Maternal deprivation induces a rapid decline in circulating leptin levels and sexually dimorphic modifications in hypothalamic trophic factors and cell turnover

Hormones and Behavior

Volumn 57, Issue 4-5, 2010, Pages 405-414

  Viveros, María Paz ^a   Díaz, Francisca ^b,c   Mateos, Beatriz ^a   Rodríguez, Noé ^a   Chowen, Julie A ^b,c  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

BDNF; Cell proliferation; Glial fibrillary acidic protein; IGF 1; Leptin; Nestin; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; NESTIN; SOMATOMEDIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEVELOPMENT; ENDOCRINE DISEASE; FEMALE; GLUCOSE BLOOD LEVEL; HYPOTHALAMUS; MALE; MATERNAL DEPRIVATION; METABOLIC DISORDER; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SEX DIFFERENCE; WISTAR RAT;

EID: 77950936826     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.01.009     Document Type: Article

References (68)

1. Ahima R.S., Prabakaran D., Flier J.S. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J. Clin. Invest. 1998, 10:1020-1027.
2. Bouret S.G., Simerly R.B. Development of leptin-sensitive circuits. J. Neuroendocrinol. 2007, 19:575-582.
3. Bouret S.G., Draper S.J., Simerly R.B. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004, 304:108-110.
4. Byerly M.S., Simon J., Lebihan-Duval E., Duclos M.J., Coqburn L.A., Porter T.E. Effects of BDNF, T3, and corticosterone on expression of the hypothalamic obesity gene network in vivo and in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R1180-1189.
5. Carrer H.F., Cambiasso M.J. Sexual differentiation of the brain: genes, estrogen, and neurotrophic factors. Cell. Mol. Neurobiol. 2002, 22:479-500.
6. Chen H., Simar D., Morris M.J. Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS One 2009, 4:e6259.
7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
8. Chowen J.A., Busiguina S., García-Segura L.M. Sexual dimorphism and sex steroid modulation of glial fibrillary acidic acid protein messenger RNA and immunoreactivity levels in the rat hypothalamus. Neuroscience 1995, 69:519-532.
9. Choy K.H., de Visser Y., Nichols N.R., van den Buuse M. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008, 18:655-667.
10. Cirulli F., Francia N., Branchi I., Antonucci M.T., Aloe L., Suomi S.J., Alleva E. Changes in plasma levels of BDNF and NGF reveal a gender-selective vulnerability to early adversity in rhesus macaques. Psychoneuroendocrinology 2009, 34:172-180.
11. Clegg D.J., Riedy C.A., Smith K.A., Benoit S.C., Woods S.C. Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 2003, 52:682-687.
12. Coupé B., Dutriez-Casteloot I., Breton C., Lefèvre F., Mairesse J., Dickes-Coopman A., Silhol M., Tapia-Arancibia L., Lesage J., Vieau D. Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J. Neuroendocrinol. 2009, 21:40-48.
13. Coutellier L., Friedrich A.C., Failing K., Würbel H. Variations in the postnatal maternal environment in mice: effects on maternal behavior and behavioural and endocrine responses in the adult offspring. Physiol. Behav. 2008, 93:395-407.
14. Cryer A., Jones H.M. The development of white adipose tissue. Effect of litter size on the lipoprotein lipase activity of four adipose-tissue depots, serum immunoreactive insulin and tissue cellularity during the first year of life in male and female rats. Biochem. J. 1980, 186:805-815.
15. Daftary S.S., Gore A.C. Developmental changes in hypothalamic insulin-like growth factor-1: relationship to gonadotropin-releasing hormone neurons. Endocrinology 2003, 144:2034-2045.
16. D'Ercole J.A., Ye P. Expanding the mind: insulin-like growth factor 1 and brain development. Endocrinology 2008, 149:5958-5962.
17. de Jongh R., Geyer M.A., Olivier B., Groenink L. The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behav. Brain Res. 2005, 161:190-196.
18. De la Fuente M., Llorente R., Baeza I., De Castro N.M., Arranz L., Cruces J., Viveros M.P. Early maternal deprivation in rats: a proposed animal model for the study of developmental neuroimmunoendocrine interactions. Ann. N.Y. Acad. Sci. 2009, 1153:176-183.
19. Desbonnet L., Garrett L., Daly E., McDermott K.W., Dinan T.G. Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int. J. Dev. Neurosci. 2008, 26:259-268.
20. Djiane J., Attig L. Role of leptin during perinatal metabolic programming and obesity. J. Physiol Pharmacol. 2008, 59(Suppl 1):55-63.
21. Ellenbroek B.A., Derks N., Park H.J. Early maternal deprivation retards neurodevelopment in Wistar rats. Stress 2005, 8:247-257.
22. Forest M.G. Plasma androgens (testosterone and 4-androstenedione) and 17-hydroxyprogesterone in the neonatal, prepubertal and peripubertal periods in the human and the rat: differences between species. J. Steroid Biochem. 1979, 11:543-548.
23. Froy O. The relationship between nutrition and circadian rhythms in mammals. Front. Neuroendocrinol. 2007, 28:61-71.
24. García-Cáceres C., Diz-Chaves Y., Lagunas N., Calmarza-Font I., Azcoitia I., Garcia-Segura L.M., Frago L.M., Argente J., Chowen J.A. The weight gain response to stress during adulthood is conditioned by sex and prenatal stress exposure. Psychoneuroendocrinology 2010, 35:403-413. (PMID: 19726133).
25. Genest S.E., Gulemetova R., Laforest S., Drolet G., Kinkead R. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J. Physiol. 2004, 554:543-557.
26. Givalois L., Naert G., Rage F., Ixart G., Arancibia S., Tapia-Arancibia L. A single brain-derived neurotrophic factor injection modifies hypothalamo-pituitary-adrenocortical axis activity in adult male rats. Mol. Cell. Neurosci. 2004, 27:280-295.
27. Guzman-Marin R., Suntsova N., Bashir T., Szymusiak R., McGinty D. Cell proliferation in the dentate gyrus of the adult rat fluctuates with the light-dark cycle. Neurosci. Lett. 2007, 422:198-201.
28. Hariz G.M., Lindberg M., Hariz M.I., Bergenheim A.T. Gender differences in disability and health-related quality of life in patients with Parkinson's disease treated with stereotactic surgery. Acta Neurol. Scand. 2003, 108:28-37.
29. Hurn P.D., Macrae I.M. Estrogen as a peruprotectant in stroke. J. Cereb. Blood Flow Metab. 2000, 20:631-652.
30. Kappeler L., De Magalhaes Filho C., Leneuve P., Xu J., Brunel N., Chatziantoniou C., Le Bouc Y., Holzenberger M. Early postnatal nutrition determines somatotropic function in mice. Endocrinology 2009, 150:314-323.
31. Kikusui T., Ichikawa S., Mori Y. Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology 2009, 34:762-772.
32. Komori T., Morikawa Y., Nanjo K., Senba E. Induction of brain-derived neurotrophic factor by leptin in the ventromedial hypothalamus. Neuroscience 2006, 139:1107-1115.
33. Lechuga-Sancho A.M., Arroba A.I., Frago L.M., García-Cáceres C., Delgado Rúbin de Célix A., Argente J., Chowen J.A. Reduction in the number of astrocytes and their projections is associated with increased synaptic protein density in the hypothalamus of poorly controlled diabetic rats. Endocrinology 2006, 147:5314-5324.
34. Lévi F., Filipski E., Iurisci I., Li X.M., Innominato P. Cross-talks between circadian timing system and cell division cycle determine cancer biology and therapeutics. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:465-475.
35. Levin B.E. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2006, 361:1107-1121.
36. Llorente R., Llorente-Berzal A., Petrosino S., Marco E.M., Guaza C., Prada C., López-Gallardo M., Di Marzo V., Viveros M.P. Gender-dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: a possible role for the endocannabinoid system. Dev. Neurobiol. 2008, 68:1334-1347.
37. Llorente R., Gallardo M.L., Berzal A.L., Prada C., Garcia-Segura L.M., Viveros M.P. Early maternal deprivation in rats induces gender-dependent effects on developing hippocampal and cerebellar cells. Int. J. Dev. Neurosci. 2009, 27:233-241.
38. López-Gallardo M., Llorente R., Llorente-Berzal A., Marco E.M., Prada C., Di Marzo V., Viveros M.P. Neuronal and glial alterations in the cerebellar cortex of maternally deprived rats: gender differences and modulatory effects of two inhibitors of endocannabinoid inactivation. Dev. Neurobiol. 2008, 68:1429-1440.
39. MacLusky N.J., Naftolin F. Sexual differentiation of the central nervous system. Science 1981, 211:1294-1302.
40. Marais L., van Rensburg S.J., van Zyl J.M., Stein D.J., Daniels W.M Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neurosci. Res. 2008, 61:106-112.
41. Marco E.M., Adriani W., Llorente R., Laviola G., Viveros M.P. Detrimental psychophysiological effects of early maternal deprivation in adolescent and adult rodents: altered responses to cannabinoid exposure. Neurosci. Biobehav. Rev. 2009, 33:498-507.
42. Matsumoto Y., Yoshihara T., Yamasaki Y. Maternal deprivation in the early versus late postnatal period differentially affects growth and stress-induced corticosterone responses in adolescent rats. Brain Res. 2006, 1115:155-161.
43. McMillen I.C., Edwards L.J., Duffield J., Muhlhausler B.S. Regulation of leptin synthesis and secretion before birth: implications for the early programming of adult obesity. Reproduction 2006, 131:415-427.
44. Mesquita A.R., Pêgo J.M., Summavielle T., Maciel P., Almeida O.F., Sousa N. Neurodevelopment milestone abnormalities in rats exposed to stress in early life. Neuroscience 2007, 147:1022-1033.
45. Mitsushima D., Takase K., Funabashi T., Kimura F. Gonadal steroid hormones maintain the stress-induced acetylcholine release in the hippocampus: simultaneous measurements of the extracellular acetylcholine and serum corticosterone levels in the same subjects. Endocrinology 2008, 149:802-811.
46. Moles A., Sarli C., Bartolomucci A., D'Amato F.R. Interaction with stressed mothers affects corticosterone levels in pups after reunion and impairs the response to dexamethasone in adult mice. Psychoneuroendocrinology 2008, 33:462-470.
47. Musholt K., Cirillo G., Cavaliere C., Rosaria Bianco M., Bock J., Helmeke C., Braun K., Papa M. Neonatal separation stress reduces glial fibrillary acidic protein- and S100beta-immunoreactive astrocytes in the rat medial precentral cortex. Dev. Neurobiol. 2009, 69:203-211.
48. Nuñez J.L., Lauschke D.M., Juraska J.M. Cell death in the development of the posterior cortex in male and female rats. J. Com. Neurol. 2001, 436:32-41.
49. Oliver P., Picó C., De Matteis R., Cinti S., Palou A. Perinatal expression of leptin in rat stomach. Dev. Dyn. 2002, 223:148-154.
50. Oomen C.A., Girardi C.E., Cahyadi R., Verbeek E.C., Krugers H., Joëls M., Lucassen P.J. Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One 2009, 4:e3675.
51. Pencea V., Bingaman K.D., Wiegand S.J., Luskin M.B. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci. 2001, 21:6706-6717.
52. Pinto S., Roseberry A.G., Liu H., Diano S., Shanabrough M., Cai X., Friedman J.M., Horvath T.L. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 2004, 304:110-115.
53. Renard G.M., Rivarola M.A., Suárez M.M. Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int. J. Dev. Neurosci. 2007, 25:373-379.
54. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol. Psychiatry 2002, 7:609-616.
55. Roceri M., Cirulli F., Pessina C., Peretto P., Racagni G., Riva M.A. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 2004, 55:708-714.
56. Sacco R.L. Newer risk factors for stroke. Neurology 2001, 5:S31-S34.
57. Sakuma Y. Gonadal steroid action and brain sex differentiation in the rat. J. Neuroendocrinol. 2009, 21:410-414.
58. Salzmann C., Otis M., Long H., Roberge C., Gallo-Payet N., Walker C.D. Inhibition of steroidogenic response to adrenocorticotropin by leptin: implications for the adrenal response to maternal separation in neonatal rats. Endocrinology 2004, 145:1810-1822.
59. Schmidt M.V., Levine S., Alam S., Harbich D., Sterlemann V., Ganea K., de Kloet E.R., Holsboer F., Müller M.B. Metabolic signals modulate hypothalamic-pituitary-adrenal axis activation during maternal separation of the neonatal mouse. J. Neuroendocrinol. 2006, 18:865-874.
60. Schmidt M.V., Leibl C., Sterlemann V., Ganea K., Hartmann J., Harbich D., Müller M.B. Neuropeptide Y mediates the initial hypothalamic-pituitary-adrenal response to maternal separation in the neonatal mouse. J. Endocrinol. 2008, 197:421-427.
61. Smith M.A., Makino S., Kim S.Y., Kvetnansky R. Stress increases brain-derived neurotropic factor messenger ribonucleic acid in the hypothalamus and pituitary. Endocrinology 1995, 136:3743-3750.
62. Srinivasan M., Patel M.S. Metabolic programming in the immediate postnatal period. Trends Endocrinol. Metab. 2008, 19:146-152.
63. Suárez J., Llorente R., Romero-Zerbo S.Y., Mateos B., Bermúdez-Silva F.J., de Fonseca F.R., Viveros M.P. Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 2009, 19:623-632.
64. Tapia-Arancibia L., Rage F., Givalois L., Arancibia S. Physiology of BDNF: focus on hypothalamic function. Front. Neuroendocrinol. 2004, 25:77-107.
65. Van Den Eeden S.K., Tanner C.M., Bernstein A.L., Fross R.D., Leimpeter A., Bloch D.A., Nelson L.M. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am. J. Epidemiol. 2003, 157:1015-1022.
66. Vital P., Larrieta E., Hiriart M. Sexual dimorphism in insulin sensitivity and susceptibility to develop diabetes in rats. J. Endocrinol. 2006, 190:425-432.
67. Viveros M.P., Llorente R., López-Gallardo M., Suarez J., Bermúdez-Silva F., De la Fuente M., Rodriguez de Fonseca F., Garcia-Segura L.M. Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology 2009, 34(Supplement 1):S217-S226.
68. Yamauchi Y., Qin L.H., Nishihara M., Sawada K., Kato K., Inoue S. Vulnerability of synaptic plasticity in the complexin II knockout mouse to maternal deprivation stress. Brain Res. 2005, 1056:59-67.