Astrocytic plasticity and patterned oxytocin neuronal activity: Dynamic interactions

Journal of Neuroscience

Volumn 29, Issue 6, 2009, Pages 1743-1754

  Wang, Yu Feng ^a,b   Hatton, Glenn I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Excitability; Gfa (glial fibrillary acidic protein); Imaging; Lactation; Protein; Supraoptic

Indexed keywords

ACTIN; AMINOADIPIC ACID; AQUAPORIN 4; CELL PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; OXYTOCIN; POTASSIUM CHANNEL; POTASSIUM ION; PROTEINASE INHIBITOR; RACEMASE; TETANUS TOXIN;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL FUNCTION; CELL INTERACTION; CELL STIMULATION; CONTROLLED STUDY; FEMALE; HORMONAL REGULATION; IMMUNOCYTOCHEMISTRY; LACTATION; MILK EJECTION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RAT; SUCKLING; SUPRAOPTIC NUCLEUS; TISSUE LEVEL; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; ASTROCYTES; FEMALE; NEURONAL PLASTICITY; NEURONS; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 60849083540     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4669-08.2009     Document Type: Article

References (65)

1. Albrecht J, Norenberg MD (2006) Glutamine: a Trojan horse in ammonia neurotoxicity. Hepatology 44:788-794.
2. + clearance associated with aquaporin-4 mislocalization: phe-notypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci U S A 100:13615-13620.
3. Anderová M, Kubinová S, Mazel T, Chvátal A, Eliasson C, Pekny M, Syková E (2001) Effect of elevated K(+), hypotonic stress, and cortical spreading depression on astrocyte swelling in GFAP-deficient mice. Glia 35:189-203.
4. Armstrong WE, Rubrum A, Teruyama R, Bond CT, Adelman JP (2005) Im-munocytochemical localization of small-conductance, calcium-dependent potassium channels in astrocytes of the rat supraoptic nucleus. J Comp Neurol 491:175-185.
5. Badaut J, Nehlig A, Verbavatz J, Stoeckel M, Freund-Mercier MJ, Lasbennes F (2000) Hypervascularization in the magnocellular nuclei of the rat hypothalamus: relationship with the distribution of aquaporin-4 and markers of energy metabolism. J Neuroendocrinol 12:960-969.
6. Baudoux S, Parker D (2008) Glial-toxin-mediated disruption of spinal cord locomotor network function and its modulation by 5-HT. Neuroscience 153:1332-1343.
7. Belin V, Moos F (1986) Paired recordings from supraoptic and paraventricular oxytocin cells in suckled rats: recruitment and synchronization. J Physiol 377:369-390.
8. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT (2006) Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53:631-636.
9. Borán MS, García A (2007) The cyclic GMP-protein kinase G pathway regulates cytoskeleton dynamics and motility in astrocytes. J Neurochem 102:216-230.
10. Catheline G, Touquet B, Lombard MC, Poulain DA, Theodosis DT (2006) A study of the role of neuro-glial remodeling in the oxytocin system at lactation. Neuroscience 137:309-316.
11. Crowley WR, Armstrong WE (1992) Neurochemical regulation of oxytocin secretion in lactation. Endocr Rev 13:33-65.
12. de Kock CP, Wierda KD, Bosman LW, Min R, Koksma JJ, Mansvelder HD, Verhage M, Brussaard AB (2003) Somatodendritic secretion in oxytocin neurons is upregulated during the female reproductive cycle. J Neurosci 23:2726-2734.
13. Dieck ST, Heuer H, Ehrchen J, Otto C, Bauer K (1999) The peptide transporter PepT2 is expressed in rat brain and mediates the accumulation of the fluorescent dipeptide derivative beta-Ala-Lys-Nepsilon-AMCA in astrocytes. Glia 25:10-20.
14. Ding M, Eliasson C, Betsholtz C, Hamberger A, Pekny M (1998) Altered taurine release following hypotonic stress in astrocytes from mice deficient for GFAP and vimentin. Brain Res Mol Brain Res 62:77-81.
15. Espallergues J, Solovieva O, TéacherV, Bauer K, Alonso G, Vincent A, Hussy N (2007) Synergistic activation of astrocytes by ATP and norepinephrine in the rat supraoptic nucleus. Neuroscience 148:712-723.
16. Evanko DS, Zhang Q, Zorec R, Haydon PG (2004) Defining pathways of loss and secretion of chemical messengers from astrocytes. Glia 47:233-240.
17. Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629-683.
18. Gommerat I, Gola M (1996) Glial potassium channels activated by neuronal firing or intracellular cyclic AMP in Helix. J Physiol 495:649-664.
19. Halpern JL, Habig WH, Trenchard H, Russell JT (1990) Effect of tetanus toxin on oxytocin and vasopressin release from nerve endings of the neurohypophysis. J Neurochem 55:2072-2078.
20. Hatton GI (2004) Morphological plasticity of astroglial/neuronal interactions: functional implications. In: Glial neuronal signaling (Hatton GI, Parpura V, eds), pp 99-124. Boston: Kluwer Academic.
21. Hatton GI, Yang QZ, Cobbett P (1987) Dye coupling among immunocyto-chemically identified neurons in the supraoptic nucleus: increased incidence in lactating rats. Neuroscience 21:923-930.
22. Hughes EG, Maguire JL, McMinn MT, Scholz RE, Sutherland ML (2004) Loss of glial fibrillary acidic protein results in decreased glutamate transport and inhibition of PKA-induced EAAT2 cell surface trafficking. Brain Res Mol Brain Res 124:114-123.
23. Inagaki M, Gonda Y, Nishizawa K, Kitamura S, Sato C, Ando S, Tanabe K, Kikuchi K, Tsuiki S, Nishi Y (1990) Phosphorylation sites linked to glial filament disassembly in vitro locate in a non-a-helical head domain. J Biol Chem 265:4722-4729.
24. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-1056.
25. Lascola CD, Kraig RP (1996) Whole-cell chloride currents in rat astrocytes accompany changes in cell morphology. J Neurosci 16:2532-2545.
26. Leng G, Shibuki K (1987) Extracellular potassium changes in the rat neurohypophysis during activation of the magnocellular neurosecretory system. J Physiol 392:97-111.
27. Li L, Lundkvist A, Andersson D, Wilhelmsson U, Nagai N, Pardo AC, Nodin C, Ståhlberg A, Aprico K, Larsson K, Yabe T, Moons L, Fotheringham A, Davies I, Carmeliet P, Schwartz JP, Pekna M, Kubista M, Blomstrand F, Maragakis N, Nilsson M, Pekny M (2008) Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab 28:468-481.
28. Martineau M, Baux G, Mothet JP (2006) D-serine signalling in the brain: friend and foe. Trends Neurosci 29:481-491.
29. McCall MA, Gregg RG, Behringer RR, Brenner M, Delaney CL, Galbreath EJ, Zhang CL, Pearce RA, Chiu SY, Messing A (1996) Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology. Proc Natl Acad Sci U S A 93:6361-6366.
30. Mercier F, Hatton GI (2004) Meninges and perivasculature as mediators of CNS plasticity. In: Advances in molecular and cellular biology, Ed 1 (Hertz L, ed), pp 215-253. San Diego: Elsevier.
31. Mong JA, Blutstein T (2006) Estradiol modulation of astrocytic form and function: implications for hormonal control of synaptic communication. Neuroscience 138:967-975.
32. Morán J, Sabanero M, Meza I, Pasantes-Morales H (1996) Changes of actin cytoskeleton during swelling and regulatory volume decrease in cultured astrocytes. Am J Physiol 271:C1901-C1907.
33. Nabekura T, Morishima S, Cover TL, Mori S, Kannan H, Komune S, Okada Y (2003) Recovery from lactacidosis-induced glial cell swelling with the aid of exogenous anion channels. Glia 41:247-259.
34. Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpres-sion with KIR4.1. Neuroscience 129:905-913.
35. Neumann I, Russell JA, Landgraf R (1993) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53:65-75.
36. Niermann H, Amiry-Moghaddam M, Holthoff K, Witte OW, Ottersen OP (2001) A novel role of vasopressin in the brain: modulation of activity-dependent water flux in the neocortex. J Neurosci 21:3045-3051.
37. Nishida H, Okabe S (2007) Visualization of synapse-glia dynamics (in Japanese). Brain Nerve 59:755-761.
38. Okere CO, Wang YF, Higuchi T, Negoro H, Okutani F, Takahashi S, Murata T (1996) The effect of systemic and central nitric oxide administration on milk availability in lactating rats. Neuroreport 8:243-247.
39. Oliet SH, Mothet JP (2006) Molecular determinants of D-serine-mediated glio transmission: from release to function. Glia 54:726-737.
40. +-dependent glutamate transport into acutely isolated Muller glial cells from guinea pig retina. Pflugers Arch 429:140-142.
41. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. New York: Academic.
42. Pekny M, Pekna M (2004) Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 204:428-437.
43. Pekny M, Wilhelmsson U, Bogestål YR, Pekna M (2007) The role of astrocytes and complement system in neural plasticity. Int Rev Neurobiol 82:95-111.
44. Pierre K, Bonhomme R, Dupouy B, Poulain DA, Theodosis DT (2001) The polysialylated neural cell adhesion molecule reaches cell surfaces of hypothalamic neurons and astrocytes via the constitutive pathway. Neuroscience 103:133-142.
45. Rosso L, Peteri-Brunbäck B, Vouret-Craviari V, Deroanne C, Van Obberghen-Schilling E, Mienville JM (2002) Vasopressin and oxytocin reverse adenosine-induced pituicyte stellation via calcium-dependent activation of Cdc42. Eur J Neurosci 16:2324-2332.
46. Rosso L, Peteri-Brunbäck B, Mienville JM (2004) Putative physiological significance of vasopressin V1a receptor activation in rat pituicytes. J Neu-roendocrinol 16:313-318.
47. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, Fujisaki T, Fujimoto K, Katoh A, Ikeda T, Chen C, Thompson RF, ItoharaS (1996) Deficient cerebellar long-term depress on, mpa red eye bl nk cond t on ng, and normal motor coordination in GFAP mutant mice. Neuron 16:587-599.
48. Simard M, Nedergaard M (2004) The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129:877-896.
49. Sizonenko SV, Camm EJ, Dayer A, Kiss JZ (2008) Glial responses to neonatal hypoxic-ischemic injury in the rat cerebral cortex. Int J Dev Neurosci 26:37-45.
50. Sullivan SM, Lee A, Björkman ST, Miller SM, Sullivan RK, Poronnik P, Cold-itz PB, Pow DV (2007) Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: an identified role for GFAP. J Biol Chem 282:29414-29423.
51. Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193-205.
52. Syková E, Vargová L, Prokopová S, Simonová Z (1999) Glial swelling and astrogliosis produce diffusion barriers in the rat spinal cord. Glia 25:56-70.
53. Takahashi M, Itakura M, Yamamori S (2007) Exocytotic release of signaling molecules from astrocytes (in Japanese). Brain Nerve 59:697-706.
54. Tekkok SB, Ransom BR (2004) The glial-neuronal interactions and signaling: an introduction. In: Glial neuronal signaling (Hatton GI, Parpura V, eds), pp 1-20. Boston: Kluwer Academic.
55. Theodosis DT, Schachner M, Neumann ID (2004) Oxytocin neuron activation in NCAM-deficient mice: anatomical and functional consequences. Eur J Neurosci 20:3270-3280.
56. Tomita M, Tanahashi N, Takeda H, Takao M, Tomita Y, Amano T, Fukuuchi Y (2003) Astroglial swelling in the neuronal depolarization ensemble. Acta Neurochir Suppl 86:219-222.
57. Vesce S, Rossi D, Brambilla L, Volterra A (2007) Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int Rev Neurobiol 82:57-71.
58. Vitellaro-Zuccarello L, Mazzetti S, Bosisio P, Monti C, De Biasi S (2005) Distribution of Aquaporin 4 in rodent spinal cord: relationship with astrocyte markers and chondroitin sulfate proteoglycans. Glia 51:148-159.
59. Wakerley JB, Clarke G, Summerlee AJ (1994) Milk ejection and its control. In: The physiology of reproduction (Knobil E, Neill JD, eds), pp 1131-1177. New York: Raven.
60. Walz W, Wuttke WA (1999) Independent mechanisms of potassium clearance by astrocytes in gliotic tissue. J Neurosci Res 56:595-603.
61. Wang YF, Hatton GI (2004) Milk ejection burst-like electrical activity evoked in supraoptic oxytocin neurons in slices from lactating rats. J Neu-rophysiol 91:2312-2321.
62. Wang YF, Hatton GI (2006) Mechanisms underlying oxytocin-induced excitation of supraoptic neurons: prostaglandin mediation of actin polymerization. J Neurophysiol 95:3933-3947.
63. Wang YF, Hatton GI (2007a) Dominant role of βγ subunits of G-proteins in oxytocin-evoked burst firing. J Neurosci 27:1902-1912.
64. Wang YF, Hatton GI (2007b) Interaction of extracellular signal-regulated protein kinase 1/2 with actin cytoskeleton in supraoptic oxytocin neurons and astrocytes: role in burst firing. J Neurosci 27:13822-13834.
65. Weinstein DE, Shelanski ML, Liem RKH (1991) Suppression by antisense mRNA demonstrates a requirement for the glial fibrillary acidic protein in the formation of stable astrocytic processes in response to neurons. J Cell Biol 112:1205-1213.