Identification and functional characterization of an aggregation domain in long myosin light chain kinase

FEBS Journal

Volumn 275, Issue 10, 2008, Pages 2489-2500

  Zhang, Wen Cheng ^a   Peng, Ya Jing ^a   He, Wei Qi ^a   Lv, Ning ^b   Chen, Chen ^a   Zhi, Gang ^c   Chen, Hua Qun ^b   Zhu, Min Sheng ^a  

^a NANJING UNIVERSITY   (China)

^b NANJING NORMAL UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

4Ig domain; Aggregation; Contraction; Mitochondria; Myosin light chain kinase

Indexed keywords

ACTIN; DETERGENT; HEAT SHOCK PROTEIN; MYOSIN LIGHT CHAIN KINASE; POLYMER;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; DIAPHRAGM; ELECTRON MICROSCOPY; EXTENSOR DIGITORUM LONGUS MUSCLE; GENETIC TRANSFECTION; HISTOPATHOLOGY; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE ATROPHY; MUSCLE FATIGUE; MUSCLE FIBRIL; MUSCLE FORCE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN VARIANT; SMOOTH MUSCLE; THIGH; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHICKENS; DIAPHRAGM; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUSCLE CONTRACTION; MUSCLE FATIGUE; MYOSIN SUBFRAGMENTS; MYOSIN-LIGHT-CHAIN KINASE; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, PROTEIN;

CYTOMEGALOVIRUS; MUS MUSCULUS;

EID: 42649090413     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06393.x     Document Type: Article

References (50)

1. Ikebe M, Hartshorne DJ Elzinga M (1987) Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase. Phosphorylation sites and effects of phosphorylation. J Biol Chem 262, 9569 9573.
2. Kamm KE Stull JT (1985) Myosin phosphorylation, force, and maximal shortening velocity in neurally stimulated tracheal smooth muscle. Am J Physiol 249, 238 247.
3. Stull JT, Lin PJ, Krueger JK, Trewhella J Zhi G (1998) Myosin light chain kinase: functional domains and structural motifs. Acta Physiol Scand 164, 471 482.
4. Kamm KE Stull JT (2000) Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276, 4527 4530.
5. Schoenwaelder SM Burridge K (1999) Bidirectional signaling between the cytoskeleton and integrins. Curr Opin Cell Biol 11, 274 286.
6. Bresnick AR (1999) Molecular mechanisms of nonmuscle myosin-II regulation. Curr Opin Cell Biol 11, 26 33.
7. Sato M, Tani E, Fujikawa H Kaibuchi K (2000) Involvement of Rho-kinase-mediated phosphorylation of myosin light chain in enhancement of cerebral vasospasm. Circ Res 87, 195 200.
8. van Nieuw Amerongen GP, Vermeer MA van Hinsbergh VW (2000) Role of RhoA and Rho kinase in lysophosphatidic acid-induced endothelial barrier dysfunction. Arterioscle Thromb Vasc Biol 20, E127 E133.
9. Jung C, Chylinski TM, Pimenta A, Ortiz D Shea TB (2004) Neurofilament transport is dependent on actin and myosin. J Neurosci 24, 9486 9496.
10. Clayburgh DR, Rosen S, Witkowski ED, Wang F, Blair S, Dudek S, Garcia JG, Alverdy JC Turner JR (2004) A differentiation-dependent splice variant of myosin light chain kinase, MLCK1, regulates epithelial tight junction permeability. J Biol Chem 279, 55506 55513.
11. Clayburgh DR, Shen L Turner JR (2004) A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 84, 282 291.
12. Tran QK, Watanabe H, Zhang XX, Takahashi R Ohno R (1999) Involvement of myosin light-chain kinase in chloride-sensitive Ca2+ influx in porcine aortic endothelial cells. Cardiovasc Res 44, 623 631.
13. Szaszi K, Kurashima K, Kapus A, Paulsen A, Kaibuchi K, Grinstein S Orlowski J (2000) RhoA and rho kinase regulate the epithelial Na+/H+ exchanger NHE3. Role of myosin light chain phosphorylation. J Biol Chem 275, 28599 28606.
14. Ammit AJ, Armour CL Black JL (2000) Smooth-muscle myosin light-chain kinase content is increased in human sensitized airways. Am J Respir Crit Care Med 161, 257 263.
15. Aromolaran AS, Albert AP Large WA (2000) Evidence for myosin light chain kinase mediating noradrenaline-evoked cation current in rabbit portal vein myocytes. Physiology 524, 853 863.
16. Watterson DM, Collinge M, Lukas TJ, Van Eldik LJ, Birukov KG, Stepanova OV Shirinsky VP (1995) Multiple gene products are produced from a novel protein kinase transcription region. FEBS Lett 373, 217 220.
17. Garcia JG, Lazar V, Gilbert-McClain LI, Gallagher PJ Verin A (1997) Myosin light chain kinase in endothelium: molecular cloning and regulation. Am J Respir Cell Mol Biol 16, 489 494.
18. Yang CX, Wei DM, Chen C, Yu WP Zhu MS (2005) 5DFRXXL region of long myosin light chain kinase causes F-actin bundle formation. Chin Sci Bull 50, 2044 2050.
19. Yang CX, Chen HQ, Chen C, Yu WP, Zhang WC, Peng YJ, He WQ, Wei DM, Gao X Zhu MS (2006) Microfilament-binding properties of N-terminal extension of the isoform of smooth muscle long myosin light chain kinase. Cell Res 16, 367 376.
20. Dulyaninova NG, Patskovsky YV Bresnick AR (2004) The N-terminus of the long MLCK induces a disruption in normal spindle morphology and metaphase arrest. J Cell Sci 117, 1481 1493.
21. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J Serrano L (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 22, 1302 1306.
22. Zhou W Freed CR (2004) Tyrosine-to-cysteine modification of human α-synuclein enhances protein aggregation and cellular toxicity. J Biol Chem 279, 10128 10135.
23. Frederikse PH, Garland D, Zigler JS Jr. Piatigorsky J (1996) Oxidative stress increases production of beta-amyloid precursor protein and beta-amyloid (Abeta) in mammalian lenses, and Abeta has toxic effects on lens epithelial cells. J Biol Chem 271, 10169 10174.
24. Ross CA Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10, S10 S17.
25. Milligan CE (2000) Caspase cleavage of APP results in a cytotoxic proteolytic peptide. Nat Med 6, 385 386.
26. Sugimoto M, Furuoka H Sugimoto Y (2003) Deletion of one of the duplicated HSP70 genes causes hereditary myopathy of diaphragmatic muscles in Holstein-Friesian cattle. Anim Genet 34, 192 197.
27. Clanton TL, Zuo L Klawitter P (1999) Oxidants and skeletal muscle function: physiological and pathophysiologic implications. Proc Soc Exp Biol Med 222, 253 262.
28. Graham WV, Wang F, Clayburgh DR, Cheng JX, Yoon B, Wang Y, Lin A Turner JR (2006) Tumor necrosis factor-induced long myosin light chain kinase transcription is regulated by differentiation-dependent signaling events: characterization of the human long myosin light chain kinase promoter. J Biol Chem 281, 26205 26215.
29. Petrache I, Birukov K, Zaiman AL, Crow MT, Deng H, Wadgaonkar R, Romer LH Garcia JG (2003) Caspase-dependent cleavage of myosin light chain kinase (MLCK) is involved in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis. FASEB J 17, 407 416.
30. Labeit S, Barlow DP, Gautel M, Gibson T, Holt J, Hsieh CL, Francke U, Leonard K, Wardale J Whiting AEA (1990) A regular pattern of two types of 100-residue motif in the sequence of titin. Nature 345, 273 276.
31. Einheber S Fischman DA (1990) Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily. Proc Natl Acad Sci USA 87, 2157 2161.
32. Noguchi J, Yanagisawa M, Imamura M, Kasuya Y, Sakurai T, Tanaka T Masaki T (1992) Complete primary structure and tissue expression of chicken pectoralis M-protein. J Biol Chem 267, 20302 20310.
33. Vaughan KT, Weber FE, Einheber S Fischman DA (1993) Molecular cloning of chicken myosin-binding protein (MyBP) H (86-kDa protein) reveals extensive homology with MyBP-C (C-protein) with conserved immunoglobulin C2 and fibronectin type III motifs. J Biol Chem 268, 3670 3676.
34. Salmikangas P, Mykkanen OM, Gronholm M, Heiska L, Kere J Carpen O (1999) Myotilin, a novel sarcomeric protein with two Ig-like domains, is encoded by a candidate gene for limb-girdle muscular dystrophy. Hum Mol Genet 8, 1329 1336.
35. Parast MM Otey CA (2000) Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J Cell Biol 150, 643 656.
36. Williams AF Barclay AN (1988) The immunoglobulin superfamily - domains for cell surface recognition. Annu Rev Immunol 6, 381 405.
37. Raffen R, Dieckman LJ, Szpunar M, Wunschl C, Pokkuluri PR, Dave P, Wilkins Stevens P, Cai X, Schiffer M Stevens FJ (1999) Physicochemical consequences of amino acid variations that contribute to fibril formation by immunoglobulin light chains. Protein Sci 8, 509 517.
38. McParland VJ, Kad NM, Kalverda AP, Brown A, Kirwin-Jones P, Hunter MG, Sunde M Radford SE (2000) Partially unfolded states of beta(2)-microglobulin and amyloid formation in vitro. Biochemistry 39, 8735 8746.
39. Wright CF, Teichmann SA, Clarke J Dobson CM (2005) The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438, 878 881.
40. Selkoe DJ (2003) Folding proteins in fatal ways. Nature 426, 900 904.
41. Furth PA, Hennighausen L, Baker C, Beatty B Woychick R (1991) The variability in activity of the universally expressed human cytomegalovirus immediate early gene 1 enhancer/promoter in transgenic mice. Nucleic Acids Res 19, 6205 6208.
42. Baskar JF, Smith PP, Nilaver G, Jupp RA, Hoffman S, Peffer NJ, Tenney DJ, Colberg-Poley AM, Ghazal P Nelson JA (1996) The enhancer domain of the human cytomegalovirus major immediate-early promoter determines cell type-specific expression in transgenic mice. J Virol 70, 3207 3214.
43. Poperechnaya A, Varlamova O, Lin PJ, Stull JT Bresnick AR (2000) Localization and activity of myosin light chain kinase isoforms during the cell cycle. J Cell Biol 151, 697 708.
44. Engel AG (1994) The muscle biopsy. In Myology (Engel AG Franzini-Amstrong B, eds pp. 822 831. McGraw-Hill, New York, NY.
45. Clancy JS, Takeshima H, Hamilton SL Reid MB (1999) Contractile function is unaltered in diaphragm from mice lacking calcium release channel isoform 3. Am J Physiol 277, R1205 R1209.
46. Ingalls CP, Warren GL, Williams JH, Ward CW Armstrong RB (1998) EC coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 85, 58 67.
47. Dahlstedt AJ, Katz A, Wieringa B Westerblad H (2000) Is creatine kinase responsible for fatigue? Studies of skeletal muscle deficient of creatine kinase. FASEB J 14, 982 990.
48. Watchko JF Sieck GC (1993) Respiratory muscle fatigue resistance relates to myosin phenotype and SDH activity during development. J Appl Physiol 75, 1341 1347.
49. Tonkonogi M, Walsh B, Svensson M Sahlin K (2000) Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress. J Physiol 528, 379 388.
50. Estabrook R (1967) Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol 10, 41 47.