Defining the acute kidney injury and repair transcriptome

Seminars in Nephrology

Volumn 34, Issue 4, 2014, Pages 404-417

  Kumar, Sanjeev ^a   Liu, Jing ^a   McMahon, Andrew P ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Acute kidney injury; Cancer; Development; MiRNA; Repair; Transcriptome; TRAP

Indexed keywords

MICRORNA; TRANSCRIPTOME;

ACUTE KIDNEY FAILURE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL SPECIFICITY; CHRONIC INFLAMMATION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE COURSE; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNE RESPONSE; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY TUBULE DISORDER; LEUKOCYTE; MACROPHAGE; MOLECULAR PATHOLOGY; NONHUMAN; REVIEW; RNA REPAIR; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; KIDNEY TUBULE; METABOLISM; REGENERATION;

ACUTE KIDNEY INJURY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; KIDNEY; KIDNEY TUBULES; REGENERATION; TRANSCRIPTOME;

EID: 84907983907     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2014.06.007     Document Type: Review

References (108)

1. Mehta R.L., Kellum J.A., Shah S.V., et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care 2007, 11:R31.
2. Waikar S.S., Liu K.D., Chertow G.M. Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol 2008, 3:844-861.
3. 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, 16:3365-3370.
4. Palevsky P.M., Zhang J.H., et al. Intensity of renal support in critically ill patients with acute kidney injury. N Engl J Med 2008, 359:7-20. VA/NIH Acute Renal Failure Trial Network.
5. Coca S.G., Singanamala S., Parikh C.R. Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis. Kidney Int 2012, 81:442-448.
6. Bonventre J.V., Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011, 121:4210-4221.
7. 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, 16:535-543. 1p following 143.
8. Bechtel W., McGoohan S., Zeisberg E.M., et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med 2010, 16:544-550.
9. 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, 231:273-289.
10. LeBleu V.S., Taduri G., O'Connell J., et al. Origin and function of myofibroblasts in kidney fibrosis. Nat Med 2013, 19:1047-1053.
11. Helbert M.J., Dauwe S.E., Van der Biest I., Nouwen E.J., De Broe M.E. Immunodissection of the human proximal nephron: flow sorting of S1S2S3, S1S2 and S3 proximal tubular cells. Kidney Int 1997, 52:414-428.
12. Heyman S.N., Evans R.G., Rosen S., Rosenberger C. Cellular adaptive changes in AKI: mitigating renal hypoxic injury. Nephrol Dial Transplant 2012, 27:1721-1728.
13. Shanley P.F., Rosen M.D., Brezis M., Silva P., Epstein F.H., Rosen S. Topography of focal proximal tubular necrosis after ischemia with reflow in the rat kidney. Am J Pathol 1986, 122:462-468.
14. Srichai M.B., Hao C., Davis L., et al. Apoptosis of the thick ascending limb results in acute kidney injury. J Am Soc Nephrol 2008, 19:1538-1546.
15. Bagnasco S., Good D., Balaban R., Burg M. Lactate production in isolated segments of the rat nephron. Am J Physiol 1985, 248:F522-F526.
16. Gobe G., Zhang X.J., Willgoss D.A., Schoch E., Hogg N.A., Endre Z.H. Relationship between expression of Bcl-2 genes and growth factors in ischemic acute renal failure in the rat. J Am Soc Nephrol 2000, 11:454-467.
17. Gobe G.C., Johnson D.W. Distal tubular epithelial cells of the kidney: potential support for proximal tubular cell survival after renal injury. Int J Biochem Cell Biol 2007, 39:1551-1561.
18. Oberbauer R., Rohrmoser M., Regele H., Muhlbacher F., Mayer G. Apoptosis of tubular epithelial cells in donor kidney biopsies predicts early renal allograft function. J Am Soc Nephrol 1999, 10:2006-2013.
19. Olsen T.S., Hansen H.E. Ultrastructure of medullary tubules in ischemic acute tubular necrosis and acute interstitial nephritis in man. APMIS 1990, 98:1139-1148.
20. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 2006, 17:1503-1520.
21. Humphreys B.D., Valerius M.T., Kobayashi A., et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008, 2:284-291.
22. Kusaba T., Humphreys B.D. Controversies on the origin of proliferating epithelial cells after kidney injury. Pediatr Nephrol 2014, 29:673-679.
23. Romagnani P., Lasagni L., Remuzzi G. Renal progenitors: an evolutionary conserved strategy for kidney regeneration. Nat Rev Nephrol 2013, 9:137-146.
24. 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, 17:2443-2456.
25. Swaminathan S., Griffin M.D. First responders: understanding monocyte-lineage traffic in the acutely injured kidney. Kidney Int 2008, 74:1509-1511.
26. Li L., Huang L., Sung S.S., et al. The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int 2008, 74:1526-1537.
27. Lee S., Huen S., Nishio H., et al. Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 2011, 22:317-326.
28. Lin S.L., Li B., Rao S., et al. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 2010, 107:4194-4199.
29. Menke J., Iwata Y., Rabacal W.A., et al. CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. J Clin Invest 2009, 119:2330-2342.
30. Duffield J.S. Macrophages in kidney repair and regeneration. J Am Soc Nephrol 2011, 22:199-201.
31. 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:F887-F899.
32. Zlokovic B.V. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci 2005, 28:202-208.
33. Venkatachalam M.A., Griffin K.A., Lan R., Geng H., Saikumar P., Bidani A.K. Acute kidney injury: a springboard for progression in chronic kidney disease. Am J Physiol Renal Physiol 2010, 298:F1078-F1094.
34. Ouellette A.J., Malt R.A., Sukhatme V.P., Bonventre J.V. Expression of two "immediate early" genes, Egr-1 and c-fos, in response to renal ischemia and during compensatory renal hypertrophy in mice. J Clin Invest 1990, 85:766-771.
35. Witzgall R., Brown D., Schwarz C., Bonventre J.V. Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest 1994, 93:2175-2188.
36. Supavekin S., Zhang W., Kucherlapati R., Kaskel F.J., Moore L.C., Devarajan P. Differential gene expression following early renal ischemia/reperfusion. Kidney Int 2003, 63:1714-1724.
37. Yuen P.S., Jo S.K., Holly M.K., Hu X., Star R.A. Ischemic and nephrotoxic acute renal failure are distinguished by their broad transcriptomic responses. Physiol Genomics 2006, 25:375-386.
38. Maki A., Berezesky I.K., Fargnoli J., Holbrook N.J., Trump B.F. Role of [Ca2+]i in induction of c-fos, c-jun, and c-myc mRNA in rat PTE after oxidative stress. FASEB J 1992, 6:919-924.
39. Ichimura T., Bonventre J.V., Bailly V., et al. Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. J Biol Chem 1998, 273:4135-4142.
40. Mishra J., Ma Q., Prada A., et al. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 2003, 14:2534-2543.
41. Huang Q., Dunn R.T., Jayadev S., et al. Assessment of cisplatin-induced nephrotoxicity by microarray technology. Toxicol Sci 2001, 63:196-207.
42. Yoshida T., Kurella M., Beato F., et al. Monitoring changes in gene expression in renal ischemia-reperfusion in the rat. Kidney Int 2002, 61:1646-1654.
43. Koyner J.L., Parikh C.R. Clinical utility of biomarkers of AKI in cardiac surgery and critical illness. Clin J Am Soc Nephrol 2013, 8:1034-1042.
44. Nath K.A. Heme oxygenase-1 and acute kidney injury. Curr Opin Nephrol Hypertens 2014, 23:17-24.
45. Schmidt-Ott K.M., Mori K., Li J.Y., et al. Dual action of neutrophil gelatinase-associated lipocalin. J Am Soc Nephrol 2007, 18:407-413.
46. McCord J.M. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985, 312:159-163.
47. Mori K., Lee H.T., Rapoport D., et al. Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 2005, 115:610-621.
48. Ichimura T., Asseldonk E.J., Humphreys B.D., Gunaratnam L., Duffield J.S., Bonventre J.V. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest 2008, 118:1657-1668.
49. Cheng C.W., Rifai A., Ka S.M., et al. Calcium-binding proteins annexin A2 and S100A6 are sensors of tubular injury and recovery in acute renal failure. Kidney Int 2005, 68:2694-2703.
50. Camors E., Monceau V., Charlemagne D. Annexins and Ca2+ handling in the heart. Cardiovasc Res 2005, 65:793-802.
51. Yung S., Cheung K.F., Zhang Q., Chan T.M. Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis. J Am Soc Nephrol 2010, 21:1912-1927.
52. Klein C.L., Hoke T.S., Fang W.F., Altmann C.J., Douglas I.S., Faubel S. Interleukin-6 mediates lung injury following ischemic acute kidney injury or bilateral nephrectomy. Kidney Int 2008, 74:901-909.
53. Kielar M.L., John R., Bennett M., et al. Maladaptive role of IL-6 in ischemic acute renal failure. J Am Soc Nephrol 2005, 16:3315-3325.
54. Suzuki C., Isaka Y., Shimizu S., et al. Bcl-2 protects tubular epithelial cells from ischemia reperfusion injury by inhibiting apoptosis. Cell Transplant 2008, 17:223-229.
55. Wei Q., Yin X.M., Wang M.H., Dong Z. Bid deficiency ameliorates ischemic renal failure and delays animal death in C57BL/6 mice. Am J Physiol Renal Physiol 2006, 290:F35-F42.
56. Wei Q., Dong G., Chen J.K., Ramesh G., Dong Z. Bax and Bak have critical roles in ischemic acute kidney injury in global and proximal tubule-specific knockout mouse models. Kidney Int 2013, 84:138-148.
57. Devarajan P., Mishra J., Supavekin S., Patterson L.T., Steven Potter S. Gene expression in early ischemic renal injury: clues towards pathogenesis, biomarker discovery, and novel therapeutics. Mol Genet Metab 2003, 80:365-376.
58. Kobayashi T., Terada Y., Kuwana H., et al. Expression and function of the Delta-1/Notch-2/Hes-1 pathway during experimental acute kidney injury. Kidney Int 2008, 73:1240-1250.
59. Imgrund M., Grone E., Grone H.J., et al. Re-expression of the developmental gene Pax-2 during experimental acute tubular necrosis in mice 1. Kidney Int 1999, 56:1423-1431.
60. Takasato M., Er P.X., Becroft M., et al. Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat Cell Biol 2014, 16:118-126.
61. 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 2014, 14:53-67.
62. Xia Y., Nivet E., Sancho-Martinez I., et al. Directed differentiation of human pluripotent cells to ureteric bud kidney progenitor-like cells. Nat Cell Biol 2013, 15:1507-1515.
63. Emery B., Barres B.A. Unlocking CNS cell type heterogeneity. Cell 2008, 135:596-598.
64. Doyle J.P., Dougherty J.D., Heiman M., et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 2008, 135:749-762.
65. Heiman M., Schaefer A., Gong S., et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 2008, 135:738-748.
66. Liu J., Krautzberger A.M., Sui S.H., et al. Cell-specific translational profiling in acute kidney injury. J Clin Invest 2014, 124:1242-1254.
67. Riss J., Khanna C., Koo S., et al. Cancers as wounds that do not heal: differences and similarities between renal regeneration/repair and renal cell carcinoma. Cancer Res 2006, 66:7216-7224.
68. Kelly K.J., Williams W.W., Colvin R.B., et al. Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 1996, 97:1056-1063.
69. Arfian N., Emoto N., Vignon-Zellweger N., Nakayama K., Yagi K., Hirata K. ET-1 deletion from endothelial cells protects the kidney during the extension phase of ischemia/reperfusion injury. Biochem Biophys Res Commun 2012, 425:443-449.
70. 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, 60:2164-2172.
71. Nath K.A., Haggard J.J., Croatt A.J., Grande J.P., Poss K.D., Alam J. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 2000, 156:1527-1535.
72. Li H.F., Cheng C.F., Liao W.J., Lin H., Yang R.B. ATF3-mediated epigenetic regulation protects against acute kidney injury. J Am Soc Nephrol 2010, 21:1003-1013.
73. Ko G.J., Grigoryev D.N., Linfert D., et al. Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI-to-CKD transition. Am J Physiol Renal Physiol 2010, 298:F1472-F1483.
74. Aikawa E., Aikawa M., Libby P., et al. Arterial and aortic valve calcification abolished by elastolytic cathepsin S deficiency in chronic renal disease. Circulation 2009, 119:1785-1794.
75. Walport M.J. Complement. First of two parts. N Engl J Med 2001, 344:1058-1066.
76. Brown K.M., Kondeatis E., Vaughan R.W., et al. Influence of donor C3 allotype on late renal-transplantation outcome. N Engl J Med 2006, 354:2014-2023.
77. Stroo I., Stokman G., Teske G.J., et al. Chemokine expression in renal ischemia/reperfusion injury is most profound during the reparative phase. Int Immunol 2010, 22:433-442.
78. Ko G.J., Linfert D., Jang H.R., et al. Transcriptional analysis of infiltrating T cells in kidney ischemia-reperfusion injury reveals a pathophysiological role for CCR5. Am J Physiol Renal Physiol 2012, 302:F762-F773.
79. Riella L.V., Sayegh M.H. T-cell co-stimulatory blockade in transplantation: two steps forward one step back!. Expert Opin Biol Ther 2013, 13:1557-1568.
80. Wei Q., Bhatt K., He H.Z., Mi Q.S., Haase V.H., Dong Z. Targeted deletion of Dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 2010, 21:756-761.
81. Godwin J.G., Ge X., Stephan K., Jurisch A., Tullius S.G., Iacomini J. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci U S A 2010, 107:14339-14344.
82. Saikumar J., Hoffmann D., Kim T.M., et al. Expression, circulation, and excretion profile of microRNA-21, -155, and -18a following acute kidney injury. Toxicol Sci 2012, 129:256-267.
83. Chau B.N., Xin C., Hartner J., et al. MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Sci Transl Med 2012, 4. (121ra18).
84. Li L., Chen X.P., Li Y.J. MicroRNA-146a and human disease. Scand J Immunol 2010, 71:227-231.
85. Ichii O., Otsuka S., Sasaki N., Namiki Y., Hashimoto Y., Kon Y. Altered expression of microRNA miR-146a correlates with the development of chronic renal inflammation. Kidney Int 2012, 81:280-292.
86. Basile D.P., Fredrich K., Alausa M., et al. Identification of persistently altered gene expression in the kidney after functional recovery from ischemic acute renal failure. Am J Physiol Renal Physiol 2005, 288:F953-F963.
87. Zhang Z.X., Shek K., Wang S., et al. Osteopontin expressed in tubular epithelial cells regulates NK cell-mediated kidney ischemia reperfusion injury. J Immunol 2010, 185:967-973.
88. Persy V.P., Verhulst A., Ysebaert D.K., De Greef K.E., De Broe M.E. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int 2003, 63:543-553.
89. Viau A., El Karoui K., Laouari D., et al. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010, 120:4065-4076.
90. Schroppel B., Kruger B., Walsh L., et al. Tubular expression of KIM-1 does not predict delayed function after transplantation. J Am Soc Nephrol 2010, 21:536-542.
91. van Timmeren M.M., Vaidya V.S., van Ree R.M., et al. High urinary excretion of kidney injury molecule-1 is an independent predictor of graft loss in renal transplant recipients. Transplantation 2007, 84:1625-1630.
92. Humphreys B.D., Xu F., Sabbisetti V., et al. Chronic epithelial kidney injury molecule-1 expression causes murine kidney fibrosis. J Clin Invest 2013, 123:4023-4035.
93. Furuichi K., Gao J.L., Horuk R., Wada T., Kaneko S., Murphy P.M. Chemokine receptor CCR1 regulates inflammatory cell infiltration after renal ischemia-reperfusion injury. J Immunol 2008, 181:8670-8676.
94. Krupa A., Jenkins R., Luo D.D., Lewis A., Phillips A., Fraser D. Loss of MicroRNA-192 promotes fibrogenesis in diabetic nephropathy. J Am Soc Nephrol 2010, 21:438-447.
95. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
96. Tran M., Tam D., Bardia A., et al. PGC-1alpha promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest 2011, 121:4003-4014.
97. Portilla D., Dai G., McClure T., et al. Alterations of PPARalpha and its coactivator PGC-1 in cisplatin-induced acute renal failure. Kidney Int 2002, 62:1208-1218.
98. Krishnamoorthy A., Ajay A.K., Hoffmann D., et al. Fibrinogen β-derived Bbeta(15-42) peptide protects against kidney ischemia/reperfusion injury. Blood 2011, 118:1934-1942.
99. Madeddu P., Vio C.P., Straino S., Salis M.B., Milia A.F., Emanueli C. Renal phenotype of low kallikrein rats. Kidney Int 2001, 59:2233-2242.
100. Kinsey G.R., Sharma R., Huang L., et al. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J Am Soc Nephrol 2009, 20:1744-1753.
101. Kim M.G., Koo T.Y., Yan J.J., et al. IL-2/anti-IL-2 complex attenuates renal ischemia-reperfusion injury through expansion of regulatory T cells. J Am Soc Nephrol 2013, 24:1529-1536.
102. Gandolfo M.T., Jang H.R., Bagnasco S.M., et al. Foxp3+ regulatory T cells participate in repair of ischemic acute kidney injury. Kidney Int 2009, 76:717-729.
103. Famulski K.S., de Freitas D.G., Kreepala C., et al. Molecular phenotypes of acute kidney injury in kidney transplants. J Am Soc Nephrol 2012, 23:948-958.
104. Famulski K.S., Reeve J., de Freitas D.G., Kreepala C., Chang J., Halloran P.F. Kidney transplants with progressing chronic diseases express high levels of acute kidney injury transcripts. Am J Transplant 2013, 13:634-644.
105. Halloran P.F., Reeve J.P., Pereira A.B., Hidalgo L.G., Famulski K.S. Antibody-mediated rejection, T cell-mediated rejection, and the injury-repair response: new insights from the Genome Canada studies of kidney transplant biopsies. Kidney Int 2014, 85:258-264.
106. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10:57-63.
107. Wilhelm B.T., Marguerat S., Watt S., et al. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 2008, 453:1239-1243.
108. Brunskill E.W., Lai H.L., Jamison D.C., Potter S.S., Patterson L.T. Microarrays and RNA-Seq identify molecular mechanisms driving the end of nephron production. BMC. Dev Biol 2011, 11:15.