Profiling of glucose-sensing neurons reveals that ghrh neurons are activated by hypoglycemia

Cell Metabolism

Volumn 18, Issue 4, 2013, Pages 596-607

  Stanley, Sarah ^a   Domingos, Ana I ^a   Kelly, Leah ^a   Garfield, Alastair ^c   Damanpour, Shadi ^a   Heisler, Lora ^d   Friedman, Jeffrey ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYGLUCOSE; ENHANCED GREEN FLUORESCENT PROTEIN; GLUCOKINASE; GLUCOSE; GONADORELIN; GROWTH HORMONE;

ANIMAL CELL; ARTICLE; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; CRE GENE; ELECTROPHYSIOLOGY; GCK GENE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH HORMONE RELEASE; HYPOGLYCEMIA; HYPOTHALAMUS; LIMBIC SYSTEM; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; DEOXYGLUCOSE; GENE EXPRESSION PROFILING; GLUCOKINASE; GLUCOSE; GREEN FLUORESCENT PROTEINS; GROWTH HORMONE-RELEASING HORMONE; HYPOGLYCEMIA; HYPOTHALAMUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; RIBOSOMAL PROTEINS;

EID: 84885145339     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.09.002     Document Type: Article

References (57)

1. Adachi, A., Kobashi, M., and Funahashi, M. (1995). Glucose-responsive neurons in the brainstem. Obes. Res. 3(Suppl 5 ), 735S-740S.
2. Bansal, S.A., Lee, L.A., and Woolf, P.D. (1981). Dopaminergic stimulation and inhibition of growth hormone secretion in normal man: studies of the pharmacologic specificity. J. Clin. Endocrinol. Metab. 53, 1273-1277.
3. Bernard,C., Dastre,A., Vulpain,A., and Bert,P. (1878). Leç ons sur les phénomènes de la vie communs aux animaux et aux végétaux.
4. Berthoud, H.R., Bereiter, D.A., and Jeanrenaud, B. (1980). Role of the autonomic nervous system in the mediation of LHA electrical stimulation-induced effects on insulinemia and glycemia. J. Auton. Nerv. Syst. 2, 183-198.
5. Blackard, W.G., and Heidingsfelder, S.A. (1968). Adrenergic receptor control mechanism for growth hormone secretion. J. Clin. Invest. 47, 1407-1414.
6. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268.
7. Briski, K.P. (1998). Glucoprivic induction of Fos immunoreactivity in hypothalamic dopaminergic neurons. Neuroreport 9, 289-295.
8. Burdakov, D., Gerasimenko, O., and Verkhratsky, A. (2005). Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J. Neurosci. 25, 2429-2433.
9. Burdakov, D., Jensen, L.T., Alexopoulos, H., Williams, R.H., Fearon, I.M., O'Kelly, I., Gerasimenko, O., Fugger, L., and Verkhratsky, A. (2006). Tandem-pore K+ channels mediate inhibition of orexin neurons by glucose. Neuron 50, 711-722.
10. Claret, M., Smith, M.A., Knauf, C., Al-Qassab, H., Woods, A., Heslegrave, A., Piipari, K., Emmanuel, J.J., Colom, A., Valet, P., et al. (2011). Deletion of Lkb1 in pro-opiomelanocortin neurons impairs peripheral glucose homeostasis in mice. Diabetes 60, 735-745.
11. Cordido, F., Dieguez, C., and Casanueva, F.F. (1990). Effect of central cholinergic neurotransmission enhancement by pyridostigmine on the growth hormone secretion elicited by clonidine, arginine, or hypoglycemia in normal and obese subjects. J. Clin. Endocrinol. Metab. 70, 1361-1370.
12. Cowley, M.A., Pronchuk, N., Fan, W., Dinulescu, D.M., Colmers, W.F., and Cone, R.D. (1999). Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24, 155-163.
13. Doyle, J.P., Dougherty, J.D., Heiman, M., Schmidt, E.F., Stevens, T.R., Ma, G., Bupp, S., Shrestha, P., Shah, R.D., Doughty, M.L., et al. (2008). Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749-762.
14. Dunn-Meynell, A.A., Govek, E., and Levin, B.E. (1997). Intracarotid glucose selectively increases Fos-like immunoreactivity in paraventricular, ventromedial and dorsomedial nuclei neurons. Brain Res. 748, 100-106.
15. Dunn-Meynell, A.A., Routh, V.H., Kang, L., Gaspers, L., and Levin, B.E. (2002). Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51, 2056-2065.
16. Frohman, L.A., Muller, E.E., and Cocchi, D. (1973). Central nervous system mediated inhibition of insulin secretion due to 2-deoxyglucose. Horm. Metab. Res. 5, 21-26.
17. Fukuda, M., Ono, T., Nishino, H., and Sasaki, K. (1984). Independent glucose effects on rat hypothalamic neurons: an in vitro study. J. Auton. Nerv. Syst. 10, 373-381.
18. Goldstein, J.L., Zhao, T.J., Li, R.L., Sherbet, D.P., Liang, G., and Brown, M.S. (2011). Surviving starvation: essential role of the ghrelin-growth hormone axis. Cold Spring Harb. Symp. Quant. Biol. 76, 121-127.
19. González, J.A., Jensen, L.T., Fugger, L., and Burdakov, D. (2008). Metabolismindependent sugar sensing in central orexin neurons. Diabetes 57, 2569-2576.
20. Goto, Y., Carpenter, R.G., Berelowitz, M., and Frohman, L.A. (1980). Effect of ventromedial hypothalamic lesions on the secretion of somatostatin, insulin, and glucagon by the perfused rat pancreas. Metabolism 29, 986-990.
21. Hakansson, M.L., and Meister, B. (1998). Transcription factor STAT3 in leptin target neurons of the rat hypothalamus. Neuroendocrinology 68, 420-427.
22. Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suárez-Fariñas, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., et al. (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748.
23. Hussain, K., Hindmarsh, P., and Aynsley-Green, A. (2003). Spontaneous hypoglycemia in childhood is accompanied by paradoxically low serum growth hormone and appropriate cortisol counterregulatory hormonal responses. J. Clin. Endocrinol. Metab. 88, 3715-3723.
24. Jaffe, C.A., DeMott-Friberg, R., and Barkan, A.L. (1996). Endogenous growth hormone (GH)-releasing hormone is required for GH responses to pharmacological stimuli. J. Clin. Invest. 97, 934-940.
25. Jetton, T.L., Liang, Y., Pettepher, C.C., Zimmerman, E.C., Cox, F.G., Horvath, K., Matschinsky, F.M., and Magnuson, M.A. (1994). Analysis of upstream glucokinase promoter activity in transgenic mice and identification of glucokinase in rare neuroendocrine cells in the brain and gut. J. Biol. Chem. 269, 3641-3654.
26. Jordan, S.D., Könner, A.C., and Brüning, J.C. (2010). Sensing the fuels: glucose and lipid signaling in the CNS controlling energy homeostasis. Cell. Mol. Life Sci. 67, 3255-3273.
27. Kang, L., Routh, V.H., Kuzhikandathil, E.V., Gaspers, L.D., and Levin, B.E. (2004). Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 53, 549-559.
28. Kang, L., Dunn-Meynell, A.A., Routh, V.H., Gaspers, L.D., Nagata, Y., Nishimura, T., Eiki, J., Zhang, B.B., and Levin, B.E. (2006). Glucokinase is a critical regulator of ventromedial hypothalamic neuronal glucosensing. Diabetes 55, 412-420.
29. Klinakis, A., Szabolcs, M., Chen, G., Xuan, S., Hibshoosh, H., and Efstratiadis, A. (2009). Igf1r as a therapeutic target in a mouse model of basal-like breast cancer. Proc. Natl. Acad. Sci. USA 106, 2359-2364.
30. Landau, B.R., and Lubs, H.A. (1958). Animal responses to 2-deoxy-D-glucose administration. Proc. Soc. Exp. Biol. Med. 99, 124-127.
31. Lewis, B.M., Dieguez, C., Ham, J., Page, M.D., Creagh, F.M., Peters, J.R., and Scanlon, M.F. (1989). Effects of glucose on thyrotrophin-releasing hormone, growth hormone-releasing hormone, somatostatin and luteinizing hormone-releasing hormone release from rat hypothalamus in vitro. J. Neuroendocrinol. 1, 437-441.
32. Lynch, R.M., Tompkins, L.S., Brooks, H.L., Dunn-Meynell, A.A., and Levin, B.E. (2000). Localization of glucokinase gene expression in the rat brain. Diabetes 49, 693-700.
33. Ma, X., Zubcevic, L., and Ashcroft, F.M. (2008). Glucose regulates the effects of leptin on hypothalamic POMC neurons. Proc. Natl. Acad. Sci. USA 105, 9811-9816.
34. Magnuson, M.A. (1992). Tissue-specific regulation of glucokinase gene expression. J. Cell. Biochem. 48, 115-121.
35. Masuda, A., Shibasaki, T., Hotta, M., Yamauchi, N., Ling, N., Demura, H., and Shizume, K. (1990). Insulin-induced hypoglycemia, L-dopa and arginine stimulate GH secretion through different mechanisms in man. Regul. Pept. 31, 53-64.
36. Meglasson, M.D., and Matschinsky, F.M. (1984). New perspectives on pancreatic islet glucokinase. Am. J. Physiol. 246, E1-E13.
37. Millán, C., Martínez, F., Cortés-Campos, C., Lizama, I., Yañez, M.J., Llanos, P., Reinicke, K., Rodríguez, F., Peruzzo, B., Nualart, F., and García, M.A. (2010). Glial glucokinase expression in adult and post-natal development of the hypothalamic region. ASN Neuro 2, e00035.
38. Murphy, B.A., Fioramonti, X., Jochnowitz, N., Fakira, K., Gagen, K., Contie, S., Lorsignol, A., Penicaud, L., Martin, W.J., and Routh, V.H. (2009). Fasting enhances the response of arcuate neuropeptide Y-glucose-inhibited neurons to decreased extracellular glucose. Am. J. Physiol. Cell Physiol. 296, C746-C756.
39. Nawaratne, V., Leach, K., Suratman, N., Loiacono, R.E., Felder, C.C., Armbruster, B.N., Roth, B.L., Sexton, P.M., and Christopoulos, A. (2008). New insights into the function of M4 muscarinic acetylcholine receptors gained using a novel allosteric modulator and a DREADD (designer receptor exclusively activated by a designer drug). Mol. Pharmacol. 74, 1119-1131.
40. Osterstock, G., Escobar, P., Mitutsova, V., Gouty-Colomer, L.A., Fontanaud, P., Molino, F., Fehrentz, J.A., Carmignac, D., Martinez, J., Guerineau, N.C., et al. (2010). Ghrelin stimulation of growth hormone-releasing hormone neurons is direct in the arcuate nucleus. PLoS ONE 5, e9159, http://dx.doi.org/ 10.1371/journal.pone.0009159.
41. Owen, O.E., Morgan, A.P., Kemp, H.G., Sullivan, J.M., Herrera, M.G., and Cahill, G.F., Jr. (1967). Brain metabolism during fasting. J. Clin. Invest. 46, 1589-1595.
42. Parton, L.E., Ye, C.P., Coppari, R., Enriori, P.J., Choi, B., Zhang, C.Y., Xu, C., Vianna, C.R., Balthasar, N., Lee, C.E., et al. (2007). Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449, 228-232.
43. Paxinos, G., and Franklin, K.B.J. (2001). The Mouse Brain in Stereotactic Co-ordinates. 2001. (Orlando: Academic Press).
44. Porte, D., Jr., Woods, S.C., Chen, M., Smith, P.H., and Ensinck, J.W. (1975). Central factors in the control of insulin and glucagon secretion. Pharmacol. Biochem. Behav. Suppl. 3, 127-133.
45. Rorsman, P. (1997). The pancreatic beta-cell as a fuel sensor: an electrophysiologist's viewpoint. Diabetologia 40, 487-495.
46. Sanz, E., Yang, L., Su, T., Morris, D.R., McKnight, G.S., and Amieux, P.S. (2009). Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc. Natl. Acad. Sci. USA 106, 13939-13944.
47. Silva, N.L., and Boulant, J.A. (1984). Effects of osmotic pressure, glucose, and temperature on neurons in preoptic tissue slices. Am. J. Physiol. 247, R335-R345.
48. Stanley, S., Pinto, S., Segal, J., Pérez, C.A., Viale, A., DeFalco, J., Cai, X., Heisler, L.K., and Friedman, J.M. (2010). Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically. Proc. Natl. Acad. Sci. USA 107, 7024-7029.
49. Stanley, S.A., Gagner, J.E., Damanpour, S., Yoshida, M., Dordick, J.S., and Friedman, J.M. (2012). Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 336, 604-608.
50. Sternson, S.M., Shepherd, G.M., and Friedman, J.M. (2005). Topographic mapping of VMH / arcuate nucleus microcircuits and their reorganization by fasting. Nat. Neurosci. 8, 1356-1363.
51. Tennese, A.A., and Wevrick, R. (2011). Impaired hypothalamic regulation of endocrine function and delayed counterregulatory response to hypoglycemia in Magel2-null mice. Endocrinology 152, 967-978.
52. Thompson, D.A., Pénicaud, L., Welle, S.L., and Jacobs, L.S. (1985). Pharmacological evidence for opioid and adrenergic mechanisms controlling growth hormone, prolactin, pancreatic polypeptide, and catecholamine levels in humans. Metabolism 34, 383-390.
53. Treherne, J.M., and Ashford, M.L. (1991). Calcium-activated potassium channels in rat dissociated ventromedial hypothalamic neurons. J. Neuroendocrinol. 3, 323-329.
54. Wang, R., Liu, X., Hentges, S.T., Dunn-Meynell, A.A., Levin, B.E., Wang, W., and Routh, V.H. (2004). The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 53, 1959-1965.
55. Yang, X.W., Model, P., and 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.
56. Zhou, L., Podolsky, N., Sang, Z., Ding, Y., Fan, X., Tong, Q., Levin, B.E., and McCrimmon, R.J. (2010). The medial amygdalar nucleus: a novel glucosesensing region that modulates the counterregulatory response to hypoglycemia. Diabetes 59, 2646-2652.
57. Zhou, L., Yueh, C.Y., Lam, D.D., Shaw, J., Osundiji, M., Garfield, A.S., Evans, M., and Heisler, L.K. (2011). Glucokinase inhibitor glucosamine stimulates feeding and activates hypothalamic neuropeptide Y and orexin neurons. Behav. Brain Res. 222, 274-278.