Literature DB >> 27093227

Optogenetic Stimulation of Arcuate Nucleus Kiss1 Neurons Reveals a Steroid-Dependent Glutamatergic Input to POMC and AgRP Neurons in Male Mice.

Casey C Nestor1, Jian Qiu1, Stephanie L Padilla1, Chunguang Zhang1, Martha A Bosch1, Wei Fan1, Sue A Aicher1, Richard D Palmiter1, Oline K Rønnekleiv1, Martin J Kelly1.   

Abstract

Kisspeptin (Kiss1) neurons are essential for reproduction, but their role in the control of energy balance and other homeostatic functions remains unclear. Proopiomelanocortin (POMC) and agouti-related peptide (AgRP) neurons, located in the arcuate nucleus (ARC) of the hypothalamus, integrate numerous excitatory and inhibitory inputs to ultimately regulate energy homeostasis. Given that POMC and AgRP neurons are contacted by Kiss1 neurons in the ARC (Kiss1(ARC)) and they express androgen receptors, Kiss1(ARC) neurons may mediate the orexigenic action of testosterone via POMC and/or AgRP neurons. Quantitative PCR analysis of pooled Kiss1(ARC) neurons revealed that mRNA levels for Kiss1 and vesicular glutamate transporter 2 were higher in castrated male mice compared with gonad-intact males. Single-cell RT-PCR analysis of yellow fluorescent protein (YFP) ARC neurons harvested from males injected with AAV1-EF1α-DIO-ChR2:YFP revealed that 100% and 88% expressed mRNAs for Kiss1 and vesicular glutamate transporter 2, respectively. Whole-cell, voltage-clamp recordings from nonfluorescent postsynaptic ARC neurons showed that low frequency photo-stimulation (0.5 Hz) of Kiss1-ChR2:YFP neurons elicited a fast glutamatergic inward current in POMC and AgRP neurons. Paired-pulse, photo-stimulation revealed paired-pulse depression, which is indicative of greater glutamate release, in the castrated male mice compared with gonad-intact male mice. Group I and group II metabotropic glutamate receptor agonists depolarized and hyperpolarized POMC and AgRP neurons, respectively, which was mimicked by high frequency photo-stimulation (20 Hz) of Kiss1(ARC) neurons. Therefore, POMC and AgRP neurons receive direct steroid- and frequency-dependent glutamatergic synaptic input from Kiss1(ARC) neurons in male mice, which may be a critical pathway for Kiss1 neurons to help coordinate energy homeostasis and reproduction.

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Year:  2016        PMID: 27093227      PMCID: PMC4884339          DOI: 10.1210/me.2016-1026

Source DB:  PubMed          Journal:  Mol Endocrinol        ISSN: 0888-8809


  80 in total

1.  Characterization of Kiss1 neurons using transgenic mouse models.

Authors:  R M Cravo; L O Margatho; S Osborne-Lawrence; J Donato; S Atkin; A L Bookout; S Rovinsky; R Frazão; C E Lee; L Gautron; J M Zigman; C F Elias
Journal:  Neuroscience       Date:  2010-11-18       Impact factor: 3.590

2.  Selective control of cortical axonal spikes by a slowly inactivating K+ current.

Authors:  Yousheng Shu; Yuguo Yu; Jing Yang; David A McCormick
Journal:  Proc Natl Acad Sci U S A       Date:  2007-06-20       Impact factor: 11.205

3.  Conditional Viral Tract Tracing Delineates the Projections of the Distinct Kisspeptin Neuron Populations to Gonadotropin-Releasing Hormone (GnRH) Neurons in the Mouse.

Authors:  Siew Hoong Yip; Ulrich Boehm; Allan E Herbison; Rebecca E Campbell
Journal:  Endocrinology       Date:  2015-04-09       Impact factor: 4.736

4.  Topographic mapping of VMH --> arcuate nucleus microcircuits and their reorganization by fasting.

Authors:  Scott M Sternson; Gordon M G Shepherd; Jeffrey M Friedman
Journal:  Nat Neurosci       Date:  2005-09-18       Impact factor: 24.884

5.  Role of protein kinase C in facilitation of luteinizing hormone (LH)-releasing hormone-induced LH surges by neuropeptide Y.

Authors:  S M Leupen; J E Levine
Journal:  Endocrinology       Date:  1999-08       Impact factor: 4.736

6.  Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area.

Authors:  C F Elias; C Aschkenasi; C Lee; J Kelly; R S Ahima; C Bjorbaek; J S Flier; C B Saper; J K Elmquist
Journal:  Neuron       Date:  1999-08       Impact factor: 17.173

7.  Role for kisspeptin/neurokinin B/dynorphin (KNDy) neurons in cutaneous vasodilatation and the estrogen modulation of body temperature.

Authors:  Melinda A Mittelman-Smith; Hemalini Williams; Sally J Krajewski-Hall; Nathaniel T McMullen; Naomi E Rance
Journal:  Proc Natl Acad Sci U S A       Date:  2012-11-12       Impact factor: 11.205

8.  Neuromedin B and gastrin-releasing peptide excite arcuate nucleus neuropeptide Y neurons in a novel transgenic mouse expressing strong Renilla green fluorescent protein in NPY neurons.

Authors:  Anthony N van den Pol; Yang Yao; Li-Ying Fu; Kylie Foo; Hao Huang; Roberto Coppari; Bradford B Lowell; Christian Broberger
Journal:  J Neurosci       Date:  2009-04-08       Impact factor: 6.167

9.  Glutamate, the dominant excitatory transmitter in neuroendocrine regulation.

Authors:  A N van den Pol; J P Wuarin; F E Dudek
Journal:  Science       Date:  1990-11-30       Impact factor: 47.728

10.  Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state.

Authors:  Stephanie L Padilla; Jian Qiu; Marta E Soden; Elisenda Sanz; Casey C Nestor; Forrest D Barker; Albert Quintana; Larry S Zweifel; Oline K Rønnekleiv; Martin J Kelly; Richard D Palmiter
Journal:  Nat Neurosci       Date:  2016-03-28       Impact factor: 24.884

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  36 in total

Review 1.  Diverse actions of estradiol on anorexigenic and orexigenic hypothalamic arcuate neurons.

Authors:  Todd L Stincic; Oline K Rønnekleiv; Martin J Kelly
Journal:  Horm Behav       Date:  2018-04-21       Impact factor: 3.587

2.  Kisspeptin Neurons in the Arcuate Nucleus of the Hypothalamus Orchestrate Circadian Rhythms and Metabolism.

Authors:  Stephanie L Padilla; Jazmine G Perez; Miriam Ben-Hamo; Christopher W Johnson; Raymond E A Sanchez; Ivana L Bussi; Richard D Palmiter; Horacio O de la Iglesia
Journal:  Curr Biol       Date:  2019-02-07       Impact factor: 10.834

Review 3.  Modulation of Feeding and Associated Behaviors by Lateral Hypothalamic Circuits.

Authors:  Emily Qualls-Creekmore; Heike Münzberg
Journal:  Endocrinology       Date:  2018-11-01       Impact factor: 4.736

4.  17β-Estradiol Increases Arcuate KNDy Neuronal Sensitivity to Ghrelin Inhibition of the M-Current in Female Mice.

Authors:  Kristie Conde; Troy A Roepke
Journal:  Neuroendocrinology       Date:  2019-09-05       Impact factor: 4.914

5.  Estradiol Protects Proopiomelanocortin Neurons Against Insulin Resistance.

Authors:  Jian Qiu; Martha A Bosch; Cecilia Meza; Uyen-Vy Navarro; Casey C Nestor; Edward J Wagner; Oline K Rønnekleiv; Martin J Kelly
Journal:  Endocrinology       Date:  2018-02-01       Impact factor: 4.736

6.  Obese Neuronal PPARγ Knockout Mice Are Leptin Sensitive but Show Impaired Glucose Tolerance and Fertility.

Authors:  Marina O Fernandez; Shweta Sharma; Sun Kim; Emily Rickert; Katherine Hsueh; Vicky Hwang; Jerrold M Olefsky; Nicholas J G Webster
Journal:  Endocrinology       Date:  2017-01-01       Impact factor: 4.736

7.  The loss of ERE-dependent ERα signaling potentiates the effects of maternal high-fat diet on energy homeostasis in female offspring fed an obesogenic diet.

Authors:  Troy A Roepke; Ali Yasrebi; Alejandra Villalobos; Elizabeth A Krumm; Jennifer A Yang; Kyle J Mamounis
Journal:  J Dev Orig Health Dis       Date:  2019-09-23       Impact factor: 2.401

8.  Glutamatergic Transmission to Hypothalamic Kisspeptin Neurons Is Differentially Regulated by Estradiol through Estrogen Receptor α in Adult Female Mice.

Authors:  Luhong Wang; Laura L Burger; Megan L Greenwald-Yarnell; Martin G Myers; Suzanne M Moenter
Journal:  J Neurosci       Date:  2017-11-07       Impact factor: 6.167

9.  The interaction of fasting, caloric restriction, and diet-induced obesity with 17β-estradiol on the expression of KNDy neuropeptides and their receptors in the female mouse.

Authors:  Jennifer A Yang; Ali Yasrebi; Marisa Snyder; Troy A Roepke
Journal:  Mol Cell Endocrinol       Date:  2016-08-06       Impact factor: 4.102

Review 10.  The impact of androgen actions in neurons on metabolic health and disease.

Authors:  Jamie J Morford; Sheng Wu; Franck Mauvais-Jarvis
Journal:  Mol Cell Endocrinol       Date:  2017-09-04       Impact factor: 4.102

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