[en] The polypyrimidine tract-binding protein-associated splicing factor (PSF), which plays an essential role in mammalian spliceosomes, has been found to be expressed by differentiating neurons in developing mouse brain. The sequence of a fragment of mouse PSF was found to be remarkably similar to that of human PSF. Both the expression of PSF mRNA in cortex and cerebellum and PSF immunoreactivity in all brain areas were high during embryonic and early postnatal life and almost disappeared in adult tissue, except in the hippocampus and olfactory bulb where various neuronal populations remained PSF-immunopositive. Double-labeling experiments with anti-PSF antibody and anti-neurofilaments or anti-glial fibrillary acidic protein antibodies on sections of cortex, hippocampus, and cerebellum indicate that PSF is expressed by differentiating neurons but not by astrocytic cells. In vitro, mouse PSF was found to be expressed by differentiating cortical and cerebellar neurons. Radial glia or astrocyte nuclei were not immunopositive; however, oligodendrocytes differentiating in vitro were found to express PSF. The restricted expression of PSF suggests that this splicing factor could be involved in the control of neuronal-specific splicing events occurring at particular stages of neuronal differentiation and maturation.
Chanas-Sacre, Grazyna; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Mazy-Servais, Cécile; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Wattiez, Ruddy; Université de Mons-Hainaut - UMH > Department of Biological Chemistry
Pirard, Sandrine; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Rogister, Bernard ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Patton, James G; Vanderbilt University > Department of Molecular biology
Belachew, Shibeshih ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie
Malgrange, Brigitte ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Moonen, Gustave ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie - Doyen de la Faculté de Médecine
Leprince, Pierre ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Language :
English
Title :
Identification of Psf, the Polypyrimidine Tract-Binding Protein-Associated Splicing Factor, as a Developmentally Regulated Neuronal Protein
Publication date :
01 July 1999
Journal title :
Journal of Neuroscience Research
ISSN :
0360-4012
eISSN :
1097-4547
Publisher :
John Wiley & Sons, Hoboken, United States - New York
Ashiya M, Grabowski PJ. 1997. A neuron-specific splicing switch mediated by an array of pre-mRNA represser sites: evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart. RNA 3:996-1015.
Belachew S, Malgrange B, Rigo J-M, Register B, Coucke P, Mazy-Servais C, Moonen G. 1998. Developmental regulation of neuroligand-induced responses in cultured oligodendroglia. Neuroreport 9:973-980.
Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
Buckanovich RJ, Yang YYL, Darnell RB. 1996. The onconeuronal antigen Nova-1 is a neuron-specific RNA-binding protein, the activity of which is inhibited by paraneoplastic antibodies. J Neurosci 16:1114-1122.
Burke JF, Bright KE, Kellet E, Benjamin PR, Saunders SE. 1992. Alternative mRNA splicing in the nervous system. Prog Brain Res 92:115-125.
Cameron RS, Rakic P. 1991. Glial cell lineage in the cerebral cortex: a review and a synthesis. Glia 4:124-137.
Caviness VS, Takahashi T, Nowakowski RS. 1995. Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model. Trends Neurosci 18:379-383.
Chan RC, Black DL. 1995. Conserved intron elements repress splicing of a neuron-specific c-src exon in vitro. Mol Cell Biol 15:6377-6385.
Chan RC, Black DL. 1997. The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream. Mol Cell Biol 17:4667-4676.
Chanas-Sacré G, Mazy-Servais C, Wattiez R, Lewin M, Pirard S, Rogister B, Patton JG, Moonen G, Leprince P. 1997. Identification of a splicing factor as a developmentally-regulated neuronal protein. Arch Physiol Biochem 105:B19.
Chomczynski P, Sacchi N. 1987. A rapid method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
Devereux J, Haeberli P, Smithies O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:4411-4427.
Dong B, Horowitz DS, Kobayashi R, Krainer AR. 1993. Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids Res 21:4085-4092.
Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. 1993. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62:289-321.
Gower HJ, Moore SE, Dickson G, Elsom VL, Nayak R, Walsh FS. 1989. Cloning and characterization of a myoblast cell surface antigen defined by 24.1D5 monoclonal antibody. Development 105:723-731.
Gressens P, Richelme C, Kadhim HJ, Gadisseux JF, Evrard P. 1992. The germinative zone produces the most cortical astrocytes after neuronal migration in the developing mammalian brain. Biol Neonate 61:4-24.
Hanamura A, Caceres JF, Mayeda A, Franza BR, Krainer AR. 1998. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4:430-444.
Hirano K, Erdödi F, Patton JG, Hartshorne DJ. 1996. Interaction of protein phosphatase type 1 with a splicing factor. FEBS Lett 389:191-194.
Kamma H, Portman DS, Dreyfuss G. 1995. Cell type-specific expression of hnRNP proteins. Exp Cell Res 221:187-196.
Leprince P, Chanas-Sacré G, Wattiez R, Lewin M, Rogister B, Mazy-Servais C, Misson J-P, Moonen G. 1996. Identification of antigens recognized in the developing mouse brain by the RC2 antibody, a marker of radial glia. Int J Dev Neurosci 14 [Suppl 1]:84.
Lin CLG, Bristol LA, Jin L, Dykes-Hoberg M, Crawford T, Clawson L, Rothstein JD. 1998. Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20:589-602.
Liu Q, Fischer U, Wang F, Dreyfuss G. 1997. The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90:1013-1021.
Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. 1996. Chain migration of neuronal precursors. Science 271:978-981.
Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
Manley JL, Tacke R. 1996. SR proteins and splicing control. Genes Dev 10:1569-1579.
Miale IL, Sidman RL. 1961. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4:277-296.
Misson J-P, Edwards MA, Yamamoto M, Caviness VS. 1988. Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Dev Brain Res 44:95-108.
Nakai K, Sakamoto H. 1994. Construction of a novel database containing aberrant splicing mutations of mammalian genes. Gene 141:171-177.
Okano HJ, Darnell RB. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
Patton JG, Porro EB, Galceran J, Tempst P, Nadal-Ginard B. 1993. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Devel 7:393-406.
Sakakibara SI, Okano H. 1997. Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial development. J Neurosci 17:8300-8312.
Schoenen J, Delrée P, Leprince P, Moonen G. 1989. Neurotransmitter phenotype plasticity in cultured dissociated adult rat dorsal root ganglia: an immunocytochemical study. J Neurosci Res 22(4): 473-487.
Straub T, Grue P, Uhse A, Lisby M, Knudsen BR, Tange TO, Westergaard O, Boege F. 1998. The RNA-splicing factor PSF/p54nrb controls DNA-topoisomerase I activity by a direct interaction. J Biol Chem 273:26261-26264.
Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
Valcarcel J, Gebauer F. 1997. Post-transcriptional regulation: the dawn of PTB. Curr Biol 7:R705-R708.
Will CL, Lührmann R. 1997. Protein functions in pre-mRNA splicing. Curr Opin Cell Biol 9:320-328.
Zahler AM, Neugebauer KM, Lane WS, Roth RF. 1993. Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260:219-222.