Rap1 promotes endothelial mechanosensing complex formation, NO release and normal endothelial function

EMBO Reports

Volumn 16, Issue 5, 2015, Pages 628-637

  Lakshmikanthan, Sribalaji ^a   Zheng, Xiaodong ^b,c   Nishijima, Yoshinori ^b   Sobczak, Magdalena ^a,d   Szabo, Aniko ^b   Vasquez Vivar, Jeannette ^b   Zhang, David X ^b   Chrzanowska Wodnicka, Magdalena ^a  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c HARBIN MEDICAL UNIVERSITY   (China)

^d NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

mechanotransduction; nitric oxide; shear stress; small GTPase Rap1; vasodilation

Indexed keywords

CD31 ANTIGEN; NITRIC OXIDE; RAP1 PROTEIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; ENDOTHELIUM CELL; HYPERTENSION; IN VIVO STUDY; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEAR STRESS; SIGNAL TRANSDUCTION; VASODILATATION; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; BLOOD PRESSURE; CAPILLARY PERMEABILITY; GENETICS; HEART LEFT VENTRICLE HYPERTROPHY; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOPHYSIOLOGY;

MURINAE;

ANIMALS; BLOOD PRESSURE; CAPILLARY PERMEABILITY; ENDOTHELIUM; HUMANS; HYPERTENSION; HYPERTROPHY, LEFT VENTRICULAR; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; ORGAN SPECIFICITY; RAP1 GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VASODILATION;

EID: 84928885238     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201439846     Document Type: Article

References (52)

1. Forstermann U, Sessa WC, (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33: 829-837, 837a-837d
2. Widlansky ME, Gokce N, Keaney JF Jr, Vita JA, (2003) The clinical implications of endothelial dysfunction. J Am Coll Cardiol 42: 1149-1160
3. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC, (1995) Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377: 239-242
4. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O, (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93: 13176-13181
5. Michel T, Feron O, (1997) Nitric oxide synthases: which, where, how, and why? J Clin Invest 100: 2146-2152
6. Hahn C, Schwartz MA, (2009) Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 10: 53-62
7. Chen K-D, Li Y-S, Kim M, Li S, Yuan S, Chien S, Shyy JY-J, (1999) Mechanotransduction in response to shear stress. J Biol Chem 274: 18393-18400
8. Jin Z-G, Ueba H, Tanimoto T, Lungu AO, Frame MD, Berk BC, (2003) Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res 93: 354-363
9. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA, (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437: 426-431
10. Fleming I, Fisslthaler B, Dixit M, Busse R, (2005) Role of PECAM-1 in the shear-stress-induced activation of Akt and the endothelial nitric oxide synthase (eNOS) in endothelial cells. J Cell Sci 118: 4103-4111
11. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC, (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601
12. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM, (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605
13. Conway D, Schwartz MA, (2012) Lessons from the endothelial junctional mechanosensory complex. F1000 Biol Rep 4: 1
14. Frische EW, Zwartkruis FJT, (2010) Rap1, a mercenary among the Ras-like GTPases. Dev Biol 340: 1-9
15. Gloerich M, Bos JL, (2011) Regulating Rap small G-proteins in time and space. Trends Cell Biol 21: 615-623
16. Chrzanowska-Wodnicka M, Smyth SS, Schoenwaelder SM, Fischer TH, White GC, (2005) Rap1b is required for normal platelet function and hemostasis in mice. J Clin Invest 115: 2296-2296
17. Chrzanowska-Wodnicka M, (2013) Distinct functions for Rap1 signaling in vascular morphogenesis and dysfunction. Exp Cell Res 319: 2350-2359
18. Duchniewicz M, Zemojtel T, Kolanczyk M, Grossmann S, Scheele JS, Zwartkruis FJT, (2006) Rap1A-deficient T and B cells show impaired integrin-mediated cell adhesion. Mol Cell Biol 26: 643-653
19. Li Y, Yan JL, De P, Chang HC, Yamauchi A, Christopherson KW, Paranavitana NC, Peng XD, Kim C, Munugulavadla V, et al, (2007) Rap1a null mice have altered myeloid cell functions suggesting distinct roles for the closely related Rap1a and 1b proteins. J Immunol 179: 8322-8331
20. Chrzanowska-Wodnicka M, Kraus AE, Gale D, White GC II, Vansluys J, (2008) Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood 111: 2647-2656
21. Yan J, Li F, Ingram DA, Quilliam LA, (2008) Rap1a is a key regulator of fibroblast growth factor 2-induced angiogenesis and together with Rap1b controls human endothelial cell functions. Mol Cell Biol 28: 5803-5810
22. Cullere X, Shaw SK, Andersson L, Hirahashi J, Luscinskas FW, Mayadas TN, (2005) Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 105: 1950-1955
23. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N, (2005) Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 25: 136-146
24. Wittchen ES, Worthylake RA, Kelly P, Casey PJ, Quilliam LA, Burridge K, (2005) Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J Biol Chem 280: 11675-11682
25. Glading A, Han J, Stockton RA, Ginsberg MH, (2007) KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell-cell junctions. J Cell Biol 179: 247-254
26. Revencu N, Vikkula M, (2006) Cerebral cavernous malformation: new molecular and clinical insights. J Med Genet 43: 716-721
27. Lakshmikanthan S, Sobczak M, Chun C, Henschel A, Dargatz J, Ramchandran R, Chrzanowska-Wodnicka M, (2011) Rap1 promotes VEGFR2 activation and angiogenesis by a mechanism involving integrin alphavbeta(3). Blood 118: 2015-2026
28. Lakshmikanthan S, Zieba BJ, Ge ZD, Momotani K, Zheng X, Lund H, Artamonov MV, Maas JE, Szabo A, Zhang DX, et al, (2014) Rap1b in smooth muscle and endothelium is required for maintenance of vascular tone and normal blood pressure. Arterioscler Thromb Vasc Biol 34: 1486-1494
29. Boettner B, Van Aelst L, (2009) Control of cell adhesion dynamics by Rap1 signaling. Curr Opin Cell Biol 21: 684-693
30. Takakura N, Huang X-L, Naruse T, Hamaguchi I, Dumont DJ, Yancopoulos GD, Suda T, (1998) Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity 9: 677-686
31. Chiu YJ, McBeath E, Fujiwara K, (2008) Mechanotransduction in an extracted cell model: Fyn drives stretch- and flow-elicited PECAM-1 phosphorylation. J Cell Biol 182: 753-763
32. De Bruyn KMT, Zwartkruis FJT, De Rooij J, Akkerman JWN, Bos JL, (2003) The small GTPase Rap1 is activated by turbulence and is involved in integrin αIIbβ3-mediated cell adhesion in human megakaryocytes. J Biol Chem 278: 22412-22417
33. Moon EY, Oh SY, Han GH, Lee CS, Park SK, (2005) Epac1-mediated Rap1 activation is not required for the production of nitric oxide in BV2, murine microglial cells. J Neurosci Res 81: 38-44
34. Tamada M, Sheetz MP, Sawada Y, (2004) Activation of a signaling cascade by cytoskeleton stretch. Dev Cell 7: 709-718
35. Chrzanowska-Wodnicka M, (2010) Regulation of angiogenesis by a small GTPase Rap1. Vascul Pharmacol 53: 1-10
36. Chen YH, Yu M, Podd A, Wen R, Chrzanowska-Wodnicka M, White GC, Wang D, (2008) A critical role of Rap1b in B-cell trafficking and marginal zone B-cell development. Blood 111: 4627-4636
37. Chu H, Awasthi A, White GC II, Chrzanowska-Wodnicka M, Malarkannan S, (2008) Rap1b regulates B cell development, homing, and T cell-dependent humoral immunity. J Immunol 181: 3373-3383
38. Rajkumar R, Konishi K, Richards TJ, Ishizawar DC, Wiechert AC, Kaminski N, Ahmad F, (2010) Genomewide RNA expression profiling in lung identifies distinct signatures in idiopathic pulmonary arterial hypertension and secondary pulmonary hypertension. Am J Physiol Heart Circ Physiol 298: H1235-H1248
39. Pan BX, Vautier F, Ito W, Bolshakov VY, Morozov A, (2008) Enhanced cortico-amygdala efficacy and suppressed fear in absence of Rap1. J Neurosci 28: 2089-2098
40. Pitulescu ME, Schmidt I, Benedito R, Adams RH, (2012) Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat Prot 5: 1518-1534
41. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, Bender JR, (2000) Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87: 677-682
42. Nelson TJ, Ge ZD, Van Orman J, Barron M, Rudy-Reil D, Hacker TA, Misra R, Duncan SA, Auchampach JA, Lough JW, (2006) Improved cardiac function in infarcted mice after treatment with pluripotent embryonic stem cells. Anat Rec A Discov Mol Cell Evol Biol 288: 1216-1224
43. Toyama K, Wulff H, Chandy KG, Azam P, Raman G, Saito T, Fujiwara Y, Mattson DL, Das S, Melvin JE, et al, (2008) The intermediate-conductance calcium-activated potassium channel KCa3.1 contributes to atherogenesis in mice and humans. J Clin Invest 118: 3025-3037
44. Kriska T, Cepura C, Magier D, Siangjong L, Gauthier KM, Campbell WB, (2012) Mice lacking macrophage 12/15-lipoxygenase are resistant to experimental hypertension. Am J Physiol Heart Circ Physiol 302: H2428-H2438
45. Moitra J, Sammani S, Garcia JGN, (2007) Re-evaluation of Evans Blue dye as a marker of albumin clearance in murine models of acute lung injury. Transl Res 150: 253-265
46. Chen Z, Tzima E, (2009) PECAM-1 is necessary for flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol 29: 1067-1073
47. 2+ influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol 298: H466-H476
48. Sobczak M, Dargatz J, Chrzanowska-Wodnicka M, (2010) Isolation and culture of pulmonary endothelial cells from neonatal mice. J Vis Exp 46: doi: 10.3791/2316.
49. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JG, Birukov KG, (2005) Differential effects of shear stress and cyclic stretch on focal adhesion remodeling, site-specific FAK phosphorylation, and small GTPases in human lung endothelial cells. Exp Cell Res 304: 40-49
50. Franke B, van Triest M, de Bruijn KMT, van Willigen G, Nieuwenhuis HK, Negrier C, Akkerman J-WN, Bos JL, (2000) Sequential regulation of the small GTPase Rap1 in human platelets. Mol Cell Biol 20: 779-785
51. Bryan NS, Grisham MB, (2007) Methods to detect nitric oxide and its metabolites in biological samples. Free Radic Biol Med 43: 645-657
52. Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, (2000) The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol 148: 1151-1158