Vitamin D suppression of endoplasmic reticulum stress promotes an antiatherogenic monocyte/macrophage phenotype in type 2 diabetic patients

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38482-38494

  Riek, Amy E ^a   Oh, Jisu ^a   Sprague, Jennifer E ^a   Timpson, Alexandra ^a   De Las Fuentes, Lisa ^b   Bernal Mizrachi, Leon ^c   Schechtman, Kenneth B ^a   Bernal Mizrachi, Carlos ^a,b  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION MOLECULES; CARDIO-VASCULAR DISEASE; COMORBIDITY; DIABETIC PATIENT; ENDOPLASMIC RETICULUM STRESS; ENHANCER-BINDING PROTEINS; ER STRESS; HOMOLOGOUS PROTEINS; INTEGRINS; MEMBRANE RECEPTORS; MONOCYTE ADHESION; MRNA EXPRESSION; RELATIVE RISKS; TYPE 2 DIABETES MELLITUS; VITAMIN-D;

ADHESION; BODY FLUIDS; CELL MEMBRANES; DISEASES; ENDOTHELIAL CELLS; MACROPHAGES; MOLECULES; PROTEINS;

VITAMINS;

25 HYDROXYVITAMIN D; BETA1 INTEGRIN; CD18 ANTIGEN; MESSENGER RNA; P SELECTIN GLYCOPROTEIN LIGAND 1; VITAMIN D; VITAMIN D RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL METABOLISM; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MALE; MONOCYTE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VITAMIN BLOOD LEVEL;

ADULT; AGED; ANTIGENS, CD18; ANTIGENS, CD29; ATHEROSCLEROSIS; CELL ADHESION; CELL DIFFERENTIATION; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; FEMALE; HUMANS; MACROPHAGES; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; MONOCYTES; PHENOTYPE; RNA, MESSENGER; RNA, SMALL INTERFERING; VITAMIN D;

EID: 84869054252     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.386912     Document Type: Article

References (62)

1. Centers for Disease Control and Prevention (2011) National Diabetes Fact Sheet: National Estimates and General Information on Diabetes and Prediabetes in the United States, United States Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA
2. Passlick, B., Flieger, D., and Ziegler-Heitbrock, H. W. (1989) Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74, 2527-2534 (Pubitemid 19286475)
3. + monocytes in coronary artery disease and their relationship to serum TNF-α levels. Thromb. Haemost. 92, 419-424
4. Rogacev, K. S., Ulrich, C., Blömer, L., Hornof, F., Oster, K., Ziegelin, M., Cremers, B., Grenner, Y., Geisel, J., Schlitt, A., Köhler, H., Fliser, D., Girndt, M., and Heine, G. H. (2010) Monocyte heterogeneity in obesity and subclinical atherosclerosis. Eur. Heart J. 31, 369-376
5. Patiño, R., Ibarra, J., Rodriguez, A., Yagüe, M. R., Pintor, E., Fernandez- Cruz, A., and Figueredo, A. (2000) Circulating monocytes in patients with diabetes mellitus, arterial disease, and increased CD14 expression. Am. J. Cardiol. 85, 1288-1291
6. Bouhlel, M. A., Derudas, B., Rigamonti, E., Dièvart, R., Brozek, J., Haulon, S., Zawadzki, C., Jude, B., Torpier, G., Marx, N., Staels, B., and Chinetti- Gbaguidi, G. (2007) PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 6, 137-143 (Pubitemid 47189091)
7. Martinez, F. O., Helming, L., and Gordon, S. (2009) Alternative activation of macrophages. An immunologic functional perspective. Annu. Rev. Immunol. 27, 451-483
8. Bories, G., Caiazzo, R., Derudas, B., Copin, C., Raverdy, V., Pigeyre, M., Pattou, F., Staels, B., and Chinetti-Gbaguidi, G. (2012) Diabetes Vasc. Dis. Res. 9, 189-195
9. Satoh, N., Shimatsu, A., Himeno, A., Sasaki, Y., Yamakage, H., Yamada, K., Suganami, T., and Ogawa, Y. (2010) Unbalanced M1/M2 phenotype of peripheral blood monocytes in obese diabetic patients. Effect of pioglitazone. Diabetes Care 33, e7
10. Tacke, F., Alvarez, D., Kaplan, T. J., Jakubzick, C., Spanbroek, R., Llodra, J., Garin, A., Liu, J., Mack, M., van Rooijen, N., Lira, S. A., Habenicht, A. J., and Randolph, G. J. (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117, 185-194 (Pubitemid 46048465)
11. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., and Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686 (Pubitemid 39457982)
12. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35
13. Martinez, F. O., Gordon, S., Locati, M., and Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization. New molecules and patterns of gene expression. J. Immunol. 177, 7303-7311 (Pubitemid 44715100)
14. van Tits, L. J., Stienstra, R., van Lent, P. L., Netea, M. G., Joosten, L. A., and Stalenhoef, A. F. (2011) Oxidized LDL enhances pro-inflammatory responses of alternatively activated M2 macrophages. A crucial role for Krüppel-like factor 2. Atherosclerosis 214, 345-349
15. Oh, J., Riek, A. E., Weng, S., Petty, M., Kim, D., Colonna, M., Cella, M., and Bernal-Mizrachi, C. (2012) Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J. Biol. Chem. 287, 11629-11641
16. Woollard, K. J., and Geissmann, F. (2010) Monocytes in atherosclerosis. Subsets and functions. Nat. Rev. Cardiol. 7, 77-86
17. Fasching, P., Waldhausl, W., and Wagner, O. F. (1996) Elevated circulating adhesion molecules in NIDDM-potential mediators in diabetic macroangiopathy. Diabetologia 39, 1242-1244 (Pubitemid 26319954)
18. Jilma, B., Fasching, P., Ruthner, C., Rumplmayr, A., Ruzicka, S., Kapiotis, S., Wagner, O. F., and Eichler, H. G. (1996) Elevated circulating P-selectin in insulin dependent diabetes mellitus. Thromb. Haemost. 76, 328-332 (Pubitemid 26373522)
19. 2 integrin subunits in diabetes mellitus. Clin. Biochem. 42, 634-640
20. Shanmugam, N., Reddy, M. A., Guha, M., and Natarajan, R. (2003) High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 52, 1256-1264 (Pubitemid 36523365)
21. Chen, N. G., Abbasi, F., Lamendola, C., McLaughlin, T., Cooke, J. P., Tsao, P. S., and Reaven, G. M. (1999) Mononuclear cell adherence to cultured endothelium is enhanced by hypertension and insulin resistance in healthy nondiabetic volunteers. Circulation 100, 940-943 (Pubitemid 29407174)
22. Chen, N. G., Holmes, M., and Reaven, G. M. (1999) Relationship between insulin resistance, soluble adhesion molecules, and mononuclear cell binding in healthy volunteers. J. Clin. Endocrinol. Metab. 84, 3485-3489 (Pubitemid 30645195)
23. + monocytes are vulnerable and functionally impaired under endoplasmic reticulum stress in patients with type 2 diabetes. Diabetes 59, 634-643
24. Han, S., Liang, C. P., DeVries-Seimon, T., Ranalletta, M., Welch, C. L., Collins-Fletcher, K., Accili, D., Tabas, I., and Tall, A. R. (2006) Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell metabolism 3, 257-266
25. Hotamisligil, G. S. (2010) Endoplasmic reticulum stress and atherosclerosis. Nat. Med. 16, 396-399
26. Hotamisligil, G. S., and Spiegelman, B. M. (2000) Diabetes Mellitus (Le- Roith, D., Taylor, S. I., and Olefsky, J. M. eds) pp. 651-658, Lippincott Williams & Wilkins, Philadelphia, PA
27. Zhou, J., Lhoták, S., Hilditch, B. A., and Austin, R. C. (2005) Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111, 1814-1821 (Pubitemid 40525147)
28. Erbay, E., Babaev, V. R., Mayers, J. R., Makowski, L., Charles, K. N., Snitow, M. E., Fazio, S., Wiest, M. M., Watkins, S. M., Linton, M. F., and Hotamisligil, G. S. (2009) Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 15, 1383-1391
29. Tabas, I. (2010) The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ. Res. 107, 839-850
30. Pittas, A. G., Chung, M., Trikalinos, T., Mitri, J., Brendel, M., Patel, K., Lichtenstein, A. H., Lau, J., and Balk, E. M. (2010) Systematic review. Vitamin D and cardiometabolic outcomes. Ann. Intern. Med. 152, 307-314
31. Wang, L., Manson, J. E., Song, Y., and Sesso, H. D. (2010) Systematic review. Vitamin D and calcium supplementation in prevention of cardiovascular events. Ann. Intern. Med. 152, 315-323
32. Melamed, M. L., Michos, E. D., Post, W., and Astor, B. (2008) 25-Hydroxyvitamin D levels and the risk of mortality in the general population. Arch. Intern. Med. 168, 1629-1637
33. Cigolini, M., Iagulli, M. P., Miconi, V., Galiotto, M., Lombardi, S., and Targher, G. (2006) Serum 25-hydroxyvitamin D3 concentrations and prevalence of cardiovascular disease among type 2 diabetic patients. Diabetes Care 29, 722-724 (Pubitemid 44115386)
34. Isaia, G., Giorgino, R., and Adami, S. (2001) High prevalence of hypovitaminosis D in female type 2 diabetic population. Diabetes Care 24, 1496
35. Polla, B. S., Healy, A. M., Amento, E. P., and Krane, S. M. (1986) 1,25-Dihydroxyvitamin D3 maintains adherence of human monocytes and protects them from thermal injury. J. Clin. Invest. 77, 1332-1339 (Pubitemid 16047157)
36. Hewison, M., Dabrowski, M., Faulkner, L., Hughson, E., Vadher, S., Rut, A., Brickell, P. M., O'Riordan, J. L., and Katz, D. R. (1994) Transfection of vitamin D receptor cDNA into the monoblastoid cell line U937. The role of vitamin D3 in homotypic macrophage adhesion. J. Immunol. 153, 5709-5719 (Pubitemid 24377707)
37. Du, T., Zhou, Z. G., You, S., Huang, G., Lin, J., Yang, L., Li, X., Zhou, W. D., and Chao, C. (2009) Modulation of monocyte hyperresponsiveness to TLR ligands by 1,25-dihydroxy-vitamin D3 from LADA and T2DM. Diabetes Res. Clin. Pract. 83, 208-214
38. Zhang, Y., Leung, D. Y., Richers, B. N., Liu, Y., Remigio, L. K., Riches, D. W., and Goleva, E. (2012) Vitamin D inhibits monocyte/macrophage proinflammatory cytokine production by targeting MAPK phosphatase-1. J. Immunol. 188, 2127-2135
39. Dickhout, J. G., Lhotak, S., Hilditch, B. A., Basseri, S., Colgan, S. M., Lynn, E. G., Carlisle, R. E., Zhou, J., Sood, S. K., Ingram, A. J., and Austin, R. C. (2011) FASEB J. 25, 576-589
40. i-increasing agents cyclopiazonic acid and thapsigargin. J. Biol. Chem. 269, 8786-8791
41. Oh, J., Weng, S., Felton, S. K., Bhandare, S., Riek, A., Butler, B., Proctor, B. M., Petty, M., Chen, Z., Schechtman, K. B., Bernal-Mizrachi, L., and Bernal-Mizrachi, C. (2009) 1,25(OH)2 vitaminDinhibits foam cell formation and suppresses macrophage cholesterol uptake in patients with type 2 diabetes mellitus. Circulation 120, 687-698
42. Myoishi, M., Hao, H., Minamino, T., Watanabe, K., Nishihira, K., Hatakeyama, K., Asada, Y., Okada, K., Ishibashi-Ueda, H., Gabbiani, G., Bochaton- Piallat, M. L., Mochizuki, N., and Kitakaze, M. (2007) Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation 116, 1226-1233 (Pubitemid 47517533)
43. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A. H., Iwakoshi, N. N., Ozdelen, E., Tuncman, G., Görgün, C., Glimcher, L. H., and Hotamisligil, G. S. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461 (Pubitemid 39372439)
44. Nemere, I., and Farach-Carson, M. C. (1998) Membrane receptors for steroid hormones. A case for specific cell surface binding sites for vitamin D metabolites and estrogens. Biochem. Biophys. Res. Commun. 248, 443-449 (Pubitemid 28404438)
45. Adams, J. S., Ren, S., Liu, P. T., Chun, R. F., Lagishetty, V., Gombart, A. F., Borregaard, N., Modlin, R. L., and Hewison, M. (2009) Vitamin D-directed rheostatic regulation of monocyte antibacterial responses. J. Immunol. 182, 4289-4295
46. Schwende, H., Fitzke, E., Ambs, P., and Dieter, P. (1996) Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J. Leukocyte Biol. 59, 555-561 (Pubitemid 26156616)
47. Grey, A., and Bolland, M. (2010) Vitamin D. A place in the sun? Arch. Intern. Med. 170, 1099-1100
48. + monocytes are associated with subclinical atherosclerosis in renal transplant patients. Am. J. Transplant. 8, 103-110
49. Khallou-Laschet, J., Varthaman, A., Fornasa, G., Compain, C., Gaston, A. T., Clement, M., Dussiot, M., Levillain, O., Graff-Dubois, S., Nicoletti, A., and Caligiuri, G. (2010) Macrophage plasticity in experimental atherosclerosis. PLoS One 5, e8852
50. Gregor, M. F., and Hotamisligil, G. S. (2007) Thematic review series. Adipocyte Biology. Adipocyte stress. The endoplasmic reticulum and metabolic disease. J. Lipid Res. 48, 1905-1914 (Pubitemid 47360610)
51. Thorp, E., Li, G., Seimon, T. A., Kuriakose, G., Ron, D., and Tabas, I. (2009) Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab. 9, 474-481
52. Feng, B., Yao, P. M., Li, Y., Devlin, C. M., Zhang, D., Harding, H. P., Sweeney, M., Rong, J. X., Kuriakose, G., Fisher, E. A., Marks, A. R., Ron, D., and Tabas, I. (2003) The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 5, 781-792 (Pubitemid 37087166)
53. Chinetti-Gbaguidi, G., and Staels, B. (2011) Macrophage polarization in metabolic disorders. Functions and regulation. Curr. Opin. Lipidol. 22, 365-372
54. Mantovani, A., Garlanda, C., and Locati, M. (2009) Macrophage diversity and polarization in atherosclerosis. A question of balance. Arterioscler. Thromb. Vasc. Biol. 29, 1419-1423
55. Mills, C. D., Kincaid, K., Alt, J. M., Heilman, M. J., and Hill, A. M. (2000) M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164, 6166-6173 (Pubitemid 30408793)
56. Chinetti-Gbaguidi, G., Baron, M., Bouhlel, M. A., Vanhoutte, J., Copin, C., Sebti, Y., Derudas, B., Mayi, T., Bories, G., Tailleux, A., Haulon, S., Zawadzki, C., Jude, B., and Staels, B. (2011) Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways. Circ. Res. 108, 985-995
57. Szeto, F. L., Reardon, C. A., Yoon, D., Wang, Y., Wong, K. E., Chen, Y., Kong, J., Liu, S. Q., Thadhani, R., Getz, G. S., and Li, Y. C. (2012) Vitamin D receptor signaling inhibits atherosclerosis in mice. Mol. Endocrinol. 26, 1091-1101
58. Feig, J. E., Parathath, S., Rong, J. X., Mick, S. L., Vengrenyuk, Y., Grauer, L., Young, S. G., and Fisher, E. A. (2011) Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques. Circulation 123, 989-998
59. Feig, J. E., Pineda-Torra, I., Sanson, M., Bradley, M. N., Vengrenyuk, Y., Bogunovic, D., Gautier, E. L., Rubinstein, D., Hong, C., Liu, J., Wu, C., van Rooijen, N., Bhardwaj, N., Garabedian, M., Tontonoz, P., and Fisher, E. A. (2010) LXR promotes the maximal egress of monocyte-derived cells from mouse aortic plaques during atherosclerosis regression. J. Clin. Invest. 120, 4415-4424
60. Feig, J. E., Rong, J. X., Shamir, R., Sanson, M., Vengrenyuk, Y., Liu, J., Rayner, K., Moore, K., Garabedian, M., and Fisher, E. A. (2011) HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc. Natl. Acad. Sci. U.S.A. 108, 7166-7171
61. Trogan, E., Feig, J. E., Dogan, S., Rothblat, G. H., Angeli, V., Tacke, F., Randolph, G. J., and Fisher, E. A. (2006) Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 103, 3781-3786 (Pubitemid 43376632)
62. Mita, T., Goto, H., Azuma, K., Jin, W. L., Nomiyama, T., Fujitani, Y., Hirose, T., Kawamori, R., and Watada, H. (2010) Impact of insulin resistance on enhanced monocyte adhesion to endothelial cells and atherosclerogenesis independent of LDL cholesterol level. Biochem. Biophys. Res. Commun. 395, 477-483