ERK-FosB signaling in dorsal MPOA neurons plays a major role in the initiation of parental behavior in mice

Molecular and Cellular Neuroscience

Volumn 36, Issue 2, 2007, Pages 121-131

  Kuroda, Kumi O ^a   Meaney, Michael J ^b   Uetani, Noriko ^c   Fortin, Yannick ^d   Ponton, André ^d   Kato, Tadafumi ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN DERIVATIVE; PROTEIN NGF1 B; PROTEIN RAD1; PROTEIN SPRY1; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE INDUCTION; KNOCKOUT MOUSE; MALE; MEDIAL PREOPTIC AREA; MOUSE; NERVE CELL; NONHUMAN; PARENTAL BEHAVIOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION; MALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PATERNAL BEHAVIOR; PHOSPHORYLATION; PREGNANCY; PREOPTIC AREA; PROTO-ONCOGENE PROTEINS C-FOS; SIGNAL TRANSDUCTION;

MUS;

EID: 34548663644     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.05.010     Document Type: Article

References (65)

1. Atkins C.M., Selcher J.C., Petraitis J.J., Trzaskos J.M., and Sweatt J.D. The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1 (1998) 602-609
2. Bridges R.S. Biochemical basis of parental behavior in the rat. In: Rosenblatt J.S., and Snowdon C.T. (Eds). Parental Care: Evolution, Mechanism, and Adaptive Significance (1996), Academic Press, San Diego 215-242
3. Bridges R.S., and Scanlan V.F. Maternal memory in adult, nulliparous rats: effects of testing interval on the retention of maternal behavior. Dev. Psychobiol. 46 (2005) 13-18
4. Brown J.R., Ye H., Bronson R.T., Dikkes P., and Greenberg M.E. A defect in nurturing in mice lacking the immediate early gene fosB. Cell 86 (1996) 297-309
5. Butcher G.Q., Lee B., and Obrietan K. Temporal regulation of light-induced extracellular signal-regulated kinase activation in the suprachiasmatic nucleus. J. Neurophysiol. 90 (2003) 3854-3863
6. Calamandrei G., and Keverne E.B. Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience. Behav. Neurosci. 108 (1994) 113-120
7. Chaudhuri A. Neural activity mapping with inducible transcription factors. NeuroReport 8 (1997) iii-vii
8. Cohen L., Mohr R., Chen Y.Y., Huang M., Kato R., Dorin D., Tamanoi F., Goga A., Afar D., Rosenberg N., and Witte O. Transcriptional activation of a ras-like gene (kir) by oncogenic tyrosine kinases. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12448-12452
9. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., and Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17 (1997) 2295-2313
10. Deng X., Ladenheim B., Tsao L.I., and Cadet J.L. Null mutation of c-fos causes exacerbation of methamphetamine-induced neurotoxicity. J. Neurosci. 19 (1999) 10107-10115
11. Ferguson S.M., and Robinson T.E. Amphetamine-evoked gene expression in striatopallidal neurons: regulation by corticostriatal afferents and the ERK/MAPK signaling cascade. J. Neurochem. 91 (2004) 337-348
12. Fifkova E., and Van Harreveld A. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6 (1977) 211-230
13. Fifkova E., and Delay R.J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J. Cell Biol. 95 (1982) 345-350
14. Fleming A.S., and Luebke C. Timidity prevents the virgin female rat from being a good mother: emotionality differences between nulliparous and parturient females. Physiol. Behav. 27 (1981) 863-868
15. Gammie S.C. Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav. Cogn. Neurosci. Rev. 4 (2005) 119-135
16. Geinisman Y., Berry R.W., Disterhoft J.F., Power J.M., and Van der Zee E.A. Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21 (2001) 5568-5573
17. Hacohen N., Kramer S., Sutherland D., Hiromi Y., and Krasnow M.A. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92 (1998) 253-263
18. Hamaguchi-Hamada K., Sanbo C., Hamada S., and Yagi T. Exposure to hexanal odor influences maternal behavior and induces neonatal death in Fyn tyrosine kinase-deficient mice. Neurosci. Res. 48 (2004) 259-267
19. Herdegen T., and Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 28 (1998) 370-490
20. Hiroi N., Brown J.R., Haile C.N., Ye H., Greenberg M.E., and Nestler E.J. FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psychomotor and rewarding effects. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10397-10402
21. Hiroi N., Marek G.J., Brown J.R., Ye H., Saudou F., Vaidya V.A., Duman R.S., Greenberg M.E., and Nestler E.J. Essential role of the FosB gene in molecular, cellular, and behavioral actions of chronic electroconvulsive seizures. J. Neurosci. 18 (1998) 6952-6962
22. Impagnatiello M.A., Weitzer S., Gannon G., Compagni A., Cotten M., and Christofori G. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152 (2001) 1087-1098
23. Jacobson C.D., Terkel J., Gorski R.A., and Sawyer C.H. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res. 194 (1980) 471-478
24. Jin S.H., Blendy J.A., and Thomas S.A. Cyclic AMP response element-binding protein is required for normal maternal nurturing behavior. Neuroscience 133 (2005) 647-655
25. Kalinichev M., Rosenblatt J.S., and Morrell J.I. The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats. Behav. Neurosci. 114 (2000) 196-210
26. Kalinichev M., Rosenblatt J.S., Nakabeppu Y., and Morrell J.I. Induction of c-fos-like and fosB-like immunoreactivity reveals forebrain neuronal populations involved differentially in pup-mediated maternal behavior in juvenile and adult rats. J. Comp. Neurol. 416 (2000) 45-78
27. Kelly K. The RGK family: a regulatory tail of small GTP-binding proteins. Trends Cell Biol. 15 (2005) 640-643
28. Keyser-Marcus L., Stafisso-Sandoz G., Gerecke K., Jasnow A., Nightingale L., Lambert K.G., Gatewood J., and Kinsley C.H. Alterations of medial preoptic area neurons following pregnancy and pregnancy-like steroidal treatment in the rat. Brain Res. Bull. 55 (2001) 737-745
29. Krasnegor N.A., and Bridges R.S. Mammalian Parenting: Biochemical, Neurobiological, and Behavioral Determinants (1990), Oxford UP, New York
30. Lamprecht R., and LeDoux J. Structural plasticity and memory. Nat. Rev., Neurosci. 5 (2004) 45-54
31. Leckman J.F., and Herman A.E. Maternal behavior and developmental psychopathology. Biol. Psychiatry 51 (2002) 27-43
32. Lee A.W., and Brown R.E. Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav. Neurosci. 116 (2002) 968-975
33. Leone A., Mitsiades N., Ward Y., Spinelli B., Poulaki V., Tsokos M., and Kelly K. The Gem GTP-binding protein promotes morphological differentiation in neuroblastoma. Oncogene 20 (2001) 3217-3225
34. Li C., Chen P., and Smith M.S. Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 94 (1999) 117-129
35. Lonstein J.S., and De Vries G.J. Sex differences in the parental behavior of rodents. Neurosci. Biobehav. Rev. 24 (2000) 669-686
36. Luo L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 18 (2002) 601-635
37. Maguire J., Santoro T., Jensen P., Siebenlist U., Yewdell J., and Kelly K. Gem: an induced, immediate early protein belonging to the Ras family. Science 265 (1994) 241-244
38. Mason J.M., Morrison D.J., Basson M.A., and Licht J.D. Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 16 (2006) 45-54
39. Mellstrom B., and Naranjo J.R. Mechanisms of Ca(2+)-dependent transcription. Curr. Opin. Neurobiol. 11 (2001) 312-319
40. Minowada G., Jarvis L.A., Chi C.L., Neubuser A., Sun X., Hacohen N., Krasnow M.A., and Martin G.R. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126 (1999) 4465-4475
41. Morgan H.D., Watchus J.A., Milgram N.W., and Fleming A.S. The long lasting effects of electrical simulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav. Brain Res. 99 (1999) 61-73
42. Numan M. Brain mechanisms and parental behavior. In: Adler N., Pfarr D., and Goy R.W. (Eds). Handbook of Behavioral Neurobiology (1985), Plenum, New York 537-605
43. Numan M. Maternal behavior. In: Knobili E., and Neill J.D. (Eds). The Physiology of Reproduction. 2nd edition (1994), Raven, New York 221-302
44. Numan M., and Numan M.J. Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav. Neurosci. 108 (1994) 379-394
45. Numan M., and Insel T.R. The Neurobiology of Parental Behavior (2003), Springer-Verlag, New York
46. Numan M., McSparren J., and Numan M.J. Dorsolateral connections of the medial preoptic area and maternal behavior in rats. Behav. Neurosci. 104 (1990) 964-979
47. Numan M., Numan M.J., Marzella S.R., and Palumbo A. Expression of c-fos, fos B, and egr-1 in the medial preoptic area and bed nucleus of the stria terminalis during maternal behavior in rats. Brain Res. 792 (1998) 348-352
48. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates (2001), Academic Press, San Diego
49. Radwanska K., Caboche J., and Kaczmarek L. Extracellular signal-regulated kinases (ERKs) modulate cocaine-induced gene expression in the mouse amygdala. Eur. J. Neurosci. 22 (2005) 939-948
50. Rosenblatt J.S. Nonhormonal basis of maternal behavior in the rat. Science 156 (1967) 1512-1514
51. Rosenblatt J.S., Hazelwood S., and Poole J. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm. Behav. 30 (1996) 201-215
52. Selcher J.C., Atkins C.M., Trzaskos J.M., Paylor R., and Sweatt J.D. A necessity for MAP kinase activation in mammalian spatial learning. Learn. Mem. 6 (1999) 478-490
53. Shi X., and McGinty J.F. Extracellular signal-regulated mitogen-activated protein kinase inhibitors decrease amphetamine-induced behavior and neuropeptide gene expression in the striatum. Neuroscience 138 (2006) 1289-1298
54. Stern J.M., and Johnson S.K. Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli. Physiol. Behav. 47 (1990) 993-1011
55. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 14 (2004) 311-317
56. Terkel J., Bridges R.S., and Sawyer C.H. Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: nest building, pup retrieval and prolactin secretion. Brain Res. 169 (1979) 369-380
57. Thomas G.M., and Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev., Neurosci. 5 (2004) 173-183
58. Toni N., Buchs P.A., Nikonenko I., Bron C.R., and Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402 (1999) 421-425
59. Valjent E., Corvol J.C., Pages C., Besson M.J., Maldonado R., and Caboche J. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J. Neurosci. 20 (2000) 8701-8709
60. Van Aelst L., and Cline H.T. Rho GTPases and activity-dependent dendrite development. Curr. Opin. Neurobiol. 14 (2004) 297-304
61. vom Saal F.S., and Howard L.S. The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 215 (1982) 1270-1272
62. Watson M.A., and Milbrandt J. The NGFI-B gene, a transcriptionally inducible member of the steroid receptor gene superfamily: genomic structure and expression in rat brain after seizure induction. Mol. Cell. Biol. 9 (1989) 4213-4219
63. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., and Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 11024-11031
64. Zhang J., Zhang D., McQuade J.S., Behbehani M., Tsien J.Z., and Xu M. c-fos regulates neuronal excitability and survival. Nat. Genet. 30 (2002) 416-420
65. Zhang L., Lou D., Jiao H., Zhang D., Wang X., Xia Y., Zhang J., and Xu M. Cocaine-induced intracellular signaling and gene expression are oppositely regulated by the dopamine D1 and D3 receptors. J. Neurosci. 24 (2004) 3344-3354