Dendritic translocation of RC3/neurogranin mRNA in normal aging, Alzheimer disease and fronto-temporal dementia

Journal of Neuropathology and Experimental Neurology

Volumn 56, Issue 10, 1997, Pages 1105-1118

  Chang, Julia W ^a   Schumacher, Eric ^a   Coulter II, Phillip M ^a   Vinters, Harry V ^a   Watson, Joseph B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer disease; Dendritic targeting; Fronto temporal dementia; Immunocytochemistry; In situ hybridization; MAP 2; RC3 neurogranin

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; NEUROGRANIN;

AGING; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEMENTIA; DENDRITE; HUMAN; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 0030884911     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199710000-00004     Document Type: Article

References (72)

1. Steward O. Targeting of mRNAs to subsynaptic microdomains in dendrites. Curr Opin Neurobiol 1995;5:55-61
2. Steward O, Levy WB. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyms. J Neurosci 1982;2:284-91
3. Steward O. Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat. J Neurosci 1983;3:177-88
4. Steward O, Falk PM. Protein-synthetic machinery at postsynaptic sites during synaptogenesis: A quantitative study of the association between polyribosomes and developing synapses. J Neurosci 1986; 6:412-23
5. Steward O, Reeves TM. Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: Association between polyribosomes and other organelles at the synaptic site. J Neurosci 1988;8:176-84
6. Greenough WT, Hwang HMF, Gorman C. Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc Natl Acad Sci USA 1985;82:4549-52
7. 2+/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 1990; 10:1788-98
8. Silva AJ, Stevens CF, Tonegawa S, Wang Y. Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 1992;257:201-5
9. Lisman JE. The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 1994;17:406-12
10. Garner CC, Tucker RP, Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP-2 in dendrites. Nature 1988; 336:674-77
11. Strong MF, Svedmyr A, Fajdusek DC, Farruto RM. The temporal expression of amyloid precursor protein mRNA in vitro in dissociated hippocampal neuron cultures. Exp Neurol 1990;109:171-79
12. Dugich-Djordjevic MM, Tocco F, Willoughby DA, et al. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron 1992;8:1127-38
13. Furuichi T, Simon-Chazottes D, Fujino I, et al. Widespread expression of inositol 1,4,5-trisphosphate receptor type-1 gene (InsP3R1) in the mouse central nervous system. Recept Chan 1993;1:11-24
14. Lyford FL, Yamagata K, Kaufmann WE, et al. Arc, a growth factor and activity-regulated gene encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995;14:433-45
15. Miyashiro K, Dichter M, Eberwine J. On the nature and differential distribution of mRNAs in hippocampal neurites: Implications for neuronal functioning. Proc Natl Acad Sci 1994;91:10800-10804
16. Watson JB, Coulter II PM, Margulies JE, de Lecea L, Danielson PE, Erlander MG, Sutcliffe JG. G-protein γ7 subunit is selectively expressed in medium-sized neurons and dendrites of the rat neostriatum. J Neurosci Res 1994;39:108-16
17. Tiedge H, Fremeau RT Jr, Weinstock PH, Arancio O, Brosius J. Dendritic location of neural BC1 RNA. Proc Natl Acad Sci USA 1991;10:143-47
18. Tiedge H, Chen W, Brosius J. Primary structure, neural-specific expression, and dendritic location of human BC200 RNA. J Neurosci 1993;13:2382-90
19. Chicurel ME, Terrian DM, Potter H. mRNA at the synapse: Analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J Neurosci 1993;13:4054-64
20. Landry CF, Watson JB, Kashima T, Campagnoni AT. Cellular influences on RNA sorting in neurons and glia: An in situ hybridization histochemical study. Brain Res Mol Brain Res 1994;27:1-11
21. Berry FB, Brown IR. CaM I mRNA is localized to apical dendrites during postnatal development of neurons in the rat brain. J Neurosci Res 1996;43:565-75
22. Watson JB, Sutcliffe JG, Fisher RS. Localization of the protein kinase C phosphorylation/calmodulin-binding substrate RC3 in dendritic spines of neostriatal neurons. Proc Natl Acad Sci USA 1992;89:8581-85
23. Cohen RW, Margulies JE, Coulter PM, Watson JB. Functional consequences of expression of the neuron-specific protein kinase C substrate RC3 (neurogranin) in Xenopus oocytes. Brain Res 1993; 627:147-52
24. Watson JB, Margulies JE, Coulter II PM, Gerendasy DD, Sutcliffe JG, Cohen RW. Functional studies of single-site variants in the calmodulin-binding domain of RC3/neurogranin in Xenopus oocytes. Neurosci Lett 1996;219:183-86
25. Watson JB, Battenberg EF, Wong KK, Bloom FE, Sutcliffe JG. Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein. J Neurosci Res 1990;26:397-408
26. Skene JHP. Axonal growth-associated proteins. Ann Rev Neurosci 1989:12:127-56
27. Gerendasy DD, Herron SR, Wong KK, Watson JB, Sutcliffe JG. Rapid purification, site-directed mutagenesis, and initial characterization of recombinant RC3/neurogranin. J Mol Neurosci 1994;5: 133-47
28. Slemmon JR, Morgan JI, Fullerton SM, Danho W, Hilbush BS, Wengenack TM. Camstatins are peptide antagonists of calmodulin based upon a conserved structural motif in PEP-19, neurogranin, and neuromodulin. J Biol Chem 1996;271:15911-17
29. Klann E, Chen SJ, Sweatt JD. Increased phosphorylation of a 17 kDa protein kinase C substrate (P17) in long-term potentiation. J Neurochem 1992;58:1576-79
30. Ramaker GM, DeGraan PN, Urban IJ, Kraay D, Tang T, Pasinelli P, Oestreic AB, Gispen WH. 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;70:13892-98
31. Lee VM. Disruption of the cytoskeleton in Alzheimer's disease. Curr Opin Neurobiol 1995;5:663-68
32. Cooper PN, Jackson M, Lennox G, Lowe J, Mann DMA. τ, ubiquitin, and αB-crystallin immunohistochemistry define the principal causes of degenerative frontotemporal dementia. Arch Neurol 1995;52:1011-15
33. Frisoni GB, Beltramello A, Geroldi C, Weiss C, Bianchetti A, Trabucchi M. Brain atrophy in frontotemporal dementia. J Neurol Neurosurg Psychiatry 1996;61:157-65
34. Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 1983;132:6-13
35. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Biotechnology 1977/1992;24:104-8
36. Chang JW, Coleman PD, O'Banion, MK. Prostaglandin G/H synthase-2 (cyclooxygenase-2) mRNA expression is decreased in Alzheimer's disease. Neurobiol Aging 1996;17:801-8
37. Khachaturian ZS. Diagnosis of Alzheimer's disease. Arch Neurol 1985;42:1097-1105
38. Mirra SS, Heyman A, McKeel D, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991;41:479-86
39. Mann DMA, South PW, Snowden JS, Neary D. Dementia of frontal lobe type: Neuropathology and immunohistochemistry. J Neurol Neurosurg Psychiatry 1993;56:605-14
40. Masliah E, Terry RD. The role of synaptic proteins in the pathogenesis of disorders of the central nervous system. Brain Path 1993; 3:77-85
41. Masliah E, Mallory M, Hansen L, DeTeresa R, Terry RD. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 1993;43:192-97
42. Callahan LM, Coleman PD. Neurons bearing neurofibrillary tangles are responsible for selected synaptic deficits in Alzheimer's disease. Neurobiol Aging 1995;16:311-14
43. Braak H, Braak E. Neuropil threads occur in dendrites of tangle-bearing nerve cells. Neuropath App Neurobiol 1988;14:39-44
44. Yamaguchi H, Nakazato Y, Shoji M, Ihara Y, Hirai S. Ultrastructure of the neuropil threads in the Alzheimer brain: Their dendritic origin and accumulation in the senile plaques. Acta Neuropathol (Berlin) 1990;80:368-74
45. Masliah E, Ellisman M, Carragher B, Mallory M, Young S, Hansen L, DeTeresa R, Terry RD. Three-dimensional analysis of the relationship between synaptic pathology and neuropil threads in Alzheimer's disease. J Neuropath Exp Neurol 1992;51:404-14
46. Scott SA. Dendritic atrophy and remodeling of amygdaloid neurons in Alzheimer's disease. Dementia 1993;3-4:264-72
47. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994;87:554-67
48. Einstein G, Buranosky R, Grain BJ. Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci 1994;14:5077-88
49. Schimdt ML, Murray JM, Trojanowski JQ. Continuity of neuropil threads with tangle-bearing and tangle-free neurons in Alzheimer disease cortex. Mol Chem Neuropath 1993;18:299-312
50. Gottlieb E. The 3′ untranslated region of localized maternal messages contains a conserved motif involved in mRNA localization. Proc Natl Acad Sci 1992;89:7164-68
51. Zhou Y, King ML. RNA transport to the vegetal cortex of Xenopus oocytes. Devel Biol 1996;170:173-83
52. Jackson RJ. Cytoplasmic regulation of mRNA function: The importance of the 3′ untranslated region. Cell 1993;74:9-14
53. Macdonald PM. The means to the ends: Localization of maternal messenger RNAs. Sem Dev Biol 1992;3:413-24
54. Rebagliati MR, Weeks DL, Harvey RP, Melton DA. Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell 1985;42:769-77
55. Breitwieser W, Markussen FH, Horstmann H, Ephrussi A. Oskar protein interaction with vasa represents an essential step in polar granule assembly. Genes Develop 1996;10:2179-88
56. Ferrandon D, Elphick L, Nusslein-Volhard C, St Johnston D, Staufen protein associates with the 3′ UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 1994; 79:1221-32
57. Schwab C, Bondada B, Sparks DL, Cahan LD, Geddes JW. Post-mortem changes in the levels and localization of microtubule-associated proteins (Tau, MAP-2, and MAP-1B) in the rat and human hippocampus. Hippocampus 1992;4:210-25
58. 2+/calmodulin-dependent protein kinase II alpha and beta isoforms in-some structures of the rat forebrain. Brain Res 1994;659:179-93
59. 2+/calmodulin dependent protein kinase type IV in the peripheral ganglia and paraganglia of developing and mature rats. Brain Res 1994;666:173-81
60. Braak H, Braak E, Bohl J. Staging of Alzheimer's-related cortical destruction. European Neurol 1993;33:403-8
61. Braak H, Braak E. Staging of Alzheimer's-related neurofibrillary changes. Neurobiol Aging 1995;16:271-78
62. O'Banion MK, Coleman PD, Callahan LM. Regional neuronal loss in aging and Alzheimer's disease: A brief review. The Neurosciences 1994;6:307-14
63. Yisraeli JK, Sokol S, Melton DA. A two-step model for the localization of maternal mRNA in Xenopus oocytes: Involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development 1990;108:289-98
64. Pokrywka NJ, Stephenson EC. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 1991;113:55-66
65. Wilhelm JE, Vale RD. RNA on the move: The mRNA localization pathway. J Cell Biol 1993;123:269-74
66. Elisha Z, Havin L, Ringel I, Yisraeli JK. Vg1 RNA binding protein mediates the association of Vg1 RNA with microtubules in Xenopus oocytes. Embo J 1995;14:5109-14
67. Brun A. Frontal lobe degeneration of non-Alzheimer-type revisited. Dementia 1993;4:126-31
68. Terry RD. Synaptic plasticity in AD. Ann Neurol 1993;34:321
69. Liu X, Erikson C, Brun A. Cortical synaptic changes and gliosis in normal aging, Alzheimer's disease, and frontal lobe degeneration. Dementia 1996;7:128-34
70. Mersalov IB, Gundelfinger E, Tsetlin VI. Cloning cDNA for human neurogranin. Bioorg Khim 1996;22:366-69
71. Piosik PA, van Groenigen M, Ponne NJ, Bohuis PA, Baas F. RC3/neurogranin structure and expression in the caprine brain in relation to congenital hypothyroidism. Brain Res Mol Brain Res 1995;29: 119-30
72. Baudier J, Deloulme JC, van Dorsselaer A, Black D, Matthes HW. Purification and characterization of a brain-specific protein kinase C substrate, neurogranin (p17). Identification of a consensus amino acid sequence between neurogranin and neuromodulin (GAP 43) that corresponds to the protein kinase C phosphorylation site and the calmodulin-binding domain. J Biol Chem 1991;266:229-37