Inflammation and hypoxia linked to renal injury by CCAAT/enhancer-binding protein δ

Kidney International

Volumn 88, Issue 2, 2015, Pages 262-275

  Yamaguchi, Junna ^a   Tanaka, Tetsuhiro ^a   Eto, Nobuaki ^b   Nangaku, Masaomi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYOWA HAKKO KOGYO CO LTD   (Japan)

Author keywords

cell signaling; hypoxia; inflammation; proximal tubule

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN DELTA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; SHORT HAIRPIN RNA; ANGIOPOIETIN; ANGPTL4 PROTEIN, MOUSE; AUTACOID; CISPLATIN; COPPER ZINC SUPEROXIDE DISMUTASE; HEME OXYGENASE 1; MESSENGER RNA; SMALL INTERFERING RNA; SOD1 PROTEIN, HUMAN; SOD1 PROTEIN, MOUSE; SOD1 PROTEIN, RAT; SUPEROXIDE DISMUTASE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HYPOXIA; INFLAMMATION; KIDNEY ARTERY STENOSIS; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; TRANSCRIPTION REGULATION; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL HYPOXIA; COMPLICATION; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; KIDNEY; KIDNEY PROXIMAL TUBULE; MALE; METABOLISM; MOUSE; NEPHRECTOMY; NEPHRITIS; PATHOLOGY; PHYSIOLOGY; REPERFUSION INJURY; SIGNAL TRANSDUCTION; UPREGULATION;

ANGIOPOIETINS; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL HYPOXIA; CELLS, CULTURED; CISPLATIN; EPITHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEME OXYGENASE-1; HUMANS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION MEDIATORS; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; NEPHRECTOMY; NEPHRITIS; NF-KAPPA B; RENAL ARTERY OBSTRUCTION; REPERFUSION INJURY; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE-1; TRANSCRIPTION, GENETIC; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84938553872     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.21     Document Type: Article

References (56)

1. Semenza GL. Oxygen sensing, homeostasis, and disease. N Engl J Med 2011; 365: 537-547
2. Bohle A, Mackensen-Haen S, Wehrmann M. Significance of postglomerular capillaries in the pathogenesis of chronic renal failure. Kidney Blood Press Res 1996; 19: 191-195
3. Fine LG, Bandyopadhay D, Norman JT. Is there a common mechanism for the progression of different types of renal diseases other than proteinuria?. Towards the unifying theme of chronic hypoxia. Kidney Int 2000; 57(Suppl 75): S22-S26
4. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 2006; 17: 17-25
5. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 2012; 148: 399-408
6. Tanaka T, Wiesener M, Bernhardt W et al. The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 2009; 424: 143-151
7. Rosenberger C, Mandriota S, Jürgensen JS et al. Expression of hypoxiainducible factor-1a and -2a in hypoxic and ischemic rat kidneys. J Am Soc Nephrol 2002; 13: 1721-1732
8. Matsumoto M, Makino Y, Tanaka T et al. Induction of renoprotective gene expression by cobalt ameliorates ischemic injury of the kidney in rats. J Am Soc Nephrol 2003; 14: 1825-1832
9. Tanaka T, Miyata T, Inagi R et al. Hypoxia in renal disease with proteinuria and/or glomerular hypertension. Am J Pathol 2004; 165: 1979-1992
10. Tanaka T, Kojima I, Ohse T et al. Hypoxia-inducible factor modulates tubular cell survival in cisplatin nephrotoxicity. Am J Physiol Renal Physiol 2005; 289: F1123-F1133
11. Tanaka T, Kojima I, Ohse T et al. Cobalt promotes angiogenesis via hypoxia-inducible factor and protects tubulointerstitium in the remnant kidney model. Lab Invest 2005; 85: 1292-1307
12. Tanaka T, Matsumoto M, Inagi R et al. Induction of protective genes by cobalt ameliorates tubulointerstitial injury in the progressive Thy1 nephritis. Kidney Int 2005; 68: 2714-2725
13. Bernhardt WM, Câmpean V, Kany S et al. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 2006; 17: 1970-1978
14. Bernhardt WM, Gottmann U, Doyon F et al. Donor treatment with a PHD-inhibitor activating HIFs prevents graft injury and prolongs survival in an allogenic kidney transplant model. Proc Natl Acad Sci USA 2009; 106: 21276-21281
15. Hill P, Shukla D, Tran MG et al. Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 2008; 19: 39-46
16. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3: 721-732
17. Blouin CC, Pagé EL, Soucy GM et al. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 2004; 103: 1124-1130
18. Rius J, Guma M, Schachtrup C et al. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 2008; 453: 807-811
19. Kojima I, Tanaka T, Inagi R et al. Metallothionein is upregulated by hypoxia and stabilizes hypoxia-inducible factor in the kidney. Kidney Int 2009; 75: 268-277
20. Takiguchi M. The C/EBP family of transcription factors in the liver and other organs. Int J Exp Pathol 1998; 79: 369-391
21. Ramji DP, Foka P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J 2002; 365: 561-575
22. Manotham K, Tanaka T, Matsumoto M et al. Evidence of tubular hypoxia in the early phase in the remnant kidney model. J Am Soc Nephrol 2004; 15: 1277-1288
23. Min Y, Ghose S, Boelte K et al. C/EBP-d regulates VEGF-C autocrine signaling in lymphangiogenesis and metastasis of lung cancer through HIF-1a. Oncogene 2011; 30: 4901-4909
24. Alam T, An MR, Papaconstantinou J. Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J Biol Chem 1992; 267: 5021-5024
25. Juan TS, Wilson DR, Wilde MD et al. Participation of the transcription factor C/EBP delta in the acute-phase regulation of the human gene for complement component C3. Proc Natl Acad Sci USA 1993; 90: 2584-2588
26. Balamurugan K, Sharan S, Klarmann KD et al. FBXW7a attenuates inflammatory signalling by downregulating C/EBPd and its target gene Tlr4. Nat Commun 2013; 4: 1662
27. Treins C, Giorgetti-Peraldi S, Murdaca J et al. Insulin stimulates hypoxiainducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem 2002; 277: 27975-27981
28. Zhong H, Chiles K, Feldser D et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 2000; 60: 1541-1545
29. Stiehl DP, Jelkmann W, Wenger RH et al. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 2002; 512: 157-162
30. Ricardo SD, Van Goor H, Eddy AA. Macrophage diversity in renal injury and repair. J Clin Invest 2008; 118: 3522-3530
31. Chung AC, Lan HY. Chemokines in renal injury. J Am Soc Nephrol 2011; 22: 802-809
32. Tanaka T, Yamaguchi J, Higashijima Y et al. Indoxyl sulfate signals for rapid mRNA stabilization of Cbp/p300-interacting transactivator with Glu/ Asp-rich carboxy-Terminal domain 2 (CITED2) and suppresses the expression of hypoxia-inducible genes in experimental CKD and uremia. FASEB J 2013; 27: 4059-4075
33. Balamurugan K, Wang JM, Tsai HH et al. The tumour suppressor C/EBPd inhibits FBXW7 expression and promotes mammary tumour metastasis. EMBO J 2010; 29: 4106-4117
34. Osada S, Yamamoto H, Nishihara T et al. DNA binding specificity of the CCAAT/enhancer-binding protein transcription factor family. J Biol Chem 1996; 271: 3891-3896
35. Litvak V, Ramsey SA, Rust AG et al. Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat Immunol 2009; 10: 437-443
36. Cao Z, Umek RM, McKnight SL. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 1991; 5: 1538-1552
37. Kinoshita S, Akira S, Kishimoto T. A member of the C/EBP family, NF-IL6 beta, forms a heterodimer and transcriptionally synergizes with NF-IL6. Proc Natl Acad Sci USA 1992; 89: 1473-1476
38. Huang AM, Montagna C, Sharan S et al. Loss of CCAAT/enhancer binding protein delta promotes chromosomal instability. Oncogene 2004; 23: 1549-1557
39. Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med 2011; 364: 656-665
40. Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 2009; 9: 609-617
41. Karhausen J, Furuta GT, Tomaszewski JE et al. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 2004; 114: 1098-1106
42. Cramer T, Yamanishi Y, Clausen BE et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 2003; 112: 645-657
43. Kobayashi H, Gilbert V, Liu Q et al. Myeloid cell-derived hypoxia-inducible factor attenuates inflammation in unilateral ureteral obstruction-induced kidney injury. J Immunol 2012; 188: 5106-5115
44. Yamanaka S, Yokote S, Yamada A et al. Adipose tissue-derived mesenchymal stem cells in long-Term dialysis patients display downregulation of PCAF expression and poor angiogenesis activation. PLoS One 2014; 9: 1-14
45. Tang D, Sivko JS, DeWille JW. Promoter methylation reduces C/EBPdelta (CEBPD) gene expression in the SUM-52PE human breast cancer cell line and in primary breast tumors. Breast Cancer Res Treat 2006; 95: 161-170
46. Ko CY, Hsu HC, Shen MR et al. Epigenetic silencing of CCAAT/enhancer-binding protein delta activity by YY1/polycomb group/DNA methyltransferase complex. J Biol Chem 2008; 283: 30919-30932
47. Fitzpatrick SF, Tambuwala MM, Bruning U et al. An intact canonical NF-kB pathway is required for inflammatory gene expression in response to hypoxia. J Immunol 2011; 186: 1091-1096
48. Bonello S, Za'hringer C, BelAiba RS et al. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007; 27: 755-761
49. LeClair KP, Blanar MA, Sharp PA. The p50 subunit of NF-kappa B associates with the NF-IL6 transcription factor. Proc Natl Acad Sci USA 1992; 89: 8145-8149
50. Lee YH, Yano M, Liu SY et al. A novel cis-acting element controlling the rat CYP2D5 gene and requiring cooperativity between C/EBP beta and an Sp1 factor. Mol Cell Biol 1994; 14: 1383-1394
51. Mink S, Haenig B, Klempnauer KH. Interaction and functional collaboration of p300 and C/EBPbeta. Mol Cell Biol 1997; 17: 6609-6617
52. Diehl JA, Hannink M. Identification of a C/EBP-Rel complex in avian lymphoid cells. Mol Cell Biol 1994; 14: 6635-6646
53. Ray A, Hannink M, Ray BK. Concerted participation of NF-kappa B and C/EBP heteromer in lipopolysaccharide induction of serum amyloid A gene expression in liver. J Biol Chem 1995; 270: 7365-7374
54. Eto N, Miyagishi M, Inagi R et al. Mitogen-activated protein 3 kinase 6mediates angiogenic and tumorigenic effects via vascular endothelial growth factor expression. Am J Pathol 2009; 174: 1553-1563
55. Tanaka T, Yamaguchi J, Shoji K et al. Anthracycline inhibits recruitment of hypoxia-inducible transcription factors and suppresses tumor cell migration and cardiac angiogenic response in the host. J Biol Chem 2012; 287: 34866-34882
56. Nishio Y, Isshiki H, Kishimoto T et al. A nuclear factor for interleukin-6 expression (NF-IL6) and the glucocorticoid receptor synergistically activate transcription of the rat alpha 1-acid glycoprotein gene via direct protein-protein interaction. Mol Cell Biol 1993; 13: 1854-1862