Long term exposure to L-arginine accelerates endothelial cell senescence through arginase-II and S6K1 signaling

Aging

Volumn 6, Issue 5, 2014, Pages 369-379

  Xiong, Yuyan ^a   Fru, Michael Forbiteh ^a   Yu, Yi ^a   Montani, Jean Pierre ^a   Ming, Xiu Fen ^a   Yang, Zhihong ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Adhesion molecules; Arginase II; Endothelium; L arginine; mTOR; Senescence

Indexed keywords

ARGINASE; ARGININE; RIBOSOMAL PROTEIN S6 KINASE, 70KD, POLYPEPTIDE 1; S6 KINASE;

CELL AGING; CELL CULTURE; DIET SUPPLEMENTATION; DRUG EFFECTS; ENDOTHELIUM CELL; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TOXICITY; WESTERN BLOTTING;

ARGINASE; ARGININE; BLOTTING, WESTERN; CELL AGING; CELLS, CULTURED; DIETARY SUPPLEMENTS; ENDOTHELIAL CELLS; HUMANS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION;

EID: 84901815548     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100663     Document Type: Article

References (50)

1. Morris SM, Jr. Recent advances in arginine metabolism: roles and regulation of the arginases. Br J Pharmacol. 2009; 157: 922-930.
2. Wu G and Meininger CJ. Arginine nutrition and cardiovascular function. J Nutr. 2000; 130: 2626-2629.
3. Palmer RM, Ashton DS and Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature. 1988; 333: 664-666.
4. Nieves C, Jr. and Langkamp-Henken B. Arginine and immunity:a unique perspective. Biomed Pharmacother. 2002; 56: 471-482.
5. McKnight JR, Satterfield MC, Jobgen WS, Smith SB, Spencer TE, Meininger CJ, McNeal CJ and Wu G. Beneficial effects of Larginine on reducing obesity: potential mechanisms and important implications for human health. Amino Acids. 2010; 39: 349-357.
6. Clemmensen C, Smajilovic S, Smith EP, Woods SC, Brauner-Osborne H, Seeley RJ, D'Alessio DA and Ryan KK. Oral L-arginine stimulates GLP-1 secretion to improve glucose tolerance in male mice. Endocrinology. 2013; 154: 3978-3983.
7. Alvares TS, Meirelles CM, Bhambhani YN, Paschoalin VM and Gomes PS. L-Arginine as a potential ergogenic aid in healthy subjects. Sports Med. 2011; 41: 233-248.
8. Girerd XJ, Hirsch AT, Cooke JP, Dzau VJ and Creager MA. Larginine augments endothelium-dependent vasodilation in cholesterol-fed rabbits. Circ Res. 1990; 67: 1301-1308.
9. Creager MA, Gallagher SJ, Girerd XJ, Coleman SM, Dzau VJ and Cooke JP. L-arginine improves endothelium-dependent vasodilation in hypercholesterolemic humans. J Clin Invest. 1992; 90: 1248-1253.
10. Clarkson P, Adams MR, Powe AJ, Donald AE, McCredie R, Robinson J, McCarthy SN, Keech A, Celermajer DS and Deanfield JE. Oral L-arginine improves endothelium-dependent dilation in hypercholesterolemic young adults. J Clin Invest. 1996; 97: 1989-1994.
11. Adams MR, McCredie R, Jessup W, Robinson J, Sullivan D and Celermajer DS. Oral L-arginine improves endotheliumdependent dilatation and reduces monocyte adhesion to endothelial cells in young men with coronary artery disease. Atherosclerosis. 1997; 129: 261-269.
12. Boger RH, Bode-Boger SM, Thiele W, Creutzig A, Alexander K and Frolich JC. Restoring vascular nitric oxide formation by Larginine improves the symptoms of intermittent claudication in patients with peripheral arterial occlusive disease. J Am Coll Cardiol. 1998; 32: 1336-1344.
13. Sydow K, Schwedhelm E, Arakawa N, Bode-Boger SM, Tsikas D, Hornig B, Frolich JC and Boger RH. ADMA and oxidative stress are responsible for endothelial dysfunction in hyperhomocyst(e)inemia: effects of L-arginine and B vitamins. Cardiovasc Res. 2003; 57: 244-252.
14. Palloshi A, Fragasso G, Piatti P, Monti LD, Setola E, Valsecchi G, Galluccio E, Chierchia SL and Margonato A. Effect of oral Larginine on blood pressure and symptoms and endothelial function in patients with systemic hypertension, positive exercise tests, and normal coronary arteries. Am J Cardiol. 2004; 93: 933-935.
15. Dong JY, Qin LQ, Zhang Z, Zhao Y, Wang J, Arigoni F and Zhang W. Effect of oral L-arginine supplementation on blood pressure: a meta-analysis of randomized, double-blind, placebocontrolled trials. Am Heart J. 2011; 162: 959-965.
16. Wennmalm A, Edlund A, Granstrom EF and Wiklund O. Acute supplementation with the nitric oxide precursor L-arginine does not improve cardiovascular performance in patients with hypercholesterolemia. Atherosclerosis. 1995; 118: 223-231.
17. Chin-Dusting JP, Alexander CT, Arnold PJ, Hodgson WC, Lux AS and Jennings GL. Effects of in vivo and in vitro L-arginine supplementation on healthy human vessels. J Cardiovasc Pharmacol. 1996; 28: 158-166.
18. Blum A, Hathaway L, Mincemoyer R, Schenke WH, Kirby M, Csako G, Waclawiw MA, Panza JA and Cannon RO III. Oral Larginine in patients with coronary artery disease on medical management. Circulation. 2000; 101: 2160-2164.
19. Oomen CM, van Erk MJ, Feskens EJ, Kok FJ and Kromhout D. Arginine intake and risk of coronary heart disease mortality in elderly men. Arterioscler Thromb Vasc Biol. 2000; 20: 2134-2139.
20. Alvares TS, Conte-Junior CA, Silva JT and Paschoalin VM. Acute L-Arginine supplementation does not increase nitric oxide production in healthy subjects. Nutr Metab (Lond). 2012; 9: 54.
21. Chen J, Kuhlencordt P, Urano F, Ichinose H, Astern J and Huang PL. Effects of chronic treatment with L-arginine on atherosclerosis in apoE knockout and apoE/inducible NO synthase double-knockout mice. Arterioscler Thromb Vasc Biol. 2003; 23: 97-103.
22. Schulman SP, Becker LC, Kass DA, Champion HC, Terrin ML, Forman S, Ernst KV, Kelemen MD, Townsend SN, Capriotti A, Hare JM and Gerstenblith G. L-arginine therapy in acute myocardial infarction: the Vascular Interaction With Age in Myocardial Infarction (VINTAGE MI) randomized clinical trial. JAMA. 2006; 295: 58-64.
23. Wilson AM, Harada R, Nair N, Balasubramanian N and Cooke JP. L-arginine supplementation in peripheral arterial disease: no benefit and possible harm. Circulation. 2007; 116: 188-195.
24. Scalera F, Closs EI, Flick E, Martens-Lobenhoffer J, Boissel JP, Lendeckel U, Heimburg A and Bode-Boger SM. Paradoxical effect of L-arginine: acceleration of endothelial cell senescence. Biochem Biophys Res Commun. 2009; 386: 650-655.
25. Yepuri G, Velagapudi S, Xiong Y, Rajapakse AG, Montani JP, Ming XF and Yang Z. Positive crosstalk between arginase-II and S6K1 in vascular endothelial inflammation and aging. Aging Cell. 2012; 11: 1005-1016.
26. Bonfils G, Jaquenoud M, Bontron S, Ostrowicz C, Ungermann C and De VC. Leucyl-tRNA Synthetase Controls TORC1 via the EGO Complex. Mol Cell. 2012; 46: 105-110.
27. Han JM, Jeong SJ, Park MC, Kim G, Kwon NH, Kim HK, Ha SH, Ryu SH and Kim S. Leucyl-tRNA Synthetase Is an Intracellular Leucine Sensor for the mTORC1-Signaling Pathway. Cell. 2012; 149: 410-424.
28. Yang Z and Ming XF. Arginase: the emerging therapeutic target for vascular oxidative stress and inflammation. Front Immunol. 2013; 4: 149.
29. Ming XF, Barandier C, Viswambharan H, Kwak BR, Mach F, Mazzolai L, Hayoz D, Ruffieux J, Rusconi S, Montani JP and Yang Z. Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation. 2004; 110: 3708-3714.
30. Ming XF, Rajapakse AG, Yepuri G, Xiong Y, Carvas JM, Ruffieux J, Scerri I, Wu Z, Popp K, Li J, Sartori C, Scherrer U, Kwak BR, Montani JP and Yang Z. Arginase II Promotes Macrophage Inflammatory Responses Through Mitochondrial Reactive Oxygen Species, Contributing to Insulin Resistance and Atherogenesis. J Am Heart Assoc. 2012; 1:e000992.
31. Xiong Y, Yu Y, Montani JP, Yang Z and Ming XF. Arginase-II Induces Vascular Smooth Muscle Cell Senescence and Apoptosis Through p66Shc and p53 Independently of Its l-Arginine Ureahydrolase Activity: Implications for Atherosclerotic Plaque Vulnerability. J Am Heart Assoc. 2013; 2:e000096.
32. Grody WW, Argyle C, Kern RM, Dizikes GJ, Spector EB, Strickland AD, Klein D and Cederbaum SD. Differential expression of the two human arginase genes in hyperargininemia. Enzymatic, pathologic, and molecular analysis. J Clin Invest. 1989; 83: 602-609.
33. Efeyan A, Zoncu R and Sabatini DM. Amino acids and mTORC1: from lysosomes to disease. Trends Mol Med. 2012; 18: 524-533.
34. Demidenko ZN, Zubova SG, Bukreeva EI, Pospelov VA, Pospelova TV and Blagosklonny MV. Rapamycin decelerates cellular senescence. Cell Cycle. 2009; 8: 1888-1895.
35. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV and Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging. 2010; 2: 344-352.
36. Kolesnichenko M, Hong L, Liao R, Vogt PK and Sun P. Attenuation of TORC1 signaling delays replicative and oncogenic RAS-induced senescence. Cell Cycle. 2012; 11: 2391-2401.
37. Nakano M, Nakashima A, Nagano T, Ishikawa S, Kikkawa U and Kamada S. Branched-chain amino acids enhance premature senescence through mammalian target of rapamycin complex Imediated upregulation of p21 protein. PloS One. 2013; 8:e80411.
38. Luo Y, Li L, Zou P, Wang J, Shao L, Zhou D and Liu L. Rapamycin enhances long-term hematopoietic reconstitution of ex vivo expanded mouse hematopoietic stem cells by inhibiting senescence. Transplantation. 2014; 97: 20-29.
39. Leontieva OV, Demidenko ZN and Blagosklonny MV. S6K in geroconversion. Cell Cycle. 2013; 12: 3249-3252.
40. Hallemeesch MM, Lamers WH and Deutz NE. Reduced arginine availability and nitric oxide production. Clin Nutr. 2002; 21: 273-279.
41. Hardy TA and May JM. Coordinate regulation of L-arginine uptake and nitric oxide synthase activity in cultured endothelial cells. Free Radic Res Commun. 2002; 32: 122-131.
42. Rajapakse NW and Mattson DL. Role of L-arginine in nitric oxide production in health and hypertension. Clin Exp Pharmacol Physiol. 2009; 36: 249-255.
43. Shin S, Mohan S and Fung HL. Intracellular L-arginine concentration does not determine NO production in endothelial cells: implications on the "L-arginine paradox". Biochem Biophys Res Commun. 2011; 414: 660-663.
44. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK and Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature. 2007; 450: 736-740.
45. Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Liu Y and Zheng P. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med. 2008; 205: 2397-2408.
46. Mohan S, Wu CC, Shin S and Fung HL. Continuous exposure to L-arginine induces oxidative stress and physiological tolerance in cultured human endothelial cells. Amino acids. 2012; 43: 1179-1188.
47. Elms S, Chen F, Wang Y, Qian J, Askari B, Yu Y, Pandey D, Iddings J, Caldwell RB and Fulton DJ. Insights into the arginine paradox: evidence against the importance of subcellular location of arginase and eNOS. Am J Physiol Heart Circ Physiol. 2013; 305:H651-H666.
48. Ming XF, Rajapakse AG, Carvas JM, Ruffieux J and Yang Z. Inhibition of S6K1 accounts partially for the anti-inflammatory effects of the arginase inhibitor L-norvaline. BMC Cardiovasc Disord. 2009; 9: 12.
49. Fallaux FJ, Kranenburg O, Cramer SJ, Houweling A, van OH, Hoeben RC and van Der Eb AJ. Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther. 1996; 7: 215-222.
50. Ming XF, Viswambharan H, Barandier C, Ruffieux J, Kaibuchi K, Rusconi S and Yang ZH. Rho GTPase/Rho kinase negatively regulates endothelial nitric oxide synthase phosphorylation through the inhibition of protein kinase B/Akt in human endothelial cells. Mol Cell Biol. 2002; 22: 8467-8477.