Neutrophil AKT2 regulates heterotypic cell-cell interactions during vascular inflammation

Journal of Clinical Investigation

Volumn 124, Issue 4, 2014, Pages 1483-1496

  Li, Jing ^a   Kim, Kyungho ^a   Hahm, Eunsil ^a   Molokie, Robert ^a,b   Hay, Nissim ^a   Gordeuk, Victor R ^a   Du, Xiaoping ^a   Cho, Jaehyung ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN; AKT3 PROTEIN; BETA2 TALIN1; INTEGRIN; ISOENZYME; PROTEIN KINASE B; PROTEIN KINASE B BETA; TALIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL OCCLUSION; BONE MARROW; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CELL ADHESION; CELL INTERACTION; CELL ISOLATION; CHIMERA; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKOCYTE ACTIVATION; MALE; MEMBRANE; MICROSCOPY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SICKLE CELL ANEMIA; THROMBOCYTE; THROMBOCYTE AGGREGATION; VASCULITIS;

ANEMIA, SICKLE CELL; ANIMALS; CALCIUM SIGNALING; CELL COMMUNICATION; DISEASE MODELS, ANIMAL; HUMANS; MACROPHAGE-1 ANTIGEN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PLATELET AGGREGATION; PROTO-ONCOGENE PROTEINS C-AKT; TALIN; VASCULITIS;

EID: 84897499880     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI72305     Document Type: Article

References (53)

1. Wagner DD, Frenette PS. The vessel wall and its interactions. Blood. 2008;111(11):5271-5281.
2. Nieswandt B, Kleinschnitz C, Stoll G. Ischaemic stroke: a thrombo-inflammatory disease? J Physiol. 2011;589(pt 17):4115-4123.
3. Zarbock A, Ley K. Neutrophil adhesion and activation under flow. Microcirculation. 2009;16(1):31-42.
4. Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nat Med. 2011;17(11):1381-1390.
5. Hidalgo A, Chang J, Jang JE, Peired AJ, Chiang EY, Frenette PS. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med. 2009; 15(4):384-391.
6. Gross PL, Furie BC, Merrill-Skoloff G, Chou J, Furie B. Leukocyte-versus microparticle-mediated tissue factor transfer during arteriolar thrombus development. J Leukoc Biol. 2005;78(6):1318-1326. (Pubitemid 41779238)
7. Wang Y, et al. Leukocyte engagement of platelet glycoprotein Ibalpha via the integrin Mac-1 is critical for the biological response to vascular injury. Circulation. 2005;112(19):2993-3000. (Pubitemid 41612303)
8. Simon DI, et al. Platelet glycoprotein ibα is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med. 2000;192(2):193-204. (Pubitemid 30470302)
9. Zarbock A, Polanowska-Grabowska RK, Ley K. Platelet-neutrophil- interactions: linking hemostasis and inflammation. Blood Rev. 2007; 21(2):99-111. (Pubitemid 46428465)
10. Hers I, Vincent EE, Tavare JM. Akt signalling in health and disease. Cell Signal. 2011;23(10):1515-1527.
11. Yang WL, Wu CY, Wu J, Lin HK. Regulation of Akt signaling activation by ubiquitination. Cell Cycle. 2010;9(3):487-497.
12. Woulfe DS. Akt signaling in platelets and thrombosis. Expert Rev Hematol. 2010;3(1):81-91.
13. Chen J, De S, Damron DS, Chen WS, Hay N, Byzova TV. Impaired platelet responses to thrombin and collagen in AKT-1-deficient mice. Blood. 2004; 104(6):1703-1710. (Pubitemid 39202277)
14. Woulfe D, Jiang H, Morgans A, Monks R, Birnbaum M, Brass LF. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J Clin Invest. 2004;113(3):441-450. (Pubitemid 38544188)
15. O'Brien KA, Stojanovic-Terpo A, Hay N, Du X. An important role for Akt3 in platelet activation and thrombosis. Blood. 2011;118(15):4215-4223.
16. Jones CI, et al. A functional genomics approach reveals novel quantitative trait loci associated with platelet signaling pathways. Blood. 2009; 114(7):1405-1416.
17. Chen J, Tang H, Hay N, Xu J, Ye RD. Akt isoforms differentially regulate neutrophil functions. Blood. 2010;115(21):4237-4246.
18. Di Lorenzo A, Fernandez-Hernando C, Cirino G, Sessa WC. Akt1 is critical for acute inflammation and histamine-mediated vascular leakage. Proc Natl Acad Sci U S A. 2009;106(34):14552-14557.
19. Fernandez-Hernando C, et al. Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 2007;6(6):446-457. (Pubitemid 350163050)
20. Ding L, et al. Akt3 deficiency in macrophages promotes foam cell formation and atherosclerosis in mice. Cell Metab. 2012;15(6):861-872.
21. Barthel SR, et al. Alpha 1,3 fucosyltransferases are master regulators of prostate cancer cell trafficking. Proc Natl Acad Sci U S A. 2009;106(46):19491-19496.
22. Zhao Z, et al. Development of potent, allosteric dual Akt1 and Akt2 inhibitors with improved physical properties and cell activity. Bioorg Med Chem Lett. 2008;18(1):49-53.
23. Konstantopoulos K, et al. Venous levels of shear support neutrophil-platelet adhesion and neutrophil aggregation in blood via P-selectin and beta2-integrin. Circulation. 1998;98(9):873-882. (Pubitemid 28397437)
24. Maugeri N, de Gaetano G, Barbanti M, Donati MB, Cerletti C. Prevention of platelet-polymorphonuclear leukocyte interactions: new clues to the antithrombotic properties of parnaparin, a low molecular weight heparin. Haematologica. 2005;90(6):833-839. (Pubitemid 40897226)
25. Evangelista V, et al. Platelet/polymorphonuclear leukocyte interaction in dynamic conditions: evidence of adhesion cascade and cross talk between P-selectin and the beta 2 integrin CD11b/CD18. Blood. 1996;88(11):4183-4194. (Pubitemid 26399164)
26. Davenpeck KL, Brummet ME, Hudson SA, Mayer RJ, Bochner BS. Activation of human leukocytes reduces surface P-selectin glycoprotein ligand-1 (PSGL-1, CD162) and adhesion to P-selectin in vitro. J Immunol. 2000;165(5):2764-2772. (Pubitemid 30660727)
27. Sengelov H, Kjeldsen L, Diamond MS, Springer TA, Borregaard N. Subcellular localization and dynamics of Mac-1 (alpha m beta 2) in human neutrophils. J Clin Invest. 1993;92(3):1467-1476. (Pubitemid 23273926)
28. Ye F, Kim C, Ginsberg MH. Molecular mechanism of inside-out integrin regulation. J Thromb Haemost. 2011;9(suppl 1):20-25.
29. Lu Z, Ballou LM, Jiang YP, Cohen IS, Lin RZ. Restoration of defective L-type Ca2+ current in cardiac myocytes of type 2 diabetic db/db mice by Akt and PKC-iota. J Cardiovasc Pharmacol. 2011;58(4):439-445.
30. Frenette PS, Atweh GF. Sickle cell disease: old discoveries, new concepts, and future promise. J Clin Invest. 2007;117(4):850-858. (Pubitemid 46556737)
31. Paszty C, et al. Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science. 1997;278(5339):876-878. (Pubitemid 27467927)
32. Borregaard N, et al. Changes in subcellular localization and surface expression of L-selectin, alkaline phosphatase, and Mac-1 in human neutrophils during stimulation with inflammatory mediators. J Leuk Biol. 1994;56(1):80-87. (Pubitemid 24241786)
33. Nanamori M, Chen J, Du X, Ye RD. Regulation of leukocyte degranulation by cGMP-dependent protein kinase and phosphoinositide 3-kinase: potential roles in phosphorylation of target membrane SNARE complex proteins in rat mast cells. J Immunol. 2007;178(1):416-427. (Pubitemid 46033625)
34. Servant G, Weiner OD, Herzmark P, Balla T, Sedat JW, Bourne HR. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science. 2000;287(5455):1037-1040. (Pubitemid 30094359)
35. Scholz T, Zhao L, Temmler U, Bath P, Heptinstall S, Losche W. The GPIIb/IIIa antagonist eptifibatide markedly potentiates platelet-leukocyte interaction and tissue factor expression following platelet activation in whole blood in vitro. Platelets. 2002;13(7):401-406. (Pubitemid 35346940)
36. Caron A, Theoret JF, Mousa SA, Merhi Y. Anti-platelet effects of GPIIb/IIIa and P-selectin antagonism, platelet activation, and binding to neutrophils. J Cardiovasc Pharmacol. 2002;40(2):296-306. (Pubitemid 34793167)
37. Kleinschnitz C, Pozgajova M, Pham M, Bendszus M, Nieswandt B, Stoll G. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation. 2007;115(17):2323-2330. (Pubitemid 46685900)
38. Adams HP Jr, et al. Emergency administration of abciximab for treatment of patients with acute ischemic stroke: results of an international phase III trial: Abciximab in Emergency Treatment of Stroke Trial (AbESTT-II). Stroke. 2008;39(1):87-99.
39. Kellert L, et al. Endovascular stroke therapy: tirofiban is associated with risk of fatal intracerebral hemorrhage and poor outcome. Stroke. 2013; 44(5):1453-1455.
40. Hahm E, Li J, Kim K, Huh S, Rogelj S, Cho J. Extracellular protein disulfide isomerase regulates ligand-binding activity of alphaMbeta2 integrin and neutrophil recruitment during vascular inflammation. Blood. 2013;121(19):3789-3800.
41. Carman CV, Springer TA. Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr Opin Cell Biol. 2003; 15(5):547-556. (Pubitemid 37176963)
42. Moser M, et al. Kindlin-3 is required for β2 integrin-mediated leukocyte adhesion to endothelial cells. Nat Med. 2009;15(3):300-305.
43. Lim J, Wiedemann A, Tzircotis G, Monkley SJ, Critchley DR, Caron E. An essential role for talin during alpha(M)beta(2)-mediated phagocytosis. Mol Biol Cell. 2007;18(3):976-985. (Pubitemid 46399501)
44. Marchi S, et al. Akt kinase reducing endoplasmic reticulum Ca2+ release protects cells from Ca2+-dependent apoptotic stimuli. Biochem Biophys Res Commun. 2008;375(4):501-505.
45. Hogan PG, Lewis RS, Rao A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol. 2010;28:491-533.
46. Chang J, Patton JT, Sarkar A, Ernst B, Magnani JL, Frenette PS. GMI-1070, a novel pan-selectin antagonist, reverses acute vascular occlusions in sickle cell mice. Blood. 2010;116(10):1779-1786.
47. Cho H, et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science. 2001; 292(5522):1728-1731. (Pubitemid 32506248)
48. Chen WS, et al. Leptin deficiency and beta-cell dysfunction underlie type 2 diabetes in compound Akt knockout mice. Mol Cell Biol. 2009; 29(11):3151-3162.
49. Mickelson JK, Lakkis NM, Villarreal-Levy G, Hughes BJ, Smith CW. Leukocyte activation with platelet adhesion after coronary angioplasty: a mechanism for recurrent disease? J Am Coll Cardiol. 1996; 28(2):345-353. (Pubitemid 26274326)
50. Chen WS, et al. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 2001;15(17):2203-2208. (Pubitemid 32843832)
51. Peng XD, et al. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 2003;17(11):1352-1365.
52. Ware J, Russell S, Ruggeri ZM. Generation and rescue of a murine model of platelet dysfunction: the Bernard-Soulier syndrome. Proc Natl Acad Sci U S A. 2000;97(6):2803-2808. (Pubitemid 30159252)
53. Kim KH, Barazia A, Cho J. Real-time imaging of heterotypic platelet-neutrophil interactions on the activated endothelium during vascular inflammation and thrombus Formation in live mice. J Vis Exp. 2013;(74).