The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
권호 표지
DOI QR코드

DOI QR Code

Angiotensin III increases monocyte chemoattractant protein-1 expression in cultured human proximal tubular epithelial cells

  • Kim, Hyung Wook (Division of Nephrology, Department of Internal Medicine, College of Medicine, St. Vincent's Hospital, The Catholic University of Korea) ;
  • Kim, Young Ok (Division of Nephrology, Department of Internal Medicine, College of Medicine, Uijeongbu St. Mary's Hospital, The Catholic University of Korea) ;
  • Yoon, Sun Ae (Division of Nephrology, Department of Internal Medicine, College of Medicine, Uijeongbu St. Mary's Hospital, The Catholic University of Korea) ;
  • Han, Jeong-Sun (Renal Research Laboratory, Division of Nephrology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea) ;
  • Chun, Hyun-Bae (Department of Medicine, Stony Brook University of New York) ;
  • Kim, Young Soo (Division of Nephrology, Department of Internal Medicine, College of Medicine, Uijeongbu St. Mary's Hospital, The Catholic University of Korea)
  • Received : 2014.07.02
  • Accepted : 2014.08.26
  • Published : 2016.01.01
⟨ Previous Next ⟩

Abstract

Background/Aims: We investigated whether angiotensin III (Ang III) is involved in monocyte recruitment through regulation of the chemokine monocyte chemoattractant protein-1 (MCP-1) in cultured human proximal tubular epithelial cells (HK-2 cells). Methods: We measured MCP-1 levels in HK-2 cells that had been treated with various concentrations of Ang III and Ang II type-1 (AT1) receptor antagonists at various time points. The phosphorylation states of p38, c-Jun N-terminal kinases (JNK), and extracellular-signal-regulated kinases were measured in Ang III-treated cells to explore the mitogen-activated protein kinase (MAPK) pathway. MCP-1 levels in HK-2 cell-conditioned media were measured after pre-treatment with the transcription factor inhibitors curcumin or pyrrolidine dithiocarbamate. Results: Ang III increased MCP-1 protein production in dose- and time-dependent manners in HK-2 cells, which was inhibited by the AT1 receptor blocker losartan. p38 MAPK activity increased significantly in HK-2 cells exposed to Ang III for 30 minutes, and was sustained at higher levels after 60 minutes (p < 0.05). Total phosphorylated JNK protein levels tended to increase 20 minutes after stimulation with Ang III. Pre-treatment with a p38 inhibitor, a JNK inhibitor, or curcumin significantly inhibited Ang III-induced MCP-1 production. Conclusions: Ang III increases MCP-1 synthesis via stimulation of intracellular p38 and JNK MAPK signaling activity and subsequent activated protein-1 transcriptional activity in HK-2 cells.

Keywords

References

  1. Igic R. A short history of the renin-angiotensin system. Acta Med Salin 2009;38:8-12.
  2. Capettini LS, Montecucco F, Mach F, Stergiopulos N, Santos RA, da Silva RF. Role of renin-angiotensin system in inflammation, immunity and aging. Curr Pharm Des 2012;18:963-970. https://doi.org/10.2174/138161212799436593
  3. Park CG, Ahn JC, Hong SJ, et al. Efficacy of irbesartan on left ventricular mass and arterial stiffness in hypertensive patients. Korean J Intern Med 2006;21:103-108. https://doi.org/10.3904/kjim.2006.21.2.103
  4. Yoon HE, Choi BS. The renin-angiotensin system and aging in the kidney. Korean J Intern Med 2014;29:291-295. https://doi.org/10.3904/kjim.2014.29.3.291
  5. Unger T. The role of the renin-angiotensin system in the development of cardiovascular disease. Am J Cardiol 2002;89:3A-9A.
  6. Brasier AR, Recinos A 3rd, Eledrisi MS. Vascular inflammation and the renin-angiotensin system. Arterioscler Thromb Vasc Biol 2002;22:1257-1266. https://doi.org/10.1161/01.ATV.0000021412.56621.A2
  7. Marchesi C, Paradis P, Schiffrin EL. Role of the renin-angiotensin system in vascular inflammation. Trends Pharmacol Sci 2008;29:367-374. https://doi.org/10.1016/j.tips.2008.05.003
  8. Suzuki Y, Ruiz-Ortega M, Lorenzo O, Ruperez M, Esteban V, Egido J. Inflammation and angiotensin II. Int J Biochem Cell Biol 2003;35:881-900. https://doi.org/10.1016/S1357-2725(02)00271-6
  9. Muller DN, Mervaala EM, Schmidt F, et al. Effect of bosentan on NF-kappaB, inflammation, and tissue factor in angiotensin II-induced end-organ damage. Hypertension 2000;36:282-290. https://doi.org/10.1161/01.HYP.36.2.282
  10. Ardaillou R. Active fragments of angiotensin II: enzymatic pathways of synthesis and biological effects. Curr Opin Nephrol Hypertens 1997;6:28-34. https://doi.org/10.1097/00041552-199701000-00006
  11. Numaguchi Y, Ishii M, Kubota R, et al. Ablation of angiotensin IV receptor attenuates hypofibrinolysis via PAI-1 downregulation and reduces occlusive arterial thrombosis. Arterioscler Thromb Vasc Biol 2009;29:2102-2108. https://doi.org/10.1161/ATVBAHA.109.195057
  12. Padia SH, Kemp BA, Howell NL, Fournie-Zaluski MC, Roques BP, Carey RM. Conversion of renal angiotensin II to angiotensin III is critical for AT2 receptor-mediated natriuresis in rats. Hypertension 2008;51:460-465. https://doi.org/10.1161/HYPERTENSIONAHA.107.103242
  13. Padia SH, Kemp BA, Howell NL, et al. Intrarenal aminopeptidase N inhibition augments natriuretic responses to angiotensin III in angiotensin type 1 receptor-blocked rats. Hypertension 2007;49:625-630. https://doi.org/10.1161/01.HYP.0000254833.85106.4d
  14. Li Q, Feenstra M, Pfaffendorf M, Eijsman L, van Zwieten PA. Comparative vasoconstrictor effects of angiotensin II, III, and IV in human isolated saphenous vein. J Cardiovasc Pharmacol 1997;29:451-456. https://doi.org/10.1097/00005344-199704000-00004
  15. Sjostrom H, Noren O, Olsen J. Structure and function of aminopeptidase N. Adv Exp Med Biol 2000;477:25-34.
  16. Song L, Healy DP. Kidney aminopeptidase A and hypertension, part II: effects of angiotensin II. Hypertension 1999;33:746-752. https://doi.org/10.1161/01.HYP.33.2.746
  17. Song L, Ye M, Troyanovskaya M, Wilk E, Wilk S, Healy DP. Rat kidney glutamyl aminopeptidase (aminopeptidase A): molecular identity and cellular localization. Am J Physiol 1994;267(4 Pt 2):F546-F557.
  18. Lorenzo O, Ruiz-Ortega M, Suzuki Y, et al. Angiotensin III activates nuclear transcription factor-kappaB in cultured mesangial cells mainly via AT(2) receptors: studies with AT(1) receptor-knockout mice. J Am Soc Nephrol 2002;13:1162-1171.
  19. Ruiz-Ortega M, Lorenzo O, Egido J. Angiotensin III up-regulates genes involved in kidney damage in mesangial cells and renal interstitial fibroblasts. Kidney Int Suppl 1998;68:S41-S45.
  20. Banas B, Luckow B, Moller M, et al. Chemokine and chemokine receptor expression in a novel human mesangial cell line. J Am Soc Nephrol 1999;10:2314-2322.
  21. Schlondorff D, Nelson PJ, Luckow B, Banas B. Chemokines and renal disease. Kidney Int 1997;51:610-621. https://doi.org/10.1038/ki.1997.90
  22. Zhuo JL. Monocyte chemoattractant protein-1: a key mediator of angiotensin II-induced target organ damage in hypertensive heart disease? J Hypertens 2004;22:451-454. https://doi.org/10.1097/00004872-200403000-00003
  23. Pearson G, Robinson F, Beers Gibson T, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001;22:153-183.
  24. Ho AW, Wong CK, Lam CW. Tumor necrosis factor-alpha up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology 2008;213:533-544. https://doi.org/10.1016/j.imbio.2008.01.003
  25. Iyoda M, Shibata T, Kawaguchi M, et al. IL-17A and IL-17F stimulate chemokines via MAPK pathways (ERK1/2 and p38 but not JNK) in mouse cultured mesangial cells: synergy with TNF-alpha and IL-1beta. Am J Physiol Renal Physiol 2010;298:F779-F787. https://doi.org/10.1152/ajprenal.00198.2009
  26. Prakash J, Sandovici M, Saluja V, et al. Intracellular delivery of the p38 mitogen-activated protein kinase inhibitor SB202190 [4-(4-fluorophenyl)-2-(4-hydroxyphenyl)-5-(4-pyridyl)1H-imidazole] in renal tubular cells: a novel strategy to treat renal fibrosis. J Pharmacol Exp Ther 2006;319:8-19. https://doi.org/10.1124/jpet.106.106054
  27. Sakai N, Wada T, Furuichi K, et al. Involvement of extracellular signal-regulated kinase and p38 in human diabetic nephropathy. Am J Kidney Dis 2005;45:54-65. https://doi.org/10.1053/j.ajkd.2004.08.039
  28. Sheryanna A, Bhangal G, McDaid J, et al. Inhibition of p38 mitogen-activated protein kinase is effective in the treatment of experimental crescentic glomerulonephritis and suppresses monocyte chemoattractant protein-1 but not IL-1beta or IL-6. J Am Soc Nephrol 2007;18:1167-1179. https://doi.org/10.1681/ASN.2006010050
  29. Ryan MJ, Johnson G, Kirk J, Fuerstenberg SM, Zager RA, Torok-Storb B. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int 1994;45:48-57. https://doi.org/10.1038/ki.1994.6
  30. Yamamoto Y, Yamamguchi T, Shimamura M, Hazato T. Angiotensin III is a new chemoattractant for polymorphonuclear leukocytes. Biochem Biophys Res Commun 1993;193:1038-1043. https://doi.org/10.1006/bbrc.1993.1729
  31. Seikaly MG, Arant BS Jr, Seney FD Jr. Endogenous angiotensin concentrations in specific intrarenal fluid compartments of the rat. J Clin Invest 1990;86:1352-1357. https://doi.org/10.1172/JCI114846
  32. Catalioto RM, Renzetti AR, Criscuoli M, Morbidelli L, Subissi A. Role of calcium in angiotensin II-induced prostaglandin release and DNA synthesis in rat vascular smooth muscle cells. J Cardiovasc Pharmacol 1996;27:195-200. https://doi.org/10.1097/00005344-199602000-00004
  33. Garcia-Sainz JA, Garcia-Caballero A, Gonzalez-Espinosa C. Angiotensin AT1 receptors in Clone 9 rat liver cells: Ca2+ signaling and c-fos expression. Eur J Pharmacol 1998;362:235-243. https://doi.org/10.1016/S0014-2999(98)00770-5
  34. Ruiz-Ortega M, Lorenzo O, Egido J. Angiotensin III increases MCP-1 and activates NF-kappaB and AP-1 in cultured mesangial and mononuclear cells. Kidney Int 2000;57:2285-2298. https://doi.org/10.1046/j.1523-1755.2000.00089.x
  35. Bohle A, Wehrmann M, Bogenschutz O, et al. The longterm prognosis of the primary glomerulonephritides: a morphological and clinical analysis of 1747 cases. Pathol Res Pract 1992;188:908-924. https://doi.org/10.1016/S0344-0338(11)80252-9
  36. Segerer S, Nelson PJ, Schlondorff D. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol 2000;11:152-176.
  37. Egido J. Vasoactive hormones and renal sclerosis. Kidney Int 1996;49:578-597. https://doi.org/10.1038/ki.1996.82
  38. Matsubara H. Pathophysiological role of angiotensin II type 2 receptor in cardiovascular and renal diseases. Circ Res 1998;83:1182-1191. https://doi.org/10.1161/01.RES.83.12.1182
  39. Naito T, Ma LJ, Yang H, et al. Angiotensin type 2 receptor actions contribute to angiotensin type 1 receptor blocker effects on kidney fibrosis. Am J Physiol Renal Physiol 2010;298:F683-F691. https://doi.org/10.1152/ajprenal.00503.2009
  40. Yang CH, Shyr MH, Tan PP, Chan SH. Participation of AT1 and AT2 receptors in the differential interaction between angiotensin II or III and alpha-2 adrenoceptors in the nucleus reticularis gigantocellularis in cardiovascular regulation and antinociception in rats. J Pharmacol Exp Ther 1996;279:795-802.
  41. Luoh HF, Chan SH. Participation of AT1 and AT2 receptor subtypes in the tonic inhibitory modulation of baroreceptor reflex response by endogenous angiotensins at the nucleus tractus solitarii in the rat. Brain Res 1998;782:73-82. https://doi.org/10.1016/S0006-8993(97)01198-0
  42. Lawrence MC, Jivan A, Shao C, et al. The roles of MAPKs in disease. Cell Res 2008;18:436-442. https://doi.org/10.1038/cr.2008.37
  43. Faust D, Schmitt C, Oesch F, et al. Differential p38-dependent signalling in response to cellular stress and mitogenic stimulation in fibroblasts. Cell Commun Signal 2012;10:6. https://doi.org/10.1186/1478-811X-10-6
  44. Ueda A, Okuda K, Ohno S, et al. NF-kappa B and Sp1 regulate transcription of the human monocyte chemoattractant protein-1 gene. J Immunol 1994;153:2052-2063.
  45. Ishikawa Y, Sugiyama H, Stylianou E, Kitamura M. Bioflavonoid quercetin inhibits interleukin-1-induced transcriptional expression of monocyte chemoattractant protein-1 in glomerular cells via suppression of nuclear factor-kappaB. J Am Soc Nephrol 1999;10:2290-2296.
  46. Rovin BH, Dickerson JA, Tan LC, Hebert CA. Activation of nuclear factor-kappa B correlates with MCP-1 expression by human mesangial cells. Kidney Int 1995;48:1263-1271. https://doi.org/10.1038/ki.1995.410
  47. Nakayama K, Furusu A, Xu Q, Konta T, Kitamura M. Unexpected transcriptional induction of monocyte chemoattractant protein 1 by proteasome inhibition: involvement of the c-Jun N-terminal kinase-activator protein 1 pathway. J Immunol 2001;167:1145-1150. https://doi.org/10.4049/jimmunol.167.3.1145
  48. Martin T, Cardarelli PM, Parry GC, Felts KA, Cobb RR. Cytokine induction of monocyte chemoattractant protein- 1 gene expression in human endothelial cells depends on the cooperative action of NF-kappa B and AP-1. Eur J Immunol 1997;27:1091-1097. https://doi.org/10.1002/eji.1830270508
  49. Shyy JY, Lin MC, Han J, Lu Y, Petrime M, Chien S. The cis-acting phorbol ester “12-O-tetradecanoylphorbol 13-acetate”-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci U S A 1995;92:8069-8073. https://doi.org/10.1073/pnas.92.17.8069
  50. Huang TS, Lee SC, Lin JK. Suppression of c-Jun/AP-1 activation by an inhibitor of tumor promotion in mouse fibroblast cells. Proc Natl Acad Sci U S A 1991;88:5292-5296. https://doi.org/10.1073/pnas.88.12.5292
  51. Smeal T, Binetruy B, Mercola D, et al. Oncoprotein-mediated signalling cascade stimulates c-Jun activity by phosphorylation of serines 63 and 73. Mol Cell Biol 1992;12:3507-3513. https://doi.org/10.1128/MCB.12.8.3507
  52. Sutcliffe AM, Clarke DL, Bradbury DA, Corbett LM, Patel JA, Knox AJ. Transcriptional regulation of monocyte chemotactic protein-1 release by endothelin-1 in human airway smooth muscle cells involves NF-kappaB and AP-1. Br J Pharmacol 2009;157:436-450. https://doi.org/10.1111/j.1476-5381.2009.00143.x

Cited by

  1. The Level and Significance of Circulating Angiotensin-III in Patients with Coronary Atherosclerosis vol.2021, pp.None, 2016, https://doi.org/10.1155/2021/1704762