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Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract

Year 2020, Volume: 13 Issue: 1, 77 - 85, 31.03.2020
https://doi.org/10.30607/kvj.666819

Abstract

Hibernation is a survival adaptation characterized by extended fasting when food is less or unavailable. Prolonged fast may affects various proteins expression including galectins binding β-galactosyl. There is no data on the expression of Galectin-1 and -3 (Gal-1 and -3) during hibernation. This study aimed to examine the expression of Gal-1 and -3 in hibernating Anatolian ground squirrel (Spermophilus xanthoprymnus) gastrointestinal tract. Intense Gal-1 immunostaining was observed in some cells of both gastric lamina propria and villous connective tissue of the small intestine. In colon and cecum, intense Gal-1 immunoreaction was observed in some connective tissue cells around the crypt epithelium, as well as in the smooth muscles of vessel walls, lamina muscularis and tunica muscularis of all the regions. Gastric foveolar epithelium showed moderate nuclear and intracytoplasmic Gal-3 immunostaining. Moreover, Gal-3 immunostaining was detected in villous epithelial cells of the duodenum and ileum. Intense Gal-3 labeling also was present in all the cryptal surface epithelial cells of the colon and cecum. In conclusion, both Gal-1and Gal-3 expression in gastrointestinal tract during hibernation was similar to that of non-hibernating species. In the gastrointestinal tract, Gal-1 did not display different expression pattern, whereas Gal-3 expression was more intense in large intestine epithelium.

Thanks

The authors thank Prof. Emel ERGÜN and Prof. Levent ERGÜN (Ankara University) for supplying primary antibodies for Galectin-1 and -3. The authors are also grateful to Prof. Feyzullah BEYAZ (Erciyes University) for supplying paraffin tissue blocks.

References

  • Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell. 1994; 76(4): 597-598.
  • Barondes SH. Soluble lectins: a new class of extracellular proteins. Science. 1984; 223(4642): 1259-1264.
  • Brassart D, Kolodziejczyk E, Granato D, Woltz A, Pavillard M, Perotti F, Frigeri LG, Liu FT, Borel Y, Neeser JR. An intestinal galactose-specific lectin mediates the binding of murine IgE to mouse intestinal epithelial cells. Eur J Biochem. 1992; 203: 393-399.
  • Brazowski E, Dotan I, Tulchinsky H, Filip I, Eisenthal A. Galectin-3 expression in pouchitis in patients with ulcerative colitis who underwent ileal pouch-anal anastomosis (IPAA). Pathol Res Pract. 2009; 205: 551-558.
  • Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology. 2006; 16(11): 137R-157R. Carey HV, Mangino MJ, Southard JH. Changes in gut function during hibernation: implications for bowel transplantation and surgery. Gut. 2001; 49(4): 459-461.
  • Case D, Irwin D, Ivester C, Harral J, Morris K, Imamura M, Roedersheimer M, Patterson A, Carr M, Hagen M, Saavedra M, Crossno J Jr, Young KA, Dempsey EC, Poirier F, West J, Majka S. Mice deficient in galectin-1 exhibit attenuated physiological responses to chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2007; 292(1): L154-164.
  • Catt JW, Harrison FL, Carleton JS. Distribution of an endogenous beta-galactoside-specific lectin during foetal and neonatal rabbit development. J Cell Sci. 1987; 87: 623-633.
  • Cebo C, Vergoten G, Zanetta JP. Lectin activities of cytokines: functions and putative carbohydrate-recognition domains. Biochim Biophys Acta. 2002; 1572(2-3): 422-434.
  • Cooper DN, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol. 1990; 110: 1681-1691.
  • Curciarello R, Steele A, Cooper D, MacDonald TT, Kruidenier L, Kudo T. The role of Galectin-1 and Galectin-3 in the mucosal immune response to Citrobacter rodentium infection. PLoS One. 2014; 9(9): e107933.
  • Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R. Requirement for galectin-3 in apical protein sorting. Curr Biol. 2006; 16(4): 408-414.
  • Delacour D, Koch A, Ackermann W, Eude-Le Parco I, Elsässer HP, Poirier F, Jacob R. Loss of galectin-3 impairs membrane polarisation of mouse enterocytes in vivo. J Cell Sci. 2008; 121: 458-465.
  • Demetter P, Nagy N, Martin B, Mathieu A, Dumont P, Decaestecker C, Salmon IJ. The galectin family and digestive disease. Pathol. 2008; 215(1): 1-12. Goletz S, Hanisch FG, Karsten U. Novel alphaGalNAc containing glycans on cytokeratins are recognized invitro by galectins with type II carbohydrate recognition domains. J Cell Sci. 1997; 110: 1585-1596.
  • Gordon-Alonso M, Bruger AM, Bruggen P. Extracellular galectins as controllers of cytokines in hematological cancer. Blood. 2018; 132(5): 484-491. Green C. Mammalian hibernation: lessons for organ preparation? Cryo Letters. 2000; 21(2): 91-98.
  • Hokama A, Mizoguchi E, Mizoguchi A. Roles of galectins in inflammatory bowel disease. World J Gastroenterol. 2008; 14: 5133-5137. Houzelstein D, Gonçalves IR, Fadden AJ, Sidhu SS, Cooper DN, Drickamer K, Leffler H, Poirier F. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol. 2004; 21(7): 1177-1187.
  • Huflejt ME, Jordan ET, Gitt MA, Barondes SH, Leffler H. Strikingly different localization of galectin-3 and galectin-4 in human colon adenocarcinoma T84 cells. Galectin-4 is localized at sites of cell adhesion. J Biol Chem. 1997; 272: 14294-14303.
  • Kaltner H, Seyrek K, Heck A, Sinowatz F, Gabius HJ. Galectin-1 and galectin-3 in fetal development of bovine respiratory and digestive tracts. Comparison of cell type-specific expression profiles and subcellular localization. Cell Tissue Res. 2002; 307(1): 35-46.
  • Kurtz CC, Carey HV. Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol. 2007; 31: 415-428.
  • Lindstedt R, Apodaca G, Barondes SH, Mostov KE, Leffler H. Apical secretion of a cytosolic protein by Madin-Darby canine kidney cells. Evidence for polarized release of an endogenous lectin by a nonclassical secretory pathway. J Biol Chem. 1993; 268(16): 11750-11757.
  • Liu FT, Patterson RJ, Wang JL. Intracellular functions of galectins. Biochim Biophys Acta 2002; 1572: 263-273.
  • Lotz MM, Andrews CW Jr, Korzelius CA, Lee EC, Steele GD Jr, Clarke A, Mercurio AM. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma. Proc Natl Acad Sci U S A. 1993; 90: 3466-3470.
  • Mizoguchi E, Mizoguchi A. Is the sugar always sweet in intestinal inflammation? Immunol Res. 2007; 37: 47-60.
  • Moiseeva EP, Javed Q, Spring EL, de Bono DP. Galectin 1 is involved in vascular smooth muscle cell proliferation. Cardiovasc Res. 2000; 45(2): 493-502.
  • Moiseeva EP, Spring EL, Baron JH, de Bono DP. Galectin 1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J Vasc Res. 1999; 36(1): 47-58.
  • Müller S, Schaffer T, Flogerzi B, Fleetwood A, Weimann R, Schoepfer AM, Seibold F. Galectin-3 modulates T cell activity and is reduced in the inflamed intestinal epithelium in IBD. Inflamm Bowel Dis. 2006; 12(7): 588-597.
  • Nio J, Kon Y, Iwanaga T. Differential cellular expression of galectin family mRNAs in the epithelial cells of the mouse digestive tract. J Histochem Cytochem. 2005; 53(11): 1323-1334.
  • Nio-Kobayashi, J. Tissue-and cell-specific localization of galectins, β-galactose-binding animal lectins, and their potential functions in health and disease. Anat Sci Int. 2017; 92(1): 25-36.
  • Ose R, Oharaa O, Nagase T. Galectin-1 and Galectin-3 mediate protocadherin-24-dependent membrane localization of β-catenin in colon cancer cell line HCT116. Curr Chem Genomics. 2012; 6: 18-26.
  • Olson ME, McCabe K. Anesthesia in the Richardson’s ground squirrel: comparison of ketamine, ketamine and xylazine, droperidol and fentanyl, and sodium pentobarbital. J Am Vet Med Assoc. 1986; 189: 1035-1037.
  • Özbek M, Hitit M, Yıldırım N, Özgenç Ö, Ergün E, Ergün L, Beyaz F, Kurtdede N, Altunay H. Expression pattern of galectin-1 and galectin-3 in rat testes and epididymis during postnatal development. Acta Histochem. 2018; 120(8): 814-827.
  • Öztop M, Özbek M, Liman N, Beyaz F, Ergün E, Ergün L. Localization profiles of natriuretic peptides in hearts of pre-hibernating and hibernating Anatolian ground squirrels (Spermophilus xanthoprymnus). Vet Res Commun. 2019; 43(2): 45-65.
  • Puthenedam M, Wu F, Shetye A, Michaels A, Rhee KJ, Kwon JH. Matrilysin-1 (MMP7) cleaves galectin-3 and inhibits wound healing in intestinal epithelial cells. Inflamm Bowel Dis. 2011; 17(1): 260-267.
  • Rubinstein N, Ilarregui JM, Toscano MA, Rabinovich GA. The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens. 2004; 64(1): 1-12.
  • Sanjuán X, Fernández PL, Castells A, Castronovo V, van den Brule F, Liu FT, Cardesa A, Campo E. Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology. 1997; 113(6): 1906-1915.
  • Santucci L, Fiorucci S, Rubinstein N, Mencarelli A, Palazzetti B, Federici B, Rabinovich GA, Morelli A. Galectin-1 suppresses experimental colitis in mice. Gastroenterology. 2003; 124: 1381-1394.
  • Sisa C, Turroni S, Amici R, Brigidi P, Candela M, Cerri M. Potential role of the gut microbiota in synthetic torpor and therapeutic hypothermia. World J Gastroenterol. 2017; 23(3): 406-413.
  • Takenaka Y, Inohara H, Yoshii T, Oshima K, Nakahara S, Akahani S, Honjo Y, Yamamoto Y, Raz A, Kubo T. Malignant transformation of thyroid follicular cells by galectin -3. Cancer Lett. 2003; 195(1): 111-119.
  • Wang J, Thio SS, Yang SS, Yu D, Yu CY, Wong YP, Liao P, Li S, Soong TW. Splice variant specific modulation of CaV1.2 calcium channel by galectin-1 regulates arterial constriction. Circ Res. 2011; 109(11): 1250-1258.
  • Wasano K, Hirakawa Y, Yamamoto T. Immunohistochemical localization of 14 kDa beta-galactoside-binding lectin in various organs of rat. Cell Tissue Res. 1990; 259(1): 43-49.
  • Woo HJ, Joo HG, Song SW, Sohn YS, Chae C. Immunohistochemical detection of galectin-3 in canine gastric carcinomas. J Comp Pathol. 2001; 124(2-3): 216-218.
  • Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci U S A. 1996; 93(13): 6737-6742.

Hibernasyondaki Anadolu Yer Sincabı (Spermophilus xanthoprymnus) Gastrointestinal Kanalında Galektin-1 ve Galektin-3'ün Ekspresyon Paternleri

Year 2020, Volume: 13 Issue: 1, 77 - 85, 31.03.2020
https://doi.org/10.30607/kvj.666819

Abstract

Hibernasyon, besinin az olduğu veya hiç olmadığı uzun süreli açlık ile karakterize olan durumlarda hayatta kalma adaptasyonudur. Uzun süreli açlık β-galaktozil bağlayan galektinler de dahil olmak üzere bir çok proteinin ekspresyonunu etkileyebilir. Galektinler, β-galaktozil bağlayan proteinlerdir. Hibernasyonda Galektin-1 ve -3 (Gal-1 ve-3)’ün ekspresyonuna ilişkin herhangi bir veri bulunmamaktadır. Bu çalışmada hibernasyondaki Anadolu yer sincabı (Spermophilus xanthoprymnus) gastrointestinal kanalında Gal-1 ve 3’ün ekspresyonunun incelenmesi amaçlanmıştır. Hem gastrik lamina propria hem de ince bağırsağın villöz bağ dokusundaki bazı hücrelerde yoğun Gal-1 immün boyanması gözlendi. Gastrointestinal kanalın bütün bölümlerindeki damar duvarları, lamina muskularis ve tunika muskularisindeki düz kaslarda yoğun Gal-1 ekspresyonu gözlendi. Ayrıca kolon ve sekumda kript epiteli etrafındaki bazı bağ dokusu hücrelerinde de yoğun Gal-1 immünoreaksiyonu belirlendi. Gastrik foveoler epitel hücreleri orta derecede nükleer ve intrasitoplazmik Gal-3 immun reaksiyon gösterdi. Duodenum ve ileumun villöz epitel hücrelerinde Gal-3 immün boyaması tespit edildi. Ayrıca, kolon ve sekumdaki kriptlerin yüzey epitel hücrelerinde yoğun Gal-3 boyanması görüldü. Sonuç olarak hibernasyon sürecinde gastrointestinal kanaldaki hem Gal-1 hem de Gal-3 ekspresyonu hibernasyona yatmayan türlerle benzerdi. Gastrointestinal kanal bölümlerinde Gal-1 ekspresyonu açısından farklılık gözlenmezken, Gal-3 ekspresyonu diğer gastrointestinal bölümlere nazaran kalın bağısak epitelinde daha yoğundu.

References

  • Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell. 1994; 76(4): 597-598.
  • Barondes SH. Soluble lectins: a new class of extracellular proteins. Science. 1984; 223(4642): 1259-1264.
  • Brassart D, Kolodziejczyk E, Granato D, Woltz A, Pavillard M, Perotti F, Frigeri LG, Liu FT, Borel Y, Neeser JR. An intestinal galactose-specific lectin mediates the binding of murine IgE to mouse intestinal epithelial cells. Eur J Biochem. 1992; 203: 393-399.
  • Brazowski E, Dotan I, Tulchinsky H, Filip I, Eisenthal A. Galectin-3 expression in pouchitis in patients with ulcerative colitis who underwent ileal pouch-anal anastomosis (IPAA). Pathol Res Pract. 2009; 205: 551-558.
  • Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology. 2006; 16(11): 137R-157R. Carey HV, Mangino MJ, Southard JH. Changes in gut function during hibernation: implications for bowel transplantation and surgery. Gut. 2001; 49(4): 459-461.
  • Case D, Irwin D, Ivester C, Harral J, Morris K, Imamura M, Roedersheimer M, Patterson A, Carr M, Hagen M, Saavedra M, Crossno J Jr, Young KA, Dempsey EC, Poirier F, West J, Majka S. Mice deficient in galectin-1 exhibit attenuated physiological responses to chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2007; 292(1): L154-164.
  • Catt JW, Harrison FL, Carleton JS. Distribution of an endogenous beta-galactoside-specific lectin during foetal and neonatal rabbit development. J Cell Sci. 1987; 87: 623-633.
  • Cebo C, Vergoten G, Zanetta JP. Lectin activities of cytokines: functions and putative carbohydrate-recognition domains. Biochim Biophys Acta. 2002; 1572(2-3): 422-434.
  • Cooper DN, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol. 1990; 110: 1681-1691.
  • Curciarello R, Steele A, Cooper D, MacDonald TT, Kruidenier L, Kudo T. The role of Galectin-1 and Galectin-3 in the mucosal immune response to Citrobacter rodentium infection. PLoS One. 2014; 9(9): e107933.
  • Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R. Requirement for galectin-3 in apical protein sorting. Curr Biol. 2006; 16(4): 408-414.
  • Delacour D, Koch A, Ackermann W, Eude-Le Parco I, Elsässer HP, Poirier F, Jacob R. Loss of galectin-3 impairs membrane polarisation of mouse enterocytes in vivo. J Cell Sci. 2008; 121: 458-465.
  • Demetter P, Nagy N, Martin B, Mathieu A, Dumont P, Decaestecker C, Salmon IJ. The galectin family and digestive disease. Pathol. 2008; 215(1): 1-12. Goletz S, Hanisch FG, Karsten U. Novel alphaGalNAc containing glycans on cytokeratins are recognized invitro by galectins with type II carbohydrate recognition domains. J Cell Sci. 1997; 110: 1585-1596.
  • Gordon-Alonso M, Bruger AM, Bruggen P. Extracellular galectins as controllers of cytokines in hematological cancer. Blood. 2018; 132(5): 484-491. Green C. Mammalian hibernation: lessons for organ preparation? Cryo Letters. 2000; 21(2): 91-98.
  • Hokama A, Mizoguchi E, Mizoguchi A. Roles of galectins in inflammatory bowel disease. World J Gastroenterol. 2008; 14: 5133-5137. Houzelstein D, Gonçalves IR, Fadden AJ, Sidhu SS, Cooper DN, Drickamer K, Leffler H, Poirier F. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol. 2004; 21(7): 1177-1187.
  • Huflejt ME, Jordan ET, Gitt MA, Barondes SH, Leffler H. Strikingly different localization of galectin-3 and galectin-4 in human colon adenocarcinoma T84 cells. Galectin-4 is localized at sites of cell adhesion. J Biol Chem. 1997; 272: 14294-14303.
  • Kaltner H, Seyrek K, Heck A, Sinowatz F, Gabius HJ. Galectin-1 and galectin-3 in fetal development of bovine respiratory and digestive tracts. Comparison of cell type-specific expression profiles and subcellular localization. Cell Tissue Res. 2002; 307(1): 35-46.
  • Kurtz CC, Carey HV. Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol. 2007; 31: 415-428.
  • Lindstedt R, Apodaca G, Barondes SH, Mostov KE, Leffler H. Apical secretion of a cytosolic protein by Madin-Darby canine kidney cells. Evidence for polarized release of an endogenous lectin by a nonclassical secretory pathway. J Biol Chem. 1993; 268(16): 11750-11757.
  • Liu FT, Patterson RJ, Wang JL. Intracellular functions of galectins. Biochim Biophys Acta 2002; 1572: 263-273.
  • Lotz MM, Andrews CW Jr, Korzelius CA, Lee EC, Steele GD Jr, Clarke A, Mercurio AM. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma. Proc Natl Acad Sci U S A. 1993; 90: 3466-3470.
  • Mizoguchi E, Mizoguchi A. Is the sugar always sweet in intestinal inflammation? Immunol Res. 2007; 37: 47-60.
  • Moiseeva EP, Javed Q, Spring EL, de Bono DP. Galectin 1 is involved in vascular smooth muscle cell proliferation. Cardiovasc Res. 2000; 45(2): 493-502.
  • Moiseeva EP, Spring EL, Baron JH, de Bono DP. Galectin 1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J Vasc Res. 1999; 36(1): 47-58.
  • Müller S, Schaffer T, Flogerzi B, Fleetwood A, Weimann R, Schoepfer AM, Seibold F. Galectin-3 modulates T cell activity and is reduced in the inflamed intestinal epithelium in IBD. Inflamm Bowel Dis. 2006; 12(7): 588-597.
  • Nio J, Kon Y, Iwanaga T. Differential cellular expression of galectin family mRNAs in the epithelial cells of the mouse digestive tract. J Histochem Cytochem. 2005; 53(11): 1323-1334.
  • Nio-Kobayashi, J. Tissue-and cell-specific localization of galectins, β-galactose-binding animal lectins, and their potential functions in health and disease. Anat Sci Int. 2017; 92(1): 25-36.
  • Ose R, Oharaa O, Nagase T. Galectin-1 and Galectin-3 mediate protocadherin-24-dependent membrane localization of β-catenin in colon cancer cell line HCT116. Curr Chem Genomics. 2012; 6: 18-26.
  • Olson ME, McCabe K. Anesthesia in the Richardson’s ground squirrel: comparison of ketamine, ketamine and xylazine, droperidol and fentanyl, and sodium pentobarbital. J Am Vet Med Assoc. 1986; 189: 1035-1037.
  • Özbek M, Hitit M, Yıldırım N, Özgenç Ö, Ergün E, Ergün L, Beyaz F, Kurtdede N, Altunay H. Expression pattern of galectin-1 and galectin-3 in rat testes and epididymis during postnatal development. Acta Histochem. 2018; 120(8): 814-827.
  • Öztop M, Özbek M, Liman N, Beyaz F, Ergün E, Ergün L. Localization profiles of natriuretic peptides in hearts of pre-hibernating and hibernating Anatolian ground squirrels (Spermophilus xanthoprymnus). Vet Res Commun. 2019; 43(2): 45-65.
  • Puthenedam M, Wu F, Shetye A, Michaels A, Rhee KJ, Kwon JH. Matrilysin-1 (MMP7) cleaves galectin-3 and inhibits wound healing in intestinal epithelial cells. Inflamm Bowel Dis. 2011; 17(1): 260-267.
  • Rubinstein N, Ilarregui JM, Toscano MA, Rabinovich GA. The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens. 2004; 64(1): 1-12.
  • Sanjuán X, Fernández PL, Castells A, Castronovo V, van den Brule F, Liu FT, Cardesa A, Campo E. Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology. 1997; 113(6): 1906-1915.
  • Santucci L, Fiorucci S, Rubinstein N, Mencarelli A, Palazzetti B, Federici B, Rabinovich GA, Morelli A. Galectin-1 suppresses experimental colitis in mice. Gastroenterology. 2003; 124: 1381-1394.
  • Sisa C, Turroni S, Amici R, Brigidi P, Candela M, Cerri M. Potential role of the gut microbiota in synthetic torpor and therapeutic hypothermia. World J Gastroenterol. 2017; 23(3): 406-413.
  • Takenaka Y, Inohara H, Yoshii T, Oshima K, Nakahara S, Akahani S, Honjo Y, Yamamoto Y, Raz A, Kubo T. Malignant transformation of thyroid follicular cells by galectin -3. Cancer Lett. 2003; 195(1): 111-119.
  • Wang J, Thio SS, Yang SS, Yu D, Yu CY, Wong YP, Liao P, Li S, Soong TW. Splice variant specific modulation of CaV1.2 calcium channel by galectin-1 regulates arterial constriction. Circ Res. 2011; 109(11): 1250-1258.
  • Wasano K, Hirakawa Y, Yamamoto T. Immunohistochemical localization of 14 kDa beta-galactoside-binding lectin in various organs of rat. Cell Tissue Res. 1990; 259(1): 43-49.
  • Woo HJ, Joo HG, Song SW, Sohn YS, Chae C. Immunohistochemical detection of galectin-3 in canine gastric carcinomas. J Comp Pathol. 2001; 124(2-3): 216-218.
  • Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci U S A. 1996; 93(13): 6737-6742.
There are 41 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section RESEARCH ARTICLE
Authors

Mehmet Özbek 0000-0002-2274-5359

Mustafa Öztop 0000-0002-2923-9280

Publication Date March 31, 2020
Acceptance Date February 17, 2020
Published in Issue Year 2020 Volume: 13 Issue: 1

Cite

APA Özbek, M., & Öztop, M. (2020). Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract. Kocatepe Veterinary Journal, 13(1), 77-85. https://doi.org/10.30607/kvj.666819
AMA Özbek M, Öztop M. Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract. kvj. March 2020;13(1):77-85. doi:10.30607/kvj.666819
Chicago Özbek, Mehmet, and Mustafa Öztop. “Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract”. Kocatepe Veterinary Journal 13, no. 1 (March 2020): 77-85. https://doi.org/10.30607/kvj.666819.
EndNote Özbek M, Öztop M (March 1, 2020) Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract. Kocatepe Veterinary Journal 13 1 77–85.
IEEE M. Özbek and M. Öztop, “Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract”, kvj, vol. 13, no. 1, pp. 77–85, 2020, doi: 10.30607/kvj.666819.
ISNAD Özbek, Mehmet - Öztop, Mustafa. “Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract”. Kocatepe Veterinary Journal 13/1 (March 2020), 77-85. https://doi.org/10.30607/kvj.666819.
JAMA Özbek M, Öztop M. Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract. kvj. 2020;13:77–85.
MLA Özbek, Mehmet and Mustafa Öztop. “Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract”. Kocatepe Veterinary Journal, vol. 13, no. 1, 2020, pp. 77-85, doi:10.30607/kvj.666819.
Vancouver Özbek M, Öztop M. Expression Patterns of Galectin-1 and Galectin-3 in Hibernating Anatolian Ground Squirrel (Spermophilus Xanthoprymnus) Gastrointestinal Tract. kvj. 2020;13(1):77-85.

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