Npvf: Hypothalamic Biomarker of Ambient Temperature Independent of Nutritional Status

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Current knowledge does not provide a clear, definite view of central mechanisms controlling energy balance upon cold-activated thermogenesis. Here we show that upon cold exposure lean mice maintain body composition but increase food intake to fuel thermogenesis, whereas cold-exposed mice with DIO utilize endogenous fat stores and then transition to increased food intake as body composition approaches that of the lean controls. Using knockout mice with leptin and Ucp1 gene deficiency our study indicates that the relative energy utilization from food intake and endogenous energy reserves to maintain body temperature during cold exposure is independent of both leptin action and brown fat-linked thermogenesis. Using a combination of genetic and biological approaches, we demonstrate that Npvf gene expression in the hypothalamus is regulated by changes in ambient temperature in a manner independent of the nutritional status of the mouse.

Vyšlo v časopise: Npvf: Hypothalamic Biomarker of Ambient Temperature Independent of Nutritional Status. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005287
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005287

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Zdroje

1. Seale P, Lazar MA (2009) Brown fat in humans: turning up the heat on obesity. Diabetes 58: 1482–1484. doi: 10.2337/db09-0622 19564460

2. Caudwell P, Gibbons C, Hopkins M, Naslund E, King N, et al. (2011) The influence of physical activity on appetite control: an experimental system to understand the relationship between exercise-induced energy expenditure and energy intake. Proc Nutr Soc 70: 171–180. doi: 10.1017/S0029665110004751 21226975

3. Kennedy GC (1953) The role of depot fat in the hypothalamic control of food intake in the rat. Proc R Soc Lond B Biol Sci 140: 578–596. 13027283

4. Cannon B, Nedergaard J (2009) Thermogenesis challenges the adipostat hypothesis for body-weight control. Proc Nutr Soc 68: 401–407. doi: 10.1017/S0029665109990255 19775494

5. Arch JR (2008) The discovery of drugs for obesity, the metabolic effects of leptin and variable receptor pharmacology: perspectives from beta3-adrenoceptor agonists. Naunyn Schmiedebergs Arch Pharmacol 378: 225–240. doi: 10.1007/s00210-008-0271-1 18612674

6. Melnyk A, Himms-Hagen J (1998) Temperature-dependent feeding: lack of role for leptin and defect in brown adipose tissue-ablated obese mice. Am J Physiol 274: R1131–1135. 9575979

7. Perello M, Stuart RC, Vaslet CA, Nillni EA (2007) Cold exposure increases the biosynthesis and proteolytic processing of prothyrotropin-releasing hormone in the hypothalamic paraventricular nucleus via beta-adrenoreceptors. Endocrinology 148: 4952–4964. 17584968

8. Park JJ, Lee HK, Shin MW, Kim SJ, Noh SY, et al. (2007) Short-term cold exposure may cause a local decrease of neuropeptide Y in the rat hypothalamus. Mol Cells 23: 88–93. 17464216

9. Cabral A, Valdivia S, Reynaldo M, Cyr NE, Nillni EA, et al. (2012) Short-term cold exposure activates TRH neurons exclusively in the hypothalamic paraventricular nucleus and raphe pallidus. Neurosci Lett 518: 86–91. doi: 10.1016/j.neulet.2012.04.059 22580206

10. Pereira-da-Silva M, Torsoni MA, Nourani HV, Augusto VD, Souza CT, et al. (2003) Hypothalamic melanin-concentrating hormone is induced by cold exposure and participates in the control of energy expenditure in rats. Endocrinology 144: 4831–4840. 12960043

11. Sanchez E, Fekete C, Lechan RM, Joseph-Bravo P (2007) Cocaine- and amphetamine-regulated transcript (CART) expression is differentially regulated in the hypothalamic paraventricular nucleus of lactating rats exposed to suckling or cold stimulation. Brain Res 1132: 120–128. 17174283

12. McCarthy HD, Kilpatrick AP, Trayhurn P, Williams G (1993) Widespread increases in regional hypothalamic neuropeptide Y levels in acute cold-exposed rats. Neuroscience 54: 127–132. 8515838

13. Egawa M, Yoshimatsu H, Bray GA (1991) Neuropeptide Y suppresses sympathetic activity to interscapular brown adipose tissue in rats. Am J Physiol 260: R328–334. 1996720

14. Small CJ, Liu YL, Stanley SA, Connoley IP, Kennedy A, et al. (2003) Chronic CNS administration of Agouti-related protein (Agrp) reduces energy expenditure. Int J Obes Relat Metab Disord 27: 530–533. 12664087

15. Chao PT, Yang L, Aja S, Moran TH, Bi S (2011) Knockdown of NPY expression in the dorsomedial hypothalamus promotes development of brown adipocytes and prevents diet-induced obesity. Cell Metab 13: 573–583. doi: 10.1016/j.cmet.2011.02.019 21531339

16. Dimitrov EL, Kim YY, Usdin TB (2011) Regulation of hypothalamic signaling by tuberoinfundibular peptide of 39 residues is critical for the response to cold: a novel peptidergic mechanism of thermoregulation. J Neurosci 31: 18166–18179. doi: 10.1523/JNEUROSCI.2619-11.2011 22159128

17. Nillni EA, Xie W, Mulcahy L, Sanchez VC, Wetsel WC (2002) Deficiencies in pro-thyrotropin-releasing hormone processing and abnormalities in thermoregulation in Cpefat/fat mice. J Biol Chem 277: 48587–48595. 12270926

18. Koza RA, Nikonova L, Hogan J, Rim JS, Mendoza T, et al. (2006) Changes in gene expression foreshadow diet-induced obesity in genetically identical mice. PLoS Genet 2: e81. 16733553

19. Ukropec J, Anunciado RV, Ravussin Y, Kozak LP (2006) Leptin is required for uncoupling protein-1-independent thermogenesis during cold stress. Endocrinology 147: 2468–2480. 16469807

20. Coleman DL (1982) Thermogenesis in diabetes-obesity syndromes in mutant mice. Diabetologia 22: 205–211. 7075918

21. Trayhurn P, James WP (1978) Thermoregulation and non-shivering thermogenesis in the genetically obese (ob/ob) mouse. Pflugers Arch 373: 189–193. 565045

22. Enerback S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, et al. (1997) Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387: 90–94. 9169872

23. Liu X, Rossmeisl M, McClaine J, Riachi M, Harper ME, et al. (2003) Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Invest 111: 399–407. 12569166

24. Golozoubova V, Hohtola E, Matthias A, Jacobsson A, Cannon B, et al. (2001) Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J 15: 2048–2050. 11511509

25. Ukropec J, Anunciado RP, Ravussin Y, Hulver MW, Kozak LP (2006) UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1-/- mice. J Biol Chem 281: 31894–31908. 16914547

26. Johnson MS, Speakman JR (2001) Limits to sustained energy intake. V. Effect of cold-exposure during lactation in Mus musculus. J Exp Biol 204: 1967–1977. 11441038

27. Melzer K, Kayser B, Saris WH, Pichard C (2005) Effects of physical activity on food intake. Clin Nutr 24: 885–895. 16039759

28. Brobeck JR (1948) Food intake as a mechanism of temperature regulation. Yale J Biol Med 20: 545–552. 18872321

29. Leibel RL, Rosenbaum M, Hirsch J (1995) Changes in energy expenditure resulting from altered body weight. N Engl J Med 332: 621–628. 7632212

30. Bukowiecki LJ (1989) Energy balance and diabetes. The effects of cold exposure, exercise training, and diet composition on glucose tolerance and glucose metabolism in rat peripheral tissues. Can J Physiol Pharmacol 67: 382–393. 2667731

31. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, et al. (2002) Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415: 339–343. 11797013

32. Guerra C, Koza RA, Walsh K, Kurtz DM, Wood PA, et al. (1998) Abnormal nonshivering thermogenesis in mice with inherited defects of fatty acid oxidation. J Clin Invest 102: 1724–1731. 9802886

33. Harris RB, Mitchell TD, Kelso EW, Flatt WP (2007) Changes in environmental temperature influence leptin responsiveness in low- and high-fat-fed mice. Am J Physiol Regul Integr Comp Physiol 293: R106–115. 17442784

34. Bing C, Frankish HM, Pickavance L, Wang Q, Hopkins DF, et al. (1998) Hyperphagia in cold-exposed rats is accompanied by decreased plasma leptin but unchanged hypothalamic NPY. Am J Physiol 274: R62–68. 9458899

35. Zhao ZJ (2011) Serum leptin, energy budget, and thermogenesis in striped hamsters exposed to consecutive decreases in ambient temperatures. Physiol Biochem Zool 84: 560–572. doi: 10.1086/662553 22030849

36. Krol E, Speakman JR (2003) Limits to sustained energy intake. VI. Energetics of lactation in laboratory mice at thermoneutrality. J Exp Biol 206: 4255–4266. 14581596

37. Speakman JR, Krol E (2011) Limits to sustained energy intake. XIII. Recent progress and future perspectives. J Exp Biol 214: 230–241. doi: 10.1242/jeb.048603 21177943

38. El-Haschimi K, Pierroz DD, Hileman SM, Bjorbaek C, Flier JS (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105: 1827–1832. 10862798

39. Yoneshiro T, Aita S, Matsushita M, Okamatsu-Ogura Y, Kameya T, et al. (2011) Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity (Silver Spring) 19: 1755–1760. doi: 10.1038/oby.2011.125 21566561

40. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, et al. (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360: 1509–1517. doi: 10.1056/NEJMoa0810780 19357406

41. Hofmann WE, Liu X, Bearden CM, Harper ME, Kozak LP (2001) Effects of genetic background on thermoregulation and fatty acid-induced uncoupling of mitochondria in UCP1-deficient mice. J Biol Chem 276: 12460–12465. 11279075

42. Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, et al. (2001) Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276: 36961–36969. 11481330

43. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, et al. (2000) New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2: 703–708. 11025660

44. Johnson MA, Tsutsui K, Fraley GS (2007) Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav 51: 171–180. 17113584

45. Yang HY, Fratta W, Majane EA, Costa E (1985) Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci U S A 82: 7757–7761. 3865193

46. Jhamandas JH, Goncharuk V (2013) Role of neuropeptide FF in central cardiovascular and neuroendocrine regulation. Front Endocrinol (Lausanne) 4: 8.

47. Tachibana T, Sato M, Takahashi H, Ukena K, Tsutsui K, et al. (2005) Gonadotropin-inhibiting hormone stimulates feeding behavior in chicks. Brain Res 1050: 94–100. 15979587

48. Cline MA, Bowden CN, Calchary WA, Layne JE (2008) Short-term anorexigenic effects of central neuropeptide VF are associated with hypothalamic changes in chicks. J Neuroendocrinol 20: 971–977. doi: 10.1111/j.1365-2826.2008.01749.x 18540998

49. Chartrel N, Dujardin C, Anouar Y, Leprince J, Decker A, et al. (2003) Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc Natl Acad Sci U S A 100: 15247–15252. 14657341

50. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, et al. (2008) Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol 199: 105–112. doi: 10.1677/JOE-08-0197 18653621

51. Klingerman CM, Williams WP 3rd, Simberlund J, Brahme N, Prasad A, et al. (2011) Food Restriction-Induced Changes in Gonadotropin-Inhibiting Hormone Cells are Associated with Changes in Sexual Motivation and Food Hoarding, but not Sexual Performance and Food Intake. Front Endocrinol (Lausanne) 2: 101. doi: 10.3389/fendo.2011.00101 22649396

52. Yano T, Iijima N, Kakihara K, Hinuma S, Tanaka M, et al. (2003) Localization and neuronal response of RFamide related peptides in the rat central nervous system. Brain Res 982: 156–167. 12915251

53. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, et al. (2006) Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A 103: 2410–2415. 16467147

54. Morrison SF, Madden CJ, Tupone D (2014) Central Neural Regulation of Brown Adipose Tissue Thermogenesis and Energy Expenditure. Cell Metab.

55. Rizwan MZ, Harbid AA, Inglis MA, Quennell JH, Anderson GM (2014) Evidence that hypothalamic RFamide related peptide-3 neurones are not leptin-responsive in mice and rats. J Neuroendocrinol 26: 247–257. doi: 10.1111/jne.12140 24612072