Cytoplasmic dynein-2: From molecules to human diseases

Frontiers in Biology

Volumn 8, Issue 1, 2013, Pages 119-126

  Rajagopalan, Vidyalakshmi ^a   D'Amico, Jonathan P ^a   Wilkes, David E ^a  

^a INDIANA UNIVERSITY SOUTH BEND   (United States)

Author keywords

cilia; dynein; flagella; intraflagellar transport; microtubule

Indexed keywords

EUKARYOTA;

EID: 84873115907     PISSN: 16747984     EISSN: 16747992     Source Type: Journal    
DOI: 10.1007/s11515-012-1242-y     Document Type: Review

References (74)

1. Adhiambo C, Forney J D, Asai D J, LeBowitz J H (2005). The two cytoplasmic dynein-2 isoforms in Leishmania mexicana perform separate functions. Mol Biochem Parasitol, 143(2): 216-225.
2. Asai D J, Beckwith S M, Kandl K A, Keating H H, Tjandra H, Forney J D (1994). The dynein genes of Paramecium tetraurelia. Sequences adjacent to the catalytic P-loop identify cytoplasmic and axonemal heavy chain isoforms. J Cell Sci, 107(Pt 4): 839-847.
3. Asai D J, Brokaw C J (1993). Dynein heavy chain isoforms and axonemal motility. Trends Cell Biol, 3(11): 398-402.
4. Asai D J, Rajagopalan V, Wilkes D E (2009). Dynein-2 and ciliogenesis in Tetrahymena. Cell Motil Cytoskeleton, 66(8): 673-677.
5. Bae Y K, Lyman-Gingerich J, Barr M M, Knobel K M (2008). Identification of genes involved in the ciliary trafficking of C. elegans PKD-2. Dev Dyn, 237(8): 2021-2029.
6. Blacque O E, Cevik S, Kaplan O I (2008). Intraflagellar transport: from molecular characterisation to mechanism. Front Biosci, 13(13): 2633-2652.
7. Brokaw C J (1994). Control of flagellar bending: a new agenda based on dynein diversity. Cell Motil Cytoskeleton, 28(3): 199-204.
8. Brokaw C J, Kamiya R (1987). Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil Cytoskeleton, 8(1): 68-75.
9. Bruno K S, Tinsley J H, Minke P F, Plamann M (1996). Genetic interactions among cytoplasmic dynein, dynactin, and nuclear distribution mutants of Neurospora crassa. Proc Natl Acad Sci U S A, 93(10): 4775-4780.
10. Burgess S A, Walker M L, Sakakibara H, Knight P J, Oiwa K (2003). Dynein structure and power stroke. Nature, 421(6924): 715-718.
11. Burkhardt J K, Echeverri C J, Nilsson T, Vallee R B (1997). Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol, 139(2): 469-484.
12. Criswell P S, Ostrowski L E, Asai D J (1996). A novel cytoplasmic dynein heavy chain: expression of DHC1b in mammalian ciliated epithelial cells. J Cell Sci, 109(Pt 7): 1891-1898.
13. Dagoneau N, Goulet M, Geneviève D, Sznajer Y, Martinovic J, Smithson S, Huber C, Baujat G, Flori E, Tecco L, Cavalcanti D, Delezoide A L, Serre V, Le Merrer M, Munnich A, Cormier-Daire V (2009). DYNC2H1 mutations cause asphyxiating thoracic dystrophy and short rib-polydactyly syndrome, type III. Am J Hum Genet, 84(5): 706-711.
14. Dutcher S K (1995). Flagellar assembly in two hundred and fifty easy-tofollow steps. Trends Genet, 11(10): 398-404.
15. Eberl D F, Hardy R W, Kernan M J (2000). Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci, 20(16): 5981-5988.
16. Echeverri C J, Paschal BM, Vaughan K T, Vallee R B (1996). Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol, 132(4): 617-633.
17. Ferkol TW, Leigh MW (2012). Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. J Pediatr, 160(3): 366-371.
18. Fridolfsson H N, Starr D A (2010). Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J Cell Biol, 191(1): 115-128.
19. Gibbons B H, Asai D J, Tang W J, Hays T S, Gibbons I R (1994). Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol Biol Cell, 5(1): 57-70.
20. Gibbons B H, Gibbons I R (1973). The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci, 13(2): 337-357.
21. Gibbons B H, Gibbons I R (1976). Functional recombination of dynein 1 with demembranated sea urchin sperm partially extracted with KC1. Biochem Biophys Res Commun, 73(1): 1-6.
22. Gibbons I R (1963). Studies on the protein components of cilia from Tetrahymena pyriformis. Proc Natl Acad Sci U S A, 50(5): 1002-1010.
23. Gibbons I R, Rowe A J (1965). Dynein: A protein with adenosine triphosphatase activity from cilia. Science, 149(3682): 424-426.
24. Grissom P M, Vaisberg E A, McIntosh J R (2002). Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2. Mol Biol Cell, 13(3): 817-829.
25. Gross S P, Welte M A, Block S M, Wieschaus E F (2000). Dyneinmediated cargo transport in vivo. A switch controls travel distance. J Cell Biol, 148(5): 945-956.
26. Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, Hirokawa N (1998). Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol, 141(1): 51-59.
27. Hildebrandt F, Benzing T, Katsanis N (2011). Ciliopathies. N Engl J Med, 364(16): 1533-1543.
28. Hirokawa N, Sato-Yoshitake R, Yoshida T, Kawashima T (1990). Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol, 111(3): 1027-1037.
29. Hou Y, Pazour G J, Witman G B (2004). A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport. Mol Biol Cell, 15(10): 4382-4394.
30. Huangfu D, Anderson K V (2005). Cilia and Hedgehog responsiveness in the mouse. Proc Natl Acad Sci U S A, 102(32): 11325-11330.
31. Ichikawa M, Watanabe Y, Murayama T, Toyoshima Y Y (2011). Recombinant human cytoplasmic dynein heavy chain 1 and 2: observation of dynein-2 motor activity in vitro. FEBS Lett, 585(15): 2419-2423.
32. Itin C, Ulitzur N, Mühlbauer B, Pfeffer S R (1999). Mapmodulin, cytoplasmic dynein, and microtubules enhance the transport of mannose 6-phosphate receptors from endosomes to the trans-golgi network. Mol Biol Cell, 10(7): 2191-2197.
33. Kim J, Kato M, Beachy P A (2009). Gli2 trafficking links Hedgehogdependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus. Proc Natl Acad Sci U S A, 106(51): 21666-21671.
34. King S J, Bonilla M, Rodgers M E, Schroer T A (2002). Subunit organization in cytoplasmic dynein subcomplexes. Protein Sci, 11(5): 1239-1250.
35. Koonce M P, Samsó M (1996). Overexpression of cytoplasmic dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium. Mol Biol Cell, 7(6): 935-948.
36. Krock B L, Mills-Henry I, Perkins B D (2009). Retrograde intraflagellar transport by cytoplasmic dynein-2 is required for outer segment extension in vertebrate photoreceptors but not arrestin translocation. Invest Ophthalmol Vis Sci, 50(11): 5463-5471.
37. Lee E, Sivan-Loukianova E, Eberl D F, Kernan M J (2008). An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr Biol, 18(24): 1899-1906.
38. Lee S W, Wisniewski J C, Dentler W L, Asai D J (1999). Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila. Mol Biol Cell, 10(3): 771-784.
39. Ma S, Triviños-Lagos L, Gräf R, Chisholm R L (1999). Dynein intermediate chain mediated dynein-dynactin interaction is required for interphase microtubule organization and centrosome replication and separation in Dictyostelium. J Cell Biol, 147(6): 1261-1274.
40. Merrill A E, Merriman B, Farrington-Rock C, Camacho N, Sebald E T, Funari V A, Schibler M J, Firestein M H, Cohn Z A, Priore M A, Thompson A K, Rimoin D L, Nelson S F, Cohn D H, Krakow D (2009). Ciliary abnormalities due to defects in the retrograde transport protein DYNC2H1 in short-rib polydactyly syndrome. Am J Hum Genet, 84(4): 542-549.
41. Mikami A, Tynan S H, Hama T, Luby-Phelps K, Saito T, Crandall J E, Besharse J C, Vallee R B (2002). Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells. J Cell Sci, 115(Pt 24): 4801-4808.
42. Nishiura M, Kon T, Shiroguchi K, Ohkura R, Shima T, Toyoshima Y Y, Sutoh K (2004). A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive the robust sliding of microtubules. J Biol Chem, 279(22): 22799-22802.
43. Ocbina P J, Anderson K V (2008). Intraflagellar transport, cilia, and mammalian Hedgehog signaling: analysis in mouse embryonic fibroblasts. Dev Dyn, 237(8): 2030-2038.
44. Ocbina P J, Eggenschwiler J T, Moskowitz I, Anderson K V (2011). Complex interactions between genes controlling trafficking in primary cilia. Nat Genet, 43(6): 547-553.
45. Palmer K J, Hughes H, Stephens D J (2009). Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol Biol Cell, 20(12): 2885-2899.
46. Palmer K J, MacCarthy-Morrogh L, Smyllie N, Stephens D J (2011). A role for Tctex-1 (DYNLT1) in controlling primary cilium length. Eur J Cell Biol, 90(10): 865-871.
47. Paschal B M, Shpetner H S, Vallee R B (1987). MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J Cell Biol, 105(3): 1273-1282.
48. Pazour G J, Dickert B L, Witman G B (1999). The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J Cell Biol, 144(3): 473-481.
49. Pazour G J, Wilkerson C G, Witman G B (1998). A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J Cell Biol, 141(4): 979-992.
50. Perrone C A, Tritschler D, Taulman P, Bower R, Yoder B K, Porter M E (2003). A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in Chlamydomonas and Mammalian cells. Mol Biol Cell, 14(5): 2041-2056.
51. Pfister K K, Shah P R, Hummerich H, Russ A, Cotton J, Annuar A A, King S M, Fisher E M (2006). Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet, 2(1): e1.
52. Porter M E (1996). Axonemal dyneins: assembly, organization, and regulation. Curr Opin Cell Biol, 8(1): 10-17.
53. Porter ME, Bower R, Knott J A, Byrd P, Dentler W (1999). Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell, 10(3): 693-712.
54. Rajagopalan V, Subramanian A, Wilkes D E, Pennock D G, Asai D J (2009). Dynein-2 affects the regulation of ciliary length but is not required for ciliogenesis in Tetrahymena thermophila. Mol Biol Cell, 20(2): 708-720.
55. Rana A A, Barbera J P, Rodriguez T A, Lynch D, Hirst E, Smith J C, Beddington R S (2004). Targeted deletion of the novel cytoplasmic dynein mD2LIC disrupts the embryonic organiser, formation of the body axes and specification of ventral cell fates. Development, 131(20): 4999-5007.
56. Reck-Peterson S L, Yildiz A, Carter A P, Gennerich A, Zhang N, Vale R D (2006). Single-molecule analysis of dynein processivity and stepping behavior. Cell, 126(2): 335-348.
57. Rompolas P, Pedersen L B, Patel-King R S, King S M (2007). Chlamydomonas FAP133 is a dynein intermediate chain associated with the retrograde intraflagellar transport motor. J Cell Sci, 120(Pt 20): 3653-3665.
58. Rosenbaum J L, Witman G B (2002). Intraflagellar transport. Nat Rev Mol Cell Biol, 3(11): 813-825.
59. + microtubule motor dynein. J Struct Biol, 146(1-2): 58-71.
60. Salina D, Bodoor K, Eckley D M, Schroer T A, Rattner J B, Burke B (2002). Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell, 108(1): 97-107.
61. Schafer J C, Haycraft C J, Thomas J H, Yoder B K, Swoboda P (2003). XBX-1 encodes a dynein light intermediate chain required for retrograde intraflagellar transport and cilia assembly in Caenorhabditis elegans. Mol Biol Cell, 14(5): 2057-2070.
62. Schnapp B J, Reese T S (1989). Dynein is the motor for retrograde axonal transport of organelles. Proc Natl Acad Sci U S A, 86(5): 1548-1552.
63. Scholey JM (2003). Intraflagellar transport. Annu Rev Cell Dev Biol, 19(1): 423-443.
64. Signor D, Wedaman K P, Orozco J T, Dwyer N D, Bargmann C I, Rose L S, Scholey J M (1999). Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J Cell Biol, 147(3): 519-530.
65. Söhle J, Machuy N, Smailbegovic E, Holtzmann U, Grönniger E, Wenck H, Stäb F, Winnefeld M (2012). Identification of new genes involved in human adipogenesis and fat storage. PLoS One, 7(2): e31193.
66. Thiel C, Kessler K, Giessl A, Dimmler A, Shalev S A, von der Haar S, Zenker M, Zahnleiter D, Stöss H, Beinder E, Abou Jamra R, Ekici A B, Schröder-Kress N, Aigner T, Kirchner T, Reis A, Brandstätter J H, Rauch A (2011). NEK1 mutations cause short-rib polydactyly syndrome type majewski. Am J Hum Genet, 88(1): 106-114.
67. Vaisberg E A, Grissom P M, McIntosh J R (1996). Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J Cell Biol, 133(4): 831-842.
68. Vale R D (2003). The molecular motor toolbox for intracellular transport. Cell, 112(4): 467-480.
69. Wicks S R, de Vries C J, van Luenen H G, Plasterk R H (2000). CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev Biol, 221(2): 295-307.
70. Wilkie G S, Davis I (2001). Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell, 105(2): 209-219.
71. Willemsen M H, Vissers L E, Willemsen M A, van Bon B W, Kroes T, de Ligt J, de Vries B B, Schoots J, Lugtenberg D, Hamel B C, van Bokhoven H, Brunner H G, Veltman J A, Kleefstra T (2012). Mutations in DYNC1H1 cause severe intellectual disability with neuronal migration defects. J Med Genet, 49(3): 179-183.
72. Woźniak M J, Bola B, Brownhill K, Yang Y C, Levakova V, Allan V J (2009). Role of kinesin-1 and cytoplasmic dynein in endoplasmic reticulum movement in VERO cells. J Cell Sci, 122(Pt 12): 1979-1989.
73. Xiang X, Beckwith S M, Morris N R (1994). Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci U S A, 91(6): 2100-2104.
74. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger S H, Zimmerman S, Jan L Y, Jan Y N (2008). Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol, 10(10): 1172-1180.