Prenatal nicotine exposure and the programming of metabolic and cardiovascular disorders

Molecular and Cellular Endocrinology

Volumn 304, Issue 1-2, 2009, Pages 69-77

  Somm, Emmanuel ^a   Schwitzgebel, Valérie M ^a   Vauthay, Delphine M ^a   Aubert, Michel L ^a   Hüppi, Petra S ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Adipocyte; Cardiovascular; Insulin resistance; Nicotine; Obesity; Pancreatic islet

Indexed keywords

GLUCOSE; NICOTINE;

ADIPOSE TISSUE; BODY WEIGHT; CARDIOVASCULAR DISEASE; CARDIOVASCULAR FUNCTION; DYSLIPIDEMIA; EXPERIMENTAL STUDY; GLUCOSE HOMEOSTASIS; HUMAN; HYPERTENSION; LIFE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET; PERINATAL DRUG EXPOSURE; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; REVIEW;

ANIMALS; BLOOD GLUCOSE; CARDIOVASCULAR DISEASES; FEMALE; FETUS; HOMEOSTASIS; HUMANS; METABOLIC DISEASES; NICOTINE; OBESITY; PANCREAS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SMOKING;

EID: 67349190864     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.02.026     Document Type: Review

References (135)

1. Adams A.K., Harvey H.E., and Prince R.J. Association of maternal smoking with overweight at age 3 y in American Indian children. Am. J. Clin. Nutr. 82 (2005) 393-398
2. Adida C., Crotty P.L., McGrath J., Berrebi D., Diebold J., and Altieri D.C. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am. J. Pathol. 152 (1998) 43-49
3. Al Mamun A., Lawlor D.A., Alati R., O'Callaghan M.J., Williams G.M., and Najman J.M. Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. Am. J. Epidemiol. 164 (2006) 317-325
4. Althabe F., Colomar M., Gibbons L., Belizan J.M., and Buekens P. [Smoking during pregnancy in Argentina and Uruguay]. Medicina (B Aires) 68 (2008) 48-54
5. Amoruso A., Bardelli C., Gunella G., Fresu L.G., Ferrero V., and Brunelleschi S. Quantification of PPAR-gamma protein in monocyte/macrophages from healthy smokers and non-smokers: a possible direct effect of nicotine. Life Sci. 81 (2007) 906-915
6. An Z., Wang H., Song P., Zhang M., Geng X., and Zou M.H. Nicotine-induced activation of AMP-activated protein kinase inhibits fatty acid synthase in 3T3L1 adipocytes: a role for oxidant stress. J. Biol. Chem. 282 (2007) 26793-26801
7. Ananth C.V., Savitz D.A., and Luther E.R. Maternal cigarette smoking as a risk factor for placental abruption, placenta previa, and uterine bleeding in pregnancy. Am. J. Epidemiol. 144 (1996) 881-889
8. Andersson K., and Arner P. Systemic nicotine stimulates human adipose tissue lipolysis through local cholinergic and catecholaminergic receptors. Int. J. Obes. Relat. Metab. Disord. 25 (2001) 1225-1232
9. Andres R.L., and Day M.C. Perinatal complications associated with maternal tobacco use. Semin. Neonatol. 5 (2000) 231-241
10. Barker D.J., and Osmond C. Diet and coronary heart disease in England and Wales during and after the Second World War. J. Epidemiol. Community Health 40 (1986) 37-44
11. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phipps K., and Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36 (1993) 62-67
12. Barker D.J. The fetal and infant origins of disease. Eur. J. Clin. Invest. 25 (1995) 457-463
13. Berghofer A., Pischon T., Reinhold T., Apovian C.M., Sharma A.M., and Willich S.N. Obesity prevalence from a European perspective: a systematic review. BMC Public Health 8 (2008) 200
14. Blake K.V., Gurrin L.C., Evans S.F., Beilin L.J., Landau L.I., Stanley F.J., and Newnham J.P. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum. Dev. 57 (2000) 137-147
15. Bray G.A. Medical consequences of obesity. J. Clin. Endocrinol. Metab. 89 (2004) 2583-2589
16. Britos S.A., Keller E.A., and Orsingher O.A. Prenatal nicotine exposure induces cardiac adrenergic subsensitivity in adult rats. Acta Physiol. Pharmacol. Ther. Latinoam. 42 (1992) 217-224
17. Bruin J., Gerstein H., Morrison K., and Holloway A. Increased pancreatic beta cell apoptosis following fetal and neonatal exposure to nicotine is mediated via the mitochondria. Toxicol. Sci. (2008)
18. Bruin J.E., Kellenberger L.D., Gerstein H.C., Morrison K.M., and Holloway A.C. Fetal and neonatal nicotine exposure and postnatal glucose homeostasis: identifying critical windows of exposure. J. Endocrinol. 194 (2007) 171-178
19. Bruin J.E., Gerstein H.C., Morrison K.M., and Holloway A.C. Increased pancreatic beta-cell apoptosis following fetal and neonatal exposure to nicotine is mediated via the mitochondria. Toxicol. Sci. 103 (2008) 362-370
20. Bruin J.E., Petre M.A., Lehman M.A., Raha S., Gerstein H.C., Morrison K.M., and Holloway A.C. Maternal nicotine exposure increases oxidative stress in the offspring. Free Radic. Biol. Med. (2008)
21. Calle E.E., Thun M.J., Petrelli J.M., Rodriguez C., and Heath Jr. C.W. Body-mass index and mortality in a prospective cohort of U S. adults. N. Engl. J. Med. 341 (1999) 1097-1105
22. Calle E.E., and Thun M.J. Obesity and cancer. Oncogene 23 (2004) 6365-6378
23. Chelmow D., Andrew D.E., and Baker E.R. Maternal cigarette smoking and placenta previa. Obstet. Gynecol. 87 (1996) 703-706
24. Cleasby M.E., Kelly P.A., Walker B.R., and Seckl J.R. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 144 (2003) 999-1007
25. Cnattingius S., and Stephansson O. The epidemiology of stillbirth. Semin. Perinatol. 26 (2002) 25-30
26. Dasgupta P., Kinkade R., Joshi B., Decook C., Haura E., and Chellappan S. Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6332-6337
27. Delpisheh A., Attia E., Drammond S., and Brabin B.J. Adolescent smoking in pregnancy and birth outcomes. Eur. J. Public Health 16 (2006) 168-172
28. Devi S. Progress on childhood obesity patchy in the USA. Lancet 371 (2008) 105-106
29. DiFranza J.R., Aligne C.A., and Weitzman M. Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113 (2004) 1007-1015
30. Dodds L. Prevalence of smoking among pregnant women in Nova Scotia from 1988 to 1992. CMAJ 152 (1995) 185-190
31. Evans C., Wang J., Neff R., and Mendelowitz D. Hypoxia recruits a respiratory-related excitatory pathway to brainstem premotor cardiac vagal neurons in animals exposed to prenatal nicotine. Neuroscience 133 (2005) 1073-1079
32. Fried P.A., James D.S., and Watkinson B. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 23 (2001) 431-436
33. Gao Y.J., Holloway A.C., Zeng Z.H., Lim G.E., Petrik J.J., Foster W.G., and Lee R.M. Prenatal exposure to nicotine causes postnatal obesity and altered perivascular adipose tissue function. Obes. Res. 13 (2005) 687-692
34. Hadley C.B., Main D.M., and Gabbe S.G. Risk factors for preterm premature rupture of the fetal membranes. Am. J. Perinatol. 7 (1990) 374-379
35. Hafstrom O., Milerad J., and Sundell H.W. Prenatal nicotine exposure blunts the cardiorespiratory response to hypoxia in lambs. Am. J. Respir. Crit. Care Med. 166 (2002) 1544-1549
36. Hales C.N. Fetal and infant growth and impaired glucose tolerance in adulthood: the "thrifty phenotype" hypothesis revisited. Acta Paediatr. (Suppl) 422 (1997) 73-77
37. Hales C.N. Metabolic consequences of intrauterine growth retardation. Acta Paediatr (1997) 184-187 Suppl. 423 discussion 188
38. Hamilton M.T., Hamilton D.G., and Zderic T.W. Role of low energy expenditure and sitting in obesity, metabolic syndrome, type 2 diabetes, and cardiovascular disease. Diabetes 56 (2007) 2655-2667
39. Hammoud A.O., Bujold E., Sorokin Y., Schild C., Krapp M., and Baumann P. Smoking in pregnancy revisited: findings from a large population-based study. Am. J. Obstet. Gynecol. 192 (2005) 1856-1862 discussion 1862-3
40. Handler A., Davis F., Ferre C., and Yeko T. The relationship of smoking and ectopic pregnancy. Am. J. Public Health. 79 (1989) 1239-1242
41. Harger J.H., Hsing A.W., Tuomala R.E., Gibbs R.S., Mead P.B., Eschenbach D.A., Knox G.E., and Polk B.F. Risk factors for preterm premature rupture of fetal membranes: a multicenter case-control study. Am. J. Obstet. Gynecol. 163 (1990) 130-137
42. Holloway A.C., Lim G.E., Petrik J.J., Foster W.G., Morrison K.M., and Gerstein H.C. Fetal and neonatal exposure to nicotine in Wistar rats results in increased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes. Diabetologia 48 (2005) 2661-2666
43. Holloway A.C., Cuu D.Q., Morrison K.M., Gerstein H.C., and Tarnopolsky M.A. Transgenerational effects of fetal and neonatal exposure to nicotine. Endocrine 31 (2007) 254-259
44. Holloway A.C., Petrik J.J., Bruin J.E., and Gerstein H.C. Rosiglitazone prevents diabetes by increasing beta-cell mass in an animal model of type 2 diabetes characterized by reduced beta-cell mass at birth. Diabetes Obes. Metab. (2007)
45. Hotamisligil G.S., Shargill N.S., and Spiegelman B.M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259 (1993) 87-91
46. Huang R.C., Burke V., Newnham J.P., Stanley F.J., Kendall G.E., Landau L.I., Oddy W.H., Blake K.V., Palmer L.J., and Beilin L.J. Perinatal and childhood origins of cardiovascular disease. Int. J. Obes. (Lond.) 31 (2007) 236-244
47. Huang Z.G., Wang X., Evans C., Gold A., Bouairi E., and Mendelowitz D. Prenatal nicotine exposure alters the types of nicotinic receptors that facilitate excitatory inputs to cardiac vagal neurons. J. Neurophysiol. 92 (2004) 2548-2554
48. Huang Z.G., Wang X., Dergacheva O., and Mendelowitz D. Prenatal nicotine exposure recruits an excitatory pathway to brainstem parasympathetic cardioinhibitory neurons during hypoxia/hypercapnia in the rat: implications for sudden infant death syndrome. Pediatr. Res. 58 (2005) 562-567
49. Isomaa B., Almgren P., Tuomi T., Forsen B., Lahti K., Nissen M., Taskinen M.R., and Groop L. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24 (2001) 683-689
50. Joy T., Lahiry P., Pollex R.L., and Hegele R.A. Genetics of metabolic syndrome. Curr. Diab. Rep. 8 (2008) 141-148
51. Juge-Aubry C.E., Somm E., Giusti V., Pernin A., Chicheportiche R., Verdumo C., Rohner-Jeanrenaud F., Burger D., Dayer J.M., and Meier C.A. Adipose tissue is a major source of interleukin-1 receptor antagonist: upregulation in obesity and inflammation. Diabetes 52 (2003) 1104-1110
52. Juge-Aubry C.E., Somm E., Pernin A., Alizadeh N., Giusti V., Dayer J.M., and Meier C.A. Adipose tissue is a regulated source of interleukin-10. Cytokine 29 (2005) 270-274
53. Kamendi H., Stephens C., Dergacheva O., Wang X., Huang Z.G., Bouairi E., Gorini C., McIntosh J.M., and Mendelowitz D. Prenatal nicotine exposure alters the nicotinic receptor subtypes that modulate excitation of parasympathetic cardiac neurons in the nucleus ambiguus from primarily alpha3beta2 and/or alpha6betaX to alpha3beta4. Neuropharmacology 51 (2006) 60-66
54. Kendrick J.S., and Merritt R.K. Women and smoking: an update for the 1990s. Am. J. Obstet. Gynecol. 175 (1996) 528-535
55. Kirkland S.A., Dodds L.A., and Brosky G. The natural history of smoking during pregnancy among women in Nova Scotia. CMAJ 163 (2000) 281-282
56. Kolas T., Nakling J., and Salvesen K.A. Smoking during pregnancy increases the risk of preterm births among parous women. Acta Obstet. Gynecol. Scand. 79 (2000) 644-648
57. Koupil I., and Toivanen P. Social and early-life determinants of overweight and obesity in 18-year-old Swedish men. Int. J. Obes. (Lond.) (2007)
58. Krechowec S.O., Vickers M., Gertler A., and Breier B.H. Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J. Endocrinol. 189 (2006) 355-363
59. Kvalvik L.G., Skjaerven R., and Haug K. Smoking during pregnancy from 1999 to 2004: a study from the Medical Birth Registry of Norway. Acta Obstet. Gynecol. Scand. 87 (2008) 280-285
60. Lawlor D.A., Najman J.M., Sterne J., Williams G.M., Ebrahim S., and Davey Smith G. Associations of parental, birth, and early life characteristics with systolic blood pressure at 5 years of age: findings from the Mater-University study of pregnancy and its outcomes. Circulation 110 (2004) 2417-2423
61. Lawrence J., Xiao D., Xue Q., Rejali M., Yang S., and Zhang L. Prenatal nicotine exposure increases heart susceptibility to ischemia/reperfusion injury in adult offspring. J. Pharmacol. Exp. Ther. 324 (2008) 331-341
62. Leary S.D., Smith G.D., Rogers I.S., Reilly J.J., Wells J.C., and Ness A.R. Smoking during pregnancy and offspring fat and lean mass in childhood. Obesity (Silver Spring) 14 (2006) 2284-2293
63. Levin E.D. Fetal nicotinic overload, blunted sympathetic responsivity, and obesity. Birth Defects Res. A Clin. Mol. Teratol. 73 (2005) 481-484
64. Levy L., and Jackson A.A. Modest restriction of dietary protein during pregnancy in the rat: fetal and placental growth. J. Dev. Physiol. 19 (1993) 113-118
65. Lindsay R.S., Lindsay R.M., Waddell B.J., and Seckl J.R. Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 39 (1996) 1299-1305
66. Liu R.H., Mizuta M., and Matsukura S. The expression and functional role of nicotinic acetylcholine receptors in rat adipocytes. J. Pharmacol. Exp. Ther. 310 (2004) 52-58
67. Lobstein T., Baur L., and Uauy R. Obesity in children and young people: a crisis in public health. Obes Rev. 1 5 (Suppl) (2004) 4-104
68. Lumley J., Oliver S.S., Chamberlain C., and Oakley L. Interventions for promoting smoking cessation during pregnancy. Cochrane Database Syst. Rev. (2004) CD001055
69. Mackay J.E.M. The Tobacco Atlas (2003), World Health Organization, Geneva
70. Martin J.A., Hamilton B.E., Sutton P.D., Ventura S.J., Menacker F., and Munson M.L. Births: final data for 2003. Natl. Vital Stat. Rep. 54 (2005) 1-116
71. Mathews T.J. Smoking during pregnancy in the 1990s. Natl. Vital Stat. Rep. 49 (2001) 1-14
72. Matsunaga E., and Shiota K. Ectopic pregnancy and myoma uteri: teratogenic effects and maternal characteristics. Teratology 21 (1980) 61-69
73. Meyer K., and Lubo Z. Fetal programming of cardiac function and disease. Reprod. Sci. 14 (2007) 209-216
74. Mizutani T., Suzuki K., Kondo N., and Yamagata Z. Association of maternal lifestyles including smoking during pregnancy with childhood obesity. Obesity (Silver Spring) 15 (2007) 3133-3139
75. Mohamed-Ali V., Goodrick S., Rawesh A., Katz D.R., Miles J.M., Yudkin J.S., Klein S., and Coppack S.W. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J. Clin. Endocrinol. Metab. 82 (1997) 4196-4200
76. Montgomery S.M., and Ekbom A. Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ 324 (2002) 26-27
77. Morley R., Leeson Payne C., Lister G., and Lucas A. Maternal smoking and blood pressure in 7 5 to 8 year old offspring. Arch. Dis. Child. 72 (1995) 120-124
78. Nabet C., Ancel P.Y., Burguet A., and Kaminski M. Smoking during pregnancy and preterm birth according to obstetric history: French national perinatal surveys. Paediatr. Perinat. Epidemiol. 19 (2005) 88-96
79. Navarro H.A., Mills E., Seidler F.J., Baker F.E., Lappi S.E., Tayyeb M.I., Spencer J.R., and Slotkin T.A. Prenatal nicotine exposure impairs beta-adrenergic function: persistent chronotropic subsensitivity despite recovery from deficits in receptor binding. Brain Res. Bull. 25 (1990) 233-237
80. Neff R.A., Wang J., Baxi S., Evans C., and Mendelowitz D. Respiratory sinus arrhythmia: endogenous activation of nicotinic receptors mediates respiratory modulation of brainstem cardioinhibitory parasympathetic neurons. Circ. Res. 93 (2003) 565-572
81. Neff R.A., Simmens S.J., Evans C., and Mendelowitz D. Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J. Neurosci. 24 (2004) 9261-9268
82. NIH State-of-the-Science Panel, 2006. National Institutes of Health State-of-the-Science conference statement: tobacco use: prevention, cessation, and control. Ann. Intern. Med. 145, 839-844.
83. Obunai K., Jani S., and Dangas G.D. Cardiovascular morbidity and mortality of the metabolic syndrome. Med. Clin. N. Am. 91 (2007) 1169-84, x
84. Ogden C.L., Carroll M.D., Curtin L.R., McDowell M.A., Tabak C.J., and Flegal K.M. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 295 (2006) 1549-1555
85. Oken E., Huh S.Y., Taveras E.M., Rich-Edwards J.W., and Gillman M.W. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes. Res. 13 (2005) 2021-2028
86. Oken E., Levitan E.B., and Gillman M.W. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int. J. Obes. (Lond.) 32 (2008) 201-210
87. Oliff H.S., and Gallardo K.A. The effect of nicotine on developing brain catecholamine systems. Front Biosci. 4 (1999) D883-D897
88. Ong K.K., Preece M.A., Emmett P.M., Ahmed M.L., and Dunger D.B. Size at birth and early childhood growth in relation to maternal smoking, parity and infant breast-feeding: longitudinal birth cohort study and analysis. Pediatr Res. 52 (2002) 863-867
89. Osmond C., Barker D.J., Winter P.D., Fall C.H., and Simmonds S.J. Early growth and death from cardiovascular disease in women. BMJ 307 (1993) 1519-1524
90. Ozanne S.E., and Hales C.N. Lifespan: catch-up growth and obesity in male mice. Nature 427 (2004) 411-412
91. Pachlopnik Schmid J.M., Kuehni C.E., Strippoli M.P., Roiha H.L., Pavlovic R., Latzin P., Gallati S., Kraemer R., Dahinden C., and Frey U. Maternal tobacco smoking and decreased leukocytes, including dendritic cells, in neonates. Pediatr. Res. 61 (2007) 462-466
92. Pauly J.R., and Slotkin T.A. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr. (2008)
93. Pausova Z., Paus T., Sedova L., and Berube J. Prenatal exposure to nicotine modifies kidney weight and blood pressure in genetically susceptible rats: a case of gene-environment interaction. Kidney Int. 64 (2003) 829-835
94. Power C., and Jefferis B.J. Fetal environment and subsequent obesity: a study of maternal smoking. Int. J. Epidemiol. 31 (2002) 413-419
95. Raymond E.G., and Mills J.L. Placental abruption Maternal risk factors and associated fetal conditions. Acta Obstet. Gynecol. Scand. 72 (1993) 633-639
96. Reilly J.J., Armstrong J., Dorosty A.R., Emmett P.M., Ness A., Rogers I., Steer C., and Sherriff A. Early life risk factors for obesity in childhood: cohort study. BMJ 330 (2005) 1357
97. Rocchini A.P. Childhood obesity and a diabetes epidemic. N. Engl. J. Med. 346 (2002) 854-855
98. Salsberry P.J., and Reagan P.B. Taking the long view: the prenatal environment and early adolescent overweight. Res. Nurs. Health. 30 (2007) 297-307
99. Scherer P.E., Williams S., Fogliano M., Baldini G., and Lodish H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270 (1995) 26746-26749
100. Seckl J.R. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol. Cell. Endocrinol. 185 (2001) 61-71
101. Seidler F.J., Levin E.D., Lappi S.E., and Slotkin T.A. Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepinephrine from rat brain regions. Brain Res. Dev. Brain. Res. 69 (1992) 288-291
102. Sekhon H.S., Proskocil B.J., Clark J.A., and Spindel E.R. Prenatal nicotine exposure increases connective tissue expression in foetal monkey pulmonary vessels. Eur. Respir. J. 23 (2004) 906-915
103. Shenassa E.D., and Brown M.J. Maternal smoking and infantile gastrointestinal dysregulation: the case of colic. Pediatrics 114 (2004) e497-505
104. Sherman J., Young A., Sherman M.P., Collazo C., and Bernert J.T. Prenatal smoking and alterations in newborn heart rate during transition. J. Obstet. Gynecol. Neonatal Nurs. 31 (2002) 680-687
105. Slotkin T.A., Navarro H.A., McCook E.C., and Seidler F.J. Fetal nicotine exposure produces postnatal up-regulation of adenylate cyclase activity in peripheral tissues. Life Sci. 47 (1990) 1561-1567
106. Slotkin T.A., Epps T.A., Stenger M.L., Sawyer K.J., and Seidler F.J. Cholinergic receptors in heart and brainstem of rats exposed to nicotine during development: implications for hypoxia tolerance and perinatal mortality. Brain Res. Dev. Brain Res. 113 (1999) 1-12
107. Somm E., Schwitzgebel V.M., Vauthay D.M., Camm E.J., Chen C.Y., Giacobino J.P., Sizonenko S.V., Aubert M.L., and Huppi P.S. Prenatal nicotine exposure alters early pancreatic islet and adipose tissue development with consequences on the control of body weight and glucose metabolism later in life. Endocrinology 149 (2008) 6289-6299
108. Sowan N.A., and Stember M.L. Effect of maternal prenatal smoking on infant growth and development of obesity. J. Perinat. Educ. 9 (2000) 22-29
109. Spinillo A., Capuzzo E., Nicola S.E., Colonna L., Egbe T.O., and Zara C. Factors potentiating the smoking-related risk of fetal growth retardation. Br. J. Obstet. Gynaecol. 101 (1994) 954-958
110. Steppan C.M., Bailey S.T., Bhat S., Brown E.J., Banerjee R.R., Wright C.M., Patel H.R., Ahima R.S., and Lazar M.A. The hormone resistin links obesity to diabetes. Nature 409 (2001) 307-312
111. Stick S.M., Burton P.R., Gurrin L., Sly P.D., and LeSouef P.N. Effects of maternal smoking during pregnancy and a family history of asthma on respiratory function in newborn infants. Lancet 348 (1996) 1060-1064
112. Sztalryd C., Hamilton J., Horwitz B.A., Johnson P., and Kraemer F.B. Alterations of lipolysis and lipoprotein lipase in chronically nicotine-treated rats. Am. J. Physiol. 270 (1996) E215-E223
113. Tapanainen P.J., Bang P., Wilson K., Unterman T.G., Vreman H.J., and Rosenfeld R.G. Maternal hypoxia as a model for intrauterine growth retardation: effects on insulin-like growth factors and their binding proteins. Pediatr. Res. 36 (1994) 152-158
114. Teran-Garcia M., and Bouchard C. Genetics of the metabolic syndrome. Appl. Physiol. Nutr. Metab. 32 (2007) 89-114
115. Tolson C.M., Seidler F.J., McCook E.C., and Slotkin T.A. Does concurrent or prior nicotine exposure interact with neonatal hypoxia to produce cardiac cell damage?. Teratology 52 (1995) 298-305
116. Toschke A.M., Koletzko B., Slikker Jr. W., Hermann M., and von Kries R. Childhood obesity is associated with maternal smoking in pregnancy. Eur. J. Pediatr. 161 (2002) 445-448
117. Toschke A.M., Ehlin A.G., von Kries R., Ekbom A., and Montgomery S.M. Maternal smoking during pregnancy and appetite control in offspring. J. Perinat. Med. 31 (2003) 251-256
118. Toschke A.M., Montgomery S.M., Pfeiffer U., and von Kries R. Early intrauterine exposure to tobacco-inhaled products and obesity. Am. J. Epidemiol. 158 (2003) 1068-1074
119. Unterman T.G., Simmons R.A., Glick R.P., and Ogata E.S. Circulating levels of insulin, insulin-like growth factor-I (IGF-I), IGF-II, and IGF-binding proteins in the small for gestational age fetal rat. Endocrinology 132 (1993) 327-336
120. Velkoska E., Cole T.J., and Morris M.J. Early dietary intervention: long-term effects on blood pressure, brain neuropeptide Y, and adiposity markers. Am. J. Physiol. Endocrinol. Metab. 288 (2005) E1236-E1243
121. Vickers M.H., Breier B.H., Cutfield W.S., Hofman P.L., and Gluckman P.D. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am. J. Physiol. Endocrinol. Metab. 279 (2000) E83-E87
122. Vik T., Jacobsen G., Vatten L., and Bakketeig L.S. Pre- and post-natal growth in children of women who smoked in pregnancy. Early Hum. Dev. 45 (1996) 245-255
123. von Kries R., Toschke A.M., Koletzko B., and Slikker Jr. W. Maternal smoking during pregnancy and childhood obesity. Am. J. Epidemiol. 156 (2002) 954-961
124. Warren C.W., Jones N.R., Eriksen M.P., and Asma S. Patterns of global tobacco use in young people and implications for future chronic disease burden in adults. Lancet 367 (2006) 749-753
125. Wideroe M., Vik T., Jacobsen G., and Bakketeig L.S. Does maternal smoking during pregnancy cause childhood overweight?. Paediatr. Perinat. Epidemiol. 17 (2003) 171-179
126. Williams C.M., and Kanagasabai T. Maternal adipose tissue response to nicotine administration in the pregnant rat: effects on fetal body fat and cellularity. Br. J. Nutr. 51 (1984) 7-13
127. Williams S., and Poulton R. Twins and maternal smoking: ordeals for the fetal origins hypothesis? A cohort study. BMJ 318 (1999) 897-900
128. Wisborg K., Kesmodel U., Henriksen T.B., Olsen S.F., and Secher N.J. Exposure to tobacco smoke in utero and the risk of stillbirth and death in the first year of life. Am. J. Epidemiol. 154 (2001) 322-327
129. Woodall S.M., Bassett N.S., Gluckman P.D., and Breier B.H. Consequences of maternal undernutrition for fetal and postnatal hepatic insulin-like growth factor-I, growth hormone receptor and growth hormone binding protein gene regulation in the rat. J. Mol. Endocrinol. 20 (1998) 313-326
130. Xiao D., Huang X., Lawrence J., Yang S., and Zhang L. Fetal and neonatal nicotine exposure differentially regulates vascular contractility in adult male and female offspring. J. Pharmacol. Exp. Ther. 320 (2007) 654-661
131. Xiao D., Xu Z., Huang X., Longo L.D., Yang S., and Zhang L. Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension (2008)
132. Xu J., Huang H., Pan C., Zhang B., Liu X., and Zhang L. Nicotine inhibits apoptosis induced by cisplatin in human oral cancer cells. Int. J. Oral Maxillofac. Surg. 36 (2007) 739-744
133. Yura S., Itoh H., Sagawa N., Yamamoto H., Masuzaki H., Nakao K., Kawamura M., Takemura M., Kakui K., Ogawa Y., and Fujii S. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell. Metab. 1 (2005) 371-378
134. Zeskind P.S., and Gingras J.L. Maternal cigarette-smoking during pregnancy disrupts rhythms in fetal heart rate. J. Pediatr. Psychol. 31 (2006) 5-14
135. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., and Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 372 (1994) 425-432