Pharmacologic rescue of axon growth defects in a human iPSC model of hereditary spastic paraplegia SPG3A

Human Molecular Genetics

Volumn 23, Issue 21, 2014, Pages 5638-5648

  Zhu, Peng Peng ^a   Denton, Kyle R ^b   Pierson, Tyler Mark ^c   Li, Xue Jun ^a,b   Blackstone, Craig ^a  

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

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATLASTIN 1 PROTEIN; F ACTIN; GUANOSINE TRIPHOSPHATASE; PROTEIN SPG3A; UNCLASSIFIED DRUG; ATL1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; TUBULIN MODULATOR;

ARTICLE; BRAIN CELL; CASE REPORT; CELL MOTILITY; CHILD; CYTOSKELETON; ENDOPLASMIC RETICULUM; FEMALE; FOREBRAIN; HAIR GROWTH; HEREDITARY MOTOR SENSORY NEUROPATHY; HETEROLOGOUS EXPRESSION; HINGE REGION; HUMAN; LOSS OF FUNCTION MUTATION; MICROTUBULE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; PLURIPOTENT STEM CELL; PRESCHOOL CHILD; PROTEIN ASSEMBLY; PROTEIN DOMAIN; ROOT HAIR; SKIN FIBROBLAST; AMINO ACID SEQUENCE; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; HETEROZYGOTE; METABOLISM; MOLECULAR GENETICS; MUTATION; NERVE CELL; NERVE FIBER; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROTEIN CONFORMATION; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

ARABIDOPSIS; EUKARYOTA; RATTUS;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CELL DIFFERENTIATION; CELL LINE; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; FEMALE; GTP-BINDING PROTEINS; HETEROZYGOTE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEURONS; PROTEIN CONFORMATION; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SPASTIC PARAPLEGIA, HEREDITARY; TUBULIN MODULATORS;

EID: 84911366123     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu280     Document Type: Article

References (57)

1. Blackstone, C. (2012) Cellular pathways of hereditary spastic paraplegia. Annu. Rev. Neurosci., 35, 25-47.
2. Finsterer, J., Löscher, W., Quasthoff, S., Wanschitz, J., Auer-Grumbach, M. and Stevanin, G. (2012) Hereditary spastic paraplegias with autosomal dominant, recessive, X-linked, or maternal trait of inheritance. J. Neurol. Sci., 318, 1-18.
3. Schüle, R. and Schö ls, L. (2011) Genetics of hereditary spastic paraplegias. Semin. Neurol., 31, 484-493.
4. Novarino, G., Fenstermaker, A.G., Zaki, M.S., Hofree, M., Silhavy, J.L., Heiberg, A.D., Abdellateef, M., Rosti, B., Scott, E., Mansour, L. et al. (2014) Exome sequencing links corticospinal motor neuron disease to common neurodegenerative disorders. Science, 343, 506-511.
5. Blackstone, C., O'Kane, C.J. and Reid, E. (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat. Rev. Neurosci., 12, 31-42.
6. Park, S.H. and Blackstone, C. (2010) Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep., 11, 515-521.
7. Zhu, P.-P., Patterson, A., Lavoie, B., Stadler, J., Shoeb, M., Patel, R. and Blackstone, C. (2003) Cellular localization, oligomerization, and membrane association of the hereditary spastic paraplegia3A (SPG3A) protein atlastin. J. Biol. Chem., 278, 49063-49071.
8. Rismanchi, N., Soderblom, C., Stadler, J., Zhu, P.-P. and Blackstone, C. (2008) Atlastin GTPases are required for Golgi apparatus and ER morphogenesis. Hum. Mol. Genet., 17, 1591-1604.
9. Hu, J., Shibata, Y., Zhu, P.-P., Voss, C., Rismanchi, N., Prinz, W.A., Rapoport, T.A. and Blackstone, C. (2009) A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell, 138, 549-561.
10. Orso, G., Pendin, D., Liu, S., Tosetto, J., Moss, T.J., Faust, J.E., Micaroni, M., Egorova, A., Martinuzzi, A., McNew, J.A. and Daga, A. (2009) Homotypic fusion ofERmembranes requires the dynamin-like GTPase atlastin. Nature, 460, 978-983.
11. Anwar, K.,Klemm,R.W., Condon, A., Severin, K.N., Zhang, M., Ghirlando, R., Hu, J., Rapoport, T.A. and Prinz, W.A. (2012) The dynamin-like GTPase Sey1p mediates homotypic ER fusion in S. cerevisiae. J. Cell Biol., 197, 209-217.
12. Chen, J., Stefano, G., Brandizzi, F. and Zheng, H. (2011) ArabidopsisRHD3 mediates the generation of the tubular ER network and is required for Golgi distribution and motility in plant cells. J Cell Sci., 124, 2241-2252.
13. Zhang, M., Wu, F., Shi, J., Zhu, Y., Zhu, Z., Gong, Q. and Hu, J. (2013) ROOT HAIR DEFECTIVE3 family of dynamin-like GTPases mediates homotypic endoplasmic reticulum fusion and is essential for Arabidopsis development. Plant Physiol., 163, 713-720.
14. Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M. and Rapoport, T.A. (2006) A class of membrane proteins shaping the endoplasmic reticulum. Cell, 124, 573-586.
15. Hu, J., Shibata, Y., Voss, C., Shemesh, T., Li, Z., Coughlin, M., Kozlov, M.M., Rapoport, T.A. and Prinz, W.A. (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science, 319, 1247-1250.
16. Park, S.H., Zhu, P.-P., Parker, R.L. and 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.
17. Zhu, P.-P., Soderblom, C., Tao-Cheng, J.-H., Stadler, J. and 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.
18. Lee, M., Paik, S.K., Lee, M.-J., Kim, Y.-J., Kim, S., Nahm, M., Oh, S.-J., Kim, H.-M., Yim, J., Lee, C.J. et al. (2009) Drosophila Atlastin regulates the stability of muscle microtubules and is required for synapse development. Dev. Biol., 330, 250-262.
19. Fassier, C., Hutt, J.A., Scholpp, S., Lumsden, A., Giros, B., Nothias, F., Schneider-Maunoury, S., Houart, C. and Hazan, J. (2010) Zebrafish atlastin controls motility and spinal motor axon architecture via inhibition of the BMP pathway. Nat. Neurosci., 13, 1380-1387.
20. Byrnes, L.J. and Sondermann, H. (2011) Structural basis for the nucleotide-dependent dimerization of the largeGprotein atlastin-1/SPG3A. Proc. Natl. Acad. Sci. USA, 108, 2216-2221.
21. de Bot, S.T., Veldink, J.H., Vermeer, S., Mensenkamp, A.R., Brugman, F., Scheffer, H., van den Berg, L.H., Kremer, H.P.H., Kamsteeg, E.J. and van de Warrenburg, B.P. (2013) ATL1 and REEP1 mutations in hereditary and sporadic upper motor neuron syndromes. J. Neurol., 260, 869-875.
22. Fischer, D., Schabhüttl, M., Wieland, T., Windhager, R., Strom, T.M. and Auer-Grumbach, M. (2014) A novel missense mutation confirms ATL3 as a gene for hereditary sensory neuropathy type 1. Brain, in press. doi:10.1093/ brain/awu091.
23. Byrnes, L.J., Singh, A., Szeto, K., Benvin, N.M., O'Donnell, J.P., Zipfel, W.R. and Sondermann, H. (2013) Structural basis for conformational switching and GTP loading of the large G protein atlastin. EMBO J., 32, 369-384.
24. Okita, K., Matsumura, Y., Sato, Y., Okada, A., Morizane, A., Okamoto, S., Hong, H., Nakagawa, M., Tanabe, K., Tezuka, K. et al. (2011) A more efficient method to generate integration-free human iPS cells. Nat. Methods, 8, 409-412.
25. Li, X.-J., Zhang, X., Johnson, M.A., Wang, Z.-B., LaVaute, T. and Zhang, S.-C. (2009) Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development, 136, 4055-4063.
26. Zeng, H., Guo, M., Martins-Taylor, K., Wang, X., Zhang, Z., Park, J.W., Zhan, S., Kronenberg, M.S., Lichtler, A., Liu, H.-X. et al. (2010) Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS One, 5, e11853.
27. Boisvert, E.M., Denton, K., Lei, L. and Li, X.-J. (2013) The specification of telencephalic glutamatergic neurons from human pluripotent stem cells. J. Vis. Exp., 74, e50321.
28. Evans, K., Keller, C., Pavur, K., Glasgow, K., Conn, B. and Lauring, B. (2006) Interaction of two hereditary spastic paraplegia gene products, spastin and atlastin, suggests a common pathway for axonal maintenance. Proc. Natl. Acad. Sci. USA, 103, 10666-10671.
29. Sanderson, C.M., Connell, J.W., Edwards, T.L., Bright, N.A., Duley, S., Thompson, A., Luzio, J.P. and Reid, E. (2006) Spastin and atlastin, two proteins mutated in autosomal-dominant hereditary spastic paraplegia, are binding partners. Hum. Mol. Genet., 15, 307-318.
30. Hazan, J., Fonknechten, N., Mavel, D., Paternotte, C., Samson, D., Artiguenave, F., Davoine, C.-S., Cruaud, C., Dürr, A., Wincker, P. 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.
31. Tarrade, A., Fassier, C., Courageot, S., Charvin, D., Vitte, J., Peris, L., Thorel, A., Mouisel, E., Fonknechten, N., Roblot, N. et al. (2006)Amutation 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.
32. Ebbing, B., Mann, K., Starosta, A., Jaud, J., Schö ls, L., Schüle, R. and Woehlke, G. (2008) Effect of spastic paraplegia mutations in KIF5A kinesin on transport activity. Hum. Mol. Genet., 17, 1245-1252.
33. Solowska, J.M., Morfini, G., Falnikar, A., Himes, B.T., Brady, S.T., Huang, D. and Baas, P.W. (2008) Quantitative and functional analyses of spastin in the nervous system: implications for hereditary spastic paraplegia. J. Neurosci., 28, 2147-2157.
34. Kasher, P.R., De Vos, K.J., Wharton, S.B., Manser, C., Bennett, E.J., Bingley, M., Wood, J.D., Milner, R., McDermott, C.J., Miller, C.C. 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.
35. Denton, K.R., Lei, L., Grenier, J., Rodionov, V., Blackstone, C. and Li, X.-J. (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.
36. De Vos, K.J., Chapman, A.L., Tennant, M.E., Manser, C., Tudor, E.L., Lau, K.-F., Brownlees, J., Ackerley, S., Shaw, P.J., McLoughlin, D.M. et al. (2007) Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet., 16, 2720-2728.
37. Fassier, C., Tarrade, A., Peris, L., Courageot, S., Mailly, P., Dalard, C., Delga, S., Roblot, N., Lefe'vre, J., Job, D. et al. (2013) Microtubule-targeting drugs rescue axonal swellings in cortical neurons from spastin knockout mice. Dis. Model Mech., 6, 72-83.
38. Meijer, I.A., Dion, P., Laurent, S., Dupré, N., Brais, B., Levert, A., Puymirat, J., Rioux, M.F., Sylvain, M., Zhu, P.-P. et al. (2007) Characterization of a novel SPG3A deletion in a French-Canadian family. Ann. Neurol., 61, 599-603.
39. Khan, T.N., Klar, J., Tariq, M., Baig, S.A., Malik, N.A., Yousaf, R., Baig, S.M. and Dahl, N. (2014) Evidence for autosomal recessive inheritance in SPG3A caused by homozygosity for a novel ATL1 missense mutation. Eur. J. Hum. Genet., In press.
40. Wang, H., Lockwood, S.K., Hoeltzel, M.F. and Schiefelbein, J.W. (1997) The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Genes Dev., 11, 799-811.
41. Zheng, H. and Chen, J. (2011) Emerging aspects of ER organization in root hair tip growth: lessons from RHD3 and Atlastin. Plant Signal. Behav., 6, 1710-1713.
42. English, A.R. and Voeltz, G.K. (2013) Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol., 5, a013227.
43. Morfini, G.A., Burns, M., Binder, L.I., Kanaan, N.M., LaPointe, N., Bosco, D.A., Brown, R.H. Jr, Brown, H., Tiwari, A., Hayward, L. et al. (2009) Axonal transport defects in neurodegenerative diseases. J. Neurosci., 29, 12776-12786.
44. Hirokawa, N., Niwa, S. and Tanaka, Y. (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron, 68, 610-638.
45. Mattson, M.P. and Partin, J. (1999) Evidence for mitochondrial control of neuronal polarity. J. Neurosci. Res., 56, 8-20.
46. Sun, T., Qiao, H., Pan, P.-Y., Chen, Y. and Sheng, Z.-H. (2013) Mobile axonal mitochondria contribute to the variability of presynaptic strength. Cell Rep., 4, 413-419.
47. Ruthel, G. and Hollenbeck, P.J. (2003) Response of mitochondrial traffic to axon determination and differential branch growth. J. Neurosci., 23, 8618-8624.
48. Zhu, Y.-B. and Sheng, Z.-H. (2011) Increased axonal mobility does not slow ALS-like disease in mutant SOD1 mice. J. Biol. Chem., 286, 23432-23440.
49. Abrahamsen, G., Fan, Y., Matigian, N., Wali, G., Bellette, B., Sutharsan, R., Raju, J., Wood, S.A., Veivers, D., Sue, C.M. and Mackay-Sim, A. (2013) A patient-derived stem cell model of hereditary spastic paraplegia with SPAST mutations. Dis. Model. Mech., 6, 489-502.
50. Soderblom, C. and Blackstone, C. (2006) Traffic accidents: molecular genetic insights into the pathogenesis of the hereditary spastic paraplegias. Pharmacol. Ther., 109, 42-56.
51. Fink, J.K. (2003) Advances in the hereditary spastic paraplegias. Exp. Neurol., 184 (Suppl. 1), S106-S110.
52. Klemm,R.W., Norton, J.P., Cole, R.A., Li, C.S., Park, S.H., Crane, M.M.,Li, L., Jin, D., Boye-Doe, A., Liu, T.Y. et al. (2013)Aconserved role for atlastin GTPases in regulating lipid droplet size. Cell Rep., 3, 1465-1475.
53. Zhao, J. and Hedera, P. (2013) Hereditary spastic paraplegia-causing mutations in atlastin-1 interfere with BMPRII trafficking. Mol. Cell. Neurosci., 52, 87-96.
54. Guelly, C., Zhu, P.-P., Leonardis, L., Papić, L., Zidar, J., Schabhüttl, M., Strohmaier, H., Weis, J., Strom, T.M., Baets, J. et al. (2011) Targeted high-throughput sequencing identifies mutations in atlastin-1 as a cause of hereditary sensory neuropathy type I. Am. J. Hum. Genet., 88, 99-105.
55. Wang, Z.-B., Zhang, X. and Li, X.-J. (2013) Recapitulation of spinal motor neuron-specific disease phenotypes in a humancell model of spinal muscular atrophy. Cell Res., 23, 378-393.
56. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
57. De Vos, K.J. and Sheetz, M.P. (2007) Visualization and quantification of mitochondrial dynamics in living animal cells. Methods Cell Biol., 80, 627-682.