Role of Axl in T-Lymphocyte Survival in Salt-Dependent Hypertension

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 8, 2016, Pages 1638-1646

  Batchu, Sri N ^a   Hughson, Angie ^a   Wadosky, Kristine M ^a   Morrell, Craig N ^a   Fowell, Deborah J ^a   Korshunov, Vyacheslav A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

apoptosis; Axl receptor tyrosine kinase; hypertension; lymphocyte; vascular remodeling

Indexed keywords

AXL RECEPTOR TYROSINE KINASE; DEOXYCORTICOSTERONE ACETATE; GAMMA INTERFERON; INTERLEUKIN 4; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; ONCOPROTEIN; RAG-1 PROTEIN; SALT INTAKE;

ADOPTIVE TRANSFER; ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD; BONE MARROW; CD4+ T LYMPHOCYTE; CELL COUNT; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CIRCULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HELPER CELL; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; INTERFERON PRODUCTION; LEUKOCYTE; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAG1-/- MOUSE; T LYMPHOCYTE; VASCULAR REMODELING; ANIMAL; BLOOD PRESSURE; CELL CULTURE; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; GENETICS; GENOTYPE; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; SALT INTAKE; SIGNAL TRANSDUCTION; TIME FACTOR; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; BLOOD PRESSURE; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DESOXYCORTICOSTERONE ACETATE; DISEASE MODELS, ANIMAL; GENOTYPE; HOMEODOMAIN PROTEINS; HYPERTENSION; INTERFERON-GAMMA; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; MALE; MICE, KNOCKOUT; PHENOTYPE; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SODIUM CHLORIDE, DIETARY; TIME FACTORS; VASCULAR REMODELING;

EID: 84976528627     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.307848     Document Type: Article

References (40)

1. Lu Q, Gore M, Zhang Q, Camenisch T, Boast S, Casagranda F, Lai C, Skinner MK, Klein R, Matsushima GK, Earp HS, Goff SP, Lemke G. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature. 1999;398:723-728. doi: 10. 1038/19554
2. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C, Mattsson K, Fisher J, Gies DR, Jones PF. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell. 1995;80:661-670
3. Angelillo-Scherrer A, de Frutos P, Aparicio C, Melis E, Savi P, Lupu F, Arnout J, Dewerchin M, Hoylaerts M, Herbert J, Collen D, Dahlbäck B, Carmeliet P. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat Med. 2001;7:215-221. doi: 10. 1038/84667
4. Angelillo-Scherrer A, Burnier L, Flores N, et al. Role of Gas6 receptors in platelet signaling during thrombus stabilization and implications for antithrombotic therapy. J Clin Invest. 2005;115:237-246. doi: 10. 1172/ JCI22079
5. Lu Q, Lemke G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science. 2001;293:306-311. doi: 10. 1126/science. 1061663
6. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol. 2008;8:327-336. doi: 10. 1038/nri2303
7. Neubauer A, Fiebeler A, Graham DK, O'Bryan JP, Schmidt CA, Barckow P, Serke S, Siegert W, Snodgrass HR, Huhn D. Expression of axl, a transforming receptor tyrosine kinase, in normal and malignant hematopoiesis. Blood. 1994;84:1931-1941
8. Ghosh AK, Secreto C, Boysen J, Sassoon T, Shanafelt TD, Mukhopadhyay D, Kay NE. The novel receptor tyrosine kinase Axl is constitutively active in B-cell chronic lymphocytic leukemia and acts as a docking site of nonreceptor kinases: implications for therapy. Blood. 2011;117:1928-1937. doi: 10. 1182/blood-2010-09-305649
9. Brandao LN, Winges A, Christoph S, Sather S, Migdall-Wilson J, Schlegel J, McGranahan A, Gao D, Liang X, Deryckere D, Graham DK. Inhibition of MerTK increases chemosensitivity and decreases oncogenic potential in T-cell acute lymphoblastic leukemia. Blood Cancer J. 2013;3:e101. doi: 10. 1038/bcj. 2012. 46
10. Cabezón R, Carrera-Silva EA, Flórez-Grau G, Errasti AE, Calderón-Gómez E, Lozano JJ, España C, Ricart E, Panés J, Rothlin CV, Benítez-Ribas D. MERTK as negative regulator of human T cell activation. J Leukoc Biol. 2015;97:751-760. doi: 10. 1189/jlb. 3A0714-334R
11. Huan T, Meng Q, Saleh MA, et al. Integrative network analysis reveals molecular mechanisms of blood pressure regulation. Mol Syst Biol. 2015;11:799
12. Yagil C, Hubner N, Monti J, Schulz H, Sapojnikov M, Luft FC, Ganten D, Yagil Y. Identification of hypertension-related genes through an integrated genomic-transcriptomic approach. Circ Res. 2005;96:617-625. doi: 10. 1161/01. RES. 0000160556. 52369. 61
13. Korshunov VA, Daul M, Massett MP, Berk BC. Axl mediates vascular remodeling induced by deoxycorticosterone acetate-salt hypertension. Hypertension. 2007;50:1057-1062. doi: 10. 1161/ HYPERTENSIONAHA. 107. 096289
14. Park JK, Theuer S, Kirsch T, Lindschau C, Klinge U, Heuser A, Plehm R, Todiras M, Carmeliet P, Haller H, Luft FC, Muller DN, Fiebeler A. Growth arrest specific protein 6 participates in DOCA-induced target-organ damage. Hypertension. 2009;54:359-364. doi: 10. 1161/ HYPERTENSIONAHA. 109. 129460
15. Batchu SN, Hughson A, Gerloff J, Fowell DJ, Korshunov VA. Role of Axl in early kidney inflammation and progression of salt-dependent hypertension. Hypertension. 2013;62:302-309. doi: 10. 1161/ HYPERTENSIONAHA. 113. 01382
16. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204:2449-2460. doi: 10. 1084/jem. 20070657
17. Itani HA, Xiao L, Saleh MA, et al. CD70 exacerbates blood pressure elevation and renal damage in response to repeated hypertensive stimuli. Circ Res. 2016;118:1233-1243. doi: 10. 1161/CIRCRESAHA. 115. 308111
18. Ye F, Han L, Lu Q, Dong W, Chen Z, Shao H, Kaplan HJ, Li Q, Lu Q. Retinal self-antigen induces a predominantly Th1 effector response in Axl and Mertk double-knockout mice. J Immunol. 2011;187:4178-4186. doi: 10. 4049/jimmunol. 1101201
19. Korshunov VA. Axl-dependent signalling: a clinical update. Clin Sci (Lond). 2012;122:361-368. doi: 10. 1042/CS20110411
20. Rothlin CV, Lemke G. TAM receptor signaling and autoimmune disease. Curr Opin Immunol. 2010;22:740-746. doi: 10. 1016/j. coi. 2010. 10. 001
21. Deng T, Zhang Y, Chen Q, Yan K, Han D. Toll-like receptor-mediated inhibition of Gas6 and ProS expression facilitates inflammatory cytokine production in mouse macrophages. Immunology. 2012;135:40-50. doi: 10. 1111/j. 1365-2567. 2011. 03511. x
22. van den Brand BT, Abdollahi-Roodsaz S, Vermeij EA, Bennink MB, Arntz OJ, Rothlin CV, van den Berg WB, van de Loo FA. Therapeutic efficacy of Tyro3, Axl, and Mer tyrosine kinase agonists in collagen-induced arthritis. Arthritis Rheum. 2013;65:671-680. doi: 10. 1002/art. 37786
23. Zheng S, Hedl M, Abraham C. TAM receptor-dependent regulation of SOCS3 and MAPKs contributes to proinflammatory cytokine downregulation following chronic NOD2 stimulation of human macrophages. J Immunol. 2015;194:1928-1937. doi: 10. 4049/jimmunol. 1401933
24. Gerloff J, Korshunov VA. Immune modulation of vascular resident cells by Axl orchestrates carotid intima-media thickening. Am J Pathol. 2012;180:2134-2143. doi: 10. 1016/j. ajpath. 2012. 01. 036
25. Batchu SN, Xia J, Ko KA, Doyley MM, Abe J, Morrell CN, Korshunov VA. Axl modulates immune activation of smooth muscle cells in vein graft remodeling. Am J Physiol Heart Circ Physiol. 2015;309:H1048-H1058. doi: 10. 1152/ajpheart. 00495. 2015
26. Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, Cohen PL, Earp HS, Matsushima GK. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 2001;411:207-211. doi: 10. 1038/35075603
27. Wan E, Yeap XY, Dehn S, et al. Enhanced efferocytosis of apoptotic cardiomyocytes through myeloid-epithelial-reproductive tyrosine kinase links acute inflammation resolution to cardiac repair after infarction. Circ Res. 2013;113:1004-1012. doi: 10. 1161/CIRCRESAHA. 113. 301198
28. Bommhardt U, Chang KC, Swanson PE, Wagner TH, Tinsley KW, Karl IE, Hotchkiss RS. Akt decreases lymphocyte apoptosis and improves survival in sepsis. J Immunol. 2004;172:7583-7591
29. Ray JP, Staron MM, Shyer JA, Ho PC, Marshall HD, Gray SM, Laidlaw BJ, Araki K, Ahmed R, Kaech SM, Craft J. The interleukin-2-mTORc1 kinase axis defines the signaling, differentiation, and metabolism of T helper 1 and follicular B helper T cells. Immunity. 2015;43:690-702. doi: 10. 1016/j. immuni. 2015. 08. 017
30. Arimura Y, Shiroki F, Kuwahara S, Kato H, Dianzani U, Uchiyama T, Yagi J. Akt is a neutral amplifier for Th cell differentiation. J Biol Chem. 2004;279:11408-11416. doi: 10. 1074/jbc. M309063200
31. Kawasaki H, Komai K, Ouyang Z, Murata M, Hikasa M, Ohgiri M, Shiozawa S. c-Fos/activator protein-1 transactivates wee1 kinase at G(1)/S to inhibit premature mitosis in antigen-specific Th1 cells. EMBO J. 2001;20:4618-4627. doi: 10. 1093/emboj/20. 16. 4618
32. Wilson C, Ye X, Pham T, Lin E, Chan S, McNamara E, Neve RM, Belmont L, Koeppen H, Yauch RL, Ashkenazi A, Settleman J. AXL inhibition sensitizes mesenchymal cancer cells to antimitotic drugs. Cancer Res. 2014;74:5878-5890. doi: 10. 1158/0008-5472. CAN-14-1009
33. Kirabo A, Fontana V, de Faria AP, et al. DC isoketal-modified proteins activate T cells and promote hypertension. J Clin Invest. 2014;124:4642-4656. doi: 10. 1172/JCI74084
34. Wang J, Tao YM, Cheng XY, Zhu TF, Chen ZF, Yao H, Su LX. Dendritic cells derived from preeclampsia patients influence Th1/Th17 cell differentiation in vitro. Int J Clin Exp Med. 2014;7:5303-5309
35. Trott DW, Thabet SR, Kirabo A, Saleh MA, Itani H, Norlander AE, Wu J, Goldstein A, Arendshorst WJ, Madhur MS, Chen W, Li CI, Shyr Y, Harrison DG. Oligoclonal CD8+ T cells play a critical role in the development of hypertension. Hypertension. 2014;64:1108-1115. doi: 10. 1161/ HYPERTENSIONAHA. 114. 04147
36. Magen E, Feldman A, Cohen Z, Alon DB, Minz E, Chernyavsky A, Linov L, Mishal J, Schlezinger M, Sthoeger Z. Circulating endothelial progenitor cells, Th1/Th2/Th17-related cytokines, and endothelial dysfunction in resistant hypertension. Am J Med Sci. 2010;339:117-122. doi: 10. 1097/ MAJ. 0b013e3181c6a968
37. Devallière J, Charreau B. The adaptor Lnk (SH2B3): an emerging regulator in vascular cells and a link between immune and inflammatory signaling. Biochem Pharmacol. 2011;82:1391-1402. doi: 10. 1016/j. bcp. 2011. 06. 023
38. Saleh MA, McMaster WG, Wu J, et al. Lymphocyte adaptor protein LNK deficiency exacerbates hypertension and end-organ inflammation. J Clin Invest. 2015;125:1189-1202. doi: 10. 1172/JCI76327
39. Batchu SN, Smolock EM, Dyachenko IA, Murashev AN, Korshunov VA. Autonomic dysfunction determines stress-induced cardiovascular and immune complications in mice. J Am Heart Assoc. 2015;4:e001952. doi: 10. 1161/JAHA. 115. 001952
40. Chan CT, Sobey CG, Lieu M, et al. Obligatory Role for B Cells in the Development of Angiotensin II-Dependent Hypertension. Hypertension. 2015;66:1023-1033. doi: 10. 1161/HYPERTENSIONAHA. 115. 05779