Skip to main content
SpringerLink
Log in

Role of upstream stimulatory factor 2 in diabetic nephropathy

  • Review
  • Published:
Frontiers in Biology

Abstract

Diabetic nephropathy (DN) is the most common cause of end-stage renal disease (ESRD). About 20%–30% of people with type 1 and type 2 diabetes develop DN. DN is characterized by both glomerulosclerosis with thickening of the glomerular basement membrane and mesangial matrix expansion, and tubulointerstitial fibrosis. Hyperglycemia and the activation of the intra-renal renin-angiotensin system (RAS) in diabetes have been suggested to play a critical role in the pathogenesis of DN. However, the mechanisms are not well known.

Studies from our laboratory demonstrated that the transcription factor—upstream stimulatory factor 2 (USF2) is an important regulator of DN. Moreover, the renin gene is a downstream target of USF2. Importantly, USF2 transgenic (Tg) mice demonstrate a specific increase in renal renin expression and angiotensin II (AngII) levels in kidney and exhibit increased urinary albumin excretion and extracellular matrix deposition in glomeruli, supporting a role for USF2 in the development of diabetic nephropathy. In this review, we summarize our findings of the mechanisms by which diabetes regulates USF2 in kidney cells and its role in regulation of renal renin-angiotensin system and the development of diabetic nephropathy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andersen S, Tarnow L, Rossing P, Hansen B V, Parving H H (2000). Renoprotective effects of angiotensin II receptor blockade in type 1 diabetic patients with diabetic nephropathy. Kidney Int, 57(2): 601–606

    Article  CAS  PubMed  Google Scholar 

  • Anderson S, Jung F F, Ingelfinger J R (1993). Renal renin-angiotensin system in diabetes: functional, immunohistochemical, and molecular biological correlations. Am J Physiol, 265(4 Pt 2): F477–F486

  • Andrade A Q, Casarini D E, Schor N, Boim M A (2002). Characterization of renin mRNA expression and enzyme activity in rat and mouse mesangial cells. Braz J Med Biol Res, 35(1): 17–24

    Article  CAS  PubMed  Google Scholar 

  • Bertoluci M C, Schmid H, Lachat J J, Coimbra T M (1996). Transforming growth factor-beta in the development of rat diabetic nephropathy. A 10-month study with insulin-treated rats. Nephron, 74(1): 189–196

    CAS  Google Scholar 

  • Bidder M, Shao J S, Charlton-Kachigian N, Loewy A P, Semenkovich C F, Towler D A (2002). Osteopontin transcription in aortic vascular smooth muscle cells is controlled by glucose-regulated upstream stimulatory factor and activator protein-1 activities. J Biol Chem, 277 (46): 44485–44496

    Article  CAS  PubMed  Google Scholar 

  • Borch-Johnsen K, Andersen P K, Deckert T (1985). The effect of proteinuria on relative mortality in type 1 (insulin-dependent) diabetes mellitus. Diabetologia, 28(8): 590–596

    Article  CAS  PubMed  Google Scholar 

  • Border W A, Noble N A (1998a). Evidence that TGF-beta should be a therapeutic target in diabetic nephropathy. Kidney Int, 54(4): 1390–1391

    Article  CAS  PubMed  Google Scholar 

  • Border W A, Noble N A (1998b). Interactions of transforming growth factor-beta and angiotensin II in renal fibrosis. Hypertension, 31(1 Pt 2): 181–188

    Article  CAS  PubMed  Google Scholar 

  • Border W A, Noble N A, Ketteler M (1995). TGF-beta: a cytokine mediator of glomerulosclerosis and a target for therapeutic intervention. Kidney Int Suppl, 49(61): S59–S61

    Google Scholar 

  • Brenner B M, Cooper M E, de Zeeuw D, Keane W F, Mitch W E, Parving H H, Remuzzi G, Snapinn S M, Zhang Z, Shahinfar S, and the RENAAL Study Investigators (2001). Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med, 345(12): 861–869

    Article  CAS  PubMed  Google Scholar 

  • Burden A C, Thurston H (1979). Plasma renin activity in diabetes mellitus. Clin Sci (Lond), 56(3): 255–259

    CAS  Google Scholar 

  • Carey R M, Siragy H M (2003). The intrarenal renin-angiotensin system and diabetic nephropathy. Trends Endocrinol Metab, 14(6): 274–281

    Article  CAS  PubMed  Google Scholar 

  • Chan J C, Ko G T, Leung D H, Cheung R C, Cheung M Y, So W Y, Swaminathan R, Nicholls M G, Critchley J A, Cockram C S (2000). Long-term effects of angiotensin-converting enzyme inhibition and metabolic control in hypertensive type 2 diabetic patients. Kidney Int, 57(2): 590–600

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Shen Y H, Wang X, Wang J, Gan Y, Chen N, Wang J, LeMaire S A, Coselli J S, Wang X L (2006). Human prolyl-4-hydroxylase alpha(I) transcription is mediated by upstream stimulatory factors. J Biol Chem, 281(16): 10849–10855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Hong S W, Iglesias-de la Cruz M C, Isono M, Casaretto A, Ziyadeh F N (2001). The key role of the transforming growth factorbeta system in the pathogenesis of diabetic nephropathy. Ren Fail, 23 (3-4): 471–481

    Article  CAS  PubMed  Google Scholar 

  • Cooper M E (2001). Interaction of metabolic and haemodynamic factors in mediating experimental diabetic nephropathy. Diabetologia, 44 (11): 1957–1972

    Article  CAS  PubMed  Google Scholar 

  • Corre S, Galibert M D (2005). Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res, 18 (5): 337–348

    Article  CAS  PubMed  Google Scholar 

  • Dabhi B, Mistry K N (2015). Oxidative stress and its association with TNF-alpha-308 G/C and IL-1alpha-889 C/T gene polymorphisms in patients with diabetes and diabetic nephropathy. Gene. 56(2): 197–202

    Article  Google Scholar 

  • Daniel C, Schaub K, Amann K, Lawler J, Hugo C (2007). Thrombospondin-1 is an endogenous activator of TGF-beta in experimental diabetic nephropathy in vivo. Diabetes, 56(12): 2982–2989

    Article  CAS  PubMed  Google Scholar 

  • Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart R E, Acton S (2000). A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res, 87(5): E1–E9

    Google Scholar 

  • Durvasula R V, Shankland S J (2008). Activation of a local renin angiotensin system in podocytes by glucose. Am J Physiol Renal Physiol, 294(4): F830–F839

    Google Scholar 

  • Erman A, Veksler S, Gafter U, Boner G, Wittenberg C, van Dijk D J (2004). Renin-angiotensin system blockade prevents the increase in plasma transforming growth factor beta 1, and reduces proteinuria and kidney hypertrophy in the streptozotocin-diabetic rat. J Renin Angiotensin Aldosterone Syst, 5(3): 146–151

    Article  CAS  PubMed  Google Scholar 

  • Feener E P, King G L (1997). Vascular dysfunction in diabetes mellitus. Lancet, 350(Suppl1): SI9–SI13

  • Feldman D L, Jin L, Xuan H, Contrepas A, Zhou Y, Webb R L, Mueller D N, Feldt S, Cumin F, Maniara W, Persohn E, Schuetz H, Jan Danser A H, Nguyen G (2008). Effects of aliskiren on blood pressure, albuminuria, and (pro)renin receptor expression in diabetic TG (mRen-2)27 rats. Hypertension, 52(1): 130–136

    Article  CAS  PubMed  Google Scholar 

  • Ferrario C M, Trask A J, Jessup J A (2005). Advances in biochemical and functional roles of angiotensin-converting enzyme 2 and angiotensin-(1-7) in regulation of cardiovascular function. Am J Physiol Heart Circ Physiol, 289(6): H2281–H2290

    Google Scholar 

  • Fogo A B (1999). Mesangial matrix modulation and glomerulosclerosis. Exp Nephrol, 7(2): 147–159

    Article  CAS  PubMed  Google Scholar 

  • Forbes J M, Fukami K, Cooper M E (2007). Diabetic nephropathy: where hemodynamics meets metabolism. Exp Clin Endocrinol Diabetes, 115(2): 69–84

    Article  CAS  PubMed  Google Scholar 

  • Giacco F, Brownlee M (2010). Oxidative stress and diabetic complications. Circ Res, 107(9): 1058–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleizes P E, Munger J S, Nunes I, Harpel J G, Mazzieri R, Noguera I, Rifkin D B (1997). TGF-beta latency: biological significance and mechanisms of activation. Stem Cells, 15(3): 190–197

    Article  CAS  PubMed  Google Scholar 

  • Gurley S B, Coffman T M (2007). The renin-angiotensin system and diabetic nephropathy. Semin Nephrol, 27(2): 144–152

    Article  CAS  PubMed  Google Scholar 

  • Hadsell D L, Bonnette S, George J, Torres D, Klimentidis Y, Gao S, Haney P M, Summy-Long J, Soloff M S, Parlow A F, Sirito M, Sawadogo M (2003). Diminished milk synthesis in upstream stimulatory factor 2 null mice is associated with decreased circulating oxytocin and decreased mammary gland expression of eukaryotic initiation factors 4E and 4G. Mol Endocrinol, 17(11): 2251–2267

    Article  CAS  PubMed  Google Scholar 

  • Hong S W, Isono M, Chen S, Iglesias-De La Cruz M C, Han D C, Ziyadeh F N (2001). Increased glomerular and tubular expression of transforming growth factor-beta1, its type II receptor, and activation of the Smad signaling pathway in the db/db mouse. Am J Pathol, 158 (5): 1653–1663

    Article  CAS  PubMed  Google Scholar 

  • Hsieh T J, Fustier P, Zhang S L, Filep J G, Tang S S, Ingelfinger J R, Fantus I G, Hamet P, Chan J S (2003). High glucose stimulates angiotensinogen gene expression and cell hypertrophy via activation of the hexosamine biosynthesis pathway in rat kidney proximal tubular cells. Endocrinology, 144(10): 4338–4349

    Article  CAS  PubMed  Google Scholar 

  • Ichihara A, Suzuki F, Nakagawa T, Kaneshiro Y, Takemitsu T, Sakoda M, Nabi 6A H, Nishiyama A, Sugaya T, Hayashi M, Inagami T (2006). Prorenin receptor blockade inhibits development of glomerulosclerosis in diabetic angiotensin II type 1a receptor-deficient mice. J Am Soc Nephrol, 17(7): 1950–1961

    Article  CAS  PubMed  Google Scholar 

  • Ishimura E, Sterzel R B, Morii H, Kashgarian M (1992). Extracellular matrix protein: gene expression and synthesis in cultured rat mesangial cells. Nihon Jinzo Gakkai Shi, 34(1): 9–17

    CAS  PubMed  Google Scholar 

  • Isono M, Chen S, Hong S W, Iglesias-de la Cruz M C, Ziyadeh F N (2002). Smad pathway is activated in the diabetic mouse kidney and Smad3 mediates TGF-beta-induced fibronectin in mesangial cells. Biochem Biophys Res Commun, 296(5): 1356–1365

    Article  CAS  PubMed  Google Scholar 

  • Kagami S, Border W A, Miller D E, Noble N A (1994). Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest, 93(6): 2431–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanwar Y S, Wada J, Sun L, Xie P, Wallner E I, Chen S, Chugh S, Danesh F R (2008). Diabetic nephropathy: mechanisms of renal disease progression. Exp Biol Med (Maywood), 233(1): 4–11

    Article  CAS  Google Scholar 

  • Kelly D J, Zhang Y, Moe G, Naik G, Gilbert R E (2007). Aliskiren, a novel renin inhibitor, is renoprotective in a model of advanced diabetic nephropathy in rats. Diabetologia, 50(11): 2398–2404

    Article  CAS  PubMed  Google Scholar 

  • Kingsley-Kallesen M, Luster T A, Rizzino A (2001). Transcriptional regulation of the transforming growth factor-beta 2 gene in glioblastoma cells. In Vitro Cell Dev Biol Anim, 37(10): 684–690

    Article  CAS  PubMed  Google Scholar 

  • Kobori H, Nangaku M, Navar L G, Nishiyama A (2007). The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev, 59(3): 251–287

    Article  CAS  PubMed  Google Scholar 

  • Lawrence D A (1996). Transforming growth factor-beta: a general review. Eur Cytokine Netw, 7(3): 363–374

    CAS  PubMed  Google Scholar 

  • Leehey D J, Singh A K, Alavi N, Singh R (2000). Role of angiotensin II in diabetic nephropathy. Kidney Int Suppl, 77(8): S93–S98

    Google Scholar 

  • Leehey D J, Singh A K, Bast J P, Sethupathi P, Singh R (2008). Glomerular renin angiotensin system in streptozotocin diabetic and Zucker diabetic fatty rats. Transl Res, 151(4): 208–216

    Article  CAS  PubMed  Google Scholar 

  • Lewis E J (2002). The role of angiotensin II receptor blockers in preventing the progression of renal disease in patients with type 2 diabetes. Am J Hypertens, 15(10 Pt 2): 123S–128S

  • Lewis E J, Hunsicker L G, Clarke W R, Berl T, Pohl M A, Lewis J B, Ritz E, Atkins R C, Rohde R, Raz I, and the Collaborative Study Group (2001). Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med, 345(12): 851–860

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang S (2010). Glycated albumin upregulates upstream stimulatory factor 2 gene transcription in mesangial cells. Am J Physiol Renal Physiol, 299(1): F121–F127

    Google Scholar 

  • Lim A Kh (2014). Diabetic nephropathy-complications and treatment. Int J Nephrol Renovasc Dis, 7: 361–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, Brezniceanu M L, Wei C C, Chénier I, Sachetelli S, Zhang S L, Filep J G, Ingelfinger J R, Chan J S (2008). Overexpression of angiotensinogen increases tubular apoptosis in diabetes. J Am Soc Nephrol, 19(2): 269–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Shi L, Wang S (2007). Overexpression of upstream stimulatory factor 2 accelerates diabetic kidney injury. Am J Physiol Renal Physiol, 293(5): F1727–F1735

    Google Scholar 

  • Lyons R M, Gentry L E, Purchio A F, Moses H L (1990). Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J Cell Biol, 110(4): 1361–1367

    Article  CAS  PubMed  Google Scholar 

  • Márquez E, Riera M, Pascual J, Soler M J (2015). Renin-angiotensin system within the diabetic podocyte. Am J Physiol Renal Physiol, 308(1): F1–F10

    Google Scholar 

  • Miyata N, Park F, Li X F, Cowley A W Jr (1999). Distribution of angiotensin AT1 and AT2 receptor subtypes in the rat kidney. Am J Physiol, 277(3 Pt 2): F437–F446

  • Navar L G, Harrison-Bernard L M, Nishiyama A, Kobori H (2002). Regulation of intrarenal angiotensin II in hypertension. Hypertension, 39(2 Pt 2): 316–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navar L G, Inscho E W, Majid S A, Imig J D, Harrison-Bernard L M, Mitchell K D (1996). Paracrine regulation of the renal microcirculation. Physiol Rev, 76(2): 425–536

    CAS  PubMed  Google Scholar 

  • Navarro-González J F, Mora-Fernández C (2008). The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol, 19(3): 433–442

    Article  PubMed  Google Scholar 

  • Nguyen G, Bouzhir L, Delarue F, Rondeau E, Sraer J D (1998). Evidence of a renin receptor on human mesangial cells: effects on PAI1 and cGMP. Nephrologie, 19(7): 411–416

    CAS  PubMed  Google Scholar 

  • Nguyen G, Delarue F, Berrou J, Rondeau E, Sraer J D (1996). Specific receptor binding of renin on human mesangial cells in culture increases plasminogen activator inhibitor-1 antigen. Kidney Int, 50 (6): 1897–1903

    Article  CAS  PubMed  Google Scholar 

  • Nicolas G, Bennoun M, Devaux I, Beaumont C, Grandchamp B, Kahn A, Vaulont S (2001). Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci USA, 98(15): 8780–8785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niranjan T, Bielesz B, Gruenwald A, Ponda M P, Kopp J B, Thomas D B, Susztak K (2008). The Notch pathway in podocytes plays a role in the development of glomerular disease. Nat Med, 14(3): 290–298

    Article  CAS  PubMed  Google Scholar 

  • Oh J H, Ha H, Yu M R, Lee H B (1998). Sequential effects of high glucose on mesangial cell transforming growth factor-beta 1 and fibronectin synthesis. Kidney Int, 54(6): 1872–1878

    Article  CAS  PubMed  Google Scholar 

  • Pan L, Black T A, Shi Q, Jones C A, Petrovic N, Loudon J, Kane C, Sigmund C D, Gross K W (2001). Critical roles of a cyclic AMP responsive element and an E-box in regulation of mouse renin gene expression. J Biol Chem, 276(49): 45530–45538

    Article  CAS  PubMed  Google Scholar 

  • Park J T, Kato M, Lanting L, Castro N, Nam B Y, Wang M, Kang S W, Natarajan R (2014). Repression of let-7 by transforming growth factor-β1-induced Lin28 upregulates collagen expression in glomerular mesangial cells under diabetic conditions. Am J Physiol Renal Physiol, 307(12): F1390–F1403

    Google Scholar 

  • Parving H H, Persson F, Lewis J B, Lewis E J, Hollenberg N K, the AVOID Study Investigators (2008). Aliskiren combined with losartan in type 2 diabetes and nephropathy. N Engl J Med, 358(23): 2433–2446

    Article  CAS  PubMed  Google Scholar 

  • Peach M J (1977). Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev, 57(2): 313–370

    CAS  PubMed  Google Scholar 

  • Petrica L, Vlad A, Gluhovschi G, Gadalean F, Dumitrascu V, Vlad D, Popescu R, Velciov S, Gluhovschi C, Bob F, Ursoniu S, Petrica M, Jianu D C (2015). Glycated peptides are associated with the variability of endothelial dysfunction in the cerebral vessels and the kidney in type 2 diabetes mellitus patients: a cross-sectional study. J Diabetes Complications, 29(2): 230–237

    Article  PubMed  Google Scholar 

  • Phillips A (2007). The role of proximal tubular cells in interstitial fibrosis: understanding TGF-beta1. Chang Gung Med J, 30(1): 2–6

    PubMed  Google Scholar 

  • Phillips A, Janssen U, Floege J (1999). Progression of diabetic nephropathy. Insights from cell culture studies and animal models. Kidney Blood Press Res, 22(1–2): 81–97

    Article  CAS  PubMed  Google Scholar 

  • Price D A, Porter L E, Gordon M, Fisher N D, De’Oliveira J M, Laffel L M, Passan D R, Williams G H, Hollenberg N K (1999). The paradox of the low-renin state in diabetic nephropathy. J Am Soc Nephrol, 10 (11): 2382–2391

    CAS  PubMed  Google Scholar 

  • Qian J, Kaytor E N, Towle H C, Olson L K (1999). Upstream stimulatory factor regulates Pdx-1 gene expression in differentiated pancreatic beta-cells. Biochem J, 341 (Pt 2): 315–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qyang Y, Luo X, Lu, Ismail P M, Krylov D, Vinson C, Sawadogo M (1999). Cell-type-dependent activity of the ubiquitous transcription factor USF in cellular proliferation and transcriptional activation. Mol Cell Biol, 19(2): 1508–1517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Re R (2007). Intracellular renin-angiotensin system: the tip of the intracrine physiology iceberg. Am J Physiol Heart Circ Physiol, 293 (2): H905–H906

    Google Scholar 

  • Riccio A, Pedone P V, Lund L R, Olesen T, Olsen H S, Andreasen P A (1992). Transforming growth factor beta 1-responsive element: closely associated binding sites for USF and CCAAT-binding transcription factor-nuclear factor I in the type 1 plasminogen activator inhibitor gene. Mol Cell Biol, 12(4): 1846–1855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rifkin D B, Kojima S, Abe M, Harpel J G (1993). TGF-beta: structure, function, and formation. Thromb Haemost, 70(1): 177–179

    CAS  PubMed  Google Scholar 

  • Rippe R A, Umezawa A, Kimball J P, Breindl M, Brenner D A (1997). Binding of upstream stimulatory factor to an E-box in the 3'-flanking region stimulates alpha1(I) collagen gene transcription. J Biol Chem, 272(3): 1753–1760

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Orteg M, Lorenzo O, Egido J (1998). Angiotensin III up-regulates genes involved in kidney damage in mesangial cells and renal interstitial fibroblasts. Kidney Int Suppl, 68(5): S41–S45

    Google Scholar 

  • Sawadogo M, Roeder R G (1985). Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell, 43(1): 165–175

    Article  CAS  PubMed  Google Scholar 

  • Schultz-Cherry S, Lawler J, Murphy-Ullrich J E (1994). The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J Biol Chem, 269(43): 26783–26788

    CAS  PubMed  Google Scholar 

  • Schultz-Cherry S, Murphy-Ullrich J E (1993). Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J Cell Biol, 122(4): 923–932

    Article  CAS  PubMed  Google Scholar 

  • Shankland S J, Scholey J W, Ly H, Thai K (1994). Expression of transforming growth factor-beta 1 during diabetic renal hypertrophy. Kidney Int, 46(2): 430–442

    Article  CAS  PubMed  Google Scholar 

  • Sharma K, Eltayeb B O, McGowan T A, Dunn S R, Alzahabi B, Rohde R, Ziyadeh F N, Lewis E J (1999). Captopril-induced reduction of serum levels of transforming growth factor-beta1 correlates with long-term renoprotection in insulin-dependent diabetic patients. Am J Kidney Dis, 34(5): 818–823

    Article  CAS  PubMed  Google Scholar 

  • Sharma K, Jin Y, Guo J, Ziyadeh F N (1996). Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes, 45(4): 522–530

    Article  CAS  PubMed  Google Scholar 

  • Sharma K, Ziyadeh F N (1994). Renal hypertrophy is associated with upregulation of TGF-beta 1 gene expression in diabetic BB rat and NOD mouse. Am J Physiol, 267(6 Pt 2): F1094–F01

  • Sharma K, Ziyadeh F N, Alzahabi B, McGowan T A, Kapoor S, Kurnik B R, Kurnik P B, Weisberg L S (1997). Increased renal production of transforming growth factor-beta1 in patients with type II diabetes. Diabetes, 46(5): 854–859

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Nikolic D, Liu S, Lu H,Wang S (2009). Activation of renal reninangiotensin system in upstream stimulatory factor 2 transgenic mice. Am J Physiol Renal Physiol, 296(2): F257–F265

    Google Scholar 

  • Singh R, Alavi N, Singh A K, Leehey D J (1999). Role of angiotensin II in glucose-induced inhibition of mesangial matrix degradation. Diabetes, 48(10): 2066–2073

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Singh A K, Leehey D J (2005). A novel mechanism for angiotensin II formation in streptozotocin-diabetic rat glomeruli. Am J Physiol Renal Physiol, 288(6): F1183–F1190

    Google Scholar 

  • Sirito M, Lin Q, Deng J M, Behringer R R, Sawadogo M (1998). Overlapping roles and asymmetrical cross-regulation of the USF proteins in mice. Proc Natl Acad Sci USA, 95(7): 3758–3763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirito M, Lin Q, Maity T, Sawadogo M (1994). Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res, 22(3): 427–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skyler J S (1996). Diabetic complications. The importance of glucose control. Endocrinol Metab Clin North Am, 25(2): 243–254

    Article  CAS  Google Scholar 

  • Sonneveld R, vander Vlag J, Baltissen M P, Verkaart S A, Wetzels J F, Berden J H, Hoenderop J G, Nijenhuis T (2014). Glucose specifically regulates TRPC6 expression in the podocyte in an AngII-dependent manner. Am J Pathol, 184(6): 1715–1726

    Article  CAS  PubMed  Google Scholar 

  • Taipale J, Lohi J, Saarinen J, Kovanen P T, Keski-Oja J (1995). Human mast cell chymase and leukocyte elastase release latent transforming growth factor-beta 1 from the extracellular matrix of cultured human epithelial and endothelial cells. J Biol Chem, 270(9): 4689–4696

    Article  CAS  PubMed  Google Scholar 

  • Tamura J, Konno A, Hashimoto Y, Kon Y (2005). Upregulation of renal renin-angiotensin system in mouse diabetic nephropathy. Jpn J Vet Res, 53(1–2): 13–26

    PubMed  Google Scholar 

  • Vallet V S, Henrion A A, Bucchini D, Casado M, Raymondjean M, Kahn A, Vaulont S (1997). Glucose-dependent liver gene expression in upstream stimulatory factor 2–/–mice. J Biol Chem, 272(35): 21944–21949

    Article  CAS  PubMed  Google Scholar 

  • Vasanthakumar R, Mohan V, Anand G, Deepa M, Babu S, Aravindhan V (2015). Serum IL-9, IL-17, and TGF-β levels in subjects with diabetic kidney disease (CURES-134). Cytokine, 72(1): 109–112

    Article  CAS  PubMed  Google Scholar 

  • Velez J C, Bland A M, Arthur J M, Raymond J R, Janech M G (2007). Characterization of renin-angiotensin system enzyme activities in cultured mouse podocytes. Am J Physiol Renal Physiol, 293(1): F398–F407

    Google Scholar 

  • Vidotti D B, Casarini D E, Cristovam P C, Leite C A, Schor N, Boim M A (2004). High glucose concentration stimulates intracellular renin activity and angiotensin II generation in rat mesangial cells. Am J Physiol Renal Physiol, 286(6): F1039–F1045

    Google Scholar 

  • Visavadiya N P, Li Y, Wang S (2011). High glucose upregulates upstream stimulatory factor 2 in human renal proximal tubular cells through angiotensin II-dependent activation of CREB. Nephron, Exp Nephrol, 117(3): e62–e70

    Google Scholar 

  • Wang S, Skorczewski J, Feng X, Mei L, Murphy-Ullrich J E (2004). Glucose up-regulates thrombospondin 1 gene transcription and transforming growth factor-beta activity through antagonism of cGMP-dependent protein kinase repression via upstream stimulatory factor 2. J Biol Chem, 279(33): 34311–34322

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Qiu L, Howard A, Solis N, Li C, Wang X, Kopp J B, Levi M (2014). Protective effects of aliskiren and valsartan in mice with diabetic nephropathy. J Renin Angiotensin Aldosterone Syst, 15(4): 384–395

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ni J, Shao D, Liu J, Shen Y, Zhou L, Huang Y, Yu C, Wang J, Xue H, Lu L (2013). Elevated transcriptional co-activator p102 mediates angiotensin II type 1 receptor up-regulation and extracellular matrix overproduction in the high glucose-treated rat glomerular mesangial cells and isolated glomeruli. Eur J Pharmacol, 702(1–3): 208–217

    Article  CAS  PubMed  Google Scholar 

  • Weigert C, Brodbeck K, Sawadogo M, Haring H U, Schleicher E D (2004). USF proteins induce human TGF-beta1 gene activation via the glucose response element–1013/–1002 in mesangial cellsupregulation of USF activity by the hexosamine biosynthetic pathway. J Biol Chem, 2: 2

    Google Scholar 

  • White K E (2006). Research into the glomerular podocyte—is it relevant to diabetic nephropathy? Diabet Med, 23(7): 715–719

    Article  CAS  PubMed  Google Scholar 

  • Wong DW, Oudit G Y, Reich H, Kassiri Z, Zhou J, Liu Q C, Backx P H, Penninger J M, Herzenberg A M, Scholey J W (2007). Loss of angiotensin-converting enzyme-2 (Ace2) accelerates diabetic kidney injury. Am J Pathol, 171(2): 438–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamout H, Lazich I, Bakris G L (2014). Blood pressure, hypertension, RAAS blockade, and drug therapy in diabetic kidney disease. Adv Chronic Kidney Dis, 21(3): 281–286

    Article  PubMed  Google Scholar 

  • Yoo T H, Li J J, Kim J J, Jung D S, Kwak S J, Ryu D R, Choi H Y, Kim J S, Kim H J, Han S H, Lee J E, Han D S, Kang SW (2007). Activation of the renin-angiotensin system within podocytes in diabetes. Kidney Int, 71(10): 1019–1027

    Article  CAS  PubMed  Google Scholar 

  • Young B A, Johnson R J, Alpers C E, Eng E, Gordon K, Floege J, Couser W G, Seidel K (1995). Cellular events in the evolution of experimental diabetic nephropathy. Kidney Int, 47(3): 935–944

    Article  CAS  PubMed  Google Scholar 

  • Zhang S L, To C, Chen X, Filep J G, Tang S S, Ingelfinger J R, Chan J S (2002). Essential role(s) of the intrarenal renin-angiotensin system in transforming growth factor-beta1 gene expression and induction of hypertrophy of rat kidney proximal tubular cells in high glucose. J Am Soc Nephrol, 13(2): 302–312

    CAS  PubMed  Google Scholar 

  • Zhang Z, Shahinfar S, Keane W F, Ramjit D, Dickson T Z, Gleim G W, Mogensen C E, de Zeeuw D, Brenner B M, Snapinn S M (2005). Importance of baseline distribution of proteinuria in renal outcomes trials: lessons from the reduction of endpoints in NIDDM with the angiotensin II antagonist losartan (RENAAL) study. J Am Soc Nephrol, 16(6): 1775–1780

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Casado M, Vaulont S, Sharma K (2005). Role of upstream stimulatory factors in regulation of renal transforming growth factorbeta1. Diabetes, 54(7): 1976–1984

    Article  CAS  PubMed  Google Scholar 

  • Ziyadeh F N (2004). Mediators of diabetic renal disease: the case for tgf- Beta as the major mediator. J Am Soc Nephrol, 15 (Suppl 1), S55–57

  • Ziyadeh F N, Sharma K, Ericksen M, Wolf G (1994). Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-beta. J Clin Invest, 93(2): 536–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology and Nutritional Sciences, University of Kentucky, Lexington, KY, 40536, USA

    Shuxia Wang

Authors
  1. Shuxia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuxia Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, S. Role of upstream stimulatory factor 2 in diabetic nephropathy. Front. Biol. 10, 221–229 (2015). https://doi.org/10.1007/s11515-015-1359-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-015-1359-x

Keywords

Search

Navigation