Computational modeling reveals optimal strategy for kinase transport by microtubules to nerve terminals

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Koon, Yen Ling ^a,b   Koh, Cheng Gee ^a,c   Chiam, Keng Hwee ^a,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d BIOINFORMATICS INSTITUTE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; JNK INTERACTING PROTEIN 1; KINESIN; KINESIN 5; SCAFFOLD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; PROTEIN KINASE;

ARTICLE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; INTRACELLULAR TRANSPORT; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MICROTUBULE; NERVE CELL; NERVE ENDING; NERVE FIBER TRANSPORT; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOSKELETON; DIFFUSION; ELECTROKYMOGRAPHY; HUMAN; KINETICS; METABOLISM;

COMPUTER SIMULATION; CYTOSKELETON; DIFFUSION; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KINETICS; KYMOGRAPHY; MICROTUBULES; MODELS, BIOLOGICAL; NERVE ENDINGS; PROTEIN KINASES; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84898875382     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092437     Document Type: Article

References (72)

1. Klipp E, Liebermeister W (2006) Mathematical modeling of intracellular signaling pathways. BMC Neurosci 7 Suppl 1: S10.
2. Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK (2006) Physicochemical modelling of cell signalling pathways. Nat Cell Biol 8: 1195-1203. (Pubitemid 44660581)
3. Kholodenko BN (2006) Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7: 165-176.
4. Bray D (1998) Signaling complexes: biophysical constraints on intracellular communication. Annu Rev Biophys Biomol Struct 27: 59-75.
5. Lipniacki T, Paszek P, Brasier AR, Luxon B, Kimmel M (2004) Mathematical model of NF-kappaB regulatory module. J Theor Biol 228: 195-215. (Pubitemid 38496282)
6. Banks GA, Roselli RJ, Chen R, Giorgio TD (2003) A model for the analysis of nonviral gene therapy. Gene Ther 10: 1766-1775. (Pubitemid 37121048)
7. Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329: 1616-1620.
8. Chiam KH, Tan CM, Bhargava V, Rajagopal G (2006) Hybrid simulations of stochastic reaction-diffusion processes for modeling intracellular signaling pathways. Phys Rev E Stat Nonlin Soft Matter Phys 74: 051910.
9. Yuste SB, Abad E, Lindenberg K (2010) Reaction-subdiffusion model of morphogen gradient formation. Phys Rev E Stat Nonlin Soft Matter Phys 82: 061123.
10. Haugh JM (2009) Analysis of reaction-diffusion systems with anomalous subdiffusion. Biophys J 97: 435-442.
11. Chiu JW, Chiam KH (2008) Monte Carlo simulation and linear stability analysis of Turing pattern formation in reaction-subdiffusion systems. Phys Rev E Stat Nonlin Soft Matter Phys 78: 056708.
12. Klann M, Koeppl H, Reuss M (2012) Spatial modeling of vesicle transport and the cytoskeleton: the challenge of hitting the right road. PLoS ONE 7: e29645.
13. Neri I, Kern N, Parmeggiani A (2013) Modeling cytoskeletal traffic: an interplay between passive diffusion and active transport. Phys Rev Lett 110: 098102.
14. Neri I, Kern N, Parmeggiani A (2013) Exclusion processes on networks as models for cytoskeletal transport. New J Phys 15: 085005.
15. Gallant PE (2000) Axonal protein synthesis and transport. J Neurocytol 29: 779-782.
16. Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519-526.
17. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10: 682-696.
18. Schnapp BJ, Reese TS (1989) Dynein is the motor for retrograde axonal transport of organelles. Proc Natl Acad Sci USA 86: 1548-1552. (Pubitemid 19078940)
19. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214. (Pubitemid 40342415)
20. Brown A (2003) Axonal transport of membranous and nonmembranous cargoes: a unified perspective. J Cell Biol 160: 817-821.
21. Roy S, Zhang B, Lee VM, Trojanowski JQ (2005) Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol 109: 5-13. (Pubitemid 40287785)
22. Good MC, Zalatan JG, Lim WA (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332: 680-686.
23. Levchenko A, Bruck J, Sternberg PW (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci USA 97: 5818-5823.
24. Shaw AS, Filbert EL (2009) Scaffold proteins and immune-cell signalling. Nat Rev Immunol 9: 47-56.
25. Chapman SA, Asthagiri AR (2009) Quantitative effect of scaffold abundance on signal propagation. Mol Syst Biol 5: 313.
26. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
27. Ip YT, Davis RJ (1998) Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Curr Opin Cell Biol 10: 205-219. (Pubitemid 28174763)
28. Whitmarsh AJ, Cavanagh J, Tournier C, Yasuda J, Davis RJ (1998) A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281: 1671-1674. (Pubitemid 28435582)
29. Morrison DK, Davis RJ (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19: 91-118. (Pubitemid 37487344)
30. Yasuda J, Whitmarsh AJ, Cavanagh J, Sharma M, Davis RJ (1999) The JIP group of mitogenactivated protein kinase scaffold proteins. Mol Cell Biol 19: 7245-7254. (Pubitemid 29441904)
31. Whitmarsh AJ, Kuan CY, Kennedy NJ, Kelkar N, Haydar TF, et al. (2001) Requirement of the JIP1 scaffold protein for stress-induced JNK activation. Genes Dev 15: 2421-2432. (Pubitemid 32899745)
32. Meyer D, Liu A, Margolis B (1999) Interaction of c-Jun amino-terminal kinase interacting protein-1 with p190 rhoGEF and its localization in differentiated neurons. J Biol Chem 274: 35113-35118. (Pubitemid 129509566)
33. Kelkar N, Gupta S, Dickens M, Davis RJ (2000) Interaction of a mitogenactivated protein kinase signaling module with the neuronal protein JIP3. Mol Cell Biol 20: 1030-1043. (Pubitemid 30044240)
34. Pellet JB, Haefliger JA, Staple JK, Widmann C, Welker E, et al. (2000) Spatial, temporal and subcellular localization of islet-brain 1 (IB1), a homologue of JIP-1, in mouse brain. Eur J Neurosci 12: 621-632. (Pubitemid 30142764)
35. Cavalli V, Kujala P, Klumperman J, Goldstein LS (2005) Sunday Driver links axonal transport to damage signaling. J Cell Biol 168: 775-787. (Pubitemid 40328161)
36. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, et al. (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152: 959-970. (Pubitemid 34286072)
37. Blacque OE, Cevik S, Kaplan OI (2008) Intraflagellar transport: from molecular characterisation to mechanism. Front Biosci 13: 2633-2652. (Pubitemid 351599709)
38. Good M, Tang G, Singleton J, Remenyi A, Lim WA (2009) The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136: 1085-1097.
39. Weston CR, Davis RJ (2002) The JNK signal transduction pathway. Curr Opin Genet Dev 12: 14-21. (Pubitemid 34094984)
40. Willoughby EA, Perkins GR, Collins MK, Whitmarsh AJ (2003) The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J Biol Chem 278: 10731-10736. (Pubitemid 36800344)
41. Blasius TL, Cai D, Jih GT, Toret CP, Verhey KJ (2007) Two binding partners cooperate to activate the molecular motor Kinesin-1. J Cell Biol 176: 11-17. (Pubitemid 46041675)
42. Verhey KJ, Lizotte DL, Abramson T, Barenboim L, Schnapp BJ, et al. (1998) Light chain-dependent regulation of Kinesin's interaction with microtubules. J Cell Biol 143: 1053-1066. (Pubitemid 28547403)
43. Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10: 765-777.
44. Kholodenko BN (2003) Four-dimensional organization of protein kinase signaling cascades: the roles of diffusion, endocytosis and molecular motors. J Exp Biol 206: 2073-2082.
45. Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68: 610-638.
46. Zhou J, Deo BK, Hosoya K, Terasaki T, Obrosova IG, et al. (2005) Increased JNK phosphorylation and oxidative stress in response to increased glucose flux through increased GLUT1 expression in rat retinal endothelial cells. Invest Ophthalmol Vis Sci 46: 3403-3410. (Pubitemid 44264331)
47. Byrd DT, Kawasaki M, Walcoff M, Hisamoto N, Matsumoto K, et al. (2001) UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32: 787-800. (Pubitemid 34024841)
48. Sakamoto R, Byrd DT, Brown HM, Hisamoto N, Matsumoto K, et al. (2005) The Caenorhabditis elegans UNC-14 RUN domain protein binds to the kinesin- 1 and UNC-16 complex and regulates synaptic vesicle localization. Mol Biol Cell 16: 483-496. (Pubitemid 40165549)
49. Horiuchi D, Collins CA, Bhat P, Barkus RV, Diantonio A, et al. (2007) Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr Biol 17: 1313-1317. (Pubitemid 47176890)
50. Morfini G, Pigino G, Szebenyi G, You Y, Pollema S, et al. (2006) JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat Neurosci 9: 907-916. (Pubitemid 43980505)
51. Stagi M, Gorlovoy P, Larionov S, Takahashi K, Neumann H (2006) Unloading kinesin transported cargoes from the tubulin track via the inflammatory c-Jun N-terminal kinase pathway. FASEB J 20: 2573-2575.
52. Dorner C, Ullrich A, Haring HU, Lammers R (1999) The kinesin-like motor protein KIF1C occurs in intact cells as a dimer and associates with proteins of the 14-3-3 family. J Biol Chem 274: 33654-33660. (Pubitemid 129511678)
53. Farzan SF, Ascano M, Ogden SK, Sanial M, Brigui A, et al. (2008) Costal2 functions as a kinesinlike protein in the hedgehog signal transduction pathway. Curr Biol 18: 1215-1220.
54. Zhang W, Zhao Y, Tong C, Wang G, Wang B, et al. (2005) Hedgehog-regulated Costal2-kinase complexes control phosphorylation and proteolytic processing of Cubitus interruptus. Dev Cell 8: 267-278. (Pubitemid 40197742)
55. Inomata H, Nakamura Y, Hayakawa A, Takata H, Suzuki T, et al. (2003) A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J Biol Chem 278: 22946-22955. (Pubitemid 36830359)
56. Taru H, Iijima K, Hase M, Kirino Y, Yagi Y, et al. (2002) Interaction of Alzheimer's beta -amyloid precursor family proteins with scaffold proteins of the JNK signaling cascade. J Biol Chem 277: 20070-20078. (Pubitemid 34967531)
57. Matsuda S, Yasukawa T, Homma Y, Ito Y, Niikura T, et al. (2001) c-Jun N-terminal kinase (JNK)- interacting protein-1b/islet-brain-1 scaffolds Alzheimer's amyloid precursor protein with JNK. J Neurosci 21: 6597-6607. (Pubitemid 32781104)
58. Klopfenstein DR, Vale RD, Rogers SL (2000) Motor protein receptors: moonlighting on other jobs. Cell 103: 537-540.
59. Schnapp BJ (2003) Trafficking of signaling modules by kinesin motors. J Cell Sci 116: 2125-2135.
60. Burack WR, Shaw AS (2000) Signal transduction: hanging on a scaffold. Curr Opin Cell Biol 12: 211-216. (Pubitemid 30142568)
61. Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, et al. (1997) A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388: 243-249. (Pubitemid 27317961)
62. Dickens M, Rogers JS, Cavanagh J, Raitano A, Xia Z, et al. (1997) A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277: 693- 696.
63. De Vos KJ, Grierson AJ, Ackerley S, Miller CC (2008) Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 31: 151-173.
64. Ventura JJ, Hubner A, Zhang C, Flavell RA, Shokat KM, et al. (2006) Chemical genetic analysis of the time course of signal transduction by JNK. Mol Cell 21: 701-710. (Pubitemid 43290736)
65. Bulinski JC (2007) Microtubule modification: acetylation speeds anterograde traffic flow. Curr Biol 17: 18-20.
66. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, et al. (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143: 777-794. (Pubitemid 28512571)
67. Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112 (Pt 14): 2355-2367. (Pubitemid 29381026)
68. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156: 1051-1063. (Pubitemid 34839854)
69. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, et al. (2002) Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21: 4896-4905.
70. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319: 1086-1089. (Pubitemid 351300789)
71. Vershinin M, Carter BC, Razafsky DS, King SJ, Gross SP (2007) Multiplemotor based transport and its regulation by Tau. Proc Natl Acad Sci USA 104: 87-92. (Pubitemid 46067989)
72. Moran U, Phillips R, Milo R (2010) SnapShot: key numbers in biology. Cell 141: 1262-1262.