups did not demonstrate a statistically significant positive difference compared to the control group. In light of these results, it was determined that the use of insulin supplementation, in preferred doses, in soybean lecithin-based drone sperm cryopreservation extenders did not have a positive effect on achieving higher productive honeybee colonies and elevating the country's yield in bee products through auxiliary biotechnological methods as desired.

Keywords

Apis mellifera anatoliaca Drone sperm Flow-cytometer Insulin Soybean lecithin Sperma cryopreservation

Project Number

Bursa Uludağ Üniversitesi Bilimsel Araştırma Projeleri Birimi (BAP) - TGA – 2022 - 718

References

  • Henry LC, Álvaro D rebolledo, Karen C medina, Jorge V rodríguez, Francisco E valente. Effect of egg yolk on sperm cryopreservation of drone (Apis mellifera). Abanico Vet. 2019;9(December):1-11. doi:10.21929/ abavet2019.921
  • Stankus T. A review and bibliography of the literature of honey bee colony collapse disorder: A poorly understood epidemic that Clearly Threatens the successful pollination of billions of dollars of crops in America. J Agric Food Inf. 2008;9(2):115-143. doi:10.1080/10496500802173939
  • Gül A, Şahinler N, Onal AG, Hopkins BK, Sheppard WS. Effects of diluents and plasma on honey bee (Apis mellifera L.) drone frozen-thawed semen fertility. Theriogenology. 2017;101:109-113. doi:10.1016/j. theriogenology.2017.06.020
  • Woyke J, Jasinski Z. Influence of Age of Drones on the Results of Instrumental Insemination of Honeybee Queens. Apidologie. 1978;9(3):203-212. doi:10.1051/ apido:19780304
  • Cobey SW. Comparison studies of instrumentally inseminated and naturally mated honey bee queens and factors affecting their performance. Apidologie. 2007;38(4):390-410. doi:10.1051/apido:2007029
  • Alçay S, Üstüner B, Çakmak İ, Çakmak S, Nur Z. Effects of Various Cryoprotective Agents on Post-Thaw Drone Semen Quality. Kafkas Univ Vet Fak Derg. 2015;21(1):31-35. doi:10.9775/kvfd.2014.11515
  • Almadaly EA, Tawfik FS, El-Kon II, Heleil BA, Fattouh ESM. Effect of different cryoprotectants on the post-thaw sperm characteristics and in vivo fertility of buffalo (Bubalus bubalis) bull semen. Slov Vet Res. 2019;56(February):541-551. doi:10.26873/SVR-792-2019
  • Tonieto RA, Goularte KL, Gastal GDA, Schiavon RS, Deschamps JC, Lucia T. Cryoprotectant effect of trehalose and low-density lipoprotein in extenders for frozen ram semen. Small Rumin Res. 2010;93(2-3):206- 209. doi:10.1016/j.smallrumres.2010.05.003
  • Abdelkader F Ben, Kairo G, Bonnet M, Barbouche N, Belzunces LP, Brunet JL. Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen. J Apic Res. 2019;58(5):740- 745. doi:10.1080/00218839.2019.1655182
  • Kulaksiz R, Daskin AD. In vitro evaluation of Saanen buck semen frozen in different extenders supplemented with various antioxidants. Ankara Üniv Vet Fak Derg. 2010;57:151-156. doi:10.1501/Vetfak_0000002369
  • Borsuk G, Kozłowska M, Anusiewicz M, Paleolog J. Nosema ceranae changes semen characteristics and damages sperm DNA in honeybee drones. Invertebr Surviv J. 2018;15:197-202.
  • Ciereszko A, Wilde J, Dietrich GJ, et al. Sperm parameters of honeybee drones exposed to imidacloprid. Apidologie. 2017;48(2):211-222. doi:10.1007/s13592- 016-0466-2
  • Toker MB, Alcay S, Gokce E, Ustuner B. Cryopreservation of ram semen with antioxidant supplemented soybean lecithin-based extenders and impacts on incubation resilience. Cryobiology. 2016;72(3):205-209. doi:10.1016/j.cryobiol.2016.05.001
  • Alcay S, Toker MB, Onder NT, Gokce E. Royal jelly supplemented soybean lecithin-based extenders improve post-thaw quality and incubation resilience of goat spermatozoa. Cryobiology. 2017;74:81-85. doi:10.1016/j.cryobiol.2016.11.011
  • Taylor MA, Guzmán-Novoa E, Morfin N, Buhr MM. Improving viability of cryopreserved honey bee (Apis mellifera L.) sperm with selected diluents, cryoprotectants, and semen dilution ratios. Theriogenology. 2009;72(2):149-159. doi:10.1016/j.theriogenology. 2009.02.012
  • Forouzanfar M, Sharafi M, Hosseini SM, et al. In vitro comparison of egg yolk-based and soybean lecithin-based extenders for cryopreservation of ram semen. Theriogenology. 2010;73(4):480-487. doi:10.1016/j.theriogenology.2009.10.005
  • Vidal AH, Batista AM, da Silva ECB, et al. Soybean lecithin- based extender as an alternative for goat sperm cryopreservation. Small Rumin Res. 2013;109(1):47-51. doi:10.1016/j.smallrumres.2012.07.022
  • Aktar A, Alçay S. L-Karnitin İlave Edilmiş Sulandırıcıların Dondurma-Çözdürme Sonrası Teke Spermasının Spermatolojik Parametleri Üzerine Etkisi. J Res Vet Med. 2022;41(1):37-42. doi:10.30782/jrvm.999299
  • Andò S, Aquila S. Arguments raised by the recent discovery that insulin and leptin are expressed in and secreted by human ejaculated spermatozoa. Mol Cell Endocrinol. 2005;245(1-2):1-6. doi:10.1016/j. mce.2005.09.011
  • Pinto SCC, Souza FA, Arruda RP, et al. Impact of adding different concentrations of IGF-I and insulin to the semen extender on bull sperm quality post-cryopreservation. Arq Bras Med Vet e Zootec. 2023;75(5):771- 786. doi:10.1590/1678-4162-12946
  • van Tilburg MF, de Oliveira RV, Gadelha CRF, et al. Effects of insulin on sperm cell quality in ram semen cooled at 5°C. Semin Agrar. 2021;42(6):3802-3812. doi:10.5433/1679-0359.2021v42n6Supl2p3803
  • Önder NT, Gökdemir T, Kiliç MC, et al. Insulin and Bull Sperm Interactions During Cryopreservation. Kafkas Univ Vet Fak Derg. 2023;29(4):401-405. doi:10.9775/kvfd.2023.29623
  • Aquila S, Gentile M, Middea E, Catalano S, Andò S. Autocrine regulation of insulin secretion in human ejaculated spermatozoa. Endocrinology. 2005;146(2):552- 557. doi:10.1210/en.2004-1252
  • Lampiao F, Du Plessis SS. Insulin and leptin enhance human sperm motility, acrosome reaction and nitric oxide production. Asian J Androl. 2008;10(5):799-807. doi:10.1111/j.1745-7262.2008.00421.x
  • Shokri S, Ebrahimi SM, Ziaeipour S, Nejatbakhsh R.Effect of insulin on functional parameters of human cryopreserved sperms. Cryobiology. 2019;87(February):68-73. doi:10.1016/j.cryobiol.2019.02.002
  • Alcay S, Cakmak S, Cakmak I, et al. L-carnitine supplemented extenders improve post-thawing quality of honey bee drone (Apis mellifera) spermatozoa[1]. Kafkas Univ Vet Fak Derg. 2021;27(4):489-493. doi:10.9775/kvfd.2021.25756
  • Alçay S, Çakmak S, Çakmak İ, et al. Drone semen cryopreservation with protein supplemented TLhepes based extender. Kafkas Univ Vet Fak Derg. 2019;25(4):553-557. doi:10.9775/kvfd.2018.21311
  • Nur Z, Seven Çakmak S, Çakmak İ, et al. Effects of Trehalose Supplementation on Post-Thaw Sperm Quality of Honey Bee Drones. Online J Anim Feed Res. 2020;10(5):191-196. doi:10.51227/ojafr.2020.27
  • Alcay S, Cakmak S, Cakmak I, et al. Successful cryopreservation of honey bee drone spermatozoa with royal jelly supplemented extenders. Cryobiology. 2019;87(October 2018):28-31. doi:10.1016/j.cryobiol. 2019.03.005
  • Wegener J, May T, Kamp G, Bienefeld K. A successful new approach to honeybee semen cryopreservation. Cryobiology. 2014;69(2):236-242. doi:10.1016/j.cryobiol. 2014.07.011
  • Gürler H, Malama E, Heppelmann M, et al. Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology. 2015;86(2):562-571. doi:10.1016/j. theriogenology.2016.02.007
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Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi

Year 2024, Volume: 43 Issue: 1, 46 - 54, 02.09.2024

Mehmed Berk Toker , Ahmet Aktar , Selvinar Seven-çakmak , İbrahim Çakmak , Mustafa Akkaşoğlu , Selim Alçay

https://doi.org/10.30782/jrvm.1420188

Abstract

Gen havuzlarının istenen yönde gelişimine katkıda bulunan üreme kontrolü, spermanın dondurması ile alakalı biyoteknolojik yöntemleri önemli bir noktaya koymaktadır. Sperma dondurmaya yöntelik çalışmalar özellikle memelilerde yoğun olarak çalışılmış olmasına rağmen, arı sperması açısından başlangıç aşamasındadır. İnsülinin seminal plazmada bulunduğu ve çeşitli sperma parametreleri üzerine etkilerinin olduğu güncel çalışmalarla desteklenmiştir. Ayrıca, soya lesitini uzun süredir, özellikle yumurta sarısına alternatif, güvenilir bir kaynak olarak sperma dondurma sulandırıcılarında tercih edilen maddelerden biridir. Bu çalışma, soya lesitini (%2) temelli arı sperma dondurma sulandırıcılarına farklı dozlarda insülin (5, 10 ve 15 IU dozda) eklenmesi sonucunda elde edilecek sonuçların, flow sitometri veya mikroskopik incelemeler aracılığıyla önemli sperma parametreleri üzerindeki etkileri değerlendirmek amacıyla gerçekleştirişmiştir. Cinsel olgunluğa ulaşmış arılardan elde edilen örnekler bireysel farklılığı engellemek adına birleştirildi (pooling). Dondurma işlemi, üç doz insülin destekli ve bir insülin içermeyen kontrol grubu olacak şekilde düzenlendi ve yöntem planlandığı şekilde uygulandı. Dondurulup çözülen örnekler; motilite, plazma membran (hipo-osmotik şişme testi) ve DNA bütünlüğü (TUNEL testi) değerlendirmelerine, floresan ataçmanı olan bir faz kontrast mikroskobu kullanılarak gerçekleştirildi. Ayrıca, akrozomal bütünlük (PNA-FITC), nitrik oksit seviyeleri (DAF-2/DA) ve mitokondriyal membran potansiyeli (JC-1), bir flow sitometri cihazı aracılığıyla araştırıldı. Beklendiği gibi, tüm sperma parametreleri dondurma işleminin doğası gereği etkilendi, ancak insülin eklenmiş çalışma grupları, kontrol grubuna kıyasla pozitif yönde bir istatistiki farkı ortaya koyamadı. Bu sonuçlar ışığında, soya lesitini temelli arı sperması dondurma sulandırıcılarında kullanılan insülin takviyesinin tercih edilen dozlarda kullanılmasının, yardımcı biyoteknolojik yöntemler aracılığıyla daha yüksek verimli arı kolonileri elde edilmesi ve arı ürünleri konusunda ülke veriminin istenilen düzeye çıkartılması konusunda olumlu bir etkiye sahip olmadığı tespit edildi.

Keywords

Apis mellifera anatoliaca Arı sperması Flow-sitometri İnsülin Soya lesitini Sperma dondurma

Project Number

Bursa Uludağ Üniversitesi Bilimsel Araştırma Projeleri Birimi (BAP) - TGA – 2022 - 718

References

  • Henry LC, Álvaro D rebolledo, Karen C medina, Jorge V rodríguez, Francisco E valente. Effect of egg yolk on sperm cryopreservation of drone (Apis mellifera). Abanico Vet. 2019;9(December):1-11. doi:10.21929/ abavet2019.921
  • Stankus T. A review and bibliography of the literature of honey bee colony collapse disorder: A poorly understood epidemic that Clearly Threatens the successful pollination of billions of dollars of crops in America. J Agric Food Inf. 2008;9(2):115-143. doi:10.1080/10496500802173939
  • Gül A, Şahinler N, Onal AG, Hopkins BK, Sheppard WS. Effects of diluents and plasma on honey bee (Apis mellifera L.) drone frozen-thawed semen fertility. Theriogenology. 2017;101:109-113. doi:10.1016/j. theriogenology.2017.06.020
  • Woyke J, Jasinski Z. Influence of Age of Drones on the Results of Instrumental Insemination of Honeybee Queens. Apidologie. 1978;9(3):203-212. doi:10.1051/ apido:19780304
  • Cobey SW. Comparison studies of instrumentally inseminated and naturally mated honey bee queens and factors affecting their performance. Apidologie. 2007;38(4):390-410. doi:10.1051/apido:2007029
  • Alçay S, Üstüner B, Çakmak İ, Çakmak S, Nur Z. Effects of Various Cryoprotective Agents on Post-Thaw Drone Semen Quality. Kafkas Univ Vet Fak Derg. 2015;21(1):31-35. doi:10.9775/kvfd.2014.11515
  • Almadaly EA, Tawfik FS, El-Kon II, Heleil BA, Fattouh ESM. Effect of different cryoprotectants on the post-thaw sperm characteristics and in vivo fertility of buffalo (Bubalus bubalis) bull semen. Slov Vet Res. 2019;56(February):541-551. doi:10.26873/SVR-792-2019
  • Tonieto RA, Goularte KL, Gastal GDA, Schiavon RS, Deschamps JC, Lucia T. Cryoprotectant effect of trehalose and low-density lipoprotein in extenders for frozen ram semen. Small Rumin Res. 2010;93(2-3):206- 209. doi:10.1016/j.smallrumres.2010.05.003
  • Abdelkader F Ben, Kairo G, Bonnet M, Barbouche N, Belzunces LP, Brunet JL. Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen. J Apic Res. 2019;58(5):740- 745. doi:10.1080/00218839.2019.1655182
  • Kulaksiz R, Daskin AD. In vitro evaluation of Saanen buck semen frozen in different extenders supplemented with various antioxidants. Ankara Üniv Vet Fak Derg. 2010;57:151-156. doi:10.1501/Vetfak_0000002369
  • Borsuk G, Kozłowska M, Anusiewicz M, Paleolog J. Nosema ceranae changes semen characteristics and damages sperm DNA in honeybee drones. Invertebr Surviv J. 2018;15:197-202.
  • Ciereszko A, Wilde J, Dietrich GJ, et al. Sperm parameters of honeybee drones exposed to imidacloprid. Apidologie. 2017;48(2):211-222. doi:10.1007/s13592- 016-0466-2
  • Toker MB, Alcay S, Gokce E, Ustuner B. Cryopreservation of ram semen with antioxidant supplemented soybean lecithin-based extenders and impacts on incubation resilience. Cryobiology. 2016;72(3):205-209. doi:10.1016/j.cryobiol.2016.05.001
  • Alcay S, Toker MB, Onder NT, Gokce E. Royal jelly supplemented soybean lecithin-based extenders improve post-thaw quality and incubation resilience of goat spermatozoa. Cryobiology. 2017;74:81-85. doi:10.1016/j.cryobiol.2016.11.011
  • Taylor MA, Guzmán-Novoa E, Morfin N, Buhr MM. Improving viability of cryopreserved honey bee (Apis mellifera L.) sperm with selected diluents, cryoprotectants, and semen dilution ratios. Theriogenology. 2009;72(2):149-159. doi:10.1016/j.theriogenology. 2009.02.012
  • Forouzanfar M, Sharafi M, Hosseini SM, et al. In vitro comparison of egg yolk-based and soybean lecithin-based extenders for cryopreservation of ram semen. Theriogenology. 2010;73(4):480-487. doi:10.1016/j.theriogenology.2009.10.005
  • Vidal AH, Batista AM, da Silva ECB, et al. Soybean lecithin- based extender as an alternative for goat sperm cryopreservation. Small Rumin Res. 2013;109(1):47-51. doi:10.1016/j.smallrumres.2012.07.022
  • Aktar A, Alçay S. L-Karnitin İlave Edilmiş Sulandırıcıların Dondurma-Çözdürme Sonrası Teke Spermasının Spermatolojik Parametleri Üzerine Etkisi. J Res Vet Med. 2022;41(1):37-42. doi:10.30782/jrvm.999299
  • Andò S, Aquila S. Arguments raised by the recent discovery that insulin and leptin are expressed in and secreted by human ejaculated spermatozoa. Mol Cell Endocrinol. 2005;245(1-2):1-6. doi:10.1016/j. mce.2005.09.011
  • Pinto SCC, Souza FA, Arruda RP, et al. Impact of adding different concentrations of IGF-I and insulin to the semen extender on bull sperm quality post-cryopreservation. Arq Bras Med Vet e Zootec. 2023;75(5):771- 786. doi:10.1590/1678-4162-12946
  • van Tilburg MF, de Oliveira RV, Gadelha CRF, et al. Effects of insulin on sperm cell quality in ram semen cooled at 5°C. Semin Agrar. 2021;42(6):3802-3812. doi:10.5433/1679-0359.2021v42n6Supl2p3803
  • Önder NT, Gökdemir T, Kiliç MC, et al. Insulin and Bull Sperm Interactions During Cryopreservation. Kafkas Univ Vet Fak Derg. 2023;29(4):401-405. doi:10.9775/kvfd.2023.29623
  • Aquila S, Gentile M, Middea E, Catalano S, Andò S. Autocrine regulation of insulin secretion in human ejaculated spermatozoa. Endocrinology. 2005;146(2):552- 557. doi:10.1210/en.2004-1252
  • Lampiao F, Du Plessis SS. Insulin and leptin enhance human sperm motility, acrosome reaction and nitric oxide production. Asian J Androl. 2008;10(5):799-807. doi:10.1111/j.1745-7262.2008.00421.x
  • Shokri S, Ebrahimi SM, Ziaeipour S, Nejatbakhsh R.Effect of insulin on functional parameters of human cryopreserved sperms. Cryobiology. 2019;87(February):68-73. doi:10.1016/j.cryobiol.2019.02.002
  • Alcay S, Cakmak S, Cakmak I, et al. L-carnitine supplemented extenders improve post-thawing quality of honey bee drone (Apis mellifera) spermatozoa[1]. Kafkas Univ Vet Fak Derg. 2021;27(4):489-493. doi:10.9775/kvfd.2021.25756
  • Alçay S, Çakmak S, Çakmak İ, et al. Drone semen cryopreservation with protein supplemented TLhepes based extender. Kafkas Univ Vet Fak Derg. 2019;25(4):553-557. doi:10.9775/kvfd.2018.21311
  • Nur Z, Seven Çakmak S, Çakmak İ, et al. Effects of Trehalose Supplementation on Post-Thaw Sperm Quality of Honey Bee Drones. Online J Anim Feed Res. 2020;10(5):191-196. doi:10.51227/ojafr.2020.27
  • Alcay S, Cakmak S, Cakmak I, et al. Successful cryopreservation of honey bee drone spermatozoa with royal jelly supplemented extenders. Cryobiology. 2019;87(October 2018):28-31. doi:10.1016/j.cryobiol. 2019.03.005
  • Wegener J, May T, Kamp G, Bienefeld K. A successful new approach to honeybee semen cryopreservation. Cryobiology. 2014;69(2):236-242. doi:10.1016/j.cryobiol. 2014.07.011
  • Gürler H, Malama E, Heppelmann M, et al. Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology. 2015;86(2):562-571. doi:10.1016/j. theriogenology.2016.02.007
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There are 54 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Sciences (Other)
Journal Section Research Articles
Authors

Mehmed Berk Toker 0000-0003-4033-9749

Ahmet Aktar 0000-0002-2975-2594

Selvinar Seven-çakmak 0000-0002-2674-0731

İbrahim Çakmak 0000-0002-8000-5770

Mustafa Akkaşoğlu 0000-0001-6876-0821

Selim Alçay 0000-0002-2472-8157

Project Number Bursa Uludağ Üniversitesi Bilimsel Araştırma Projeleri Birimi (BAP) - TGA – 2022 - 718
Publication Date September 2, 2024
Submission Date January 17, 2024
Acceptance Date March 27, 2024
Published in Issue Year 2024 Volume: 43 Issue: 1

Cite

APA Toker, M. B., Aktar, A., Seven-çakmak, S., Çakmak, İ., et al. (2024). Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi. Journal of Research in Veterinary Medicine, 43(1), 46-54. https://doi.org/10.30782/jrvm.1420188
AMA Toker MB, Aktar A, Seven-çakmak S, Çakmak İ, Akkaşoğlu M, Alçay S. Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi. J Res Vet Med. September 2024;43(1):46-54. doi:10.30782/jrvm.1420188
Chicago Toker, Mehmed Berk, Ahmet Aktar, Selvinar Seven-çakmak, İbrahim Çakmak, Mustafa Akkaşoğlu, and Selim Alçay. “Arı Sperması (Apis Mellifera Anatoliaca) Ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak Incelenmesi”. Journal of Research in Veterinary Medicine 43, no. 1 (September 2024): 46-54. https://doi.org/10.30782/jrvm.1420188.
EndNote Toker MB, Aktar A, Seven-çakmak S, Çakmak İ, Akkaşoğlu M, Alçay S (September 1, 2024) Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi. Journal of Research in Veterinary Medicine 43 1 46–54.
IEEE M. B. Toker, A. Aktar, S. Seven-çakmak, İ. Çakmak, M. Akkaşoğlu, and S. Alçay, “Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi”, J Res Vet Med, vol. 43, no. 1, pp. 46–54, 2024, doi: 10.30782/jrvm.1420188.
ISNAD Toker, Mehmed Berk et al. “Arı Sperması (Apis Mellifera Anatoliaca) Ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak Incelenmesi”. Journal of Research in Veterinary Medicine 43/1 (September 2024), 46-54. https://doi.org/10.30782/jrvm.1420188.
JAMA Toker MB, Aktar A, Seven-çakmak S, Çakmak İ, Akkaşoğlu M, Alçay S. Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi. J Res Vet Med. 2024;43:46–54.
MLA Toker, Mehmed Berk et al. “Arı Sperması (Apis Mellifera Anatoliaca) Ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak Incelenmesi”. Journal of Research in Veterinary Medicine, vol. 43, no. 1, 2024, pp. 46-54, doi:10.30782/jrvm.1420188.
Vancouver Toker MB, Aktar A, Seven-çakmak S, Çakmak İ, Akkaşoğlu M, Alçay S. Arı Sperması (Apis mellifera anatoliaca) ve İnsülin Etkileşiminin Soya Lesitini Temelli Kriyoprezervasyon Sulandırıcılarında Flow Sitometri Olarak incelenmesi. J Res Vet Med. 2024;43(1):46-54.
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