The pathological significance of dipeptidyl peptidase-4 in endothelial cell homeostasis and kidney fibrosis

Diabetology International

Volumn 7, Issue 3, 2016, Pages 212-220

  Kanasaki, Keizo ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Extracellular matrix; Fibrosis; Integrin; microRNA; Peptidase

Indexed keywords

BETA1 INTEGRIN; DIPEPTIDYL PEPTIDASE IV; DIPEPTIDYL PEPTIDASE IV INHIBITOR; MICRORNA; TRANSFORMING GROWTH FACTOR BETA;

CELL TRANSFORMATION; DIABETIC NEPHROPATHY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; FIBROGENESIS; HOMEOSTASIS; HUMAN; KIDNEY FIBROSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

EID: 84983638433     PISSN: 21901678     EISSN: 21901686     Source Type: Journal    
DOI: 10.1007/s13340-016-0281-z     Document Type: Review

References (95)

1. Pinzani M. Welcome to fibrogenesis and tissue repair. Fibrogenesis Tissue Repair. 2008;1:1. doi:10.1186/1755-1536-1-1.
2. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008;214:199–210. doi:10.1002/path.2277.
3. Zeisberg M, Neilson EG. Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol. 2010;21:1819–34. doi:10.1681/ASN.2010080793.
4. Boor P, Ostendorf T, Floege J. Renal fibrosis: novel insights into mechanisms and therapeutic targets. Nat Rev Nephrol. 2010;6:643–56. doi:10.1038/nrneph.2010.120.
5. Eddy AA. Molecular basis of renal fibrosis. Pediatr Nephrol. 2000;15:290–301.
6. Schmierer B, Hill CS. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol. 2007;8:970–82. doi:10.1038/nrm2297.
7. Medici D, et al. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med. 2010;16:1400–6. doi:10.1038/nm.2252.
8. Medici D, Potenta S, Kalluri R. Transforming growth factor-beta2 promotes Snail-mediated endothelial–mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling. Biochem J. 2011;437:515–20. doi:10.1042/BJ20101500.
9. Lebrin F, Deckers M, Bertolino P, Ten Dijke P. TGF-beta receptor function in the endothelium. Cardiovasc Res. 2005;65:599–608. doi:10.1016/j.cardiores.2004.10.036.
10. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 1994;370:341–7. doi:10.1038/370341a0.
11. De Meester I, Korom S, Van Damme J, Scharpe S. CD26, let it cut or cut it down. Immunol Today. 1999;20:367–75.
12. Mulvihill EE, Drucker DJ. Pharmacology, physiology, and mechanisms of action of dipeptidyl peptidase-4 inhibitors. Endocr Rev. 2014;35:992–1019. doi:10.1210/er.2014-1035.
13. Chien CH, et al. One site mutation disrupts dimer formation in human DPP-IV proteins. J Biol Chem. 2004;279:52338–45. doi:10.1074/jbc.M406185200.
14. Lambeir AM, Durinx C, Scharpe S, De Meester I. Dipeptidyl-peptidase IV from bench to bedside: an update on structural properties, functions, and clinical aspects of the enzyme DPP IV. Crit Rev Clin Lab Sci. 2003;40:209–94. doi:10.1080/713609354.
15. Kameoka J, Tanaka T, Nojima Y, Schlossman SF, Morimoto C. Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science. 1993;261:466–9.
16. Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer. 2007;7:800–8. doi:10.1038/nrc2228.
17. Lu G, et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature. 2013;500:227–31. doi:10.1038/nature12328.
18. Kahne T, et al. Dipeptidyl peptidase IV: a cell surface peptidase involved in regulating T cell growth (review). Int J Mol Med. 1999;4:3–15.
19. Boerrigter G, Costello-Boerrigter LC, Harty GJ, Lapp H, Burnett JC Jr. Des-serine-proline brain natriuretic peptide 3-32 in cardiorenal regulation. Am J Physiol Regul Integr Comp Physiol. 2007;292:R897–901. doi:10.1152/ajpregu.00569.2006.
20. Brandt I, et al. Dipeptidyl-peptidase IV converts intact B-type natriuretic peptide into its des-SerPro form. Clin Chem. 2006;52:82–7. doi:10.1373/clinchem.2005.057638.
21. Mentlein R. Dipeptidyl-peptidase IV (CD26)—role in the inactivation of regulatory peptides. Regul Pept. 1999;85:9–24.
22. Marchetti C, et al. High mobility group box 1 is a novel substrate of dipeptidyl peptidase-IV. Diabetologia. 2012;55:236–44. doi:10.1007/s00125-011-2213-6.
23. Kirby M, Yu DM, O’Connor S, Gorrell MD. Inhibitor selectivity in the clinical application of dipeptidyl peptidase-4 inhibition. Clin Sci (Lond). 2010;118:31–41. doi:10.1042/CS20090047.
24. Gorrell MD, Gysbers V, McCaughan GW. CD26: a multifunctional integral membrane and secreted protein of activated lymphocytes. Scand J Immunol. 2001;54:249–64.
25. Broxmeyer HE, et al. Dipeptidylpeptidase 4 negatively regulates colony-stimulating factor activity and stress hematopoiesis. Nat Med. 2012;18:1786–96. doi:10.1038/nm.2991.
26. Ferreira L, et al. Effects of sitagliptin treatment on dysmetabolism, inflammation, and oxidative stress in an animal model of type 2 diabetes (ZDF rat). Mediat Inflamm. 2010;2010:592760. doi:10.1155/2010/592760.
27. Lu HY, et al. Dipeptidyl peptidase-4 inhibitor decreases abdominal aortic aneurysm formation through GLP-1-dependent monocytic activity in mice. PLoS One. 2015;10:e0121077. doi:10.1371/journal.pone.0121077.
28. Bose AK, Mocanu MM, Carr RD, Brand CL, Yellon DM. Glucagon-like peptide 1 can directly protect the heart against ischemia/reperfusion injury. Diabetes. 2005;54:146–51.
29. Shah Z, et al. Long-term dipeptidyl-peptidase 4 inhibition reduces atherosclerosis and inflammation via effects on monocyte recruitment and chemotaxis. Circulation. 2011;124:2338–49. doi:10.1161/CIRCULATIONAHA.111.041418.
30. Huang CY, et al. Dipeptidyl peptidase-4 inhibitor improves neovascularization by increasing circulating endothelial progenitor cells. Br J Pharmacol. 2012;167:1506–19. doi:10.1111/j.1476-5381.2012.02102.x.
31. Cernea S, Raz I. Therapy in the early stage: incretins. Diabetes Care. 2011;34(Suppl 2):S264–71. doi:10.2337/dc11-s223.
32. Bostick B, et al. Dipeptidyl peptidase inhibition prevents diastolic dysfunction and reduces myocardial fibrosis in a mouse model of Western diet induced obesity. Metabolism. 2014;63:1000–11. doi:10.1016/j.metabol.2014.04.002.
33. Hirakawa H, et al. A DPP-4 inhibitor suppresses fibrosis and inflammation on experimental autoimmune myocarditis in mice. PLoS One. 2015;10:e0119360. doi:10.1371/journal.pone.0119360.
34. Kaji K, et al. Dipeptidyl peptidase-4 inhibitor attenuates hepatic fibrosis via suppression of activated hepatic stellate cell in rats. J Gastroenterol. 2013;. doi:10.1007/s00535-013-0783-4.
35. Gao C, Huang W, Kanasaki K, Xu Y. The role of ubiquitination and sumoylation in diabetic nephropathy. Biomed Res Int. 2014;2014:160692. doi:10.1155/2014/160692.
36. Sun AL, et al. Dipeptidyl peptidase-IV is a potential molecular biomarker in diabetic kidney disease. Diabetes Vasc Dis Res. 2012;9:301–8. doi:10.1177/1479164111434318.
37. Stefanovic V, et al. Interferon-gamma induces dipeptidylpeptidase IV expression in human glomerular epithelial cells. Immunology. 1993;80:465–70.
38. Yang J, et al. Increase in DPP-IV in the intestine, liver and kidney of the rat treated with high fat diet and streptozotocin. Life Sci. 2007;81:272–9. doi:10.1016/j.lfs.2007.04.040.
39. Panchapakesan U, Mather A, Pollock C. Role of GLP-1 and DPP-4 in diabetic nephropathy and cardiovascular disease. Clin Sci (Lond). 2013;124:17–26. doi:10.1042/CS20120167.
40. Mitic B, Lazarevic G, Vlahovic P, Rajic M, Stefanovic V. Diagnostic value of the aminopeptidase N,N-acetyl-beta-d-glucosaminidase and dipeptidylpeptidase IV in evaluating tubular dysfunction in patients with glomerulopathies. Ren Fail. 2008;30:896–903. doi:10.1080/08860220802359048.
41. Mega C, et al. Diabetic nephropathy amelioration by a low-dose sitagliptin in an animal model of type 2 diabetes (Zucker diabetic fatty rat). Exp Diabetes Res. 2011;2011:162092. doi:10.1155/2011/162092.
42. Liu WJ, et al. Dipeptidyl peptidase IV inhibitor attenuates kidney injury in streptozotocin-induced diabetic rats. J Pharmacol Exp Ther. 2012;340:248–55. doi:10.1124/jpet.111.186866.
43. GangadharanKomala M, Gross S, Zaky A, Pollock C, Panchapakesan U. Saxagliptin reduces renal tubulointerstitial inflammation, hypertrophy and fibrosis in diabetes. Nephrology (Carlton). 2016;21:423–31. doi:10.1111/nep.12618.
44. Alter ML, et al. DPP-4 inhibition on top of angiotensin receptor blockade offers a new therapeutic approach for diabetic nephropathy. Kidney Blood Press Res. 2012;36:119–30. doi:10.1159/000341487.
45. Groop PH, et al. Linagliptin lowers albuminuria on top of recommended standard treatment in patients with type 2 diabetes and renal dysfunction. Diabetes Care. 2013;36:3460–8. doi:10.2337/dc13-0323.
46. Min HS, et al. Dipeptidyl peptidase IV inhibitor protects against renal interstitial fibrosis in a mouse model of ureteral obstruction. Lab Invest. 2014;94:598–607. doi:10.1038/labinvest.2014.50.
47. Eisenberg LM, Markwald RR. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res. 1995;77:1–6.
48. Piera-Velazquez S, Li Z, Jimenez SA. Role of endothelial–mesenchymal transition (EndoMT) in the pathogenesis of fibrotic disorders. Am J Pathol. 2011;179:1074–80. doi:10.1016/j.ajpath.2011.06.001.
49. Zeisberg EM, Potenta SE, Sugimoto H, Zeisberg M, Kalluri R. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol. 2008;19:2282–7.
50. Xavier S, et al. Curtailing endothelial TGF-beta signaling is sufficient to reduce endothelial–mesenchymal transition and fibrosis in CKD. J Am Soc Nephrol. 2015;26:817–29. doi:10.1681/ASN.2013101137.
51. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 2007;67:10123–8.
52. Zeisberg EM, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 2007;13:952–61.
53. Potenta S, Zeisberg E, Kalluri R. The role of endothelial-to-mesenchymal transition in cancer progression. Br J Cancer. 2008;99:1375–9.
54. Xu X, et al. Endocardial fibroelastosis is caused by aberrant endothelial to mesenchymal transition. Circ Res. 2015;116:857–66. doi:10.1161/CIRCRESAHA.116.305629.
55. Xu X, et al. Epigenetic balance of aberrant Rasal1 promoter methylation and hydroxymethylation regulates cardiac fibrosis. Cardiovasc Res. 2015;105:279–91. doi:10.1093/cvr/cvv015.
56. Xu X, et al. Snail is a direct target of hypoxia-inducible factor 1alpha (HIF1alpha) in hypoxia-induced endothelial to mesenchymal transition of human coronary endothelial cells. J Biol Chem. 2015;290:16653–64. doi:10.1074/jbc.M115.636944.
57. Charytan DM, et al. Increased concentration of circulating angiogenesis and nitric oxide inhibitors induces endothelial to mesenchymal transition and myocardial fibrosis in patients with chronic kidney disease. Int J Cardiol. 2014;176:99–109. doi:10.1016/j.ijcard.2014.06.062.
58. Zeisberg M, Zeisberg EM. Evidence for antifibrotic incretin-independent effects of the DPP-4 inhibitor linagliptin. Kidney Int. 2015;88:429–31. doi:10.1038/ki.2015.175.
59. Shi S, et al. Interactions of DPP-4 and integrin beta1 influences endothelial-to-mesenchymal transition. Kidney Int. 2015;88:479–89. doi:10.1038/ki.2015.103.
60. Pozzi A, Zent R. Extracellular matrix receptors in branched organs. Curr Opin Cell Biol. 2011;23:547–53. doi:10.1016/j.ceb.2011.04.003.
61. Pozzi A, Zent R. Integrins: sensors of extracellular matrix and modulators of cell function. Nephron Exp Nephrol. 2003;94:e77–84. doi:10.1159/000072025.
62. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110:673–87.
63. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. Ligand binding to integrins. J Biol Chem. 2000;275:21785–8. doi:10.1074/jbc.R000003200.
64. Park EJ, Yuki Y, Kiyono H, Shimaoka M. Structural basis of blocking integrin activation and deactivation for anti-inflammation. J Biomed Sci. 2015;22:51. doi:10.1186/s12929-015-0159-6.
65. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619–47. doi:10.1146/annurev.immunol.25.022106.141618.
66. Arnaout MA, Goodman SL, Xiong JP. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol. 2007;19:495–507. doi:10.1016/j.ceb.2007.08.002.
67. Zent R, et al. Glomerular injury is exacerbated in diabetic integrin alpha1-null mice. Kidney Int. 2006;70:460–70. doi:10.1038/sj.ki.5000359.
68. Chen X, et al. Integrin alpha1beta1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol Cell Biol. 2007;27:3313–26. doi:10.1128/MCB.01476-06.
69. Yeh YC, et al. Transforming growth factor-{beta}1 induces Smad3-dependent {beta}1 integrin gene expression in epithelial-to-mesenchymal transition during chronic tubulointerstitial fibrosis. Am J Pathol. 2010;177:1743–54. doi:10.2353/ajpath.2010.091183.
70. Hamzeh MT, Sridhara R, Alexander LD. Cyclic stretch-induced TGF-beta1 and fibronectin expression is mediated by beta1-integrin through c-Src- and STAT3-dependent pathways in renal epithelial cells. Am J Physiol Renal Physiol. 2015;308:F425–36. doi:10.1152/ajprenal.00589.2014.
71. Tang XH, Huang SM, Tan SQ, Ma YL. Effect of rosiglitazone on integrin beta1 expression and apoptosis of proximal tubular cell exposed to high glucose. Sichuan Da Xue Xue Bao Yi Xue Ban. 2007;38:291–4.
72. Glynne PA, Picot J, Evans TJ. Coexpressed nitric oxide synthase and apical beta(1) integrins influence tubule cell adhesion after cytokine-induced injury. J Am Soc Nephrol. 2001;12:2370–83.
73. Elias BC, et al. The integrin beta1 subunit regulates paracellular permeability of kidney proximal tubule cells. J Biol Chem. 2014;289:8532–44. doi:10.1074/jbc.M113.526509.
74. Lal H, et al. Integrins and proximal signaling mechanisms in cardiovascular disease. Front Biosci (Landmark Ed). 2009;14:2307–34.
75. Kanasaki K, et al. Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. Dev Biol. 2008;313:584–93. doi:10.1016/j.ydbio.2007.10.047.
76. Liu S, Kapoor M, Denton CP, Abraham DJ, Leask A. Loss of beta1 integrin in mouse fibroblasts results in resistance to skin scleroderma in a mouse model. Arthritis Rheum. 2009;60:2817–21. doi:10.1002/art.24801.
77. Sato T, et al. CD26 regulates p38 mitogen-activated protein kinase-dependent phosphorylation of integrin beta1, adhesion to extracellular matrix, and tumorigenicity of T-anaplastic large cell lymphoma Karpas 299. Cancer Res. 2005;65:6950–6. doi:10.1158/0008-5472.CAN-05-0647.
78. Srivastava SP, Koya D, Kanasaki K. MicroRNAs in kidney fibrosis and diabetic nephropathy: roles on EMT and EndMT. Biomed Res Int. 2013;2013:125469. doi:10.1155/2013/125469.
79. Nitta K, et al. Oral administration of N-acetyl-seryl-aspartyl-lysyl-proline ameliorates kidney disease in both type 1 and type 2 diabetic mice via a therapeutic regimen. Biomed Res Int. 2016;2016:9172157. doi:10.1155/2016/9172157.
80. Sekiya Y, Ogawa T, Yoshizato K, Ikeda K, Kawada N. Suppression of hepatic stellate cell activation by microRNA-29b. Biochem Biophys Res Commun. 2011;412:74–9. doi:10.1016/j.bbrc.2011.07.041.
81. Wang H, et al. miRNA-29c suppresses lung cancer cell adhesion to extracellular matrix and metastasis by targeting integrin beta1 and matrix metalloproteinase2 (MMP2). PLoS One. 2013;8:e70192. doi:10.1371/journal.pone.0070192.
82. Srivastava SP, et al. Effect of antifibrotic microRNAs crosstalk on the action of N-acetyl-seryl-aspartyl-lysyl-proline in diabetes-related kidney fibrosis. Sci Rep. 2016;6:29884. doi:10.1038/srep29884.
83. Chen PY, et al. FGF regulates TGF-beta signaling and endothelial-to-mesenchymal transition via control of let-7 miRNA expression. Cell Reports. 2012;2:1684–96. doi:10.1016/j.celrep.2012.10.021.
84. Shi S, Kanasaki K, Koya D. Linagliptin but not sitagliptin inhibited transforming growth factor-beta2-induced endothelial DPP-4 activity and the endothelial–mesenchymal transition. Biochem Biophys Res Commun. 2016;471:184–90. doi:10.1016/j.bbrc.2016.01.154.
85. Havale SH, Pal M. Medicinal chemistry approaches to the inhibition of dipeptidyl peptidase-4 for the treatment of type 2 diabetes. Bioorg Med Chem. 2009;17:1783–802. doi:10.1016/j.bmc.2009.01.061.
86. Liu Y, Hu Y, Liu T. Recent advances in non-peptidomimetic dipeptidyl peptidase 4 inhibitors: medicinal chemistry and preclinical aspects. Curr Med Chem. 2012;19:3982–99.
87. Terawaki Y, et al. Efficacy of dipeptidyl peptidase-4 inhibitor linagliptin in patients with type 2 diabetes undergoing hemodialysis. Diabetol Metab Syndr. 2015;7:44. doi:10.1186/s13098-015-0043-2.
88. Fitzpatrick S, Taylor S, Booth SW, Newton MJ. The development of a stable, coated pellet formulation of a water-sensitive drug, a case study: development of a stable core formulation. Pharm Dev Technol. 2006;11:521–8. doi:10.1080/10837450600941079.
89. Nabeno M, et al. A comparative study of the binding modes of recently launched dipeptidyl peptidase IV inhibitors in the active site. Biochem Biophys Res Commun. 2013;434:191–6. doi:10.1016/j.bbrc.2013.03.010.
90. Tang HK, et al. Role of a propeller loop in the quaternary structure and enzymatic activity of prolyl dipeptidases DPP-IV and DPP9. FEBS Lett. 2011;585:3409–14. doi:10.1016/j.febslet.2011.10.009.
91. Abbott CA, McCaughan GW, Levy MT, Church WB, Gorrell MD. Binding to human dipeptidyl peptidase IV by adenosine deaminase and antibodies that inhibit ligand binding involves overlapping, discontinuous sites on a predicted beta propeller domain. Eur J Biochem. 1999;266:798–810.
92. Bjelke JR, et al. Tyrosine 547 constitutes an essential part of the catalytic mechanism of dipeptidyl peptidase IV. J Biol Chem. 2004;279:34691–7. doi:10.1074/jbc.M405400200.
93. Wang H, et al. NRF2 activation by antioxidant antidiabetic agents accelerates tumor metastasis. Sci Transl Med. 2016;8:334ra351. doi:10.1126/scitranslmed.aad6095.
94. Kanasaki K, et al. Three ileus cases associated with the use of dipeptidyl peptidase-4 inhibitors in diabetic patients. J Diabetes Investig. 2013;4:673–5. doi:10.1111/jdi.12095.
95. Attaway A, Mersfelder TL, Vaishnav S, Baker JK. Bullous pemphigoid associated with dipeptidyl peptidase IV inhibitors. A case report and review of literature. J Dermatol Case Rep. 2014;8:24–8. doi:10.3315/jdcr.2014.1166.