N88S seipin mutant transgenic mice develop features of seipinopathy/BSCL2-related motor neuron disease via endoplasmic reticulum stress

Human Molecular Genetics

Volumn 20, Issue 19, 2011, Pages 3831-3840

  Yagi, Takuya ^a   Ito, Daisuke ^a   Nihei, Yoshihiro ^a   Ishihara, Tadayuki ^b   Suzuki, Norihiro ^a  

^a KEIO UNIVERSITY   (Japan)

^b Hakone National Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; GLUCOSE REGULATED PROTEIN 78; MUTANT PROTEIN; PROTEIN DISULFIDE ISOMERASE; SEIPIN PROTEIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL LOSS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; GLIOSIS; HEREDITARY MOTOR SENSORY NEUROPATHY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MOLECULAR PATHOLOGY; MOTOR NEUROPATHY; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIPINOPATHY; SPASTICITY; SPINAL CORD; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; GTP-BINDING PROTEIN GAMMA SUBUNITS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR NEURON DISEASE; MUTATION, MISSENSE; SPINAL CORD;

MURINAE; MUS; MUS MUSCULUS;

EID: 80052726190     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr304     Document Type: Article

References (35)

1. Magre, J.,Delepine, M.,Khallouf, E., Gedde-Dahl, T., Jr,Van Maldergem, L., Sobel, E., Papp, J., Meier, M., Megarbane, A., Bachy, A. et al. (2001) Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat Genet., 28, 365-370.
2. Cui, X., Wang, Y., Tang, Y., Liu, Y., Zhao, L., Deng, J., Xu, G., Peng, X., Ju, S., Liu, G. and Yang, H. (2011) Seipin ablation in mice results in severe generalized lipodystrophy. Hum. Mol. Genet. [Epub ahead of print].
3. Windpassinger, C., Auer-Grumbach, M., Irobi, J., Patel, H., Petek, E., Hörl, G., Malli, R., Reed, J.A., Dierick, I., Verpoorten, N. et al. (2004) Heterozygous missense mutations in BSCL2 are associated with distal hereditary motor neuropathy and Silver syndrome. Nat. Genet., 36, 271-276.
4. Auer-Grumbach, M., Schlotter-Weigel, B., Lochmüller, H., Strobl-Wildemann, G., Auer-Grumbach, P., Fischer, R., Offenbacher, H., Zwick, E.B., Robl, T., Hartl, G. et al. (2005) Phenotypes of the N88S Berardinelli-Seip congenital lipodystrophy 2 mutation. Ann. Neurol., 57, 415-424.
5. Irobi, J., Van den Bergh, P., Merlini, L., Verellen, C., Van Maldergem, L., Dierick, I., Verpoorten, N., Jordanova, A., Windpassinger, C., De Vriendt, E. et al. (2004) The phenotype of motor neuropathies associated with BSCL2 mutations is broader than Silver syndrome and distal HMN type V. Brain, 127, 2124-2130.
6. Ito, D. and Suzuki, N. (2009) Seipinopathy: a novel endoplasmic reticulum stress-associated disease. Brain, 132, 8-15.
7. Ito, D., Fujisawa, T., Iida, H. and Suzuki, N. (2008) Characterization of seipin/BSCL2, a protein associated with spastic paraplegia 17. Neurobiol. Dis., 31, 266-277.
8. Ito, D. and Suzuki, N. (2007) Molecular pathogenesis of seipin/ BSCL2-related motor neuron diseases. Ann. Neurol., 61, 237-250.
9. Zhao, L. and Ackerman, S.L. (2006) Endoplasmic reticulum stress in health and disease. Curr. Opin. Cell Biol., 18, 444-452.
10. Vidal, M., Morris, R., Grosveld, F. and Spanopoulou, E. (1990) Tissue-specific control elements of the Thy-1 gene. EMBO J., 9, 833-840.
11. Moechars, D., Dewachter, I., Lorent, K., Reversé, D., Baekelandt, V., Naidu, A., Tesseur, I., Spittaels, K., Haute, C.V., Checler, F. et al. (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem., 274, 6483-6492.
12. Wils, H., Kleinberger, G., Janssens, J., Pereson, S., Joris, G., Cuijt, I., Smits, V., Ceuterick-de Groote, C., Van Broeckhoven, C. and Kumar-Singh, S. (2010) TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc. Natl Acad. Sci. USA, 107, 3858-3863.
13. Igaz, L.M., Kwong, L.K., Lee, E.B., Chen-Plotkin, A., Swanson, E., Unger, T., Malunda, J., Xu, Y., Winton, M.J., Trojanowski, J.Q. et al. (2011) Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest., 121, 726-738.
14. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E. et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature, 441, 880-884.
15. Cemal, C.K., Carroll, C.J., Lawrence, L., Lowrie, M.B., Ruddle, P., Al-Mahdawi, S., King, R.H., Pook, M.A., Huxley, C. and Chamberlain, S. (2002) YAC transgenic mice carrying pathological alleles of the MJD1 locus exhibit a mild and slowly progressive cerebellar deficit. Hum. Mol. Genet., 11, 1075-1094.
16. Tsai, K.J., Yang, C.H., Fang, Y.H., Cho, K.H., Chien, W.L., Wang, W.T., Wu, T.W., Lin, C.P., Fu, W.M. and Shen, C.K. (2010) Elevated expression of TDP-43 in the forebrain of mice is sufficient to cause neurological and pathological phenotypes mimicking FTLD-U. J. Exp. Med., 207, 1661-1673.
17. Stallings, N.R., Puttaparthi, K., Luther, C.M., Burns, D.K. and Elliott, J.L. (2010) Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol. Dis., 40, 404-414.
18. Xu, Y.F., Gendron, T.F., Zhang, Y.J., Lin, W.L., D'Alton, S., Sheng, H., Casey, M.C., Tong, J., Knight, J., Yu, X. et al. (2010) Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J. Neurosci., 30, 10851-10859.
19. Feeney, S.J., McKelvie, P.A., Austin, L., Jean-Francois, M.J., Kapsa, R., Tombs, S.M. and Byrne, E. (2001) Presymptomatic motor neuron loss and reactive astrocytosis in the SOD1 mouse model of amyotrophic lateral sclerosis. Muscle Nerve, 24, 1510-1519.
20. Katayama, T., Imaizumi, K., Manabe, T., Hitomi, J., Kudo, T. and Tohyama, M. (2004) Induction of neuronal death by ER stress in Alzheimer's disease. J. Chem. Neuroanat., 28, 67-78.
21. Paschen, W. and Mengesdorf, T. (2005) Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium, 38, 409-415.
22. Marciniak, S.J. and Ron, D. (2006) Endoplasmic reticulum stress signaling in disease. Physiol. Rev., 86, 1133-1149.
23. Ilieva, E.V., Ayala, V., Jové, M., Dalfó, E., Cacabelos, D., Povedano, M., Bellmunt, M.J., Ferrer, I., Pamplona, R. and Portero-Otín, M. (2007) Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain, 130, 3111-3123.
24. Ito, D., Walker, J.R., Thompson, C.S., Moroz, I., Lin, W., Veselits, M.L., Hakim, A.M., Fienberg, A.A. and Thinakaran, G. (2004) Characterization of stanniocalcin 2, a novel target of the mammalian unfolded protein response with cytoprotective properties. Mol. Cell Biol., 24, 9456-9469.
25. Kaufman, R.J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev., 13, 1211-1233.
26. Liu, C.Y. and Kaufman, R.J. (2003) The unfolded protein response. J. Cell Sci., 116, 1861-1862.
27. Rao, R.V., Peel, A., Logvinova, A., del Rio, G., Hermel, E., Yokota, T., Goldsmith, P.C., Ellerby, L.M., Ellerby, H.M. and Bredesen, D.E. (2002) Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett., 514, 122-128.
28. Reddy, R.K., Mao, C., Baumeister, P., Austin, R.C., Kaufman, R.J. and Lee, A.S. (2003) Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem., 278, 20915-20924.
29. De Vos, K.J., Grierson, A.J., Ackerley, S. and Miller, C.C. (2008) Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci., 31, 151-173.
30. Bilsland, L.G., Sahai, E., Kelly, G., Golding, M., Greensmith, L. and Schiavoa, G. (2010) Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl Acad. Sci. USA, 107, 20523-20528.
31. Shan, X., Chiang, P.M., Price, D.L. and Wong, P.C. (2010) Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc. Natl Acad. Sci. USA, 107, 16325-16330.
32. Wegorzewska, I., Bell, S., Cairns, N.J., Miller, T.M. and Baloh, R.H. (2009) TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl Acad. Sci. USA, 106, 18809-18814.
33. Harding, H.P. and Ron, D. (2002) Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes, 51 (Suppl. 3), S455-S461.
34. Ito, D., Tanaka, K., Suzuki, S., Dembo, T. and Fukuuchi, Y. (2001) Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke, 32, 1208-1215.
35. Ito, D., Tanaka, K., Suzuki, S., Dembo, T., Kosakai, A. and Fukuuchi, Y. (2001) Up-regulation of the Ire1-mediated signaling molecule, Bip, in ischemic rat brain. Neuroreport, 12, 4023-4028.