EphrinB2 reverse signaling protects against capillary rarefaction and fibrosis after kidney injury

Journal of the American Society of Nephrology

Volumn 24, Issue 4, 2013, Pages 559-572

  Kida, Yujiro ^a   Ieronimakis, Nicholas ^b   Schrimpf, Claudia ^a   Reyes, Morayma ^b   Duffield, Jeremy S ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN A2; EPHRIN A4; EPHRIN B2; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY BASEMENT MEMBRANE; CELL ACTIVATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; GLOMERULUS CAPILLARY; KIDNEY FIBROSIS; KIDNEY INJURY; MACROPHAGE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL PROTECTION; SIGNAL TRANSDUCTION;

EID: 84875748988     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012080871     Document Type: Article

References (39)

1. Basile DP: Rarefaction of peritubular capillaries following ischemic acute renal failure: A potential factor predisposing to progressive nephropathy. Curr Opin Nephrol Hypertens 13: 1-7, 2004
2. Eardley KS, Kubal C, Zehnder D, Quinkler M, Lepenies J, Savage CO, Howie AJ, Kaur K, Cooper MS, Adu D, Cockwell P: The role of capillary density, macrophage infiltration and interstitial scarring in the pathogenesis of human chronic kidney disease. Kidney Int 74: 495-504, 2008
3. Steegh FM, Gelens MA, Nieman FH, van Hooff JP, Cleutjens JP, van Suylen RJ, Daemen MJ, van Heurn EL, Christiaans MH, Peutz-Kootstra CJ: Early loss of peritubular capillaries after kidney transplantation. J AmSoc Nephrol 22: 1024-1029, 2011
4. Lin SL, Chang FC, Schrimpf C, Chen YT, Wu CF, Wu VC, Chiang WC, Kuhnert F, Kuo CJ, Chen YM, Wu KD, Tsai TJ, Duffield JS: Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 178: 911-923, 2011
5. Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, Davis GE, Gharib SA, Humphreys BD, Duffield JS: Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol 23: 868-883, 2012
6. Lin SL, Kisseleva T, Brenner DA, Duffield JS: Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173: 1617-1627, 2008
7. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010
8. Kida Y, Duffield JS: Pivotal role of pericytes in kidney fibrosis. Clin Exp Pharmacol Physiol 38: 467-473, 2011
9. Schrimpf C, Duffield JS: Mechanisms of fibrosis: The role of the pericyte. Curr Opin Nephrol Hypertens 20: 297-305, 2011
10. Wang HU, Chen ZF, Anderson DJ: Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93: 741-753, 1998
11. Gerety SS, Wang HU, Chen ZF, Anderson DJ: Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 4: 403-414, 1999
12. Kuijper S, Turner CJ, Adams RH: Regulation of angiogenesis by Ephephrin interactions. Trends Cardiovasc Med 17: 145-151, 2007
13. Adams RH, Diella F, Hennig S, Helmbacher F, Deutsch U, Klein R: The cytoplasmic domain of the ligand ephrinB2 is required for vascular morphogenesis but not cranial neural crest migration. Cell 104: 57-69, 2001
14. Sawamiphak S, Seidel S, Essmann CL, Wilkinson GA, Pitulescu ME, Acker T, Acker-Palmer A: Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 465: 487-491, 2010
15. Wang Y, Nakayama M, Pitulescu ME, Schmidt TS, Bochenek ML, Sakakibara A, Adams S, Davy A, Deutsch U, Lüthi U, Barberis A, Benjamin LE, Mäkinen T, Nobes CD, Adams RH: Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465: 483-486, 2010
16. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH: Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 124: 161-173, 2006
17. Salvucci O, Maric D, Economopoulou M, Sakakibara S, Merlin S, Follenzi A, Tosato G: EphrinB reverse signaling contributes to endothelial and mural cell assembly into vascular structures. Blood 114: 1707-1716, 2009
18. Palmer A, ZimmerM, Erdmann KS, Eulenburg V, Porthin A, Heumann R, Deutsch U, Klein R: EphrinB phosphorylation and reverse signaling: Regulation by Src kinases and PTP-BL phosphatase. Mol Cell 9: 725-737, 2002
19. Mäkinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA: PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19: 397-410, 2005
20. Lin SL, Castaño AP, Nowlin BT, Lupher ML Jr, Duffield JS: Bone marrow Ly6Chigh monocytes are selectively recruited to injured kidney and differentiate into functionally distinct populations. J Immunol 183: 6733-6743, 2009
21. Okazaki T, Ni A, Baluk P, Ayeni OA, Kearley J, Coyle AJ, Humbles A, McDonald DM: Capillary defects and exaggerated inflammatory response in the airways of EphA2-deficientmice. Am J Pathol 174: 2388-2399, 2009
22. Saunders WB, Bayless KJ, Davis GE: MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci 118: 2325-2340, 2005
23. Stockinger H, Gadd SJ, Eher R, Majdic O, Schreiber W, Kasinrerk W, Strass B, Schnabl E, Knapp W: Molecular characterization and functional analysis of the leukocyte surface protein CD31. J Immunol 145: 3889-3897, 1990
24. Ieronimakis N, Balasundaram G, Reyes M: Direct isolation, culture and transplant of mouse skeletal muscle derived endothelial cells with angiogenic potential. PLoS ONE 3: e0001753, 2008
25. Reinhart-King CA: Endothelial cell adhesion and migration. Methods Enzymol 443: 45-64, 2008
26. Eichmann A, Simons M: VEGF signaling inside vascular endothelial cells and beyond. Curr Opin Cell Biol 24: 188-193, 2012
27. Bochenek ML, Dickinson S, Astin JW, Adams RH, Nobes CD: Ephrin-B2 regulates endothelial cell morphology and motility independently of Eph-receptor binding. J Cell Sci 123: 1235-1246, 2010
28. Cirone P, Lin S, Griesbach HL, Zhang Y, Slusarski DC, Crews CM: A role for planar cell polarity signaling in angiogenesis. Angiogenesis 11: 347-360, 2008
29. Lin D, Gish GD, Songyang Z, Pawson T: The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J Biol Chem 274: 3726-3733, 1999
30. Krempen K, Grotkopp D, Hall K, Bache A, Gillan A, Rippe RA, Brenner DA, Breindl M: Far upstream regulatory elements enhance position-independent and uterus-specific expression of the murine alpha1(I) collagen promoter in transgenic mice. Gene Expr 8: 151-163, 1999
31. Yata Y, Scanga A, Gillan A, Yang L, Reif S, Breind lM, Brenner DA, Rippe RA: DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 37: 267-276, 2003
32. Li B, Cohen A, Hudson TE, Motlagh D, Amrani DL, Duffield JS: Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury. Circulation 121: 2211-2220, 2010
33. Ichimura T, Asseldonk EJ, Humphreys BD, Gunaratnam L, Duffield JS, Bonventre JV: Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest 118: 1657-1668, 2008
34. Lin SL, Li B, Rao S, Yeo EJ, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS: MacrophageWnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 107: 4194-4199, 2010
35. Chau BN, Xin C, Hartner J, Ren S, Castano AP, Linn G, Li J, Tran PT, Kaimal V, Huang X, Chang AN, Li S, Kalra A, Grafals M, Portilla D, MacKenna DA, Orkin SH, Duffield JS: MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Sci Transl Med 4: 121ra18, 2012
36. Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB: NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 222: 218-227, 2001
37. Wang S, Li X, Parra M, Verdin E, Bassel-Duby R, Olson EN: Control of endothelial cell proliferation and migration by VEGF signaling to histone deacetylase 7. Proc Natl Acad Sci U S A 105: 7738-7743, 2008
38. Saunders WB, Bohnsack BL, Faske JB, Anthis NJ, Bayless KJ, Hirschi KK, DavisGE: Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 175: 179-191, 2006
39. Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE: Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114: 5091-5101, 2009