Neonatal leptin exposure specifies innervation of presympathetic hypothalamic neurons and improves the metabolic status of leptin-deficient mice

Journal of Neuroscience

Volumn 33, Issue 2, 2013, Pages 840-851

  Bouyer, Karine ^a   Simerly, Richard B ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; LEPTIN; MELANOCORTIN; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; AUTONOMIC INNERVATION; BODY WEIGHT; CONTROLLED STUDY; ENERGY BALANCE; FEMALE; GLUCOSE TOLERANCE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; ANIMALS, NEWBORN; BODY TEMPERATURE REGULATION; BODY WEIGHT; EATING; ENERGY METABOLISM; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUCOSE TOLERANCE TEST; GLUTAMIC ACID; HYPOTHALAMUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LEPTIN; MALE; MICE; MICE, KNOCKOUT; NEURONS; NEUROSECRETORY SYSTEMS; PARASYMPATHETIC NERVOUS SYSTEM; PEPTIDES;

EID: 84872073192     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3215-12.2013     Document Type: Article

References (44)

1. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123:493-505. CrossRef Medline
2. Biag J, Huang Y, Gou L, Hintiryan H, Askarinam A, Hahn JD, Toga AW, Dong HW (2012) Cyto-and chemoarchitecture of the hypothalamic paraventricular nucleus in the C57BL/6J male mouse: a study of immunostaining and multiple fluorescent tract tracing. J Comp Neurol 520: 6-33. CrossRef Medline
3. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29. CrossRef Medline
4. Bouret SG (2010) Development of hypothalamic neural networks controlling appetite. Forum Nutr 63:84-93. Medline
5. Bouret SG, Draper SJ, Simerly RB (2004a) Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 24:2797-2805. CrossRef Medline
6. Bouret SG, Draper SJ, Simerly RB (2004b) Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304:108-110. CrossRef Medline
7. Bouret SG, Bates SH, Chen S, MyersMGJr, Simerly RB (2012) Distinct roles for specific leptin receptor signals in the development of hypothalamic feeding circuits. J Neurosci 32:1244-1252. CrossRef Medline
8. Buettner C, Muse ED, Cheng A, Chen L, Scherer T, Pocai A, Su K, Cheng B, Li X, Harvey-White J, Schwartz GJ, Kunos G, Rossetti L, Buettner C (2008) Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat Med 14:667-675. CrossRef Medline
9. Cesa R, Strata P (2009) Axonal competition in the synaptic wiring of the cerebellar cortex during development and in the mature cerebellum. Neuroscience 162:624-632. CrossRef Medline
10. Collin M, Bäckberg M, Ovesjö ML, Fisone G, Edwards RH, Fujiyama F, Meister B (2003) Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight. Eur J Neurosci 18:1265-1278. CrossRef Medline
11. Coppari R, Ichinose M, Lee CE, Pullen AE, Kenny CD, McGovern RA, Tang V, Liu SM, Ludwig T, Chua SC Jr, Lowell BB, Elmquist JK (2005) The hypothalamic arcuate nucleus: a key site for mediating leptin's effects on glucose homeostasis and locomotor activity. Cell Metab 1:63-72. CrossRef Medline
12. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484. CrossRef Medline
13. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, Laborie C, Lesage J, Vieau D (2008) Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149:470-475. CrossRef Medline
14. Dong HW (2008) Allen reference atlas: a digital color brain atlas of the C57BL/6J male mouse. New York: Wiley.
15. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR, Kuhar MJ, Saper CB, Elmquist JK (1998) Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21:1375-1385. CrossRef Medline
16. Enriori PJ, Sinnayah P, Simonds SE, Garcia Rudaz C, Cowley MA (2011) Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance. J Neurosci 31:12189-12197. CrossRef Medline
17. Fekete C, Légrádi G, Mihály E, Huang QH, Tatro JB, Rand WM, Emerson CH, Lechan RM (2000) alpha-Melanocyte-stimulating hormone is contained in nerve terminals innervating thyrotropin-releasing hormonesynthesizing neurons in the hypothalamic paraventricular nucleus and prevents fasting-induced suppression of prothyrotropin-releasing hormone gene expression. J Neurosci 20:1550-1558. Medline
18. Fetissov SO, Bergström U, Johansen JE, Hökfelt T, Schalling M, Ranscht B (2005) Alterations of arcuate nucleus neuropeptidergic development in contactin-deficient mice: comparison with anorexia and food-deprived mice. Eur J Neurosci 22:3217-3228. CrossRef Medline
19. Gibson DA, Ma L (2011) Developmental regulation of axon branching in the vertebrate nervous system. Development 138:183-195. CrossRef Medline
20. Hentges ST, Otero-Corchon V, Pennock RL, King CM, Low MJ (2009) Proopiomelanocortin expression in both GABA and glutamate neurons. J Neurosci 29:13684-13690. CrossRef Medline
21. Ho A, Chin A (1988) Circadian feeding and drinking patterns of genetically obese mice fed solid chow diet. Physiol Behav 43:651-656. CrossRef Medline
22. Horvath TL, Bechmann I, Naftolin F, Kalra SP, Leranth C (1997) Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res 756: 283-286. CrossRef Medline
23. Ibrahim N, Bosch MA, Smart JL, Qiu J, Rubinstein M, Rønnekleiv OK, Low MJ, Kelly MJ (2003) Hypothalamic proopiomelanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology 144:1331-1340. CrossRef Medline
24. Kolodkin AL, Tessier-Lavigne M (2010) Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol 3(6) pii: a001727.
25. Lu B, Wang KH, Nose A (2009) Molecular mechanisms underlying neural circuit formation. Curr Opin Neurobiol 19:162-167. CrossRef Medline
26. Luiten PG, ter Horst GJ, Karst H, Steffens AB (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res 329:374-378. CrossRef Medline
27. Madden CJ, Morrison SF (2009) Neurons in the paraventricular nucleus of the hypothalamus inhibit sympathetic outflow to brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 296:R831-R843. CrossRef Medline
28. McCarthy M, De Vries G, Forger N (2009) Sexual differentiation of the brain: mode, mechanisms and meaning. Hormones Brain Behav 3:1707-1744.
29. Padilla SL, Carmody JS, Zeltser LM (2010) Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits. Nat Med 16:403-405. CrossRef Medline
30. Parton LE, Ye CP, Coppari R, Enriori PJ, Choi B, Zhang CY, Xu C, Vianna CR, Balthasar N, Lee CE, Elmquist JK, Cowley MA, Lowell BB (2007) Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449:228-232. CrossRef Medline
31. Persson S, Havton LA (2009) Retrogradely transported fluorogold accumulates in lysosomes of neurons and is detectable ultrastructurally using post-embedding immuno-gold methods. J Neurosci Methods 184:42-47. CrossRef Medline
32. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304:110-115. CrossRef Medline
33. Roland BL, Sawchenko PE (1993) Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 332:123-143. CrossRef Medline
34. Rossi J, Balthasar N, Olson D, Scott M, Berglund E, Lee CE, Choi MJ, Lauzon D, Lowell BB, Elmquist JK (2011) Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab 13:195-204. CrossRef Medline
35. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661-671. Medline
36. Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536. CrossRef Medline
37. Simerly RB (2008) Hypothalamic substrates of metabolic imprinting. Physiol Behav 94:79-89. CrossRef Medline
38. Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113-164. CrossRef Medline
39. Swanson LW, Kuypers HG (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194: 555-570. CrossRef Medline
40. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7:493-494. CrossRef Medline
41. Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell BB (2011) Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154. CrossRef Medline
42. Williams KW, Margatho LO, Lee CE, Choi M, Lee S, Scott MM, Elias CF, Elmquist JK (2010) Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. J Neurosci 30:2472-2479. CrossRef Medline
43. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, Fujii S (2005) Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 1:371-378. CrossRef Medline
44. Zhang Y, Kerman IA, Laque A, Nguyen P, Faouzi M, Louis GW, Jones JC, Rhodes C, Münzberg H (2011) Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J Neurosci 31:1873-1884. CrossRef Medline