Calpain 3 is a rapid-action, unidirectional proteolytic switch central to muscle remodeling

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  de Morrée, Antoine ^a   Hulsik, David Lutje ^b   Impagliazzo, Antonietta ^a   van Haagen, Herman H H B M ^a   de Galan, Paula ^a   van Remoortere, Alexandra ^a   't Hoen, Peter A C ^a   van Ommen, GertJan B ^a   Frants, Rune R ^a   van der Maarel, Silvère M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN 3; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN INHIBITOR OF ACTIVATED STAT1; PROTEIN INHIBITOR OF ACTIVATED STAT2; PROTEIN INHIBITOR OF ACTIVATED STAT3; PROTEIN INHIBITOR OF ACTIVATED STAT4; SUMO 2 PROTEIN; UNCLASSIFIED DRUG; CALPAIN;

ARTICLE; CONTROLLED STUDY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIMB GIRDLE MUSCULAR DYSTROPHY; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN MOTIF; SEQUENCE ANALYSIS; SKELETAL MUSCLE; STRUCTURE ANALYSIS; SUMOYLATION; AMINO ACID SEQUENCE; BIOLOGY; CHEMISTRY; CONSENSUS SEQUENCE; CYTOLOGY; CYTOSKELETON; KINETICS; METABOLISM; MOLECULAR GENETICS; MUSCLE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CALPAIN; COMPUTATIONAL BIOLOGY; CONSENSUS SEQUENCE; CYTOSKELETON; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; MUSCLES;

EID: 77957268911     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011940     Document Type: Article

References (54)

1. Lebart MC, Benyamin Y (2006) Calpain involvement in the remodeling ofcytoskeletal anchorage complexes. FEBS J 273: 3415-3426.
2. Ono Y, Shimada H, Sorimachi H, Richard I, Saido TC, et al. (1998) Functionaldefects of a muscle-specific calpain, p94, caused by mutations associated withlimb-girdle muscular dystrophy type 2A. J Biol Chem 273: 17073-17078.
3. Kinbara K, Ishiura S, Tomioka S, Sorimachi H, Jeong SY, et al. (1998)Purification of native p94, a muscle-specific calpain, and characterization of itsautolysis. Biochem J 335(Pt 3): 589-596.
4. Murphy RM, Lamb GD (2009) Endogenous calpain-3 activation is primarilygoverned by small increases in resting cytoplasmic [Ca2+] and is not dependenton stretch. J Biol Chem.
5. Beckmann JS, Spencer M (2008) Calpain 3, the gatekeeper of propersarcomere assembly, turnover and maintenance. Neuromuscul Disord 18:913-921.
6. Cohen N, Kudryashova E, Kramerova I, Anderson LV, Beckmann JS, et al.(2006) Identification of putative in vivo substrates of calpain 3 by comparativeproteomics of overexpressing transgenic and nontransgenic mice. Proteomics 6:6075-6084.
7. Duguez S, Bartoli M, Richard I (2006) Calpain 3: a key regulator of thesarcomere? FEBS J 273: 3427-3436.
8. Taveau M, Bourg N, Sillon G, Roudaut C, Bartoli M, et al. (2003) Calpain 3 isactivated through autolysis within the active site and lyses sarcomeric andsarcolemmal components. Mol Cell Biol 23: 9127-9135.
9. Cuerrier D, Moldoveanu T, Davies PL (2005) Determination of peptidesubstrate specificity for mu-calpain by a peptide library-based approach: theimportance of primed side interactions. J Biol Chem 280: 40632-40641.
10. Sakai K, Akanuma H, Imahori K, Kawashima S (1987) A unique specificity of acalcium activated neutral protease indicated in histone hydrolysis. J Biochem101: 911-918.
11. Shumway SD, Maki M, Miyamoto S (1999) The PEST domain of IkappaBalphais necessary and sufficient for in vitro degradation by mu-calpain. J Biol Chem274: 30874-30881.
12. Carillo S, Pariat M, Steff A, Jariel-Encontre I, Poulat F, et al. (1996) PESTmotifs are not required for rapid calpain-mediated proteolysis of c-fos protein. Biochem J 313(Pt 1): 245-251.
13. Tompa P, Buzder-Lantos P, Tantos A, Farkas A, Szilagyi A, et al. (2004) Onthe sequential determinants of calpain cleavage. J Biol Chem 279: 20775-20785.
14. Hubbard SJ (1998) The structural aspects of limited proteolysis of nativeproteins. Biochim Biophys Acta 1382: 191-206.
15. Chou KC (1996) Prediction of human immunodeficiency virus protease cleavagesites in proteins. Anal Biochem 233: 1-14.
16. Guyon JR, Kudryashova E, Potts A, Dalkilic I, Brosius MA, et al. (2003) Calpain3 cleaves filamin C and regulates its ability to interact with gamma- and deltasarcoglycans.Muscle Nerve 28: 472-483.
17. Huang Y, de Morree A, van Remoortere A, Bushby K, Frants RR, et al. (2008)Calpain 3 is a modulator of the dysferlin protein complex in skeletal muscle. Hum Mol Genet 17: 1855-1866.
18. Rigoutsos I, Floratos A (1998) Combinatorial pattern discovery in biologicalsequences: The TEIRESIAS algorithm. Bioinformatics 14: 55-67.
19. Jelier R, Schuemie MJ, Veldhoven A, Dorssers LC, Jenster G, et al. (2008) Anni2.0: a multipurpose text-mining tool for the life sciences. Genome Biol 9: R96.
20. Stuelsatz P, Pouzoulet F, Lamarre Y, Dargelos E, Poussard S, et al. (2010)Down-regulation of MyoD by calpain 3 promotes generation of reserve cells inC2C12 myoblasts. J Biol Chem.
21. Richard I, Roudaut C, Marchand S, Baghdiguian S, Herasse M, et al. (2000)Loss of calpain 3 proteolytic activity leads to muscular dystrophy and toapoptosis-associated IkappaBalpha/nuclear factor kappaB pathway perturbationin mice. J Cell Biol 151: 1583-1590.
22. Baghdiguian S, Richard I, Martin M, Coopman P, Beckmann JS, et al. (2001)Pathophysiology of limb girdle muscular dystrophy type 2A: hypothesis and newinsights into the IkappaBalpha/NF-kappaB survival pathway in skeletal muscle.J Mol Med 79: 254-261.
23. Dargelos E, Moyen C, Dedieu S, Veschambre P, Poussard S, et al. (2002)Development of an inducible system to assess p94 (CAPN3) function in culturedmuscle cells. J Biotechnol 96: 271-279.
24. Kramerova I, Kudryashova E, Wu B, Ottenheijm C, Granzier H, et al. (2008)Novel role of calpain-3 in the triad-associated protein complex regulatingcalcium release in skeletal muscle. Hum Mol Genet 17: 3271-3280.
25. Jang HD, Yoon K, Shin YJ, Kim J, Lee SY (2004) PIAS3 suppresses NFkappaB-mediated transcription by interacting with the p65/RelA subunit. J BiolChem 279: 24873-24880.
26. Vertegaal AC, Ogg SC, Jaffray E, Rodriguez MS, Hay RT, et al. (2004) Aproteomic study of SUMO-2 target proteins. J Biol Chem 279: 33791-33798.
27. Welm AL, Timchenko NA, Ono Y, Sorimachi H, Radomska HS, et al. (2002)C/EBPalpha is required for proteolytic cleavage of cyclin A by calpain 3 inmyeloid precursor cells. J Biol Chem 277: 33848-33856.
28. Krahn M, Bernard R, Pecheux C, Hammouda eH, Eymard B, et al. (2006)Screening of the CAPN3 gene in patients with possible LGMD2A. Clin Genet 69: 444-449.
29. Fanin M, Fulizio L, Nascimbeni AC, Spinazzi M, Piluso G, et al. (2004)Molecular diagnosis in LGMD2A: mutation analysis or protein testing? HumMutat 24: 52-62.
30. Garnham C, Hanna R, Chou J, Low K, Gourlay K, et al. (2009) Limb-girdlemuscular dystrophy type 2A can result from accelerated autoproteolyticinactivation of calpain 3. Biochemistry.
31. Diaz BG, Moldoveanu T, Kuiper MJ, Campbell RL, Davies PL (2004) Insertionsequence 1 of muscle-specific calpain, p94, acts as an internal propeptide. J BiolChem 279: 27656-27666.
32. Sorimachi H, Toyama-Sorimachi N, Saido TC, Kawasaki H, Sugita H, et al.(1993) Muscle-specific calpain, p94, is degraded by autolysis immediately aftertranslation, resulting in disappearance from muscle. J Biol Chem 268:10593-10605.
33. Kramerova I, Kudryashova E, Tidball JG, Spencer MJ (2004) Null mutation ofcalpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and invitro. Hum Mol Genet 13: 1373-1388.
34. Kramerova I, Kudryashova E, Venkatraman G, Spencer MJ (2005) Calpain 3participates in sarcomere remodeling by acting upstream of the ubiquitinproteasomepathway. Hum Mol Genet 14: 2125-2134.
35. Qu J, Liu GH, Wu K, Han P, Wang P, et al. (2007) Nitric oxide destabilizesPias3 and regulates sumoylation. PLoS ONE 2: e1085.
36. Frosk P, Weiler T, Nylen E, Sudha T, Greenberg CR, et al. (2002) Limb-girdlemuscular dystrophy type 2H associated with mutation in TRIM32, a putativeE3-ubiquitin-ligase gene. Am J Hum Genet 70: 663-672.
37. Chou KC, Shen HB (2007) Signal-CF: a subsite-coupled and window-fusingapproach for predicting signal peptides. Biochem Biophys Res Commun 357:633-640.
38. Pereg Y, Lam S, Teunisse A, Biton S, Meulmeester E, et al. (2006) Differentialroles of ATM- and Chk2-mediated phosphorylations of Hdmx in response toDNA damage. Mol Cell Biol 26: 6819-6831.
39. Chou KC, Shen HB (2008) Cell-PLoc: a package of Web servers for predictingsubcellular localization of proteins in various organisms. Nat Protoc 3: 153-162.
40. Chou KC, Zhang CT (1995) Prediction of protein structural classes. Crit RevBiochem Mol Biol 30: 275-349.
41. Chou KC, Shen HB (2007) Recent progress in protein subcellular locationprediction. Anal Biochem 370: 1-16.
42. Chou KC, Shen HB (2010) A new method for predicting the subcellularlocalization of eukaryotic proteins with both single and multiple sites: EukmPLoc2.0. PLoS One 5: e9931.
43. Lin H (2008) The modified Mahalanobis Discriminant for predicting outermembrane proteins by using Chou's pseudo amino acid composition. J TheorBiol 252: 350-356.
44. Chen C, Chen L, Zou X, Cai P (2009) Prediction of protein secondary structurecontent by using the concept of Chou's pseudo amino acid composition andsupport vector machine. Protein Pept Lett 16: 27-31.
45. de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, et al.(2006) ScanProsite: detection of PROSITE signature matches and ProRuleassociatedfunctional and structural residues in proteins. Nucleic Acids Res 34:W362-W365.
46. Hulo N, Bairoch A, Bulliard V, Cerutti L, de Castro E, et al. (2006) ThePROSITE database. Nucleic Acids Res 34: D227-D230.
47. Sigrist CJ, de Castro E, Langendijk-Genevaux PS, Le S, V, Bairoch A, et al.(2005) ProRule: a new database containing functional and structural informationon PROSITE profiles. Bioinformatics 21: 4060-4066.
48. McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structureprediction server. Bioinformatics 16: 404-405.
49. Jones DT (1999) Protein secondary structure prediction based on positionspecificscoring matrices. J Mol Biol 292: 195-202.
50. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA (2008) Exploringthe extremes of sequence/structure space with ensemble fold recognition in theprogram Phyre. Proteins 70: 611-625.
51. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODELworkspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
52. Moldoveanu T, Gehring K, Green DR (2008) Concerted multi-pronged attackby calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature456: 404-408.
53. Palma PN, Krippahl L, Wampler JE, Moura JJ (2000) BiGGER: a new (soft)docking algorithm for predicting protein interactions. Proteins 39: 372-384.
54. Krippahl L, Moura JJ, Palma PN (2003) Modeling protein complexes withBiGGER. Proteins 52: 19-23.