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Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 26, 2023 - Issue 4
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Research Article

Short-term exposure to an obesogenic diet causes dynamic dysregulation of proteasome-mediated protein degradation in the hypothalamus of female rats

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References

  • Caballero B. The global epidemic of obesity: an overview. Epidemiol Rev. 2007;29:1–5.
  • Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest. 2000;106(4):473–81.
  • Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature. 2006;444(7121):840–6.
  • Kleinert M, Clemmensen C, Hofmann SM, Moore MC, Renner S, Woods SC, et al. Animal models of obesity and diabetes mellitus. Nat Rev Endocrinol. 2018;14(3):140–62.
  • Thaler JP, Guyenet SJ, Dorfman MD, Wisse BE, Schwartz MW. Hypothalamic inflammation: marker or mechanism of obesity pathogenesis? Diabetes. 2013;62(8):2629–34.
  • Velloso LA, Araujo EP, de Souza CT. Diet-induced inflammation of the hypothalamus in obesity. Neuroimmunomodulation. 2008;15(3):189–93.
  • Velloso LA, Schwartz MW. Altered hypothalamic function in diet-induced obesity. Int J Obes. 2011;35(12):1455–65.
  • Gamber KM, Huo L, Ha S, Hairston JE, Greeley S, Bjorbaek C. Over-expression of leptin receptors in hypothalamic POMC neurons increases susceptibility to diet-induced obesity. PLoS One. 2012;7(1):e30485.
  • Xu L, Li H, Zhou G, Lu W, Yang R, Liu H, Yang G. DNA-binding activity of STAT3 increased in hypothalamus of DIO mice; the reduction of STAT3 phosphorylation may facilitate leptin signaling. Biochem Biophys Res Commun. 2018;505(1):229–35.
  • Jarome TJ, Helmstetter FJ. The ubiquitin-proteasome system as a critical regulator of synaptic plasticity and long-term memory formation. Neurobiol Learn Mem. 2013;105:107–16.
  • Bedford L, Paine S, Sheppard PW, Mayer RJ, Roelofs J. Assembly, structure, and function of the 26S proteasome. Trends Cell Biol. 2010;20(7):391–401.
  • Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425–79.
  • Akutsu M, Dikic I, Bremm A. Ubiquitin chain diversity at a glance. J Cell Sci. 2016;129(5):875–80.
  • Musaus M, Navabpour S, Jarome TJ. The diversity of linkage-specific polyubiquitin chains and their role in synaptic plasticity and memory formation. Neurobiol Learn Mem. 2020;174:107286.
  • Ehlers MD. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci. 2003;6(3):231–42.
  • Bingol B, Schuman EM. Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature. 2006;441(7097):1144–8.
  • Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nagerl UV. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron. 2006;52(2):239–45.
  • Dong C, Upadhya SC, Ding L, Smith TK, Hegde AN. Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation. Learn Mem. 2008;15(5):335–47.
  • Hanna J, Guerra-Moreno A, Ang J, Micoogullari Y. Protein degradation and the pathologic basis of disease. Am J Pathol. 2019;189(1):94–103.
  • Wang QM, Yang H, Tian DR, Cai Y, Wei ZN, Wang F, et al. Proteomic analysis of rat hypothalamus revealed the role of ubiquitin-proteasome system in the genesis of DR or DIO. Neurochem Res. 2011;36(6):939–46.
  • Ignacio-Souza LM, Bombassaro B, Pascoal LB, Portovedo MA, Razolli DS, Coope A, et al. Defective regulation of the ubiquitin/proteasome system in the hypothalamus of obese male mice. Endocrinology. 2014;155(8):2831–44.
  • McFadden T, Musaus M, Nelsen JL, Martin K, Jones N, Smith P, et al. Dysregulation of protein degradation in the hippocampus is associated with impaired spatial memory during the development of obesity. Behav Brain Res. 2020;393:112787.
  • Lovejoy JC, Sainsbury A, Stock Conference Working Group G. Sex differences in obesity and the regulation of energy homeostasis. Obes Rev. 2009;10(2):154–67.
  • Morselli E, Frank AP, Palmer BF, Rodriguez-Navas C, Criollo A, Clegg DJ. A sexually dimorphic hypothalamic response to chronic high fat diet consumption. Int J Obes. 2016;40(2):206–9.
  • Devulapalli R, Jones N, Farrell K, Musaus M, Kugler H, McFadden T, et al. Males and females differ in the regulation and engagement of, but not requirement for, protein degradation in the amygdala during fear memory formation. Neurobiol Learn Mem. 2021;180:107404.
  • Jarome TJ, Perez GA, Webb WM, Hatch KM, Navabpour S, Musaus M, et al. Ubiquitination of histone H2B by proteasome subunit RPT6 controls histone methylation chromatin dynamics during memory formation. Biol Psychiatry. 2021;89(12):1176–87.
  • Butler AA, Johnston DR, Kaur S, Lubin FD. Long noncoding RNA NEAT1 mediates neuronal histone methylation and age-related memory impairment. Sci Signal. 2019;12(588):1–11.
  • McFadden T, Devulapalli RK, Jarome TJ. Quantifying subcellular ubiquitin-proteasome activity in the rodent brain. J Visualized Exp. 2019;147:e59695.
  • Giles ED, Jackman MR, MacLean PS. Modeling diet-induced obesity with obesity-prone rats: implications for studies in females. Front Nutr. 2016;3:50.
  • Reddy SS, Shruthi K, Reddy VS, Raghu G, Suryanarayana P, Giridharan NV, Reddy GB. Altered ubiquitin-proteasome system leads to neuronal cell death in a spontaneous obese rat model. Biochim Biophys Acta. 2014;1840(9):2924–34.
  • Vilchez D, Boyer L, Morantte I, Lutz M, Merkwirth C, Joyce D, et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature. 2012;489(7415):304–8.
  • Suraweera A, Munch C, Hanssum A, Bertolotti A. Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol Cell. 2012;48(2):242–53.
  • Farrell K, Musaus M, Navabpour S, Martin K, Ray WK, Helm RF, Jarome TJ. Proteomic analysis reveals sex-specific protein degradation targets in the amygdala during fear memory formation. Front Mol Neurosci. 2021;14:716284.
  • Martin K, Musaus M, Navabpour S, Gustin A, Ray WK, Helm RF, Jarome TJ. Females, but not males, require protein degradation in the hippocampus for contextual fear memory formation. Learn Mem. 2021;28(8):248–53.
  • Dulka BN, Trask S, Helmstetter FJ. Age-related memory impairment and sex-specific alterations in phosphorylation of the Rpt6 proteasome subunit and polyubiquitination in the basolateral amygdala and medial prefrontal cortex. Front Aging Neurosci. 2021;13:656944.
  • Giles ED, Jackman MR, Johnson GC, Schedin PJ, Houser JL, MacLean PS. Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats. Am J Phys Regul Integr Comp Phys. 2010;299(6):R1634–42.
  • Amengual-Cladera E, Llado I, Gianotti M, Proenza AM. Sex differences in the effect of high fat diet feeding on rat white adipose tissue mitochondrial function and insulin sensitivity. Metabolism. 2012;61(8):1108–17.
  • Sadagurski M, Debarba LK, Werneck-de-Castro JP, Ali Awada A, Baker TA, Bernal-Mizrachi E. Sexual dimorphism in hypothalamic inflammation in the offspring of dams exposed to a diet rich in high fat and branched-chain amino acids. Am J Phys Endocrinol Metab. 2019;317(3):E526–E534.
  • Shansky RM, Murphy AZ. Considering sex as a biological variable will require a global shift in science culture. Nat Neurosci. 2021;24(4):457–64.
  • Djakovic SN, Marquez-Lona EM, Jakawich SK, Wright R, Chu C, Sutton MA, Patrick GN. Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J Neurosci. 2012;32(15):5126–31.
  • Scudder SL, Gonzales FR, Howell KK, Stein IS, Dozier LE, Anagnostaras SG, et al. Altered phosphorylation of the proteasome subunit Rpt6 has minimal impact on synaptic plasticity and learning. eNeuro. 2021;8(3):1–12.
  • Dasuri K, Zhang L, Ebenezer P, Liu Y, Fernandez-Kim SO, Keller JN. Aging and dietary restriction alter proteasome biogenesis and composition in the brain and liver. Mech Ageing Dev. 2009;130(11–12):777–83.
  • Aksenova MV, Aksenov MY, Carney JM, Butterfield DA. Protein oxidation and enzyme activity decline in old brown Norway rats are reduced by dietary restriction. Mech Ageing Dev. 1998;100(2):157–68.
  • Li F, Zhang L, Craddock J, Bruce-Keller AJ, Dasuri K, Nguyen A, Keller JN. Aging and dietary restriction effects on ubiquitination, sumoylation, and the proteasome in the heart. Mech Ageing Dev. 2008;129(9):515–21.

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