Heterogeneous nuclear ribonucleoprotein F suppresses angiotensinogen gene expression and attenuates hypertension and kidney injury in diabetic mice

Diabetes

Volumn 61, Issue 10, 2012, Pages 2597-2608

  Lo, Chao Sheng ^a   Chang, Shiao Ying ^a   Chenier, Isabelle ^a   Filep, Janos G ^b   Ingelfinger, Julie R ^c   Zhang, Shao Ling ^a   Chan, John S D ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN; ANGIOTENSIN II; ANGIOTENSINOGEN; COMPLEMENTARY DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN F; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE MODEL; GENE EXPRESSION; HYPERTENSION; IN VITRO STUDY; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANGIOTENSINOGEN; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; FIBROSIS; GENE EXPRESSION; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP F-H; HYPERTENSION; KIDNEY; KIDNEY DISEASES; MICE; MICE, TRANSGENIC; RENIN-ANGIOTENSIN SYSTEM; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84866596488     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-1349     Document Type: Article

References (43)

1. Dzau VJ, Ingelfinger JR. Molecular biology and pathophysiology of the intrarenal renin-angiotensin system. J Hypertens Suppl 1989;7:S3-S8 (Pubitemid 20087623)
2. Zhang SL, Filep JG, Hohman TC, Tang SS, Ingelfinger JR, Chan JS. Molecular mechanisms of glucose action on angiotensinogen gene expression in rat proximal tubular cells. Kidney Int 1999;55:454-464 (Pubitemid 29082872)
3. Zhang SL, Tang SS, Chen X, Filep JG, Ingelfinger JR, Chan JS. High levels of glucose stimulate angiotensinogen gene expression via the P38 mitogenactivated protein kinase pathway in rat kidney proximal tubular cells. Endocrinology 2000;141:4637-4646 (Pubitemid 32055143)
4. Hsieh TJ, Zhang SL, Filep JG, Tang SS, Ingelfinger JR, Chan JS. High glucose stimulates angiotensinogen gene expression via reactive oxygen species generation in rat kidney proximal tubular cells. Endocrinology 2002;143:2975-2985 (Pubitemid 34809870)
5. Hsieh TJ, Fustier P, Zhang SL, et al. High glucose stimulates angiotensinogen gene expression and cell hypertrophy via activation of the hexosamine biosynthesis pathway in rat kidney proximal tubular cells. Endocrinology 2003;144:4338-4349 (Pubitemid 37204833)
6. Zhang SL, To C, Chen X, et al. Essential role(s) of the intrarenal reninangiotensin 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 2002;13:302-312 (Pubitemid 34106271)
7. Zhang SL, To C, Chen X, et al. Effect of renin-angiotensin system blockade on the expression of the angiotensinogen gene and induction of hypertrophy in rat kidney proximal tubular cells. Exp Nephrol 2001;9:109-117 (Pubitemid 32041488)
8. Sachetelli S, Liu Q, Zhang SL, et al. RAS blockade decreases blood pressure and proteinuria in transgenic mice overexpressing rat angiotensinogen gene in the kidney. Kidney Int 2006;69:1016-1023 (Pubitemid 43372176)
9. Liu F, Brezniceanu ML, Wei CC, et al. Overexpression of angiotensinogen increases tubular apoptosis in diabetes. J Am Soc Nephrol 2008;19:269-280 (Pubitemid 351240649)
10. Zhang SL, Chen X, Filep JG, Tang SS, Ingelfinger JR, Chan JS. Insulin inhibits angiotensinogen gene expression via the mitogen-activated protein kinase pathway in rat kidney proximal tubular cells. Endocrinology 1999;140:5285-5292
11. Zhang SL, Chen X, Wei CC, et al. Insulin inhibits dexamethasone effect on angiotensinogen gene expression and induction of hypertrophy in rat kidney proximal tubular cells in high glucose. Endocrinology 2002;143:4627-4635 (Pubitemid 35397604)
12. Chen X, Zhang SL, Pang L, et al. Characterization of a putative insulinresponsive element and its binding protein(s) in rat angiotensinogen gene promoter: regulation by glucose and insulin. Endocrinology 2001;142:2577-2585 (Pubitemid 32473113)
13. Wei CC, Guo DF, Zhang SL, Ingelfinger JR, Chan JS. Heterogenous nuclear ribonucleoprotein F modulates angiotensinogen gene expression in rat kidney proximal tubular cells. J Am Soc Nephrol 2005;16:616-628 (Pubitemid 41725098)
14. Wei CC, Zhang SL, Chen YW, et al. Heterogeneous nuclear ribonucleoprotein K modulates angiotensinogen gene expression in kidney cells. J Biol Chem 2006;281:25344-25355
15. Wang L, Lei C, Zhang SL, et al. Synergistic effect of dexamethasone and isoproterenol on the expression of angiotensinogen in immortalized rat proximal tubular cells. Kidney Int 1998;53:287-295 (Pubitemid 28097845)
16. Ding Y, Davisson RL, Hardy DO, et al. The kidney androgen-regulated protein promoter confers renal proximal tubule cell-specific and highly androgen-responsive expression on the human angiotensinogen gene in transgenic mice. J Biol Chem 1997;272:28142-28148 (Pubitemid 27473625)
17. Brezniceanu ML, Liu F, Wei CC, et al. Catalase overexpression attenuates angiotensinogen expression and apoptosis in diabetic mice. Kidney Int 2007;71:912-923 (Pubitemid 46663797)
18. Brezniceanu ML, Liu F, Wei CC, et al. Attenuation of interstitial fibrosis and tubular apoptosis in db/db transgenic mice overexpressing catalase in renal proximal tubular cells. Diabetes 2008;57:451-459
19. Liu F, Wei CC, Wu SJ, et al. Apocynin attenuates tubular apoptosis and tubulointerstitial fibrosis in transgenic mice independent of hypertension. Kidney Int 2009;75:156-166
20. Godin N, Liu F, Lau GJ, et al. Catalase overexpression prevents hypertension and tubular apoptosis in angiotensinogen transgenic mice. Kidney Int 2010;77:1086-1097
21. Ingelfinger JR, Jung F, Diamant D, et al. Rat proximal tubule cell line transformed with origin-defective SV40 DNA: autocrine ANG II feedback. Am J Physiol 1999;276:F218-F227 (Pubitemid 29102286)
22. Dreyfuss G, Matunis MJ, Piñol-Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 1993;62:289-321 (Pubitemid 23237873)
23. Han SP, Tang YH, Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem J 2010;430:379-392
24. Min H, Chan RC, Black DL. The generally expressed hnRNP F is involved in a neural-specific pre-mRNA splicing event. Genes Dev 1995;9:2659-2671
25. Chen CD, Kobayashi R, Helfman DM. Binding of hnRNP H to an exonic splicing silencer is involved in the regulation of alternative splicing of the rat beta-tropomyosin gene. Genes Dev 1999;13:593-606 (Pubitemid 29131883)
26. Hastings ML, Wilson CM, Munroe SH. A purine-rich intronic element enhances alternative splicing of thyroid hormone receptor mRNA. RNA 2001;7:859-874 (Pubitemid 32552873)
27. Garneau D, Revil T, Fisette JF, Chabot B. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 2005;280:22641-22650 (Pubitemid 40853168)
28. Dominguez C, Fisette JF, Chabot B, Allain FH. Structural basis of G-tract recognition and encaging by hnRNP F quasi-RRMs. Nat Struct Mol Biol 2010;17:853-861
29. Decorsière A, Cayrel A, Vagner S, Millevoi S. Essential role for the interaction between hnRNP H/F and a G quadruplex in maintaining p53 premRNA 39-end processing and function during DNA damage. Genes Dev 2011;25:220-225
30. Veraldi KL, Arhin GK, Martincic K, Chung-Ganster LH, Wilusz J, Milcarek C. hnRNP F influences binding of a 64-kilodalton subunit of cleavage stimulation factor to mRNA precursors in mouse B cells. Mol Cell Biol 2001;21:1228-1238 (Pubitemid 32114971)
31. Yoshida T, Makino Y, Tamura T. Association of the rat heterogeneous nuclear RNA-ribonucleoprotein F with TATA-binding protein. FEBS Lett 1999;457:251-254 (Pubitemid 29401938)
32. Gamberi C, Izaurralde E, Beisel C, Mattaj IW. Interaction between the human nuclear cap-binding protein complex and hnRNP F. Mol Cell Biol 1997;17:2587-2597 (Pubitemid 27175140)
33. Chen Y, Schnetz MP, Irarrazabal CE, et al. Proteomic identification of proteins associated with the osmoregulatory transcription factor TonEBP/OREBP: functional effects of Hsp90 and PARP-1. Am J Physiol Renal Physiol 2007;292:F981-F992 (Pubitemid 46393424)
34. Yoshioka M, Kayo T, Ikeda T, Koizumi A. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes 1997;46:887-894 (Pubitemid 27188269)
35. Haseyama T, Fujita T, Hirasawa F, et al. Complications of IgA nephropathy in a non-insulin-dependent diabetes model, the Akita mouse. Tohoku J Exp Med 2002;198:233-244 (Pubitemid 36305128)
36. Sanchez AP, Zhao J, You Y, Declèves AE, Diamond-Stanic M, Sharma K. Role of the USF1 transcription factor in diabetic kidney disease. Am J Physiol Renal Physiol 2011;301:F271-F279
37. Pohl M, Kaminski H, Castrop H, et al. Intrarenal renin angiotensin system revisited: role of megalin-dependent endocytosis along the proximal nephron. J Biol Chem 2010;285:41935-41946
38. Susztak K, Raff AC, Schiffer M, Böttinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006;55:225-233 (Pubitemid 43343319)
39. Border WA, Okuda S, Languino LR, Sporn MB, Ruoslahti E. Suppression of experimental glomerulonephritis by antiserum against transforming growth factor beta 1. Nature 1990;346:371-374
40. Yamamoto T, Nakamura T, Noble NA, Ruoslahti E, Border WA. Expression of transforming growth factor beta is elevated in human and experimental diabetic nephropathy. Proc Natl Acad Sci U S A 1993;90:1814-1818 (Pubitemid 23069947)
41. Qian JF, Wang TT, Wu XH, et al. Angiotensinogen gene expression is stimulated by the cAMP-responsive element binding protein in opossum kidney cells. J Am Soc Nephrol 1997;8:1072-1079
42. Awazu M, Omori S, Ishikura K, Hida M, Fujita H. The lack of cyclin kinase inhibitor p27(Kip1) ameliorates progression of diabetic nephropathy. J Am Soc Nephrol 2003;14:699-708 (Pubitemid 36246014)
43. Wolf G, Schanze A, Stahl RA, Shankland SJ, Amann K. p27(Kip1) Knockout mice are protected from diabetic nephropathy: evidence for p27(Kip1) haplotype insufficiency. Kidney Int 2005;68:1583-1589 (Pubitemid 43169903)