Spastic Paraplegia Mutation N256S in the Neuronal Microtubule Motor KIF5A Disrupts Axonal Transport in a Drosophila HSP Model

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Füger, Petra ^a,b   Sreekumar, Vrinda ^a,b,c   Schüle, Rebecca ^a   Kern, Jeannine V ^a   Stanchev, Doychin T ^a   Schneider, Carola D ^a,b   Karle, Kathrin N ^a   Daub, Katharina J ^a   Siegert, Vera K ^a   Flötenmeyer, Matthias ^d   Schwarz, Heinz ^d   Schöls, Ludger ^a,c   Rasse, Tobias M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; KINESIN 1; MOLECULAR MOTOR; PROTEIN KIF5A; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DISRUPTION; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE LOSS; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC CODE; HAPLOINSUFFICIENCY; HEREDITARY MOTOR SENSORY NEUROPATHY; HETEROZYGOTE; KIF5A GENE; LARVAL STAGE; MALE; MICROTUBULE; MITOCHONDRIAL MEMBRANE; MOUSE; MUTATIONAL ANALYSIS; NERVE FIBER TRANSPORT; NEUROFILAMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT; SYNAPSE VESICLE;

ANIMALS; AXONAL TRANSPORT; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION; HUMANS; KINESIN; MICE; MICROTUBULES; MUTATION; SPASTIC PARAPLEGIA, HEREDITARY; SYNAPSES;

ARTHROPODA;

EID: 84870666177     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003066     Document Type: Article

References (53)

1. Wharton SB, McDermott CJ, Grierson AJ, Wood JD, Gelsthorpe C, et al. (2003) The cellular and molecular pathology of the motor system in hereditary spastic paraparesis due to mutation of the spastin gene. J Neuropathol Exp Neurol 62: 1166-1177.
2. 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.
3. Blackstone C, O'Kane CJ, Reid E, (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat Rev Neurosci 12: 31-42.
4. Schule R, Kremer BP, Kassubek J, Auer-Grumbach M, Kostic V, et al. (2008) SPG10 is a rare cause of spastic paraplegia in European families. J Neurol Neurosurg Psychiatry 79: 584-587.
5. Crimella C, Baschirotto C, Arnoldi A, Tonelli A, Tenderini E, et al. (2011) Mutations in the motor and stalk domains of KIF5A in spastic paraplegia type 10 and in axonal Charcot-Marie-Tooth type 2. Clin Genet.
6. 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.
7. Ebbing B, Mann K, Starosta A, Jaud J, Schols L, et al. (2008) Effect of spastic paraplegia mutations in KIF5A kinesin on transport activity. Hum Mol Genet 17: 1245-1252.
8. Kozielski F, Sack S, Marx A, Thormahlen M, Schonbrunn E, et al. (1997) The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell 91: 985-994.
9. Goizet C, Boukhris A, Mundwiller E, Tallaksen C, Forlani S, et al. (2009) Complicated forms of autosomal dominant hereditary spastic paraplegia are frequent in SPG10. Hum Mutat 30: E376-385.
10. Brendza KM, Rose DJ, Gilbert SP, Saxton WM, (1999) Lethal kinesin mutations reveal amino acids important for ATPase activation and structural coupling. J Biol Chem 274: 31506-31514.
11. Brendza KM, Sontag CA, Saxton WM, Gilbert SP, (2000) A kinesin mutation that uncouples motor domains and desensitizes the gamma-phosphate sensor. J Biol Chem 275: 22187-22195.
12. 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.
13. Hurd DD, Saxton WM, (1996) Kinesin Mutations Cause Motor Neuron Disease Phenotypes by Disrupting Fast Axonal Transport in Drosophila. Genetics 144: 1075-1085.
14. 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.
15. Djagaeva I, Rose DJ, Lim A, Venter CE, Brendza KM, et al. (2012) Three Routes to Suppression of the Neurodegenerative Phenotypes Caused by Kinesin Heavy Chain Mutations. Genetics.
16. Schmidt I, Thomas S, Kain P, Risse B, Naffin E, et al. (2012) Kinesin heavy chain function in Drosophila glial cells controls neuronal activity. J Neurosci 32: 7466-7476.
17. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, et al. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441: 1162-1166.
18. Barkus RV, Klyachko O, Horiuchi D, Dickson BJ, Saxton WM, (2007) Identification of an Axonal Kinesin-3 Motor for Fast Anterograde Vesicle Transport that Facilitates Retrograde Transport of Neuropeptides. Mol Biol Cell pp. E07-03-0261.
19. Mahr A, Aberle H, (2006) The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns 6: 299-309.
20. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, et al. (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24: 10466-10474.
21. Husain QM, Ewer J, (2004) Use of targetable gfp-tagged neuropeptide for visualizing neuropeptide release following execution of a behavior. J Neurobiol 59: 181-191.
22. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
23. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, et al. (2006) Bruchpilot Promotes Active Zone Assembly, Ca2+-Channel Clustering, and Vesicle Release. Science.
24. Pack-Chung E, Kurshan PT, Dickman DK, Schwarz TL, (2007) A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nature Neurosci 10: 980-989.
25. Pulipparacharuvil S, Akbar MA, Ray S, Sevrioukov EA, Haberman AS, et al. (2005) Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J Cell Sci 118: 3663-3673.
26. Kohler K, Brunner E, Guan XL, Boucke K, Greber UF, et al. (2009) A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvation-induced autophagy in Drosophila. Autophagy 5: 980-990.
27. Nixon RA, Cataldo AM, (1995) The endosomal-lysosomal system of neurons: new roles. Trends Neurosci 18: 489-496.
28. Uchida A, Alami NH, Brown A, (2009) Tight functional coupling of kinesin-1A and dynein motors in the bidirectional transport of neurofilaments. Mol Biol Cell 20: 4997-5006.
29. Wang L, Brown A, (2010) A hereditary spastic paraplegia mutation in kinesin-1A/KIF5A disrupts neurofilament transport. Mol Neurodegener 5: 52.
30. Karle KN, Mockel D, Reid E, Schols L, (2012) Axonal transport deficit in a KIF5A(-/-) mouse model. Neurogenetics 13: 169-179.
31. Eaton BA, Fetter RD, Davis GW, (2002) Dynactin is necessary for synapse stabilization. Neuron 34: 729-741.
32. Pielage J, Fetter RD, Davis GW, (2005) Presynaptic spectrin is essential for synapse stabilization. Curr Biol 15: 918-928.
33. Eaton BA, Davis GW, (2005) LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47: 695-708.
34. Pielage J, Cheng L, Fetter RD, Carlton PM, Sedat JW, et al. (2008) A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron 58: 195-209.
35. Fan Y, Bergmann A, (2010) The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ 17: 534-539.
36. Muller HJ, (1932) Further studies on the nature and causes of gene mutations. Proceedings of the Sixth International Congress of Genetics, Ithaca, New York 1: 213-255.
37. Bryantseva SA, Zhapparova ON, (2012) Bidirectional transport of organelles: unity and struggle of opposing motors. Cell Biol Int 36: 1-6.
38. Soppina V, Rai AK, Ramaiya AJ, Barak P, Mallik R, (2009) Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc Natl Acad Sci U S A 106: 19381-19386.
39. Gross SP, Welte MA, Block SM, Wieschaus EF, (2002) Coordination of opposite-polarity microtubule motors. J Cell Biol 156: 715-724.
40. Muller MJ, Klumpp S, Lipowsky R, (2008) Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc Natl Acad Sci U S A 105: 4609-4614.
41. Muller MJ, Klumpp S, Lipowsky R, (2010) Bidirectional transport by molecular motors: enhanced processivity and response to external forces. Biophys J 98: 2610-2618.
42. 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.
43. 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.
44. Dadon-Nachum M, Melamed E, Offen D, (2011) The "dying-back" phenomenon of motor neurons in ALS. J Mol Neurosci 43: 470-477.
45. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, et al. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185: 232-240.
46. Frey D, Schneider C, Xu L, Borg J, Spooren W, et al. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20: 2534-2542.
47. Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, et al. (2000) Comparative genomics of the eukaryotes. Science 287: 2204-2215.
48. Lasek RJ, Oblinger MM, Drake PF, (1983) Molecular biology of neuronal geometry: expression of neurofilament genes influences axonal diameter. Cold Spring Harb Symp Quant Biol 48 Pt 2: 731-744.
49. Kasher PR, De Vos KJ, Wharton SB, Manser C, Bennett EJ, et al. (2009) Direct evidence for axonal transport defects in a novel mouse model of mutant spastin-induced hereditary spastic paraplegia (HSP) and human HSP patients. J Neurochem 110: 34-44.
50. Rasse TM, Fouquet W, Schmid A, Kittel RJ, Mertel S, et al. (2005) Glutamate receptor dynamics organizing synapse formation in vivo. Nat Neurosci 8: 898-905.
51. Zhang Y, Fuger P, Hannan SB, Kern JV, Lasky B, et al. (2010) In vivo imaging of intact Drosophila larvae at sub-cellular resolution. J Vis Exp.
52. Fuger P, Behrends LB, Mertel S, Sigrist SJ, Rasse TM, (2007) Live imaging of synapse development and measuring protein dynamics using two-color fluorescence recovery after photo-bleaching at Drosophila synapses. Nat Protoc 2: 3285-3298.
53. Ramot D, Johnson BE, Berry TL Jr, Carnell L, Goodman MB, (2008) The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 3: e2208 doi:10.1371/journal.pone.0002208.