Prolactin administration during early postnatal life decreases hippocampal and olfactory bulb neurogenesis and results in depressive-like behavior in adulthood

Hormones and Behavior

Volumn 64, Issue 5, 2013, Pages 781-789

  Lajud, Naima ^a   Gonzalez Zapien, Rubén ^a   Roque, Angélica ^a   Tinajero, Eréndira ^a   Valdez, Juan José ^b   Clapp, Carmen ^c   Torner, Luz ^a  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO   (Mexico)

^c INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

Author keywords

Anxiety; BrdU; Development; Neonate; Neuroendocrine; Stress

Indexed keywords

BROXURIDINE; CORTICOSTERONE; PROLACTIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BRAIN DEVELOPMENT; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; EARLY LIFE STRESS; FEMALE; HIPPOCAMPUS; MALE; MENTAL DISEASE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PERINATAL PERIOD; PRIORITY JOURNAL; RAT;

ANXIETY; BRDU; DEVELOPMENT; NEONATE; NEUROENDOCRINE; STRESS;

AGING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; DEPRESSION; FEMALE; HIPPOCAMPUS; MALE; NEUROGENESIS; OLFACTORY BULB; PROLACTIN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84887179697     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.10.005     Document Type: Article

References (66)

1. Ali E.Y., Adam G.K., Ahmed S., Ali N.I., Adam I. Maternal and neonatal hormonal profiles in anaemic pregnant women of eastern Sudan. J. Obstet. Gynaecol. 2009, 29:311-314.
2. Bakowska J.C., Morrell J.I. Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat. J. Comp. Neurol. 1997, 386:161-177.
3. Bales K.L., Boone E., Epperson P., Hoffman G., Carter C.S. Are behavioral effects of early experience mediated by oxytocin?. Front. Psychiatry 2011, 2:24.
4. Bole-Feysot C., Goffin V., Edery M., Binart N., Kelly P.A. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 1998, 19:225-268.
5. Brummelte S., Pawluski J.L., Galea L.A. High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm. Behav. 2006, 50:370-382.
6. Campbell S., Macqueen G. The role of the hippocampus in the pathophysiology of major depression. J. Psychiatry Neurosci. 2004, 29(6):417-426.
7. Chapman D.P., Whitfield C.L., Felitti V.J., Dube S.R., Edwards V.J., Anda R.F. Adverse childhood experiences and the risk of depressive disorders in adulthood. J. Affect. Disord. 2004, 82:217-225.
8. Cohen R.A., Paul R.H., Stroud L., Gunstad J., Hitsman B.L., McCaffery J., Sweet L., Niaura R., MacFarlane A., Bryant R.A., Gordon E. Early life stress and adult emotional experience: an international perspective. Int. J. Psychiatry Med. 2006, 36:35-52.
9. Donner N., Neumann I.D. Effects of chronic intracerebral prolactin on the oxytocinergic and vasopressinergic system of virgin ovariectomized rats. Neuroendocrinology 2009, 90(3):315-322.
10. Dorner G., Plagemann A. Perinatal hyperinsulinism as possible predisposing factor for diabetes mellitus, obesity and enhanced cardiovascular risk in later life. Horm. Metab. Res. 1994, 26:213-221.
11. Drago F., Lissandrello C.O. The "low-dose" concept and the paradoxical effects of prolactin on grooming and sexual behavior. Eur. J. Pharmacol. 2000, 405:131-137.
12. Drago F., Pulvirenti L., Spadaro F., Pennisi G. Effects of TRH and prolactin in the behavioral despair (swim) model of depression in rats. Psychoneuroendocrinology 1990, 15:349-356.
13. Ebner K., Wotjak C.T., Landgraf R., Engelmann M. Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles. Horm. Behav. 2005, 47:14-21.
14. Faure J., Uys J.D., Marais L., Stein D.J., Daniels W.M. Early maternal separation alters the response to traumatization: resulting in increased levels of hippocampal neurotrophic factors. Metab. Brain Dis. 2007, 22:183-195.
15. Fernandez-Twinn D.S., Ozanne S.E., Ekizoglou S., Doherty C., James L., Gusterson B., Hales C.N. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br. J. Nutr. 2003, 90:815-822.
16. Ferraris J., Radl D.B., Zarate S., Jaita G., Eijo G., Zaldivar V., Clapp C., Seilicovich A., Pisera D. N-terminal prolactin-derived fragments, vasoinhibins, are proapoptotic and antiproliferative in the anterior pituitary. PLoS One 2011, 6:e21806.
17. Fuchs E., Czéh B., Kole M.H., Michaelis T., Lucassen P.J. Alterations of neuroplasticity in depression: the hippocampus and beyond. Eur. Neuropsychopharmacol. 2004, 14(Suppl. 5):S481-S490.
18. George E.D., Bordner K.A., Elwafi H.M., Simen A.A. Maternal separation with early weaning: a novel mouse model of early life neglect. BMC Neurosci. 2010, 11:123.
19. Gould E., Woolley C.S., McEwen B.S. Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J. Comp. Neurol. 1991, 313:479-485.
20. Grosvenor C.E., Whitworth N.S. Accumulation of prolactin by maternal milk and its transfer to circulation of neonatal rat-a review. Endocrinol. Exp. 1983, 17:271-282.
21. Heim C., Owens M.J., Plotsky P.M., Nemeroff C.B. The role of early adverse life events in the etiology of depression and posttraumatic stress disorder. Focus on corticotropin-releasing factor. Ann. N. Y. Acad. Sci. 1997, 821:194-207.
22. Hernández M.L., Fernández-Ruiz J.J., Navarro M., de Miguel R., Cebeira M., Vaticón L., Ramos J.A. Modifications of mesolimbic and nigrostriatal dopaminergic activities after intracerebroventricular administration of prolactin. J. Neural Transm. Gen. Sect. 1994, 96(1):63-79.
23. Jaroenporn S., Nagaoka K., Kasahara C., Ohta R., Watanabe G., Taya K. Physiological roles of prolactin in the adrenocortical response to acute restraint stress. Endocr. J. 2007, 54:703-711.
24. Joels M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
25. Kelly J.P., Wrynn A.S., Leonard B.E. The olfactory bulbectomized rat as a model of depression: an update. Pharmacol. Ther. 1997, 74(3):299-316.
26. Khodr C.E., Hurley D.L., Phelps C.J. Prolactin induces tuberoinfundibular dopaminergic neurone differentiation in Snell dwarf mice if administered beginning at 3days of age. J. Neuroendocrinol. 2009, 21(6):558-567.
27. Korosi A., Naninck E.F., Oomen C.A., Schouten M., Krugers H., Fitzsimons C., Lucassen P.J. Early-life stress mediated modulation of adult neurogenesis and behavior. Behav. Brain Res. 2011, 227:400-409.
28. Lajud N., Roque A., Cajero M., Gutierrez-Ospina G., Torner L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 2012, 37:410-420.
29. Larsen C.M., Grattan D.R. Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 2010, 151:3805-3814.
30. Lee J.H., Kim H.J., Kim J.G., Ryu V., Kim B.T., Kang D.W., Jahng J.W. Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci. Res. 2007, 58:32-39.
31. Legido A., Lago P., Chung H.J., Sperling M., Clancy R.R. Serum prolactin in neonates with seizures. Epilepsia 1995, 36:682-686.
32. Lozoff B. Early iron deficiency has brain and behavior effects consistent with dopaminergic dysfunction. J. Nutr. 2011, 141(4):740S-746S.
33. Lucassen P.J., Bosch O.J., Jousma E., Krömer S.A., Andrew R., Seckl J.R., Neumann I.D. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur. J. Neurosci. 2009, 29(1):97-103.
34. Luef G. Hormonal alterations following seizures. Epilepsy Behav. 2010, 19:131-133.
35. Lukas M., Bredewold R., Neumann I.D., Veenema A.H. Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 2010, 58(1):78-87.
36. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000, 20:9104-9110.
37. Mirescu C., Peters J.D., Gould E. Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 2004, 7:841-846.
38. Morales A., Bass N.E., Verhulst S.J. Serum prolactin levels and neonatal seizures. Epilepsia 1995, 36:349-354.
39. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., Holsboer F., Wotjak C.T., Almeida O.F., Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 2009, 12:1559-1566.
40. Nguyen N., Zhu Y. Prolactin functions as a survival factor during zebrafish embryogenesis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 153:88-93.
41. Porter T.E., Frawley L.S. Regulation of lactotrope differentiation in neonatal rats by a milk-borne peptide: a review. Endocr. Regul. 1993, 27:125-131.
42. Rault J.L., Carter C.S., Garner J.P., Marchant-Forde J.N., Richert B.T., Lay D.C. Repeated intranasal oxytocin administration in early life dysregulates the HPA axis and alters social behavior. Physiol. Behav. 2013, 112-113:40-48.
43. Royster M., Driscoll P., Kelly P.A., Freemark M. The prolactin receptor in the fetal rat: cellular localization of messenger ribonucleic acid, immunoreactive protein, and ligand-binding activity and induction of expression in late gestation. Endocrinology 1995, 136:3892-3900.
44. Rynikova A., Koppel J., Kuchar S., Cikos S., Mozes S. Effects of ovine prolactin in infant rats. Exp. Clin. Endocrinol. 1988, 92:241-244.
45. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 1986, 396:64-76.
46. Schapiro S. Pituitary ACTH and compensatory adrenal hypertrophy in stress-non-responsive infant rats. Endocrinology 1962, 71:986-989.
47. Schlessinger A.R., Cowan W.M., Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 1975, 159:149-175.
48. Seggie J.A., Brown G.M. Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can. J. Physiol. Pharmacol. 1975, 53:629-637.
49. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
50. Shyr S.W., Crowley W.R., Grosvenor C.E. Effect of neonatal prolactin deficiency on prepubertal tuberoinfundibular and tuberohypophyseal dopaminergic neuronal activity. Endocrinology 1986, 119:1217-1221.
51. Tejadilla D., Cerbon M., Morales T. Prolactin reduces the damaging effects of excitotoxicity in the dorsal hippocampus of the female rat independently of ovarian hormones. Neuroscience 2010, 169:1178-1185.
52. Torner L., Toschi N., Pohlinger A., Landgraf R., Neumann I.D. Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J. Neurosci. 2001, 21:3207-3214.
53. Torner L., Karg S., Blume A., Kandasamy M., Kuhn H.G., Winkler J., Aigner L., Neumann I.D. Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J. Neurosci. 2009, 29:1826-1833.
54. Tzschoppe A.A., Struwe E., Dorr H.G., Goecke T.W., Beckmann M.W., Schild R.L., Dotsch J. Differences in gene expression dependent on sampling site in placental tissue of fetuses with intrauterine growth restriction. Placenta 2010, 31:178-185.
55. van Oers H.J., de Kloet E.R., Levine S. Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res. Dev. Brain Res. 1998, 111:245-252.
56. Varvarigou A., Vagenakis A.G., Makri M., Frimas C., Beratis N.G. Prolactin and growth hormone in perinatal asphyxia. Biol. Neonate 1996, 69(2):76-83.
57. Veenema A.H., Blume A., Niederle D., Buwalda B., Neumann I.D. Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 2006, 24(6):1711-1720.
58. Vega C., Moreno-Carranza B., Zamorano M., Quintanar-Stephano A., Mendez I., Thebault S., Martinez de la Escalera G., Clapp C. Prolactin promotes oxytocin and vasopressin release by activating neuronal nitric oxide synthase in the supraoptic and paraventricular nuclei. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R1701-R1708.
59. Verina T., Rohde C.A., Guilarte T.R. Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats. Neuroscience 2007, 145:1037-1047.
60. Walker T.L., Vukovic J., Koudijs M.M., Blackmore D.G., Mackay E.W., Sykes A.M., Overall R.W., Hamlin A.S., Bartlett P.F. Prolactin stimulates precursor cells in the adult mouse hippocampus. PLoS One 2012, 7:e44371.
61. Walsh R.J., Slaby F.J., Posner B.I. A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 1987, 120:1846-1850.
62. Whitworth N.S., Grosvenor C.E. Transfer of milk prolactin to the plasma of neonatal rats by intestinal absorption. J. Endocrinol. 1978, 79:191-199.
63. \Wigger A., Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 1999, 66:293-302.
64. Yang D., Li Q., Fang L., Cheng K., Zhang R., Zheng P., Zhan Q., Qi Z., Zhong S., Xie P. Reduced neurogenesis and pre-synaptic dysfunction in the olfactory bulb of a rat model of depression. Neuroscience 2011, 192:609-618.
65. Zhang L., Hernandez V.S. Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalamic supraoptic and paraventricular nuclei. Neuroscience 2012, (Epub 2012 Oct 17). 10.1016/j.neuroscience.2012.10.010.
66. Zhang G.Y., Lu X.M., Sun R.P., Wang S.Z. Serum growth hormone and prolactin levels in neonates with hypoxic-ischemic encephalopathy. Zhongguo Dang Dai Er Ke Za Zhi 2006, 8(6):450-452.