Spastin-interacting protein NA14/SSNA1 functions in cytokinesis and axon development

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Goyal, Uma ^a   Renvoisé, Benoît ^a   Chang, Jaerak ^a   Blackstone, Craig ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; NA14 PROTEIN; SPASTIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; AUTOANTIGEN; NA14 NUCLEAR AUTOANTIGEN; NUCLEAR PROTEIN; SMALL INTERFERING RNA; SPAST PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BRAIN CELL CULTURE; CELL DIVISION; CENTRIOLE; CENTROSOME; CONTROLLED STUDY; CYTOKINESIS; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; MICROTUBULE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIMARY CULTURE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOTONEURON; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

RATTUS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AUTOANTIGENS; AXONS; CELL DIFFERENTIATION; CENTROSOME; CEREBRAL CORTEX; CYTOKINESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELA CELLS; HUMANS; MICROTUBULES; MOTOR NEURONS; NEUROGENESIS; NUCLEAR PROTEINS; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84911478031     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112428     Document Type: Article

References (50)

1. Soderblom C, Blackstone C (2006) Traffic accidents: molecular genetic insights into the pathogenesis of the hereditary spastic paraplegias. Pharmacol Ther 109: 42-56.
2. Blackstone C (2012) Cellular pathways of hereditary spastic paraplegia. Annu Rev Neurosci 35: 25-47.
3. Fink JK (2013) Hereditary spastic paraplegia: clinico-pathologic features and emerging molecular mechanisms. Acta Neuropathol 126: 307-328.
4. Finsterer J, Löscher W, Quasthoff S, Wanschitz J, Auer-Grumbach M, et al. (2012) Hereditary spastic paraplegias with autosomal dominant, recessive, Xlinked, or maternal trait of inheritance. J Neurol Sci 318: 1-18.
5. Harding AE (1983) Classification of the hereditary ataxias and paraplegias. Lancet 1(8334): 1151-1155.
6. Reid E (2003) Science in motion: common molecular pathological themes emerge in the hereditary spastic paraplegias. J Med Genet 40: 81-86.
7. Blackstone C, O'Kane CJ, Reid E (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat Rev Neurosci 12: 31-42.
8. Hazan J, Fonknechten N, Mavel D, Paternotte C, Samson D, et al. (1999) Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat Genet 23: 296-303.
9. Errico A, Ballabio A, Rugarli EI (2002) Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11: 153-163.
10. Claudiani P, Riano E, Errico A, Andolfi G, Rugarli EI (2005) Spastin subcellular localization is regulated through usage of different translation start sites and active export from the nucleus. Exp Cell Res 309: 358-369.
11. Park SH, Zhu P-P, Parker RL, Blackstone C (2010) Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J Clin Invest 120: 1097-1110.
12. Connell JW, Lindon C, Luzio JP, Reid E (2009) Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 10: 42-56.
13. Svenson IK, Kloos MT, Jacon A, Gallione C, Horton AC, et al. (2005) Subcellular localization of spastin: implications for the pathogenesis of hereditary spastic paraplegia. Neurogenetics 6: 135-141.
14. Errico A, Claudiani P, D'Addio M, Rugarli EI (2004) Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Hum Mol Genet 13: 2121-2132.
15. Ramos-Morales F, Infante C, Fedriani C, Bornens M, Rios RM (1998) NA14 is a novel nuclear autoantigen with a coiled-coil domain. J Biol Chem 273: 1634-1639.
16. Nozawa K, Ikeda K, Satoh M, Reeves WH, Stewart CM, et al. (2009) Autoantibody to NA14 is an independent marker primarily for Sjogren's syndrome. Front Biosci 14: 3733-3739.
17. Price HP, Hodgkinson MR, Curwen RS, MacLean LM, Brannigan JA, et al. (2012) The orthologue of Sjo?gren's syndrome nuclear autoantigen 1 (SSNA1) in Trypanosoma brucei is an immunogenic self-assembling molecule. PLoS One 7: e31842.
18. Pfannenschmid F, Wimmer VC, Rios R-M, Geimer S, Kröckel U, et al. (2003) Chlamydomonas DIP13 and human NA14: a new class of proteins associated with microtubule structures is involved in cell division. J Cell Sci 116: 1449-1462.
19. Schoppmeier J, Mages W, Lechtreck K-F (2005) GFP as a tool for the analysis of proteins in the flagellar basal apparatus of Chlamydomonas. Cell Motil Cytoskeleton 61: 189-200.
20. Dogterom M, Surrey T (2013) Microtubule organization in vitro. Curr Opin Cell Biol 25: 23-29.
21. Piel M, Nordberg J, Euteneuer U, Bornens M (2001) Centrosome-dependent exit of cytokinesis in animal cells. Science 291: 1550-1553.
22. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, et al. (2006) Flies without centrioles. Cell 125: 1375-1386.
23. Avidor-Reiss T, Gopalakrishnan J (2013) Building a centriole. Curr Opin Cell Biol 25: 72-77.
24. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, et al. (2005) Centrosome localization determines neuronal polarity. Nature 436: 704-708.
25. Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30: 276-283.
26. Baas PW, Yu W (1996) A composite model for establishing the microtubule arrays of the neuron. Mol Neurobiol 12: 145-161.
27. Zmuda JF, Rivas RJ (1998) The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil Cytoskeleton 41: 18-38.
28. Zhu P-P, Patterson A, Lavoie B, Stadler J, Shoeb M, et al. (2003) Cellular localization, oligomerization, and membrane association of the hereditary spastic paraplegia 3A (SPG3A) protein atlastin. J Biol Chem 278: 49063-49071.
29. Yang D, Rismanchi N, Renvoisé B, Lippincott-Schwartz J, Blackstone C, et al. (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15: 1278-1286.
30. Zhu P-P, Soderblom C, Tao-Cheng J-H, Stadler J, Blackstone C (2006) SPG3A protein atlastin-1 is enriched in growth cones and promotes axon elongation during neuronal development. Hum Mol Genet 15: 1343-1353.
31. Lee S, Chang J, RenvoiséB, Tipirneni A, Yang S, et al. (2012) MITD1 is recruited to midbodies by ESCRT-III and participates in cytokinesis. Mol Biol Cell 23: 4347-4361.
32. Casanova M, Crobu L, Blaineau C, Bourgeois N, Bastien P, et al. (2009) Microtubule-severing proteins are involved in flagellar length control and mitosis in Trypanosomatids. Mol Microbiol 71: 1353-1370.
33. Charron F, Tessier-Lavigne M (2007) The Hedgehog, TGF-b/BMP, and Wnt families of morphogens in axon guidance. Adv Exp Med Biol 621: 116-133.
34. Solowska JM, Morfini G, Falnikar A, Himes BT, Brady ST, et al. (2008) Quantitative and functional analyses of spastin in the nervous system: implications for hereditary spastic paraplegia. J Neurosci 28: 2147-2157.
35. Raino E, Martignoni M, Cartelli D, Crippa F, Toldo I, et al. (2009) Pleitropic effects of spastin on neurite growth depending depending on expression levels. J Neurochem 108: 1277-1288.
36. Renvoisé B, Stadler J, Singh R, Bakowska JC, Blackstone C (2012) Spg20-/- mice reveal multimodal functions for Troyer syndrome protein spartin in lipid droplet maintenance, cytokinesis and BMP signaling. Hum Mol Genet 2012; 21: 3604-3618.
37. Denton KR, Lei L, Grenier J, Rodionov V, Blackstone C, et al. (2014) Loss of spastin function results in disease-specific axonal defects in human pluripotent stem cell-based models of hereditary spastic paraplegia. Stem Cells 32: 414-423.
38. Havlicek S, Kohl Z, Mishra HK, Prots I, Eberhardt E, et al. (2014) Gene dosage-dependent rescue of HSP neurite defects in SPG4 patients' neurons. Hum Mol Genet 23: 2527-2541.
39. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, et al. (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426: 570-574.
40. Renvoisé B, Parker RL, Yang D, Bakowska JC, Hurley JH, et al. (2010) SPG20 protein spartin is recruited to midbodies by ESCRT-III protein Ist1 and participates in cytokinesis. Mol Biol Cell 21: 3293-3303.
41. van Vlierberghe P, Meijerink JPP, Lee C, Ferrando AA, Look AT, et al. (2006) A new recurrent 9q34 duplication in pediatric T-cell acute lymphoblastic leukemia. Leukemia 20: 1245-1253.
42. Gress TM, Müller-Pillasch F, Geng M, Zimmerhackl F, Zehetner G, et al. (1996) Oncogene 13: 1819-1830.
43. McDermott CJ, Grierson AJ, Wood JD, Bingley M, Wharton SB, et al. (2003) Hereditary spastic paraparesis: disrupted intracellular transport associated with spastin mutation. Ann Neurol 54: 748-59.
44. Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, et al. (2008) The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19: 1485-1498.
45. Stone MC, Rao K, Gheres KW, Kim S, Tao J, et al. (2012) Normal spastin gene dosage is specifically required for axon regeneration. Cell Rep 2: 1340-1350.
46. McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75: 419-429.
47. Ahmad FJ, Yu W, McNally FJ, Baas PW (1999) An essential role for katanin in severing microtubules in the neuron. J Cell Biol 145: 305-315.
48. Rodríguez-Rodríguez M, Treviño MA, Laurents DV, Arranz R, Valpuesta JM, et al. (2011) Characterization of the structure and self-recognition of the human centrosomal protein NA14: implications for stability and function. Protein Eng Des Sel 24: 883-892.
49. Aki T, Funakoshi T, Nishida-Kitayama J, Mizukami Y (2008) TPRA40/ GPR175 regulates early mouse embryogenesis through functional membrane transport by Sjogren's syndrome-associated protein NA14. J Cell Physiol 217: 194-206.
50. Lai CK, Gupta N, Wen X, Rangell L, Chih B, et al. (2011) Functional characterization of putative cilia genes by high-content analysis. Mol Biol Cell 22: 1104-1119.