Differential regulation of actin microfilaments by human MICAL proteins

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 614-624

  Giridharan, Sai Srinivas Panapakkam ^a   Rohn, Jennifer L ^b   Naslavsky, Naava ^a   Caplan, Steve ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Actin; Actin rich protrusions; MICAL1; MICAL2; Microfilaments; Reactive oxygen species

Indexed keywords

ACTIN; CELL PROTEIN; MOLECULE INTERACTING WITH CASL PROTEIN; MOLECULE INTERACTING WITH CASL PROTEIN 1; MOLECULE INTERACTING WITH CASL PROTEIN 2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CARCINOMA CELL; CELL STRESS; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FIBROBLAST; HUMAN; HUMAN CELL; MICROFILAMENT; NEUROBLASTOMA CELL; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AXONS; BASE SEQUENCE; CELL ADHESION MOLECULES; CELL LINE; CYTOSKELETAL PROTEINS; DNA PRIMERS; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; LIM DOMAIN PROTEINS; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SEMAPHORINS; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 84858119850     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.089367     Document Type: Article

References (33)

1. Ashida, S., Furihata, M., Katagiri, T., Tamura, K., Anazawa, Y., Yoshioka, H., Miki, T., Fujioka, T., Shuin, T., Nakamura, Y. et al. (2006). Expression of novel molecules, MICAL2-PV (MICAL2 prostate cancer variants), increases with high Gleason score and prostate cancer progression. Clin. Cancer Res. 12, 2767-2773.
2. Beuchle, D., Schwarz, H., Langegger, M., Koch, I. and Aberle, H. (2007). Drosophila MICAL regulates myofilament organization and synaptic structure. Mech. Dev. 124, 390-406.
3. Bron, R., Vermeren, M., Kokot, N., Andrews, W., Little, G. E., Mitchell, K. J. and Cohen, J. (2007). Boundary cap cells constrain spinal motor neuron somal migration at motor exit points by a semaphorin-plexin mechanism. Neural Dev. 2, 21.
4. Dalle-Donne, I., Rossi, R., Giustarini, D., Gagliano, N., Di Simplicio, P., Colombo, R. and Milzani, A. (2002). Methionine oxidation as a major cause of the functional impairment of oxidized actin. Free Radic. Biol. Med. 32, 927-937.
5. Faix, J., Breitsprecher, D., Stradal, T. E. and Rottner, K. (2009). Filopodia: complex models for simple rods. Int. J. Biochem. Cell Biol. 41, 1656-1664.
6. Fedorova, M., Kuleva, N. and Hoffmann, R. (2010). Identification of cysteine, methionine and tryptophan residues of actin oxidized in vivo during oxidative stress. J. Proteome Res. 9, 1598-1609.
7. Grigoriev, I., Yu, K. L., Martinez-Sanchez, E., Serra-Marques, A., Smal, I., Meijering, E., Demmers, J., Peranen, J., Pasterkamp, R. J., van der Sluijs, P. et al. (2011). Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr. Biol. 21, 967-974.
8. He, Z., Wang, K. C., Koprivica, V., Ming, G. and Song, H. J. (2002). Knowing how to navigate: mechanisms of semaphorin signaling in the nervous system. Sci. STKE 2002, re1.
9. Hung, R. J. and Terman, J. R. (2011). Extracellular inhibitors repellents and semaphorin/plexin/MICAL-mediated actin filament disassembly. Cytoskeleton (Hoboken) 68, 415-433.
10. Hung, R. J., Yazdani, U., Yoon, J., Wu, H., Yang, T., Gupta, N., Huang, Z., van Berkel, W. J. and Terman, J. R. (2010). Mical links semaphorins to F-actin disassembly. Nature 463, 823-827.
11. Kalil, K. and Dent, E. W. (2005). Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr. Opin. Neurobiol. 15, 521-526.
12. Kirilly, D., Gu, Y., Huang, Y., Wu, Z., Bashirullah, A., Low, B. C., Kolodkin, A. L., Wang, H. and Yu, F. (2009). A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat. Neurosci. 12, 1497-1505.
13. Kolk, S. M. and Pasterkamp, R. J. (2007). MICAL flavoprotein monooxygenases: structure, function and role in semaphorin signaling. Adv. Exp. Med. Biol. 600, 38-51.
14. Moldovan, L., Irani, K., Moldovan, N. I., Finkel, T. and Goldschmidt-Clermont, P. J. (1999). The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antioxid. Redox Signal. 1, 29-43.
15. Nadella, M., Bianchet, M. A., Gabelli, S. B., Barrila, J. and Amzel, L. M. (2005). Structure and activity of the axon guidance protein MICAL. Proc. Natl. Acad. Sci. USA 102, 16830-16835.
16. Naslavsky, N., Rahajeng, J., Sharma, M., Jovic, M. and Caplan, S. (2006). Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol. Biol. Cell 17, 163-177.
17. Nimnual, A. S., Taylor, L. J. and Bar-Sagi, D. (2003). Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5, 236-241.
18. Pak, C. W., Flynn, K. C. and Bamburg, J. R. (2008). Actin-binding proteins take the reins in growth cones. Nat. Rev. Neurosci. 9, 136-147.
19. Pasterkamp, R. J., Dai, H. N., Terman, J. R., Wahlin, K. J., Kim, B., Bregman, B. S., Popovich, P. G. and Kolodkin, A. L. (2006). MICAL flavoprotein monooxygenases: expression during neural development and following spinal cord injuries in the rat. Mol. Cell Neurosci. 31, 52-69.
20. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
21. Raper, J. A. (2000). Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10, 88-94.
22. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
23. Schmidt, E. F., Shim, S. O. and Strittmatter, S. M. (2008). Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein. J. Neurosci. 28, 2287-2297.
24. Sharma, M., Giridharan, S. S., Rahajeng, J., Naslavsky, N. and Caplan, S. (2009). MICAL-L1 links EHD1 to tubular recycling endosomes and regulates receptor recycling. Mol. Biol. Cell 20, 5181-5194.
25. Sutherland, J. D. and Witke, W. (1999). Molecular genetic approaches to understanding the actin cytoskeleton. Curr. Opin. Cell Biol. 11, 142-151.
26. Suzuki, T., Nakamoto, T., Ogawa, S., Seo, S., Matsumura, T., Tachibana, K., Morimoto, C. and Hirai, H. (2002). MICAL, a novel CasL interacting molecule, associates with vimentin. J. Biol. Chem. 277, 14933-14941.
27. Terai, T., Nishimura, N., Kanda, I., Yasui, N. and Sasaki, T. (2006). JRAB/MICALL2 is a junctional Rab13-binding protein mediating the endocytic recycling of occludin. Mol. Biol. Cell 17, 2465-2475.
28. Terman, J. R., Mao, T., Pasterkamp, R. J., Yu, H. H. and Kolodkin, A. L. (2002). MICALs, a family of conserved flavoprotein oxidoreductases, function in plexinmediated axonal repulsion. Cell 109, 887-900.
29. Weide, T., Teuber, J., Bayer, M. and Barnekow, A. (2003). MICAL-1 isoforms, novel rab1 interacting proteins. Biochem. Biophys. Res. Commun. 306, 79-86.
30. Yu, H. H., Araj, H. H., Ralls, S. A. and Kolodkin, A. L. (1998). The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 20, 207-220.
31. Zhou, Y., Adolfs, Y., Pijnappel, W. W., Fuller, S. J., van der Schors, R. C., Li, K. W., Sugden, P. H., Smit, A. B., Hergovich, A. and Pasterkamp, R. J. (2011b). MICAL-1 is a Negative Regulator of MST-NDR Kinase Signaling and Apoptosis. Mol. Cell Biol. 31, 3603-3615.
32. Zhou, Y., Gunput, R. A., Adolfs, Y. and Pasterkamp, R. J. (2011a). MICALs in control of the cytoskeleton exocytosis and cell death. Cell Mol. Life Sci. 68, 4033-4044.
33. Zucchini, D., Caprini, G., Pasterkamp, R. J., Tedeschi, G. and Vanoni, M. A. (2011). Kinetic and spectroscopic characterization of the putative monooxygenase domain of human MICAL-1. Arch. Biochem. Biophys. 515, 1-13.