PP2A regulatory subunit Bα controls endothelial contractility and vessel lumen integrity via regulation of HDAC7

EMBO Journal

Volumn 32, Issue 18, 2013, Pages 2491-2503

  Martin, Maud ^a   Geudens, Ilse ^b,c   Bruyr, Jonathan ^a   Potente, Michael ^d,e   Bleuart, Anouk ^a   Lebrun, Marielle ^a   Simonis, Nicolas ^f   Deroanne, Christophe ^a   Twizere, Jean Claude ^a   Soubeyran, Philippe ^g   Peixoto, Paul ^a   Mottet, Denis ^a   Janssens, Veerle ^h   Hofmann, Wolf Karsten ⁱ   Claes, Filip ^c   Carmeliet, Peter ^b,c   Kettmann, Richard ^a   Gerhardt, Holger ^b,c,j   Dequiedt, Franck ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^e GOETHE UNIVERSITY   (Germany)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^g AIX MARSEILLE UNIVERSITY   (France)

^h LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

ⁱ UNIVERSITY OF HEIDELBERG   (Germany)

^j IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

more..

Author keywords

Angiogenesis; Cytoskeleton; HDAC; Lumen maintenance; Phosphatase

Indexed keywords

ADAPTOR PROTEIN; HISTONE DEACETYLASE 7; HOLOENZYME; MYOSIN ADENOSINE TRIPHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A B ALPHA; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; ZEBRA FISH;

ANIMALS; CELL ADHESION; COLLAGEN; DRUG COMBINATIONS; ENDOTHELIUM, VASCULAR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HOMEODOMAIN PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LAMININ; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN PHOSPHATASE 2; PROTEOGLYCANS; RNA, SMALL INTERFERING; VASCULAR PATENCY; ZEBRAFISH;

DANIO RERIO;

EID: 84884282084     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.187     Document Type: Article

References (72)

1. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478
2. Bayless KJ, Davis GE (2004) Microtubule depolymerization rapidly collapses capillary tube networks in vitro and angiogenic vessels in vivo through the small GTPase Rho. J Biol Chem 279: 11686-11695
3. Bayless KJ, Johnson GA (2011) Role of the cytoskeleton in formation and maintenance of angiogenic sprouts. J Vasc Res 48: 369-385
4. Bengtsson L, Schwappacher R, Roth M, Boergermann JH, Hassel S, Knaus P (2009) PP2A regulates BMP signalling by interacting with BMP receptor complexes and by dephosphorylating both the C-terminus and the linker region of Smad1. J Cell Sci 122: 1248-1257
5. Bershadsky A, Chausovsky A, Becker E, Lyubimova A, Geiger B (1996) Involvement of microtubules in the control of adhesiondependent signal transduction. Curr Biol 6: 1279-1289
6. Bi W, Drake CJ, Schwarz JJ (1999) The transcription factor MEF2Cnull mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev Biol 211: 255-267
7. Blum Y, Belting HG, Ellertsdottir E, Herwig L, Luders F, Affolter M (2008) Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev Biol 316: 312-322
8. Brownlee CW, Klebba JE, Buster DW, Rogers GC (2011) The Protein Phosphatase 2A regulatory subunit Twins stabilizes Plk4 to induce centriole amplification. J Cell Biol 195: 231-243
9. Burridge K, Chrzanowska-Wodnicka M, Zhong C (1997) Focal adhesion assembly. Trends in cell biology 7: 342-347
10. Cestra G, Toomre D, Chang S, De Camilli P (2005) The Abl/Arg substrate ArgBP2/nArgBP2 coordinates the function of multiple regulatory mechanisms converging on the actin cytoskeleton. Proc Natl Acad Sci USA 102: 1731-1736
11. Chan LY, Amon A (2009) The protein phosphatase 2A functions in the spindle position checkpoint by regulating the checkpoint kinase Kin4. Genes Dev 23: 1639-1649
12. Chang JH, Gill S, Settleman J, Parsons SJ (1995) c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation. J Cell Biol 130: 355-368
13. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN (2006) Histone Deacetylase 7 Maintains Vascular Integrity by Repressing Matrix Metalloproteinase 10. Cell 126: 321-334
14. Deakin NO, Turner CE (2008) Paxillin comes of age. J Cell Sci 121: 2435-2444
15. Foley EA, Maldonado M, Kapoor TM (2011) Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat Cell Biol 13: 1265-1271
16. Gabel S, Benefield J, Meisinger J, Petruzzelli GJ, Young M (1999) Protein phosphatases 1 and 2A maintain endothelial cells in a resting state, limiting the motility that is needed for the morphogenic process of angiogenesis. Otolaryngol Head Neck Surg 121: 463-468
17. Galan Moya EM, Le Guelte A, Gavard J (2009) PAKing up to the endothelium. Cell Signal 21: 1727-1737
18. Geudens I, Gerhardt H (2011) Coordinating cell behaviour during blood vessel formation. Development 138: 4569-4583
19. Guenebeaud C, Goldschneider D, Castets M, Guix C, Chazot G, Delloye-Bourgeois C, Eisenberg-Lerner A, Shohat G, Zhang M, Laudet V, Kimchi A, Bernet A, Mehlen P (2010) The dependence receptor UNC5H2/B triggers apoptosis via PP2A-mediated dephosphorylation of DAP kinase. Mol Cell 40: 863-876
20. Hernandez SE, Settleman J, Koleske AJ (2004) Adhesion-dependent regulation of p190RhoGAP in the developing brain by the Ablrelated gene tyrosine kinase. Curr Biol 14: 691-696
21. Hoang MV, Nagy JA, Fox JE, Senger DR (2010) Moderation of calpain activity promotes neovascular integration and lumen formation during VEGF-induced pathological angiogenesis. PLoS One 5: e13612
22. Hoang MV, Nagy JA, Senger DR (2011) Cdc42-mediated inhibition of GSK-3beta improves angio-architecture and lumen formation during VEGF-driven pathological angiogenesis. Microvasc Res 81: 34-43
23. Im E, Kazlauskas A (2007) Src family kinases promote vessel stability by antagonizing the Rho/ROCK pathway. J Biol Chem 282: 29122-29129
24. Iruela-Arispe ML, Davis GE (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16: 222-231
25. Isoda M, Sako K, Suzuki K, Nishino K, Nakajo N, Ohe M, Ezaki T, Kanemori Y, Inoue D, Ueno H, Sagata N (2011) Dynamic regulation of Emi2 by Emi2-bound Cdk1/Plk1/CK1 and PP2A-B56 in meiotic arrest of Xenopus eggs. Dev Cell 21: 506-519
26. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM (2003) Angiogenic network formation in the developing vertebrate trunk. Development 130: 5281-5290
27. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439
28. Jayadeva G, Kurimchak A, Garriga J, Sotillo E, Davis AJ, Haines DS, Mumby M, Grana X (2010) B55alpha PP2A holoenzymes modulate the phosphorylation status of the retinoblastoma-related protein p107 and its activation. J Biol Chem 285: 29863-29873
29. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132: 5199-5209
30. Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE,Weinstein BM (2006) Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442: 453-456
31. Kioka N, Ueda K, Amachi T (2002) Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction. Cell Struct Funct 27: 1-7
32. Koh W, Sachidanandam K, Stratman AN, Sacharidou A, Mayo AM, Murphy EA, Cheresh DA, Davis GE (2009) Formation of endothelial lumens requires a coordinated PKCepsilon-, Src-, Pak- and Raf-kinase-dependent signaling cascade downstream of Cdc42 activation. J Cell Sci 122: 1812-1822
33. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318
34. Le Guelte A, Galan-Moya EM, Dwyer J, Treps L, Kettler G, Hebda JK, Dubois S, Auffray C, Chneiweiss H, Bidere N, Gavard J (2012) Semaphorin 3A elevates endothelial cell permeability through PP2A inactivation. J Cell Sci 125: 4137-4146
35. Manchado E, Guillamot M, de Carcer G, Eguren M, Trickey M, Garcia-Higuera I, Moreno S, Yamano H, Canamero M, Malumbres M (2010) Targeting mitotic exit leads to tumor regression in vivo: modulation by Cdk1, Mastl, and the PP2A/B55alpha,delta phosphatase. Cancer Cell 18: 641-654
36. Martin M, Kettmann R, Dequiedt F (2007) Class IIa histone deacetylases: regulating the regulators. Oncogene 26: 5450-5467
37. Martin M, Potente M, Janssens V, Vertommen D, Twizere JC, Rider MH, Goris J, Dimmeler S, Kettmann R, Dequiedt F (2008) Protein phosphatase 2A controls the activity of histone deacetylase 7 during Tcell apoptosis and angiogenesis. Proc Natl Acad Sci USA 105: 4727-4732
38. Merrick SE, Trojanowski JQ, Lee VM (1997) Selective destruction of stable microtubules and axons by inhibitors of protein serine/threonine phosphatases in cultured human neurons. J Neurosci 17: 5726-5737
39. Merrill RA, Slupe AM, Strack S (2012) N-terminal phosphorylation of protein phosphatase 2A/Bbeta2 regulates translocation to mitochondria, dynamin-related protein 1 dephosphorylation, and neuronal survival. FEBS J 280: 662-673
40. Mottet D, Bellahcene A, Pirotte S, Waltregny D, Deroanne C, Lamour V, Lidereau R, Castronovo V (2007) Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ Res 101: 1237-1246
41. Nunbhakdi-Craig V, Schuechner S, Sontag JM, Montgomery L, Pallas DC, Juno C, Mudrak I, Ogris E, Sontag E (2007) Expression of protein phosphatase 2A mutants and silencing of the regulatory B alpha subunit induce a selective loss of acetylated and detyrosinated microtubules. J Neurochem 101: 959-971
42. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11: 633-643
43. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146: 873-887
44. Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, Kollipara R, DePinho RA, Zeiher AM, Dimmeler S (2005) Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Investig 115: 2382-2392
45. Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18: 578-585
46. Rodgers JT, Vogel RO, Puigserver P (2011) Clk2 and B56beta mediate insulin-regulated assembly of the PP2A phosphatase holoenzyme complex on Akt. Mol Cell 41: 471-479
47. Roignot J, Soubeyran P (2009) ArgBP2 and the SoHo family of adapter proteins in oncogenic diseases. Cell Adhes Migr 3: 167-170
48. Roman BL, Pham VN, Lawson ND, Kulik M, Childs S, Lekven AC, Garrity DM, Moon RT, Fishman MC, Lechleider RJ, Weinstein BM (2002) Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129: 3009-3019
49. Sastry SK, Rajfur Z, Liu BP, Cote JF, Tremblay ML, Burridge K (2006) PTP-PEST couples membrane protrusion and tail retraction via VAV2 and p190RhoGAP. J Biol Chem 281: 11627-11636
50. Schmidt A, Wenzel D, Thorey I, Sasaki T, Hescheler J, Timpl R, Addicks K, Werner S, Fleischmann BK, Bloch W (2006) Endostatin influences endothelial morphology via the activated ERK1/2-kinase endothelial morphology and signal transduction. Microvasc Res 71: 152-162
51. Sents W, Ivanova E, Lambrecht C, Haesen D, Janssens V (2012) The biogenesis of active protein phosphatase 2A holoenzymes: a tightly regulated process creating phosphatase specificity. FEBS J 280: 644-661
52. Sheehan KA, Ke Y, Solaro RJ (2007) p21-Activated kinase-1 and its role in integrated regulation of cardiac contractility. Am J Physiol Regul Integr Compar Physiol 293: R963-R973
53. Song MH, Liu Y, Anderson DE, Jahng WJ, O'Connell KF (2011) Protein Phosphatase 2A-SUR-6/B55 regulates centriole duplication in C. elegans by controlling the levels of centriole assembly factors. Dev Cell 20: 563-571
54. Sontag E, Nunbhakdi-Craig V, Bloom GS, Mumby MC (1995) A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J Cell Biol 128: 1131-1144
55. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White 3rd CL, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274: 25490-25498
56. Soubeyran P, Barac A, Szymkiewicz I, Dikic I (2003) Cbl-ArgBP2 complex mediates ubiquitination and degradation of c-Abl. Biochem J 370: 29-34
57. Stehbens S, Wittmann T (2012) Targeting and transport: How microtubules control focal adhesion dynamics. J Cell Biol 198: 481-489
58. Strilic B, Kucera T, Eglinger J, Hughes MR, McNagny KM, Tsukita S, Dejana E, Ferrara N, Lammert E (2009) The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17: 505-515
59. Strilic B, Kucera T, Lammert E (2010) Formation of cardiovascular tubes in invertebrates and vertebrates. Cell Mol Life Sci 67: 3209-3218
60. Tar K, Csortos C, Czikora I, Olah G, Ma SF, Wadgaonkar R, Gergely P, Garcia JG, Verin AD (2006) Role of protein phosphatase 2A in the regulation of endothelial cell cytoskeleton structure. J Cell Biochem 98: 931-953
61. Traver D, Paw BH, Poss KD, Penberthy WT, Lin S, Zon LI (2003) Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol 4: 1238-1246
62. Tsubouchi A, Sakakura J, Yagi R, Mazaki Y, Schaefer E, Yano H, Sabe H (2002) Localized suppression of RhoA activity by Tyr31/118-phosphorylated paxillin in cell adhesion and migration. J Cell Biol 159: 673-683
63. Virshup DM, Shenolikar S (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 33: 537-545
64. Wang P, Pinson X, Archambault V (2011) PP2A-twins is antagonized by greatwall and collaborates with polo for cell cycle progression and centrosome attachment to nuclei in drosophila embryos. PLoS Genet 7: e1002227
65. Wang Y, Kaiser MS, Larson JD, Nasevicius A, Clark KJ,Wadman SA, Roberg-Perez SE, Ekker SC, Hackett PB, McGrail M, Essner JJ (2010) Moesin1 and Ve-cadherin are required in endothelial cells during in vivo tubulogenesis. Development 137: 3119-3128
66. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1: 136-143
67. Wolfenson H, Henis YI, Geiger B, Bershadsky AD (2009) The heel and toe of the cell's foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions. Cell Motil Cytoskeleton 66: 1017-1029
68. Xu K, Cleaver O (2011) Tubulogenesis during blood vessel formation. Semin Cell Dev Biol 22: 993-1004
69. Yan L, Guo S, Brault M, Harmon J, Robertson RP, Hamid R, Stein R, Yang E (2012) The B55alpha-containing PP2A holoenzyme dephosphorylates FOXO1 in islet beta-cells under oxidative stress. Biochem J 444: 239-247
70. Yan L, Mieulet V, Burgess D, Findlay GM, Sully K, Procter J, Goris J, Janssens V, Morrice NA, Lamb RF (2010) PP2A T61 epsilon is an inhibitor of MAP4K3 in nutrient signaling to mTOR. Mol Cell 37: 633-642
71. Yan Z, Fedorov SA, Mumby MC, Williams RS (2000) PR48, a novel regulatory subunit of protein phosphatase 2A, interacts with Cdc6 and modulates DNA replication in human cells. Mol Cell Biol 20: 1021-1029
72. Zaidel-Bar R, Milo R, Kam Z, Geiger B (2007) A paxillin tyrosine phosphorylation switch regulates the assembly and form of cellmatrix adhesions. J Cell Sci 120: 137-148