Phosphoinositide 3-kinase β mediates microvascular endothelial repair of thrombotic microangiopathy

Blood

Volumn 124, Issue 13, 2014, Pages 2142-2149

  Haddad, George ^a   Zhabyeyev, Pavel ^a   Farhan, Maikel ^a   Zhu, Lin Fu ^a   Kassiri, Zamaneh ^a   Rayner, David C ^a   Vanhaesebroeck, Bart ^b   Oudit, Gavin Y ^a   Murray, Allan G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN; FIBRIN; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE BETA; PROTEIN DII4; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; PROTEIN KINASE B; VASCULOTROPIN A;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY ENDOTHELIAL CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; THROMBOTIC THROMBOCYTOPENIC PURPURA; ANIMAL; APOPTOSIS; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENETICS; GLOMERULUS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MICROVASCULATURE; MORTALITY; PATHOLOGY; PHOSPHORYLATION; VASCULAR ENDOTHELIUM;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CLASS II PHOSPHATIDYLINOSITOL 3-KINASES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; KIDNEY GLOMERULUS; MICE; MICE, KNOCKOUT; MICROVESSELS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; THROMBOTIC MICROANGIOPATHIES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84907478646     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-02-557975     Document Type: Article

References (43)

1. Noris M, Remuzzi G. Atypical hemolytic-uremic syndrome. N Engl J Med. 2009;361(17):1676-1687.
2. Laskin BL, Goebel J, Davies SM, Jodele S. Small vessels, big trouble in the kidneys and beyond: hematopoietic stem cell transplantation-associated thrombotic microangiopathy. Blood. 2011;118(6):1452-1462.
3. Petruzziello-Pellegrini TN, Marsden PA. Shiga toxin-associated hemolytic uremic syndrome: advances in pathogenesis and therapeutics. Curr Opin Nephrol Hypertens. 2012;21(4):433-440.
4. Siegler RL. Postdiarrheal Shiga toxin-mediated hemolytic uremic syndrome. JAMA. 2003;290(10):1379-1381.
5. Pomajzl RJ, Varman M, Holst A, Chen A. Hemolytic uremic syndrome (HUS) - incidence and etiologies at a regional Children's Hospital in 2001-2006. Eur J Clin Microbiol Infect Dis. 2009;28(12):1431-1435.
6. Frank C, Werber D, Cramer JP, et al HUS Investigation Team. Epidemic profile of Shigatoxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med. 2011;365(19):1771-1780.
7. Loos S, Ahlenstiel T, Kranz B, et al. An outbreak of Shiga toxin-producing Escherichia coli O104: H4 hemolytic uremic syndrome in Germany: presentation and short-term outcome in children. Clin Infect Dis. 2012;55(6):753-759.
8. Menne J, Nitschke M, Stingele R, et al; EHEC-HUS consortium. Validation of treatment strategies for enterohaemorrhagic Escherichia coli O104:H4 induced haemolytic uraemic syndrome: case-control study. BMJ. 2012;345:e4565.
9. Shalaby F, Ho J, Stanford WL, et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89(6):981-990.
10. Allende ML, Yamashita T, Proia RL. G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood. 2003;102(10):3665-3667.
11. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473(7347):298-307.
12. Duronio V. The life of a cell: apoptosis regulation by the PI3K/PKB pathway. Biochem J. 2008;415(3):333-344.
13. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B. The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol. 2010;11(5):329-341.
14. Kurosu H, Maehama T, Okada T, et al. Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110beta is synergistically activated by the betagamma subunits of G proteins and phosphotyrosyl peptide. J Biol Chem. 1997;272(39):24252-24256.
15. Guillermet-Guibert J, Bjorklof K, Salpekar A, et al. The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc Natl Acad Sci USA. 2008;105(24):8292-8297.
16. Fritsch R, de Krijger I, Fritsch K, et al. RAS and RHO families of GTPases directly regulate distinct phosphoinositide 3-kinase isoforms. Cell. 2013;153(5):1050-1063.
17. Lelievre E, Bourbon PM, Duan LJ, Nussbaum RL, Fong GH. Deficiency in the p110alpha subunit of PI3K results in diminished Tie2 expression and Tie2(-/-)-like vascular defects in mice. Blood. 2005;105(10):3935-3938.
18. Graupera M, Guillermet-Guibert J, Foukas LC, et al. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature. 2008;453(7195):662-666.
19. Kulkarni S, Sitaru C, Jakus Z, et al. PI3Kβ plays a critical role in neutrophil activation by immune complexes. Sci Signal. 2011;4(168):ra23.
20. Forde A, Constien R, Gröne H-J, Hämmerling G, Arnold B. Temporal Cre-mediated recombination exclusively in endothelial cells using Tie2 regulatory elements. Genesis. 2002;33(4):191-197.
21. Haddad G, Zhu LF, Rayner D, Murray AG. Experimental glomerular microvascular endothelial injury in vivo. PLoS One. 2013;8:e78244-e78254.
22. Ingram DA, Mead LE, Tanaka H, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104(9):2752-2760.
23. Nakhaei-Nejad M, Haddad G, Zhang Q-X, Murray AG. Facio-genital dysplasia-5 regulates matrix adhesion and survival of human endothelial cells. Arterioscler Thromb Vasc Biol. 2012;32:2694-2701.
24. Nakatsu MN, Hughes CC. An optimized three-dimensional in vitro model for the analysis of angiogenesis. Methods Enzymol. 2008;443:65-82.
25. Melero-Martin JM, Khan ZA, Picard A, Wu X, Paruchuri S, Bischoff J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood. 2007;109(11):4761-4768.
26. Boor P, van Roeyen CR, Kunter U, et al. PDGF-C mediates glomerular capillary repair. Am J Pathol. 2010;177(1):58-69.
27. del Toro R, Prahst C, Mathivet T, et al. Identification and functional analysis of endothelial tip cell-enriched genes. Blood. 2010;116(19):4025-4033.
28. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163-1177.
29. Strasser GA, Kaminker JS, Tessier-Lavigne M. Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood. 2010;115(24):5102-5110.
30. Khachigian LM, Lindner V, Williams AJ, Collins T. Egr-1-induced endothelial gene expression: a common theme in vascular injury. Science. 1996;271(5254):1427-1431.
31. Baffert F, Le T, Sennino B, et al. Cellular changes in normal blood capillaries undergoing regression after inhibition of VEGF signaling. Am J Physiol Heart Circ Physiol. 2006;290(2):H547-H559.
32. Mancuso MR, Davis R, Norberg SM, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest. 2006;116(10):2610-2621.
33. Kasai A, Shintani N, Kato H, et al. Retardation of retinal vascular development in apelin-deficient mice. Arterioscler Thromb Vasc Biol. 2008;28(10):1717-1722.
34. Eyries M, Siegfried G, Ciumas M, et al. Hypoxia-induced apelin expression regulates endothelial cell proliferation and regenerative angiogenesis. Circ Res. 2008;103(4):432-440.
35. Hellström M, Phng LK, Hofmann JJ, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445(7129):776-780.
36. Suchting S, Freitas C, le Noble F, et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA. 2007;104(9):3225-3230.
37. Lobov IB, Renard RA, Papadopoulos N, et al. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA. 2007;104(9):3219-3224.
38. Jackson SP, Schoenwaelder SM, Goncalves I, et al. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med. 2005;11(5):507-514.
39. Cosemans JM, Munnix IC, Wetzker R, Heller R, Jackson SP, Heemskerk JW. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood. 2006;108(9):3045-3052.
40. Martin V, Guillermet-Guibert J, Chicanne G, et al. Deletion of the p110beta isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitro and in vivo. Blood. 2010;115(10):2008-2013.
41. Lee S, Chen TT, Barber CL, et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130(4):691-703.
42. Eremina V, Jefferson JA, Kowalewska J, et al. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358(11):1129-1136.
43. Jeansson M, Gawlik A, Anderson G, et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest. 2011;121(6):2278-2289.