Live cell imaging reveals differential modifications to cytoplasmic dynein properties by phospho- and dephosphomimic mutations of the intermediate chain 2C S84

Journal of Neuroscience Research

Volumn 92, Issue 9, 2014, Pages 1143-1154

  Blasier, Kiev R ^a   Humsi, Michael K ^a   Ha, Junghoon ^a   Ross, Mitchell W ^a   Smiley, W Russell ^a   Inamdar, Nirja A ^a   Mitchell, David J ^a   Lo, Kevin W H ^a   Pfister, K Kevin ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Axonal transport; Cytoplasmic dynein; Cytoskeleton; Motor protein

Indexed keywords

CYTOPLASMIC DYNEIN; DYNEIN PUNCTA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; DYNEIN IC2 PROTEIN, RAT; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; SERINE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; FIBROBLAST; GENE OVEREXPRESSION; HEAVY CHAIN; IMAGING AND DISPLAY; LIVE CELL IMAGING; MICROTUBULE; MITOCHONDRION; NERVE CELL; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RAT; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; GROWTH CONE; HIPPOCAMPUS; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; AXONAL TRANSPORT; CELLS, CULTURED; CYTOPLASMIC DYNEINS; EMBRYO, MAMMALIAN; GREEN FLUORESCENT PROTEINS; GROWTH CONES; HIPPOCAMPUS; MICROSCOPY, CONFOCAL; MUTATION; NEURONS; PHOSPHORYLATION; PROTEIN ISOFORMS; RATS; SERINE; TRANSFECTION;

EID: 84904250079     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23388     Document Type: Article

References (49)

1. Abe TK, Honda T, Takei K, Mikoshiba K, Hoffman-Kim D, Jay DG, Kuwano R. 2008. Dynactin is essential for growth cone advance. Biochem Biophys Res Commun 372:418-422.
2. Addinall SG, Mayr PS, Doyle S, Sheehan JK, Woodman PG, Allan VJ. 2001. Phosphorylation by cdc2-CyclinB1 kinase releases cytoplasmic dynein from membranes. J Biol Chem 276:15939-15944.
3. Akhmanova A, Hammer JA III. 2010. Linking molecular motors to membrane cargo. Curr Opin Cell Biol 22:479-487.
4. Ally S, Larson AG, Barlan K, Rice SE, Gelfand VI. 2009. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J Cell Biol 187:1071-1082.
5. Baas PW, Deitch JS, Black MM, Banker GA. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci U S A 85:8335-8339.
6. Brady ST, Lasek RJ, Allen RD. 1982. Fast axonal transport in extruded axoplasm from squid giant axon. Science 218:1129-1131.
7. Brady ST, Pfister KK, Bloom GS. 1990. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci U S A 87:1061-1065.
8. Dillman JF III, Pfister KK. 1994. Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. J Cell Biol 127:1671-1681.
9. Grabham PW, Seale GE, Bennecib M, Goldberg DJ, Vallee RB. 2007. Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodeling and fast axonal outgrowth. J Neurosci 27:5823-5834.
10. Gross SP, Welte MA, Block SM, Wieschaus EF. 2002. Coordination of opposite-polarity microtubule motors. J Cell Biol 156:715-724.
11. Ha J, Lo KW, Myers KR, Carr TM, Humsi MK, Rasoul BA, Segal RA, Pfister KK. 2008. A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. J Cell Biol 181:1027-1039.
12. Habura A, Tikhonenko I, Chisholm RL, Koonce MP. 1999. Interaction mapping of a dynein heavy chain. Identification of dimerization and intermediate-chain binding domains. J Biol Chem 274:15447-15453.
13. Hendricks AG, Perlson E, Ross JL, Schroeder HW III, Tokito M, Holzbaur EL. 2010. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr Biol 20:697-702.
14. 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.
15. 2+-phosphate transfection efficiency in low-density neuronal cultures. Nat Protoc 1:695-700.
16. Kaether C, Skehel P, Dotti CG. 2000. Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 11:1213-1224.
17. Kardon JR, Vale RD. 2009. Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10:854-865.
18. Karki S, Tokito MK, Holzbaur EL. 1997. Casein kinase II binds to and phosphorylates cytoplasmic dynein. J Biol Chem 272:5887-5891.
19. King SJ, Brown CL, Maier KC, Quintyne NJ, Schroer TA. 2003. Analysis of the dynein-dynactin interaction in vitro and in vivo. Mol Biol Cell 14:5089-5097.
20. Kumar S, Lee IH, Plamann M. 2000. Cytoplasmic dynein ATPase activity is regulated by dynactin-dependent phosphorylation. J Biol Chem 275:31798-31804.
21. Kumar S, Zhou Y, Plamann M. 2001. Dynactin-membrane interaction is regulated by the C-terminal domains of p150(Glued). EMBO J 2:939-944.
22. Kuta A, Deng W, Morsi El-Kadi A, Banks GT, Hafezparast M, Pfister KK, Fisher EM. 2010. Mouse cytoplasmic dynein intermediate chains: identification of new isoforms, alternative splicing and tissue distribution of transcripts. PloS One 5:e11682.
23. Lin SX, Ferro KL, Collins CA. 1994. Cytoplasmic dynein undergoes intracellular redistribution concomitant with phosphorylation of the heavy chain in response to serum starvation and okadaic acid. J Cell Biol 127:1009-1019.
24. Lo KW, Kogoy JM, Pfister KK. 2007. The DYNLT3 light chain directly links cytoplasmic dynein to a spindle checkpoint protein, Bub3. J Biol Chem 282:11205-11212.
25. Mallik R, Carter BC, Lex SA, King SJ, Gross SP. 2004. Cytoplasmic dynein functions as a gear in response to load. Nature 427:649-652.
26. Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, Saxton WM. 1999. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10:3717-3728.
27. McKenney RJ, Weil SJ, Scherer J, Vallee RB. 2011. Mutually exclusive cytoplasmic dynein regulation by NudE-Lis1 and dynactin. J Biol Chem 286:39615-39622.
28. Mitchell DJ, Blasier KR, Jeffery ED, Ross MW, Pullikuth AK, Suo D, Park J, Smiley WR, Lo KW, Shabanowitz J, Deppmann CD, Trinidad JC, Hunt DF, Catling AD, Pfister KK. 2012. Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J Neurosci 32:15495-15510.
29. Myers KR, Lo KW, Lye RJ, Kogoy JM, Soura V, Hafezparast M, Pfister KK. 2007. Intermediate chain subunit as a probe for cytoplasmic dynein function: biochemical analyses and live cell imaging in PC12 cells. J Neurosci Res 85:2640-2647.
30. Nakata T, Terada S, Hirokawa N. 1998. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 140:659-674.
31. Niclas J, Allan VJ, Vale RD. 1996. Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport. J Cell Biol 133:585-593.
32. Pfister KK, Lo KW-H. 2012. Cytoplasmic dynein function defined by subunit composition. In: King SM, editor. Dyneins. London: Academic Press. p 424-439.
33. Pfister KK, Salata MW, Dillman JF III, Torre E, Lye RJ. 1996a. Identification and developmental regulation of a neuron-specific subunit of cytoplasmic dynein. Mol Biol Cell 7:331-343.
34. Pfister KK, Salata MW, Dillman JF III, Vaughan KT, Vallee RB, Torre E, Lye RJ. 1996b. Differential expression and phosphorylation of the 74-kDa intermediate chains of cytoplasmic dynein in cultured neurons and glia. J Biol Chem 271:1687-1694.
35. Pfister KK, Shah PR, Hummerich H, Russ A, Cotton J, Annuar AA, King SM, Fisher EM. 2006. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet 2:e1.
36. Pilling AD, Horiuchi D, Lively CM, Saxton WM. 2006. Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 17:2057-2068.
37. Qi Y, Wang JK, McMillian M, Chikaraishi DM. 1997. Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J Neurosci 17:1217-1225.
38. Salata MW, Dillman JF III, Lye RJ, Pfister KK. 2001. Growth factor regulation of cytoplasmic dynein intermediate chain subunit expression preceding neurite extension. J Neurosci Res 65:408-416.
39. Saxton WM, Hollenbeck PJ. 2012. The axonal transport of mitochondria. J Cell Sci 125:2095-2104.
40. Shubeita GT, Tran SL, Xu J, Vershinin M, Cermelli S, Cotton SL, Welte MA, Gross SP. 2008. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell 135:1098-1107.
41. Silverman MA, Kaech S, Jareb M, Burack MA, Vogt L, Sonderegger P, Banker G. 2001. Sorting and directed transport of membrane proteins during development of hippocampal neurons in culture. Proc Natl Acad Sci U S A 98:7051-7057.
42. Vallee RB, Williams JC, Varma D, Barnhart LE. 2004. Dynein: An ancient motor protein involved in multiple modes of transport. J Neurobiol 58:189-200.
43. Vaughan KT, Vallee RB. 1995. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J Cell Biol 131:1507-1516.
44. Vaughan PS, Leszyk JD, Vaughan KT. 2001. Cytoplasmic dynein intermediate chain phosphorylation regulates binding to dynactin. J Biol Chem 276:26171-26179.
45. Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL. 1997. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci U S A 94:12180-12185.
46. Whyte J, Bader JR, Tauhata SB, Raycroft M, Hornick J, Pfister KK, Lane WS, Chan GK, Hinchcliffe EH, Vaughan PS, Vaughan KT. 2008. Phosphorylation regulates targeting of cytoplasmic dynein to kinetochores during mitosis. J Cell Biol 183:819-834.
47. Yi JY, Ori-McKenney KM, McKenney RJ, Vershinin M, Gross SP, Vallee RB. 2011. High-resolution imaging reveals indirect coordination of opposite motors and a role for LIS1 in high-load axonal transport. J Cell Biol 195:193-201.
48. Zhang J, Twelvetrees AE, Lazarus JE, Blasier KR, Yao X, Inamdar NA, Holzbaur EL, Pfister KK, Xiang X. 2013. Establishing a novel knock-in mouse line for studying neuronal cytoplasmic dynein under normal and pathologic conditions. Cytoskeleton 70:215-227.
49. Zhou HM, Brust-Mascher I, Scholey JM. 2001. Direct visualization of the movement of the monomeric axonal transport motor UNC-104 along neuronal processes in living Caenorhabditis elegans. J Neurosci 21:3749-3755.