Ascorbic acid or L-arginine improves cutaneous microvascular function in chronic kidney disease

Journal of Applied Physiology

Volumn 111, Issue 6, 2011, Pages 1561-1567

  DuPont, Jennifer J ^a   Farquhar, William B ^a   Townsend, Raymond R ^b   Edwards, David G ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Nitric oxide; Oxidative stress; Skin blood flow

Indexed keywords

ARGININE; ASCORBIC ACID; DRUG DERIVATIVE; N,N DIMETHYLARGININE; N,N-DIMETHYLARGININE; NITRIC OXIDE;

ADULT; ARTICLE; CASE CONTROL STUDY; CHRONIC KIDNEY FAILURE; DRUG EFFECT; FEMALE; HEAT; HUMAN; MALE; MICROCIRCULATION; MICRODIALYSIS; MIDDLE AGED; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; SKIN; VASCULARIZATION; VASODILATATION;

ADULT; ARGININE; ASCORBIC ACID; CASE-CONTROL STUDIES; FEMALE; HOT TEMPERATURE; HUMANS; MALE; MICROCIRCULATION; MICRODIALYSIS; MIDDLE AGED; NITRIC OXIDE; OXIDATIVE STRESS; RENAL INSUFFICIENCY, CHRONIC; SKIN; VASODILATION;

EID: 83655191537     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00419.2011     Document Type: Article

References (52)

1. Abularrage CJ, Sidawy AN, Aidinian G, Singh N, Weiswasser JM, Arora S. Evaluation of the microcirculation in vascular disease. J Vasc Surg 42: 574-581, 2005. (Pubitemid 41323857)
2. Alp NJ, Channon KM. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 24: 413-420, 2004. (Pubitemid 38326132)
3. Annuk M, Lind L, Linde T, Fellstrom B. Impaired endotheliumdependent vasodilation in renal failure in humans. Nephrol Dial Transplant 16: 302-306, 2001. (Pubitemid 32123918)
4. Arellano-Mendoza MG, Vargas-Robles H, Del Valle-Mondragon L, Rios A, Escalante B. Prevention of renal injury and endothelial dysfunction by chronic L-arginine and antioxidant treatment. Ren Fail 33: 47-53, 2011.
5. Baylis C. Arginine, arginine analogs, and nitric oxide production in chronic kidney disease. Nat Clin Pract Nephrol 2: 209-220, 2006. (Pubitemid 43787287)
6. Berkowitz DE, White R, Li D, Minhas KM, Cernetich A, Kim S, Burke S, Shoukas AA, Nyhan D, Champion HC, Hare JM. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 108: 2000-2006, 2003. (Pubitemid 37296546)
7. Cohuet G, Struijker-Boudier H. Mechanisms of target organ damage caused by hypertension: therapeutic potential. Pharmacol Ther 111: 81-98, 2006. (Pubitemid 43765539)
8. Cross JM, Donald AE, Nuttall SL, Deanfield JE, Woolfson RG, MacAllister RJ. Vitamin C improves resistance but not conduit artery endothelial function in patients with chronic renal failure. Kidney Int 63: 1433-1442, 2003. (Pubitemid 36350008)
9. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol 34: 906-911, 2007. (Pubitemid 47083958)
10. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714, 2006.
11. Ghiadoni L, Cupisti A, Huang Y, Mattei P, Cardinal H, Favilla S, Rindi P, Barsotti G, Taddei S, Salvetti A. Endothelial dysfunction and oxidative stress in chronic renal failure. J Nephrol 17: 512-519, 2004. (Pubitemid 39302878)
12. Heller R, Unbehaun A, Schellenberg B, Mayer B, Werner-Felmayer G, Werner ER. L-ascorbic acid potentiates endothelial nitric oxide synthesis via a chemical stabilization of tetrahydrobiopterin. J Biol Chem 276: 40-47, 2001. (Pubitemid 32050286)
13. Holowatz LA, Kenney WL. Local ascorbate administration augments NO-and non-NO-dependent reflex cutaneous vasodilation in hypertensive humans. Am J Physiol Heart Circ Physiol 293: H1090-H1096, 2007. (Pubitemid 47254209)
14. Holowatz LA, Kenney WL. Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilatation in hypertensive humans. J Physiol 581: 863-872, 2007. (Pubitemid 46831778)
15. Holowatz LA, Santhanam L, Webb A, Berkowitz DE, Kenney WL. Oral atorvastatin therapy restores cutaneous microvascular function by decreasing arginase activity in hypercholesterolaemic humans. J Physiol 589: 2011.
16. Holowatz LA, Thompson-Torgerson CS, Kenney WL. The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 105: 370-372, 2008.
17. Holowatz LA, Thompson CS, Kenney WL. Acute ascorbate supplementation alone or combined with arginase inhibition augments reflex cutaneous vasodilation in aged human skin. Am J Physiol Heart Circ Physiol 291: H2965-H2970, 2006. (Pubitemid 44911034)
18. Holowatz LA, Thompson CS, Kenney WL. L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin. J Physiol 574: 573-581, 2006.
19. Houghton BL, Holowatz LA, Minson CT. Influence of progestin bioactivity on cutaneous vascular responses to passive heating. Med Sci Sports Exerc 37: 45-51, 2005. (Pubitemid 40076014)
20. Huynh NN, Andrews KL, Head GA, Khong SM, Mayorov DN, Murphy AJ, Lambert G, Kiriazis H, Xu Q, Du XJ, Chin-Dusting JP. Arginase II knockout mouse displays a hypertensive phenotype despite a decreased vasoconstrictory profile. Hypertension 54: 294-301, 2009.
21. Kellogg DL Jr, Liu Y, Kosiba IF, O'Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol 86: 1185-1190, 1999. (Pubitemid 29172150)
22. Kellogg DL Jr, Zhao JL, Wu Y. Endothelial nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo. Am J Physiol Heart Circ Physiol 295: H123-H129, 2008.
23. Kellogg DL Jr, Zhao JL, Wu Y. Neuronal nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo. J Physiol 586: 847-857, 2008. (Pubitemid 351194122)
24. Kim JH, Bugaj LJ, Oh YJ, Bivalacqua TJ, Ryoo S, Soucy KG, Santhanam L, Webb A, Camara A, Sikka G, Nyhan D, Shoukas AA, Ilies M, Christianson DW, Champion HC, Berkowitz DE. Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J Appl Physiol 107: 1249-1257, 2009.
25. Leiper J, Murray-Rust J, McDonald N, Vallance P. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc Natl Acad Sci USA 99: 13527-13532, 2002. (Pubitemid 35215415)
26. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Ann Intern Med 130: 461-470, 1999. (Pubitemid 29135798)
27. Levy BI, Ambrosio G, Pries AR, Struijker-Boudier HA. Microcirculation in hypertension: a new target for treatment? Circulation 104: 735-740, 2001. (Pubitemid 32738532)
28. Locatelli F, Marcelli D, Conte F, D'Amico M, Del Vecchio L, Limido A, Malberti F, Spotti D. Cardiovascular disease in chronic renal failure: The challenge continues. Nephrol Dial Transplant 15: 69-80, 2000.
29. Massy ZA, Borderie D, Nguyen-Khoa T, Drüeke TB, Ekindjian OG, Lacour B. Increased plasma S-nitrosothiol levels in chronic haemodialysis patients. Nephrol Dial Transplant 18: 153-157, 2003. (Pubitemid 36104492)
30. Minson CT, Berry LT, Joyner MJ. Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91: 1619-1626, 2001. (Pubitemid 32900352)
31. Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW. Decreased nitric oxide-and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol 93: 1644-1649, 2002. (Pubitemid 36082975)
32. Morris ST, McMurray JJ, Rodger RS, Jardine AG. Impaired endothelium-dependent vasodilation in uremia. Nephrol Dial Transplant 15: 1194-1200, 2000.
33. Oberg BP, McMenamin E, Lucas FL, McMonagle E, Morrow J, Ikizler TA, Himmelfarb J. Increased prevalance of oxidant stress and inflammation in patients with moderate to severe chronic kidney disease. Kidney Int 65: 1009-1016, 2004. (Pubitemid 38251077)
34. Ochodnicky P, Vettoretti S, Henning R, Buikema H, Van Dokkum R, de Zeeuw D. Endothelial dysfunction in chronic kidney disease: determinant of susceptibility to end-organ damage and therapeutic response. J Nephrol 19: 246-258, 2006. (Pubitemid 46785535)
35. Ramos LF, Shintani A, Ikizler TA, Himmelfarb J. Oxidative stress and inflammation are associated with adiposity in moderate to severe CKD. J Am Soc Nephrol 19: 593-599, 2008. (Pubitemid 351355403)
36. Rossi M, Carpi A, Galetta F, Franzoni F, Santoro G. The investigation of skin blood flowmotion: a new approach to study the microcirculatory impairment in vascular diseases? Biomed Pharmacother 60: 437-442, 2006.
37. Santhanam L, Lim HK, Lim HK, Miriel V, Brown T, Patel M, Balanson S, Ryoo S, Anderson M, Irani K, Khanday F, Di Costanzo L, Nyhan D, Hare JM, Christianson DW, Rivers R, Shoukas A, Berkowitz DE. Inducible NO synthase dependent S-nitrosylation and activation of arginase1 contribute to age-related endothelial dysfunction. Circ Res 101: 692-702, 2007. (Pubitemid 47494100)
38. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, Parfrey P, Pfeffer M, Raij L, Spinosa DJ, Wilson PW. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Hypertension 42: 1050-1065, 2003. (Pubitemid 37413751)
39. Schiffrin EL, Lipman ML, JFEM. Chronic kidney disease: effects on the cardiovascular system. Circulation 116: 85-97, 2007. (Pubitemid 47016250)
40. Segal MS, Baylis C, Johnson RJ. Endothelial health and diversity in the kidney. J Am Soc Nephrol 17: 323-324, 2006.
41. Shilpak MG, Fried LF, Cushman M, Manolio TA, Peterson D, Stehman-Breen C, Bleyer A, Newman A, Siscovick D, Psaty B. Cardiovascular mortality risk in chronic kidney disease. JAMA 293: 1737-1745, 2005.
42. Sibal L, Agarwal SC, Home PD, Boger RH. The role of asymmetric dimethylarginine (ADMA) in endothelial dysfunction and cardiovascular disease. Curr Cardiol Rev 6: 82-90, 2010.
43. Stewart JM, Kohen A, Brouder D, Rahim F, Adler S, Garrick R, Goligorsky MS. Noninvasive interrogation of microvasculature for signs of endothelial dysfunction in patients with chronic renal failure. Am J Physiol Heart Circ Physiol 287: H2687-H2696, 2004. (Pubitemid 39557141)
44. Stewart JM, Medow MS, Minson CT, Taneja I. Cutaneous neuronal nitric oxide is specifically decreased in postural tachycardia syndrome. Am J Physiol Heart Circ Physiol 293: H2161-H2167, 2007. (Pubitemid 47605858)
45. Strom NA, Sawyer JR, Roberts SR, Kingsley-Berg SM. Local sensory nerve control of skin blood flow during local warming in type 2 diabetes mellitus. J Appl Physiol 108: 293-297, 2010.
46. Sydow K, Munzel T. ADMA and oxidative stress. Atherosclerosis S4: 41-51, 2003. (Pubitemid 38234494)
47. Torgrimson BT, Meendering JR, Kaplan PF, Minson CT. Endothelial function across an oral contraceptive cycle in women using levonorgestrel and ethinyl estradiol. Am J Physiol Heart Circ Physiol 288: H103-H110, 2005.
48. Vallance P, Leiper J. Cardiovascular biology of the asymmetric dimethylarginine: dimethylarginine dimethylaminohydrolase pathyway. Arterioscler Thromb Vasc Biol 24: 1023-1030, 2004. (Pubitemid 38737826)
49. Vallance P, Leone A, Calver A, Collier J, Moncada S. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339: 572-576, 1992.
50. Yamamizu K, Shinozaki K, Ayajiki K, Gemba M, Okamura T. Oral administration of both tetrahydrobiopterin and L-arginine prevents endothelial dysfunction in rats with chronic renal failure. J Cardiovasc Pharmacol 49: 131-139, 2007. (Pubitemid 46579946)
51. Yilmaz MI, Saglam M, Caglar K, Cakir E, Sonmez A, Ozgurtas T, Aydin A, Eyileten T, Ozcan O, Acikel C, Tasar M, Genctoy G, Erbil K, Vural A, Zoccali C. The determinants of endothelial dysfunction in CKD: oxidative stress and asymmetric dimethylarginine. Am J Kidney Dis 47: 42-50, 2006. (Pubitemid 41828265)
52. Young JM, Terrin N, Wang X, Greene T, Beck GJ, Kusek JW, Collins AJ, Sarnak MJ, Menon V. Asymmetric dimethylarginine in stages 3 to 4 chronic kidney disease. Clin J Am Soc Nephrol 4: 1115-1120, 2009.