EphrinBs regulate D-serine synthesis and release in astrocytes

Journal of Neuroscience

Volumn 30, Issue 47, 2010, Pages 16015-16024

  Zhuang, Zhiye ^a   Yang, Bing ^a   Theus, Michelle H ^a   Sick, Justin T ^a   Bethea, John R ^a   Sick, Thomas J ^a   Liebl, Daniel J ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRO SERINE; EPHRIN; EPHRIN A4; EPHRIN B1; EPHRIN B2; EPHRIN B3; EPHRIN RECEPTOR; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C ALPHA; RACEMASE; SERINE; SERINE RACEMASE; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; EPHRIN-B3; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONAL PLASTICITY; PROTEIN BIOSYNTHESIS; RECEPTOR, EPHA4; SERINE; STEREOISOMERISM; SYNAPTIC TRANSMISSION;

EID: 78649414612     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0481-10.2010     Document Type: Article

References (58)

1. Angulo MC, Kozlov AS, Charpak S, Audinat E (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24:6920-6927. (Pubitemid 39045449)
2. Aoto J, Ting P, Maghsoodi B, Xu N, Henkemeyer M, Chen L (2007) Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. J Neurosci 27:7508-7519.
3. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208-215.
4. Bains JS, Oliet SH (2007) Glia: they make your memories stick! Trends Neurosci 30:417-424.
5. Baumgart F, Rodríguez-Crespo I (2008) D-amino acids in the brain: the biochemistry of brain serine racemase. FEBS J 275:3538-3545.
6. Blits-Huizinga CT, Nelersa CM, Malhotra A, Liebl DJ (2004) Ephrins and their receptors: binding versus biology. IUBMB Life 56:257-265.
7. Brückner K, Pablo Labrador J, Scheiffele P, Herb A, Seeburg PH, Klein R (1999) EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22:511-524. (Pubitemid 29159850)
8. Cook SP, Galve-Roperh I, Martínez del Pozo A, Rodríguez- Crespo I (2002) Direct calcium binding results in activation of brain serine racemase. J Biol Chem 277:27782-27792.
9. Cotrina ML, Lin JH, López-García JC, Naus CC, Nedergaard M (2000) ATP-mediated glia signaling. J Neurosci 20:2835-2844.
10. Fellin T, Carmignoto G (2004) Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. J Physiol 559:3-15.
11. Fields RD, Stevens-Graham B (2002) New insights into neuron-glia communication. Science 298:556-562.
12. Foltyn VN, Bendikov I, De Miranda J, Panizzutti R, Dumin E, Shleper M, Li P, Toney MD, Kartvelishvily E, Wolosker H (2005) Serine racemase modulates intracellular D-serine levels through an alpha, beta-elimination activity. J Biol Chem 280:1754-1763.
13. Fujii K, Maeda K, Hikida T, Mustafa AK, Balkissoon R, Xia J, Yamada T, Ozeki Y, Kawahara R, Okawa M, Huganir RL, Ujike H, Snyder SH, Sawa A (2006) Serine racemase binds to PICK1: potential relevance to schizophrenia. Mol Psychiatry 11:150-157.
14. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19.
15. Gordon GR, Baimoukhametova DV, Hewitt SA, Rajapaksha WR, Fisher TE, Bains JS (2005) Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 8:1078-1086.
16. Grunwald IC, Korte M, Adelmann G, Plueck A, Kullander K, Adams RH, Frotscher M, Bonhoeffer T, Klein R (2004) Hippocampal plasticity requires postsynaptic ephrinBs. Nat Neurosci 7:33-40. (Pubitemid 38032165)
17. Halassa MM, Fellin T, Haydon PG (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13:54-63.
18. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2:185-193.
19. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009-1031.
20. Helmbacher F, Schneider-Maunoury S, Topilko P, Tiret L, Charnay P (2000) Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127:3313-3324.
21. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R (1996) Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86:35-46.
22. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326.
23. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232-236.
24. Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, Sheng M (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 8:906-915.
25. Inoue R, Hashimoto K, Harai T, Mori H (2008) NMDA- and beta-amyloid1-42-induced neurotoxicity is attenuated in serine racemase knock-out mice. J Neurosci 28:14486-14491.
26. Iwasato T, Katoh H, Nishimaru H, Ishikawa Y, Inoue H, Saito YM, Ando R, Iwama M, Takahashi R, Negishi M, Itohara S (2007) Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130:742-753.
27. Jevince AR, Kadison SR, Pittman AJ, Chien CB, Kaprielian Z (2006) Distribution of EphB receptors and ephrin-B1 in the developing vertebrate spinal cord. J Comp Neurol 497:734-750.
28. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen V, Volterra A (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10:331-339. (Pubitemid 46310468)
29. Junjaud G, Rouaud E, Turpin F, Mothet JP, Billard JM (2006) Age-related effects of the neuromodulator D-serine on neurotransmission and synaptic potentiation in the CA1 hippocampal area of the rat. J Neurochem 98:1159-1166.
30. Kim PM, Aizawa H, Kim PS, Huang AS, Wickramasinghe SR, Kashani AH, Barrow RK, Huganir RL, Ghosh A, Snyder SH (2005) Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. Proc Natl Acad Sci U S A 102:2105-2110.
31. Klein R (2009) Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 12:15-20.
32. Martineau M, Baux G, Mothet JP (2006) D-serine signalling in the brain: friend and foe. Trends Neurosci 29:481-491.
33. Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci U S A 97:4926-4931.
34. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci U S A 102:5606-5611.
35. Mothet JP, Rouaud E, Sinet PM, Potier B, Jouvenceau A, Dutar P, Videau C, Epelbaum J, Billard JM (2006) A critical role for the glial-derived neuromodulator D-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell 5:267-274.
36. Mustafa AK, Kim PM, Snyder SH (2004) D-Serine as a putative glial neurotransmitter. Neuron Glia Biol 1:275-281.
37. Neary JT, Whittemore SR, Zhu Q, Norenberg MD (1994) Synergistic activation of DNA synthesis in astrocytes by fibroblast growth factors and extracellular ATP. J Neurochem 63:490-494. (Pubitemid 24233680)
38. Newman EA (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23:1659-1666.
39. Panatier A, Gentles SJ, Bourque CW, Oliet SH (2006a) Activity-dependent synaptic plasticity in the supraoptic nucleus of the rat hypothalamus. J Physiol 573:711-721.
40. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH (2006b) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125:775-784.
41. Pasquale EB (2008) Eph-ephrin bidirectional signaling in physiology and disease. Cell 133:38-52.
42. Perez JL, Khatri L, Chang C, Srivastava S, Osten P, Ziff EB (2001) PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J Neurosci 21:5417-5428.
43. Rodenas-Ruano A, Perez-Pinzon MA, Green EJ, Henkemeyer M, Liebl DJ (2006) Distinct roles for ephrinB3 in the formation and function of hippocampal synapses. Dev Biol 292:34-45.
44. Schell MJ, Brady RO Jr, Molliver ME, Snyder SH (1997) D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J Neurosci 17:1604-1615.
45. Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417:83-87.
46. Shleper M, Kartvelishvily E, Wolosker H (2005) D-serine is the dominant endogenous coagonist for NMDA receptor neurotoxicity in organotypic hippocampal slices. J Neurosci 25:9413-9417.
47. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
48. Staudinger J, Zhou J, Burgess R, Elledge SJ, Olson EN (1995) PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J Cell Biol 128:263-271.
49. Stevens ER, Esguerra M, Kim PM, Newman EA, Snyder SH, Zahs KR, Miller RF (2003) D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors. Proc Natl Acad Sci U S A 100:6789-6794.
50. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, Bredt DS, Gale NW, Yancopoulos GD (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21:1453-1463. (Pubitemid 29022546)
51. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897-6906.
52. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640.
53. Wolosker H, Sheth KN, Takahashi M, Mothet JP, Brady RO Jr, Ferris CD, Snyder SH (1999a) Purification of serine racemase: biosynthesis of the neuromodulator D-serine. Proc Natl Acad Sci U S A 96:721-725.
54. Wolosker H, Blackshaw S, Snyder SH (1999b) Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission. Proc Natl Acad Sci U S A 96:13409-13414.
55. Yang S, Qiao H, Wen L, Zhou W, Zhang Y (2005) D-serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci Lett 379:7-12.
56. 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 U S A 100:15194-15199.
57. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40:971-982. (Pubitemid 37522054)
58. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C, Strichartz GR, Decosterd I, Ji RR (2006) A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J Neurosci 26:3551-3560.