The molecular basis of the specificity and cross-reactivity of the NeuN epitope of the neuron-specific splicing regulator, Rbfox3

Histochemistry and Cell Biology

Volumn 141, Issue 1, 2014, Pages 43-55

  Maxeiner, Stephan ^a   Glassmann, Alexander ^b,c   Kao, Hung Teh ^d   Schilling, Karl ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c Life Science Inkubator   (Germany)

^d BROWN UNIVERSITY   (United States)

Author keywords

Epitope; Fixation; Immunocytochemistry; Neuron

Indexed keywords

EPITOPE; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN; SPLICING FACTOR RBFOX 3; SYNAPSIN I; UNCLASSIFIED DRUG; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NUCLEAR PROTEIN; SYNAPSIN;

ADULT; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTIGENICITY; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CROSS REACTION; CYTOPLASM; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SINGLE CELL ANALYSIS; WESTERN BLOTTING; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; C57BL MOUSE; CELL CULTURE; FEMALE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PHOSPHORYLATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; BRAIN; CELLS, CULTURED; CROSS REACTIONS; EPITOPES; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PHOSPHORYLATION; SEQUENCE ALIGNMENT; SYNAPSINS;

EID: 84892825644     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-013-1159-9     Document Type: Article

References (44)

1. Abello N, Kerstjens HAM, Postma DS, Bischoff R. (2007) Selective acylation of primary amines in peptides and proteins. J Proteome Res 6:4770-4776
2. Barbosa-Morais N.L., Irimia M, Pan Q., Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C., Watt S, Colak R, Kim T, Misquitta-Ali CM, Wilson MD, Kim PM, Odom DT, Frey BJ, Blencowe BJ (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587-1593
3. Blom N, Gammeltoft S, Brunak S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351-1362
4. Cannon JR, Greenamyre J.T. (2009) NeuN is not a reliable marker of dopamine neurons in rat substantia nigra. Neurosci Lett 464:14-17
5. Canova-Davis E., Eng M, Mukku V., Reifsnyder DH, Olson CV, Ling V.T. (1992) Chemical heterogeneity as a result of hydroxylamine cleavage of a fusion protein of human insulin-like growth factor I. Biochem J 285:207-213
6. Chin LS, Li L, Ferreira A., Kosik KS, Greengard P. (1995) Impairment of axonal development and of synaptogenesis in hippocampal neurons of Synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9230-9234
7. Damianov A, Black D.L. (2010) Autoregulation of Fox protein expression to produce dominant negative splicing factors. RNA 16:405-416
8. Dredge BK, Jensen K.B. (2011) NeuN/Rbfox3 nuclear and cytoplas-mic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS ONE 6:e21585
9. Dubuc AM, Morrissy AS, Kloosterhof N.K., Northcott PA, Yu EP, Shih D, Peacock J., Grajkowska W, van Meter T, Eberhart CG, Pfister S, Marra MA, Weiss WA, Scherer SW, Rutka JT, French PJ, Taylor MD (2012) Subgroup-specific alternative splicing in medul-loblastoma. Acta Neuropathol 123:485-499
10. Feng J, Chi P, Blanpied T.A., Xu Y., Magarinos AM, Ferreira A, Takahashi RH, Kao H.T., McEwen BS, Ryan TA, Augustine GJ, Green-gard P (2002) Regulation of neurotransmitter release by Synapsin III. J Neurosci 22:4372-4380
11. Ferreira A, Chin LS, Li L, Lanier L.M., Kosik KS, Greengard P. (1998) Distinct roles of Synapsin I and Synapsin II during neuronal development. Mol Med 4:22-28
12. Gitler D, Takagishi Y, Feng J., Ren Y, Rodriguiz RM, Wetsel W.C., Greengard P., Augustine G.J. (2004) Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci 24:11368-11380
13. Glassmann A, Molly S, Surchev L., Nazwar TA, Holst M, Hartmann W, Baader S.L., Oberdick J., Pietsch T, Schilling K (2007) Developmental expression and differentiation-related neuron-specific splicing of metastasis suppressor 1 (Mtss1) in normal and transformed cerebellar cells. BMC Dev Biol 7(111):111
14. Jung YJ, Park SJ, Park J.S., Lee K.E. (2004) Glucose/oxygen deprivation induces the alteration of Synapsin I and phosphosynapsin. Brain Res 996:47-54
15. Kim KK, Adelstein RS, Kawamoto S. (2009) Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:31052-31061
16. Kim KK, Kim YC, Adelstein R.S., Kawamoto S. (2011) Fox-3 and PSF interact to activate neural cell-specific alternative splicing. Nucleic Acids Res 39:3064-3078
17. Kim KK, Nam J, Mukouyama Y.S., Kawamoto S. (2013) Rbfox3-regulated alternative splicing of Numb promotes neuronal differentiation during development. J Cell Biol 200:443-458
18. Kuroyanagi H (2009) Fox-1 family of RNA-binding proteins. Cell Mol Life Sci 66:3895-3907
19. la Cour T., Kiemer L, Molgaard A., Gupta R, Skriver K, Brunak S. (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 17:527-536
20. Lal D, Reinthaler EM, Altmuller J, Toliat M.R., Thiele H., Nurnberg P, Lerche H, Hahn A., Moller RS, Muhle H, Sander T, Zimprich F, Neubauer BA (2013) RBFOX1 and RBFOX3 mutations in rolan-dic epilepsy. PLoS ONE 8:e73323
21. Lee BJ, Cansizoglu AE, Suel K.E., Louis TH, Zhang Z, Chook Y.M. (2006) Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 126:543-558
22. Lee JA, Tang ZZ, Black D.L. (2009) An inducible change in fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons. Genes Dev 23:2284-2293
23. Lin JC, Hsu M, Tarn W.Y. (2007) Cell stress modulates the function of splicing regulatory protein RBM4 in translation control. Proc Natl Acad Sci USA 104:2235-2240
24. Lind D, Franken S, Kappler J., Jankowski J, Schilling K. (2005) Characterization of the neuronal marker NeuN as a multiply phospho-rylated antigen with discrete subcellular localization. J Neurosci Res 79:295-302
25. Lowery LA, Rubin J, Sive H. (2007) Whitesnake/sfpq is required for cell survival and neuronal development in the zebrafish. Dev Dyn 236:1347-1357
26. Marsala M, Kakinohana O, Hefferan M.P., Cizkova D., Kinjoh K, Marsala S. (2005) Synaptogenesis and amino acid release from long term embryonic rat spinal cord neuronal culture using tissue culture inserts. J Neurosci Methods 141:21-27
27. McPhail LT, McBride CB, McGraw J, Steeves J.D., Tetzlaff W. (2004) Axotomy abolishes NeuN expression in facial but not rubrospinal neurons. Exp Neurol 185:182-190
28. Melloni RH J.r., Apostolides PJ, Hamos J.E., DeGennaro L.J. (1994) Dynamics of Synapsin I gene expression during the establishment and restoration of functional synapses in the rat hippocampus. Neuroscience 58:683-703
29. Metz B, Kersten GF, Hoogerhout P, Brugghe H.F., Timmermans HA, de Jong A, Meiring H, ten Hove J, Hennink WE, Crommelin DJ, Jiskoot W (2004) Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J Biol Chem 279:6235-6243
30. Metz B, Kersten GF, Baart G.J., de Jong A, Meiring H, ten Hove J, van Steenbergen MJ, Hennink WE, Crommelin DJ, Jiskoot W (2006) Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug Chem 17:815-822
31. Morgan JI, Curran T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451
32. Mullen RJ, Buck CR, Smith A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211
33. Portiansky EL, Barbeito CG, Gimeno E.J., Zuccolilli GO, Goya R.G. (2006) Loss of NeuN immunoreactivity in rat spinal cord neurons during aging. Exp Neurol 202:519-521
34. Puchtler H, Meloan S.N. (1985) On the chemistry of formaldehyde fixation and its effects on immunohistochemical reactions. Histochemistry 82:201-204
35. Ramachandran LK, Narita K. (1958) Reactions involving the amide and carboxyl groups of tobacco mosaic virus (TMV) protein. Biochim Biophys Acta 30:616-624
36. Sahdev S, Khattar SK, Saini K.S. (2008) Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 307:249-264
37. Schilling K, Luk D, Curran T., Morgan J.I. (1991) Regulation of a fos-lacZ fusion gene: a paradigm for quantitative analysis of stimulus-transcription coupling. Proc Natl Acad Sci USA 88:5665-5669
38. Skopp RN, Lane L.C. (1988) Fingerprinting of proteins cleaved in solution by cyanogen bromide. Appl Theor Electrophor 1:61
39. Smith BJ (2002) Chemical cleavage of proteins at asparaginyl-glycyl peptide bonds. In: Walker JM (ed) The protein protocols handbook. Humana Press, Totowa, NJ, pp 507-510
40. Toews J, Rogalski JC, Clark T.J., Kast J. (2008) Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal Chim Acta 618:168-183
41. Unal-Cevik I., Kilinc M, Gursoy-Ozdemir Y, Gurer G., Dalkara T. (2004) Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 1015:169-174
42. Voineagu I, Wang X, Johnston P., Lowe JK, Tian Y, Horvath S, Mill J., Cantor RM, Blencowe BJ, Geschwind DH (2011) Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474:380-384
43. Weyer A, Schilling K. (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73:400-409
44. Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297:249-260