MICAL-1 is a negative regulator of MST-NDR kinase signaling and apoptosis

Molecular and Cellular Biology

Volumn 31, Issue 17, 2011, Pages 3603-3615

  Zhou, Yeping ^a   Adolfs, Youri ^a   Pijnappel, W W M Pim ^b   Fuller, Stephen J ^c   Van der Schors, Roel C ^d   Li, Ka Wan ^d   Sugden, Peter H ^c   Smit, August B ^d   Hergovich, Alexander ^e   Pasterkamp, R Jeroen ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF READING   (United Kingdom)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN STE 20 LIKE KINASE; MOLECULE INTERACTING WITH CASL 1; NUCLEAR DBF2 RELATED KINASE 1; NUCLEAR DBF2 RELATED KINASE 2; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYDROPHOBICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; L CELLS (CELL LINE); MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MIXED FUNCTION OXYGENASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

MAMMALIA; MUS;

EID: 80052277450     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01389-10     Document Type: Article

References (46)

1. Ben-Zvi, A., et al. 2008. The Semaphorin receptor PlexinA3 mediates neuronal apoptosis during dorsal root ganglia development. J. Neurosci. 28:12427-12432.
2. Beuchle, D., H. Schwarz, M. Langegger, I. Koch, and H. Aberle. 2007. Drosophila MICAL regulates myofilament organization and synaptic structure. Mech. Dev. 124:390-406.
3. Bichsel, S. J., R. Tamaskovic, M. R. Stegert, and B. A. Hemmings. 2004. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J. Biol. Chem. 279:35228-35235.
4. Cornils, H., et al. 2010. Ablation of the kinase NDR1 predisposes mice to the development of T cell lymphoma. Sci. Signal. 3:ra47.
5. Emoto, K., et al. 2004. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons. Cell 119:245-256.
6. Emoto, K., J. Z. Parrish, L. Y. Jan, and Y. N. Jan. 2006. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443:210-213.
7. Franco, M., and L. Tamagnone. 2008. Tyrosine phosphorylation in semaphorin signalling: shifting into overdrive. EMBO Rep. 9:865-871.
8. Fuller, S. J., et al. 2008. Nuclear Dbf2-related protein kinases (NDRs) in isolated cardiac myocytes and the myocardium: activation by cellular stresses and by phosphoprotein serine-/threonine-phosphatase inhibitors. Cell Signal. 20:1564-1577.
9. Gallegos, M. E., and C. I. Bargmann. 2004. Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 44:239-249.
10. Hergovich, A., S. J. Bichsel, and B. A. Hemmings. 2005. Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. Mol. Cell. Biol. 25:8259-8272.
11. Hergovich, A., et al. 2009. The MST1 and hMOB1 tumor suppressors control human centrosome duplication by regulating NDR kinase phosphorylation. Curr. Biol. 19:1692-1702.
12. Hergovich, A., M. R. Stegert, D. Schmitz, and B. A. Hemmings. 2006. NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 7:253-264.
13. Hung, R. J., et al. 2010. Mical links semaphorins to F-actin disassembly. Nature 463:823-827.
14. Irwin, N., Y. M. Li, J. E. O'Toole, and L. I. Benowitz. 2006. Mst3b, a purine-sensitive Ste20-like protein kinase, regulates axon outgrowth. Proc. Natl. Acad. Sci. U. S. A. 103:18320-18325.
15. Kirilly, D., et al. 2009. A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat. Neurosci. 12:1497-1505.
16. Kohler, R. S., D. Schmitz, H. Cornils, B. A. Hemmings, and A. Hergovich.2010. Differential NDR/LATS interactions with the human MOB family reveal a negative role for human MOB2 in the regulation of human NDR kinases. Mol. Cell. Biol. 30:4507-4520.
17. Kolk, S. M., et al. 2009. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J. Neurosci. 29:12542-12557.
18. Kolk, S. M., and R. J. Pasterkamp. 2007. MICAL flavoprotein monooxygenases: structure, function and role in semaphorin signaling. Adv. Exp. Med. Biol. 600:38-51.
19. Kubo, A., S. Itoh, K. Itoh, and T. Kamataki. 1997. Determination of FAD-binding domain in flavin-containing monooxygenase 1 (FMO1). Arch. Biochem. Biophys. 345:271-277.
20. Lahiry, P., A. Torkamani, N. J. Schork, and R. A. Hegele. 2010. Kinase mutations in human disease: interpreting genotype-phenotype relationships. Nat. Rev. Genet. 11:60-74.
21. Lawton, M. P., and R. M. Philpot. 1993. Functional characterization of flavin-containing monooxygenase 1B1 expressed in Saccharomyces cerevisiae and Escherichia coli and analysis of proposed FAD- and membrane-binding domains. J. Biol. Chem. 268:5728-5734.
22. Li, K. W., et al. 2007. Quantitative proteomics and protein network analysis of hippocampal synapses of CaMKIIalpha mutant mice. J. Proteome Res. 6:3127-3133.
23. Millward, T. A., D. Hess, and B. A. Hemmings. 1999. Ndr protein kinase is regulated by phosphorylation on two conserved sequence motifs. J. Biol. Chem. 274:33847-33850.
24. Moretti, S., et al. 2008. Semaphorin3A signaling controls Fas (CD95)-mediated apoptosis by promoting Fas translocation into lipid rafts. Blood 111:2290-2299.
25. Nadella, M., M. A. Bianchet, S. B. Gabelli, J. Barrila, and L. M. Amzel. 2005. Structure and activity of the axon guidance protein MICAL. Proc. Natl. Acad. Sci. U. S. A. 102:16830-16835.
26. Pasterkamp, R. J., et al. 2006. MICAL flavoprotein monooxygenases: expression during neural development and following spinal cord injuries in the rat. Mol. Cell Neurosci. 31:52-69.
27. Pasterkamp, R. J., and R. J. Giger. 2009. Semaphorin function in neural plasticity and disease. Curr. Opin. Neurobiol. 19:263-274.
28. Schmidt, E. F., S. O. Shim, and S. M. Strittmatter. 2008. Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein. J. Neurosci. 28:2287-2297.
29. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
30. Siebold, C., et al. 2005. High-resolution structure of the catalytic region of MICAL (molecule interacting with CasL), a multidomain flavoenzyme-signaling molecule. Proc. Natl. Acad. Sci. U. S. A. 102:16836-16841.
31. Song, H., et al. 2010. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc. Natl. Acad. Sci. U. S. A. 107:1431-1436.
32. Stegert, M. R., A. Hergovich, R. Tamaskovic, S. J. Bichsel, and B. A. Hemmings. 2005. Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol. Cell. Biol. 25:11019-11029.
33. Stegert, M. R., R. Tamaskovic, S. J. Bichsel, A. Hergovich, and B. A. Hemmings. 2004. Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calcium-binding protein. J. Biol. Chem. 279:23806-23812.
34. Stork, O., et al. 2004. Neuronal functions of the novel serine/threonine kinase Ndr2. J. Biol. Chem. 279:45773-45781.
35. Stossel, T. P. 2010. Filamins and the potential of complexity. Cell Cycle 9:1463.
36. Suto, F., et al. 2005. Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neurosci. 25:3628-3637.
37. Suzuki, T., et al. 2002. MICAL, a novel CasL interacting molecule, associates with vimentin. J. Biol. Chem. 277:14933-14941.
38. Tamaskovic, R., S. J. Bichsel, H. Rogniaux, M. R. Stegert, and B. A. Hemmings. 2003. Mechanism of Ca2 -mediated regulation of NDR protein kinase through autophosphorylation and phosphorylation by an upstream kinase. J. Biol. Chem. 278:6710-6718.
39. Terman, J. R., T. Mao, R. J. Pasterkamp, H. H. Yu, and A. L. Kolodkin. 2002. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109:887-900.
40. Vichalkovski, A., et al. 2008. NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 18:1889-1895.
41. Weide, T., J. Teuber, M. Bayer, and A. Barnekow. 2003. MICAL-1 isoforms, novel rab1 interacting proteins. Biochem. Biophys. Res. Commun. 306:79-86.
42. Weirich, C. S., J. P. Erzberger, and Y. Barral. 2008. The septin family of GTPases: architecture and dynamics. Nat. Rev. Mol. Cell Biol. 9:478-489.
43. Wessel, D., and U. I. Flugge. 1984. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138:141-143.
44. Wierenga, R. K., P. Terpstra, and W. G. Hol. 1986. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:101-107.
45. Zhao, B., L. Li, Q. Lei, and K. L. Guan. 2010. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24:862-874.
46. Zhou, Y., R. A. Gunput, and R. J. Pasterkamp. 2008. Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci. 33:161-170.