A Functional Mouse Retroposed Gene Rps23r1 Reduces Alzheimer's β-Amyloid Levels and Tau Phosphorylation

Neuron

Volumn 64, Issue 3, 2009, Pages 328-340

  Zhang, Yun wu ^a,b   Liu, Shijie ^b   Zhang, Xue ^b   Li, Wu Bo ^c   Chen, Yaomin ^b   Huang, Xiumei ^a,b   Sun, Liangwu ^b   Luo, Wenjie ^d   Netzer, William J ^d   Threadgill, Richard ^c   Wiegand, Gordon ^c   Wang, Ruishan ^a,b   Cohen, Stanley N ^e   Greengard, Paul ^d   Liao, Francesca Fang ^b,g   Li, Limin ^c,f   Xu, Huaxi ^b  

^a XIAMEN UNIVERSITY   (China)

^b BURNHAM INSTITUTE   (United States)

^c Functional Genetics Inc   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^g UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

Author keywords

CELLBIO; HUMDISEASE; MOLNEURO

Indexed keywords

ADENYLATE CYCLASE; AMYLOID BETA PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3; RIBOSOMAL PROTEIN S23 RETROPOSITION 1; RIBOSOME PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE IDENTIFICATION; GENETIC SCREENING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; RETROPOSON; TRANSGENIC MOUSE;

ADENYLATE CYCLASE; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BASE SEQUENCE; BRAIN; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLYCOGEN SYNTHASE KINASE 3; HELA CELLS; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PC12 CELLS; PHOSPHORYLATION; RATS; RIBOSOMAL PROTEINS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SYNAPSES; TAU PROTEINS;

EID: 70350747578     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.08.036     Document Type: Article

References (57)

1. Ancolio K., Dumanchin C., Barelli H., Warter J.M., Brice A., Campion D., Frebourg T., and Checler F. Unusual phenotypic alteration of beta amyloid precursor protein (betaAPP) maturation by a new Val-715→ Met betaAPP-770 mutation responsible for probable early-onset Alzheimer's disease. Proc. Natl. Acad. Sci. USA 96 (1999) 4119-4124
2. Babushok D.V., Ostertag E.M., and Kazazian Jr. H.H. Current topics in genome evolution: molecular mechanisms of new gene formation. Cell. Mol. Life Sci. 64 (2007) 542-554
3. Barelli H., Lebeau A., Vizzavona J., Delaere P., Chevallier N., Drouot C., Marambaud P., Ancolio K., Buxbaum J.D., Khorkova O., et al. Characterization of new polyclonal antibodies specific for 40 and 42 amino acid-long amyloid beta peptides: their use to examine the cell biology of presenilins and the immunohistochemistry of sporadic Alzheimer's disease and cerebral amyloid angiopathy cases. Mol. Med. 3 (1997) 695-707
4. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., and Hof P.R. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Brain Res. Rev. 33 (2000) 95-130
5. Buxbaum J.D., Ruefli A.A., Parker C.A., Cypess A.M., and Greengard P. Calcium regulates processing of the Alzheimer amyloid protein precursor in a protein kinase C-independent manner. Proc. Natl. Acad. Sci. USA 91 (1994) 4489-4493
6. Cai H., Wang Y., McCarthy D., Wen H., Borchelt D.R., Price D.L., and Wong P.C. BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat. Neurosci. 4 (2001) 233-234
7. Chen F., Yang D.S., Petanceska S., Yang A., Tandon A., Yu G., Rozmahel R., Ghiso J., Nishimura M., Zhang D.M., et al. Carboxyl-terminal fragments of Alzheimer beta-amyloid precursor protein accumulate in restricted and unpredicted intracellular compartments in presenilin 1-deficient cells. J. Biol. Chem. 275 (2000) 36794-36802
8. Cole S.L., and Vassar R. The Alzheimer's disease beta-secretase enzyme, BACE1. Mol. Neurodegener. 2 (2007) 22
9. De Strooper B. Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38 (2003) 9-12
10. De Strooper B., Simons M., Multhaup G., Van Leuven F., Beyreuther K., and Dotti C.G. Production of intracellular amyloid-containing fragments in hippocampal neurons expressing human amyloid precursor protein and protection against amyloidogenesis by subtle amino acid substitutions in the rodent sequence. EMBO J. 14 (1995) 4932-4938
11. Fang X., Yu S.X., Lu Y., Bast Jr. R.C., Woodgett J.R., and Mills G.B. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl. Acad. Sci. USA 97 (2000) 11960-11965
12. Flaherty D.B., Soria J.P., Tomasiewicz H.G., and Wood J.G. Phosphorylation of human tau protein by microtubule-associated kinases: GSK3beta and cdk5 are key participants. J. Neurosci. Res. 62 (2000) 463-472
13. Frame S., and Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359 (2001) 1-16
14. Gasparini L., Gouras G.K., Wang R., Gross R.S., Beal M.F., Greengard P., and Xu H. Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J. Neurosci. 21 (2001) 2561-2570
15. Halagappa V.K., Guo Z., Pearson M., Matsuoka Y., Cutler R.G., Laferla F.M., and Mattson M.P. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 26 (2007) 212-220
16. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
17. Hollis G.F., Hieter P.A., McBride O.W., Swan D., and Leder P. Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing. Nature 296 (1982) 321-325
18. Hori N., Murakawa K., Matoba R., Fukushima A., Okubo K., and Matsubara K. A cDNA sequence of human ribosomal protein, homologue of yeast S28. Nucleic Acids Res. 21 (1993) 4394
19. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., Copeland N.G., Lee M.K., Younkin L.H., Wagner S.L., et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 13 (2004) 159-170
20. Jankowsky J.L., Younkin L.H., Gonzales V., Fadale D.J., Slunt H.H., Lester H.A., Younkin S.G., and Borchelt D.R. Rodent A beta modulates the solubility and distribution of amyloid deposits in transgenic mice. J. Biol. Chem. 282 (2007) 22707-22720
21. Jeffs P., and Ashburner M. Processed pseudogenes in Drosophila. Proc. Biol. Sci. 244 (1991) 151-159
22. Johnstone E.M., Chaney M.O., Norris F.H., Pascual R., and Little S.P. Conservation of the sequence of the Alzheimer's disease amyloid peptide in dog, polar bear and five other mammals by cross-species polymerase chain reaction analysis. Brain Res. Mol. Brain Res. 10 (1991) 299-305
23. Kaessmann H., Vinckenbosch N., and Long M. RNA-based gene duplication: mechanistic and evolutionary insights. Nat. Rev. Genet. 10 (2009) 19-31
24. Kamenetsky M., Middelhaufe S., Bank E.M., Levin L.R., Buck J., and Steegborn C. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362 (2006) 623-639
25. Karin M., and Richards R.I. Human metallothionein genes-primary structure of the metallothionein-II gene and a related processed gene. Nature 299 (1982) 797-802
26. Kopan R., and Goate A. A common enzyme connects notch signaling and Alzheimer's disease. Genes Dev. 14 (2000) 2799-2806
27. Lazarov O., Robinson J., Tang Y.P., Hairston I.S., Korade-Mirnics Z., Lee V.M., Hersh L.B., Sapolsky R.M., Mirnics K., and Sisodia S.S. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120 (2005) 701-713
28. Lee V.M., Goedert M., and Trojanowski J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24 (2001) 1121-1159
29. Li L., and Cohen S.N. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85 (1996) 319-329
30. Lih C.J., Wei W., and Cohen S.N. Txr1: a transcriptional regulator of thrombospondin-1 that modulates cellular sensitivity to taxanes. Genes Dev. 20 (2006) 2082-2095
31. Lin P., Li F., Zhang Y.W., Huang H., Tong G., Farquhar M.G., and Xu H. Calnuc binds to Alzheimer's beta-amyloid precursor protein and affects its biogenesis. J. Neurochem. 100 (2007) 1505-1514
32. Liu K., Li L., Nisson P.E., Gruber C., Jessee J., and Cohen S.N. Reversible tumorigenesis induced by deficiency of vasodilator-stimulated phosphoprotein. Mol. Cell. Biol. 19 (1999) 3696-3703
33. Liu K., Li L., and Cohen S.N. Antisense RNA-mediated deficiency of the calpain protease, nCL-4, in NIH3T3 cells is associated with neoplastic transformation and tumorigenesis. J. Biol. Chem. 275 (2000) 31093-31098
34. Liu K., Li L., Nisson P.E., Gruber C., Jessee J., and Cohen S.N. Neoplastic transformation and tumorigenesis associated with sam68 protein deficiency in cultured murine fibroblasts. J. Biol. Chem. 275 (2000) 40195-40201
35. Long M., Betran E., Thornton K., and Wang W. The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4 (2003) 865-875
36. Martinez A., Castro A., Dorronsoro I., and Alonso M. Glycogen synthase kinase 3 (GSK-3) inhibitors as new promising drugs for diabetes, neurodegeneration, cancer, and inflammation. Med. Res. Rev. 22 (2002) 373-384
37. Mathern G.W., Bertram III E.H., Babb T.L., Pretorius J.K., Kuhlman P.A., Spradlin S., and Mendoza D. In contrast to kindled seizures, the frequency of spontaneous epilepsy in the limbic status model correlates with greater aberrant fascia dentata excitatory and inhibitory axon sprouting, and increased staining for N-methyl-D-aspartate, AMPA and GABA(A) receptors. Neuroscience 77 (1997) 1003-1019
38. Medina M., and Castro A. Glycogen synthase kinase-3 (GSK-3) inhibitors reach the clinic. Curr. Opin. Drug Discov. Dev. 11 (2008) 533-543
39. Mighell A.J., Smith N.R., Robinson P.A., and Markham A.F. Vertebrate pseudogenes. FEBS Lett. 468 (2000) 109-114
40. Naviglio S., Caraglia M., Abbruzzese A., Chiosi E., Di Gesto D., Marra M., Romano M., Sorrentino A., Sorvillo L., Spina A., and Illiano G. Protein kinase A as a biological target in cancer therapy. Expert Opin. Ther. Targets 13 (2009) 83-92
41. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., and LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39 (2003) 409-421
42. Phiel C.J., Wilson C.A., Lee V.M., and Klein P.S. GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423 (2003) 435-439
43. Rost B., Yachdav G., and Liu J. The PredictProtein server. Nucleic Acids Res. 32 (2004) W321-W326
44. Takashima A., Yamaguchi H., Noguchi K., Michel G., Ishiguro K., Sato K., Hoshino T., Hoshi M., and Imahori K. Amyloid beta peptide induces cytoplasmic accumulation of amyloid protein precursor via tau protein kinase I/glycogen synthase kinase-3 beta in rat hippocampal neurons. Neurosci. Lett. 198 (1995) 83-86
45. Tanzi R.E., and Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120 (2005) 545-555
46. Taylor S.S., Kim C., Cheng C.Y., Brown S.H., Wu J., and Kannan N. Signaling through cAMP and cAMP-dependent protein kinase: diverse strategies for drug design. Biochim. Biophys. Acta 1784 (2008) 16-26
47. Ueda S., Nakai S., Nishida Y., Hisajima H., and Honjo T. Long terminal repeat-like elements flank a human immunoglobulin epsilon pseudogene that lacks introns. EMBO J. 1 (1982) 1539-1544
48. Vinckenbosch N., Dupanloup I., and Kaessmann H. Evolutionary fate of retroposed gene copies in the human genome. Proc. Natl. Acad. Sci. USA 103 (2006) 3220-3225
49. Wang R., Zhang Y.W., Zhang X., Liu R., Zhang X., Hong S., Xia K., Xia J., Zhang Z., and Xu H. Transcriptional regulation of APH-1A and increased gamma-secretase cleavage of APP and Notch by HIF-1 and hypoxia. FASEB J. 20 (2006) 1275-1277
50. Xu H., Sweeney D., Greengard P., and Gandy S. Metabolism of Alzheimer beta-amyloid precursor protein: regulation by protein kinase A in intact cells and in a cell-free system. Proc. Natl. Acad. Sci. USA 93 (1996) 4081-4084
51. Xu H., Sweeney D., Wang R., Thinakaran G., Lo A.C., Sisodia S.S., Greengard P., and Gandy S. Generation of Alzheimer beta-amyloid protein in the trans-Golgi network in the apparent absence of vesicle formation. Proc. Natl. Acad. Sci. USA 94 (1997) 3748-3752
52. Xu H., Gouras G.K., Greenfield J.P., Vincent B., Naslund J., Mazzarelli L., Fried G., Jovanovic J.N., Seeger M., Relkin N.R., et al. Estrogen reduces neuronal generation of Alzheimer beta-amyloid peptides. Nat. Med. 4 (1998) 447-451
53. York R.D., Molliver D.C., Grewal S.S., Stenberg P.E., McCleskey E.W., and Stork P.J. Role of phosphoinositide 3-kinase and endocytosis in nerve growth factor-induced extracellular signal-regulated kinase activation via Ras and Rap1. Mol. Cell. Biol. 20 (2000) 8069-8083
54. Zhang Y.W., and Xu H. Molecular and cellular mechanisms for Alzheimer's disease: understanding app metabolism. Curr. Mol. Med. 7 (2007) 687-696
55. Zhang Z., Harrison P., and Gerstein M. Identification and analysis of over 2000 ribosomal protein pseudogenes in the human genome. Genome Res. 12 (2002) 1466-1482
56. Zhang Z., Carriero N., and Gerstein M. Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet. 20 (2004) 62-67
57. Zhang X., Zhou K., Wang R., Cui J., Lipton S.A., Liao F.F., Xu H., and Zhang Y.W. Hypoxia-inducible factor 1alpha (HIF-1alpha)-mediated hypoxia increases BACE1 expression and beta-amyloid generation. J. Biol. Chem. 282 (2007) 10873-10880