Selr Reverses Mical-Mediated Oxidation of Actin to Regulate F-Actin Dynamics

Nature Cell Biology

Volumn 15, Issue 12, 2013, Pages 1445-1454

  Hung, Ruei Jiun ^a   Spaeth, Christopher S ^a   Yesilyurt, Hunkar Gizem ^a   Terman, Jonathan R ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; METHIONINE SULFOXIDE REDUCTASE; MICAL PROTEIN, DROSOPHILA; SELR PROTEIN, DROSOPHILA;

3T3 CELL LINE; ANIMAL; CHEMISTRY; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; MALE; METABOLISM; MOUSE; NERVE FIBER; OXIDATION REDUCTION REACTION; PHENOTYPE; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; ARTICLE; CELL STRAIN 3T3;

3T3 CELLS; ACTINS; ANIMALS; AXONS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; METHIONINE SULFOXIDE REDUCTASES; MICE; OXIDATION-REDUCTION; PHENOTYPE; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 84893385313     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2871     Document Type: Article

References (84)

1. Pollard, T. D. & Cooper, J. A. Actin, a central player in cell shape and movement. Science 326, 1208–1212 (2009).
2. Fletcher, D. A. & Mullins, R. D. Cell mechanics and the cytoskeleton. Nature 463, 485–492 (2010).
3. Terman, J. R. & Kashina, A. Post-translational modification and regulation of actin. Curr. Opin. Cell Biol. 25, 30–38 (2013).
4. Hung, R. J., Pak, C. W. & Terman, J. R. Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334, 1710–1713 (2011).
5. Hung, R. J. et al. Mical links semaphorins to F-actin disassembly. Nature 463, 823–827 (2010).
6. Hung, R. J. & Terman, J. R. Extracellular inhibitors, repellents, and semaphorin/ plexin/MICAL-mediated actin filament disassembly. Cytoskeleton 68, 415–433 (2011).
7. Zhou, Y., Gunput, R. A., Adolfs, Y. & Pasterkamp, R. J. MICALs in control of the cytoskeleton, exocytosis, and cell death. Cell Mol. Life Sci. 68, 4033–4044 (2011).
8. Caplan, S. & Giridharan, S. S. MICAL-family proteins: complex regulators of the actin cytoskeleton. Antioxid. Redox Signal. http://dx.doi.org/10.1089/ars.2013. 5487 (2013).
9. Vanoni, M. A., Vitali, T. & Zucchini, D. MICAL, the flavoenzyme participating in cytoskeleton dynamics. Int. J. Mol. Sci. 14, 6920–6959 (2013).
10. Beuchle, D., Schwarz, H., Langegger, M., Koch, I. & Aberle, H. Drosophila MICAL regulates myofilament organization and synaptic structure. Mech. Dev. 124, 390–406 (2007).
11. Giridharan, S. S., Rohn, J. L., Naslavsky, N. & Caplan, S. Differential regulation of actin microfilaments by human MICAL proteins. J. Cell Sci. 125, 614–624 (2012).
12. Morinaka, A. et al. Thioredoxin mediates oxidation-dependent phosphorylation of CRMP2 and growth cone collapse. Sci. Signal. 4, ra26 (2011).
13. Terman, J. R., Mao, T., Pasterkamp, R. J., Yu, H. H. & Kolodkin, A. L. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109, 887–900 (2002).
14. Kolodkin, A. L. et al. Fasciclin IV: sequence, expression, and function during growth cone guidance in the grasshopper embryo. Neuron 9, 831–835 (1992).
15. Kolodkin, A. L. & Tessier-Lavigne, M. Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3, a001727 (2011).
16. Luo, Y., Raible, D. & Raper, J. A. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217–227 (1993).
17. Schmidt, E. F., Shim, S. O. & Strittmatter, S. M. Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein. J. Neurosci. 28, 2287–2297 (2008).
18. Gillespie, P. G. & Walker, R. G. Molecular basis of mechanosensory transduction. Nature 413, 194–202 (2001).
19. Gillespie, P. G. & Muller, U. Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139, 33–44 (2009).
20. Tilney, L. G. & DeRosier, D. J. How to make a curved Drosophila bristle using straight actin bundles. Proc. Natl Acad. Sci. USA 102, 18785–18792 (2005).
21. Sutherland, J. D. & Witke, W. Molecular genetic approaches to understanding the actin cytoskeleton. Curr. Opin. Cell Biol. 11, 142–151 (1999).
22. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).
23. Kryukov, G. V., Kumar, R. A., Koc, A., Sun, Z. & Gladyshev, V. N. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc. Natl Acad. Sci. USA 99, 4245–4250 (2002).
24. Kim, H. Y. & Gladyshev, V. N. Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem. J. 407, 321–329 (2007).
25. Kumar, R. A., Koc, A., Cerny, R. L. & Gladyshev, V. N. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J. Biol. Chem. 277, 37527–37535 (2002).
26. Lundblad, R. L. Chemical Reagents for Protein Modification 3rd edn 205–211 (CRC Press, 2005).
27. Lee, B. C. & Gladyshev, V. N. The biological significance of methionine sulfoxide stereochemistry. Free Radic. Biol. Med. 50, 221–227 (2011).
28. Graveley, B. R. et al. The developmental transcriptome of Drosophila melanogaster. Nature 471, 473–479 (2011).
29. Robinson, S. W., Herzyk, P., Dow, J. A. & Leader, D. P. FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Res. 41, D744-750 (2013).
30. Cherbas, L. et al. The transcriptional diversity of 25 Drosophila cell lines. Genome Res. 21, 301–314 (2011).
31. Knowles-Barley, S., Longair, M. & Armstrong, J. D. BrainTrap: a database of 3D protein expression patterns in the Drosophila brain. Database (Oxford) 2010, baq005 (2010).
32. Tran, T. S., Kolodkin, A. L. & Bharadwaj, R. Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 23, 263–292 (2007).
33. Dent, E. W., Gupton, S. L. & Gertler, F. B. The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3, a001800 (2011).
34. Kraut, R., Menon, K. & Zinn, K. A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. Curr. Biol. 11, 417–430 (2001).
35. Winberg, M. L. et al. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95, 903–916 (1998).
36. Ayoob, J. C., Yu, H. H., Terman, J. R. & Kolodkin, A. L. The Drosophila receptor guanylyl cyclase Gyc76C is required for semaphorin-1a-plexin A-mediated axonal repulsion. J. Neurosci. 24, 6639–6649 (2004).
37. Yang, T. & Terman, J. R. 14-3-3epsilon couples protein kinase A to semaphorin signaling and silences plexin RasGAP-mediated axonal repulsion. Neuron 74, 108–121 (2012).
38. Stadtman, E. R., Moskovitz, J. & Levine, R. L. Oxidation of methionine residues of proteins: biological consequences. Antioxid. Redox Signal. 5, 577–582 (2003).
39. Laing, N. G. et al. Mutations and polymorphisms of the skeletal muscle alpha-actin gene (ACTA1). Hum. Mutat. 30, 1267–1277 (2009).
40. Sheterline, P., Clayton, J. & Sparrow, J. C. Actin 4th edn (Oxford Univ. Press, 1998).
41. Dominguez, R. & Holmes, K. C. Actin structure and function. Annu. Rev. Biophys. 40, 169–186 (2011).
42. Shacter, E. Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 32, 307–326 (2000).
43. Walsh, C. T. Posttranslational Modification of Proteins. Expanding Nature’s Inventory (Roberts Company, 2006).
44. Lee, B. C. et al. MsrB1 and MICALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Mol. Cell 51, 397–404 (2013).
45. Yu, H. H., Araj, H. H., Ralls, S. A. & Kolodkin, A. L. The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 20, 207–220 (1998).
46. He, H., Yang, T., Terman, J. R. & Zhang, X. Crystal structure of the plexin A3 intracellular region reveals an autoinhibited conformation through active site sequestration. Proc. Natl Acad. Sci. USA 106, 15610–15615 (2009).
47. Tilney, L. G. et al. The role actin filaments play in providing the characteristic curved form of Drosophila bristles. Mol. Biol. Cell 15, 5481–5491 (2004).
48. Tilney, L. G., Connelly, P. S., Ruggiero, L., Vranich, K. A. & Guild, G. M. Actin filament turnover regulated by cross-linking accounts for the size, shape, location, and number of actin bundles in Drosophila bristles. Mol. Biol. Cell 14, 3953–3966 (2003).
49. Guild, G. M., Connelly, P. S., Ruggiero, L., Vranich, K. A. & Tilney, L. G. Long continuous actin bundles in Drosophila bristles are constructed by overlapping short filaments. J. Cell Biol. 162, 1069–1077 (2003).
50. De la Cova, C., Abril, M., Bellosta, P., Gallant, P. & Johnston, L. A. Drosophila myc regulates organ size by inducing cell competition. Cell 117, 107–116 (2004).
51. Hopmann, R. & Miller, K. G. A balance of capping protein and profilin functions is required to regulate actin polymerization in Drosophila bristle. Mol. Biol. Cell 14, 118–128 (2003).
52. Tilney, L. G., Connelly, P., Smith, S. & Guild, G. M. F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J. Cell Biol. 135, 1291–1308 (1996).
53. Grimaud, R. et al. Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J. Biol. Chem. 276, 48915–48920 (2001).
54. Cooper, J. A. The Cytoskeleton: A Practical Approach 47–71 (The Pratical Approach Series, Oxford Univ. Press, 1992).
55. Moskovitz, J., Weissbach, H. & Brot, N. Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc. Natl Acad. Sci. USA 93, 2095–2099 (1996).
56. Arner, E. S., Zhong, L. & Holmgren, A. Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol. 300, 226–239 (1999).
57. Bergen, H. R. 3rd, Ajtai, K., Burghardt, T. P., Nepomuceno, A. I. & Muddiman, D. C. Mass spectral determination of skeletal/cardiac actin isoform ratios in cardiac muscle. Rapid Commun. Mass Spectrom. 17, 1467–1471 (2003).
58. Van Vactor, D., Sink, H., Fambrough, D., Tsoo, R. & Goodman, C. S. Genes that control neuromuscular specificity in Drosophila. Cell 73, 1137–1153 (1993).
59. Budnik, V., Gorczyca, M. & Prokop, A. Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int. Rev. Neurobiol. 75, 323–365 (2006).
60. Kisiel, M., Majumdar, D., Campbell, S. & Stewart, B. A. Myosin VI contributes to synaptic transmission and development at the Drosophila neuromuscular junction. BMC Neurosci. 12, 65–65 (2011).
61. Parks, A. L. et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288–292 (2004).
62. Hung, R.J. et al. Mical links semaphorins to F-actin disassembly. Nature 463, 823-827 (2010).
63. Takahashi, T. et al. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99, 59-69 (1999).
64. He, H., Yang, T., Terman, J.R. & Zhang, X. Crystal structure of the plexin A3 intracellular region reveals an autoinhibited conformation through active site sequestration. Proc Natl Acad Sci U S A 106, 15610-15615 (2009).
65. Yu, L., Zhou, Y., Cheng, S. & Rao, Y. Plexin a-semaphorin-1a reverse signaling regulates photoreceptor axon guidance in Drosophila. J Neurosci 30, 12151-12156 (2010).
66. Kryukov, G.V., Kumar, R.A., Koc, A., Sun, Z. & Gladyshev, V.N. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci U S A 99, 4245-4250 (2002).
67. Kumar, R.A., Koc, A., Cerny, R.L. & Gladyshev, V.N. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-Rsulfoxide reductase. J Biol Chem 277, 37527-37535 (2002).
68. Kim, H.Y. & Gladyshev, V.N. Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem J 407, 321-329 (2007).
69. Lassing, I. et al. Molecular and structural basis for redox regulation of beta-actin. J Mol Biol 370, 331-348 (2007).
70. Thom, S.R., Bhopale, V.M., Milovanova, T.N., Yang, M. & Bogush, M. Thioredoxin reductase linked to cytoskeleton by focal adhesion kinase reverses actin S-nitrosylation and restores neutrophil beta(2) integrin function. J Biol Chem 287, 30346-30357 (2012).
71. Wang, X. et al. Redox regulation of actin by thioredoxin-1 is mediated by the interaction of the proteins via cysteine 62. Antioxid Redox Signal 13, 565-573 (2010).
72. Morinaka, A. et al. Thioredoxin Mediates Oxidation-Dependent Phosphorylation of CRMP2 and Growth Cone Collapse. Sci Signal 4, ra26 (2011).
73. Kim, H.Y. Glutaredoxin serves as a reductant for methionine sulfoxide reductases with or without resolving cysteine. Acta Biochim Biophys Sin (Shanghai) 44, 623-627 (2012).
74. Sagher, D. et al. Thionein can serve as a reducing agent for the methionine sulfoxide reductases. Proc Natl Acad Sci U S A 103, 8656-8661 (2006).
75. Hung, R.J., Pak, C.W. & Terman, J.R. Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334, 1710-1713 (2011).
76. Hung, R.J. & Terman, J.R. Extracellular inhibitors, repellents, and semaphorin/plexin/MICAL-mediated actin filament disassembly. Cytoskeleton (Hoboken) 68, 415-433 (2011).
77. Terman, J.R. & Kashina, A. Post-translational modification and regulation of actin. Curr Opin Cell Biol 25, 30-38 (2013).
78. Beuchle, D., Schwarz, H., Langegger, M., Koch, I. & Aberle, H. Drosophila MICAL regulates myofilament organization and synaptic structure. Mech Dev 124, 390-406 (2007).
79. Knowles-Barley, S., Longair, M. & Armstrong, J.D. BrainTrap: a database of 3D protein expression patterns in the Drosophila brain. Database (Oxford) 2010, baq005 (2010).
80. Terman, J.R., Mao, T., Pasterkamp, R.J., Yu, H.H. & Kolodkin, A.L. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexinmediated axonal repulsion. Cell 109, 887-900 (2002).
81. Parks, A.L. et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36, 288-292 (2004).
82. Yu, H.H., Araj, H.H., Ralls, S.A. & Kolodkin, A.L. The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 20, 207-220. (1998).
83. Winberg, M.L. et al. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95, 903-916 (1998).
84. Yang, T. & Terman, J.R. 14-3-3epsilon couples protein kinase A to semaphorin signaling and silences plexin RasGAP-mediated axonal repulsion. Neuron 74, 108-121 (2012).