Extracellular Redox State Regulates Catecholamine Biosynthesis in PC12 Cells with Insulin Resistance

H. L. Zheng; S. M. Yan; D. H. Hu; X. Zhang; Y. T. Zhang; Q. H. Guan; Q. L. Ding

doi:10.1055/s-0034-1374613

Hormone and Metabolic Research, Inhaltsverzeichnis

Horm Metab Res 2014; 46(06): 412-418
DOI: 10.1055/s-0034-1374613

Endocrine Research

Extracellular Redox State Regulates Catecholamine Biosynthesis in PC12 Cells with Insulin Resistance

H. L. Zheng

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

S. M. Yan

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

D. H. Hu

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

X. Zhang

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

Y. T. Zhang

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

Q. H. Guan

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

,

Q. L. Ding

¹Experimental and Teaching Center of Medical Basis for Pharmacy, China, Pharmaceutical University, Nanjing, Jiangsu, China

› Institutsangaben

Abstract

Extracellular cysteine (Cys)/cystine (CySS) redox potential (E_h) plays a crucial role in maintaining redox homeostasis and an alteration of redox state occurs in various physiological conditions, including diabetes, cancer, and aging. This study was designed to determine whether a variation in extracellular redox state would alter the function of insulin-resistant PC12 cells. Various redox states were established by providing different extracellular Cys/CySS E_h to insulin-resistant PC12 cells. We intensively investigated the relationship between redox state and catecholamine biosynthesis in PC12 cells, and evaluated the changes in cellular reactive oxygen species (ROS), catecholamine (CA) synthesis, tyrosine hydroxylase (TH) expressions, and the activity of rate-limiting enzyme in CA synthesis by using DCF-fluorescence, HPLC, and the real-time PCR, respectively. We also determined the protein levels of NF-E2-related factor 2 (Nrf2), a redox sensitive transcription factor, using an ELISA assay. We found that the oxidized Cys/CySS E_h (0 mV) pretreatment decreased CA, TH, and Nrf2 levels, but induced ROS overproduction. Insulin induced a significant increase in CA synthesis and ROS production, blocked by more reducing redox conditions. The paradox of CA and TH alterations between insulin and 0 mV groups may be attributed to degree of redox imbalance as evidenced by different ROS levels in 2 groups, which is further confirmed by CA alterations in different concentrations of hydrogen peroxide. Additionally, dithiole-3-thione (D3T, an inducer of Nrf2) corrected 0 mV-induced TH inhibition. In conclusion, CA biosynthesis in insulin-resistant PC12 cells could be influenced by extracellular Cys/CySS redox effects on cellular redox sensitive transcription factors.

Key words

tyrosine hydroxylase - redox balance - Cys/CySS E_h - reactive oxygen species

Volltext

Referenzen

References
1 Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84
2 Reaven GM. The insulin resistance syndrome: definition and dietary approaches to treatment. Annu Rev Nutr 2005; 25: 391-406
3 Zhang SP, Du XG, Pu XP. 3-O-Demethylswertipunicoside Protects against Oxidative Toxicity in PC12 Cells. Biol Pharm Bull 2010; 33: 1529-1533
4 Imhoff BR, Hansen JM. Extracellular redox status regulates Nrf2 activation through mitochondrial reactive oxygen species. Biochem J 2009; 424: 491-500
5 Go YM, Park H, Koval M, Orr M, Reed M, Liang Y, Smith D, Pohl J, Jones DP. A key role for mitochondria in endothelial signaling by plasma cysteine/cystine redox potential. Free Radic Biol Med 2010; 48: 275-283
6 Smirnova J, Muhhuna J, Tõugu V, Palumaa P. Redox and metal ion binding properties of human insulin-like growth factor 1 determined by electrospray ionization mass spectrometry. Biochemistry 2012; 51: 5851-5859
7 Jiang S, Moriarty-Craige SE, Orr M, Cai J, Sternberg Jr G, Jones DP. Oxidant-induced apoptosis in human retinal pigment epithelial cells: dependence on extracellular redox state. Invest Ophthalmol Vis Sci 2005; 46: 1054-1061
8 Go YM, Jones DP. Cysteine/cystine redox signaling in cardiovascular disease. Free Radic Biol Med 2011; 50: 495-509
9 Chaiswing L, Zhong W, Oberley TD. Distinct Redox Profiles of Selected Human Prostate Carcinoma Cell Lines: Implications for Rational Design of Redox Therapy. Cancers (Basel) 2011; 3: 3557-3584
10 Zhu JW, Yuan JF, Yang HM, Wang ST, Zhang CG, Yang H, Zhang H. Extracellular cysteine (Cys)/cystine (CySS) redox regulates metabotropic glutamate receptor 5 activity. Biochimie 2012; 94: 617-627
11 Li J, Ichikawa T, Janicki JS, Cui T. Targeting the Nrf2 pathway against cardiovascular disease. Expert Opin Ther Targets 2009; 13: 785-794
12 Li W, Kong AN. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 2009; 48: 91-104
13 Sykiotis GP, Habeos IG, Samuelson AV, Bohmann D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care 2011; 14: 41-48
14 Pi J, Zhang Q, Fu J, Woods CG, Hou Y, Corkey BE, Collins S, Andersen ME. ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell Function. Toxicol Appl Pharmacol 2010; 244: 77-83
15 Leclercq IA, Da Silva Morais A, Schroyen B, Van Hul N, Geerts A. Insulin resistance in hepatocytes and sinusoidal liver cells: Mechanisms and consequences. Journal of Hepatol 2007; 47: 142-156
16 Ricort JM, Tanti JF, Van Obberghen E, Le Marchand-Brustel Y. Alterations in insulin signalling pathway induced by prolonged insulin treatment of 3T3-L1 adipocytes. Diabetoloqia 1995; 38: 1148-1156
17 Ramirez A, Ramadan B, Ritzenthaler JD, Rivera HN, Jones DP, Roman J. Extracellular cysteine/cystine redox potential controls lung fibroblast proliferation and matrix expression through upregulation of transforming growth factor-β. Am J Physiol Lung Cell Mol Physiol 2007; 293: L972-L981
18 Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem 1994; 269: 3568-3573
19 Chen YW, Huang CF, Tsai KS, Yang RS, Yen CC, Yang CY, Lin-Shiau SY, Liu SH. The role of phosphoinositide 3-kinase/Akt signaling in low-dose mercury-induced mouse pancreatic β-cell dysfunction in vitro and in vivo. Diabetes 2006; 55: 1614-1624
20 Lee JE, Park JH, Shin IC, Koh HC. Reactive oxygen species regulated mitochondria-mediated apoptosis in PC12 cells exposed to chlorpyrifos. Toxicol Appl Pharmacol 2012; 263: 148-162
21 Fauss D, Motter R, Dofiles L, Rodrigues MA, You M, Diep L, Yang Y, Seto P, Tanaka K, Baker J, Bergeron M. Development of an enzyme-linked immunosorbent assay (ELISA) to measure the level of tyrosine hydroxylase protein in brain tissue from Parkinson’s disease models. J Neurosci Meth 2013; 215: 245-257
22 Zhu X, Tao K, Li Y, Li S, Zhang L, Wang D, Zhong L, Feng W. A new recombinant immunotoxin hscFv-ETA’ demonstrates specific cytotoxicity against chronic myeloid leukemia cells in vitro. Immunol Lett 2013; 154: 18-24
23 Vucetic Z, Carlin JL, Totoki K, Reyes TM. Epigenetic dysregulation of the dopamine system in diet-induced obesity. J Neurochem 2012; 120: 891-898
24 Volpicelli F, De Greqorio R, Pulcrano S, Perrone-Capano C, di Porzio U, Bellenchi GC. Direct Regulation of Pitx3 Expression by Nurr1 in Culture and in Developing Mouse Midbrain. PLoS One 2012; 7: e30661
25 Iyer SS, Ramirez AM, Ritzenthaler JD, Torres-Gonzalez E, Roser-Page S, Mora AL, Brighan KL, Jones DP, Roman J, Rojas M. Oxidation of extracellular cysteine/cystine redox state in bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2009; 296: L37-L45
26 Ishihara Y, Itoh K, Mitsuda Y, Shimada T, Kubota T, Kato C, Song SY, Kobayashi Y, Mori-Yasumoto K, Sekita S, Kirino Y, Yamazaki T, Shimamoto N. Involvement of brain oxidation in the cognitive impairment in a triple transgenic mouse model of Alzheimer’s disease: Noninvasive measurement of the brain redox state by magnetic resonance imaging. Free Radic Res 2013; 47: 731-739
27 Nquyen D, Samson SL, Reddy VT, Gonzalez EV, Sekhar RV. Impaired mitochondrial fatty acid oxidation and insulin resistance in aging: novel protective role of glutathione. Aqing Cell 2013; 12: 415-425
28 Chaiswing L, Zhong W, Liang Y, Jones DP, Oberley TD. Regulation of prostate cancer cell invasion by modulation of extra- and intracellular redox balance. Free Radic Biol Med 2012; 52: 452-461
29 Cheng X, Siow RC, Mann GE. Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxid Redox Signal 2011; 14: 469-487
30 Tan Y, Ichikawa T, Li J, Si Q, Yang H, Chen X, Goldblatt CS, Meyer CJ, Li X, Cai L, Cui T. Diabetic Downregulation of Nrf2 Activity via ERK Contributes to Oxidative Stress-Induced Insulin Resistance in Cardiac Cells In Vitro and In Vivo. Diabetes 2011; 60: 625-633
31 Fiqlewicz DP, Bentson K, Ocrant I. The Effect of Insulin on Norepinephrine Uptake by PC12 Cells. Brain Res Bull 1993; 32: 425-431
32 Bach LA, Leeding KS. Insulin-like Growth Factors Decrease Catecholamine Content in PC12 Rat Pheochromocytoma Cells. Horm Metab Res 2002; 34: 487-491
33 Pachori AS, Custer L, Hansen D, Clapp S, Kemppa E, Klingensmith J. Bone morphogenetic protein 4 mediates myocardial ischemic injury through JNK-dependent signaling pathway. J Mol Cell Cardiol 2010; 48: 1255-1265
34 Liang X, Naqai A, Terashima M, Sheikh AM, Shiota Y, Mitaki S, Kim SU, Yamaquchi S. Cystatin C induces apoptosis and tyrosine hydroxylase gene expression through JNK-dependent pathway in neuronal cells. Neurosci Lett 2011; 496: 100-105
35 Lee MY, Choi EJ, Lee MK, Lee JJ. Epigallocatechin gallate attenuates L-DOPA-induced apoptosis in rat PC12 cells. Nutr Res Pract 2013; 7: 249-255