Unique function of Kinesin Kif5A in localization of mitochondria in axons

Journal of Neuroscience

Volumn 34, Issue 44, 2014, Pages 14717-14732

  Campbell, Philip D ^a   Shen, Kimberle ^b   Sapio, Matthew R ^a   Glenn, Thomas D ^b   Talbot, William S ^b   Marlow, Florence L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axon degeneration; CMT; HSP; Kinesin; Mitochondria; Sensory neuron

Indexed keywords

GENOMIC DNA; TRANSCRIPTION FACTOR GAL4; KINESIN;

ADULT; ARTICLE; CELL LABELING; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; DRUG SENSITIVITY; EMBRYO; FEMALE; GENE; GENE CONSTRUCT; GENE LOCATION; GENE MUTATION; GENE SEQUENCE; GENE VECTOR; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPING TECHNIQUE; HEREDITARY MOTOR SENSORY NEUROPATHY; IMMUNOHISTOCHEMISTRY; KINESIN SUPERFAMILY PROTEIN 1B GENE; KINESIN SUPERFAMILY PROTEIN 5A GENE; KINESIN SUPERFAMILY PROTEIN 5AA GENE; KINESIN SUPERFAMILY PROTEIN 5AB GENE; KINESIN SUPERFAMILY PROTEIN 5S GENE; LYSOSOME; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; MOLECULAR CLONING; NERVE FIBER; NERVE FIBER DEGENERATION; NERVE FIBER TRANSPORT; NERVOUS SYSTEM FUNCTION; NONHUMAN; POLYNEUROPATHY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; SENSORY NERVE CELL; SYNAPSE VESICLE; TRANSMISSION ELECTRON MICROSCOPY; ZEBRA FISH; ANIMAL; GENETICS; METABOLISM; NERVE DEGENERATION; PHYSIOLOGY;

ANIMALS; AXONAL TRANSPORT; AXONS; KINESIN; MITOCHONDRIA; NERVE DEGENERATION; ZEBRAFISH;

EID: 84908352427     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2770-14.2014     Document Type: Article

References (72)

1. Afrikanova T, Serruys AS, Buenafe OE, Clinckers R, Smolders I, de Witte PA, Crawford AD, Esguerra CV (2013) Validation of the zebrafish pentylenetetrazol seizure model: locomotor versus electrographic responses to antiepileptic drugs. PloS One 8:e54166. CrossRef Medline
2. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10:413-420. CrossRef Medline
3. Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, et al. (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32:13819-13840. CrossRef Medline
4. Baraban SC, Taylor MR, Castro PA, Baier H (2005) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131:759-768. CrossRef Medline
5. Baraban SC, Dinday MT, Castro PA, Chege S, Guyenet S, Taylor MR (2007) A large-scale mutagenesis screen to identify seizure-resistant zebrafish. Epilepsia 48:1151-1157. CrossRef Medline
6. Baxendale S, Holdsworth CJ, Meza Santoscoy PL, Harrison MR, Fox J, Parkin CA, Ingham PW, Cunliffe VT (2012) Identification of compounds with anti-convulsant properties in a zebrafish model of epileptic seizures. Dis Model Mech 5:773-784. CrossRef Medline
7. Billger M, Wallin M, Karlsson JO (1988) Proteolysis of tubulin and microtubule-associated proteins 1 and 2 by calpain I and II: difference in sensitivity of assembled and disassembled microtubules. Cell Calcium 9:33-44. CrossRef Medline
8. Blair MA, Ma S, Hedera P (2006) Mutation in KIF5A can also cause adult- onset hereditary spastic paraplegia. Neurogenetics 7:47-50. CrossRef Medline
9. Brickley K, Stephenson FA (2011) Trafficking kinesin protein (TRAK)- mediated transport of mitochondria in axons of hippocampal neurons. J Biol Chem 286:18079-18092. CrossRef Medline
10. Brickley K, Smith MJ, Beck M, Stephenson FA (2005) GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J Biol Chem 280:14723-14732. CrossRef Medline
11. Buss RR, Drapeau P (2001) Synaptic drive to motoneurons during fictive swimming in the developing zebrafish. J Neurophysiol 86:197-210 Medline
12. Campbell PD, Marlow FL (2013) Temporal and tissue specific gene expression patterns of the zebrafish kinesin-1 heavy chain family, kif5s, during development. Gene Expr Patterns 13:271-279. CrossRef Medline
13. Chen Y, Sheng ZH (2013) Kinesin-1-syntaphilin coupling mediates activity- dependent regulation of axonal mitochondrial transport. J Cell Biol 202:351-364. CrossRef Medline
14. Coleman M (2005) Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6:889-898. CrossRef Medline
15. Coy DL, Hancock WO, Wagenbach M, Howard J (1999) Kinesin’s tail domain is an inhibitory regulator of the motor domain. Nat Cell Biol 1:288-292. CrossRef Medline
16. Crimella C, Baschirotto C, Arnoldi A, Tonelli A, Tenderini E, Airoldi G, Martinuzzi A, Trabacca A, Losito L, Scarlato M, Benedetti S, Scarpini E, Spinicci G, Bresolin N, Bassi MT (2012) Mutations in the motor and stalk domains of KIF5A in spastic paraplegia type 10 and in axonal Charcot-Marie-Tooth type 2. Clin Genet 82:157-164. CrossRef Medline
17. Deluca GC, Ebers GC, Esiri MM (2004) The extent of axonal loss in the long tracts in hereditary spastic paraplegia. Neuropathol Appl Neurobiol 30: 576-584. CrossRef Medline
18. Drerup CM, Nechiporuk AV (2013) JNK-interacting protein 3 mediates the retrograde transport of activated c-Jun N-terminal kinase and lysosomes. PLoS Genet 9:e1003303. CrossRef Medline
19. Fichera M, Lo Giudice M, Falco M, Sturnio M, Amata S, Calabrese O, Bigoni S, Calzolari E, Neri M (2004) Evidence of kinesin heavy chain (KIF5A) involvement in pure hereditary spastic paraplegia. Neurology 63:1108-1110. CrossRef Medline
20. Finsterer J, Löscher W, Quasthoff S, Wanschitz J, Auer-Grumbach M, Stevanin G (2012) Hereditary spastic paraplegias with autosomal dominant, recessive, X-linked, or maternal trait of inheritance. J Neurol Sci 318:1-18. CrossRef Medline
21. Friedman DS, Vale RD (1999) Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat Cell Biol 1:293-297. CrossRef Medline
22. Goizet C, Boukhris A, Mundwiller E, Tallaksen C, Forlani S, Toutain A, Carriere N, Paquis V, Depienne C, Durr A, Stevanin G, Brice A (2009) Complicated forms of autosomal dominant hereditary spastic paraplegia are frequent in SPG10. Hum Mutat 30:E376-E385. CrossRef Medline
23. Hackney DD, Stock MF (2000) Kinesin’s IAK tail domain inhibits initial microtubule-stimulated ADP release. Nat Cell Biol 2:257-260. CrossRef Medline
24. Hackney DD, Baek N, Snyder AC (2009) Half-site inhibition of dimeric kinesin head domains by monomeric tail domains. Biochemistry 48: 3448-3456. CrossRef Medline
25. Hartley JL, Temple GF, Brasch MA (2000) DNA cloning using in vitro site- specific recombination. Genome Res 10:1788-1795. CrossRef Medline
26. Hedera P, Eldevik OP, Maly P, Rainier S, Fink JK (2005) Spinal cord magnetic resonance imaging in autosomal dominant hereditary spastic paraplegia. Neuroradiology 47:730-734. CrossRef Medline
27. Hinckelmann MV, Zala D, Saudou F (2013) Releasing the brake: restoring fast axonal transport in neurodegenerative disorders. Trends Cell Biol 23:634-643. CrossRef Medline
28. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682-696. CrossRef Medline
29. 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. CrossRef Medline
30. Hoerndli FJ, Maxfield DA, Brockie PJ, Mellem JE, Jensen E, Wang R, Madsen DM, Maricq AV (2013) Kinesin-1 regulates synaptic strength by mediating the delivery, removal, and redistribution of AMPA receptors. Neuron 80:1421-1437. CrossRef Medline
31. Johnson GV, Litersky JM, Jope RS (1991) Degradation of microtubule- associated protein 2 and brain spectrin by calpain: a comparative study. J Neurochem 56:1630-1638. CrossRef Medline
32. Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, Hirokawa N (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20:6374-6384 Medline
33. Karle KN, Möckel D, Reid E, Schöls L (2012) Axonal transport deficit in a KIF5A/ mouse model. Neurogenetics 13:169-179. CrossRef Medline
34. Kawaguchi K (2013) Role of kinesin-1 in the pathogenesis of SPG10, a rare form of hereditary spastic paraplegia. Neuroscientist 19:336-344. CrossRef Medline
35. Kettleborough RN, Busch-Nentwich EM, Harvey SA, Dooley CM, de Bruijn E, van Eeden F, Sealy I, White RJ, Herd C, Nijman IJ, Fényes F, Mehroke S, Scahill C, Gibbons R, Wali N, Carruthers S, Hall A, Yen J, Cuppen E, Stemple DL (2013) A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 496:494-497. CrossRef Medline
36. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099. CrossRef Medline
37. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. CrossRef Medline
38. Lyons DA, Naylor SG, Mercurio S, Dominguez C, Talbot WS (2008) KBP is essential for axonal structure, outgrowth and maintenance in zebrafish, providing insight into the cellular basis of Goldberg-Shprintzen syndrome. Development 135:599-608. CrossRef Medline
39. Lyons DA, Naylor SG, Scholze A, Talbot WS (2009) Kif1b is essential for mRNA localization in oligodendrocytes and development of myelinated axons. Nat Genet 41:854-858. CrossRef Medline
40. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:W597-W600. CrossRef Medline
41. Meyer MP, Smith SJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3614. CrossRef Medline
42. 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. CrossRef Medline
43. Moua P, Fullerton D, Serbus LR, Warrior R, Saxton WM (2011) Kinesin-1 tail autoregulation and microtubule-binding regions function in salutatory transport but not ooplasmic streaming. Development 138:1087-1092. CrossRef Medline
44. Nakajima K, Yin X, Takei Y, Seog DH, Homma N, Hirokawa N (2012) Molecular motor KIF5A is essential for GABA(A) receptor transport, and KIF5A deletion causes epilepsy. Neuron 76:945-961. CrossRef Medline
45. Nangaku M, Sato-Yoshitake R, Okada Y, Noda Y, Takemura R, Yamazaki H, Hirokawa N (1994) KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79:1209-1220. CrossRef Medline
46. Neff MM, Neff JD, Chory J, Pepper AE (1998) DCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387-392. CrossRef Medline
47. Nojima H, Rothhämel S, Shimizu T, Kim CH, Yonemura S, Marlow FL, Hibi M (2010) Syntabulin, a motor protein linker, controls dorsal determination. Development 137:923-933. CrossRef Medline
48. Palanca AM, Lee SL, Yee LE, Joe-Wong C, Trinh le A, Hiroyasu E, Husain M, Fraser SE, Pellegrini M, Sagasti A (2013) New transgenic reporters identify somatosensory neuron subtypes in larval zebrafish. Dev Neurobiol 73:152-167. CrossRef Medline
49. Paquet D, Bhat R, Sydow A, Mandelkow EM, Berg S, Hellberg S, Fälting J, Distel M, Köster RW, Schmid B, Haass C (2009) A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest 119:1382-1395. CrossRef Medline
50. Patel N, Thierry-Mieg D, Mancillas JR (1993) Cloning by insertional mutagenesis of a cDNA encoding Caenorhabditis elegans kinesin heavy chain. Proc Natl Acad Sci U S A 90:9181-9185. CrossRef Medline
51. Plucińska G, Paquet D, Hruscha A, Godinho L, Haass C, Schmid B, Misgeld T (2012) In vivo imaging of disease-related mitochondrial dynamics in a vertebrate model system. J Neurosci 32:16203-16212. CrossRef Medline
52. Poirier K, Lebrun N, Broix L, Tian G, Saillour Y, Boscheron C, Parrini E, Valence S, Pierre BS, Oger M, Lacombe D, Geneviève D, Fontana E, Darra F, Cances C, Barth M, Bonneau D, Bernadina BD, N guyen S, Gitiaux C, et al. (2013) Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat Genet 45: 639-647. CrossRef Medline
53. Randall TS, Moores C, Stephenson FA (2013) Delineation of the TRAK binding regions of the kinesin-1 motor proteins. FEBS Lett 587:3763-3769. CrossRef Medline
54. Reid E, Kloos M, Ashley-Koch A, Hughes L, Bevan S, Svenson IK, Graham FL, Gaskell PC, Dearlove A, Pericak-Vance MA, Rubinsztein DC, Marchuk DA (2002) A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). Am J Hum Genet 71:1189-1194. CrossRef Medline
55. Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnóczky G (2008) Bidirectional Ca2 -dependent control of mitochondrial dynamics by the miro GTPase. Proc Natl Acad Sci U S A 105:20728-20733. CrossRef Medline
56. Sato T, Takahoko M, Okamoto H (2006) HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 44:136-142. CrossRef Medline
57. 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. CrossRef Medline
58. Schule R, Kremer BP, Kassubek J, Auer-Grumbach M, Kostic V, Klopstock T, Klimpe S, Otto S, Boesch S, van de Warrenburg BP, Schöls L (2008) SPG10 is a rare cause of spastic paraplegia in European families. J Neurol Neurosurg Psychiatry 79:584-587. CrossRef Medline
59. Schwarz TL (2013) Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol 5:a011304. CrossRef Medline
60. Sheng ZH, Cai Q (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 13:77-93. CrossRef Medline
61. Smith MJ, Pozo K, Brickley K, Stephenson FA (2006) Mapping the GRIF-1 binding domain of the kinesin, KIF5C, substantiates a role for GRIF-1 as an adaptor protein in the anterograde trafficking of cargoes. J Biol Chem 281:27216-27228. CrossRef Medline
62. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N (1998) Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93:1147-1158. CrossRef Medline
63. Vallat JM, Mathis S, Funalot B (2013) The various Charcot-Marie-tooth diseases. Curr Opin Neurol 26:473-480. CrossRef Medline
64. van Spronsen M, Mikhaylova M, Lipka J, Schlager MA, van den Heuvel DJ, Kuijpers M, Wulf PS, Keijzer N, Demmers J, Kapitein LC, Jaarsma D, Gerritsen HC, Akhmanova A, Hoogenraad CC (2013) TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 77:485-502. CrossRef Medline
65. Villefranc JA, Amigo J, Lawson ND (2007) Gateway compatible vectors for analysis of gene function in the zebrafish. Dev Dyn 236:3077-3087. CrossRef Medline
66. Walhout AJ, Temple GF, Brasch MA, Hartley JL, Lorson MA, van den Heuvel S, Vidal M (2000) GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol 328:575-592. CrossRef Medline
67. Wang JT, Medress ZA, Barres BA (2012) Axon degeneration: molecular mechanisms of a self-destruction pathway. J Cell Biol 196:7-18. CrossRef Medline
68. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191. CrossRef Medline
69. Westerfield M (1995) The zebrafish book: a guide for the laboratory use of Zebrafish (Danio rerio), Ed 3. Eugene, OR: University of Oregon.
70. Wozniak MJ, Melzer M, Dorner C, Haring HU, Lammers R (2005) The novel protein KBP regulates mitochondria localization by interaction with a kinesin-like protein. BMC Cell Biol 6:35. CrossRef Medline
71. Xia CH, Roberts EA, Her LS, Liu X, Williams DS, Cleveland DW, Goldstein LS (2003) Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J Cell Biol 161:55-66. CrossRef Medline
72. Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, Takeda S, Yang HW, Terada S, Nakata T, Takei Y, Saito M, Tsuji S, Hayashi Y, Hirokawa N (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105:587-597. CrossRef Medline