Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 15, 2010, Pages 7024-7029

  Stanley, Sarah ^a   Pinto, Shirly ^a,b   Segal, Jeremy ^a,c   Pérez, Cristian A ^a   Viale, Agnes ^a,d   DeFalco, Jeff ^a,e   Cai, Xiaoli ^a   Heisler, Lora K ^f   Friedman, Jeffrey M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e EVOTEC AG   (Germany)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Autonomic nervous system; Neuronal tracing; Pseudorabies virus

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; MELANIN CONCENTRATING HORMONE; NEUROPEPTIDE Y; OREXIN; OXYTOCIN; PROOPIOMELANOCORTIN;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN STEM; CELL POPULATION; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; LIVER; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADIPOSE TISSUE; ANIMALS; BRAIN STEM; GREEN FLUORESCENT PROTEINS; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; MALE; MELANINS; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; NEURONS; NEUROPEPTIDE Y; NEUROPEPTIDES; PITUITARY HORMONES; PRO-OPIOMELANOCORTIN;

MUS; SUID HERPESVIRUS 1;

EID: 77951029840     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1002790107     Document Type: Article

References (41)

1. Cannon WB (1929) Organization for physiological homeostasis. Physiol Rev 9:399-431.
2. Anderson EA, Wallin BG, Mark AL (1987) Dissociation of sympathetic nerve activity in arm and leg muscle during mental stress. Hypertension 9:III114-III119.
3. Brito MN, Brito NA, Baro DJ, Song CK, Bartness TJ (2007) Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148:5339-5347.
4. Püschel GP(2004)Control of hepatocytemetabolismby sympathetic andparasympathetic hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol 280:854-867.
5. Fredholm BB, Karlsson J (1970) Metabolic effects of prolonged sympathetic nerve stimulation in canine subcutaneous adipose tissue. Acta Physiol Scand 80:567-576.
6. Niijima A (1989) Nervous regulation of metabolism. Prog Neurobiol 33:135-147.
7. Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD (1989) A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res 491:156-162.
8. Bamshad M, Aoki VT, Adkison MG, Warren WS, Bartness TJ (1998) Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am J Physiol 275:R291-R299. (Pubitemid 28376320)
9. la Fleur SE, Kalsbeek A, Wortel J, Buijs RM (2000) Polysynaptic neural pathways between the hypothalamus, including the suprachiasmatic nucleus, and the liver. Brain Res 871:50-56. (Pubitemid 30406867)
10. Roseberry AG, Liu H, Jackson AC, Cai X, Friedman JM (2004) Neuropeptide Y-mediated inhibition of proopiomelanocortin neurons in the arcuate nucleus shows enhanced desensitization in ob/ob mice. Neuron 41:711-722. (Pubitemid 38326834)
11. Pinto S, et al. (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304:110-115. (Pubitemid 38451468)
12. Li Y, Gao XB, Sakurai T, van den Pol AN (2002) Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36:1169-1181. (Pubitemid 36044516)
13. Qu D, et al. (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243-247. (Pubitemid 26090645)
14. Huo L, Grill HJ, Bjørbaek C (2006) Divergent regulation of proopiomelanocortin neurons by leptin in the nucleus of the solitary tract and in the arcuate hypothalamic nucleus. Diabetes 55:567-573. (Pubitemid 43343211)
15. Uyama N, Geerts A, Reynaert H (2004) Neural connections between the hypothalamus and the liver. Anat Rec A Discov Mol Cell Evol Biol 280:808-820.
16. Kalsbeek A, La Fleur S, Van Heijningen C, Buijs RM (2004) Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 24:7604-7613. (Pubitemid 39186814)
17. Kreier F, et al. (2006) Tracing from fat tissue, liver, and pancreas: A neuroanatomical framework for the role of the brain in type 2 diabetes. Endocrinology 147:1140-1147. (Pubitemid 43244345)
18. Giordano A, et al. (2006) White adipose tissue lacks significant vagal innervation and immunohistochemical evidence of parasympathetic innervation. Am J Physiol Regul Integr Comp Physiol 291:R1243-R1255.
19. Shi H, Bartness TJ (2001) Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Res Bull 54:375-385. (Pubitemid 32288718)
20. Cano G, Card JP, Sved AF (2004) Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. J Comp Neurol 471:462-481. (Pubitemid 38401743)
21. Card JP (1998) Exploring brain circuitry with neurotropic viruses: New horizons in neuroanatomy. Anat Rec 253:176-185.
22. Jansen AS, Nguyen XV, Karpitskiy V, Mettenleiter TC, Loewy AD (1995) Central command neurons of the sympathetic nervous system: Basis of the fight-or-flight response. Science 270:644-646.
23. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263-1268. (Pubitemid 43348147)
24. Larsen PJ, Hay-Schmidt A, Mikkelsen JD (1994) Efferent connections from the lateral hypothalamic region and the lateral preoptic area to the hypothalamic paraventricular nucleus of the rat. J Comp Neurol 342:299-319. (Pubitemid 24100133)
25. Diano S, Naftolin F, Goglia F, Csernus V, Horvath TL (1998) Monosynaptic pathway between the arcuate nucleus expressing glial type II iodothyronine 5′-deiodinase mRNA and the median eminence-projective TRH cells of the rat paraventricular nucleus. J Neuroendocrinol 10:731-742. (Pubitemid 28446144)
26. Hermes SM, Mitchell JL, Aicher SA (2006) Most neurons in the nucleus tractus solitarii do not send collateral projections to multiple autonomic targets in the rat brain. Exp Neurol 198:539-551.
27. Jansen AS, Wessendorf MW, Loewy AD (1995) Transneuronal labeling of CNS neuropeptide and monoamine neurons after pseudorabies virus injections into the stellate ganglion. Brain Res 683:1-24.
28. Jaferi A, Bhatnagar S (2007) Corticotropin-releasing hormone receptors in the medial prefrontal cortex regulate hypothalamic-pituitary-adrenal activity and anxietyrelated behavior regardless of prior stress experience. Brain Res 1186:212-223.
29. Ring RH, et al. (2006) Anxiolytic-like activity of oxytocin in male mice: Behavioral and autonomic evidence, therapeutic implications. Psychopharmacology (Berl) 185:218-225.
30. Krout KE, Mettenleiter TC, Loewy AD (2003) Single CNS neurons link both central motor and cardiosympathetic systems: A double-virus tracing study. Neuroscience 118:853-866.
31. Kerman IA, et al. (2007) Distinct populations of presympathetic-premotor neurons express orexin or melanin-concentrating hormone in the rat lateral hypothalamus. J Comp Neurol 505:586-601.
32. Song CK, Jackson RM, Harris RB, Richard D, Bartness TJ (2005) Melanocortin-4 receptor mRNA is expressed in sympathetic nervous system outflow neurons to white adipose tissue. Am J Physiol Regul Integr Comp Physiol 289:R1467-R1476. (Pubitemid 41507413)
33. Scislo TJ, O'Leary DS (2002) Mechanisms mediating regional sympathoactivatory responses to stimulation of NTS A(1) adenosine receptors. Am J Physiol Heart Circ Physiol 283:H1588-H1599.
34. Kerman IA, Enquist LW, Watson SJ, Yates BJ (2003) Brainstem substrates of sympathomotor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J Neurosci 23:4657-4666.
35. Krout KE, Mettenleiter TC, Karpitskiy V, Nguyen XV, Loewy AD (2005) CNS neurons with links to both mood-related cortex and sympathetic nervous system. Brain Res 1050:199-202. (Pubitemid 40922734)
36. Lee TK, Lois JH, Troupe JH, Wilson TD, Yates BJ (2007) Transneuronal tracing of neural pathways that regulate hindlimb muscle blood flow. Am J Physiol Regul Integr Comp Physiol 292:R1532-R1541.
37. Doyle JP, et al. (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749-762.
38. DeFalco J, et al. (2001) Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science 291:2608-2613. (Pubitemid 32249686)
39. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotactic Co-ordinates (Academic Press, New York).
40. Yang XW, Model P, Heintz N (1997) Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865. (Pubitemid 27391778)
41. Elmquist JK, Bjørbaek C, Ahima RS, Flier JS, Saper CB (1998) Distributions of leptin receptor mRNA isoforms in the rat brain. J Comp Neurol 395:535-547. (Pubitemid 28226097)