Intracranial self-stimulation to the lateral hypothalamus, a memory improving treatment, results in hippocampal changes in gene expression

Neuroscience

Volumn 162, Issue 2, 2009, Pages 359-374

  Huguet, G ^a   Aldavert Vera, L ^b   Kadar E ^a   Pena de Ortiz S ^c   Morgado Bernal, I ^b   Segura Torres, P ^b  

^a UNIVERSITY OF GIRONA   (Spain)

^b INSTITUT DE NEUROCIÈNCIES   (Spain)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

c Fos immunohistochemistry; deep brain stimulation; intracranial self stimulation; microarray; neural plasticity; neuroprotection

Indexed keywords

ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE 1; CALMODULIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70 1A; PHOSPHODIESTERASE I; PHOSPHODIESTERASE IA; POLYPEPTIDE; PROTEIN C FOS; PROTEIN FOS; PROTEIN RET; SERUM AND GLUCOCORTICOID REGULATED KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; FACILITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; MEMORY; MICROARRAY ANALYSIS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THERAPY EFFECT;

EID: 67649367529     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.04.074     Document Type: Article

References (99)

1. Adamik A., and Telegdy G. Effects of pituitary adenylate cyclase polypeptide (PACAP) on extinction of active avoidance learning in rats: involvement of neurotransmitters. Regul Pept 127 (2005) 55-62
2. Aimone J.B., Wiles J., and Gage F.H. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9 (2006) 723-727
3. Albrecht D. Angiotensin-(1-7)-induced plasticity changes in the lateral amygdala are mediated by COX-2 and NO. Learn Mem 14 (2007) 177-184
4. Aldavert-Vera L., Costa-Miserachs D., Massanes-Rotger E., Soriano-Mas C., Segura-Torres P., and Morgado-Bernal I. Facilitation of a distributed shuttle-box conditioning with posttraining intracranial self-stimulation in old rats. Neurobiol Learn Mem 67 (1997) 254-258
5. Aldavert-Vera L., Segura-Torres P., Costa-Miserachs D., and Morgado-Bernal I. Shuttle-box memory facilitation by posttraining intracranial self-stimulation: differential effects in rats with high and low basic conditioning levels. Behav Neurosci 110 (1996) 346-352
6. Arvanitogiannis A., Flores C., and Shizgal P. Fos-like immunoreactivity in the caudal diencephalon and brainstem following lateral hypothalamic self-stimulation. Behav Brain Res 88 (1997) 275-279
7. Bakshi A., Shimizu S., Keck C.A., Cho S., LeBold D.G., Morales D., Arenas E., Snyder E.Y., Watson D.J., and McIntosh T.K. Neural progenitor cells engineered to secrete GDNF show enhanced survival, neuronal differentiation and improve cognitive function following traumatic brain injury. Eur J Neurosci 23 (2006) 2119-2134
8. Barlow A., de Graaff E., and Pachnis V. Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron 40 (2003) 905-916
9. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57 (1995) 289-300
10. Bertaina-Anglade V., Tramu G., and Destrade C. Differential learning-stage dependent patterns of c-Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur J Neurosci 12 (2000) 3803-3812
11. Blokland A., Schreiber R., and Prickaerts J. Improving memory: a role for phosphodiesterases. Curr Pharm Des 12 (2006) 2511-2523
12. Brenneman D.E. Neuroprotection: a comparative view of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Peptides 28 (2007) 1720-1726
13. Carra S., Seguin S.J., Lambert H., and Landry J. HspB8 chaperone activity toward poly(Q)-containing proteins depends on its association with Bag3, a stimulator of macroautophagy. J Biol Chem 283 (2008) 1437-1444
14. Charych E.I., Akum B.F., Goldberg J.S., Jornsten R.J., Rongo C., Zheng J.Q., and Firestein B.L. Activity-independent regulation of dendrite patterning by postsynaptic density protein PSD-95. J Neurosci 26 (2006) 10164-10176
15. Chen Y., Fenoglio K.A., Dube C.M., Grigoriadis D.E., and Baram T.Z. Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol Psychiatry 11 (2006) 992-1002
16. Chen W., Li N., Chen T., Han Y., Li C., Wang Y., He W., Zhang L., Wan T., and Cao X. The lysosome-associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway. J Biol Chem 280 (2005) 40985-40995
17. Cohen J. Statistical power analysis for the behavioural sciences (1988), Academic Press, New York
18. Cotman C.W., and Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25 (2002) 295-301
19. Countryman R.A., Kaban N.L., and Colombo P.J. Hippocampal c-fos is necessary for long-term memory of a socially transmitted food preference. Neurobiol Learn Mem 84 (2005) 175-183
20. Countryman R.A., Orlowski J.D., Brightwell J.J., Oskowitz A.Z., and Colombo P.J. CREB phosphorylation and c-Fos expression in the hippocampus of rats during acquisition and recall of a socially transmitted food preference. Hippocampus 15 (2005) 56-67
21. Dalla C., Bangasser D.A., Edgecomb C., and Shors T.J. Neurogenesis and learning: acquisition and asymptotic performance predict how many new cells survive in the hippocampus. Neurobiol Learn Mem 88 (2007) 143-148
22. Departament de Medi Ambient. Generalitat de Catalunya (1995) Generalitat de Catalunya. LAW 5/1995 on protection of animals used for experimentation and other scientific purposes. DOGC num. 2073.
23. Doong H., Vrailas A., and Kohn E.C. What's in the "BAG"-a functional domain analysis of the BAG-family proteins. Cancer Lett 188 (2002) 25-32
24. Epp J.R., Spritzer M.D., and Galea L.A. Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 149 (2007) 273-285
25. Falluel-Morel A., Chafai M., Vaudry D., Basille M., Cazillis M., Aubert N., Louiset E., de Jouffrey S., Le Bigot J.F., Fournier A., Gressens P., Rostene W., Vaudry H., and Gonzalez B.J. The neuropeptide pituitary adenylate cyclase-activating polypeptide exerts anti-apoptotic and differentiating effects during neurogenesis: focus on cerebellar granule neurones and embryonic stem cells. J Neuroendocrinol 19 (2007) 321-327
26. Fleischmann A., Hvalby O., Jensen V., Strekalova T., Zacher C., Layer L.E., Kvello A., Reschke M., Spanagel R., Sprengel R., Wagner E.F., and Gass P. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23 (2003) 9116-9122
27. Fujikake N., Nagai Y., Popiel H.A., Okamoto Y., Yamaguchi M., and Toda T. Heat shock transcription factor 1-activating compounds suppress polyglutamine-induced neurodegeneration through induction of multiple molecular chaperones. J Biol Chem 283 (2008) 26188-26197
28. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., Hornik K., Hothorn T., Huber W., Iacus S., Irizarry R., Leisch F., Li C., Maechler M., Rossini A.J., Sawitzki G., Smith C., Smyth G., Tierney L., Yang J.Y., and Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 (2004) R80
29. Giffard R.G., Xu L., Zhao H., Carrico W., Ouyang Y., Qiao Y., Sapolsky R., Steinberg G., Hu B., and Yenari M.A. Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J Exp Biol 207 (2004) 3213-3220
30. Gil G.A., Bussolino D.F., Portal M.M., Pecchio A.A., Renner M.L., Borioli G.A., Guido M.E., and Caputto B.L. c-Fos activated phospholipid synthesis is required for neurite elongation in differentiating PC12 cells. Mol Biol Cell 15 (2004) 1881-1894
31. Giraudier S., Chagraoui H., Komura E., Barnache S., Blanchet B., LeCouedic J.P., Smith D.F., Larbret F., Taksin A.L., Moreau-Gachelin F., Casadevall N., Tulliez M., Hulin A., Debili N., and Vainchenker W. Overexpression of FKBP51 in idiopathic myelofibrosis regulates the growth factor independence of megakaryocyte progenitors. Blood 100 (2002) 2932-2940
32. Glass G.V. Primary, secondary, and meta-analysis of research. Ed Res 10 (1976) 3-8
33. Hamani C., Neimat J.S., and Lozano A.M. Deep brain stimulation and chemical neuromodulation: current use and perspectives for the future. Acta Neurochir Suppl 97 (2007) 127-133
34. Henning J., Koczan D., Glass A., Karopka T., Pahnke J., Rolfs A., Benecke R., and Gimsa U. Deep brain stimulation in a rat model modulates TH, CaMKIIa and Homer1 gene expression. Eur J Neurosci 25 (2007) 239-250
35. Hsu K., Passey R.J., Endoh Y., Rahimi F., Youssef P., Yen T., and Geczy C.L. Regulation of S100A8 by glucocorticoids. J Immunol 174 (2005) 2318-2326
36. Humbert S., and Saudou F. Huntington's disease: intracellular signaling pathways and neuronal death. J Soc Biol 199 (2005) 247-251
37. Huston J.P., and Mueller C.C. Enhanced passive avoidance learning and appetitive T-maze learning with post-trial rewarding hypothalamic stimulation. Brain Res Bull 3 (1978) 265-270
38. Kadoyama K., Takahashi Y., Higashida H., Tanabe T., and Yoshimoto T. Cyclooxygenase-2 stimulates production of amyloid beta-peptide in neuroblastoma x glioma hybrid NG108-15 cells. Biochem Biophys Res Commun 281 (2001) 483-490
39. Katoh Y., and Katoh M. Comparative genomics on SLIT1, SLIT2, and SLIT3 orthologs. Oncol Rep 14 (2005) 1351-1355
40. Kendziorski C., Irizarry R.A., Chen K.S., Haag J.D., and Gould M.N. On the utility of pooling biological samples in microarray experiments. Proc Natl Acad Sci U S A 102 (2005) 4252-4257
41. Koylu E.O., Balkan B., Kuhar M.J., and Pogun S. Cocaine and amphetamine regulated transcript (CART) and the stress response. Peptides 27 (2006) 1956-1969
42. Leach L., Whishaw I.Q., and Kolb B. Effects of kainic acid lesions in the lateral hypothalamus on behavior and hippocampal and neocortical electroencephalographic (EEG) activity in the rat. Behav Brain Res 1 (1980) 411-431
43. Lee T.H., Jang M.H., Shin M.C., Lim B.V., Kim Y.P., Kim H., Choi H.H., Lee K.S., Kim E.H., and Kim C.J. Dependence of rat hippocampal c-fos expression on intensity and duration of exercise. Life Sci 72 (2003) 1421-1436
44. Leuner B., Gould E., and Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 16 (2006) 216-224
45. Lin K.M., Hollander J.M., Kao V.Y., Lin B., Macpherson L., and Dillmann W.H. Myocyte protection by 10 kD heat shock protein (Hsp10) involves the mobile loop and attenuation of the Ras GTP-ase pathway. FASEB J 18 (2004) 1004-1006
46. Ma Y.L., Tsai M.C., Hsu W.L., and Lee E.H. SGK protein kinase facilitates the expression of long-term potentiation in hippocampal neurons. Learn Mem 13 (2006) 114-118
47. Mao P., Ardeshiri A., Jacks R., Yang S., Hurn P.D., and Alkayed N.J. Mitochondrial mechanism of neuroprotection by CART. Eur J Neurosci 26 (2007) 624-632
48. Marie-Claire C., Laurendeau I., Canestrelli C., Courtin C., Vidaud M., Roques B., and Noble F. Fos but not Cart (cocaine and amphetamine regulated transcript) is overexpressed by several drugs of abuse: a comparative study using real-time quantitative polymerase chain reaction in rat brain. Neurosci Lett 345 (2003) 77-80
49. Matsuyama S., Matsumoto A., Hashimoto H., Shintani N., and Baba A. Impaired long-term potentiation in vivo in the dentate gyrus of pituitary adenylate cyclase-activating polypeptide (PACAP) or PACAP type 1 receptor-mutant mice. Neuroreport 14 (2003) 2095-2098
50. Mizokami A., Kanematsu T., Ishibashi H., Yamaguchi T., Tanida I., Takenaka K., Nakayama K.I., Fukami K., Takenawa T., Kominami E., Moss S.J., Yamamoto T., Nabekura J., and Hirata M. Phospholipase C-related inactive protein is involved in trafficking of gamma2 subunit-containing GABA(A) receptors to the cell surface. J Neurosci 27 (2007) 1692-1701
51. Myers S.M., and Mulligan L.M. The RET receptor is linked to stress response pathways. Cancer Res 64 (2004) 4453-4463
52. Nakahara D., Nakamura M., Oki Y., and Ishida Y. Lack of glucocorticoids attenuates the self-stimulation-induced increase in the in vivo synthesis rate of dopamine but not serotonin in the rat nucleus accumbens. Eur J Neurosci 12 (2000) 1495-1500
53. Ousman S.S., Tomooka B.H., van Noort J.M., Wawrousek E.F., O'Connor K.C., Hafler D.A., Sobel R.A., Robinson W.H., and Steinman L. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448 (2007) 474-479
54. Park J., Kim M., Na G., Jeon I., Kwon Y.K., Kim J.H., Youn H., and Koo Y. Glucocorticoids modulate NF-kappaB-dependent gene expression by up-regulating FKBP51 expression in Newcastle disease virus-infected chickens. Mol Cell Endocrinol 278 (2007) 7-17
55. Park J.S., Onodera T., Nishimura S., Thompson R.F., and Itohara S. Molecular evidence for two-stage learning and partial laterality in eyeblink conditioning of mice. Proc Natl Acad Sci U S A 103 (2006) 5549-5554
56. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1998), Academic Press, San Diego
57. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 (2001) e45
58. Pizarro J.M., Haro L.S., and Barea-Rodriguez E.J. Learning associated increase in heat shock cognate 70 mRNA and protein expression. Neurobiol Learn Mem 79 (2003) 142-151
59. Rall J.M., Mach S.A., and Dash P.K. Intrahippocampal infusion of a cyclooxygenase-2 inhibitor attenuates memory acquisition in rats. Brain Res 968 (2003) 273-276
60. Ramkumar K., Srikumar B.N., Shankaranarayana Rao B.S., and Raju T.R. Self-stimulation rewarding experience restores stress-induced CA3 dendritic atrophy, spatial memory deficits and alterations in the levels of neurotransmitters in the hippocampus. Neurochem Res 33 (2008) 1651-1662
61. Rao B.S., Desiraju T., Meti B.L., and Raju T.R. Plasticity of hippocampal and motor cortical pyramidal neurons induced by self-stimulation experience. Indian J Physiol Pharmacol 38 (1994) 23-28
62. Rao B.S., Desiraju T., and Raju T.R. Neuronal plasticity induced by self-stimulation rewarding experience in rats-a study on alteration in dendritic branching in pyramidal neurons of hippocampus and motor cortex. Brain Res 627 (1993) 216-224
63. Rao B.S., Raju T.R., and Meti B.L. Increased numerical density of synapses in CA3 region of hippocampus and molecular layer of motor cortex after self-stimulation rewarding experience. Neuroscience 91 (1999) 799-803
64. Redolar-Ripoll D., Aldavert-Vera L., Soriano-Mas C., Segura-Torres P., and Morgado-Bernal I. Intracranial self-stimulation facilitates memory consolidation, but not retrieval: its effects are more effective than increased training. Behav Brain Res 129 (2002) 65-75
65. Redolar-Ripoll D., Soriano-Mas C., Guillazo-Blanch G., Aldavert-Vera L., Segura-Torres P., and Morgado-Bernal I. Posttraining intracranial self-stimulation ameliorates the detrimental effects of parafascicular thalamic lesions on active avoidance in young and aged rats. Behav Neurosci 117 (2003) 246-256
66. Roberto M., Scuri R., and Brunelli M. Differential effects of PACAP-38 on synaptic responses in rat hippocampal CA1 region. Learn Mem 8 (2001) 265-271
67. Romanelli P., Di Matteo L., Cobellis G., Varriale B., Menegazzi M., Gironi Carnevale U.A., Ruocco L.A., and Sadile A.G. Transcription factor expression, RNA synthesis and NADPH-diaphorase across the rat brain and exposure to spatial novelty. Behav Brain Res 184 (2007) 91-100
68. Roozendaal B., Okuda S., Van der Zee E.A., and McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 103 (2006) 6741-6746
69. Ruiz-Medina J., Morgado-Bernal I., Redolar-Ripoll D., Aldavert-Vera L., and Segura-Torres P. Intracranial self-stimulation facilitates a spatial learning and memory task in the Morris water maze. Neuroscience 154 (2008) 424-430
70. Ruiz-Medina J., Redolar-Ripoll D., Morgado-Bernal I., Aldavert-Vera L., and Segura-Torres P. Intracranial self-stimulation improves memory consolidation in rats with little training. Neurobiol Learn Mem 89 (2008) 574-581
71. Salin P., Manrique C., Forni C., and Kerkerian-Le Goff L. High-frequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci 22 (2002) 5137-5148
72. Sarter M., and Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95 (2000) 933-952
73. Sasaki T., Kitagawa K., Sugiura S., Omura-Matsuoka E., Tanaka S., Yagita Y., Okano H., Matsumoto M., and Hori M. Implication of cyclooxygenase-2 on enhanced proliferation of neural progenitor cells in the adult mouse hippocampus after ischemia. J Neurosci Res 72 (2003) 461-471
74. Saunders R.C., and Aggleton J.P. Origin and topography of fibers contributing to the fornix in macaque monkeys. Hippocampus 17 (2007) 396-411
75. Scheier B., Foletti A., Stark G., Aoyama A., Dobbeling U., Rusconi S., and Klemenz R. Glucocorticoids regulate the expression of the stress protein alpha B-crystallin. Mol Cell Endocrinol 123 (1996) 187-198
76. Schultz W. Multiple reward signals in the brain. Nat Rev Neurosci 1 (2000) 199-207
77. Segura-Torres P., Portell-Cortes I., and Morgado-Bernal I. Improvement of shuttle-box avoidance with post-training intracranial self-stimulation, in rats: a parametric study. Behav Brain Res 42 (1991) 161-167
78. Shankaranarayana Rao B.S., Raju T.R., and Meti B.L. Self-stimulation rewarding experience induced alterations in dendritic spine density in CA3 hippocampal and layer V motor cortical pyramidal neurons. Neuroscience 89 (1999) 1067-1077
79. Sharifzadeh M., Tavasoli M., Soodi M., Mohammadi-Eraghi S., Ghahremani M.H., and Roghani A. A time course analysis of cyclooxygenase-2 suggests a role in spatial memory retrieval in rats. Neurosci Res 54 (2006) 171-179
80. Shirvalkar P., Seth M., Schiff N.D., and Herrera D.G. Cognitive enhancement with central thalamic electrical stimulation. Proc Natl Acad Sci U S A 103 (2006) 17007-17012
81. Smyth G.K. Limma: linear models for microarray data. In: Gentleman R., Carey S., Dudoit S., Irizarry R., and Huber W. (Eds). Bioinformatics and computational biology solutions using R and Bioconductor (2005), Springer, New York 397-420
82. Somasundaram T., and Bhat S.P. Developmentally dictated expression of heat shock factors: exclusive expression of HSF4 in the postnatal lens and its specific interaction with alphaB-crystallin heat shock promoter. J Biol Chem 279 (2004) 44497-44503
83. Soriano-Mas C., Redolar-Ripoll D., Aldavert-Vera L., Morgado-Bernal I., and Segura-Torres P. Post-training intracranial self-stimulation facilitates a hippocampus-dependent task. Behav Brain Res 160 (2005) 141-147
84. Takeuchi H., Kobayashi Y., Yoshihara T., Niwa J., Doyu M., Ohtsuka K., and Sobue G. Hsp70 and Hsp40 improve neurite outgrowth and suppress intracytoplasmic aggregate formation in cultured neuronal cells expressing mutant SOD1. Brain Res 949 (2002) 11-22
85. Teather L.A., Packard M.G., and Bazan N.G. Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation. Learn Mem 9 (2002) 41-47
86. Teshigawara K., Ogawa W., Mori T., Matsuki Y., Watanabe E., Hiramatsu R., Inoue H., Miyake K., Sakaue H., and Kasuga M. Role of Kruppel-like factor 15 in PEPCK gene expression in the liver. Biochem Biophys Res Commun 327 (2005) 920-926
87. von Hertzen L.S., and Giese K.P. Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25 (2005) 1935-1942
88. Wang H., Kubica N., Ellisen L.W., Jefferson L.S., and Kimball S.R. Dexamethasone represses signaling through the mammalian target of rapamycin in muscle cells by enhancing expression of REDD1. J Biol Chem 281 (2006) 39128-39134
89. Wang H., and Monteiro M.J. Ubiquilin overexpression reduces GFP-polyalanine-induced protein aggregates and toxicity. Exp Cell Res 313 (2007) 2810-2820
90. Waraczynski M.A. The central extended amygdala network as a proposed circuit underlying reward valuation. Neurosci Biobehav Rev 30 (2006) 472-496
91. Wirtshafter D. Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment. Brain Res 1051 (2005) 57-65
92. Wu B., Hu S., Yang M., Pan H., and Zhu S. CART peptide promotes the survival of hippocampal neurons by upregulating brain-derived neurotrophic factor. Biochem Biophys Res Commun 347 (2006) 656-661
93. Xu D., Patten R.D., Force T., and Kyriakis J.M. Gene 33/RALT is induced by hypoxia in cardiomyocytes, where it promotes cell death by suppressing phosphatidylinositol 3-kinase and extracellular signal-regulated kinase survival signaling. Mol Cell Biol 26 (2006) 5043-5054
94. Yachi K., Inoue K., Tanaka H., Yoshikawa H., and Tohyama M. Localization of glucocorticoid-induced leucine zipper (GILZ) expressing neurons in the central nervous system and its relationship to the stress response. Brain Res 1159 (2007) 141-147
95. Yang T.T., Tsao C.W., Li J.S., Wu H.T., Hsu C.T., and Cheng J.T. Changes of dopamine content and cell proliferation by dexamethsone via pituitary adenylate cyclase-activating polypeptide in PC12 cell. Neurosci Lett 426 (2007) 45-48
96. Yoganarasimha D., and Meti B.L. Amelioration of fornix lesion induced learning deficits by self-stimulation rewarding experience. Brain Res 845 (1999) 246-251
97. Yoganarasimha D., Shankaranarayana Rao B.S., Raju T.R., and Meti B.L. Facilitation of acquisition and performance of operant and spatial learning tasks in self-stimulation experienced rats. Behav Neurosci 112 (1998) 725-729
98. Zhang H.M., Cheung P., Yanagawa B., McManus B.M., and Yang D.C. BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 8 (2003) 229-236
99. Zhang Y., Zhu W., Wang Y.G., Liu X.J., Jiao L., Liu X., Zhang Z.H., Lu C.L., and He C. Interaction of SH2-Bbeta with RET is involved in signaling of GDNF-induced neurite outgrowth. J Cell Sci 119 (2006) 1666-1676