Pomc-expressing Progenitors Give Rise to Antagonistic Neuronal Populations in Hypothalamic Feeding Circuits

Overview

Journal Nat Med

Specialties General Medicine
Molecular Biology

Date 2010 Mar 30

PMID 20348924

Citations 177

Authors

Stephanie L Padilla

Jill S Carmody

Lori M Zeltser

Affiliations

Soon will be listed here.

Abstract

Hypothalamic neuron circuits regulating energy balance are highly plastic and develop in response to nutrient and hormonal cues. To identify processes that might be susceptible to gestational influences in mice, we characterized the ontogeny of proopiomelanocortin (POMC) and neuropeptide Y (NPY) cell populations, which exert opposing influences on food intake and body weight. These analyses revealed that Pomc is broadly expressed in immature hypothalamic neurons and that half of embryonic Pomc-expressing precursors subsequently adopt a non-POMC fate in adult mice. Moreover, nearly one quarter of the mature NPY+ cell population shares a common progenitor with POMC+ cells.

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References

Ibrahim N, Bosch M, Smart J, Qiu J, Rubinstein M, Ronnekleiv O . Hypothalamic proopiomelanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology. 2003; 144(4):1331-40. DOI: 10.1210/en.2002-221033. View

Schwartz M, Porte Jr D . Diabetes, obesity, and the brain. Science. 2005; 307(5708):375-9. DOI: 10.1126/science.1104344. View

Broad K, Curley J, Keverne E . Increased apoptosis during neonatal brain development underlies the adult behavioral deficits seen in mice lacking a functional paternally expressed gene 3 (Peg3). Dev Neurobiol. 2009; 69(5):314-25. DOI: 10.1002/dneu.20702. View

Fioramonti X, Contie S, Song Z, Routh V, Lorsignol A, Penicaud L . Characterization of glucosensing neuron subpopulations in the arcuate nucleus: integration in neuropeptide Y and pro-opio melanocortin networks?. Diabetes. 2007; 56(5):1219-27. DOI: 10.2337/db06-0567. View

Pinto S, Roseberry A, Liu H, Diano S, Shanabrough M, Cai X . Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science. 2004; 304(5667):110-5. DOI: 10.1126/science.1089459. View

Cottrell E, Cripps R, Duncan J, Barrett P, Mercer J, Herwig A . Developmental changes in hypothalamic leptin receptor: relationship with the postnatal leptin surge and energy balance neuropeptides in the postnatal rat. Am J Physiol Regul Integr Comp Physiol. 2009; 296(3):R631-9. PMC: 2665846. DOI: 10.1152/ajpregu.90690.2008. View

Shimada M, Nakamura T . Time of neuron origin in mouse hypothalamic nuclei. Exp Neurol. 1973; 41(1):163-73. DOI: 10.1016/0014-4886(73)90187-8. View

Saper C, Chou T, Elmquist J . The need to feed: homeostatic and hedonic control of eating. Neuron. 2002; 36(2):199-211. DOI: 10.1016/s0896-6273(02)00969-8. View

Zinyk D, MERCER E, Harris E, Anderson D, Joyner A . Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr Biol. 1998; 8(11):665-8. DOI: 10.1016/s0960-9822(98)70255-6. View

10.

Shankar K, Harrell A, Liu X, Gilchrist J, Ronis M, Badger T . Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2007; 294(2):R528-38. DOI: 10.1152/ajpregu.00316.2007. View

11.

Bouret S, Draper S, Simerly R . Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004; 304(5667):108-10. DOI: 10.1126/science.1095004. View

12.

Ogden C, Carroll M, Curtin L, McDowell M, Tabak C, Flegal K . Prevalence of overweight and obesity in the United States, 1999-2004. JAMA. 2006; 295(13):1549-55. DOI: 10.1001/jama.295.13.1549. View

13.

Balthasar N, Coppari R, McMinn J, Liu S, Lee C, Tang V . Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron. 2004; 42(6):983-91. DOI: 10.1016/j.neuron.2004.06.004. View

14.

Taylor P, Poston L . Developmental programming of obesity in mammals. Exp Physiol. 2006; 92(2):287-98. DOI: 10.1113/expphysiol.2005.032854. View

15.

van den Top M, Lyons D, Lee K, Coderre E, Renaud L, Spanswick D . Pharmacological and molecular characterization of ATP-sensitive K(+) conductances in CART and NPY/AgRP expressing neurons of the hypothalamic arcuate nucleus. Neuroscience. 2006; 144(3):815-24. DOI: 10.1016/j.neuroscience.2006.09.059. View

16.

Ollmann M, Wilson B, Yang Y, Kerns J, Chen Y, Gantz I . Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science. 1997; 278(5335):135-8. DOI: 10.1126/science.278.5335.135. View

17.

Altman J, Bayer S . Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J Comp Neurol. 1978; 182(4 Pt 2):945-71. DOI: 10.1002/cne.901820511. View

18.

Nilsson I, Johansen J, Schalling M, Hokfelt T, Fetissov S . Maturation of the hypothalamic arcuate agouti-related protein system during postnatal development in the mouse. Brain Res Dev Brain Res. 2005; 155(2):147-54. DOI: 10.1016/j.devbrainres.2005.01.009. View

19.

Levin B . Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond B Biol Sci. 2006; 361(1471):1107-21. PMC: 1642705. DOI: 10.1098/rstb.2006.1851. View

20.

Cowley M, Smart J, Rubinstein M, Cerdan M, Diano S, Horvath T . Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 2001; 411(6836):480-4. DOI: 10.1038/35078085. View