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Abstract:

Leptin is an adipose-derived hormone that controls appetite and energy expenditure. Leptin receptors are expressed on extra-hypothalamic ventrobasal (VB) and reticular thalamic (RTN) nuclei from embryonic stages. Here, we studied the effects of pressure-puff, local application of leptin on both synaptic transmission and action potential properties of thalamic neurons in thalamocortical slices. We used whole-cell patch-clamp recordings of thalamocortical VB neurons from wild-type (WT) and leptin-deficient obese (ob/ob) mice. We observed differences in VB neurons action potentials and synaptic currents kinetics when comparing WT vs. ob/ob. Leptin reduced GABA release onto VB neurons throughout the activation of a JAK2-dependent pathway, without affecting excitatory glutamate transmission. We observed a rapid and reversible reduction by leptin of the number of action potentials of VB neurons via the activation of large conductance Ca 2+ -dependent potassium channels. These leptin effects were observed in thalamocortical slices from up to 5-week-old WT but not in leptin-deficient obese mice. Results described here suggest the existence of a leptin-mediated trophic modulation of thalamocortical excitability during postnatal development. These findings could contribute to a better understanding of leptin within the thalamocortical system and sleep deficits in obesity. © 2018, Springer-Verlag GmbH Germany, part of Springer Nature.

Registro:

Documento: Artículo
Título:Leptin alters somatosensory thalamic networks by decreasing gaba release from reticular thalamic nucleus and action potential frequency at ventrobasal neurons
Autor:Perissinotti, P.P.; Rivero-Echeto, M.C.; Garcia-Rill, E.; Bisagno, V.; Urbano, F.J.
Filiación:Departamento de Fisiología, Facultad de Ciencias Exactas y Naturales, Biología Molecular y Celular “Dr. Héctor Maldonado”, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, Ciudad Autónoma de Buenos Aires, C1428EGA, Argentina
Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Instituto de Investigaciones Farmacológicas (ININFA), CONICET-Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Department of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, AR, United States
Palabras clave:GABA; Leptin; Mouse; ob/ob; Thalamic reticular nucleus; 4 aminobutyric acid; calcium activated potassium channel; glutamic acid; Janus kinase 2; leptin; recombinant leptin; 4 aminobutyric acid; 6 cyano 7 nitro 2,3 quinoxalinedione; alpha-cyano-(3,4-dihydroxy)-N-benzylcinnamide; amino acid receptor blocking agent; enzyme inhibitor; Jak2 protein, mouse; Janus kinase 2; leptin; sodium channel blocking agent; tetrodotoxin; tyrphostin; 4 aminobutyric acid release; action potential; animal experiment; animal tissue; Article; brain slice; controlled study; GABAergic transmission; glutamatergic synapse; male; mouse; nerve excitability; neuromodulation; nonhuman; obesity; priority journal; synaptic transmission; thalamus reticular nucleus; thalamus ventral nucleus; whole cell patch clamp; animal; body temperature; C57BL mouse; cytology; deficiency; drug effect; genetics; metabolism; nerve cell; physiology; signal transduction; synaptic potential; thalamus nucleus; transgenic mouse; 6-Cyano-7-nitroquinoxaline-2,3-dione; Action Potentials; Animals; Body Temperature; Enzyme Inhibitors; Excitatory Amino Acid Antagonists; gamma-Aminobutyric Acid; Janus Kinase 2; Leptin; Male; Mice; Mice, Inbred C57BL; Mice, Transgenic; Neurons; Signal Transduction; Sodium Channel Blockers; Synaptic Potentials; Synaptic Transmission; Tetrodotoxin; Thalamic Nuclei; Tyrphostins
Año:2018
Volumen:223
Número:5
Página de inicio:2499
Página de fin:2514
DOI: http://dx.doi.org/10.1007/s00429-018-1645-x
Título revista:Brain Structure and Function
Título revista abreviado:Brain Struct. Funct.
ISSN:18632653
CAS:4 aminobutyric acid, 28805-76-7, 56-12-2; glutamic acid, 11070-68-1, 138-15-8, 56-86-0, 6899-05-4; 6 cyano 7 nitro 2,3 quinoxalinedione, 115066-14-3; tetrodotoxin, 4368-28-9, 4664-41-9; 6-Cyano-7-nitroquinoxaline-2,3-dione; alpha-cyano-(3,4-dihydroxy)-N-benzylcinnamide; Enzyme Inhibitors; Excitatory Amino Acid Antagonists; gamma-Aminobutyric Acid; Jak2 protein, mouse; Janus Kinase 2; Leptin; Sodium Channel Blockers; Tetrodotoxin; Tyrphostins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_18632653_v223_n5_p2499_Perissinotti

Referencias:

  • Ahima, R.S., Flier, J.S., Leptin (2000) Annu Rev Physiol, 62, pp. 413-437
  • Ahima, R.S., Prabakaran, D., Flier, J.S., Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function (1998) J Clin Inves, 101, pp. 1020-1027
  • Ahima, R.S., Bjorbaek, C., Osei, S., Flier, J.S., Regulation of neuronal and glial proteins by leptin: implications for. brain development (1999) Endocrinology, 140, pp. 2755-2762
  • Banks, W.A., Kastin, A.J., Huang, W., Jaspan, J.B., Maness, L.M., Leptin enters the brain by a saturable system independent of insulin (1996) Peptides, 17, pp. 305-311. , PID: 8801538
  • Baquero, A.F., de Solis, A.J., Developmental switch of leptin signaling in arcuate nucleus neurons (2014) J Neurosci, 34, pp. 9982-9994
  • Beck, P., Mahaffey, S., Urbano, F.J., Garcia-Rill, E., Role of G-proteins in the effects of leptin on pedunculopontine nucleus neurons (2013) J Neurochem, 126, pp. 705-714
  • Beck, P., Urbano, F.J., Williams, D.K., Garcia-Rill, E., Effects of leptin on pedunculopontine nucleus (PPN) neurons (2013) J Neural Transm, 120, pp. 1027-1038
  • Bereiter, D.A., Jeanrenaud, B., Altered neuroanatomical organization in the central nervous system of the genetically obese (ob/ob) mouse (1979) Brain Res, 165, pp. 249-260. , PID: 421139
  • Beretta, M., Bauer, M., Hirsch, E., PI3K signaling in the pathogenesis of obesity: the cause and the cure (2015) Adv Biol Regul, 58, pp. 1-15
  • Biella, G., Meis, S., Pape, H.-C., Modulation of a Ca2+-dependent K+-current by intracellular cAMP. in rat thalamocortical relay neurons (2001) Thalamus Relat Syst, 1, pp. 157-167
  • Bisagno, V., Raineri, M., Peskin, V., Wikinski, S.I., Uchitel, O.D., Llinas, R.R., Urbano, F.J., Effects of T-type calcium channel blockers on cocaine-induced hyperlocomotion and thalamocortical GABAergic abnormalities in mice (2010) Psychopharmacology, 212, pp. 205-214
  • Bouret, S.G., Draper, S.J., Simerly, R.B., Trophic action of leptin on hypothalamic neurons that regulate feeding (2004) Science, 304, pp. 108-110
  • Castro-Alamancos, M.A., Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs (2002) J Neurophysiol, 87, pp. 946-953. , PID: 11826059
  • Crandall, S.R., Cruikshank, S.J., Connors, B.W., A corticothalamic switch: controlling the thalamus with dynamic synapses (2015) Neuron, 86, pp. 768-782
  • Crick, F., Function of the thalamic reticular complex: the searchlight hypothesis (1984) Proc Natl Acad Sci USA, 81, pp. 4586-4590. , PID: 6589612
  • De Biasi, S., Amadeo, A., Arcelli, P., Frassoni, C., Spreafico, R., Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: a light and electron microscopic study (1997) Neuroscience, 76, pp. 503-515. , PID: 9015334
  • Dixon, J.B., Dixon, M.E., Anderson, M.L., Schachter, L., O’Brien, P.E., Daytime sleepiness in the obese: not as simple as obstructive sleep apnea (2007) Obesity (Silver Spring), 15, pp. 2504-2511
  • Durakoglugil, M., Irving, A.J., Harvey, J., Leptin induces a novel form of NMDA receptor-dependent long-term depression (2005) J Neurochem, 95, pp. 396-405
  • Ehling, P., Cerina, M., Meuth, P., Kanyshkova, T., Bista, P., Coulon, P., Meuth, S.G., Budde, T., Ca(2+)-dependent large conductance K(+) currents in thalamocortical relay neurons of different rat strains (2013) Pflugers Arch, 465, pp. 469-480
  • Elmquist, J.K., Bjorbaek, C., Ahima, R.S., Flier, J.S., Saper, C.B., Distributions of leptin receptor mRNA isoforms in the rat brain (1998) J Comp Neurol, 395, pp. 535-547. , PID: 9619505
  • Finocchietto, P.V., Holod, S., Barreyro, F., Peralta, J.G., Alippe, Y., Giovambattista, A., Carreras, M.C., Poderoso, J.J., Defective leptin-AMP-dependent kinase pathway induces nitric oxide release and contributes to mitochondrial dysfunction and obesity in ob/ob mice (2011) Antioxid Redox Signal, 15, pp. 2395-2406
  • Gambarana, C., Beattie, C.E., Rodriguez, Z.R., Siegel, R.E., Region-specific expression of messenger RNAs encoding GABAA receptor subunits in the developing rat brain (1991) Neuroscience, 45, pp. 423-432. , PID: 1662337
  • Goitia, B., Raineri, M., Gonzalez, L.E., Rozas, J.L., Garcia-Rill, E., Bisagno, V., Urbano, F.J., Differential effects of methylphenidate and cocaine on GABA transmission in sensory thalamic nuclei (2013) J Neurochem, 124, pp. 602-612
  • Goitia, B., Rivero-Echeto, M.C., Weisstaub, N.V., Gingrich, J.A., Garcia-Rill, E., Bisagno, V., Urbano, F.J., Modulation of GABA release from the thalamic reticular nucleus by cocaine and caffeine: role of serotonin receptors (2016) J Neurochem, 136, pp. 526-535
  • Gonzalez, B., Gonzalez, C., Bisagno, V., Urbano, F.J., Effects of methamphetamine on locomotor activity and thalamic gene expression in leptin-deficient obese mice (2017) Trans Brain Rhyth, 2, pp. 1-6
  • Guillery, R.W., Feig, S.L., Lozsadi, D.A., Paying attention to the thalamic reticular nucleus (1998) Trends Neurosci, 21, pp. 28-32. , PID: 9464683
  • Hallanger, A.E., Levey, A.I., Lee, H.J., Rye, D.B., Wainer, B.H., The origins of cholinergic and other subcortical afferents to the thalamus in the rat (1987) J Comp Neurol, 262, pp. 105-124
  • Huntsman, M.M., Huguenard, J.R., Nucleus-specific differences in GABA(A)-receptor-mediated inhibition are enhanced during thalamic development (2000) J Neurophysiol, 83, pp. 350-358. , PID: 10634878
  • Ihle, J.N., Cytokine receptor signalling (1995) Nature, 377, pp. 591-594
  • Kitamura, T., Feng, Y., Kitamura, Y.I., Chua, S.C., Jr., Xu, A.W., Barsh, G.S., Rossetti, L., Accili, D., Forkhead protein FoxO1 mediates Agrp-dependent effects of leptin on food intake (2006) Nat Med, 12, pp. 534-540
  • Kurrimbux, D., Gaffen, Z., Farrell, C.L., Martin, D., Thomas, S.A., The involvement of the blood-brain and the blood-cerebrospinal fluid barriers in the distribution of leptin into and out of the rat brain (2004) Neuroscience, 123, pp. 527-536. , PID: 14698759
  • Laposky, A.D., Shelton, J., Bass, J., Dugovic, C., Perrino, N., Turek, F.W., Altered sleep regulation in leptin-deficient mice (2006) Am J Physiol Regul Integr Comp Physiol, 290
  • Laposky, A.D., Bradley, M.A., Williams, D.L., Bass, J., Turek, F.W., Sleep-wake regulation is altered in leptin-resistant (db/db) genetically obese and diabetic mice (2008) Am J Physiol Regul Integr Comp Physiol, 295
  • Laurie, D.J., Wisden, W., Seeburg, P.H., The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development (1992) J Neurosci, 12, pp. 4151-4172. , PID: 1331359
  • Lhuillier, L., Dryer, S.E., Developmental regulation of neuronal K(Ca) channels by TGFbeta1: an essential role for PI3 kinase signaling and membrane insertion (2002) J Neurophysiol, 88, pp. 954-964. , PID: 12163544
  • Liu, X.B., Warren, R.A., Jones, E.G., Synaptic distribution of afferents from reticular nucleus in ventroposterior nucleus of cat thalamus (1995) J Comp Neurol, 352, pp. 187-202
  • Liu, J.J., Bello, N.T., Pang, Z.P., Pre-synaptic regulation of leptin in a defined lateral hypothalamus ventral tegmental area neurocircuitry depends on energy state (2017) J Neurosci
  • Macdonald, R.L., Olsen, R.W., GABAA receptor channels (1994) Ann Rev Neurosci, 17, pp. 569-602
  • Matsuda, J., Yokota, I., Tsuruo, Y., Murakami, T., Ishimura, K., Shima, K., Kuroda, Y., Development changes in long-form leptin receptor expression and localization in rat brain (1999) Endocrinology, 140, pp. 5233-5238
  • Mistry, A.M., Swick, A., Romsos, D.R., Leptin alters metabolic rates before acquisition of its anorectic effect in developing neonatal mice (1999) Am J Physiol, 277, p. R742R747
  • Pangratz-Fuehrer, S., Sieghart, W., Rudolph, U., Parada, I., Huguenard, J.R., Early postnatal switch in GABAA receptor alpha-subunits in the reticular thalamic nucleus (2016) J Neurophysiol, 115, pp. 1183-1195
  • Pelleymounter, M.A., Cullen, M.J., Baker, M.B., Hecht, R., Winters, D., Boone, T., Collins, F., Effects of the obese gene product on body weight regulation in ob/ob mice (1995) Science, 269, pp. 540-543. , PID: 7624776
  • Pinault, D., The thalamic reticular nucleus: structure, function and concept Brain research (2004) Brain Res Rev, 46, pp. 1-31
  • Poulter, M.O., Barker, J.L., O’Carroll, A.M., Lolait, S.J., Mahan, L.C., Differential and transient expression of GABAA receptor alpha-subunit mRNAs in the developing rat CNS (1992) J Neurosci, 12, pp. 2888-2900. , PID: 1322978
  • Qiu, J., Fang, Y., Ronnekleiv, O.K., Kelly, M.J., Leptin excites proopiomelanocortin neurons via activation of TRPC channels (2010) J Neurosci, 30, pp. 1560-1565
  • Sahu, A., Leptin signaling in the hypothalamus: emphasis on energy homeostasis and leptin resistance (2003) Front Neuroendocrinol, 24, pp. 225-253. , PID: 14726256
  • Sena, A., Sarlieve, L.L., Rebel, G., Brain myelin of genetically obese mice (1985) J Neurol Sci, 68, pp. 233-243. , PID: 2989440
  • Shanley, L.J., Irving, A.J., Rae, M.G., Ashford, M.L., Harvey, J., Leptin inhibits rat hippocampal neurons via activation of large conductance calcium-activated K + channels (2002) Nat Neurosci, 5, pp. 299-300
  • Shouse, M.N., Siegel, J.M., Pontine regulation of REM sleep components in cats: integrity of the pedunculopontine tegmentum (PPT) is important for phasic events but unnecessary for atonia during REM sleep (1992) Brain res, 571, pp. 50-63. , PID: 1611494
  • Sinton, C.M., Fitch, T.E., Gershenfeld, H.K., The effects of leptin on REM sleep and slow wave delta in rats are reversed by food deprivation (1999) J Sleep Res, 8, pp. 197-203. , PID: 10476006
  • Solovyova, N., Moult, P.R., Milojkovic, B., Lambert, J.J., Harvey, J., Bi-directional modulation of fast inhibitory synaptic transmission by leptin (2009) J Neurochem, 108, pp. 190-201
  • Spanswick, D., Smith, M.A., Groppi, V.E., Logan, S.D., Ashford, M.L., Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels (1997) Nature, 390, pp. 521-525
  • Steppan, C.M., Swick, A.G., A role for leptin in brain development (1999) Biochem Biophys Res Comm, 256, pp. 600-602
  • Steriade, M., Llinas, R.R., The functional states of the thalamus and the associated neuronal interplay (1988) Physiol Rev, 68, pp. 649-742. , PID: 2839857
  • Steriade, M., Datta, S., Pare, D., Oakson, G., Curro Dossi, R.C., Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems (1990) J Neurosci, 10, pp. 2541-2559. , PID: 2388079
  • Thompson, J.L., Borgland, S.L., Presynaptic leptin action suppresses excitatory synaptic transmission onto ventral tegmental area dopamine neurons (2013) Biol Psych, 73, pp. 860-868
  • Udagawa, J., Hatta, T., Naora, H., Otani, H., Expression of the long form of leptin receptor (Ob-Rb) mRNA in the brain of mouse embryos and newborn mice (2000) Brain Res, 868, pp. 251-258. , PID: 10854577
  • Urbano, F.J., Bisagno, V., Wikinski, S.I., Uchitel, O.D., Llinas, R.R., Cocaine acute “binge” administration results in altered thalamocortical interactions in mice (2009) Biol Psych, 66, pp. 769-776
  • van den Top, M., Lee, K., Whyment, A.D., Blanks, A.M., Spanswick, D., Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus (2004) Nat Neurosci, 7, pp. 493-494
  • Vgontzas, A.N., Bixler, E.O., Tan, T.L., Kantner, D., Martin, L.F., Kales, A., Obesity without sleep apnea is associated with daytime sleepiness (1998) Arch Intern Med, 158, pp. 1333-1337. , PID: 9645828
  • Vong, L., Ye, C., Yang, Z., Choi, B., Chua, S., Jr., Lowell, B.B., Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons (2011) Neuron, 71, pp. 142-154
  • Warren, R.A., Agmon, A., Jones, E.G., Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro (1994) J Neurophysiol, 72, pp. 1993-2003. , PID: 7823113
  • Wayner, M.J., Armstrong, D.L., Phelix, C.F., Oomura, Y., Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo (2004) Peptides, 25, pp. 991-996
  • Yingling, C.D., Skinner, J.E., Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami (1976) Electroencephalogr Clin Neurophysiol, 41, pp. 476-482. , PID: 61851
  • Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., Friedman, J.M., Positional cloning of the mouse obese gene and its human homologue (1994) Nature, 372, pp. 425-432
  • Zhang, S.J., Huguenard, J.R., Prince, D.A., GABAA receptor-mediated Cl-currents in rat thalamic reticular and relay neurons (1997) J Neurophysiol, 78, pp. 2280-2286. , PID: 9356381
  • Zucker, R.S., Short-term synaptic plasticity (1989) Ann Rev Neurosci, 12, pp. 13-31

Citas:

---------- APA ----------
Perissinotti, P.P., Rivero-Echeto, M.C., Garcia-Rill, E., Bisagno, V. & Urbano, F.J. (2018) . Leptin alters somatosensory thalamic networks by decreasing gaba release from reticular thalamic nucleus and action potential frequency at ventrobasal neurons. Brain Structure and Function, 223(5), 2499-2514.
http://dx.doi.org/10.1007/s00429-018-1645-x
---------- CHICAGO ----------
Perissinotti, P.P., Rivero-Echeto, M.C., Garcia-Rill, E., Bisagno, V., Urbano, F.J. "Leptin alters somatosensory thalamic networks by decreasing gaba release from reticular thalamic nucleus and action potential frequency at ventrobasal neurons" . Brain Structure and Function 223, no. 5 (2018) : 2499-2514.
http://dx.doi.org/10.1007/s00429-018-1645-x
---------- MLA ----------
Perissinotti, P.P., Rivero-Echeto, M.C., Garcia-Rill, E., Bisagno, V., Urbano, F.J. "Leptin alters somatosensory thalamic networks by decreasing gaba release from reticular thalamic nucleus and action potential frequency at ventrobasal neurons" . Brain Structure and Function, vol. 223, no. 5, 2018, pp. 2499-2514.
http://dx.doi.org/10.1007/s00429-018-1645-x
---------- VANCOUVER ----------
Perissinotti, P.P., Rivero-Echeto, M.C., Garcia-Rill, E., Bisagno, V., Urbano, F.J. Leptin alters somatosensory thalamic networks by decreasing gaba release from reticular thalamic nucleus and action potential frequency at ventrobasal neurons. Brain Struct. Funct. 2018;223(5):2499-2514.
http://dx.doi.org/10.1007/s00429-018-1645-x