Nudel/NudE and Lis1 promote dynein and dynactin interaction in the context of spindle morphogenesis

Molecular Biology of the Cell

Volumn 24, Issue 22, 2013, Pages 3522-3533

  Wang, Shusheng ^a   Ketcham, Stephanie A ^b   Schön, Arne ^b   Goodman, Benjamin ^a   Wang, Yueju ^c   Yates III, John ^c   Freire, Ernesto ^b   Schroer, Trina A ^b   Zheng, Yixian ^a,b  

^a GEOPHYSICAL LABORATORY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DYNEIN; DYNACTIN; GREEN FLUORESCENT PROTEIN; LIS 1 PROTEIN; NUDE PROTEIN; NUDEL PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CLONING; COMPLEX FORMATION; CONTROLLED STUDY; HYPOTHESIS; IMMUNOPRECIPITATION; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; M PHASE CELL CYCLE CHECKPOINT; MASS SPECTROMETRY; MITOSIS SPINDLE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SPINDLE POLE BODY; WESTERN BLOTTING; XENOPUS;

ANIMALS; DYNEINS; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KINETOCHORES; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MORPHOGENESIS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPERMATOZOA; SPINDLE APPARATUS; XENOPUS LAEVIS; XENOPUS PROTEINS; ZYGOTE;

EID: 84888271452     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-05-0283     Document Type: Article

References (63)

1. Allan VJ (2011). Cytoplasmic dynein. Biochem Soc Trans 39, 1169-1178.
2. Bi W et al. (2009). Increased LIS1 expression affects human and mouse brain development. Nat Genet 41, 168-177.
3. Bingham JB, King SJ, Schroer TA (1998). Purification of dynactin and dynein from brain tissue. Methods Enzymol 298, 171-184. (Pubitemid 28450751)
4. Burgess SA, Walker ML, Sakakibara H, Knight PJ, Oiwa K (2003). Dynein structure and power stroke. Nature 421, 715-718. (Pubitemid 36227616)
5. Carter AP, Cho C, Jin L, Vale RD (2011). Crystal structure of the dynein motor domain. Science 331, 1159-1165.
6. Derewenda U et al. (2007). The structure of the coiled-coil domain of Ndel1 and the basis of its interaction with Lis1, the causal protein of Miller-Dieker lissencephaly Structure 15, 1467-1481.
7. Efimov VP (2003). Roles of NUDE and NUDF proteins of Aspergillus nidulans: insights from intracellular localization and overexpression effects. Mol Biol Cell 14, 871-888. (Pubitemid 36337439)
8. Efimov VP, Morris NR (2000). The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J Cell Biol 150, 681-688. (Pubitemid 30641409)
9. Egan MJ, Tan K, Reck-Peterson SL (2012). Lis1 is an initiation factor for dynein-driven organelle transport. J Cell Biol 197, 971-982.
10. Feng Y, Olson EC, Stukenberg PT, Flanagan LA, Kirschner MW, Walsh CA (2000). LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 28, 665-679. (Pubitemid 32038063)
11. Gaetz J, Kapoor TM (2004). Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J Cell Biol 166, 465-471. (Pubitemid 39097165)
12. Gaglio T, Dionne MA, Compton DA (1997). Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. J Cell Biol 138, 1055-1066. (Pubitemid 27386455)
13. Gaglio T, Saredi A, Bingham JB, Hasbani MJ, Gill SR, Schroer TA, Compton DA (1996). Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J Cell Biol 135, 399-414. (Pubitemid 26359334)
14. Gibbons IR, Garbarino JE, Tan CE, Reck-Peterson SL, Vale RD, Carter AP (2005). The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk. J Biol Chem 280, 23960-23965. (Pubitemid 40884884)
15. Goodman B, Channels W, Qiu M, Iglesias P, Yang G, Zheng Y (2010). Lamin B counteracts the kinesin Eg5 to restrain spindle pole separation during spindle assembly. J Biol Chem 285, 35238-35244.
16. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996). Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420-425. (Pubitemid 26264851)
17. Heald R, Tournebize R, Habermann A, Karsenti E, Hyman A (1997). Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J Cell Biol 138, 615-628. (Pubitemid 27349842)
18. Huang J, Roberts AJ, Leschziner AE, Reck-Peterson SL (2012). Lis1 acts as a "Clutch" between the ATPase and microtubule-binding domains of the dynein motor. Cell 150, 975-986.
19. Kardon JR, Reck-Peterson SL, Vale RD (2009). Regulation of the processivity and intracellular localization of Saccharomyces cerevisiae dynein by dynactin. Proc Natl Acad Sci USA 106, 5669-5674.
20. Kardon JR, Vale RD (2009). Regulators of the cytoplasmic dynein motor. Nature Rev Mol Cell Biol 10, 854-865.
21. Karki S, Holzbaur EL (1995). Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J Biol Chem 270, 28806-28811.
22. 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. (Pubitemid 37484822)
23. King SJ, Schroer TA (2000). Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2, 20-24.
24. Kon T, Imamula K, Roberts AJ, Ohkura R, Knight PJ, Gibbons IR, Burgess SA, Sutoh K (2009). Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nat Struct Mol Biol 16, 325-333.
25. Kon T, Oyama T, Shimo-Kon R, Imamula K, Shima T, Sutoh K, Kurisu G (2012). The 2.8 A crystal structure of the dynein motor domain. Nature 484, 345-350.
26. Lam C, Vergnolle MA, Thorpe L, Woodman PG, Allan VJ (2010). Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning. J Cell Sci 123, 202-212.
27. Lee WL, Oberle JR, Cooper JA (2003). The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J Cell Biol 160, 355-364. (Pubitemid 36182726)
28. Liang Y, Yu W, Li Y, Yang Z, Yan X, Huang Q, Zhu X (2004). Nudel functions in membrane traffic mainly through association with Lis1 and cytoplasmic dynein. J Cell Biol 164, 557-566. (Pubitemid 38233317)
29. Liu H, Sadygov RG, Yates JR 3rd (2004). A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76, 4193-4201. (Pubitemid 38943698)
30. Ma L, Tsai MY, Wang S, Lu B, Chen R, Iii JR, Zhu X, Zheng Y (2009). Requirement for Nudel and dynein for assembly of the lamin B spindle matrix. Nat Cell Biol 11, 247-256.
31. McDonald WH, Tabb DL, Sadygov RG, MacCoss MJ, Venable J, Graumann J, Johnson JR, Cociorva D, Yates JR 3rd (2004). MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and Identifications. Rapid Commun Mass Spectrom 18, 2162-2168. (Pubitemid 39222458)
32. McKenney RJ, Vershinin M, Kunwar A, Vallee RB, Gross SP (2010). LIS1 and NudE induce a persistent dynein force-producing state. Cell 141, 304-314.
33. 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.
34. Mesngon MT, Tarricone C, Hebbar S, Guillotte AM, Schmitt EW, Lanier L, Musacchio A, King SJ, Smith DS (2006). Regulation of cytoplasmic dynein ATPase by Lis1. J Neurosci 26, 2132-2139.
35. Morgan JL, Song Y, Barbar E (2011). Structural dynamics and multiregion interactions in dynein-dynactin recognition. J Biol Chem 286, 39349-39359.
36. Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee MS, Morabito M, Tsai LH (2000). NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28, 697-711. (Pubitemid 32038065)
37. Nyarko A, Song Y, Barbar E (2012). Intrinsic disorder in dynein intermediate chain modulates its interactions with NudE and dynactin. J Biol Chem 287, 24884-24893.
38. Pandey J P, Smith DS (2011). A Cdk5-dependent switch regulates Lis1/Ndel1/dynein-driven organelle transport in adult axons. J Neurosci 31, 17207-17219.
39. Raaijmakers JA, Tanenbaum ME, Medema RH (2013). Systematic dissection of dynein regulators in mitosis. J Cell Biol 201, 201-215.
40. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH (1993). Isolation of a Miller-Dieker lissencephaly gene containing G protein β-subunit-like repeats. Nature 364, 717-721. (Pubitemid 23273124)
41. Roberts AJ et al. (2012). ATP-driven remodeling of the linker domain in the dynein motor. Structure 20, 1670-1680.
42. Ross JL, Wallace K, Shuman H, Goldman YE, Holzbaur EL (2006). Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat Cell Biol 8, 562-570. (Pubitemid 43827348)
43. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S (2000). A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28, 681-696. (Pubitemid 32038064)
44. Schroer TA (2004). Dynactin. Annu Rev Cell Dev Biol 20, 759-779. (Pubitemid 39488657)
45. Schroer TA, Sheetz MP (1991). Two activators of microtubule-based vesicle transport. J Cell Biol 115, 1309-1318. (Pubitemid 21909976)
46. Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D, Hoyt MA, Pellman D (2003). Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr Biol 13, 364-372. (Pubitemid 36280453)
47. Smith DS, Niethammer M, Ayala R, Zhou Y, Gambello MJ, Wynshaw-Boris A, Tsai LH (2000). Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat Cell Biol 2, 767-775.
48. Stehman SA, Chen Y, McKenney RJ, Vallee RB (2007). NudE and NudEL are required for mitotic progression and are involved in dynein recruitment to kinetochores. J Cell Biol 178, 583-594. (Pubitemid 47267271)
49. Tai C Y, Dujardin DL, Faulkner NE, Vallee RB (2002). Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J Cell Biol 156, 959-968. (Pubitemid 34839846)
50. Tarricone C, Perrina F, Monzani S, Massimiliano L, Kim MH, Derewenda ZS, Knapp S, Tsai LH, Musacchio A (2004). Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 44, 809-821. (Pubitemid 39575634)
51. Torisawa T, Nakayama A, Furuta K, Yamada M, Hirotsune S, Toyoshima YY (2011). Functional dissection of LIS1 and NDEL1 towards understanding the molecular mechanisms of cytoplasmic dynein regulation. J Biol Chem 286, 1959-1965.
52. Vallee RB, McKenney RJ, Ori-McKenney KM (2012). Multiple modes of cytoplasmic dynein regulation. Nat Cell Biol 14, 224-230.
53. 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.
54. Wang S, Zheng Y (2011). Identification of a novel dynein binding domain in Nudel essential for spindle pole organization in Xenopus egg extract. J Biol Chem 286, 587-593.
55. Wynshaw-Boris A (2007). Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin Genet 72, 296-304. (Pubitemid 47394219)
56. Xiang X, Osmani AH, Osmani SA, Xin M, Morris NR (1995). NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol Biol Cell 6, 297-310.
57. Xu T, Venable JD, Park SK, Cociorva D, Lu B, Liao L, Wohlschlegel J, Hewel J, Yates JR 3rd (2006). ProLuCID, a fast and sensitive tandem mass spectra-based protein Identification program. Mol Cell Proteomics 5, 5174.
58. Yamada M et al. (2008). LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27, 2471-2483.
59. Yeh TY, Quintyne NJ, Scipioni BR, Eckley DM, Schroer TA (2012). Dynactin's pointed-end complex is a cargo-targeting module. Mol Biol Cell 23, 3827-3837.
60. Yi JY, Ori-McKenney KM, McKenney RJ, Vershinin M, Gross S P, 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.
61. Zhang J, Yao X, Fischer L, Abenza JF, Penalva MA, Xiang X (2011). The p25 subunit of the dynactin complex is required for dynein-early endosome interaction. J Cell Biol 193, 1245-1255.
62. Zhang J, Zhuang L, Lee Y, Abenza JF, Penalva MA, Xiang X (2010). The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J Cell Sci 123, 3596-3604.
63. Zylkiewicz E, Kijanska M, Choi WC, Derewenda U, Derewenda ZS, Stukenberg PT (2011). The N-terminal coiled-coil of Ndel1 is a regulated scaffold that recruits LIS1 to dynein. J Cell Biol 192, 433-445.