Altered quality control in the endoplasmic reticulum causes cortical dysplasia in knock-in mice expressing a mutant BiP

Molecular and Cellular Biology

Volumn 28, Issue 1, 2008, Pages 293-301

  Mimura, Naoya ^a   Yuasa, Shigeki ^b   Soma, Miho ^b   Jin, Hisayo ^a   Kimura, Keita ^a   Goto, Shigemasa ^a   Koseki, Haruhiko ^c   Aoe, Tomohiko ^a  

^a CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING IMMUNOGLOBULIN PROTEIN; PROTEIN DERIVATIVE; REELIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CEREBELLUM; CONTROLLED STUDY; CORTICAL DYSPLASIA; EMBRYO; ENDOPLASMIC RETICULUM; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; QUALITY CONTROL;

ANIMALS; BRAIN DISEASES; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; DOWN-REGULATION; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK PROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR CHAPERONES; MUTANT PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PROTEIN FOLDING; RNA, MESSENGER; SERINE ENDOPEPTIDASES;

MUS;

EID: 37549015265     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00473-07     Document Type: Article

References (50)

1. Banker, G., and K. Goslin. 1988. Developments in neuronal cell culture. Nature 336:185-186.
2. Beffert, U., E. J. Weeber, A. Durudas, S. Qiu, I. Masiulis, J. D. Sweatt, W. P. Li, G. Adelmann, M. Frotscher, R. E. Hammer, and J. Herz. 2005. Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47:567-579.
3. Beh, C. T., and M. D. Rose. 1995. Two redundant systems maintain levels of resident proteins within the yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92:9820-9823.
4. Bonifacino, J. S., and A. M. Weissman. 1998. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol. 14:19-57.
5. Bothwell, M., and E. Giniger. 2000. Alzheimer's disease: neurodevelopment converges with neurodegeneration. Cell 102:271-273.
6. Brodsky, J. L., and A. A. McCracken. 1999. ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10:507-513.
7. Caviness, V. S., Jr. 1982. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 256:293-302.
8. D'Arcangelo, G., R. Homayouni, L. Keshvara, D. S. Rice, M. Sheldon, and T. Curran. 1999. Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.
9. D'Arcangelo, G., G. G. Miao, S. C. Chen, H. D. Soares, J. I. Morgan, and T. Curran. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.
10. D'Arcangelo, G., K. Nakajima, T. Miyata, M. Ogawa, K. Mikoshiba, and T. Curran. 1997. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci. 17:23-31.
11. de Bergeyck, V., K. Nakajima, C. Lambert de Rouvroit, B. Naerhuyzen, A. M. Goffinet, T. Miyata, M. Ogawa, and K. Mikoshiba. 1997. A truncated Reelin protein is produced but not secreted in the 'Orleans' reeler mutation (Rel-n[rl-Orl]). Brain Res. Mol. Brain Res. 50:85-90.
12. Ellgaard, L., and A. Helenius. 2003. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4:181-191.
13. Falconer, D. S. 1951. Two new mutant, 'trembler' and 'reeler,' with neurological actions in the house mouse (Mus muscululus L.). J. Genet. 50:192-201.
14. Fatemi, S. H. 2005. Reelin glycoprotein: structure, biology and roles in health and disease. Mol. Psych. 10:251-257.
15. Hamada, H., M. Suzuki, S. Yuasa, N. Mimura, N. Shinozuka, Y. Takada, T. Nishino, H. Nakaya, H. Koseki, and T. Aoe. 2004. Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice. Mol. Cell. Biol. 24:8007-8017.
16. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
17. Harding, H. P., and D. Ron. 2002. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51(Suppl. 3):S455-S461.
18. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
19. Haynes, C. M., S. Caldwell, and A. A. Cooper. 2002. An HRD/DER-independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J. Cell Biol. 158:91-101.
20. Hsu, V. W., N. Shah, and R. D. Klausner. 1992. A brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1. Cell 69:625-635.
21. Imai, Y., M. Soda, H. Inoue, N. Hattori, Y. Mizuno, and R. Takahashi. 2001. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105:891-902.
22. Kakiuchi, C., K. Iwamoto, M. Ishiwata, M. Bundo, T. Kasahara, I. Kusumi, T. Tsujita, Y. Okazaki, S. Nanko, H. Kunugi, T. Sasaki, and T. Kato. 2003. Impaired feedback regulation of XBP1 as a genetic risk factor for bipolar disorder. Nat. Genet. 35:171-175.
23. Katayama, T., K. Imaizumi, N. Sato, K. Miyoshi, T. Kudo, J. Hitomi, T. Morihara, T. Yoneda, F. Gomi, Y. Mori, Y. Nakano, J. Takeda, T. Tsuda, Y. Itoyama, O. Murayama, A. Takashima, P. St. George-Hyslop, M. Takeda, and M. Tohyama. 1999. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat. Cell Biol. 1:479-485.
24. Kaufman, R. J. 2002. Orchestrating the unfolded protein response in health and disease. J. Clin. Investig. 110:1389-1398.
25. Kleizen, B., and I. Braakman. 2004. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16:343-349.
26. Kopito, R. R., and D. Ron. 2000. Conformational disease. Nat. Cell Biol. 2:E207-E209.
27. Lewis, M. J., and H. R. Pelham. 1990. A human homologue of the yeast HDEL receptor. Nature 348:162-163.
28. Luo, S., C. Mao, B. Lee, and A. S. Lee. 2006. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol. 26:5688-5697.
29. Mimura, N., H. Hamada, M. Kashio, H. Jin, Y. Toyama, K. Kimura, M. Iida, S. Goto, H. Saisho, K. Toshimori, H. Koseki, and T. Aoe. 2007. Aberrant quality control in the endoplasmic reticulum impairs the biosynthesis of pulmonary surfactant in mice expressing mutant BiP. Cell Death Differ. 14:1475-1485.
30. Munro, S., and H. R. Pelham. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899-907.
31. Munro, S., and H. R. Pelham. 1986. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291-300.
32. Ogawa, M., T. Miyata, K. Nakajima, K. Yagyu, M. Seike, K. Ikenaka, H. Yamamoto, and K. Mikoshiba. 1995. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912.
33. Ohshima, T., J. M. Ward, C. G. Huh, G. Longenecker, Veeranna, H. C. Pant, R. O. Brady, L. J. Martin, and A. B. Kulkarni. 1996. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. USA 93:11173-11178.
34. Oyadomari, S., A. Koizumi, K. Takeda, T. Gotoh, S. Akira, E. Araki, and M. Mori. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Investig. 109:525-532.
35. Patil, C., and P. Walter. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349-355.
36. Reimold, A. M., A. Etkin, I. Clauss, A. Perkins, D. S. Friend, J. Zhang, H. F. Horton, A. Scott, S. H. Orkin, M. C. Byrne, M. J. Grusby, and L. H. Glimcher. 2000. An essential role in liver development for transcription factor XBP-1. Genes Dev. 14:152-157.
37. Reimold, A. M., N. N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E. M. Gravallese, D. Friend, M. J. Grusby, F. Alt, and L. H. Glimcher. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300-307.
38. Scheuner, D., B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonner-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
39. Schroder, M., and R. J. Kaufman. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74:739-789.
40. Sonnichsen, B., J. Fullekrug, P. N. Van, W. Diekmann, D. G. Robinson, and G. Mieskes. 1994. Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J. Cell Sci. 107:2705-2717.
41. Tajiri, S., S. Oyadomari, S. Yano, M. Morioka, T. Gotoh, J. I. Hamada, Y. Ushio, and M. Mori. 2004. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. 11:403-415.
42. Taxis, C., F. Vogel, and D. H. Wolf. 2002. ER-Golgi traffic is a prerequisite for efficient ER degradation. Mol. Biol. Cell 13:1806-1818.
43. Tissir, F., and A. M. Goffinet. 2003. Reelin and brain development. Nat. Rev. Neurosci. 4:496-505.
44. Utsunomiya-Tate, N., K. Kubo, S. Tate, M. Kainosho, E. Katayama, K. Nakajima, and K. Mikoshiba. 2000. Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proc. Natl. Acad. Sci. USA 97:9729-9734.
45. Vashist, S., and D. T. Ng. 2004. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165:41-52.
46. Wu, J., and R. J. Kaufman. 2006. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13:374-384.
47. Yamamoto, K., R. Fujii, Y. Toyofuku, T. Saito, H. Koseki, V. W. Hsu, and T. Aoe. 2001. The KDEL receptor mediates a retrieval mechanism that contributes to quality control at the endoplasmic reticulum. EMBO J. 20:3082-3091.
48. Yuasa, S., J. Kitoh, S. Oda, and K. Kawamura. 1993. Obstructed migration of Purkinje cells in the developing cerebellum of the reeler mutant mouse. Anat. Embryol. (Berlin) 188:317-329.
49. Zhao, L., C. Longo-Guess, B. S. Harris, J. W. Lee, and S. L. Ackerman. 2005. Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat. Genet. 37:974-979.
50. Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.