Postsynaptic deregulation in GAP-43 heterozygous mouse barrel cortex

Cerebral Cortex

Volumn 20, Issue 7, 2010, Pages 1696-1707

  Kelly, Emily A ^a   Tremblay, Marie Ève ^a   McCasland, James S ^b   Majewska, Ania K ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

cortical development; dendrite morphology; glutamate receptors; postsynaptic specialization

Indexed keywords

CYTOCHROME C OXIDASE; GLUTAMATE RECEPTOR 1; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROMODULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CELL; BRAIN METABOLISM; CONVALESCENCE; DENDRITE; GOLGI COMPLEX; HETEROZYGOTE; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHENOTYPE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATOSENSORY CORTEX; SYNAPTOGENESIS; WILD TYPE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; DENDRITES; ELECTRON TRANSPORT COMPLEX IV; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; RECEPTORS, AMPA; SILVER STAINING; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 77955968791     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp231     Document Type: Article

References (70)

1. Albright MJ, Weston MC, Inan M, Rosenmund C, Crair MC. 2007. Increased thalamocortical synaptic response and decreased layer IV innervation in GAP-43 knockout mice. J Neurophysiol. 98: 1610-1625.
2. Bennett-Clarke CA, Hankin MH, Leslie MJ, Chiaia NL, Rhoades RW. 1994. Patterning of the neocortical projections from the raphe nuclei in perinatal rats: investigation of potential organizational mechanisms. J Comp Neurol. 348:277-290.
3. Benowitz LI, Routtenberg A. 1997. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:84-91.
4. Blue ME, Johnston MV. 1995. The ontogeny of glutamate receptors in rat barrel field cortex. Brain Res Dev Brain Res. 84:11-25.
5. Brennan EM, Martin LJ, Johnston MV, Blue ME. 1997. Ontogeny of non-NMDA glutamate receptors in rat barrel field cortex: II. Alpha-AMPA and kainate receptors. J Comp Neurol. 386:29-45.
6. Brown KE, Arends JJ, Wasserstrom SP, Zantua JB, Jacquin MF, Woolsey TA. 1995. Developmental transformation of dendritic arbors in mouse whisker thalamus. Brain Res Dev Brain Res. 86:335-339.
7. Cook EH, Jr., Scherer SW. 2008. Copy-number variations associated with neuropsychiatric conditions. Nature. 455:919-923.
8. Craig AM. 1998. Activity and synaptic receptor targeting: the long view. Neuron. 21:459-462.
9. Datwani A, Iwasato T, Itohara S, Erzurumlu RS. 2002. NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dendritic differentiation in the barrel cortex. Mol Cell Neurosci. 21:477-492.
10. Daw MI, Scott HL, Isaac JT. 2007. Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol Cell Neurosci. 34:493-502.
11. Dekker LV, De Graan PN, Versteeg DH, Oestreicher AB, Gispen WH. 1989. Phosphorylation of B-50 (GAP43) is correlated with neurotransmitter release in rat hippocampal slices. J Neurochem. 52:24-30.
12. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG. 2002. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci. 5:783-789.
13. Domenici L, Cellerino A, Berardi N, Cattaneo A, Maffei L. 1994. Antibodies to nerve growth factor (NGF) prolong the sensitive period for monocular deprivation in the rat. Neuroreport. 5:2041-2044.
14. Donovan SL, Mamounas LA, Andrews AM, Blue ME, McCasland JS. 2002. GAP-43 is critical for normal development of the serotonergic innervation in forebrain. J Neurosci. 22:3543-3552.
15. Donovan SL, McCasland JS. 2008. GAP-43 is critical for normal targeting of thalamocortical and corticothalamic, but not trigemi-nothalamic axons in the whisker barrel system. Somatosens Mot Res. 25:33-47.
16. Erzurumlu RS, Kind PC. 2001. Neural activity: sculptor of 'barrels' in the neocortex. Trends Neurosci. 24:589-595.
17. Feldman DE, Nicoll RA, Malenka RC. 1999. Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J Neurobiol. 41:92-101.
18. Gianotti C, Nunzi MG, Gispen WH, Corradetti R. 1992. Phosphorylation of the presynaptic protein B-50 (GAP-43) is increased during electrically induced long-term potentiation. Neuron. 8:843-848.
19. Gil OD, Needleman L, Huntley GW. 2002. Developmental patterns of cadherin expression and localization in relation to compartmentalized thalamocortical terminations in rat barrel cortex. J Comp Neurol. 453:372-388.
20. Harris KM. 1999. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol. 9:343-348.
21. Haruta T, Takami N, Ohmura M, Misumi Y, Ikehara Y. 1997. Ca2+-dependent interaction of the growth-associated protein GAP-43 with the synaptic core complex. Biochem J. 325(Pt 2): 455-463.
22. Inan M, Crair MC. 2007. Development of cortical maps: perspectives from the barrel cortex. Neuroscientist. 13:49-61.
23. Inan M, Lu HC, Albright MJ, She WC, Crair MC. 2006. Barrel map development relies on protein kinase A regulatory subunit II beta-mediated cAMP signaling. J Neurosci. 26:4338-4349.
24. Isaac JT, Crair MC, Nicoll RA, Malenka RC. 1997. Silent synapses during development of thalamocortical inputs. Neuron. 18:269-280.
25. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron. 15:427-434.
26. Ivy GO, Killackey HP. 1981. The ontogeny of the distribution of callosal projection neurons in the rat parietal cortex. J Comp Neurol. 195:367-389.
27. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knopfel T, Erzurumlu RS, Itohara S. 2000. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature. 406:726-731.
28. Killackey HP, Rhoades RW, Bennett-Clarke CA. 1995. The formation of a cortical somatotopic map. Trends Neurosci. 18:402-407.
29. Kitt CA, Struble RG, Cork LC, Mobley WC, Walker LC, Joh TH, Price DL. 1985. Catecholaminergic neurites in senile plaques in prefrontal cortex of aged nonhuman primates. Neuroscience. 16:691-699.
30. Kleschevnikov AM, Routtenberg A. 2001. PKC activation rescues LTP from NMDA receptor blockade. Hippocampus. 11:168-175.
31. Lee LJ, Iwasato T, Itohara S, Erzurumlu RS. 2005. Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol. 485:280-292.
32. Lee LJ, Lo FS, Erzurumlu RS. 2005. NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci. 25:2304-2311.
33. Liao D, Scannevin RH, Huganir R. 2001. Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J Neurosci. 21:6008-6017.
34. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL. 1999. Regulation of morphological postsynaptic silent synapses in developing hippo-campal neurons. Nat Neurosci. 2:37-43.
35. Lopez-Bendito G, Molnar Z. 2003. Thalamocortical development: how are we going to get there? Nat Rev Neurosci. 4:276-289.
36. Lu HC, She WC, Plas DT, Neumann PE, Janz R, Crair MC. 2003. Adenylyl cyclase I regulates AMPA receptor trafficking during mouse cortical 'barrel' map development. Nat Neurosci. 6:939-947.
37. Lund JS, Holbach SM, Chung WW. 1991. Postnatal development of thalamic recipient neurons in the monkey striate cortex: II. Influence of afferent driving on spine acquisition and dendritic growth of layer 4C spiny stellate neurons. J Comp Neurol. 309:129-140.
38. Maier DL, Mani S, Donovan SL, Soppet D, Tessarollo L, McCasland JS, Meiri KF. 1999. Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice. Proc Natl Acad Sci USA. 96:9397-9402.
39. Majewska B, Skangiel-Kramska J. 1996. Dendritic pattern in mouse barrel field after a neonatal vibrissal follicles removal: MAP-2 immunohistochemistry. Acta Neurobiol Exp (Warsz). 56:561-566.
40. Matus A, Bernhardt R, Hugh-Jones T. 1981. High molecular weight microtubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proc Natl Acad Sci USA. 78:3010-3014.
41. McIlvain V, McCasland JS. 2006. GAP-43 heterozygous mice show delayed barrel patterning, differentiation of radial glia, and down-regulation of GAP-43. Anat Rec. 288:143-157.
42. McIlvain VA, Robertson DR, Maimone MM, McCasland JS. 2003. Abnormal thalamocortical pathfinding and terminal arbors lead to enlarged barrels in neonatal GAP-43 heterozygous mice. J Comp Neurol. 462:252-264.
43. Miller B, Blake NM, Erinjeri JP, Reistad CE, Sexton T, Admire P, Woolsey TA. 2001. Postnatal growth of intrinsic connections in mouse barrel cortex. J Comp Neurol. 436:17-31.
44. Molnar Z, Hannan AJ. 2000. Development of thalamocortical projections in normal and mutant mice. Results Probl Cell Differ. 30:293-332.
45. Mumm JS, Williams PR, Godinho L, Koerber A, Pittman AJ, Roeser T, Chien CB, Baier H, Wong RO. 2006. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron. 52:609-621.
46. Neve RL, Coopersmith R, McPhie DL, Santeufemio C, Pratt KG, Murphy CJ, Lynn SD. 1998. The neuronal growth-associated protein GAP-43 interacts with rabaptin-5 and participates in endocytosis. J Neurosci. 18:7757-7767.
47. Niell CM, Meyer MP, Smith SJ. 2004. In vivo imaging of synapse formation on a growing dendritic arbor. Nat Neurosci. 7:254-260.
48. Olavarria J, Van Sluyters RC, Killackey HP. 1984. Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res. 291:364-368.
49. Pasternak JF, Woolsey TA. 1975. On the "selectivity" of the Golgi-Cox method. J Comp Neurol. 160:307-312.
50. Perez-Otano I, Ehlers MD. 2005. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci. 28:229-238.
51. Peters A, Palay SL, Webster H. 1991. The fine structure of the nervous system: the neurons and supporting cells. Philadelphia (PA): W.B. Saunders Company.
52. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R. 1999. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci. 2:31-36.
53. Pinon MC, Jethwa A, Jacobs E, Campagnoni A, Molnar Z. 2009. Dynamic integration of subplate neurons into the cortical barrel field circuitry during postnatal development in the Golli-tau-eGFP (GTE) mouse. J Physiol. 587:1903-1915.
54. Rocha M, Sur M. 1995. Rapid acquisition of dendritic spines by visual thalamic neurons after blockade of N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA. 92:8026-8030.
55. Routtenberg A. 1999. Tagging the Hebb synapse. Trends Neurosci. 22:255-256.
56. Routtenberg A, Cantallops I, Zaffuto S, Serrano P, Namgung U. 2000. Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA. 97:7657-7662.
57. Rusakov DA, Stewart MG. 1995. Quantification of dendritic spine populations using image analysis and a tilting disector. J Neurosci Methods. 60:11-21.
58. Tremblay ME, Riad M, Bouvier D, Murai KK, Pasquale EB, Descarries L, Doucet G. 2007. Localization of EphA4 in axon terminals and dendritic spines of adult rat hippocampus. J Comp Neurol. 501:691-702.
59. Tremblay ME, Riad M, Chierzi S, Murai KK, Pasquale EB, Doucet G. 2009. Developmental course of EphA4 cellular and subcellular localization in the postnatal rat hippocampus. J Comp Neurol. 512:798-813.
60. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 391:892-896.
61. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci. 5:97-107.
62. Watson RF, Abdel-Majid RM, Barnett MW, Willis BS, Katsnelson A, Gillingwater TH, McKnight GS, Kind PC, Neumann PE. 2006. Involvement of protein kinase A in patterning of the mouse somatosensory cortex. J Neurosci. 26:5393-5401.
63. White EL, Peters A. 1993. Cortical modules in the posteromedial barrel subfield (Sml) of the mouse. J Comp Neurol. 334:86-96.
64. Wierenga CJ, Ibata K, Turrigiano GG. 2005. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci. 25:2895-2905.
65. Wong PT, Neo LH, Teo WL, Feng H, Xue YD, Loke WH. 1997. Deficits in water escape performance and alterations in hippocampal cholin-ergic mechanisms associated with neonatal monosodium glutamate treatment in mice. Pharmacol Biochem Behav. 57:383-388.
66. Wong-Riley MT. 1989. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 12:94-101.
67. Wong-Riley MT, Hevner RF, Cutlan R, Earnest M, Egan R, Frost J, Nguyen T. 1993. Cytochrome oxidase in the human visual cortex: distribution in the developing and the adult brain. Vis Neurosci. 10:41-58.
68. Wong-Riley MT, Kageyama GH. 1986. Localization of cytochrome oxidase in the mammalian spinal cord and dorsal root ganglia, with quantitative analysis of ventral horn cells in monkeys. J Comp Neurol. 245:41-61.
69. Wong-Riley MT, Welt C. 1980. Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA. 77:2333-2337.
70. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitec-tonic units. Brain Res. 17:205-242.