Increased CRMP2 phosphorylation is observed in Alzheimer's disease; does this tell us anything about disease development?

Current Alzheimer Research

Volumn 6, Issue 3, 2009, Pages 269-278

  Soutar, M P M ^a   Thornhill, P ^a   Cole, A R ^a   Sutherland, C ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2C; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; BRAIN CORTEX; CELL POLARITY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; GENOTYPE PHENOTYPE CORRELATION; HUMAN; MILD COGNITIVE IMPAIRMENT; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SHORT SURVEY;

ALZHEIMER DISEASE; ANIMALS; CYCLIN-DEPENDENT KINASE 5; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVE TISSUE PROTEINS; PHOSPHORYLATION;

EID: 67149093780     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720509788486572     Document Type: Short Survey

References (81)

1. Cole AR, Astell A, Green C, Sutherland C. Molecular connexions between dementia and diabetes. Neurosci Biobehav Rev 31(7): 1046-1063 (2007). (Pubitemid 47332620)
2. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, Connolly CN, et al. GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 279(48): 50176-50180 (2004).
3. Gu Y, Hamajima N, Ihara Y. Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39(15): 4267-4275 (2000). (Pubitemid 30212642)
4. Ryan KA, Pimplikar SW. Activation of GSK-3 and phosphorylation of CRMP2 in transgenic mice expressing APP intracellular domain. J Cell Biol 171(2): 327-335 (2005). (Pubitemid 41540024)
5. Yoshida H, Watanabe A, Ihara Y. Collapsin response mediator protein-2 is associated with neurofibrillary tangles in Alzheimer's disease. J Biol Chem 273(16): 9761-9768 (1998). (Pubitemid 28183069)
6. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376(6540): 509-514 (1995).
7. Wang LH, Strittmatter SM. Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J Neurochem 69(6): 2261-2269 (1997). (Pubitemid 27495410)
8. Hedgecock EM, Culotti JG, Thomson JN, Perkins LA. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol 111(1): 158-170 (1985).
9. Inatome R, Tsujimura T, Hitomi T, Mitsui N, Hermann P, Kuroda S, et al. Identification of CRAM, a novel unc-33 gene family protein that associates with CRMP3 and protein-tyrosine kinase(s) in the developing rat brain. J Biol Chem 275(35): 27291-27302 (2000).
10. Deo RC, Schmidt EF, Elhabazi A, Togashi H, Burley SK, Strittmatter SM. Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J 23(1): 9-22 (2004). (Pubitemid 38165743)
11. Li T, Hawkes C, Qureshi HY, Kar S, Paudel HK. Cyclin-dependent protein kinase 5 primes microtubule-associated protein tau sitespecifically for glycogen synthase kinase 3beta. Biochemistry 45(10): 3134-3145 (2006). (Pubitemid 43376332)
12. Majava V, Löytynoja N, Chen WQ, Lubec G, Kursula P. Crystal and solution structure, stability and post-translational modifications of collapsin response mediator protein 2. FEBS J 275(18):4583-4596 (2008).
13. Yuasa-Kawada J, Suzuki R, Kano F, Ohkawara T, Murata M, Noda M. Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. Eur J Neurosci 17(11): 2329-2343 (2003). (Pubitemid 36793742)
14. Minturn JE, Fryer HJ, Geschwind DH, Hockfield S. TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J Neurosci 15(10): 6757-6766 (1995).
15. Minturn JE, Geschwind DH, Fryer HJ, Hockfield S. Early postmitotic neurons transiently express TOAD-64, a neural specific protein. J Comp Neurol 355(3): 369-379 (1995).
16. Wang LH, Strittmatter SM. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci 16(19): 6197-6207 (1996). (Pubitemid 26313994)
17. Vincent P, Collette Y, Marignier R, Vuaillat C, Rogemond V, Davoust N, et al. A role for the neuronal protein collapsin response mediator protein 2 in T lymphocyte polarization and migration. J Immunol 175(11): 7650-7660 (2005).
18. Charrier E, Reibel S, Rogemond V, Aguera M, Thomasset N, Honnorat J. Collapsin response mediator proteins (CRMPs): involvement in nervous system development and adult neurodegenerative disorders. Mol Neurobiol 28(1): 51-64 (2003). (Pubitemid 38156435)
19. Inagaki N, Chihara K, Arimura N, Ménager C, Kawano Y, Matsuo N, et al. CRMP2 induces axons in cultured hippocampal neurons. Nat Neurosci 4(8): 781-782 (2001).
20. Fukata Y, Kimura T, Kaibuchi K. Axon specification in hippocampal neurons. Neurosci Res 43(4): 305-315 (2002). (Pubitemid 34828231)
21. Brown M, Jacobs T, Eickholt B, Ferrari G, Teo M, Monfries C, et al. Alpha2-chimaerin, cyclin-dependent Kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J Neurosci 24(41): 8994-9004 (2004).
22. Arimura N, Ménager C, Kawano Y, Yoshimura T, Kawabata S, Hattori A, et al. Phosphorylation by Rho kinase regulates CRMP2 activity in growth cones. Mol Cell Biol 25(22): 9973-9984 (2005).
23. Bretin S, Reibel S, Charrier E, Maus-Moatti M, Auvergnon N, Thevenoux A, et al. Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. J Comp Neurol 486(1): 1-17 (2005).
24. Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, et al. Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27(46): 12546-12554 (2007).
25. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, et al. Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10(2): 165-179 (2005).
26. Quinn CC, Chen E, Kinjo TG, Kelly G, Bell AW, Elliott RC, et al. TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. J Neurosci 23(7): 2815-2823 (2003).
27. Fukata Y, Itoh TJ, Kimura T, Ménager C, Nishimura T, Shiromizu T, et al. CRMP2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4(8): 583-591 (2002).
28. Gu Y, Ihara Y. Evidence that collapsin response mediator protein-2 is involved in the dynamics of microtubules. J Biol Chem 275(24): 17917-17920 (2000). (Pubitemid 30414732)
29. Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K. Tubulin and CRMP2 complex is transported via Kinesin-1. J Neurochem 93(6): 1371-1382 (2005). (Pubitemid 40853260)
30. Kawano Y, Yoshimura T, Tsuboi D, Kawabata S, Kaneko-Kawano T, Shirataki H, et al. CRMP2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol Cell Biol 25(22): 9920-9935 (2005).
31. Castellani V, Falk J, Rougon G. Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol Cell Neurosci 26(1): 89-100 (2004). (Pubitemid 38581025)
32. Nishimura T, Fukata Y, Kato K, Yamaguchi T, Matsuura Y, Kamiguchi H, et al. CRMP2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 5(9): 819-826 (2003).
33. Akimoto Y, Comer FI, Cole RN, Kudo A, Kawakami H, Hirano H, et al. Localization of the O-GlcNAc transferase and O-GlcNAc-modified proteins in rat cerebellar cortex. Brain Res 966(2): 194-205 (2003).
34. Mitsui N, Inatome R, Takahashi S, Goshima Y, Yamamura H, Yanagi S. Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J 21(13): 3274-3285 (2002). (Pubitemid 34760560)
35. Shapovalova Z, Tabunshchyk K, Greer PA. The Fer tyrosine kinase regulates an axon retraction response to Semaphorin 3A in dorsal root ganglion neurons. BMC Dev Biol 7: 133 (2007). (Pubitemid 351191378)
36. Horiuchi M, Loebrich S, Brandstaetter JH, Kneussel M, Betz H. Cellular localization and subcellular distribution of Unc-33-like protein 6, a brain-specific protein of the collapsin response mediator protein family that interacts with the neuronal glycine transporter 2. J Neurochem 94(2): 307-315 (2005). (Pubitemid 40995247)
37. Arimura N, Inagaki N, Chihara K, Ménager C, Nakamura N, Amano M, et al. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 275(31): 23973-23980 (2000).
38. Cole AR, Causeret F, Yadirgi G, Hastie CJ, McLauchlan H, McManus EJ, et al. Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. J Biol Chem 281(24): 16591-16598 (2006). (Pubitemid 43909612)
39. Cole AR, Soutar MP, Rembutsu M, van Aalten L, Hastie CJ, McLauchlan H, et al. Relative resistance of Cdk5-phosphorylated CRMP2 to dephosphorylation. J Biol Chem 283(26): 18227-18237 (2008).
40. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. GSK-3beta regulates phosphorylation of CRMP2 and neuronal polarity. Cell 120(1): 137-149 (2005). (Pubitemid 40094609)
41. Sweeney HL, Yang Z, Zhi G, Stull JT, Trybus KM. Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation. Proc Natl Acad Sci USA 91(4): 1490-1494 (1994). (Pubitemid 24059038)
42. Rembutsu M, Soutar MP, Van Aalten L, Gourlay R, Hastie CJ, McLauchlan H, et al. Novel procedure to investigate the effect of phosphorylation on protein complex formation in vitro and in cells. Biochemistry 47(7): 2153-2161 (2008). (Pubitemid 351287141)
43. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 24: 1121-1159 (2001). (Pubitemid 32695256)
44. Cole AR, Noble W, van Aalten L, Plattner F, Meimaridou R, Hogan D, et al. Collapsin response mediator protein-2 hyperphosphorylation is an early event in Alzheimer's disease progression. J Neurochem 103(3): 1132-1144 (2007).
45. Gong CX, Liu F, Grundke-Iqbal I, Iqbal K. Post-translational modifications of tau protein in Alzheimer's disease. J Neural Transm 112(6): 813-838 (2005). (Pubitemid 40655573)
46. Hanger DP, Byers HL, Wray S, Leung KY, Saxton MJ, Seereeram A, et al. Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis. J Biol Chem 282(32): 23645-23654 (2007).
47. Ksiezak-Reding H, Liu WK, Yen SH. Phosphate analysis and dephosphorylation of modified tau associated with paired helical filaments. Brain Res 597(2): 209-219 (1992). (Pubitemid 23003689)
48. Goedert M, Jakes R, Crowther RA, Six J, Lübke U, Vandermeeren M, et al. The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 90(11): 5066-5070 (1993).
49. Liu F, Tung EJ, Grundke-Iqbal I, Iqbal K, Gong CX. Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation. Eur J Neurosci 26(12): 3429-3436 (2007). (Pubitemid 350243526)
50. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83(13): 4913-4917 (1986). (Pubitemid 16075509)
51. Wang JZ, Grundke-Iqbal I, Iqbal K. Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 25(1): 59-68 (2007). (Pubitemid 46098893)
52. Goedert M, Klug A, Crowther RA. Tau protein, the paired helical filament and Alzheimer's disease. J Alzheimers Dis 9(Suppl3): 195-207 (2006). (Pubitemid 44253313)
53. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72(5): 1858-1862 (1975).
54. Sasaki Y, Cheng C, Uchida Y, Nakajima O, Ohshima T, Yagi T, et al. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35(5): 907-920 (2002).
55. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, et al. Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38(4): 555-565 (2003). (Pubitemid 36645031)
56. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402(6762): 615-622 (1999). (Pubitemid 129516324)
57. Arioka M, Tsukamoto M, Ishiguro K, Kato R, Sato K, Imahori K, et al. Tau protein kinase II is involved in the regulation of the normal phosphorylation state of tau protein. J Neurochem 60(2): 461-468 (1993).
58. Ishiguro K, Shiratsuchi A, Sato S, Omori A, Arioka M, Kobayashi S, et al. Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett 325(3): 167-172 (1993).
59. Kerr F, Rickle A, Nayeem N, Brandner S, Cowburn RF, Lovestone S. PTEN, a negative regulator of PI3 kinase signalling, alters tau phosphorylation in cells by mechanisms independent of GSK-3. FEBS Lett 580(13): 3121-3128 (2006). (Pubitemid 43744526)
60. Nayeem N, Kerr F, Naumann H, Linehan J, Lovestone S, Brandner S. Hyperphosphorylation of tau and neurofilaments and activation of CDK5 and ERK1/2 in PTEN-deficient cerebella. Mol Cell Neurosci 34(3): 400-408 (2007). (Pubitemid 46330042)
61. Tseng HC, Zhou Y, Shen Y, Tsai LH. A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett 523(1-3): 58-62 (2002). (Pubitemid 34786058)
62. Cohen PT. Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem Sci 22(7): 245-251 (1997). (Pubitemid 27310944)
63. Liu F, Grundke-Iqbal I, Iqbal K, Gong CX. Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 22(8): 1942-1950 (2005). (Pubitemid 41579384)
64. Goedert M, Cohen ES, Jakes R, Cohen P. p42 MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. Implications for Alzheimer's disease [corrected]. FEBS Lett 312(1): 95-99 (1992).
65. Lim J, Lu KP. Pinning down phosphorylated tau and tauopathies. Biochim Biophys Acta 1739(2-3): 311-322 (2005). (Pubitemid 40018547)
66. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399(6738): 784-788 (1999). (Pubitemid 29293174)
67. Bamberger ME. Landreth GE. Microglial interaction with beta-amyloid: implications for the pathogenesis of Alzheimer's disease. Microsc Res Tech 54(2): 59-70 (2001).
68. Zhu X, Lee HG, Raina AK, Perry G, Smith MA. The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11(5): 270-281 (2002). (Pubitemid 37494394)
69. Wray S, Saxton M, Anderton BH, Hanger DP. Direct analysis of tau from PSP brain identifies new phosphorylation sites and a major fragment of N-terminally cleaved tau containing four microtubule-binding repeats. J Neurochem (2008). (Pubitemid 351782262)
70. Alonso AC, Li B, Grundke-Iqbal I, Iqbal K. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 5(4): 375-384 (2008).
71. Frankfort SV, Tulner LR, van Campen JP, Verbeek MM, Jansen RW, Beijnen JH. Amyloid beta protein and tau in cerebrospinal fluid and plasma as biomarkers for dementia: a review of recent literature. Curr Clin Pharmacol 3(2): 123-131 (2008).
72. Tremblay C, Pilote M, Phivilay A, Emond V, Bennett DA, Calon F. Biochemical characterization of Abeta and tau pathologies in mild cognitive impairment and Alzheimer's disease. J Alzheimer Dis 12(4): 377-390 (2007).
73. Ewers M, Buerger K, Teipel SJ, Scheltens P, Schröder J, Zinkowski RP, et al. Multicenter assessment of CSF-phosphorylated tau for the prediction of conversion of MCI. Neurology 69(24): 2205-2212 (2007).
74. Brys M, Pirraglia E, Rich K, Rolstad S, Mosconi L, Switalski R, et al. Prediction and longitudinal study of CSF biomarkers in mild cognitive impairment. Neurobiol Aging (2007).
75. Lubec G, Nonaka M, Krapfenbauer K, Gratzer M, Cairns N, Fountoulakis M. Expression of the dihydropyrimidinase related protein 2 (DRP-2) in Down syndrome and Alzheimer's disease brain is downregulated at the mRNA and dysregulated at the protein level. J Neural Transm Suppl 57: 161-177 (1999).
76. Wishart TM, Paterson JM, Short DM, Meredith S, Robertson KA, Sutherland C, et al. Differential proteomics analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow Wallerian degeneration (Wlds) gene. Mol Cell Proteomics 6(8): 1318-1330 (2007).
77. Jiang SX, Kappler J, Zurakowski B, Desbois A, Aylsworth A, Hou ST. Calpain cleavage of collapsin response mediator proteins in ischemic mouse brain. Eur J Neurosci 26(4): 801-809 (2007). (Pubitemid 47274611)
78. Zhang Z, Ottens AK, Sadasivan S, Kobeissy FH, Fang T, Hayes RL, et al. Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J Neurotrauma 24(3): 460-472 (2007).
79. Czech T, Yang JW, Csaszar E, Kappler J, Baumgartner C, Lubec G. Reduction of hippocampal collapsin response mediated protein-2 in patients with mesial temporal lobe epilepsy. Neurochem Res 29(12): 2189-2196 (2004). (Pubitemid 40036890)
80. Bretin S, Rogemond V, Marin P, Maus M, Torrens Y, Honnorat J, et al. Calpain product of WT-CRMP2 reduces the amount of surface NR2B NMDA receptor subunit. J Neurochem 98(4): 1252-1265 (2006).
81. Kowara R, Chen Q, Milliken M, Chakravarthy B. Calpain-mediated truncation of dihydropyrimidinase-like 3 protein (DPYSL3) in response to NMDA and H2O2 toxicity. J Neurochem 95(2): 466-474 (2005). (Pubitemid 41457515)