A GnRH neuronal population in the olfactory bulb translates socially relevant odors into reproductive behavior in male mice.

Journal

Nature neuroscience

ISSN: 1546-1726

Titre abrégé: Nat Neurosci

Pays: United States

ID NLM: 9809671

Informations de publication

Date de publication:
02 Aug 2024

Historique:

received: 17 05 2023

accepted: 03 07 2024

medline: 3 8 2024

pubmed: 3 8 2024

entrez: 2 8 2024

Statut: aheadofprint

Résumé

Hypothalamic gonadotropin-releasing hormone (GnRH) neurons regulate fertility and integrate hormonal status with environmental cues to ensure reproductive success. Here we show that GnRH neurons in the olfactory bulb (GnRH

Identifiants

DOI: 10.1038/s41593-024-01724-1 PMID: 39095587

pubmed: 39095587

doi: 10.1038/s41593-024-01724-1

pii: 10.1038/s41593-024-01724-1

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Subventions

Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)

ID : 725149

Organisme : Agence Nationale de la Recherche (French National Research Agency)

ID : ANR-19-CE16-0021-02

Organisme : Agence Nationale de la Recherche (French National Research Agency)

ID : ANR-18-CE14-00

Informations de copyright

Références

Dulac, C. & Torello, A. T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 4, 551–562 (2003).

pubmed: 12838330 doi: 10.1038/nrn1140

Belluscio, L., Koentges, G., Axel, R. & Dulac, C. A map of pheromone receptor activation in the mammalian brain. Cell 97, 209–220 (1999).

pubmed: 10219242 doi: 10.1016/S0092-8674(00)80731-X

Rodriguez, I., Feinstein, P. & Mombaerts, P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97, 199–208 (1999).

pubmed: 10219241 doi: 10.1016/S0092-8674(00)80730-8

Lehman, M. N., Winans, S. S. & Powers, J. B. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science 210, 557–560 (1980).

pubmed: 7423209 doi: 10.1126/science.7423209

Baird, A. D., Wilson, S. J., Bladin, P. F., Saling, M. M. & Reutens, D. C. The amygdala and sexual drive: insights from temporal lobe epilepsy surgery. Ann. Neurol. 55, 87–96 (2004).

pubmed: 14705116 doi: 10.1002/ana.10997

Bayless, D. W. et al. A neural circuit for male sexual behavior and reward. Cell 186, 3862–3881 (2023).

pubmed: 37572660 doi: 10.1016/j.cell.2023.07.021

Keller, M., Pillon, D. & Bakker, J. Olfactory systems in mate recognition and sexual behavior. Vitam. Horm. 83, 331–350 (2010).

pubmed: 20831953 doi: 10.1016/S0083-6729(10)83014-6

Keverne, E. B. Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav. 83, 177–187 (2004).

pubmed: 15488538 doi: 10.1016/j.physbeh.2004.08.013

Aoki, M. et al. Prolactin-sensitive olfactory sensory neurons regulate male preference in female mice by modulating responses to chemosensory cues. Sci. Adv. 7, eabg4074 (2021).

pubmed: 34623921 pmcid: 8500514 doi: 10.1126/sciadv.abg4074

Mandiyan, V. S., Coats, J. K. & Shah, N. M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 8, 1660–1662 (2005).

pubmed: 16261133 doi: 10.1038/nn1589

Wang, Z. et al. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 26, 7375–7379 (2006).

pubmed: 16837584 pmcid: 6674185 doi: 10.1523/JNEUROSCI.1967-06.2006

Duittoz, A. H. et al. Development of the gonadotropin-releasing hormone system. J. Neuroendocrinol. 34, e13087 (2022).

pubmed: 35067985 pmcid: 9286803 doi: 10.1111/jne.13087

Herbison, A. E. Control of puberty onset and fertility by gonadotropin-releasing hormone neurons. Nat. Rev. Endocrinol. 12, 452–466 (2016).

pubmed: 27199290 doi: 10.1038/nrendo.2016.70

Bronson, F. H. The regulation of luteinizing hormone secretion by estrogen: relationships among negative feedback, surge potential, and male stimulation in juvenile, peripubertal, and adult female mice. Endocrinology 108, 506–516 (1981).

pubmed: 7449740 doi: 10.1210/endo-108-2-506

Dluzen, D. E., Ramirez, V. D., Carter, C. S. & Getz, L. L. Male vole urine changes luteinizing hormone-releasing hormone and norepinephrine in female olfactory bulb. Science 212, 573–575 (1981).

pubmed: 7010608 doi: 10.1126/science.7010608

Boehm, U., Zou, Z. & Buck, L. B. Feedback loops link odor and pheromone signaling with reproduction. Cell 123, 683–695 (2005).

pubmed: 16290036 doi: 10.1016/j.cell.2005.09.027

Yoon, H., Enquist, L. W. & Dulac, C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123, 669–682 (2005).

pubmed: 16290037 doi: 10.1016/j.cell.2005.08.039

Casoni, F. et al. Development of the neurons controlling fertility in humans: new insights from 3D imaging and transparent fetal brains. Development 143, 3969–3981 (2016).

pubmed: 27803058 doi: 10.1242/dev.139444

Boehm, U. et al. Expert consensus document: European Consensus Statement on congenital hypogonadotropic hypogonadism–pathogenesis, diagnosis and treatment. Nat. Rev. Endocrinol. 11, 547–564 (2015).

pubmed: 26194704 doi: 10.1038/nrendo.2015.112

Messina, A. et al. A microRNA switch regulates the rise in hypothalamic GnRH production before puberty. Nat. Neurosci. 19, 835–844 (2016).

pubmed: 27135215 doi: 10.1038/nn.4298

Belle, M. et al. Tridimensional visualization and analysis of early human development. Cell 169, 161–173 (2017).

pubmed: 28340341 doi: 10.1016/j.cell.2017.03.008

Renier, N. et al. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).

pubmed: 25417164 doi: 10.1016/j.cell.2014.10.010

Spergel, D. J., Kruth, U., Hanley, D. F., Sprengel, R. & Seeburg, P. H. GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J. Neurosci. 19, 2037–2050 (1999).

pubmed: 10066257 pmcid: 6782541 doi: 10.1523/JNEUROSCI.19-06-02037.1999

Wang, J. & Hamill, O. P. Piezo2-peripheral baroreceptor channel expressed in select neurons of the mouse brain: a putative mechanism for synchronizing neural networks by transducing intracranial pressure pulses. J. Integr. Neurosci. 20, 825–837 (2021).

pubmed: 34997707 doi: 10.31083/j.jin2004085

Zeppilli, S. et al. Molecular characterization of projection neuron subtypes in the mouse olfactory bulb. eLife 10, e65445 (2021).

pubmed: 34292150 pmcid: 8352594 doi: 10.7554/eLife.65445

Jammal Salameh, L., Bitzenhofer, S. H., Hanganu-Opatz, I. L., Dutschmann, M. & Egger, V. Blood pressure pulsations modulate central neuronal activity via mechanosensitive ion channels. Science 383, eadk8511 (2024).

pubmed: 38301001 doi: 10.1126/science.adk8511

Galliano, E. et al. Embryonic and postnatal neurogenesis produce functionally distinct subclasses of dopaminergic neuron. eLife 7, e32373 (2018).

pubmed: 29676260 pmcid: 5935487 doi: 10.7554/eLife.32373

Castle, M. J., Gershenson, Z. T., Giles, A. R., Holzbaur, E. L. & Wolfe, J. H. Adeno-associated virus serotypes 1, 8, and 9 share conserved mechanisms for anterograde and retrograde axonal transport. Hum. Gene Ther. 25, 705–720 (2014).

pubmed: 24694006 pmcid: 4137353 doi: 10.1089/hum.2013.189

Vardy, E. et al. A new DREADD facilitates the multiplexed chemogenetic interrogation of behavior. Neuron 86, 936–946 (2015).

pubmed: 25937170 pmcid: 4441592 doi: 10.1016/j.neuron.2015.03.065

Johnston, R. E. & Bronson, F. Endocrine control of female mouse odors that elicit luteinizing hormone surges and attraction in males. Biol. Reprod. 27, 1174–1180 (1982).

pubmed: 7159661 doi: 10.1095/biolreprod27.5.1174

Maruniak, J. A. & Bronson, F. H. Gonadotropic responses of male mice to female urine. Endocrinology 99, 963–969 (1976).

pubmed: 987903 doi: 10.1210/endo-99-4-963

Chu, Z. & Moenter, S. M. Endogenous activation of metabotropic glutamate receptors modulates GABAergic transmission to gonadotropin-releasing hormone neurons and alters their firing rate: a possible local feedback circuit. J. Neurosci. 25, 5740–5749 (2005).

pubmed: 15958740 pmcid: 1201448 doi: 10.1523/JNEUROSCI.0913-05.2005

Yang, C. F. et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896–909 (2013).

pubmed: 23663785 pmcid: 3767768 doi: 10.1016/j.cell.2013.04.017

Wen, S. et al. Genetic identification of GnRH receptor neurons: a new model for studying neural circuits underlying reproductive physiology in the mouse brain. Endocrinology 152, 1515–1526 (2011).

pubmed: 21303944 doi: 10.1210/en.2010-1208

Wen, S. et al. Functional characterization of genetically labeled gonadotropes. Endocrinology 149, 2701–2711 (2008).

pubmed: 18325995 doi: 10.1210/en.2007-1502

Kang, N., Baum, M. J. & Cherry, J. A. A direct main olfactory bulb projection to the ‘vomeronasal’ amygdala in female mice selectively responds to volatile pheromones from males. Eur. J. Neurosci. 29, 624–634 (2009).

pubmed: 19187265 pmcid: 2669936 doi: 10.1111/j.1460-9568.2009.06638.x

Kevetter, G. A. & Winans, S. S. Connections of the corticomedial amygdala in the golden hamster. II. Efferents of the “olfactory amygdala”. J. Comp. Neurol. 197, 99–111 (1981).

pubmed: 6164703 doi: 10.1002/cne.901970108

Pineda, R., Plaisier, F., Millar, R. P. & Ludwig, M. Amygdala kisspeptin neurons: putative mediators of olfactory control of the gonadotropic axis. Neuroendocrinology 104, 223–238 (2017).

pubmed: 27054958 doi: 10.1159/000445895

Seminara, S. B. et al. The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 349, 1614–1627 (2003).

pubmed: 14573733 doi: 10.1056/NEJMoa035322

Topaloglu, A. K. et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N. Engl. J. Med. 366, 629–635 (2012).

pubmed: 22335740 doi: 10.1056/NEJMoa1111184

de Roux, N. et al. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl Acad. Sci. USA 100, 10972–10976 (2003).

pubmed: 12944565 pmcid: 196911 doi: 10.1073/pnas.1834399100

Stephens, S. B. Z. & Kauffman, A. S. Regulation and possible functions of kisspeptin in the medial amygdala. Front. Endocrinol. 8, 191 (2017).

doi: 10.3389/fendo.2017.00191

Lin, D. Y., Zhang, S. Z., Block, E. & Katz, L. C. Encoding social signals in the mouse main olfactory bulb. Nature 434, 470–477 (2005).

pubmed: 15724148 doi: 10.1038/nature03414

Shani-Narkiss, H. et al. Young adult-born neurons improve odor coding by mitral cells. Nat. Commun. 11, 5867 (2020).

pubmed: 33203831 pmcid: 7673122 doi: 10.1038/s41467-020-19472-8

Hellier, V. et al. Female sexual behavior in mice is controlled by kisspeptin neurons. Nat. Commun. 9, 400 (2018).

pubmed: 29374161 pmcid: 5786055 doi: 10.1038/s41467-017-02797-2

Manfredi-Lozano, M. et al. GnRH replacement rescues cognition in Down syndrome. Science 377, eabq4515 (2022).

pubmed: 36048943 pmcid: 7613827 doi: 10.1126/science.abq4515

Schang, A. L. et al. GnRH receptor gene expression in the developing rat hippocampus: transcriptional regulation and potential roles in neuronal plasticity. Endocrinology 152, 568–580 (2011).

pubmed: 21123436 doi: 10.1210/en.2010-0840

Skrapits, K. et al. The cryptic gonadotropin-releasing hormone neuronal system of human basal ganglia. eLife 10, e67714 (2021).

pubmed: 34128468 pmcid: 8245125 doi: 10.7554/eLife.67714

Hurst, J. L. Female recognition and assessment of males through scent. Behav. Brain Res 200, 295–303 (2009).

pubmed: 19146884 doi: 10.1016/j.bbr.2008.12.020

Choi, J. M. et al. Development of the main olfactory system and main olfactory epithelium-dependent male mating behavior are altered in Go-deficient mice. Proc. Natl Acad. Sci. USA 113, 10974–10979 (2016).

pubmed: 27625425 pmcid: 5047177 doi: 10.1073/pnas.1613026113

Adekunbi, D. A. et al. Kisspeptin neurones in the posterodorsal medial amygdala modulate sexual partner preference and anxiety in male mice. J. Neuroendocrinol. 30, e12572 (2018).

pubmed: 29356147 pmcid: 5873280 doi: 10.1111/jne.12572

Lehman, M. N. & Winans, S. S. Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior: autoradiographic and behavioral analyses. Brain Res. 240, 27–41 (1982).

pubmed: 7093718 doi: 10.1016/0006-8993(82)90641-2

Wood, R. I. & Newman, S. W. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J. Neurosci. 15, 7261–7269 (1995).

pubmed: 7472480 pmcid: 6578098 doi: 10.1523/JNEUROSCI.15-11-07261.1995

Gomez, D. M. & Newman, S. W. Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J. Comp. Neurol. 317, 195–218 (1992).

pubmed: 1573064 doi: 10.1002/cne.903170208

Kevetter, G. A. & Winans, S. S. Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the “vomeronasal amygdala”. J. Comp. Neurol. 197, 81–98 (1981).

pubmed: 6164702 doi: 10.1002/cne.901970107

Meredith, M. Human vomeronasal organ function: a critical review of best and worst cases. Chem. Senses 26, 433–445 (2001).

pubmed: 11369678 doi: 10.1093/chemse/26.4.433

Frasnelli, J., Lundstrom, J. N., Boyle, J. A., Katsarkas, A. & Jones-Gotman, M. The vomeronasal organ is not involved in the perception of endogenous odors. Hum. Brain Mapp. 32, 450–460 (2011).

pubmed: 20578170 doi: 10.1002/hbm.21035

Zhang, G. et al. Hypothalamic programming of systemic ageing involving IKK-β, NF-κB and GnRH. Nature 497, 211–216 (2013).

pubmed: 23636330 pmcid: 3756938 doi: 10.1038/nature12143

Mayer, C. et al. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc. Natl Acad. Sci. USA 107, 22693–22698 (2010).

pubmed: 21149719 pmcid: 3012491 doi: 10.1073/pnas.1012406108

Zheng, G. X. et al. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049 (2017).

pubmed: 28091601 pmcid: 5241818 doi: 10.1038/ncomms14049

Imamura, F., Ito, A. & LaFever, B. J. Subpopulations of projection neurons in the olfactory bulb. Front. Neural Circuits 14, 561822 (2020).

pubmed: 32982699 pmcid: 7485133 doi: 10.3389/fncir.2020.561822

Tepe, B. et al. Single-cell RNA-seq of mouse olfactory bulb reveals cellular heterogeneity and activity-dependent molecular census of adult-born neurons. Cell Rep. 25, 2689–2703 (2018).

pubmed: 30517858 pmcid: 6342206 doi: 10.1016/j.celrep.2018.11.034

Steyn, F. J. et al. Development of a methodology for and assessment of pulsatile luteinizing hormone secretion in juvenile and adult male mice. Endocrinology 154, 4939–4945 (2013).

pubmed: 24092638 pmcid: 5398599 doi: 10.1210/en.2013-1502

Brock, O., Bakker, J. & Baum, M. J. Assessment of urinary pheromone discrimination, partner preference, and mating behaviors in female mice. Methods Mol. Biol. 1068, 319–329 (2013).

pubmed: 24014373 doi: 10.1007/978-1-62703-619-1_24

Chachlaki, K. et al. NOS1 mutations cause hypogonadotropic hypogonadism with sensory and cognitive deficits that can be reversed in infantile mice. Sci. Transl. Med. 14, eabh2369 (2022).

pubmed: 36197968 pmcid: 7613826 doi: 10.1126/scitranslmed.abh2369

Silva, M. S. B. et al. Female sexual behavior is disrupted in a preclinical mouse model of PCOS via an attenuated hypothalamic nitric oxide pathway. Proc. Natl Acad. Sci. USA 26, e2203503119 (2022).

doi: 10.1073/pnas.2203503119