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BioMed Research International
Volume 2018 (2018), Article ID 1864107, 14 pages
https://doi.org/10.1155/2018/1864107
Research Article

Glucagon-Like Peptide-1 Mediates the Protective Effect of the Dipeptidyl Peptidase IV Inhibitor on Renal Fibrosis via Reducing the Phenotypic Conversion of Renal Microvascular Cells in Monocrotaline-Treated Rats

1Department of Respiratory & Critical Care Medicine, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu 210029, China
2Department of Critical Care Medicine, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu 210029, China

Correspondence should be addressed to Hong Wang and Xiangrong Zuo

Received 21 June 2017; Revised 24 November 2017; Accepted 4 December 2017; Published 23 January 2018

Academic Editor: Bo Zuo

Copyright © 2018 Jian Xu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. S. Duffield, “Cellular and molecular mechanisms in kidney fibrosis,” The Journal of Clinical Investigation, vol. 124, no. 6, pp. 2299–2306, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. I. Grgic, J. S. Duffield, and B. D. Humphreys, “The origin of interstitial myofibroblasts in chronic kidney disease,” Pediatric Nephrology, vol. 27, no. 2, pp. 183–193, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Zeisberg and E. G. Neilson, “Mechanisms of tubulointerstitial fibrosis,” Journal of the American Society of Nephrology, vol. 21, no. 11, pp. 1819–1834, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Boor, T. Ostendorf, and J. Floege, “Renal fibrosis: novel insights into mechanisms and therapeutic targets,” Nature Reviews Nephrology, vol. 6, no. 11, pp. 643–656, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Piera-Velazquez, Z. Li, and S. A. Jimenez, “Role of endothelial-mesenchymal transition (EndoMT) in the pathogenesis of fibrotic disorders,” The American Journal of Pathology, vol. 179, no. 3, pp. 1074–1080, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. V. S. Lebleu, G. Taduri, J. O'Connell et al., “Origin and function of myofibroblasts in kidney fibrosis,” Nature Medicine, vol. 19, no. 8, pp. 1047–1053, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. P. G. Smith, Q. Fan, R. Zhang, and J. D. Warn, “Cellular terrain surrounding sympathetic nerve pathways in the rat orbit: Comparisons of orbital connective tissue and smooth muscle cell phenotypes,” Journal of Comparative Neurology, vol. 400, no. 4, pp. 529–543, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. G. J. Becker, V. Perkovic, and T. D. Hewitson, “Pharmacological intervention in renal fibrosis and vascular sclerosis,” Journal of Nephrology, vol. 14, no. 5, pp. 332–339, 2001. View at Google Scholar · View at Scopus
  9. A. Pai, E. M. Leaf, M. El-Abbadi, and C. M. Giachelli, “Elastin degradation and vascular smooth muscle cell phenotype change precede cell loss and arterial medial calcification in a uremic mouse model of chronic kidney disease,” The American Journal of Pathology, vol. 178, no. 2, pp. 764–773, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Anderson, J. B. Halter, W. R. Hazzard et al., “Prediction, progression, and outcomes of chronic kidney disease in older adults,” Journal of the American Society of Nephrology, vol. 20, no. 6, pp. 1199–1209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. A. R. Chade and J. E. Hall, “Role of the Renal Microcirculation in Progression of Chronic Kidney Injury in Obesity,” American Journal of Nephrology, vol. 44, no. 5, pp. 354–367, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. D. A. Long, J. T. Norman, and L. G. Fine, “Restoring the renal microvasculature to treat chronic kidney disease,” Nature Reviews Nephrology, vol. 8, no. 4, pp. 244–250, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. M. H. A. Muskiet, M. M. Smits, L. M. Morsink, and M. Diamant, “The gut-renal axis: do incretin-based agents confer renoprotection in diabetes?” Nature Reviews Nephrology, vol. 10, no. 2, pp. 88–103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Tanaka, Y. Higashijima, T. Wada, and M. Nangaku, “The potential for renoprotection with incretin-based drugs,” Kidney International, vol. 86, no. 4, pp. 701–711, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Matsui, S. Nakashima, Y. Nishino et al., “Dipeptidyl peptidase-4 deficiency protects against experimental diabetic nephropathy partly by blocking the advanced glycation end products-receptor axis,” Laboratory Investigation, vol. 95, no. 5, pp. 525–533, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. S. W. Lim, L. Jin, S. G. Piao, B. H. Chung, and C. W. Yang, “Inhibition of dipeptidyl peptidase IV protects tacrolimus-induced kidney injury,” Laboratory Investigation, vol. 95, no. 10, pp. 1174–1185, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Eun Lee, J. E. Kim, M. H. Lee et al., “DA-1229, a dipeptidyl peptidase IV inhibitor, protects against renal injury by preventing podocyte damage in an animal model of progressive renal injury,” Laboratory Investigation, vol. 96, no. 5, pp. 547–560, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. S. H. Baek, S. H. Kim, J. W. Kim, Y. J. Kim, K.-W. Lee, and K. Y. Na, “Effects of a DPP4 inhibitor on cisplatin-induced acute kidney injury: Study protocol for a randomized controlled trial,” Trials, vol. 16, no. 1, article no. 239, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. L. L. F. Glorie, A. Verhulst, V. Matheeussen et al., “DPP4 inhibition improves functional outcome after renal ischemia-reperfusion injury,” American Journal of Physiology-Renal Physiology, vol. 303, no. 5, pp. F681–F688, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Katagiri, Y. Hamasaki, K. Doi et al., “Protection of glucagon-like peptide-1 in cisplatin-induced renal injury elucidates gut-kidney connection,” Journal of the American Society of Nephrology, vol. 24, no. 12, pp. 2034–2043, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. H. S. Min, J. E. Kim, M. H. Lee et al., “Dipeptidyl peptidase IV inhibitor protects against renal interstitial fibrosis in a mouse model of ureteral obstruction,” Laboratory Investigation, vol. 94, no. 6, pp. 598–607, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. J. R. Ussher and D. J. Drucker, “Cardiovascular actions of incretin-based therapies,” Circulation Research, vol. 114, no. 11, pp. 1788–1803, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Dalle, R. Burcelin, and P. Gourdy, “Specific actions of GLP-1 receptor agonists and DPP4 inhibitors for the treatment of pancreatic β-cell impairments in type 2 diabetes,” Cellular Signalling, vol. 25, no. 2, pp. 570–579, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. L. A. Carstens and J. R. Allen, “Arterial degeneration and glomerular hyalinization in the kidney of monocrotaline-intoxicated rats.,” The American Journal of Pathology, vol. 60, no. 1, pp. 75–92, 1970. View at Google Scholar · View at Scopus
  25. J.-J. Wang, X.-R. Zuo, J. Xu et al., “Evaluation and Treatment of Endoplasmic Reticulum (ER) Stress in Right Ventricular Dysfunction during Monocrotaline-Induced Rat Pulmonary Arterial Hypertension,” Cardiovascular Drugs and Therapy, vol. 30, no. 6, pp. 587–598, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Koole, K. Pabreja, E. E. Savage et al., “Recent advances in understanding GLP-1R (glucagon-like peptide-1 receptor) function,” Biochemical Society Transactions, vol. 41, no. 1, pp. 172–179, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. M.-D. Wang, Y. Huang, G.-P. Zhang et al., “Exendin-4 improved rat cortical neuron survival under oxygen/glucose deprivation through PKA pathway,” Neuroscience, vol. 226, pp. 388–396, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Kanasaki, G. Taduri, and D. Koya, “Diabetic nephropathy: the role of inflammation in fibroblast activation and kidney fibrosis,” Frontiers in Endocrinology, vol. 4, article 7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. J. He, Y. Xu, D. Koya, and K. Kanasaki, “Role of the endothelial-to-mesenchymal transition in renal fibrosis of chronic kidney disease,” Clinical and Experimental Nephrology, vol. 17, no. 4, pp. 488–497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. E. M. Zeisberg, O. Tarnavski, M. Zeisberg et al., “Endothelial-to-mesenchymal transition contributes to cardiac fibrosis,” Nature Medicine, vol. 13, no. 8, pp. 952–961, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. E. G. Neilson, “Mechanisms of disease: fibroblasts—a new look at an old problem,” Nature Clinical Practice Nephrology, vol. 2, no. 2, pp. 101–108, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. M. P. Rastaldi, “Epithelial-mesenchymal transition and its implications for the development of renal tubulointerstitial fibrosis,” Journal of Nephrology, vol. 19, no. 4, pp. 407–412, 2006. View at Google Scholar · View at Scopus
  33. M. Zeisberg and R. Kalluri, “Fibroblasts emerge via epithelial-mesenchymal transition in chronic kidney fibrosis,” Frontiers in Bioscience, vol. 13, no. 18, pp. 6991–6998, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Potenta, E. Zeisberg, and R. Kalluri, “The role of endothelial-to-mesenchymal transition in cancer progression,” British Journal of Cancer, vol. 99, no. 9, pp. 1375–1379, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Zafrani and C. Ince, “Microcirculation in acute and chronic kidney diseases,” American Journal of Kidney Diseases, vol. 66, no. 6, pp. 1083–1094, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Kurozumi, K. Tanaka, M. Kido, and Y. Shoyama, “Monocrotaline-induced renal lesions,” Experimental and Molecular Pathology, vol. 39, no. 3, pp. 377–386, 1983. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Yao, C.-G. Li, L.-K. Gong et al., “Hepatic cytochrome P450s play a major role in monocrotaline-induced renal toxicity in mice,” Acta Pharmacologica Sinica, vol. 35, no. 2, pp. 292–300, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. M. S. Abdel-Bakky, M. A. Hammad, L. A. Walker, and M. K. Ashfaq, “Silencing of tissue factor by antisense deoxyoligonucleotide prevents monocrotaline/LPS renal injury in mice,” Archives of Toxicology, vol. 85, no. 10, pp. 1245–1256, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Li, C. Wei, I.-K. Kim, Y. Janssen-Heininger, and S. Gupta, “Inhibition of nuclear factor-κB in the lungs prevents monocrotaline-induced pulmonary hypertension in mice,” Hypertension, vol. 63, no. 6, pp. 1260–1269, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. J.-H. Ye, M.-H. Liu, X.-L. Zhang, and J.-Y. He, “Chemical profiles and protective effect of Hedyotis diffusa willd in lipopolysaccharide-induced renal inflammation mice,” International Journal of Molecular Sciences, vol. 16, no. 11, pp. 27252–27269, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Amirshahrokhi and A.-R. Khalili, “Thalidomide Ameliorates Cisplatin-Induced Nephrotoxicity by Inhibiting Renal Inflammation in an Experimental Model,” Inflammation, vol. 38, no. 2, pp. 476–484, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Solini, S. Menini, C. Rossi et al., “The purinergic 2X7 receptor participates in renal inflammation and injury induced by high-fat diet: Possible role of NLRP3 inflammasome activation,” The Journal of Pathology, vol. 231, no. 3, pp. 342–353, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Alique, E. Civantos, and E. Sanchez-Lopez, “Integrin-linked kinase plays a key role in the regulation of angiotensin II-induced renal inflammation,” Clinical Science, vol. 127, no. 1, pp. 19–31, 2014. View at Publisher · View at Google Scholar
  44. A. A. Elmarakby, J. Faulkner, M. Al-Shabrawey, M.-H. Wang, K. R. Maddipati, and J. D. Imig, “Deletion of soluble epoxide hydrolase gene improves renal endothelial function and reduces renal inflammation and injury in streptozotocin-induced type 1 diabetes,” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 301, no. 5, pp. R1307–R1317, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. L. L. Baggio and D. J. Drucker, “Biology of incretins: GLP-1 and GIP,” Gastroenterology, vol. 132, no. 6, pp. 2131–2157, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Sharma, J. E. Mells, P. P. Fu, N. K. Saxena, and F. A. Anania, “GLP-1 analogs reduce hepatocyte steatosis and improve survival by enhancing the unfolded protein response and promoting macroautophagy,” PLoS ONE, vol. 6, no. 9, Article ID e25269, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. B. N. Davis-Dusenbery, C. Wu, and A. Hata, “Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 11, pp. 2370–2377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. M. Spin, L. Maegdefessel, and P. S. Tsao, “Vascular smooth muscle cell phenotypic plasticity: Focus on chromatin remodelling,” Cardiovascular Research, vol. 95, no. 2, pp. 147–155, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. G. K. Owens, M. S. Kumar, and B. R. Wamhoff, “Molecular regulation of vascular smooth muscle cell differentiation in development and disease,” Physiological Reviews, vol. 84, no. 3, pp. 767–801, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Ross, “Atherosclerosis—an inflammatory disease,” The New England Journal of Medicine, vol. 340, no. 2, pp. 115–126, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. V. A. Belo, D. A. Guimarães, and M. M. Castro, “Matrix metalloproteinase 2 as a potential mediator of vascular smooth muscle cell migration and chronic vascular remodeling in hypertension,” Journal of Vascular Research, vol. 52, no. 4, pp. 221–231, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Casella, A. Bielli, A. Mauriello, and A. Orlandi, “Molecular pathways regulating macrovascular pathology and vascular smooth muscle cells phenotype in type 2 diabetes,” International Journal of Molecular Sciences, vol. 16, no. 10, pp. 24353–24368, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. D. B. Wright, T. Trian, S. Siddiqui et al., “Phenotype modulation of airway smooth muscle in asthma,” Pulmonary pharmacology therapeutics, vol. 26, no. 1, pp. 42–49, 2013. View at Publisher · View at Google Scholar
  54. D. B. Wright, T. Trian, S. Siddiqui et al., “Functional phenotype of airway myocytes from asthmatic airways,” Pulmonary pharmacology therapeutics, vol. 26, no. 1, pp. 95–104, 2013. View at Publisher · View at Google Scholar
  55. E. M. Zeisberg, S. E. Potenta, H. Sugimoto, M. Zeisberg, and R. Kalluri, “Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition,” Journal of the American Society of Nephrology, vol. 19, no. 12, pp. 2282–2287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. B. C. Cooley, J. Nevado, and J. Mellad, “TGF-β signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling,” Science Translational Medicine, vol. 6, no. 227, Article ID 227ra34, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Y. Chen, L. Qin, N. Baeyens et al., “Endothelial-to-mesenchymal transition drives atherosclerosis progression,” The Journal of Clinical Investigation, vol. 125, no. 12, pp. 4514–4528, 2015. View at Publisher · View at Google Scholar
  58. A. M. Reynolds, M. D. Holmes, S. M. Danilov, and P. N. Reynolds, “Targeted gene delivery of BMPR2 attenuates pulmonary hypertension,” European Respiratory Journal, vol. 39, no. 2, pp. 329–343, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Shi, S. P. Srivastava, M. Kanasaki et al., “Interactions of DPP-4 and integrin β1 influences endothelial-to-mesenchymal transition,” Kidney International, vol. 88, no. 3, pp. 479–489, 2015. View at Publisher · View at Google Scholar
  60. K. Kanasaki, S. Shi, M. Kanasaki et al., “Linagliptin-mediated DPP-4 inhibition ameliorates kidney fibrosis in streptozotocin-induced diabetic mice by inhibiting endothelial-to-mesenchymal transition in a therapeutic regimen,” Diabetes, vol. 63, no. 6, pp. 2120–2131, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Nistala, J. Habibi, G. Lastra et al., “Prevention of obesity-induced renal injury in male mice by DPP4 inhibition,” Endocrinology, vol. 155, no. 6, pp. 2266–2276, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Tanaka, S. Kume, M. Chin-Kanasaki et al., “Renoprotective effect of DPP-4 inhibitors against free fatty acid-bound albumin-induced renal proximal tubular cell injury,” Biochemical and Biophysical Research Communications, vol. 470, no. 3, pp. 539–545, 2016. View at Publisher · View at Google Scholar · View at Scopus