Expression of δ- and μ-opioid receptors in the ventricular and subventricular zones of the developing human neocortex

Neuroscience Research

Volumn 61, Issue 3, 2008, Pages 257-270

  Tripathi, Anushree ^a   Khurshid, Nazia ^a   Kumar, Praveen ^b   Iyengar, Soumya ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

^b BASE HOSPITAL   (India)

Author keywords

OR; OR; Cerebral cortex; Human; Opioid receptor; Subventricular; Ventricular

Indexed keywords

MESSENGER RNA; MU OPIATE RECEPTOR; SIGMA OPIATE RECEPTOR;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN VENTRICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FETUS; GESTATIONAL AGE; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MULTIPOTENT STEM CELL; NEOCORTEX; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBVENTRICULAR ZONE;

AGE FACTORS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBRAL VENTRICLES; FETUS; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEOCORTEX; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; POSTMORTEM CHANGES; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU; RNA, MESSENGER; STEM CELLS;

EID: 44149126706     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2008.03.002     Document Type: Article

References (71)

1. Abbadie C., Pan Y.X., Drake C.T., and Pasternak G.W. Comparative immunohistochemical distributions of carboxy terminus epitopes from the mu-opioid receptor splice variants MOR-1D, MOR-1 and MOR-1C in the mouse and rat CNS. Neuroscience 100 (2000) 141-153
2. Akil H., Owens C., Gutstein H., Taylor L., Curran E., and Watson S. Endogenous opioids: overview and current issues. Drug Alcohol Depend. 51 1-2 (1998) 127-140
3. Alvarez-Buylla A., García-Verdugo J.M., and Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2 4 (2001) 287-293
4. Anton E.S., Cameron R.S., and Rakic P. Role of neuron-glial junctional domain proteins in the maintenance and termination of neuronal migration across the embryonic cerebral wall. J. Neurosci. 16 7 (1996) 2283-2293
5. Arvidsson U., Dado R.J., Riedl M., Lee J.H., Law P.Y., Loh H.H., Elde R., and Wessendorf M.W. Delta-opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J. Neurosci. 15 2 (1995) 1215-1235
6. 2+ mobilization in rat C6 glioma cells. J. Neurosci. 14 10 (1994) 5858-5864
7. Bayer S.A., and Altman J. The Human Brain During the Second Trimester, vol. 3 (2004), CRC Press, Florida pp. 2-4
8. Bystron I., Rakic P., Molnár Z., and Blakemore C. The first neurons of the human cerebral cortex. Nat. Neurosci. 9 7 (2006) 880-886
9. Cameron R.S., and Rakic P. Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4 2 (1991) 124-137
10. Clancy B., Darlington R.B., and Finlay B.L. Translating developmental time across mammalian species. Neuroscience 105 (2001) 7-17
11. Corbett A.D., Paterson S.J., McKnight A.T., Magnan J., and Kosterlitz H.W. Dynorphin and dynorphin are ligands for the kappa-subtype of opiate receptor. Nature 299 5878 (1982) 79-81
12. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 (1999) 703-716
13. Doyle G.A., Sheng X.R., Lin S.S., Press D.M., Grice D.E., Buono R.J., Ferraro T.N., and Berrettini W.H. Identification of five mouse mu-opioid receptor (MOR) gene (Oprm1) splice variants containing a newly identified alternatively spliced exon. Gene 395 1-2 (2007) 98-107
14. Eisch A.J., Barrot M., Schad C.A., Self D.W., and Nestler E.J. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 7579-7584
15. Evans C.J., Erdelyi E., Weber E., and Barchas J.D. Identification of pro opiomelanocortin-derived peptides in the human adrenal medulla. Science 221 4614 (1983) 957-960
16. Feng G.J., Kellett E., Scorer C.A., Wilde J., White J.H., and Milligan G. Selective interactions between helix VIII of the human mu-opioid receptors and the C terminus of periplakin disrupt G protein activation. J. Biol. Chem. 278 August 29 (35) (2003) 33400-33407
17. Gao W.Q., and Hatten M.E. Neuronal differentiation rescued by implantation of Weaver granule cell precursors into wild-type cerebellar cortex. Science 260 5106 (1993) 367-369
18. Gao W.Q., and Hatten M.E. Immortalizing oncogenes subvert the establishment of granule cell identity in developing cerebellum. Development 120 5 (1994) 1059-1070
19. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., and Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92 (1998) 63-72
20. Goldstein A., Fischli W., Lowney L.I., Hunkapiller M., and Hood L. Porcine pituitary dynorphin: complete amino acid sequence of the biologically active heptadecapeptide. Proc. Natl. Acad. Sci. U.S.A. 78 11 (1981) 7219-7223
21. Hauser K.F., McLaughlin P.J., and Zagon I.S. Endogenous opioids regulate dendritic growth and spine formation in developing rat brain. Brain Res. 416 1 (1987) 157-161
22. Hauser K.F., Stiene-Martin A., Mattson M.P., Elde R.P., Ryan S.E., and Godleske C.C. Mu-opioid receptor-induced Ca2+ mobilization and astroglial development: morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca(2+)-dependent mechanism. Brain Res. 720 1-2 (1996) 191-203
23. Hauser K.F., Houdi A.A., Turbek C.S., Elde R.P., and Maxson III W. Opioids intrinsically inhibit the genesis of mouse cerebellar granule neuron precursors in vitro: differential impact of μ and δ receptor activation on proliferation and neurite elongation. Eur. J. Neurosci. 12 (2000) 1281-1293
24. Hockfield S., and McKay R.D. Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5 12 (1985) 3310-3328
25. Howard B., Chen Y., and Zecevic N. Cortical progenitor cells in the developing human telencephalon. Glia 53 1 (2006) 57-66
26. Hu S., Sheng W.S., Lokensgard J.R., and Peterson P.K. Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 42 6 (2002) 829-836
27. Iacopetti P., Michelini M., Stuckmann I., Oback B., Aaku-Saraste E., and Huttner W.B. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 4639-4644
28. Kadhim H.J., Gadisseux J.F., and Evrard P. Topographical and cytological evolution of the glial phase during prenatal development of the human brain: histochemical and electron microscopic study. J. Neuropathol. Exp. Neurol. 47 (1988) 166-188
29. Kameyama Y. Sensitive phases for teratogen-induced developmental defects in the brain. J. Toxicol. Sci. 16 Suppl. 1 (1991) 25-35
30. Kieffer B.L., Befort K., Gaveriaux-Ruff C., and Hirth C.G. The delta-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc. Natl. Acad. Sci. U.S.A. 89 24 (1992) 12048-12052
31. Kim E., Clark A.L., Kiss A., Hahn J.W., Wesselschmidt R., Coscia C.J., and Belcheva M.M. μ- and κ-opioids induce the differentiation of embryonic stem cells to neural progenitors. J. Biol. Chem. 281 (2006) 33749-33760
32. Kopecky E.A., Simone C., Knie B., and Koren G. Transfer of morphine across the human placenta and its interaction with naloxone. Life Sci. 65 (1999) 2359-2371
33. Liao D., Lin H., Law P.Y., and Loh H.H. Mu-opioid receptors modulate the stability of dendritic spines. Proc. Natl. Acad. Sci. U.S.A. 102 February 1 (5) (2005) 1725-1730
34. Levitt P., Cooper M.L., and Rakic P. Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1 1 (1981) 27-39
35. Li C.H., and Chung D. Primary structure of human beta-lipotropin. Nature 260 (1976) 622-624
36. Magnan J., and Tiberi M. Evidence for the presence of mu- and kappa- but not of delta-opioid sites in the human fetal brain. Brain Res. Dev. Brain Res. 45 2 (1989) 275-281
37. Maharajan P., Prencipe R., Di Francesco P., Paino G., Ravagnan G., and Maharajan V. Maternal morphine alters parvalbumin immunoreactivity patterns in neonatal mouse brain. Synapse 35 4 (2000) 265-271
38. Narita M., Kuzumaki N., Miyatake M., Sato F., Wachi H., Seyama Y., and Suzuki T. Role of δ-opioid receptor function in neurogenesis and neuroprotection. J. Neurochem. 97 (2006) 1494-1505
39. Olive M.F., Anton B., Micevych P., Evans C.J., and Maidment N.T. Presynaptic versus postsynaptic localization of μ and δ opioid receptors in dorsal and ventral striatopallidal pathways. J. Neurosci. 17 19 (1997) 7471-7479
40. Pan Y.X. Identification and characterization of a novel promoter of the mouse opioid receptor gene (Oprm) that generates eight splice variants. Gene 295 (2002) 97-108
41. Pan Y.X., Xu J., Mahurter L., Xu M., Gilbert A.K., and Pasternak G.W. Identification and characterization of two new human mu opioid receptor splice variants, hMOR-1O and hMOR-1X. Biochem. Biophys. Res. Commun. 301 4 (2003) 1057-1061
42. Pan L., Xu J., Yu R., Xu M.M., Pan Y.X., and Pasternak G.W. Identification and characterization of six new alternatively spliced variants of the human mu opioid receptor gene, Oprm. Neuroscience 133 1 (2005) 209-220
43. Pert C.B., and Snyder S.H. Opiate receptor: demonstration in nervous tissue. Science 179 77 (1973) 1011-1014
44. Przewlocki R. Opioid abuse and brain gene expression. Eur. J. Pharmacol. 500 (2004) 331-349
45. Qin J., Mizuguchi M., Itoh M., and Takashima S. Immunohistochemical expression of doublecortin in the human cerebrum: comparison of normal development and neuronal migration disorders. Brain Res. 863 1-2 (2000) 225-232
46. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A golgi and electronmicroscopic study in Macacus rhesus. J. Comp. Neurol. 141 3 (1971) 283-312
47. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145 May (1) (1972) 61-83
48. Rakic P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18 (1995) 383-388
49. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 (1992) 1707-1710
50. Reznikov K., Hauser K.F., Nazarevskaja G., Trunova Y., Derjabin V., and Bakalkin G. Opioids modulate cell division in the germinal zone of the late embryonic neocortex. Eur. J. Neurosci. 11 8 (1999) 2711-2719
51. Ricalde A.A., and Hammer Jr. R.P. Perinatal opiate treatment delays growth of cortical dendrites. Neurosci. Lett. 115 2-3 (1990) 137-143
52. Robinson T.E., Gorny G., Savage V.R., and Kolb B. Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46 4 (2002) 271-279
53. Sailaja K., Ahuja R.K., and Gopinath G. Biparietal diameter: a useful measure for determining gestational age of human abortuses. Natl. Med. J. India 9 (1996) 165-167
54. Sargeant T.J., Day D.J., Mrkusich E.M., Foo D.F., and Miller J.H. Mu opioid receptors are expressed on radial glia but not migrating neuroblasts in the late embryonic mouse brain. Brain Res. 1175 (2007) 28-38
55. Sauvageot C.M., and Stiles C.D. Molecular mechanisms controlling cortical gliogenesis. Curr. Opin. Neurobiol. 12 (2002) 244-249
56. Seatriz J.V., and Hammer Jr. R.P. Effects of opiates on neuronal development in the rat cerebral cortex. Brain Res. Bull. 30 5-6 (1993) 523-527
57. Shmechel D.E., and Rakic P. Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 227 (1979) 303-305
58. Sheng W.S., Hu S., Herr G., Ni H.T., Rock R.B., Gekker G., Lokensgard J.R., and Peterson P.K. Human neural precursor cells express functional κ-opioid receptors. J. Pharmacol. Exp. Ther. 322 3 (2007) 957-963
59. Sidman R.L., and Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62 1 (1973) 1-35
60. Slotkin T.A., Seidler F.J., and Yanai J. Heroin neuroteratogenicity: targeting adenylyl cyclase as an underlying biochemical mechanism. Dev. Brain Res. 132 (2001) 69-79
61. Stiene-Martin A., Gurwell J.A., and Hauser K.F. Morphine alters astrocyte growth in primary cultures of mouse glial cells: evidence for a direct effect of opiates on neural maturation. Brain Res. Dev. Brain Res. 60 1 (1991) 1-7
62. Stiene-Martin A., Knapp P.E., Martin K., Gurwell J.A., Ryan S., Thornton S.R., Smith F.L., and Hauser K.F. Opioid system diversity in developing neurons, astroglia, and oligodendroglia in the subventricular zone and striatum: impact on gliogenesis in vivo. Glia 36 1 (2001) 78-88
63. Steingart R.A., Abu-Roumi M., Newman M.E., Silverman W.F., Slotkin T.A., and Yanai J. Neurobehavioral damage to cholinergic systems caused by prenatal exposure to heroin or phenobarbital: cellular mechanisms and the reversal of deficits by neural grafts. Dev. Brain Res. 122 (2000) 125-133
64. Temple S. The development of neural stem cells. Nature 414 (2001) 112-117
65. Wang X., Dow-Edwards D., Anderson V., Minkoff H., and Hurd Y.L. Discrete opioid gene expression impairment in the human fetal brain associated with maternal marijuana use. Pharmacogenom. J. 6 (2006) 255-264
66. Yanai J., Avraham Y., Levy S., Maslaton J., Pick C.G., Rogel-Fuchs Y., and Zahalka E.A. Alterations in septohippocampal cholinergic innervations and related behaviors after early exposure to heroin and phencyclidine. Brain Res. Dev. Brain Res. 69 2 (1992) 207-214
67. Zagon I.S., McLaughlin P.J., Weaver D.J., and Zagon E. Opiates, endorphins and the developing organism: a comprehensive bibliography. Neurosci. Biobehav. Rev. 6 4 (Winter) (1982) 439-479
68. Zagon I.S., McLaughlin P.J., and Zagon E. Opiates, endorphins and the developing organism: a comprehensive bibliography. Neurosci. Biobehav. Rev. 8 (1984) 387-403
69. Zecevic N., and Rakic P. Development of layer I neurons in the primate cerebral cortex. J. Neurosci. 21 (2001) 5607-5619
70. Zhang Y., Pana Y.X., Kolesnikovb Y., and Pasternak G.W. Immunohistochemical labelling of the mu opioid receptor carboxy terminal splice variant mMOR-1B4 in the mouse central nervous system. Brain Res. 1099 (2006) 33-43
71. Zhu Y., Hsu M.S., and Pintar J.E. Developmental expression of the μ, κ, and δ opioid receptor mRNAs in mouse. J. Neurosci. 18 (1998) 2538-2549