Muscle RING-Finger Protein-1 (MuRF1) as a Connector of Muscle Energy Metabolism and Protein Synthesis

Journal of Molecular Biology

Volumn 376, Issue 5, 2008, Pages 1224-1236

  Koyama, Suguru ^a,b   Hata, Shoji ^a   Witt, Christian C ^c   Ono, Yasuko ^a   Lerche, Stefanie ^c   Ojima, Koichi ^a,d   Chiba, Tomoki ^a   Doi, Naoko ^a,d   Kitamura, Fujiko ^a   Tanaka, Keiji ^a   Abe, Keiko ^b   Witt, Stephanie H ^c   Rybin, Vladimir ^e   Gasch, Alexander ^c   Franz, Thomas ^e   Labeit, Siegfried ^c   Sorimachi, Hiroyuki ^a,d  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

creatine kinase; MuRF1; muscle atrophy; RING finger protein; titin connectin

Indexed keywords

AMINO ACID; CREATINE KINASE; GLUCOCORTICOID; MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN;

ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; HEART MUSCLE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SKELETAL MUSCLE;

MUS;

EID: 39149134903     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.049     Document Type: Article

References (55)

1. Engel A., and Franzini-Armstrong C. Myology: Basic and Clinical. 3rd edit. (2004), McGraw-Hill, Medical Publishing Division, New York, NY
2. Pepato M.T., Migliorini R.H., Goldberg A.L., and Kettelhut I.C. Role of different proteolytic pathways in degradation of muscle protein from streptozotocin-diabetic rats. Am. J. Physiol. 271 (1996) E340-E347
3. Tiao G., Fagan J.M., Samuels N., James J.H., Hudson K., Lieberman M., et al. Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J. Clin. Invest. 94 (1994) 2255-2264
4. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18 (2004) 39-51
5. Baracos V.E., DeVivo C., Hoyle D.H., and Goldberg A.L. Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am. J. Physiol. 268 (1995) E996-E1006
6. Tawa Jr. N.E., Odessey R., and Goldberg A.L. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 100 (1997) 197-203
7. Solomon V., and Goldberg A.L. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J. Biol. Chem. 271 (1996) 26690-26697
8. Mitch W.E., Bailey J.L., Wang X., Jurkovitz C., Newby D., and Price S.R. Evaluation of signals activating ubiquitin-proteasome proteolysis in a model of muscle wasting. Am. J. Physiol. 276 (1999) C1132-C1138
9. Smith I.J., and Dodd S.L. Calpain activation causes a proteasome dependent increase in protein degradation and inhibits the Akt signaling pathway in rat diaphragm muscle. Exp. Physiol. 92 (2007) 561-573
10. Attaix D., Ventadour S., Codran A., Bechet D., Taillandier D., and Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem. 41 (2005) 173-186
11. Bodine S.C., Latres E., Baumhueter S., Lai V.K., Nunez L., Clarke B.A., et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294 (2001) 1704-1708
12. Wray C.J., Mammen J.M., Hershko D.D., and Hasselgren P.O. Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int. J. Biochem. Cell Biol. 35 (2003) 698-705
13. Dehoux M.J., van Beneden R.P., Fernandez-Celemin L., Lause P.L., and Thissen J.P. Induction of MafBx and Murf ubiquitin ligase mRNAs in rat skeletal muscle after LPS injection. FEBS Lett. 544 (2003) 214-217
14. Nikawa T., Ishidoh K., Hirasaka K., Ishihara I., Ikemoto M., Kano M., et al. Skeletal muscle gene expression in space-flown rats. FASEB J. 18 (2004) 522-524
15. Gomes M.D., Lecker S.H., Jagoe R.T., Navon A., and Goldberg A.L. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc. Natl Acad. Sci. USA 98 (2001) 14440-14445
16. Short K.M., and Cox T.C. Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding. J. Biol. Chem. 281 (2006) 8970-8980
17. Borden K.L. RING domains: master builders of molecular scaffolds?. J. Mol. Biol. 295 (2000) 1103-1112
18. Centner T., Yano J., Kimura E., McElhinny A.S., Pelin K., Witt C.C., et al. Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. J. Mol. Biol. 306 (2001) 717-726
19. Witt S.H., Granzier H., Witt C.C., and Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J. Mol. Biol. 350 (2005) 713-722
20. Maruyama K. Connectin, an elastic protein from myofibrils. J. Biochem. 80 (1976) 405-407
21. Labeit S., and Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270 (1995) 293-296
22. Mrosek M., Labeit D., Witt S., Heerklotz H., von Castelmur E., Labeit S., and Mayans O. Molecular determinants for the recruitment of the ubiquitin-ligase MuRF-1 onto M-line titin. FASEB J. 21 (2007) 1383-1392
23. Labeit S., Gautel M., Lakey A., and Trinick J. Towards a molecular understanding of titin. EMBO J. 11 (1992) 1711-1716
24. Sorimachi H., Kinbara K., Kimura S., Takahashi M., Ishiura S., Sasagawa N., et al. 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
25. Ojima K., Ono Y., Doi N., Yoshioka K., Kawabata Y., Labeit S., and Sorimachi H. Myogenic stage, sarcomere length, and protease activity modulate localization of muscle-specific calpain. J. Biol. Chem. 282 (2007) 14493-14504
26. Ojima K., Ono Y., Hata S., Koyama S., Doi N., and Sorimachi H. Possible functions of p94 in connectin-mediated signaling pathways in skeletal muscle cells. J. Muscle Res. Cell Motil. 26 (2005) 409-417
27. Lange S., Xiang F., Yakovenko A., Vihola A., Hackman P., Rostkova E., et al. The kinase domain of titin controls muscle gene expression and protein turnover. Science 308 (2005) 1599-1603
28. Gregorio C.C., Perry C.N., and McElhinny A.S. Functional properties of the titin/connectin-associated proteins, the muscle-specific RING finger proteins (MURFs), in striated muscle. J. Muscle Res. Cell Motil. 26 (2005) 389-400
29. Kedar V., McDonough H., Arya R., Li H.H., Rockman H.A., and Patterson C. Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc. Natl Acad. Sci. USA 101 (2004) 18135-18140
30. McElhinny A.S., Kakinuma K., Sorimachi H., Labeit S., and Gregorio C.C. Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1. J. Cell Biol. 157 (2002) 125-136
31. McElhinny A.S., Perry C.N., Witt C.C., Labeit S., and Gregorio C.C. Muscle-specific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development. J. Cell Sci. 117 (2004) 3175-3188
32. Pizon V., Iakovenko A., Van Der Ven P.F., Kelly R., Fatu C., Furst D.O., et al. Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein. J. Cell Sci. 115 (2002) 4469-4482
33. Spencer J.A., Eliazer S., Ilaria Jr. R.L., Richardson J.A., and Olson E.N. Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J. Cell Biol. 150 (2000) 771-784
34. Dai K.S., and Liew C.C. A novel human striated muscle RING zinc finger protein, SMRZ, interacts with SMT3b via its RING domain. J. Biol. Chem. 276 (2001) 23992-23999
35. Bessman S.P., and Carpenter C.L. The creatine-creatine phosphate energy shuttle. Annu. Rev. Biochem. 54 (1985) 831-862
36. Wallimann T., Wyss M., Brdiczka D., Nicolay K., and Eppenberger H.M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 281 (1992) 21-40
37. Turner D.C., Wallimann T., and Eppenberger H.M. A protein that binds specifically to the M-line of skeletal muscle is identified as the muscle form of creatine kinase. Proc. Natl Acad. Sci. USA 70 (1973) 702-705
38. Wallimann T., Turner D.C., and Eppenberger H.M. Localization of creatine kinase isoenzymes in myofibrils. I. Chicken skeletal muscle. J. Cell Biol. 75 (1977) 297-317
39. Ventura-Clapier R., Kaasik A., and Veksler V. Structural and functional adaptations of striated muscles to CK deficiency. Mol. Cell. Biochem. 256-257 (2004) 29-41
40. Chang T.W., and Goldberg A.L. The metabolic fates of amino acids and the formation of glutamine in skeletal muscle. J. Biol. Chem. 253 (1978) 3685-3693
41. Robinson W.G., and Coon M.J. The purification and properties of beta-hydroxyisobutyric dehydrogenase. J. Biol. Chem. 225 (1957) 511-521
42. Lokanath N.K., Ohshima N., Takio K., Shiromizu I., Kuroishi C., Okazaki N., et al. Crystal structure of novel NADP-dependent 3-hydroxyisobutyrate dehydrogenase from Thermus thermophilus HB8. J. Mol. Biol. 352 (2005) 905-917
43. Shoham N.G., Centola M., Mansfield E., Hull K.M., Wood G., Wise C.A., and Kastner D.L. Pyrin binds the PSTPIP1/CD2BP1 protein, defining familial Mediterranean fever and PAPA syndrome as disorders in the same pathway. Proc. Natl Acad. Sci. USA 100 (2003) 13501-13506
44. Javanbakht H., Diaz-Griffero F., Stremlau M., Si Z., and Sodroski J. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J. Biol. Chem. 280 (2005) 26933-26940
45. Beenders B., Jones P.L., and Bellini M. The tripartite motif of nuclear factor 7 is required for its association with transcriptional units. Mol. Cell. Biol. 27 (2007) 2615-2624
46. Zhao T.J., Yan Y.B., Liu Y., and Zhou H.M. The generation of the oxidized form of creatine kinase is a negative regulation on muscle creatine kinase. J. Biol. Chem. 282 (2007) 12022-12029
47. Hata S., Koyama S., Kawahara H., Doi N., Maeda T., Toyama-Sorimachi N., et al. Stomach-specific calpain, nCL-2, localizes in mucus cells and proteolyzes the beta-subunit of coatomer complex, beta-COP. J. Biol. Chem. 281 (2006) 11214-11224
48. Sorimachi H., Toyama-Sorimachi N., Saido T.C., Kawasaki H., Sugita H., Miyasaka M., et al. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268 (1993) 10593-10605
49. Wilm M., Shevchenko A., Houthaeve T., Breit S., Schweigerer L., Fotsis T., and Mann M. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379 (1996) 466-469
50. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
51. Gharahdaghi F., Weinberg C.R., Meagher D.A., Imai B.S., and Mische S.M. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20 (1999) 601-605
52. Watchko J.F., Daood M.J., and LaBella J.J. Creatine kinase activity in rat skeletal muscle relates to myosin phenotype during development. Pediatr. Res. 40 (1996) 53-58
53. Witt, C. C., Witt, S. H., Lerche, S., Labeit, D., Back, W. & Labeit, S. (2008). Cooperative control of striated muscle mass and metabolism by MuRF1 and MuRF2. EMBO J., In press. doi:10.1038/sj.emboj.7601952.
54. Dardevet D., Sornet C., Bayle G., Prugnaud J., Pouyet C., and Grizard J. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J. Nutr. 132 (2002) 95-100
55. Prod'homme M., Balage M., Debras E., Farges M.C., Kimball S., Jefferson L., and Grizard J. Differential effects of insulin and dietary amino acids on muscle protein synthesis in adult and old rats. J. Physiol. 563 (2005) 235-248