Developmental expression of GPR3 in rodent cerebellar granule neurons is associated with cell survival and protects neurons from various apoptotic stimuli

Neurobiology of Disease

Volumn 68, Issue , 2014, Pages 215-227

  Tanaka, Shigeru ^a   Miyagi, Tatsuhiro ^a   Dohi, Eisuke ^a   Seki, Takahiro ^a   Hide, Izumi ^a   Sotomaru, Yusuke ^a   Saeki, Yoshinaga ^b   Antonio Chiocca, E ^c   Matsumoto, Masayasu ^a   Sakai, Norio ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b Saeki Hospital   (Japan)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Apoptosis; Brain ischemia; CAMP; Cerebellar granular neurons; GPR3; Neuronal protection

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 12; G PROTEIN COUPLED RECEPTOR 3; G PROTEIN COUPLED RECEPTOR 6; KT 5720; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; CULTURE MEDIUM; ENZYME INHIBITOR; FORSKOLIN; GPR3 PROTEIN, MOUSE;

ADULT; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GRANULE CELL; HABENULA; HIPPOCAMPUS; HYPOXIA; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLFACTORY BULB; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PURKINJE CELL; SIGNAL TRANSDUCTION; UPREGULATION; AGE; ANIMAL; C57BL MOUSE; CULTURE MEDIUM; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PATHOLOGY; PHARMACOLOGY; RAT; WISTAR RAT;

AGE FACTORS; ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CELL SURVIVAL; CEREBELLUM; COLFORSIN; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ISCHEMIA; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84901626066     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.04.007     Document Type: Article

References (80)

1. Ahn S., et al. {Beta}-arrestin-2 mediates anti-apoptotic signaling through regulation of BAD phosphorylation. J. Biol. Chem. 2009, 284:8855-8865.
2. Allais A., et al. Altered cerebellar development in mice lacking pituitary adenylate cyclase-activating polypeptide. Eur. J. Neurosci. 2007, 25:2604-2618.
3. Basille M., et al. Localization and characterization of PACAP receptors in the rat cerebellum during development: evidence for a stimulatory effect of PACAP on immature cerebellar granule cells. Neuroscience 1993, 57:329-338.
4. Basille M., et al. Comparative distribution of pituitary adenylate cyclase-activating polypeptide (PACAP) binding sites and PACAP receptor mRNAs in the rat brain during development. J. Comp. Neurol. 2000, 425:495-509.
5. Bertelsen L.S., et al. Gs protein-coupled receptor agonists induce transactivation of the epidermal growth factor receptor in T84 cells: implications for epithelial secretory responses. J. Biol. Chem. 2004, 279:6271-6279.
6. Brunet A., et al. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 2001, 11:297-305.
7. Chan P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 2001, 21:2-14.
8. Datta S.R., et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91:231-241.
9. Datta S.R., et al. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol. Cell 2000, 6:41-51.
10. Delcourt N., et al. PACAP type I receptor transactivation is essential for IGF-1 receptor signalling and antiapoptotic activity in neurons. EMBO J. 2007, 26:1542-1551.
11. D'Mello S.R., et al. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:10989-10993.
12. Eggerickx D., et al. Molecular cloning of an orphan G-protein-coupled receptor that constitutively activates adenylate cyclase. Biochem. J. 1995, 309(Pt 3):837-843.
13. Falluel-Morel A., et al. 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. 2007, 19:321-327.
14. Falluel-Morel A., et al. Granule cell survival is deficient in PAC1-/- mutant cerebellum. J. Mol. Neurosci. 2008, 36:38-44.
15. Friedlander R.M. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 2003, 348:1365-1375.
16. Funahashi Y., et al. ERK2-mediated phosphorylation of Par3 regulates neuronal polarization. J. Neurosci. 2013, 33:13270-13285.
17. Gasz B., et al. Pituitary adenylate cyclase activating polypeptide protects cardiomyocytes against oxidative stress-induced apoptosis. Peptides 2006, 27:87-94.
18. Gavrieli Y., et al. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119:493-501.
19. Gesty-Palmer D., et al. Distinct beta-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 2006, 281:10856-10864.
20. Gonzalez B.J., et al. Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Neuroscience 1997, 78:419-430.
21. González-Polo R.A., et al. Paraquat-induced apoptotic cell death in cerebellar granular cells. Brain Res. 2004, 1011:170-176.
22. Guegan C., et al. Reduction of ischemic damage in NGF-transgenic mice: correlation with enhancement of antioxidant enzyme activities. Neurobiol. Dis. 1999, 6:180-189.
23. Hanson M.G., et al. Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J. Neurosci. 1998, 18:7361-7371.
24. Hara H., et al. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2007-2012.
25. Harada H., et al. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 1999, 3:413-422.
26. Harmar A.J., et al. International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol. Rev. 1998, 50:265-270.
27. Hatten M.E. Neuronal regulation of astroglial morphology and proliferation in vitro. J. Cell Biol. 1985, 100:384-396.
28. Hatten M.E. The role of migration in central nervous system neuronal development. Curr. Opin. Neurobiol. 1993, 3:38-44.
29. Herrup K., Sunter K. Numerical matching during cerebellar development: quantitative analysis of granule cell death in staggerer mouse chimeras. J. Neurosci. 1987, 7:829-836.
30. Hu B.R., et al. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J. Cereb. Blood Flow Metab. 2000, 20:1294-1300.
31. Kooijman R., et al. Insulin-like growth factor I: a potential neuroprotective compound for the treatment of acute ischemic stroke?. Stroke 2009, 40:e83-e88.
32. Le D.A., et al. Caspase activation and neuroprotection in caspase-3-deficient mice after in vivo cerebral ischemia and in vitro oxygen glucose deprivation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15188-15193.
33. Li Y., et al. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 1995, 15:389-397.
34. Lonze B.E., et al. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 2002, 34:371-385.
35. Lowther K.M., et al. Regulation of constitutive GPR3 signaling and surface localization by GRK2 and beta-arrestin-2 overexpression in HEK293 cells. PLoS One 2013, 8:e65365.
36. Mehlmann L.M., et al. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 2004, 306:1947-1950.
37. Mei Y.A., et al. PACAP inhibits delayed rectifier potassium current via a cAMP/PKA transduction pathway: evidence for the involvement of I k in the anti-apoptotic action of PACAP. Eur. J. Neurosci. 2004, 19:1446-1458.
38. Michel P.P., Agid Y. Chronic activation of the cyclic AMP signaling pathway promotes development and long-term survival of mesencephalic dopaminergic neurons. J. Neurochem. 1996, 67:1633-1642.
39. Miyazaki H., et al. Glial cell line-derived neurotrophic factor protects against delayed neuronal death after transient forebrain ischemia in rats. Neuroscience 1999, 89:643-647.
40. Mollace V., et al. The role of oxidative stress in paraquat-induced neurotoxicity in rats: protection by non peptidyl superoxide dismutase mimetic. Neurosci Lett. 2003, 335:163-166.
41. Nakao N. An increase in intracellular levels of cyclic AMP produces trophic effects on striatal neurons developing in culture. Neuroscience 1998, 82:1009-1020.
42. Namura S., et al. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 1998, 18:3659-3668.
43. Nicole O., et al. Neuroprotection mediated by glial cell line-derived neurotrophic factor: involvement of a reduction of NMDA-induced calcium influx by the mitogen-activated protein kinase pathway. J. Neurosci. 2001, 21:3024-3033.
44. Niizuma K., et al. Oxidative stress and mitochondrial dysfunction as determinants of ischemic neuronal death and survival. J. Neurochem. 2009, 109(Suppl. 1):133-138.
45. Niizuma K., et al. Mitochondrial and apoptotic neuronal death signaling pathways in cerebral ischemia. Biochim. Biophys. Acta 2010, 1802:92-99.
46. Ohtaki H., et al. Pituitary adenylate cyclase-activating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7488-7493.
47. Povsic T.J., et al. Beta-arrestin1 mediates insulin-like growth factor 1 (IGF-1) activation of phosphatidylinositol 3-kinase (PI3K) and anti-apoptosis. J. Biol. Chem. 2003, 278:51334-51339.
48. Racz B., et al. The neuroprotective effects of PACAP in monosodium glutamate-induced retinal lesion involve inhibition of proapoptotic signaling pathways. Regul. Pept. 2006, 137:20-26.
49. Racz B., et al. Effects of pituitary adenylate cyclase activating polypeptide (PACAP) on the PKA-Bad-14-3-3 signaling pathway in glutamate-induced retinal injury in neonatal rats. Neurotox. Res. 2007, 12:95-104.
50. Racz B., et al. PKA-Bad-14-3-3 and Akt-Bad-14-3-3 signaling pathways are involved in the protective effects of PACAP against ischemia/reperfusion-induced cardiomyocyte apoptosis. Regul. Pept. 2008, 145:105-115.
51. Rajagopal R., et al. Transactivation of Trk neurotrophin receptors by G-protein-coupled receptor ligands occurs on intracellular membranes. J. Neurosci. 2004, 24:6650-6658.
52. Ren X.R., et al. Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1448-1453.
53. Riccio A., et al. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 1999, 286:2358-2361.
54. Rossiter J.P., et al. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury. Acta Neuropathol. 2002, 103:66-73.
55. Ruiz-Medina J., et al. GPR3 orphan receptor is involved in neuropathic pain after peripheral nerve injury and regulates morphine-induced antinociception. Neuropharmacology 2011, 61:43-50.
56. Ruscher K., et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J. Neurosci. 2002, 22:10291-10301.
57. Rydel R.E., Greene L.A. cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of nerve growth factor. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1257-1261.
58. Saeki Y., et al. Molecular cloning of a novel putative G protein-coupled receptor (GPCR21) which is expressed predominantly in mouse central nervous system. FEBS Lett. 1993, 336:317-322.
59. Schabitz W.R., et al. A neuroprotective function for the hematopoietic protein granulocyte-macrophage colony stimulating factor (GM-CSF). J. Cereb. Blood Flow Metab. 2008, 28:29-43.
60. Scheid M.P., et al. Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase. J. Biol. Chem. 1999, 274:31108-31113.
61. Schneider A., et al. The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J. Clin. Invest. 2005, 115:2083-2098.
62. Shenoy S.K., Lefkowitz R.J. Beta-arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 2011, 32:521-533.
63. Shenoy S.K., et al. Beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J. Biol. Chem. 2006, 281:1261-1273.
64. Siren A.L., et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4044-4049.
65. Song Z.H., et al. Molecular cloning of a novel candidate G protein-coupled receptor from rat brain. FEBS Lett. 1994, 351:375-379.
66. Stumm R., et al. Pituitary adenylate cyclase-activating polypeptide is up-regulated in cortical pyramidal cells after focal ischemia and protects neurons from mild hypoxic/ischemic damage. J. Neurochem. 2007, 103:1666-1681.
67. Tanaka S., et al. Neural expression of G protein-coupled receptors GPR3, GPR6, and GPR12 up-regulates cyclic AMP levels and promotes neurite outgrowth. J. Biol. Chem. 2007, 282:10506-10515.
68. Tanaka S., et al. The Gs-linked receptor GPR3 inhibits the proliferation of cerebellar granule cells during postnatal development. PLoS One 2009, 4:e5922.
69. Thathiah A., et al. The orphan G protein-coupled receptor 3 modulates amyloid-beta peptide generation in neurons. Science 2009, 323:946-951.
70. Thathiah A., et al. Beta-arrestin 2 regulates Abeta generation and gamma-secretase activity in Alzheimer's disease. Nat. Med. 2013, 19:43-49.
71. Tourino C., et al. The orphan receptor GPR3 modulates the early phases of cocaine reinforcement. Br. J. Pharmacol. 2012, 167:892-904.
72. Uhlenbrock K., et al. Sphingosine 1-phosphate is a ligand of the human gpr3, gpr6 and gpr12 family of constitutively active G protein-coupled receptors. Cell. Signal. 2002, 14:941-953.
73. Valverde O., et al. GPR3 receptor, a novel actor in the emotional-like responses. PLoS One 2009, 4:e4704.
74. Vaudry D., et al. PACAP protects cerebellar granule neurons against oxidative stress-induced apoptosis. Eur. J. Neurosci. 2002, 15:1451-1460.
75. Vaudry D., et al. Endogenous PACAP acts as a stress response peptide to protect cerebellar neurons from ethanol or oxidative insult. Peptides 2005, 26:2518-2524.
76. Velier J.J., et al. Caspase-8 and caspase-3 are expressed by different populations of cortical neurons undergoing delayed cell death after focal stroke in the rat. J. Neurosci. 1999, 19:5932-5941.
77. Wei H., et al. Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10782-10787.
78. Yan G.M., et al. Activation of G proteins bidirectionally affects apoptosis of cultured cerebellar granule neurons. J. Neurochem. 1995, 65:2425-2431.
79. Zheng H., et al. Selective recruitment of G protein-coupled receptor kinases (GRKs) controls signaling of the insulin-like growth factor 1 receptor. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7055-7060.
80. Zhou X., et al. N-methyl-d-aspartate-stimulated ERK1/2 signaling and the transcriptional up-regulation of plasticity-related genes are developmentally regulated following in vitro neuronal maturation. J. Neurosci. Res. 2009, 87:2632-2644.