Dynamics of β-adrenergic/cAMP signaling and morphological changes in cultured astrocytes

GLIA

Volumn 62, Issue 4, 2014, Pages 566-579

  Vardjan, Nina ^a,b   Kreft, Marko ^a,b,c   Zorec, Robert ^a,b  

^a Celica Biomedical Sciences Center   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

adrenergic signaling; Astrocytes; CAMP; Fluorescence resonance energy transfer; Stellation

Indexed keywords

ASTROCYTES; CAMP; FLUORESCENCE RESONANCE ENERGY TRANSFER; STELLATION; Β-ADRENERGIC SIGNALING;

1-METHYL-3-ISOBUTYLXANTHINE; ADRENERGIC AGENTS; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; COLFORSIN; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; LUMINESCENT PROTEINS; PHOSPHODIESTERASE INHIBITORS; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84893734691     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22626     Document Type: Article

References (68)

1. Abe K, Saito H. 1999. Effect of ATP on astrocyte stellation is switched from suppressive to stimulatory during development. Brain Res 850:150-157.
2. Allaman I, Lengacher S, Magistretti PJ, Pellerin L. 2003. A2B receptor activation promotes glycogen synthesis in astrocytes through modulation of gene expression. Am J Physiol Cell Physiol 284:C696-704.
3. Aoki C. 1992. Beta-adrenergic receptors: Astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry. J Neurosci 12:781-792.
4. Baillie GS. 2009. Compartmentalized signalling: Spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J 276:1790-1799.
5. Balázs R, Miller S, Chun Y, O'Toole J, Cotman CW. 1998. Metabotropic glutamate receptor agonists potentiate cyclic AMP formation induced by forskolin or beta-adrenergic receptor activation in cerebral cortical astrocytes in culture. J Neurochem 70:2446-2458.
6. Bardehle, S, Krüger M, Buggenthin, F, Schwausch, J, Ninkovic, J, Clevers, H, Snippert, HJ, Theis, FJ, Meyer-Luehmann M, Bechmann, I, Dimou, L, Götz M 2013. Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci 16:580-586.
7. Beavo JA, Brunton LL. 2002. Cyclic nucleotide research-Still expanding after half a century. Nat Rev Mol Cell Biol 3:710-718.
8. Bicknell RJ, Luckman SM, Inenaga K, Mason WT, Hatton GI. 1989. Beta-adrenergic and opioid receptors on pituicytes cultured from adult rat neurohypophysis: Regulation of cell morphology. Brain Res Bull 22:379-388.
9. Bolton S, Greenwood K, Hamilton N, Butt AM. 2006. Regulation of the astrocyte resting membrane potential by cyclic AMP and protein kinase A. Glia 54:316-328.
10. Börner S, Schwede F, Schlipp A, Berisha F, Calebiro D, Lohse MJ, Nikolaev VO. 2011. FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat Protoc 6:427-438.
11. Burgstaller G, Gregor M, Winter L, Wiche G. 2010. Keeping the vimentin network under control: Cell-matrix adhesion-associated plectin 1f affects cell shape and polarity of fibroblasts. Mol Biol Cell 21:3362-3375.
12. Catus SL, Gibbs ME, Sato M, Summers RJ, Hutchinson DS. 2011. Role of β-adrenoceptors in glucose uptake in astrocytes using β-adrenoceptor knockout mice. Br J Pharmacol 162:1700-1715.
13. Ciccarelli R, D'Alimonte I, Ballerini P, D'Auro M, Nargi E, Buccella S, Di Iorio P, Bruno V, Nicoletti F, Caciagli F. 2007. Molecular signalling mediating the protective effect of A1 adenosine and mGlu3 metabotropic glutamate receptor activation against apoptosis by oxygen/glucose deprivation in cultured astrocytes. Mol Pharmacol 71:1369-1380.
14. Cohen JE, Fields RD. 2008. Activity-dependent neuron-glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development. Neuron Glia Biol 4:43-55.
15. Cooper DM, Mons N, Karpen JW. 1995. Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374:421-424.
16. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, Bos JL. 1998. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474-477.
17. DiPilato LM, Cheng X, Zhang J. 2004. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc Natl Acad Sci USA 101:16513-16518.
18. Durand D, Carniglia L, Caruso C, Lasaga M. 2011. Reduced cAMP, Akt activation and p65-c-Rel dimerization: Mechanisms involved in the protective effects of mGluR3 agonists in cultured astrocytes. PLoS One 6:e22235.
19. Gharami K, Das S. 2004. Delayed but sustained induction of mitogen-activated protein kinase activity is associated with beta-adrenergic receptor-mediated morphological differentiation of astrocytes. J Neurochem 88:12-22.
20. Goldman JE, Abramson B. 1990. Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Res 528:189-196.
21. Griffith R, Sutin J. 1996. Reactive astrocyte formation in vivo is regulated by noradrenergic axons. J Comp Neurol 371:362-375.
22. Guček A, Vardjan N, Zorec R. 2012. Exocytosis in astrocytes: Transmitter release and membrane signal regulation. Neurochem Res 37:2351-2363.
23. Hammerschmidt T, Kummer MP, Terwel D, Martinez A, Gorji A, Pape HC, Rommelfanger KS, Schroeder JP, Stoll M, Schultze J, Weinshenker D, Heneka MT. 2013. Selective loss of noradrenaline exacerbates early cognitive dysfunction and synaptic deficits in APP/PS1 mice. Biol Psychiatry 73:454-463.
24. Hatton GI, Luckman SM, Bicknell RJ. 1991. Adrenalin activation of beta 2-adrenoceptors stimulates morphological changes in astrocytes (pituicytes) cultured from adult rat neurohypophyses. Brain Res Bull 26:765-769.
25. Kanno T, Nishizaki T. 2012. A(2a) adenosine receptor mediates PKA-dependent glutamate release from synaptic-like vesicles and Ca efflux from an IP(3)- and ryanodine-insensitive intracellular calcium store in astrocytes. Cell Physiol Biochem 30:1398-1412.
26. Kreft M, Bak LK, Waagepetersen HS, Schousboe A. 2012. Aspects of astrocyte energy metabolism, amino acid neurotransmitter homoeostasis and metabolic compartmentation. ASN Neuro 4.
27. Landa LR, Harbeck M, Kaihara K, Chepurny O, Kitiphongspattana K, Graf O, Nikolaev VO, Lohse MJ, Holz GG, Roe MW. 2005. Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 beta-cell line. J Biol Chem 280:31294-31302.
28. Laureys G, Clinckers R, Gerlo S, Spooren A, Wilczak N, Kooijman R, Smolders I, Michotte Y, De Keyser J. 2010. Astrocytic beta(2)-adrenergic receptors: From physiology to pathology. Prog Neurobiol 91:189-199.
29. Lee RK, Araki W, Wurtman RJ. 1997. Stimulation of amyloid precursor protein synthesis by adrenergic receptors coupled to cAMP formation. Proc Natl Acad Sci USA 94:5422-5426.
30. Lim R, Mitsunobu K, Li WK. 1973. Maturation-stimulation effect of brain extract and dibutyryl cyclic AMP on dissociated embryonic brain cells in culture. Exp Cell Res 79:243-246.
31. Mironov SL, Skorova E, Taschenberger G, Hartelt N, Nikolaev VO, Lohse MJ, Kügler S. 2009. Imaging cytoplasmic cAMP in mouse brainstem neurons. BMC Neurosci 10:29.
32. Nikolaev VO, Bünemann M, Hein L, Hannawacker A, Lohse MJ. 2004. Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279:37215-37218.
33. Nikolaev VO, Bünemann M, Schmitteckert E, Lohse MJ, Engelhardt S. 2006. Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta1-adrenergic but locally confined beta2-adrenergic receptor-mediated signaling. Circ Res 99:1084-1091.
34. Norris JG, Benveniste EN. 1993. Interleukin-6 production by astrocytes: Induction by the neurotransmitter norepinephrine. J Neuroimmunol 45:137-145.
35. Olabarria M, Noristani HN, Verkhratsky A, Rodríguez JJ. 2010. Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer's disease. Glia 58:831-838.
36. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A. 2012. Glial cells in (patho)physiology. J Neurochem 121:4-27.
37. Polak PE, Kalinin S, Feinstein DL. 2011. Locus coeruleus damage and noradrenaline reductions in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 134:665-677.
38. Prebil M, Jensen J, Zorec R, Kreft M. 2011a. Astrocytes and energy metabolism. Arch Physiol Biochem 117:64-69.
39. Prebil M, Vardjan N, Jensen J, Zorec R, Kreft M. 2011b. Dynamic monitoring of cytosolic glucose in single astrocytes. Glia 59:903-913.
40. Racchetti G, D'Alessandro R, Meldolesi J. 2012. Astrocyte stellation, a process dependent on Rac1 is sustained by the regulated exocytosis of enlargeosomes. Glia 60:465-475.
41. Rathbone MP, Middlemiss PJ, DeLuca B, Jovetich M. 1991. Extracellular guanosine increases astrocyte cAMP: Inhibition by adenosine A2 antagonists. Neuroreport 2:661-664.
42. Rich TC, Tse TE, Rohan JG, Schaack J, Karpen JW. 2001. In vivo assessment of local phosphodiesterase activity using tailored cyclic nucleotide-gated channels as cAMP sensors. J Gen Physiol 118:63-78.
43. Rosenberg PA, Li Y. 1995. Adenylyl cyclase activation underlies intracellular cyclic AMP accumulation, cyclic AMP transport, and extracellular adenosine accumulation evoked by beta-adrenergic receptor stimulation in mixed cultures of neurons and astrocytes derived from rat cerebral cortex. Brain Res 692:227-232.
44. Roy ML, Sontheimer H. 1995. Beta-adrenergic modulation of glial inwardly rectifying potassium channels. J Neurochem 64:1576-1584.
45. Safavi-Abbasi S, Wolff JR, Missler M. 2001. Rapid morphological changes in astrocytes are accompanied by redistribution but not by quantitative changes of cytoskeletal proteins. Glia 36:102-115.
46. Schultz C, Vajanaphanich M, Genieser HG, Jastorff B, Barrett KE, Tsien RY. 1994. Membrane-permeant derivatives of cyclic AMP optimized for high potency, prolonged activity, or rapid reversibility. Mol Pharmacol 46:702-708.
47. Schwartz JP, Nishiyama N. 1994. Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res Bull 35:403-407.
48. Schwartz, J, Wilson, D. 1992. Preparation and characterization of type 1 astrocytes cultured from adult rat cortex, cerebellum, and striatum. Glia 5:75-80.
49. Shain W, Forman DS, Madelian V, Turner JN. 1987. Morphology of astroglial cells is controlled by beta-adrenergic receptors. J Cell Biol 105:2307-2314.
50. Shao Y, Enkvist MO, McCarthy KD. 1994. Glutamate blocks astroglial stellation: Effect of glutamate uptake and volume changes. Glia 11:1-10.
51. Shapiro DL. 1973. Morphological and biochemical alterations in foetal rat brain cells cultured in the presence of monobutyryl cyclic AMP. Nature 241:203-204.
52. Sorg O, Magistretti PJ. 1992. Vasoactive intestinal peptide and noradrenaline exert long-term control on glycogen levels in astrocytes: Blockade by protein synthesis inhibition. J Neurosci 12:4923-4931.
53. Sutherland EW, Rall TW. 1960. Formation of adenosine-3, 5-phosphate (cyclic adenylate) and its relation to the action of several neurohormones or hormones. Acta Endocrinol Suppl (Copenh) 34(Suppl 50):171-174.
54. Sutin J, Griffith R. 1993. Beta-adrenergic receptor blockade suppresses glial scar formation. Exp Neurol 120:214-222.
55. Sutin J, Shao Y. 1992. Resting and reactive astrocytes express adrenergic receptors in the adult rat brain. Brain Res Bull 29:277-284.
56. Theodosis DT, Poulain DA, Oliet SH. 2008. Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88:983-1008.
57. Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M, Ellisman MH, Pekny M. 2006. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA 103:17513-17518.
58. Willoughby D, Cooper DM. 2006. Ca2+ stimulation of adenylyl cyclase generates dynamic oscillations in cyclic AMP. J Cell Sci 119:828-836.
59. Willoughby D, Cooper DM. 2008. Live-cell imaging of cAMP dynamics. Nat Methods 5:29-36.
60. Won CL, Oh YS. 2000. cAMP-induced stellation in primary astrocyte cultures with regional heterogeneity. Brain Res 887:250-258.
61. Wurm A, Lipp S, Pannicke T, Linnertz R, Färber K, Wiedemann P, Reichenbach A, Bringmann A. 2009. Involvement of A(1) adenosine receptors in osmotic volume regulation of retinal glial cells in mice. Mol Vis 15:1858-1867.
62. Wurm A, Lipp S, Pannicke T, Linnertz R, Krügel U, Schulz A, Färber K, Zahn D, Grosse J, Wiedemann P, Chen J, Schöneberg T, Illes P, Reichenbach A, Bringmann A. 2010. Endogenous purinergic signaling is required for osmotic volume regulation of retinal glial cells. J Neurochem 112:1261-1272.
63. Yu N, Martin JL, Stella N, Magistretti PJ. 1993. Arachidonic acid stimulates glucose uptake in cerebral cortical astrocytes. Proc Natl Acad Sci USA 90:4042-4046.
64. Zaccolo M, De Giorgi F, Cho CY, Feng L, Knapp T, Negulescu PA, Taylor SS, Tsien RY, Pozzan T. 2000. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol 2:25-29.
65. Zeinstra E, Wilczak N, De Keyser J. 2000. [3H]dihydroalprenolol binding to beta adrenergic receptors in multiple sclerosis brain. Neurosci Lett 289:75-77.
66. Zhang J, Hupfeld CJ, Taylor SS, Olefsky JM, Tsien RY. 2005. Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437:569-573.
67. Zhang J, Ma Y, Taylor SS, Tsien RY. 2001. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Natl Acad Sci USA 98:14997-15002.
68. Zorec R, Araque A, Carmignoto G, Haydon PG, Verkhratsky A, Parpura V. 2012. Astroglial excitability and gliotransmission: An appraisal of Ca2+ as a signalling route. ASN Neuro 4.