Early leptin intervention reverses perturbed energy balance regulating hypothalamic neuropeptides in the pre- and postnatal calorie-restricted female rat offspring

Journal of Neuroscience Research

Volumn 93, Issue 6, 2015, Pages 902-912

  Gibson, Leena Caroline ^a   Shin, Bo Chul ^a   Dai, Yun ^a   Freije, William ^b   Kositamongkol, Sudatip ^a   Cho, John ^a   Devaskar, Sherin U ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AgRP; CART; Energy expenditure; Fetal programming; Hypothalamus; Leptin; NPY; POMC; STAT3

Indexed keywords

AGOUTI RELATED PROTEIN; ANTISENSE OLIGONUCLEOTIDE; CARBON DIOXIDE; LEPTIN; LEPTIN RECEPTOR; NEUROPEPTIDE; NEUROPEPTIDE Y; STAT3 PROTEIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; NERVE PROTEIN; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHROPOMETRIC PARAMETERS; ARTICLE; BODY WEIGHT; CALORIC INTAKE; CALORIC RESTRICTION; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; FEMALE; FOOD INTAKE; HYPERPHAGIA; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MILK; NONHUMAN; OBESITY; OXYGEN CONSUMPTION; PERINATAL PERIOD; PHENOTYPIC VARIATION; PHYSICAL ACTIVITY; POSTNATAL CARE; POSTNATAL GROWTH; PRENATAL CARE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; AGE; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; MALE; METABOLISM; NEWBORN; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE; SPRAGUE DAWLEY RAT;

AGE FACTORS; AGOUTI-RELATED PROTEIN; ANIMALS; ANIMALS, NEWBORN; CALORIC RESTRICTION; ENERGY INTAKE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOTHALAMUS; LEPTIN; MALE; NERVE TISSUE PROTEINS; NEUROPEPTIDE Y; NEUROPEPTIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRO-OPIOMELANOCORTIN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84927539094     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23560     Document Type: Article

References (55)

1. Ahima RS, Hileman SM. 2000. Postnatal regulation of hypothalamic neuropeptide expression by leptin: implications for energy balance and body weight regulation. Regul Pept 92(1-3):1-7.
2. Attig L, Larcher T, Gertler A, Abdennebi-Najar L, Djiane J. 2011. Postnatal leptin is necessary for maturation of numerous organs in newborn rats. Organogenesis 7:88-94.
3. Barker DJ. 2007. The origins of the developmental origins theory. J Intern Med 261:412-417.
4. Bluher S, Shah S, Mantzoros CS. 2009. Leptin deficiency: clinical implications and opportunities for therapeutic interventions. J Investig Med 57:784-788.
5. Bouret SG, Draper SJ, Simerly RB. 2004a. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 24:2797-2805.
6. Bouret SG, Draper SJ, Simerly RB. 2004b. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304:108-110.
7. Chauhan NB. 2002. Trafficking of intracerebroventricularly injected antisense oligonucleotides in the mouse brain. Antisense Nucleic Acid Drug Dev 12:353-357.
8. Chauhan NB, Siegel GJ. 2007. Antisense inhibition at the beta-secretase-site of beta-amyloid precursor protein reduces cerebral amyloid and acetyl cholinesterase activity in Tg2576. Neuroscience 146:143-151.
9. Claire Wang Y, Gortmaker SL, Taveras EM. 2011. Trends and racial/ethnic disparities in severe obesity among US children and adolescents, 1976-2006. Int J Pediatr Obes 6:12-20.
10. Cottrell EC, Mercer JG, Ozanne SE. 2010. Postnatal development of hypothalamic leptin receptors. Vitam Horm 82:201-217.
11. De Jonghe BC, Hayes MR, Banno R, Skibicka KP, Zimmer DJ, Bowen KA, Leichner TM, Alhadeff AL, Kanoski SE, Cyr NE, Nillni EA, Grill HJ, Bence KK. 2011. Deficiency of PTP1B in POMC neurons leads to alterations in energy balance and homeostatic response to cold exposure. Am J Physiol Endocrinol Metab 300(6):E1002-E1011.
12. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, Laborie C, Lesage J, Vieau D. 2008. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149:470-475.
13. Farooqi IS, Jebb SA, Langmack G, Lawrence E, Cheetham CH, Prentice AM, Hughes IA, McCamish MA, O'Rahilly S. 1999. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. N Engl J Med 341:879-884.
14. Faulconbridge LF, Hayes MR. 2011. Regulation of energy balance and body weight by the brain: a distributed system prone to disruption. Psychiatr Clin North Am 34:733-745.
15. Fukushima N, Yokouchi K, Kawagishi K, Moriizumi T. 2006. Effect of maternal deprivation on milk intake in normal and bilaterally facial nerve-injured developing rats. Neurosci Res 54:154-157.
16. Fung C, Evans E, Shin D, Shin BC, Zhao Y, Sankar R, Chaudhuri G, Devaskar SU. 2010. Hypoxic-ischemic brain injury exacerbates neuronal apoptosis and precipitates spontaneous seizures in glucose transporter isoform 3 heterozygous null mice. J Neurosci Res 88:3386-3398.
17. Garg M, Thamotharan M, Dai Y, Thamotharan S, Shin BC, Stout D, Devaskar SU. 2012. Early postnatal caloric restriction protects adult male intrauterine growth-restricted offspring from obesity. Diabetes 61:1391-1398.
18. Good D, Morse SA, Ventura HO, Reisin E. 2008. Obesity, hypertension, and the heart. J Cardiometab Syndr 3:168-172.
19. Hales CN, Barker DJ. 2001. The thrifty phenotype hypothesis. Br Med Bull 60:5-20.
20. Harrold JA. 2004. Hypothalamic control of energy balance. Curr Drug Targets 5:207-219.
21. He J, Varma A, Weissfeld LA, Devaskar SU. 2004. Postnatal glucocorticoid exposure alters the adult phenotype. Am J Physiol Regul Integr Comp Physiol 287(1):R198-R208.
22. Hill JO, Wyatt HR, Peters JC. 2012. Energy balance and obesity. Circulation 126:126-132.
23. Huan JN, Li J, Han Y, Chen K, Wu N, Zhao AZ. 2003. Adipocyte-selective reduction of the leptin receptors induced by antisense RNA leads to increased adiposity, dyslipidemia, and insulin resistance. J Biol Chem 278:45638-45650.
24. Hukshorn CJ, Saris WH, Westerterp-Plantenga MS, Farid AR, Smith FJ, Campfield LA. 2000. Weekly subcutaneous pegylated recombinant native human leptin (PEG-OB) administration in obese men. J Clin Endocrinol Metab 85:4003-4009.
25. Hukshorn CJ, van Dielen FM, Buurman WA, Westerterp-Plantenga MS, Campfield LA, Saris WH. 2002. The effect of pegylated recombinant human leptin (PEG-OB) on weight loss and inflammatory status in obese subjects. Int J Obes Relat Metab Disord 26:504-509.
26. James WP. 2008. The epidemiology of obesity: the size of the problem. J Intern Med 263:336-352.
27. Kennedy A, Gettys TW, Watson P, Wallace P, Ganaway E, Pan Q, Garvey WT. 1997. The metabolic significance of leptin in humans: gender-based differences in relationship to adiposity, insulin sensitivity, and energy expenditure. J Clin Endocrinol Metab 82:1293-1300.
28. Key TJ, Spencer EA, Reeves GK. 2010. Symposium 1: Overnutrition: consequences and solutions. Obesity and cancer risk. Proc Nutr Soc 69:86-90.
29. Konieczna J, Garcia AP, Sanchez J, Palou M, Palou A, Pico C. 2013. Oral leptin treatment in suckling rats ameliorates detrimental effects in hypothalamic structure and function caused by maternal caloric restriction during gestation. PLoS One 8(11):e81906.
30. Kumar VB, Farr SA, Flood JF, Kamlesh V, Franko M, Banks WA, Morley JE. 2000. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 21:1769-1775.
31. La Vecchia C, Franceschi S, Decarli A, Gallus G, Tognoni G. 1984. Risk factors for endometrial cancer at different ages. J Natl Cancer Inst 73:667-671.
32. Lapidus L, Helgesson O, Merck C, Bjorntorp P. 1988. Adipose tissue distribution and female carcinomas. A 12-year follow-up of participants in the population study of women in Gothenburg, Sweden. Int J Obes 12:361-368.
33. Leibowitz SF, Sepiashvili K, Akabayashi A, Karatayev O, Davydova Z, Alexander JT, Wang J, Chang GQ. 2005. Function of neuropeptide Y and agouti-related protein at weaning: relation to corticosterone, dietary carbohydrate and body weight. Brain Res 1036(1-2):180-191.
34. Li C, Wong WH. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98:31-36.
35. Licinio J, Caglayan S, Ozata M, Yildiz BO, de Miranda PB, O'Kirwan F, Whitby R, Liang L, Cohen P, Bhasin S, Krauss RM, Veldhuis JD, Wagner AJ, DePaoli AM, McCann SM, Wong ML. 2004. Phenotypic effects of leptin replacement on morbid obesity, diabetes mellitus, hypogonadism, and behavior in leptin-deficient adults. Proc Natl Acad Sci U S A 101:4531-4536.
36. Meas T, Deghmoun S, Armoogum P, Alberti C, Levy-Marchal C. 2008. Consequences of being born small for gestational age on body composition: an 8-year follow-up study. J Clin Endocrinol Metab 93:3804-3809.
37. Mela V, Diaz F, Gertler A, Solomon G, Argente J, Viveros MP, Chowen JA. 2012. Neonatal treatment with a pegylated leptin antagonist has a sexually dimorphic effect on hypothalamic trophic factors and neuropeptide levels. J Neuroendocrinol 24:756-765.
38. Messerli FH. 1982. Cardiovascular effects of obesity and hypertension. Lancet 1:1165-1168.
39. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. Academic Press.
40. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH. 2006. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 113:898-918.
41. Rayner DV, Dalgliesh GD, Duncan JS, Hardie LJ, Hoggard N, Trayhurn P. 1997. Postnatal development of the ob gene system: elevated leptin levels in suckling fa/fa rats. Am J Physiol 273(1 Pt 2):R446-R450.
42. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. 2001. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 185(1-2):93-98.
43. Shih CD, Au LC, Chan JY. 2003. Differential role of leptin receptors at the hypothalamic paraventricular nucleus in tonic regulation of food intake and cardiovascular functions. J Biomed Sci 10:367-378.
44. Shin BC, Dai Y, Thamotharan M, Gibson LC, Devaskar SU. 2012. Pre- and postnatal calorie restriction perturbs early hypothalamic neuropeptide and energy balance. J Neurosci Res 90:1169-1182.
45. Shin BC, McKnight RA, Devaskar SU. 2004. Glucose transporter GLUT8 translocation in neurons is not insulin responsive. J Neurosci Res 75:835-844.
46. Shin BC, Suzuki M, Inukai K, Anai M, Asano T, Takata K. 1998. Multiple isoforms of the regulatory subunit for phosphatidylinositol 3-kinase (PI3-kinase) are expressed in neurons in the rat brain. Biochem Biophys Res Commun 246:313-319.
47. Smith JT, Waddell BJ. 2003. Developmental changes in plasma leptin and hypothalamic leptin receptor expression in the rat: peripubertal changes and the emergence of sex differences. J Endocrinol 176:313-319.
48. Stevens A, Begum G, Cook A, Connor K, Rumball C, Oliver M, Challis J, Bloomfield F, White A. 2010. Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology 151:3652-3664.
49. Stevens A, Begum G, White A. 2011. Epigenetic changes in the hypothalamic pro-opiomelanocortin gene: a mechanism linking maternal undernutrition to obesity in the offspring? Eur J Pharmacol 660:194-201.
50. Thamotharan M, Shin BC, Suddirikku DT, Thamotharan S, Garg M, Devaskar SU. 2005. GLUT4 expression and subcellular localization in the intrauterine growth-restricted adult rat female offspring. Am J Physiol Endocrinol Metab 288(5):E935-E947.
51. Varma A, He J, Shin BC, Weissfeld LA, Devaskar SU. 2004. Postnatal intracerebroventricular exposure to leptin causes an altered adult female phenotype. Am J Physiol Endocrinol Metab 287(6):E1132-E1141.
52. Varma A, He J, Weissfeld L, Devaskar SU. 2003. Postnatal intracerebroventricular exposure to neuropeptide Y causes weight loss in female adult rats. Am J Physiol Regul Integr Comp Physiol 284(6):R1560-R1566.
53. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, Breier BH, Harris M. 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146:4211-4216.
54. Wabitsch M, Blum WF, Muche R, Braun M, Hube F, Rascher W, Heinze E, Teller W, Hauner H. 1997. Contribution of androgens to the gender difference in leptin production in obese children and adolescents. J Clin Invest 100:808-813.
55. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, Fujii S. 2005. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 1:371-378.