- Original Article
- Published:
Preclinical Research
Effect of Short-Term Cigarette Smoke Exposure on Body Weight, Appetite and Brain Neuropeptide Y in Mice
- Hui Chen1,
- Ross Vlahos2,3,
- Steve Bozinovski1,3,
- Jessica Jones1,3,
- Gary P Anderson1,2,3 &
- …
- Margaret J Morris1
Neuropsychopharmacologyvolume 30, pages713–719 (2005)Cite this article
7808Accesses
131Citations
10Altmetric
Abstract
Although nicotinic receptors have been demonstrated in hypothalamic appetite-regulating areas and nicotine administration alters food intake and body weight in both animals and humans, the mechanisms underlying the effects of smoking on appetite circuits remain unclear. Conflicting effects of nicotine on the major orexigenic peptide, neuropeptide Y (NPY), have been observed in the brain, but the effects of smoking are unknown. Thus, we aimed to investigate how cigarette smoking affects body weight, food intake, plasma leptin concentration, hypothalamic NPY peptide, adipose mass and mRNA expression of uncoupling proteins (UCP), and tumor necrosis factor (TNF)α. Balb/C mice (8 weeks) were exposed to cigarette smoke (three cigarettes, three times a day for 4 consecutive days) or sham exposed. Body weight and food intake were recorded. Plasma leptin and brain NPY were measured by radioimmunoassay. UCPs and TNFα mRNA were measured by real-time PCR. Food intake dropped significantly from the first day of smoking, and weight loss became evident within 2 days. Brown fat and retroperitoneal white fat masses were significantly reduced, and plasma leptin concentration was decreased by 34%, in line with the decreased fat mass. NPY concentrations in hypothalamic subregions were similar between two groups. UCP1 mRNA was decreased in white fat and UCP3 mRNA increased in brown fat in smoking group. Short-term cigarette smoke exposure led to reduced body weight, food intake, and fat mass. The reduction in plasma leptin concentration may have been too modest to increase NPY production; alternatively, change in NPY or its function might have been offset by nicotine or other elements in cigarette smoke.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more onnature.com
or
References
Albanes D, Jones DY, Micozzi MS, Mattson ME (1987). Association between smoking and body weight in the US population: analysis of NHANES II.Am J Public Health77: 439–444.
Arai K, Kim K, Kaneko K, Iketani M, Otagiri A, Yamauchi Net al (2001). Nicotine infusion alters leptin and uncoupling protein 1 mRNA expression in adipose tissues of rats.Am J Physiol Endocrinol Metab280: E867–E876.
Bai FL, Yamano M, Shiotani Y, Emson PC, Smith AD, Powell JFet al (1985). An arcuato-paraventricular and-dorsomedial hypothalamic neuropeptide Y-containing system which lacks noradrenaline in the rat.Brain Res331: 172–175.
Beck B, Jhanwar-Uniyal M, Burlet A, Chapleur-Chateau M, Leibowitz SF, Burlet C (1990). Rapid and localized alternation of neuropeptide Y in discrete hypothalamic nuclei with feeding status.Brain Res528: 245–249.
Bellinger L, Cepeda-Benito A, Wellman PJ (2003). Meal patterns in male rats during and after intermittent nicotine administration.Pharmacol Biochem Behav74: 495–504.
Benowitz NL, Kuyt F, Jacob III P (1982). Circadian blood nicotine concentrations during cigarette smoking.Clin Pharmacol Ther32: 758–764.
Bishop C, Parker GC, Coscina DV (2002). Nicotine and its withdrawal alter feeding induced by paraventricular hypothalamic injections of neuropeptide Y in Sprague-Dawley rats.Psychopharmacology (Berl)162: 265–272.
Bishop C, Parker GC, Coscina DV (2004). Systemic nicotine alters whole-body fat utilization in female rats.Physiol Behav80: 563–567.
Bozinovski S, Jones J, Beavitt SJ, Cook AD, Hamilton JA, Anderson GP (2004). Innate immune responses to LPS in mouse lung are suppressed and reversed by neutralization of GM-CSF via repression of TLR-4.Am J Physiol Lung Cell Mol Physiol286: L877–L885.
Brady LS, Smith MA, Gold PW, Herkenham M (1990). Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rat.Neuroendocrinology52: 441–447.
Bullo-Bonet M, Garcia-Lorda P, Lopez-Soriano FJ, Argiles JM, Salas-Salvado J (1999). Tumor necrosis factor, a key role in obesity?FEBS Lett451: 215–219.
Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL (1985). The anatomy of neuropeptide-Y-containing neurons in rat brain.Neuroscience15: 1159–1181.
Crisp A, Sedgwick P, Halek C, Joughin N, Humphrey H (1999). Why may teenage girls persist in smoking?J Adolesc22: 657–672.
Cusin I, Rohner-Jeanrenaud F, Stricker-Krongrad A, Jeanrenaud B (1996). The weight-reducing effect of an intracerebroventricular bolus injection of leptin in genetically obesefa/fa rats. Reduced sensitivity compared with lean animals.Diabetes45: 1446–1450.
Dalgaard LT, Pedersen O (2001). Uncoupling proteins: functional characteristics and role in the pathogenesis of obesity and Type II diabetes.Diabetologia44: 946–965.
De clercq L, Genart C, Boone C, Remacle C (1996). Effects of acute or chronic administration of tumor necrosis factor on rat adipose tissue development.J Anim Sci74: 2745–2751.
Elmquist JK, Elias CF, Saper CB (1999). From lesions to leptin: hypothalamic control of food intake and body weight.Neuron22: 221–232.
Erickson JC, Hollopeter G, Palmiter RD (1996). Attenuation of the obesity syndrome of ob/ob mice by the loss of neuropeptide Y.Science274: 1704–1707.
Fantino M, Wieteska L (1993). Evidence for a direct central anorectic effect of tumor-necrosis-factor-alpha in the rat.Physiol Behav53: 477–483.
Fernandez-Real JM, Broch M, Vendrell J, Ricart W (2003). Smoking, fat mass and activation of the tumor necrosis factor-alpha pathway.Int J Obes Relat Metab Disord27: 1552–1556.
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 Res694: 139–146.
Furness JB, Koopmans HS, Robbins HL, Clerc N, Tobin JM, Morris MJ (2001). Effects of vagal and splanchnic section on food intake, weight, serum leptin and hypothalamic neuropeptide Y in rat.Auton Neurosci92: 28–36.
Grunberg NE, Bowen DJ, Winders SE (1986). Effects of nicotine on body weight and food consumption in female rats.Psychopharmacology (Berl)90: 101–105.
Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo Het al (2004). The development of emphysema in cigarette smoke exposed mice is strain dependent.Am J Respir Crit Care Med170: July 28 [Epub ahead of print].
Hajek P, Jackson P, Belcher M (1988). Long-term use of nicotine chewing gum. Occurrence, determinants, and effect on weight gain.JAMA260: 1593–1596.
Hansen MJ, Jovanovska V, Morris MJ (2004). Adaptive responses in hypothalamic neuropeptide Y in the face of prolonged high-fat feeding in the rat.J Neurochem88: 909–916.
Jo YH, Talmage DA, Role LW (2002). Nicotinic receptor-mediated effects on appetite and food intake.J Neurobiol53: 618–632.
Kern PA (1997). Potential role of TNFalpha and lipoprotein lipase as candidate genes for obesity.J Nutr127: 1917S–1922S.
Klesges RC, Meyers AW, Klesges LM, La Vasque ME (1989). Smoking, body weight, and their effects on smoking behavior: a comprehensive review of the literature.Psychol Bull6: 204–230.
Kopecky J, Hodny Z, Rossmeisl M, Syrovy I, Kozak LP (1996). Reduction of dietary obesity in aP2-Ucp transgenic mice: physiology and adipose tissue distribution.Am J Physiol270: E768–E775.
Langhans W, Hrupka B (1999). Interleukins and tumor necrosis factor as inhibitors of food intake.Neuropeptides33: 415–424.
Levin ED, Morgan MM, Galvez C, Ellison GD (1987). Chronic nicotine and withdrawal effects on body weight and food and water consumption in female rats.Physiol Behav39: 441–444.
Li MD, Kane JK, Parker SL, McAllen K, Matta SG, Sharp BM (2000). Nicotine administration enhances NPY expression in the rat hypothalamus.Brain Res867: 157–164.
Liu RH, Kurose T, Matsukura S (2001). Oral nicotine administration decreases tumor necrosis factor-alpha expression in fat tissues in obese rats.Metabolism50: 79–85.
McCarthy DO (2000). Tumor necrosis factor alpha and interleukin-6 have differential effects on food intake and gastric emptying in fasted rats.Res Nurs Health23: 222–228.1.
Morris MJ, Russell AE, Kapoor V, Cain MD, Elliott JM, West MJet al (1986). Increase in plasma neuropeptide Y concentrations during sympathetic activation in man.J Auton Nerv Syst17: 143–149.
Nagase I, Yoshida T, Kumamoto K, Umekawa T, Sakane N, Nikami Het al (1996). Expression of uncoupling protein in skeletal muscle and white fat of obese mice treated with thermogenicβ3-adrenergic agonist.J Clin Invest97: 2898–2904.
O'Hara P, Connett JE, Lee WW, Nides M, Murray R, Wise R (1998). Early and late weight gain following smoking cessation in the lung health study.Am J Epidemiol148: 821–830.
Ouyang Y, Virasch N, Hao P, Aubrey MT, Mukerjee N, Bierer BEet al (2000). Suppression of human IL-1beta, IL-2, IFN-gamma, and TNF-alpha production by cigarette smoke extracts.J Allergy Clin Immunol106: 280–287.
Perkins KA (1992). Effects of tobacco smoking on caloric intake.Br J Addict87: 193–205.
Samec S, Seydoux J, Dulloo AG (1998). Role of UCP homologues in skeletal muscles and brown adipose tissue: mediators of thermogenesis or regulators of lipids as fuel substrate?FASEB J12: 715–724.
Sivitz WI, Fink BD, Donohoue PA (1999). Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression.Endocrinology140: 1511–1519.
Sonti G, Ilyin SE, Plata-Salaman CR (1996). Anorexia induced by cytokine interactions at pathophysiological concentrations.Am J Physiol270: R1394–R1402.
Spiegelman BM, Hotamisligil GS (1993). Through thick and thin: wasting, obesity, and TNF alpha.Cell73: 625–627.
Stamford BA, Matter S, Fell RD, Papanek P (1986). Effects of smoking cessation on weight gain, metabolism rate, caloric consumption, and blood lipids.Am J Clin Nutr43: 486–494.
Stephens TW, Basinski M, Bristow PK, Bue-Valleskey JM, Burgett SG, Craft Let al (1995). The role of neuropeptide Y in the antiobesity action of the obese gene product.Nature377: 530–532.
Swart I, Jahng JW, Overton JM, Houpt TA (2002). Hypothalamic NPY, AGRP, and POMC mRNA responses to leptin and refeeding in mice.Am J Physiol Regul Integr Comp Physiol283: R1020–R1026.
Toomey D, Redmond HP, Bouchier-Hayes D (1995). Mechanisms mediating cancer cachexia.Cancer76: 2418–2426.
Torti FM, Torti SV, Larrick JW, Ringold GM (1989). Modulation of adipocyte differentiation by tumor necrosis factor and transforming growth factor beta.J Cell Biol108: 1105–1113.
Tracey KJ, Cerami A (1992). Tumor necrosis factor and regulation metabolism in infection: roles of systemicversus tissue levels.Proc Soc Exp Biol Med200: 233–239.
Vaisman N, Hahn T (1991). Tumor necrosis factor-alpha and anorexia—cause or effect?Metabolism40: 720–723.
Ventre J, Doebber T, Wu M, MacNaul K, Stevens K, Pasparakis Met al (1997). Targeted disruption of the tumor necrosis factor-alpha gene: metabolic consequences in obese and nonobese mice.Diabetes46: 1526–1531.
Wager-srdar SA, Levine AS, Morley JE, Hoidal JR, Niewoehner DE (1984). Effects of cigarette smoke and nicotine on feeding and energy.Physiol Behav32: 389–395.
Wee CC, Rigotti NA, Davis RB, Phillips RS (2001). Relationship between smoking and weight control efforts among adults in the United States.Arch Intern Med161: 546–550.
Wilding JP, Gilbey SG, Bailey CJ, Batt RA, Williams G, Ghatei MAet al (1993). Increased neuropeptide-Y messenger ribonucleic acid (mRNA) and decreased neurotensin mRNA in the hypothalamus of the obese (ob/ob) mouse.Endocrinology132: 1939–1944.
Williamson DF, Madans J, Anda RF, Kleinman JC, Giovino GA, Byers T (1991). Smoking cessation and severity of weight gain in a national cohort.N Engl J Med324: 739–745.
Woods SC, Seeley Jr R, Porte Jr D, Schwartz MW (1998). Signals that regulate food intake and energy homeostasis.Science280: 1378–1382.
Yoshida T, Sakane N, Umekawa T, Kogure A, Kondo M, Kumamoto Ket al (1999). Nicotine induces uncoupling protein 1 in white adipose tissue of obese mice.Int J Obes Relat Metab Disord23: 570–575.
Zarjevski N, Cusin I, Vettor R, Rohner-Jeanrenaud F, Jeanrenaud B (1993). Chronic intracerebroventricular neuropeptide-Y administration to normal rats mimics hormonal and metabolic changes of obesity.Endocrinology133: 1753–1758.
Acknowledgements
This work was funded by National Health and Medical Research Council of Australia and the CRC for Chronic Inflammatory Diseases. We thank Dr Michelle J Hansen for helpful discussion.
Author information
Authors and Affiliations
Department of Pharmacology, The University of Melbourne, Victoria, Australia
Hui Chen, Steve Bozinovski, Jessica Jones, Gary P Anderson & Margaret J Morris
Department of Medicine, The University of Melbourne, Royal Melbourne Hospital, Victoria, Australia
Ross Vlahos & Gary P Anderson
CRC for Chronic Inflammatory Diseases, The University of Melbourne, Victoria, Australia
Ross Vlahos, Steve Bozinovski, Jessica Jones & Gary P Anderson
- Hui Chen
Search author on:PubMed Google Scholar
- Ross Vlahos
Search author on:PubMed Google Scholar
- Steve Bozinovski
Search author on:PubMed Google Scholar
- Jessica Jones
Search author on:PubMed Google Scholar
- Gary P Anderson
Search author on:PubMed Google Scholar
- Margaret J Morris
Search author on:PubMed Google Scholar
Corresponding author
Correspondence toMargaret J Morris.
Additional information
Part of this work was presented in abstract form to the 24th annual meeting of Australian Neuroscience Society, January 2004.
Rights and permissions
About this article
Cite this article
Chen, H., Vlahos, R., Bozinovski, S.et al. Effect of Short-Term Cigarette Smoke Exposure on Body Weight, Appetite and Brain Neuropeptide Y in Mice.Neuropsychopharmacol30, 713–719 (2005). https://doi.org/10.1038/sj.npp.1300597
Received:
Revised:
Accepted:
Published:
Issue date:
Share this article
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.
Provided by the Springer Nature SharedIt content-sharing initiative
Keywords
This article is cited by
Short-term exposure to JUUL electronic cigarettes can worsen ischemic stroke outcome
- Ali Ehsan Sifat
- Sabrina Rahman Archie
- Thomas J. Abbruscato
Fluids and Barriers of the CNS (2022)
Modulation of mouse laryngeal inflammatory and immune cell responses by low and high doses of mainstream cigarette smoke
- Meena Easwaran
- Joshua D. Martinez
- Elizabeth Erickson-DiRenzo
Scientific Reports (2022)
Pharmacological Effects and Regulatory Mechanisms of Tobacco Smoking Effects on Food Intake and Weight Control
- Tongyuan Hu
- Zhongli Yang
- Ming D. Li
Journal of Neuroimmune Pharmacology (2018)
Apocynin and ebselen reduce influenza A virus-induced lung inflammation in cigarette smoke-exposed mice
- L. C. Oostwoud
- P. Gunasinghe
- R. Vlahos
Scientific Reports (2016)
Smoking and body weight: evidence from China health and nutrition survey
- Qing Wang
BMC Public Health (2015)


