PLEIAD/SIMC1/C5orf25, a novel autolysis regulator for a skeletal-muscle-specific calpain, CAPN3, scaffolds a CAPN3 substrate, CTBP1

Journal of Molecular Biology

Volumn 425, Issue 16, 2013, Pages 2955-2972

  Ono, Yasuko ^a,b   Iemura, Shun Ichiro ^a,c,d   Novak, Stefanie M ^b   Doi, Naoko ^a   Kitamura, Fujiko ^a   Natsume, Tohru ^c   Gregorio, Carol C ^b   Sorimachi, Hiroyuki ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^d FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

Author keywords

autolysis; calpain; scaffold; skeletal muscle; substrate

Indexed keywords

BINDING PROTEIN; CALPAIN 3; CTBP1 PROTEIN; SUMO 1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOLYSIS; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS7; CHROMOSOME 5; CONTROLLED STUDY; ENZYME ACTIVITY; EXON; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SARCOMERE;

VERTEBRATA;

EID: 84880916547     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.05.009     Document Type: Article

References (61)

1. H. Sorimachi, S. Imajoh-Ohmi, Y. Emori, H. Kawasaki, S. Ohno, Y. Minami, and K. Suzuki Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle J. Biol. Chem. 264 1989 20106 20111 (Pubitemid 20008132)
2. D.E. Goll, V.F. Thompson, H. Li, W. Wei, and J. Cong The calpain system Physiol. Rev. 83 2003 731 801 (Pubitemid 36828925)
3. J. Liu, M.C. Liu, and K.K. Wang Calpain in the CNS: from synaptic function to neurotoxicity Sci. Signaling 1 2008 re1
4. H. Sorimachi, S. Hata, and Y. Ono Calpain chronicle - an enzyme family under multidisciplinary characterization Proc. Jpn. Acad., Ser. B 87 2011 287 327
5. H. Sorimachi, S. Hata, and Y. Ono Impact of genetic insights into calpain biology J. Biochem. 150 2011 23 37
6. Y. Ono, and H. Sorimachi Calpains: an elaborate proteolytic system Biochim. Biophys. Acta 1824 2012 224 236
7. H. Sorimachi, H. Mamitsuka, and Y. Ono Understanding the substrate specificity of conventional calpains Biol. Chem. 393 2012 853 871
8. I. Richard, O. Broux, V. Allamand, F. Fougerousse, N. Chiannilkulchai, and N. Bourg Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A Cell 81 1995 27 40
9. J.S. Beckmann, and M. Spencer Calpain 3, the "gatekeeper" of proper sarcomere assembly, turnover and maintenance Neuromuscular Disord. 18 2008 913 921
10. I. Richard, C. Roudaut, S. Marchand, S. Baghdiguian, M. Herasse, and D. Stockholm Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IκBα/nuclear factor κB pathway perturbation in mice J. Cell Biol. 151 2000 1583 1590 (Pubitemid 32047605)
11. F. Fougerousse, P. Gonin, M. Durand, I. Richard, and J.M. Raymackers Force impairment in calpain 3-deficient mice is not correlated with mechanical disruption Muscle Nerve 27 2003 616 623 (Pubitemid 36523522)
12. I. Kramerova, E. Kudryashova, J.G. Tidball, and M.J. Spencer Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro Hum. Mol. Genet. 13 2004 1373 1388 (Pubitemid 38961644)
13. I. Kramerova, E. Kudryashova, B. Wu, and M.J. Spencer Regulation of the M-cadherin-β-catenin complex by calpain 3 during terminal stages of myogenic differentiation Mol. Cell. Biol. 26 2006 8437 8447 (Pubitemid 44748577)
14. I. Kramerova, E. Kudryashova, B. Wu, C. Ottenheijm, H. Granzier, and M.J. Spencer Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle Hum. Mol. Genet. 17 2008 3271 3280
15. I. Kramerova, E. Kudryashova, B. Wu, S. Germain, K. Vandenborne, and N. Romain Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle Hum. Mol. Genet. 18 2009 3194 3205
16. I. Kramerova, E. Kudryashova, N. Ermolova, A. Saenz, O. Jaka, A. Lopez de Munain, and M.J. Spencer Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of calpain 3 Hum. Mol. Genet. 21 2012 3193 3204
17. O. Jaka, I. Kramerova, M. Azpitarte, A. Lopez de Munain, M. Spencer, and A. Saenz C3KO mouse expression analysis: downregulation of the muscular dystrophy Ky protein and alterations in muscle aging Neurogenetics 13 2012 347 357
18. K. Ojima, Y. Kawabata, H. Nakao, K. Nakao, N. Doi, and F. Kitamura Dynamic distribution of muscle-specific calpain in mice has a key role in physical-stress adaptation and is impaired in muscular dystrophy J. Clin. Invest. 120 2010 2672 2683
19. K. Ojima, Y. Ono, C. Ottenheijm, S. Hata, H. Suzuki, H. Granzier, and H. Sorimachi Non-proteolytic functions of calpain-3 in sarcoplasmic reticulum in skeletal muscles J. Mol. Biol. 407 2011 439 449
20. K. Tagawa, C. Taya, Y. Hayashi, M. Nakagawa, Y. Ono, and R. Fukuda Myopathy phenotype of transgenic mice expressing active site-mutated inactive p94 skeletal muscle-specific calpain, the gene product responsible for limb girdle muscular dystrophy type 2A Hum. Mol. Genet. 9 2000 1393 1402 (Pubitemid 30312488)
21. H. Sorimachi, N. Toyama-Sorimachi, T.C. Saido, H. Kawasaki, H. Sugita, and M. Miyasaka Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle J. Biol. Chem. 268 1993 10593 10605 (Pubitemid 23150250)
22. H. Sorimachi, K. Kinbara, S. Kimura, M. Takahashi, S. Ishiura, and N. Sasagawa Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence J. Biol. Chem. 270 1995 31158 31162 (Pubitemid 26012203)
23. K. Kinbara, H. Sorimachi, S. Ishiura, and K. Suzuki Muscle-specific calpain, p94, interacts with the extreme C-terminal region of connectin, a unique region flanked by two immunoglobulin C2 motifs Arch. Biochem. Biophys. 342 1997 99 107 (Pubitemid 27217106)
24. K. Kinbara, S. Ishiura, S. Tomioka, H. Sorimachi, S.Y. Jeong, and S. Amano Purification of native p94, a muscle-specific calpain, and characterization of its autolysis Biochem. J. 335 1998 589 596 (Pubitemid 28515412)
25. Y. Ono, F. Torii, K. Ojima, N. Doi, K. Yoshioka, and Y. Kawabata Suppressed disassembly of autolyzing p94/CAPN3 by N2A connectin/titin in a genetic reporter system J. Biol. Chem. 281 2006 18519 18531 (Pubitemid 44035511)
26. C. Hayashi, Y. Ono, N. Doi, F. Kitamura, M. Tagami, and R. Mineki Multiple molecular interactions implicate the connectin/titin N2A region as a modulating scaffold for p94/calpain 3 activity in skeletal muscle J. Biol. Chem. 283 2008 14801 14814
27. K. Ojima, Y. Ono, N. Doi, K. Yoshioka, Y. Kawabata, S. Labeit, and H. Sorimachi Myogenic stage, sarcomere length, and protease activity modulate localization of muscle-specific calpain J. Biol. Chem. 282 2007 14493 14504 (Pubitemid 47100485)
28. T. Natsume, Y. Yamauchi, H. Nakayama, T. Shinkawa, M. Yanagida, N. Takahashi, and T. Isobe A direct nanoflow liquid chromatography-tandem mass spectrometry system for interaction proteomics Anal. Chem. 74 2002 4725 4733
29. H. Sun, and T. Hunter Poly-small ubiquitin-like modifier (PolySUMO)-binding proteins identified through a string search J. Biol. Chem. 287 2012 42071 42083
30. D. Corda, A. Colanzi, and A. Luini The multiple activities of CtBP/BARS proteins: the Golgi view Trends Cell Biol. 16 2006 167 173 (Pubitemid 43358005)
31. G. Chinnadurai The transcriptional corepressor CtBP: a foe of multiple tumor suppressors Cancer Res. 69 2009 731 734
32. +-dependent protease J. Biol. Chem. 285 2010 22986 22998
33. S. Matsuoka, B.A. Ballif, A. Smogorzewska, E.R. McDonald 3rd, K.E. Hurov, and J. Luo ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 316 2007 1160 1166 (Pubitemid 46877472)
34. M. Kuppuswamy, S. Vijayalingam, L.J. Zhao, Y. Zhou, T. Subramanian, J. Ryerse, and G. Chinnadurai Role of the PLDLS-binding cleft region of CtBP1 in recruitment of core and auxiliary components of the corepressor complex Mol. Cell. Biol. 28 2008 269 281
35. M. Herasse, Y. Ono, F. Fougerousse, E. Kimura, D. Stockholm, and C. Beley Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events Mol. Cell. Biol. 19 1999 4047 4055 (Pubitemid 29241979)
36. D.A. duVerle, Y. Ono, H. Sorimachi, and H. Mamitsuka Calpain cleavage prediction using multiple kernel learning PLoS One 6 2011 e19035
37. H. Ma, M. Shih, C. Fukiage, M. Azuma, M.K. Duncan, and N.A. Reed Influence of specific regions in Lp82 calpain on protein stability, activity, and localization within lens Invest. Ophthalmol. Visual Sci. 41 2000 4232 4239
38. M. Bakay, Z. Wang, G. Melcon, L. Schiltz, J. Xuan, and P. Zhao Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration Brain 129 2006 996 1013
39. T.S. Mikkelsen, M.J. Wakefield, B. Aken, C.T. Amemiya, J.L. Chang, and S. Duke Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences Nature 447 2007 167 177 (Pubitemid 46763085)
40. J. Jurka, V.V. Kapitonov, O. Kohany, and M.V. Jurka Repetitive sequences in complex genomes: structure and evolution Annu. Rev. Genomics Hum. Genet. 8 2007 241 259
41. G.M. Riefler, and B.L. Firestein Binding of neuronal nitric-oxide synthase (nNOS) to carboxyl-terminal-binding protein (CtBP) changes the localization of CtBP from the nucleus to the cytosol: a novel function for targeting by the PDZ domain of nNOS J. Biol. Chem. 276 2001 48262 48268
42. X. Lin, B. Sun, M. Liang, Y.Y. Liang, A. Gast, and J. Hildebrand Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding Mol. Cell 11 2003 1389 1396 (Pubitemid 36645156)
43. E.B. Dammer, and M.B. Sewer Phosphorylation of CtBP1 by cAMP-dependent protein kinase modulates induction of CYP17 by stimulating partnering of CtBP1 and 2 J. Biol. Chem. 283 2008 6925 6934
44. N. Kitamura, Y. Motoi, A. Mori, H. Tatsumi, S. Nemoto, and H. Miyoshi Suppressive role of C-terminal binding protein 1 in IL-4 synthesis in human T cells Biochem. Biophys. Res. Commun. 382 2009 326 330
45. C. Bhambhani, J.L. Chang, D.L. Akey, and K.M. Cadigan The oligomeric state of CtBP determines its role as a transcriptional co-activator and co-repressor of Wingless targets EMBO J. 30 2011 2031 2043
46. S. Kajimura, P. Seale, T. Tomaru, H. Erdjument-Bromage, M.P. Cooper, and J.L. Ruas Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex Genes Dev. 22 2008 1397 1409 (Pubitemid 351717529)
47. V. Perissi, C. Scafoglio, J. Zhang, K.A. Ohgi, D.W. Rose, C.K. Glass, and M.G. Rosenfeld TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints Mol. Cell 29 2008 755 766 (Pubitemid 351400927)
48. P.K. Purbey, S. Singh, D. Notani, P.P. Kumar, A.S. Limaye, and S. Galande Acetylation-dependent interaction of SATB1 and CtBP1 mediates transcriptional repression by SATB1 Mol. Cell. Biol. 29 2009 1321 1337
49. M.D. Stern, H. Aihara, G.A. Roccaro, L. Cheung, H. Zhang, D. Negeri, and Y. Nibu CtBP is required for proper development of peripheral nervous system in Drosophila Mech. Dev. 126 2009 68 79
50. S.Y. Wang, M. Iordanov, and Q. Zhang c-Jun NH2-terminal kinase promotes apoptosis by down-regulating the transcriptional co-repressor CtBP J. Biol. Chem. 281 2006 34810 34815 (Pubitemid 46036520)
51. R.A. Phelps, S. Chidester, S. Dehghanizadeh, J. Phelps, I.T. Sandoval, and K. Rai A two-step model for colon adenoma initiation and progression caused by APC loss Cell 137 2009 623 634
52. P. Tompa Intrinsically disordered proteins: a 10-year recap Trends Biochem. Sci. 37 2012 509 516
53. T. Moldoveanu, K. Gehring, and D.R. Green Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains Nature 456 2008 404 408
54. R.A. Hanna, R.L. Campbell, and P.L. Davies Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin Nature 456 2008 409 412
55. N. Sato, H. Kawahara, A. Toh-e, and T. Maeda Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteasome system Mol. Cell. Biol. 23 2003 6662 6671 (Pubitemid 37075775)
56. Y. Ono, H. Shimada, H. Sorimachi, I. Richard, T.C. Saido, and J.S. Beckmann Functional defects of a muscle-specific calpain, p94, caused by mutations associated with limb-girdle muscular dystrophy type 2A J. Biol. Chem. 273 1998 17073 17078 (Pubitemid 28311741)
57. A. Almenar-Queralt, C.C. Gregorio, and V.M. Fowler Tropomodulin assembles early in myofibrillogenesis in chick skeletal muscle: evidence that thin filaments rearrange to form striated myofibrils J. Cell Sci. 112 1999 1111 1123 (Pubitemid 29218901)
58. C.T. Pappas, N. Bhattacharya, J.A. Cooper, and C.C. Gregorio Nebulin interacts with CapZ and regulates thin filament architecture within the Z-disc Mol. Biol. Cell 19 2008 1837 1847
59. K. Katoh, G. Asimenos, and H. Toh Multiple alignment of DNA sequences with MAFFT Methods Mol. Biol. 537 2009 39 64
60. A. Heger, and L. Holm Rapid automatic detection and alignment of repeats in protein sequences Proteins 41 2000 224 237
61. D. duVerle, I. Takigawa, Y. Ono, H. Sorimachi, and H. Mamitsuka CaMPDB: a resource for calpain and modulatory proteolysis Genome Inform. 22 2010 202 213