Kappa opioids promote the proliferation of astrocytes via Gβγ and β-arrestin 2-dependent MAPK-mediated pathways

Journal of Neurochemistry

Volumn 107, Issue 6, 2008, Pages 1753-1765

  McLennan, Gregory P ^a   Kiss, Alexi ^a   Miyatake, Mayumi ^a   Belcheva, Mariana M ^a   Chambers, Kari T ^a   Pozek, John J ^a   Mohabbat, Yasmin ^a   Moyer, Robert A ^b   Bohn, Laura M ^b   Coscia, Carmine J ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

arrestins; Astrocytes; Extracellular signal regulated kinase mitogen activated protein kinase; GTP binding regulatory proteins; Opioid receptors; Opioids

Indexed keywords

BETA ARRESTIN 2; C(2) METHOXYMETHYL SALVINORIN B; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; SALVINORIN A; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL CULTURE; CELL DIVISION; CELL GROWTH; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE SILENCING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANALGESICS; ANIMALS; ANIMALS, NEWBORN; ARRESTINS; ASTROCYTES; BENZENEACETAMIDES; BROMODEOXYURIDINE; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; ENZYME INHIBITORS; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEINS; HUMANS; MAP KINASE SIGNALING SYSTEM; PERTUSSIS TOXIN; PYRROLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, KAPPA; RNA, SMALL INTERFERING; TIME FACTORS; TRANSFECTION;

EID: 56749092253     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05745.x     Document Type: Article

References (65)

1. Ahn S. K., Shenoy S. K., Wei H. J. Lefkowitz R. J. (2004) Differential kinetic and spatial patterns of β-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J. Biol. Chem. 279, 35518 35525.
2. Barak L. S., Ferguson S. S. G., Zhang J. Caron M. G. (1997) A β-arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J. Biol. Chem. 272, 27497 27500.
3. Barg J., Belcheva M. M., Rowinski J. Coscia C. J. (1993) κ-Opioid agonist modulation of [3H]thymidine incorporation into DNA: evidence for the involvement of pertussis toxin-sensitive G protein-coupled phosphoinositide turnover. J. Neurochem. 60, 1505 1511.
4. 2+ mobilization in rat C6 glioma cells. J. Neurosci. 14, 5858 5864.
5. Bar-Joseph Z., Siegfried Z., Brandeis M., Brors B., Lu Y., Eils R., Dynlacht B. D. Simon I. (2008) Genome-wide transcriptional analysis of the human cell cycle identifies genes differentially regulated in normal and cancer cells. Proc. Natl Acad. Sci. USA 105, 955 960.
6. Barnes W. G., Reiter E., Violin J. D., Ren X.-R., Milligan G. Lefkowitz R. J. (2005) β-Arrestin 1 and Gαq/11 coordinately activate RhoA and stress fiber formation following receptor stimulation. J. Biol. Chem. 280, 8041 8050.
7. Belcheva M. M., Vogel Z., Ignatova E., Avidor-Reiss T., Zippel R., Levy R., Young E. C., Barg J. Coscia C. J. (1998) Opioid modulation of extracellular signal-regulated protein kinase activity is Ras-dependent and involves G(βγ) subunits. J. Neurochem. 70, 635 645.
8. Belcheva M. M., Wong Y. H. Coscia C. J. (2000) Evidence for transduction of μ but not κ opioid modulation of extracellular signal-regulated kinase activity by G(z) and G(12) proteins. Cell. Signal. 12, 481 489.
9. Belcheva M. M., Szucs M., Wang D. X., Sadee W. Coscia C. J. (2001) μ-Opioid receptor-mediated Erk activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J. Biol. Chem. 276, 33847 33853.
10. Belcheva M. M., Tan Y., Heaton V. M., Clark A. L. Coscia C. J. (2003) μ-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.
11. Belcheva M. M., Clark A. L., Haas P. D., Serna J. S., 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. 280, 27662 27669.
12. Bell J. E., Brettle R. P., Chiswick A. Simmonds P. (1998) HIV encephalitis, proviral load and dementia in drug users and homosexuals with AIDS. Effect of neocortical involvement. Brain 121, 2043 2052.
13. Biesiada E., Razandi M. Levin E. R. (1996) Egr-1 activates basic fibroblast growth factor transcription. Mechanistic implications for astrocyte proliferation. J. Biol. Chem. 271, 18576 18581.
14. Bohn L. M., Belcheva M. M. Coscia C. J. (2000) 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.
15. Bohn L. M., Dykstra L. A., Lefkowitz R. J., Caron M. G. Barak L. S. (2004) Relative opioid efficacy is determined by the complements of the G protein-coupled receptor desensitization machinery. Mol. Pharmacol. 66, 106 112.
16. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
17. Bruchas M. R., Macey T. A., Lowe J. D. Chavkin C. (2006) κ Opioid receptor activation of p38 MAPK is GRK3- and arrestin-dependent in neurons and astrocytes. J. Biol. Chem. 281, 18081 18089.
18. Bruchas M. R., Yang T., Schreiber S., DeFino M., Kwan S. C., Li S. Chavkin C. (2007) Long-acting κ Opioid antagonists disrupt receptor signaling and produce noncompetitive effects by activating c-Jun N-terminal kinase. J. Biol. Chem. 282, 29803 29811.
19. Buffo A., Rite I., Tripathi P., Lepier A., Colak D., Horn A. P., Mori T. Gotz M. (2008) Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl Acad. Sci. USA 105, 3581 3586.
20. Christopherson K. S., Ullian E. M., Stokes C. C., Mullowney C. E., Hell J. W., Agah A., Lawler J., Mosher D. F., Bornstein P. Barres B. A. (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421 433.
21. Crespo P., Cachero T. G., Xu N. Gutkind J. S. (1995) Dual effect of β-adrenergic receptors on mitogen-activated protein kinase. Evidence for a βγ-dependent activation and a Gαs-cAMP-mediated inhibition. J. Biol. Chem. 270, 25259 25265.
22. Diamond J. S. (2006) Astrocytes put down the broom and pick up the baton. Cell 125, 639 641.
23. Fanton C. P., McMahon M. Pieper R. O. (2001) Dual growth arrest pathways in astrocytes and astrocytic tumors in response to Raf-1 activation. J. Biol. Chem. 276, 18871 18877.
24. Fatemi S. H., Folsom T. D., Reutiman T. J. Lee S. (2008) Expression of astrocytic markers aquaporin 4 and connexin 43 is altered in brains of subjects with autism. Synapse 62, 501 507.
25. Gesty-Palmer D., Chen M., Reiter E. et al. (2006) Distinct β-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 281, 10856 10864.
26. Gorodinsky A., Barg J., Belcheva M. M., Levy R., McHale R. J., Vogel Z. Coscia C. J. (1995) Dynorphins modulate DNA synthesis in fetal brain cell aggregates. J. Neurochem. 65, 1481 1486.
27. Groer C. E., Tidgewell K., Moyer R. A., Harding W. W., Rothman R. B., Prisinzano T. E. Bohn L. M. (2007) An opioid agonist that does not induce μ opioid receptor - arrestin interactions or receptor internalization. Mol. Pharmacol. 71, 549 557.
28. 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. Perspect. Dev. Neurobiol. 5, 437 449.
29. 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. Brain Res. Dev. Brain Res. 62, 245 255.
30. Hauser K. F., Aldrich J. V., Anderson K. J. et al. (2005) Pathobiology of dynorphins in trauma and disease. Front Biosci. 10, 216 235.
31. Hooker J. M., Xu Y., Schiffer W., Shea C., Carter P. Fowler J. S. (2008) Pharmacokinetics of the potent hallucinogen, salvinorin A in primates parallels the rapid onset and short duration of effects in humans. Neuroimage 41, 1044 1050.
32. Ishibashi T., Dakin K. A., Stevens B., Lee P. R., Kozlov S. V., Stewart C. L. Fields R. D. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823 832.
33. Jiao J.-W., Feldheim D. A. Chen D. F. (2008) Ephrins as negative regulators of adult neurogenesis in diverse regions of the central nervous system. Proc. Natl Acad. Sci. USA 105, 8778 8783.
34. Kurino M., Fukunaga K., Ushio Y. Miyamoto E. (1996) Cyclic AMP inhibits activation of mitogen-activated protein kinase and cell proliferation in response to growth factors in cultured rat cortical astrocytes. J. Neurochem. 67, 2246 2255.
35. Lazarini F., Strosberg A. D., Couraud P. O. Cazaubon S. M. (1996) Coupling of ETB endothelin receptor to mitogen-activated protein kinase stimulation and DNA synthesis in primary cultures of rat astrocytes. J. Neurochem. 66, 459 465.
36. Lee D. Y., Karnati V. V., He M. et al. (2005) Synthesis and in vitro pharmacological studies of new C(2) modified salvinorin A analogues. Bioorg. Med. Chem. Lett. 15, 3744 3747.
37. Lefkowitz R. J. Shenoy S. K. (2005) Transduction of receptor signals by β-arrestins. Science 308, 512 517.
38. Lefkowitz R. J., Rajagopal K. Whalen E. J. (2006) New roles for β-arrestins in cell signaling: not just for seven-transmembrane receptors. Mol. Cell 24, 643 652.
39. Lenz G., Goncalves D., Luo Z. J., Avruch J., Rodnight R. Neary J. T. (2001) Extracellular ATP stimulates an inhibitory pathway towards growth factor-induced cRaf-1 and MEKK activation in astrocyte cultures. J. Neurochem. 77, 1001 1009.
40. Mahajan S. D., Schwartz S. A., Aalinkeel R., Chawda R. P., Sykes D. E. Nair M. P. (2005) Morphine modulates chemokine gene regulation in normal human astrocytes. Clin. Immunol. 115, 323 332.
41. McGrew L., Chang M. S. S. Sanders-Bush E. (2002) Phospholipase D activation by endogenous 5-hydroxytryptamine 2C receptors is mediated by Gα13 and pertussis toxin-insensitive Gβγ subunits. Mol. Pharmacol. 62, 1339 1343.
42. Mukhopadhyay S. Howlett A. C. (2005) Chemically distinct ligands promote differential CB1 cannabinoid receptor-Gi protein interactions. Mol. Pharmacol. 67, 2016 2024.
43. Muroyama Y., Fujiwara Y., Orkin S. H. Rowitch D. H. (2005) Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438, 360 363.
44. Nishida H. Okabe S. (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. J. Neurosci. 27, 331 340.
45. Panatier A., Theodosis D. T., Mothet J. P., Touquet B., Pollegioni L., Poulain D. A. Oliet S. H. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775 784.
46. Radany E. H., Brenner M., Besnard F., Bigornia V., Bishop J. M. Deschepper C. F. (1992) Directed establishment of rat brain cell lines with the phenotypic characteristics of type 1 astrocytes. Proc. Natl Acad. Sci. USA 89, 6467 6471.
47. Raff M. C., Abney E. R., Cohen J., Lindsay R. Noble M. (1983) Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J. Neurosci. 3, 1289 1300.
48. Riboni L., Viani P., Bassi R., Stabilini A. Tettamanti G. (2000) Biomodulatory role of ceramide in basic fibroblast growth factor-induced proliferation of cerebellar astrocytes in primary culture. Glia 32, 137 145.
49. Riboni L., Viani P., Bassi R., Giussani P. Tettamanti G. (2001) Basic fibroblast growth factor-induced proliferation of primary astrocytes - evidence for the involvement of sphingomyelin biosynthesis. J. Biol. Chem. 276, 12797 12804.
50. Roth B. L., Baner K., Westkaemper R., Siebert D., Rice K. C., Steinberg S., Ernsberger P. Rothman R. B. (2002) Salvinorin A: a potent naturally occurring nonnitrogenous kappa opioid selective agonist. Proc. Natl Acad. Sci. USA 99, 11934 11939.
51. Seifert G., Schilling K. Steinhauser C. (2006) Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat. Rev. Neurosci. 7, 194.
52. Shah B. H., Farshori M. P., Jambusaria A. Catt K. J. (2003) Roles of Src and epidermal growth factor receptor transactivation in transient and sustained Erk1/2 responses to gonadotropin-releasing hormone receptor activation. J. Biol. Chem. 278, 19118 19126.
53. Shenoy S. K., Drake M. T., Nelson C. D., Houtz D. A., Xiao K., Madabushi S., Reiter E., Premont R. T., Lichtarge O. Lefkowitz R. J. (2006) β-Arrestin-dependent, G protein-independent ERK1/2 activation by the β2 adrenergic receptor. J. Biol. Chem. 281, 1261 1273.
54. Stiene-Martin A., Gurwell J. A. Hauser K. F. (1991) 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 7.
55. Stommel J. M., Kimmelman A. C., Ying H. et al. (2007) Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318, 287 290.
56. Terai K., Iwai A., Kawabata S., Sasamata M., Miyata K. Yamaguchi T. (2001) Apolipoprotein E deposition and astrogliosis are associated with maturation of beta-amyloid plaques in betaAPPswe transgenic mouse: implications for the pathogenesis of Alzheimer's disease. Brain Res. 900, 48 56.
57. Tidgewell K., Groer C. E., Harding W. W. et al. (2008) Herkinorin analogues with differential beta-arrestin-2 interactions. J. Med. Chem. 51, 2421 2431.
58. Tohgo A. K., Pierce K. L., Choy E. W., Lefkowitz R. J. Luttrell L. M. (2002) β-Arrestin scaffolding of the ERK cascade enhances cytosolic ERK activity but inhibits ERK-mediated transcription following angiotensin AT1a receptor stimulation. J. Biol. Chem. 277, 9429 9436.
59. Urban J. D., Clarke W. P., von Zastrow M. et al. (2007) Functional selectivity and classical concepts of quantitative pharmacology. J. Pharmacol. Exp. Ther. 320, 1 13.
60. Vortherms T. A., Mosier P. D., Westkaemper R. B. Roth B. L. (2007) Differential helical orientations among related G protein-coupled receptors provide a novel mechanism for selectivity: studies with salvinorin A and the κ-opioid receptor. J. Biol. Chem. 282, 3146 3156.
61. Wang L. C., Baird D. H., Hatten M. E. Mason C. A. (1994) Astroglial differentiation is required for support of neurite outgrowth. J. Neurosci. 14, 3195 3207.
62. Xu M., Bruchas M. R., Ippolito D. L., Gendron L. Chavkin C. (2007) Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by κ opioid activation of p38 mitogen-activated protein kinase. J. Neurosci. 27, 2570 2581.
63. Yan F. Roth B. L. (2004) Salvinorin A: a novel and highly selective κ-opioid receptor agonist. Life Sci. 75, 2615 2619.
64. Yang Y., Ge W., Chen Y., Zhang Z., Shen W., Wu C., Poo M. Duan S. (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of d-serine. Proc. Natl Acad. Sci. USA 100, 15194 15199.
65. Yang Y., Zhang P., Xiong Y., Li X., Qi Y. Hu H. (2007) Ectopia of meningeal fibroblasts and reactive gliosis in the cerebral cortex of the mouse model of muscle-eye-brain disease. J. Comp. Neurol. 505, 459 477.