Proteomic analysis of dynein-interacting proteins in amyotrophic lateral sclerosis synaptosomes reveals alterations in the RNA-binding protein staufen

Molecular and Cellular Proteomics

Volumn 15, Issue 2, 2016, Pages 506-522

  Gershoni Emek, Noga ^a   Mazza, Arnon ^a   Chein, Michael ^a   Gradus Pery, Tal ^a   Xiang, Xin ^b   Li, Ka Wan ^c   Sharan, Roded ^a   Perlson, Eran ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DYNEIN; RNA BINDING PROTEIN; STAU1 PROTEIN, MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; AXON; BIOSYNTHESIS; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MOTONEURON; MOUSE; MUTATION; PATHOLOGY; PROTEOMICS; SYNAPSE; SYNAPTOSOME;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; CYTOPLASMIC DYNEINS; DISEASE MODELS, ANIMAL; HUMANS; MICE; MOTOR NEURONS; MUTATION; PROTEOMICS; RNA-BINDING PROTEINS; SYNAPSES; SYNAPTOSOMES;

EID: 84957900256     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.049965     Document Type: Article

References (79)

1. Moloney, E. B., de Winter, F., and Verhaagen, J. (2014) ALS as a distal axonopathy: Molecular mechanisms affecting neuromuscular junction stability in the presymptomatic stages of the disease. Frontiers Neurosci 8, 252
2. De Vos, K. J., Grierson, A. J., Ackerley, S., and Miller, C. C. (2008) Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 31, 151-173
3. Perlson, E., Maday, S., Fu, M. M., Moughamian, A. J., and Holzbaur, E. L. (2010) Retrograde axonal transport: pathways to cell death? Trends Neurosci. 33, 335-344
4. Kardon, J. R., and Vale, R. D. (2009) Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 10, 854-865
5. Fu, M. M., and Holzbaur, E. L. (2014) Integrated regulation of motor-driven organelle transport by scaffolding proteins. Trends Cell Biol. 24, 564-574
6. Kiyomitsu, T., and Cheeseman, I. M. (2012) Chromosome-And spindlepole-derived signals generate an intrinsic code for spindle position and orientation. Nature Cell Biol. 14, 311-317
7. Perlson, E., Hendricks, A. G., Lazarus, J. E., Ben-Yaakov, K., Gradus, T., Tokito, M., and Holzbaur, E. L. (2013) Dynein interacts with the neural cell adhesion molecule (NCAM180) to tether dynamic microtubules and maintain synaptic density in cortical neurons. J. Biolog. Chem. 288, 27812-27824
8. Meignin, C., and Davis, I. (2010) Transmitting the message: Intracellular mRNA localization. Curr. Opin. Cell Biol. 22, 112-119
9. Whyte, J., Bader, J. R., Tauhata, S. B., Raycroft, M., Hornick, J., Pfister, K. K., Lane, W. S., Chan, G. K., Hinchcliffe, E. H., Vaughan, P. S., and Vaughan, K. T. (2008) Phosphorylation regulates targeting of cytoplasmic dynein to kinetochores during mitosis. J. Cell Biol. 183, 819-834
10. Allan, V. (1995) Protein phosphatase 1 regulates the cytoplasmic dyneindriven formation of endoplasmic reticulum networks in vitro. J. Cell Biol. 128, 879-891
11. Hinckelmann, M. V., Zala, D., and Saudou, F. (2013) Releasing the brake: Restoring fast axonal transport in neurodegenerative disorders. Trends Cell Biol. 23, 634-643
12. Gershoni-Emek, N., Chein, M., Gluska, S., and Perlson, E. (2015) Amyotrophic lateral sclerosis as a spatiotemporal mislocalization disease: Location, location, location. Int. Rev. Cell Mol. Biol. 315, 23-71
13. Kieran, D., Hafezparast, M., Bohnert, S., Dick, J. R., Martin, J., Schiavo, G., Fisher, E. M., and Greensmith, L. (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J. Cell Biol. 169, 561-567
14. Lloyd, T. E., Machamer, J., OHara, K., Kim, J. H., Collins, S. E., Wong, M. Y., Sahin, B., Imlach, W., Yang, Y., Levitan, E. S., McCabe, B. D., and Kolodkin, A. L. (2012) The p150(Glued) CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron 74, 344-360
15. Ikenaka, K., Kawai, K., Katsuno, M., Huang, Z., Jiang, Y. M., Iguchi, Y., Kobayashi, K., Kimata, T., Waza, M., Tanaka, F., Mori, I., and Sobue, G. (2013) dnc-1/dynactin 1 knockdown disrupts transport of autophagosomes and induces motor neuron degeneration. PloS One 8, e54511
16. Eschbach, J., and Dupuis, L. (2011) Cytoplasmic dynein in neurodegeneration. Pharmacol. Therapeut. 130, 348-363
17. Zetterström, P., Stewart, H. G., Bergemalm, D., Jonsson, P. A., Graffmo, K. S., Andersen, P. M., Brännström, T., Oliveberg, M., and Marklund, S. L. (2007) Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models. Proc. Natl. Acad. Sci. U.S.A. 104, 14157-14162
18. Bergemalm, P. O., Hennerdal, S., Persson, B., Lyxell, B., and Borg, E. (2009) Perception of the acoustic environment and neuroimaging findings: A report of six cases with a history of closed head injury. Acta Oto-Laryngolog. 129, 801-808
19. Ekegren, T., Hanrieder, J., Aquilonius, S. M., and Bergquist, J. (2006) Focused proteomics in post-mortem human spinal cord. J. Proteome Res. 5, 2364-2371
20. Grant, S. G. (2003) Synapse signalling complexes and networks: Machines underlying cognition. BioEssays 25, 1229-1235
21. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P., and Grant, S. G. (2000) Proteomic analysis of NMDA receptor-Adhesion protein signaling complexes. Nature Neurosci. 3, 661-669
22. Li, K. W., Klemmer, P., and Smit, A. B. (2010) Interaction proteomics of synapse protein complexes. Anal. Bioanal. Chem. 397, 3195-3202
23. Klemmer, P., Smit, A. B., and Li, K. W. (2009) Proteomics analysis of immuno-precipitated synaptic protein complexes. J. Proteomics 72, 82-90
24. Westphal, R. S., Tavalin, S. J., Lin, J. W., Alto, N. M., Fraser, I. D., Langeberg, L. K., Sheng, M., and Scott, J. D. (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285, 93-96
25. Jiménez, C. R., Eyman, M., Lavina, Z. S., Gioio, A., Li, K. W., van der Schors, R. C., Geraerts, W. P., Giuditta, A., Kaplan, B. B., and van Minnen, J. (2002) Protein synthesis in synaptosomes: A proteomics analysis. J. Neurochem. 81, 735-744
26. Khanna, R., Zougman, A., and Stanley, E. F. (2007) A proteomic screen for presynaptic terminal N-Type calcium channel (CaV2.2) binding partners. J. Biochem. Mol. Biol. 40, 302-314
27. Yosef, N., Zalckvar, E., Rubinstein, A. D., Homilius, M., Atias, N., Vardi, L., Berman, I., Zur, H., Kimchi, A., Ruppin, E., and Sharan, R. (2011) ANAT: A tool for constructing and analyzing functional protein networks. Science Signal. 4, pl1
28. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H. X., and et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264, 1772-1775
29. Zhang, J., Twelvetrees, A. E., Lazarus, J. E., Blasier, K. R., Yao, X., Inamdar, N. A., Holzbaur, E. L., Pfister, K. K., and Xiang, X. (2013) Establishing a novel knock-in mouse line for studying neuronal cytoplasmic dynein under normal and pathologic conditions. Cytoskeleton 70, 215-227
30. Schaefer, M. H., Fontaine, J. F., Vinayagam, A., Porras, P., Wanker, E. E., and Andrade-Navarro, M. A. (2012) HIPPIE: Integrating protein interaction networks with experiment based quality scores. PloS One 7, e31826
31. Mudunuri, U., Che, A., Yi, M., and Stephens, R. M. (2009) bioDBnet: The biological database network. Bioinformatics 25, 555-556
32. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
33. Kalmar, B., and Greensmith, L. (2009) Activation of the heat shock response in a primary cellular model of motoneuron neurodegeneration-evidence for neuroprotective and neurotoxic effects. Cell. Mol. Biol. Lett. 14, 319-335
34. Camu, W., and Henderson, C. E. (1994) Rapid purification of embryonic rat motoneurons: An in vitro model for studying MND/ALS pathogenesis. J. Neurolog. Sci. 124, 73-74
35. Pfister, K. K. (2015) Distinct functional roles of cytoplasmic dynein defined by the intermediate chain isoforms. Experiment. Cell Res. 334, 54-60
36. Wang, S., Ketcham, S. A., Schön, A., Goodman, B., Wang, Y., Yates, J., 3rd, Freire, E., Schroer, T. A., and Zheng, Y. (2013) Nudel/NudE and Lis1 promote dynein and dynactin interaction in the context of spindle morphogenesis. Mol. Biol. Cell 24, 3522-3533
37. McKenney, R. J., Weil, S. J., Scherer, J., and Vallee, R. B. (2011) Mutually exclusive cytoplasmic dynein regulation by NudE-Lis1 and dynactin. J. Biolog. Chem. 286, 39615-39622
38. Schafer, D. A., Gill, S. R., Cooper, J. A., Heuser, J. E., and Schroer, T. A. (1994) Ultrastructural analysis of the dynactin complex: An actin-related protein is a component of a filament that resembles F-Actin. J. Cell Biol. 126, 403-412
39. Soo, K. Y., Halloran, M., Sundaramoorthy, V., Parakh, S., Toth, R. P., Southam, K. A., McLean, C. A., Lock, P., King, A., Farg, M. A., and Atkin, J. D. (2015) Rab1-dependent ER-Golgi transport dysfunction is a common pathogenic mechanism in SOD1, TDP-43 and FUS-Associated ALS. Acta Neuropatholog.
40. Bordelon, J. R., Smith, Y., Nairn, A. C., Colbran, R. J., Greengard, P., and Muly, E. C. (2005) Differential localization of protein phosphatase-1alpha, beta and gamma1 isoforms in primate prefrontal cortex. Cereb Cortex 15, 1928-1937
41. Monshausen, M., Rehbein, M., Richter, D., and Kindler, S. (2002) The RNA-binding protein Staufen from rat brain interacts with protein phosphatase-1. J. Neurochem. 81, 557-564
42. Bélanger, G., Stocksley, M. A., Vandromme, M., Schaeffer, L., Furic, L., Des Groseillers, L., and Jasmin, B. J. (2003) Localization of the RNA-binding proteins Staufen1 and Staufen2 at the mammalian neuromuscular junction. J. Neurochem. 86, 669-677
43. Tübing, F., Vendra, G., Mikl, M., Macchi, P., Thomas, S., and Kiebler, M. A. (2010) Dendritically localized transcripts are sorted into distinct ribonucleoprotein particles that display fast directional motility along dendrites of hippocampal neurons. J. Neurosci. 30, 4160-4170
44. Kanai, Y., Dohmae, N., and Hirokawa, N. (2004) Kinesin transports RNA: isolation and characterization of an RNA-Transporting granule. Neuron 43, 513-525
45. Droppelmann, C. A., Campos-Melo, D., Ishtiaq, M., Volkening, K., and Strong, M. J. (2014) RNA metabolism in ALS: When normal processes become pathological. ALS Frontotemporal Degen. 15, 321-336
46. Rohrer, J. D., Isaacs, A. M., Mizlienska, S., Mead, S., Lashley, T., Wray, S., Sidle, K., Fratta, P., Orrell, R. W., Hardy, J., Holton, J., Revesz, T., Rossor, M. N., and Warren, J. D. (2015) C9orf72 expansions in frontotemporal dementia and amyotrophic lateral sclerosis. The Lancet. Neurology
47. Alami, N. H., Smith, R. B., Carrasco, M. A., Williams, L. A., Winborn, C. S., Han, S. S., Kiskinis, E., Winborn, B., Freibaum, B. D., Kanagaraj, A., Clare, A. J., Badders, N. M., Bilican, B., Chaum, E., Chandran, S., Shaw, C. E., Eggan, K. C., Maniatis, T., and Taylor, J. P. (2014) Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron 81, 536-543
48. Delanoue, R., Herpers, B., Soetaert, J., Davis, I., and Rabouille, C. (2007) Drosophila Squid/hnRNP helps dynein switch from a gurken mRNA transport motor to an ultrastructural static anchor in sponge bodies. Developmental Cell 13, 523-538
49. Kotak, S., Busso, C., and Gönczy, P. (2012) Cortical dynein is critical for proper spindle positioning in human cells. J. Cell Biol. 199, 97-110
50. Ligon, L. A., and Holzbaur, E. L. (2007) Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic 8, 808-819
51. Holt, C. E., and Bullock, S. L. (2009) Subcellular mRNA localization in animal cells and why it matters. Science 326, 1212-1216
52. Heraud-Farlow, J. E., and Kiebler, M. A. (2014) The multifunctional Staufen proteins: Conserved roles from neurogenesis to synaptic plasticity. Trends Neurosci. 37, 470-479
53. Tosar, L. J., Thomas, M. G., Baez, M. V., Ibanez, I., Chernomoretz, A., and Boccaccio, G. L. (2012) Staufen: From embryo polarity to cellular stress and neurodegeneration. Front. Biosci. 4, 432-452
54. Goldstein, L. H., Atkins, L., Landau, S., Brown, R. G., and Leigh, P. N. (2006) Longitudinal predictors of psychological distress and self-esteem in people with ALS. Neurology 67, 1652-1658
55. St. Johnston, D., Beuchle, D., and Nüsslein-Volhard, C. (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63
56. Breuer, A. C., and Atkinson, M. B. (1988) Fast axonal transport alterations in amyotrophic lateral sclerosis (ALS) and in parathyroid hormone (PTH)-Treated axons. Cell Motility Cytoskeleton 10, 321-330
57. Allison, R., Czaplinski, K., Git, A., Adegbenro, E., Stennard, F., Houliston, E., and Standart, N. (2004) Two distinct Staufen isoforms in Xenopus are vegetally localized during oogenesis. RNA 10, 1751-1763
58. Ferrandon, D., Elphick, L., Nüsslein-Volhard, C., and St. Johnston, D. (1994) Staufen protein associates with the 3UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79, 1221-1232
59. Ramos, A., Grünert, S., Adams, J., Micklem, D. R., Proctor, M. R., Freund, S., Bycroft, M., St Johnston, D., and Varani, G. (2000) RNA recognition by a Staufen double-stranded RNA-binding domain. EMBO J. 19, 997-1009
60. Kim, Y. K., Furic, L., Parisien, M., Major, F., Des Groseillers, L., and Maquat, L. E. (2007) Staufen1 regulates diverse classes of mammalian transcripts. EMBO J. 26, 2670-2681
61. Lebeau, G., Maher-Laporte, M., Topolnik, L., Laurent, C. E., Sossin, W., Desgroseillers, L., and Lacaille, J. C. (2008) Staufen1 regulation of protein synthesis-dependent long-Term potentiation and synaptic function in hippocampal pyramidal cells. Mol. Cell. Biol. 28, 2896-2907
62. Dubnau, J., Chiang, A. S., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., Broger, C., and Tully, T. (2003) The staufen/pumilio pathway is involved in Drosophila long-Term memory. Current Biol. 13, 286-296
63. Mallardo, M., Deitinghoff, A., Müller, J., Goetze, B., Macchi, P., Peters, C., and Kiebler, M. A. (2003) Isolation and characterization of Staufencontaining ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. U.S.A. 100, 2100-2105
64. Gardiol, A., and St Johnston, D. (2014) Staufen targets coracle mRNA to Drosophila neuromuscular junctions and regulates GluRIIA synaptic accumulation and bouton number. Developmental Biol. 392, 153-167
65. Wang, I. F., Wu, L. S., Chang, H. Y., and Shen, C. K. (2008) TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105, 797-806
66. Yu, Z., Fan, D., Gui, B., Shi, L., Xuan, C., Shan, L., Wang, Q., Shang, Y., and Wang, Y. (2012) Neurodegeneration-Associated TDP-43 interacts with Fragile X mental retardation protein (FMRP)/Staufen (STAU1) and regulates SIRT1 expression in neuronal cells. J. Biolog. Chem. 287, 22560-22572
67. Massignan, T., Casoni, F., Basso, M., Stefanazzi, P., Biasini, E., Tortarolo, M., Salmona, M., Gianazza, E., Bendotti, C., and Bonetto, V. (2007) Proteomic analysis of spinal cord of presymptomatic amyotrophic lateral sclerosis G93A SOD1 mouse. Biochem. Biophys. Res. Commun. 353, 719-725
68. Palma, A. S., De Carvalho, M., Grammel, N., Pinto, S., Barata, N., Conradt, H. S., and Costa, J. (2008) Proteomic analysis of plasma from Portuguese patients with familial amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis 9, 339-349
69. Maurer, M. H., Haux, D., Unterberg, A. W., and Sakowitz, O. W. (2008) Proteomics of human cerebral microdialysate: From detection of biomarkers to clinical application. Proteomics Clin. Applications 2, 437-443
70. Nardo, G., Pozzi, S., Mantovani, S., Garbelli, S., Marinou, K., Basso, M., Mora, G., Bendotti, C., and Bonetto, V. (2009) Nitroproteomics of peripheral blood mononuclear cells from patients and a rat model of ALS. Antioxidants Redox Signal. 11, 1559-1567
71. Willis, D., Li, K. W., Zheng, J. Q., Chang, J. H., Smit, A. B., Kelly, T., Merianda, T. T., Sylvester, J., van Minnen, J., and Twiss, J. L. (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 25, 778-791
72. Michaelevski, I., Medzihradszky, K. F., Lynn, A., Burlingame, A. L., and Fainzilber, M. (2010) Axonal transport proteomics reveals mobilization of translation machinery to the lesion site in injured sciatic nerve. Mol. Cell. Proteomics 9, 976-987
73. Peredo, J., Villacé, P., Ortin, J., and de Lucas, S. (2014) Human Staufen1 associates to miRNAs involved in neuronal cell differentiation and is required for correct dendritic formation. PloS One 9, e113704
74. Moughamian, A. J., and Holzbaur, E. L. (2012) Dynactin is required for transport initiation from the distal axon. Neuron 74, 331-343
75. Moughamian, A. J., Osborn, G. E., Lazarus, J. E., Maday, S., and Holzbaur, E. L. (2013) Ordered recruitment of dynactin to the microtubule plus-end is required for efficient initiation of retrograde axonal transport. J. Neurosci. 33, 13190-13203
76. Sorolla, M. A., Reverter-Branchat, G., Tamarit, J., Ferrer, I., Ros, J., and Cabiscol, E. (2008) Proteomic and oxidative stress analysis in human brain samples of Huntington disease. Free Radical Biol. 45, 667-678
77. Chen, S., Lu, F. F., Seeman, P., and Liu, F. (2012) Quantitative proteomic analysis of human substantia nigra in Alzheimers disease, Huntingtons disease and multiple sclerosis. Neurochem. Res. 37, 2805-2813
78. Zabel, C., Mao, L., Woodman, B., Rohe, M., Wacker, M. A., Kläre, Y., Koppelstätter, A., Nebrich, G., Klein, O., Grams, S., Strand, A., Luthi-Carter, R., Hartl, D., Klose, J., and Bates, G. P. (2009) A large number of protein expression changes occur early in life and precede phenotype onset in a mouse model for Huntington disease. Mol. Cell. Proteomics 8, 720-734
79. Basso, M., Samengo, G., Nardo, G., Massignan, T., DAlessandro, G., Tartari, S., Cantoni, L., Marino, M., Cheroni, C., De Biasi, S., Giordana, M. T., Strong, M. J., Estevez, A. G., Salmona, M., Bendotti, C., and Bonetto, V. (2009) Characterization of detergent-insoluble proteins in ALS indicates a causal link between nitrative stress and aggregation in pathogenesis. PloS One 4, e8130