Endothelial cell transforming growth factor-β receptor activation causes tacrolimus-induced renal arteriolar hyalinosis

Kidney International

Volumn 82, Issue 8, 2012, Pages 857-866

  Chiasson, Valorie L ^a   Jones, Kathleen A ^b   Kopriva, Shelley E ^a   Mahajan, Ashutosh ^a   Young, Kristina J ^a   Mitchell, Brett M ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; COLLAGEN; FIBRONECTIN; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 12; RECEPTOR BLOCKING AGENT; SB 505124; SMAD2 PROTEIN; SMAD3 PROTEIN; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; CAUSAL ATTRIBUTION; CELL SPECIFICITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; ENDOTHELIUM CELL; HYALINE DEGENERATION; LIGAND BINDING; LOW DRUG DOSE; MALE; MOLECULAR PATHOLOGY; MOUSE; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RENAL ARTERIOLAR HYALINOSIS; RENOVASCULAR DISEASE; VASCULAR RING;

EID: 84867030114     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.104     Document Type: Article

References (40)

1. Falkenhain ME, Cosio FG, Sedmak DD. Progressive histologic injury in kidneys from heart and liver transplant recipients receiving cyclosporine. Transplantation 1996; 62: 364-370.
2. Nankivell BJ, Borrows RJ, Fung CLS et al. Calcineurin inhibitor toxicity: longitudinal assessment by protocol histology. Transplantation 2004; 78: 557-565.
3. Nankivell BJ, Borrows RJ, Fung CLS et al. The natural history of chronic allograft nephropathy. N Engl J Med 2003; 349: 2326-2333.
4. Kambham N, Nagarajan S, Shah S et al. A novel, semiquantitative, clinically correlated calcineurin inhibitor toxicity score for renal allograft biopsies. Clin J Am Soc Nephrol 2007; 2: 135-142.
5. Takeda A, Uchida K, Haba T et al. Chronic cyclosporin nephropathy: longterm effects of cyclosporin on renal allografts. Clin Transplant 2001; 15: 22-29.
6. Andoh TF, Bennett WM. Chronic cyclosporine nephrotoxicity. Curr Opin Nephrol Hypertens 1996; 7: 265-270.
7. Shihab FS, Yi H, Bennett WM et al. Effect of nitric oxide modulation on TGF-beta1 and matrix proteins in chronic cyclosporine nephrotoxicity. Kidney Int 2000; 58: 1174-1185.
8. Islam M, Burke JF, McGowan TA et al. Effect of anti-transforming growth factor-b antibodies in cyclosporine-induced renal dysfunction. Kidney Int 2001; 59: 498-506.
9. Saurina A, Campistol JM, Lario S et al. Conversion from calcineurin inhibitors to sirolimus in kidney transplant patients reduces the urinary transforming growth factor-beta1 concentration. Transplant Proc 2007; 39: 2138-2141.
10. Yang F, Chung ACK, Huang XR et al. Angiotensin II induces connective tissue growth factor and collagen I expression via transforming growth factor-b-dependent and-indpendent Smad pathways. The role of Smad3. Hypertension 2009; 54: 877-884.
11. Bing P, Maode L, Li F et al. Comparison of expression of TGF-b1, its receptors TGFb1R-I and TGFb1R-II in rat kidneys during chronic nephropathy induced by cyclosporine and tacrolimus. Transplant Proc 2006; 38: 2180-2218.
12. Maluccio M, Sharma V, Lagman M et al. Tacrolimus enhances transforming growth factor-b1 expression and promotes tumor progression. Transplantation 2003; 76: 597-602.
13. Khanna A, Cairns V, Hosenpud JD. Tacrolimus induces increased expression of transforming growth factor-[beta]1 in mammalian lymphoid as well as nonlymphoid cells. Transplantation 1999; 67: 614-619.
14. Wang T, Li BY, Danielson PD et al. The immunophilin FKBP12 functions as a common inhibitor of the TGFb family type I receptors. Cell 1996; 86: 435-444.
15. Chen YG, Liu F, Massague J. Mechanism of TGFb receptor inhibition by FKBP12. EMBO J 1997; 16: 3866-3876.
16. Cook LG, Chiasson VL, Long C et al. Tacrolimus reduces nitric oxide synthase function by binding to FKBP rather than by its calcineurin effect. Kidney Int 2009; 75: 719-726.
17. Long C, Cook LG, Hamilton SL et al. FK506 binding protein 12/12.6 depletion increases endothelial nitric oxide synthase threonine 495 phosphorylation and blood pressure. Hypertension 2007; 49: 569-576.
18. Long C, Cook LG, Wu GY et al. Removal of FKBP12/12.6 from endothelial ryanodine receptors leads to an intracellular calcium leak and endothelial dysfunction. Arterioscler Thromb Vasc Biol 2007; 27: 1580-1586.
19. Akool ES, Doller A, Babelova A et al. Molecular mechanisms of TGFb receptor-triggered signaling cascades rapidly induced by the calcineurin inhibitors cyclosporine A and FK506. J Immunol 2008; 181: 2831-2845.
20. DaCosta Byfield S, Major C, Laping NJ et al. SB-505124 is a selective inhibitor of transforming growth factor-b type I receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2004; 65: 744-752.
21. Andoh TF, Lam TT, Lindsley J et al. Enhancement of chronic cyclosporine nephrotoxicity by sodium depletion in an experimental mouse model. Nephrology 1997; 3: 471-478.
22. Pichler RH, Franceschini N, Young BA et al. Pathogenesis of cyclosporine nephropathy: roles of angiotensin II and osteopontin. J Am Soc Nephrol 1995; 6: 1186-1196.
23. Hoorn EJ, Walsh SB, McCormick JA et al. The calcineurin inhibitor tacrolimus activates the renal sodium chloride cotransporter to cause hypertension. Nat Med 2011; 17: 1304-1309.
24. Araki K, Gangappa S, Dillehay DL et al. Pathogenic virus-specific T cells cause disease during treatment with the calcineurin inhibitor FK506: implications for transplantation. J Exp Med 2010; 207: 2355-2367.
25. Deniz H, Ogutmen B, Cakalagaoglu F et al. Inhibition of the renin angiotensin system decreases fibrogenic cytokine expression in tacrolimus nephrotoxicity in rats. Transplant Proc 2006; 38: 483-486.
26. Andersson J, Nagy S, Groth CG et al. Effects of FK 506 and cyclosporin A on cytokine production studied in vitro at a single-cell level. Immunology 1992; 75: 136-142.
27. Goto T, Kino T, Hatanaka H et al. FK 506: historical perspectives. Transplant Proc 1991; 23: 2713-2717.
28. Dumont FJ, Staruch MJ, Flattery A et al. Up-regulation of gene expression by FK 506. Transplant Proc 1991; 23: 2870-2872.
29. Khanna A. Tacrolimus and cyclosporine in vitro and in vivo induce osteopontin mRNA and protein expression in renal tissues. Nephron Exp Nephrol 2005; 101: e119-e126.
30. Mazzali M, Hughes J, Dantas M et al. Effects of cyclosporine in osteopontin null mice. Kidney Int 2002; 62: 78-85.
31. Kreis H, Oberbauer R, Campistol JM et al. Long-term benefits with sirolimus-based therapy after early cyclosporine withdrawal. J Am Soc Nephrol 2004; 15: 809-817.
32. Osman B, Doller A, Akool el-S et al. Rapamycin induces the TGFbeta1/Smad signaling cascade in renal mesangial cells upstream of mTOR. Cell Signal 2009; 21: 1806-1817.
33. Giordano A, Romano S, Mallardo M et al. FK506 can activate transforming growth factor-b signaling in vascular smooth muscle cells and promote proliferation. Cardiovasc Res 2008; 79: 519-526.
34. Gooch JL, Roberts BR, Cobbs SL et al. Loss of the a-isoform of calcineurin is sufficient to induce nephrotoxicity and altered expression of transforming growth factor-b. Transplantation 2007; 83: 439-447.
35. Lee LK, Meyer TW, Pollock AS et al. Endothelial cell injury initiates glomerular sclerosis in the rat remnant kidney. J Clin Invest 1995; 96: 953-964.
36. Mahalak SM, Lin WL, Essner E et al. Increased immunoreactivity of collagen types II I, and V, fibronectin and TGF-b in retinal vessels of rats with experimental autoimmune uveoretinitis. Curr Eye Res 1991; 10: 1059-1063.
37. Myers JC. Differential expression of type I collagen and cellular fibronectin isoforms in endothelial cell variants. Kidney Int 1993; 43: 45-52.
38. Sage H, Crouch E, Bornstein P. Collagen synthesis by bovine aortic endothelial cells in culture. Biochemistry 1979; 18: 5433-5442.
39. Jaffe EA, Mosher DF. Synthesis of fibronectin by cultured human endothelial cells. J Exp Med 1978; 147: 1779-1791.
40. Tang W, Ingalls CP, Durham WJ et al. Altered excitation-contraction coupling with skeletal muscle specific FKBP12 deficiency. FASEB J 2004; 18: 1597-1599.