The genetics of axonal transport and axonal transport disorders

PLoS Genetics

Volumn 2, Issue 9, 2006, Pages 1275-1284

  Duncan, Jason E ^a   Goldstein, Lawrence S B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MOLECULAR MOTOR; TAU PROTEIN;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CYTOARCHITECTURE; DEGENERATIVE DISEASE; DENDRITIC CELL; GENETIC ANALYSIS; HUMAN; HUNTINGTON CHOREA; MUTATION; NERVE FIBER TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; REVIEW; SYNAPSE; UNINDEXED SEQUENCE; ANIMAL; BIOLOGICAL MODEL; GENETICS; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; AXONAL TRANSPORT; BIOLOGICAL TRANSPORT; HUMANS; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; MUTATION; NEURODEGENERATIVE DISEASES;

EID: 33749398995     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0020124     Document Type: Review

References (105)

1. Goldstein LS (2003) Do disorders of movement cause movement disorders and dementia? Neuron 40: 415-425.
2. Heidemann SR, Landers JM, Hamborg MA (1981) Polarity orientation of axonal microtubules. J Cell Biol 91: 661-665.
3. Hanlon DW, Yang Z, Goldstein LS (1997) Characterization of KIFC2, a neuronal kinesin superfamily member in mouse. Neuron 18: 439-451.
4. Yang Z, Hanlon DW, Marszalek JR, Goldstein LS (1997) Identification, partial characterization, and genetic mapping of kinesin-like protein genes in mouse. Genomics 45: 123-131.
5. Miki H, Setou M, Kaneshiro K, Hirokawa N (2001) All kinesin superfamily protein, KIF, genes in mouse and human. Proc Natl Acad Sci U S A 98: 7004-7011.
6. Goldstein LS (2001) Molecular motors: From one motor many tails to one motor many tales. Trends Cell Biol 11: 477-482.
7. Pfister KK, Shah PR, Hummerich H, Russ A, Cotton J, et al. (2006) Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet 2: DOI: 10.1371/journal.pgen.0020001
8. Tai AW, Chuang JZ, Sung CH (2001) Cytoplasmic dynein regulation by subunit heterogeneity and its role in apical transport. J Cell Biol 153: 1499-1509.
9. Gill SR, Schroer TA, Szilak I, Steuer ER, Sheetz MP, et al. (1991) Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J Cell Biol 115: 1639-1650.
10. King SJ, Schroer TA (2000) Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2: 20-24.
11. Goldstein LS, Yang Z (2000) Microtubule-based transport systems in neurons: The roles of kinesins and dyneins. Annu Rev Neurosci 23: 39-71.
12. Shah JV, Cleveland DW (2002) Slow axonal transport: Fast motors in the slow lane. Curr Opin Cell Biol 14: 58-62.
13. Wang L, Ho CL, Sun D, Liem RK, Brown A (2000) Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat Cell Biol 2: 137-141.
14. Roy S, Coffee P, Smith G, Liem RK, Brady ST, et al. (2000) Neurofilaments are transported rapidly but intermittently in axons: Implications for slow axonal transport. J Neurosci 20: 6849-6861.
15. Xia CH, Roberts EA, Her LS, Liu X, Williams DS, et al. (2003) Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J Cell Biol 161: 55-66.
16. Brady ST (1985) A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317: 73-75.
17. Vale RD, Reese TS, Sheetz MP (1985) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42: 39-50.
18. Paschal BM, Vallee RB (1987) Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330: 181-183.
19. Paschal BM, Shpetner HS, Vallee RB (1987) MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dyneinlike properties. J Cell Biol 105: 1273-1282.
20. Schnapp BJ, Reese TS (1989) Dynein is the motor for retrograde axonal transport of organelles. Proc Natl Acad Sci U S A 86: 1548-1552.
21. Gindhart JG Jr, Desai CJ, Beushausen S, Zinn K, Goldstein LS (1998) Kinesin light chains are essential for axonal transport in Drosophila. J Cell Biol 141: 443-454.
22. Saxton WM, Hicks J, Goldstein LS, Raff EC (1991) Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell 64: 1093-1102.
23. Hurd DD, Saxton WM (1996) Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144: 1075-1085.
24. Reid E, Kloos M, Ashley-Koch A, Hughes L, Bevan S, et al. (2002) A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). Am J Hum Genet 71: 1189-1194.
25. Fichera M, Lo Giudice M, Falco M, Sturnio M, Amata S, et al. (2004) Evidence of kinesin heavy chain (KIF5A) involvement in pure hereditary spastic paraplegia. Neurology 63: 1108-1110.
26. McDermott C, White K, Bushby K, Shaw P (2000) Hereditary spastic paraparesis: A review of new developments. J Neurol Neurosurg Psychiatry 69: 150-160.
27. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, et al. (1998) Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93: 1147-1158.
28. Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, et al. (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20: 6374-6384.
29. Hall DH, Hedgecock EM (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65: 837-847.
30. Yonekawa Y, Harada A, Okada Y, Funakoshi T, Kanai Y, et al. (1998) Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J Cell Biol 141: 431-441.
31. Okada Y, Yamazaki H, Sekine-Aizawa Y, Hirokawa N (1995) The neuronspecific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81: 769-780.
32. Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, et al. (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105: 587-597.
33. Gepner J, Li M, Ludmann S, Kortas C, Boylan K, et al. (1996) Cytoplasmic dynein function is essential in Drosophila melanogaster. Genetics 142: 865-878.
34. Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, et al. (1998) Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol 141: 51-59.
35. Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, et al. (1999) Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10: 3717-3728.
36. Koushika SP, Schaefer AM, Vincent R, Willis JH, Bowerman B, et al. (2004) Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J Neurosci 24: 3907-3916.
37. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300: 808-812.
38. Gross SP (2003) Dynactin: Coordinating motors with opposite inclinations. Curr Biol 13: R320-R322.
39. Gross SP, Welte MA, Block SM, Wieschaus EF (2002) Coordination of opposite-polarity microtubule motors. J Cell Biol 156: 715-724.
40. Deacon SW, Serpinskaya AS, Vaughan PS, Lopez Fanarraga M, Vernos I, et al. (2003) Dynactin is required for bidirectional organelle transport. J Cell Biol 160: 297-301.
41. 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.
42. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, et al. (2002) Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34: 715-727.
43. Puls I, Jonnakuty C, LaMonte BH, Holzbaur EL, Tokito M, et al. (2003) Mutant dynactin in motor neuron disease. Nat Genet 33: 455-456.
44. Puls I, Oh SJ, Sumner CJ, Wallace KE, Floeter MK, et al. (2005) Distal spinal and bulbar muscular atrophy caused by dynactin mutation. Ann Neurol 57: 687-694.
45. Munch C, Sedlmeier R, Meyer T, Homberg V, Sperfeld AD, et al. (2004) Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology 63: 724-726.
46. Kamal A, Goldstein LS (2002) Principles of cargo attachment to cytoplasmic motor proteins. Curr Opin Cell Biol 14: 63-68.
47. 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.
48. 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.
49. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4: 521-533.
50. Stockinger W, Brandes C, Fasching D, Hermann M, Gotthardt M, et al. (2000) The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2. J Biol Chem 275: 25625-25632.
51. Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, et al. (2000) Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J Biol Chem 275: 25616-25624.
52. Horiuchi D, Barkus RV, Pilling AD, Gassman A, Saxton WM (2005) APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr Biol 15: 2137-2141.
53. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, et al. (2000) Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103: 583-594.
54. Cavalli V, Kujala P, Klumperman J, Goldstein LS (2005) Sunday driver links axonal transport to damage signaling. J Cell Biol 168: 775-787.
55. Nakata T, Hirokawa N (2003) Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 162: 1045-1055.
56. Hasegawa M, Smith MJ, Goedert M (1998) Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 437: 207-210.
57. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, et al. (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282: 1914-1917.
58. Zhang B, Higuchi M, Yoshiyama Y, Ishihara T, Forman MS, et al. (2004) Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J Neurosci 24: 4657-4667.
59. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, et al. (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 155: 2153-2165.
60. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, et al. (1999) Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24: 751-762.
61. 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.
62. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E (2003) Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging 24: 1079-1085.
63. Delcroix JD, Valletta JS, Wu C, Hunt SJ, Kowal AS, et al. (2003) NGF signaling in sensory neurons: Evidence that early endosomes carry NGF retrograde signals. Neuron 39: 69-84.
64. Gorska-Andrzejak J, Stowers RS, Borycz J, Kostyleva R, Schwarz TL, et al. (2003) Mitochondria are redistributed in Drosophila photoreceptors lacking milton, a kinesin-associated protein. J Comp Neurol 463: 372-388.
65. Stowers RS, Megeath LJ, Gorska-Andrzejak J, Meinertzhagen IA, Schwarz TL (2002) Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36: 1063-1077.
66. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, et al. (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47: 379-393.
67. Cummings JL, Vinters HV, Cole GM, Khachaturian ZS (1998) Alzheimer's disease: Etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology 51: S2-S17; discussion S65-S17.
68. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, et al. (1990) Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci U S A 87: 1561-1565.
69. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-459.
70. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414: 643-648.
71. Gunawardena S, Goldstein LS (2001) Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32: 389-401.
72. Block-Galarza J, Chase KO, Sapp E, Vaughn KT, Vallee RB, et al. (1997) Fast transport and retrograde movement of huntingtin and HAP 1 in axons. Neuroreport 8: 2247-2251.
73. Li SH, Gutekunst CA, Hersch SM, Li XJ (1998) Interaction of huntingtin-associated protein with dynactin P150Glued. J Neurosci 18: 1261-1269.
74. Engelender S, Sharp AH, Colomer V, Tokito MK, Lanahan A, et al. (1997) Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum Mol Genet 6: 2205-2212.
75. McGuire JR, Rong J, Li SH, Li XJ (2006) Interaction of Huntingtin-associated Protein-1 with Kinesin Light Chain: Implication in intracellular trafficking in neurons. J Biol Chem 281: 3552-3559.
76. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, et al. (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40: 25-40.
77. Trushina E, Dyer RB, Badger JD II, Ure D, Eide L, et al. (2004) Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol 24: 8195-8209.
78. Gauthier LR, Charrin BC, Borrell-Pages M, Dompierre JP, Rangone H, et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118: 127-138.
79. Szebenyi G, Morfini GA, Babcock A, Gould M, Selkoe K, et al. (2003) Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport. Neuron 40: 41-52.
80. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
81. Orrell RW (2000) Amyotrophic lateral sclerosis: Copper/zinc superoxide dismutase (SOD1) gene mutations. Neuromuscul Disord 10: 63-68.
82. Borchelt DR, Wong PC, Becher MW, Pardo CA, Lee MK, et al. (1998) Axonal transport of mutant superoxide dismutase 1 and focal axonal abnormalities in the proximal axons of transgenic mice. Neurobiol Dis 5: 27-35.
83. Williamson TL, Cleveland DW (1999) Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci 2: 50-56.
84. Zhang B, Tu P, Abtahian F, Trojanowski JQ, Lee VM (1997) Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J Cell Biol 139: 1307-1315.
85. Sasaki S, Warita H, Abe K, Iwata M (2004) Slow component of axonal transport is impaired in the proximal axon of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol (Berl) 107: 452-460.
86. Munoz DG, Greene C, Perl DP, Selkoe DJ (1988) Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J Neuropathol Exp Neurol 47: 9-18.
87. Rouleau GA, Clark AW, Rooke K, Pramatarova A, Krizus A, et al. (1996) SOD1 mutation is associated with accumulation of neurofilaments in amyotrophic lateral sclerosis. Ann Neurol 39: 128-131.
88. Ligon LA, LaMonte BH, Wallace KE, Weber N, Kalb RG, et al. (2005) Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport 16: 533-536.
89. Kieran D, Hafezparast M, Bohnert S, Dick JR, Martin J, et al. (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol 169: 561-567.
90. Teuchert M, Fischer D, Schwalenstoecker B, Habisch HJ, Bockers TM, et al. (2006) A dynein mutation attenuates motor neuron degeneration in SOD1(G93A) mice. Exp Neurol 198: 271-274.
91. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, et al. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-1288.
92. 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.
93. Yamazaki H, Nakata T, Okada Y, Hirokawa N (1995) KIF3A/B: A heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J Cell Biol 130: 1387-1399.
94. Takeda S, Yamazaki H, Seog DH, Kanai Y, Terada S, et al. (2000) Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J Cell Biol 148: 1255-1265.
95. Ray K, Perez SE, Yang Z, Xu J, Ritchings BW, et al. (1999) Kinesin-II is required for axonal transport of choline acetyltransferase in Drosophila. J Cell Biol 147: 507-518.
96. Baqri R, Charan R, Schimmelpfeng K, Chavan S, Ray K (2006) Kinesin-2 differentially regulates the anterograde axonal transports of acetylcholinesterase and choline acetyltransferase in Drosophila. J Neurobiol 66: 378-392.
97. Bowman AB, Patel-King RS, Benashski SE, McCaffery JM, Goldstein LS, et al. (1999) Drosophila roadblock and Chlamydomonas LC7: Aconserved family of dynein-associated proteins involved in axonal transport, flagellar motility, and mitosis. J Cell Biol 146: 165-180.
98. Levy JR, Sumner CJ, Caviston JP, Tokito MK, Ranganathan S, et al. (2006) A motor neuron disease-associated mutation in p150Glued perturbs dynactin function and induces protein aggregation. J Cell Biol 172: 733-745.
99. Pigino G, Morfini G, Pelsman A, Mattson MP, Brady ST, et al. (2003) Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 23: 4499-4508.
100. Gindhart JG, Chen J, Faulkner M, Gandhi R, Doerner K, et al. (2003) The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol Biol Cell 14: 3356-3365.
101. Tekotte H, Davis I (2002) Intracellular mRNA localization: Motors move messages. Trends Genet 18: 636-642.
102. Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, et al. (2004) Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet 36: 602-606.
103. Ackerley S, James PA, Kalli A, French S, Davies KE, et al. (2006) A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet 15: 347-354.
104. Ferreirinha F, Quattrini A, Pirozzi M, Valsecchi V, Dina G, et al. (2004) Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J Clin Invest 113: 231-242.
105. 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.