Functional interactions between BM88/Cend1, Ran-binding protein M and Dyrk1B kinase affect cyclin D1 levels and cell cycle progression/exit in mouse

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Tsioras, Konstantinos ^a   Papastefanaki, Florentia ^a   Politis, Panagiotis K ^b   Matsas, Rebecca ^a   Gaitanou, Maria ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BETA III TUBULIN; BETA TUBULIN; CELL CYCLE EXIT AND NEURONAL DIFFERENTIATION 1 PROTIEN; CELL CYCLE PROTEIN; COMPLEMENTARY DNA; CYCLIN D1; DYRK1B KINASE; MESSENGER RNA; PHOSPHOTRANSFERASE; RAN BINDING PROTEIN M; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING COMPETITION; BRAIN CELL CULTURE; BRAIN HOMOGENATE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME DEGRADATION; ENZYME METABOLISM; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR STABILITY; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BASE SEQUENCE; CELL CYCLE; CELL LINE, TUMOR; CYCLIN D1; CYTOSKELETAL PROTEINS; DNA PRIMERS; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; NEUROBLASTOMA; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84896712829     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082172     Document Type: Article

References (58)

1. Nguyen L, Besson A, Roberts JM, Guillemot F (2006) Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5: 2314-2318. doi:10.4161/cc.5.20.3381. PubMed: 17102618. (Pubitemid 44785839)
2. Ohnuma S, Harris WA (2003) Neurogenesis and the cell cycle. Neuron 40: 199-208. doi:10.1016/S0896-6273(03)00632-9. PubMed: 14556704. (Pubitemid 37244092)
3. Pitto L, Cremisi F (2010) Timing neurogenesis by cell cycle? Cell Cycle 9: 434-435. doi:10.4161/cc.9.3.10762. PubMed: 20090420.
4. Politis PK, Thomaidou D, Matsas R (2008) Coordination of cell cycle exit and differentiation of neuronal progenitors. Cell Cycle 7: 691-697. doi:10.4161/cc.7.6.5550. PubMed: 18239460. (Pubitemid 351520027)
5. Katsimpardi L, Gaitanou M, Malnou CE, Lledo PM, Charneau P et al. (2008) BM88/Cend1 expression levels are critical for proliferation and differentiation of subventricular zone-derived neural precursor cells. Stem Cells 26: 1796-1807. doi:10.1634/stemcells.2007-0921. PubMed: 18499894.
6. Makri G, Lavdas AA, Katsimpardi L, Charneau P, Thomaidou D et al. (2010) Transplantation of embryonic neural stem/precursor cells overexpressing BM88/Cend1 enhances the generation of neuronal cells in the injured mouse cortex. Stem Cells 28: 127-139. PubMed: 19911428.
7. Politis PK, Makri G, Thomaidou D, Geissen M, Rohrer H et al. (2007) BM88/CEND1 coordinates cell cycle exit and differentiation of neuronal precursors. Proc Natl Acad Sci U S A 104: 17861-17866. doi:10.1073/pnas. 0610973104. PubMed: 17971443. (Pubitemid 350210925)
8. Koutmani Y, Hurel C, Patsavoudi E, Hack M, Gotz M et al. (2004) BM88 is an early marker of proliferating precursor cells that will differentiate into the neuronal lineage. Eur J Neurosci 20: 2509-2523. doi:10.1111/j.1460-9568. 2004.03724.x. PubMed: 15548196. (Pubitemid 39573768)
9. Politis PK, Rohrer H, Matsas R (2007) Expression pattern of BM88 in the developing nervous system of the chick and mouse embryo. Gene Expr Patterns 7: 165-177. doi:10.1016/j.modgep.2006.06.007. PubMed: 16949349. (Pubitemid 44712737)
10. Sergaki MC, Guillemot F, Matsas R (2010) Impaired cerebellar development and deficits in motor coordination in mice lacking the neuronal protein BM88/Cend1. Mol Cell Neurosci 44: 15-29. doi: 10.1016/j.mcn.2010.01.011. PubMed: 20153830.
11. Cesi V, Tanno B, Vitali R, Mancini C, Giuffrida ML et al. (2002) Cyclin D1-dependent regulation of B-myb activity in early stages of neuroblastoma differentiation. Cell Death Differ 9: 1232-1239. doi: 10.1038/sj.cdd.4401103. PubMed: 12404122. (Pubitemid 35331770)
12. Georgopoulou N, Hurel C, Politis PK, Gaitanou M, Matsas R et al. (2006) BM88 is a dual function molecule inducing cell cycle exit and neuronal differentiation of neuroblastoma cells via cyclin D1 downregulation and retinoblastoma protein hypophosphorylation. J Biol Chem 281: 33606-33620. doi:10.1074/jbc.M602689200. PubMed: 16893893. (Pubitemid 46036741)
13. Weng L, Lin YF, Li AL, Wang CE, Yan S et al. (2013) Loss of Ahi1 Affects Early Development by Impairing BM88/Cend1-Mediated Neuronal. Differentiation - J Neuroscience 33: 8172-8184.
14. Poirier Y, Jolicoeur P (1989) Distinct helper virus requirements for Abelson murine leukemia virus-induced pre-B- and T-cell lymphomas. J Virol 63: 2088-2098. PubMed: 2539505. (Pubitemid 19107806)
15. Gitten J, Dede D, Fennell E, Quisling R, Maria BL (1998) Neurobehavioral development in Joubert syndrome. J Child Neurol 13: 391-397. doi:10.1177/088307389801300806. PubMed: 9721895. (Pubitemid 28412965)
16. Maria BL, Boltshauser E, Palmer SC, Tran TX (1999) Clinical features and revised diagnostic criteria in Joubert syndrome. J Child Neurol 14: 581-590; discussion: 10488903.
17. Koshy B, Oommen SP, Jasper S, Danda S, Surendrababu NR (2010) Development and dysmorphism in Joubert syndrome - short case series from India. J Trop Pediatr 56: 209-212. doi:10.1093/tropej/fmp084. PubMed: 19755534.
18. Holroyd S, Reiss AL, Bryan RN (1991) Autistic features in Joubert syndrome: a genetic disorder with agenesis of the cerebellar vermis. Biol Psychiatry 29: 287-294. doi:10.1016/0006-3223(91)91291-X. PubMed: 2015333.
19. Amann-Zalcenstein D, Avidan N, Kanyas K, Ebstein RP, Kohn Y et al. (2006) AHI1, a pivotal neurodevelopmental gene, and C6orf217 are associated with susceptibility to schizophrenia. Eur J Hum Genet 14: 1111-1119. doi:10.1038/sj.ejhg.5201675. PubMed: 16773125. (Pubitemid 44463970)
20. Ingason A, Giegling I, Cichon S, Hansen T, Rasmussen HB et al. (2010) A large replication study and meta-analysis in European samples provides further support for association of AHI1 markers with schizophrenia. Hum Mol Genet 19: 1379-1386. doi:10.1093/hmg/ddq009. PubMed: 20071346.
21. Ingason A, Sigmundsson T, Steinberg S, Sigurdsson E, Haraldsson M et al. (2007) Support for involvement of the AHI1 locus in schizophrenia. Eur J Hum Genet 15: 988-991. doi:10.1038/sj.ejhg.5201848. PubMed: 17473831.
22. Alvarez Retuerto AI, Cantor RM, Gleeson JG, Ustaszewska A, Schackwitz WS et al. (2008) Association of common variants in the Joubert syndrome gene (AHI1) with autism. Hum Mol Genet 17: 3887-3896. doi:10.1093/hmg/ddn291. PubMed: 18782849. (Pubitemid 352762851)
23. Torri F, Akelai A, Lupoli S, Sironi M, Amann-Zalcenstein D et al. (2010) Fine mapping of AHI1 as a schizophrenia susceptibility gene: from association to evolutionary evidence. FASEB J 24: 3066-3082. doi: 10.1096/fj.09-152611. PubMed: 20371615.
24. Gaitanou M, Buanne P, Pappa C, Georgopoulou N, Mamalaki A et al. (2001) Cloning, expression and localization of human BM88 shows that it maps to chromosome 11p15.5, a region implicated in Beckwith-Wiedemann syndrome and tumorigenesis. Biochem J 355: 715-724. PubMed: 11311134. (Pubitemid 32434089)
25. Mamalaki A, Boutou E, Hurel C, Patsavoudi E, Tzartos S et al. (1995) The BM88 antigen, a novel neuron-specific molecule, enhances the differentiation of mouse neuroblastoma cells. J Biol Chem 270: 14201-14208. doi:10.1074/jbc.270.23. 14201. PubMed: 7775480.
26. Patsavoudi E, Merkouri E, Thomaidou D, Sandillon F, Alonso G et al. (1995) Characterization and localization of the BM88 antigen in the developing and adult rat brain. J Neurosci Res 40: 506-518. doi: 10.1002/jnr.490400410. PubMed: 7616611.
27. Murrin LC, Talbot JN (2007) RanBPM, a scaffolding protein in the immune and nervous systems. J Neuroimmune Pharmacol 2: 290-295. doi:10.1007/s11481-007- 9079-x. PubMed: 18040864.
28. Chang Y, Paramasivam M, Girgenti MJ, Walikonis RS, Bianchi E et al. (2010) RanBPM regulates the progression of neuronal precursors through M-phase at the surface of the neocortical ventricular zone. Dev Neurobiol 70: 1-15. PubMed: 19790105.
29. Zou Y, Lim S, Lee K, Deng X, Friedman E (2003) Serine/threonine kinase Mirk/Dyrk1B is an inhibitor of epithelial cell migration and is negatively regulated by the Met adaptor Ran-binding protein M. J Biol Chem 278: 49573-49581. doi:10.1074/jbc.M307556200. PubMed: 14500717.
30. Aranda S, Laguna A, de la Luna S (2011) DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J 25: 449-462. doi:10.1096/fj.10-165837. PubMed: 21048044.
31. Mercer SE, Friedman E (2006) Mirk/Dyrk1B: a multifunctional dual-specificity kinase involved in growth arrest, differentiation, and cell survival. Cell Biochem Biophys 45: 303-315. doi:10.1385/CBB:45:3:303. PubMed: 16845176. (Pubitemid 44127946)
32. Hämmerle B, Ulin E, Guimera J, Becker W, Guillemot F et al. (2011) Transient expression of Mnb/Dyrk1a couples cell cycle exit and differentiation of neuronal precursors by inducing p27KIP1 expression and suppressing NOTCH signaling. Development 138: 2543-2554. doi: 10.1242/dev.066167. PubMed: 21610031.
33. Tejedor FJ, Hämmerle B (2011) MNB/DYRK1A as a multiple regulator of neuronal development. FEBS J 278: 223-235. doi:10.1111/j.1742-4658.2010.07954.x. PubMed: 21156027.
34. Yabut O, Domogauer J, D'Arcangelo G (2010) Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells. J Neurosci 30: 4004-4014. doi:10.1523/JNEUROSCI.4711-09.2010. PubMed: 20237271.
35. Takahashi-Yanaga F, Mori J, Matsuzaki E, Watanabe Y, Hirata M et al. (2006) Involvement of GSK-3beta and DYRK1B in differentiation-inducing factor-3-induced phosphorylation of cyclin D1 in HeLa cells. J Biol Chem 281: 38489-38497. doi:10.1074/jbc.M605205200. PubMed: 17046823. (Pubitemid 46041973)
36. Zou Y, Ewton DZ, Deng X, Mercer SE, Friedman E (2004) Mirk/dyrk1B kinase destabilizes cyclin D1 by phosphorylation at threonine 288. J Biol Chem 279: 27790-27798. doi:10.1074/jbc.M403042200. PubMed: 15075324. (Pubitemid 38812621)
37. Jin K, Ewton DZ, Park S, Hu J, Friedman E (2009) Mirk regulates the exit of colon cancer cells from quiescence. J Biol Chem 284: 22916-22925. doi:10.1074/jbc.M109.035519. PubMed: 19542220.
38. Gaitanou M, Mamalaki A, Merkouri E, Matsas R (1997) Purification and cDNA cloning of mouse BM89 antigen shows that it is identical with the synaptic vesicle protein synaptophysin. J Neurosci Res 48: 507-514. doi:10.1002/(SICI) 1097-4547(19970615)48:6. PubMed: 9210520. (Pubitemid 27276680)
39. Riboni L, Prinetti A, Bassi R, Caminiti A, Tettamanti G (1995) A mediator role of ceramide in the regulation of neuroblastoma Neuro2a cell differentiation. J Biol Chem 270: 26868-26875. doi:10.1074/jbc.270.45.26868. PubMed: 7592930.
40. Sutherland HG, Lam YW, Briers S, Lamond AI, Bickmore WA (2004) 3D3/lyric: a novel transmembrane protein of the endoplasmic reticulum and nuclear envelope, which is also present in the nucleolus. Exp Cell Res 294: 94-105. doi:10.1016/j.yexcr.2003.11.020. PubMed: 14980505. (Pubitemid 38229784)
41. Foskolou IP, Stellas D, Rozani I, Lavigne MD, Politis PK (2013) Prox1 suppresses the proliferation of neuroblastoma cells via a dual action in p27-Kip1 and Cdc25A. Oncogene 32: 947-960. doi:10.1038/onc.2012.129. PubMed: 22508481.
42. Kaltezioti V, Kouroupi G, Oikonomaki M, Mantouvalou E, Stergiopoulos A et al. (2010) Prox1 regulates the notch1-mediated inhibition of neurogenesis. PLoS Biol 8: e1000565. PubMed: 21203589.
43. Denti S, Sirri A, Cheli A, Rogge L, Innamorati G et al. (2004) RanBPM is a phosphoprotein that associates with the plasma membrane and interacts with the integrin LFA-1. J Biol Chem 279: 13027-13034. PubMed: 14722085. (Pubitemid 38445880)
44. Nakamura M, Masuda H, Horii J, Kuma Ki, Yokoyama N et al. (1998) When overexpressed, a novel centrosomal protein, RanBPM, causes ectopic microtubule nucleation similar to gamma-tubulin. J Cell Biol 143: 1041-1052. doi:10.1083/jcb.143.4.1041. PubMed: 9817760. (Pubitemid 28547402)
45. Nishitani H, Hirose E, Uchimura Y, Nakamura M, Umeda M et al. (2001) Full-sized RanBPM cDNA encodes a protein possessing a long stretch of proline and glutamine within the N-terminal region, comprising a large protein complex. Gene 272: 25-33. doi:10.1016/S0378-1119(01)00553-4. PubMed: 11470507. (Pubitemid 32695395)
46. Politis PK, Akrivou S, Hurel C, Papadodima O, Matsas R (2008) BM88/Cend1 is involved in histone deacetylase inhibition-mediated growth arrest and differentiation of neuroblastoma cells. FEBS Lett 582: 741-748. doi:10.1016/j.febslet.2008.01.052. PubMed: 18258204.
47. Alao JP (2007) The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol Cancer 6: 24. doi:10.1158/1535-7163.MCT-06-0443. PubMed: 17407548.
48. Martí E, Altafaj X, Dierssen M, de la Luna S, Fotaki V et al. (2003) Dyrk1A expression pattern supports specific roles of this kinase in the adult central nervous system. Brain Res 964: 250-263. doi:10.1016/S0006-8993(02) 04069-6. PubMed: 12576186. (Pubitemid 36165150)
49. Frost D, Meechoovet B, Wang T, Gately S, Giorgetti M et al. (2011) beta-carboline compounds, including harmine, inhibit DYRK1A and tau phosphorylation at multiple Alzheimer's disease-related sites. PLOS ONE 6: e19264. doi:10.1371/journal.pone.0019264. PubMed: 21573099.
50. Wakabayashi T, Kosaka J, Mochii M, Miki Y, Mori T et al. (2010) C38, equivalent to BM88, is developmentally expressed in maturing retinal neurons and enhances neuronal maturation. J Neurochem 112: 1235-1248. doi:10.1111/j.1471- 4159.2009.06536.x. PubMed: 20002527.
51. Das G, Choi Y, Sicinski P, Levine EM (2009) Cyclin D1 fine-tunes the neurogenic output of embryonic retinal progenitor cells. Neural Dev 4: 15. doi:10.1186/1749-8104-4-15. PubMed: 19416500.
52. Sumrejkanchanakij P, Tamamori-Adachi M, Matsunaga Y, Eto K, Ikeda MA (2003) Role of cyclin D1 cytoplasmic sequestration in the survival of postmitotic neurons. Oncogene 22: 8723-8730. doi:10.1038/sj.onc.1206870. PubMed: 14647467. (Pubitemid 38010496)
53. Wang Y, Marion Schneider E, Li X, Duttenhöfer I, Debatin K et al. (2002) HIPK2 associates with RanBPM. Biochem Biophys Res Commun 297: 148-153. doi:10.1016/S0006-291X(02)02020-X. PubMed: 12220523.
54. Kramer S, Ozaki T, Miyazaki K, Kato C, Hanamoto T et al. (2005) Protein stability and function of p73 are modulated by a physical interaction with RanBPM in mammalian cultured cells. Oncogene 24: 938-944. doi:10.1038/sj.onc. 1208257. PubMed: 15558019. (Pubitemid 40216101)
55. Suresh B, Ramakrishna S, Kim YS, Kim SM, Kim MS et al. (2010) Stability and function of mammalian lethal giant larvae-1 oncoprotein are regulated by the scaffolding protein RanBPM. J Biol Chem 285: 35340-35349. doi:10.1074/jbc.M110. 156836. PubMed: 20829363.
56. Suresh B, Ramakrishna S, Baek KH (2012) Diverse roles of the scaffolding protein RanBPM. Drug Discov Today, 17: 379-87. PubMed: 22094242.
57. Brancati F, Dallapiccola B, Valente EM (2010) Joubert Syndrome and related disorders. Orphanet J Rare Dis 5: 20. doi:10.1186/1750-1172-5-S1-P20. PubMed: 20615230.
58. Ferland RJ, Eyaid W, Collura RV, Tully LD, Hill RS et al. (2004) Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nat Genet 36: 1008-1013. doi: 10.1038/ng1419. PubMed: 15322546. (Pubitemid 39167500)