Sex-Specific Differences in the Transport and Availability of Energy Substrates in the Hippocampus of Rats During Neurodevelopment

Edmond J (1992) Energy metabolism in developing brain cells. Can J Physiol Pharmacol 70:S118–29. https://doi.org/10.1139/y92-253

Schelp AO, Burini RC (1995) Control of supply and use of energy substrates in the encephalon. Arq Neuropsiquiatr 53. https://doi.org/10.1590/s0004-282x1995000400025

Lust WD, Pundik S, Zechel J, et al (2003) Changing metabolic and energy profiles in fetal, neonatal, and adult rat brain. Metab Brain Dis 18. https://doi.org/10.1023/A:1025503115837

Zhang WW, Churchill S, Churchill P (1989) Developmental regulation of D-β-hydroxybutyrate dehydrogenase in rat liver and brain. FEBS Lett 256. https://doi.org/10.1016/0014-5793(89)81720-X

Jensen NJ, Wodschow HZ, Nilsson M, Rungby J. Effects of Ketone Bodies on Brain Metabolism and Function in Neurodegenerative Diseases. Int J Mol Sci 21(22):8767. https://doi.org/10.3390/ijms21228767

Vicario C, Arizmendi C, Malloch G, et al (1991) Lactate utilization by isolated cells from early neonatal rat brain. J Neurochem 57. https://doi.org/10.1111/j.1471-4159.1991.tb06370.x

Stafstrom CE, Rho JM (2012) The ketogenic diet as a treatment paradigm for diverse neurological disorders. Front Pharmacol 3. https://doi.org/10.3389/fphar.2012.00059

Doretto S, Malerba M, Ramos M, et al (2011) Oligodendrocytes as regulators of neuronal networks during early postnatal development. PLoS One 6. https://doi.org/10.1371/journal.pone.0019849

Jha MK, Morrison BM (2018) Glia-neuron energy metabolism in health and diseases: New insights into the role of nervous system metabolic transporters. Exp Neurol 309:23-31. https://doi.org/10.1016/j.expneurol.2018.07.009

Felmlee MA, Jones RS, Rodriguez-Cruz V, Follman KE, Morris ME (2020) Monocarboxylate Transporters (SLC16): Function, Regulation, and Role in Health and Disease. Pharmacol Rev 72(2):466–485. https://doi.org/10.1124/pr.119.018762

Machado UF (1998) Transportadores de glicose. Arq Bras Endocrinol Metabol 42. https://doi.org/10.1590/s0004-27301998000600003

Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27(11):1766–91. https://doi.org/10.1038/sj.jcbfm.9600521

Dombrowski GJ, Swiatek KR, Chao KL (1989) Lactate, 3-hydroxybutyrate, and glucose as substrates for the early postnatal rat brain. Neurochem Res 14. https://doi.org/10.1007/BF00964877

Cahill L, Aswad D (2015) Sex influences on the brain: an issue whose time has come. Neuron 88:1084–1085

Article  CAS  PubMed  Google Scholar 

Amateur SK, McCarthy MM (2002) Sexual differentiation of astrocyte morphology in the developing rat preoptic area. J Neuroendocrinol 14. https://doi.org/10.1046/j.1365-2826.2002.00858.x

Garcia-Segura LM, Dueñas M, Busiguina S et al (1995) Gonadal hormone regulation of neuronal-glial interactions in the developing neuroendocrine hypothalamus. J Steroid Biochem Mol Biol 53:293–298. https://doi.org/10.1016/0960-0760(95)00066-9

Article  CAS  PubMed  Google Scholar 

Mong JA, Kurzweil RL, Davis AM, et al (1996) Evidence for sexual differentiation of glia in rat brain. Horm Behav 30. https://doi.org/10.1006/hbeh.1996.0058

Nelson LH, Warden S, Lenz KM (2017) Sex differences in microglial phagocytosis in the neonatal hippocampus. Brain Behav Immun 64. https://doi.org/10.1016/j.bbi.2017.03.010

Swamydas M, Bessert D, Skoff R (2009) Sexual dimorphism of oligodendrocytes is mediated by differential regulation of signaling pathways. J Neurosci Res 87. https://doi.org/10.1002/jnr.21943

Weis SN, Souza JMF, Hoppe JB, et al (2021) In-depth quantitative proteomic characterization of organotypic hippocampal slice culture reveals sex-specific differences in biochemical pathways. Sci Rep 11. https://doi.org/10.1038/s41598-021-82016-7

Garcia-Segura LM, Azcoitia I, DonCarlos LL (2001) Neuroprotection by estradiol. Prog Neurobiol 63(1):29–60. https://doi.org/10.1016/s0301-0082(00)00025-3

McEwen BS, Milner TA (2017) Understanding the broad influence of sex hormones and sex differences in the brain. J Neurosci Res 95(1-2):24–39. https://doi.org/10.1002/jnr.23809

Hanamsagar R, Bilbo SD (2016) Sex differences in neurodevelopmental and neurodegenerative disorders: focus on microglial function and neuroinflammation during development. J Steroid Biochem Mol Biol 160:127–33. https://doi.org/10.1016/j.jsbmb.2015.09.039

Schwarz JM, Bilbo SD(2012) Sex, glia, and development: interactions in health and disease. Horm Behav 62(3):243–53. https://doi.org/10.1016/j.yhbeh.2012.02.018

Netto CA, Sanches E, Odorcyk FK et al (2017) Sex-dependent consequences of neonatal brain hypoxia-ischemia in the rat. J Neurosci Res 95:409–421

Article  CAS  PubMed  Google Scholar 

Gillies GE, Pienaar IS, Vohra S, Qamhawi Z (2014) Sex differences in Parkinson's disease. Front Neuroendocrinol 35(3):370–84. https://doi.org/10.1016/j.yfrne.2014.02.002

Odorcyk FK, Duran-Carabali LE, Rocha DS et al (2020) Differential glucose and beta-hydroxybutyrate metabolism confers an intrinsic neuroprotection to the immature brain in a rat model of neonatal hypoxia ischemia. Exp Neurol 330:113317. https://doi.org/10.1016/J.EXPNEUROL.2020.113317

Article  CAS  PubMed  Google Scholar 

Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91. https://doi.org/10.1073/pnas.91.22.10625

Durán-Carabali LE, Odorcky FK, Grun LK, et al (2024) Maternal environmental enrichment protects neonatal brains from hypoxic-ischemic challenge by mitigating brain energetic dysfunction and modulating glial cell responses. Exp Neurol 374. https://doi.org/10.1016/j.expneurol.2024.114713

Seddon AM, Curnow P, Booth PJ (2004) Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666(1–2):105–17. https://doi.org/10.1016/j.bbamem.2004.04.011

Büttner‐Ennever J (1997) The rat brain in stereotaxic coordinates, 3rd edn. By George Paxinos and Charles Watson. (Pp. xxxiii+80; illustrated; £$69.95 paperback; ISBN 0 12 547623; comes with CD‐ROM.) San Diego: Academic Press. 1996. J Anat 191. https://doi.org/10.1046/j.1469-7580.1997.191203153.x

Aranguez MI, Goya L, Pascual-Leone AM (1986) Changes in blood glucose, liver glycogen, ketone bodies and plasma insulin in suckling rats treated with a single high cortisol dose one day after birth. Acta Endocrinol (Copenh) 113. https://doi.org/10.1530/acta.0.1130598

Ferré P, Decaux JF, Issad T, Girard J (1986). Changes in energy metabolism during the suckling and weaning period in the newborn. Reprod Nutr Dev 26(2B):619–31. https://doi.org/10.1051/rnd:19860413

MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211(4488):1294–302. https://doi.org/10.1126/science.6163211

De Angelis LC, Brigati G, Polleri G, Malova M, Parodi A, Minghetti D, Rossi A, Massirio P, Traggiai C, Maghnie M, Ramenghi LA (2021) Neonatal Hypoglycemia and Brain Vulnerability. Front Endocrinol (Lausanne) 12:634305. https://doi.org/10.3389/fendo.2021.634305

Nicholas KR, Hartmann PE (1991) Milk secretion in the rat: progressive changes in milk composition during lactation and weaning and the effect of diet. Comp Biochem Physiol -- Part A Physiol 98. https://doi.org/10.1016/0300-9629(91)90443-G

Almeida A, Bolaños JP, Medina JM (1992) Ketogenesis from lactate in rat liver during the perinatal period. Pediatr Res 31. https://doi.org/10.1203/00006450-199204000-00022

Brückner G, Biesold D (1981) Histochemistry of glycogen deposition in perinatal rat brain: importance of radial glial cells. J Neurocytol 10. https://doi.org/10.1007/BF01262651

Roumes H, Dumont U, Sanchez S, et al (2021) Neuroprotective role of lactate in rat neonatal hypoxia-ischemia. J Cereb Blood Flow Metab 41. https://doi.org/10.1177/0271678X20908355

Pellerin L, Pellegri G, Martin JL, Magistretti PJ (1998) Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc Natl Acad Sci U S A 95. https://doi.org/10.1073/pnas.95.7.3990

Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623. https://doi.org/10.1016/0006-8993(93)91429-V

Pierre K, Pellerin L, Debernardi R, et al (2000) Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience 100. https://doi.org/10.1016/S0306-4522(00)00294-3

Yeh YY, Sheehan PM (1985) Preferential utilization of ketone bodies in the brain and lung of newborn rats. Fed Proc 44(7):2352–8

Edmond J, Robbins RA, Bergstrom JD, et al (1987) Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes, and oligodendrocytes from developing brain in primary culture. J Neurosci Res 18. https://doi.org/10.1002/jnr.490180407

Vannucci SJ, Simpson IA (2003) Developmental switch in brain nutrient transporter expression in the rat. Am J Physiol - Endocrinol Metab 285. https://doi.org/10.1152/ajpendo.00187.2003

Morris AAM (2005) Cerebral ketone body metabolism. J Inherit Metab Dis 28. https://doi.org/10.1007/s10545-005-5518-0

Picut CA, Remick AK, de Rijk EPCT, et al (2015) Postnatal development of the testis in the rat. Toxicol Pathol 43. https://doi.org/10.1177/0192623314547279

Rust RS (1994) Energy metabolism of developing brain. Curr Opin Neurol 7(2):160–5. https://doi.org/10.1097/00019052-199404000-00013

Angel JF, Back DW (1985) Weaning and metabolic regulation in the rat. Can J Physiol Pharmacol 63(5):538–45. https://doi.org/10.1139/y85-093

Girard J, Issad T, Maury J, et al (1993) Influence of the weaning diet on the changes of glucose metabolism and of insulin sensitivity. Proc Nutr Soc 52. https://doi.org/10.1079/pns19930068

Adam C (2010) Emotions driven by estrogens. From regular estrous cycle to Turner syndrome patients. J Psychosom Obstet Gynecol 31

Kim YS, Stumpf WE, Sar M, et al (1978) Estrogen and androgen target cells in the brain of fishes, reptiles and birds: phylogeny and ontogeny. Integr Comp Biol 18. https://doi.org/10.1093/icb/18.3.425

Madeira MD, Sousa N, Paula-Barbosa MM (1991) Sexual dimorphism in the mossy fiber synapses of the rat hippocampus. Exp Brain Res 87. https://doi.org/10.1007/BF00227079

Stockman SL, Kight KE, Bowers JM, McCarthy MM (2022) Neurogenesis in the neonatal rat hippocampus is regulated by sexually dimorphic epigenetic modifiers. Biol Sex Differ 13. https://doi.org/10.1186/s13293-022-00418-2

Bittar PG, Charnay Y, Pellerin L, et al (1996) Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J Cereb Blood Flow Metab 16. https://doi.org/10.1097/00004647-199611000-00001

Falkowska A, Gutowska I, Goschorska M, Nowacki P, Chlubek D, Baranowska-Bosiacka I (2015) Energy Metabolism of the Brain, Including the Cooperation between Astrocytes and Neurons, Especially in the Context of Glycogen Metabolism. Int J Mol Sci 16(11):25959–81. https://doi.org/10.3390/ijms161125939

Majou D, Dermenghem AL (2023) DHA (omega-3 fatty acid) and estradiol: key roles in regional cerebral glucose uptake. OCL 30:22

Amateau SK, Alt JJ, Stamps CL, McCarthy MM (2004) Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145. https://doi.org/10.1210/en.2003-1363

Konkle ATM, McCarthy MM (2011) Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152. https://doi.org/10.1210/en.2010-0607

McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14(6):677–83. https://doi.org/10.1038/nn.2834

Nugent BM, McCarthy MM (2011) Epigenetic underpinnings of developmental sex differences in the brain. Neuroendocrinology 93(3):150–8. https://doi.org/10.1159/000325264

Pacheco-Velázquez SC, Ortega-Mejía II, Vargas-Navarro JL, et al (2022) 17-β Estradiol up-regulates energy metabolic pathways, cellular proliferation and tumor invasiveness in ER+ breast cancer spheroids. Front Oncol 12. https://doi.org/10.3389/fonc.2022.1018137

Chowen JA, Garcia-Segura LM (2021) Role of glial cells in the generation of sex differences in neurodegenerative diseases and brain aging. Mech Ageing Dev 196. https://doi.org/10.1016/j.mad.2021.111473

Dhillon SK, Gunn ER, Lear BA, King VJ, Lear CA, Wassink G, Davidson JO, Bennet L, Gunn AJ (2022) Cerebral Oxygenation and Metabolism After Hypoxia-Ischemia. Front Pediatr 10:925951. https://doi.org/10.3389/fped.2022.925951

Rettberg JR, Yao J, Brinton RD (2014) Estrogen: a master regulator of bioenergetic systems in the brain and body. Front Neuroendocrinol 35(1):8–30. https://doi.org/10.1016/j.yfrne.2013.08.001

Acaz-Fonseca E, Avila-Rodriguez M, Garcia-Segura LM, Barreto GE (2016) Regulation of astroglia by gonadal steroid hormones under physiological and pathological conditions. Prog Neurobiol 144:5–26. https://doi.org/10.1016/j.pneurobio.2016.06.002

Garcia CK, Brown MS, Pathak RK, Goldstein JL (1995) cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J Biol Chem 270. https://doi.org/10.1074/jbc.270.4.1843

Yasuda K, Maki T, Kinoshita H, et al (2020) Sex-specific differences in transcriptomic profiles and cellular characteristics of oligodendrocyte precursor cells. Stem Cell Res 46. https://doi.org/10.1016/j.scr.2020.101866

Bowers JM, Waddell J, McCarthy MM (2010) A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol. Biol Sex Differ 1. https://doi.org/10.1186/2042-6410-1-8

Demarest TG, McCarthy MM (2015) Sex differences in mitochondrial (dys)function: Implications for neuroprotection. J Bioenerg Biomembr 47(1–2):173–88. https://doi.org/10.1007/s10863-014-9583-7

Gaignard P, Liere P, Thérond P, Schumacher M, Slama A, Guennoun R (2017) Role of sex hormones on brain mitochondrial function, with special reference to aging and neurodegenerative diseases. Front Aging Neurosci 9:406. https://doi.org/10.3389/fnagi.2017.00406

Pereira LO, Arteni NS, Petersen RC, et al (2007) Effects of daily environmental enrichment on memory deficits and brain injury following neonatal hypoxia-ischemia in the rat. Neurobiol Learn Mem 87. https://doi.org/10.1016/j.nlm.2006.07.003

Charriaut-Marlangue C, Besson VC, Baud O (2017) Sexually dimorphic outcomes after neonatal stroke and hypoxia-ischemia. Int J Mol Sci 19(1):61. https://doi.org/10.3390/ijms19010061

Durán-Carabali LE, Sanches EF, Marques MR et al (2017) Longer hypoxia–ischemia periods to neonatal rats causes motor impairments and muscular changes. Neuroscience 340:291–298. https://doi.org/10.1016/j.neuroscience.2016.10.068

Article  CAS  PubMed  Google Scholar 

Vagnerova K, Koerner IP, Hurn PD (2008) Gender and the injured brain. Anesth Analg 107(1):201–14. https://doi.org/10.1213/ane.0b013e31817326a5

Mirza MA, Ritzel R, Xu Y, et al (2015) Sexually dimorphic outcomes and inflammatory responses in hypoxic-ischemic encephalopathy. J Neuroinflammation 12. https://doi.org/10.1186/s12974-015-0251-6

Passarella S, de Bari L, Valenti D, Pizzuto R, Paventi G, Atlante A (2008) Mitochondria and L-lactate metabolism. FEBS Lett 582(25–26):3569–76. https://doi.org/10.1016/j.febslet.2008.09.042

Hashimoto T, Hussien R, Oommen S, et al (2007) Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis . FASEB J 21. https://doi.org/10.1096/fj.07-8174com

Pierre K, Pellerin L (2005) Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J Neurochem 94(1):1–14. https://doi.org/10.1111/j.1471-4159.2005.03168.x

Comments (0)

No login
gif