Skip to main content

Advertisement

Log in

Preliminary array analysis reveals novel genes regulated by ovarian steroids in the monkey raphe region

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

We hypothesize that ovarian hormones may improve serotonin neuron survival. We sought the effect of estradiol (E) and progesterone (P) on novel gene expression in the macaque dorsal raphe region with Affymetrix array analysis. Nine spayed rhesus macaques were treated with either placebo, E or E+P via Silastic implant for 1 month prior to euthanasia (n=3 per treatment). RNA was extracted from a small block of midbrain containing the dorsal raphe and examined on an Agilent Bioanalyzer. The RNA from each monkey was labeled and hybridized to an Affymetrix HG_U95AV Human GeneChip Array. After filtering and sorting, 25 named genes remained that were regulated by E, and 24 named genes remained that were regulated by supplemental P. These genes further sorted into functional categories that would promote neuronal plasticity, transmitter synthesis, and trafficking, as well as reduce apoptosis. The relative abundance of four pivotal genes was examined in all nine animals with quantitative RT-PCR and normalized by glyceraldehyde 3-phosphate dehydrogenase (GAPDH). E±P caused a significant threefold reduction in JNK-1 (a pro-apoptosis gene, p<0.007); and a significant sixfold decrease in kynurenine mono-oxygenase (produces neurotoxic quinolones, p<0.05). GABA-A receptor (α3 subunit; benzodiazepine site) and E2F1 (interferes with cytokine signaling) were unaffected by E, but increased sevenfold (p<0.02) and fourfold (p<0.009), respectively, upon treatment with P. In summary, subsets of genes related to tissue remodeling or apoptosis were up- or down-regulated by E and P in a tissue block containing the dorsal raphe. These changes could promote cellular resilience in the region where serotonin neurons originate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Armano S, Coco S, Bacci A, Pravettoni E, Schenk U, Verderio C, Varoqui H, Erickson JD, Matteoli M (2002) Localization and functional relevance of system a neutral amino acid transporters in cultured hippocampal neurons. J Biol Chem 277:10467–10473

    Article  Google Scholar 

  • Aruga J, Yokota N, Hashimoto M, Furuichi T, Fukuda M, Mikoshiba K (1994) A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J Neurochem 63:1880–1890

    Google Scholar 

  • Avital A, Goshen I, Kamsler A, Segal M, Iverfeldt K, Richter-Levin G, Yirmiya R (2003) Impaired interleukin-1 signaling is associated with deficits in hippocampal memory processes and neural plasticity. Hippocampus 13:826–834

    Article  Google Scholar 

  • Azmitia EC (1978) The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei. In: Iverson LL, Iverson SD, Synder SH (eds) Handbook of Psychopharmacology, vol. 9. Plenum Publishing Corp., Baltimore, pp 233–313

    Google Scholar 

  • Barton HA, Marletta MA (1988) Kinetic and immunochemical studies of a receptor-like protein that binds aromatic hydrocarbons. J Biol Chem 263:5825–5832

    Google Scholar 

  • Bethea CL (1993) Colocalization of progestin receptors with serotonin in raphe neurons of macaque. Neuroendocrinology 57:1–6

    Google Scholar 

  • Bethea CL (1994) Regulation of progestin receptors in raphe neurons of steroid-treated monkeys. Neuroendocrinology 60:50–61

    Google Scholar 

  • Bethea CL, Mirkes SJ, Shively CA, Adams MR (2000) Steroid regulation of tryptophan hydroxylase protein in the dorsal raphe of macaques. Biol Psychiatry 47:562–576

    CAS  PubMed  Google Scholar 

  • Bethea CL, Lu NZ, Gundlah C, Streicher JM (2002) Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 23:41–100

    Article  Google Scholar 

  • Bethea CL, Pau FK-Y, Fox S, Hess DL, Berga SL, Cameron JL (2004a) Sensitivity to stress-induced reproductive dysfunction linked to activity of the serotonergic system. Fertil Steril 83:148–155

    Google Scholar 

  • Bethea CL, Streicher JM, Mirkes SJ, Sanchez RL, Cameron JL (2004b) Serotonin-related gene expression in female monkeys with differential sensitivity to stress. Neuroscience (in press)

  • Biggio G, Follesa P, Sanna E, Purdy RH, Concas A (2001) GABAA-receptor plasticity during long-term exposure to and withdrawal from progesterone. Int Rev Neurobiol 46:207–241

    Google Scholar 

  • Blits-Huizinga CT, Nelersa CM, Malhotra A, Liebl DJ (2004) Ephrins and their receptors: binding versus biology. IUBMB Life 56:257–265

    Google Scholar 

  • Brenner RM, Slayden OD (1994) Cyclic changes in the primate oviduct and endometrium. In: Knobil E, Neill JD (eds) The Physiology of Reproduction, 2nd edn. Raven Press, Ltd., New York, pp 541–569

    Google Scholar 

  • Briggs RC, Kao WY, Dworkin LL, Briggs JA, Dessypris EN, Clark J (1994) Regulation and specificity of MNDA expression in monocytes, macrophages, and leukemia/B lymphoma cell lines. J Cell Biochem 56:559–567

    Google Scholar 

  • Carpenedo R, Meli E, Peruginelli F, Pellegrini-Giampietro DE, Moroni F (2002) Kynurenine 3-mono-oxygenase inhibitors attenuate post-ischemic neuronal death in organotypic hippocampal slice cultures. J Neurochem 82:1465–1471

    Article  Google Scholar 

  • Chan SW, Hong W (2001) Retinoblastoma-binding protein 2 (Rbp2) potentiates nuclear hormone receptor-mediated transcription. J Biol Chem 276:28402–28412

    Article  Google Scholar 

  • Chiarugi A, Cozzi A, Ballerini C, Massacesi L, Moroni F (2001a) Kynurenine 3-mono-oxygenase activity and neurotoxic kynurenine metabolites increase in the spinal cord of rats with experimental allergic encephalomyelitis. Neuroscience 102:687–695

    Article  Google Scholar 

  • Chiarugi A, Meli E, Moroni F (2001b) Similarities and differences in the neuronal death processes activated by 3OH-kynurenine and quinolinic acid. J Neurochem 77:1310–1318

    Article  Google Scholar 

  • Christen S, Peterhans E, Stocker R (1990) Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc Natl Acad Sci U S A 87:2506–2510

    Google Scholar 

  • Clement Y, Chapouthier G (1998) Biological bases of anxiety. Neurosci Biobehav Rev 22:623–633

    Article  CAS  PubMed  Google Scholar 

  • Dedeoglu A, Fisher A (1994) Cardiovascular activation by serotonergic stimulation: role of corticotropin-releasing factor. Am J Physiol 267:R859–R864

    Google Scholar 

  • de Sauvage FJ, Camerato TR, Goeddel DV (1991) Primary structure and functional expression of the human receptor for Escherichia coli heat-stable enterotoxin. J Biol Chem 266:17912–17918

    Google Scholar 

  • Doering CB, Coursey C, Spangler W, Danner DJ (1998) Murine branched chain alpha-ketoacid dehydrogenase kinase; cDNA cloning, tissue distribution, and temporal expression during embryonic development. Gene 212:213–219

    Article  Google Scholar 

  • Earl CJ, Streicher JM, Bethea CL (2001) Ovarian hormone replacement decreases NFκB immunodetection in serotonin neurons of rhesus macaques. 83rd Annual Meeting of the Endocrine Society, pg 128, Abstract #P3-302, Denver, CO

  • Eastman CL, Guilarte TR (1989) Cytotoxicity of 3-hydroxykynurenine in a neuronal hybrid cell line. Brain Res 495:225–231

    Article  Google Scholar 

  • Erickson JB, Flanagan EM, Russo S, Reinhard JF Jr (1992) A radiometric assay for kynurenine 3-hydroxylase based on the release of 3H2O during hydroxylation of l-[3,5-3H]kynurenine. Anal Biochem 205: 257–262

    Article  Google Scholar 

  • Finch RA, Donoviel DB, Potter D, Shi M, Fan A, Freed DD, Wang CY, Zambrowicz BP, Ramirez-Solis R, Sands AT, Zhang N (2002) MDMX is a negative regulator of p53 activity in vivo. Cancer Res 62:3221–3225

    Google Scholar 

  • Ganapathy V, Daniels T, Casiano CA (2003) LEDGF/p75: a novel nuclear autoantigen at the crossroads of cell survival and apoptosis. Autoimmun Rev 2:290–297

    Article  Google Scholar 

  • Goold RG, Gordon-Weeks PR (2004) Glycogen synthase kinase 3beta and the regulation of axon growth. Biochem Soc Trans 32:809–811

    Article  Google Scholar 

  • Gray NW, Fourgeaud L, Huang B, Chen J, Cao H, Oswald BJ, Hemar A, McNiven MA (2003) Dynamin 3 is a component of the postsynapse, where it interacts with mGluR5 and Homer. Curr Biol 13:510–515

    Article  Google Scholar 

  • Guidetti P, Eastman CL, Schwarcz R (1995) Metabolism of [5-3H]kynurenine in the rat brain in vivo: evidence for the existence of a functional kynurenine pathway. J Neurochem 65:2621–2632

    Google Scholar 

  • Gundlah C, Kohama SG, Mirkes SJ, Garyfallou VT, Urbanski HF, Bethea CL (2000) Distribution of estrogen receptor beta (ERβ) mRNA in hypothalamus, midbrain and temporal lobe of spayed macaque: continued expression with hormone replacement. Mol Brain Res 76:191–204

    CAS  PubMed  Google Scholar 

  • Gundlah C, Lu NZ, Bethea CL (2001a) Ovarian steroid regulation of monoamine oxidase-A and -B mRNAs in the macaque dorsal raphe and hypothalamic nuclei. Psychopharmacology 160: 271–282

    Article  Google Scholar 

  • Gundlah C, Lu NZ, Mirkes SJ, Bethea CL (2001b) Estrogen receptor beta (ERβ) mRNA and protein in serotonin neurons of macaques. Mol Brain Res 91:14–22

    Article  Google Scholar 

  • Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, Derijard B, Davis RJ (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15:2760–2770

    Google Scholar 

  • Haft CR, de la Luz Sierra M, Barr VA, Haft DH, Taylor SI (1998) Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol Cell Biol 18:7278–7287

    Google Scholar 

  • Hall KT, Boumsell L, Schultze JL, Boussiotis VA, Dorfman DM, Cardoso AA, Bensussan A, Nadler LM, Freeman GJ (1996) Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. Proc Natl Acad Sci U S A 93:11780–11785

    Article  Google Scholar 

  • Hartmann H, Busciglio J, Baumann KH, Staufenbiel M, Yankner BA (1997) Developmental regulation of presenilin-1 processing in the brain suggests a role in neuronal differentiation. J Biol Chem 272:14505–14508

    Article  Google Scholar 

  • Henkel V, Baghai TC, Eser D, Zill P, Mergl R, Zwanzger P, Schule C, Bottlender R, Jager M, Rupprecht R, Hegerl U, Moller HJ, Bondy B (2004) The gamma amino butyric acid (GABA) receptor alpha-3 subunit gene polymorphism in unipolar depressive disorder: a genetic association study. Am J Med Genet 126B:82–87

    Article  Google Scholar 

  • Hofmann I, Mertens C, Brettel M, Nimmrich V, Schnolzer M, Herrmann H (2000) Interaction of plakophilins with desmoplakin and intermediate filament proteins: an in vitro analysis. J Cell Sci 113(Pt 13):2471–2483

    Google Scholar 

  • Hornung JP (2003) The human raphe nuclei and the serotonergic system. J Chem Neuroanat 26:331–343

    Article  Google Scholar 

  • Hou ST, Callaghan D, Fournier MC, Hill I, Kang L, Massie B, Morley P, Murray C, Rasquinha I, Slack R, MacManus JP (2000) The transcription factor E2F1 modulates apoptosis of neurons. J Neurochem 75:91–100

    Article  Google Scholar 

  • Hou ST, Cowan E, Walker T, Ohan N, Dove M, Rasqinha I, MacManus JP (2001) The transcription factor E2F1 promotes dopamine-evoked neuronal apoptosis by a mechanism independent of transcriptional activation. J Neurochem 78:287–297

    Article  Google Scholar 

  • Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ, Saxena PR, Humphrey PA (1994) International union of pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol Rev 46:157–203

    CAS  PubMed  Google Scholar 

  • Irvin DK, Zurcher SD, Nguyen T, Weinmaster G, Kornblum HI (2001) Expression patterns of Notch1, Notch2, and Notch3 suggest multiple functional roles for the Notch-DSL signaling system during brain development. J Comp Neurol 436:167–181

    Google Scholar 

  • Ito Y, Saito K, Maruta K, Nakagami Y, Koike T, Oguri Y, Nagamura Y (1999) Kynurenine concentration of serum was increased by exercise. Adv Exp Med Biol 467:717–722

    Google Scholar 

  • Ito D, Tanahashi N, Murata M, Sato H, Saito I, Watanabe K, Fukuuchi Y (2002) Notch3 gene polymorphism and ischaemic cerebrovascular disease. J Neurol Neurosurg Psychiatry 72:382–384

    Article  Google Scholar 

  • Itoh A, Miyabayashi T, Ohno M, Sakano S (1998) Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for slit in the formation and maintenance of the nervous system. Brain Res Mol Brain Res 62:175–186

    Article  Google Scholar 

  • Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165–231

    Google Scholar 

  • Julius D (1991) Molecular biology of serotonin receptors. Annu Rev Neurosci 14:335–360

    Article  Google Scholar 

  • Kolodkin AL (1998) Semaphorin-mediated neuronal growth cone guidance. Prog Brain Res 117:115–132

    Google Scholar 

  • Konishi Y, Bonni A (2003) The E2F-Cdc2 cell-cycle pathway specifically mediates activity deprivation-induced apoptosis of postmitotic neurons. J Neurosci 23:1649–1658

    Google Scholar 

  • Kristensen P, Judge ME, Thim L, Ribel U, Christjansen KN, Wulff BS, Clausen JT, Jensen PB, Madsen OD, Vrang N, Larsen PJ, Hastrup S (1998) Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 393:72–76

    Google Scholar 

  • Kumagae Y, Zhang Y, Kim OJ, Miller CA (1999) Human c-Jun N-terminal kinase expression and activation in the nervous system. Brain Res Mol Brain Res 67:10–17

    Article  Google Scholar 

  • Lambert JJ, Belelli D, Peden DR, Vardy AW, Peters JA (2003) Neurosteroid modulation of GABAA receptors. Prog Neurobiol 71:67–80

    Article  Google Scholar 

  • Lazarow PB (2003) Peroxisome biogenesis: advances and conundrums. Curr Opin Cell Biol 15:489–497

    Article  Google Scholar 

  • Lesch K-P, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer DH, Murphy DL (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531

    Article  CAS  PubMed  Google Scholar 

  • Lu NZ, Bethea CL (2002) Ovarian steroid regulation of 5HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology 27:12–24

    Google Scholar 

  • Lu NZ, Eshleman AJ, Janowsky A, Bethea CL (2003) Ovarian steroid regulation of serotonin reuptake transporter (SERT) binding, distribution and function in female macaques. Mol Psychiatry 8:353–360

    Article  Google Scholar 

  • Luo Y, Long JM, Spangler EL, Longo DL, Ingram DK, Weng NP (2001) Identification of maze learning-associated genes in rat hippocampus by cDNA microarray. J Mol Neurosci 17:397–404

    Article  Google Scholar 

  • Mages HW, Rilke O, Bravo R, Senger G, Kroczek RA (1994) NOT, a human immediate–early response gene closely related to the steroid/thyroid hormone receptor NAK1/TR3. Mol Endocrinol 8:1583–1591

    Article  Google Scholar 

  • Malina HZ, Martin XD (1995) Deamination of 3-hydroxykynurenine in bovine lenses: a possible mechanism of cataract formation in general. Graefes Arch Clin Exp Ophthalmol 233:38–44

    Article  Google Scholar 

  • Malina HZ, Richter C, Mehl M, Hess OM (2001) Pathological apoptosis by xanthurenic acid, a tryptophan metabolite: activation of cell caspases but not cytoskeleton breakdown. BMC Physiol 1:7

    Article  Google Scholar 

  • McDonald D (2004) A SNAP decision in neural cell fate. Nat Cell Biol 6:187

    Article  Google Scholar 

  • Meneses A (1999) 5-HT system and cognition. Neurosci Biobehav Rev 23:1111–1125

    Article  CAS  PubMed  Google Scholar 

  • Morita T, Saito K, Takemura M, Maekawa N, Fujigaki S, Fujii H, Wada H, Takeuchi S, Noma A, Seishima M (1999) l-tryptophan–kynurenine pathway metabolite 3-hydroxyanthranilic acid induces apoptosis in macrophage-derived cells under pathophysiological conditions. Adv Exp Med Biol 467:559–563

    Google Scholar 

  • Motoi Y, Aizawa T, Haga S, Nakamura S, Namba Y, Ikeda K (1999) Neuronal localization of a novel mosaic apolipoprotein E receptor, LR11, in rat and human brain. Brain Res 833:209–215

    Article  Google Scholar 

  • Mueller RF, Hornung S, Furlong CE, Anderson J, Giblett ER, Motulsky AG (1983) Plasma paraoxonase polymorphism: a new enzyme assay, population, family, biochemical, and linkage studies. Am J Hum Genet 35:393–408

    Google Scholar 

  • Muldoon MF, Mackey RH, Williams KV, Korytkowski MT, Flory JD, Manuck SB (2004) Low central nervous system serotonergic responsivity is associated with the metabolic syndrome and physical inactivity. J Clin Endocrinol Metab 89:266–271

    Google Scholar 

  • Okuda S, Nishiyama N, Saito H, Katsuki H (1998) 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem 70:299–307

    Google Scholar 

  • Park DS, Stefanis L, Yan CY, Farinelli SE, Greene LA (1996) Ordering the cell death pathway. Differential effects of BCL2, an interleukin-1-converting enzyme family protease inhibitor, and other survival agents on JNK activation in serum/nerve growth factor-deprived PC12 cells. J Biol Chem 271:21898–21905

    Article  Google Scholar 

  • Patki V, Virbasius J, Lane WS, Toh BH, Shpetner HS, Corvera S (1997) Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 94:7326–7330

    Article  Google Scholar 

  • Pecins-Thompson M, Bethea CL (1998) Ovarian steroid regulation of 5HT1A autoreceptor messenger ribonucleic acid expression in the dorsal raphe of rhesus macaques. Neuroscience 89:267–277

    Article  Google Scholar 

  • Pecins-Thompson M, Brown NA, Bethea CL (1998) Regulation of serotonin re-uptake transporter mRNA expression by ovarian steroids in rhesus macaques. Mol Brain Res 53:120–129

    Article  Google Scholar 

  • Peluso JJ (2003) Basic fibroblast growth factor (bFGF) regulation of the plasma membrane calcium ATPase (PMCA) as part of an anti-apoptotic mechanism of action. Biochem Pharmacol 66:1363–1369

    Article  Google Scholar 

  • Perez-Torres S, Cortes R, Tolnay M, Probst A, Palacios JM, Mengod G (2003) Alterations on phosphodiesterase type 7 and 8 isozyme mRNA expression in Alzheimer’s disease brains examined by in situ hybridization. Exp Neurol 182:322–334

    Article  Google Scholar 

  • Plowman GD, Green JM, McDonald VL, Neubauer MG, Disteche CM, Todaro GJ, Shoyab M (1990) The amphiregulin gene encodes a novel epidermal growth factor-related protein with tumor-inhibitory activity. Mol Cell Biol 10:1969–1981

    Google Scholar 

  • Poelzl G, Kasai Y, Mochizuki N, Shaul PW, Brown M, Mendelsohn ME (2000) Specific association of estrogen receptor beta with the cell cycle spindle assembly checkpoint protein, MAD2. Proc Natl Acad Sci U S A 97:2836–2839

    Article  Google Scholar 

  • Ravichandran V, Roche PA (1997) Cloning and identification of human syntaxin 5 as a synaptobrevin/VAMP binding protein. J Mol Neurosci 8:159–161

    Google Scholar 

  • Rupprecht R (2003) Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 28:139–168

    Article  Google Scholar 

  • Saito K, Heyes MP (1996) Kynurenine pathway enzymes in brain. Properties of enzymes and regulation of quinolinic acid synthesis. Adv Exp Med Biol 398:485–492

    Google Scholar 

  • Sanchez RL, Reddy AP, Cameron JL, Bethea CL (2004) Ovarian steroid regulation of tryptophan hydroxylase-2 (TPH-2) gene expression in the dorsal raphe of macaques. Annual meeting of the Society for Neuroscience, San Diego, CA, pp 887.10

  • Satokata I, Iwai K, Matsuda T, Okada Y, Tanaka K (1993) Genomic characterization of the human DNA excision repair-controlling gene XPAC. Gene 136:345–348

    Article  Google Scholar 

  • Schauwecker PE (2000) Seizure-induced neuronal death is associated with induction of c-Jun N-terminal kinase and is dependent on genetic background. Brain Res 884:116–128

    Article  Google Scholar 

  • Schjott JM, Hsu SC, Plummer MR (2003) The neuronal beta 4 subunit increases the unitary conductance of L-type voltage-gated calcium channels in PC12 cells. J Biol Chem 278:33936–33942

    Article  Google Scholar 

  • Shively CA, Laber-Laird K, Anton RF (1997) The behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41:871–882

    Article  Google Scholar 

  • Simonsen A, Bremnes B, Ronning E, Aasland R, Stenmark H (1998) Syntaxin-16, a putative Golgi t-SNARE. Eur J Cell Biol 75:223–231

    Google Scholar 

  • Smith S, Giriat I, Schmitt A, de Lange T (1998) Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484–1487

    Article  CAS  PubMed  Google Scholar 

  • Smith LJ, Henderson JA, Abell CW, Bethea CL (2004) Effects of ovarian steroids and raloxifene on proteins that synthesize, transport and degrade serotonin in the raphe region of macaques. Neuropsychopharmacology 29:2035–2045

    Article  Google Scholar 

  • Stone TW (2001) Endogenous neurotoxins from tryptophan. Toxicon 39:61–73

    Article  Google Scholar 

  • Stone TW, Mackay GM, Forrest CM, Clark CJ, Darlington LG (2003) Tryptophan metabolites and brain disorders. Clin Chem Lab Med 41:852–859

    Article  Google Scholar 

  • Sturm RA, Das G, Herr W (1988) The ubiquitous octamer-binding protein Oct-1 contains a POU domain with a homeo box subdomain. Genes Dev 2:1582–1599

    Google Scholar 

  • Suda K, Holmberg EG, Nornes HO, Neuman T (1994) DNA synthesis is induced in adult neurons after expression of E2F1 and E1A. NeuroReport 5:1749–1751

    Google Scholar 

  • Thakur S, Lin HC, Tseng WT, Kumar S, Bravo R, Foss F, Gelinas C, Rabson AB (1994) Rearrangement and altered expression of the NFKB-2 gene in human cutaneous T-lymphoma cells. Oncogene 9:2335–2344

    Google Scholar 

  • Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG et al (2001) The sequence of the human genome. Science 291:1304–1351

    Article  CAS  PubMed  Google Scholar 

  • Wafford KA, Macaulay AJ, Fradley R, O’Meara GF, Reynolds DS, Rosahl TW (2004) Differentiating the role of gamma-aminobutyric acid type A (GABAA) receptor subtypes. Biochem Soc Trans 32:553–556

    Article  Google Scholar 

  • Wang X, Kilimann MW (1997) Identification of two new mu-adaptin-related proteins, mu-ARP1 and mu-ARP2. FEBS Lett 402:57–61

    Article  Google Scholar 

  • Wei H, Leeds P, Chen RW, Wei W, Leng Y, Bredesen DE, Chuang DM (2000) Neuronal apoptosis induced by pharmacological concentrations of 3-hydroxykynurenine: characterization and protection by dantrolene and Bcl-2 overexpression. J Neurochem 75:81–90

    Article  Google Scholar 

  • Williams T, Tjian R (1991) Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev 5:670–682

    Google Scholar 

  • Wurst W, Auerbach AB, Joyner AL (1994) Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120:2065–2075

    CAS  PubMed  Google Scholar 

  • Yokoyama M, Nishi Y, Miyamoto Y, Nakamura M, Akiyama K, Matsubara K, Okubo K (1996) Molecular cloning of a human neuroD from a neuroblastoma cell line specifically expressed in the fetal brain and adult cerebellum. Brain Res Mol Brain Res 42:135–139

    Article  Google Scholar 

  • Yu YH, Sabatini DD, Kreibich G (1990) Antiribophorin antibodies inhibit the targeting to the ER membrane of ribosomes containing nascent secretory polypeptides. J Cell Biol 111:1335–1342

    Article  Google Scholar 

  • Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC (2002) Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res 30:48

    Article  Google Scholar 

Download references

Acknowledgements

We are deeply grateful to the dedicated staff of the Division of Animal Resources including the staff of the Departments of Surgery and Pathology for their expertise and helpfulness in all aspects of monkey management. We are indebted to the staff of the OHSU Gene Microarray Shared Resource, particularly Dr. Chris Harrington, Kristina Vartanian, and Brian Tompkins. We thank Dr. Eliot Spindel, supervisor of the Molecular and Cellular Biology Core, for his patience and advice as we performed the qRT-PCR assay.

This work is supported by NIH grants MH62677 (to C.L.B.), U54 contraceptive Center Grant HD 18185, and RR000163 for the operation of ONPRC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cynthia L. Bethea.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reddy, A.P., Bethea, C.L. Preliminary array analysis reveals novel genes regulated by ovarian steroids in the monkey raphe region. Psychopharmacology 180, 125–140 (2005). https://doi.org/10.1007/s00213-005-2154-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-005-2154-1

Keywords

Navigation