A Hereditary Spastic Paraplegia Mouse Model Supports a Role of ZFYVE26/SPASTIZIN for the Endolysosomal System

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Khundadze, Mukhran ^a   Kollmann, Katrin ^b   Koch, Nicole ^a   Biskup, Christoph ^a   Nietzsche, Sandor ^a   Zimmer, Geraldine ^a   Hennings, J Christopher ^a   Huebner, Antje K ^a   Symmank, Judit ^a   Jahic, Amir ^a   Ilina, Elena I ^c   Karle, Kathrin ^c,d   Schöls, Ludger ^c,d   Kessels, Michael ^a   Braulke, Thomas ^b   Qualmann, Britta ^a   Kurth, Ingo ^a   Beetz, Christian ^a   Hübner, Christian A ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; EARLY ENDOSOME ANTIGEN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; SPASTIZIN PROTEIN; UNCLASSIFIED DRUG;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELLULAR DISTRIBUTION; CEREBELLAR ATAXIA; CONTROLLED STUDY; DENSITY GRADIENT; EMBRYO; HEREDITARY MOTOR SENSORY NEUROPATHY; MALE; MOLECULAR PATHOLOGY; MOTONEURON; MOUSE; NERVE FIBER DEGENERATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PURKINJE CELL;

ANIMALS; BRAIN; CARRIER PROTEINS; CORPUS CALLOSUM; DISEASE MODELS, ANIMAL; ENDOSOMES; HUMANS; LYSOSOMES; MICE; MICE, KNOCKOUT; MOTOR NEURONS; MUTATION; RETINAL DEGENERATION; SPASTIC PARAPLEGIA, HEREDITARY;

EID: 84892728118     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003988     Document Type: Article

References (49)

1. Depienne C, Stevanin G, Brice A, Durr A, (2007) Hereditary spastic paraplegias: an update. Curr Opin Neurol 20: 674-680.
2. Harding AE, (1983) Classification of the hereditary ataxias and paraplegias. Lancet 1: 1151-1155.
3. Reid E, (1999) The hereditary spastic paraplegias. J Neurol 246: 995-1003.
4. Blackstone C, (2012) Cellular pathways of hereditary spastic paraplegia. Annu Rev Neurosci 35: 25-47.
5. Hanein S, Martin E, Boukhris A, Byrne P, Goizet C, et al. (2008) Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome. Am J Hum Genet 82: 992-1002.
6. Schule R, Schlipf N, Synofzik M, Klebe S, Klimpe S, et al. (2009) Frequency and phenotype of SPG11 and SPG15 in complicated hereditary spastic paraplegia. J Neurol Neurosurg Psychiatry 80: 1402-1404.
7. Schule R, Schols L, (2011) Genetics of hereditary spastic paraplegias. Semin Neurol 31: 484-493.
8. Lupas A, (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21 (10) (): 375-82.
9. Kutateladze T, Overduin M, (2001) Structural mechanism of endosome docking by the FYVE domain. Science 291: 1793-1796.
10. Sagona AP, Nezis IP, Pedersen NM, Liestol K, Poulton J, et al. (2010) PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat Cell Biol 12: 362-371.
11. Stevanin G, Santorelli FM, Azzedine H, Coutinho P, Chomilier J, et al. (2007) Mutations in SPG11, encoding spatacsin, are a major cause of spastic paraplegia with thin corpus callosum. Nat Genet 39: 366-372.
12. Martin E, Yanicostas C, Rastetter A, Naini SM, Maouedj A, et al. (2012) Spatacsin and spastizin act in the same pathway required for proper spinal motor neuron axon outgrowth in zebrafish. Neurobiol Dis 48: 299-308.
13. Slabicki M, Theis M, Krastev DB, Samsonov S, Mundwiller E, et al. (2010) A genome-scale DNA repair RNAi screen identifies SPG48 as a novel gene associated with hereditary spastic paraplegia. PLoS Biol 8: e1000408.
14. Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MN, et al. (2011) The fifth adaptor protein complex. PLOS Biol 9: e1001170.
15. Hirst J, Borner GH, Edgar J, Hein MY, Mann M, et al. (2013) Interaction Between AP-5 and the Hereditary Spastic Paraplegia Proteins SPG11 and SPG15. Mol Biol Cell 24: 2558-69.
16. Anderson GW, Goebel HH, Simonati A, (2012) Human pathology in NCL. Biochim Biophys Acta 1832 (11) (): 1807-26.
17. Dickinson ME, Bearman G, Tille S, Lansford R, Fraser SE, (2001) Multi-spectral imaging and linear unmixing add a whole new dimension to laser scanning fluorescence microscopy. Biotechniques 31: 1272, 1274-1276, 1278.
18. Zimmermann T, Rietdorf J, Pepperkok R, (2003) Spectral imaging and its applications in live cell microscopy. FEBS Lett 546: 87-92.
19. Boukhris A, Stevanin G, Feki I, Denora P, Elleuch N, et al. (2009) Tunisian hereditary spastic paraplegias: clinical variability supported by genetic heterogeneity. Clin Genet 75: 527-536.
20. 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.
21. Tarrade A, Fassier C, Courageot S, Charvin D, Vitte J, et al. (2006) A mutation of spastin is responsible for swellings and impairment of transport in a region of axon characterized by changes in microtubule composition. Hum Mol Genet 15: 3544-3558.
22. Beetz C, Koch N, Khundadze M, Zimmer G, Nietzsche S, et al. (2013) A spastic paraplegia mouse model reveals REEP1-dependent ER shaping. J Clin Invest 123 (10) (): 4273-4282.
23. Fink JK, (2006) Hereditary spastic paraplegia. Curr Neurol Neurosci Rep 6: 65-76.
24. Elleder M, (1978) A histochemical and ultrastructural study of stored material in neuronal ceroid lipofuscinosis. Virchows Arch B Cell Pathol 28: 167-178.
25. Terman A, Brunk UT, (2004) Lipofuscin. Int J Biochem Cell Biol 36: 1400-1404.
26. Prasad VV, Pullarkat RK, (1996) Brain lysosomal hydrolases in neuronal ceroid-lipofuscinoses. Mol Chem Neuropathol 29: 169-179.
27. Brunk UT, Terman A, (2002) Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic Biol Med 33: 611-619.
28. Murmu RP, Martin E, Rastetter A, Esteves T, Muriel MP, et al. (2011) Cellular distribution and subcellular localization of spatacsin and spastizin, two proteins involved in hereditary spastic paraplegia. Mol Cell Neurosci 47: 191-202.
29. Stenmark H, Aasland R, Toh BH, D'Arrigo A, (1996) Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem 271: 24048-24054.
30. Simons JP, Al-Shawi R, Minogue S, Waugh MG, Wiedemann C, et al. (2009) Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons. Proc Natl Acad Sci U S A 106: 11535-11539.
31. Salazar G, Craige B, Wainer BH, Guo J, De Camilli P, et al. (2005) Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol Biol Cell 16: 3692-3704.
32. Ohno H, (2006) Physiological roles of clathrin adaptor AP complexes: lessons from mutant animals. J Biochem 139: 943-948.
33. Hirst J, Irving C, Borner GH, (2013) Adaptor Protein Complexes AP-4 and AP-5: New Players in Endosomal Trafficking and Progressive Spastic Paraplegia. Traffic 14: 153-164.
34. Schwenk F, Baron U, Rajewsky K, (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081.
35. Hennings JC, Picard N, Huebner AK, Stauber T, Maier H, et al. (2012) A mouse model for distal renal tubular acidosis reveals a previously unrecognized role of the V-ATPase a4 subunit in the proximal tubule. EMBO Mol Med 4: 1057-1071.
36. Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, et al. (2011) Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci 31: 18364-18380.
37. Sinning A, Liebmann L, Kougioumtzes A, Westermann M, Bruehl C, et al. (2011) Synaptic glutamate release is modulated by the Na+-driven Cl-/HCO3- exchanger Slc4a8. J Neurosci 31: 7300-7311.
38. Rust MB, Alper SL, Rudhard Y, Shmukler BE, Vicente R, et al. (2007) Disruption of erythroid K-Cl cotransporters alters erythrocyte volume and partially rescues erythrocyte dehydration in SAD mice. J Clin Invest 117: 1708-1717.
39. Claussen M, Kubler B, Wendland M, Neifer K, Schmidt B, et al. (1997) Proteolysis of insulin-like growth factors (IGF) and IGF binding proteins by cathepsin D. Endocrinology 138: 3797-3803.
40. Rust MB, Faulhaber J, Budack MK, Pfeffer C, Maritzen T, et al. (2006) Neurogenic mechanisms contribute to hypertension in mice with disruption of the K-Cl cotransporter KCC3. Circ Res 98: 549-56.
41. Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS, (2008) Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab 8: 512-521.
42. Joyner AL (1993) Gene targeting: a practical approach. IRL Press.
43. Karle KN, Möckel D, Reid E, Schöls L, (2012) Neurogenetics 13 (2) (): 169-79.
44. Marschner K, Kollmann K, Schweizer M, Braulke T, Pohl S, (2011) A key enzyme in the biogenesis of lysosomes is a protease that regulates cholesterol metabolism. Science 333: 87-90.
45. Kollmann K, Damme M, Markmann S, Morelle W, Schweizer M, et al. (2012) Lysosomal dysfunction causes neurodegeneration in mucolipidosis II 'knock-in' mice. Brain 135: 2661-2675.
46. Jacobs S, Ruusuvuori E, Sipilä ST, Haapanen A, Damkier HH, Kurth I, et al. (2008) Mice with targeted Slc4a10 gene disruption have small brain ventricles and show reduced neuronal excitability. Proc Natl Acad Sci U S A 105 (1) (): 311-6.
47. Irintchev A, Simova O, Eberhardt KA, Morellini F, Schachner M, (2005) Impacts of lesion severity and tyrosine kinase receptor B deficiency on functional outcome of femoral nerve injury assessed by a novel single-frame motion analysis in mice. The European journal of neuroscience 22: 802-808.
48. Schnell SA, Staines WA, Wessendorf MW, (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47: 719-730.
49. Poët M, Kornak U, Schweizer M, Zdebik AA, Scheel O, et al. (2006) Lysosomal storage disease upon disruption of the neuronal chloride transport protein ClC-6. Proc Natl Acad Sci U S A.