1,25-dihydroxyvitamin D3 Protects against Macrophage-Induced Activation of NFκB and MAPK Signalling and Chemokine Release in Human Adipocytes

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Ding, Cherlyn ^a   Wilding, John P H ^a   Bing, Chen ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; CHEMOKINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRANSCRIPTION FACTOR RELA;

ADIPOCYTE; ADULT; ARTICLE; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; DRUG EFFECT; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MONOCYTE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ADIPOCYTES; ADULT; ANIMALS; CELL LINE; CELL MOVEMENT; CHEMOKINES; CYTOKINES; ENZYME ACTIVATION; FEMALE; HUMANS; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MONOCYTES; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; VITAMIN D;

EID: 84876541437     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061707     Document Type: Article

References (64)

1. Mellanby E, (1976) Nutrition Classics. The Lancet 1:407-12, 1919. An experimental investigation of rickets. Edward Mellanby. Nutr Rev 34: 338-340.
2. Holick MF, (2011) Vitamin D: evolutionary, physiological and health perspectives. Curr Drug Targets 12: 4-18.
3. Chiu KC, Chu A, Go VL, Saad MF, (2004) Hypovitaminosis D is associated with insulin resistance and beta cell dysfunction. Am J Clin Nutr 79: 820-825.
4. Barchetta I, Angelico F, Del Ben M, Baroni MG, Pozzilli P, et al. (2011) Strong association between non alcoholic fatty liver disease (NAFLD) and low 25(OH) vitamin D levels in an adult population with normal serum liver enzymes. BMC Med 9: 85.
5. Olson ML, Maalouf NM, Oden JD, White PC, Hutchison MR, (2012) Vitamin D deficiency in obese children and its relationship to glucose homeostasis. J Clin Endocrinol Metab 97: 279-285.
6. Goldner WS, Stoner JA, Thompson J, Taylor K, Larson L, et al. (2008) Prevalence of vitamin D insufficiency and deficiency in morbidly obese patients: a comparison with non-obese controls. Obes Surg 18: 145-150.
7. Fish E, Beverstein G, Olson D, Reinhardt S, Garren M, et al. (2010) Vitamin D status of morbidly obese bariatric surgery patients. J Surg Res 164: 198-202.
8. Brock K, Huang WY, Fraser DR, Ke L, Tseng M, et al. (2010) Low vitamin D status is associated with physical inactivity, obesity and low vitamin D intake in a large US sample of healthy middle-aged men and women. J Steroid Biochem Mol Biol 121: 462-466.
9. Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF, (2000) Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr 72: 690-693.
10. Kull M, Kallikorm R, Lember M, (2009) Body mass index determines sunbathing habits: implications on vitamin D levels. Intern Med J 39: 256-258.
11. Demay MB, (2006) Mechanism of vitamin D receptor action. Ann N Y Acad Sci 1068: 204-213.
12. Zhang Y, Kong J, Deb DK, Chang A, Li YC, (2010) Vitamin D receptor attenuates renal fibrosis by suppressing the renin-angiotensin system. J Am Soc Nephrol 21: 966-973.
13. Wamberg L, Christiansen T, Paulsen SK, Fisker S, Rask P, et al. (2012) Expression of vitamin D-metabolizing enzymes in human adipose tissue-the effect of obesity and diet-induced weight loss. Int J Obes (Lond).
14. Ching S, Kashinkunti S, Niehaus MD, Zinser GM, (2011) Mammary adipocytes bioactivate 25-hydroxyvitamin D(3) and signal via vitamin D(3) receptor, modulating mammary epithelial cell growth. J Cell Biochem 112: 3393-3405.
15. Ding C, Gao D, Wilding J, Trayhurn P, Bing C, (2012) Vitamin D signalling in adipose tissue. British Journal of Nutrition 108: 1915-1923.
16. Skurk T, Alberti-Huber C, Herder C, Hauner H, (2007) Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92: 1023-1033.
17. Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S, (2007) Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 56: 1010-1013.
18. Bourlier V, Bouloumie A, (2009) Role of macrophage tissue infiltration in obesity and insulin resistance. Diabetes Metab 35: 251-260.
19. Lolmede K, Duffaut C, Zakaroff-Girard A, Bouloumie A, (2011) Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab 37: 283-290.
20. Keophiphath M, Achard V, Henegar C, Rouault C, Clement K, et al. (2009) Macrophage-secreted factors promote a profibrotic phenotype in human preadipocytes. Mol Endocrinol 23: 11-24.
21. Gao D, Bing C (2011) Macrophage-induced expressio and release of matrix metalloproteinase 1 and 3 by human preadipocytes is mediated by IL-1B via activation of MAPK signaling. J Cell Physiol doi:10.1002/jcp.22630.
22. Gao D, Trayhurn P, Bing C, (2010) Macrophage-secreted factors inhibit ZAG expression and secretion by human adipocytes. Mol Cell Endocrinol 325: 135-142.
23. Kos K, Wong S, Tan B, Gummesson A, Jernas M, et al. (2009) Regulation of the fibrosis and angiogenesis promoter SPARC/osteonectin in human adipose tissue by weight change, leptin, insulin, and glucose. Diabetes 58: 1780-1788.
24. Giulietti A, van Etten E, Overbergh L, Stoffels K, Bouillon R, et al. (2007) 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: 47-57.
25. Cohen-Lahav M, Douvdevani A, Chaimovitz C, Shany S, (2007) The anti-inflammatory activity of 1,25-dihydroxyvitamin D3 in macrophages. J Steroid Biochem Mol Biol 103: 558-562.
26. Martinesi M, Treves C, d'Albasio G, Bagnoli S, Bonanomi AG, et al. (2008) Vitamin D derivatives induce apoptosis and downregulate ICAM-1 levels in peripheral blood mononuclear cells of inflammatory bowel disease patients. Inflamm Bowel Dis 14: 597-604.
27. Stio M, Martinesi M, Bruni S, Treves C, Mathieu C, et al. (2007) The Vitamin D analogue TX 527 blocks NF-kappaB activation in peripheral blood mononuclear cells of patients with Crohn's disease. J Steroid Biochem Mol Biol 103: 51-60.
28. Suzuki Y, Ichiyama T, Ohsaki A, Hasegawa S, Shiraishi M, et al. (2009) 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: 134-138.
29. Zhang Y, Leung DY, Richers BN, Liu Y, Remigio LK, et al. (2012) Vitamin D inhibits monocyte/macrophage proinflammatory cytokine production by targeting MAPK phosphatase-1. J Immunol 188: 2127-2135.
30. An H, Ford AL, Vo K, Eldeniz C, Ponisio R, et al. (2011) Early changes of tissue perfusion after tissue plasminogen activator in hyperacute ischemic stroke. Stroke 42: 65-72.
31. Sun X, Zemel MB, (2008) Calcitriol and calcium regulate cytokine production and adipocyte-macrophage cross-talk. J Nutr Biochem 19: 392-399.
32. Lira FS, Rosa JC, Cunha CA, Ribeiro EB, do Nascimento CO, et al. (2011) Supplementing alpha-tocopherol (vitamin E) and vitamin D3 in high fat diet decrease IL-6 production in murine epididymal adipose tissue and 3T3-L1 adipocytes following LPS stimulation. Lipids Health Dis 10: 37.
33. Marcotorchino J, Gouranton E, Romier B, Tourniaire F, Astier J, et al. (2012) Vitamin D reduces the inflammatory response and restores glucose uptake in adipocytes. Mol Nutr Food Res.
34. Gao D, Trayhurn P, Bing C (2012) 1,25-Dihydroxyvitamin D(3) inhibits the cytokine-induced secretion of MCP-1 and reduces monocyte recruitment by human preadipocytes. Int J Obes (Lond).
35. Lorente-Cebrian S, Eriksson A, Dunlop T, Mejhert N, Dahlman I, et al. (2012) Differential effects of 1alpha,25-dihydroxycholecalciferol on MCP-1 and adiponectin production in human white adipocytes. Eur J Nutr 51: 335-342.
36. Bao Y, Bing C, Hunter L, Jenkins JR, Wabitsch M, et al. (2005) Zinc-alpha2-glycoprotein, a lipid mobilizing factor, is expressed and secreted by human (SGBS) adipocytes. FEBS Lett 579: 41-47.
37. Tak PP, Firestein GS, (2001) NF-kappaB: a key role in inflammatory diseases. J Clin Invest 107: 7-11.
38. Bonizzi G, Karin M, (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
39. Gregor MF, Hotamisligil GS, (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445.
40. Vincenti MP, Brinckerhoff CE, (2002) Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4: 157-164.
41. Mutt SJ, Karhu T, Lehtonen S, Lehenkari P, Carlberg C, et al. (2012) Inhibition of cytokine secretion from adipocytes by 1,25-dihydroxyvitamin D3 via the NF-kappaB pathway. Faseb J 26: 4400-4407.
42. Bhavsar P, Hew M, Khorasani N, Torrego A, Barnes PJ, et al. (2008) Relative corticosteroid insensitivity of alveolar macrophages in severe asthma compared with non-severe asthma. Thorax 63: 784-790.
43. Fain JN, Madan AK, (2005) Regulation of monocyte chemoattractant protein 1 (MCP-1) release by explants of human visceral adipose tissue. Int J Obes (Lond) 29: 1299-1307.
44. Bashan N, Dorfman K, Tarnovscki T, Harman-Boehm I, Liberty IF, et al. (2007) Mitogen-activated protein kinases, inhibitory-kappaB kinase, and insulin signaling in human omental versus subcutaneous adipose tissue in obesity. Endocrinology 148: 2955-2962.
45. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83: 835-839.
46. Carlberg C, (2003) Current understanding of the function of the nuclear vitamin D receptor in response to its natural and synthetic ligands. Recent Results Cancer Res 164: 29-42.
47. Waugh DJ, Wilson C, (2008) The interleukin-8 pathway in cancer. Clin Cancer Res 14: 6735-6741.
48. Elgazar-Carmon V, Rudich A, Hadad N, Levy R, (2008) Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res 49: 1894-1903.
49. Neels JG, Badeanlou L, Hester KD, Samad F, (2009) Keratinocyte-derived chemokine in obesity: expression, regulation, and role in adipose macrophage infiltration and glucose homeostasis. J Biol Chem 284: 20692-20698.
50. Bruun JM, Lihn AS, Madan AK, Pedersen SB, Schiott KM, et al. (2004) Higher production of IL-8 in visceral vs. subcutaneous adipose tissue. Implication of nonadipose cells in adipose tissue. Am J Physiol Endocrinol Metab 286: E8-13.
51. Sun X, Casbas-Hernandez P, Bigelow C, Makowski L, Joseph Jerry D, et al. (2012) Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res Treat 131: 1003-1012.
52. Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, et al. (2012) CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61: 1680-1690.
53. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, et al. (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 116: 115-124.
54. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, et al. (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505.
55. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, et al. (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117: 902-909.
56. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, et al. (2006) Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281: 26602-26614.
57. Matter CM, Handschin C, (2007) RANTES (regulated on activation, normal T cell expressed and secreted), inflammation, obesity, and the metabolic syndrome. Circulation 115: 946-948.
58. Keophiphath M, Rouault C, Divoux A, Clement K, Lacasa D, (2010) CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol 30: 39-45.
59. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, et al. (2007) T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 115: 1029-1038.
60. Kristiansen OP, Mandrup-Poulsen T, (2005) Interleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54Suppl 2: S114-124.
61. Cohen-Lahav M, Shany S, Tobvin D, Chaimovitz C, Douvdevani A, (2006) Vitamin D decreases NFkappaB activity by increasing IkappaBalpha levels. Nephrol Dial Transplant 21: 889-897.
62. Nimitphong H, Holick MF, Fried SK, Lee MJ, (2012) 25-hydroxyvitamin D(3) and 1,25-dihydroxyvitamin D(3) promote the differentiation of human subcutaneous preadipocytes. PLoS ONE 7: e52171.
63. Dusso AS, Finch J, Brown A, Ritter C, Delmez J, et al. (1991) Extrarenal production of calcitriol in normal and uremic humans. J Clin Endocrinol Metab 72: 157-164.
64. Blum M, Dolnikowski G, Seyoum E, Harris SS, Booth SL, et al. (2008) Vitamin D-3 in fat tissue. Endocrine 33: 90-94.