In vivo evidence suggesting reciprocal renal hypoxia-inducible factor-1 upregulation and signal transducer and activator of transcription 3 activation in response to hypoxic and non-hypoxic stimuli

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 4, 2013, Pages 262-272

  Nechemia Arbely, Yael ^a   Khamaisi, Mogher ^b   Rosenberger, Christian ^c   Koesters, Robert ^d   Shina, Ahuva ^a   Geva, Carmit ^a   Shriki, Anat ^a   Klaus, Stephen ^e   Rosen, Seymour ^f   Rose John, Stefan ^g   Galun, Eithan ^a   Axelrod, Jonathan H ^a   Heyman, Samuel N ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e FIBROGEN INC   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF KIEL   (Germany)

Author keywords

Acute kidney injury; Hypoxia; Hypoxia inducible factor; Signal transducer and activator of transcription 3; Von Hippel Lindau factor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MIMOSINE; STAT3 PROTEIN; VON HIPPEL LINDAU PROTEIN; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; STAT3 PROTEIN, MOUSE; VHLH PROTEIN, MOUSE;

ACUTE KIDNEY FAILURE; ARTICLE; CELL TYPE; CONTROLLED STUDY; GENE ACTIVATION; HYPOXIA; IMMUNOHISTOCHEMISTRY; KIDNEY CELL; KIDNEY INJURY; MALE; MOUSE; NONHUMAN; RAT; RHABDOMYOLYSIS; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANOXIA; BAGG ALBINO MOUSE; DRUG EFFECTS; GENETICS; KIDNEY; KNOCKOUT MOUSE; METABOLISM; SPRAGUE DAWLEY RAT;

ACUTE KIDNEY INJURY; ANIMALS; ANOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84875645849     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12064     Document Type: Article

References (51)

1. Gunaratnam L, Bonventre JV. HIF in kidney disease and development. J. Am. Soc. Nephrol. 2009; 20: 1877-87.
2. Haase VH. The VHL/HIF oxygen-sensing pathway and its relevance to kidney disease. Kidney Int. 2006; 69: 1302-7.
3. Nangaku M, Eckardt KU. Hypoxia and the HIF system in kidney disease. J. Mol. Med. 2007; 85: 1325-30.
4. Noman MZ, Buart S, Van Pelt J et al. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J. Immunol. 2009; 182: 3510-21.
5. Selvendiran K, Bratasz A, Kuppusamy ML, Tazi MF, Rivera BK, Kuppusamy P. Hypoxia induces chemoresistance in ovarian cancer cells by activation of signal transducer and activator of transcription 3. Int. J. Cancer 2009; 125: 2198-204.
6. Wang GS, Qian GS, Zhou DS, Zhao JQ. JAK-STAT signaling pathway in pulmonary arterial smooth muscle cells is activated by hypoxia. Cell Biol. Int. 2005; 29: 598-603.
7. Nechemia-Arbely Y, Barkan D, Pizov G et al. IL-6/IL-6R axis plays a critical role in acute kidney injury. J. Am. Soc. Nephrol. 2008; 19: 1106-15.
8. Rosenberger C, Heyman SN, Rosen S et al. Up-regulation of HIF in experimental acute renal failure: Evidence for a protective transcriptional response to hypoxia. Kidney Int. 2005; 67: 531-42.
9. Wang M, Tan J, Coffey A, Fehrenbacher J, Weil BR, Meldrum DR. Signal transducer and activator of transcription 3-stimulated hypoxia inducible factor-1alpha mediates estrogen receptor-alpha-induced mesenchymal stem cell vascular endothelial growth factor production. J. Thorac. Cardiovasc. Surg. 2009; 138: 163-71.
10. Wincewicz A, Koda M, Sulkowska M, Kanczuga-Koda L, Wincewicz D, Sulkowski S. STAT3 and hypoxia induced proteins: HIF-1alpha, EPO and EPOR in relation with Bax and Bcl-xL in nodal metastases of ductal breast cancers. Folia Histochem. Cytobiol. 2009; 47: 425-30.
11. Aggarwal BB, Kunnumakkara AB, Harikumar KB et al. Signal transducer and activator of transcription-3, inflammation, and cancer: How intimate is the relationship? Ann. N.Y. Acad. Sci. 2009; 1171: 59-76.
12. Chen Z, Han ZC. STAT3: A critical transcription activator in angiogenesis. Med. Res. Rev. 2008; 28: 185-200.
13. Levy DE, Lee CK. What does Stat3 do? J. Clin. Invest. 2002; 109: 1143-8.
14. YuH, Pardoll D, Jove R. STATs in cancer inflammation and immunity: A leading role for STAT3. Nat. Rev. Cancer 2009; 9: 798-809.
15. Gray MJ, Zhang J, Ellis LM et al. HIF-1alpha, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene 2005; 24: 3110-20.
16. Jung JE, Lee HG, Cho IH et al. STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J. 2005; 19: 1296-8.
17. Wincewicz A, Koda M, Sulkowska M, Kanczuga-Koda L, Sulkowski S. Comparison of STAT3 with HIF-1alpha, Ob and ObR expressions in human endometrioid adenocarcinomas. Tissue Cell 2008; 40: 405-10.
18. Wincewicz A, Sulkowska M, Koda M, Lesniewicz T, Kanczuga-Koda L, Sulkowski S. STAT3, HIF-1alpha, EPO and EPOR: Signaling proteins in human primary ductal breast cancers. Folia Histochem. Cytobiol. 2007; 45: 81-6.
19. Jung JE, Kim HS, Lee CS et al. STAT3 inhibits the degradation of HIF-1alpha by pVHL-mediated ubiquitination. Exp. Mol. Med. 2008; 40: 479-85.
20. Lang SA, Moser C, Gaumann A et al. Targeting heat shock protein 90 in pancreatic cancer impairs insulin-like growth factor-I receptor signaling, disrupts an interleukin-6/signal-transducer and activator of transcription 3/hypoxia-inducible factor-1alpha autocrine loop, and reduces orthotopic tumor growth. Clin. Cancer Res. 2007; 13: 6459-68.
21. Moser C, Lang SA, Mori A et al. ENMD-1198, a novel tubulin-binding agent reduces HIF-1alpha and STAT3 activity in human hepatocellular carcinoma (HCC) cells, and inhibits growth and vascularization in vivo. BMC Cancer 2008; 8: 206.
22. Singh-Gupta V, Zhang H, Banerjee S et al. Radiation-induced HIF-1alpha cell survival pathway is inhibited by soy isoflavones in prostate cancer cells. Int. J. Cancer 2009; 124: 1675-84.
23. Ghosh AK, Shanafelt TD, Cimmino A et al. Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells. Blood 2009; 113: 5568-74.
24. Santra M, Santra S, Zhang J, Chopp M. Ectopic decorin expression up-regulates VEGF expression in mouse cerebral endothelial cells via activation of the transcription factors Sp1, HIF1alpha, and Stat3. J. Neurochem. 2008; 105: 324-37.
25. Xu Q, Briggs J, Park S et al. Targeting Stat3 blocks both HIF-1 and VEGF expression induced by multiple oncogenic growth signaling pathways. Oncogene 2005; 24: 5552-60.
26. Nasimuzzaman M, Waris G, Mikolon D, Stupack DG, Siddiqui A. Hepatitis C virus stabilizes hypoxia-inducible factor 1alpha and stimulates the synthesis of vascular endothelial growth factor. J. Virol. 2007; 81: 10249-57.
27. Rosenberger C, Mandriota S, Jurgensen JS et al. Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J. Am. Soc. Nephrol. 2002; 13: 1721-32.
28. Rosenberger C, Pratschke J, Rudolph B et al. Immunohistochemical detection of hypoxia-inducible factor-1alpha in human renal allograft biopsies. J. Am. Soc. Nephrol. 2007; 18: 343-51.
29. Goldfarb M, Rosenberger C, Abassi Z et al. Acute-on-chronic renal failure in the rat: Functional compensation and hypoxia tolerance. Am. J. Nephrol. 2006; 26: 22-33.
30. Rosenberger C, Khamaisi M, Abassi Z et al. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int. 2008; 73: 34-42.
31. Fischer M, Goldschmitt J, Peschel C et al. A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat. Biotechnol. 1997; 15: 142-5.
32. Agmon Y, Peleg H, Greenfeld Z, Rosen S, Brezis M. Nitric oxide and prostanoids protect the renal outer medulla from radiocontrast toxicity in the rat. J. Clin. Invest. 1994; 94: 1069-75.
33. Rosenberger C, Goldfarb M, Shina A et al. Evidence for sustained renal hypoxia and transient hypoxia adaptation in experimental rhabdomyolysis-induced acute kidney injury. Nephrol. Dial. Transplant. 2008; 23: 1135-43.
34. Schonig K, Schwenk F, Rajewsky K, Bujard H. Stringent doxycycline dependent control of CRE recombinase in vivo. Nucleic Acids Res. 2002; 30: e134.
35. Traykova-Brauch M, Schonig K, Greiner O et al. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat. Med. 2008; 14: 979-84.
36. Mathia S, Paliege A, Koesters R et al. Action of hypoxia-inducible factor in liver and kidney from mice with Pax8-Rtta based deletion of von Hippel-Lindau protein. Acta Physiol. 2013; 207: 565-75.
37. Khamaisi M, Raz I, Shilo V et al. Diabetes and radiocontrast media increase endothelin converting enzyme-1 in the kidney. Kidney Int. 2008; 74: 91-100.
38. Darnell JE Jr. Reflections on STAT3, STAT5, and STAT6 as fat STATs. Proc. Natl Acad. Sci. USA 1996; 93: 6221-4.
39. Peters M, Blinn G, Solem F, Fischer M, Meyer zum Buschenfelde KH, Rose-John S. In vivo and in vitro activities of the gp130-stimulating designer cytokine Hyper-IL-6. J. Immunol. 1998; 161: 3575-81.
40. Rosenberger C, Rosen S, Shina A et al. Activation of hypoxia-inducible factors ameliorates hypoxic distal tubular injury in the isolated perfused rat kidney. Nephrol. Dial. Transplant. 2008; 23: 3472-8.
41. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem. Pharmacol. 2002; 64: 993-8.
42. Weidemann A, Bernhardt WM, Klanke B et al. HIF activation protects from acute kidney injury. J. Am. Soc. Nephrol. 2008; 19: 486-94.
43. Berthier CC, Zhang H, Schin M et al. Enhanced expression of Janus kinase-signal transducer and activator of transcription pathway members in human diabetic nephropathy. Diabetes 2009; 58: 469-77.
44. Heyman SN, Rosenberger C, Rosen S. Experimental ischemia-reperfusion: Biases and myths: The proximal vs. distal hypoxic tubular injury debate revisited. Kidney Int. 2010; 77: 9-16.
45. Rosenberger C, Griethe W, Gruber G et al. Cellular responses to hypoxia after renal segmental infarction. Kidney Int. 2003; 64: 874-86.
46. Rosenberger C, Rosen S, Heyman SN. Renal parenchymal oxygenation and hypoxia adaptation in acute kidney injury. Clin. Exp. Pharmacol. Physiol. 2006; 33: 980-8.
47. Paliege A, Rosenberger C, Bondke A et al. Hypoxia-inducible factor-2alpha-expressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. Kidney Int. 2010; 77: 312-18.
48. Boengler K, Hilfiker-Kleiner D, Drexler H, Heusch G, Schulz R. The myocardial JAK/STAT pathway: From protection to failure. Pharmacol. Ther. 2008; 120: 172-85.
49. Schodel J, Klanke B, Weidemann A et al. HIF-prolyl hydroxylases in the rat kidney: Physiologic expression patterns and regulation in acute kidney injury. Am. J. Pathol. 2009; 174: 1663-74.
50. Chen SH, Murphy DA, Lassoued W, Thurston G, Feldman MD, Lee WM. Activated STAT3 is a mediator and biomarker of VEGF endothelial activation. Cancer Biol. Ther. 2008; 7: 1994-2003.
51. Westenfelder C, Biddle DL, Baranowski RL. Human, rat, and mouse kidney cells express functional erythropoietin receptors. Kidney Int. 1999; 55: 808-20.