Tie1 controls angiopoietin function in vascular remodeling and inflammation

Journal of Clinical Investigation

Volumn 126, Issue 9, 2016, Pages 3495-3510

  Korhonen, Emilia A ^a   Lampinen, Anita ^a   Giri, Hemant ^a   Anisimov, Andrey ^a   Kim, Minah ^b   Allen, Breanna ^b   Fang, Shentong ^a   D'Amico, Gabriela ^a   Sipilä, Tuomas J ^a   Lohela, Marja ^a   Strandin, Tomas ^a   Vaheri, Antti ^a   Ylä Herttuala, Seppo ^c   Koh, Gou Young ^d   McDonald, Donald M ^b   Alitalo, Kari ^a   Saharinen, Pipsa ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; BETA1 INTEGRIN; PROTEIN KINASE B; TIE 1 RECEPTOR; TRANSCRIPTION FACTOR FKHR; VASCULAR ENDOTHELIAL CADHERIN; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL JUNCTION; ENDOTHELIUM CELL; ENDOTOXEMIA; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRACHEAL BLOOD VESSEL; TRANSCRIPTION INITIATION; VASCULAR REMODELING; ADULT; AGED; ANIMAL; CASE CONTROL STUDY; CHEMISTRY; COHORT ANALYSIS; GENE DELETION; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; SEPSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; YOUNG ADULT;

ADULT; AGED; ANGIOPOIETIN-1; ANGIOPOIETIN-2; ANIMALS; ANTIGENS, CD29; CASE-CONTROL STUDIES; COHORT STUDIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENDOTOXEMIA; FEMALE; GENE DELETION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; PHOSPHORYLATION; RECEPTOR, TIE-1; RECEPTOR, TIE-2; SEPSIS; SIGNAL TRANSDUCTION; VASCULAR REMODELING; YOUNG ADULT;

EID: 84987818362     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI84923     Document Type: Article

References (84)

1. Hu J, et al. Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat. Science. 2014;343(6169):416-419
2. Ramasamy SK, Kusumbe AP, Adams RH. Regulation of tissue morphogenesis by endothelial cell-derived signals. Trends Cell Biol. 2015;25(3):148-157
3. Jeltsch M, Leppänen VM, Saharinen P, Alitalo K. Receptor tyrosine kinase-mediated angiogenesis. Cold Spring Harb Perspect Biol. 2013;5(9):a009183
4. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009;10(3):165-177
5. Saharinen P, Jeltsch M, Santoyo MM, Leppänen VM, Alitalo K. The TIE Receptor Family. In: Wheeler DE, Yarden Y, eds. Receptor Tyrosine Kinases: Family and Subfamilies. Springer International Publishing Switzerland; 2015:743-775
6. Partanen J, et al. A novel endothelial cell surface receptor tyrosine kinase with extracellular epidermal growth factor homology domains. Mol Cell Biol. 1992;12(4):1698-1707
7. Dumont DJ, Yamaguchi TP, Conlon RA, Rossant J, Breitman ML. tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene. 1992;7(8):1471-1480
8. Davis S, et al. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996;87(7):1161-1169
9. Maisonpierre PC, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277(5322):55-60
10. Daly C, et al. Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev. 2004;18(9):1060-1071
11. Zhang X, et al. Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J Biol Chem. 2002;277(47):45276-45284
12. Wilhelm K, et al. FOXO1 couples metabolic activity and growth state in the vascular endothelium. Nature. 2016;529(7585):216-220
13. Puri MC, Partanen J, Rossant J, Bernstein A. Interaction of the TEK and TIE receptor tyrosine kinases during cardiovascular development. Development. 1999;126(20):4569-4580
14. Jeansson M, et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest. 2011;121(6):2278-2289
15. Puri MC, Rossant J, Alitalo K, Bernstein A, Partanen J. The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells. EMBO J. 1995;14(23):5884-5891
16. D'Amico G, Korhonen EA, Waltari M, Saharinen P, Laakkonen P, Alitalo K. Loss of endothelial Tie1 receptor impairs lymphatic vessel development-brief report. Arterioscler Thromb Vasc Biol. 2010;30(2):207-209
17. Qu X, Tompkins K, Batts LE, Puri M, Baldwin HS. Abnormal embryonic lymphatic vessel development in Tie1 hypomorphic mice. Development. 2010;137(8):1285-1295
18. Shen B, et al. Genetic dissection of tie pathway in mouse lymphatic maturation and valve development. Arterioscler Thromb Vasc Biol. 2014;34(6):1221-1230
19. Qu X, Zhou B, Scott Baldwin H. Tie1 is required for lymphatic valve and collecting vessel development. Dev Biol. 2015;399(1):117-128
20. D'Amico G, et al. Tie1 deletion inhibits tumor growth and improves angiopoietin antagonist therapy. J Clin Invest. 2014;124(2):824-834
21. Savant S, et al. The Orphan Receptor Tie1 Controls Angiogenesis and Vascular Remodeling by Differentially Regulating Tie2 in Tip and Stalk Cells. Cell Rep. 2015;12(11):1761-1773
22. Korhonen J, et al. Enhanced expression of the tie receptor tyrosine kinase in endothelial cells during neovascularization. Blood. 1992;80(10):2548-2555
23. Kaipainen A, et al. Enhanced expression of the tie receptor tyrosine kinase mesenger RNA in the vascular endothelium of metastatic melanomas. Cancer Res. 1994;54(24):6571-6577
24. Chan B, Sukhatme VP. Suppression of Tie-1 in endothelial cells in vitro induces a change in the genome-wide expression profile reflecting an inflammatory function. FEBS Lett. 2009;583(6):1023-1028
25. Woo KV, et al. Tie1 attenuation reduces murine atherosclerosis in a dose-dependent and shear stress-specific manner. J Clin Invest. 2011;121(4):1624-1635
26. Kim KE, Cho CH, Kim HZ, Baluk P, McDonald DM, Koh GY. In vivo actions of angiopoietins on quiescent and remodeling blood and lymphatic vessels in mouse airways and skin. Arterioscler Thromb Vasc Biol. 2007;27(3):564-570
27. Fuxe J, et al. Angiopoietin/Tie2 signaling transforms capillaries into venules primed for leukocyte trafficking in airway inflammation. Am J Pathol. 2010;176(4):2009-2018
28. Tabruyn SP, et al. Angiopoietin-2-driven vascular remodeling in airway inflammation. Am J Pathol. 2010;177(6):3233-3243
29. Le CT, et al. Synergistic actions of blocking angiopoietin-2 and tumor necrosis factor-α in suppressing remodeling of blood vessels and lymphatics in airway inflammation. Am J Pathol. 2015;185(11):2949-2968
30. Parikh SM, et al. Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med. 2006;3(3):e46
31. David S, et al. Angiopoietin-2 may contribute to multiple organ dysfunction and death in sepsis. Crit Care Med. 2012;40(11):3034-3041
32. Ziegler T, et al. Angiopoietin 2 mediates microvascular hemodynamic alterations in sepsis. J Clin Invest. 2013;123(8):3436-3445
33. David S, et al. Acute administration of recombinant Angiopoietin-1 ameliorates multiple-organ dysfunction syndrome and improves survival in murine sepsis. Cytokine. 2011;55(2):251-259
34. McCarter SD, et al. Cell-based angiopoietin-1 gene therapy for acute lung injury. Am J Respir Crit Care Med. 2007;175(10):1014-1026
35. Ghosh CC, et al. Gene control of tyrosine kinase TIE2 and vascular manifestations of infections. Proc Natl Acad Sci U S A. 2016;113(9):2472-2477
36. Syrjälä SO, et al. Angiopoietin-2 inhibition prevents transplant ischemia-reperfusion injury and chronic rejection in rat cardiac allografts. Am J Transplant. 2014;14(5):1096-1108
37. Hammes HP, et al. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes. 2004;53(4):1104-1110
38. Felcht M, et al. Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J Clin Invest. 2012;122(6):1991-2005
39. Park SW, Yun JH, Kim JH, Kim KW, Cho CH, Kim JH. Angiopoietin 2 induces pericyte apoptosis via α3β1 integrin signaling in diabetic retinopathy. Diabetes. 2014;63(9):3057-3068
40. Hakanpaa L, et al. Endothelial destabilization by angiopoietin-2 via integrin β1 activation. Nat Commun. 2015;6:5962
41. Cascone I, Napione L, Maniero F, Serini G, Bussolino F. Stable interaction between α5β1 integrin and Tie2 tyrosine kinase receptor regulates endothelial cell response to Ang-1. J Cell Biol. 2005;170(6):993-1004
42. Saharinen P, et al. Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie2. J Cell Biol. 2005;169(2):239-243
43. Yuan HT, et al. Activation of the orphan endothelial receptor Tie1 modifies Tie2-mediated intracellular signaling and cell survival. FASEB J. 2007;21(12):3171-3183
44. Fukuhara S, et al. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol. 2008;10(5):513-526
45. Saharinen P, et al. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol. 2008;10(5):527-537
46. Kontos CD, Cha EH, York JD, Peters KG. The endothelial receptor tyrosine kinase Tie1 activates phosphatidylinositol 3-kinase and Akt to inhibit apoptosis. Mol Cell Biol. 2002;22(6):1704-1713
47. Marron MB, et al. Regulated proteolytic processing of Tie1 modulates ligand responsiveness of the receptor-tyrosine kinase Tie2. J Biol Chem. 2007;282(42):30509-30517
48. Seegar TC, et al. Tie1-Tie2 interactions mediate functional differences between angiopoietin ligands. Mol Cell. 2010;37(5):643-655
49. Cho CH, et al. COMP-Ang1: a designed angiopoietin-1 variant with nonleaky angiogenic activity. Proc Natl Acad Sci U S A. 2004;101(15):5547-5552
50. Holopainen T, et al. Effects of angiopoietin-2-blocking antibody on endothelial cell-cell junctions and lung metastasis. J Natl Cancer Inst. 2012;104(6):461-475
51. Kim M, Carman CV, Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science. 2003;301(5640):1720-1725
52. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PI. Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science. 2002;295(5560):1708-1711
53. Grecco HE, et al. In situ analysis of tyrosine phosphorylation networks by FLIM on cell arrays. Nat Methods. 2010;7(6):467-472
54. Daly C, et al. Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells. Proc Natl Acad Sci U S A. 2006;103(42):15491-15496
55. Cho CH, et al. Long-term and sustained COMP-Ang1 induces long-lasting vascular enlargement and enhanced blood flow. Circ Res. 2005;97(1):86-94
56. Mofarrahi M, Nouh T, Qureshi S, Guillot L, Mayaki D, Hussain SN. Regulation of angiopoietin expression by bacterial lipopolysaccharide. Am J Physiol Lung Cell Mol Physiol. 2008;294(5):L955-L963
57. Scholz A, Plate KH, Reiss Y. Angiopoietin-2: a multifaceted cytokine that functions in both angiogenesis and inflammation. Ann N Y Acad Sci. 2015;1347:45-51
58. Vaheri A, et al. Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol. 2013;11(8):539-550
59. Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG. Into the eye of the cytokine storm. Microbiol Mol Biol Rev. 2012;76(1):16-32
60. Singh H, Hansen TM, Patel N, Brindle NP. The molecular balance between receptor tyrosine kinases Tie1 and Tie2 is dynamically controlled by VEGF and TNFα and regulates angiopoietin signalling. PLoS ONE. 2012;7(1):e29319
61. Teichert-Kuliszewska K, et al. Biological action of angiopoietin-2 in a fibrin matrix model of angiogenesis is associated with activation of Tie2. Cardiovasc Res. 2001;49(3):659-670
62. Han S, et al. Amelioration of sepsis by TIE2 activation-induced vascular protection. Sci Transl Med. 2016;8(335):335ra55
63. Gale NW, et al. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell. 2002;3(3):411-423
64. Lee J, et al. Angiopoietin-1 guides directional angiogenesis through integrin αvβ5 signaling for recovery of ischemic retinopathy. Sci Transl Med. 2013;5(203):203ra127
65. Patan S. TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth. Microvasc Res. 1998;56(1):1-21
66. Thomson BR, et al. A lymphatic defect causes ocular hypertension and glaucoma in mice. J Clin Invest. 2014;124(10):4320-4324
67. Nätynki M, et al. Common and specific effects of Tie2 mutations causing venous malformations. Hum Mol Genet. 2015;24(22):6374-6389
68. Boscolo E, et al. Rapamycin improves TIE2-mutated venous malformation in murine model and human subjects. J Clin Invest. 2015;125(9):3491-3504
69. Yuan HT, Khankin EV, Karumanchi SA, Parikh SM. Angiopoietin 2 is a partial agonist/antagonist of Tie2 signaling in the endothelium. Mol Cell Biol. 2009;29(8):2011-2022
70. Kim M, et al. Opposing actions of angiopoietin-2 on Tie2 signaling and FOXO1 activation. J Clin Invest.2016;126(9):3511-3525
71. Kim HZ, Jung K, Kim HM, Cheng Y, Koh GY. A designed angiopoietin-2 variant, pentameric COMP-Ang2, strongly activates Tie2 receptor and stimulates angiogenesis. Biochim Biophys Acta. 2009;1793(5):772-780
72. Frye M, et al. Interfering with VE-PTP stabilizes endothelial junctions in vivo via Tie-2 in the absence of VE-cadherin. J Exp Med. 2015;212(13):2267-2287
73. Stiehl T, et al. Lung-targeted RNA interference against angiopoietin-2 ameliorates multiple organ dysfunction and death in sepsis. Crit Care Med. 2014;42(10):e654-662
74. Kurniati NF, et al. The flow dependency of Tie2 expression in endotoxemia. Intensive Care Med. 2013;39(7):1262-1271
75. Ghosh CC, et al. Drug Repurposing Screen Identifies Foxo1-Dependent Angiopoietin-2 Regulation in Sepsis. Crit Care Med. 2015;43(7):e230-e240
76. Yabkowitz R, Meyer S, Black T, Elliott G, Merewether LA, Yamane HK. Inflammatory cytokines and vascular endothelial growth factor stimulate the release of soluble tie receptor from human endothelial cells via metalloprotease activation. Blood. 1999;93(6):1969-1979
77. Karnani P, Kairemo K. The new Tie-1 monoclonal antibodies detect angiogenesis in metastatic malignancies. Clin Cancer Res. 2003; 9(10 Pt 2):3827S-3830S
78. Rasmussen AL, et al. Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance. Science. 2014;346(6212):987-991
79. Claxton S, Kostourou V, Jadeja S, Chambon P, Hodivala-Dilke K, Fruttiger M. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis. 2008;46(2):74-80
80. Wang Y, et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 2010;465(7297):483-486
81. Sun JF, et al. Microvascular patterning is controlled by fine-tuning the Akt signal. Proc Natl Acad Sci U S A. 2005;102(1):128-133
82. Sarao R, Dumont DJ. Conditional transgene expression in endothelial cells. Transgenic Res. 1998;7(6):421-427
83. Verveer PJ, Rocks O, Harpur AG, Bastiaens PI. Imaging protein interactions by FRET microscopy: FLIM measurements. CSH Protoc. 2006;2006(6): prot4599
84. Strandin T, et al. Interferons Induce STAT1-Dependent Expression of Tissue Plasminogen Activator, a Pathogenicity Factor in Puumala Hantavirus Disease. J Infect Dis. 2016;213(10):1632-1641