Hereditary spastic paraplegia SPG4: What is known and not known about the disease

Brain

Volumn 138, Issue 9, 2015, Pages 2471-2484

  Solowska, Joanna M ^a   Baas, Peter W ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

endosome; hereditary spastic paraplegia; microtubule endoplasmic reticulum; SPAST; spastin

Indexed keywords

SPASTIN; ADENOSINE TRIPHOSPHATASE; SPAST PROTEIN, HUMAN;

ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CLINICAL FEATURE; COGNITIVE DEFECT; DISEASE COURSE; FRUIT FLY MODEL; GENE DELETION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; LIMITED MOBILITY; LOSS OF FUNCTION MUTATION; MICROTUBULE; MISSENSE MUTATION; MOUSE MODEL; NERVE FIBER TRANSPORT; NONHUMAN; NONSENSE MUTATION; ONSET AGE; PENETRANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; ANIMAL; CHEMISTRY; DISEASE MODEL; GENETICS; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AXONAL TRANSPORT; DISEASE MODELS, ANIMAL; HUMANS; MUTATION; SPASTIC PARAPLEGIA, HEREDITARY;

EID: 84940734550     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv178     Document Type: Article

References (94)

1. Allison R, Lumb JH, Fassier C, Connell JW, Ten Martin D, Seaman MN, et al. An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J Cell Biol 2013; 202: 527-43.
2. Aridon P, Ragonese P, De Fusco M, Lo Coco D, Salemi G, Casari G, et al. Autosomal dominant hereditary spastic paraplegia: report of a large Italian family with R581X spastin mutation. Neurol Sci 2007; 28: 171-4.
3. Aulitzky A, Friedrich K, Gläser D, Gastl R, Kubisch C, Ludolph AC, et al. A complex form of hereditary spastic paraplegia in three siblings due to somatic mosaicism for a novel SPAST mutation in the mother. J Neurol Sci 2014; 347: 352-5.
4. Baas PW, Ahmad FJ. Beyond taxol: microtubule-based treatment of disease and injury of the nervous system [Review]. Brain 2013; 136: 2937-51.
5. Baas PW, Vidya Nadar C, Myers KA. Axonal transport of microtubules: the long and short of it [Review]. Traffic 2006; 7: 490-8.
6. Beetz C, Nygren AO, Schickel J, Auer-Grumbach M, Bürk K, Heide G, et al. High frequency of partial SPAST deletions in autosomal dominant hereditary spastic paraplegia. Neurology 2006; 67: 1926-30.
7. Beetz C, Schüle R, Deconinck T, Tran-Viet KN, Zhu H, Kremer BP, et al. REEP1 mutation spectrum and genotype/phenotype correlation in hereditary spastic paraplegia type 31. Brain 2008; 131: 1078-86.
8. Blackstone C, O'Kane CJ, Reid, E. Hereditary spastic paraplegias: membrane traffic and the motor pathway [Review]. Nat Rev Neurosci 2011; 12: 31-42.
9. Blackstone C. Cellular pathways of hereditary spastic paraplegia [Review]. Annu Rev Neurosci 2012; 35: 25-47.
10. Blair MA, Riddle ME, Wells JF, Breviu BA, Hedera P. Infantile onset of hereditary spastic paraplegia poorly predicts the genotype. Pediatr Neurol 2007; 36: 382-6.
11. Boone PM, Yuan B, Campbell IM, Scull JC, Withers MA, Baggett BC, et al. The Alu-rich genomic architecture of SPAST predisposes to diverse and functionally distinct disease-associated CNV alleles. Am J Hum Genet 2014; 95: 143-61.
12. Burger J, Fonknechten N, Hoeltzenbein M, Neumann L, Bratanoff E, Hazan J, et al. Hereditary spastic paraplegia caused by mutations in the SPG4 gene. Eur J Hum Genet 2000; 8: 771-6.
13. Cai D, McEwen DP, Martens JR, Meyhofer E, Verhey KJ. Single molecule imaging reveals differences in microtubule track selection between Kinesin motors. PLoS Biol 2009; 7: e1000216.
14. Charron F, Tessier-Lavigne M. The Hedgehog, TGF-beta/bone morphogenic protein and Wnt families of morphogens in axon guidance [Review]. Adv Exp Med Biol 2007; 621: 116-33.
15. Chinnery PF, Keers SM, Holden MJ, Ramesh V, Dalton A. Infantile hereditary spastic paraparesis due to codominant mutations in the spastin gene. Neurology 2004; 63: 710-12.
16. Claudiani P, Riano E, Errico A, Andolfi G, Rugarli EI. Spastin subcellular localization is regulated through usage of different translation start sites and active export from the nucleus. Exp Cell Res 2005; 309: 358-69.
17. Connell JW, Lindon C, Luzio JP, Reid E. Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 2009; 10: 42-56.
18. Crippa F, Panzeri C, Martinuzzi A, Arnoldi A, Redaelli F, Tonelli A, et al. Eight novel mutations in SPG4 in a large sample of patients with hereditary spastic paraplegia. Arch Neurol 2006; 63: 750-5.
19. Denton KR, Lei L, Grenier J, Rodionov V, Blackstone C, Li XJ. Loss of spastin function results in disease-specific axonal defects in human pluripotent stem cell-based models of hereditary spastic paraplegia. Stem Cells 2014; 32: 414-23.
20. Depienne C, Fedirko E, Forlani S, Cazeneuve C, Ribä P, Feki I, et al. Exon deletions of SPG4 are a frequent cause of hereditary spastic paraplegia. J Med Genet 2007; 44: 281-4.
21. Dürr A, Tallaksen C, Depienne C. Spastic paraplegia 4. In: Pagon RA, Adam MP, Ardinger HH, Bird TD, Dolan CR, et al. , editors. GeneReviews[Internet] Seattle (WA): University of Washington, Seattle. 1993-2014. 2003 Apr 17 [updated 2012 Aug 16].
22. Eckert T, Link S, Le DT, Sobczak JP, Gieseke A, Richter K, et al. Subunit Interactions and cooperativity in the microtubule-severing AAA ATPase spastin. J Biol Chem 2012; 287: 26278-90.
23. Erichsen AK, Inderhaug E, Mattingsdal M, Eiklid K, Tallaksen CM. Seven novel mutations and four exon deletions in a collection of Norwegian patients with SPG4 hereditary spastic paraplegia. Eur J Neurol 2007; 14: 809-14.
24. Errico A, Ballabio A, Rugarli EI. Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 2002; 11: 153-63.
25. Errico A, Claudiani P, D'Addio M, Rugarli EI. Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Hum Mol Genet 2004; 13: 2121-32.
26. Evans KJ, Gomes ER, Reisenweber SM, Gundersen GG, Lauring BP. Linking axonal degeneration to microtubule remodeling by Spastinmediated microtubule severing. J Cell Biol 2005; 168: 599-606.
27. Evans K, Keller C, Pavur K, Glasgow K, Conn B, Lauring B. Interaction of two hereditary spastic paraplegia gene products, spastin and atlastin, suggests a common pathway for axonal maintenance. Proc Natl Acad Sci USA 2006; 103: 10666-71.
28. Fassier C, Tarrade A, Peris L, Courageot S, Mailly P, Dalard C, et al. Microtubule-targeting drugs rescue axonal swellings in cortical neurons from spastin knock-out mice. Dis Model Mech 2013; 6: 72-83.
29. Fink JK. Hereditary spastic paraplegia: clinico-pathologic features and emerging molecular mechanisms [Review]. Acta Neuropathol 2013; 126: 307-28.
30. Fonknechten N, Mavel D, Byrne P, Davoine CS, Cruaud C, Bonsch D, et al. Spectrum of SPG4 mutations in autosomal dominant spastic paraplegia. Hum Mol Genet 2000; 9: 637-44.
31. Friedman JR, Webster BM, Mastronarde DN, Verhey KJ, Voeltz GK. ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J Cell Biol 2010; 190: 363-75.
32. Goyal U, Renvoisé B, Chang J, Blackstone C. Spastin-interacting protein NA14/SSNA1 functions in cytokinesis and axon development. PLoS One 2014; 9: e112428.
33. Guizetti J, Schermelleh L, Mäntler J, Maar S, Poser I, Leonhardt H, et al. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 2011; 331: 1616-20.
34. Havlicek S, Kohl Z, Mishra HK, Prots I, Eberhardt E, Denguir N, et al. Gene dosage-dependent rescue of HSP neurite defects in SPG4 patients' neurons. Hum Mol Genet 2014; 23: 2527-41.
35. Hazan J, Fonknechten N, Mavel D, Paternotte C, Samson D, Artiguenave F, et al. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat Gene 1999; 23: 296-303.
36. Hu J1, Shibata Y, Zhu PP, Voss C, Rismanchi N, Prinz WA, et al. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 2009; 138: 549-61.
37. Jonsson PA, Ernhill K, Andersen PM, Bergemalm D, Brännström T, Gredal O, et al. Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 2004; 127: 73-88.
38. Kasher PR, De Vos KJ, Wharton SB, Manser C, Bennett EJ, Bingley M, et al. 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 2009; 110: 34-44.
39. Kozak M. Pushing the limits of the scanning mechanism for initiation of translation [Review]. Gene 2002; 299: 1-34.
40. Lacroix B, van Dijk J, Gold ND, Guizetti J, Aldrian-Herrada G, Rogowski K, et al. Tubulin polyglutamylation stimulates spastinmediated microtubule severing. J Cell Biol 2010; 189: 945-54.
41. Lindsey JC, Lusher ME, McDermott CJ, White KD, Reid E, Rubinsztein DC, et al. Mutation analysis of the spastin gene (SPG4) in patients with hereditary spastic paraparesis. J Med Genet 2000; 37: 759-65.
42. Lo Giudice T, Lombardi F, Santorelli FM, Kawarai T, Orlacchio A. Hereditary spastic paraplegia: clinical-genetic characteristics and evolving molecular mechanisms. [Review] Exp Neurol 2014; 261: 518-39.
43. Lumb JH, Connell JW, Allison R, Reid E. The AAA ATPase spastin links microtubule severing to membrane modelling [Review]. Biochim Biophys Acta 2012; 1823: 192-7.
44. Mancuso G, Rugarli EI. A cryptic promoter in the first exon of the SPG4 gene directs the synthesis of the 60-kDa spastin isoform. BMC Biol 2008; 6: 31.
45. Mannan AU, Boehm J, Sauter SM, Rauber A, Byrne PC, Neesen J, et al. Spastin, the most commonly mutated protein in hereditary spastic paraplegia interacts with Reticulon 1 an endoplasmic reticulum protein. Neurogenetics 2006; 7: 93-103.
46. Matsuda D, Sato H, Maquat LE. Studying nonsense-mediated mRNA decay in mammalian cells. Methods Enzymol 2008; 449: 177-201.
47. McDermott CJ, Burness CE, Kirby J, Cox LE, Rao DG, Hewamadduma C, et al. Clinical features of hereditary spastic paraplegia due to spastin mutation. Neurology 2006; 67: 45-51.
48. Erratum in: Neurology 2009; 72: 1534.
49. McDermott CJ, Grierson AJ, Wood JD, Bingley M, Wharton SB, Bushby KM, et al. Hereditary spastic paraparesis: disrupted intracellular transport associated with spastin mutation. Ann Neurol 2003; 54: 748-59.
50. Meijer IA, Hand CK, Cossette P, Figlewicz DA, Rouleau GA. Spectrum of SPG4 mutations in a large collection of North American families with hereditary spastic paraplegia. Arch Neurol 2002; 59: 281-6.
51. Morfini GA, Burns M, Binder LI, Kanaan NM, LaPointe N, Bosco DA, et al. Axonal transport defects in neurodegenerative diseases. J Neurosci 2009; 29: 12776-86.
52. Nielsen JE, Johnsen B, Koefoed P, Scheuer KH, Grønbech-Jensen M, Law I, et al. Hereditary spastic paraplegia with cerebellar ataxia: A complex phenotype associated with a new SPG4 gene mutation. Eur J Neurol 2004; 11: 817-24.
53. Novarino G, Fenstermaker AG, Zaki MS, Hofree M, Silhavy JL, Heiberg AD, et al. Exome sequencing links corticospinal motor neuron disease to common neurodegenerative disorders. Science 2014; 343: 506-11.
54. Orlacchio A, Kawarai T, Totaro A, Errico A, St George-Hyslop PH, Rugarli EI, et al. Hereditary spastic paraplegia: clinical genetic study of 15 families. Arch Neurol 2004; 61: 849-55.
55. Orso G, Martinuzzi A, Rossetto MG, Sartori E, Feany M. Daga A. Disease-related phenotypes in a Drosophila model of hereditary spastic paraplegia are ameliorated by treatment with vinblastine. J Clin Invest 2005; 11: 3026-34.
56. Park SH, Zhu PP, Parker RL, Blackstone C. Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J Clin Invest 2010; 120: 1097-110.
57. Patrono C, Scarano V, Cricchi F, Melone MA, Chiriaco M, Napolitano A, et al. Autosomal dominant hereditary spastic paraplegia: DHPLC-based mutation analysis of SPG4 reveals eleven novel mutations. Hum Mutat 2005; 25: 506.
58. Qiang L, Yu W, Liu M, Solowska JM, Baas PW. Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules. Mol Biol Cell 2010; 21: 334-44.
59. Rebbapragada I, Lykke-Andersen J. Execution of nonsense-mediated mRNA decay: what defines a substrate? [Review]. Curr Opin Cell Biol 2009; 21: 394-402.
60. Reid E, Connell J, Edwards TL, Duley S, Brown SE, Sanderson CM. The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum Mol Genet 2005; 14: 19-38.
61. Riano E, Martignoni M, Mancuso, G, Cartelli D, Crippa F, Toldo I, et al. Pleiotropic effects of spastin on neurite growth, depending on expression levels. J Neurochem 2009; 108: 1277-88.
62. Roll-Mecak A, Vale RD. The Drosophila homologue of the hereditary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr Biol 2005; 15: 650-5.
63. Roll-Mecak A, Vale RD. Making more microtubules by severing: A common theme of noncentrosomal microtubule arrays? J Cell Biol 2006; 175: 849-51.
64. Roll-Mecak A, Vale RD. Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature 2008; 451: 363-67.
65. Ruano L, Melo C, Silva MC, Coutinho P. The global epidemiology of hereditary ataxia and spastic paraplegia: A systematic review of prevalence studies. Neuroepidemiology 2014; 42: 174-83.
66. Salinas S, Proukakis C, Crosby A, Warner TT. Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. [Review] Lancet Neurol 2008; 7: 1127-38.
67. Sanderson CM, Connell JW, Edwards TL, Bright NA, Duley S, Thompson A, et al. Spastin and atlastin, two proteins mutated in autosomal-dominant hereditary spastic paraplegia, are binding partners. Hum Mol Genet 2006; 15: 307-18.
68. Sauter S, Miterski B, Klimpe S, Bönsch D, Schöls L, Visbeck A, et al. Mutation analysis of the spastin gene (SPG4) in patients in Germany with autosomal dominant hereditary spastic paraplegia. Hum Mutat 2002; 20: 127-32.
69. Schickel J, Pamminger T, Ehrsam A, Münch S, Huang X, Klopstock T, et al. Isoform-specific increase of spastin stability by N-terminal missense variants including intragenic modifiers of SPG4 hereditary spastic paraplegia. Eur J Neurol 2007; 14: 1322-8.
70. Schweingruber C1, Rufener SC, Zünd D, Yamashita A, Mühlemann O. Nonsense-mediated mRNA decay-mechanisms of substrate mRNA recognition and degradation in mammalian cells [Review]. Biochim Biophys Acta 2013; 1829: 612-23
71. Sherwood NT, Sun Q, Xue M, Zhang B, Zinn K. Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biology 2004; 2: e429.
72. Shoukier M, Neesen J, Sauter SM, Argyriou L, Doerwald N, Pantakani DV, et al. Expansion of mutation spectrum, determination of mutation cluster regions and predictive structural classification of SPAST mutations in hereditary spastic paraplegia. Eur J Hum Genet 2009; 17: 187-94.
73. Smith JL, Xiong S, Markesbery WR, Lovell MA. Altered expression of zinc transporters-4 and-6 in mild cognitive impairment, early and late Alzheimer's disease brain. Neuroscience 2006; 140: 879-88.
74. Solowska J, Garbern J, Baas PW. Evaluation of loss-of-function as an explanation for SPG4-based hereditary spastic paraplegia. Human Molec Genetics 2010; 19: 2767-79.
75. Solowska JM, D'Rozario M, Jean DC, Davidson MW, Marenda DR, Baas PW. Pathogenic Mutation of Spastin Has Gain-of-Function Effects on Microtubule Dynamics. J Neurosci 2014; 34: 1856-67.
76. Solowska JM, Morfini G, Falnikar A, Himes BT, Brady ST, Huang D, et al. Quantitative and functional analyses of spastin in the nervous system: implications for hereditary spastic paraplegia. J Neurosci 2008; 28: 2147-57.
77. Stone MC, Rao K, Gheres KW, Kim S, Tao J, La Rochelle C, et al. Normal spastin gene dosage is specifically required for axon regeneration. Cell Rep 2012; 2: 1340-50.
78. Svenson IK, Ashley-Koch AE, Gaskell PC, Riney TJ, Cumming WJ, Kingston HM, et al. Identification and expression analysis of spastin gene mutations in hereditary spastic paraplegia. Am J Hum Genet 2001; 68: 1077-85.
79. Svenson IK, Kloos MT, Gaskell PC, Nance MA, Garbern JY, Hisanaga S, et al. Intragenic modifiers of hereditary spastic paraplegia due to spastin gene mutations. Neurogenetics 2004; 5: 157-64.
80. Tarrade A, Fassier C, Courageot S, Charvin D, Vitte J, Peris L, et al. 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 2006; 15: 3544-58.
81. Thomsen B, Nissen PH, Agerholm JS, Bendixen C. Congenital bovine spinal dysmyelination is caused by a missense mutation in the SPAST gene. Neurogenetics 2010; 11: 175-83.
82. Trotta N, Orso G, Rossetto MG, Daga A, Broadie K. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr Biol 2004; 14: 1135-47.
83. Tsang HT, Edwards TL, Wang X, Connell JW, Davies RJ, Durrington HJ, et al. The hereditary spastic paraplegia proteins NIPA1, spastin and spartin are inhibitors of mammalian bone morphogenic protein signalling. Hum Mol Genet 2009; 18: 3805-21.
84. Wang L, Brown A. Rapid movement of microtubules in axons. Curr Biol 2002; 12: 1496-501.
85. Watanabe Y, Yasui K, Nakano T, Doi K, Fukada Y, Kitayama M, et al. Mouse motor neuron disease caused by truncated SOD1 with or without C-terminal modification. Brain Res Mol Brain Res 2005; 135: 12-20.
86. Wharton SB, McDermott CJ, Grierson AJ, Wood JD, Gelsthorpe C, Ince PG, et al. The cellular and molecular pathology of the motor system in hereditary spastic paraparesis due to mutation of the spastin gene. J Neuropathol Exp Neurol 2003; 62: 1166-77.
87. White SR, Evans KJ, Lary J, Cole JL, Lauring B. Recognition of C-terminal amino acids in tubulin by pore loops in Spastin is important for microtubule severing. J Cell Biol 2007; 176: 995-1005.
88. Wood JD, Landers JA, Bingley M, McDermott CJ, Thomas-McArthur V, Gleadall LJ, et al. The microtubule-severing protein Spastin is essential for axon outgrowth in the zebrafish embryo. Hum Mol Genet 2006; 15: 2763-71.
89. Yang D, Rismanchi N, Renvoisé B, Lippincott-Schwartz J, Blackstone C, Hurley JH. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 2008; 15: 1278-86.
90. Yang H, Ganguly A, Cabral F. Inhibition of cell migration and cell division correlates with distinct effects of microtubule inhibiting drugs. J Biol Chem 2010; 285: 32242-50.
91. Yip AG, Durr A, Marchuk DA, Ashley-Koch A, Hentati A, Rubinsztein DC, et al. Meta-analysis of age at onset in spastin-associted hereditary spastic paraplegia provides no evidence for a correlation with mutational class. J Med Genet 2003; 40: e106.
92. Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, Baas, PW. The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 2008; 19: 1081-98.
93. Zhao X, Alvarado D, Rainier S, Lemons R, Hedera P, Weber CH, et al. Mutations in a newly identified GTPase gene cause autosomal dominant hereditary spastic paraplegia. Nat Genet 2001; 29: 326-31.
94. Zhu PP, Denton KR, Pierson TM, Li XJ, Blackstone C. Pharmacologic rescue of axon growth defects in a human iPSC model of hereditary spastic paraplegia. Hum Mol Genet 2014; 23: 5638-48.