98
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Steroidogenic Factor-1 Regulation of Dorsomedial Ventromedial Hypothalamic Nucleus Ghrh Neuron Transmitter Marker and Estrogen Receptor Gene Expression in Male Rat

, , & ORCID Icon
Article: 2368382 | Accepted 10 May 2024, Published online: 15 Jul 2024

References

  • Adams, J. M., Legan, S. J., Ott, C. E., & Jackson, B. A. (2005). Modulation of hypoglycemia-induced increases in plasma epinephrine by estrogen in the female rat. Journal of Neuroscience Research, 79(3), 360–367. https://doi.org/10.1002/jnr.20369
  • Ahmed-Sorour, H., & Bailey, C. J. (1980). Role of ovarian hormones in the long-term control of glucose homeostasis. Interaction with insulin, glucagon, and epinephrine. Hormone Research, 13(6), 396–403. https://doi.org/10.1159/000179307
  • Ahmed-Sorour, H., & Bailey, C. J. (1981). Role of ovarian hormones in the long-term control of glucose homeostasis, glycogen formation, and gluconeogenesis. Annals of Nutrition & Metabolism, 25(4), 208–212. https://doi.org/10.1159/000176496
  • Ali, M. H., Alshamrani, A. A., & Briski, K. P. (2022a). Hindbrain lactate regulation of hypoglycemia-associated patterns of catecholamine and metabolic-sensory biomarker gene expression in A2 noradrenergic neurons innervating the ventromedial hypothalamic nucleus in male versus female rat. Journal of Chemical Neuroanatomy, 122, 102102. https://doi.org/10.1016/j.jchemneu.2022.102102
  • Ali, M. H., Alshamrani, A. A., Napit, P. R., & Briski, K. P. (2022b). Single-cell multiplex qPCR evidence for sex-dimorphic glutamate decarboxylase, estrogen receptor, and 5’-AMP-activated protein kinase alpha subunit mRNA expression by ventromedial hypothalamic nucleus GABAergic neurons. Journal of Chemical Neuroanatomy, 27, 102132. https://doi.org/10.1016/j.jchemneu.2022.102132
  • Alshamrani, A. A., Ibrahim, M. M. H., & Briski, K. P. (2022). Effects of short-term food deprivation on catecholamine and metabolic-sensory biomarker gene expression in hindbrain A2 noradrenergic neurons projecting to the forebrain rostral preoptic area: Impact of negative versus positive estradiol feedback. IBRO Neuroscience Reports, 13, 38–46. https://doi.org/10.1016/j.ibneur.2022.06.001
  • Bailey, C. J., & Ahmed-Sorour, H. (1980). Role of ovarian hormones in the long-term control of glucose homeostasis. Effects of insulin secretion. Diabetologia, 19(5), 475–481. https://doi.org/10.1007/BF00281829
  • Behar, K. L. (2009). GABA synthesis and metabolism. Encyclopedia of Neuroscience, 433–439. https://doi.org/10.1016/B978-008045046-9.01240-7
  • Bheemanapally, K., Ibrahim, M. M. H., Alshamrani, A., & Briski, K. P. (2021). Ventromedial hypothalamic nucleus glycogen phosphorylase regulation of metabolic-sensory neuron AMPK and neurotransmitter protein expression: Role of L-lactate. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 320(6), R791–R799. https://doi.org/10.1152/ajpregu.00292.2020
  • Briski, K. P., & Nedungadi, T. P. (2009). Adaptation of feeding and counter-regulatory hormone responses to intermediate insulin-induced hypoglycaemia in the ovariectomised female rat: Effects of oestradiol. Journal of Neuroendocrinology, 21(6), 578–585. https://doi.org/10.1111/j.1365-2826.2009.01872.x
  • Briski, K. P., Mandal, S. K., Bheemanapally, K., & Ibrahim, M. M. H. (2020). Effects of acute versus recurrent insulin-induced hypoglycemia on ventromedial hypothalamic nucleus metabolic-sensory neuron AMPK activity: Impact of alpha1-adrenergic receptor signaling. Brain Research Bulletin, 157, 41–50. https://doi.org/10.1016/j.brainresbull.2020.01.013
  • Burgunder, J. M. (1991). Perinatal ontogeny of growth hormone releasing hormone expression in rat Hypothalamus. Developmental Neuroscience, 13(6), 397–402. https://doi.org/10.1159/000112190
  • Chan, O., & Sherwin, R. (2013). Influence of VMH fuel sensing on hypoglycemic responses. Trends in Endocrinology and Metabolism, 24(12), 616–624. https://doi.org/10.1016/j.tem.2013.08.005
  • Cheung, C. C., Kurrasch, D. M., Liang, J. K., & Ingraham, H. A. (2013). Genetic labeling of steroidogenic factor-1 (SF-1) neurons in mice reveals ventromedial nucleus of the hypothalamus (VMH) circuitry beginning at neurogenesis and development of a separate non-SF-1 neuronal cluster in the ventrolateral VMH. Journal of Comparative Neurology, 521(6), 1268–1288. https://doi.org/10.1002/cne.23226
  • Choi, Y. H., Fujikawa, T., Lee, J., Reuter, A., & Kim, K. W. (2013). Revisiting the ventral medial nucleus of the hypothalamus: the roles of SF-1 neurons in energy homeostasis. Frontiers in Neuroscience, 7, 71. https://doi.org/10.3389/fnins.2013.00071.
  • Davis, A. M., Seney, M. L., Stallings, N. R., Zhao, L., Parker, K. L., & Tobet, S. A. (2004). Loss of steroidogenic factor 1 alters cellular topography in the mouse ventromedial hypothalamic nucleus of the hypothalamus. Journal of Neurobiology, 60(4), 424–436. https://doi.org/10.1002/neu.20030
  • Faure, A., Haouari, M., & Sutter, B. C. (1988). Short term and direct influence of oestradiol on glucagon secretion stimulated by arginine. Diabetes Metab, 14, 452–454.
  • Frohman, L. A., Nernardis, L. L., & Kant, K. J. (1968). Hypothalamic stimulation of growth hormone. Science, 162(3853), 580–582. https://doi.org/10.1126/science.162.3853.580
  • Garfield, A. S., Shah, B. P., Madara, J. C., Burke, L. K., Patterson, C. M., Flak, J., Neve, R. L., Evans, M. L., Lowell, B. B., Myers, M. G., & Heisler, L. K. (2014). A parabrachial-hypothalamic cholecystokinin neurocircuit controls counterregulatory responses to hypoglycemia. Cell Metabolism, 20(6), 1030–1037. https://doi.org/10.1016/j.cmet.2014.11.006
  • Han, S. M., Namkoong, C., Jang, P. G., Park, I. S., Hong, S. W., Katakami, H., Chun, S., Kim, S. W., Park, J. Y., Lee, K. U., & Kim, M. S. (2005). Hypothalamic AMP-activated protein kinase mediates counter-regulatory responses to hypoglycaemia in rats. Diabetologia, 48(10), 2170–2178. https://doi.org/10.1007/s00125-005-1913-1
  • Hardie, D. G., & Lin, S. C. (2017). AMP-activated protein kinase – not just an energy sensor. F1000Research, 6, 1724. https://doi.org/10.12688/f1000research.11960.1
  • Hardie, D. G., Ross, F. A., & Hawley, S. A. (2012). AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nature Reviews. Molecular Cell Biology, 13(4), 251–262. https://doi.org/10.1038/nrm3311
  • Hardie, D. G., Schaffer, B. E., & Brunet, A. (2016). AMPK: An energy-sensing pathway with multiple inputs and outputs. Trends in Cell Biology, 26(3), 190–201. https://doi.org/10.1016/j.tcb.2015.10.013
  • Ibrahim, M. M. H., Alhamami, H. N., & Briski, K. P. (2019). Norepinephrine regulation of ventromedial hypothalamic nucleus metabolic transmitter biomarker and astrocyte enzyme and receptor expression: impact of 5’-AMP-activated protein kinase. Brain Research, 1711, 48–57. https://doi.org/10.1016/j.brainres.2019.01.012
  • Ibrahim, M. M. H., Bheemanapally, K., Alhamami, H. N., & Briski, K. P. (2020). Effects of intracerebroventricular glycogen phosphorylase inhibitor CP-316,819 infusion on hypothalamic glycogen content and metabolic neuron AMPK activity and neurotransmitter expression in the male rat. Journal of Molecular Neuroscience, 70(5), 647–658. https://doi.org/10.1007/s12031-019-01471-0
  • Kim, D. W., Yao, Z., Graybuck, L. T., Kim, T. K., Nguyen, T. N., Smith, K. A., Fong, O., Yi, L., Koulena, N., Pierson, N., Shah, S., Lo, L., Pool, A. H., Oka, Y., Pachter, L., Cai, L., Tasic, B., Zeng, H., & Anderson, D. J. (2019). Multimodal analysis of cell types in a hypothalamic node controlling social behavior. Cell, 179(3), 713–728. https://doi.org/10.1016/j.cell.2019.09.020
  • Kim, K. W., Donato, J., Berglund, E. D., Choi, Y.-H., Kohno, D., Elias, C. F., Depinho, R. A., & Elmquist, J. K. (2012). FOXO1 in the ventromedial hypothalamus regulates energy balance. The Journal of Clinical Investigation, 122(7), 2578–2589. https://doi.org/10.1172/JCI62848
  • Kim, K. W., Zhao, L., & Parker, K. L. (2009). Central nervous system-specific knockout of steroidogenic factor 1. Molecular and Cellular Endocrinology, 300(1–2), 132–136. https://doi.org/10.1016/j.mce.2008.09.026
  • Kim, K. W., Zhao, L., Donato, J., Kohno, D., Xu, Y., Elias, C. F., Lee, C., Parker, K. L., & Elmquist, J. K. (2011). Steroidogenic factor 1 directs programs regulating diet-induced thermogenesis and leptin action in the ventral medial hypothalamic nucleus. Proceedings of the National Academy of Sciences of the United States of America, 108(26), 10673–10678. https://doi.org/10.1073/pnas.1102364108
  • Komesaroff, P. A., Esler, M., Clarke, I. J., Fullerton, M. J., & Funder, J. W. (1988). Effects of estrogen and estrous cycle on glucocorticoid and catecholamine responses to stress in sheep. American Journal of Physiology-Endocrinology and Metabolism, 275(4), E671–E678. https://doi.org/10.1152/ajpendo.1998.275.4.E671
  • Lenzen, S., & Bailey, C. J. (1984). Thyroid hormones, gonadal and adrenocortical steroids and the function of the islets of Langerhans. Endocrine Reviews, 5(3), 411–434. https://doi.org/10.1210/edrv-5-3-411
  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(t) method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
  • López, M. (2018). Hypothalamic AMPK and energy balance. European Journal of Clinical Investigation, 48(9), e12996. https://doi.org/10.1111/eci.12996
  • Mahmood, A. S. M. H., Uddin, M. M., Mandal, S. K., Ibrahim, M. M. H., Alhamami, N. H., & Briski, K. P. (2018). Sex differences in forebrain estrogen receptor regulation of hypoglycemic patterns of counter-regulatory hormone secretion and ventromedial hypothalamic nucleus gluco-regulatory neurotransmitter and astrocyte glycogen metabolic enzyme expression. Neuropeptides, 72, 65–74. https://doi.org/10.1016/j.npep.2018.10.003
  • Martin, D. L., & Barke, K. E. (1998). Are GAD65 and GAD67 associated with specific pools of GABA in brain? Perspectives on Development Neurobiology, 5(2–3), 119–129.
  • McClellan, K. M., Parker, K. L., & Tobet, S. (2006). Development of the ventromedial nucleus of the hypothalamus. Frontiers in Neuroendocrinology, 27(2), 193–209. https://doi.org/10.1016/j.yfrne.2006.02.002
  • McCrimmon, R. J., Shaw, M., Fan, X., Cheng, H., Ding, Y., Vella, M. C., Zhou, L., McNay, E. C., & Sherwin, R. S. (2008). Key role for AMP-activated protein kinase in the ventromedial hypothalamus in regulating counterregulatory hormone responses to acute hypoglycemia. Diabetes, 57(2), 444–450. https://doi.org/10.2337/db07-0837
  • Meek, T. H., Nelson, J. T., Matsen, M. E., Dorfman, M. D., Guyenet, S. J., Damian, V., Allison, M. B., Scarlett, J. M., Nguyen, H. T., Thaler, J. P., Olson, D. P., Myers, M. G., Schwartz, M. W., & Morton, G. J. (2016). Functional identification of a neurocircuit regulating blood glucose. Proceedings of the National Academy of Sciences of the United States of America, 113(14), E2073–E2082. https://doi.org/10.1073/pnas.1521160113
  • Napit, P. R., Ali, M. H., Shakya, M., Mandal, S. K., Bheemanapally, K., Mahmood, A. S. M. H., Ibrahim, M. M. H., & Briski, K. P. (2019). Hindbrain estrogen receptor regulation of counter-regulatory hormone secretion and ventromedial hypothalamic nucleus glycogen content and glucoregulatory transmitter signaling in hypoglycemic female rats. Neuroscience, 411, 211–221. https://doi.org/10.1016/j.neuroscience.2019.05.007
  • Nedungadi, T. P., & Briski, K. P. (2012). Site-specific effects of intracranial estradiol administration on recurrent insulin-induced hypoglycemia in the ovariectomized female rat. Neuroendocrinology, 96(4), 311–323. https://doi.org/10.1159/000338407
  • Paranjape, S. A., & Briski, K. P. (2005). Recurrent insulin-induced hypoglycemia causes site-specific patterns of habituation or amplification of CNS neuronal genomic activation. Neuroscience, 130(4), 957–970. https://doi.org/10.1016/j.neuroscience.2004.09.030
  • Pimentel, G. D., Ropelle, E. R., Rocha, G. Z., & Carvalheira, J. B. C. (2013). The role of neuronal AMPK as a mediator of nutritional regulation of food intake and energy homeostasis. Metabolism: Clinical and Experimental, 62(2), 171–178. https://doi.org/10.1016/j.metabol.2012.07.001
  • Roy, S. C., Napit, P. R., Pasula, M., Bheemanapally, K., & Briski, K. P. (2023). G protein-coupled lactate receptor GPR81 control of ventrolateral ventromedial hypothalamic nucleus glucoregulatory neurotransmitter and 5'-AMP-activated protein kinase expression. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 324(1), R20–R34. https://doi.org/10.1152/ajpregu.00100.2022
  • Sapkota, S., Ali, M. H., Alshamrani, A. A., Napit, P. R., Roy, S. C., Pasula, M. B., & Briski, K. P. (2023). GHRH neurons from the ventromedial hypothalamic nucleus provide dynamic and sex-specific input to the brain glucose-regulatory network. Neuroscience, 529, 73–87. https://doi.org/10.1016/j.neuroscience.2023.08.006
  • Schousboe, A., & Waagepetersen, H. S. (2017). Gamma-aminobutyric acid (GABA). In Reference module in neuroscience and biobehavioral psychology. Elsevier. https://doi.org/10.1016/B978-0-12-809324-5.02341-5
  • Tavazzani, E., Tritto, S., Spaiardi, P., Botta, L., Manca, M., Prigioni, I., Masetto, S., & Russo, G. (2014). Glutamic acid decarboxylase 67 expression by a distinct population of mouse vestibular supporting cells. Frontiers in Cellular Neuroscience, 8, 428. https://doi.org/10.3389/fncel.2014.00428
  • Tong, Q., Ye, C. P., McCrimmon, R. J., Dhillon, H., Choi, B., Kramer, M. D., Yu, J., Yang, Z., Christiansen, L. M., Lee, C. E., Choi, C. S., Zigman, J. M., Shulman, G. I., Sherwin, R. S., Elmquist, J. K., & Lowell, B. B. (2007). Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell Metabolism, 5(5), 383–393. https://doi.org/10.1016/j.cmet.2007.04.001
  • Tu, L., Fukuda, M., Tong, Q., & Xu, Y. (2022). The ventromedial hypothalamic nucleus: Watchdog of whole-body glucose homeostasis. Cell & Bioscience, 12(1), 71. https://doi.org/10.1186/s13578-022-00799-2
  • Watts, A. G., & Donovan, C. M. (2010). Sweet talk in the brain: glucosensing, neural networks, and hypoglycemic counterregulation. Frontiers in Neuroendocrinology, 31(1), 32–43. https://doi.org/10.1016/j.yfrne.2009.10.006
  • Woods, A., Salt, I., Scott, J., Hardie, D. G., & Carling, D. (1996). The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Letters, 397(2-3), 347–351. https://doi.org/10.1016/s0014-5793(96)01209-4
  • Wurtman, J. J., & Baum, M. J. (1980). Estrogen reduced total food and carbohydrate intake, but not protein intake, in female rats. Physiology & Behavior, 24(5), 823–827. https://doi.org/10.1016/0031-9384(80)90134-1
  • Xu, Y., Nedungadi, T. P., Zhu, L., Sobhani, N., Irani, B. G., Davis, K. E., Zhang, X., Zou, F., Gent, L. M., Hahner, L. D., Khan, S. A., Elias, C. F., Elmquist, J. K., & Clegg, D. J. (2011). Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metabolism, 14(4), 453–465. https://doi.org/10.1016/j.cmet.2011.08.009
  • Xue, B., & Kahn, B. B. (2006). AMPK integrates nutrient and hormonal signals to regulate food intake and energy balance through effects in the hypothalamus and peripheral tissues. The Journal of Physiology, 574(Pt 1), 73–83. https://doi.org/10.1113/jphysiol.2006.113217
  • Zhang, R., Dhillon, H., Yin, H., Yoshimura, A., Lowell, B. B., Maratos-Flier, E., & Flier, J. S. (2008). Selective inactivation of Socs3 in SF1 neurons improves glucose homeostasis without affecting body weight. Endocrinology, 149(11), 5654–5661. https://doi.org/10.1210/en.2008-0805
  • Zhao, L., Kim, K. W., Ikeda, Y., Anderson, K. K., Beck, L., Chase, S., Tobet, S. A., & Parker, K. L. (2008). Central nervous system-specific knockout of steroidogenic factor 1 results in increased anxiety-like behavior. Molecular Endocrinology, 22(6), 1403–1415. https://doi.org/10.1210/me.2008-0034