A novel conserved isoform of the ubiquitin ligase UFD2a/UBE4b is expressed exclusively in mature striated muscle cells

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Mammen, Andrew L ^a   Mahoney, James A ^a   Germain, Amanda ^c   Badders, Nisha ^b   Taylor, J Paul ^b   Rosen, Antony ^a   Spinette, Sarah ^c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c RHODE ISLAND COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARDIOTOXIN; ISOENZYME; MESSENGER RNA; PROTEIN P97; PROTEIN UFD2A; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; CDC48 PROTEIN; CELL CYCLE PROTEIN;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME SPECIFICITY; EXON; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEART MUSCLE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INTRON; MALE; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN INTERACTION; SKELETAL MUSCLE; UFD2A GENE; UPREGULATION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; ANIMAL MODEL; ANTIBODY SPECIFICITY; CELL LINE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUSCLE CELL; NUCLEOTIDE MOTIF; PROTEIN BINDING; REGENERATION;

ADENOSINE TRIPHOSPHATASES; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINE; CONSERVED SEQUENCE; EXONS; FEMALE; ISOENZYMES; MALE; MICE; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; MUSCLE CELLS; MUSCLE DEVELOPMENT; MUSCLE, STRIATED; MYOCARDIUM; NUCLEOTIDE MOTIFS; ORGAN SPECIFICITY; PROTEIN BINDING; REGENERATION; RNA, MESSENGER; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION; ZEBRAFISH;

EID: 83055173839     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028861     Document Type: Article

References (63)

1. Castle JC, Zhang C, Shah JK, Kulkarni AV, Kalsotra A, et al. (2008) Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat Genet 40: 1416-1425.
2. Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, et al. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302: 2141-2144.
3. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
4. Bland CS, Wang ET, Vu A, David MP, Castle JC, et al. (2010) Global regulation of alternative splicing during myogenic differentiation. Nucleic Acids Res 38: 7651-7664.
5. Kalsotra A, Xiao X, Ward AJ, Castle JC, Johnson JM, et al. (2008) A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci U S A 105: 20333-20338.
6. Townsend PJ, Barton PJ, Yacoub MH, Farza H, (1995) Molecular cloning of human cardiac troponin T isoforms: expression in developing and failing heart. J Mol Cell Cardiol 27: 2223-2236.
7. McAuliffe JJ, Gao LZ, Solaro RJ, (1990) Changes in myofibrillar activation and troponin C Ca2+binding associated with troponin T isoform switching in developing rabbit heart. Circ Res 66: 1204-1216.
8. Warren CM, Krzesinski PR, Campbell KS, Moss RL, Greaser ML, (2004) Titin isoform changes in rat myocardium during development. Mech Dev 121: 1301-1312.
9. Ladd AN, Stenberg MG, Swanson MS, Cooper TA, (2005) Dynamic balance between activation and repression regulates pre-mRNA alternative splicing during heart development. Dev Dyn 233: 783-793.
10. Abu Hatoum O, Gross-Mesilaty S, Breitschopf K, Hoffman A, Gonen H, et al. (1998) Degradation of myogenic transcription factor MyoD by the ubiquitin pathway in vivo and in vitro: regulation by specific DNA binding. Mol Cell Biol 18: 5670-5677.
11. Sun L, Trausch-Azar JS, Ciechanover A, Schwartz AL, (2005) Ubiquitin-proteasome-mediated degradation, intracellular localization, and protein synthesis of MyoD and Id1 during muscle differentiation. J Biol Chem 280: 26448-26456.
12. Sun L, Trausch-Azar JS, Ciechanover A, Schwartz AL, (2007) E2A protein degradation by the ubiquitin-proteasome system is stage-dependent during muscle differentiation. Oncogene 26: 441-448.
13. Lindon C, Montarras D, Pinset C, (1998) Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J Cell Biol 140: 111-118.
14. Heuze ML, Lamsoul I, Baldassarre M, Lad Y, Leveque S, et al. (2008) ASB2 targets filamins A and B to proteasomal degradation. Blood 112: 5130-5140.
15. Solomon V, Goldberg AL, (1996) Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J Biol Chem 271: 26690-26697.
16. Campos Y, Qiu X, Zanoteli E, Moshiach S, Vergani N, et al. (2010) Ozz-E3 ubiquitin ligase targets sarcomeric embryonic myosin heavy chain during muscle development. PLoS One 5: e9866.
17. Barral JM, Hutagalung AH, Brinker A, Hartl FU, Epstein HF, (2002) Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295: 669-671.
18. Landsverk ML, Li S, Hutagalung AH, Najafov A, Hoppe T, et al. (2007) The UNC-45 chaperone mediates sarcomere assembly through myosin degradation in Caenorhabditis elegans. J Cell Biol 177: 205-210.
19. Hoppe T, Cassata G, Barral JM, Springer W, Hutagalung AH, et al. (2004) Regulation of the myosin-directed chaperone UNC-45 by a novel E3/E4-multiubiquitylation complex in C. elegans. Cell 118: 337-349.
20. Hutagalung AH, Landsverk ML, Price MG, Epstein HF, (2002) The UCS family of myosin chaperones. J Cell Sci 115: 3983-3990.
21. Ardley HC, Robinson PA, (2005) E3 ubiquitin ligases. Essays Biochem 41: 15-30.
22. Sorokin AV, Kim ER, Ovchinnikov LP, (2009) Proteasome system of protein degradation and processing. Biochemistry (Mosc) 74: 1411-1442.
23. Spinette S, Lengauer C, Mahoney JA, Jallepalli PV, Wang Z, et al. (2004) Ufd2, a novel autoantigen in scleroderma, regulates sister chromatid separation. Cell Cycle 3: 1638-1644.
24. Mahoney JA, Odin JA, White SM, Shaffer D, Koff A, et al. (2002) The human homologue of the yeast polyubiquitination factor Ufd2p is cleaved by caspase 6 and granzyme B during apoptosis. 361: 587-595.
25. Kaneko C, Hatakeyama S, Matsumoto M, Yada M, Nakayama K, et al. (2003) Characterization of the mouse gene for the U-box-type ubiquitin ligase UFD2a. Biochem Biophys Res Commun 300: 297-304.
26. Aravind L, Koonin EV, (2000) The U box is a modified RING finger- a common domain in ubiquitination. Curr Biol 10: R132-134.
27. Matsumoto M, Yada M, Hatakeyama S, Ishimoto H, Tanimura T, et al. (2004) Molecular clearance of ataxin-3 is regulated by a mammalian E4. Embo J 23: 659-669.
28. Spinette S, Mahoney JA, Rosen A, (2006) The MPAC domain is a novel mitotically regulated domain, removed by apoptotic protease cleavage during cell death. Biochem Biophys Res Commun 347: 1103-1112.
29. Nordquist KA, Dimitrova YN, Brzovic PS, Ridenour WB, Munro KA,et al. Structural and functional characterization of the monomeric U-box domain from E4B. Biochemistry 49: 347-355.
30. Benirschke RC, Thompson JR, Nomine Y, Wasielewski E, Juranic N,et al. Molecular basis for the association of human E4B U box ubiquitin ligase with E2-conjugating enzymes UbcH5c and Ubc4. Structure 18: 955-965.
31. Kaneko-Oshikawa C, Nakagawa T, Yamada M, Yoshikawa H, Matsumoto M, et al. (2005) Mammalian E4 is required for cardiac development and maintenance of the nervous system. Mol Cell Biol 25: 10953-10964.
32. Susaki E, Kaneko-Oshikawa C, Miyata K, Tabata M, Yamada T, et al. (5547).
33. Sugnet CW, Srinivasan K, Clark TA, O'Brien G, Cline MS, et al. (2006) Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput Biol 2: e4.
34. Higgins DG, (1994) CLUSTAL V: multiple alignment of DNA and protein sequences. Methods Mol Biol 25: 307-318.
35. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
36. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, et al. (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15: 867-877.
37. Kuang S, Gillespie MA, Rudnicki MA, (2008) Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2: 22-31.
38. Kuang S, Rudnicki MA, (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14: 82-91.
39. Yaffe D, Saxel O, (1977) A myogenic cell line with altered serum requirements for differentiation. Differentiation 7: 159-166.
40. Yaffe D, Saxel O, (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
41. Brand-Saberi B, (2005) Genetic and epigenetic control of skeletal muscle development. Ann Anat 187: 199-207.
42. Couteaux R, Mira JC, d'Albis A, (1988) Regeneration of muscles after cardiotoxin injury. I. Cytological aspects. Biol Cell 62: 171-182.
43. Kimura K, Wakamatsu A, Suzuki Y, Ota T, Nishikawa T, et al. (2006) Diversification of transcriptional modulation: large-scale identification and characterization of putative alternative promoters of human genes. Genome Res 16: 55-65.
44. Li W, Wu G, Wan Y, (2007) The dual effects of Cdh1/APC in myogenesis. Faseb J 21: 3606-3617.
45. Samson T, Will C, Knoblauch A, Sharek L, von der Mark K, et al. (2007) Def-6, a guanine nucleotide exchange factor for Rac1, interacts with the skeletal muscle integrin chain alpha7A and influences myoblast differentiation. J Biol Chem 282: 15730-15742.
46. McElhinny AS, Perry CN, Witt CC, Labeit S, Gregorio CC, (2004) 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: 3175-3188.
47. Cao PR, Kim HJ, Lecker SH, (2005) Ubiquitin-protein ligases in muscle wasting. Int J Biochem Cell Biol 37: 2088-2097.
48. Lecker SH, Goldberg AL, Mitch WE, (2006) Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17: 1807-1819.
49. Janiesch PC, Kim J, Mouysset J, Barikbin R, Lochmuller H, et al. (2007) The ubiquitin-selective chaperone CDC-48/p97 links myosin assembly to human myopathy. Nat Cell Biol 9: 379-390.
50. Price MG, Landsverk ML, Barral JM, Epstein HF, (2002) Two mammalian UNC-45 isoforms are related to distinct cytoskeletal and muscle-specific functions. J Cell Sci 115: 4013-4023.
51. Srikakulam R, Liu L, Winkelmann DA, (2008) Unc45b forms a cytosolic complex with Hsp90 and targets the unfolded myosin motor domain. PLoS One 3: e2137.
52. Kachur TM, Pilgrim DB, (2008) Myosin assembly, maintenance and degradation in muscle: Role of the chaperone UNC-45 in myosin thick filament dynamics. Int J Mol Sci 9: 1863-1875.
53. Ni W, Hutagalung AH, Li S, Epstein HF, (2011) The myosin-binding UCS domain but not the Hsp90-binding TPR domain of the UNC-45 chaperone is essential for function in Caenorhabditis elegans. J Cell Sci 124: 3164-3173.
54. Etheridge L, Diiorio P, Sagerstrom CG, (2002) A zebrafish unc-45-related gene expressed during muscle development. Dev Dyn 224: 457-460.
55. Kachur T, Ao W, Berger J, Pilgrim D, (2004) Maternal UNC-45 is involved in cytokinesis and colocalizes with non-muscle myosin in the early Caenorhabditis elegans embryo. J Cell Sci 117: 5313-5321.
56. Bazzaro M, Santillan A, Lin Z, Tang T, Lee MK, et al. (2007) Myosin II co-chaperone general cell UNC-45 overexpression is associated with ovarian cancer, rapid proliferation, and motility. Am J Pathol 171: 1640-1649.
57. Bernick EP, Zhang PJ, Du S Knockdown and overexpression of Unc-45b result in defective myofibril organization in skeletal muscles of zebrafish embryos. BMC Cell Biol 11: 70.
58. Cao K, Nakajima R, Meyer HH, Zheng Y, (2003) The AAA-ATPase Cdc48/p97 regulates spindle disassembly at the end of mitosis. Cell 115: 355-367.
59. Ramadan K, Bruderer R, Spiga FM, Popp O, Baur T, et al. (2007) Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450: 1258-1262.
60. Custer SK, Neumann M, Lu H, Wright AC, Taylor JP Transgenic mice expressing mutant forms VCP/p97 recapitulate the full spectrum of IBMPFD including degeneration in muscle, brain, Hum Mol Genet 19: bone, (1741-1755).
61. Guinto JB, Ritson GP, Taylor JP, Forman MS, (2007) Valosin-containing protein and the pathogenesis of frontotemporal dementia associated with inclusion body myopathy. Acta Neuropathol 114: 55-61.
62. Ju JS, Weihl CC Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet 19: R38-45.
63. Vesa J, Su H, Watts GD, Krause S, Walter MC, et al. (2009) Valosin containing protein associated inclusion body myopathy: abnormal vacuolization, autophagy and cell fusion in myoblasts. Neuromuscular Disorders 19: 766-772.