1,25(OH) 2 D 3 inhibits oxidative stress and monocyte adhesion by mediating the upregulation of GCLC and GSH in endothelial cells treated with acetoacetate (ketosis)

Journal of Steroid Biochemistry and Molecular Biology

Volumn 159, Issue , 2016, Pages 94-101

  Kanikarla Marie, Preeti ^a   Jain, Sushil K ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

1,25(OH)2D3; Endothelium; Ketones; Oxidative stress; Type 1 diabetes; Vitamin D

Indexed keywords

ACETOACETIC ACID; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE CYSTEINE LIGASE CATALYTIC SUBUNIT; GLUTATHIONE; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VITAMIN D; VITAMIN D RECEPTOR; ACETOACETIC ACID DERIVATIVE; CALCITRIOL; CALCITRIOL RECEPTOR; CYTOKINE; GCLC PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG MECHANISM; ENDOTHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; KETOACIDOSIS; MONOCYTE; OXIDATIVE STRESS; PROTEIN EXPRESSION; UMBILICAL VEIN ENDOTHELIAL CELL; CELL LINE; GENETICS; METABOLISM; PRECLINICAL STUDY; UPREGULATION;

ACETOACETATES; CALCITRIOL; CELL ADHESION; CELL LINE; CYTOKINES; DRUG EVALUATION, PRECLINICAL; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; KETOSIS; MONOCYTES; OXIDATIVE STRESS; RECEPTORS, CALCITRIOL; UP-REGULATION;

EID: 84961124995     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2016.03.002     Document Type: Article

References (61)

1. R.M. Daly, C. Gagnon, Z.X. Lu, D.J. Magliano, D.W. Dunstan, K.A. Sikaris, P.Z. Zimmet, P.R. Ebeling, and J.E. Shaw Prevalence of vitamin D deficiency and its determinants in Australian adults aged 25 years and older: a national population-based study Clin. Endocrinol. (Oxf.) 77 2012 26 35
2. F. Farrokhyar, R. Tabasinejad, D. Dao, D. Peterson, O.R. Ayeni, R. Hadioonzadeh, and M. Bhandari Prevalence of vitamin D inadequacy in athletes: a systematic-review and meta-analysis Sports Med. 45 2015 365 378
3. K.Y. Forrest, and W.L. Stuhldreher Prevalence and correlates of vitamin D deficiency in US adults Nutr. Res. 31 2011 48 54
4. M.F. Holick Vitamin D deficiency N. Engl. J. Med. 357 2007 266 281
5. M.M. Alvarez, A.C. Reiff e Vieira, R.R. Luiz, and G.V. da Veiga Validation of capillary glycemia as a strategy for the screening of diabetes mellitus in adolescents Pediatr. Diabetes 10 2009 449 454
6. C. Mathieu, C. Gysemans, A. Giulietti, and R. Bouillon Vitamin D and diabetes Diabetologia 48 2005 1247 1257
7. C. Mathieu, and K. Badenhoop Vitamin D and type 1 diabetes mellitus: state of the art Trends Endocrinol. Metab. 16 2005 261 266
8. P. Anagnostis, V.G. Athyros, F. Adamidou, M. Florentin, and A. Karagiannis Vitamin D and cardiovascular disease: a novel agent for reducing cardiovascular risk? Curr. Vasc. Pharmacol. 8 2010 720 730
9. A.E. Riek, J. Oh, J.E. Sprague, A. Timpson, L. de las Fuentes, L. Bernal-Mizrachi, K.B. Schechtman, and C. Bernal-Mizrachi Vitamin D suppression of endoplasmic reticulum stress promotes an anti-atherogenic monocyte/macrophage phenotype in type 2 diabetic patients J. Biol. Chem 2012
10. G. Targher, L. Bertolini, R. Padovani, L. Zenari, L. Scala, M. Cigolini, and G. Arcaro Serum 25-hydroxyvitamin D3 concentrations and carotid artery intima-media thickness among type 2 diabetic patients Clin. Endocrinol. (Oxf.) 65 2006 593 597
11. S. Weng, J.E. Sprague, J. Oh, A.E. Riek, K. Chin, M. Garcia, and C. Bernal-Mizrachi Vitamin D deficiency induces high blood pressure and accelerates atherosclerosis in mice PLoS One 8 2013 e54625
12. K.L. Jablonski, M. Chonchol, G.L. Pierce, A.E. Walker, and D.R. Seals 25-Hydroxyvitamin D deficiency is associated with inflammation-linked vascular endothelial dysfunction in middle-aged and older adults Hypertension 57 2011 63 69
13. I. Mozos, and O. Marginean Links between Vitamin D deficiency and cardiovascular diseases BioMed. Res. Int. 2015 2015 109275
14. S.F. Chen 1 alpha, 25-Dihydroxyvitamin D3 decreased ICAM-1 and ELAM-1 expressions on pulmonary microvascular endothelial cells and neutrophil motivation J. Steroid Biochem. Mol. Biol. 52 1995 67 70
15. Y. Suzuki, T. Ichiyama, A. Ohsaki, S. Hasegawa, M. Shiraishi, and S. Furukawa Anti-inflammatory effect of 1alpha,25-dihydroxyvitamin D(3) in human coronary arterial endothelial cells: Implication for the treatment of Kawasaki disease J. Steroid Biochem. Mol. Biol. 113 2009 134 138
16. S.I. Sokol, V. Srinivas, J.P. Crandall, M. Kim, G. Tellides, A.H. Lebastchi, Y. Yu, A.K. Gupta, and M.H. Alderman The effects of vitamin D repletion on endothelial function and inflammation in patients with coronary artery disease Vasc. Med. (London, England) 17 2012 394 404
17. J.A. Sugden, J.I. Davies, M.D. Witham, A.D. Morris, and A.D. Struthers Vitamin D improves endothelial function in patients with Type 2 diabetes mellitus and low vitamin D levels Diabetic Med.: J. Br. Diabetic Assoc. 25 2008 320 325
18. M.D. Witham, F.J. Dove, J.A. Sugden, A.S. Doney, and A.D. Struthers The effect of vitamin D replacement on markers of vascular health in stroke patients - a randomised controlled trial Nutr. Metab. Cardiovasc. Dis.: NMCD 22 2012 864 870
19. M. Martinesi, C. Treves, G. d'Albasio, S. Bagnoli, A.G. Bonanomi, and M. Stio Vitamin D derivatives induce apoptosis and downregulate ICAM-1 levels in peripheral blood mononuclear cells of inflammatory bowel disease patients Inflamm. Bowel Dis. 14 2008 597 604
20. K. Kudo, S. Hasegawa, Y. Suzuki, R. Hirano, H. Wakiguchi, S. Kittaka, and T. Ichiyama 1alpha 25-Dihydroxyvitamin D(3) inhibits vascular cellular adhesion molecule-1 expression and interleukin-8 production in human coronary arterial endothelial cells J. Steroid Biochem. Mol. Biol. 132 2012 290 294
21. A. Giulietti, E. van Etten, L. Overbergh, K. Stoffels, R. Bouillon, and C. Mathieu Monocytes from type 2 diabetic patients have a pro-inflammatory profile. 1,25-Dihydroxyvitamin D(3) works as anti-inflammatory Diabetes Res. Clin. Pract. 77 2007 47 57
22. A.E. Riek, J. Oh, and C. Bernal-Mizrachi 1,25(OH) 2 vitamin D suppresses macrophage migration and reverses atherogenic cholesterol metabolism in type 2 diabetic patients J. Steroid Biochem. Mol. Biol. 136 2013 309 312
23. H.D. Margeirsdottir, K.H. Stensaeth, J.R. Larsen, C. Brunborg, and K. Dahl-Jorgensen Early signs of atherosclerosis in diabetic children on intensive insulin treatment: a population-based study Diabetes Care 33 2010 2043 2048
24. V.K. Capellini, A.C. Celotto, C.F. Baldo, V.C. Olivon, F. Viaro, A.J. Rodrigues, and P.R. Evora Diabetes and vascular disease: basic concepts of nitric oxide physiology, endothelial dysfunction, oxidative stress and therapeutic possibilities Curr. Vasc. Pharmacol. 8 2009 526 544
25. Z. Fatehi-Hassanabad, C.B. Chan, and B.L. Furman Reactive oxygen species and endothelial function in diabetes Eur. J. Pharmacol. 636 2010 8 17
26. F. Giacco, and M. Brownlee Oxidative stress and diabetic complications Circ. Res. 107 2010 1058 1070
27. Y. Levy, S. Blum, and A.P. Levy Antioxidants in the prevention of atherosclerosis: the importance of proper patient selection Clin. Nutr. 28 2009 581 582
28. I.A. van den Oever, H.G. Raterman, M.T. Nurmohamed, and S. Simsek Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus Mediators Inflamm. 2010 2010 792393
29. Y.W. Lee, P.H. Kim, W.H. Lee, and A.A. Hirani Interleukin-4, oxidative stress, vascular inflammation and atherosclerosis Biomol. Ther. (Seoul) 18 2010 135 144
30. S.K. Jain, K. Kannan, and R. McVie Effect of hyperketonemia on blood monocytes in type-I diabetic patients and apoptosis in cultured U937 monocytes Antioxid. Redox Signal. 1 1999 211 220
31. S.K. Jain, K. Kannan, and G. Lim Ketosis (acetoacetate) can generate oxygen radicals and cause increased lipid peroxidation and growth inhibition in human endothelial cells Free Radic. Biol. Med. 25 1998 1083 1088
32. J.L. Rains, and S.K. Jain Hyperketonemia increases monocyte adhesion to endothelial cells and is mediated by LFA-1 expression in monocytes and ICAM-1 expression in endothelial cells Am. J. Physiol. Endocrinol. Metab. 301 2011 E298 306
33. W.H. Hoffman, C. Cheng, G.G. Passmore, J.E. Carroll, and D. Hess Acetoacetate increases expression of intercellular adhesion molecule-1 (ICAM-1) in human brain microvascular endothelial cells Neurosci. Lett. 334 2002 71 74
34. P. Kanikarla-Marie, and S.K. Jain Hyperketonemia (acetoacetate) upregulates NADPH oxidase 4 and elevates oxidative stress, icam-1, and monocyte adhesivity in endothelial cells Cell Physiol. Biochem. 35 2015 364 373
35. P. Manna, and S.K. Jain Effect of PIP3 on adhesion molecules and adhesion of THP-1 monocytes to HUVEC treated with high glucose Cell Physiol. Biochem. 33 2014 1197 1204
36. P. Manna, and S.K. Jain Vitamin D up-regulates glucose transporter 4 (GLUT4) translocation and glucose utilization mediated by cystathionine-{gamma}-lyase (CSE) activation and H2S formation in 3T3L1 adipocytes J. Biol. Chem. 287 2012 42324 42332
37. P. Kanikarla-Marie, and S.K. Jain L-Cysteine supplementation reduces high-glucose and ketone-induced adhesion of monocytes to endothelial cells by inhibiting ROS Mol. Cell. Biochem. 391 2014 251 256
38. C.M. Pfeiffer, D.L. Huff, and E.W. Gunter Rapid and accurate HPLC assay for plasma total homocysteine and cysteine in a clinical laboratory setting Clin. Chem. 45 1999 290 292
39. S.K. Jain, and D. Micinski Vitamin D upregulates glutamate cysteine ligase and glutathione reductase, and GSH formation and decreases ROS and MCP-1 and IL-8 secretion in high-glucose exposed U937 monocytes Biochem. Biophys. Res. Commun. 437 2013 7 11
40. L. Laffel Ketone bodies: a review of physiology, pathophysiology and application of monitoring to diabetes Diabetes Metab. Res. Rev. 15 1999 412 426
41. J.L. Rains, and S.K. Jain Effect of hyperketonemia (Acetoacetate) on nuclear factor-kappaB and p38 mitogen-activated protein kinase activation mediated intercellular adhesion molecule 1 upregulation in endothelial cells Metab. Syndr. Relat. Disord. 13 2015 71 77
42. J.L. Rains, P. Kanikarla-Marie, and S.K. Jain Hyperketonemia induces upregulation of LFA-1 in monocytes, which is mediated by ROS and P38 MAPK activation Can. J. Physiol. Pharmacol. 90 2012 1642 1646
43. J.E. Harrison, and F.A. Saeed Acetoacetate is an electron donor to myeloperoxidase and a promoter of myeloperoxidase-catalyzed fatty acid peroxidation Biochem. Med. 26 1981 339 355
44. M.A. Abdelmegeed, S.K. Kim, K.J. Woodcroft, and R.F. Novak Acetoacetate activation of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in primary cultured rat hepatocytes: role of oxidative stress J. Pharmacol. Exp. Ther. 310 2004 728 736
45. T. Zitman-Gal, E. Golan, J. Green, J. Bernheim, and S. Benchetrit Vitamin D receptor activation in a diabetic-like environment: potential role in the activity of the endothelial pro-inflammatory and thioredoxin pathways J. Steroid Biochem. Mol. Biol. 132 2012 1 7
46. S.C. Lu Glutathione synthesis Biochim. Biophys. Acta 1830 2013 3143 3153
47. J.A. Colwell, M. Lopes-Virella, and P.V. Halushka Pathogenesis of atherosclerosis in diabetes mellitus Diabetes Care 4 1981 121 133
48. A.E. Vendrov, Z.S. Hakim, N.R. Madamanchi, M. Rojas, C. Madamanchi, and M.S. Runge Atherosclerosis is attenuated by limiting superoxide generation in both macrophages and vessel wall cells Arterioscler. Thromb. Vasc. Biol. 27 2007 2714 2721
49. S. Blankenberg, S. Barbaux, and L. Tiret Adhesion molecules and atherosclerosis Atherosclerosis 170 2003 191 203
50. A. Tedgui, and Z. Mallat Cytokines in atherosclerosis: pathogenic and regulatory pathways Physiol. Rev. 86 2006 515 581
51. D. Steinberg The LDL modification hypothesis of atherogenesis: an update J Lipid Res 50 Suppl 2009 S376 S381
52. S.K. Jain, R. McVie, and J.A. Bocchini Jr. Hyperketonemia (ketosis), oxidative stress and type 1 diabetes Pathophysiology 13 2006 163 170
53. M.L. Marcovecchio, and F. Chiarelli Microvascular disease in children and adolescents with type 1 diabetes and obesity Pediatr. Nephrol. 26 2010 365 375
54. P. Manna, N. Gungor, R. McVie, and S.K. Jain Decreased cystathionine-gamma-lyase (CSE) activity in livers of type 1 diabetic rats and peripheral blood mononuclear cells (PBMC) of type 1 diabetic patients J. Biol. Chem. 289 2014 11767 11778
55. C.H. Lee, Y.S. Shieh, F.C. Hsiao, F.C. Kuo, C.Y. Lin, C.H. Hsieh, and Y.J. Hung High glucose induces human endothelial dysfunction through an axl-dependent mechanism Cardiovasc. Diabetol. 13 2014 53
56. R. Piga, Y. Naito, S. Kokura, O. Handa, and T. Yoshikawa Short-term high glucose exposure induces monocyte-endothelial cells adhesion and transmigration by increasing VCAM-1 and MCP-1 expression in human aortic endothelial cells Atherosclerosis 193 2007 328 334
57. J.A. Ford, G.S. MacLennan, A. Avenell, M. Bolland, A. Grey, and M. Witham Cardiovascular disease and vitamin D supplementation: trial analysis, systematic review, and meta-analysis Am. J. Clin. Nutr. 100 2014 746 755
58. T.E. Close, G. Cepinskas, T. Omatsu, K.L. Rose, K. Summers, E.K. Patterson, and D.D. Fraser Diabetic ketoacidosis elicits systemic inflammation associated with cerebrovascular endothelial cell dysfunction Microcirculation 20 2013 534 543
59. S.K. Jain, K. Kannan, G. Lim, J. Matthews-Greer, R. McVie, and J.A. Bocchini Jr. Elevated blood interleukin-6 levels in hyperketonemic type 1 diabetic patients and secretion by acetoacetate-treated cultured U937 monocytes Diabetes Care 26 2003 2139 2143
60. S.K. Jain, K. Kannan, G. Lim, R. McVie, and J.A. Bocchini Jr. Hyperketonemia increases tumor necrosis factor-alpha secretion in cultured U937 monocytes and Type 1 diabetic patients and is apparently mediated by oxidative stress and cAMP deficiency Diabetes 51 2002 2287 2293
61. R.V. Sekhar, S.V. McKay, S.G. Patel, A.P. Guthikonda, V.T. Reddy, A. Balasubramanyam, and F. Jahoor Glutathione synthesis is diminished in patients with uncontrolled diabetes and restored by dietary supplementation with cysteine and glycine Diabetes Care 34 2010 162 167