GAP-43 in synaptic plasticity: molecular perspectives

References

• Snipes GJ, Chan SY, McGuire CB, et al. Evidence for the coidentification of GAP-43, a growth-associated protein, and F1, a plasticity-associated protein. J Neurosci. 1987;7(12):4066–4075.
   Web of Science ®Google Scholar
• Grabczyk E, Zuber MX, Federoff HJ, Ng SC, Pack A, Fishman MC. Cloning and characterization of the rat gene encoding GAP-43. Eur J Neurosci. 1990;2(10):822–827.
   Web of Science ®Google Scholar
• Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997;20(2):84–91.
   PubMed Web of Science ®Google Scholar
• Sanna MD, Quattrone A, Mello T, Ghelardini C, Galeotti N. The RNA-binding protein HuD promotes spinal GAP43 overexpression in antiretroviral-induced neuropathy. Exp Neurol. 2014;261:343–353.
   PubMed Web of Science ®Google Scholar
• Mobarak CD, Anderson KD, Morin M, et al. The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells. Mol Biol Cell. 2000;11(9):3191–3203.
   PubMed Web of Science ®Google Scholar
• Deschenes-Furry J, Mousavi K, Bolognani F, et al. The RNA-binding protein HuD binds acetylcholinesterase mRNA in neurons and regulates its expression after axotomy. J Neurosci. 2007;27(3):665–675.
   Web of Science ®Google Scholar
• Perrone-Bizzozero N, Bolognani F. Role of HuD and other RNA-binding proteins in neural development and plasticity. J Neurosci Res. 2002;68(2):121–126.
   Web of Science ®Google Scholar
• Bolognani F, Tanner DC, Merhege M, Deschenes-Furry J, Jasmin B, Perrone-Bizzozero NI. In vivo post-transcriptional regulation of GAP-43 mRNA by overexpression of the RNA-binding protein HuD. J Neurochem. 2006;96(3):790–801.
   Web of Science ®Google Scholar
• Chan SY, Murakami K, Routtenberg A. Phosphoprotein F1: purification and characterization of a brain kinase C substrate related to plasticity. J Neurosci. 1986;6(12):3618–3627.
   Web of Science ®Google Scholar
• Basi GS, Jacobson RD, Virag I, Schilling J, Skene JH. Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth. Cell. 1987;49(6):785–791.
   Web of Science ®Google Scholar
• Strittmatter SM, Valenzuela D, Fishman MC. An amino-terminal domain of the growth-associated protein GAP-43 mediates its effects on filopodial formation and cell spreading. J Cell Sci. 1994;107 Pt 1:195–204.
   Google Scholar
• McLaughlin RE, Denny JB. Palmitoylation of GAP-43 by the ER-Golgi intermediate compartment and Golgi apparatus. Biochim Biophys Acta. 999;1451(1):82–92.
   Web of Science ®Google Scholar
• Coggins PJ, Zwiers H. Evidence for a single protein kinase C-mediated phosphorylation site in rat brain protein B-50. J Neurochem. 1989;53(6):1895–1901.
   Web of Science ®Google Scholar
• Meiri KF, Willard M, Johnson MI. Distribution and phosphorylation of the growth-associated protein GAP-43 in regenerating sympathetic neurons in culture. J Neurosci. 1988;8(7):2571–2581.
   Web of Science ®Google Scholar
• Sheu FS, Marais RM, Parker PJ, Bazan NG, Routtenberg A. Neuron-specific protein F1/GAP-43 shows substrate specificity for the beta subtype of protein kinase C. Biochem Biophys Res Commun. 1990;171(3):1236–1243.
   Web of Science ®Google Scholar
• Rosenthal A, Chan SY, Henzel W, et al. Primary structure and mRNA localization of protein F1, a growth-related protein kinase C substrate associated with synaptic plasticity. EMBO J. 1987;6(12):3641–3646.
   Web of Science ®Google Scholar
• Chao S, Benowitz LI, Krainc D, Irwin N. Use of a two-hybrid system to investigate molecular interactions of GAP-43. Brain Res Mol Brain Res. 996;40(2):195–202.
   Google Scholar
• Kumar V, Chichili VP, Zhong L, et al. Structural basis for the interaction of unstructured neuron specific substrates neuromodulin and neurogranin with calmodulin. Sci Rep. 2013;3:1392.
   Web of Science ®Google Scholar
• Neve RL, Coopersmith R, McPhie DL, et al. The neuronal growth-associated protein GAP-43 interacts with rabaptin-5 and participates in endocytosis. J Neurosci. 1998;18(19):7757–7767.
   Web of Science ®Google Scholar
• Cousin MA. Synaptic vesicle endocytosis: calcium works overtime in the nerve terminal. Mol Neurobiol. 2000;22(1–3):115–128.
   Web of Science ®Google Scholar
• Hou XE, Dahlstrom A. Synaptic vesicle proteins and neuronal plasticity in adrenergic neurons. Neurochem Res. 2000;25(9–10):1275–1300.
   Web of Science ®Google Scholar
• Verkade P, Verkleij AJ, Annaert WG, Gispen WH, Oestreicher AB. Ultrastructural localization of B-50/growth-associated protein-43 to anterogradely transported synaptophysin-positive and calcitonin gene-related peptide-negative vesicles in the regenerating rat sciatic nerve. Neuroscience. 1996;71(2):489–505.
   Web of Science ®Google Scholar
• Rekart JL, Routtenberg A. Overexpression of GAP-43 reveals unexpected properties of hippocampal mossy fibers. Hippocampus. 2010;20(1):46–57.
   Web of Science ®Google Scholar
• Goutan E, Marti E, Ferrer I. Expression of synaptic proteins in the developing rat cerebellum following ionizing radiation. Int J Dev Neurosci. 1999;17(4):275–283.
   Web of Science ®Google Scholar
• Chia PH, Li P, Shen K. Cell biology in neuroscience: cellular and molecular mechanisms underlying presynapse formation. J Cell Biol. 2013;203(1):11–22.
   Web of Science ®Google Scholar
• Arber S, Barbayannis FA, Hanser H, et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 1998;393(6687):805–809.
   PubMed Web of Science ®Google Scholar
• Heng JI, Chariot A, Nguyen L. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci. 2010;33(1):38–47.
   Web of Science ®Google Scholar
• Schaechter JD, Benowitz LI. Activation of protein kinase C by arachidonic acid selectively enhances the phosphorylation of GAP-43 in nerve terminal membranes. J Neurosci. 1993;13(10):4361–4371.
   Web of Science ®Google Scholar
• Vitkovic L, Steisslinger HW, Aloyo VJ, Mersel M. The 43-kDa neuronal growth-associated protein (GAP-43) is present in plasma membranes of rat astrocytes. Proc Natl Acad Sci U S A. 1988;85(21):8296–8300.
   Web of Science ®Google Scholar
• Vitkovic L, Mersel M. Growth-associated protein 43 is down-regulated in cultured astrocytes. Metab Brain Dis. 1989;4(1):47–53.
   Web of Science ®Google Scholar
• Han MH, Jiao S, Jia JM, et al. The novel caspase-3 substrate Gap43 is involved in AMPA receptor endocytosis and long-term depression. Mol Cell Proteomics. 2013;12(12):3719–3731.
   Web of Science ®Google Scholar
• Chao HM, Spencer RL, Sakai RR, McEwen BS. The expression of growth-associated protein GAP-43 mRNA in the rat hippocampus in response to adrenalectomy and aging. Mol Cell Neurosci. 1992;3(6):529–535.
   Web of Science ®Google Scholar
• Barnes CA, Mizumori SJ, Lovinger DM, et al. Selective decline in protein F1 phosphorylation in hippocampus of senescent rats. Neurobiol Aging. 1988;9(4):393–398.
   Web of Science ®Google Scholar
• Casoli T, Spagna C, Fattoretti P, Gesuita R, Bertoni-Freddari C. Neuronal plasticity in aging: a quantitative immunohistochemical study of GAP-43 distribution in discrete regions of the rat brain. Brain Res. 1996;714(1–2):111–117.
   Web of Science ®Google Scholar
• Casoli T, Di Stefano G, Gracciotti N, et al. Cellular distribution of GAP-43 mRNA in hippocampus and cerebellum of adult rat brain by in situ RT-PCR. J Histochem Cytochem. 2001;49(9):1195–1196.
   Web of Science ®Google Scholar
• Meberg PJ, Routtenberg A. Selective expression of protein F1/(GAP-43) mRNA in pyramidal but not granule cells of the hippocampus. Neuroscience. 1991;45(3):721–733.
   Web of Science ®Google Scholar
• Kruger L, Bendotti C, Rivolta R, Samanin R. GAP-43 mRNA localization in the rat hippocampus CA3 field. Brain Res Mol Brain Res. 1992;13(3):267–272.
   Google Scholar
• McGuire CB, Snipes GJ, Norden JJ. Light-microscopic immunolocalization of the growth- and plasticity-associated protein GAP-43 in the developing rat brain. Brain Res. 1988;469(1–2):277–291.
   Google Scholar
• De la Monte SM, Federoff HJ, Ng SC, Grabczyk E, Fishman MC. GAP-43 gene expression during development: persistence in a distinctive set of neurons in the mature central nervous system. Brain Res Dev Brain Res. 1989;46(2):161–168.
   Google Scholar
• Casoli T, Stefano GD, Fattoretti P, et al. GAP-43 mRNA detection by in situ hybridization, direct and indirect in situ RT-PCR in hippocampal and cerebellar tissue sections of adult rat brain. Micron. 2003;34(8):415–422.
   Web of Science ®Google Scholar
• McNamara RK, Lenox RH. Comparative distribution of myristoylated alanine-rich C kinase substrate (MARCKS) and F1/GAP-43 gene expression in the adult rat brain. J Comp Neurol. 1997;379(1):48–71.
   Web of Science ®Google Scholar
• Rosskothen-Kuhl N, Illing RB. Gap43 transcription modulation in the adult brain depends on sensory activity and synaptic cooperation. PLoS One. 2014;9(3):e92624.
   Web of Science ®Google Scholar
• Ramakers GJ, Verhaagen J, Oestreicher AB, Margolis FL, van Bergen en Henegouwen PM, Gispen WH. Immunolocalization of B-50 (GAP-43) in the mouse olfactory bulb: predominant presence in preterminal axons. J Neurocytol. 1992;21(12):853–869.
   Google Scholar
• Benowitz LI, Apostolides PJ, Perrone-Bizzozero N, Finklestein SP, Zwiers H. Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J Neurosci. 1988;8(1):339–352.
   Web of Science ®Google Scholar
• Bendotti C, Servadio A, Samanin R. Distribution of GAP-43 mRNA in the brain stem of adult rats as evidenced by in situ hybridization: localization within monoaminergic neurons. J Neurosci. 1991;11(3):600–607.
   Web of Science ®Google Scholar
• Kruger L, Bendotti C, Rivolta R, Samanin R. Distribution of GAP-43 mRNA in the adult rat brain. J Comp Neurol. 1993;333(3):417–434.
   Web of Science ®Google Scholar
• McKinney M, Kent C. Differential expression of GAP-43 mRNA in adult central cholinergic neuronal populations. Brain Res Mol Brain Res. 1994;23(3):213–220.
   Google Scholar
• Berg A, Zelano J, Stephan A, et al. Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3. Exp Neurol. 2012;237(1):8–17.
   Web of Science ®Google Scholar
• Gordon T, You S, Cassar SL, Tetzlaff W. Reduced expression of regeneration associated genes in chronically axotomized facial motoneurons. Exp Neurol. 2015;264:26–32.
   PubMed Web of Science ®Google Scholar
• Curtis R, Averill S, Priestley JV, Wilkin GP. The distribution of GAP-43 in normal rat spinal cord. J Neurocytol. 1993;22(1):39–50.
   Google Scholar
• Kapfhammer JP, Schwab ME. Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity? J Comp Neurol. 1994;340(2):194–206.
   Web of Science ®Google Scholar
• DiFiglia M, Roberts RC, Benowitz LI. Immunoreactive GAP-43 in the neuropil of adult rat neostriatum: localization in unmyelinated fibers, axon terminals, and dendritic spines. J Comp Neurol. 1990;302(4):992–1001.
   Web of Science ®Google Scholar
• Carriel V, Garzon I, Campos A, Cornelissen M, Alaminos M. Differential expression of GAP-43 and neurofilament during peripheral nerve regeneration through bio-artificial conduits. J Tissue Eng Regen Med. July 31, 2014. [Epub ahead of print.]
   Google Scholar
• He Q, Dent EW, Meiri KF. Modulation of actin filament behavior by GAP-43 (neuromodulin) is dependent on the phosphorylation status of serine 41, the protein kinase C site. J Neurosci. 1997;17(10):3515–3524.
   PubMed Web of Science ®Google Scholar
• Frey D, Laux T, Xu L, Schneider C, Caroni P. Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J Cell Biol. 2000;149(7):1443–1454.
   Web of Science ®Google Scholar
• Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P. GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol. 2000;149(7):1455–1472.
   Web of Science ®Google Scholar
• Grasselli G, Mandolesi G, Strata P, Cesare P. Impaired sprouting and axonal atrophy in cerebellar climbing fibres following in vivo silencing of the growth-associated protein GAP-43. PLoS One. 2011;6(6):e20791.
   Web of Science ®Google Scholar
• Onodera N, Kakehata A, Araki I. Differential expression of GAP-43 protein in the rostral brain neurons of early chick embryos. Tohoku J Exp Med. 2013;231(4):293–298.
   Web of Science ®Google Scholar
• Console-Bram LM, Fitzpatrick-McElligott SG, McElligott JG. Distribution of GAP-43 mRNA in the immature and adult cerebellum: a role for GAP-43 in cerebellar development and neuroplasticity. Brain Res Dev Brain Res. 1996;95(1):97–106.
   Google Scholar
• Horvath M, Forster CR, Illing RB. Postnatal development of GAP-43 immunoreactivity in the auditory brainstem of the rat. J Comp Neurol. 1997;382(1):104–115.
   Web of Science ®Google Scholar
• Sheu FS, Kasamatsu T, Routtenberg A. Protein kinase C activity and substrate (F1/GAP-43) phosphorylation in developing cat visual cortex. Brain Res. 1990;524(1):144–148.
   Web of Science ®Google Scholar
• Morita S, Miyata S. Synaptic localization of growth-associated protein 43 in cultured hippocampal neurons during synaptogenesis. Cell Biochem Funct. 2013;31(5):400–411.
   Web of Science ®Google Scholar
• Kapfhammer JP, Christ F, Schwab ME. The expression of GAP-43 and synaptophysin in the developing rat retina. Brain Res Dev Brain Res. 1994;80(1–2):251–260.
   Google Scholar
• Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell. 1995;80(3):445–452.
   PubMed Web of Science ®Google Scholar
• Burry RW, Lah JJ, Hayes DM. Redistribution of GAP-43 during growth cone development in vitro; immunocytochemical studies. J Neurocytol. 1991;20(2):133–144.
   Google Scholar
• Holtmaat AJ, Dijkhuizen PA, Oestreicher AB, et al. Directed expression of the growth-associated protein B-50/GAP-43 to olfactory neurons in transgenic mice results in changes in axon morphology and extraglomerular fiber growth. J Neurosci. 1995;15(12):7953–7965.
   Web of Science ®Google Scholar
• Cantallops I, Routtenberg A. Activity-dependent regulation of axonal growth: posttranscriptional control of the GAP-43 gene by the NMDA receptor in developing hippocampus. J Neurobiol. 1999;41(2):208–220.
   PubMedGoogle Scholar
• Irwin N, Chao S, Goritchenko L, et al. Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19. Proc Natl Acad Sci U S A. 2002;99(19):12427–12431.
   Web of Science ®Google Scholar
• Costello B, Meymandi A, Freeman JA. Factors influencing GAP-43 gene expression in PC12 pheochromocytoma cells. J Neurosci. 1990;10(4):1398–1406.
   Web of Science ®Google Scholar
• Neve RL, Ivins KJ, Benowitz LI, During MJ, Geller AI. Molecular analysis of the function of the neuronal growth-associated protein GAP-43 by genetic intervention. Mol Neurobiol. 1991;5(2–4):131–141.
   Web of Science ®Google Scholar
• Meiri KF, Saffell JL, Walsh FS, Doherty P. Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci. 1998;18(24):10429–10437.
   PubMed Web of Science ®Google Scholar
• Patterson SI, Skene JH. A shift in protein S-palmitoylation, with persistence of growth-associated substrates, marks a critical period for synaptic plasticity in developing brain. J Neurobiol. 1999;39(3):423–437.
   Google Scholar
• Strittmatter SM, Valenzuela D, Vartanian T, Sudo Y, Zuber MX, Fishman MC. Growth cone transduction: Go and GAP-43. J Cell Sci Suppl. 1991;15:27–33.
   Google Scholar
• Strittmatter SM, Igarashi M, Fishman MC. GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J Neurosci. 1994;14(9):5503–5513.
   Web of Science ®Google Scholar
• Strittmatter SM, Cannon SC, Ross EM, Higashijima T, Fishman MC. GAP-43 augments G protein-coupled receptor transduction in Xenopus laevis oocytes. Proc Natl Acad Sci U S A. 1993;90(11):5327–5331.
   PubMed Web of Science ®Google Scholar
• Caroni P, Aigner L, Schneider C. Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction. J Cell Biol. 1997;136(3):679–692.
   Web of Science ®Google Scholar
• Gispen WH, Boonstra J, De Graan PN, et al. B-50/GAP-43 in neuronal development and repair. Restor Neurol Neurosci. 1990;1(3):237–244.
   Google Scholar
• Woolf CJ, Reynolds ML, Molander C, O’Brien C, Lindsay RM, Benowitz LI. The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience. 1990;34(2):465–478.
   Web of Science ®Google Scholar
• Allegra Mascaro AL, Cesare P, Sacconi L, et al. In vivo single branch axotomy induces GAP-43-dependent sprouting and synaptic remodeling in cerebellar cortex. Proc Natl Acad Sci U S A. 2013;110(26):10824–10829.
   Web of Science ®Google Scholar
• Verhaagen J, Oestreicher AB, Grillo M, Khew-Goodall YS, Gispen WH, Margolis FL. Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J Neurosci Res. 1990;26(1):31–44.
   Web of Science ®Google Scholar
• Baekelandt V, Arckens L, Annaert W, Eysel UT, Orban GA, Vandesande F. Alterations in GAP-43 and synapsin immunoreactivity provide evidence for synaptic reorganization in adult cat dorsal lateral geniculate nucleus following retinal lesions. Eur J Neurosci. 1994;6(5):754–765.
   Web of Science ®Google Scholar
• Alonso G, Ridet JL, Oestreicher AB, Gispen WH, Privat A. B-50 (GAP-43) immunoreactivity is rarely detected within intact catecholaminergic and serotonergic axons innervating the brain and spinal cord of the adult rat, but is associated with these axons following lesion. Exp Neurol. 1995;134(1):35–48.
   Web of Science ®Google Scholar
• Illing RB, Horvath M. Re-emergence of GAP-43 in cochlear nucleus and superior olive following cochlear ablation in the rat. Neurosci Lett. 1995;194(1–2):9–12.
   Web of Science ®Google Scholar
• Cheng MY, Wang EH, Woodson WJ, et al. Optogenetic neuronal stimulation promotes functional recovery after stroke. Proc Natl Acad Sci U S A. 2014;111(35):12913–12918.
   Web of Science ®Google Scholar
• Dunn-Meynell AA, Benowitz LI, Levin BE. Vibrissectomy induced changes in GAP-43 immunoreactivity in the adult rat barrel cortex. J Comp Neurol. 1992;315(2):160–170.
   Web of Science ®Google Scholar
• Levin BE, Dunn-Meynell A. Regulation of growth-associated protein 43 (GAP-43) messenger RNA associated with plastic change in the adult rat barrel receptor complex. Brain Res Mol Brain Res. 1993;18(1–2):59–70.
   Google Scholar
• Lin LH, Bock S, Carpenter K, Rose M, Norden JJ. Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. Brain Res Mol Brain Res. 1992;14(1–2):147–153.
   Google Scholar
• Cantallops I, Routtenberg A. Rapid induction by kainic acid of both axonal growth and F1/GAP-43 protein in the adult rat hippocampal granule cells. J Comp Neurol. 1996;366(2):303–319.
   Web of Science ®Google Scholar
• Akers RF, Routtenberg A. Protein kinase C phosphorylates a 47 Mr protein (F1) directly related to synaptic plasticity. Brain Res. 1985;334(1):147–151.
   Web of Science ®Google Scholar
• Routtenberg A, Lovinger DM. Selective increase in phosphorylation of a 47-kDa protein (F1) directly related to long-term potentiation. Behav Neural Biol. 1985;43(1):3–11.
   Google Scholar
• Son H, Davis PJ, Carpenter DO. Time course and involvement of protein kinase C-mediated phosphorylation of F1/GAP-43 in area CA3 after mossy fiber stimulation. Cell Mol Neurobiol. 1997;17(2):171–194.
   Web of Science ®Google Scholar
• Lovinger DM, Akers RF, Nelson RB, Barnes CA, McNaughton BL, Routtenberg A. A selective increase in phosporylation of protein F1, a protein kinase C substrate, directly related to three day growth of long term synaptic enhancement. Brain Res. 1985;343(1):137–143.
   Web of Science ®Google Scholar
• Namgung U, Matsuyama S, Routtenberg A. Long-term potentiation activates the GAP-43 promoter: selective participation of hippocampal mossy cells. Proc Natl Acad Sci U S A. 1997;94(21):11675–11680.
   Web of Science ®Google Scholar
• Ramakers GM, De Graan PN, Urban IJ, et al. Temporal differences in the phosphorylation state of pre- and postsynaptic protein kinase C substrates B-50/GAP-43 and neurogranin during long-term potentiation. J Biol Chem. 1995;270(23):13892–13898.
   Web of Science ®Google Scholar
• Ramakers GM, McNamara RK, Lenox RH, De Graan PN. Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanine-rich C kinase substrate and growth-associated protein-43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J Neurochem. 1999;73(5):2175–2183.
   Web of Science ®Google Scholar
• Meberg PJ, Valcourt EG, Routtenberg A. Protein F1/GAP-43 and PKC gene expression patterns in hippocampus are altered 1–2 h after LTP. Brain Res Mol Brain Res. 1995;34(2):343–346.
   Google Scholar
• Meberg PJ, Barnes CA, McNaughton BL, Routtenberg A. Protein kinase C and F1/GAP-43 gene expression in hippocampus inversely related to synaptic enhancement lasting 3 days. Proc Natl Acad Sci U S A. 1993;90(24):12050–12054.
   Web of Science ®Google Scholar
• Fedorov NB, Pasinelli P, Oestreicher AB, DeGraan PN, Reymann KG. Antibodies to postsynaptic PKC substrate neurogranin prevent long-term potentiation in hippocampal CA1 neurons. Eur J Neurosci. 1995;7(4):819–822.
   Web of Science ®Google Scholar
• Hulo S, Alberi S, Laux T, Muller D, Caroni P. A point mutant of GAP-43 induces enhanced short-term and long-term hippocampal plasticity. Eur J Neurosci. 2002;15(12):1976–1982.
   Web of Science ®Google Scholar
• Luo Y, Vallano ML. Arachidonic acid, but not sodium nitroprusside, stimulates presynaptic protein kinase C and phosphorylation of GAP-43 in rat hippocampal slices and synaptosomes. J Neurochem. 1995;64(4):1808–1818.
   Web of Science ®Google Scholar
• Rekart JL, Meiri K, Routtenberg A. Hippocampal-dependent memory is impaired in heterozygous GAP-43 knockout mice. Hippocampus. 2005;15(1):1–7.
   PubMed Web of Science ®Google Scholar
• Young E, Cesena T, Meiri KF, Perrone-Bizzozero NI. Changes in protein kinase C (PKC) activity, isozyme translocation, and GAP-43 phosphorylation in the rat hippocampal formation after a single-trial contextual fear conditioning paradigm. Hippocampus. 2002;12(4):457–464.
   Web of Science ®Google Scholar
• Aigner L, Arber S, Kapfhammer JP, et al. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell. 1995;83(2):269–278.
   Web of Science ®Google Scholar
• Holahan M, Routtenberg A. The protein kinase C phosphorylation site on GAP-43 differentially regulates information storage. Hippocampus. 2008;18(11):1099–1102.
   Web of Science ®Google Scholar
• Holahan MR, Honegger KS, Tabatadze N, Routtenberg A. GAP-43 gene expression regulates information storage. Learn Mem. 2007;14(6):407–415.
   Web of Science ®Google Scholar
• Maviel T, Durkin TP, Menzaghi F, Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science. 2004;305(5680):96–99.
   PubMed Web of Science ®Google Scholar
• Lerch JP, Yiu AP, Martinez-Canabal A, et al. Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage. 2011;54(3):2086–2095.
   Web of Science ®Google Scholar
• Narayana PA, Herrera JJ, Bockhorst KH, et al. Chronic cocaine administration causes extensive white matter damage in brain: diffusion tensor imaging and immunohistochemistry studies. Psychiatry Res. 2014;221(3):220–230.
   PubMed Web of Science ®Google Scholar
• Gnegy ME, Hong P, Ferrell ST. Phosphorylation of neuromodulin in rat striatum after acute and repeated, intermittent amphetamine. Brain Res Mol Brain Res. 1993;20(4):289–298.
   Google Scholar
• Park YH, Kantor L, Wang KK, Gnegy ME. Repeated, intermittent treatment with amphetamine induces neurite outgrowth in rat pheochromocytoma cells (PC12 cells). Brain Res. 2002;951(1):43–52.
   Web of Science ®Google Scholar
• Grignaschi G, Burbassi S, Zennaro E, Bendotti C, Cervo L. A single high dose of cocaine induces behavioural sensitization and modifies mRNA encoding GluR1 and GAP-43 in rats. Eur J Neurosci. 2004;20(10):2833–2837.
   Web of Science ®Google Scholar
• Kim HJ, Choi KM, Ku BM, et al. Acute ethanol administration decreases GAP-43 and phosphorylated-GAP-43 in the rat hippocampus. Brain Res. 2006;1112(1):16–25.
   Google Scholar