Gabapentin Receptor α2δ-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis

Cell

Volumn 139, Issue 2, 2009, Pages 380-392

  Eroglu, Çagla ^a,b   Allen, Nicola J ^b   Susman, Michael W ^b   O'Rourke, Nancy A ^b   Park, Chan Young ^b   Özkan, Engin ^b   Chakraborty, Chandrani ^b   Mulinyawe, Sara B ^b   Annis, Douglas S ^c   Huberman, Andrew D ^b   Green, Eric M ^b   Lawler, Jack ^e   Dolmetsch, Ricardo ^b   Garcia, K Christopher ^b   Smith, Stephen J ^b   Luo, Z David ^d   Rosenthal, Arnon ^f   Mosher, Deane F ^c   Barres, Ben A ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MazorX Inc   (United States)

Author keywords

MOLNEURO

Indexed keywords

DRUG RECEPTOR; EPIDERMAL GROWTH FACTOR; GABAPENTIN; GABAPENTIN RECEPTOR ALPHA2DELTA 1; RECEPTOR; RECEPTOR SUBUNIT; THROMBOSPONDIN RECEPTOR; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; ALPHA2DELTA 1 PROTEIN, RAT; ALPHA2DELTA-1 PROTEIN, RAT; AMINE; CALCIUM CHANNEL; CD36 ANTIGEN; CYCLOHEXANECARBOXYLIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DRUG MECHANISM; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM FUNCTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SYNAPSE; SYNAPTOGENESIS; ANIMAL; DRUG EFFECT; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; RAT; SPRAGUE DAWLEY RAT;

AMINES; ANIMALS; ANTIGENS, CD36; CALCIUM CHANNELS; CYCLOHEXANECARBOXYLIC ACIDS; GAMMA-AMINOBUTYRIC ACID; MICE; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 70350368006     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.09.025     Document Type: Article

References (48)

1. Adams J.C., and Lawler J. The thrombospondins. Int. J. Biochem. Cell Biol. 36 (2004) 961-968
2. Annis D.S., Murphy-Ullrich J.E., and Mosher D.F. Function-blocking antithrombospondin-1 monoclonal antibodies. J. Thromb. Haemost. 4 (2006) 459-468
3. Annis D.S., Gunderson K.A., and Mosher D.F. Immunochemical analysis of the structure of the signature domains of thrombospondin-1 and thrombospondin-2 in low calcium concentrations. J. Biol. Chem. 282 (2007) 27067-27075
4. Arber S., and Caroni P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J. Cell Biol. 131 (1995) 1083-1094
5. Arikkath J., and Campbell K.P. Auxiliary subunits: essential components of the voltage-gated calcium channel complex. Curr. Opin. Neurobiol. 13 (2003) 298-307
6. Bork P., and Rohde K. More von Willebrand factor type A domains? Sequence similarities with malaria thrombospondin-related anonymous protein, dihydropyridine-sensitive calcium channel and inter-alpha-trypsin inhibitor. Biochem. J. 279 (1991) 908-910
7. Bornstein P., Agah A., and Kyriakides T.R. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int. J. Biochem. Cell Biol. 36 (2004) 1115-1125
8. Carlson C.B., Lawler J., and Mosher D.F. Structures of thrombospondins. Cell. Mol. Life Sci. 65 (2008) 672-686
9. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
10. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., and Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120 (2005) 421-433
11. Cole R.L., Lechner S.M., Williams M.E., Prodanovich P., Bleicher L., Varney M.A., and Gu G. Differential distribution of voltage-gated calcium channel alpha-2 delta (alpha2delta) subunit mRNA-containing cells in the rat central nervous system and the dorsal root ganglia. J. Comp. Neurol. 491 (2005) 246-269
12. Davies A., Hendrich J., Van Minh A.T., Wratten J., Douglas L., and Dolphin A.C. Functional biology of the alpha(2)delta subunits of voltage-gated calcium channels. Trends Pharmacol. Sci. 28 (2007) 220-228
13. Dickman D.K., Kurshan P.T., and Schwarz T.L. Mutations in a Drosophila alpha2delta voltage-gated calcium channel subunit reveal a crucial synaptic function. J. Neurosci. 28 (2008) 31-38
14. Dooley D.J., Taylor C.P., Donevan S., and Feltner D. Ca2+ channel alpha2delta ligands: novel modulators of neurotransmission. Trends Pharmacol. Sci. 28 (2007) 75-82
15. Eroglu C., Barres B.A., and Stevens B. Glia as active paricipants in the development and function of synapses. In: Hell J., and Ehlers M. (Eds). Structural and Functional Organization of the Synapse (2008), Springer, New York 683-714
16. Erzurumlu R.S., Chen Z.F., and Jacquin M.F. Molecular determinants of the face map development in the trigeminal brainstem. Anat. Rec. 288 (2006) 121-134
17. Field M.J., Cox P.J., Stott E., Melrose H., Offord J., Su T.Z., Bramwell S., Corradini L., England S., Winks J., et al. Identification of the alpha2-delta-1 subunit of voltage-dependent calcium channels as a molecular target for pain mediating the analgesic actions of pregabalin. Proc. Natl. Acad. Sci. USA 103 (2006) 17537-17542
18. Fox M.A., and Umemori H. Seeking long-term relationship: axon and target communicate to organize synaptic differentiation. J. Neurochem. 97 (2006) 1215-1231
19. Fremeau Jr. R.T., Voglmaier S., Seal R.P., and Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 27 (2004) 98-103
20. Garcia K., Nabhani T., and Garcia J. The calcium channel alpha2/delta1 subunit is involved in extracellular signaling. J. Physiol. 586 (2007) 727-738
21. Gee N.S., Brown J.P., Dissanayake V.U., Offord J., Thurlow R., and Woodruff G.N. The novel anticonvulsant drug, gabapentin (Neurontin), binds to the alpha2delta subunit of a calcium channel. J. Biol. Chem. 271 (1996) 5768-5776
22. Gurnett C.A., De Waard M., and Campbell K.P. Dual function of the voltage-dependent Ca2+ channel alpha 2 delta subunit in current stimulation and subunit interaction. Neuron 16 (1996) 431-440
23. Kaltenbach L.S., Romero E., Becklin R.R., Chettier R., Bell R., Phansalkar A., Strand A., Torcassi C., Savage J., Hurlburt A., et al. Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet. 3 (2007) e82
24. Klugbauer N., Marais E., and Hofmann F. Calcium channel alpha2delta subunits: differential expression, function, and drug binding. J. Bioenerg. Biomembr. 35 (2003) 639-647
25. Kurshan P.T., Matos A.O., and Schwarz T.L. The presynaptic Ca2+-channel subunit! 2″-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat. Neurosci. 12 (2009) 10.1038/nn.2417 in press
26. Li C.Y., Song Y.H., Higuera E.S., and Luo Z.D. Spinal dorsal horn calcium channel alpha2delta-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J. Neurosci. 24 (2004) 8494-8499
27. Li C.Y., Zhang X.L., Matthews E.A., Li K.W., Kurwa A., Boroujerdi A., Gross J., Gold M.S., Dickenson A.H., Feng G., et al. Calcium channel alpha2delta1 subunit mediates spinal hyperexcitability in pain modulation. Pain 125 (2006) 20-34
28. Liauw J., Hoang S., Choi M., Eroglu C., Choi M., Sun G.H., Percy M., Wildman-Tobriner B., Bliss T., Guzman R.G., et al. Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke. J. Cereb. Blood Flow Metab. 28 (2008) 1722-1732
29. Lin T.N., Kim G.M., Chen J.J., Cheung W.M., He Y.Y., and Hsu C.Y. Differential regulation of thrombospondin-1 and thrombospondin-2 after focal cerebral ischemia/reperfusion. Stroke 34 (2003) 177-186
30. Liu L., Rudin M., and Kozlova E.N. Glial cell proliferation in the spinal cord after dorsal rhizotomy or sciatic nerve transection in the adult rat. Exp. Brain Res. 131 (2000) 64-73
31. Lohmann C., and Bonhoeffer T. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 59 (2008) 253-260
32. Meyer-Franke A., Kaplan M.R., Pfrieger F.W., and Barres B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15 (1995) 805-819
33. Micheva K.D., and Smith S.J. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55 (2007) 25-36
34. Miyazaki T., Fukaya M., Shimizu H., and Watanabe M. Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur. J. Neurosci. 17 (2003) 2563-2572
35. Nakamura K., Hioki H., Fujiyama F., and Kaneko T. Postnatal changes of vesicular glutamate transporter (VGluT)1 and VGluT2 immunoreactivities and their colocalization in the mouse forebrain. J. Comp. Neurol. 492 (2005) 263-288
36. Pluskota E., Stenina O.I., Krukovets I., Szpak D., Topol E.J., and Plow E.F. Mechanism and effect of thrombospondin-4 polymorphisms on neutrophil function. Blood 106 (2005) 3970-3978
37. Prince D.A. Epileptogenic neurons and circuits. Adv. Neurol. 79 (1999) 665-684
38. Ridet J.L., Malhotra S.K., Privat A., and Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20 (1997) 570-577
39. Suman-Chauhan N., Webdale L., Hill D.R., and Woodruff G.N. Characterisation of [3H]gabapentin binding to a novel site in rat brain: homogenate binding studies. Eur. J. Pharmacol. 244 (1993) 293-301
40. Traa B.S., Mulholland J.D., Kadam S.D., Johnston M.V., and Comi A.M. Gabapentin neuroprotection and seizure suppression in immature mouse brain ischemia. Pediatr. Res. 64 (2008) 81-85
41. Ullian E.M., Sapperstein S.K., Christopherson K.S., and Barres B.A. Control of synapse number by glia. Science 291 (2001) 657-661
42. Valder C.R., Liu J.J., Song Y.H., and Luo Z.D. Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J. Neurochem. 87 (2003) 560-573
43. Wang H., Sun H., Della Penna K., Benz R.J., Xu J., Gerhold D.L., Holder D.J., and Koblan K.S. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114 (2002) 529-546
44. Wang M., Offord J., Oxender D.L., and Su T.Z. Structural requirement of the calcium-channel subunit alpha2delta for gabapentin binding. Biochem. J. 342 (1999) 313-320
45. Whittaker C.A., and Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 13 (2002) 3369-3387
46. Wierenga C.J., Becker N., and Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 11 (2008) 1044-1052
47. Wilkins J.A., Li A., Ni H., Stupack D.G., and Shen C. Control of beta1 integrin function. Localization of stimulatory epitopes. J. Biol. Chem. 271 (1996) 3046-3051
48. Wycisk K.A., Budde B., Feil S., Skosyrski S., Buzzi F., Neidhardt J., Glaus E., Nurnberg P., Ruether K., and Berger W. Structural and functional abnormalities of retinal ribbon synapses due to Cacna2d4 mutation. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3523-3530