Investigating the Process of Renal Epithelial Repair to Develop New Therapies

Kidney Development, Disease, Repair and Regeneration

Volumn , Issue , 2015, Pages 381-393

  Humphreys, Benjamin D ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

Acute kidney injury; De differentiation; Stem cell; Therapy

Indexed keywords

EID: 85068182031     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-800102-8.00028-X     Document Type: Chapter

References (125)

1. Basile D.P., Anderson M.D., Sutton T.A. Pathophysiology of acute kidney injury. Compr Physiol 2012, 2(2):1303-1353.
2. Coca S.G., Singanamala S., Parikh C.R. Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis. Kidney Int 2012, 81(5):442-448.
3. Ali T., Khan I., Simpson W., et al. Incidence and outcomes in acute kidney injury: a comprehensive population-based study. J Am Soc Nephrol 2007, 18(4):1292-1298.
4. Chertow G.M., Burdick E., Honour M., Bonventre J.V., Bates D.W. Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. J Am Soc Nephrol 2005, 16(11):3365-3370.
5. Feest T.G., Round A., Hamad S. Incidence of severe acute renal failure in adults: results of a community based study. BMJ 1993, 306(6876):481-483.
6. Groeneveld A.B., Tran D.D., van der Meulen J., Nauta J.J., Thijs L.G. Acute renal failure in the medical intensive care unit: predisposing, complicating factors and outcome. Nephron 1991, 59(4):602-610.
7. Macias-Nunez J.F., Lopez-Novoa J.M., Martinez-Maldonado M. Acute renal failure in the aged. Semin Nephrol 1996, 16(4):330-338.
8. Ferenbach D.A., Nkejabega N.C., McKay J., et al. The induction of macrophage hemeoxygenase-1 is protective during acute kidney injury in aging mice. Kidney Int 2011, 79(9):966-976.
9. Chawla L.S., Kimmel P.L. Acute kidney injury and chronic kidney disease: an integrated clinical syndrome. Kidney Int 2012, 82(5):516-524.
10. Ishani A., Xue J.L., Himmelfarb J., et al. Acute kidney injury increases risk of ESRD among elderly. J Am Soc Nephrol 2009, 20(1):223-228.
11. Coca S.G. Long-term outcomes of acute kidney injury. Curr Opin Nephrol Hypertens 2010, 19(3):266-272.
12. Goldstein S.L., Jaber B.L., Faubel S., Chawla L.S. Acute Kidney Injury Advisory Group of American Society of N. AKI transition of care: a potential opportunity to detect and prevent CKD. Clin J Am Soc Nephrol 2013, 8(3):476-483.
13. Basile D.P., Leonard E.C., Tonade D., Friedrich J.L., Goenka S. Distinct effects on long-term function of injured and contralateral kidneys following unilateral renal ischemia-reperfusion. Am J Physiol Renal Physiol 2012, 302(5):F625-F635.
14. Basile D.P. Rarefaction of peritubular capillaries following ischemic acute renal failure: a potential factor predisposing to progressive nephropathy. Curr Opin Nephrol Hypertens 2004, 13(1):1-7.
15. Bonventre J.V., Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011, 121(11):4210-4221.
16. Uchida S., Endou H. Substrate specificity to maintain cellular ATP along the mouse nephron. Am J Physiol 1988, 255(5 Pt 2):F977-F983.
17. Lieberthal W., Nigam S.K. Acute renal failure. I. Relative importance of proximal vs. distal tubular injury. Am J Physiol 1998, 275(5 Pt 2):F623-F631.
18. Heyman S.N., Rosenberger C., Rosen S. Experimental ischemia-reperfusion: biases and myths-the proximal vs. distal hypoxic tubular injury debate revisited. Kidney Int 2010, 77(1):9-16.
19. Bonventre J.V. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 2003, 14(Suppl. 1):S55-S61.
20. Kusaba T., Humphreys B.D. Controversies on the origin of proliferating epithelial cells after kidney injury. Pediatr Nephrol 2014, 29(4):673-679.
21. Sagrinati C., Netti G.S., Mazzinghi B., et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 2006, 17(9):2443-2456.
22. Lazzeri E., Crescioli C., Ronconi E., et al. Regenerative potential of embryonic renal multipotent progenitors in acute renal failure. J Am Soc Nephrol 2007, 18(12):3128-3138.
23. Ronconi E., Sagrinati C., Angelotti M.L., et al. Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 2009, 20(2):322-332.
24. Angelotti M.L., Ronconi E., Ballerini L., et al. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells 2012, 30(8):1714-1725.
25. Romagnani P., Remuzzi G. Renal progenitors in non-diabetic and diabetic nephropathies. Trends Endocrinol Metab 2013, 24(1):13-20.
26. Smeets B., Boor P., Dijkman H., et al. Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration. J Pathol 2012, 229(5):645-659.
27. Lindgren D., Bostrom A.K., Nilsson K., et al. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am J Pathol 2011, 178(2):828-837.
28. Humphreys B.D., Valerius M.T., Kobayashi A., et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008, 2(3):284-291.
29. Berger K., Bangen J.M., Hammerich L., et al. Origin of regenerating tubular cells after acute kidney injury. Proc Natl Acad Sci USA 2014, 111(4):1533-1538.
30. Smeets B., Boor P., Dijkman H., et al. Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration. J Pathol 2013, 229(5):645-659.
31. Kemper K., Sprick M.R., de Bree M., et al. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 2010, 70(2):719-729.
32. Angelotti M.L., Lazzeri E., Lasagni L., Romagnani P. Only anti-CD133 antibodies recognizing the CD133/1 or the CD133/2 epitopes can identify human renal progenitors. Kidney Int 2010, 78(6):620-621. author reply 1.
33. Kusaba T., Lalli M., Kramann R., Kobayashi A., Humphreys B.D. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci USA 2014, 111(4):1527-1532.
34. Madjdpour C., Bacic D., Kaissling B., Murer H., Biber J. Segment-specific expression of sodium-phosphate cotransporters NaPi-IIa and -IIc and interacting proteins in mouse renal proximal tubules. Pflugers Archiv Eur J Physiol 2004, 448(4):402-410.
35. Humphreys B.D., Czerniak S., Dirocco D.P., Hasnain W., Cheema R., Bonventre J.V. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 2011, 108(22):9226-9231.
36. Romagnani P. Of mice and men: the riddle of tubular regeneration. J Pathol 2013, 229(5):641-644.
37. Humes H.D., Cieslinski D.A., Coimbra T.M., Messana J.M., Galvao C. Epidermal growth factor enhances renal tubule cell regeneration and repair and accelerates the recovery of renal function in postischemic acute renal failure. J Clin Invest 1989, 84(6):1757-1761.
38. Wang Z., Chen J.K., Wang S.W., Moeckel G., Harris R.C. Importance of functional EGF receptors in recovery from acute nephrotoxic injury. J Am Soc Nephrol 2003, 14(12):3147-3154.
39. Tang J., Liu N., Zhuang S. Role of epidermal growth factor receptor in acute and chronic kidney injury. Kidney Int 2013, 83(5):804-810.
40. Chen J., Chen J.K., Harris R.C. Deletion of the epidermal growth factor receptor in renal proximal tubule epithelial cells delays recovery from acute kidney injury. Kidney Int 2012, 82(1):45-52.
41. Liu N., Guo J.K., Pang M., et al. Genetic or pharmacologic blockade of EGFR inhibits renal fibrosis. J Am Soc Nephrol 2012, 23(5):854-867.
42. Tang J., Liu N., Tolbert E., et al. Sustained activation of EGFR triggers renal fibrogenesis after acute kidney injury. Am J Pathol 2013, 183(1):160-172.
43. Nusse R., van Ooyen A., Cox D., Fung Y.K., Varmus H. Mode of proviral activation of a putative mammary oncogene (int-1) on mouse chromosome 15. Nature 1984, 307(5947):131-136.
44. Aberle H., Bauer A., Stappert J., Kispert A., Kemler R. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 1997, 16(13):3797-3804.
45. Costantini F., Kopan R. Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev Cell 2010, 18(5):698-712.
46. Hendry C., Rumballe B., Moritz K., Little M.H. Defining and redefining the nephron progenitor population. Pediatr Nephrol 2011, 26(9):1395-1406.
47. Taguchi A., Kaku Y., Ohmori T., et al. Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell 2013.
48. Stark K., Vainio S., Vassileva G., McMahon A.P. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 1994, 372(6507):679-683.
49. Zhou D., Li Y., Lin L., Zhou L., Igarashi P., Liu Y. Tubule-specific ablation of endogenous beta-catenin aggravates acute kidney injury in mice. Kidney Int 2012, 82(5):537-547.
50. Zhou D., Tan R.J., Zhou L., Li Y., Liu Y. Kidney tubular beta-catenin signaling controls interstitial fibroblast fate via epithelial-mesenchymal communication. Sci Rep 2013, 3:1878.
51. He W., Dai C., Li Y., Zeng G., Monga S.P., Liu Y. Wnt/beta-catenin signaling promotes renal interstitial fibrosis. J Am Soc Nephrol 2009, 20(4):765-776.
52. Wang Z., Havasi A., Gall J.M., Mao H., Schwartz J.H., Borkan S.C. Beta-catenin promotes survival of renal epithelial cells by inhibiting Bax. J Am Soc Nephrol 2009, 20(9):1919-1928.
53. He W., Tan R.J., Li Y., et al. Matrix metalloproteinase-7 as a surrogate marker predicts renal Wnt/beta-catenin activity in CKD. J Am Soc Nephrol 2012, 23(2):294-304.
54. Zhou L., Li Y., Zhou D., Tan R.J., Liu Y. Loss of Klotho contributes to kidney injury by derepression of Wnt/beta-catenin signaling. J Am Soc Nephrol 2013, 24(5):771-785.
55. Satoh M., Nagasu H., Morita Y., Yamaguchi T.P., Kanwar Y.S., Kashihara N. Klotho protects against mouse renal fibrosis by inhibiting Wnt signaling. Am J Physiol Renal Physiol 2012, 303(12):F1641-F1651.
56. Dugo L., Collin M., Thiemermann C. Glycogen synthase kinase 3beta as a target for the therapy of shock and inflammation. Shock 2007, 27(2):113-123.
57. Kozar K., Ciemerych M.A., Rebel V.I., et al. Mouse development and cell proliferation in the absence of D-cyclins. Cell 2004, 118(4):477-491.
58. Malumbres M., Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 2009, 9(3):153-166.
59. Megyesi J., Andrade L., Vieira J.M., Safirstein R.L., Price P.M. Positive effect of the induction of p21WAF1/CIP1 on the course of ischemic acute renal failure. Kidney Int 2001, 60(6):2164-2172.
60. Price P.M., Safirstein R.L., Megyesi J. Protection of renal cells from cisplatin toxicity by cell cycle inhibitors. Am J Physiol Renal Physiol 2004, 286(2):F378-F384.
61. Price P.M., Yu F., Kaldis P., et al. Dependence of cisplatin-induced cell death in vitro and in vivo on cyclin-dependent kinase 2. J Am Soc Nephrol 2006, 17(9):2434-2442.
62. Nath K.A. Provenance of the protective property of p21. Am J Physiol Renal Physiol 2005, 289(3):F512-F513.
63. Dirocco D., Bisi J., Roberts P., et al. CDK4/6 inhibition induces epithelial cell cycle arrest and ameliorates acute kidney injury. Am J Physiol Renal Physiol 2013.
64. Price P.M., Safirstein R.L., Megyesi J. The cell cycle and acute kidney injury. Kidney Int 2009, 76(6):604-613.
65. Safirstein R. Renal regeneration: reiterating a developmental paradigm. Kidney Int 1999, 56(4):1599-1600.
66. Yang L., Besschetnova T.Y., Brooks C.R., Shah J.V., Bonventre J.V. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 2010, 16(5):535-543. 1p following 143.
67. Melk A., Ramassar V., Helms L.M., et al. Telomere shortening in kidneys with age. J Am Soc Nephrol 2000, 11(3):444-453.
68. Westhoff J.H., Schildhorn C., Jacobi C., et al. Telomere shortening reduces regenerative capacity after acute kidney injury. J Am Soc Nephrol 2010, 21(2):327-336.
69. Agarwal A., Bolisetty S. Adaptive responses to tissue injury: role of heme oxygenase-1. Trans Am Clin Climatol Assoc 2013, 124:111-122.
70. Nath K.A., Balla G., Vercellotti G.M., et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 1992, 90(1):267-270.
71. Bach F.H. Heme oxygenase-1: a therapeutic amplification funnel. FASEB J 2005, 19(10):1216-1219.
72. Li Volti G., Rodella L.F., Di Giacomo C., et al. Role of carbon monoxide and biliverdin in renal ischemia/reperfusion injury. Nephron Exp Nephrol 2006, 104(4):e135-e139.
73. Neto J.S., Nakao A., Kimizuka K., et al. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol 2004, 287(5):F979-F989.
74. Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science 1987, 235(4792):1043-1046.
75. Alam J., Cook J.L. How many transcription factors does it take to turn on the heme oxygenase-1 gene?. Am J Respir Cell Mol Biol 2007, 36(2):166-174.
76. Wu Q.Q., Wang Y., Senitko M., et al. Bardoxolone methyl (BARD) ameliorates ischemic AKI and increases expression of protective genes Nrf2, PPARgamma, and HO-1. Am J Physiol Renal Physiol 2011, 300(5):F1180-F1192.
77. Kramann R., Dirocco D.P., Humphreys B.D. Understanding the origin, activation and regulation of matrix-producing myofibroblasts for treatment of fibrotic disease. J Pathol 2013, 231(3):273-289.
78. Yamamoto K., Wilson D.R., Baumal R. Outer medullary circulatory defect in ischemic acute renal failure. Am J Pathol 1984, 116(2):253-261.
79. Kwon O., Hong S.M., Sutton T.A., Temm C.J. Preservation of peritubular capillary endothelial integrity and increasing pericytes may be critical to recovery from postischemic acute kidney injury. Am J Physiol Renal Physiol 2008, 295(2):F351-F359.
80. Goligorsky M.S., Brodsky S.V., Noiri E. NO bioavailability, endothelial dysfunction, and acute renal failure: new insights into pathophysiology. Semin Nephrol 2004, 24(4):316-323.
81. Chander V., Chopra K. Renal protective effect of molsidomine and L-arginine in ischemia-reperfusion induced injury in rats. J Surg Res 2005, 128(1):132-139.
82. Basile D.P., Donohoe D., Roethe K., Osborn J.L. Renal ischemic injury results in permanent damage to peritubular capillaries and influences long-term function. Am J Physiol Renal Physiol 2001, 281(5):F887-F899.
83. Tanaka T., Nangaku M. Angiogenesis and hypoxia in the kidney. Nat Rev Nephrol 2013, 9(4):211-222.
84. O'Riordan E., Mendelev N., Patschan S., et al. Chronic NOS inhibition actuates endothelial-mesenchymal transformation. Am J Physiol Heart Circ Physiol 2007, 292(1):H285-H294.
85. Yuan H.T., Li X.Z., Pitera J.E., Long D.A., Woolf A.S. Peritubular capillary loss after mouse acute nephrotoxicity correlates with down-regulation of vascular endothelial growth factor-A and hypoxia-inducible factor-1?. Am J Pathol 2003, 163(6):2289-2301.
86. Horbelt M., Lee S.Y., Mang H.E., et al. Acute and chronic microvascular alterations in a mouse model of ischemic acute kidney injury. Am J Physiol Renal Physiol 2007, 293(3):F688-F695.
87. Kang D.H., Joly A.H., Oh S.W., et al. Impaired angiogenesis in the remnant kidney model: I. Potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol 2001, 12(7):1434-1447.
88. Choi Y.J., Chakraborty S., Nguyen V., et al. Peritubular capillary loss is associated with chronic tubulointerstitial injury in human kidney: altered expression of vascular endothelial growth factor. Human Pathol 2000, 31(12):1491-1497.
89. Seron D., Alexopoulos E., Raftery M.J., Hartley B., Cameron J.S. Number of interstitial capillary cross-sections assessed by monoclonal antibodies: relation to interstitial damage. Nephrol Dial Transplant 1990, 5(10):889-893.
90. Bohle A., Mackensen-Haen S., Wehrmann M. Significance of postglomerular capillaries in the pathogenesis of chronic renal failure. Kidney Blood Press Res 1996, 19(3-4):191-195.
91. Kida Y., Ieronimakis N., Schrimpf C., Reyes M., Duffield J.S. EphrinB2 reverse signaling protects against capillary rarefaction and fibrosis after kidney injury. J Am Soc Nephrol 2013, 24(4):559-572.
92. Kida Y., Tchao B.N., Yamaguchi I. Peritubular capillary rarefaction: a new therapeutic target in chronic kidney disease. Pediatr Nephrol 2013.
93. Kramann R., Tanaka M., Humphreys B.D. Fluorescence microangiography for quantitative assessment of peritubular capillary changes after acute kidney injury in mouse. J Am Soc Nephrol 2014, 25(9):1924-1931.
94. Basile D.P., Fredrich K., Chelladurai B., Leonard E.C., Parrish A.R. Renal ischemia reperfusion inhibits VEGF expression and induces ADAMTS-1, a novel VEGF inhibitor. Am J Physiol Renal Physiol 2008, 294(4):F928-F936.
95. Leonard E.C., Friedrich J.L., Basile D.P. VEGF-121 preserves renal microvessel structure and ameliorates secondary renal disease following acute kidney injury. Am J Physiol Renal Physiol 2008, 295(6):F1648-F1657.
96. Lin S.L., Chang F.C., Schrimpf C., et al. Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 2011, 178(2):911-923.
97. Bijkerk R., van Solingen C., de Boer H.C., et al. Hematopoietic microRNA-126 protects against renal ischemia/reperfusion injury by promoting vascular integrity. J Am Soc Nephrol 2014.
98. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001, 15(23):3059-3087.
99. Mao J., Kim B.M., Rajurkar M., Shivdasani R.A., McMahon A.P. Hedgehog signaling controls mesenchymal growth in the developing mammalian digestive tract. Development 2010, 137(10):1721-1729.
100. Yu J., Carroll T.J., McMahon A.P. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 2002, 129(22):5301-5312.
101. Cain J.E., Rosenblum N.D. Control of mammalian kidney development by the Hedgehog signaling pathway. Pediatr Nephrol 2010.
102. Hu M.C., Mo R., Bhella S., et al. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 2006, 133(3):569-578.
103. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999, 126(17):3915-3924.
104. Tian H., Callahan C.A., DuPree K.J., et al. Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc Natl Acad Sci USA 2009, 106(11):4254-4259.
105. Yauch R.L., Gould S.E., Scales S.J., et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455(7211):406-410.
106. Olive K.P., Jacobetz M.A., Davidson C.J., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324(5933):1457-1461.
107. Shin K., Lee J., Guo N., et al. Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature 2011, 472(7341):110-114.
108. Omenetti A., Porrello A., Jung Y., et al. Hedgehog signaling regulates epithelial-mesenchymal transition during biliary fibrosis in rodents and humans. J Clin Invest 2008, 118(10):3331-3342.
109. Syn W.K., Choi S.S., Liaskou E., et al. Osteopontin is induced by hedgehog pathway activation and promotes fibrosis progression in nonalcoholic steatohepatitis. Hepatology 2011, 53(1):106-115.
110. Choi S.S., Omenetti A., Witek R.P., et al. Hedgehog pathway activation and epithelial-to-mesenchymal transitions during myofibroblastic transformation of rat hepatic cells in culture and cirrhosis. Am J Physiol Gastrointest Liver Physiol 2009, 297(6):G1093-G1106.
111. Choi S.S., Omenetti A., Syn W.K., Diehl A.M. The role of Hedgehog signaling in fibrogenic liver repair. Int J Biochem Cell Biol 2011, 43(2):238-244.
112. Michelotti G.A., Xie G., Swiderska M., et al. Smoothened is a master regulator of adult liver repair. J Clin Invest 2013, 123:2380-2394.
113. Stewart G.A., Hoyne G.F., Ahmad S.A., et al. Expression of the developmental Sonic hedgehog (Shh) signalling pathway is up-regulated in chronic lung fibrosis and the Shh receptor patched 1 is present in circulating T lymphocytes. J Pathol 2003, 199(4):488-495.
114. Fabian S.L., Penchev R.R., St-Jacques B., et al. Hedgehog-Gli pathway activation during kidney fibrosis. Am J Pathol 2012, 180(4):1441-1453.
115. Sahebjam S., Siu L.L., Razak A.A. The utility of hedgehog signaling pathway inhibition for cancer. Oncologist 2012, 17(8):1090-1099.
116. Ding H., Zhou D., Hao S., et al. Sonic hedgehog signaling mediates epithelial-mesenchymal communication and promotes renal fibrosis. J Am Soc Nephrol 2012, 23(5):801-813.
117. Jenkins D. Hedgehog signalling: emerging evidence for non-canonical pathways. Cell Signalling 2009, 21(7):1023-1034.
118. Eklund L., Saharinen P. Angiopoietin signaling in the vasculature. Exp Cell Res 2013, 319(9):1271-1280.
119. Suri C., Jones P.F., Patan S., et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87(7):1171-1180.
120. Fukuhara S., Sako K., Minami T., 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.
121. Jeansson M., Gawlik A., Anderson G., et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest 2011, 121(6):2278-2289.
122. Khairoun M., van der Pol P., de Vries D.K., et al. Renal ischemia-reperfusion induces a dysbalance of angiopoietins, accompanied by proliferation of pericytes and fibrosis. Am J Physiol Renal Physiol 2013, 305(6):F901-F910.
123. de Vries D.K., Khairoun M., Lindeman J.H., et al. Renal ischemia-reperfusion induces release of angiopoietin-2 from human grafts of living and deceased donors. Transplantation 2013, 96(3):282-289.
124. Kim W., Moon S.O., Lee S.Y., et al. COMP-angiopoietin-1 ameliorates renal fibrosis in a unilateral ureteral obstruction model. J Am Soc Nephrol 2006, 17(9):2474-2483.
125. Foo S.S., Turner C.J., Adams S., et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 2006, 124(1):161-173.