Leptin Induces Oxidative Stress Through Activation of NADPH Oxidase in Renal Tubular Cells: Antioxidant Effect of L-Carnitine

Journal of Cellular Biochemistry

Volumn , Issue , 2016, Pages 2281-2288

  Blanca, Antonio J ^a   Ruiz Armenta, María V ^a   Zambrano, Sonia ^a   Salsoso, Rocío ^a,b   Miguel Carrasco, José L ^a   Fortuño, Ana ^c   Revilla, Elisa ^a   Mate, Alfonso ^a,d   Vázquez, Carmen M ^a,d  

^a UNIVERSITY OF SEVILLE   (Spain)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF NAVARRA   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

L CARNITINE; LEPTIN; NADPH OXIDASE; OXIDATIVE STRESS

Indexed keywords

3 NITROTYROSINE; CARNITINE; CATALASE; HYDROGEN PEROXIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEPTIN; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; INFLAMMATION; KIDNEY EPITHELIUM; KIDNEY TUBULE CELL; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

EID: 84984996505     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25526     Document Type: Article

References (47)

1. Ahima RS, Flier JS. 2000. Leptin. Leptin Annu Rev Physiol 62:413–437.
2. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.
3. Caldefie-Chezet F, Poulin A, Tridon A, Sion B, Vasson MP. 2001. Leptin: A potential regulator of polymorphonuclear neutrophil bactericidal action? J Leukoc Biol 69:414–418.
4. Chen JX, Stinnett A. 2008. Critical role of the NADPH oxidase subunit p47phox on vascular TLR expression and neointimal lesion formation in high-fat diet-induced obesity. Lab Invest 88:1316–1328.
5. Chen YC, Chen CH, Hsu YH, Chen TH, Sue YM, Cheng CY, Chen TW. 2011. Leptin reduces gentamicin-induced apoptosis in rat renal tubular cells via the PI3K-Akt signaling pathway. Eur J Pharmacol 658:213–218.
6. Chetboun M, Abitbol G, Rozenberg K, Rozenfeld H, Deutsch A, Sampson SR, Rosenzweig T. 2012. Maintenance of redox state and pancreatic beta-cell function: Role of leptin and adiponectin. J Cell Biochem 113:1966–1976.
7. Chomczynski P, Sacchi N. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nat Protoc 1:581–585.
8. Derosa G, Maffioli P, Ferrari I, D'Angelo A, Fogari E, Palumbo I, Randazzo S, Cicero AFG. 2011. Comparison between orlistat plus l-carnitine and orlistat alone on inflammation parameters in obese diabetic patients. Fundam Clin Pharmacol 25:642–651.
9. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. 2008. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med 45:1340–1351.
10. Dong F, Zhang X, Ren J. 2006. Leptin regulates cardiomyocyte contractile function through endothelin-1 receptor-NADPH oxidase pathway. Hypertension 47:222–229.
11. Edwards DH, Li Y, Griffith TM. 2008. Hydrogen peroxide potentiates the EDHF phenomenon by promoting endothelial Ca2+ mobilization. Arterioscler Thromb Vasc Biol 28:1774–1781.
12. Filippin LI, Vercelino R, Marroni NP, Xavier RM. 2008. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol 152:415–422.
13. Fortuño A, Bidegain J, Baltanas A, Moreno MU, Montero L, Landecho MF, Belogui O, Díez J, Zalba G. 2010. Is leptin involved in phagocytic NADPH oxidase overactivity in obesity? Potential clinical implications. J Hypertens 28:1944–1950.
14. Foster MC, Hwang SJ, Larson MG, Lichtman JH, Parikh NI, Vasan RS, Levi D, Fox CS. 2008. Overweight, obesity, and the development of stage 3 CKD: The Framingham Heart Study. Am J Kidney Dis 52:39–48.
15. Frederich RC, Hamann A, Anderson S, Löllmann B, Lowell BB, Flier JS. 1995. Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action. Nat Med 1:1311–1314.
16. Hanson RL, Narayan KMV, McCance DR, Pettitt DJ, Jacobsson LTH, Bennett PH, Knowler WC. 1995. Original articles: Rate of weight gain, weight fluctuation, and incidence of NIDDM. Diabetes 44:261–266.
17. Haynes WG. 2005. Role of leptin in obesity-related hypertension. Exp Physiol 90:683–688.
18. Houseknecht KL, Baile CA, Matteri RL, Spurlock ME. 1998. The biology of leptin: A review. J Anim Sci 76:1405–1420.
19. Indra MR, Karyono S, Ratnawati R, Malik SG. 2013. Quercetin suppresses inflammation by reducing ERK1/2 phosphorylation and NF kappa B activation in leptin-induced human umbilical vein endothelial cells (HUVECs). BMC Res Notes 6:275.
20. Jang A, Kim D, Sung KS, Jung S, Kim HJ, Jo C. 2014. The effect of dietary α-lipoic acid, betaine, l-carnitine, and swimming on the obesity of mice induced by a high-fat diet. Food Funct 5:1966–1974.
21. Kang JS, Lee WK, Lee CW, Yoon WK, Kim N, Park SK, Lee HS, Park HK, Han SB, Yun J, Lee K, Lee KH, Park SK, Kim HM. 2011. Improvement of high-fat diet-induced obesity by a mixture of red grape extract, soy isoflavone and l-carnitine: Implications in cardiovascular and non-alcoholic fatty liver diseases. Food Chem Toxicol 49:2453–2458.
22. Koh KK, Park SM, Quon MJ. 2008. Leptin and cardiovascular disease: Response to therapeutic interventions. Circulation 117:3238–3249.
23. Lappas M, Permezel M, Rice GE. 2005. Leptin and adiponectin stimulate the release of proinflammatory cytokines and prostaglandins from human placenta and maternal adipose tissue via nuclear factor-kappaB, peroxisomal proliferator-activated receptor-gamma and extracellularly regulated kinase 1/2. Endocrinology 146:3334–3342.
24. Lau DCW, Dhillon B, Yan H, Szmitko PE, Verma S. 2005. Adipokines: Molecular links between obesity and atherosclerosis. Am J Physiol Heart Circ Physiol 288:H2031–H2041.
25. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402–408.
26. Mate A, Miguel-Carrasco JL, Monserrat MT, Vazquez CM. 2010. Systemic antioxidant properties of L-carnitine in two different models of arterial hypertension. J Physiol Biochem 66:127–136.
27. Mate A, Miguel-Carrasco JL, Vazquez CM. 2010. The therapeutic prospects of using L-carnitine to manage hypertension-related organ damage. Drug Discov Today 15:484–492.
28. Miguel-Carrasco JL, Mate A, Monserrat MT, Arias JL, Aramburu O, Vazquez CM. 2008. The role of inflammatory markers in the cardioprotective effect of L-carnitine in L-NAME-induced hypertension. Am J Hypertens 21:1231–1237.
29. Morawietz H. 2011. Endothelial NADPH oxidases: Friends or foes? Basic Res Cardiol 106:521–525.
30. Morawietz H, Bornstein SR. 2006. Leptin, endothelin, NADPH oxidase, and heart failure. Hypertension 47:e20–e21; e20 author rely.
31. Oswal A, Yeo G. 2010. Leptin and the control of body weight: A review of its diverse central targets, signaling mechanisms, and role in the pathogenesis of obesity. Obesity (Silver Spring) 18:221–229.
32. Pedone C, Roshanravan B, Scarlata S, Patel KV, Ferrucci L, Incalzi RA. 2015. Longitudinal association between serum leptin concentration and glomerular filtration rate in humans. PLoS ONE 10:e0117828.
33. Rahmouni K, Haynes WG. 2004. Leptin and the cardiovascular system. Recent Prog Horm Res 59:225–244.
34. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom-Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, Shah AM. 2011. Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol 31:1368–1376.
35. Schroeter MR, Leifheit-Nestler M, Hubert A, Schumann B, Glückermann R, Eschholz N, Krüger N, Lutz S, Hasenfuss G, Konstantinides S, Schäfer K. 2013. Leptin promotes neointima formation and smooth muscle cell proliferation via NADPH oxidase activation and signalling in caveolin-rich microdomains. Cardiovasc Res 99:555–565.
36. Singh M, Bedi US, Singh PP, Arora R, Khosla S. 2010. Leptin and the clinical cardiovascular risk. Int J Cardiol 140:266–271.
37. Singh P, Hoffmann M, Wolk R, Shamsuzzaman AS, Somers VK. 2007. Leptin induces C-reactive protein expression in vascular endothelial cells. Arterioscler Thromb Vasc Biol 27:e302–e307.
38. Su CC, Chang CS, Chou CH, Wu YHS, Yang KT, Tseng JK, Chang YY, Chen YC. 2015. L-carnitine ameliorates dyslipidemic and hepatic disorders induced by a high-fat diet via regulating lipid metabolism, self-antioxidant capacity, and inflammatory response. J Funct Foods 15:497–508.
39. Uddin S, Bu R, Ahmed M, Hussain AR, Ajarim D, Al-Dayel F, Bavi P, Al-kuraya KS. 2010. Leptin receptor expression and its association with PI3K/AKT signaling pathway in diffuse large B-cell lymphoma. Leuk Lymphoma 51:1305–1314.
40. Von Lohneysen K, Noack D, Wood MR, Friedman JS, Knaus UG. 2010. Structural insights into Nox4 and Nox2: Motifs involved in function and cellular localization. Mol Cell Biol 30:961–975.
41. Xu FP, Chen MS, Wang YZ, Yi Q, Lin SB, Chen AF, Luo JD. 2004. Leptin induces hypertrophy via endothelin-1-reactive oxygen species pathway in cultured neonatal rat cardiomyocytes. Circulation 110:1269–1275.
42. Yamagishi S, Amano S, Inagaki Y, Okamoto T, Takeuchi M, Inoue H. 2003. Pigment epithelium-derived factor inhibits leptin-induced angiogenesis by suppressing vascular endothelial growth factor gene expression through anti-oxidative properties. Microvasc Res 65:186–190.
43. Yang R, Barouch LA. 2007. Leptin signaling and obesity: Cardiovascular consequences. Circ Res 101:545–559.
44. Zambrano S, Blanca AJ, Ruiz-Armenta MV, Miguel-Carrasco JL, Arevalo M, Mate A, Vazquez CM. 2014. L-carnitine attenuates the development of kidney fibrosis in hypertensive rats by upregulating PPAR-gamma. Am J Hypertens 27:460–470.
45. Zambrano S, Blanca AJ, Ruiz-Armenta MV, Miguel-Carrasco JL, Arevalo M, Vazquez MJ, Mate A, Vazquez CM. 2013. L-carnitine protects against arterial hypertension-related cardiac fibrosis through modulation of PPAR-gamma expression. Biochem Pharmacol 85:937–944.
46. Zambrano S, Blanca AJ, Ruiz-Armenta MV, Miguel-Carrasco JL, Revilla E, Santa-Maria C, Mate A, Vazquez CM. 2013. The renoprotective effect of L-carnitine in hypertensive rats is mediated by modulation of oxidative stress-related gene expression. Eur J Nutr 52:1649–1659.
47. Zhang J, Johnston G, Stebler B, Keller ET. 2001. Hydrogen peroxide activates NFkappaB and the interleukin-6 promoter through NFkappaB-inducing kinase. Antioxid Redox Signal 3:493–504.