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Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation

Year 2024, Volume: 17 Issue: 2, 198 - 203, 31.12.2024
https://doi.org/10.47027/duvetfd.1587520

Abstract

This study aims to investigate the expression patterns of Galectin-1 (Gal-1) and Gal-3 in the testis and epididymis of Anatolian ground squirrel (Spermophilus xanthoprymnus) during nonbreeding pre-hibernation and hibernation periods. Hibernation is a physiological state characterized by a reduction in metabolic rate and body temperature. Gal-1 and -3 are implicated in many biological functions. Twelve squirrels were used in this study. Followed by routine tissue processing, tissue samples underwent immunohistochemical procedure. Histological examination and statistical analysis were performed. Immunohistochemical investigation revealed that Gal-1 expression during pre-hibernation was confined to peritubular myoid cells and vascular smooth muscle cells, with no expression observed in Sertoli or spermatogenic cells. Gal-1 in the epididymis was localized to smooth muscle cells encircling the epithelium and within blood vessel walls, exhibiting markedly elevated expression across the caput, corpus, and cauda regions. During hibernation, testicular and epidydimal Gal-1 expression exhibited a considerable reduction. During pre-hibernation, Gal-3 exhibited a unique pattern, with expression noted in the seminiferous epithelium and Leydig cells. Gal-3 was detected in the epithelial cells throughout the epididymis, with greater intensity in specific epithelial cells. During hibernation, Gal-3 expression increased in Sertoli cells, spermatogonia, and spermatocytes within the testis, while exhibiting diminished intensity in the epididymal epithelium across all regions. The findings suggest that Gal-1 and -3 may be involved in seasonal reproductive adaptability during nonbreeding pre-hibernation and hibernation. Further research could clarify their specific molecular functions in hibernating species.

Ethical Statement

All animal experiments in this study were performed in accordance with the ethical guidelines established by the Erciyes University Animal Experiments Local Ethics Committee. Approval for the procedures was granted under the ethical approval number 15/140, Kayseri.

Thanks

We sincerely thank Prof. Dr. Feyzullah Beyaz for generously providing the testis and epididymis tissues of the Anatolian ground squirrel, as well as Prof. Dr. Emel Ergun for kindly supplying the primary antibodies used in this research. Part of this study was presented at the "2nd International Health Science and Life Congress (IHSLC 2019), held on April 24-27, 2019, in Burdur, Turkey."

References

  • Ruf T, Geiser F (2014). Daily torpor and hibernation in birds and mammals. Biol Rev Camb Philos Soc., 90(3): 891.
  • Jiménez R, Burgos M, Barrionuevo FJ (2015). Circannual testis changes in seasonally breeding mammals. Sex Dev., 9(4): 205-215.
  • Klonisch T, Schön J, Hombach-Klonisch S, Blottner S et al. (2006). The roe deer as a model for studying seasonal regulation of testis function. Int J Androl., 29(1): 122-128.
  • Young KA, Nelson RJ (2001). Mediation of seasonal testicular regression by apoptosis. Reproduction, 122(5): 677-685.
  • Johannes L, Jacob R, Leffler H (2018). Galectins at a glance. J Cell Sci., 131(9).
  • Barondes SH, Castronovo V, Cooper DNW, Cummings RD et al. (1994). Galectins: A family of animal beta-galactoside-binding lectins. Cell, 76(4): 597-598.
  • Liu FT, Rabinovich GA (2005). Galectins as modulators of tumour progression. Nat Rev Cancer, 5(1): 29-41.
  • Yang RY, Rabinovich GA, Liu FT (2008). Galectins: structure, function and therapeutic potential. Expert Rev Mol Med., 10(17).
  • Özbek M, Hitit M, Yıldırım N, Özgenç Ö et al. (2018). Expression pattern of galectin-1 and galectin-3 in rat testes and epididymis during postnatal development. Acta Histochem., 120(8): 814-827.
  • Dettin L, Rubinstein N, Aoki A, Rabinovich GA et al. (2003). Regulated expression and ultrastructural localization of galectin-1, a proapoptotic beta-galactoside-binding lectin, during spermatogenesis in rat testis. Biol Reprod., 68(1): 51-59.
  • Wollina U, Schreiber G, Gornig M, Feldrappe S et al. (1999). Sertoli cell expression of galectin-1 and -3 and accessible binding sites in normal human testis and Sertoli cell-only syndrome. Histol Histopathol., 14: 779-784.
  • Chui K, Trivedi A, Cheng CY, Cherbavaz DB et al. (2011). Characterization and functionality of proliferative human Sertoli cells. Cell Transplant., 20(5): 619-635.
  • Akahani S, Nangia-Makker P, Inohara H, Kim H-RC et al. (1997). Galectin-3: A novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res., 57(23): 5272-5276.
  • Gür H, Gür MK (2005). Annual cycle of activity, reproduction, and body mass of Anatolian ground squirrels (Spermophilus xanthoprymnus) in Turkey. J Mammal., 86(1): 7-14.
  • Kart Gür M, Gür H (2015). Age and sex differences in hibernation patterns in free-living Anatolian ground squirrels. Mamm Biol., 80(4): 265-272.
  • Kart Gür M, Refinetti R, Gür H (2009). Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions. J Comp Physiol B., 179(2): 155-164.
  • Jensen EC (2013). Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec (Hoboken)., 296(3): 378-381.
  • Khorsandi L, Orazizadeh M (2011). Immunolocalization of Galectin-3 in mouse testicular tissue. Iran J Basic Med Sci., 14(4): 349.
  • Deschildre C, Ji JW, Chater S, Dacheux F et al. (2007). Expression of galectin-3 and its regulation in the testes. Int J Androl., 30(1): 28-40.
  • Coppin L, Jannin A, Ait Yahya E, Thuillier C et al. (2020). Galectin-3 modulates epithelial cell adaptation to stress at the ER-mitochondria interface. Cell Death Dis., 11(5).
  • Nio J, Kon Y, Iwanaga T (2005). Differential cellular expression of galectin family mRNAs in the epithelial cells of the mouse digestive tract. J Histochem Cytochem., 53(11): 1323-1334.
  • Koch A, Poirier F, Jacob R, Delacour D (2010). Galectin-3, a novel centrosome-associated protein, required for epithelial morphogenesis. Mol Biol Cell., 21(2): 219-231.
  • Kim H, Ahn M, Moon C, Kim S et al. (2008). Immunohistochemical study of galectin-3 in mature and immature bull testis and epididymis. J Vet Sci., 9(4): 339-344.

Üreme Dışı Aktif ve Hibernasyon Dönemlerinde Anadolu Yer Sincabı (Spermophilus xanthoprymnus) Testis ve Epididimisinde Galektin-1 ve -3 Ekspresyonu

Year 2024, Volume: 17 Issue: 2, 198 - 203, 31.12.2024
https://doi.org/10.47027/duvetfd.1587520

Abstract

Bu çalışma, üreme dışı aktif ve hibernasyon dönemlerinde Anadolu yer sincabı (Spermophilus xanthoprymnus) testis ve epididimisinde Galectin-1 (Gal-1) ve Gal-3 ekspresyonunu araştırmayı amaçlamaktadır. Hibernasyon, metabolik hız ve vücut sıcaklığındaki azalma ile karakterize fizyolojik bir durumdur. Gal-1 ve Gal-3 birçok biyolojik fonksiyonda rol oynamaktadır. Bu çalışmada on iki sincap kullanılmıştır. Rutin doku işleme tabi tutulduktan sonra, doku örnekleri immünohistokimyasal prosedüre tabi tutuldu. İnceleme ve istatistiksel analiz yapıldı. İmmünohistokimyasal inceleme, aktif dönemde Gal-1 ekspresyonunun peritübüler miyoid hücreler ve vasküler düz kas hücreleriyle sınırlı olduğunu, Sertoli veya spermatogenik hücrelerde ekspresyon gözlemlenmediğini ortaya koymuştur. Epididimisde Gal-1, epiteli çevreleyen düz kas hücrelerinde ve kan damarı duvarlarında lokalize olmuş, kaput, korpus ve kauda bölgelerinde belirgin şekilde yüksek ekspresyon sergilemiştir. Kış uykusu sırasında testis ve epididimal Gal-1 ekspresyonunda önemli bir azalma gözlenmiştir. Aktif dönemde Gal-3 kendine has bir ekspresyon göstermiş olup seminifer epitel ve Leydig hücrelerinde gözlemlenmiştir. Gal-3, epididimis boyunca epitel hücrelerinde tespit edilmiş, belirli epitel hücrelerinde daha yoğun olarak bulunmuştur. Kış uykusu sırasında Gal-3 ekspresyonu testisteki Sertoli hücrelerinde, spermatogonyumlarda ve spermatositlerde artarken, tüm bölgelerde epididimal epitelde yoğunluk azalmıştır. Bulgular, Gal-1 ve Gal-3’ün üreme dışı ön kış uykusu ve kış uykusu sırasında mevsimsel üreme adaptasyonunda rol oynayabileceğini göstermektedir. Kış uykusuna yatan türlerde spesifik moleküler işlevlerini açıklığa kavuşturmak için daha fazla çalışmaya ihtiyaç duyulmaktadır.

References

  • Ruf T, Geiser F (2014). Daily torpor and hibernation in birds and mammals. Biol Rev Camb Philos Soc., 90(3): 891.
  • Jiménez R, Burgos M, Barrionuevo FJ (2015). Circannual testis changes in seasonally breeding mammals. Sex Dev., 9(4): 205-215.
  • Klonisch T, Schön J, Hombach-Klonisch S, Blottner S et al. (2006). The roe deer as a model for studying seasonal regulation of testis function. Int J Androl., 29(1): 122-128.
  • Young KA, Nelson RJ (2001). Mediation of seasonal testicular regression by apoptosis. Reproduction, 122(5): 677-685.
  • Johannes L, Jacob R, Leffler H (2018). Galectins at a glance. J Cell Sci., 131(9).
  • Barondes SH, Castronovo V, Cooper DNW, Cummings RD et al. (1994). Galectins: A family of animal beta-galactoside-binding lectins. Cell, 76(4): 597-598.
  • Liu FT, Rabinovich GA (2005). Galectins as modulators of tumour progression. Nat Rev Cancer, 5(1): 29-41.
  • Yang RY, Rabinovich GA, Liu FT (2008). Galectins: structure, function and therapeutic potential. Expert Rev Mol Med., 10(17).
  • Özbek M, Hitit M, Yıldırım N, Özgenç Ö et al. (2018). Expression pattern of galectin-1 and galectin-3 in rat testes and epididymis during postnatal development. Acta Histochem., 120(8): 814-827.
  • Dettin L, Rubinstein N, Aoki A, Rabinovich GA et al. (2003). Regulated expression and ultrastructural localization of galectin-1, a proapoptotic beta-galactoside-binding lectin, during spermatogenesis in rat testis. Biol Reprod., 68(1): 51-59.
  • Wollina U, Schreiber G, Gornig M, Feldrappe S et al. (1999). Sertoli cell expression of galectin-1 and -3 and accessible binding sites in normal human testis and Sertoli cell-only syndrome. Histol Histopathol., 14: 779-784.
  • Chui K, Trivedi A, Cheng CY, Cherbavaz DB et al. (2011). Characterization and functionality of proliferative human Sertoli cells. Cell Transplant., 20(5): 619-635.
  • Akahani S, Nangia-Makker P, Inohara H, Kim H-RC et al. (1997). Galectin-3: A novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res., 57(23): 5272-5276.
  • Gür H, Gür MK (2005). Annual cycle of activity, reproduction, and body mass of Anatolian ground squirrels (Spermophilus xanthoprymnus) in Turkey. J Mammal., 86(1): 7-14.
  • Kart Gür M, Gür H (2015). Age and sex differences in hibernation patterns in free-living Anatolian ground squirrels. Mamm Biol., 80(4): 265-272.
  • Kart Gür M, Refinetti R, Gür H (2009). Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions. J Comp Physiol B., 179(2): 155-164.
  • Jensen EC (2013). Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec (Hoboken)., 296(3): 378-381.
  • Khorsandi L, Orazizadeh M (2011). Immunolocalization of Galectin-3 in mouse testicular tissue. Iran J Basic Med Sci., 14(4): 349.
  • Deschildre C, Ji JW, Chater S, Dacheux F et al. (2007). Expression of galectin-3 and its regulation in the testes. Int J Androl., 30(1): 28-40.
  • Coppin L, Jannin A, Ait Yahya E, Thuillier C et al. (2020). Galectin-3 modulates epithelial cell adaptation to stress at the ER-mitochondria interface. Cell Death Dis., 11(5).
  • Nio J, Kon Y, Iwanaga T (2005). Differential cellular expression of galectin family mRNAs in the epithelial cells of the mouse digestive tract. J Histochem Cytochem., 53(11): 1323-1334.
  • Koch A, Poirier F, Jacob R, Delacour D (2010). Galectin-3, a novel centrosome-associated protein, required for epithelial morphogenesis. Mol Biol Cell., 21(2): 219-231.
  • Kim H, Ahn M, Moon C, Kim S et al. (2008). Immunohistochemical study of galectin-3 in mature and immature bull testis and epididymis. J Vet Sci., 9(4): 339-344.
There are 23 citations in total.

Details

Primary Language English
Subjects Veterinary Histology and Embryology
Journal Section Research
Authors

Mehmet Özbek 0000-0002-2274-5359

Mustafa Öztop 0000-0002-2923-9280

Publication Date December 31, 2024
Submission Date November 18, 2024
Acceptance Date December 13, 2024
Published in Issue Year 2024 Volume: 17 Issue: 2

Cite

APA Özbek, M., & Öztop, M. (2024). Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation. Dicle Üniversitesi Veteriner Fakültesi Dergisi, 17(2), 198-203. https://doi.org/10.47027/duvetfd.1587520
AMA Özbek M, Öztop M. Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation. Dicle Üniv Vet Fak Derg. December 2024;17(2):198-203. doi:10.47027/duvetfd.1587520
Chicago Özbek, Mehmet, and Mustafa Öztop. “Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus Xanthoprymnus) During Non-Breeding Periods of Pre-Hibernation and Hibernation”. Dicle Üniversitesi Veteriner Fakültesi Dergisi 17, no. 2 (December 2024): 198-203. https://doi.org/10.47027/duvetfd.1587520.
EndNote Özbek M, Öztop M (December 1, 2024) Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation. Dicle Üniversitesi Veteriner Fakültesi Dergisi 17 2 198–203.
IEEE M. Özbek and M. Öztop, “Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation”, Dicle Üniv Vet Fak Derg, vol. 17, no. 2, pp. 198–203, 2024, doi: 10.47027/duvetfd.1587520.
ISNAD Özbek, Mehmet - Öztop, Mustafa. “Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus Xanthoprymnus) During Non-Breeding Periods of Pre-Hibernation and Hibernation”. Dicle Üniversitesi Veteriner Fakültesi Dergisi 17/2 (December 2024), 198-203. https://doi.org/10.47027/duvetfd.1587520.
JAMA Özbek M, Öztop M. Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation. Dicle Üniv Vet Fak Derg. 2024;17:198–203.
MLA Özbek, Mehmet and Mustafa Öztop. “Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus Xanthoprymnus) During Non-Breeding Periods of Pre-Hibernation and Hibernation”. Dicle Üniversitesi Veteriner Fakültesi Dergisi, vol. 17, no. 2, 2024, pp. 198-03, doi:10.47027/duvetfd.1587520.
Vancouver Özbek M, Öztop M. Galectin-1 and -3 Expression in the Testis and Epididymis of Anatolian Ground Squirrels (Spermophilus xanthoprymnus) during Non-Breeding Periods of Pre-Hibernation and Hibernation. Dicle Üniv Vet Fak Derg. 2024;17(2):198-203.