Vertebrate GLD2 poly(A) polymerases in the germline and the brain

RNA

Volumn 11, Issue 7, 2005, Pages 1117-1130

  Rouhana, Labib ^a   Wang, Liaoteng ^a   Buter, Natascha ^a   Jae, Eun Kwak ^a   Schiltz, Craig A ^b   Gonzalez, Tania ^a,c   Kelley, Ann E ^b   Landry, Charles F ^b   Wickens, Marvin ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c GENENTECH INC   (United States)

Author keywords

GLD2; Poly(A) polymerase; Translational control

Indexed keywords

CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; MESSENGER RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE GLD 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN; COGNITION; CONTROLLED STUDY; EMOTION; FEMALE; GERM LINE; HIPPOCAMPUS; LEARNING; MAMMAL; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VERTEBRATE; XENOPUS;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CATALYTIC DOMAIN; FEMALE; GLUTATHIONE TRANSFERASE; HUMANS; MICE; MICROINJECTIONS; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; OOCYTES; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPLEEN; XENOPUS; XENOPUS PROTEINS;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 22244445521     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2630205     Document Type: Article

References (67)

1. Alarcon, J.M., Hodgman, R., Theis, M., Huang, Y.S., Kandel, E.R., and Richter, J.D. 2004. Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn. Mem. 11: 318-327.
2. Aravind, L. and Koonin, E.V. 1998. Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res. 26: 3746-3752.
3. Ballantyne, S., Bilger, A., Astrom, J., Virtanen, A., and Wickens, M. 1995. Poly (A) polymerases in the nucleus and cytoplasm of frog oocytes: Dynamic changes during oocyte maturation and early development. RNA 1: 64-78.
4. Ballantyne, S., Daniel Jr., D.L., and Wickens, M. 1997. A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol. Biol. Cell 8: 1633-1648.
5. Barnard, D.C., Ryan, K., Manley, J.L., and Richter, J.D. 2004. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119: 641-651.
6. Bernstein, D., Hook, B., Hajarnavis, A., Opperman, L., and Wickens, M. 2005. Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 11: 447-458.
7. Bilger, A., Fox, C.A., Wahle, E., and Wickens, M. 1994. Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes & Dev. 8: 1106-1116.
8. Dehlin, E., von Gabain, A., Alm, G., Dingelmaier, R., and Resnekov, O. 1996. Repression of β interferon gene expression in virus-infected cells is correlated with a poly(A) tail elongation. Mol. Cell Biol. 16: 468-474.
9. Dickson, K.S., Bilger, A., Ballantyne, S., and Wickens, M.P. 1999. The cleavage and polyadenylation specificity factor in Xenopus laevis oocytes is a cytoplasmic factor involved in regulated polyadenylation. Mol. Cell Biol. 19: 5707-5717.
10. Dickson, K.S., Thompson, S.R., Gray, N.K., and Wickens, M. 2001. Poly(A) polymerase and the regulation of cytoplasmic polyadenylation. J. Biol. Chem. 276: 41810-41816.
11. Dubnau, J., Chiang, A.S., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., et al. 2003. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13: 286-296.
12. Ebersole, T.A., Chen, Q., Justice, M.J., and Artzt, K. 1996. The quaking gene product necessary in embryogenesis and myelination combines features of RNA binding and signal transduction proteins. Nat. Genet. 12: 260-265.
13. Eichenbaum, H. 2004. Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109-120.
14. Fox, C.A., Sheets, M.D., and Wickens, M.P. 1989. Poly(A) addition during maturation of frog oocytes: Distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes & Dev. 3: 2151-2162.
15. Frey, U., Krug, M., Reymann, K.G., and Matthies, H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452: 57-65.
16. Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., and Inokuchi, K. 2003. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38: 447-460.
17. Gebauer, F. and Richter, J.D. 1995. Cloning and characterization of a Xenopus poly(A) polymerase. Mol. Cell Biol. 15: 1422-1430.
18. Good, P.J., Abler, L., Herring, D., and Sheets, M.D. 2004. Xenopus embryonic poly(A) binding protein 2 (ePABP2) defines a new family of cytoplasmic poly(A) binding proteins expressed during the early stages of vertebrate development. Genesis 38: 166-175.
19. Hake, L.E., Mendez, R., and Richter, J.D. 1998. Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol. Cell Biol. 18: 685-693.
20. Hentze, M.W. 1995. Translational regulation: Versatile mechanisms for metabolic and developmental control. Curr. Opin. Cell. Biol. 7: 393-398.
21. Huang, Y.S., Jung, M.Y., Sarkissian, M., and Richter, J.D. 2002. N-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and α CaMKII mRNA polyadenylation at synapses. EMBO J. 21: 2139-2148.
22. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., and O'Shea, E.K. 2003. Global analysis of protein localization in budding yeast. Nature 425: 686-691.
23. Jenny, A., Hauri, H.P., and Keller, W. 1994. Characterization of cleavage and polyadenylation specificity factor and cloning of its 100-kilodalton subunit. Mol. Cell Biol. 14: 8183-8190.
24. Jones, M.W., Errington, M.L., French, P.J., Fine, A., Bliss, T.V., Garel, S., Charnay, P., Bozon, B., Laroche, S., and Davis, S. 2001. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4: 289-296.
25. Kadaba, S., Krueger, A., Trice, T., Krecic, A.M., Hinnebusch, A.G., and Anderson, J. 2004. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes & Dev. 18: 1227-1240.
26. Kobayashi, H., Minshull, J., Ford, C., Goldsteyn, R., Poon, R., and Hunt, T. 1991. On the synthesis and destruction of A- and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis. J. Cell. Biol. 114: 755-765.
27. Kraemer, B., Crittenden, S., Gallegos, M., Moulder, G., Barstead, R., Kimble, J., and Wickens, M. 1999. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 9: 1009-1018.
28. Kuersten, S. and Goodwin, E.B. 2003. The power of the 3′ UTR: Translational control and development. Nat. Rev. Genet. 4: 626-637.
29. Kwak, J.E., Wang, L., Ballantyne, S., Kimble, J., and Wickens, M. 2004. Mammalian GLD-2 homologs are poly(A) polymerases. Proc. Natl. Acad. Sci. 101: 4407-4412.
30. Liu, J. and Schwartz, J.H. 2003. The cytoplasmic polyadenylation element binding protein and polyadenylation of messenger RNA in Aplysia neurons. Brain Res. 959: 68-76.
31. Lund, E. and Paine, P.L. 1990. Nonaqueous isolation of transcriptionally active nuclei from Xenopus oocytes. Methods Enzymol. 181: 36-43.
32. Malkani, S., Wallace, K.J., Donley, M.P., and Rosen, J.B. 2004. An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning. Learn. Mem. 11: 617-624.
33. Martin, G., Keller, W., and Doublie, S. 2000. Crystal structure of mammalian poly(A) polymerase in complex with an analog of ATP. EMBO J. 19: 4193-4203.
34. Martin, G., Moglich, A., Keller, W., and Doublie, S. 2004. Biochemical and structural insights into substrate binding and catalytic mechanism of mammalian poly(A) polymerase. J. Mol. Biol. 341: 911-925.
35. Matsuzaki, M., Honkura, N., Ellis-Davies, G.C., and Kasai, H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766.
36. Mendez, R. and Richter, J.D. 2001. Translational control by CPEB: A means to the end. Nat. Rev. Mol. Cell. Biol. 2: 521-529.
37. Mendez, R., Murthy, K.G., Ryan, K., Manley, J.L., and Richter, J.D. 2000. Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol. Cell 6: 1253-1259.
38. Miller, S., Yasuda, M., Coats, J.K., Jones, Y., Martone, M.E., and Mayford, M. 2002. Disruption of dendritic translation of CaMKIIα impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36: 507-519.
39. Muckenthaler, M., Gunkel, N., Stripecke, R., and Hentze, M.W. 1997. Regulated poly(A) tail shortening in somatic cells mediated by cap-proximal translational repressor proteins and ribosome association. RNA 3: 983-995.
40. Nakahata, S., Katsu, Y., Mita, K., Inoue, K., Nagahama, Y., and Yamashita, M. 2001. Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J. Biol. Chem. 276: 20945-20953.
41. Nakahata, S., Kotani, T., Mita, K., Kawasaki, T., Katsu, Y., Nagahama, Y., and Yamashita, M. 2003. Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech. Dev. 120: 865-880.
42. Nguyen, P.V., Abel, T., and Kandel, E.R. 1994. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265: 1104-1107.
43. Otmakhov, N., Tao-Cheng, J.H., Carpenter, S., Asrican, B., Dosemeci, A., Reese, T.S., and Lisman, J. 2004. Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J. Neurosci. 24: 9324-9331.
44. Pang, P.T., Teng, H.K., Zaitsev, E., Woo, N.T., Sakata, K., Zhen, S., Teng, K.K., Yung, W.H., Hempstead, B.L., and Lu, B. 2004. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306: 487-491.
45. Pawlak, R., Nagai, N., Urano, T., Napiorkowska-Pawlak, D., Ihara, H., Takada, Y., Collen, D., and Takada, A. 2002. Rapid, specific and active site-catalyzed effect of tissue-plasminogen activator on hippocampus-dependent learning in mice. Neuroscience 113: 995-1001.
46. Read, R.L., Martinho, R.G., Wang, S.W., Carr, A.M., and Norbury, C.J. 2002. Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest. Proc. Natl. Acad. Sci. 99: 12079-12084.
47. Richter, J.D. 2000. The influence of polyadenylation-induced translation on metazoan development and neuronal synaptic function. In Translational control (eds. J.W.B. Hershey et al.), pp. 785-805. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. _. 2001. Think globally, translate locally: What mitotic spindles and neuronal synapses have in common. Proc. Natl. Acad. Sci. 98: 7069-7071.
49. Romanowski, P., Madine, M.A., and Laskey, R.A. 1996. XMCM7, a novel member of the Xenopus MCM family, interacts with XMCM3 and colocalizes with it throughout replication. Proc. Natl. Acad. Sci. 93: 10189-10194.
50. Saitoh, S., Chabes, A., McDonald, W.H., Thelander, L., Yates, J.R., and Russell, P. 2002. Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 109: 563-573.
51. Scoville, W.B. and Milner, B. 1957. Loss of recent memory after bilateral hippocampal lesions. J. Neurochem. 20: 11-21.
52. Sheets, M.D., Fox, C.A., Hunt, T., Vande Woude, G., and Wickens, M. 1994. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes & Dev. 8: 926-938.
53. Shin, C.Y., Kundel, M., and Wells, D.G. 2004. Rapid, activity-induced increase in tissue plasminogen activator is mediated by metabotropic glutamate receptor-dependent mRNA translation. J. Neurosci. 24: 9425-9433.
54. Si, K., Giustetto, M., Etkin, A., Hsu, R., Janisiewicz, A.M., Miniaci, M.C., Kim, J.H., Zhu, H., and Kandel, E.R. 2003a. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115: 893-904.
55. Si, K., Lindquist, S., and Kandel, E.R. 2003b. A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115: 879-891.
56. Simon, P., Schott, K., Williams, R.W., and Schaeffel, F. 2004. Posttranscriptional regulation of the immediate-early gene EGR1 by light in the mouse retina. Eur. J. Neurosci. 20: 3371-3377.
57. Sonenberg, N. 1994. mRNA translation: Influence of the 5′ and 3′ untranslated regions. Curr. Opin. Genet. Dev. 4: 310-315.
58. Sonoda, J. and Wharton, R.P. 1999. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes & Dev. 13: 2704-2712.
59. Stebbins-Boaz, B., Cao, Q., de Moor, C.H., Mendez, R., and Richter, J.D. 1999. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell 4: 1017-1027.
60. Steward, O. and Worley, P.F. 2001. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 30: 227-240.
61. Tang, S.J. and Schuman, E.M. 2002. Protein synthesis in the dendrite. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 521-529.
62. Theis, M., Si, K., and Kandel, E.R. 2003. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc. Natl. Acad. Sci. 100: 9602-9607.
63. Wang, L., Eckmann, C.R., Kadyk, L.C., Wickens, M., and Kimble, J. 2002. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419: 312-316.
64. Wells, D.G., Richter, J.D., and Fallon, J.R. 2000. Molecular mechanisms for activity-regulated protein synthesis in the synaptodendritic compartment. Curr. Opin. Neurobiol. 10: 132-137.
65. Wickens, M., Bernstein, D.S., Kimble, J., and Parker, R. 2002. A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet. 18: 150-157.
66. Wu, L., Wells, D., Tay, J., Mendis, D., Abbott, M.A., Barnitt, A., Quinlan, E., Heynen, A., Fallon, J.R., and Richter, J.D. 1998. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses. Neuron 21: 1129-1139.
67. Ye, B., Petritsch, C., Clark, I.E., Gavis, E.R., Jan, L.Y., and Jan, Y.N. 2004. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr. Biol. 14: 314-321.