Age and low levels of circulating vitamin D are associated with impaired innate immune function

Journal of Leukocyte Biology

Volumn 91, Issue 5, 2012, Pages 829-838

  Alvarez Rodriguez, Lorena ^a   Lopez Hoyos, Marcos ^a   Garcia Unzueta, Maite ^a   Amado, Jose Antonio ^a,b   Cacho, Pedro Munoz ^b   Martinez Taboad, Victor Manuel ^a,b  

^a HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Aging; Cathelicidin; Innate immunity; Toll like receptor; Vitamin D

Indexed keywords

CATHELICIDIN; LIGAND; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; VITAMIN D;

ADULT; AGE DISTRIBUTION; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IN VIVO STUDY; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VITAMIN BLOOD LEVEL;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNITY, INNATE; MIDDLE AGED; MONOCYTES; TOLL-LIKE RECEPTORS; VITAMIN D; YOUNG ADULT;

EID: 84860909869     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1011523     Document Type: Article

References (64)

1. Holick, M. F. (2004) Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease. Am. J. Clin. Nutr. 80 (Suppl.), 1678S-1688S.
2. Yamshchikov, A. V., Desai, N. S., Blumberg, H. M., Ziegler, T. R., Tang-pricha, V. (2009) Vitamin D for treatment and prevention of infectious diseases: a systematic review of randomized controlled trials. Endocr. Pract. 2, 1-29.
3. Mora, J. R., Iwata, M., von Andrian, U. H. (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 8, 685-698.
4. Cutolo, M., Plebani, M., Shoenfeld, Y., Adorini, L., Tincani, A. (2011) Vitamin D endocrine system and the immune response in rheumatic diseases. Vitam. Horm. 86, 327-351.
5. Cantorna, M. T., Mahon, B. D. (2004) Mounting evidence for vitamin D as an enviromental factor affecting autoimmune disease prevalence. Exp. Biol. Med. 229, 1136-1142.
6. Arnson, Y., Amital, H., Shoenfeld, Y. (2007) Vitamin D and autoimmunity: new aetiological and therapeutic considerations. Ann. Rheum. Dis. 66, 1137-1142.
7. Shapira, Y., Agmon-Levin, N., Shoenfeld, Y. (2010) Geoepidemiology of autoimmune rheumatic diseases. Nat. Rev. Rheumatol. 6, 468-476.
8. Raghuwanshi, A., Joshi, S. S., Christakos, S. (2008) Vitamin D and multiple sclerosis. J. Cell. Biochem. 105, 338-343.
9. Vagianos, K., Bector, S., McConnell, J., Bernstein, C. N. (2007) Nutrition assessment of patients with inflammatory bowel disease. JPEN J. Parenter. Enteral. Nutr. 31, 311-319.
10. Shoenfeld, N., Amital, H., Shoenfeld, Y. (2009) The effect of melanism and vitamin D synthesis on the incidence of autoimmune disease. Nat. Clin. Pract. Rheumatol. 5, 99-105.
11. Antonen, J. A., Hannula, P. M., Pyhälä, R, Saha, H. H., Ala-Houhala, I. O., Pasternack, A. I. (2000) Adequate seroresponse to influenza vaccination in dialysis patients. Nephron 86, 56-61.
12. Agmon-Levin, N., Blank, M., Zandman-Goddard, G., Orbach, H., Meroni, P. L., Tincani, A., Doria, A., Cervera, R., Miesbach, W., Stojanovich, L., Barak, V., Porat-Katz, B. S., Amital, H., Shoenfeld, Y. (2011) Vitamin D: an instrumental factor in the anti-phospholipid syndrome by inhibition of tissue factor expression. Ann. Rheum. Dis. 70, 145-150.
13. Souberbielle J. C., Body J. J., Lappe J. M., Plebani M., Shoenfeld Y., Wang T. J., Bischoff-Ferrari H. A., Cavalier E., Ebeling P. R., Fardellone P., Gandini S., Gruson D., Guérin A. P., Heickendorff L., Hollis B. W., Ish-Shalom S., Jean G., von Landenberg P., Largura A., Olsson T., Pier-rot-Deseilligny C., Pilz S., Tincani A., Valcour A., Zittermann A. (2010) Vitamin D and musculoskeletal health, cardiovascular disease, autoimmunity and cancer: recommendations for clinical practice. Autoimmun. Rev. 9, 709-715.
14. Pérez-López, F. R., Chedraui, P., Fernández-Alonso, A. M. (2011) Vitamin D and aging: beyond calcium and bone metabolism. Maturitas 69, 27-36.
15. Autier, P., Gandini, S. (2007) Vitamin D supplementation and total mortality: a meta-analysis of randomized controlled trials. Arch. Intern. Med. 167, 1730-1737.
16. Cannell, J. J., Vieth, R., Umhau, J. C., Holick, M. F., Grant, W. B., Mad-ronich, S., Garland, C. F., Giovannucci, E. (2006) Epidemic influenza and vitamin D. Epidemiol. Infect. 134, 1129-1140.
17. Von Essen, M. R., Kongsbak, M., Schjerling, P., Olgaard, K., Odum, N., Geisler, C. (2010) Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat. Immunol. 11, 344-349.
18. Adams J. S., Ren S., Liu P. T., Chun R. F., Lagishetty V., Gombart A. F., Borregaard N., Modlin R. L., Hewison M. (2009) Vitamin D-directed rheostatic regulation of monocyte antibacterial responses. J. Immunol. 182, 4289-4295.
19. Yamshchikov, A. V., Kurbatova, E. V., Kumari, M., Blumberg, H. M., Ziegler, T. R., Ray, S. M., Tangpricha, V. (2010) Vitamin D status and antimicrobial peptide cathelicidin (LL-37) concentrations in patients with active pulmonary tuberculosis. Am. J. Clin. Nutr. 92, 603-611.
20. Kawai, T., Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384.
21. Kabelitz, D. (2007) Expression and function of Toll-like receptors in T lymphocytes. Curr. Opin. Immunol. 19, 39-45.
22. Xu, D., Komai-Koma, M., Liew, F. Y. (2005) Expression and function of Toll-like receptor on T cells. Cell. Immunol. 233, 85-89.
23. Sutmuller R, Garritsen A, Adema, G. J. (2007) Regulatory T cells and Toll-like receptors: regulating the regulators. Ann. Rheum. Dis. 66 (Suppl. 3), 91-95.
24. Muzio, M., Polentarutti, N., Bosisio, D., Prahladan, M. K., Mantovani, A. (2000) Toll-like receptors: a growing family of immune receptors that are differentially expressed and regulated by different leukocytes. J. Leukoc. Biol. 67, 450-456.
25. Hornung, V., Rothenfusser, S., Britsch, S., Krug, A., Jahrsdörfer, B., Giese, T., Endres, H., Hartmann, G. (2002) Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168, 4531-4537.
26. Adams, J. S., Hewison, M. (2010) Update in vitamin D. J. Clin. Endocrinol. Metab. 95, 471-478.
27. Sørensen, O., Cowland, J. B., Askaa, J., Borregaard, N. (1997) An ELISA for hCAP-18, the cathelicidin present in human neutrophils and plasma. J. Immunol. Methods 206, 53-59.
28. Bals, R., Weiner, D. J., Moscioni, A. D., Meegalla, R. L., Wilson, J. M. (1999) Augmentation of innate host defense by expression of a cathelici-din antimicrobial peptide. Infect. Immun. 67, 6084-6089.
29. Jeng, L., Yamshchikov, A. V., Judd, S. E., Blumberg, H. M., Martin, G. S., Ziegler, T. R., Tangpricha, V. (2009) Alterations in vitamin D status and anti-microbial peptide levels in patients in the intensive care unit with sepsis. J. Transl. Med. 7, 28.
30. Liu P. T., Stenger S., Li H., Wenzel L., Tan B. H., Krutzik S. R., Ochoa M. T., Schauber J., Wu K., Meinken C., Kamen D. L., Wagner M., Bals R., Steinmeyer A., Zügel U., Gallo R. L., Eisenberg D., Hewison M., Hollis B. W., Adams J. S., Bloom B. R., Modlin R. L. (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 1770-1773.
31. Hosmer, D. W., Lemeshow, S. (2000) Applied Logistic Regression, 2nd ed., Wiley, New York, NY, USA.
32. Menard, S. (2001) Applied logistic regression analysis. Sage University Paper Series on Quantitative Applications in the Social Sciences, 07-106. Sage, Thousand Oaks, CA, USA.
33. Nagelkerke, N. J. D. (1991) A note on general definition of the coefficient of determination. Biometrika 78, 691-692.
34. Álvarez Rodríguez L., López-Hoyos M., Mata C., Fontalba A., Calvo Alen J., Marín M. J., Fernández-Luna J. L., Aguero Balbín J., Aranzamendi Zal-dunbide M., Blanco R., Martínez-Taboada V. M. (2011) Expression and function of Toll-like receptors in peripheral blood mononuclear cells of patients with polymyalgia rheumatica and giant cell arteritis. Ann. Rheum. Dis. 70, 1677-1683.
35. Walker, V. P., Zhang, X., Rastegar, I., Liu, P. T., Hollis, B. W., Adams, J. S., Modlin, R. L. (2011) Cord blood vitamin D status impacts innate immune responses. J. Clin. Endocrinol. Metab. 96, 1835-1843.
36. Hertting O., Holm Å., Lüthje P., Brauner H., Dyrdak R, Jonasson A F., Wik-lund P., Chromek M., Brauner A. (2010) Vitamin D induction of the human antimicrobial peptide cathelicidin in the urinary bladder. PLoS One 5, e15580.
37. Bhan, I., Camargo, C. A, Wenger, J., Ricciardi, C, Ye, J., Borregaard, N., Thadhani, R (2011) Circulating levels of 25-hydroxyvitamin D and human cathelicidin in healthy adults. J. Allergy Clin. Immunol. 127, 1302-1304.
38. Mata-Granados, J. M., Luque de Castro, M. D., Quesada Gomez, J. M. (2008) Inappropriate serum levels of retinol, a-tocopherol, 25 hydroxyvi-tamin D3 and 24,25 dihydroxyvitamin D3 levels in healthy Spanish adults: simultaneous assessment by HPLC. Clin. Biochem. 41, 676-680.
39. Rodríguez Sangrador, M., Beltran de Miguel, B., Cuadrado Vives, C, Moreiras Tuny, O. (2010) Influence of sun exposure and diet to the nutritional status of vitamin D in adolescent Spanish women: the five countries study (OPTIFORD Project). Nutr. Hosp. 25, 755-762.
40. Shaw, A. C, Panda, A., Joshi, S. R., Qian, F., Allore, H. G., Montgomery, R R (2011) Dysregulation of human Toll-like receptor function in aging. Ageing Res. Rev. 10, 346-353.
41. Agarwal, S., Busse, P.J. (2010) Innate and adaptive immunosenescence. Ann. Allergy Asthma Immunol. 104, 183-190.
42. Weiskopf, D., Weinberger, B., Grubeck-Loebenstein, B. (2009) The aging of the immune system. Transpl. Int. 22, 1041-1050.
43. Panda, A, Arjona, A, Sapey, E., Bai, F., Fikrig, E., Montgomery, R R, Lord, J. M., Shaw, A. C. (2009) Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol. 30, 325-333.
44. Kovacs, E. J., Palmer, J. L., Fortin, C. F., Fülop, T., Goldstein, D. R, Linton, P. J. (2009) Aging and innate immunity in the mouse: impact of intrinsic and extrinsic factors. Trends Immunol. 30, 319-324.
45. Renshaw, M., Rockwell, J., Engleman, C, Gewirtz, A, Katz, J., Sambhara, S. (2002) Cutting edge: impaired Toll-like receptor expression and function in aging. J. Immunol. 169, 4697-4701.
46. Wong, C. P., Magnusson, K. R, Ho, E. (2010) Aging is associated with altered dendritic cells subset distribution and impaired proinflammatory cytokine production. Exp. Gerontol. 45, 163-169.
47. Stout-Delgado, H. W., Yang, X., Walker, W. E., Tesar, B. M., Goldstein, D. R (2008) Aging impairs IFN regulatory factor 7 up-regulation in plas-macytoid dendritic cells during TLR9 activation. J. Immunol. 181, 6747-6756.
48. Arranz, L., De Castro, N. M., Baeza, I., De la Fuente, M. (2010) Differential expresion of Toll-like receptor 2 and 4 on peritoneal leukocyte populations from long-lived and non-selected old female mice. Biogerontology 11, 475-482.
49. Hinojosa, E., Boyd, A. R, Orihuela, C. J. (2009) Age-associated inflammation and Toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia. J. Infect. Dis. 200, 546-554.
50. Van Duin, D., Shaw, A. C. (2007) Toll-like receptors in older adults. J. Am. Geriatr. Soc. 5, 1438-1444.
51. Van Duin D., Mohanty S., Thomas V., Ginter S., Montgomery RR, Fikrig E., Allore H. G., Medzhitov R, Shaw A. C. (2007) Age-associated defect in human TLR-1/2 function. J. Immunol. 178, 970-975.
52. Agrawal, A, Tay, J., Ton, S., Agrawal, S., Gupta, S. (2009) Increased reactivity of dendritic cells from aged subjects to self-antigen, the human DNA. J. Immunol. 182, 1138-1145.
53. Panda A, Qian F., Mohanty S., van Duin D., Newman F. K, Zhang L., Chen S., Towle V., Belshe R B., Fikrig E., Allore H. G., Montgomery RR, Shaw A. C. (2010) Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J. Immunol. 184, 2518-2527.
54. Krutzik, S. R, Hewison, M., Liu, P. T., Robles, J. A., Stenger, S., Adams, J. S., Modlin, R L. (2008) IL-15 links TLR2/1-induced macrophage differentiation to the vitamin D-dependent antimicrobial pathway. J. Immunol. 181, 7115-7120.
55. Adams, J. S., Hewison, M. (2008) Unexpected actions of vitamin D: new perspectives on the regulation of innate and adaptive immunity. Nat. Clin. Pract. Endocrinol. Metab. 4, 80-90.
56. Ginde, A. A, Mansbach, J. M., Camargo, C. A. (2009) Association between serum 25-hydroxyvitamin D level and upper respiratory tract infection in the Third National Health and Nutrition Examination Survey. Arch. Intern. Med. 169, 384-390.
57. Wang, J. P., Bowen, G. N., Padden, C, Cerny, A, Finberg, R W., New-burger, P. E., Kurt-Jones, E. A. (2008) Toll-like receptor-mediated activation of neutrophils by influenza A virus. Blood 112, 2028-2034.
58. Cannell, J. J., Zasloff, M., Garland, C. F., Scragg, R, Giovannucci, E. (2008) On the epidemiology of influenza. Virol. J. 5, 29.
59. Aloia, J. F., Li-Ng, M. (2007) Re: epidemic influenza and vitamin D. Epidemiol. Infect. 135, 1095-1096.
60. Sadeghi K, Wessner B., Laggner U., Ploder M., Tamandl D., Friedl J., Zugel U., Steinmeyer A, Pollak A, Roth E., Boltz-Nitulescu G., Spittler A. (2006) Vitamin D3 down-regulates monocyte TLR expression and triggers hyporesponsiveness to pathogen-associated molecular patterns. Eur. J. Immunol. 36, 361-370.
61. Dickie, L. J., Church, L. D., Coulthard, L. R, Mathews, R J., Emery, P., McDermott, M. F. (2010) Vitamin D3 down-regulates intracellular Tolllike receptor 9 expression and Toll-like receptor 9-induced IL-6 production in human monocytes. Rheumatology (Oxford) 49, 1466-1471.
62. Khoo, A. L., Chai, L. Y, Koenen, H. J., Sweep, F. C, Joosten, I., Netea, M. G., van der Ven, A. J. (2011) Regulation of cytokine responses by seasonality of vitamin D status in healthy individuals. Clin. Exp. Immunol. 164, 72-79.
63. Timonen, T., Nayha, S., Koskela, T., Pukkala, E. (2007) Are sunlight deprivation and influenza epidemics associated with the onset of acute leukemia? Haematologica 92, 1553-1556.
64. Laaksi, I., Ruohola, J. P., Tuohimaa, P., Auvinen, A., Haataja, R., Pihla-jamaki, H., Yikomi, T. (2007) An association of serum vitamin D concentrations < 40 nmol/L with acute respiratory tract infection in young Finnish men. Am. J. Clin. Nutr. 86, 714-717.