Advertisement

Tobacco Smoking, Food Intake, and Weight Control

  • Ming D. Li
Chapter

Abstract

Beyond promoting smoking initiation and preventing smokers from quitting, nicotine can reduce food intake and body weight and thus is seen as desirable by some smokers, perhaps especially women. During the last several decades, the molecular mechanisms underlying the inverse correlation between smoking and body weight have been investigated extensively. This appears to be especially true for the stimulation by nicotine of α3β4 nAChRs receptors, which are located on proopiomelanocortin (POMC) neurons in the arcuate nucleus (ARC), leading to the activation of the melanocortin (MC) brain circuit that is associated with food intake. Further, α7- and α4β2-containing nAChRs have been implicated in energy homeostasis, and the effects of peripheral hormones such as leptin, ghrelin, and peptide YY (PYY) are mediated by alterations in the MC circuit. This chapter summarizes current understanding of the regulatory effects of nicotine on food intake and body weight according to the findings from the pharmacological, molecular genetics, electrophysiological, and feeding studies on these appetite-regulating molecules, such as α3β4, α7, α4β2 nAChRs, neuropeptide Y, POMC, melanocortin 4 receptor, agouti-related peptide (AgRP), leptin, ghrelin, and PYY.

Keywords

Body weight Food intake nAChRs α3β4 α7 α4β2 nAChRs Neuropeptide Y POMC Melanocortin 4 receptor Agouti-related peptide (AgRP) Leptin Ghrelin PYY 

References

  1. Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, Elsworth JD, Roth RH, Sleeman MW, Picciotto MR, Tschop MH, Gao XB, Horvath TL (2006) Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 116:3229–3239. https://doi.org/10.1172/JCI29867 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E, Flier JS (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382:250–252. https://doi.org/10.1038/382250a0 PubMedCrossRefGoogle Scholar
  3. Al’Absi M, Lemieux A, Nakajima M (2014) Peptide YY and ghrelin predict craving and risk for relapse in abstinent smokers. Psychoneuroendocrinology 49:253–259. https://doi.org/10.1016/j.psyneuen.2014.07.018 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Albanes D, Jones DY, Micozzi MS, Mattson ME (1987) Associations between smoking and body weight in the US population: analysis of NHANES II. Am J Public Health 77:439–444PubMedPubMedCentralCrossRefGoogle Scholar
  5. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73–120. https://doi.org/10.1152/physrev.00015.2008 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow TJ, Bloom SR, Polak JM (1983) Neuropeptide Y distribution in the rat brain. Science 221:877–879PubMedCrossRefGoogle Scholar
  7. Andersson K, Arner P (2001) Systemic nicotine stimulates human adipose tissue lipolysis through local cholinergic and catecholaminergic receptors. Int J Obes Relat Metab Disord 25:1225–1232. https://doi.org/10.1038/sj.ijo.0801654 PubMedCrossRefGoogle Scholar
  8. Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P (2012) Weight gain in smokers after quitting cigarettes: meta-analysis. BMJ 345:e4439. https://doi.org/10.1136/bmj.e4439 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Banks WA, Tschop M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302:822–827. https://doi.org/10.1124/jpet.102.034827 PubMedCrossRefGoogle Scholar
  10. Batterham RL, Bloom SR (2003) The gut hormone peptide YY regulates appetite. Ann N Y Acad Sci 994:162–168PubMedCrossRefGoogle Scholar
  11. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR (2002) Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418:650–654. https://doi.org/10.1038/nature02666 PubMedCrossRefGoogle Scholar
  12. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, Ghatei MA, Bloom SR (2003) Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 349:941–948. https://doi.org/10.1056/NEJMoa030204 PubMedCrossRefGoogle Scholar
  13. Batterham RL, Heffron H, Kapoor S, Chivers JE, Chandarana K, Herzog H, Le Roux CW, Thomas EL, Bell JD, Withers DJ (2006) Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab 4:223–233. https://doi.org/10.1016/j.cmet.2006.08.001 PubMedCrossRefGoogle Scholar
  14. Bencherif M, Lippiello PM, Lucas R, Marrero MB (2011) Alpha7 nicotinic receptors as novel therapeutic targets for inflammation-based diseases. Cell Mol Life Sci 68:931–949. https://doi.org/10.1007/s00018-010-0525-1 PubMedCrossRefGoogle Scholar
  15. Boggiano MM, Chandler PC, Oswald KD, Rodgers RJ, Blundell JE, Ishii Y, Beattie AH, Holch P, Allison DB, Schindler M, Arndt K, Rudolf K, Mark M, Schoelch C, Joost HG, Klaus S, Thone-Reineke C, Benoit SC, Seeley RJ, Beck-Sickinger AG, Koglin N, Raun K, Madsen K, Wulff BS, Stidsen CE, Birringer M, Kreuzer OJ, Deng XY, Whitcomb DC, Halem H, Taylor J, Dong J, Datta R, Culler M, Ortmann S, Castaneda TR, Tschop M (2005) PYY3-36 as an anti-obesity drug target. Obes Rev 6:307–322. https://doi.org/10.1111/j.1467-789X.2005.00218.x PubMedCrossRefGoogle Scholar
  16. Bouloumie A, Curat CA, Sengenes C, Lolmede K, Miranville A, Busse R (2005) Role of macrophage tissue infiltration in metabolic diseases. Curr Opin Clin Nutr Metab Care 8:347–354PubMedCrossRefGoogle Scholar
  17. Bourlier V, Bouloumie A (2009) Role of macrophage tissue infiltration in obesity and insulin resistance. Diabetes Metab 35:251–260. https://doi.org/10.1016/j.diabet.2009.05.001 PubMedCrossRefGoogle Scholar
  18. Brady LS, Smith MA, Gold PW, Herkenham M (1990) Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 52:441–447PubMedCrossRefGoogle Scholar
  19. Breen TL, Conwell IM, Wardlaw SL (2005) Effects of fasting, leptin, and insulin on AGRP and POMC peptide release in the hypothalamus. Brain Res 1032:141–148. https://doi.org/10.1016/j.brainres.2004.11.008 PubMedCrossRefGoogle Scholar
  20. Breese CR, Marks MJ, Logel J, Adams CE, Sullivan B, Collins AC, Leonard S (1997) Effect of smoking history on [3H]nicotine binding in human postmortem brain. J Pharmacol Exp Ther 282:7–13PubMedGoogle Scholar
  21. Brugman S, Clegg DJ, Woods SC, Seeley RJ (2002) Combined blockade of both micro – and kappa-opioid receptors prevents the acute orexigenic action of agouti-related protein. Endocrinology 143:4265–4270. https://doi.org/10.1210/en.2002-220230 PubMedCrossRefGoogle Scholar
  22. Burnstock G (1987) Mechanisms of interaction of peptide and nonpeptide vascular neurotransmitter systems. J Cardiovasc Pharmacol 10(Suppl 12):S74–S81PubMedGoogle Scholar
  23. Cancello R, Clement K (2006) Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. BJOG 113:1141–1147. https://doi.org/10.1111/j.1471-0528.2006.01004.x PubMedCrossRefGoogle Scholar
  24. Cancello R, Zulian A, Maestrini S, Mencarelli M, Della Barba A, Invitti C, Liuzzi A, Di Blasio AM (2012) The nicotinic acetylcholine receptor alpha7 in subcutaneous mature adipocytes: downregulation in human obesity and modulation by diet-induced weight loss. Int J Obes 36:1552–1557. https://doi.org/10.1038/ijo.2011.275 CrossRefGoogle Scholar
  25. Challis BG, Pinnock SB, Coll AP, Carter RN, Dickson SL, O’Rahilly S (2003) Acute effects of PYY3-36 on food intake and hypothalamic neuropeptide expression in the mouse. Biochem Biophys Res Commun 311:915–919PubMedCrossRefGoogle Scholar
  26. Chen H, Vlahos R, Bozinovski S, Jones J, Anderson GP, Morris MJ (2005) Effect of short-term cigarette smoke exposure on body weight, appetite and brain neuropeptide Y in mice. Neuropsychopharmacology 30:713–719. https://doi.org/10.1038/sj.npp.1300597 PubMedCrossRefGoogle Scholar
  27. Chen H, Hansen MJ, Jones JE, Vlahos R, Bozinovski S, Anderson GP, Morris MJ (2006) Cigarette smoke exposure reprograms the hypothalamic neuropeptide Y axis to promote weight loss. Am J Respir Crit Care Med 173:1248–1254. https://doi.org/10.1164/rccm.200506-977OC PubMedCrossRefGoogle Scholar
  28. Chen H, Saad S, Sandow SL, Bertrand PP (2012) Cigarette smoking and brain regulation of energy homeostasis. Front Pharmacol 3:147. https://doi.org/10.3389/fphar.2012.00147 PubMedPubMedCentralGoogle Scholar
  29. Cheng PY, Lee YM, Law KK, Lin CW, Yen MH (2007) The involvement of AMP-activated protein kinases in the anti-inflammatory effect of nicotine in vivo and in vitro. Biochem Pharmacol 74:1758–1765. https://doi.org/10.1016/j.bcp.2007.08.004 PubMedCrossRefGoogle Scholar
  30. Collins S, Kuhn CM, Petro AE, Swick AG, Chrunyk BA, Surwit RS (1996) Role of leptin in fat regulation. Nature 380:677. https://doi.org/10.1038/380677a0 PubMedCrossRefGoogle Scholar
  31. Cone RD (2005) Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571–578. https://doi.org/10.1038/nn1455 PubMedCrossRefGoogle Scholar
  32. Corrigall WA, Franklin KB, Coen KM, Clarke PB (1992) The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 107:285–289CrossRefGoogle Scholar
  33. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, Horvath TL (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37:649–661PubMedCrossRefGoogle Scholar
  34. Cummings DE, Frayo RS, Marmonier C, Aubert R, Chapelot D (2004) Plasma ghrelin levels and hunger scores in humans initiating meals voluntarily without time- and food-related cues. Am J Physiol Endocrinol Metab 287:E297–E304. https://doi.org/10.1152/ajpendo.00582.2003 PubMedCrossRefGoogle Scholar
  35. Dani JA, Bertrand D (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47:699–729. https://doi.org/10.1146/annurev.pharmtox.47.120505.105214 PubMedCrossRefGoogle Scholar
  36. Dezfuli G, Kellar KJ, Dretchen KL, Tizabi Y, Sahibzada N, Gillis RA (2016) Evidence for the role of beta2* nAChR desensitization in regulating body weight in obese mice. Neuropharmacology 110:165–174. https://doi.org/10.1016/j.neuropharm.2016.07.020 PubMedCrossRefGoogle Scholar
  37. Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, Horvath B, Gaskin FS, Nonaka N, Jaeger LB, Banks WA, Morley JE, Pinto S, Sherwin RS, Xu L, Yamada KA, Sleeman MW, Tschop MH, Horvath TL (2006) Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 9:381–388. https://doi.org/10.1038/nn1656 PubMedCrossRefGoogle Scholar
  38. Dickson SL, Hrabovszky E, Hansson C, Jerlhag E, Alvarez-Crespo M, Skibicka KP, Molnar CS, Liposits Z, Engel JA, Egecioglu E (2010) Blockade of central nicotine acetylcholine receptor signaling attenuate ghrelin-induced food intake in rodents. Neuroscience 171:1180–1186. https://doi.org/10.1016/j.neuroscience.2010.10.005 PubMedCrossRefGoogle Scholar
  39. Egecioglu E, Jerlhag E, Salome N, Skibicka KP, Haage D, Bohlooly YM, Andersson D, Bjursell M, Perrissoud D, Engel JA, Dickson SL (2010) Ghrelin increases intake of rewarding food in rodents. Addict Biol 15:304–311. https://doi.org/10.1111/j.1369-1600.2010.00216.x PubMedPubMedCentralCrossRefGoogle Scholar
  40. Eliasson B, Smith U (1999) Leptin levels in smokers and long-term users of nicotine gum. Eur J Clin Investig 29:145–152CrossRefGoogle Scholar
  41. Elmquist JK, Maratos-Flier E, Saper CB, Flier JS (1998) Unraveling the central nervous system pathways underlying responses to leptin. Nat Neurosci 1:445–450. https://doi.org/10.1038/2164 PubMedCrossRefGoogle Scholar
  42. Engel JA, Jerlhag E (2014) Role of appetite-regulating peptides in the pathophysiology of addiction: implications for pharmacotherapy. CNS Drugs 28:875–886. https://doi.org/10.1007/s40263-014-0178-y PubMedPubMedCentralCrossRefGoogle Scholar
  43. Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 307:491–497. https://doi.org/10.1001/jama.2012.39 PubMedCrossRefGoogle Scholar
  44. Fornari A, Pedrazzi P, Lippi G, Picciotto MR, Zoli M, Zini I (2007) Nicotine withdrawal increases body weight, neuropeptide Y and agouti-related protein expression in the hypothalamus and decreases uncoupling protein-3 expression in the brown adipose tissue in high-fat fed mice. Neurosci Lett 411:72–76. https://doi.org/10.1016/j.neulet.2006.10.014 PubMedCrossRefGoogle Scholar
  45. Frankish HM, Dryden S, Wang Q, Bing C, MacFarlane IA, Williams G (1995) Nicotine administration reduces neuropeptide Y and neuropeptide Y mRNA concentrations in the rat hypothalamus: NPY may mediate nicotine’s effects on energy balance. Brain Res 694:139–146PubMedCrossRefGoogle Scholar
  46. Freathy RM, Kazeem GR, Morris RW, Johnson PC, Paternoster L, Ebrahim S, Hattersley AT, Hill A, Hingorani AD, Holst C, Jefferis BJ, Kring SI, Mooser V, Padmanabhan S, Preisig M, Ring SM, Sattar N, Upton MN, Vollenweider P, Waeber G, Sorensen TI, Frayling TM, Watt G, Lawlor DA, Whincup PH, Tozzi F, Davey Smith G, Munafo M (2011) Genetic variation at CHRNA5-CHRNA3-CHRNB4 interacts with smoking status to influence body mass index. Int J Epidemiol 40:1617–1628. https://doi.org/10.1093/ije/dyr077 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Fruhbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393:7–20. https://doi.org/10.1042/BJ20051578 PubMedCrossRefGoogle Scholar
  48. Fulton S (2010) Appetite and reward. Front Neuroendocrinol 31:85–103. https://doi.org/10.1016/j.yfrne.2009.10.003 PubMedCrossRefGoogle Scholar
  49. Gomez G, Lambertz I, Udupi V, Qi X, Thompson JC, Greeley GH Jr (1996) Influence of nicotine on gastrin and peptide YY in the rat. Regul Pept 67:55–61PubMedCrossRefGoogle Scholar
  50. Grady SR, Moretti M, Zoli M, Marks MJ, Zanardi A, Pucci L, Clementi F, Gotti C (2009) Rodent habenulo-interpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release. J Neurosci 29:2272–2282. https://doi.org/10.1523/JNEUROSCI.5121-08.2009 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Graupner M, Maex R, Gutkin B (2013) Endogenous cholinergic inputs and local circuit mechanisms govern the phasic mesolimbic dopamine response to nicotine. PLoS Comput Biol 9:e1003183. https://doi.org/10.1371/journal.pcbi.1003183 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Grossman HC, Hadjimarkou MM, Silva RM, Giraudo SQ, Bodnar RJ (2003) Interrelationships between mu opioid and melanocortin receptors in mediating food intake in rats. Brain Res 991:240–244PubMedCrossRefGoogle Scholar
  53. Grunberg NE (1991) Smoking cessation and weight gain. N Engl J Med 324:768–769. https://doi.org/10.1056/NEJM199103143241111 PubMedCrossRefGoogle Scholar
  54. Grunberg NE, Winders SE, Popp KA (1987) Sex differences in nicotine’s effects on consummatory behavior and body weight in rats. Psychopharmacology (Berl) 91:221–225CrossRefGoogle Scholar
  55. Gualillo O, Eiras S, Lago F, Dieguez C, Casanueva FF (2000) Elevated serum leptin concentrations induced by experimental acute inflammation. Life Sci 67:2433–2441PubMedCrossRefGoogle Scholar
  56. Hagan MM, Rushing PA, Benoit SC, Woods SC, Seeley RJ (2001) Opioid receptor involvement in the effect of AgRP- (83-132) on food intake and food selection. Am J Phys Regul Integr Comp Phys 280:R814–R821Google Scholar
  57. Han ZY, Le Novere N, Zoli M, Hill JA Jr, Champtiaux N, Changeux JP (2000) Localization of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur J Neurosci 12:3664–3674PubMedCrossRefGoogle Scholar
  58. Han ZY, Zoli M, Cardona A, Bourgeois JP, Changeux JP, Le Novere N (2003) Localization of [3H]nicotine, [3H]cytisine, [3H]epibatidine, and [125I]alpha-bungarotoxin binding sites in the brain of Macaca Mulatta. J Comp Neurol 461:49–60. https://doi.org/10.1002/cne.10659 PubMedCrossRefGoogle Scholar
  59. Hansson C, Haage D, Taube M, Egecioglu E, Salome N, Dickson SL (2011) Central administration of ghrelin alters emotional responses in rats: behavioural, electrophysiological and molecular evidence. Neuroscience 180:201–211. https://doi.org/10.1016/j.neuroscience.2011.02.002 PubMedCrossRefGoogle Scholar
  60. Haslam DW, James WP (2005) Obesity. Lancet 366:1197–1209. https://doi.org/10.1016/S0140-6736(05)67483-1 PubMedCrossRefGoogle Scholar
  61. Higuchi H, Yang HY, Costa E (1988) Age-related bidirectional changes in neuropeptide Y peptides in rat adrenal glands, brain, and blood. J Neurochem 50:1879–1886PubMedCrossRefGoogle Scholar
  62. Hiremagalur B, Sabban EL (1995) Nicotine elicits changes in expression of adrenal catecholamine biosynthetic enzymes, neuropeptide Y and immediate early genes by injection but not continuous administration. Brain Res Mol Brain Res 32:109–115PubMedCrossRefGoogle Scholar
  63. Hodge AM, Westerman RA, de Courten MP, Collier GR, Zimmet PZ, Alberti KG (1997) Is leptin sensitivity the link between smoking cessation and weight gain? Int J Obes Relat Metab Disord 21:50–53PubMedCrossRefGoogle Scholar
  64. Horvath TL, Diano S, Tschop M (2004) Brain circuits regulating energy homeostasis. Neuroscientist 10:235–246. https://doi.org/10.1177/1073858403262151 PubMedCrossRefGoogle Scholar
  65. Huang H, Xu Y, van den Pol AN (2011) Nicotine excites hypothalamic arcuate anorexigenic proopiomelanocortin neurons and orexigenic neuropeptide Y neurons: similarities and differences. J Neurophysiol 106:1191–1202. https://doi.org/10.1152/jn.00740.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hur YN, Hong GH, Choi SH, Shin KH, Chun BG (2010) High fat diet altered the mechanism of energy homeostasis induced by nicotine and withdrawal in C57BL/6 mice. Mol Cell 30:219–226. https://doi.org/10.1007/s10059-010-0110-3 CrossRefGoogle Scholar
  67. Hussain T, Al-Daghri NM, Al-Attas OS, Draz HM, Abd Al-Rahman SH, Yakout SM (2012) Plasma neuropeptide Y levels relate cigarette smoking and smoking cessation to body weight regulation. Regul Pept 176:22–27. https://doi.org/10.1016/j.regpep.2012.02.005 PubMedCrossRefGoogle Scholar
  68. Hussmann GP, DeDominicis KE, Turner JR, Yasuda RP, Klehm J, Forcelli PA, Xiao Y, Richardson JR, Sahibzada N, Wolfe BB, Lindstrom J, Blendy JA, Kellar KJ (2014) Chronic sazetidine-A maintains anxiolytic effects and slower weight gain following chronic nicotine without maintaining increased density of nicotinic receptors in rodent brain. J Neurochem 129:721–731. https://doi.org/10.1111/jnc.12653 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, Gu W, Kesterson RA, Boston BA, Cone RD, Smith FJ, Campfield LA, Burn P, Lee F (1997) Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88:131–141PubMedCrossRefGoogle Scholar
  70. Imamura M (2002) Effects of surgical manipulation of the intestine on peptide YY and its physiology. Peptides 23:403–407PubMedCrossRefGoogle Scholar
  71. Jerlhag E, Egecioglu E, Dickson SL, Svensson L, Engel JA (2008) Alpha-conotoxin MII-sensitive nicotinic acetylcholine receptors are involved in mediating the ghrelin-induced locomotor stimulation and dopamine overflow in nucleus accumbens. Eur Neuropsychopharmacol 18:508–518. https://doi.org/10.1016/j.euroneuro.2008.02.006 PubMedCrossRefGoogle Scholar
  72. Jerlhag E, Janson AC, Waters S, Engel JA (2012) Concomitant release of ventral tegmental acetylcholine and accumbal dopamine by ghrelin in rats. PLoS One 7:e49557. https://doi.org/10.1371/journal.pone.0049557 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Jha P (2009) Avoidable global cancer deaths and total deaths from smoking. Nat Rev Cancer 9:655–664. https://doi.org/10.1038/nrc2703 PubMedCrossRefGoogle Scholar
  74. Josselyn SA, Beninger RJ (1993) Neuropeptide Y: intraaccumbens injections produce a place preference that is blocked by cis-flupenthixol. Pharmacol Biochem Behav 46:543–552PubMedCrossRefGoogle Scholar
  75. Kageyama H, Takenoya F, Hirako S, Wada N, Kintaka Y, Inoue S, Ota E, Ogawa T, Shioda S (2012) Neuronal circuits involving neuropeptide Y in hypothalamic arcuate nucleus-mediated feeding regulation. Neuropeptides 46:285–289. https://doi.org/10.1016/j.npep.2012.09.007 PubMedCrossRefGoogle Scholar
  76. Kalkman HO, Feuerbach D (2016) Modulatory effects of alpha7 nAChRs on the immune system and its relevance for CNS disorders. Cell Mol Life Sci 73:2511–2530. https://doi.org/10.1007/s00018-016-2175-4 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kane JK, Parker SL, Li MD (2001) Hypothalamic orexin-A binding sites are downregulated by chronic nicotine treatment in the rat. Neurosci Lett 298:1–4PubMedCrossRefGoogle Scholar
  78. Karra E, Batterham RL (2010) The role of gut hormones in the regulation of body weight and energy homeostasis. Mol Cell Endocrinol 316:120–128. https://doi.org/10.1016/j.mce.2009.06.010 PubMedCrossRefGoogle Scholar
  79. Kastin AJ, Akerstrom V (1999) Nonsaturable entry of neuropeptide Y into brain. Am J Phys 276:E479–E482Google Scholar
  80. Kishi T, Aschkenasi CJ, Lee CE, Mountjoy KG, Saper CB, Elmquist JK (2003) Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 457:213–235. https://doi.org/10.1002/cne.10454 PubMedCrossRefGoogle Scholar
  81. Klesges RC, Ward KD, Ray JW, Cutter G, Jacobs DR Jr, Wagenknecht LE (1998) The prospective relationships between smoking and weight in a young, biracial cohort: the coronary artery risk development in young adults study. J Consult Clin Psychol 66:987–993PubMedCrossRefGoogle Scholar
  82. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660. https://doi.org/10.1038/45230 PubMedCrossRefGoogle Scholar
  83. Koopmann A, Bez J, Lemenager T, Hermann D, Dinter C, Reinhard I, Hoffmann H, Wiedemann K, Winterer G, Kiefer F (2015) Effects of cigarette smoking on plasma concentration of the appetite-regulating peptide ghrelin. Ann Nutr Metab 66:155–161. https://doi.org/10.1159/000381834 PubMedCrossRefGoogle Scholar
  84. Kotz CM, Grace MK, Billington CJ, Levine AS (1993) The effect of norbinaltorphimine, beta-funaltrexamine and naltrindole on NPY-induced feeding. Brain Res 631:325–328PubMedCrossRefGoogle Scholar
  85. Kroemer NB, Wuttig F, Bidlingmaier M, Zimmermann US, Smolka MN (2015) Nicotine enhances modulation of food-cue reactivity by leptin and ghrelin in the ventromedial prefrontal cortex. Addict Biol 20:832–844. https://doi.org/10.1111/adb.12167 PubMedCrossRefGoogle Scholar
  86. Krude H, Biebermann H, Schnabel D, Tansek MZ, Theunissen P, Mullis PE, Gruters A (2003) Obesity due to proopiomelanocortin deficiency: three new cases and treatment trials with thyroid hormone and ACTH4-10. J Clin Endocrinol Metab 88:4633–4640. https://doi.org/10.1210/jc.2003-030502 PubMedCrossRefGoogle Scholar
  87. Lakhan SE, Kirchgessner A (2011) Anti-inflammatory effects of nicotine in obesity and ulcerative colitis. J Transl Med 9:129. https://doi.org/10.1186/1479-5876-9-129 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Larsson A, Engel JA (2004) Neurochemical and behavioral studies on ethanol and nicotine interactions. Neurosci Biobehav Rev 27:713–720. https://doi.org/10.1016/j.neubiorev.2003.11.010 PubMedCrossRefGoogle Scholar
  89. Leinninger GM, Jo YH, Leshan RL, Louis GW, Yang H, Barrera JG, Wilson H, Opland DM, Faouzi MA, Gong Y, Jones JC, Rhodes CJ, Chua S Jr, Diano S, Horvath TL, Seeley RJ, Becker JB, Munzberg H, Myers MG Jr (2009) Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab 10:89–98. https://doi.org/10.1016/j.cmet.2009.06.011 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lemieux AM, Al’Absi M (2017) Changes in circulating peptide YY and ghrelin are associated with early smoking relapse. Biol Psychol. https://doi.org/10.1016/j.biopsycho.2017.03.007
  91. Levine AS, Grace M, Billington CJ (1990) The effect of centrally administered naloxone on deprivation and drug-induced feeding. Pharmacol Biochem Behav 36:409–412PubMedCrossRefGoogle Scholar
  92. Lewis JA, Yakel JL, Pandya AA (2017) Levamisole: a positive allosteric modulator for the alpha3beta4 nicotinic acetylcholine receptors prevents weight gain in CD-1 mice on a high fat diet. Curr Pharm Des 23:1869–1872. https://doi.org/10.2174/1381612822666161201145648 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Li MD, Kane JK (2003) Effect of nicotine on the expression of leptin and forebrain leptin receptors in the rat. Brain Res 991:222–231PubMedCrossRefGoogle Scholar
  94. Li MD, Kane JK, Parker SL, McAllen K, Matta SG, Sharp BM (2000a) Nicotine administration enhances NPY expression in the rat hypothalamus. Brain Res 867:157–164PubMedCrossRefGoogle Scholar
  95. Li MD, Parker SL, Kane JK (2000b) Regulation of feeding-associated peptides and receptors by nicotine. Mol Neurobiol 22:143–165PubMedCrossRefGoogle Scholar
  96. Lin S, Storlien LH, Huang XF (2000) Leptin receptor, NPY, POMC mRNA expression in the diet-induced obese mouse brain. Brain Res 875:89–95PubMedCrossRefGoogle Scholar
  97. Luetje CW, Patrick J (1991) Both alpha- and beta-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 11:837–845PubMedGoogle Scholar
  98. Mao D, Perry DC, Yasuda RP, Wolfe BB, Kellar KJ (2008) The alpha4beta2alpha5 nicotinic cholinergic receptor in rat brain is resistant to up-regulation by nicotine in vivo. J Neurochem 104:446–456. https://doi.org/10.1111/j.1471-4159.2007.05011.x PubMedGoogle Scholar
  99. Marangon K, Herbeth B, Lecomte E, Paul-Dauphin A, Grolier P, Chancerelle Y, Artur Y, Siest G (1998) Diet, antioxidant status, and smoking habits in French men. Am J Clin Nutr 67:231–239PubMedCrossRefGoogle Scholar
  100. Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, Collins AC (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J Neurosci 12:2765–2784PubMedGoogle Scholar
  101. Marks MJ, McClure-Begley TD, Whiteaker P, Salminen O, Brown RW, Cooper J, Collins AC, Lindstrom JM (2011) Increased nicotinic acetylcholine receptor protein underlies chronic nicotine-induced up-regulation of nicotinic agonist binding sites in mouse brain. J Pharmacol Exp Ther 337:187–200. https://doi.org/10.1124/jpet.110.178236 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Marks MJ, O’Neill HC, Wynalda-Camozzi KM, Ortiz NC, Simmons EE, Short CA, Butt CM, McIntosh JM, Grady SR (2015) Chronic treatment with varenicline changes expression of four nAChR binding sites in mice. Neuropharmacology 99:142–155. https://doi.org/10.1016/j.neuropharm.2015.07.019 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Marrero MB, Lucas R, Salet C, Hauser TA, Mazurov A, Lippiello PM, Bencherif M (2010) An alpha7 nicotinic acetylcholine receptor-selective agonist reduces weight gain and metabolic changes in a mouse model of diabetes. J Pharmacol Exp Ther 332:173–180. https://doi.org/10.1124/jpet.109.154633 PubMedCrossRefGoogle Scholar
  104. Martinez de Morentin PB, Whittle AJ, Ferno J, Nogueiras R, Dieguez C, Vidal-Puig A, Lopez M (2012) Nicotine induces negative energy balance through hypothalamic AMP-activated protein kinase. Diabetes 61:807–817. https://doi.org/10.2337/db11-1079 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Maskos U, Molles BE, Pons S, Besson M, Guiard BP, Guilloux JP, Evrard A, Cazala P, Cormier A, Mameli-Engvall M, Dufour N, Cloez-Tayarani I, Bemelmans AP, Mallet J, Gardier AM, David V, Faure P, Granon S, Changeux JP (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436:103–107PubMedCrossRefGoogle Scholar
  106. Masuda Y, Tanaka T, Inomata N, Ohnuma N, Tanaka S, Itoh Z, Hosoda H, Kojima M, Kangawa K (2000) Ghrelin stimulates gastric acid secretion and motility in rats. Biochem Biophys Res Commun 276:905–908. https://doi.org/10.1006/bbrc.2000.3568 PubMedCrossRefGoogle Scholar
  107. McCallum SE, Parameswaran N, Bordia T, Fan H, McIntosh JM, Quik M (2006) Differential regulation of mesolimbic alpha 3/alpha 6 beta 2 and alpha 4 beta 2 nicotinic acetylcholine receptor sites and function after long-term oral nicotine to monkeys. J Pharmacol Exp Ther 318:381–388. https://doi.org/10.1124/jpet.106.104414 PubMedCrossRefGoogle Scholar
  108. McCallum SE, Taraschenko OD, Hathaway ER, Vincent MY, Glick SD (2011) Effects of 18-methoxycoronaridine on ghrelin-induced increases in sucrose intake and accumbal dopamine overflow in female rats. Psychopharmacology 215:247–256. https://doi.org/10.1007/s00213-010-2132-0 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Mineur YS, Abizaid A, Rao Y, Salas R, DiLeone RJ, Gundisch D, Diano S, De Biasi M, Horvath TL, Gao XB, Picciotto MR (2011) Nicotine decreases food intake through activation of POMC neurons. Science 332:1330–1332. https://doi.org/10.1126/science.1201889 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Moretti M, Mugnaini M, Tessari M, Zoli M, Gaimarri A, Manfredi I, Pistillo F, Clementi F, Gotti C (2010) A comparative study of the effects of the intravenous self-administration or subcutaneous minipump infusion of nicotine on the expression of brain neuronal nicotinic receptor subtypes. Mol Pharmacol 78:287–296. https://doi.org/10.1124/mol.110.064071 PubMedCrossRefGoogle Scholar
  111. Naleid AM, Grace MK, Cummings DE, Levine AS (2005) Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides 26:2274–2279. https://doi.org/10.1016/j.peptides.2005.04.025 PubMedCrossRefGoogle Scholar
  112. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P, Huang Q, McClure-Begley T, Lindstrom JM, Labarca C, Collins AC, Marks MJ, Lester HA (2007) Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 27:8202–8218. https://doi.org/10.1523/JNEUROSCI.2199-07.2007 PubMedCrossRefGoogle Scholar
  113. Oeser A, Goffaux J, Snead W, Carlson MG (1999) Plasma leptin concentrations and lipid profiles during nicotine abstinence. Am J Med Sci 318:152–157PubMedCrossRefGoogle Scholar
  114. Olszewski PK, Wirth MM, Grace MK, Levine AS, Giraudo SQ (2001) Evidence of interactions between melanocortin and opioid systems in regulation of feeding. Neuroreport 12:1727–1730PubMedCrossRefGoogle Scholar
  115. Pace CJ, Glick SD, Maisonneuve IM, He LW, Jokiel PA, Kuehne ME, Fleck MW (2004) Novel iboga alkaloid congeners block nicotinic receptors and reduce drug self-administration. Eur J Pharmacol 492:159–167. https://doi.org/10.1016/j.ejphar.2004.03.062 PubMedCrossRefGoogle Scholar
  116. Painsipp E, Herzog H, Holzer P (2010) Evidence from knockout mice that neuropeptide-Y Y2 and Y4 receptor signalling prevents long-term depression-like behaviour caused by immune challenge. J Psychopharmacol 24:1551–1560. https://doi.org/10.1177/0269881109348171 PubMedCrossRefGoogle Scholar
  117. Pankova A, Kralikova E, Kavalkova P, Stepankova L, Zvolska K, Haluzik M (2016) No change in serum incretins levels but rise of leptin levels after smoking cessation: a pilot study. Physiol Res 65:651–659PubMedGoogle Scholar
  118. Papke RL, Heinemann SF (1994) Partial agonist properties of cytisine on neuronal nicotinic receptors containing the beta 2 subunit. Mol Pharmacol 45:142–149PubMedGoogle Scholar
  119. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, Collins F (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269:540–543PubMedCrossRefGoogle Scholar
  120. Perry DC, Davila-Garcia MI, Stockmeier CA, Kellar KJ (1999) Increased nicotinic receptors in brains from smokers: membrane binding and autoradiography studies. J Pharmacol Exp Ther 289:1545–1552PubMedGoogle Scholar
  121. Picciotto MR, Mineur YS (2013) Nicotine, food intake, and activation of POMC neurons. Neuropsychopharmacology 38:245. https://doi.org/10.1038/npp.2012.163 PubMedCrossRefGoogle Scholar
  122. Picciotto MR, Mineur YS (2014) Molecules and circuits involved in nicotine addiction: the many faces of smoking. Neuropharmacology 76(Pt B):545–553. https://doi.org/10.1016/j.neuropharm.2013.04.028 PubMedCrossRefGoogle Scholar
  123. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173–177PubMedCrossRefGoogle Scholar
  124. Proulx E, Piva M, Tian MK, Bailey CD, Lambe EK (2014) Nicotinic acetylcholine receptors in attention circuitry: the role of layer VI neurons of prefrontal cortex. Cell Mol Life Sci 71:1225–1244. https://doi.org/10.1007/s00018-013-1481-3 PubMedCrossRefGoogle Scholar
  125. Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, Perusse L, Bouchard C (2006) The human obesity gene map: the 2005 update. Obesity (Silver Spring) 14:529–644. https://doi.org/10.1038/oby.2006.71 CrossRefGoogle Scholar
  126. Rosenbaum M, Leibel RL (2014) 20 years of leptin: role of leptin in energy homeostasis in humans. J Endocrinol 223:T83–T96. https://doi.org/10.1530/JOE-14-0358 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rudski JM, Grace M, Kuskowski MA, Billington CJ, Levine AS (1996) Behavioral effects of naloxone on neuropeptide Y-induced feeding. Pharmacol Biochem Behav 54:771–777PubMedCrossRefGoogle Scholar
  128. Schick RR, Schusdziarra V, Nussbaumer C, Classen M (1991) Neuropeptide Y and food intake in fasted rats: effect of naloxone and site of action. Brain Res 552:232–239PubMedCrossRefGoogle Scholar
  129. Schloegl H, Percik R, Horstmann A, Villringer A, Stumvoll M (2011) Peptide hormones regulating appetite – focus on neuroimaging studies in humans. Diabetes Metab Res Rev 27:104–112. https://doi.org/10.1002/dmrr.1154 PubMedCrossRefGoogle Scholar
  130. Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG (1996) Identification of targets of leptin action in rat hypothalamus. J Clin Invest 98:1101–1106. https://doi.org/10.1172/JCI118891 PubMedPubMedCentralCrossRefGoogle Scholar
  131. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661–671. https://doi.org/10.1038/35007534 PubMedCrossRefGoogle Scholar
  132. Seeley RJ, Sandoval DA (2011) Neuroscience: weight loss through smoking. Nature 475:176–177. https://doi.org/10.1038/475176a PubMedCrossRefGoogle Scholar
  133. Shin AC, Filatova N, Lindtner C, Chi T, Degann S, Oberlin D, Buettner C (2017) Insulin receptor signaling in POMC, but not AgRP, neurons controls adipose tissue insulin action. Diabetes 66:1560–1571. https://doi.org/10.2337/db16-1238 PubMedCrossRefGoogle Scholar
  134. Skibicka KP, Shirazi RH, Hansson C, Dickson SL (2012) Ghrelin interacts with neuropeptide Y Y1 and opioid receptors to increase food reward. Endocrinology 153:1194–1205. https://doi.org/10.1210/en.2011-1606 PubMedCrossRefGoogle Scholar
  135. Smart JL, Low MJ (2003) Lack of proopiomelanocortin peptides results in obesity and defective adrenal function but normal melanocyte pigmentation in the murine C57BL/6 genetic background. Ann N Y Acad Sci 994:202–210PubMedCrossRefGoogle Scholar
  136. Soderpalm B, Ericson M (2013) Neurocircuitry involved in the development of alcohol addiction: the dopamine system and its access points. Curr Top Behav Neurosci 13:127–161. https://doi.org/10.1007/7854_2011_170 PubMedCrossRefGoogle Scholar
  137. Stadler M, Tomann L, Storka A, Wolzt M, Peric S, Bieglmayer C, Pacini G, Dickson SL, Brath H, Bech P, Prager R, Korbonits M (2014) Effects of smoking cessation on beta-cell function, insulin sensitivity, body weight, and appetite. Eur J Endocrinol 170:219–217. https://doi.org/10.1530/EJE-13-0590 PubMedCrossRefGoogle Scholar
  138. Stephens TW, Basinski M, Bristow PK, Bue-Valleskey JM, Burgett SG, Craft L, Hale J, Hoffmann J, Hsiung HM, Kriauciunas A et al (1995) The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377:530–532. https://doi.org/10.1038/377530a0 PubMedCrossRefGoogle Scholar
  139. Stewart ST, Cutler DM, Rosen AB (2009) Forecasting the effects of obesity and smoking on U.S. life expectancy. N Engl J Med 361:2252–2260. https://doi.org/10.1056/NEJMsa0900459 PubMedPubMedCentralCrossRefGoogle Scholar
  140. Tao YX (2010) The melanocortin-4 receptor: physiology, pharmacology, and pathophysiology. Endocr Rev 31:506–543. https://doi.org/10.1210/er.2009-0037 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Tapper AR, McKinney SL, Nashmi R, Schwarz J, Deshpande P, Labarca C, Whiteaker P, Marks MJ, Collins AC, Lester HA (2004) Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science 306:1029–1032. https://doi.org/10.1126/science.1099420 PubMedCrossRefGoogle Scholar
  142. Taraschenko OD, Rubbinaccio HY, Maisonneuve IM, Glick SD (2008) 18-methoxycoronaridine: a potential new treatment for obesity in rats? Psychopharmacology (Berl) 201:339–350. https://doi.org/10.1007/s00213-008-1290-9 CrossRefGoogle Scholar
  143. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908–913. https://doi.org/10.1038/35038090 PubMedCrossRefGoogle Scholar
  144. Vaisse C, Clement K, Durand E, Hercberg S, Guy-Grand B, Froguel P (2000) Melanocortin-4 receptor mutations are a frequent and heterogeneous cause of morbid obesity. J Clin Invest 106:253–262. https://doi.org/10.1172/JCI9238 PubMedPubMedCentralCrossRefGoogle Scholar
  145. Valassi E, Scacchi M, Cavagnini F (2008) Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis 18:158–168. https://doi.org/10.1016/j.numecd.2007.06.004 PubMedCrossRefGoogle Scholar
  146. van der Lely AJ, Tschop M, Heiman ML, Ghigo E (2004) Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr Rev 25:426–457. https://doi.org/10.1210/er.2002-0029 PubMedCrossRefGoogle Scholar
  147. Volkow ND, Wang GJ, Fowler JS, Tomasi D, Baler R (2012) Food and drug reward: overlapping circuits in human obesity and addiction. Curr Top Behav Neurosci 11:1–24. https://doi.org/10.1007/7854_2011_169 PubMedGoogle Scholar
  148. Wang H, Storlien LH, Huang XF (2002) Effects of dietary fat types on body fatness, leptin, and ARC leptin receptor, NPY, and AgRP mRNA expression. Am J Physiol Endocrinol Metab 282:E1352–E1359. https://doi.org/10.1152/ajpendo.00230.2001 PubMedCrossRefGoogle Scholar
  149. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384–388. https://doi.org/10.1038/nature01339 PubMedCrossRefGoogle Scholar
  150. Wang X, Yang Z, Xue B, Shi H (2011) Activation of the cholinergic antiinflammatory pathway ameliorates obesity-induced inflammation and insulin resistance. Endocrinology 152:836–846. https://doi.org/10.1210/en.2010-0855 PubMedPubMedCentralCrossRefGoogle Scholar
  151. Wei M, Stern MP, Haffner SM (1997) Serum leptin levels in Mexican Americans and non-Hispanic whites: association with body mass index and cigarette smoking. Ann Epidemiol 7:81–86PubMedCrossRefGoogle Scholar
  152. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808. https://doi.org/10.1172/JCI19246 PubMedPubMedCentralCrossRefGoogle Scholar
  153. Williams DL, Schwartz MW (2005) The melanocortin system as a central integrator of direct and indirect controls of food intake. Am J Phys Regul Integr Comp Phys 289:R2–R3. https://doi.org/10.1152/ajpregu.00226.2005 Google Scholar
  154. Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG, Dhillo WS, Ghatei MA, Bloom SR (2001) Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 86:5992. https://doi.org/10.1210/jcem.86.12.8111 PubMedCrossRefGoogle Scholar
  155. Wynne K, Stanley S, McGowan B, Bloom S (2005) Appetite control. J Endocrinol 184:291–318. https://doi.org/10.1677/joe.1.05866 PubMedCrossRefGoogle Scholar
  156. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821–1830. https://doi.org/10.1172/JCI19451 PubMedPubMedCentralCrossRefGoogle Scholar
  157. Xu TY, Guo LL, Wang P, Song J, Le YY, Viollet B, Miao CY (2012) Chronic exposure to nicotine enhances insulin sensitivity through alpha7 nicotinic acetylcholine receptor-STAT3 pathway. PLoS One 7:e51217. https://doi.org/10.1371/journal.pone.0051217 PubMedPubMedCentralCrossRefGoogle Scholar
  158. Yang W, Kelly T, He J (2007) Genetic epidemiology of obesity. Epidemiol Rev 29:49–61. https://doi.org/10.1093/epirev/mxm004 PubMedCrossRefGoogle Scholar
  159. Ypsilantis P, Politou M, Anagnostopoulos C, Tsigalou C, Kambouromiti G, Kortsaris A, Simopoulos C (2013) Effects of cigarette smoke exposure and its cessation on body weight, food intake and circulating leptin, and ghrelin levels in the rat. Nicotine Tob Res 15:206–212. https://doi.org/10.1093/ntr/nts113 PubMedCrossRefGoogle Scholar
  160. Zaveri NT, Bertrand S, Yasuda D, Bertrand D (2015) Functional characterization of AT-1001, an alpha3beta4 nicotinic acetylcholine receptor ligand, at human alpha3beta4 and alpha4beta2 nAChR. Nicotine Tob Res 17:361–367. https://doi.org/10.1093/ntr/ntu170 PubMedCrossRefGoogle Scholar
  161. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432. https://doi.org/10.1038/372425a0 PubMedCrossRefGoogle Scholar
  162. Zoli M, Picciotto MR (2012) Nicotinic regulation of energy homeostasis. Nicotine Tob Res 14:1270–1290. https://doi.org/10.1093/ntr/nts159 PubMedPubMedCentralCrossRefGoogle Scholar
  163. Zoli M, Moretti M, Zanardi A, McIntosh JM, Clementi F, Gotti C (2002) Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J Neurosci 22:8785–8789PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Ming D. Li
    • 1
    • 2
  1. 1.University of VirginiaCharlottesvilleUSA
  2. 2.Zhejiang UniversityHangzhouChina

Personalised recommendations