Cell Type- and Region-Specific Expression of Protein Kinase C-Substrate mRNAs in the Cerebellum of the Macaque Monkey

Journal of Comparative Neurology

Volumn 467, Issue 2, 2003, Pages 135-149

  Higo, Noriyuki ^a   Oishi, Takao ^a,b   Yamashita, Akiko ^c   Matsuda, Keiji ^a   Hayashi, Motoharu ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

GAP 43; Growth associated protein; Inferior olive; MARCKS; Neurogranin; Vestibulocerebellum

Indexed keywords

MARCKS PROTEIN; MESSENGER RNA; NEUROGRANIN; NEUROMODULIN; PROTEIN KINASE C;

AGE DISTRIBUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL FUNCTION; CELL SPECIFICITY; CELL TYPE; CEREBELLUM; CEREBELLUM CORTEX; CEREBELLUM FLOCCULUS; CEREBELLUM NUCLEUS; CEREBELLUM VERMIS; CONTROLLED STUDY; DORSAL PARAFLOCCULUS; ENZYME LOCALIZATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GRANULE CELL; HISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFERIOR OLIVE; MACACA; MOLECULAR BIOLOGY; MONKEY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RADIOACTIVITY; SIGNAL TRANSDUCTION;

AGE FACTORS; ANIMALS; BRAIN MAPPING; CALMODULIN-BINDING PROTEINS; CEREBELLUM; GAP-43 PROTEIN; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACACA; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEUROGRANIN; NEURONS; PROTEIN KINASE C; PROTEINS; RNA, MESSENGER; TISSUE DISTRIBUTION;

EID: 0242266912     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10850     Document Type: Article

References (112)

1. Aderem A. 1992. Signal transduction and the actin cytoskeleton: the roles of MARCKS and profilin. Trends Biochem Sci 17:438-443.
2. Aderem AA, Albert KA, Keum MM, Wang JKT, Greengard P, Cohn ZA. 1988. Stimulus-dependent myristoylation of a major substrate for protein kinase C. Nature 332:362-364.
3. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner H-R, Caroni P. 1995. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
4. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J Comp Neurol 145:353-397.
5. Anderson BJ, Alcantara AA, Greenough WT. 1996. Motor-skill learning: changes in synaptic organization of the rat cerebellar cortex. Neurobiol Learn Mem 66:221-229.
6. Barmack NH, Baughman RW, Eckenstein FP. 1992. Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J Comp Neurol 317:233-249.
7. Barmack NH, Qian Z, Yoshimura J. 2000. Regional and cellular distribution of protein kinase C in rat cerebellar Purkinje cells. J Comp Neurol 427:235-254.
8. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M. 1992. Cerebellar nuclei and the nucleocortical projections in the rat: retro-grade tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74-84.
9. Baudier J, Deloulme JC, Van Dorsselaer A, Black D, Matthes HW. 1991. Purification and characterization of a brain-specific protein kinase C substrate, neurograinin (p17). Identification of a consensus amno acid sequence between neurogranin and neuromodulin (GAP43) that corresponds to the protein kinase C phosphorylation site and the calmodulin-binding domain. J Biol Chem 266:229-237.
10. Bendotti C, Servadio A, Samanin R. 1991. Distribution of GAP-43 mRNA in the brain stem of adult rats as evidenced by in situ hybridization: localization within monoaminergic neurons. J Neurosci 11:600-607.
11. Bendotti C, Baldessari S, Pende M, Southgate T, Guglielmetti F, Samanin R. 1997. Relationship between GAP-43 expression in the dentate gyrus and synaptic reorganization of hippocampal mossy fibres in rats treated with kainic acid. Eur J Neurosci 9:93-101.
12. Benowitz LI, Apostolides PJ, Perrone-Bizzozero N, Finklestein SP, Zwiers H. 1988. Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J Neurosci 8:339-352.
13. Benowitz LI, Perrone-Bizzozero NI, Finklestein SP, Bird ED. 1989. Localization of the growth-associated phosphoprotein GAP-43 (B-50, F1) in the human cerebral cortex. J Neurosci 9:990-995.
14. Bogdanovic N, Davidsson P, Volkmann I, Winblad B, Blennow K. 2000. Growth-associated protein GAP-43 in the frontal cortex and in the hippocampus in Alzheimer's disease: an immunohistochemical and quantitative study. J Neural Transm 107:463-478.
15. Brandt SJ, Niedel JE, Bell RM, Young WS III. 1987. Distinct patterns of expression of different protein kinase C mRNAs in rat tissues. Cell 49:57-63.
16. Callahan LM, Selski DJ, Martzen MR, Cheetham JE, Coleman PD. 1994. Preliminary evidence: decreased GAP-43 message in tangle-bearing neurons relative to adjacent tangle-free neurons in Alzheimer's disease parahippocampal gyrus. Neurobiol Aging 15:381-386.
17. 2+-calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci 22:12-16.
18. Chang JW, Schumacher E, Coulter PM Jr, Vinters HV, Watson JB. 1997. Dendritic translocation of RC3/neurogranin mRNA in normal aging, Alzheimer disease and fronto-temporal dementia. J Neuropathol Exp Neurol 56:1105-1118.
19. Cheetham JE, Martzen MR, Kazee AM, Coleman PD. 1996. Gap-43 message levels in anterior cerebellum in Alzheimer's disease. Brain Res Mol Brain Res 36:145-151.
20. Chen SJ, Sweatt JD, Klann E. 1997. Enhanced phosphorylation of the postsynaptic protein kinase C substrate RC3/neurogranin during long-term potentiation. Brain Res 749:181-187.
21. Chong MS, Reynold ML, Irwin N, Coggeshall RE, Emson PC, Benowitz LI, Woolf CJ. 1994. GAP-43 Expression in primary sensory neurons following central axotomy. J Neurosci 14:4375-4385.
22. Console-Bram LM, Fitzpatrick-McElligott SG, McElligott JG. 1996. 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 95:97-106.
23. Davidsson P, Blennow K. 1998. Neurochemical dissection of synaptic pathology in Alzheimer's disease. Int Psychogeriatr 10:11-23.
24. de la Monte SM, Federoff HJ, Ng S-C, Grabczyk E, Fishman MC. 1989. GAP-43 gene expression during development: persistence in a distinctive set of neurons in the mature central nervous system. Dev Brain Res 46:161-168.
25. de la Monte SM, Ng SC, Hsu DW. 1995. Aberrant GAP-43 gene expression in Alzheimer's disease. Am J Pathol 147:934-946.
26. Dino MR, Willard FH, Mugnaini E. 1999. Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytol 28:99-123.
27. Fedorov NB, Pasinelli P, Oestreicher AB, DeGraan PN, Reymann KG. 1995. Antibodies to postsynaptic PKC substrate neurogranin prevent long-term potentiation in hippocampal CA1 neurons. Eur J Neurosci 7:819-822.
28. Fortin M, Marchand R, Parent A. 1998. Calcium-binding proteins in primate cerebellum. Neurosci Res 30:155-168.
29. Fredette BJ, Mugnaini E. 1991. The GABAergic cerebello-olivary projection in the rat. Anat Embryol (Berl) 184:225-243.
30. Garcia MM, Harlan RE. 1997. Protein kinase C in central vestibular, cerebellar, and precerebeller pathways of the rat. J Comp Neurol 385:26-42.
31. Gerendasy DD, Sutcliffe JG. 1997. RC3/neurogranin, a postsynaptic calpacitin for setting the response threshold to calcium influxes. Mol Neurobiol 15:131-163.
32. 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.
33. Harding DI, Greensmith L, Mason M, Anderson PN, Vrbova G. 1999. Overexpression of GAP-43 induces prolonged sprouting and causes death of adult motoneurons. Eur J Neurosci 11:2237-2242.
34. He Q, Dent EW, Meiri KF. 1997. 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 17:3515-3524.
35. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 1998. Gene expression of growth-associated proteins, GAP-43 and SCG10, in the hippocampal formation of the macaque monkey: non-radioactive in situ hybridization study. Hippocampus 8:533-547.
36. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 1999. Quantitative non-radioactive in situ hybridization study of GAP-43 and SCG10 mRNAs in the cerebral cortex of adult and infant macaque monkeys. Cereb Cortex 9:317-331.
37. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2000a. Expression of GAP-43 and SCG10 mRNAs in lateral geniculate nucleus of normal and monocularly deprived macaque monkeys. J Neurosci 20:6030-6038.
38. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2000b. Expression of MARCKS mRNA in the hippocampus and cerebral neocortex of infant and adult macaque monkeys. COE International Symposium (Development and Aging of Primates) Abstract 1:37.
39. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2001a. Expression of protein kinase C substrate (GAP-43, MARCKS and neurogranin) mRNAs in the cerebellum of macaque monkey. Soc Neurosci Abstr 27:1360.
40. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2001b. Gene expression of protein kinase C-substrates in the cerebellum of macaque monkey. Neurosci Res Suppl 25.
41. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2002a. Expression of MARCKS mRNA in lateral geniculate nucleus and visual cortex of normal and monocularly deprived macaque monkeys. Vis Neurosci 19:633-643.
42. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2002b. Expression of neurogranin mRNA in area 17 of infant and adult macaque monkeys. Soc Neurosci Abstr 28:530.512.
43. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2002c. Gene expression of neurogranin in the cerebral cortex of macaque monkey. Neurosci Res Suppl 26.
44. Higo N, Oishi T, Yamashita A, Matsuda K, Hayashi M. 2002d. Northern blot and in situ hybridization analyses of MARCKS mRNA expression in the cerebral cortex of the macaque monkey. Cereb Cortex 12:552-564.
45. Holtmaat AJGD, Dijkhuizen PA, Oestreicher AB, Romijn HJ, Van der Lugt NMT, Berns A, Margolis FL, Gispen WH, Verhaagen J. 1995. 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 15:7953-7965.
46. Huang FL, Yoshida Y, Nakabayashi H, Young WS III, Huang KP. 1988. Immunocytochemical localization of protein kinase C isozymes in rat brain. J Neurosci 8:4734-4744.
47. Jacobs KM, Neve RL, Donoghue JP. 1993. Neocortex and hippocampus contain distinct distributions of calcium-calmodulin protein kinase II and GAP43 mRNA. J Comp Neurol 336:151-160.
48. Jacobson RD, Virag I, Skene JHP. 1986. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J Neurosci 6:1843-1855.
49. Kaczmarek LK. 1987. The role of protein kinase C in the regulation of ion channels and neurotransmitter release. Trends Neurosci 10:30-34.
50. Kalyuzhny AE, Wessendorf MW. 1998. Relationship of mu- and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J Comp Neurol 392:528-547.
51. Kleim JA, Swain RA, Czerlanis CM, Kelly JL, Pipitone MA, Greenough WT. 1997. Learning-dependent dendritic hypertrophy of cerebellar stellate cells: plasticity of local circuit neurons. Neurobiol Learn Mem 67:29-33.
52. Kleim JA, Pipitone MA, Czerlanis C, Greenough WT. 1998a. Structural stability within the lateral cerebellar nucleus of the rat following complex motor learning. Neurobiol Learn Mem 69:290-306.
53. Kleim JA, Swain RA, Armstrong KA, Napper RM, Jones TA, Greenough WT. 1998b. Selective synaptic plasticity within the cerebellar cortex following complex motor skill learning. Neurobiol Learn Mem 69:274-289.
54. Kruger L, Bendotti C, Rivolta R, Samanin R. 1992. GAP-43 mRNA localization in the rat hippocampus CA3 field. Mol Brain Res 13:267-272.
55. Kruger L, Bendotti C, Rivolta R, Samanin R. 1993. Distribution of GAP-43 mRNA in the adult rat brain. J Comp Neurol 333:417-434.
56. Leahy JC, Luo Y, Kent CS, Meiri KF, Vallano ML. 1993. Demonstration of presynaptic protein kinase C activation following long-term potentiation in rat hippocampal slices. Neuroscience 52:563-574.
57. Leclerc N, Dore L, Parent A, Hawkes R. 1990. The compartmentalization of the monkey and rat cerebellar cortex: zebrin I and cytochrome oxidase. Brain Res 506:70-78.
58. Levin BE, Dunn-Meynell A. 1993. Regulation of growth-associated protein 43 (GAP-43) messenger RNA associated with plastic change in the adult rat barrel receptor complex. Mol Brain Res 18:59-70.
59. Linda H, Piehl F, Dagerlind A, Verge VMK, Arvidsson U, Chullheim S, Risling M, Ulfhake B, Hokfelt T. 1992. Expression of GAP-43 mRNA in the adult mammalian spinal cord under normal conditions and after different types of lesions, with special reference to motoneurons. Exp Brain Res 941:284-295.
60. Linden DJ, Routtenberg A. 1989. The role of protein kinase C in long-term potentiation: a testable model. Brain Res Rev 14:279-296.
61. Linden DJ, Wong KL, Sheu FS, Routtenberg A. 1988. NMDA receptor blockade prevents the increase in protein kinase C substrate (protein F1) phosphorylation produced by long-term potentiation. Brain Res 458:142-146.
62. Lovinger DM, Akers RF, Nelson RB, Barnes CA, McNaughton BL, Routtenberg A. 1985. 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 343:137-143.
63. Madigan JC, Carpenter MB. 1971. Cerebellum of the rhesus monkey: atlas of lobules, laminae, and folia, in sections. Baltimore: University Park Press.
64. Masliah E, Mallory M, Hansen L, Alford M, Albright T, DeTeresa R, Terry R, Baudier J, Saitoh T. 1991. Patterns of aberrant sprouting in Alzheimer's disease. Neuron 6:729-739.
65. McIntosh H, Daw N, Parkinson D. 1990. GAP-43 in the cat visual cortex during postnatal development. Vis Neurosci 4:585-593.
66. McNamara RK, Lenox RH. 1997. Comparative distribution of myristoylated alanine-rich C kinase substrate (MARCKS) and F1/GAP-43 gene expression in the adult rat brain. J Comp Neurol 379:48-71.
67. McNamara RK, Lenox RH. 1998. Distribution of the protein kinase C substrates MARCKS and MRP in the postnatal developing rat brain. J Comp Neurol 397:337-356.
68. McNamara RK, Lenox RH. 2000. Differential regulation of primary protein kinase C substrate (MARCKS, MLP, GAP-43, RC3) mRNAs in the hippocampus during kainic acid-induced seizures and synaptic reorganization. J Neurosci Res 62:416-426.
69. McNamara RK, Stumpo DJ, Morel LM, Lewis MH, Wakeland EK, Blackshear PJ, Lenox RH. 1998. Effect of reduced myristoylated alanine-rich C kinase substrate expression on hippocampal mossy fiber development and spatial learning in mutant mice: transgenic rescue and interactions with gene background. Proc Natl Acad Sci U S A 95:14517-14522.
70. McNamara RK, Jiang Y, Streit WJ, Lenox RH. 2000. Facial motor neuron regeneration induces a unique spatial and temporal pattern of myristoylated alanine-rich C kinase substrate expression. Neuroscience 97: 581-589.
71. Meiri KF, Pfenninger KH, Willard MB. 1986. Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci U S A 83:3537-3541.
72. Meiri KF, Willard M, Johnson MI. 1988. Distribution and phosphorylation of the growth-associated protein GAP-43 in regenerating sympathetic neurons in culture. J Neurosci 8:2571-2581.
73. Mower GD, Rosen KM. 1993. Developmental and environmental changes in GAP-43 gene expression in cat visual cortex. Mol Brain Res 20:254-258.
74. Mufson EJ, Higgins GA, Kordower JH. 1991. Nerve growth factor receptor immunoreactivity in the new world monkey (Cebus apella) and human cerebellum. J Comp Neurol 308:555-575.
75. Mugnaini E, Floris A. 1994. The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J Comp Neurol 339:174-180.
76. Nelson RB, Routtenberg A. 1985. Characterization of protein F1 (47 kDa, 4.5 pI): a kinase C substrate directly related to neural plasticity. Exp Neurol 89:213-224.
77. Neve RL, Bear MF. 1989. Visual experience regulates gene expression in the developing striate cortex. Proc Natl Acad Sci U S A 86:4781-4784.
78. Neve RL, Perrone-Bizzozero NI, Finkelestein S, Zwiers H, Bird E, Kurnit DM, Benowitz LI. 1987. The neuronal growth-associated protein GAP-43 (B-50, F1): neuronal specificity, developmental regulation, and regional distribution of the human and rat mRNAs. Mol Brain Res 2:177-183.
79. Nishizuka Y. 1986. Studies and perspectives of protein kinase C. Science 233:305-312.
80. Nishizuka Y. 1995. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9:484-496.
81. Nunzi MG, Mugnaini E. 2000. Unipolar brush cell axons form a large system of intrinsic mossy fibers in the postnatal vestibulocerebellum. J Comp Neurol 422:55-65.
82. Nunzi MG, Birnstiel S, Bhattacharyya BJ, Slater NT, Mugnaini E. 2001. Unipolar brush cells form a glutamatergic projection system within the mouse cerebellar cortex. J Comp Neurol 434:329-341.
83. Oehrlein SA, Parker PJ, Herget T. 1996. Phosphorylation of GAP-43 (growth-associated protein of 43 kDa) by conventional, novel and atypical isotypes of the protein kinase C gene family: differences between oligopeptide and polypeptide phosphorylation. Biochem J 317(Pt 1): 219-224.
84. Oishi T, Higo N, Umino Y, Matsuda K, Hayashi M. 1998. Development of GAP-43 mRNA in the macaque cerebral cortex. Dev Brain Res 109:87-97.
85. Ouimet CC, Wang JK, Walaas SI, Albert KA, Greengard P. 1990. Localization of the MARCKS (87 kDa) protein, a major specific substrate for protein kinase C, in rat brain. J Neurosci 10:1683-1698.
86. Pak JH, Huang FL, Li J, Balschun D, Reymann KG, Chiang C, Westphal H, Huang KP. 2000. Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: a study with knockout mice. Proc Natl Acad Sci U S A 97:11232-11237.
87. Patal J, Klingman D. 1987. Purification and characterization of an Mr 87,000 protein kinase C substrate from rat brain. J Biol Chem 262: 16686-16691.
88. Ramakers GM, De Graan PN, Urban IJ, Kraay D, Tang T, Pasinelli P, Oestreicher AB, Gispen WH. 1995. 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 270:13892-13898.
89. Ramakers GM, McNamara RK, Lenox RH, De Graan PN. 1999. 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 73:2175-2183.
90. Ramakers GM, Heinen K, Gispen WH, de Graan PN. 2000a. Long term depression in the CA1 field is associated with a transient decrease in pre- and postsynaptic PKC substrate phosphorylation. J Biol Chem 275:28682-28687.
91. Ramakers GM, Pasinelli P, van Beest M, van der Slot A, Gispen WH, De Graan PN. 2000b. Activation of pre- and postsynaptic protein kinase C during tetraethylammonium-induced long-term potentiation in the CA1 field of the hippocampus. Neurosci Lett 286:53-56.
92. Represa A, Deloulme JC, Sensenbrenner M, Ben-Ari Y, Baudier J. 1990. Neurogranin: immunocytochemical localization of a brain-specific protein kinase C substrate. J Neurosci 10:3782-3792.
93. Rosenthal A, Chan SY, Henzel W, Haskell C, Kuang WJ, Chen E, Wilcox JN, Ullrich A, Goeddel DV, Routtenberg A. 1987. Primary structure and mRNA localization of protein F1, a growth-related protein kinase C substrate associated with synaptic plasticity. EMBO J 6:3641-3646.
94. Routtenberg A, Lovinger DM, Steward O. 1985. Selective increase in phosphorylation of a 47-kDa protein (F1) directly related to long-term potentiation. Behav Neural Biol 43:3-11.
95. 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 U S A 97:7657-7662.
96. Ryan M, Starkey M, Faull R, Emson P, Bahn S. 2001. Indexing-based differential display: studies on post-mortem Alzheimer's brains. Brain Res Mol Brain Res 88:199-202.
97. Saito N, Itouji A, Totani Y, Osawa I, Koide H, Fujisawa N, Ogita K, Tanaka C. 1993. Cellular and intracellular localization of epsilon-subspecies of protein kinase C in the rat brain; presynaptic localization of the epsilon-subspecies. Brain Res 607:241-248.
98. Saitoh T, Horsburgh K, Masliah E. 1993. Hyperactivation of signal transduction systems in Alzheimer's disease. Ann N Y Acad Sci 695:34-41.
99. Schwaller B, Buchwald P, Blumcke I, Celio MR, Hunziker W. 1993. Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639-648.
100. Sheu FS, Marais RM, Parker PJ, Bazan NG, Routtenberg A. 1990. Neuron-specific protein F1/GAP-43 shows substrate specificity for the beta sub-type of protein kinase C. Biochem Biophys Res Commun 171:1236-1243.
101. Skene JHP, Jacobson RD, Snipes GJ, McGuire CB, Norden JJ, Freeman JA. 1986. A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 233:783-786.
102. Swierczynski SL, Blackshear PJ. 1995. Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. Mutational analysis provides evidence for complex interactions. J Biol Chem 270:13436-13445.
103. Tanaka C, Nishizuka Y. 1994. The protein kinase C family for neuronal signaling. Annu Rev Neurosci 17:551-567.
104. Tanigawa H, Fujita I, Kato M, Ojima H. 1998. Distribution, morphology, and gamma-aminobutyric acid immunoreactivity of horizontally projecting neurons in the macaque inferior temporal cortex. J Comp Neurol 401:129-143.
105. Tetzlaff W, Alexander SW, Miller FD, Bisby MA. 1991. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11:2528-2544.
106. Van der Zee CEEM, Nielander HB, Vos JP, Lopes da Silva S, Verhaagen J, Oestreicher AB, Schrama LH, Schotman P, Gispen WH. 1989. Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting. J Neurosci 9:3505-3512.
107. Voogd J, Gerrits NM, Ruigrok TJ. 1996. Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553-579.
108. Watson JB, Battenberg EF, Wong KK, Bloom FE, Sutcliffe JG. 1990. Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein. J Neurosci Res 26:397-408.
109. Watson JB, Sutcliffe JG, Fisher RS. 1992. Localization of the protein kinase C phosphorylation/calmodulin-binding substrate RC3 in dendritic spines of neostriatal neurons. Proc Natl Acad Sci U S A 89:8581-8585.
110. Yamashita A, Hayashi M. 1996. Ontogeny of GABA-immunoreactive cells in the primate cerebellar cortex: comparison with somatostatin-immunoreactivity. Anat Embryol (Berl) 194:215-222.
111. Yao GL, Kiyama H, Tohyama M. 1993. Distribution of GAP-43(B50/F1) mRNA in the adult rat brain by in situ hybridization using an alkaline phosphatase labeled probe. Mol Brain Res 18:1-16.
112. Young WS III. 1988. Expression of three (and a putative four) protein kinase C genes in brains of rat and rabbit. J Chem Neuroanat 1: 177-194.