Hypoxia-inducible factor-2α and TGF-β signaling interact to promote normoxic glomerular fibrogenesis

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 9, 2013, Pages

  Hanna, Christian ^a,b   Hubchak, Susan C ^a   Liang, Xiaoyan ^a   Rozen Zvi, Benaya ^a   Schumacker, Paul T ^a,b   Hayashida, Tomoko ^a,b   William Schnaper, H ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CHILDREN'S MEMORIAL HOSPITAL   (United States)

Author keywords

Collagen; Fibrosis; HIF; TGF

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; DOXORUBICIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROGENESIS; GENE OVEREXPRESSION; GLOMERULOSCLEROSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY TUBULE CELL; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84886997795     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00155.2013     Document Type: Article

References (30)

1. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor α-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275: 36803-36810, 2000.
2. Basu RK, Hubchak S, Hayashida T, Runyan CE, Schumacker PT, Schnaper HW. Interdependence of HIF-1+ and TGF-α/Smad3 signaling in normoxic and hypoxic renal epithelial cell collagen expression. Am J Physiol Renal Physiol 300: F898-F905, 2011.
3. Bernhardt WM, Câmpean V, Kany S, Jürgensen JS, Weidemann A, Warnecke C, Arend M, Klaus S, Günzler V, Amann K, Willam C, Wiesener MS, Eckardt KU. Preconditional activation of hypoxia-induc-ible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 17: 1970-1978, 2006.
4. Berra E, Pages G, Pouyssegur J. MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev 19: 139-145, 2000.
5. Bottinger EP, Bitzer M. TGF-α signaling in renal disease. J Am Soc Nephrol 13: 2600-2610, 2002.
6. 2 sensing. J Biol Chem 275: 25130-25138, 2000.
7. Edgley AJ, Gow RM, Kelly DJ. Laser-capture microdissection and pressure catapulting for the analysis of gene expression in the renal glomerulus. Methods Mol Biol 611: 29-40, 2010.
8. Finer G, Schnaper HW, Kanwar YS, Liang X, Lin HY, Hayashida T. Divergent roles of Smad3 and PI3-kinase in murine adriamycin nephropathy indicate distinct mechanisms of proteinuria and fibrogenesis. Kidney Int 82: 525-536, 2012.
9. Flügel D, Görlach A, Michiels C, Kietzmann T. Glycogen synthase kinase 3 phosphorylates hypoxia-inducible factor 1+ and mediates its destabilization in a VHL-independent manner. Mol Cell Biol 27: 3253-3265, 2007.
10. Haase VH. The VHL/HIF oxygen-sensing pathway and its relevance to kidney disease. Kidney Int 69: 1302-1307, 2006.
11. 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. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117: 3810-3820, 2007.
12. Holmquist-Mengelbier L, Fredlund E, Löfstedt T, Noguera R, Navarro S, Nilsson H, Pietras A, Vallo Christersson J, Borg A, Gradin K, Poellinger L, Påhlman S. Recruitment of HIF-1+ and HIF-2+ to common target genes is differentially regulated in neuroblastoma: HIF-2+ promotes an aggressive phenotype. Cancer Cell 10: 413-423, 2006.
13. Keith B, Johnson RS, Simon MC. HIF1+ and HIF2+: sibling rivalry in hypoxic tumor growth and progression. Nat Rev Cancer 12: 9-22, 2012.
14. Kietzmann T, Roth U, Jungermann K. Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes. Blood 94: 4177-4185, 1999.
15. Kimura K, Iwano M, Higgins DF, Yamaguchi Y, Nakatani K, Harada K, Kubo A, Akai Y, Rankin EB, Neilson EG, Haase VH, Saito Y. Stable expression of HIF-1+ in tubular epithelial cells promotes interstitial fibrosis. Am J Physiol Renal Physiol 295: F1023-F1029, 2008.
16. Koh MY, Lemos R Jr, Liu X, Powis G. The hypoxia-associated factor switches cells from HIF-1+-to HIF-2+-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res 71: 4015-4027, 2011.
17. Okuda S, Oh Y, Tsuruda H, Onoyama K, Fujimi S, Fujishima M. Adriamycin-induced nephropathy as a model of chronic progressive glomerular disease. Kidney Int 29: 502-510, 1986.
18. Page EL, Robitaille GA, Pouyssegur J, Richard DE. Induction of hypoxia-inducible factor-1+ by transcriptional and translational mechanisms. J Biol Chem 277: 48403-48409, 2002.
19. Poncelet AC, de Caestecker MP, Schnaper HW. The transforming growth factor-β/SMAD signaling pathway is present and functional in human mesangial cells. Kidney Int 56: 1354-1365, 1999.
20. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443, 2006.
21. Richard DE, Berra E, Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1+ in vascular smooth muscle cells. J Biol Chem 275: 26765-26771, 2000.
22. Rosenberger C, Mandriota S, Jürgensen JS, Wiesener MS, Hörstrup JH, Frei U, Ratcliffe PJ, Maxwell PH, Bachmann S, Eckardt KU. Expression of hypoxia-inducible factor-1+ and-2+ in hypoxic and ischemic rat kidneys. J Am Soc Nephrol 13: 1721-1732, 2002.
23. Rozen-zvi B, Hayashida T, Hubchak SC, Hanna C, Platanias L, Schnaper HW. TGF-β/Smad3 activates mammalian target of rapamycin complex-1 to promote collagen production by increasing HIF-1+ expression. Am J Physiol Renal Physiol 305: F485-F494, 2013.
24. Schnaper HW, Hubchak SC, Runyan CE, Browne JA, Finer G, Liu X, Hayashida T. A conceptual framework for the molecular pathogenesis of progressive kidney disease. Pediatr Nephrol 25: 2223-2230, 2010.
25. Schnaper HW, Jandeska S, Runyan CE, Hubchak SC, Basu RK, Curley JF, Smith RD, Hayashida T. TGF-β signal transduction in chronic kidney disease. Front Biosci 14: 2448-2465, 2009.
26. Schnaper HW, Kopp JB, Poncelet AC, Hubchak SC, Stetler-Stevenson WG, Klotman PE, Kleinman HK. Increased expression of extracellular matrix proteins and decreased expression of matrix proteases after serial passage of glomerular mesangial cells. J Cell Sci 109: 2521-2528, 1996.
27. 2 homeostasis by hypoxiainducible factor 1. Annu Rev Cell Dev Biol 15: 551-578, 1999.
28. Sharma K, Ziyadeh FN. Hyperglycemia and diabetic kidney disease. The case for transforming growth factor-β as a key mediator. Diabetes 44: 1139-1146, 1995.
29. Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza GL, Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem 277: 27975-27981, 2002.
30. Yan Q, Bartz S, Mao M, Li L, Kaelin WG Jr. The hypoxia-inducible factor 2+ N-terminal and C-terminal transactivation domains cooperate to promote renal tumorigenesis in vivo. Mol Cell Biol 27: 2092-2102, 2007.