The extracellular signal-regulated kinase 3 (mitogen-activated protein kinase 6 [mapk6])-mapk-activated protein kinase 5 signaling complex regulates septin function and dendrite morphology

Molecular and Cellular Biology

Volumn 32, Issue 13, 2012, Pages 2467-2478

  Brand, Frank ^a   Schumacher, Stefanie ^a   Kant, Shashi ^a,b   Menon, Manoj B ^a   Simon, Ruth ^c   Turgeon, Benjamin ^d,e   Britsch, Stefan ^c   Meloche, Sylvain ^d,e   Gaestel, Matthias ^a   Kotlyarov, Alexey ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ULM   (Germany)

^d INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; KALIRIN 7; MITOGEN ACTIVATED PROTEIN KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 5; PROTEIN SERINE THREONINE KINASE; REGULATOR PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SEPTIN; TERNARY COMPLEX FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; ENZYME ACTIVATION; ENZYME SUBSTRATE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; DENDRITES; DNA PRIMERS; GTP-BINDING PROTEIN REGULATORS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HELA CELLS; HIPPOCAMPUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 6; MODELS, NEUROLOGICAL; MULTIPROTEIN COMPLEXES; NEUROGENESIS; NEURONS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SEPTINS; TRANSFECTION;

MUS;

EID: 84864001546     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06633-11     Document Type: Article

References (59)

1. Aberg E, et al. 2006. Regulation of MAPK-activated protein kinase 5 activity and subcellular localization by the atypical MAPK ERK4/MAPK4. J. Biol. Chem. 281:35499 -35510.
2. Aberg E, et al. 2009. Docking of PRAK/MK5 to the atypical MAPKs ERK3 and ERK4 defines a novel MAPK interaction motif. J. Biol. Chem. 284: 19392-19401.
3. Barral Y. 2010. Cell biology. Septins at the nexus. Science 329:1289 -1290.
4. Barral Y, Mansuy IM. 2007. Septins: cellular and functional barriers of neuronal activity. Curr. Biol. 17:R961-R963.
5. Broder YC, Katz S, Aronheim A. 1998. The ras recruitment system, a novel approach to the study of protein-protein interactions. Curr. Biol. 8:1121-1124.
6. Cheng M, et al. 1996. Characterization of a protein kinase that phosphorylates serine 189 of the mitogen-activated protein kinase homolog ERK3. J. Biol. Chem. 271:12057-12062.
7. Coulombe P, Meloche S. 2007. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim. Biophys. Acta 1773: 1376-1387.
8. De la Mota-Peynado A, Chernoff J, Beeser A. 2011. Identification of the atypical MAPK Erk3 as a novel substrate for p21-activated kinase (Pak) activity. J. Biol. Chem. 286:13603-13611.
9. Deleris P, et al. 2008. Activation loop phosphorylation of the atypical MAP kinases ERK3 and ERK4 is required for binding, activation and cytoplasmic relocalization of MK5. J. Cell. Physiol. 217:778 -788.
10. Deleris P, et al. 2011. Activation loop phosphorylation of ERK3/ERK4 by group I p21-activated kinases (PAKs) defines a novel PAK-ERK3/4-MAPK-activated protein kinase 5 signaling pathway. J. Biol. Chem. 286: 6470-6478.
11. Dobbelaere J, Gentry MS, Hallberg RL, Barral Y. 2003. Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev. Cell 4:345-357.
12. Feng G, et al. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
13. Gerits N, Van Belle W, Moens U. 2007. Transgenic mice expressing constitutive active MAPKAPK5 display gender-dependent differences in exploration and activity. Behav. Brain Funct. 3:58.
14. Gnad F, Gunawardena J, Mann M. 2011. PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 39:D253-D260. doi: 10.1093/nar/gkq1159.
15. Gonzalez FA, Raden DL, Rigby MR, Davis RJ. 1992. Heterogeneous expression of four MAP kinase isoforms in human tissues. FEBS Lett. 304:170 -178.
16. Hansen CA, Bartek J, Jensen S. 2008. A functional link between the human cell cycle-regulatory phosphatase Cdc14A and the atypical mitogen-activated kinase Erk3. Cell Cycle 7:325-334.
17. Heimrich B, Frotscher M. 1991. Differentiation of dentate granule cells in slice cultures of rat hippocampus: a Golgi/electron microscopic study. Brain Res. 538:263-268.
18. Joberty G, et al. 2001. Borg proteins control septin organization and are negatively regulated by Cdc42. Nat. Cell Biol. 3:861- 866.
19. Kant S, et al. 2006. Characterization of the atypical MAPK ERK4 and its activation of the MAPK-activated protein kinase MK5. J. Biol. Chem. 281:35511-35519.
20. Kim SK, et al. 2010. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329:1337-1340.
21. Kinoshita M. 2003. Assembly of mammalian septins. J. Biochem. 134: 491-496.
22. Kinoshita M. 2006. Diversity of septin scaffolds. Curr. Opin. Cell Biol. 18:54-60.
23. Kinoshita, M. 2003. The septins. Genome Biol. 4:236.
24. Kiraly DD, et al. 2011. Identification of kalirin-7 as a potential postsynaptic density signaling hub. J. Proteome Res. 10:2828 -2841.
25. Klinger S, et al. 2009. Loss of Erk3 function in mice leads to intrauterine growth restriction, pulmonary immaturity, and neonatal lethality. Proc. Natl. Acad. Sci. U. S. A. 106:16710 -16715.
26. Kress TR, et al. 2011. The MK5/PRAK kinase and Myc form a negative feedback loop that is disrupted during colorectal tumorigenesis. Mol. Cell 41:445- 457.
27. Lein ES, et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168 -176.
28. Liao D, Scannevin RH, Huganir R. 2001. Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J. Neurosci. 21:6008-6017.
29. Lippincott-Schwartz J, Snapp E, Kenworthy A. 2001. Studying protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 2:444-456.
30. Ma XM, et al. 2008. Kalirin-7 is required for synaptic structure and function. J. Neurosci. 28:12368 -12382.
31. Martinez C, et al. 2004. Mammalian septin function in hemostasis and beyond. Exp. Biol. Med. 229:1111-1119.
32. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681- 683.
33. Mostowy S, Cossart P. 2012. Septins: the fourth component of the cytoskeleton. Nat. Rev. Mol. Cell Biol. 13:183-194.
34. New L, Jiang Y, Han J. 2003. Regulation of PRAK subcellular location by p38 MAP kinases. Mol. Biol. Cell 14:2603-2616.
35. Peng J, et al. 2004. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 279: 21003-21011.
36. Penzes P, et al. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
37. Perander M, et al. 2008. The serine 186 phospho-acceptor site within ERK4 is essential for its ability to interact with and activate PRAK/MK5. Biochem. J. 411:613- 622.
38. Rousseau J, et al. 2010. Targeted inactivation of Mapk4 in mice reveals specific nonredundant functions of Erk3/Erk4 subfamily mitogenactivated protein kinases. Mol. Cell. Biol. 30:5752-5763.
39. Sandrock K, et al. 2011. Characterization of human septin interactions. Biol. Chem. 392:751-761.
40. Schiller MR, et al. 2006. Regulation of RhoGEF activity by intramolecular and intermolecular SH3 domain interactions. J. Biol. Chem. 281:18774- 18786.
41. Schumacher S, et al. 2004. Scaffolding by ERK3 regulates MK5 in development. EMBO J. 23:4770-4779.
42. Seternes OM, et al. 2004. Activation of MK5/PRAK by the atypical MAP kinase ERK3 defines a novel signal transduction pathway. EMBO J. 23: 4780-4791.
43. Sheffield PJ, et al. 2003. Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments. J. Biol. Chem. 278:3483-3488.
44. Shi Y, et al. 2003. Elimination of protein kinase MK5/PRAK activity by targeted homologous recombination. Mol. Cell. Biol. 23:7732-7741.
45. Shiryaev A, Dumitriu G, Moens U. 2011. Distinct roles of MK2 and MK5 in cAMP/PKA- and stress/p38MAPK-induced heat shock protein 27 phosphorylation. J. Mol. Signal. 6:4.
46. Shiryaev A, Moens U. 2010. Mitogen-activated protein kinase p38 and MK2, MK3 and MK5: menage a trois or menage a quatre? Cell. Signal. 22:1185-1192.
47. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87:387- 406. 47a.
48. Sirajuddin M, et al. 2007. Structural insight into filament formation by mammalian septins. Nature 449:311-315.
49. Spiliotis ET, Kinoshita M, Nelson WJ. 2005. A mitotic septin scaffold required for mammalian chromosome congression and segregation. Science 307:1781-1785.
50. Spiliotis ET, Nelson WJ. 2006. Here come the septins: novel polymers that coordinate intracellular functions and organization. J. Cell Sci. 119: 4-10.
51. Sun P, et al. 2007. PRAK is essential for ras-induced senescence and tumor suppression. Cell 128:295-308.
52. Tada T, et al. 2007. Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr. Biol. 17:1752-1758.
53. Turgeon B, Meloche S. 2009. Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases. Physiol. Rev. 89:1-26.
54. Unger T, Jacobovitch Y, Dantes A, Bernheim R, Peleg Y. 2010. Applications of the restriction free (RF) cloning procedure for molecular manipulations and protein expression. J. Struct. Biol. 172:34-44.
55. Vrabioiu AM, Mitchison TJ. 2006. Structural insights into yeast septin organization from polarized fluorescence microscopy. Nature 443:466- 469.
56. Xie Y, et al. 2007. The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr. Biol. 17:1746- 1751.
57. Xie Z, et al. 2007. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640-656.
58. Zheng M, et al. 2011. Inactivation of Rheb by PRAK-mediated phosphorylation is essential for energy-depletion-induced suppression of mTORC1. Nat. Cell Biol. 13:263-272.
59. Zhu AX, Zhao Y, Moller DE, Flier JS. 1994. Cloning and characterization of p97MAPK, a novel human homolog of rat ERK-3. Mol. Cell. Biol. 14:8202- 8211.