Regulation of neuronal differentiation by proteins associated with nuclear bodies

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Förthmann, Benjamin ^a,b   Van Bergeijk, Jeroen ^a   Lee, Yu Wei ^c   Lub̈ben, Verena ^a   Schill, Yvonne ^a   Brinkmann, Hella ^a   Ratzka, Andreas ^a   Stachowiak, Michal K ^c   Hebert, Michael ^d   Grothe, Claudia ^a,b   Claus, Peter ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c UNIVERSITY AT BUFFALO   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 23; ISOPROTEIN; NUCLEAR PROTEIN; PROTEIN COILIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL NUCLEUS INCLUSION BODY; COILED BODY; CONTROLLED STUDY; CORRELATION ANALYSIS; GEMINI OF COILED BODIES; GROWTH INHIBITION; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; TISSUE DIFFERENTIATION;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; COILED BODIES; FIBROBLAST GROWTH FACTOR 2; HUMANS; NEURITES; NEUROGENESIS; NEURONS; NUCLEAR PROTEINS; PC12 CELLS; PROTEIN BINDING; RATS; SMN COMPLEX PROTEINS;

EID: 84893052860     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082871     Document Type: Article

References (67)

1. Dundr M, Misteli T (2001) Functional architecture in the cell nucleus. Biochem J 356: 297-310.
2. Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK (2009) Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev Cell 17: 639-647.
3. Cajal Ry (1903) Un sencillo metodo de coloracion selectiva del reticulo protoplasmico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Lab Invest Biol Univ (Madrid): 129-143.
4. Gall JG (2000) Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 16: 273-300.
5. Liu Q, Dreyfuss G (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J 15: 3555-3565.
6. Lefebvre S, Burlet P, Liu Q, Bertrandy S, Clermont O, et al. (1997) Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 16: 265-269.
7. Forthmann B, Brinkmann H, Ratzka A, Stachowiak MK, Grothe C, et al. (2013) Immobile survival of motoneuron (SMN) protein stored in Cajal bodies can be mobilized by protein interactions. Cell Mol Life Sci 70: 2555-2568.
8. Sorensen V, Nilsen T, Wiedlocha A (2006) Functional diversity of FGF-2 isoforms by intracellular sorting. Bioessays 28: 504-514.
9. Claus P, Bruns AF, Grothe C (2004) Fibroblast growth factor-2(23) binds directly to the survival of motoneuron protein and is associated with small nuclear RNAs. Biochem J 384: 559-565.
10. Claus P, Doring F, Gringel S, Muller-Ostermeyer F, Fuhlrott J, et al. (2003) Differential intranuclear localization of fibroblast growth factor-2 isoforms and specific interaction with the survival of motoneuron protein. J Biol Chem 278: 479-485.
11. Bruns AF, van Bergeijk J, Lorbeer C, Nolle A, Jungnickel J, et al. (2009) Fibroblast growth factor-2 regulates the stability of nuclear bodies. Proc Natl Acad Sci U S A 106: 12747-12752.
12. Reilly JF, Maher PA (2001) Importin beta-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J Cell Biol 152: 1307-1312.
13. Peng H, Myers J, Fang X, Stachowiak EK, Maher PA, et al. (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J Neurochem 81: 506-524.
14. Stachowiak MK, Fang X, Myers JM, Dunham SM, Berezney R, et al. (2003) Integrative nuclear FGFR1 signaling (INFS) as a part of a universal "feed-forward-and-gate" signaling module that controls cell growth and differentiation. J Cell Biochem 90: 662-691.
15. Stachowiak MK, Maher PA, Stachowiak EK (2007) Integrative nuclear signaling in cell development - a role for FGF receptor-1. DNA Cell Biol 26: 811-826.
16. Andrade LE, Chan EK, Raska I, Peebles CL, Roos G, et al. (1991) Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med 173: 1407-1419.
17. Hebert MD, Szymczyk PW, Shpargel KB, Matera AG (2001) Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev 15: 2720-2729.
18. Lam YW, Lyon CE, Lamond AI (2002) Large-scale isolation of Cajal bodies from HeLa cells. Mol Biol Cell 13: 2461-2473.
19. Gilder AS, Do PM, Carrero ZI, Cosman AM, Broome HJ, et al. (2011) Coilin participates in the suppression of RNA polymerase I in response to cisplatin-induced DNA damage. Mol Biol Cell 22: 1070-1079.
20. Velma V, Carrero ZI, Cosman AM, Hebert MD (2010) Coilin interacts with Ku proteins and inhibits in vitro non-homologous DNA end joining. FEBS Lett 584: 4735-4739.
21. Morency E, Sabra M, Catez F, Texier P, Lomonte P (2007) A novel cell response triggered by interphase centromere structural instability. J Cell Biol 177: 757-768.
22. Broome HJ, Hebert MD (2012) In vitro RNase and nucleic acid binding activities implicate coilin in U snRNA processing. PLoS One 7: e36300.
23. Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, et al. (2001) Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Biol 154: 293-307.
24. Hebert MD, Shpargel KB, Ospina JK, Tucker KE, Matera AG (2002) Coilin methylation regulates nuclear body formation. Dev Cell 3: 329-337.
25. Tapia O, Bengoechea R, Berciano MT, Lafarga M (2010) Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma 119: 527-540.
26. Toyota CG, Davis MD, Cosman AM, Hebert MD (2010) Coilin phosphorylation mediates interaction with SMN and SmB'. Chromosoma 119: 205-215.
27. Gangwani L, Mikrut M, Theroux S, Sharma M, Davis RJ (2001) Spinal muscular atrophy disrupts the interaction of ZPR1 with the SMN protein. Nat Cell Biol 3: 376-383.
28. Mahmoudi S, Henriksson S, Weibrecht I, Smith S, Soderberg O, et al. (2010) WRAP53 is essential for Cajal body formation and for targeting the survival of motor neuron complex to Cajal bodies. PLoS Biol 8: e1000521.
29. Takata H, Nishijima H, Maeshima K, Shibahara K (2012) The integrator complex is required for integrity of Cajal bodies. J Cell Sci 125: 166-175.
30. van Bergeijk J, Rydel-Konecke K, Grothe C, Claus P (2007) The spinal muscular atrophy gene product regulates neurite outgrowth: importance of the C terminus. FASEB J 21: 1492-1502.
31. Baron O, Forthmann B, Lee YW, Terranova C, Ratzka A, et al. (2012) Cooperation of nuclear fibroblast growth factor receptor 1 and Nurr1 offers new interactive mechanism in postmitotic development of mesencephalic dopaminergic neurons. J Biol Chem 287: 19827-19840.
32. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
33. Maira M, Martens C, Philips A, Drouin J (1999) Heterodimerization between members of the Nur subfamily of orphan nuclear receptors as a novel mechanism for gene activation. Mol Cell Biol 19: 7549-7557.
34. Kim EL, Esparza FM, Stachowiak MK (1996) The roles of CRE, TRE, and TRE-adjacent S1 nuclease sensitive element in the regulation of tyrosine hydroxylase gene promoter activity by angiotensin II. J Neurochem 67: 26-36.
35. Lee YW, Terranova C, Birkaya B, Narla S, Kehoe D, et al. (2012) A novel nuclear FGF Receptor-1 partnership with retinoid and Nur receptors during developmental gene programming of embryonic stem cells. J Cell Biochem 113: 2920-2936.
36. Lee JH, Kim KT (2004) Induction of cyclin-dependent kinase 5 and its activator p35 through the extracellular-signal-regulated kinase and protein kinase A pathways during retinoic-acid mediated neuronal differentiation in human neuroblastoma SK-N-BE(2)C cells. J Neurochem 91: 634-647.
37. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73: 2424-2428.
38. van Bergeijk J, Haastert K, Grothe C, Claus P (2006) Valproic acid promotes neurite outgrowth in PC12 cells independent from regulation of the survival of motoneuron protein. Chem Biol Drug Des 67: 244-247.
39. Farias GG, Valles AS, Colombres M, Godoy JA, Toledo EM, et al. (2007) Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 27: 5313-5325.
40. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, et al. (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24: 4070-4081.
41. Grothe C, Meisinger C, Holzschuh J, Wewetzer K, Cattini P (1998) Overexpression of the 18 kD and 21/23 kD fibroblast growth factor-2 isoforms in PC12 cells and Schwann cells results in altered cell morphology and growth. Brain Res Mol Brain Res 57: 97-105.
42. Muller-Ostermeyer F, Claus P, Grothe C (2001) Distinctive effects of rat fibroblast growth factor-2 isoforms on PC12 and Schwann cells. Growth Factors 19: 175-191.
43. Nolle A, Zeug A, van Bergeijk J, Tonges L, Gerhard R, et al. (2011) The spinal muscular atrophy disease protein SMN is linked to the Rho-kinase pathway via profilin. Hum Mol Genet 20: 4865-4878.
44. Rossoll W, Jablonka S, Andreassi C, Kroning AK, Karle K, et al. (2003) 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 163: 801-812.
45. Fang X, Stachowiak EK, Dunham-Ems SM, Klejbor I, Stachowiak MK (2005) Control of CREB-binding protein signaling by nuclear fibroblast growth factor receptor-1: a novel mechanism of gene regulation. J Biol Chem 280: 28451-28462.
46. Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, et al. (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276: 248-250.
47. Rohwedel J, Guan K, Wobus AM (1999) Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 165: 190-202.
48. Shpargel KB, Ospina JK, Tucker KE, Matera AG, Hebert MD (2003) Control of Cajal body number is mediated by the coilin C-terminus. J Cell Sci 116: 303-312.
49. Hebert MD, Matera AG (2000) Self-association of coilin reveals a common theme in nuclear body localization. Mol Biol Cell 11: 4159-4171.
50. Meisinger C, Grothe C (1997) Differential regulation of fibroblast growth factor (FGF)-2 and FGF receptor 1 mRNAs and FGF-2 isoforms in spinal ganglia and sciatic nerve after peripheral nerve lesion. J Neurochem 68: 1150-1158.
51. Jungnickel J, Haastert K, Grzybek M, Thau N, Lipokatic-Takacs E, et al. (2010) Mice lacking basic fibroblast growth factor showed faster sensory recovery. Exp Neurol 223: 166-172.
52. Jungnickel J, Claus P, Gransalke K, Timmer M, Grothe C (2004) Targeted disruption of the FGF-2 gene affects the response to peripheral nerve injury. Mol Cell Neurosci 25: 444-452.
53. Takizawa T, Meshorer E (2008) Chromatin and nuclear architecture in the nervous system. Trends Neurosci 31: 343-352.
54. Young PJ, Le TT, Dunckley M, Nguyen TM, Burghes AH, et al. (2001) Nuclear gems and Cajal (coiled) bodies in fetal tissues: nucleolar distribution of the spinal muscular atrophy protein, SMN. Exp Cell Res 265: 252-261.
55. Clelland AK, Kinnear NP, Oram L, Burza J, Sleeman JE (2009) The SMN protein is a key regulator of nuclear architecture in differentiating neuroblastoma cells. Traffic 10: 1585-1598.
56. Janevski J, Park PC, De Boni U (1997) Changes in morphology and spatial position of coiled bodies during NGF-induced neuronal differentiation of PC12 cells. J Histochem Cytochem 45: 1523-1531.
57. Santama N, Dotti CG, Lamond AI (1996) Neuronal differentiation in the rat hippocampus involves a stage-specific reorganization of subnuclear structure both in vivo and in vitro. Eur J Neurosci 8: 892-905.
58. Pena E, Berciano MT, Fernandez R, Ojeda JL, Lafarga M (2001) Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J Comp Neurol 430: 250-263.
59. Navascues J, Berciano MT, Tucker KE, Lafarga M, Matera AG (2004) Targeting SMN to Cajal bodies and nuclear gems during neuritogenesis. Chromosoma 112: 398-409.
60. Buhler D, Raker V, Luhrmann R, Fischer U (1999) Essential role for the tudor domain of SMN in spliceosomal U snRNP assembly: implications for spinal muscular atrophy. Hum Mol Genet 8: 2351-2357.
61. Sleeman JE, Ajuh P, Lamond AI (2001) snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci 114: 4407-4419.
62. Bellini M, Gall JG (1998) Coilin can form a complex with the U7 small nuclear ribonucleoprotein. Mol Biol Cell 9: 2987-3001.
63. Strzelecka M, Trowitzsch S, Weber G, Luhrmann R, Oates AC, et al. (2010) Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat Struct Mol Biol 17: 403-409.
64. Yoon JH, Parker R (2010) Coil-in-to snRNP assembly and Cajal bodies. Nat Struct Mol Biol 17: 391-393.
65. Strzelecka M, Oates AC, Neugebauer KM (2010) Dynamic control of Cajal body number during zebrafish embryogenesis. Nucleus 1: 96-108.
66. Chambon P (1996) A decade of molecular biology of retinoic acid receptors. FASEB J 10: 940-954.
67. Vaudry D, Stork PJ, Lazarovici P, Eiden LE (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296: 1648-1649.