Opioidergic regulation of astroglial/neuronal proliferation: Where are we now?

Journal of Neurochemistry

Volumn 107, Issue 4, 2008, Pages 883-897

  Sargeant, Tim J ^a   Miller, John H ^a   Day, Darren J ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Astrocyte; Neurogenesis; Opioid; Proliferation; Radial glia

Indexed keywords

MORPHINE; NALTREXONE; OPIATE; OPIATE RECEPTOR;

ASTROCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; HIPPOCAMPUS; HUMAN; NERVOUS SYSTEM DEVELOPMENT; OLIGODENDROGLIA; ONTOGENY; OPIATE ADDICTION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ADULT STEM CELLS; ANALGESICS, OPIOID; ANIMALS; ASTROCYTES; BRAIN; CELL PROLIFERATION; HUMANS; NEURONS; OPIOID PEPTIDES; RECEPTORS, OPIOID; SIGNAL TRANSDUCTION;

ANIMALIA; MUS;

EID: 54349107513     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05671.x     Document Type: Review

References (179)

1. Altman J. (1962) Are new neurons formed in the brains of adult mammals? Science 135, 1127 1128.
2. Altman J. (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat. Rec. 145, 573 591.
3. Altman J. Das G. D. (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319 335.
4. Angelogianni P., Li H. L. Gianoulakis C. (2000) Ontogenesis of proopiomelanocortin and its processing to beta-endorphin by the fetal and neonatal rat brain. Neuroendocrinology 72, 231 241.
5. Anthony T. E., Klein C., Fishell G. Heintz N. (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881 890.
6. Barr G. A. Zadina J. E. (1999) The ontogeny of endomorphin-1- and endomorphin-2-like immunoreactivity in rat brain and spinal cord. Ann. N. Y. Acad. Sci. 897, 145 153.
7. Barry D. McDermott K. (2005) Differentiation of radial glia from radial precursor cells and transformation into astrocytes in the developing rat spinal cord. Glia 50, 187 197.
8. Bartolome J. V., Bartolome M. B., Lorber B. A., Dileo S. J. Schanberg S. M. (1991) Effects of central administration of beta-endorphin on brain and liver DNA synthesis in preweanling rats. Neuroscience 40, 289 294.
9. Bartolome J. V., Lorber B. A. Bartolome M. B. (1994) Brain cholecystokinin and beta-endorphin systems may antagonistically interact to regulate tissue DNA synthesis in rat pups. Brain Res. 661, 19 24.
10. Bayer B. M., Daussin S., Hernandez M. Irvin L. (1990) Morphine inhibition of lymphocyte activity is mediated by an opioid dependent mechanism. Neuropharmacology 29, 369 374.
11. Belcheva M. M., Szucs M., Wang D., Sadee W. Coscia C. J. (2001) μ-opioid receptor-mediated ERK activiation involves calmodulin-dependent epidermal growth factor receptor transactivation. J. Biol. Chem. 276, 33847 33853.
12. Belcheva M. M., Tan Y., Heaton V. M., Clark A. L. Coscia C. J. (2003) Mu opioid transactivation and down-regulation of the epidermal growth factor receptor in astrocytes: implications for mitogen-activated protein kinase signaling. Mol. Pharmacol. 64, 1391 1401.
13. Belcheva M. M., Clark A. L., Haas P. D., Serna J. J., Hahn J. W., Kiss A. Coscia C. J. (2005) μ and κ opioid receptors activate ERK/MAPK via different protein kinase C isoforms and secondary messengers in astrocytes. J. Biol. Chem. 30, 27662 27669.
14. Bibel M., Richter J., Schrenk K., Tucker K. L., Staiger V., Korte M., Goetz M. Barde Y. A. (2004) Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 7, 1003 1009.
15. Binder T. Vavrinková B. (2008) Prospective randomised comparative study of the effect of buprenorphine, methadone and heroin on the course of pregnancy, birthweight of newborns, early postpartum adaptation and course of the neonatal abstinence syndrome (NAS) in women followed up in the outpatient department. Neuro Endocrinol. Lett. 29, 80 86.
16. Binétruy B., Heasley L., Bost F., Caron L. Aouadi M. (2007) Concise review: regulation of embryonic stem cell lineage commitment by mitogen-activated protein kinases. Stem Cells 25, 1090 1095.
17. Bohn L. M. Raehal K. M. (2006) Opioid receptor signalling: relevance for gastrointestinal therapy. Curr. Opin. Pharmacol. 6, 559 563.
18. Bohn L. M., Belcheva M. M. Coscia C. J. (2000a) Mu-opioid agonist inhibition of kappa-opioid receptor-stimulated extracellular signal-related kinase phosphorylation is dynamin dependent in C6 glioma cells. J. Neurochem. 74, 574 581.
19. Bohn L. M., Belcheva M. M. Coscia C. J. (2000b) Mitogenic signaling via endogenous kappa-opioid receptors in C6 glioma cells: evidence for the involvement of protein kinase C and the mitogen-activated protein kinase signaling cascade. J. Neurochem. 74, 564 573.
20. Bunikowski R., Grimmer I., Heiser A., Metze B., Schafer A. Obladen M. (1998) Neurodevelopmental outcome after prenatal exposure to opiates. Eur. J. Pediatr. 157, 724 730.
21. Cameron H. A., Hazel T. G. McKay R. D. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36, 287 306.
22. Canales J. J. (2007) Adult neurogenesis and the memories of drug addiction. Eur. Arch. Psychiatry Clin. Neurosci. 257, 261 270.
23. Charron C., Messier C. Plamondon H. (2008) Neuroprotection and functional recovery conferred by administration of kappa- and delta 1-opioid agonists in a rat model of global ischemia. Physiol. Behav. 93, 502 511.
24. Chen Y., Mestek A., Liu J. Yu L. (1993a) Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem. J. 295, 625 628.
25. Chen Y., Mestek A., Liu J., Hurley J. A. Yu L. (1993b) Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol. Pharmacol. 44, 8 12.
26. Chen Y. L., Law P. Y. Loh H. H. (2008) The other side of the opioid story: modulation of cell growth and survival signaling. Curr. Med. Chem. 15, 772 778.
27. Cheng F., Zagon I. S., Verderame M. F. McLaughlin P. J. (2007) The opioid growth factor (OGF)-OGF receptor axis uses the p16 pathway to inhibit head and neck cancer. Cancer Res. 67, 10511 10518.
28. Cheng F., McLaughlin P. J., Verderame M. F. Zagon I. S. (2008) The OGF-OGFR axis utilizes the p21 pathway to restrict progression of human pancreatic cancer. Mol. Cancer 7, 5.
29. Clendeninn N. J., Petraitis M. Simon E. J. (1976) Ontological development of opiate receptors in rodent brain. Brain Res. 118, 157 160.
30. Colman A. S. Miller J. H. (2001) Modulation of breathing by mu1 and mu2 opioid receptor stimulation in neonatal and adult rats. Respir. Physiol. 127, 157 172.
31. Connor M. Christie M. J. (1999) Opioid receptor signalling mechanisms. Clin. Exp. Pharmacol. Physiol. 26, 493 499.
32. 3H]naloxone binding in rat brain. Neuropharmacology 15, 555 560.
33. Curtis M. A., Kam M., Nannmark U. et al. (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315, 1243 1249.
34. Dahl J. L., Epstein M. L., Silva B. L. Lindberg I. (1982) Multiple immunoreactive forms of met- and leu-enkephalin in fetal and neonatal rat brain and in rat gut. Life Sci. 31, 1853 1856.
35. Doetsch F., Caillé I., Lim D. A., García-Verdugo J. M. Alvarez-Buylla A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703 716.
36. Dutriez I., Sales N., Fournie-Zaluski M. C. Roques B. P. (1992) Pre- and post-natal ontogeny of neutral endopeptidase 24-11 ('enkephalinase') studied by in vitro autoradiography in the rat. Experientia 48, 290 300.
37. Edwards M. A., Yamamoto M. Caviness V. S. Jr. (1990) Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience 36, 121 144.
38. Eisch A. J., Barrot M., Schad C. A., Self D. W. Nestler E. J. (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Nat. Acad. Sci. USA 97, 7579 7584.
39. Emeterio E. P., Tramullas M. Hurlé M. A. (2006) Modulation of apoptosis in the mouse brain after morphine treatments and morphine withdrawal. J. Neurosci. Res. 83, 1352 1361.
40. Eppler C. M., Hulmes J. D., Wang J. B., Johnson B., Corbett M., Luthin D. R., Uhl G. R. Linden J. (1993) Purification and partial amino acid sequence of a mu opioid receptor from rat brain. J. Biol. Chem. 268, 26447 26451.
41. Erdos E. G. Skidgel R. A. (1989) Neutral endopeptidase 24.11 (enkephalinase) and related regulators of peptide hormones. FASEB J. 3, 145 151.
42. Evans C. J. (2004) Secrets of the opium poppy revealed. Neuropharmacology 47, 293 299.
43. Evans C. J., Keith D. E., Morrison H., Magendzo K. Edwards R. H. (1992) Cloning of a delta opioid receptor by functional expression. Science 258, 1952 1955.
44. Fields H. (2004) State-dependent opioid control of pain. Nat. Rev. Neurosci. 5, 565 575.
45. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L. P., Yamaguchi M., Kettenmann H. Kempermann G. (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23, 373 382.
46. Fukuda S., Kato F., Tozuka Y., Yamaguchi M., Miyamoto Y. Hisatsune T. (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23, 9357 9366.
47. Gadisseux J. F. Evrard P. (1985) Glial-neuronal relationship in the developing central nervous system. A histochemical-electron microscope study of radial glial cell particulate glycogen in normal and reeler mice and the human fetus. Dev. Neurosci. 7, 12 32.
48. Ganat Y. M., Silbereis J., Cave C., Ngu H., Anderson G. M., Ohkubo Y., Ment L. R. Vaccarino F. M. (2006) Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 26, 8609 8621.
49. Gaveriauv-Ruff G. Kieffer B. L. (2002) Opioid receptor genes inactivated in mice: The highlights. Neuropeptides 36, 62 71.
50. Georges F., Normand E., Bloch B. LeMoine C. (1998) Opioid receptor gene expression in the rat brain during ontogeny, with special reference to the mesostriatal system: an in situ hybridization study. Dev. Brain Res. 109, 187 199.
51. Goldstein A., Tachibana S., Lowney L. I., Hunkapiller M. Hood L. (1979) Dynorphin-(1-13), an extraordinarily potent opioid peptide. Proc. Natl Acad. Sci. USA 76, 6666 6670.
52. Gomes I., Jordan B. A., Trapaidze N., Nagy V. Devi L. A. (2000) Heterodimerization of μ and δ opioid receptors: A role in opioid synergy. J. Neurosci. 20 RC110 (1-5).
53. Götz M. Huttner W. B. (2005) The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777 788.
54. Gould E., Cameron H. A., Daniels D. C., Woolley C. S. McEwen B. S. (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 12, 3642 3650.
55. Grisel J. E., Bartels J. L., Allen S. A. Turgeon V. L. (2008) Influence of β-endorphin on anxious behaviour in mice: Interaction with EtOH. Psychopharmacology 200, 105 115.
56. Hans S. L. Jeremy R. J. (2001) Postneonatal mental and motor development of infants exposed in utero to opioid drugs. Infant Ment. Health J. 22, 300 315.
57. Hartfuss E., Galli R., Heins N. Gotz M. (2001) Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15 30.
58. Hauser K. F. Mangoura D. (1998) Diversity of the endogenous opioid system in development. Novel signal transduction translates multiple extracellular signals into neural cell growth and differentiation. Prospect. Dev. Neurobiol. 5, 437 449.
59. Hauser K. F. Stiene-Martin A. (1991) Characterization of opioid-dependent glial development in dissociated and organotypic cultures of mouse central nervous system: Critical periods and target specificity. Dev. Brain Res. 62, 245 255.
60. Hauser K. F., Osborne J. G., Stiene-Martin A. Melner M. H. (1990) Cellular localization of proenkephalin mRNA and enkephalin peptide products in cultured astrocytes. Brain Res. 522, 347 353.
61. 2+-dependent mechanism. Brain Res. 720, 191 203.
62. Hauser K. F., Khurdayan V. K., Goody R. J., Nath A., Saria A. Pauly J. R. (2003) Selective vulnerability of cerebellar granule neuroblasts and their progeny to drugs with abuse liability. Cerebellum 2, 184 195.
63. Hernandez M. C., Flores L. R. Bayer B. M. (1993) Immunosuppression by morphine is mediated by central pathways. J. Pharmacol. Exp. Ther. 267, 1336 1341.
64. Hockfield S. McKay R. D. G. (1985) Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5, 3310 3328.
65. Holmes M. M. Galea L. A. (2002) Defensive behavior and hippocampal cell proliferation: differential modulation by naltrexone during stress. Behav. Neurosci. 116, 160 168.
66. Hughes J. (1975) Isolation of an endogenous compound from the brain with pharmacological properties similar to morphine. Brain Res. 88, 295 308.
67. Hughes J., Smith T. W., Kosterlitz H. W., Fothergill L. A., Morgan B. A. Morris H. R. (1975a) Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 258, 577 579.
68. Hughes J., Smith T., Morgan B. Fothergill L. (1975b) Purification and properties of enkephalin - the possible endogenous ligand for the morphine receptor. Life Sci. 16, 1753 1758.
69. Hull E. M. Dominguez J. M. (2007) Sexual behavior in male rodents. Horm. Behav. 52, 45 55.
70. Kahila H., Saisto T., Kivitie-Kallio S., Haukkamaa M. Halmesmäki E. (2007) A prospective study on buprenorphine use during pregnancy: Effects on maternal and neonatal outcome. Acta Obstet. Gynecol. Scand. 86, 185 190.
71. Kahn L., Alonso G., Normand E. Manzoni O. J. (2005) Repeated morphine treatment alters polysialylated neural cell adhesion molecule, glutamate decarboxylase-67 expression and cell proliferation in the adult rat hippocampus. Eur. J. Neurosci. 21, 493 500.
72. Kayemba-Kay S. Laclyde J. P. (2003) Buprenorphine withdrawal syndrome in newborns: A report of 13 cases. Addiction 98, 1599 1604.
73. Kent J. L., Pert C. B. Herkenham M. (1982) Ontogeny of opiate receptors in rat forebrain: Visualization by in vitro autoradiography. Dev. Brain Res. 2, 487 504.
74. Khachaturian H., Alessi N. E., Munfakh N. Watson S. J. (1983) Ontogeny of opioid and related peptides in the rat CNS and pituitary: An immunocytochemical study. Life Sci. 33, 61 64.
75. Kieffer B. L. Gaveriaux-Ruff C. (2002) Exploring the opioid system by gene knockout. Prog. Neurobiol. 66, 285 306.
76. Kieffer B. L., Befort K., Gaveriaux-Ruff C. Hirth C. G. (1992) The delta-opioid receptor: Isolation of a cDNA by expression cloning and pharmacological characterization. Proc. Natl Acad. Sci. USA 89, 12048 12052.
77. Kim E., Clark A. L., Kiss A., Hahn J. W., Wesselschmidt R., Coscia C. J. Belcheva M. M. (2006) μ- and κ-opioids induce the differentiation of embryonic stem cells to neural progenitors. J. Biol. Chem. 281, 33749 33760.
78. Koehl M., Meerlo P., Gonzales D., Rontal A., Turek F. W. Abrous D. N. (2008) Exercise-induced promotion of hippocampal cell proliferation requires beta-endorphin. FASEB J. 22, 2253 2262.
79. Kolodziej A., Stumm R., Becker A. Hollt V. (2008) Endogenous opioids inhibit ischemia-induced generation of immature hippocampal neurons via the mu-opioid receptor. Eur. J. Neurosci. 27, 1311 1319.
80. Kornblum H. I., Loughlin S. E. Leslie F. M. (1987) Effects of morphine on DNA synthesis in neonatal rat brain. Dev. Brain Res. 31, 45 52.
81. Korzh A., Keren O., Gafni M., Bar-Josef H. Sarne Y. (2008) Modulation of extracellular signal-regulated kinase (ERK) by opioid and cannabinoid receptors that are expressed in the same cell. Brain Res. 1189, 23 32.
82. Law P. Y., Wong Y. H. Loh H. H. (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40, 389 430.
83. Lejeune C., Simmat-Durand L., Gourarier L. Aubisson S. (2006) Prospective multicenter observational study of 260 infants born to 259 opiate-dependent mothers on methadone or high-dose buprenophine substitution. Drug Alcohol Depend. 82, 250 257.
84. Leslie F. Loughlin S. (1993) Ontogeny and plasticity of opioid systems, in The Neurobiology of Opiates (Hammer R. P., ed pp. 85 123. CRC Press, Boca Raton, FL.
85. Leslie F. M., Chen Y. Winzer-Serhan U. H. (1998) Opioid receptor and peptide mRNA expression in proliferative zones of fetal rat central nervous system. Can. J. Physiol. Pharmacol. 76, 284 293.
86. Lester B. M., ElSohly M., Wright L. L. et al. (2001) The Maternal Lifestyle Study: Drug use by meconium toxicology and maternal self-report. Pediatrics 107, 309 317.
87. Lester B. M., Tronick E. Z., LaGasse L. et al. (2002) The maternal lifestyle study: Effects of substance exposure during pregnancy on neurodevelopmental outcome in 1-month-old infants. Pediatrics 110, 1182 1192.
88. Lester B. M., Tronick E. Z., LaGasse L., Seifer R., Bauer C. R., Shankaran S., Bada H. S., Wright L. L., Smeriglio V. L. Lu J. (2004) Summary statistics of neonatal intensive care unit network neurobehavioral scale scores from the maternal lifestyle study: A quasinformative sample. Pediatrics 113, 668 675.
89. Levine A. S. Billington C. J. (2004) Opioids as agents of reward-related feeding: A consideration of the evidence. Physiol. Behav. 82, 57 61.
90. Li C. H. Chung D. (1976) Isolation and structure of an untriakontapeptide with opiate activity from camel pituitary glands. Proc. Natl Acad. Sci. USA 73, 1145 1148.
91. Li S., Zhu J., Chen C., Chen Y. W., Deriel J. K., Ashby B. Liu-Chen L. Y. (1993) Molecular cloning and expression of a rat kappa opioid receptor. Biochem. J. 295, 629 633.
92. Li Y., Eitan S., Wu J., Evans C. J., Kieffer B., Sun X. Polakiewicz R. D. (2003) Morphine induces desensitization of insulin receptor signaling. Mol. Cell. Biol. 23, 6255 6266.
93. Li Z., Theus M. H. Wei L. (2006) Role of ERK 1/2 signaling in neuronal differentiation of cultured embryonic stem cells. Dev. Growth. Differ. 48, 513 523.
94. Lois C. Alvarez-Buylla A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074 2077.
95. Lorber B. A., Freitag S. K. Bartolome J. V. (1990) Effects of beta-endorphin on DNA synthesis in brain regions of preweanling rats. Brain Res. 531, 329 332.
96. Lord J. A., Waterfield A. A., Hughes J. Kosterlitz H. W. (1977) Endogenous opioid peptides: Multiple agonists and receptors. Nature 267, 495 499.
97. Lysle D. T., Hoffman K. E. Dykstra L. A. (1996) Evidence for the involvement of the caudal region of the periaqueductal gray in a subset of morphine-induced alterations of immune status. J. Pharmacol. Exp. Ther. 277, 1533 1540.
98. Malatesta P., Hartfuss E. Gotz M. (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253 5263.
99. Malatesta P., Hack M. A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F. Gotz M. (2003) Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 37, 751 764.
100. Mandyam C. D., Norris R. D. Eisch A. J. (2004) Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J. Neurosci. Res. 76, 783 794.
101. Martin W. R., Eades C. G., Thompson J. A., Huppler R. E. Gilbert P. E. (1976) The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197, 517 532.
102. Melner M. H., Low K. G., Allen R. G., Nielsen C. P., Young S. L. Saneto R. P. (1990) The regulation of proenkephalin expression in a distinct population of glial cells. EMBO J. 9, 791 796.
103. Meloche S. Pouysségur J. (2007) The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene 26, 3227 3239.
104. Meng F., Xie G. X., Thompson R. C., Mansour A., Goldstein A., Watson S. J. Akil H. (1993) Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc. Natl Acad. Sci. USA 90, 9954 9958.
105. Merkle F. T., Tramontin A. D., García-Verdugo J. M. Alvarez-Buylla A. (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl Acad. Sci. USA 101, 17528 17532.
106. 3H- thymidine into brain striatal DNA. Brain Res. Bull. 4, 615 619.
107. 3H-thymidine incorporation in the subependyma of the rat: An autoradiographic study. J. Comp. Neurol. 208, 209 214.
108. Milligan G. (2005) Opioid receptors and their interacting proteins. Neuromolecular Med. 7, 431 439.
109. Minami M., Toya T., Katao Y., Maekawa K., Nakamura S., Onogi T., Kaneko S. Satoh M. (1993) Cloning and expression of a cDNA for the rat kappa-opioid receptor. FEBS Lett. 329, 291 295.
110. Misson J. P., Edwards M. A., Yamamoto M. Caviness V. S. Jr. (1988) Identification of radial glial cells within the developing murine central nervous system: Studies based upon a new immunohistochemical marker. Dev. Brain Res. 44, 95 108.
111. Miyata T., Kawaguchi A., Okano H. Ogawa M. (2001) Asymmetric inheritance of radial glial fibres of cortical neurons. Neuron 31, 727 741.
112. Moles A., Kieffer B. L. D'Amato F. S. R. (2004) Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 304, 1983 1986.
113. Mollereau C., Parmentier M., Mailleux P., Butour J. L., Moisand C., Chalon P., Caput D., Vassart G. Meunier J. C. (1994) ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett. 341, 33 38.
114. Mrkusich E. M., Kivell B. M., Miller J. H. Day D. J. (2004) Abundant expression of mu and delta opioid receptor mRNA and protein in the cerebellum of the fetal, neonatal, and adult rat. Dev. Brain Res. 148, 213 222.
115. Nanba D. Higashiyama S. (2004) Dual intracellular signaling by proteolytic cleavage of membrane-anchored heparin-binding EGF-like growth factor. Cytokine Growth Factor Rev. 15, 13 19.
116. Narita M., Kuzumaki N., Miyatake M., Sato F., Wachi H., Seyama Y. Suzuki T. (2006) Role of δ-opioid receptor function in neurogenesis and neuroprotection. J. Neurochem. 97, 1494 1505.
117. Nestler E. J. (2004) Historical review: Molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol. Sci. 25, 210 218.
118. Noctor S. C., Flint A. C., Weissman T. A., Dammerman R. S. Kriegstein A. R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714 720.
119. Ornoy A., Michailevskaya V., Lukashov I., Bar-Hamburger R. Harel S. (1996) The developmental outcome of children born to heroin-dependent mothers, raised at home or adopted. Child Abuse Negl. 20, 385 396.
120. Papaleo F., Kieffer B. L., Tabarin A. Contarino A. (2007) Decreased motivation to eat in mu-opioid receptor-deficient mice. Eur. J. Neurosci. 25, 3398 3405.
121. Parenty G., Applbe S. Milligan G. (2008) CXCR2 chemokine receptor antagonism enhances DOP opioid receptor function via allosteric regulation of the CXCR2-DOP receptor heterodimer. Biochem. J. 412, 245 256.
122. Persson A. I., Thorlin T., Bull C. Eriksson P. S. (2003a) Opioid-induced proliferation through the MAPK pathway in cultures of adult hippocampal progenitors. Mol. Cell. Neurosci. 23, 360 372.
123. Persson A. I., Thorlin T., Bull C., Zarnegar P., Ekman R., Terenius L. Eriksson P. S. (2003b) Mu- and delta-opioid receptor antagonists decrease proliferation and increase neurogenesis in cultures of rat adult hippocampal progenitors. Eur. J. Neurosci. 17, 1159 1172.
124. Persson A. I., Naylor A. S., Jonsdottir I. H., Nyberg F., Eriksson P. S. Thorlin T. (2004) Differential regulation of hippocampal progenitor proliferation by opioid receptor antagonists in running and non-running spontaneously hypertensive rats. Eur. J. Neurosci. 19, 1847 1855.
125. Powrozek T. A., Sari Y., Singh R. P. Zhou F. C. (2004) Neurotransmitters and substances of abuse: Effects on adult neurogenesis. Curr. Neurovasc. Res. 1, 251 260.
126. Prenzel N., Zwick E., Daub H., Leserer M., Abraham R., Wallasch C. Ullrich A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884 888.
127. Ra S. M., Kim H., Jang M. H., Shin M. C., Lee T. H., Lim B. V., Kim C. J., Kim E. H., Kim K. M. Kim S. S. (2002) Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci. Lett. 333, 123 126.
128. Raman M., Chen W. Cobb M. H. (2007) Differential regulation and properties of MAPKs. Oncogene 26, 3100 3112.
129. Raynor K., Kong H., Chen Y., Yasuda K., Yu L., Bell G. I. Reisine T. (1994) Pharmacological characterization of the cloned kappa-, delta-, and mu-opioid receptors. Mol. Pharmacol. 45, 330 334.
130. Reznikov K., Hauser K. F., Nazarevskaja G., Trunova Y., Derjabin V. Bakalkin G. (1999) Opioids modulate cell division in the germinal zone of the late embryonic neocortex. Eur. J. Neurosci. 11, 2711 2719.
131. Rius R. A., Barg J., Bem W. T., Coscia C. J. Loh Y. P. (1991) The prenatal development profile of expression of opioid peptides and receptors in the mouse brain. Dev. Brain Res. 58, 237 241.
132. Roy S., Sedqi M., Ramakrishnan S., Barke R. A. Loh H. H. (1996) Differential effects of opioids on the proliferation of a macrophage cell line, Bac 1.2F5. Cell. Immunol. 169, 271 277.
133. Ruzicka B. B., Fox C. A., Thompson R. C., Meng F., Watson S. J. Akil H. (1995) Primary astroglial cultures derived from several rat brain regions differentially express mu, delta and kappa opioid receptor mRNA. Mol. Brain Res. 34, 209 220.
134. Sanchez-Simon F. M. Rodriguez R. E. (2008) Developmental expression and distribution of opioid receptors in zebrafish. Neuroscience 151, 129 137.
135. Sargeant T. J., Day D. J., Mrkusich E. M., Foo D. F. Miller J. H. (2007) Mu opioid receptors are expressed on radial glia but not migrating neuroblasts in the late embryonic mouse brain. Brain Res. 1175, 28 39.
136. 2/M phase transition in radial glial an basal progenitor cells in the dorsal telencephalon of the E15.5 embryonic mouse. Eur. J. Neurosci. 28, 1060 1067.
137. Schindler S. D., Eder H., Ortner R., Rohrmeister K., Langer M. Fischer G. (2003) Neonatal outcome following buprenorphine maintenance during conception and throughout pregnancy. Addiction 98, 103 110.
138. Schmahl W., Funk R., Miaskowski U. Plendl J. (1989) Long-lasting effects of naltrexone, an opioid receptor antagonist, on cell proliferation in developing rat forebrain. Brain Res. 486, 297 300.
139. Schwartz J. C., Malfroy B. De La Baume S. (1981) Biological inactivation of enkephalins and the role of enkephalin-dipeptidyl-carboxypeptidase ("enkephalinase") as neuropeptidase. Life Sci. 29, 1715 1740.
140. Seatriz J. V. Hammer R. P. (1993) Effects of opiates on neuronal development in the rat cerebral cortex. Brain Res. Bull. 30, 523 527.
141. Seri B., Garcia-Verdugo J. M., McEwen B. S. Alvarez-Buylla A. (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153 7160.
142. Seri B., Garcia-Verdugo J. M., Collado-Morente L., McEwen B. S. Alvarez-Buylla A. (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478, 359 378.
143. Sheng W. S., Hu S., Herr G., Ni H. T., Rock R. B., Gekker G., Lokensgard J. R. Peterson P. K. (2007) Human neural precursor cells express functional kappa opioid receptors. J. Pharmacol. Exp. Ther. 322, 957 963.
144. Shinoda H., Marini A. M., Cosi C. Schwartz J. P. (1989) Brain region and gene specificity of neuropeptide gene expression in cultured astrocytes. Science 245, 415 417.
145. Shinoda H., Marini A. M. Schwartz J. P. (1992) Developmental expression of the proenkephalin and prosomatostatin genes in cultured cortical and cerebellar astrocytes. Dev. Brain Res. 67, 205 210.
146. Spencer-Dene B., Thorogood P., Nair S., Kenny A. J., Harris M. Henderson B. (1994) Distribution of, and a putative role for, the cell-surface neutral metallo-endopeptidases during mammalian craniofacial development. Development 120, 3213 3226.
147. Spruce B. A., Curtis R., Wilkin G. P. Glover D. M. (1990) A neuropeptide precursor in cerebellum: Proenkephalin exists in subpopulations of both neurons and astrocytes. EMBO J. 9, 1787 1795.
148. Steiner B., Klempin F., Wang L., Kott M., Kettenmann H. Kempermann G. (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54, 805 814.
149. Stiene-Martin A. Hauser K. F. (1990) Opioid-dependent growth of glial cultures: Suppression of astrocyte DNA synthesis by met-enkephalin. Life Sci. 46, 91 98.
150. Stiene-Martin A. Hauser K. F. (1991) Glial growth is regulated by agonists selective for multiple opioid receptor types in vitro. J. Neurosci. Res. 29, 538 548.
151. Stiene-Martin A. Hauser K. F. (1993) Morphine suppresses DNA synthesis in cultured murine astrocytes from cortex, hippocampus and striatum. Neurosci. Lett. 157, 1 3.
152. Stiene-Martin A., Osborne J. G. Hauser K. F. (1991a) Co-localization of proenkephalin mRNA using cRNA probes and a cell-type-specific immunocytochemical marker for intact astrocytes in vitro. J. Neurosci. Methods 36, 119 126.
153. Stiene-Martin A., Gurwell J. A. Hauser K. F. (1991b) Morphine alters astrocyte growth in primary cultures of mouse glial cells: Evidence for a direct effect of opiates on neural maturation. Dev. Brain Res. 60, 1 7.
154. Stiene-Martin A., Zhou R. Hauser K. F. (1998) Regional, developmental and cell cycle-dependent differences in μ, δ, and κ-opioid receptor expression among cultured mouse astrocytes. Glia 22, 249 259.
155. Stiene-Martin A., Knapp P. E., Martin K., Gurwell J. A., Ryan S., Thornton S. R., Smith F. L. Hauser K. F. (2001) Opioid system diversity in developing neurons, astroglia and oligodendroglia in the subventricular zone and striatum: Impact on gliogenesis in vivo. Glia 36, 78 88.
156. Takahashi T., Nowakowski R. S. Caviness V. S. Jr. (1996) Interkinetic and migratory behaviour of a cohort of neocortical neurons arising in the early embryonic murine cerebral wall. J. Neurosci. 16, 5762 5776.
157. Takahashi T., Goto T., Miyama S., Nowakowski R. S. Caviness V. S. Jr. (1999) Sequence of neuron origin and neocortical laminar fate: Relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19, 10357 10371.
158. Tegeder I. Geisslinger G. (2004) Opioids as modulators of cell death and survival - Unraveling mechanisms and revealing new indications. Pharmacol. Rev. 56, 351 369.
159. Terenius L. Wahlstrom A. (1975) Search for an endogenous ligand for the opiate receptor. Acta Physiol. Scand. 94, 74 81.
160. Thompson R. C., Mansour A., Akil H. Watson S. J. (1993) Cloning and pharmacological characterization of a rat mu opioid receptor. Neuron 11, 903 913.
161. Tian M., Broxmeyer H. E., Fan Y. et al. (1997) Altered hematopoiesis, behavior, and sexual function in mu opioid receptor-deficient mice. J. Exp. Med. 185, 1517 1522.
162. Tong Y., Chabot J. G., Shen S. H., O'Dowd B. F., George S. R. Quirion R. (2000) Ontogenic profile of the expression of the mu opioid receptor gene in the rat telencephalon and diencephalon: An in situ hybridization study. J. Chem. Neuroanat. 18, 209 222.
163. Tramontin A. D., García-Verdugo J. M., Lim D. A. Alvarez-Buylla A. (2003) Postnatal development of radial glia and the ventricular zone (VZ): A continuum of the neural stem cell compartment. Cereb. Cortex 13, 580 587.
164. Tripathi A., Khurshid N., Kumar P. Iyengar S. (2008) Expression of δ- and μ-opioid receptors in the ventricular and subventricular zones of the developing human neocortex. Neurosci. Res. 61, 257 270.
165. Venkatesan A., Nath A., Ming G. L. Song H. (2007) Adult hippocampal neurogenesis: Regulation by HIV and drugs of abuse. Cell. Mol. Life Sci. 64, 2120 2132.
166. Vértes Z., Melegh G., Vértes M. Kovács S. (1982) Effect of naloxone and D-met2-pro5-enkephalinamide treatment on the DNA synthesis in the developing rat brain. Life Sci. 31, 119 126.
167. Vilijn M. H., Vaysse P. J., Zukin R. S. Kessler J. A. (1988) Expression of preproenkephalin mRNA by cultured astrocytes and neurons. Proc. Natl Acad. Sci. USA 85, 6551 6555.
168. Wang Z. J. Wang L. X. (2006) Phosphorylation: A molecular switch in opioid tolerance. Life Sci. 70, 1681 1691.
169. Wang J. B., Imai Y., Eppler C. M., Gregor P., Spivak C. E. Uhl G. R. (1993) Mu opiate receptor: cDNA cloning and expression. Proc. Natl Acad. Sci. USA 90, 10230 10234.
170. Wang D., Sadee W. Quillan J. M. (1999) Calmodulin binding to G protein-coupling domain of opioid receptors. J. Biol. Chem. 274, 22081 22088.
171. Wang D., Quillan J. M., Winans K., Lucas J. L. Sadee W. (2001) Single nucleotide polymorphisms in the human μ opioid receptor gene alter basal G protein coupling and calmodulin binding. J. Biol. Chem. 37, 34624 34630.
172. 2a and the
173. Young K. M., Fogarty M., Kessaris N. Richardson W. D. (2007) Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 27, 8286 8296.
174. Zadina J. E., Hackler L., Ge L. J. Kastin A. J. (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386, 499 502.
175. Zagon I. S., Isayama T. McLaughlin P. J. (1994) Preproenkephalin mRNA expression in the developing and adult rat brain. Mol. Brain Res. 21, 85 98.
176. Zagon I. S., Verderame M. F., Allen S. S. McLaughlin P. J. (1999a) Cloning, sequencing, expression and function of a cDNA encoding a receptor for the opioid growth factor, [Met(5)]enkephalin. Brain Res. 849, 147 154.
177. Zagon I. S., Wu Y. McLaughlin P. J. (1999b) Opioid growth factor and organ development in rat and human embryos. Brain Res. 839, 313 322.
178. Zhang Y., Wang D. Sadee W. (2005) Calmodulin interaction with peptides from G-protein coupled receptors measured with S-tag labeling. Biochem. Biophys. Res. Commun. 333, 390 395.
179. Zhu Y., Hsu M. S. Pintar J. E. (1998) Developmental expression of the mu, kappa and delta opioid receptor mRNAs in mouse. J. Neurosci. 18, 2538 2549.