Quantitative proteomics reveals dynamic interaction of c-Jun N-terminal kinase (JNK) with RNA transport granule proteins splicing factor proline- and glutamine-rich (Sfpq) and non-POU domain-containing octamer-binding protein (Nono) during neuronal differentiation

Molecular and Cellular Proteomics

Volumn 14, Issue 1, 2015, Pages 50-65

  Sury, Matthias D ^a   McShane, Erik ^a   Hernandez Miranda, Luis Rodrigo ^a   Birchmeier, Carmen ^a   Selbach, Matthias ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARRIER PROTEIN; GLUTAMINE; NERVE GROWTH FACTOR; NON POU DOMAIN CONTAINING OCTAMER BINDING PROTEIN; PROLINE; PROTEIN; RNA BINDING PROTEIN; RNA TRANSPORT GRANULE PROTEIN; SPLICING FACTOR PROLINE AND GLUTAMINE RISH; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; NONO PROTEIN, MOUSE; PTB-ASSOCIATED SPLICING FACTOR; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PC12 CELL LINE; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; RNA TRANSPORT;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; NERVE GROWTH FACTORS; NEURONS; PC12 CELLS; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; RATS; RNA TRANSPORT; RNA-BINDING PROTEINS;

EID: 84920473846     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.039370     Document Type: Article

References (73)

1. Haeusgen, W., Boehm, R., Zhao, Y., Herdegen, T., and Waetzig, V. (2009) Specific activities of individual c-Jun N-terminal kinases in the brain. Neuroscience 161, 951-959
2. Waetzig, V., Zhao, Y., and Herdegen, T. (2006) The bright side of JNKs-multitalented mediators in neuronal sprouting, brain development and nerve fiber regeneration. Prog. Neurobiol. 80, 84-97
3. Barr, R. K., and Bogoyevitch, M. A. (2001) The c-Jun N-terminal protein kinase family of mitogen-activated protein kinases (JNK MAPKs). Int. J. Biochem. Cell Biol. 33, 1047-1063
4. Weston, C. R., and Davis, R. J. (2007) The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19, 142-149
5. Bjorkblom, B., Vainio, J. C., Hongisto, V., Herdegen, T., Courtney, M. J., and Coffey, E. T. (2008) All JNKs can kill, but nuclear localization is critical for neuronal death. J. Biol. Chem. 283, 19704-19713
6. Bogoyevitch, M. A., and Kobe, B. (2006) Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70, 1061-1095
7. Eminel, S., Roemer, L., Waetzig, V., and Herdegen, T. (2007) c-Jun N-terminal kinases trigger both degeneration and neurite outgrowth in primary hippocampal and cortical neurons. J. Neurochem. 104, 957-969
8. Waetzig, V., and Herdegen, T. (2003) A single c-Jun N-terminal kinase isoform (JNK3-p54) is an effector in both neuronal differentiation and cell death. J. Biol. Chem. 278, 567-572
9. Neidhart, S., Antonsson, B., Gillieron, C., Vilbois, F., Grenningloh, G., and Arkinstall, S. (2001) c-Jun N-terminal kinase-3 (JNK3)/stress-activated protein kinase-beta (SAPKbeta) binds and phosphorylates the neuronal microtubule regulator SCG10. FEBS Lett. 508, 259-264
10. Tararuk, T., Ostman, N., Li, W., Bjorkblom, B., Padzik, A., Zdrojewska, J., Hongisto, V., Herdegen, T., Konopka, W., Courtney, M. J., and Coffey, E. T. (2006) JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J. Cell Biol. 173, 265-277
11. Bjorkblom, B., Ostman, N., Hongisto, V., Komarovski, V., Filen, J. J., Nyman, T. A., Kallunki, T., Courtney, M. J., and Coffey, E. T. (2005) Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J. Neurosci. 25, 6350-6361
12. Bjorkblom, B., Padzik, A., Mohammad, H., Westerlund, N., Komulainen, E., Hollos, P., Parviainen, L., Papageorgiou, A. C., Iljin, K., Kallioniemi, O., Kallajoki, M., Courtney, M. J., Magard, M., James, P., and Coffey, E. T. (2012) c-Jun N-terminal kinase phosphorylation of MARCKSL1 determines actin stability and migration in neurons and in cancer cells. Mol. Cell. Biol. 32, 3513-3526
13. Chang, L., Jones, Y., Ellisman, M. H., Goldstein, L. S., and Karin, M. (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell 4, 521-533
14. Gdalyahu, A., Ghosh, I., Levy, T., Sapir, T., Sapoznik, S., Fishler, Y., Azoulai, D., and Reiner, O. (2004) DCX, a new mediator of the JNK pathway. EMBO J. 23, 823-832
15. Podkowa, M., Zhao, X., Chow, C. W., Coffey, E. T., Davis, R. J., and Attisano, L. (2010) Microtubule stabilization by bone morphogenetic protein receptor-mediated scaffolding of c-Jun N-terminal kinase promotes dendrite formation. Mol. Cell. Biol. 30, 2241-2250
16. Westerlund, N., Zdrojewska, J., Padzik, A., Komulainen, E., Bjorkblom, B., Rannikko, E., Tararuk, T., Garcia-Frigola, C., Sandholm, J., Nguyen, L., Kallunki, T., Courtney, M. J., and Coffey, E. T. (2011) Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat. Neurosci. 14, 305-313
17. Francavilla, C., Rigbolt, K. T., Emdal, K. B., Carraro, G., Vernet, E., Bekker-Jensen, D. B., Streicher, W., Wikstrom, M., Sundstrom, M., Bellusci, S., Cavallaro, U., Blagoev, B., and Olsen, J. V. (2013) Functional proteomics defines the molecular switch underlying FGF receptor trafficking and cellular outputs. Mol. Cell 51, 707-722
18. Rigbolt, K. T., and Blagoev, B. (2012) Quantitative phosphoproteomics to characterize signaling networks. Semin. Cell Dev. Biol. 23, 863-871
19. Greene, L. A., and Tischler, A. S. (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
20. Greene, L. A., Aletta, J. M., Rukenstein, A., and Green, S. H. (1987) PC12 pheochromocytoma cells: culture, nerve growth factor treatment, and experimental exploitation. Methods Enzymol. 147, 207-216
21. Chevet, E., Lemaitre, G., Janjic, N., Barritault, D., Bikfalvi, A., and Katinka, M. D. (1999) Fibroblast growth factor receptors participate in the control of mitogen-activated protein kinase activity during nerve growth factor-induced neuronal differentiation of PC12 cells. J. Biol. Chem. 274, 20901-20908
22. Kaplan, D. R., and Stephens, R. M. (1994) Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25, 1404-1417
23. Waetzig, V., and Herdegen, T. (2003) The concerted signaling of ERK1/2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins. Mol. Cell. Neurosci. 24, 238-249
24. Leppa, S., Saffrich, R., Ansorge, W., and Bohmann, D. (1998) Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 17, 4404-4413
25. Heasley, L. E., Storey, B., Fanger, G. R., Butterfield, L., Zamarripa, J., Blumberg, D., and Maue, R. A. (1996) GTPase-deficient G alpha 16 and G alpha q induce PC12 cell differentiation and persistent activation of cJun NH2-terminal kinases. Mol. Cell. Biol. 16, 648-656
26. Tso, P. H., Morris, C. J., Yung, L. Y., Ip, N. Y., and Wong, Y. H. (2009) Multiple Gi proteins participate in nerve growth factor-induced activation of c-Jun N-terminal kinases in PC12 cells. Neurochem. Res. 34, 1101-1112
27. York, R. D., Yao, H., Dillon, T., Ellig, C. L., Eckert, S. P., McCleskey, E. W., and Stork, P. J. (1998) Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392, 622-626
28. Hernandez-Miranda, L. R., Cariboni, A., Faux, C., Ruhrberg, C., Cho, J. H., Cloutier, J. F., Eickholt, B. J., Parnavelas, J. G., and Andrews, W. D. (2011) Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain. J. Neurosci. 31, 6174-6187
29. Ishima, T., and Hashimoto, K. (2012) Potentiation of nerve growth factor-induced neurite outgrowth in PC12 cells by ifenprodil: the role of sigma-1 and IP(3) receptors. PLoS One 7, e37989
30. Nishimura, T., Ishima, T., Iyo, M., and Hashimoto, K. (2008) Potentiation of nerve growth factor-induced neurite outgrowth by fluvoxamine: role of sigma-1 receptors, IP3 receptors and cellular signaling pathways. PLoS One 3, e2558
31. Lahiri, D. K., and Ge, Y. (2000) Electrophoretic mobility shift assay for the detection of specific DNA-protein complex in nuclear extracts from the cultured cells and frozen autopsy human brain tissue. Brain Res. Brain Res. Protoc. 5, 257-265
32. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670
33. Sury, M. D., Chen, J. X., and Selbach, M. (2010) The SILAC fly allows for accurate protein quantification in vivo. Mol. Cell. Proteomics 9, 2173-2183
34. Ishihama, Y., Rappsilber, J., Andersen, J. S., and Mann, M. (2002) Micro-columns with self-assembled particle frits for proteomics. J. Chromatogr. A 979, 233-239
35. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705
36. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
37. Cox, J., Michalski, A., and Mann, M. (2011) Software lock mass by two-dimensional minimization of peptide mass errors. J. Am. Soc. Mass Spectrom. 22, 1373-1380
38. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
39. Eriksson, M., Taskinen, M., and Leppa, S. (2007) Mitogen activated protein kinase-dependent activation of c-Jun and c-Fos is required for neuronal differentiation but not for growth and stress response in PC12 cells. J. Cell. Physiol. 210, 538-548
40. Kita, Y., Kimura, K. D., Kobayashi, M., Ihara, S., Kaibuchi, K., Kuroda, S., Ui, M., Iba, H., Konishi, H., Kikkawa, U., Nagata, S., and Fukui, Y. (1998) Microinjection of activated phosphatidylinositol-3 kinase induces process outgrowth in rat PC12 cells through the Rac-JNK signal transduction pathway. J. Cell Sci. 111, 907-915
41. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
42. Blagoev, B., Ong, S. E., Kratchmarova, I., and Mann, M. (2004) Temporal analysis of 2 phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 22, 1139-1145
43. Cavalli, V., Kujala, P., Klumperman, J., and Goldstein, L. S. (2005) Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 168, 775-787
44. Mochizuki, N., Yamashita, S., Kurokawa, K., Ohba, Y., Nagai, T., Miyawaki, A., and Matsuda, M. (2001) Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068
45. Jeon, C. Y., Kim, H. J., Lee, J. Y., Kim, J. B., Kim, S. C., and Park, J. B. (2010) p190RhoGAP and Rap-dependent RhoGAP (ARAP3) inactivate RhoA in response to nerve growth factor leading to neurite outgrowth from PC12 cells. Exp. Mol. Med. 42, 335-344
46. Rappsilber, J., Ryder, U., Lamond, A. I., and Mann, M. (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res. 12, 1231-1245
47. Kanai, Y., Dohmae, N., and Hirokawa, N. (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525
48. Fox, A. H., and Lamond, A. I. (2010) Paraspeckles. Cold Spring Harb. Perspect. Biol. 2, a000687
49. Nakagawa, S., and Hirose, T. (2012) Paraspeckle nuclear bodies-useful uselessness? Cell. Mol. Life Sci. 69, 3027-3036
50. Lowery, L. A., Rubin, J., and Sive, H. (2007) Whitesnake/sfpq is required for cell survival and neuronal development in the zebrafish. Dev. Dyn. 236, 1347-1357
51. Kulkarni, S. J., Steinlauf, A. F., and Hall, J. C. (1988) The dissonance mutant of courtship song in Drosophila melanogaster: isolation, behavior and cytogenetics. Genetics 118, 267-285
52. Bogoyevitch, M. A., and Arthur, P. G. (2008) Inhibitors of c-Jun N-terminal kinases: JuNK no more? Biochim. Biophys. Acta 1784, 76-93
53. Bonny, C., Oberson, A., Negri, S., Sauser, C., and Schorderet, D. F. (2001) Cell-permeable peptide inhibitors of JNK: novel blockers of beta-cell death. Diabetes 50, 77-82
54. Brugidou, J., Legrand, C., Mery, J., and Rabie, A. (1995) The retro-inverso form of a homeobox-derived short peptide is rapidly internalised by cultured neurones: a new basis for an efficient intracellular delivery system. Biochem. Biophys. Res. Commun. 214, 685-693
55. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285, 1569-1572
56. Borsello, T., Clarke, P. G., Hirt, L., Vercelli, A., Repici, M., Schorderet, D. F., Bogousslavsky, J., and Bonny, C. (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 9, 1180-1186
57. Sury, M. D., Agarinis, C., Widmer, H. R., Leib, S. L., and Christen, S. (2008) JNK is activated but does not mediate hippocampal neuronal apoptosis in experimental neonatal pneumococcal meningitis. Neurobiol. Dis. 32, 142-150
58. Wang, J., Van De Water, T. R., Bonny, C., de Ribaupierre, F., Puel, J. L., and Zine, A. (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against both aminoglycoside and acoustic trauma-induced auditory hair cell death and hearing loss. J. Neurosci. 23, 8596-8607
59. Mizui, T., Kojima, N., Yamazaki, H., Katayama, M., Hanamura, K., and Shirao, T. (2009) Drebrin E is involved in the regulation of axonal growth through actin-myosin interactions. J. Neurochem. 109, 611-622
60. Jeon, Y. J., Choi, J. S., Lee, J. Y., Yu, K. R., Ka, S. H., Cho, Y., Choi, E. J., Baek, S. H., Seol, J. H., Park, D., Bang, O. S., and Chung, C. H. (2008) Filamin B serves as a molecular scaffold for type I interferon-induced c-Jun NH2-terminal kinase signaling pathway. Mol. Biol. Cell 19, 5116-5130
61. Haeusgen, W., Herdegen, T., and Waetzig, V. (2010) Specific regulation of JNK signalling by the novel rat MKK7gamma1 isoform. Cell Signal. 22, 1761-1772
62. Soderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
63. McBurney, M. W., Reuhl, K. R., Ally, A. I., Nasipuri, S., Bell, J. C., and Craig, J. (1988) Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J. Neurosci. 8, 1063-1073
64. Keene, J. D. (2007) RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8, 533-543
65. Sonenberg, N., and Hinnebusch, A. G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745
66. Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
67. Holt, C. E., and Schuman, E. M. (2013) The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80, 648-657
68. Prasanth, K. V., Prasanth, S. G., Xuan, Z., Hearn, S., Freier, S. M., Bennett, C. F., Zhang, M. Q., and Spector, D. L. (2005) Regulating gene expression through RNA nuclear retention. Cell 123, 249-263
69. Kiebler, M. A., and Bassell, G. J. (2006) Neuronal RNA granules: movers and makers. Neuron 51, 685-690
70. Han, T. W., Kato, M., Xie, S., Wu, L. C., Mirzaei, H., Pei, J., Chen, M., Xie, Y., Allen, J., Xiao, G., and McKnight, S. L. (2012) Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149, 768-779
71. Kato, M., Han, T. W., Xie, S., Shi, K., Du, X., Wu, L. C., Mirzaei, H., Goldsmith, E. J., Longgood, J., Pei, J., Grishin, N. V., Frantz, D. E., Schneider, J. W., Chen, S., Li, L., Sawaya, M. R., Eisenberg, D., Tycko, R., and McKnight, S. L. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753-767
72. Wippich, F., Bodenmiller, B., Trajkovska, M. G., Wanka, S., Aebersold, R., and Pelkmans, L. (2013) Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152, 791-805
73. Heo, Y. S., Kim, S. K., Seo, C. I., Kim, Y. K., Sung, B. J., Lee, H. S., Lee, J. I., Park, S. Y., Kim, J. H., Hwang, K. Y., Hyun, Y. L., Jeon, Y. H., Ro, S., Cho, J. M., Lee, T. G., and Yang, C. H. (2004) Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J. 23, 2185-2195