Divergent functions through alternative splicing: The Drosophila CRMP gene in pyrimidine metabolism, brain, and behavior

Genetics

Volumn 191, Issue 4, 2012, Pages 1227-1238

  Morris, Deanna H ^a   Dubnau, Josh ^b   Park, Jae H ^c   Rawls, John M ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN; PYRIMIDINE; RAC PROTEIN; RAS PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; BRAIN DEVELOPMENT; CIRCADIAN RHYTHM; DROSOPHILA; EXON; EYE DEVELOPMENT; FLY; GENE EXPRESSION; GENE FUNCTION; INSECT GENETICS; LOSS OF FUNCTION MUTATION; MAMMAL; MEMORY DISORDER; METABOLISM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; TISSUE SPECIFICITY; VERTEBRATE;

EID: 84865101571     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.141101     Document Type: Article

References (69)

1. Abendroth, J., K. Niefind, and D. Schomburg, 2002a X-ray structure of dihydropyrimidinase from a Thermus sp. at 1.3 Å resolution. J. Mol. Biol. 320: 143-156.
2. Abendroth, J., K. Niefind, O. May, M. Siemann, C. C. Syldatk et al., 2002b The structure of L-hydantoinase from Arthobacter aurescens leads to an understanding of dihydropyrimidinase substrate and enantio specificity. Biochemistry 9: 8589-8597.
3. Amano, M., Y. Fukata, and K. Kaibuchi, 2000 Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261: 44-51.
4. Arimura, N., N. Inagaki, K. Chihara, C. Menager, N. Nakamura et al., 2000 Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J. Biol. Chem. 275: 23973-23980.
5. Arimura, N., C. Menager, Y. Kawano, T. Yoshimura, S. Kawabata et al., 2005 Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol. Cell. Biol. 25: 9973-9984.
6. Bahn, J., G. Li, and J. Park, 2009 Comparative analysis of Pdfmediated circadian behaviors between Drosophila melanogaster and Drosophila virilis. Genetics 181: 965-975.
7. Blum, A. L., W. Li, M. Cressy, and J. Dubnau, 2009 Short-and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr. Biol. 19: 1-10.
8. Bradford, M., 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
9. Brand, A., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
10. Brown, M., T. Jacobs, B. Eickholt, G. Ferrari, M. Teo et al., 2004 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: 8994-9004.
11. Chi, X., B. Schmutzler, J. Brittain, Y. Wang, C. Hingtgen et al., 2009 Regulation of N-type voltage-gated calcium channels (Cav2.2) and transmitter release by collapsin response mediator protein-2 (CRMP-2) in sensory neurons. J. Cell Sci. 122: 4351-4362.
12. Chintapalli, V., J. Wang, and J. Dow, 2007 Using FlyAtlas to identify better Drosophila models of human disease. Nat. Genet. 39: 715-720.
13. Cole, A., A. Knebel, N. Morrice, L. Robertson, A. Irving et al., 2004 GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem. 279: 50176-50180.
14. Deo, R., E. Schmidt, A. Elhabazi, H. Togashi, S. Burley et al., 2004 Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J. 23: 9-22.
15. Duffy, J., 2002 GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34: 1-15.
16. Dura, J., T. Preat, and T. Tully, 1993 Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9: 1-14.
17. Fanto, M., U. Weber, S. Strutt, and M. Mlodzik, 2000 Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr. Biol. 10: 979-988.
18. Fukata, Y., T. Itoh, T. Kimura, C. Menager, T. Nishimura et al., 2002 CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4: 583-591.
19. Gu, Y., N. Hamajima, and Y. Ihara, 2000 Neurofibrillary tangleassociated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39: 4267-4275.
20. Hall, C., G. Michael, N. Cann, G. Ferrari, M. Teo et al., 2001a a2-chimaerin, a Cdc42/Rac1 regulator, is selectively expressed in the rat embryonic nervous system and is involved in neuritogenesis in N1E-115 neuroblastoma cells. J. Neurosci. 21: 5191-5202.
21. Hall, D., M. Brown, T. Jacobs, G. Ferrari, N. Cann et al., 2001b Collapsin response mediator protein switches RhoA and Rac1 morphology in N1E-115 neuroblastoma cells and is regulated by Rho kinase. J. Biol. Chem. 276: 43482-43486.
22. Hamajima, N., K. Matsuda, S. Sakata, N. Tamaki, M. Sasaki et al., 1996 A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene 180: 157-163.
23. Hamajima, N., M. Kouwaki, P. Vreken, K. Matsuda, S. Sumi et al., 1998 Dihydropyrimidinase deficiency: structural organization, chromosomal localization, and mutation analysis of the human dihydropyrimidinase gene. Am. J. Hum. Genet. 63: 717-726.
24. Hamblen-Coyle, M. J., D. A. Wheeler, J. E. Rutila, M. Rosbash, and J. C. Hall, 1992 Behavior of period-altered circadian rhythm mutants of Drosophila in light:dark cycles (Diptera: Drosophilidae). J. Insect Behav. 5: 417-446.
25. Hou, S., S. Jiang, and R. Smith, 2008 Permissive and repulsive cues and signaling pathways of axonal outgrowth and regeneration. Int. Rev. Cell Molec. Biol. 267: 125-181.
26. Jin, Z., and S. M. Strittmatter, 1997 Rac1 mediates collapsin-1-induced growth cone collapse. J. Neurosci. 17: 6256-6263.
27. Kautz, J., and K. Schnackerz, 1989 Purification and properties of 5,6-dihydropyrimidine amidohydrolase from calf liver. Eur. J. Biochem. 181: 431-435.
28. Kawano, Y., T. Yoshimura, D. Tsuboi, S. Kawabata, T. Kaneko-Kawano et al., 2005 CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol. Cell. Biol. 22: 9920-9935.
29. Liu, X., Q. Yu, Z. Huang, L. Zwiebel, J. C. Hall et al., 1991 The strength and periodicity of D. melanogaster circadian rhythms are differentially affected by alterations in period gene expression. Neuron 6: 753-766.
30. Livingstone, M. S., P. P. Sziber, and W. G. Quinn, 1984 Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37: 205-215.
31. Lohkamp, B., B. Andersen, J. Piškur, and D. Dobritzsch, 2006 The crystal structure of dihydropyrimidinases reaffirm the close relationship between cyclic amidohydrolases and explain their substrate specificity. J. Biol. Chem. 281: 13762-13776.
32. Mitsui, N., R. Inatome, S. Takahashi, Y. Goshima, H. Yamamura et al., 2002 Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 21: 3274-3285.
33. Müller, D., S. Kugler, A. Preiss, D. Maier, and A. Nagel, 2005 Genetic modifier screens on hairless gain-of-function phenotypes reveal genes involved in cell differentiation, cell growth and apoptosis in Drosophila melanogaster. Genetics 171: 1137-1152.
34. Ng, J., and L. Luo, 2004 Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44: 779-793.
35. Ng, J., T. Nardine, M. Harms, J. Tzu, A. Goldstein et al., 2002 GTPases control axon growth, guidance and branching. Nature 416: 442-447.
36. Park, J. H., 2002 Downloading central clock information in Drosophila. Mol. Neurobiol. 26: 217-233.
37. Qian, M., G. Pan, L. Sun, C. Feng, and Z. Xie et al., 2007 Receptorlike tyrosine phosphatase PTP10D is required for long-term memory in Drosophila. J. Neurosci. 27: 4396-4402.
38. Rawls, J., 2006 Analysis of pyrimidine catabolism in Drosophila melanogaster using epistatic interactions with mutations of pyrimidine biosynthesis and b-alanine metabolism. Genetics 172: 1665-1674.
39. Renn, S. C. P., J. H. Park, M. Rosbash, J. C. Hall, and P. H. Taghert, 1999 A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802.
40. Rørth, P., K. Szabo, A. Bailey, T. Laverty, J. Rehm et al., 1998 Systematic gain-of-function genetics in Drosophila. Development 125: 1049-1057.
41. Rosato, E., and C. P. Kyriacou, 2006 Analysis of locomotor activity rhythms in Drosophila. Nat. Protoc. 1: 559-568.
42. Rubin, G., L. Hong, P. Brokstein, M. Evans-Holm, E. Frise et al., 2000 A Drosophila complementary DNA resource. Science 287: 2222-2224.
43. Schmidt, E., and S. Strittmatter, 2007 The CRMP family of proteins and their role in Sema3A signaling. Adv. Exp. Med. Biol. 600: 1-11.
44. Schmidt, E., S. Shim, and S. Strittmatter, 2008 Release of MICAL autoinhibition by Semaphorin-Plex signaling promotes interaction with collapsin response mediator protein. J. Neurosci. 28: 2287-2297.
45. Schnackerz, K., and D. Dobritzch, 2008 Amidohydrolases of the reductive pyrimidine catabolic pathway purification, characterization, structure, reaction mechanisms and enzyme deficiency. Biochim. Biophys. Acta 1784: 431-444.
46. Schwaerzel, M., M. Heisenberg, and T. Zars, 2002 Extinction antagonizes olfactory memory at the subcellular level. Neuron 35: 951-960.
47. Shuai, Y., B. Lu, L. Wang, K. Sun, and Y. Zhong, 2010 Forgetting is regulated through Rac activity in Drosophila. Cell 140: 579-589.
48. Simmons, A., J. Rawls, J. Piškur, and J. Davidson, 1999 A mutation that uncouples uncouples allosteric regulation of carbamyl phosphate synthetase in Drosophila. J. Mol. Biol. 287: 277-285.
49. Stenmark, P., D. Ogg, S. Flodin, A. Flores, T. Kotenyova et al., 2007 The structure of human collapsin response mediator protein 2, a regulator of axonal growth. J. Neurochem. 101: 906-917.
50. Su, K., W. Chien, W. Fu, I.-S. Yu, H. Huang et al., 2007 Mice deficient in collapsin response mediator protein-1 exhibit impaired long-term potentiation and impaired spatial learning and memory. J. Neurosci. 27: 2513-2524.
51. Takemoto, T., Y. Sasaki, N. Hamajima, Y. Goshima, M. Nonaka et al., 2000 Cloning and characterization of the Caenorhabditis elegans CeCRMP/DHP-1 and-2; common ancestors of CRMP and dihydropyrimidinase? Gene 261: 259-267.
52. Tanaka, N., A. Arnova, and B. Schwer, 2007 Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev. 21: 2312-2325.
53. Terman, J., T. Mao, R. Pasterkamp, H. Yu, and A. Kolodkin, 2002 MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109: 887-900.
54. Tseng, A., and I. Hariharan, 2002 An overexpression screen in Drosophila for genes that restrict growth or cell-cycle progression in the developing eye. Genetics 162: 229-243.
55. Tully, T., and W. G. Quinn, 1985 Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 157: 263-277.
56. Tully, T., T. Preat, S. C. Boynton, and M. Del Vecchio, 1994 Genetic dissection of consolidated memory in Drosophila. Cell 79: 35-47.
57. Tweedie, S., M. Ashburner, K. Falls, P. Leyland, P. McQuilton et al., 2009 FlyBase: enhancing Drosophila gene ontology annotations. Nucleic Acids Res. 37: D555-D559.
58. Uchida, Y., T. Ohshima, Y. Sasaki, H. Suzuki, S. Yanai et al., 2005 Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3b phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10: 165-179.
59. Van Kuilenburg, A., H. Van Lenthe, and A. Van Gennip, 2006 Activity of pyrimidine degradation enzymes in normal tissues. Nucleosides Nucleotides Nucleic Acids 25: 1211-1214.
60. Wang, L., and S. Strittmatter, 1996 A family of rat CRMP genes is differentially expressed in the nervous system. J. Neurosci. 16: 6197-6207.
61. Wang, L., and S. Strittmatter, 1997 Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J. Neurochem. 69: 2261-2269.
62. Wu, C., S. Xia, T. Fu, H. Wang, Y. Chen et al., 2007 Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat. Neurosci. 10: 1578-1586.
63. Yamashita, N., and Y. Goshima, 2012 Collapsin response mediator proteins regulate neuronal development and plasticity by switching their phosphorylation status. Mol. Neurobiol. 45: 234-246.
64. Yang, J., L. Porter, and J. Rawls, 1995 Expression of the dihydroorotate dehydrogenase gene, dhod, during spermatogenesis in Drosophila melanogaster. Mol. Gen. Genet. 246: 334-341.
65. Yoshimura, T., Y. Kawano, N. Arimura, S. Kawabata, A. Kikuchi et al., 2005 GSK-3b regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120: 137-149.
66. Xu, S., Y. Liu, Y. Yang, W. Jiang, E. Arnold et al., 2003 Crystal structure of D-hydantoinase from Burkholderia pickettii at a resolution of 2.7 Angstroms: insights into the molecular basis of enzyme thermostability. J. Bacteriol. 185: 4038-4049.
67. Yin, J. C., J. S. Wallach, M. Del Vecchio, E. L. Wilder, H. Zhou et al., 1994 Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79: 49-58.
68. Yin, J. C., M. Del Vecchio, H. Zhou, and T. Tully, 1995 CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81: 107-115.
69. Zars, T., M. Fischer, R. Schulz, and M. Heisenberg, 2000 Localization of a short-term memory in Drosophila. Science 288: 672-675.