- Tytuł:
- Untangling the effect of insulin action on brain mitochondria and metabolism.
- Autorzy:
- Źródło:
- Journal of neuroendocrinology [J Neuroendocrinol] 2021 Apr; Vol. 33 (4), pp. e12932. Date of Electronic Publication: 2021 Jan 28.
- Typ publikacji:
- Journal Article; Research Support, Non-U.S. Gov't; Review
- Język:
- English
- Imprint Name(s):
-
Publication: <2010->: Malden, MA : Wiley & Sons
Original Publication: Eynsham, Oxon, UK : Oxford University Press, c1989- - MeSH Terms:
-
Brain/*metabolism
Energy Metabolism/*physiology
Insulin/*metabolism
Mitochondria/*metabolism
Animals ; Neurons/metabolism ; Signal Transduction/physiology - References:
-
Pocai A, Obici S, Schwartz GJ, Rossetti L. A brain-liver circuit regulates glucose homeostasis. Cell Metab. 2005;1:53-61.
Plum L, Schubert M, Bruning JC. The role of insulin receptor signaling in the brain. Trends Endocrinol Metab. 2005;16:59-65.
Kleinridders A, Ferris HA, Cai W, Kahn CR. Insulin action in brain regulates systemic metabolism and brain function. Diabetes. 2014;63:2232-2243.
Kullmann S, Kleinridders A, Small DM, et al. Central nervous pathways of insulin action in the control of metabolism and food intake. Lancet Diabetes Endocrinol. 2020;8:524-534.
Kleinridders A. Deciphering brain insulin receptor and insulin-like growth factor 1 receptor signalling. J Neuroendocrinol. 2016;28(11).
Boucher J, Kleinridders A, Kahn CR. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb Perspect Biol. 2014;6:a009191.
Contreras L, Drago I, Zampese E, Pozzan T. Mitochondria: the calcium connection. Biochim Biophys Acta. 2010;1797:607-618.
Wang C, Youle RJ. The role of mitochondria in apoptosis*. Annu Rev Genet. 2009;43:95-118.
Ebert D, Haller RG, Walton ME. Energy contribution of octanoate to intact rat brain metabolism measured by 13C nuclear magnetic resonance spectroscopy. J Neurosci. 2003;23:5928-5935.
Timper K, Paeger L, Sánchez-Lasheras C, et al. Mild impairment of mitochondrial OXPHOS promotes fatty acid utilization in POMC neurons and improves glucose homeostasis in obesity. Cell Rep. 2018;25:383-397 e10.
Andersson U, Filipsson K, Abbott CR, et al. AMP-activated protein kinase plays a role in the control of food intake. J Biol Chem. 2004;279:12005-12008.
Wu S-B, Wu Y-T, Wu T-P, Wei Y-H. Role of AMPK-mediated adaptive responses in human cells with mitochondrial dysfunction to oxidative stress. Biochim Biophys Acta. 2014;1840:1331-1344.
Domise M, Sauvé F, Didier S, et al. Neuronal AMP-activated protein kinase hyper-activation induces synaptic loss by an autophagy-mediated process. Cell Death Dis. 2019;10:221.
Minokoshi Y, Alquier T, Furukawa N, et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature. 2004;428:569-574.
Yavari A, Stocker CJ, Ghaffari S, et al. Chronic activation of gamma2 AMPK induces obesity and reduces beta cell function. Cell Metab. 2016;23:821-836.
Valentine RJ, Coughlan KA, Ruderman NB, Saha AK. Insulin inhibits AMPK activity and phosphorylates AMPK Ser(4)(8)(5)/(4)(9)(1) through Akt in hepatocytes, myotubes and incubated rat skeletal muscle. Arch Biochem Biophys. 2014;562:62-69.
Aghanoori M-R, Smith DR, Shariati-Ievari S, et al. Insulin-like growth factor-1 activates AMPK to augment mitochondrial function and correct neuronal metabolism in sensory neurons in type 1 diabetes. Mol Metab. 2019;20:149-165.
Aghanoori M-R, Smith DR, Chowdhury SR, Sabbir MG, Calcutt NA, Fernyhough P. Insulin prevents aberrant mitochondrial phenotype in sensory neurons of type 1 diabetic rats. Exp Neurol. 2017;297:148-157.
Ryan MT, Hoogenraad NJ. Mitochondrial-nuclear communications. Annu Rev Biochem. 2007;76:701-722.
Quiros PM, Mottis A, Auwerx J. Mitonuclear communication in homeostasis and stress. Nat Rev Mol Cell Biol. 2016;17:213-226.
Wardelmann K, et al. Insulin action in the brain regulates mitochondrial stress responses and reduces diet-induced weight gain. Mol Metab. 2019;21:68-81.
Fernandez-Marcos PJ, Auwerx J. Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr. 2011;93:884S-890S.
Wai T, Langer T. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab. 2016;27:105-117.
Santel A, Fuller MT. Control of mitochondrial morphology by a human mitofusin. J Cell Sci. 2001;114:867-874.
Kim SW, Lee JK. NO-induced downregulation of HSP10 and HSP60 expression in the postischemic brain. J Neurosci Res. 2007;85:1252-1259.
Frank M, et al. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta. 2012;1823:2297-2310.
Dietrich MO, Liu ZW, Horvath TL. Mitochondrial dynamics controlled by mitofusins regulate Agrp neuronal activity and diet-induced obesity. Cell. 2013;155:188-199.
Kitada T, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998;392:605-608.
Ye X, et al. Parkin-mediated mitophagy in mutant hAPP neurons and Alzheimer's disease patient brains. Hum Mol Genet. 2015;24:2938-2951.
Misgeld T, Schwarz TL. Mitostasis in neurons: maintaining mitochondria in an extended cellular architecture. Neuron. 2017;96:651-666.
Kleinridders A, et al. Leptin regulation of Hsp60 impacts hypothalamic insulin signaling. J Clin Invest. 2013;123:4667-4680.
Schneeberger M, et al. Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell. 2013;155:172-187.
Ruegsegger GN, et al. Exercise and metformin counteract altered mitochondrial function in the insulin-resistant brain. JCI Insight. 2019;4:e130681.
Schell M, et al. Interplay of dietary fatty acids and cholesterol impacts brain mitochondria and insulin action. Nutrients. 2020;12:1518.
He K, Aizenman E. ERK signaling leads to mitochondrial dysfunction in extracellular zinc-induced neurotoxicity. J Neurochem. 2010;114:452-461.
Yao J, et al. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci USA. 2009;106:14670-14675.
Talbot K, et al. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest. 2012;122:1316-1338.
Huang TJ, et al. Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes. 2003;52:2129-2136.
Ribeiro M, et al. Insulin and IGF-1 improve mitochondrial function in a PI-3K/Akt-dependent manner and reduce mitochondrial generation of reactive oxygen species in Huntington's disease knock-in striatal cells. Free Radic Biol Med. 2014;74:129-144.
Pang Y, et al. IGF-1 protects oligodendrocyte progenitors against TNFalpha-induced damage by activation of PI3K/Akt and interruption of the mitochondrial apoptotic pathway. Glia. 2007;55:1099-1107.
Chong ZZ, Li F, Maiese K. Activating Akt and the brain's resources to drive cellular survival and prevent inflammatory injury. Histol Histopathol. 2005;20:299-315.
Bijur GN, Jope RS. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J Neurochem. 2003;87:1427-1435.
Chen YH, et al. Mitochondrial Akt signaling modulated reprogramming of somatic cells. Sci Rep. 2019;9:9919.
Gazit N, et al. IGF-1 Receptor differentially regulates spontaneous and evoked transmission via mitochondria at hippocampal synapses. Neuron. 2016;89:583-597.
Born J, et al. Sniffing neuropeptides: a transnasal approach to the human brain. Nat Neurosci. 2002;5:514-516.
Schmid V, et al. Safety of intranasal human insulin: a review. Diabetes Obes Metab. 2018;20:1563-1577.
Jauch-Chara K, et al. Intranasal insulin suppresses food intake via enhancement of brain energy levels in humans. Diabetes. 2012;61:2261-2268.
Hallschmid M, et al. Intranasal insulin reduces body fat in men but not in women. Diabetes. 2004;53:3024-3029.
Benedict C, et al. Intranasal insulin improves memory in humans. Psychoneuroendocrinology. 2004;29:1326-1334.
Zhang Y, et al. Intranasal insulin prevents anesthesia-induced spatial learning and memory deficit in mice. Sci Rep. 2016;6:21186.
Guo Z, et al. Long-term treatment with intranasal insulin ameliorates cognitive impairment, tau hyperphosphorylation, and microglial activation in a streptozotocin-induced Alzheimer's rat model. Sci Rep. 2017;7:45971.
Johri A, Beal MF. Mitochondrial dysfunction in neurodegenerative diseases. J Pharmacol Exp Ther. 2012;342:619-630.
Ruegsegger GN, et al. Insulin deficiency and intranasal insulin alter brain mitochondrial function: a potential factor for dementia in diabetes. FASEB J. 2019;33:4458-4472.
Li H, et al. Intranasal administration of insulin reduces chronic behavioral abnormality and neuronal apoptosis induced by general anesthesia in neonatal mice. Front Neurosci. 2019;13:706.
Gabbouj S, et al. Intranasal insulin activates Akt2 signaling pathway in the hippocampus of wild-type but not in APP/PS1 Alzheimer model mice. Neurobiol Aging. 2019;75:98-108.
Konner AC, et al. Insulin action in AgRP-expressing neurons is required for suppression of hepatic glucose production. Cell Metab. 2007;5:438-449.
Klockener T, et al. High-fat feeding promotes obesity via insulin receptor/PI3K-dependent inhibition of SF-1 VMH neurons. Nat Neurosci. 2011;14:911-918.
Correia SC, et al. Mitochondrial abnormalities in a streptozotocin-induced rat model of sporadic Alzheimer's disease. Curr Alzheimer Res. 2013;10:406-419.
Schwartz MW, et al. Insulin in the brain: a hormonal regulator of energy balance. Endocr Rev. 1992;13:387-414.
Bruning JC, et al. Role of brain insulin receptor in control of body weight and reproduction. Science. 2000;289:2122-2125.
Kleinridders A, et al. Insulin resistance in brain alters dopamine turnover and causes behavioral disorders. Proc Natl Acad Sci USA. 2015;112:3463-3468.
George C, et al. The Alzheimer's disease transcriptome mimics the neuroprotective signature of IGF-1 receptor-deficient neurons. Brain. 2017;140:2012-2027.
Kappeler L, et al. Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol. 2008;6:e254.
Gontier G, et al. Blocking IGF signaling in adult neurons alleviates Alzheimer's disease pathology through amyloid-beta clearance. J Neurosci. 2015;35:11500-11513.
Sadagurski M, et al. IRS2 increases mitochondrial dysfunction and oxidative stress in a mouse model of Huntington disease. J Clin Invest. 2011;121:4070-4081.
Chong AC, et al. Central insulin signaling modulates hypothalamus-pituitary-adrenal axis responsiveness. Mol Metab. 2015;4:83-92.
Shin AC, et al. Insulin receptor signaling in POMC, but Not AgRP, neurons controls adipose tissue insulin action. Diabetes. 2017;66:1560-1571.
Loh K, et al. Insulin controls food intake and energy balance via NPY neurons. Mol Metab. 2017;6:574-584.
Konner AC, et al. Role for insulin signaling in catecholaminergic neurons in control of energy homeostasis. Cell Metab. 2011;13:720-728.
Cai W, et al. Insulin regulates astrocyte gliotransmission and modulates behavior. J Clin Invest. 2018;128:2914-2926.
Garcia-Caceres C, et al. Astrocytic insulin signaling couples brain glucose uptake with nutrient availability. Cell. 2016;166:867-880.
Logan S, et al. Insulin-like growth factor receptor signaling regulates working memory, mitochondrial metabolism, and amyloid-beta uptake in astrocytes. Mol Metab. 2018;9:141-155.
Ratcliffe LE, et al. Loss of IGF1R in human astrocytes alters complex I activity and support for neurons. Neuroscience. 2018;390:46-59.
Woods SC, Porte D Jr. Relationship between plasma and cerebrospinal fluid insulin levels of dogs. Am J Physiol. 1977;233:E331-E334.
Heni M, et al. Evidence for altered transport of insulin across the blood-brain barrier in insulin-resistant humans. Acta Diabetol. 2014;51:679-681.
Havrankova J, Roth J, Brownstein MJ. Concentrations of insulin and insulin receptors in the brain are independent of peripheral insulin levels. Studies of obese and streptozotocin-treated rodents. J Clin Invest. 1979;64:636-642.
Kaiyala KJ, et al. Obesity induced by a high-fat diet is associated with reduced brain insulin transport in dogs. Diabetes. 2000;49:1525-1533.
Kern W, et al. Low cerebrospinal fluid insulin levels in obese humans. Diabetologia. 2006;49:2790-2792.
Glombik K, et al. Brain metabolic alterations in rats showing depression-like and obesity phenotypes. Neurotox Res. 2020;37:406-424.
Chowdhury SK, et al. Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment. Diabetes. 2010;59:1082-1091.
Sakamoto Y, Kuzuya T, Yoshida H. Insulin content and insulin receptors in the rat brain (author's transl). Horumon to Rinsho. 1981;29:1047-1051.
Santos RX, et al. Insulin therapy modulates mitochondrial dynamics and biogenesis, autophagy and tau protein phosphorylation in the brain of type 1 diabetic rats. Biochim Biophys Acta. 2014;1842:1154-1166.
Pharaoh G, et al. Disparate central and peripheral effects of circulating IGF-1 deficiency on tissue mitochondrial function. Mol Neurobiol. 2020;57:1317-1331.
Pintana H, et al. Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci. 2012;91:409-414.
Pipatpiboon N, et al. PPARgamma agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term high-fat diets. Endocrinology. 2012;153:329-338.
Sa-Nguanmoo P, et al. SGLT2-inhibitor and DPP-4 inhibitor improve brain function via attenuating mitochondrial dysfunction, insulin resistance, inflammation, and apoptosis in HFD-induced obese rats. Toxicol Appl Pharmacol. 2017;333:43-50.
Pintana H, et al. DPP-4 inhibitors improve cognition and brain mitochondrial function of insulin-resistant rats. J Endocrinol. 2013;218:1-11.
Pipatpiboon N, et al. DPP4-inhibitor improves neuronal insulin receptor function, brain mitochondrial function and cognitive function in rats with insulin resistance induced by high-fat diet consumption. Eur J Neurosci. 2013;37:839-849.
Marques-Neto SR, et al. Effects of incretin-based therapies on neuro-cardiovascular dynamic changes induced by high fat diet in rats. PLoS One. 2016;11:e0148402.
Sa-Nguanmoo P, et al. FGF21 improves cognition by restored synaptic plasticity, dendritic spine density, brain mitochondrial function and cell apoptosis in obese-insulin resistant male rats. Horm Behav. 2016;85:86-95.
Sarruf DA, et al. Fibroblast growth factor 21 action in the brain increases energy expenditure and insulin sensitivity in obese rats. Diabetes. 2010;59:1817-1824.
Murphy CT, Hu PJ. Insulin/insulin-like growth factor signaling in C elegans. WormBook. 2013;1-43. https://doi.org/10.1895/wormbook.1.164.1.
Billing O, Kao G, Naredi X. Mitochondrial function is required for secretion of DAF-28/insulin in C elegans. PLoS One. 2011;6:e14507.
Halaschek-Wiener J, et al. Analysis of long-lived C elegans daf-2 mutants using serial analysis of gene expression. Genome Res. 2005;15:603-615.
Gami MS, Wolkow CA. Studies of Caenorhabditis elegans DAF-2/insulin signaling reveal targets for pharmacological manipulation of lifespan. Aging Cell. 2006;5:31-37.
Azpurua J, et al. IGF1R levels in the brain negatively correlate with longevity in 16 rodent species. Aging. 2013;5:304-314.
Holzenberger M, et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature. 2003;421:182-187.
Durieux J, Wolff S, Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell. 2011;144:79-91.
Salway KD, et al. Higher levels of heat shock proteins in longer-lived mammals and birds. Mech Ageing Dev. 2011;132:287-297.
Gatsi R, et al. Prohibitin-mediated lifespan and mitochondrial stress implicate SGK-1, insulin/IGF and mTORC2 in C elegans. PLoS One. 2014;9:e107671.
Intine RV, Olsen AS, Sarras M Jr. A zebrafish model of diabetes mellitus and metabolic memory. J Vis Exp. 2013;72:e50232.
Moss JB, et al. Regeneration of the pancreas in adult zebrafish. Diabetes. 2009;58:1844-1851.
Meng XH, Chen B, Zhang J. Intracellular insulin and impaired autophagy in a zebrafish model and a cell model of type 2 diabetes. Int J Biol Sci. 2017;13:985-995.
Beshel J, Dubnau J, Zhong Y. A leptin analog locally produced in the brain acts via a conserved neural circuit to modulate obesity-linked behaviors in Drosophila. Cell Metab. 2017;25:208-217.
Brent AE, Rajan A. Insulin and leptin/Upd2 exert opposing influences on synapse number in fat-sensing neurons. Cell Metab. 2020;32:786-800.
Huang Y, et al. Insulin signaling in Drosophila melanogaster mediates Abeta toxicity. Commun Biol. 2019;2:13.
Smit AB, et al. Growth-controlling molluscan neurons produce the precursor of an insulin-related peptide. Nature. 1988;331:535-538.
Kits KS, de Vries NJ, Ebberink RH. Molluscan insulin-related neuropeptide promotes neurite outgrowth in dissociated neuronal cell cultures. Neurosci Lett. 1990;109:253-258.
Murakami J, et al. Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis. J Neurosci. 2013;33:371-383.
Bergmann F, Keller BU. Impact of mitochondrial inhibition on excitability and cytosolic Ca2+ levels in brainstem motoneurones from mouse. J Physiol. 2004;555:45-59.
Kreutzer C, et al. Hypothalamic inflammation in human obesity is mediated by environmental and genetic factors. Diabetes. 2017;66:2407-2415.
Yeo GS, et al. A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat Genet. 1998;20:111-112.
Timpson NJ, et al. The fat mass- and obesity-associated locus and dietary intake in children. Am J Clin Nutr. 2008;88:971-978.
Cecil JE, et al. An obesity-associated FTO gene variant and increased energy intake in children. N Engl J Med. 2008;359:2558-2566.
Al-Serri A, Alroughani R, Al-Temaimi RA. The FTO gene polymorphism rs9939609 is associated with obesity and disability in multiple sclerosis patients. Sci Rep. 2019;9:19071.
Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111-1119.
Little JP, et al. Mitochondrial transcription factor A (Tfam) is a pro-inflammatory extracellular signaling molecule recognized by brain microglia. Mol Cell Neurosci. 2014;60:88-96.
Alcantar-Fernandez J, et al. High-glucose diets induce mitochondrial dysfunction in Caenorhabditis elegans. PLoS One. 2019;14:e0226652.
Peng Y, et al. Mitochondrial dysfunction precedes depression of AMPK/AKT signaling in insulin resistance induced by high glucose in primary cortical neurons. J Neurochem. 2016;137:701-713.
Rom S, et al. Hyperglycemia-driven neuroinflammation compromises BBB leading to memory loss in both diabetes mellitus (DM) type 1 and type 2 mouse models. Mol Neurobiol. 2019;56:1883-1896.
Mayer CM, Belsham DD. Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 5' monophosphate-activated protein kinase activation. Endocrinology. 2010;151:576-585.
Thaler JP, et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest. 2012;122:153-162.
Chambers JW, LoGrasso PV. Mitochondrial c-Jun N-terminal kinase (JNK) signaling initiates physiological changes resulting in amplification of reactive oxygen species generation. J Biol Chem. 2011;286:16052-16062.
Schriever S. Type 2 diabetes risk gene Dusp8 regulates hypothalamic Jnk signaling and insulin sensitivity. J Clin Invest. 2020;130:6093-6108.
Arnold SE, et al. High fat diet produces brain insulin resistance, synaptodendritic abnormalities and altered behavior in mice. Neurobiol Dis. 2014;67:79-87.
Sripetchwandee J, Chattipakorn N, Chattipakorn SC. Links between obesity-induced brain insulin resistance, brain mitochondrial dysfunction, and dementia. Front Endocrinol. 2018;9:496.
Cavaliere G, et al. High-fat diet induces neuroinflammation and mitochondrial impairment in mice cerebral cortex and synaptic fraction. Front Cell Neurosci. 2019;13:509.
Egea J, et al. European contribution to the study of ROS: A summary of the findings and prospects for the future from the COST action BM1203 (EU-ROS). Redox Biol. 2017;13:94-162.
Pinti MV, et al. Mitochondrial dysfunction in type 2 diabetes mellitus: an organ-based analysis. Am J Physiol Endocrinol Metab. 2019;316:E268-E285.
Heni M, et al. Central insulin administration improves whole-body insulin sensitivity via hypothalamus and parasympathetic outputs in men. Diabetes. 2014;63:4083-4088.
Szego EM, et al. Cytosolic trapping of a mitochondrial heat shock protein is an early pathological event in synucleinopathies. Cell Rep. 2019;28:65-77 e6.
Castro JP, et al. Mitochondrial chaperones in the brain: safeguarding brain health and metabolism? Front Endocrinol. 2018;9:196. - Contributed Indexing:
- Keywords: brain; energy homeostasis; inflammation; insulin signalling; metabolism; mitochondrial function
- Substance Nomenclature:
- 0 (Insulin)
- Entry Date(s):
- Date Created: 20210128 Date Completed: 20211203 Latest Revision: 20211214
- Update Code:
- 20240105
- DOI:
- 10.1111/jne.12932
- PMID:
- 33506556
- Czasopismo naukowe
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