AKAP9 regulation of microtubule dynamics promotes Epac1-induced endothelial barrier properties

Blood

Volumn 117, Issue 2, 2011, Pages 708-718

  Sehrawat, Seema ^a   Ernandez, Thomas ^a   Cullere, Xavier ^a   Takahashi, Mikiko ^b   Ono, Yoshitaka ^b   Komarova, Yulia ^c   Mayadas, Tanya N ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b KOBE UNIVERSITY   (Japan)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A KINASE ANCHORING PROTEIN 9; ACTIN; CYCLIC AMP BINDING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; INTEGRIN; PROTEIN EPAC 1; RAP1 PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEADY STATE;

EID: 78751480860     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-02-268870     Document Type: Article

References (54)

1. Vestweber D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol. 2008;28(2):223-232. (Pubitemid 351161193)
2. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86(1):279-367.
3. Wu MH, Ustinova E, Granger HJ. Integrin binding to fibronectin and vitronectin maintains the barrier function of isolated porcine coronary venules. J Physiol. 2001;532(Pt 3):785-791. (Pubitemid 32427891)
4. Lampugnani MG, Resnati M, Dejana E, Marchisio PC. The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol. 1991;112(3):479-490. (Pubitemid 21926002)
5. Taskén K, Aandahl EM. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev. 2004;84:137-167. (Pubitemid 38049878)
6. Dodge-Kafka KL, Soughayer J, Pare GC, et al. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature. 2005;437:574-578.
7. Nijholt IM, Dolga AM, Ostroveanu A, Luiten PG, Schmidt M, Eisel UL. Neuronal AKAP150 coordinates PKA and Epac-mediated PKB/Akt phosphorylation. Cell Signal. 2008;20(10):1715-1724.
8. Gloerich M, Bos JL. Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol. 2010;50:355-375.
9. Yarwood SJ. Microtubule-associated proteins (MAPs) regulate cAMP signalling through exchange protein directly activated by cAMP (EPAC). Biochem Soc Trans. 2005;33(6):1327-1329.
10. Mei FC, Cheng X. Interplay between exchange protein directly activated by cAMP (Epac) and microtubule cytoskeleton. Mol Biosyst. 2005;1:325-331. (Pubitemid 41579325)
11. Sehrawat S, Cullere X, Patel S, Italiano J Jr, Mayadas TN. Role of Epac1, an exchange factor for Rap GTPases, in endothelial microtubule dynamics and barrier function. Mol Biol Cell. 2008;19(3):1261-1270.
12. Stehbens SJ, Akhmanova A, Yap AS. Microtubules and cadherins: a neglected partnership. Front Biosci. 2009;14:3159-3167.
13. Akhmanova A, Steinmetz MO. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol. 2008;9(4):309-322. (Pubitemid 351430849)
14. Wong W, Scott JD. AKAP signalling complexes: Focal points in space and time. Nat Rev Mol Cell Biol. 2004;5(12):959-970. (Pubitemid 39611533)
15. Larocca MC, Jin M, Goldenring JR. AKAP350 modulates microtubule dynamics. Eur J Cell Biol. 2006;85(7):611-619.
16. Rivero S, Cardenas J, Bornens M, Rios RM. Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J. 2009;28(8):1016-1028.
17. Chen L, Kurokawa J, Kass RS. Phosphorylation of the A-kinase-anchoring protein Yotiao contributes to protein kinase A regulation of a heart potassium channel. J Biol Chem. 2005;280(36): 31347-31352.
18. Campbell KS, Cooper S, Dessing M, Yates S, Buder A. Interaction of p59fyn kinase with the dynein light chain, Tctex-1, and colocalization during cytokinesis. J Immunol. 1998;161(4):1728-1737. (Pubitemid 28387590)
19. Gundersen GG, Kalnoski MH, Bulinski JC. Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell. 1984;38(3):779-789.
20. Stepanova T, Slemmer J, Hoogenraad CC, et al. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci. 2003;23(7):2655-2664.
21. Kim HS, Takahashi M, Matsuo K, Ono Y. Recruitment of CG-NAP to the Golgi apparatus through interaction with dynein-dynactin complex. Genes Cells. 2007;12(3):421-434. (Pubitemid 46359594)
22. Mei FC, Qiao J, Tsygankova OM, Meinkoth JL, Quilliam LA, Cheng X. Differential signaling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation. J Biol Chem. 2002;277(13):11497-11504.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-408. (Pubitemid 34164012)
24. Tudor EL, Perkinton MS, Schmidt A, et al. ALS2/Alsin regulates. Rac-PAK signaling and neurite outgrowth. J Biol Chem. 2005;280(41):34735-34740.
25. Komarova YA, Vorobjev IA, Borisy GG. Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci. 2002;115(Pt 17):3527-3539.
26. Cullere X, Shaw SK, Andersson L, Hirahashi J, Luscinskas FW, Mayadas TN. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood. 2005;105(5):1950-1955. (Pubitemid 40731777)
27. Chen L, Marquardt ML, Tester DJ, Sampson KJ, Ackerman MJ, Kass RS. Mutation of an A-kinase-anchoring protein causes long-QT syndrome. Proc Natl Acad Sci U S A. 2007;104(52):20990-20995.
28. Westermann S, Weber K. Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol. 2003;4(12):938-947. (Pubitemid 37493642)
29. Bos JL. Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci. 2006;31(12):680-686.
30. Baumer Y, Drenckhahn D, Waschke J. cAMP induced Rac 1-mediated cytoskeletal reorganization in microvascular endothelium. Histochem Cell Biol. 2008;129(6):765-778.
31. Poppe H, Rybalkin SD, Rehmann H, et al. Cyclic nucleotide analogs as probes of signaling pathways. Nat Methods. 2008;5(4):277-278.
32. Qiao J, Mei FC, Popov VL, Vergara LA, Cheng X. Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J Biol Chem. 2002;277(29):26581-26586.
33. Magiera MM, Gupta M, Rundell CJ, Satish N, Ernens I, Yarwood SJ. Exchange protein directly activated by cAMP (EPAC) interacts with the light chain (LC) 2 of MAP1A. Biochem J. 2004;382(Pt 3):803-810. (Pubitemid 39312894)
34. Lampugnani MG, Corada M, Caveda L, et al. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol. 1995;129(1):203-217.
35. Ligon LA, Holzbaur EL. Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic. 2007;8(7):808-819.
36. Rangarajan S, Enserink JM, Kuiperij HB, et al. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol. 2003;160(4):487-493.
37. Berryman MA, Goldenring JR. CLIC4 is enriched at cell-cell junctions and colocalizes with AKAP350 at the centrosome and midbody of cultured mammalian cells. Cell Motil Cytoskeleton. 2003;56(3):159-172.
38. Takahashi M, Yamagiwa A, Nishimura T, Mukai H, Ono Y. Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring gamma-tubulin ring complex. Mol Biol Cell. 2002;13(9):3235-3245. (Pubitemid 35034258)
39. Morrison EE, Wardleworth BN, Askham JM, Markham AF, Meredith DM. EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene. 1998;17(26):3471-3477.
40. Gundersen GG, Gomes ER, Wen Y. Cortical control of microtubule stability and polarization. Curr Opin Cell Biol. 2004;16(1):106-112. (Pubitemid 38368160)
41. Ligon LA, Karki S, Tokito M, Holzbaur EL. Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol. 2001;3(10):913-917. (Pubitemid 32952256)
42. Taskén KA, Collas P, Kemmner WA, Witczak O, Conti M, Tasken K. Phosphodiesterase 4D and protein kinase a type II constitute a signaling unit in the centrosomal area. J Biol Chem. 2001;276(25):21999-22002.
43. Takahashi M, Shibata H, Shimakawa M, Miyamoto M, Mukai H, Ono Y. Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus. J Biol Chem. 1999;274(24):17267-17274.
44. Hong K, Lou L, Gupta S, Ribeiro-Neto F, Altschuler DL. A novel Epac-Rap-PP2A signaling module controls cAMP-dependent Akt regulation. J Biol Chem. 2008;283(34):23129-23138.
45. Sakurai A, Fukuhara S, Yamagishi A, et al. MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol Biol Cell. 2006;17(2):966-976.
46. Birukova AA, Cokic I, Moldobaeva N, Birukov KG. Paxillin is involved in the differential regulation of endothelial barrier by HGF and VEGF. Am J Respir Cell Mol Biol. 2009;40(1):99-107.
47. Zhang Z, Morla AO, Vuori K, Bauer JS, Juliano RL, Ruoslahti E. The alpha v beta 1 integrin functions as a fibronectin receptor but does not support fibronectin matrix assembly and cell migration on fibronectin. J Cell Biol. 1993;122(1):235-242.
48. Pedchenko V, Zent R, Hudson BG. Alpha(v)beta3 and alpha(v)beta5 integrins bind both the proximal RGD site and non-RGD motifs within noncollagenous (NC1) domain of the alpha3 chain of type IV collagen: implication for the mechanism of endothelia cell adhesion. J Biol Chem. 2004;279(4):2772-2780.
49. Su G, Hodnett M, Wu N, et al. Integrin alphavbeta5 regulates lung vascular permeability and pulmonary endothelial barrier function. Am J Respir Cell Mol Biol. 2007;36(3):377-386.
50. Chen X, Gumbiner BM. Crosstalk between different adhesion molecules. Curr Opin Cell Biol. 2006;18(5):572-578.
51. Glading A, Han J, Stockton RA, Ginsberg MH. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J Cell Biol. 2007;179(2):247-254.
52. Fujita H, Fukuhara S, Sakurai A, et al. Local activation of Rap1 contributes to directional vascular endothelial cell migration accompanied by extension of microtubules on which RAPL, a Rap1-associating molecule, localizes. J Biol Chem. 2005;280(6):5022-5031.
53. Béraud-Dufour S, Gautier R, Albiges-Rizo C, Chardin P, Faurobert E. Krit 1 interactions with microtubules and membranes are regulated by Rap1 and integrin cytoplasmic domain associated protein-1. FEBS J. 2007;274(21):5518- 5532.
54. Bos JL. Linking Rap to cell adhesion. Curr Opin Cell Biol. 2005;17(2):123-128.