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[1]T. C. Sudhof: A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat Med 19(10), 1227-1231 (2013)
[2]C. Czibener, N. M. Sherer, S. M. Becker, M. Pypaert, E. Hui, E. R. Chapman, W. Mothes, N. W. Andrews: Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J Cell Biol 174(7), 997-1007 (2006)
[3]Z. T. Hu, M. R. Chen, Z. Ping, Y. M. Dong, R. Y. Zhang, T. Xu, Z. X. Wu: Synaptotagmin IV regulates dense core vesicle (DCV) release in LbetaT2 cells. Biochem Biophys Res Commun 371(4), 781-786 (2008)
[4]H. Zhao, Y. Ito, J. Chappel, N. W. Andrews, S. L. Teitelbaum, F. P. Ross: Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev Cell 14(6), 914-925 (2008)
[5]C. W. Davis, B. F. Dickey: Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70, 487-512 (2008)
[6]Y. Li, P. Wang, J. Xu, F. Gorelick, H. Yamazaki, N. Andrews, G. V. Desir: Regulation of insulin secretion and GLUT4 trafficking by the calcium sensor synaptotagmin VII. Biochem Biophys Res Commun 362(3), 658-664 (2007)
[7]W. D. Matthew, L. Tsavaler, L. F. Reichardt: Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol 91(1), 257-269 (1981)
[8]Y. Hu, J. E. Ippolito, E. M. Garabedian, P. A. Humphrey, J. I. Gordon: Molecular characterization of a metastatic neuroendocrine cell cancer arising in the prostates of transgenic mice. J Biol Chem 277(46), 44462-44474 (2002)
[9]W. C. Tucker, E. R. Chapman: Role of synaptotagmin in Ca2+-triggered exocytosis. Biochem J 366(Pt 1), 1-13 (2002)
[10]J. Z. Zhang, B. A. Davletov, T. C. Sudhof, R. G. Anderson: Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78(5), 751-760 (1994)
[11]N. Jarousse, R. B. Kelly: The AP2 binding site of synaptotagmin 1 is not an internalization signal but a regulator of endocytosis. J Cell Biol 154(4), 857-866 (2001)
[12]V. Kiessling, S. Ahmed, M. K. Domanska, M. G. Holt, R. Jahn, L. K. Tamm: Rapid fusion of synaptic vesicles with reconstituted target SNARE membranes. Biophys J 104(9), 1950-1958 (2013)
[13]M. W. Musch, D. L. Arvans, M. M. Walsh-Reitz, K. Uchiyama, M. Fukuda, E. B. Chang: Synaptotagmin I binds intestinal epithelial NHE3 and mediates cAMP-and Ca2+-induced endocytosis by recruitment of AP2 and clathrin. Am J Physiol Gastrointest Liver Physiol 292(6), G1549-G1558 (2007)
[14]M. W. Musch, D. L. Arvans, Y. Wang, Y. Nakagawa, E. Solomaha, E. B. Chang: Cyclic AMP-mediated endocytosis of intestinal epithelial NHE3 requires binding to synaptotagmin 1. Am J Physiol Gastrointest Liver Physiol 298(2), G203-G211 (2010)
[15]E. Selga, F. J. Perez-Cano, A. Franch, C. Ramirez-Santana, M. Rivero, C. J. Ciudad, C. Castellote, V. Noe: Gene expression profiles in rat mesenteric lymph nodes upon supplementation with conjugated linoleic acid during gestation and suckling. BMC Genomics 12, 182 (2011)
[16]S. W. Messenger, D. D. Thomas, M. A. Falkowski, J. A. Byrne, F. S. Gorelick, G. E. Groblewski: Tumor protein D52 controls trafficking of an apical endolysosomal secretory pathway in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 305(6), G439-G452 (2013)
[17]G. Jacobsson, A. J. Bean, R. H. Scheller, L. Juntti-Berggren, J. T. Deeney, P. O. Berggren, B. Meister: Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Sci U S A 91(26), 12487-12491 (1994)
[18]J. Lang, M. Fukuda, H. Zhang, K. Mikoshiba, C. B. Wollheim: The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic beta-cells: action of synaptotagmin at low micromolar calcium. EMBO J 16(19), 5837-5846 (1997)
[19]N. Nakajima-Nagata, M. Sugai, T. Sakurai, J. Miyazaki, Y. Tabata, A. Shimizu: Pdx-1 enables insulin secretion by regulating synaptotagmin 1 gene expression. Biochem Biophys Res Commun 318(3), 631-635 (2004)
[20]M. P. Rastaldi, S. Armelloni, S. Berra, N. Calvaresi, A. Corbelli, L. A. Giardino, M. Li, G. Q. Wang, A. Fornasieri, A. Villa, E. Heikkila, R. Soliymani, A. Boucherot, C. D. Cohen, M. Kretzler, A. Nitsche, M. Ripamonti, A. Malgaroli, M. Pesaresi, G. L. Forloni, D. Schlondorff, H. Holthofer, G. D’Amico: Glomerular podocytes contain neuron-like functional synaptic vesicles. Faseb J 20(7), 976-978 (2006)
[21]C. Pattaro, A. De Grandi, V. Vitart, C. Hayward, A. Franke, Y. S. Aulchenko, A. Johansson, S. H. Wild, S. A. Melville, A. Isaacs, O. Polasek, D. Ellinghaus, I. Kolcic, U. Nothlings, L. Zgaga, T. Zemunik, C. Gnewuch, S. Schreiber, S. Campbell, N. Hastie, M. Boban, T. Meitinger, B. A. Oostra, P. Riegler, C. Minelli, A. F. Wright, H. Campbell, C. M. van Duijn, U. Gyllensten, J. F. Wilson, M. Krawczak, I. Rudan, P. P. Pramstaller: A meta-analysis of genome-wide data from five European isolates reveals an association of COL22A1, SYT1, and GABRR2 with serum creatinine level. BMC Med Genet 11, 41 (2010)
[22]N. Guillen, M. A. Navarro, C. Arnal, E. Noone, J. M. Arbones-Mainar, S. Acin, J. C. Surra, P. Muniesa, H. M. Roche, J. Osada: Microarray analysis of hepatic gene expression identifies new genes involved in steatotic liver. Physiol Genomics 37(3), 187-198 (2009)
[23]S. Sancho-Knapik, N. Guillén, J. Osada: Cloning and expression of hepatic synaptotagmin 1 in mouse. Gene 562, 236-243 (2015)
[24]S. Acin, M. A. Navarro, R. Carnicer, J. M. Arbones-Mainar, M. A. Guzman, C. Arnal, G. Beltran, M. Uceda, N. Maeda, J. Osada: Dietary cholesterol suppresses the ability of olive oil to delay the development of atherosclerotic lesions in apolipoprotein E knockout mice. Atherosclerosis 182(1), 17-28 (2005)
[25]J. M. Arbones-Mainar, M. A. Navarro, S. Acin, M. A. Guzman, C. Arnal, J. C. Surra, R. Carnicer, H. M. Roche, J. Osada: Trans-10, cis-12-and cis-9, trans-11-conjugated linoleic acid isomers selectively modify HDL-apolipoprotein composition in apolipoprotein E knockout mice. J Nutr 136(2), 353-359 (2006)
[26]C. Gabas-Rivera, R. Martinez-Beamonte, J. L. Rios, M. A. Navarro, J. C. Surra, C. Arnal, M. J. Rodriguez-Yoldi, J. Osada: Dietary oleanolic acid mediates circadian clock gene expression in liver independently of diet and animal model but requires apolipoprotein A1. J Nutr Biochem 24(12), 2100-2109 (2013)
[27]N. Guillen, S. Acin, M. A. Navarro, J. S. Perona, J. M. Arbones-Mainar, C. Arnal, A. J. Sarria, J. C. Surra, R. Carnicer, I. Orman, J. C. Segovia, V. Ruiz-Gutierrez, J. Osada: Squalene in a sex-dependent manner modulates atherosclerotic lesion which correlates with hepatic fat content in apoE-knockout male mice. Atherosclerosis 196, 558-564 (2008)
[28]R. Martinez-Beamonte, M. A. Navarro, A. Larraga, M. Strunk, C. Barranquero, S. Acin, M. A. Guzman, P. Inigo, J. Osada: Selection of reference genes for gene expression studies in rats. J Biotechnol 151(4), 325-334 (2011)
[29]J. Folch, M. Lees, G. H. Sloane Stanley: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1), 497-509 (1957)
[30]P. R. Kiela, A. J. Midura, N. Kuscuoglu, S. D. Jolad, A. M. Solyom, D. G. Besselsen, B. N. Timmermann, F. K. Ghishan: Effects of Boswellia serrata in mouse models of chemically induced colitis. Am J Physiol Gastrointest Liver Physiol 288(4), G798-G808 (2005)
[31]Y.-R. Chen, C. F. Meyer, T.-H. Tan: Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in γ radiation-induced apoptosis. J Biol Chem 271(2), 631-634 (1996)
[32]C. Brenner, L. Galluzzi, O. Kepp, G. Kroemer: Decoding cell death signals in liver inflammation. J Hepatol 59(3), 583-594 (2013)
[33]J. Xu, Q. Li: Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol 17(9), 1681-1692 (2003)
[34]J. C. Surra, N. Guillen, J. M. Arbones-Mainar, C. Barranquero, M. A. Navarro, C. Arnal, I. Orman, J. C. Segovia, J. Osada: Sex as a profound modifier of atherosclerotic lesion development in apolipoprotein E-deficient mice with different genetic backgrounds. J Atheroscler Thromb 17(7), 712-721 (2010)
[35]P. G. Reeves, F. H. Nielsen, G. C. Fahey, Jr.: AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11), 1939-1951 (1993)
[36]A. J. Sarria, J. C. Surra, S. Acín, R. Carnicer, M. A. Navarro, J. M. Arbonés-Mainar, N. Guillén, M. V. Martínez-Gracia, C. Arnal, J. Osada: Understanding the role of dietary components on atherosclerosis using genetic engineered mouse models. Front Biosci 11, 955-967 (2006)
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Frontiers in Bioscience-Elite (FBE) is published by IMR Press from Volume 13 Issue 2 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Diet and sex hormones regulate hepatic Synaptotagmin 1 mRNA in mice
1 Departamento de Bioquimica y Biologia Molecular y Celular, Facultad de Veterinaria, Instituto Investigacion Sanitaria de Aragon (IIS), Universidad de Zaragoza, Spain
2 Instituto de Investigacion Sanitaria de Aragon (IIS), Universidad de Zaragoza, Spain
3 Departamento de Produccion Animal, Escuela Politecnica Superior de Huesca, Spain
4 Departamento de Patologia Animal, Facultad de Veterinaria, Universidad de Zaragoza, Spain
5 CIBER de Fisiopatologia de la Obesidad y Nutricion, Instituto de Salud Carlos III, Spain
*Author to whom correspondence should be addressed.
Abstract
The expression of Synaptotagmin 1 (Syt1) has been found to be associated with the lipid droplets in liver. Here, we studied the expression of Syt1 in Apoe-deficient mice receiving cholesterol, Western diet, squalene, and oleanolic acid. We also studied the influence of sex and impact of surgical castration. Dietary cholesterol increased hepatic Syt1 expression, an effect that was enhanced when cholesterol was combined with saturated fat present in a Western diet. This potentiation was modified by the administration of 10 mg/kg oleanolic acid or 1 g/kg squalene. Females fed chow or Western diet showed higher levels of hepatic Syt1 expression as compared to male mice on the same diet. Surgical castration of males did not modify the Syt1 expression; however, ovariectomy led to decreased levels. The data show that hepatic Syt1 expression is influenced by diet and hormonal milieu.
Keywords
- Synaptotagmin 1
- Cholesterol
- Apolipoprotein E Deficient Mice
- Squalene
- High-Fat Diet
- Syt1
- sex
References
- [1] T. C. Sudhof: A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat Med 19(10), 1227-1231 (2013)
- [2] C. Czibener, N. M. Sherer, S. M. Becker, M. Pypaert, E. Hui, E. R. Chapman, W. Mothes, N. W. Andrews: Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J Cell Biol 174(7), 997-1007 (2006)
- [3] Z. T. Hu, M. R. Chen, Z. Ping, Y. M. Dong, R. Y. Zhang, T. Xu, Z. X. Wu: Synaptotagmin IV regulates dense core vesicle (DCV) release in LbetaT2 cells. Biochem Biophys Res Commun 371(4), 781-786 (2008)
- [4] H. Zhao, Y. Ito, J. Chappel, N. W. Andrews, S. L. Teitelbaum, F. P. Ross: Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev Cell 14(6), 914-925 (2008)
- [5] C. W. Davis, B. F. Dickey: Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70, 487-512 (2008)
- [6] Y. Li, P. Wang, J. Xu, F. Gorelick, H. Yamazaki, N. Andrews, G. V. Desir: Regulation of insulin secretion and GLUT4 trafficking by the calcium sensor synaptotagmin VII. Biochem Biophys Res Commun 362(3), 658-664 (2007)
- [7] W. D. Matthew, L. Tsavaler, L. F. Reichardt: Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol 91(1), 257-269 (1981)
- [8] Y. Hu, J. E. Ippolito, E. M. Garabedian, P. A. Humphrey, J. I. Gordon: Molecular characterization of a metastatic neuroendocrine cell cancer arising in the prostates of transgenic mice. J Biol Chem 277(46), 44462-44474 (2002)
- [9] W. C. Tucker, E. R. Chapman: Role of synaptotagmin in Ca2+-triggered exocytosis. Biochem J 366(Pt 1), 1-13 (2002)
- [10] J. Z. Zhang, B. A. Davletov, T. C. Sudhof, R. G. Anderson: Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78(5), 751-760 (1994)
- [11] N. Jarousse, R. B. Kelly: The AP2 binding site of synaptotagmin 1 is not an internalization signal but a regulator of endocytosis. J Cell Biol 154(4), 857-866 (2001)
- [12] V. Kiessling, S. Ahmed, M. K. Domanska, M. G. Holt, R. Jahn, L. K. Tamm: Rapid fusion of synaptic vesicles with reconstituted target SNARE membranes. Biophys J 104(9), 1950-1958 (2013)
- [13] M. W. Musch, D. L. Arvans, M. M. Walsh-Reitz, K. Uchiyama, M. Fukuda, E. B. Chang: Synaptotagmin I binds intestinal epithelial NHE3 and mediates cAMP-and Ca2+-induced endocytosis by recruitment of AP2 and clathrin. Am J Physiol Gastrointest Liver Physiol 292(6), G1549-G1558 (2007)
- [14] M. W. Musch, D. L. Arvans, Y. Wang, Y. Nakagawa, E. Solomaha, E. B. Chang: Cyclic AMP-mediated endocytosis of intestinal epithelial NHE3 requires binding to synaptotagmin 1. Am J Physiol Gastrointest Liver Physiol 298(2), G203-G211 (2010)
- [15] E. Selga, F. J. Perez-Cano, A. Franch, C. Ramirez-Santana, M. Rivero, C. J. Ciudad, C. Castellote, V. Noe: Gene expression profiles in rat mesenteric lymph nodes upon supplementation with conjugated linoleic acid during gestation and suckling. BMC Genomics 12, 182 (2011)
- [16] S. W. Messenger, D. D. Thomas, M. A. Falkowski, J. A. Byrne, F. S. Gorelick, G. E. Groblewski: Tumor protein D52 controls trafficking of an apical endolysosomal secretory pathway in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 305(6), G439-G452 (2013)
- [17] G. Jacobsson, A. J. Bean, R. H. Scheller, L. Juntti-Berggren, J. T. Deeney, P. O. Berggren, B. Meister: Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Sci U S A 91(26), 12487-12491 (1994)
- [18] J. Lang, M. Fukuda, H. Zhang, K. Mikoshiba, C. B. Wollheim: The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic beta-cells: action of synaptotagmin at low micromolar calcium. EMBO J 16(19), 5837-5846 (1997)
- [19] N. Nakajima-Nagata, M. Sugai, T. Sakurai, J. Miyazaki, Y. Tabata, A. Shimizu: Pdx-1 enables insulin secretion by regulating synaptotagmin 1 gene expression. Biochem Biophys Res Commun 318(3), 631-635 (2004)
- [20] M. P. Rastaldi, S. Armelloni, S. Berra, N. Calvaresi, A. Corbelli, L. A. Giardino, M. Li, G. Q. Wang, A. Fornasieri, A. Villa, E. Heikkila, R. Soliymani, A. Boucherot, C. D. Cohen, M. Kretzler, A. Nitsche, M. Ripamonti, A. Malgaroli, M. Pesaresi, G. L. Forloni, D. Schlondorff, H. Holthofer, G. D’Amico: Glomerular podocytes contain neuron-like functional synaptic vesicles. Faseb J 20(7), 976-978 (2006)
- [21] C. Pattaro, A. De Grandi, V. Vitart, C. Hayward, A. Franke, Y. S. Aulchenko, A. Johansson, S. H. Wild, S. A. Melville, A. Isaacs, O. Polasek, D. Ellinghaus, I. Kolcic, U. Nothlings, L. Zgaga, T. Zemunik, C. Gnewuch, S. Schreiber, S. Campbell, N. Hastie, M. Boban, T. Meitinger, B. A. Oostra, P. Riegler, C. Minelli, A. F. Wright, H. Campbell, C. M. van Duijn, U. Gyllensten, J. F. Wilson, M. Krawczak, I. Rudan, P. P. Pramstaller: A meta-analysis of genome-wide data from five European isolates reveals an association of COL22A1, SYT1, and GABRR2 with serum creatinine level. BMC Med Genet 11, 41 (2010)
- [22] N. Guillen, M. A. Navarro, C. Arnal, E. Noone, J. M. Arbones-Mainar, S. Acin, J. C. Surra, P. Muniesa, H. M. Roche, J. Osada: Microarray analysis of hepatic gene expression identifies new genes involved in steatotic liver. Physiol Genomics 37(3), 187-198 (2009)
- [23] S. Sancho-Knapik, N. Guillén, J. Osada: Cloning and expression of hepatic synaptotagmin 1 in mouse. Gene 562, 236-243 (2015)
- [24] S. Acin, M. A. Navarro, R. Carnicer, J. M. Arbones-Mainar, M. A. Guzman, C. Arnal, G. Beltran, M. Uceda, N. Maeda, J. Osada: Dietary cholesterol suppresses the ability of olive oil to delay the development of atherosclerotic lesions in apolipoprotein E knockout mice. Atherosclerosis 182(1), 17-28 (2005)
- [25] J. M. Arbones-Mainar, M. A. Navarro, S. Acin, M. A. Guzman, C. Arnal, J. C. Surra, R. Carnicer, H. M. Roche, J. Osada: Trans-10, cis-12-and cis-9, trans-11-conjugated linoleic acid isomers selectively modify HDL-apolipoprotein composition in apolipoprotein E knockout mice. J Nutr 136(2), 353-359 (2006)
- [26] C. Gabas-Rivera, R. Martinez-Beamonte, J. L. Rios, M. A. Navarro, J. C. Surra, C. Arnal, M. J. Rodriguez-Yoldi, J. Osada: Dietary oleanolic acid mediates circadian clock gene expression in liver independently of diet and animal model but requires apolipoprotein A1. J Nutr Biochem 24(12), 2100-2109 (2013)
- [27] N. Guillen, S. Acin, M. A. Navarro, J. S. Perona, J. M. Arbones-Mainar, C. Arnal, A. J. Sarria, J. C. Surra, R. Carnicer, I. Orman, J. C. Segovia, V. Ruiz-Gutierrez, J. Osada: Squalene in a sex-dependent manner modulates atherosclerotic lesion which correlates with hepatic fat content in apoE-knockout male mice. Atherosclerosis 196, 558-564 (2008)
- [28] R. Martinez-Beamonte, M. A. Navarro, A. Larraga, M. Strunk, C. Barranquero, S. Acin, M. A. Guzman, P. Inigo, J. Osada: Selection of reference genes for gene expression studies in rats. J Biotechnol 151(4), 325-334 (2011)
- [29] J. Folch, M. Lees, G. H. Sloane Stanley: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1), 497-509 (1957)
- [30] P. R. Kiela, A. J. Midura, N. Kuscuoglu, S. D. Jolad, A. M. Solyom, D. G. Besselsen, B. N. Timmermann, F. K. Ghishan: Effects of Boswellia serrata in mouse models of chemically induced colitis. Am J Physiol Gastrointest Liver Physiol 288(4), G798-G808 (2005)
- [31] Y.-R. Chen, C. F. Meyer, T.-H. Tan: Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in γ radiation-induced apoptosis. J Biol Chem 271(2), 631-634 (1996)
- [32] C. Brenner, L. Galluzzi, O. Kepp, G. Kroemer: Decoding cell death signals in liver inflammation. J Hepatol 59(3), 583-594 (2013)
- [33] J. Xu, Q. Li: Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol 17(9), 1681-1692 (2003)
- [34] J. C. Surra, N. Guillen, J. M. Arbones-Mainar, C. Barranquero, M. A. Navarro, C. Arnal, I. Orman, J. C. Segovia, J. Osada: Sex as a profound modifier of atherosclerotic lesion development in apolipoprotein E-deficient mice with different genetic backgrounds. J Atheroscler Thromb 17(7), 712-721 (2010)
- [35] P. G. Reeves, F. H. Nielsen, G. C. Fahey, Jr.: AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11), 1939-1951 (1993)
- [36] A. J. Sarria, J. C. Surra, S. Acín, R. Carnicer, M. A. Navarro, J. M. Arbonés-Mainar, N. Guillén, M. V. Martínez-Gracia, C. Arnal, J. Osada: Understanding the role of dietary components on atherosclerosis using genetic engineered mouse models. Front Biosci 11, 955-967 (2006)
