Tetramethylpyrazine inhibits angiotensin II-induced activation of hepatic stellate cells associated with interference of platelet-derived growth factor β receptor pathways

FEBS Journal

Volumn 281, Issue 12, 2014, Pages 2754-2768

  Zhang, Xiaoping ^a   Zhang, Feng ^a   Kong, Desong ^a   Wu, Xiafei ^a   Lian, Naqi ^a   Chen, Li ^a   Lu, Yin ^a   Zheng, Shizhong ^a  

^a NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

angiotensin II; hepatic fibrosis; hepatic stellate cell; platelet derived growth factor receptor; tetramethylpyrazine

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CASPASE; FOCAL ADHESION KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROCOLLAGEN; PROCOLLAGEN ALPHA1(I); PROTEIN BCL 2; PROTEIN KINASE B; TETRAMETHYLPYRAZINE; UNCLASSIFIED DRUG;

ALPHA SMOOTH MUSCLE ACTIN GENE; ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL GROWTH; CELL INVASION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; MALE; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROCOLLAGEN ALPHA1(I) GENE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; STELLATE CELL;

ANGIOTENSIN II; HEPATIC FIBROSIS; HEPATIC STELLATE CELL; PLATELET-DERIVED GROWTH FACTOR Β RECEPTOR; TETRAMETHYLPYRAZINE;

ANGIOTENSIN II; ANIMALS; APOPTOSIS; CELL DIVISION; CELL PROLIFERATION; FLOW CYTOMETRY; G2 PHASE; HEPATIC STELLATE CELLS; MALE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; TOR SERINE-THREONINE KINASES;

EID: 84903637684     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12818     Document Type: Article

References (60)

1. Hernandez-Gea V, &, Friedman SL, (2011) Pathogenesis of liver fibrosis. Annu Rev Pathol 6, 425-456.
2. Senoo H, Yoshikawa K, Morii M, Miura M, Imai K, &, Mezaki Y, (2010) Hepatic stellate cell (vitamin A-storing cell) and its relative-past, present and future. Cell Biol Int 34, 1247-1272.
3. Rockey DC, (2008) Current and future anti-fibrotic therapies for chronic liver disease. Clin Liver Dis 12, 939-962, xi.
4. Tox U, &, Steffen HM, (2006) Impact of inhibitors of the renin-angiotensin-aldosterone system on liver fibrosis and portal hypertension. Curr Med Chem 13, 3649-3661.
5. Pereira RM, dos Santos RA, da Costa Dias FL, Teixeira MM, &, Simoes e Silva AC, (2009) Renin-angiotensin system in the pathogenesis of liver fibrosis. World J Gastroenterol 15, 2579-2586.
6. Zaman MA, Oparil S, &, Calhoun DA, (2002) Drugs targeting the renin-angiotensin-aldosterone system. Nat Rev Drug Discov 1, 621-636.
7. Fallowfield JA, &, Iredale JP, (2004) Targeted treatments for cirrhosis. Expert Opin Ther Targets 8, 423-435.
8. Hunyady L, &, Catt KJ, (2006) Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol 20, 953-970.
9. Bataller R, Sancho-Bru P, Gines P, Lora JM, Al-Garawi A, Sole M, Colmenero J, Nicolas JM, Jimenez W, Weich N, et al,. (2003) Activated human hepatic stellate cells express the renin-angiotensin system and synthesize angiotensin II. Gastroenterology 125, 117-125.
10. Bataller R, Gines P, Nicolas JM, Gorbig MN, Garcia-Ramallo E, Gasull X, Bosch J, Arroyo V, &, Rodes J, (2000) Angiotensin II induces contraction and proliferation of human hepatic stellate cells. Gastroenterology 118, 1149-1156.
11. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Nakatani T, Tsujinoue H, &, Fukui H, (2001) Angiotensin-II type 1 receptor interaction is a major regulator for liver fibrosis development in rats. Hepatology 34, 745-750.
12. Bataller R, Gabele E, Parsons CJ, Morris T, Yang L, Schoonhoven R, Brenner DA, &, Rippe RA, (2005) Systemic infusion of angiotensin II exacerbates liver fibrosis in bile duct-ligated rats. Hepatology 41, 1046-1055.
13. Bataller R, Schwabe RF, Choi YH, Yang L, Paik YH, Lindquist J, Qian T, Schoonhoven R, Hagedorn CH, Lemasters JJ, et al,. (2003) NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 112, 1383-1394.
14. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Yanase K, Namisaki T, Yamazaki M, Tsujinoue H, Imazu H, et al,. (2003) Angiotensin-II induces the tissue inhibitor of metalloproteinases-1 through the protein kinase-C signaling pathway in rat liver fibrosis development. Hepatol Res 27, 51-56.
15. Baker KM, &, Kumar R, (2006) Intracellular angiotensin II induces cell proliferation independent of AT1 receptor. Am J Physiol Cell Physiol 291, C995-C1001.
16. Turner NA, Ball SG, &, Balmforth AJ, (2001) The mechanism of angiotensin II-induced extracellular signal-regulated kinase-1/2 activation is independent of angiotensin AT(1A) receptor internalisation. Cell Signal 13, 269-277.
17. Lee WS, Yang HY, Kao PF, Liu JC, Chen CH, Cheng TH, &, Chan P, (2005) Tetramethylpyrazine downregulates angiotensin II-induced endothelin-1 gene expression in vascular endothelial cells. Clin Exp Pharmacol Physiol 32, 845-850.
18. Yu L, She T, Li M, Shi C, Han L, &, Cheng M, (2013) Tetramethylpyrazine inhibits angiotensin II-induced cardiomyocyte hypertrophy and tumor necrosis factor-alpha secretion through an NF-kappaB-dependent mechanism. Int J Mol Med 32, 717-722.
19. Yu LM, Si SY, Li SG, Meng LN, &, Lu B, (2008) Mechanism of preventive and therapeutic effects of tetramethylpyrazine on liver fibrosis in rats: effects on expression of TGF-β1, Smad3, Smad7 and leptin. Chin J Gastroenterol Hepatol 17, 798-801.
20. Chen W, Chen WW, Lu YM, Chen JL, &, Yao HX, (2007) Experimental studies on the therapeutic effects of ligustrazine on liver fibrosis in rats. World Clin Drug 28, 522-525.
21. Chen W, Chen WX, Jin Y, &, Lu YM, (2010) Effect of ligustrazine on the expression of TNF-α, IL-4 and IFN-γ in rats with liver fibrosis. World Clin Drug 31, 153-156.
22. Friedman SL, (2004) Stellate cells: a moving target in hepatic fibrogenesis. Hepatology 40, 1041-1043.
23. Hengartner MO, (2000) The biochemistry of apoptosis. Nature 407, 770-776.
24. Kuwana T, &, Newmeyer DD, (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15, 691-699.
25. Kuranaga E, (2011) Caspase signaling in animal development. Dev Growth Differ 53, 137-148.
26. Takahashi T, Taniguchi T, Konishi H, Kikkawa U, Ishikawa Y, &, Yokoyama M, (1999) Activation of Akt/protein kinase B after stimulation with angiotensin II in vascular smooth muscle cells. Am J Physiol 276, H1927-H1934.
27. Dugourd C, Gervais M, Corvol P, &, Monnot C, (2003) Akt is a major downstream target of PI3-kinase involved in angiotensin II-induced proliferation. Hypertension 41, 882-890.
28. Son G, Hines IN, Lindquist J, Schrum LW, &, Rippe RA, (2009) Inhibition of phosphatidylinositol 3-kinase signaling in hepatic stellate cells blocks the progression of hepatic fibrosis. Hepatology 50, 1512-1523.
29. Pinzani M, (2002) PDGF and signal transduction in hepatic stellate cells. Front Biosci 7, d1720-d1726.
30. Hsia DA, Mitra SK, Hauck CR, Streblow DN, Nelson JA, Ilic D, Huang S, Li E, Nemerow GR, Leng J, et al,. (2003) Differential regulation of cell motility and invasion by FAK. J Cell Biol 160, 753-767.
31. Weinstein IB, (2000) Disorders in cell circuitry during multistage carcinogenesis: the role of homeostasis. Carcinogenesis 21, 857-864.
32. Michalides RJ, (1999) Cell cycle regulators: mechanisms and their role in aetiology, prognosis, and treatment of cancer. J Clin Pathol 52, 555-568.
33. Zhang F, Kong DS, Zhang ZL, Lei N, Zhu XJ, Zhang XP, Chen L, Lu Y, &, Zheng SZ, (2013) Tetramethylpyrazine induces G0/G1 cell cycle arrest and stimulates mitochondrial-mediated and caspase-dependent apoptosis through modulating ERK/p53 signaling in hepatic stellate cells in vitro. Apoptosis 18, 135-149.
34. Khosravi-Far R, &, Esposti MD, (2004) Death receptor signals to mitochondria. Cancer Biol Ther 3, 1051-1057.
35. Wang C, &, Youle RJ, (2009) The role of mitochondria in apoptosis. Annu Rev Genet 43, 95-118.
36. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, &, Green DR, (2010) The BCL-2 family reunion. Mol Cell 37, 299-310.
37. Alenzi FQ, (2004) Links between apoptosis, proliferation and the cell cycle. Br J Biomed Sci 61, 99-102.
38. Lu B, Yu L, Li S, Si S, &, Zeng Y, (2010) Alleviation of CCl4-induced cirrhosis in rats by tetramethylpyrazine is associated with downregulation of leptin and TGF-beta1 pathway. Drug Chem Toxicol 33, 310-315.
39. Foster KG, &, Fingar DC, (2010) Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J Biol Chem 285, 14071-14077.
40. Perez de Obanos MP, Lopez Zabalza MJ, Prieto J, Herraiz MT, &, Iraburu MJ, (2006) Leucine stimulates procollagen alpha1(I) translation on hepatic stellate cells through ERK and PI3K/Akt/mTOR activation. J Cell Physiol 209, 580-586.
41. Perez de Obanos MP, Lopez-Zabalza MJ, Arriazu E, Modol T, Prieto J, Herraiz MT, &, Iraburu MJ, (2007) Reactive oxygen species (ROS) mediate the effects of leucine on translation regulation and type I collagen production in hepatic stellate cells. Biochim Biophys Acta 1773, 1681-1688.
42. Carloni V, Romanelli RG, Pinzani M, Laffi G, &, Gentilini P, (1997) Focal adhesion kinase and phospholipase C gamma involvement in adhesion and migration of human hepatic stellate cells. Gastroenterology 112, 522-531.
43. Reif S, Lang A, Lindquist JN, Yata Y, Gabele E, Scanga A, Brenner DA, &, Rippe RA, (2003) The role of focal adhesion kinase-phosphatidylinositol 3-kinase-akt signaling in hepatic stellate cell proliferation and type I collagen expression. J Biol Chem 278, 8083-8090.
44. Carloni V, Defranco RM, Caligiuri A, Gentilini A, Sciammetta SC, Baldi E, Lottini B, Gentilini P, &, Pinzani M, (2002) Cell adhesion regulates platelet-derived growth factor-induced MAP kinase and PI-3 kinase activation in stellate cells. Hepatology 36, 582-591.
45. Patsenker E, Popov Y, Wiesner M, Goodman SL, &, Schuppan D, (2007) Pharmacological inhibition of the vitronectin receptor abrogates PDGF-BB-induced hepatic stellate cell migration and activation in vitro. J Hepatol 46, 878-887.
46. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Franklin RA, Montalto G, Cervello M, Libra M, Candido S, Malaponte G, et al,. (2012) Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascade inhibitors: how mutations can result in therapy resistance and how to overcome resistance. Oncotarget 3, 1068-1111.
47. Yanyu X, Qineng P, Zhigui S, Hongying L, &, Jiangxiu N, (2012) Preparation and pharmacokinetics in beagle dogs of once-a-day tetramethylpyrazine phosphate sustained-release pellets. Drug Dev Ind Pharm 38, 301-306.
48. Wang LS, Shi ZF, Zhang YF, Guo Q, Huang YW, &, Zhou LL, (2012) Effect of Xiongbing compound on the pharmacokinetics and brain targeting of tetramethylpyrazine. J Pharm Pharmacol 64, 1688-1694.
49. Feng J, Li F, Zhao Y, Feng Y, &, Abe Y, (2009) Brain pharmacokinetics of tetramethylpyrazine after intranasal and intravenous administration in awake rats. Int J Pharm 375, 55-60.
50. Tsai TH, &, Liang C, (2001) Pharmacokinetics of tetramethylpyrazine in rat blood and brain using microdialysis. Int J Pharm 216, 61-66.
51. Buchdunger E, Cioffi CL, Law N, Stover D, Ohno-Jones S, Druker BJ, &, Lydon NB, (2000) Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 295, 139-145.
52. Malavaki CJ, Roussidis AE, Gialeli C, Kletsas D, Tsegenidis T, Theocharis AD, Tzanakakis GN, &, Karamanos NK, (2013) Imatinib as a key inhibitor of the platelet-derived growth factor receptor mediated expression of cell surface heparan sulfate proteoglycans and functional properties of breast cancer cells. FEBS J 280, 2477-2489.
53. Jones RL, &, Judson IR, (2005) The development and application of imatinib. Expert Opin Drug Saf 4, 183-191.
54. Buchdunger E, O'Reilly T, &, Wood J, (2002) Pharmacology of imatinib (STI571). Eur J Cancer 38 (Suppl 5), S28-S36.
55. Svegliati-Baroni G, Ridolfi F, Di Sario A, Casini A, Marucci L, Gaggiotti G, Orlandoni P, Macarri G, Perego L, Benedetti A, et al,. (1999) Insulin and insulin-like growth factor-1 stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: differential effects on signal transduction pathways. Hepatology 29, 1743-1751.
56. Lin J, Zheng S, &, Chen A, (2009) Curcumin attenuates the effects of insulin on stimulating hepatic stellate cell activation by interrupting insulin signaling and attenuating oxidative stress. Lab Invest 89, 1397-1409.
57. Erion MD, van Poelje PD, Mackenna DA, Colby TJ, Montag AC, Fujitaki JM, Linemeyer DL, &, Bullough DA, (2005) Liver-targeted drug delivery using HepDirect prodrugs. J Pharmacol Exp Ther 312, 554-560.
58. Davis BH, Pratt BM, &, Madri JA, (1987) Retinol and extracellular collagen matrices modulate hepatic Ito cell collagen phenotype and cellular retinol binding protein levels. J Biol Chem 262, 10280-10286.
59. Zhang F, Ni C, Kong D, Zhang X, Zhu X, Chen L, Lu Y, &, Zheng S, (2012) Ligustrazine attenuates oxidative stress-induced activation of hepatic stellate cells by interrupting platelet-derived growth factor-beta receptor-mediated ERK and p38 pathways. Toxicol Appl Pharmacol 265, 51-60.
60. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, &, Reed MW, (2000) Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285, 194-204.