Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons
Studies in humans and rodents indicate that a minimum amount of stored energy is required for normal pubertal development. The adipocyte-derived hormone leptin is a key metabolic signal to the neuroendocrine reproductive axis. Humans and mice lacking leptin or the leptin receptor (LepR) (ob/ob and d...
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Published in | The Journal of clinical investigation Vol. 121; no. 1; pp. 355 - 368 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Society for Clinical Investigation
01.01.2011
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Subjects | |
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Abstract | Studies in humans and rodents indicate that a minimum amount of stored energy is required for normal pubertal development. The adipocyte-derived hormone leptin is a key metabolic signal to the neuroendocrine reproductive axis. Humans and mice lacking leptin or the leptin receptor (LepR) (ob/ob and db/db mice, respectively) are infertile and fail to enter puberty. Leptin administration to leptin-deficient subjects and ob/ob mice induces puberty and restores fertility, but the exact site or sites of leptin action are unclear. Here, we found that genetic deletion of LepR selectively from hypothalamic Kiss1 neurons in mice had no effect on puberty or fertility, indicating that direct leptin signaling in Kiss1 neurons is not required for these processes. However, bilateral lesions of the ventral premammillary nucleus (PMV) of ob/ob mice blunted the ability of exogenous leptin to induce sexual maturation. Moreover, unilateral reexpression of endogenous LepR in PMV neurons was sufficient to induce puberty and improve fertility in female LepR-null mice. This LepR reexpression also normalized the increased hypothalamic GnRH content characteristic of leptin-signaling deficiency. These data suggest that the PMV is a key site for leptin's permissive action at the onset of puberty and support the hypothesis that the multiple actions of leptin to control metabolism and reproduction are anatomically dissociated. |
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AbstractList | Studies in humans and rodents indicate that a minimum amount of stored energy is required for normal pubertal development. The adipocyte-derived hormone leptin is a key metabolic signal to the neuroendocrine reproductive axis. Humans and mice lacking leptin or the leptin receptor (LepR) (ob/ob and db/db mice, respectively) are infertile and fail to enter puberty. Leptin administration to leptin-deficient subjects and ob/ob mice induces puberty and restores fertility, but the exact site or sites of leptin action are unclear. Here, we found that genetic deletion of LepR selectively from hypothalamic Kiss1 neurons in mice had no effect on puberty or fertility, indicating that direct leptin signaling in Kiss1 neurons is not required for these processes. However, bilateral lesions of the ventral premammillary nucleus (PMV) of ob/ob mice blunted the ability of exogenous leptin to induce sexual maturation. Moreover, unilateral reexpression of endogenous LepR in PMV neurons was sufficient to induce puberty and improve fertility in female LepR-null mice. This LepR reexpression also normalized the increased hypothalamic GnRH content characteristic of leptin-signaling deficiency. These data suggest that the PMV is a key site for leptin's permissive action at the onset of puberty and support the hypothesis that the multiple actions of leptin to control metabolism and reproduction are anatomically dissociated. Studies in humans and rodents indicate that a minimum amount of stored energy is required for normal pubertal development. The adipocyte-derived hormone leptin is a key metabolic signal to the neuroendocrine reproductive axis. Humans and mice lacking leptin or the leptin receptor (LepR) ( ob/ob and db/db mice, respectively) are infertile and fail to enter puberty. Leptin administration to leptin-deficient subjects and ob/ob mice induces puberty and restores fertility, but the exact site or sites of leptin action are unclear. Here, we found that genetic deletion of LepR selectively from hypothalamic Kiss1 neurons in mice had no effect on puberty or fertility, indicating that direct leptin signaling in Kiss1 neurons is not required for these processes. However, bilateral lesions of the ventral premammillary nucleus (PMV) of ob/ob mice blunted the ability of exogenous leptin to induce sexual maturation. Moreover, unilateral reexpression of endogenous LepR in PMV neurons was sufficient to induce puberty and improve fertility in female LepR-null mice. This LepR reexpression also normalized the increased hypothalamic GnRH content characteristic of leptin-signaling deficiency. These data suggest that the PMV is a key site for leptin’s permissive action at the onset of puberty and support the hypothesis that the multiple actions of leptin to control metabolism and reproduction are anatomically dissociated. |
Author | Lee, Syann Donato, Jr, Jose Scott, Michael M Margatho, Lisandra O Lee, Charlotte Lachey, Jennifer Castro, Inar A Friedman, Jeffrey Richardson, James A Elias, Carol F Coppari, Roberto Cravo, Roberta M Frazão, Renata Zigman, Jeffrey M Elmquist, Joel K Gautron, Laurent Chua, Jr, Streamson |
AuthorAffiliation | 1 Department of Internal Medicine, Division of Hypothalamic Research, University of Texas Southwestern Medical Center, Dallas, Texas, USA. 2 Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. 3 Acceleron Pharma, Boston, Massachusetts, USA. 4 Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil. 5 Department of Pathology, University of Texas Southwestern Medical Center, Dallas, Texas, USA. 6 Laboratory of Molecular Genetics and Howard Hughes Medical Institute, The Rockefeller University, New York, New York, USA. 7 Departments of Medicine and Neuroscience, Albert Einstein College of Medicine, New York, New York, USA. 8 Department of Psychiatry and 9 Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas, USA |
AuthorAffiliation_xml | – name: 1 Department of Internal Medicine, Division of Hypothalamic Research, University of Texas Southwestern Medical Center, Dallas, Texas, USA. 2 Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. 3 Acceleron Pharma, Boston, Massachusetts, USA. 4 Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil. 5 Department of Pathology, University of Texas Southwestern Medical Center, Dallas, Texas, USA. 6 Laboratory of Molecular Genetics and Howard Hughes Medical Institute, The Rockefeller University, New York, New York, USA. 7 Departments of Medicine and Neuroscience, Albert Einstein College of Medicine, New York, New York, USA. 8 Department of Psychiatry and 9 Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas, USA |
Author_xml | – sequence: 1 givenname: Jose surname: Donato, Jr fullname: Donato, Jr, Jose organization: Department of Internal Medicine, Division of Hypothalamic Research, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9077, USA – sequence: 2 givenname: Roberta M surname: Cravo fullname: Cravo, Roberta M – sequence: 3 givenname: Renata surname: Frazão fullname: Frazão, Renata – sequence: 4 givenname: Laurent surname: Gautron fullname: Gautron, Laurent – sequence: 5 givenname: Michael M surname: Scott fullname: Scott, Michael M – sequence: 6 givenname: Jennifer surname: Lachey fullname: Lachey, Jennifer – sequence: 7 givenname: Inar A surname: Castro fullname: Castro, Inar A – sequence: 8 givenname: Lisandra O surname: Margatho fullname: Margatho, Lisandra O – sequence: 9 givenname: Syann surname: Lee fullname: Lee, Syann – sequence: 10 givenname: Charlotte surname: Lee fullname: Lee, Charlotte – sequence: 11 givenname: James A surname: Richardson fullname: Richardson, James A – sequence: 12 givenname: Jeffrey surname: Friedman fullname: Friedman, Jeffrey – sequence: 13 givenname: Streamson surname: Chua, Jr fullname: Chua, Jr, Streamson – sequence: 14 givenname: Roberto surname: Coppari fullname: Coppari, Roberto – sequence: 15 givenname: Jeffrey M surname: Zigman fullname: Zigman, Jeffrey M – sequence: 16 givenname: Joel K surname: Elmquist fullname: Elmquist, Joel K – sequence: 17 givenname: Carol F surname: Elias fullname: Elias, Carol F |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21183787$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | Copyright American Society for Clinical Investigation Jan 2011 Copyright © 2011, American Society for Clinical Investigation |
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Title | Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons |
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