#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Undernutrition is associated with perturbations in T cell-, B cell-, monocyte- and dendritic cell- subsets in latent Mycobacterium tuberculosis infection


Autoři: Anuradha Rajamanickam aff001;  Saravanan Munisankar aff001;  Chandra Kumar Dolla aff002;  Subash Babu aff001
Působiště autorů: National Institute of Health-NIRT-International Center for Excellence in Research, Chennai, India aff001;  National Institute for Research in Tuberculosis, Chennai, India aff002;  Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225611

Souhrn

Undernutrition, as described by low body mass index (BMI), is a foremost risk factor for the progression of active Tuberculosis (TB). Undernutrition is also known to impact the baseline frequencies of innate and adaptive immune cells in animal models. To verify whether undernutrition has any influence on the baseline frequencies of immune cells in latent Mycobacterium tuberculosis infection (LTBI), we examined the frequencies of T cell-, B cell, monocyte- and dendritic cell (DC)- subsets in individuals with LTBI and low BMI (LBMI) and contrasted them with LTBI and normal BMI (NBMI) groups. LBMI was characterized by decreased frequencies and absolute cell counts of T cells, B cells and NK cells in comparison with NBMI. LBMI individuals demonstrated significantly enhanced frequencies of naïve and effector CD4+ and CD8+ T cells and significantly decreased frequencies of central memory, effector memory CD4+ and CD8+ T cells and regulatory T cells. Among B cell subsets, LBMI individuals demonstrated significantly diminished frequencies of naïve, immature, classical memory, activated memory, atypical memory and plasma cells. In addition, LBMI individuals showed significantly decreased frequencies of classical monocytes, myeloid DCs and plasmacytoid DCs and significantly increased frequencies of intermediate and non-classical monocytes and myeloid derived suppressor cells. BMI exhibited a positive correlation with B cell and NK cell counts. Our data, therefore, demonstrates that coexistent undernutrition in LTBI is characterized by the occurrence of a significant modulation in the frequency of innate and adaptive immune cell subsets.

Klíčová slova:

T cells – Cytotoxic T cells – B cells – Monocytes – Malnutrition – Memory T cells – Memory B cells


Zdroje

1. Houben RM, Dodd PJ. The Global Burden of Latent Tuberculosis Infection: A Re-estimation Using Mathematical Modelling. PLoS Med. 2016;13(10):e1002152. Epub 2016/10/26. doi: 10.1371/journal.pmed.1002152 27780211; PubMed Central PMCID: PMC5079585.

2. Barry CE 3rd, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol. 2009;7(12):845–55. Epub 2009/10/27. doi: 10.1038/nrmicro2236 19855401; PubMed Central PMCID: PMC4144869.

3. de Valliere S, Abate G, Blazevic A, Heuertz RM, Hoft DF. Enhancement of innate and cell-mediated immunity by antimycobacterial antibodies. Infect Immun. 2005;73(10):6711–20. Epub 2005/09/24. doi: 10.1128/IAI.73.10.6711-6720.2005 16177348; PubMed Central PMCID: PMC1230956.

4. Chandrasekaran P, Saravanan N, Bethunaickan R, Tripathy S. Malnutrition: Modulator of Immune Responses in Tuberculosis. Front Immunol. 2017;8:1316. Epub 2017/11/03. doi: 10.3389/fimmu.2017.01316 29093710; PubMed Central PMCID: PMC5651251.

5. Savy M, Edmond K, Fine PE, Hall A, Hennig BJ, Moore SE, et al. Landscape analysis of interactions between nutrition and vaccine responses in children. J Nutr. 2009;139(11):2154S–218S. Epub 2009/10/02. doi: 10.3945/jn.109.105312 19793845.

6. Schaible UE, Kaufmann SH. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med. 2007;4(5):e115. Epub 2007/05/03. doi: 10.1371/journal.pmed.0040115 17472433; PubMed Central PMCID: PMC1858706.

7. Chandra RK. Nutrition and the immune system: an introduction. Am J Clin Nutr. 1997;66(2):460S–3S. Epub 1997/08/01. doi: 10.1093/ajcn/66.2.460S 9250133.

8. Lonnroth K, Williams BG, Cegielski P, Dye C. A consistent log-linear relationship between tuberculosis incidence and body mass index. Int J Epidemiol. 2010;39(1):149–55. Epub 2009/10/13. doi: 10.1093/ije/dyp308 19820104.

9. Cegielski JP, McMurray DN. The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis. 2004;8(3):286–98. Epub 2004/05/14. 15139466.

10. Lonnroth K, Jaramillo E, Williams BG, Dye C, Raviglione M. Drivers of tuberculosis epidemics: the role of risk factors and social determinants. Soc Sci Med. 2009;68(12):2240–6. Epub 2009/04/28. doi: 10.1016/j.socscimed.2009.03.041 19394122.

11. Radhakrishna S, Frieden TR, Subramani R, Tuberculosis Research C. Association of initial tuberculin sensitivity, age and sex with the incidence of tuberculosis in south India: a 15-year follow-up. Int J Tuberc Lung Dis. 2003;7(11):1083–91. Epub 2003/11/06. 14598969.

12. Anuradha R, Munisankar S, Bhootra Y, Kumar NP, Dolla C, Babu S. Malnutrition is associated with diminished baseline and mycobacterial antigen—stimulated chemokine responses in latent tuberculosis infection. J Infect. 2018;77(5):410–6. Epub 2018/05/20. doi: 10.1016/j.jinf.2018.05.003 29777718; PubMed Central PMCID: PMC6340055.

13. Sinha DP, Bang FB. Protein and calorie malnutrition, cell-mediated immunity, and B.C.G. vaccination in children from rural West Bengal. Lancet. 1976;2(7985):531–4. Epub 1976/09/11. doi: 10.1016/s0140-6736(76)91791-8 60620.

14. McMurray DN, Watson RR, Reyes MA. Effect of renutrition on humoral and cell-mediated immunity in severely malnourished children. Am J Clin Nutr. 1981;34(10):2117–26. Epub 1981/10/01. doi: 10.1093/ajcn/34.10.2117 6794344.

15. Pena-Cruz V, Reiss CS, McIntosh K. Sendai virus infection of mice with protein malnutrition. J Virol. 1989;63(8):3541–4. Epub 1989/08/01. 2545924; PubMed Central PMCID: PMC250935.

16. Taylor AK, Cao W, Vora KP, De La Cruz J, Shieh WJ, Zaki SR, et al. Protein energy malnutrition decreases immunity and increases susceptibility to influenza infection in mice. J Infect Dis. 2013;207(3):501–10. Epub 2012/09/06. doi: 10.1093/infdis/jis527 22949306.

17. Najera O, Gonzalez C, Toledo G, Lopez L, Ortiz R. Flow cytometry study of lymphocyte subsets in malnourished and well-nourished children with bacterial infections. Clin Diagn Lab Immunol. 2004;11(3):577–80. Epub 2004/05/13. doi: 10.1128/CDLI.11.3.577-580.2004 15138185; PubMed Central PMCID: PMC404584.

18. Savino W. The thymus gland is a target in malnutrition. Eur J Clin Nutr. 2002;56 Suppl 3:S46-9. Epub 2002/07/27. doi: 10.1038/sj.ejcn.1601485 12142962.

19. Schlesinger L, Ohlbaum A, Grez L, Stekel A. Decreased interferon production by leukocytes in marasmus. Am J Clin Nutr. 1976;29(7):758–61. Epub 1976/07/01. doi: 10.1093/ajcn/29.7.758 180790.

20. Boyman O, Purton JF, Surh CD, Sprent J. Cytokines and T-cell homeostasis. Curr Opin Immunol. 2007;19(3):320–6. Epub 2007/04/17. doi: 10.1016/j.coi.2007.04.015 17433869.

21. Becker TC, Wherry EJ, Boone D, Murali-Krishna K, Antia R, Ma A, et al. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J Exp Med. 2002;195(12):1541–8. Epub 2002/06/19. doi: 10.1084/jem.20020369 12070282; PubMed Central PMCID: PMC2193552.

22. Iyer SS, Chatraw JH, Tan WG, Wherry EJ, Becker TC, Ahmed R, et al. Protein energy malnutrition impairs homeostatic proliferation of memory CD8 T cells. J Immunol. 2012;188(1):77–84. Epub 2011/11/26. doi: 10.4049/jimmunol.1004027 22116826; PubMed Central PMCID: PMC3244573.

23. Hoang T, Agger EM, Cassidy JP, Christensen JP, Andersen P. Protein energy malnutrition during vaccination has limited influence on vaccine efficacy but abolishes immunity if administered during Mycobacterium tuberculosis infection. Infect Immun. 2015;83(5):2118–26. Epub 2015/03/11. doi: 10.1128/IAI.03030-14 25754202; PubMed Central PMCID: PMC4399034.

24. Procaccini C, De Rosa V, Galgani M, Carbone F, Cassano S, Greco D, et al. Leptin-induced mTOR activation defines a specific molecular and transcriptional signature controlling CD4+ effector T cell responses. J Immunol. 2012;189(6):2941–53. Epub 2012/08/21. doi: 10.4049/jimmunol.1200935 22904304.

25. Gerriets VA, Danzaki K, Kishton RJ, Eisner W, Nichols AG, Saucillo DC, et al. Leptin directly promotes T-cell glycolytic metabolism to drive effector T-cell differentiation in a mouse model of autoimmunity. Eur J Immunol. 2016;46(8):1970–83. Epub 2016/05/26. doi: 10.1002/eji.201545861 27222115; PubMed Central PMCID: PMC5154618.

26. Cohen S, Danzaki K, MacIver NJ. Nutritional effects on T-cell immunometabolism. Eur J Immunol. 2017;47(2):225–35. Epub 2017/01/06. doi: 10.1002/eji.201646423 28054344; PubMed Central PMCID: PMC5342627.

27. Kozakiewicz L, Phuah J, Flynn J, Chan J. The role of B cells and humoral immunity in Mycobacterium tuberculosis infection. Adv Exp Med Biol. 2013;783:225–50. Epub 2013/03/08. doi: 10.1007/978-1-4614-6111-1_12 23468112; PubMed Central PMCID: PMC4184189.

28. Chan J, Mehta S, Bharrhan S, Chen Y, Achkar JM, Casadevall A, et al. The role of B cells and humoral immunity in Mycobacterium tuberculosis infection. Semin Immunol. 2014;26(6):588–600. Epub 2014/12/03. doi: 10.1016/j.smim.2014.10.005 25458990; PubMed Central PMCID: PMC4314354.

29. Torrado E, Fountain JJ, Robinson RT, Martino CA, Pearl JE, Rangel-Moreno J, et al. Differential and site specific impact of B cells in the protective immune response to Mycobacterium tuberculosis in the mouse. PLoS One. 2013;8(4):e61681. Epub 2013/04/25. doi: 10.1371/journal.pone.0061681 23613902; PubMed Central PMCID: PMC3627912.

30. Vordermeier HM, Venkataprasad N, Harris DP, Ivanyi J. Increase of tuberculous infection in the organs of B cell-deficient mice. Clin Exp Immunol. 1996;106(2):312–6. Epub 1996/11/01. doi: 10.1046/j.1365-2249.1996.d01-845.x 8918578; PubMed Central PMCID: PMC2200584.

31. Abe M, Akbar F, Matsuura B, Horiike N, Onji M. Defective antigen-presenting capacity of murine dendritic cells during starvation. Nutrition. 2003;19(3):265–9. Epub 2003/03/07. doi: 10.1016/s0899-9007(02)00854-7 12620532.

32. Joosten SA, van Meijgaarden KE, Del Nonno F, Baiocchini A, Petrone L, Vanini V, et al. Patients with Tuberculosis Have a Dysfunctional Circulating B-Cell Compartment, Which Normalizes following Successful Treatment. PLoS Pathog. 2016;12(6):e1005687. Epub 2016/06/16. doi: 10.1371/journal.ppat.1005687 27304615; PubMed Central PMCID: PMC4909319.

33. O'Shea MK, Tanner R, Muller J, Harris SA, Wright D, Stockdale L, et al. Immunological correlates of mycobacterial growth inhibition describe a spectrum of tuberculosis infection. Sci Rep. 2018;8(1):14480. Epub 2018/09/29. doi: 10.1038/s41598-018-32755-x 30262883; PubMed Central PMCID: PMC6160428.

34. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, et al. Nomenclature of monocytes and dendritic cells in blood. Blood. 2010;116(16):e74–80. Epub 2010/07/16. doi: 10.1182/blood-2010-02-258558 20628149.

35. Yang J, Zhang L, Yu C, Yang XF, Wang H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res. 2014;2(1):1. Epub 2014/01/09. doi: 10.1186/2050-7771-2-1 24398220; PubMed Central PMCID: PMC3892095.

36. Wong KL, Yeap WH, Tai JJ, Ong SM, Dang TM, Wong SC. The three human monocyte subsets: implications for health and disease. Immunol Res. 2012;53(1–3):41–57. Epub 2012/03/21. doi: 10.1007/s12026-012-8297-3 22430559.

37. Chimen M, Yates CM, McGettrick HM, Ward LS, Harrison MJ, Apta B, et al. Monocyte Subsets Coregulate Inflammatory Responses by Integrated Signaling through TNF and IL-6 at the Endothelial Cell Interface. J Immunol. 2017;198(7):2834–43. Epub 2017/02/15. doi: 10.4049/jimmunol.1601281 28193827; PubMed Central PMCID: PMC5357784.

38. Sanchez MD, Garcia Y, Montes C, Paris SC, Rojas M, Barrera LF, et al. Functional and phenotypic changes in monocytes from patients with tuberculosis are reversed with treatment. Microbes Infect. 2006;8(9–10):2492–500. Epub 2006/07/29. doi: 10.1016/j.micinf.2006.06.005 16872859.

39. Maecker HT, McCoy JP, Nussenblatt R. Standardizing immunophenotyping for the Human Immunology Project. Nat Rev Immunol. 2012;12(3):191–200. Epub 2012/02/22. doi: 10.1038/nri3158 22343568; PubMed Central PMCID: PMC3409649.

40. Khader SA, Partida-Sanchez S, Bell G, Jelley-Gibbs DM, Swain S, Pearl JE, et al. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med. 2006;203(7):1805–15. Epub 2006/07/05. doi: 10.1084/jem.20052545 16818672; PubMed Central PMCID: PMC2118335.

41. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med. 1999;5(8):919–23. Epub 1999/07/30. doi: 10.1038/11360 10426316.

42. Lozza L, Farinacci M, Fae K, Bechtle M, Staber M, Dorhoi A, et al. Crosstalk between human DC subsets promotes antibacterial activity and CD8+ T-cell stimulation in response to bacille Calmette-Guerin. Eur J Immunol. 2014;44(1):80–92. Epub 2013/10/12. doi: 10.1002/eji.201343797 24114554; PubMed Central PMCID: PMC3992850.

43. Knaul JK, Jorg S, Oberbeck-Mueller D, Heinemann E, Scheuermann L, Brinkmann V, et al. Lung-residing myeloid-derived suppressors display dual functionality in murine pulmonary tuberculosis. Am J Respir Crit Care Med. 2014;190(9):1053–66. Epub 2014/10/03. doi: 10.1164/rccm.201405-0828OC 25275852.

44. du Plessis N, Loebenberg L, Kriel M, von Groote-Bidlingmaier F, Ribechini E, Loxton AG, et al. Increased frequency of myeloid-derived suppressor cells during active tuberculosis and after recent mycobacterium tuberculosis infection suppresses T-cell function. Am J Respir Crit Care Med. 2013;188(6):724–32. Epub 2013/07/28. doi: 10.1164/rccm.201302-0249OC 23885784.

45. Obregon-Henao A, Henao-Tamayo M, Orme IM, Ordway DJ. Gr1(int)CD11b+ myeloid-derived suppressor cells in Mycobacterium tuberculosis infection. PLoS One. 2013;8(11):e80669. Epub 2013/11/14. doi: 10.1371/journal.pone.0080669 24224058; PubMed Central PMCID: PMC3815237.

46. El Daker S, Sacchi A, Tempestilli M, Carducci C, Goletti D, Vanini V, et al. Granulocytic myeloid derived suppressor cells expansion during active pulmonary tuberculosis is associated with high nitric oxide plasma level. PLoS One. 2015;10(4):e0123772. Epub 2015/04/17. doi: 10.1371/journal.pone.0123772 25879532; PubMed Central PMCID: PMC4400140.

47. Hughes SM, Amadi B, Mwiya M, Nkamba H, Tomkins A, Goldblatt D. Dendritic cell anergy results from endotoxemia in severe malnutrition. J Immunol. 2009;183(4):2818–26. Epub 2009/07/25. doi: 10.4049/jimmunol.0803518 19625645.


Článok vyšiel v časopise

PLOS One


2019 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#