PPP4R2 regulates neuronal cell differentiation and survival, functionally cooperating with SMN

European Journal of Cell Biology

Volumn 91, Issue 8, 2012, Pages 662-674

  Bosio, Ylenia ^a   Berto, Gaia ^a   Camera, Paola ^a   Bianchi, Federico ^a   Ambrogio, Chiara ^a   Claus, Peter ^b   Di Cunto, Ferdinando ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Apoptosis; Neuronal differentiation; Protein phosphatase 4; SMN

Indexed keywords

DNA; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN PHOSPHATASE 4R2; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL LINE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MOLECULAR DYNAMICS; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL SURVIVAL; DNA DAMAGE; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HIPPOCAMPUS; HUMANS; MICE; NEUROGENESIS; NEURONS; PC12 CELLS; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; RATS; SURVIVAL OF MOTOR NEURON 1 PROTEIN; TRANSFECTION;

RATTUS;

EID: 84861713816     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2012.03.002     Document Type: Article

References (54)

1. Banker G., Goslin K. Developments in neuronal cell culture. Nature 1988, 336:185-186.
2. Baumer D., Lee S., Nicholson G., Davies J.L., Parkinson N.J., Murray L.M., Gillingwater T.H., Ansorge O., Davies K.E., Talbot K. Alternative splicing events are a late feature of pathology in a mouse model of spinal muscular atrophy. PLoS Genet. 2009, 5:e1000773.
3. Bebee T.W., Gladman J.T., Chandler D.S. Splicing regulation of the survival motor neuron genes and implications for treatment of spinal muscular atrophy. Front. Biosci. 2010, 15:1191-1204.
4. Boulisfane N., Choleza M., Rage F., Neel H., Soret J., Bordonne R. Impaired minor tri-snRNP assembly generates differential splicing defects of U12-type introns in lymphoblasts derived from a type I SMA patient. Hum. Mol. Genet. 2011, 20:641-648.
5. Bowerman M., Shafey D., Kothary R. Smn depletion alters Profilin II expression and leads to upregulation of the RhoA/ROCK pathway and defects in neuronal integrity. J. Mol. Neurosci. 2007, 32:120-131.
6. Bradke F., Dotti C.G. Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 1997, 19:1175-1186.
7. Broccolini A., Engel W.K., Askanas V. Localization of survival motor neuron protein in human apoptotic-like and regenerating muscle fibers, and neuromuscular junctions. Neuroreport 1999, 10:1637-1641.
8. Burghes A.H., Beattie C.E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick?. Nat. Rev. Neurosci. 2009, 10:597-609.
9. Carnegie G.K., Sleeman J.E., Morrice N., Hastie C.J., Peggie M.W., Philp A., Lamond A.I., Cohen P.T. Protein phosphatase 4 interacts with the Survival of Motor Neurons complex and enhances the temporal localisation of snRNPs. J. Cell Sci. 2003, 116:1905-1913.
10. Cashman N.R., Durham H.D., Blusztajn J.K., Oda K., Tabira T., Shaw I.T., Dahrouge S., Antel J.P. Neuroblastoma×spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 1992, 194:209-221.
11. Cauchi R.J. SMN and Gemins: 'we are family' ... or are we?: insights into the partnership between Gemins and the spinal muscular atrophy disease protein SMN. Bioessays 2010, 32:1077-1089.
12. Chari A., Golas M.M., Klingenhager M., Neuenkirchen N., Sander B., Englbrecht C., Sickmann A., Stark H., Fischer U. An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs. Cell 2008, 135:497-509.
13. Chari A., Paknia E., Fischer U. The role of RNP biogenesis in spinal muscular atrophy. Curr. Opin. Cell Biol. 2009, 21:387-393.
14. Cohen P.T., Philp A., Vazquez-Martin C. Protein phosphatase 4 - from obscurity to vital functions. FEBS Lett. 2005, 579:3278-3286.
15. Fanarraga M.L., Avila J., Zabala J.C. Expression of unphosphorylated class III beta-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur. J. Neurosci. 1999, 11:516-527.
16. Gabanella F., Butchbach M.E., Saieva L., Carissimi C., Burghes A.H., Pellizzoni L. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS ONE 2007, 2:e921.
17. Gingras A.C., Caballero M., Zarske M., Sanchez A., Hazbun T.R., Fields S., Sonenberg N., Hafen E., Raught B., Aebersold R. A novel, evolutionarily conserved protein phosphatase complex involved in cisplatin sensitivity. Mol. Cell. Proteomics 2005, 4:1725-1740.
18. Han X., Gomes J.E., Birmingham C.L., Pintard L., Sugimoto A., Mains P.E. The role of protein phosphatase 4 in regulating microtubule severing in the Caenorhabditis elegans embryo. Genetics 2009, 181:933-943.
19. Hastie C.J., Carnegie G.K., Morrice N., Cohen P.T. A novel 50kDa protein forms complexes with protein phosphatase 4 and is located at centrosomal microtubule organizing centres. Biochem. J 2000, 347(Pt 3):845-855.
20. Hastie C.J., Vazquez-Martin C., Philp A., Stark M.J., Cohen P.T. The Saccharomyces cerevisiae orthologue of the human protein phosphatase 4 core regulatory subunit R2 confers resistance to the anticancer drug cisplatin. FEBS J. 2006, 273:3322-3334.
21. Lee D.H., Pan Y., Kanner S., Sung P., Borowiec J.A., Chowdhury D. A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nat. Struct. Mol. Biol. 2010, 17:365-372.
22. Lefebvre S., Burglen L., Reboullet S., Clermont O., Burlet P., Viollet L., Benichou B., Cruaud C., Millasseau P., Zeviani M., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
23. Lorson C.L., Rindt H., Shababi M. Spinal muscular atrophy: mechanisms and therapeutic strategies. Hum. Mol. Genet. 2010, 19:R111-R118.
24. Lorson C.L., Strasswimmer J., Yao J.M., Baleja J.D., Hahnen E., Wirth B., Le T., Burghes A.H., Androphy E.J. SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat. Genet. 1998, 19:63-66.
25. Martin-Granados C., Philp A., Oxenham S.K., Prescott A.R., Cohen P.T. Depletion of protein phosphatase 4 in human cells reveals essential roles in centrosome maturation, cell migration and the regulation of Rho GTPases. Int. J. Biochem. Cell Biol. 2008, 40:2315-2332.
26. Miguel-Aliaga I., Chan Y.B., Davies K.E., van den Heuvel M. Disruption of SMN function by ectopic expression of the human SMN gene in Drosophila. FEBS Lett. 2000, 486:99-102.
27. Miguel-Aliaga I., Culetto E., Walker D.S., Baylis H.A., Sattelle D.B., Davies K.E. The Caenorhabditis elegans orthologue of the human gene responsible for spinal muscular atrophy is a maternal product critical for germline maturation and embryonic viability. Hum. Mol. Genet. 1999, 8:2133-2143.
28. Mourtada-Maarabouni M., Kirkham L., Jenkins B., Rayner J., Gonda T.J., Starr R., Trayner I., Farzaneh F., Williams G.T. Functional expression cloning reveals proapoptotic role for protein phosphatase 4. Cell Death Differ. 2003, 10:1016-1024.
29. Nolle A., Zeug A., van Bergeijk J., Tonges L., Gerhard R., Brinkmann H., Al Rayes S., Hensel N., Schill Y., Apkhazava D., et al. The spinal muscular atrophy disease protein SMN is linked to the Rho-kinase pathway via Profilin. Hum. Mol. Genet. 2011, 20:4865-4878.
30. Otter S., Grimmler M., Neuenkirchen N., Chari A., Sickmann A., Fischer U. A comprehensive interaction map of the human survival of motor neuron (SMN) complex. J. Biol. Chem. 2007, 282:5825-5833.
31. Paushkin S., Gubitz A.K., Massenet S., Dreyfuss G. The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 2002, 14:305-312.
32. Pellizzoni L. Chaperoning ribonucleoprotein biogenesis in health and disease. EMBO Rep. 2007, 8:340-345.
33. Rossoll W., Jablonka S., Andreassi C., Kroning A.K., Karle K., Monani U.R., Sendtner M. Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol. 2003, 163:801-812.
34. Schrank B., Gotz R., Gunnersen J.M., Ure J.M., Toyka K.V., Smith A.G., Sendtner M. Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9920-9925.
35. Shanmugarajan S., Tsuruga E., Swoboda K.J., Maria B.L., Ries W.L., Reddy S.V. Bone loss in survival motor neuron (Smn(-/-) SMN2) genetic mouse model of spinal muscular atrophy. J. Pathol. 2009, 219:52-60.
36. Shui J.W., Hu M.C., Tan T.H. Conditional knockout mice reveal an essential role of protein phosphatase 4 in thymocyte development and pre-T-cell receptor signaling. Mol. Cell. Biol. 2007, 27:79-91.
37. Silva J.M., Li M.Z., Chang K., Ge W., Golding M.C., Rickles R.J., Siolas D., Hu G., Paddison P.J., Schlabach M.R., et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 2005, 37:1281-1288.
38. Sleigh J.N., Gillingwater T.H., Talbot K. The contribution of mouse models to understanding the pathogenesis of spinal muscular atrophy. Dis. Model Mech. 2011, 4:457-467.
39. Sternberger L.A., Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:6126-6130.
40. Sumner C.J. Molecular mechanisms of spinal muscular atrophy. J. Child Neurol. 2007, 22:979-989.
41. Swoboda K.J., Prior T.W., Scott C.B., McNaught T.P., Wride M.C., Reyna S.P., Bromberg M.B. Natural history of denervation in SMA: relation to age, SMN2 copy number, and function. Ann. Neurol. 2005, 57:704-712.
42. Toyo-oka K., Mori D., Yano Y., Shiota M., Iwao H., Goto H., Inagaki M., Hiraiwa N., Muramatsu M., Wynshaw-Boris A., et al. Protein phosphatase 4 catalytic subunit regulates Cdk1 activity and microtubule organization via NDEL1 dephosphorylation. J. Cell Biol. 2008, 180:1133-1147.
43. Trulzsch B., Garnett C., Davies K., Wood M. Knockdown of SMN by RNA interference induces apoptosis in differentiated P19 neural stem cells. Brain Res. 2007, 1183:1-9.
44. van Bergeijk J., Rydel-Konecke K., Grothe C., Claus P. The spinal muscular atrophy gene product regulates neurite outgrowth: importance of the C terminus. FASEB J. 2007, 21:1492-1502.
45. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649.
46. Vitte J.M., Davoult B., Roblot N., Mayer M., Joshi V., Courageot S., Tronche F., Vadrot J., Moreau M.H., Kemeny F., Melki J. Deletion of murine Smn exon 7 directed to liver leads to severe defect of liver development associated with iron overload. Am. J. Pathol. 2004, 165:1731-1741.
47. Vyas S., Bechade C., Riveau B., Downward J., Triller A. Involvement of survival motor neuron (SMN) protein in cell death. Hum. Mol. Genet. 2002, 11:2751-2764.
48. Will C.L., Luhrmann R. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 2001, 13:290-301.
49. Winkler C., Eggert C., Gradl D., Meister G., Giegerich M., Wedlich D., Laggerbauer B., Fischer U. Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev. 2005, 19:2320-2330.
50. Yong J., Wan L., Dreyfuss G. Why do cells need an assembly machine for RNA-protein complexes?. Trends Cell Biol. 2004, 14:226-232.
51. Young P.J., Man N.T., Lorson C.L., Le T.T., Androphy E.J., Burghes A.H., Morris G.E. The exon 2b region of the spinal muscular atrophy protein, SMN, is involved in self-association and SIP1 binding. Hum. Mol. Genet. 2000, 9:2869-2877.
52. Zhang H., Xing L., Rossoll W., Wichterle H., Singer R.H., Bassell G.J. Multiprotein complexes of the survival of motor neuron protein SMN with Gemins traffic to neuronal processes and growth cones of motor neurons. J. Neurosci. 2006, 26:8622-8632.
53. Zhang H.L., Pan F., Hong D., Shenoy S.M., Singer R.H., Bassell G.J. Active transport of the survival motor neuron protein and the role of exon-7 in cytoplasmic localization. J. Neurosci. 2003, 23:6627-6637.
54. Zhang Z., Lotti F., Dittmar K., Younis I., Wan L., Kasim M., Dreyfuss G. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 2008, 133:585-600.