Protective role of insulin-like growth factor-1 receptor in endothelial cells against unilateral ureteral obstruction - Induced renal fibrosis

American Journal of Pathology

Volumn 185, Issue 5, 2015, Pages 1234-1250

  Liang, Ming ^a,b   Woodard, Lauren E ^c   Liang, Anlin ^b   Luo, Jinlong ^b   Wilson, Matthew H ^c   Mitch, William E ^b   Cheng, Jizhong ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; COLLAGEN TYPE 1; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FIBRONECTIN; HYDROGEN PEROXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1 ANTIBODY; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR CELL ADHESION MOLECULE 1; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; BLOOD VESSEL PERMEABILITY; CELL ADHESION; CELL DENSITY; CELL FUNCTION; CELL INFILTRATION; CELL JUNCTION; CELL LEVEL; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL STRUCTURE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME STABILITY; GENE OVEREXPRESSION; GENE SILENCING; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY FIBROSIS; KIDNEY INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TRANSPOSON; UPREGULATION; URETER OBSTRUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHRONIC KIDNEY FAILURE; DISEASE MODEL; FIBROSIS; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UMBILICAL VEIN; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FIBROSIS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; POLYMERASE CHAIN REACTION; RECEPTOR, IGF TYPE 1; RENAL INSUFFICIENCY, CHRONIC; TRANSFECTION; UMBILICAL VEINS; URETERAL OBSTRUCTION;

EID: 84928027546     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.01.027     Document Type: Article

References (55)

1. A.J. Collins, R.N. Foley, C. Herzog, B.M. Chavers, D. Gilbertson, and A. Ishani et al. Excerpts from the US Renal Data System 2009 Annual Data Report Am J Kidney Dis 55 2010 S1 S420 A426-427
2. M. Feletou, and P.M. Vanhoutte Endothelial dysfunction: a multifaceted disorder (the wiggers award lecture) Am J Physiol Heart Circ Physiol 291 2006 H985 H1002
3. J.E. Deanfield, J.P. Halcox, and T.J. Rabelink Endothelial function and dysfunction: testing and clinical relevance Circulation 115 2007 1285 1295
4. W. Kim, S.O. Moon, S.Y. Lee, K.Y. Jang, C.H. Cho, G.Y. Koh, K.S. Choi, K.H. Yoon, M.J. Sung, D.H. Kim, S. Lee, K.P. Kang, and S.K. Park Comp-angiopoietin-1 ameliorates renal fibrosis in a unilateral ureteral obstruction model J Am Soc Nephrol 17 2006 2474 2483
5. M. Pollak Insulin-like growth factor physiology and cancer risk Eur J Cancer 36 2000 1224 1228
6. R. Mitsui, J. Fujita-Yoshigaki, T. Narita, M. Matsuki-Fukushima, K. Satoh, B. Qi, M.Y. Guo, O. Katsumata-Kato, and H. Sugiya Maintenance of paracellular barrier function by insulin-like growth factor-I in submandibular gland cells Arch Oral Biol 55 2010 963 969
7. S.I. Chisalita, and H.J. Arnqvist Insulin-like growth factor I receptors are more abundant than insulin receptors in human micro- and macrovascular endothelial cells Am J Physiol Endocrinol Metab 286 2004 E896 E901
8. G. Pandini, F. Frasca, R. Mineo, L. Sciacca, R. Vigneri, and A. Belfiore Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved J Biol Chem 277 2002 39684 39695
9. F. Paneni, J.A. Beckman, M.A. Creager, and F. Cosentino Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I Eur Heart J 34 2013 2436 2443
10. P.E. Spoerri, E.A. Ellis, R.W. Tarnuzzer, and M.B. Grant Insulin-like growth factor: receptor and binding proteins in human retinal endothelial cell cultures of diabetic and non-diabetic origin Growth Horm IGF Res 8 1998 125 132
11. E. Dejana, F. Orsenigo, and M.G. Lampugnani The role of adherens junctions and VE-cadherin in the control of vascular permeability J Cell Sci 121 2008 2115 2122
12. J. Cheng, and J. Du Mechanical stretch simulates proliferation of venous smooth muscle cells through activation of the insulin-like growth factor-1 receptor Arterioscler Thromb Vasc Biol 27 2007 1744 1751
13. M. Holzenberger, J. Dupont, B. Ducos, P. Leneuve, A. Geloen, P.C. Even, P. Cervera, and Y. Le Bouc Igf-1 receptor regulates lifespan and resistance to oxidative stress in mice Nature 421 2003 182
14. M. Liang, A. Liang, Y. Wang, J. Jiang, and J. Cheng Smooth muscle cells from the anastomosed artery are the major precursors for neointima formation in both artery and vein grafts Basic Res Cardiol 109 2014 431
15. S.K. Saridey, L. Liu, J.E. Doherty, A. Kaja, D.L. Galvan, B.S. Fletcher, and M.H. Wilson Piggybac transposon-based inducible gene expression in vivo after somatic cell gene transfer Mol Ther 17 2009 2115 2120
16. A. Liang, Y. Wang, L.E. Woodard, M.H. Wilson, R. Sharma, Y.C. Awasthi, J. Du, W.E. Mitch, and J. Cheng Loss of glutathione S-transferase A4 accelerates obstruction-induced tubule damage and renal fibrosis J Pathol 228 2012 448 458
17. J. Cheng, L.D. Truong, X. Wu, D. Kuhl, F. Lang, and J. Du Serum- and glucocorticoid-regulated kinase 1 is upregulated following unilateral ureteral obstruction causing epithelial-mesenchymal transition Kidney Int 78 2010 668 678
18. A. Liang, Y. Wang, G. Han, L. Truong, and J. Cheng Chronic kidney disease accelerates endothelial barrier dysfunction in a mouse model of an arteriovenous fistula Am J Physiol Renal Physiol 304 2013 F1413 F1420
19. J. Cheng, Y. Wang, A. Liang, L. Jia, and J. Du Fsp-1 silencing in bone marrow cells suppresses neointima formation in vein graft Circ Res 110 2012 230 240
20. A.J. Nappi, and E. Vass Hydrogen peroxide production in immune-reactive drosophila melanogaster J Parasitol 84 1998 1150 1157
21. C.J. Jackson, P.K. Garbett, B. Nissen, and L. Schrieber Binding of human endothelium to Ulex europaeus I-coated Dynabeads: application to the isolation of microvascular endothelium J Cell Sci 96 Pt 2 1990 257 262
22. S. McGinn, P. Poronnik, E.D. Gallery, and C.A. Pollock A method for the isolation of glomerular and tubulointerstitial endothelial cells and a comparison of characteristics with the human umbilical vein endothelial cell model Nephrology (Carlton) 9 2004 229 237
23. M. Fernández, A. Medina, F. Santos, E. Carbajo, J. Rodriguez, J. Alvarez, and A. Cobo Exacerbated inflammatory response induced by insulin-like growth factor I treatment in rats with ischemic acute renal failure J Am Soc Nephrol 12 2001 1900 1907
24. J.A. Alva, A.C. Zovein, A. Monvoisin, T. Murphy, A. Salazar, N.L. Harvey, P. Carmeliet, and M.L. Iruela-Arispe VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells Dev Dyn 235 2006 759 767
25. F. Orsenigo, C. Giampietro, A. Ferrari, M. Corada, A. Galaup, S. Sigismund, G. Ristagno, L. Maddaluno, G.Y. Koh, D. Franco, V. Kurtcuoglu, D. Poulikakos, P. Baluk, D. McDonald, M. Grazia Lampugnani, and E. Dejana Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo Nat Commun 3 2012 1208
26. E. Monaghan-Benson, and K. Burridge The regulation of vascular endothelial growth factor-induced microvascular permeability requires rac and reactive oxygen species J Biol Chem 284 2009 25602 25611
27. F.E. Nwariaku, Z. Liu, X. Zhu, D. Nahari, C. Ingle, R.F. Wu, Y. Gu, G. Sarosi, and L.S. Terada NADPH oxidase mediates vascular endothelial cadherin phosphorylation and endothelial dysfunction Blood 104 2004 3214 3220
28. M. Hayashi, A. Majumdar, X. Li, J. Adler, Z. Sun, S. Vertuani, C. Hellberg, S. Mellberg, S. Koch, A. Dimberg, G.Y. Koh, E. Dejana, H.G. Belting, M. Affolter, G. Thurston, L. Holmgren, D. Vestweber, and L. Claesson-Welsh VE-PTP regulates VEGFR2 activity in stalk cells to establish endothelial cell polarity and lumen formation Nat Commun 4 2013 1672
29. M.H. Wilson, C.J. Coates, and A.L. George Jr. Piggybac transposon-mediated gene transfer in human cells Mol Ther 15 2007 139 145
30. D.B. Cines, E.S. Pollak, C.A. Buck, J. Loscalzo, G.A. Zimmerman, R.P. McEver, J.S. Pober, T.M. Wick, B.A. Konkle, B.S. Schwartz, E.S. Barnathan, K.R. McCrae, B.A. Hug, A.M. Schmidt, and D.M. Stern Endothelial cells in physiology and in the pathophysiology of vascular disorders Blood 91 1998 3527 3561
31. N. Jourde-Chiche, L. Dou, C. Cerini, F. Dignat-George, and P. Brunet Vascular incompetence in dialysis patients: protein-bound uremic toxins and endothelial dysfunction Semin Dial 24 2011 327 337
32. P. Libby, P.M. Ridker, and A. Maseri Inflammation and atherosclerosis Circulation 105 2002 1135 1143
33. C. Schrimpf, C. Xin, G. Campanholle, S.E. Gill, W. Stallcup, S.L. Lin, G.E. Davis, S.A. Gharib, B.D. Humphreys, and J.S. Duffield Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury J Am Soc Nephrol 23 2012 868 883
34. Y. Furukawa, A. Matsumori, N. Ohashi, T. Shioi, K. Ono, A. Harada, K. Matsushima, and S. Sasayama Anti-monocyte chemoattractant protein-1/monocyte chemotactic and activating factor antibody inhibits neointimal hyperplasia in injured rat carotid arteries Circ Res 84 1999 306 314
35. A. Zernecke, A. Schober, I. Bot, P. von Hundelshausen, E.A. Liehn, B. Möpps, M. Mericskay, P. Gierschik, E.A. Biessen, and C. Weber SDF-1α/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells Circ Res 96 2005 784 791
36. M. Bjarnegård, M. Enge, J. Norlin, S. Gustafsdottir, S. Fredriksson, A. Abramsson, M. Takemoto, E. Gustafsson, R. Fässler, and C. Betsholtz Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities Development 131 2004 1847 1857
37. M. Serradell, M. Diaz-Ricart, A. Cases, M.J. Zurbano, J. Lopez-Pedret, O. Arranz, A. Ordinas, and G. Escolar Uremic medium causes expression, redistribution and shedding of adhesion molecules in cultured endothelial cells Haematologica 87 2002 1053 1061
38. N.D. Vaziri, Z. Ni, F. Oveisi, K. Liang, and R. Pandian Enhanced nitric oxide inactivation and protein nitration by reactive oxygen species in renal insufficiency Hypertension 39 2002 135 141
39. R. Wever, P. Boer, M. Hijmering, E. Stroes, M. Verhaar, J. Kastelein, K. Versluis, F. Lagerwerf, H. van Rijn, H. Koomans, and T. Rabelink Nitric oxide production is reduced in patients with chronic renal failure Arterioscler Thromb Vasc Biol 19 1999 1168 1172
40. P. Delafontaine, Y.H. Song, and Y. Li Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels Arterioscler Thromb Vasc Biol 24 2004 435 444
41. E. Conti, C. Carrozza, E. Capoluongo, M. Volpe, F. Crea, C. Zuppi, and F. Andreotti Insulin-like growth factor-1 as a vascular protective factor Circulation 110 2004 2260 2265
42. A. Nadjar, O. Berton, S. Guo, P. Leneuve, S. Dovero, E. Diguet, F. Tison, B. Zhao, M. Holzenberger, and E. Bezard IGF-1 signaling reduces neuro-inflammatory response and sensitivity of neurons to MPTP Neurobiol Aging 30 2009 2021 2030
43. F. Fleissner, and T. Thum The IGF-1 receptor as a therapeutic target to improve endothelial progenitor cell function Mol Med 14 2008 235 237
44. H. Imrie, H. Viswambharan, P. Sukumar, A. Abbas, R.M. Cubbon, N. Yuldasheva, M. Gage, J. Smith, S. Galloway, A. Skromna, S.T. Rashid, T.S. Futers, S. Xuan, V.K. Gatenby, P.J. Grant, K.M. Channon, D.J. Beech, S.B. Wheatcroft, and M.T. Kearney Novel role of the IGF-1 receptor in endothelial function and repair: studies in endothelium-targeted IGF-1 receptor transgenic mice Diabetes 61 2012 2359 2368
45. K. Bäck, R. Islam, G.S. Johansson, S.I. Chisalita, and H.J. Arnqvist Insulin and IGF1 receptors in human cardiac microvascular endothelial cells: metabolic, mitogenic and anti-inflammatory effects J Endocrinol 215 2012 89 96
46. R. Troncoso, C. Ibarra, J.M. Vicencio, E. Jaimovich, and S. Lavandero New insights into IGF-1 signaling in the heart Trends Endocrinol Metab 25 2014 128 137
47. L. Zhang, X.H. Wang, H. Wang, J. Du, and W.E. Mitch Satellite cell dysfunction and impaired IGF-1 signaling cause CKD-induced muscle atrophy J Am Soc Nephrol 21 2010 419 427
48. R. Benedito, C. Roca, I. Sorensen, S. Adams, A. Gossler, M. Fruttiger, and R.H. Adams The notch ligands dll4 and jagged1 have opposing effects on angiogenesis Cell 137 2009 1124 1135
49. Y. Wang, A. Liang, J. Luo, M. Liang, G. Han, W.E. Mitch, and J. Cheng Blocking Notch in endothelial cells prevents arteriovenous fistula failure despite CKD J Am Soc Nephrol 25 2014 773 783
50. P.P. Kapitsinou, H. Sano, M. Michael, H. Kobayashi, O. Davidoff, A. Bian, B. Yao, M.Z. Zhang, R.C. Harris, K.J. Duffy, C.L. Erickson-Miller, T.A. Sutton, and V.H. Haase Endothelial HIF-2 mediates protection and recovery from ischemic kidney injury J Clin Invest 124 2014 2396 2409
51. E. Dejana, and C. Giampietro Vascular endothelial-cadherin and vascular stability Curr Opin Hematol 19 2012 218 223
52. D. Vestweber, M. Winderlich, G. Cagna, and A.F. Nottebaum Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player Trends Cell Biol 19 2009 8 15
53. C.N. Hao, Y.J. Geng, F. Li, T. Yang, D.F. Su, J.L. Duan, and Y. Li Insulin-like growth factor-1 receptor activation prevents hydrogen peroxide-induced oxidative stress, mitochondrial dysfunction and apoptosis Apoptosis 16 2011 1118 1127
54. A. Canonici, W. Steelant, V. Rigot, A. Khomitch-Baud, H. Boutaghou-Cherid, E. Bruyneel, F. Van Roy, F. Garrouste, G. Pommier, and F. André Insulin-like growth factor-I receptor, E-cadherin and αv integrin form a dynamic complex under the control of α-catenin Int J Cancer 122 2008 572 582
55. P.A. Pennisi, V. Barr, N.P. Nunez, B. Stannard, and D. Le Roith Reduced expression of insulin-like growth factor I receptors in MCF-7 breast cancer cells leads to a more metastatic phenotype Cancer Res 62 2002 6529 6537