The Oxygen Sensor PHD2 Controls Dendritic Spines and Synapses via Modification of Filamin A

Cell Reports

Volumn 14, Issue 11, 2016, Pages 2653-2667

  Segura, Inmaculada ^a,b   Lange, Christian ^a,b   Knevels, Ellen ^a,b   Moskalyuk, Anastasiya ^c   Pulizzi, Rocco ^c   Eelen, Guy ^a,b   Chaze, Thibault ^d   Tudor, Cicerone ^b   Boulegue, Cyril ^d   Holt, Matthew ^b   Daelemans, Dirk ^e   Matondo, Mariette ^d   Ghesquière, Bart ^b   Giugliano, Michele ^c,f,g   Ruiz de Almodovar, Carmen ^a,b,h   Dewerchin, Mieke ^a,b   Carmeliet, Peter ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d INSTITUT PASTEUR   (France)

^e REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^f Belgium   (Belgium)

^g EPFL   (Switzerland)

^h UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN PHD; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; DICARBOXYLIC AMINO ACID; EGLN1 PROTEIN, MOUSE; FILAMIN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; OXALYLGLYCINE; OXYGEN; TUBULIN; VHL PROTEIN, MOUSE; VON HIPPEL LINDAU PROTEIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DENDRITIC SPINE; HIPPOCAMPUS; HYDROXYLATION; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SYNAPSE; UBIQUITINATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; RAT; TUMOR CELL LINE; WISTAR RAT;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; CELLS, CULTURED; DENDRITIC SPINES; FILAMINS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; MICE; MICE, KNOCKOUT; OXYGEN; RATS; RATS, WISTAR; SYNAPSES; TUBULIN; UP-REGULATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84962504115     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.02.047     Document Type: Article

References (37)

1. Araya R., Jiang J., Eisenthal K.B., Yuste R. The spine neck filters membrane potentials. Proc. Natl. Acad. Sci. USA 2006, 103:17961-17966.
2. Bolduc F.V., Bell K., Rosenfelt C., Cox H., Tully T. Fragile x mental retardation 1 and filamin a interact genetically in Drosophila long-term memory. Front. Neural Circuits 2010, 3:22.
3. Brown C.E., Boyd J.D., Murphy T.H. Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. J. Cereb. Blood Flow Metab. 2010, 30:783-791.
4. Cho K.O., Hunt C.A., Kennedy M.B. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 1992, 9:929-942.
5. Corcoran A., Kunze R., Harney S.C., Breier G., Marti H.H., O'Connor J.J. A role for prolyl hydroxylase domain proteins in hippocampal synaptic plasticity. Hippocampus 2013, 23:861-872.
6. Epstein A.C., Gleadle J.M., McNeill L.A., Hewitson K.S., O'Rourke J., Mole D.R., Mukherji M., Metzen E., Wilson M.I., Dhanda A., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
7. Erecińska M., Silver I.A. Tissue oxygen tension and brain sensitivity to hypoxia. Respir. Physiol. 2001, 128:263-276.
8. Ethell I.M., Pasquale E.B. Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 2005, 75:161-205.
9. Gaillard S., Bailly Y., Benoist M., Rakitina T., Kessler J.P., Fronzaroli-Molinières L., Dargent B., Castets F. Targeting of proteins of the striatin family to dendritic spines: role of the coiled-coil domain. Traffic 2006, 7:74-84.
10. Gambazzi L., Gokce O., Seredenina T., Katsyuba E., Runne H., Markram H., Giugliano M., Luthi-Carter R. Diminished activity-dependent brain-derived neurotrophic factor expression underlies cortical neuron microcircuit hypoconnectivity resulting from exposure to mutant huntingtin fragments. J. Pharmacol. Exp. Ther. 2010, 335:13-22.
11. Hotulainen P., Hoogenraad C.C. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 2010, 189:619-629.
12. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292:464-468.
13. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., von Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
14. Mazzone M., Dettori D., Leite de Oliveira R., Loges S., Schmidt T., Jonckx B., Tian Y.M., Lanahan A.A., Pollard P., Ruiz de Almodovar C., et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009, 136:839-851.
15. Meller R., Thompson S.J., Lusardi T.A., Ordonez A.N., Ashley M.D., Jessick V., Wang W., Torrey D.J., Henshall D.C., Gafken P.R., et al. Ubiquitin proteasome-mediated synaptic reorganization: a novel mechanism underlying rapid ischemic tolerance. J. Neurosci. 2008, 28:50-59.
16. Nakamura F., Stossel T.P., Hartwig J.H. The filamins: organizers of cell structure and function. Cell Adhes. Migr. 2011, 5:160-169.
17. Nestor M.W., Cai X., Stone M.R., Bloch R.J., Thompson S.M. The actin binding domain of βI-spectrin regulates the morphological and functional dynamics of dendritic spines. PLoS ONE 2011, 6:e16197.
18. Noam Y., Phan L., McClelland S., Manders E.M., Ehrengruber M.U., Wadman W.J., Baram T.Z., Chen Y. Distinct regional and subcellular localization of the actin-binding protein filamin A in the mature rat brain. J. Comp. Neurol. 2012, 520:3013-3034.
19. Nwabuisi-Heath E., LaDu M.J., Yu C. Simultaneous analysis of dendritic spine density, morphology and excitatory glutamate receptors during neuron maturation in vitro by quantitative immunocytochemistry. J. Neurosci. Methods 2012, 207:137-147.
20. Oruganty-Das A., Ng T., Udagawa T., Goh E.L., Richter J.D. Translational control of mitochondrial energy production mediates neuron morphogenesis. Cell Metab. 2012, 16:789-800.
21. Pacary E., Haas M.A., Wildner H., Azzarelli R., Bell D.M., Abrous D.N., Guillemot F. Visualization and genetic manipulation of dendrites and spines in the mouse cerebral cortex and hippocampus using in utero electroporation. J. Vis. Exp. 2012, 26:4163.
22. Reinartz S., Biro I., Gal A., Giugliano M., Marom S. Synaptic dynamics contribute to long-term single neuron response fluctuations. Front. Neural Circuits 2014, 8:71.
23. Sarkisian M.R., Bartley C.M., Chi H., Nakamura F., Hashimoto-Torii K., Torii M., Flavell R.A., Rakic P. MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 2006, 52:789-801.
24. Segura I., Essmann C.L., Weinges S., Acker-Palmer A. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat. Neurosci. 2007, 10:301-310.
25. Song D., Li L.S., Heaton-Johnson K.J., Arsenault P.R., Master S.R., Lee F.S. Prolyl hydroxylase domain protein 2 (PHD2) binds a Pro-Xaa-Leu-Glu motif, linking it to the heat shock protein 90 pathway. J. Biol. Chem. 2013, 288:9662-9674.
26. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2001, 2:138-145.
27. Tashiro A., Yuste R. Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol. Cell. Neurosci. 2004, 26:429-440.
28. Tsuchiya H., Iseda T., Hino O. Identification of a novel protein (VBP-1) binding to the von Hippel-Lindau (VHL) tumor suppressor gene product. Cancer Res. 1996, 56:2881-2885.
29. van der Flier A., Sonnenberg A. Structural and functional aspects of filamins. Biochim. Biophys. Acta 2001, 1538:99-117.
30. Vogel S., Wottawa M., Farhat K., Zieseniss A., Schnelle M., Le-Huu S., von Ahlen M., Malz C., Camenisch G., Katschinski D.M. Prolyl hydroxylase domain (PHD) 2 affects cell migration and F-actin formation via RhoA/rho-associated kinase-dependent cofilin phosphorylation. J. Biol. Chem. 2010, 285:33756-33763.
31. Wong B.W., Kuchnio A., Bruning U., Carmeliet P. Emerging novel functions of the oxygen-sensing prolyl hydroxylase domain enzymes. Trends Biochem. Sci. 2013, 38:3-11.
32. Zhang J., Neal J., Lian G., Shi B., Ferland R.J., Sheen V. Brefeldin A-inhibited guanine exchange factor 2 regulates filamin A phosphorylation and neuronal migration. J. Neurosci. 2012, 32:12619-12629.
33. Zhang J., Neal J., Lian G., Hu J., Lu J., Sheen V. Filamin A regulates neuronal migration through brefeldin A-inhibited guanine exchange factor 2-dependent Arf1 activation. J. Neurosci. 2013, 33:15735-15746.
34. Zhang L., Bartley C.M., Gong X., Hsieh L.S., Lin T.V., Feliciano D.M., Bordey A. MEK-ERK1/2-dependent FLNA overexpression promotes abnormal dendritic patterning in tuberous sclerosis independent of mTOR. Neuron 2014, 84:78-91.
35. Zheng L., Michelson Y., Freger V., Avraham Z., Venken K.J., Bellen H.J., Justice M.J., Wides R. Drosophila Ten-m and filamin affect motor neuron growth cone guidance. PLoS ONE 2011, 6:e22956.
36. Zheng X., Zhou A.X., Rouhi P., Uramoto H., Borén J., Cao Y., Pereira T., Akyürek L.M., Poellinger L. Hypoxia-induced and calpain-dependent cleavage of filamin A regulates the hypoxic response. Proc. Natl. Acad. Sci. USA 2014, 111:2560-2565.
37. Zhou A.X., Hartwig J.H., Akyürek L.M. Filamins in cell signaling, transcription and organ development. Trends Cell Biol. 2010, 20:113-123.