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PMID: 18758446 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The Creb1 coactivator Crtc1 is required for energy balance and fertility.

Nature medicine ·Vol. 14 ·No. 10 ·2008-10-00 ·Pages 1112-7

Altarejos JY, Goebel N, Conkright MD, Inoue H, Xie J, Arias CM, Sawchenko PE, Montminy M

Abstract

The adipocyte-derived hormone leptin maintains energy balance by acting on hypothalamic leptin receptors (Leprs) that act on the signal transducer and activator of transcription 3 (Stat3). Although disruption of Lepr-Stat3 signaling promotes obesity in mice, other features of Lepr function, such as fertility, seem normal, pointing to the involvement of additional regulators. Here we show that the cyclic AMP responsive element-binding protein-1 (Creb1)-regulated transcription coactivator-1 (Crtc1) is required for energy balance and reproduction-Crtc1(-/-) mice are hyperphagic, obese and infertile. Hypothalamic Crtc1 was phosphorylated and inactive in leptin-deficient ob/ob mice, while leptin administration increased amounts of dephosphorylated nuclear Crtc1. Dephosphorylated Crtc1 stimulated expression of the Cartpt and Kiss1 genes, which encode hypothalamic neuropeptides that mediate leptin's effects on satiety and fertility. Crtc1 overexpression in hypothalamic cells increased Cartpt and Kiss1 gene expression, whereas Crtc1 depletion decreased it. Indeed, leptin enhanced Crtc1 activity over the Cartpt and Kiss1 promoters in cells overexpressing Lepr, and these effects were disrupted by expression of a dominant-negative Creb1 polypeptide. As leptin administration increased recruitment of hypothalamic Crtc1 to Cartpt and Kiss1 promoters, our results indicate that the Creb1-Crtc1 pathway mediates the central effects of hormones and nutrients on energy balance and fertility.

MeSH Terms
Animals Cells, Cultured Cyclic AMP Response Element-Binding Protein/physiology Energy Metabolism Female Fertility Kisspeptins Leptin/physiology Male Mice Mice, Inbred C57BL Mice, Obese Nerve Tissue Proteins/genetics,physiology Phosphorylation Proteins/genetics,physiology Transcription Factors/genetics,physiology
Chemicals
Creb1 protein, mouse Crtc1 protein, mouse Cyclic AMP Response Element-Binding Protein Kiss1 protein, mouse Kisspeptins Leptin Nerve Tissue Proteins Proteins Transcription Factors cocaine- and amphetamine-regulated transcript protein
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Altarejos Judith Y
Peptide Biology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, California 92037, USA.
Goebel Naomi
Conkright Michael D
Inoue Hiroshi
Xie Jianxin
Arias Carlos M
Sawchenko Paul E
Montminy Marc
References (48)
48 references, click to expand
  1. Heterozygosity for Lep(ob) or Lep(rdb) affects body composition and leptin homeostasis in adult mice.
    Am J Physiol. 1998 Apr;274(4):R985-90 PMID: 9575960
  2. CART gene promoter transcription is regulated by a cyclic adenosine monophosphate response element.
    Obes Res. 2002 Dec;10(12):1291-8 PMID: 12490674
  3. Leptin activates hypothalamic CART neurons projecting to the spinal cord.
    Neuron. 1998 Dec;21(6):1375-85 PMID: 9883730
  4. Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF receptors.
    Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2843-8 PMID: 11226328
  5. Genetics of obesity in humans.
    Endocr Rev. 2006 Dec;27(7):710-18 PMID: 17122358
  6. CART peptides in the central control of feeding and interactions with neuropeptide Y.
    Synapse. 1998 Aug;29(4):293-8 PMID: 9661247
  7. CART promoter CRE site binds phosphorylated CREB.
    Brain Res Mol Brain Res. 2002 Jul 15;104(1):81-5 PMID: 12117553
  8. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice.
    Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8878-83 PMID: 9238071
  9. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse.
    J Neuroendocrinol. 2006 Apr;18(4):298-303 PMID: 16503925
  10. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector.
    Cell. 2004 Oct 1;119(1):61-74 PMID: 15454081
  11. Silencing the constitutive active transcription factor CREB by the LKB1-SIK signaling cascade.
    FEBS J. 2006 Jun;273(12):2730-48 PMID: 16817901
  12. The function of leptin in nutrition, weight, and physiology.
    Nutr Rev. 2002 Oct;60(10 Pt 2):S1-14; discussion S68-84, 85-7 PMID: 12403078
  13. Hypothalamic CART is a new anorectic peptide regulated by leptin.
    Nature. 1998 May 7;393(6680):72-6 PMID: 9590691
  14. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty.
    J Neurosci. 2005 Dec 7;25(49):11349-56 PMID: 16339030
  15. Mechanisms of leptin action and leptin resistance.
    Annu Rev Physiol. 2008;70:537-56 PMID: 17937601
  16. Expression of hypothalamic KiSS-1 system and rescue of defective gonadotropic responses by kisspeptin in streptozotocin-induced diabetic male rats.
    Diabetes. 2006 Sep;55(9):2602-10 PMID: 16936210
  17. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat.
    Neuroendocrinology. 2004;80(4):264-72 PMID: 15665556
  18. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus.
    Nature. 2004 Apr 1;428(6982):569-74 PMID: 15058305
  19. The adipocyte as an active participant in energy balance and metabolism.
    Gastroenterology. 2007 May;132(6):2103-15 PMID: 17498506
  20. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4459-64 PMID: 15753290
  21. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity.
    Nature. 2007 Sep 13;449(7159):228-32 PMID: 17728716
  22. Role of melanocortinergic neurons in feeding and the agouti obesity syndrome.
    Nature. 1997 Jan 9;385(6612):165-8 PMID: 8990120
  23. Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons.
    Endocrinology. 2005 Mar;146(3):1043-7 PMID: 15591135
  24. The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction.
    Annu Rev Physiol. 2008;70:213-38 PMID: 17988212
  25. TRB3 links the E3 ubiquitin ligase COP1 to lipid metabolism.
    Science. 2006 Jun 23;312(5781):1763-6 PMID: 16794074
  26. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene.
    Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10714-9 PMID: 17563351
  27. TORCs: transducers of regulated CREB activity.
    Mol Cell. 2003 Aug;12(2):413-23 PMID: 14536081
  28. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2.
    Nature. 2007 Sep 20;449(7160):366-9 PMID: 17805301
  29. Role of brain insulin receptor in control of body weight and reproduction.
    Science. 2000 Sep 22;289(5487):2122-5 PMID: 11000114
  30. Cooperative interactions between CBP and TORC2 confer selectivity to CREB target gene expression.
    EMBO J. 2007 Jun 20;26(12):2880-9 PMID: 17476304
  31. The insulin-regulated CREB coactivator TORC promotes stress resistance in Drosophila.
    Cell Metab. 2008 May;7(5):434-44 PMID: 18460334
  32. Leptin is a metabolic signal to the reproductive system.
    Endocrinology. 1996 Jul;137(7):3144-7 PMID: 8770941
  33. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism.
    Nature. 2005 Oct 20;437(7062):1109-11 PMID: 16148943
  34. Leptin signaling in the central nervous system and the periphery.
    Recent Prog Horm Res. 2004;59:305-31 PMID: 14749508
  35. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition.
    Endocrinology. 2005 Sep;146(9):3917-25 PMID: 15932928
  36. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14379-84 PMID: 16980408
  37. Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins.
    Curr Biol. 2004 Dec 14;14(23):2156-61 PMID: 15589160
  38. Identification of a family of cAMP response element-binding protein coactivators by genome-scale functional analysis in mammalian cells.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12147-52 PMID: 14506290
  39. Corticotropin-releasing factor: co-expression within distinct subsets of oxytocin-, vasopressin-, and neurotensin-immunoreactive neurons in the hypothalamus of the male rat.
    J Neurosci. 1984 Apr;4(4):1118-29 PMID: 6609226
  40. A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos.
    Mol Cell Biol. 1998 Feb;18(2):967-77 PMID: 9447994
  41. A public gene trap resource for mouse functional genomics.
    Nat Genet. 2004 Jun;36(6):543-4 PMID: 15167922
  42. Morphological characterization of immortalized hypothalamic neurons synthesizing luteinizing hormone-releasing hormone.
    Endocrinology. 1991 Sep;129(3):1575-83 PMID: 1874189
  43. Reproductive hormonal function in the genetically obese (ob/ob) mouse.
    Endocrinology. 1976 Jun;98(6):1359-64 PMID: 1278106
  44. Characterization of the cocaine- and amphetamine-regulated transcript (CART) peptide gene promoter and its activation by a cyclic AMP-dependent signaling pathway in GH3 cells.
    J Neurochem. 2002 Mar;80(5):885-93 PMID: 11948252
  45. The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization.
    J Comp Neurol. 1992 May 8;319(2):218-45 PMID: 1522246
  46. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus.
    Nature. 2001 May 24;411(6836):480-4 PMID: 11373681
  47. Appropriate inhibition of orexigenic hypothalamic arcuate nucleus neurons independently of leptin receptor/STAT3 signaling.
    J Neurosci. 2007 Jan 3;27(1):69-74 PMID: 17202473
  48. BayGenomics: a resource of insertional mutations in mouse embryonic stem cells.
    Nucleic Acids Res. 2003 Jan 1;31(1):278-81 PMID: 12520002
Article Info
Journal
Nature medicine
Abbr.
Nat Med
ISSN
1546-170X
Published
2008-10-00
Epub
2008-00-31
Pages
1112-7
Language
English
Region
United States
NLM ID
9502015
PMCID
PMC2667698
Subset
IM
Grants
NIDDK NIH HHS · R01 DK049777-12 · United States
NIDDK NIH HHS · R01 DK049777-15 · United States
NIDDK NIH HHS · R01 DK049777-11 · United States
NIDDK NIH HHS · R01 DK049777-13 · United States
NIDDK NIH HHS · DK049777 · United States
NIDDK NIH HHS · R01 DK049777-14 · United States
NIDDK NIH HHS · R01 DK049777 · United States
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