Peritubular capillary rarefaction: A new therapeutic target in chronic kidney disease

Pediatric Nephrology

Volumn 29, Issue 3, 2014, Pages 333-342

  Kida, Yujiro ^a   Tchao, Bie Nga ^a   Yamaguchi, Ikuyo ^a,b  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

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

Author keywords

Angiogenesis; Angiogenic growth factors; CKD; Endothelial cell; Pericytes

Indexed keywords

ANGIOGENIC PROTEINS; ANIMALS; APOPTOSIS; CAPILLARIES; CELL HYPOXIA; CELL SURVIVAL; DISEASE PROGRESSION; ENDOTHELIAL CELLS; HUMANS; KIDNEY TUBULES; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION;

EID: 84894271163     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2430-y     Document Type: Review

References (107)

1. Collins AJ, Foley RN, Chavers B, Gilbertson D, Herzog C, Johansen K, Kasiske B, Kutner N, Liu J, St Peter W, Guo H, Gustafson S, Heubner B, Lamb K, Li S, Peng Y, Qiu Y, Roberts T, Skeans M, Snyder J, Solid C, Thompson B, Wang C, Weinhandl E, Zaun D, Arko C, Chen SC, Daniels F, Ebben J, Frazier E, Hanzlik C, Johnson R, Sheets D, Wang X, Forrest B, Constantini E, Everson S, Eggers P, Agodoa L (2012) United States Renal Data System 2011 annual data report: atlas of chronic kidney disease & end-stage renal disease in the United States. Am J Kidney Dis 59(A7):e1-e420
2. Himmelfarb J, Shankland SJ (2009) Creating research infrastructure and functionality to address chronic kidney disease: the Kidney Research Institute. Semin Nephrol 29:457-466
3. Levey AS, Coresh J (2012) Chronic kidney disease. Lancet 379:165-180
4. Fine LG, Norman JT (2008) Chronic hypoxia as a mechanism of progression of chronic kidney diseases: from hypothesis to novel therapeutics. Kidney Int 74:867-872
5. Choi YJ, Chakraborty S, Nguyen V, Nguyen C, Kim BK, Shim SI, Suki WN, Truong LD (2000) Peritubular capillary loss is associated with chronic tubulointerstitial injury in human kidney: altered expression of vascular endothelial growth factor. Hum Pathol 31:1491-1497 (Pubitemid 32049007)
6. Seron D, Alexopoulos E, Raftery MJ, Hartley B, Cameron JS (1990) Number of interstitial capillary cross-sections assessed by monoclonal antibodies: relation to interstitial damage. Nephrol Dial Transplant 5:889-893
7. Bohle A, Mackensen-Haen S, Wehrmann M (1996) Significance of postglomerular capillaries in the pathogenesis of chronic renal failure. Kidney Blood Press Res 19:191-195 (Pubitemid 26379989)
8. Ishii Y, Sawada T, Kubota K, Fuchinoue S, Teraoka S, Shimizu A (2005) Injury and progressive loss of peritubular capillaries in the development of chronic allograft nephropathy. Kidney Int 67:321-332 (Pubitemid 40019255)
9. Ohashi R, Kitamura H, Yamanaka N (2000) Peritubular capillary injury during the progression of experimental glomerulonephritis in rats. J Am Soc Nephrol 11:47-56 (Pubitemid 30020425)
10. Kang DH, Joly AH, Oh SW, Hugo C, Kerjaschki D, Gordon KL, Mazzali M, Jefferson JA, Hughes J, Madsen KM, Schreiner GF, Johnson RJ (2001) Impaired angiogenesis in the remnant kidney model: I. Potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol 12:1434-1447 (Pubitemid 32666326)
11. Ohashi R, Shimizu A, Masuda Y, Kitamura H, Ishizaki M, Sugisaki Y, Yamanaka N (2002) Peritubular capillary regression during the progression of experimental obstructive nephropathy. J Am Soc Nephrol 13:1795-1805 (Pubitemid 34700604)
12. Rouschop KM, Claessen N, Pals ST, Weening JJ, Florquin S (2006) CD44 disruption prevents degeneration of the capillary network in obstructive nephropathy via reduction of TGF-beta1-induced apoptosis. J Am Soc Nephrol 17:746-753
13. Eddy AA, Lopez-Guisa JM, Okamura DM, Yamaguchi I (2012) Investigating mechanisms of chronic kidney disease in mouse models. Pediatr Nephrol 27:1233-1247
14. Yamaguchi I, Tchao BN, Burger ML, Yamada M, Hyodo T, Giampietro C, Eddy AA (2012) Vascular endothelial cadherin modulates renal interstitial fibrosis. Nephron Exp Nephrol 120:e20-e31
15. Kang DH, Anderson S, Kim YG, Mazzalli M, Suga S, Jefferson JA, Gordon KL, Oyama TT, Hughes J, Hugo C, Kerjaschki D, Schreiner GF, Johnson RJ (2001) Impaired angiogenesis in the aging kidney: vascular endothelial growth factor and thrombospondin-1 in renal disease. Am J Kidney Dis 37:601-611 (Pubitemid 32195301)
16. Basile DP, Donohoe D, Roethe K, Osborn JL (2001) Renal ischemic injury results in permanent damage to peritubular capillaries and influences long-term function. Am J Physiol Renal Physiol 281:F887-F899
17. Horbelt M, Lee SY, Mang HE, Knipe NL, Sado Y, Kribben A, Sutton TA (2007) Acute and chronic microvascular alterations in a mouse model of ischemic acute kidney injury. Am J Physiol Renal Physiol 293:F688-F695 (Pubitemid 47403338)
18. Ishani A, Xue JL, Himmelfarb J, Eggers PW, Kimmel PL, Molitoris BA, Collins AJ (2009) Acute kidney injury increases risk of ESRD among elderly. J Am Soc Nephrol 20:223-228
19. Wald R, Quinn RR, Luo J, Li P, Scales DC, Mamdani MM, Ray JG (2009) Chronic dialysis and death among survivors of acute kidney injury requiring dialysis. JAMA 302:1179-1185
20. Konda R, Sato H, Sakai K, Sato M, Orikasa S, Kimura N (1999) Expression of platelet-derived endothelial cell growth factor and its potential role in up-regulation of angiogenesis in scarred kidneys secondary to urinary tract diseases. Am J Pathol 155:1587-1597
21. Pillebout E, Burtin M, Yuan HT, Briand P, Woolf AS, Friedlander G, Terzi F (2001) Proliferation and remodeling of the peritubular microcirculation after nephron reduction: association with the progression of renal lesions. Am J Pathol 159:547-560 (Pubitemid 32751085)
22. Nyberg P, Xie L, Kalluri R (2005) Endogenous inhibitors of angiogenesis. Cancer Res 65:3967-3979 (Pubitemid 40775631)
23. Maciel TT, Coutinho EL, Soares D, Achar E, Schor N, Bellini MH (2008) Endostatin, an antiangiogenic protein, is expressed in the unilateral ureteral obstruction mice model. J Nephrol 21:753-760
24. Bellini MH, Coutinho EL, Filgueiras TC, Maciel TT, Schor N (2007) Endostatin expression in the murine model of ischaemia/reperfusion-induced acute renal failure. Nephrology (Carlton) 12:459-465 (Pubitemid 47366650)
25. Sanz AB, Santamaria B, Ruiz-Ortega M, Egido J, Ortiz A (2008) Mechanisms of renal apoptosis in health and disease. J Am Soc Nephrol 19:1634-1642
26. Winn RK, Harlan JM (2005) The role of endothelial cell apoptosis in inflammatory and immune diseases. J Thromb Haemost 3:1815-1824 (Pubitemid 41716568)
27. Dimmeler S, Assmus B, Hermann C, Haendeler J, Zeiher AM (1998) Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: involvement in suppression of apoptosis. Circ Res 83:334-341 (Pubitemid 28371324)
28. Kida Y, Duffield JS (2011) Pivotal role of pericytes in kidney fibrosis. Clin Exp Pharmacol Physiol 38:417-423
29. Grgic I, Campanholle G, Bijol V, Wang C, Sabbisetti VS, Ichimura T, Humphreys BD, Bonventre JV (2012) Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int 82:172-183
30. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298-307
31. Kottgen A, Pattaro C, Boger CA, Fuchsberger C, Olden M, Glazer NL, Parsa A, Gao X, Yang Q, Smith AV, O'Connell JR, Li M, Schmidt H, Tanaka T, Isaacs A, Ketkar S, Hwang SJ, Johnson AD, Dehghan A, Teumer A, Pare G, Atkinson EJ, Zeller T, Lohman K, Cornelis MC, Probst-Hensch NM, Kronenberg F, Tonjes A, Hayward C, Aspelund T, Eiriksdottir G, Launer LJ, Harris TB, Rampersaud E, Mitchell BD, Arking DE, Boerwinkle E, Struchalin M, Cavalieri M, Singleton A, Giallauria F, Metter J, de Boer IH, Haritunians T, Lumley T, Siscovick D, Psaty BM, Zillikens MC, Oostra BA, Feitosa M, Province M, de Andrade M, Turner ST, Schillert A, Ziegler A, Wild PS, Schnabel RB, Wilde S, Munzel TF, Leak TS, Illig T, Klopp N, Meisinger C, Wichmann HE, Koenig W, Zgaga L, Zemunik T, Kolcic I, Minelli C, Hu FB, Johansson A, Igl W, Zaboli G, Wild SH, Wright AF, Campbell H, Ellinghaus D, Schreiber S, Aulchenko YS, Felix JF, Rivadeneira F, Uitterlinden AG, Hofman A, Imboden M, Nitsch D, Brandstatter A, Kollerits B, Kedenko L, Magi R, Stumvoll M, Kovacs P, Boban M, Campbell S, Endlich K, Volzke H, Kroemer HK, Nauck M, Volker U, Polasek O, Vitart V, Badola S, Parker AN, Ridker PM, Kardia SL, Blankenberg S, Liu Y, Curhan GC, Franke A, Rochat T, Paulweber B, Prokopenko I, Wang W, Gudnason V, Shuldiner AR, Coresh J, Schmidt R, Ferrucci L, Shlipak MG, van Duijn CM, Borecki I, Kramer BK, Rudan I, Gyllensten U, Wilson JF, Witteman JC, Pramstaller PP, Rettig R, Hastie N, Chasman DI, Kao WH, Heid IM, Fox CS (2010) New loci associated with kidney function and chronic kidney disease. Nat Genet 42:376-384
32. Eremina V, Cui S, Gerber H, Ferrara N, Haigh J, Nagy A, Ema M, Rossant J, Jothy S, Miner JH, Quaggin SE (2006) Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol 17:724-735
33. Eremina V, Quaggin SE (2004) The role of VEGF-A in glomerular development and function. Curr Opin Nephrol Hypertens 13:9-15 (Pubitemid 39069893)
34. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE (2003) Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111:707-716 (Pubitemid 36278589)
35. Tufro A, Norwood VF, Carey RM, Gomez RA (1999) Vascular endothelial growth factor induces nephrogenesis and vasculogenesis. J Am Soc Nephrol 10:2125-2134 (Pubitemid 29453490)
36. Burt LE, Forbes MS, Thornhill BA, Kiley SC, Chevalier RL (2007) Renal vascular endothelial growth factor in neonatal obstructive nephropathy. I. Endogenous VEGF. Am J Physiol Renal Physiol 292:F158-F167 (Pubitemid 46105255)
37. Woolf AS, Yuan HT (2001) Angiopoietin growth factors and Tie receptor tyrosine kinases in renal vascular development. Pediatr Nephrol 16:177-184 (Pubitemid 32125170)
38. Long DA, Price KL, Ioffe E, Gannon CM, Gnudi L, White KE, Yancopoulos GD, Rudge JS, Woolf AS (2008) Angiopoietin-1 therapy enhances fibrosis and inflammation following folic acid-induced acute renal injury. Kidney Int 74:300-309 (Pubitemid 352001243)
39. Lancrin C, Sroczynska P, Serrano AG, Gandillet A, Ferreras C, Kouskoff V, Lacaud G (2010) Blood cell generation from the hemangioblast. J Mol Med (Berl) 88:167-172
40. Lobov IB, Brooks PC, Lang RA (2002) Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci USA 99:11205-11210 (Pubitemid 34920903)
41. Fiedler U, Reiss Y, Scharpfenecker M, Grunow V, Koidl S, Thurston G, Gale NW, Witzenrath M, Rosseau S, Suttorp N, Sobke A, Herrmann M, Preissner KT, Vajkoczy P, Augustin HG (2006) Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat Med 12:235-239 (Pubitemid 43214752)
42. Davis B, Dei Cas A, Long DA, White KE, Hayward A, Ku CH, Woolf AS, Bilous R, Viberti G, Gnudi L (2007) Podocyte-specific expression of angiopoietin-2 causes proteinuria and apoptosis of glomerular endothelia. J Am Soc Nephrol 18:2320-2329 (Pubitemid 47203848)
43. Yuan HT, Suri C, Yancopoulos GD, Woolf AS (1999) Expression of angiopoietin-1, angiopoietin-2, and the Tie-2 receptor tyrosine kinase during mouse kidney maturation. J Am Soc Nephrol 10:1722-1736 (Pubitemid 29364671)
44. Woolf AS, Gnudi L, Long DA (2009) Roles of angiopoietins in kidney development and disease. J Am Soc Nephrol 20:239-244
45. Kim W, Moon SO, Lee SY, Jang KY, Cho CH, Koh GY, Choi KS, Yoon KH, Sung MJ, Kim DH, Lee S, Kang KP, Park SK (2006) COMP-angiopoietin-1 ameliorates renal fibrosis in a unilateral ureteral obstruction model. J Am Soc Nephrol 17:2474-2483 (Pubitemid 44300963)
46. Jeansson M, Gawlik A, Anderson G, Li C, Kerjaschki D, Henkelman M, Quaggin SE (2011) Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest 121:2278-2289
47. Floege J, Hudkins KL, Eitner F, Cui Y, Morrison RS, Schelling MA, Alpers CE (1999) Localization of fibroblast growth factor-2 (basic FGF) and FGF receptor-1 in adult human kidney. Kidney Int 56:883-897 (Pubitemid 29411716)
48. Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, Robbins ES, Shapiro RL, Galloway AC, Rifkin DB, Mignatti P (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141:1659-1673 (Pubitemid 28309179)
49. Murakami M, Nguyen LT, Hatanaka K, Schachterle W, Chen PY, Zhuang ZW, Black BL, Simons M (2011) FGF-dependent regulation of VEGF receptor 2 expression in mice. J Clin Invest 121:2668-2678
50. Murakami M, Nguyen LT, Zhuang ZW, Moodie KL, Carmeliet P, Stan RV, Simons M (2008) The FGF system has a key role in regulating vascular integrity. J Clin Invest 118:3355-3366
51. Strutz F, Zeisberg M, Hemmerlein B, Sattler B, Hummel K, Becker V, Muller GA (2000) Basic fibroblast growth factor expression is increased in human renal fibrogenesis and may mediate autocrine fibroblast proliferation. Kidney Int 57:1521-1538 (Pubitemid 30207911)
52. Wever R, Boer P, Hijmering M, Stroes E, Verhaar M, Kastelein J, Versluis K, Lagerwerf F, van Rijn H, Koomans H, Rabelink T (1999) Nitric oxide production is reduced in patients with chronic renal failure. Arterioscler Thromb Vasc Biol 19:1168-1172 (Pubitemid 29227634)
53. Zoccali C, Bode-Boger S, Mallamaci F, Benedetto F, Tripepi G, Malatino L, Cataliotti A, Bellanuova I, Fermo I, Frolich J, Boger R (2001) Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study. Lancet 358:2113-2117 (Pubitemid 34094901)
54. Kajimoto H, Kai H, Aoki H, Yasuoka S, Anegawa T, Aoki Y, Ueda S, Okuda S, Imaizumi T (2012) Inhibition of eNOS phosphorylation mediates endothelial dysfunction in renal failure: new effect of asymmetric dimethylarginine. Kidney Int 81:762-768
55. Sun D, Wang Y, Liu C, Zhou X, Li X, Xiao A (2012) Effects of nitric oxide on renal interstitial fibrosis in rats with unilateral ureteral obstruction. Life Sci 90:900-909
56. Nakayama T, Sato W, Kosugi T, Zhang L, Campbell-Thompson M, Yoshimura A, Croker BP, Johnson RJ, Nakagawa T (2009) Endothelial injury due to eNOS deficiency accelerates the progression of chronic renal disease in the mouse. Am J Physiol Renal Physiol 296:F317-F327
57. Satoh M, Fujimoto S, Arakawa S, Yada T, Namikoshi T, Haruna Y, Horike H, Sasaki T, Kashihara N (2008) Angiotensin II type 1 receptor blocker ameliorates uncoupled endothelial nitric oxide synthase in rats with experimental diabetic nephropathy. Nephrol Dial Transplant 23:3806-3813
58. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5:343-354 (Pubitemid 38579472)
59. Rosenberger C, Mandriota S, Jurgensen JS, Wiesener MS, Horstrup JH, Frei U, Ratcliffe PJ, Maxwell PH, Bachmann S, Eckardt KU (2002) Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J Am Soc Nephrol 13:1721-1732 (Pubitemid 34700596)
60. Higgins DF, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, Saito Y, Johnson RS, Kretzler M, Cohen CD, Eckardt KU, Iwano M, Haase VH (2007) Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117:3810-3820 (Pubitemid 350224091)
61. Kimura K, Iwano M, Higgins DF, Yamaguchi Y, Nakatani K, Harada K, Kubo A, Akai Y, Rankin EB, Neilson EG, Haase VH, Saito Y (2008) Stable expression of HIF-1alpha in tubular epithelial cells promotes interstitial fibrosis. Am J Physiol Renal Physiol 295:F1023-F1029
62. Kolyada AY, Tighiouart H, Perianayagam MC, Liangos O, Madias NE, Jaber BL (2009) A genetic variant of hypoxia-inducible factor-1alpha is associated with adverse outcomes in acute kidney injury. Kidney Int 75:1322-1329
63. Tanaka T, Kojima I, Ohse T, Ingelfinger JR, Adler S, Fujita T, Nangaku M (2005) Cobalt promotes angiogenesis via hypoxia-inducible factor and protects tubulointerstitium in the remnant kidney model. Lab Invest 85:1292-1307 (Pubitemid 41348643)
64. Nangaku M, Inagi R, Miyata T, Fujita T (2008) Hypoxia and hypoxia-inducible factor in renal disease. Nephron Exp Nephrol 110:e1-e7
65. Hill P, Shukla D, Tran MG, Aragones J, Cook HT, Carmeliet P, Maxwell PH (2008) Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 19:39-46
66. Tang N, Wang L, Esko J, Giordano FJ, Huang Y, Gerber HP, Ferrara N, Johnson RS (2004) Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6:485-495 (Pubitemid 39469984)
67. Skuli N, Majmundar AJ, Krock BL, Mesquita RC, Mathew LK, Quinn ZL, Runge A, Liu L, Kim MN, Liang J, Schenkel S, Yodh AG, Keith B, Simon MC (2012) Endothelial HIF-2alpha regulates murine pathological angiogenesis and revascularization processes. J Clin Invest 122:1427-1443
68. Bige N, Shweke N, Benhassine S, Jouanneau C, Vandermeersch S, Dussaule JC, Chatziantoniou C, Ronco P, Boffa JJ (2012) Thrombospondin-1 plays a profibrotic and pro-inflammatory role during ureteric obstruction. Kidney Int 81:1226-1238
69. Zhang X, Kazerounian S, Duquette M, Perruzzi C, Nagy JA, Dvorak HF, Parangi S, Lawler J (2009) Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. FASEB J 23:3368-3376
70. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41-48 (Pubitemid 30048524)
71. Isenberg JS, Ridnour LA, Perruccio EM, Espey MG, Wink DA, Roberts DD (2005) Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proc Natl Acad Sci USA 102:13141-13146 (Pubitemid 41324992)
72. Basile DP, Fredrich K, Chelladurai B, Leonard EC, Parrish AR (2008) Renal ischemia reperfusion inhibits VEGF expression and induces ADAMTS-1, a novel VEGF inhibitor. Am J Physiol Renal Physiol 294:F928-F936
73. Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, Davis GE, Gharib SA, Humphreys BD, Duffield JS (2012) Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol 23:868-883
74. Bussolino F, Di Renzo MF, Ziche M, Bocchietto E, Olivero M, Naldini L, Gaudino G, Tamagnone L, Coffer A, Comoglio PM (1992) Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol 119:629-641
75. Gong R, Rifai A, Dworkin LD (2006) Anti-inflammatory effect of hepatocyte growth factor in chronic kidney disease: targeting the inflamed vascular endothelium. J Am Soc Nephrol 17:2464-2473 (Pubitemid 44300962)
76. Gong R, Rifai A, Dworkin LD (2006) Hepatocyte growth factor suppresses acute renal inflammation by inhibition of endothelial E-selectin. Kidney Int 69:1166-1174
77. Kang DH, Hughes J, Mazzali M, Schreiner GF, Johnson RJ (2001) Impaired angiogenesis in the remnant kidney model: II. Vascular endothelial growth factor administration reduces renal fibrosis and stabilizes renal function. J Am Soc Nephrol 12:1448-1457 (Pubitemid 32666327)
78. Iliescu R, Fernandez SR, Kelsen S, Maric C, Chade AR (2010) Role of renal microcirculation in experimental renovascular disease. Nephrol Dial Transplant 25:1079-1087
79. Long DA, Mu W, Price KL, Roncal C, Schreiner GF, Woolf AS, Johnson RJ (2006) Vascular endothelial growth factor administration does not improve microvascular disease in the salt-dependent phase of post-angiotensin II hypertension. Am J Physiol Renal Physiol 291:F1248-F1254 (Pubitemid 44887238)
80. Burt LE, Forbes MS, Thornhill BA, Kiley SC, Minor JJ, Chevalier RL (2007) Renal vascular endothelial growth factor in neonatal obstructive nephropathy. II. Exogenous VEGF. Am J Physiol Renal Physiol 292:F168-F174 (Pubitemid 46105256)
81. Sato W, Tanabe K, Kosugi T, Hudkins K, Lanaspa MA, Zhang L, Campbell-Thompson M, Li Q, Long DA, Alpers CE, Nakagawa T (2011) Selective stimulation of VEGFR2 accelerates progressive renal disease. Am J Pathol 179:155-166
82. Schrijvers BF, Flyvbjerg A, Tilton RG, Rasch R, Lameire NH, De Vriese AS (2005) Pathophysiological role of vascular endothelial growth factor in the remnant kidney. Nephron Exp Nephrol 101:e9-e15 (Pubitemid 41159946)
83. Leonard EC, Friedrich JL, Basile DP (2008) VEGF-121 preserves renal microvessel structure and ameliorates secondary renal disease following acute kidney injury. Am J Physiol Renal Physiol 295:F1648-F1657
84. Jung YJ, Kim DH, Lee AS, Lee S, Kang KP, Lee SY, Jang KY, Sung MJ, Park SK, Kim W (2009) Peritubular capillary preservation with COMP-angiopoietin-1 decreases ischemia-reperfusion-induced acute kidney injury. Am J Physiol Renal Physiol 297:F952-F960
85. Gavard J, Patel V, Gutkind JS (2008) Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev Cell 14:25-36
86. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE (2008) VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 358:1129-1136 (Pubitemid 351398487)
87. Eremina V, Quaggin SE (2010) Biology of anti-angiogenic therapy-induced thrombotic microangiopathy. Semin Nephrol 30:582-590
88. Goligorsky MS, Yasuda K, Ratliff B (2010) Dysfunctional endothelial progenitor cells in chronic kidney disease. J Am Soc Nephrol 21:911-919
89. Chade AR, Zhu X, Lavi R, Krier JD, Pislaru S, Simari RD, Napoli C, Lerman A, Lerman LO (2009) Endothelial progenitor cells restore renal function in chronic experimental renovascular disease. Circulation 119:547-557
90. Zhu XY, Urbieta Caceres VH, Favreau FD, Krier JD, Lerman A, Lerman LO (2011) Enhanced endothelial progenitor cell angiogenic potency, present in early experimental renovascular hypertension, deteriorates with disease duration. J Hypertens 29:1972-1979
91. Togel F, Isaac J, Hu Z, Weiss K, Westenfelder C (2005) Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int 67:1772-1784 (Pubitemid 40577712)
92. Krenning G, Dankers PY, Drouven JW, Waanders F, Franssen CF, van Luyn MJ, Harmsen MC, Popa ER (2009) Endothelial progenitor cell dysfunction in patients with progressive chronic kidney disease. Am J Physiol Renal Physiol 296:F1314-F1322
93. Perry TE, Song M, Despres DJ, Kim SM, San H, Yu ZX, Raghavachari N, Schnermann J, Cannon RO 3rd, Orlic D (2009) Bone marrow-derived cells do not repair endothelium in a mouse model of chronic endothelial cell dysfunction. Cardiovasc Res 84:317-325
94. Li B, Cohen A, Hudson TE, Motlagh D, Amrani DL, Duffield JS (2010) Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury. Circulation 121:2211-2220
95. 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 (2011) Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 178:911-923
96. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512-523 (Pubitemid 41361741)
97. Richeldi L, Costabel U, Selman M, Kim DS, Hansell DM, Nicholson AG, Brown KK, Flaherty KR, Noble PW, Raghu G, Brun M, Gupta A, Juhel N, Kluglich M, du Bois RM (2011) Efficacy of a tyrosine kinase inhibitor in idiopathic pulmonary fibrosis. N Engl J Med 365:1079-1087
98. Zeisberg EM, Potenta SE, Sugimoto H, Zeisberg M, Kalluri R (2008) Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 19:2282-2287
99. Oladipupo S, Hu S, Kovalski J, Yao J, Santeford A, Sohn RE, Shohet R, Maslov K, Wang LV, Arbeit JM (2011) VEGF is essential for hypoxia-inducible factor-mediated neovascularization but dispensable for endothelial sprouting. Proc Natl Acad Sci 108:13264-13269
100. Rabelink TJ, de Boer HC, van Zonneveld AJ (2010) Endothelial activation and circulating markers of endothelial activation in kidney disease. Nat Rev Nephrol 6:404-414
101. Luttun A, Tjwa M, Carmeliet P (2002) Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann N Y Acad Sci 979:80-93 (Pubitemid 36121141)
102. Chen YT, Chang FC, Wu CF, Chou YH, Hsu HL, Chiang WC, Shen J, Chen YM, Wu KD, Tsai TJ, Duffield JS, Lin SL (2011) Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Int 80:1170-1181
103. Claesson-Welsh L, Welsh M, Ito N, Anand-Apte B, Soker S, Zetter B, O'Reilly M, Folkman J (1998) Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD. Proc Natl Acad Sci U S A 95:5579-5583 (Pubitemid 28224137)
104. Mu W, Long DA, Ouyang X, Agarwal A, Cruz PE, Roncal CA, Nakagawa T, Yu X, Hauswirth WW, Johnson RJ (2009) Angiostatin overexpression is associated with an improvement in chronic kidney injury by an anti-inflammatory mechanism. Am J Physiol Renal Physiol 296:F145-152
105. Kim YM, Hwang S, Pyun BJ, Kim TY, Lee ST, Gho YS, Kwon YG (2002) Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem 277:27872-27879 (Pubitemid 34966733)
106. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111:649-658 (Pubitemid 36278583)
107. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, Roberts DD (2010) Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J Biol Chem 285:38923-38932