Endogenous CNS expression of neurotensin and neurotensin receptors is altered during the postpartum period in outbred mice

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Driessen, Terri M ^a   Zhao, Changjiu ^a   Whittlinger, Anna ^a   Williams, Horecia ^b   Gammie, Stephen C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b FORT VALLEY STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NEUROTENSIN; NEUROTENSIN ANTIBODY; NEUROTENSIN RECEPTOR; NEUROTENSIN RECEPTOR 1; NEUROTENSIN RECEPTOR 2; PEPTIDE ANTIBODY; SORTILIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DORSAL STRIA TERMINALIS BED NUCLEUS; DOWN REGULATION; FEMALE; GENE EXPRESSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; MALE; MATERNAL BEHAVIOR; MEDIAL PREOPTIC AREA; MOUSE; NONHUMAN; OUTBRED MOUSE STRAIN; PROTEIN EXPRESSION; PUERPERIUM; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEPTUM PELLUCIDUM; STRIA TERMINALIS; UPREGULATION; VIRGINITY;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, OUTBRED STRAINS; BRAIN; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED ICR; NEUROTENSIN; POSTPARTUM PERIOD; RECEPTORS, NEUROTENSIN; RNA, MESSENGER;

EID: 84897403566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083098     Document Type: Article

References (108)

1. Lonstein JS, Gammie SC (2002) Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 26: 869-888. (Pubitemid 36347813)
2. Numan M, Insel TR (2003) The neurobiology of parental behavior. New York: Springer.
3. Petraglia F, Baraldi M, Giarre G, Facchinetti F, Santi M, et al. (1985) Opioid peptides of the pituitary and hypothalamus: changes in pregnant and lactating rats. J Endocrinol 105: 239-245. (Pubitemid 15117291)
4. Insel TR (1990) Regional Changes in Brain Oxytocin Receptors Post-Partum: Time-Course and Relationship to Maternal Behaviour. J Neuroendocrinol 2: 539-545.
5. Young LJ, Muns S, Wang Z, Insel TR (1997) Changes in Oxytocin Receptor mRNA in Rat Brain During Pregnancy and the Effects of Estrogen and Interleukin-6. J Neuroendocrinol 9: 859-865. (Pubitemid 27488768)
6. Gammie SC, Hasen NS, Awad TA, Auger AP, Jessen HM, et al. (2005) Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice. Brain Res Mol Brain Res 139: 201-211. (Pubitemid 41317932)
7. Maharjan S, Serova L, Sabban EL (2005) Transcriptional regulation of tyrosine hydroxylase by estrogen: opposite effects with estrogen receptors α and β and interactions with cyclic AMP. J Neurochem 93: 1502-1514. (Pubitemid 40853273)
8. Neumann ID (2008) Brain Oxytocin: A Key Regulator of Emotional and Social Behaviours in Both Females and Males. J Neuroendocrinol 20: 858-865.
9. Tsuneoka Y, Maruyama T, Yoshida S, Nishimori K, Kato T, et al. (2013) Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol 521: 1633-1663.
10. Johnstone LE, Leng G, Brown CH (2004) Effects of Neurotensin on the Organization of Activity in Supraoptic Nucleus Cells in Virgin and Lactating Rats. J Neuroendocrinol 16: 605-611. (Pubitemid 39029093)
11. Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, et al. (1989) Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp Brain Res 76: 593-602. (Pubitemid 19203612)
12. Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65: 768-779.
13. Gammie SC, D'Anna KL, Gerstein H, Stevenson SA (2009) Neurotensin Inversely Modulates Maternal Aggression. Neuroscience 158: 1215-1223.
14. Gammie SC, Lee G, Scotti ML, Stevenson SA, Gessay GM (2012) Neurotensin induced Egr-1 activity is altered in the postpartum period in mice. Brain Res 1433: 47-55.
15. Scotti ML, Stevenson SA, Gammie SC (2011) Changes in CNS response to neurotensin accompany the postpartum period in mice. Horm Behav 60: 177-184.
16. Carraway RE, Leeman SE (1973) The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 248: 6854-6861.
17. Tanaka K, Masu M, Nakanishi S (1990) Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4: 847-854. (Pubitemid 20208510)
18. Chalon P, Vita N, Kaghad M, Guillemot M, Bonnin J, et al. (1996) Molecular cloning of a levocabastine-sensitive neurotensin binding site. FEBS Lett 386: 91-94. (Pubitemid 26173063)
19. Mazella J, Botto JM, Guillemare E, Coppola T, Sarret P, et al. (1996) Structure, functional expression, and cerebral localization of the levocabastine-sensitive neurotensin/neuromedin N receptor from mouse brain. J Neurosci 16: 5613-5620. (Pubitemid 26293385)
20. Mazella J, Zsurger N, Navarro V, Chabry J, Kaghad M, et al. (1998) The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J Biol Chem 273: 26273-26276. (Pubitemid 28471624)
21. Nielsen MS, Jacobsen C, Olivecrona G, Gilemann J, Petersen CM (1999) Sortilin/neurotensin receptor-3 binds and mediates degradation of lipoprotein lipase. J Biol Chem 274: 8832-8836. (Pubitemid 29164682)
22. Uhl GR, Kuhar MJ, Snyder SH (1977) Neurotensin: immunohistochemical localization in rat central nervous system. Proc Natl Acad Sci 74: 4059-4063. (Pubitemid 8197775)
23. Jennes L, Stumpf WE, Kalivas PW (1982) Neurotensin: topographical distribution in rat brain by immunohistochemistry. J Comp Neurol 210: 211-224. (Pubitemid 12036966)
24. Alexander MJ, Miller MA, Dorsa DM, Bullock BP, Melloni RH Jr, et al. (1989) Distribution of neurotensin/neuromedin N mRNA in rat forebrain: unexpected abundance in hippocampus and subiculum. Proc Natl Acad Sci 86: 5202-5206. (Pubitemid 19182262)
25. Boudin H, Pelaprat D, Rostene W, Beaudet A (1996) Cellular distribution of neurotensin receptors in rat brain: immunohistochemical study using an antipeptide antibody against the cloned high affinity receptor. J Comp Neurol 373: 76-89. (Pubitemid 26292120)
26. Alexander MJ, Leeman SE (1998) Widespread expression in adult rat forebrain of mRNA encoding high-affinity neurotensin receptor. J Comp Neurol 402: 475-500. (Pubitemid 29001076)
27. Walker N, Lepee-Lorgeoux I, Fournier J, Betancur C, Rostene W, et al. (1998) Tissue distribution and cellular localization of the levocabastine- sensitive neurotensin receptor mRNA in adult rat brain. Brain Res Mol Brain Res 57: 193-200. (Pubitemid 28284671)
28. Sarret P, Krzywkowski P, Segal L, Nielsen MS, Petersen CM, et al. (2003) Distribution of NTS3 receptor/sortilin mRNA and protein in the rat central nervous system. J Comp Neurol 461: 483-505. (Pubitemid 36628998)
29. Binder EB, Kinkead B, Owens MJ, Nemeroff CB (2001) Neurotensin and dopamine interactions. Pharmacol Rev 53: 453-486. (Pubitemid 33136236)
30. Dobner PR (2005) Multitasking with neurotensin in the central nervous system. Cell Mol Life Sci 62: 1946-1963.
31. Sorenson CA, Gordon M (1975) Effects of 6-hydroxydopamine on shocke-licited aggression, emotionality and maternal behavior in female rats. Pharmacol Biochem Behav 3: 331-335.
32. Byrnes EM, Rigero BA, Bridges RS (2002) Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol Biochem Behav 73: 869-875. (Pubitemid 35246236)
33. Numan M, Numan MJ, Pliakou N, Stolzenberg DS, Mullins OJ, et al. (2005) The effects of D1 or D2 dopamine receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on the maternal retrieval response and other aspects of maternal behavior in rats. Behav Neurosci 119: 1588-1604. (Pubitemid 43145730)
34. Rowe W, Viau V, Meaney MJ, Quirion R (1995) Stimulation of CRH-mediated ACTH secretion by central administration of neurotensin: evidence for the participation of the paraventricular nucleus. J Neuroendocrinol 7: 109-117.
35. Nicot A, Rowe WB, De Kloet ER, Betancur C, Jessop DS, et al. (1997) Endogenous neurotensin regulates hypothalamic-pituitary-adrenal axis activity and peptidergic neurons in the rat hypothalamic paraventricular nucleus. J Neuroendocrinol 9: 263-269. (Pubitemid 27168432)
36. Nemeroff CB, Bissette G, Prange AJ Jr, Loosen PT, Barlow TS, et al. (1977) Neurotensin: central nervous system effects of a hypothalamic peptide. Brain Res 128: 485-496. (Pubitemid 8136671)
37. Remaury A, Vita N, Gendreau S, Jung M, Arnone M, et al. (2002) Targeted inactivation of the neurotensin type 1 receptor reveals its role in body temperature control and feeding behavior but not in analgesia. Brain Res 953: 63-72. (Pubitemid 35217808)
38. Dobner PR (2006) Neurotensin and pain modulation. Peptides 27: 2405-2414.
39. Nemeroff CB (1986) The interaction of neurotensin with dopaminergic pathways in the central nervous system: basic neurobiology and implications for the pathogenesis and treatment of schizophrenia. Psychoneuroendocrinology 11: 15-37.
40. Kinkead B, Nemeroff CB (2006) Novel treatments of schizophrenia: targeting the neurotensin system. CNS Neurol Disord Drug Targets 5: 205-218. (Pubitemid 43803124)
41. Angelidou A, Francis K, Vasiadi M, Alysandratos KD, Zhang B, et al. (2010) Neurotensin is increased in serum of young children with autistic disorder. J Neuroinflammation 7: 48.
42. Bridges RS (1996) Biochemical basis of parental behavior in the rat. In: Rosenblatt JS, Snowden CT (Eds), Parental care: evolution, mechanisms, and adaptive significance. Academic Press, San Diego.
43. Koch M, Ehret G (1989) Immunocytochemical localization and quantitation of estrogen-binding cells in the male and female (virgin, pregnant, lactating) mouse brain. Brain Res 489: 101-112. (Pubitemid 19144111)
44. Axelson JF, Shannon W, Van Leeuwen FW (1992) Immunocytochemical localization of estrogen receptors within neurotensin cells in the rostral preoptic area of the rat hypothalamus. Neurosci Lett 136: 5-9.
45. Lonstein JS, Greco B, De Vries GJ, Stern JM, Blaustein JD (2000) Maternal behavior stimulates c-fos activity within estrogen receptor alpha-containing neurons in lactating rats. Neuroendocrinology 72: 91-101.
46. Zhao C, Driessen TM, Gammie SC (2012) Glutamic acid decarboxylase 65 and 67 expression in the lateral septum is up-regulated in association with the postpartum period in mice. Brain Res 1470: 35-44.
47. O'Connor WT, Tanganelli S, Ungerstedt U, Fuxe K (1992) The effects of neurotensin on GABA and acetylcholine release in the dorsal striatum of the rat: an in vivo microdialysis study. Brain Res 573: 209-216.
48. Watters JJ, Dorsa DM (1998) Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms. J Neurosci 18: 6672-6680. (Pubitemid 28387999)
49. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176. (Pubitemid 46095716)
50. Conrad LC, Pfaff DW (1976) Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area. J Comp Neurol 169: 185-219.
51. Berk ML, Finkelstein JA (1981) Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6: 1601-1624. (Pubitemid 11043031)
52. Insel TR, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45: 1033-1041. (Pubitemid 19158297)
53. Consiglio AR, Lucion AB (1996) Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol Behav 59: 591-596. (Pubitemid 26110671)
54. Ziegler DR, Herman JP (2002) Neurocircuitry of stress integration: anatomical pathways regulating the hypothalamo-pituitary-adrenocortical axis of the rat. Integr Comp Biol 42: 541-551. (Pubitemid 35426503)
55. Slattery DA, Neumann ID (2008) No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 586: 377-385.
56. Silverman AJ, Hoffman DL, Zimmerman EA (1981) The descending afferent connections of the paraventricular nucleus of the hypothalamus (PVN). Brain Res Bull 6: 47-61. (Pubitemid 11129583)
57. Tribollet E, Dreifuss JJ (1981) Localization of neurones projecting to the hypothalamic paraventricular nucleus area of the rat: a horseradish peroxidase study. Neuroscience 6: 1315-1328. (Pubitemid 11074861)
58. Sawchenko PE, Swanson LW (1983) The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 218: 121-144. (Pubitemid 13035072)
59. Wakerley JB, Juss TS, Farrington R, Ingram CD (1990) Role of the paraventricular nucleus in controlling the frequency of milk ejection and the facilitatory effect of centrally administered oxytocin in the suckled rat. J Endocrinol 125: 467-475. (Pubitemid 20187737)
60. Insel TR, Shapiro LE (1992) Oxytocin receptors and maternal behavior. Ann N Y Acad Sci 652: 122-141.
61. Souaze F, Rostene W, Forgez P (1997) Neurotensin agonist induces differential regulation of neurotensin receptor mRNA. Identification of distinct transcriptional and post-transcriptional mechanisms. J Biol Chem 272: 10087-10094. (Pubitemid 27171684)
62. Najimi M, Souaze F, Mendez M, Hermans E, Berbar T, et al. (1998) Activation of receptor gene transcription is required to maintain cell sensitization after agonist exposure. Study on neurotensin receptor. J Biol Chem 273: 21634-21641. (Pubitemid 28405335)
63. Souaze F, Forgez P (2006) Molecular and cellular regulation of neurotensin receptor under acute and chronic agonist stimulation. Peptides 27: 2493-2501. (Pubitemid 44429935)
64. Gammie SC, Auger AP, Jessen HM, Vanzo RJ, Awad TA, et al. (2007) Altered gene expression in mice selected for high maternal aggression. Genes Brain Behav 6: 432-443. (Pubitemid 47028460)
65. Sheehan TP, Chambers RA, Russell DS (2004) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Brain Res Rev 46: 71-117. (Pubitemid 39036164)
66. D'Anna KL, Gammie SC (2009) Activation of corticotropin-releasing factor receptor 2 in lateral septum negatively regulates maternal defense. Behav Neurosci 123: 356-368.
67. Lee G, Gammie SC (2009) GABA(A) receptor signaling in the lateral septum regulates maternal aggression in mice. Behav Neurosci 123: 1169-1177.
68. Scotti MA, Lee G, Gammie SC (2011) Maternal defense is modulated by beta adrenergic receptors in lateral septum in mice. Behav Neurosci 125: 434-445.
69. Forray MI, Gysling K (2004) Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary- adrenal axis. Brain Res Brain Res Rev 47: 145-160. (Pubitemid 39574317)
70. Dunn JD (1987) Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 407: 327-331.
71. Herman JP, Cullinan WE, Watson SJ (1994) Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 6: 433-442. (Pubitemid 24254243)
72. Cullinan WE, Helmreich DL, Watson SJ (1996) Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neurol 368: 88-99. (Pubitemid 26131646)
73. Kendrick KM, Keverne EB, Hinton MR, Goode JA (1992) Oxytocin, amino acid and monoamine release in the region of the medial preoptic area and bed nucleus of the stria terminalis of the sheep during parturition and suckling. Brain Res 569: 199-209.
74. Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12: 1145-1148.
75. Allen GV, Cechetto DF (1995) Neurotensin in the lateral hypothalamic area: origin and function. Neuroscience 69: 533-544.
76. Nieuwenhuys R, Geeraedts LM, Veening JG (1982) The medial forebrain bundle of the rat. I. General introduction. J Comp Neurol 206: 49-81. (Pubitemid 12103431)
77. Numan M, Morrell JI, Pfaff DW (1985) Anatomical identification of neurons in selected brain regions associated with maternal behavior deficits induced by knife cuts of the lateral hypothalamus in rats. J Comp Neurol 237: 552-564. (Pubitemid 15072870)
78. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, et al. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci 95: 322-327. (Pubitemid 28103952)
79. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585. (Pubitemid 28101119)
80. D'Anna KL, Gammie SC (2006) Hypocretin-1 dose-dependently modulates maternal behaviour in mice. J Neuroendocrinol 18: 553-566.
81. Kalivas PW (1993) Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Brain Res Rev 18: 75-113.
82. Kislauskis E, Bullock B, McNeil S, Dobner PR (1988) The rat gene encoding neurotensin and neuromedin N. Structure, tissue-specific expression, and evolution of exon sequences. J Biol Chem 263: 4963-4968.
83. Maeno H, Yoshimura R, Fujita S, Su Q, Tanaka K, et al. (1996) Cloning and characterization of the rat neurotensin receptor gene promoter. Brain Res Mol Brain Res 40: 97-104. (Pubitemid 26241790)
84. Sun YJ, Maeno H, Aoki S, Wada K (2001) Mouse neurotensin receptor 2 gene (Ntsr2): genomic organization, transcriptional regulation and genetic mapping on chromosome 12. Brain Res Mol Brain Res 95: 167-171. (Pubitemid 33000376)
85. Kitabgi P, De Nadai F, Rovere C, Bidard JN (1992) Biosynthesis, maturation, release, and degradation of neurotensin and neuromedin N. Ann N Y Acad Sci 668: 30-42. (Pubitemid 23025844)
86. Kitabgi P (2006) Differential processing of pro-neurotensin/neuromedin N and relationship to pro-hormone convertases. Peptides 27: 2508-2514.
87. Kitabgi P (2006) Inactivation of neurotensin and neuromedin N by Zn metallopeptidases. Peptides 27: 2515-2522.
88. Mazella J, Vincent JP (2006) Internalization and recycling properties of neurotensin receptors. Peptides 27: 2488-2492. (Pubitemid 44425364)
89. Nelson RJ (1997) The use of genetic "knockout" mice in behavioral endocrinology research. Horm Behav 31:188-196.
90. Pettibone DJ, Hess JF, Hey PJ, Jacobson MA, Leviten M, et al. (2002) The effects of deleting the mouse neurotensin receptor NTR1 on central and peripheral responses to neurotensin. J Pharmacol Exp Ther 300: 305-313. (Pubitemid 34028541)
91. Maeno H, Yamada K, Santo-Yamada Y, Aoki K, Sun YJ, et al. (2004) Comparison of mice deficient in the high- or low-affinity neurotensin receptors, Ntsr1 or Ntsr2, reveals a novel function for Ntsr2 in thermal nociception. Brain Res 998: 122-129. (Pubitemid 38077132)
92. Dobner PR, Fadel J, Deitemeyer N, Carraway RE, Deutch AY (2001) Neurotensin-deficient mice show altered responses to antipsychotic drugs. Proc Natl Acad Sci 98: 8048-8053. (Pubitemid 32642684)
93. Brown KJ, Grunberg NE (1995) Effects of housing on male and female rats: crowding stresses male but calm females. Physiol Behav 58: 1085-1089. (Pubitemid 26003569)
94. Palanza P, Gioiosa L, Parmigiani S (2001) Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol Behav 73: 411-420. (Pubitemid 32595716)
95. Levine JB, Leeder AD, Parekkadan B, Berdichevsky Y, Rauch SL, et al. (2008) Isolation rearing impairs wound healing and is associated with increased locomotion and decreased immediate early gene expression in the medial prefrontal cortex of juvenile rats. Neuroscience 151: 589-603.
96. Miller SM, Piasecki CC, Peabody MF, Lonstein JS (2010) GABA-A receptor antagonism in the ventrocaudal periaqueductal gray increases anxiety in the anxiety-resistant postpartum rat. Pharmacol Biochem Behav 95: 1457-1465.
97. Jurek B, Slattery DA, Maloumby R, Hillerer K, Koszinowski S, et al. (2012) Differential contribution of hypothalamic MAPK activity in anxiety-like behaviour in virgin and lactating rats. PLoS ONE 7(5):e37060.
98. Young LJ, Muns S, Wang Z, Insel TR (1997) Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin-6. J Neuroendocrinol 9: 859-865. (Pubitemid 27488768)
99. Pawluski JL, Barakauskas VE, Galea LAM (2010) Pregnancy decreases oestrogen receptor alpha expression and pyknosis, but not cell proliferation or survival, in the hippocampus. J Neuroendocrinol 22: 248-257.
100. Marcondes FK, Bianchi FJ, Tanno AP (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62: 609-614.
101. Bonefeld BE, Elfving B, Wegener G (2008) Reference genes for normalization: a study of rat brain tissue. Synapse 62: 302-309. (Pubitemid 351365003)
102. Nelissen K, Smeets K, Mulder M, Hendriks JJ, Ameloot M (2010) Selection of reference genes for gene expression studies in rat oligodendrocytes using quantitative real time PCR. J Neurosci Methods 187: 78-83.
103. Zhao C, Saul MC, Driessen TM, Gammie SC (2012) Gene expression changes in the septum: possible implications for microRNAs in sculpting the maternal brain. PLoS One 7: e38602.
104. Cui H, Cai F, Belsham DD (2005) Anorexigenic hormones leptin, insulin, and alpha-melanocyte-stimulating hormone directly induce neurotensin (NT) gene expression in novel NT-expressing cell models. J Neurosci 25: 9497-9506. (Pubitemid 41464764)
105. Geerling JC, Kawata M, Loewy AD (2006) Aldosterone-sensitive neurons in the rat central nervous system. J Comp Neurol 494: 515-527. (Pubitemid 41790999)
106. Geisler S, Zahm DS (2006) Neurotensin afferents of the ventral tegmental area in the rat: [1] re-examination of their origins and [2] responses to acute psychostimulant and antipsychotic drug administration. Eur J Neurosci 24: 116-134. (Pubitemid 44050672)
107. Dobner PR, Barber DL, Villa-Komaroff L, McKiernan C (1987) Cloning and sequence analysis of cDNA for the canine neurotensin/neuromedin N precursor. Proc Natl Acad Sci 84: 3516-3520. (Pubitemid 17085435)
108. Gammie SC, Negron A, Newman SM, Rhodes JS (2004) Corticotropin-releasing factor inhibits maternal aggression in mice. Behav Neurosci 118: 805-814. (Pubitemid 38970501)