Protein energy malnutrition during vaccination has limited influence on vaccine efficacy but abolishes immunity if administered during Mycobacterium tuberculosis infection

Infection and Immunity

Volumn 83, Issue 5, 2015, Pages 2118-2126

  Hoang, Truc ^a   Agger, Else Marie ^a   Cassidy, Joseph P ^b   Christensen, Jan P ^c   Andersen, Peter ^a  

^a STATENS SERUM INSTITUT   (Denmark)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; INTERLEUKIN 2; SUBUNIT VACCINE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNITY; IMMUNOHISTOCHEMISTRY; INFECTION CONTROL; LUNG GRANULOMA; LYMPHOCYTE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROTEIN CALORIE MALNUTRITION; RELAPSE; TUBERCULOSIS; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; IMMUNOLOGY; MYCOBACTERIUM TUBERCULOSIS; PROCEDURES; SECRETION (PROCESS); T LYMPHOCYTE SUBPOPULATION; VACCINATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; FEMALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; PROTEIN-ENERGY MALNUTRITION; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; TUBERCULOSIS VACCINES; VACCINATION;

EID: 84928181024     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.03030-14     Document Type: Article

References (56)

1. World Health Organization. 2014. Global tuberculosis report 2014. World Health Organization, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/137094/1/9789241564809_eng.pdf.
2. Selwyn PA, Sckell BM, Alcabes P, Friedland GH, Klein RS, Schoenbaum EE. 1992. High risk of active tuberculosis in HIV-infected drug users with cutaneous anergy. JAMA 268:504-509. http://dx.doi.org/10.1001/jama.268.4.504.
3. Lienhardt C. 2001. From exposure to disease: the role of environmental factors in susceptibility to and development of tuberculosis. Epidemiol Rev 23:288-301. http://dx.doi.org/10.1093/oxfordjournals.epirev.a000807.
4. Cegielski JP, McMurray DN. 2004. The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis 8:286-298.
5. Chan J, Tian Y, Tanaka KE, Tsang MS, Yu K, Salgame P, Carroll D, Kress Y, Teitelbaum R, Bloom BR. 1996. Effects of protein calorie malnutrition on tuberculosis in mice. Proc Natl Acad Sci U S A 93:14857-14861. http://dx.doi.org/10.1073/pnas.93.25.14857.
6. Dai G, Phalen S, McMurray DN. 1998. Nutritional modulation of host responses to mycobacteria. Front Biosci 3:e110-122.
7. McMurray DN, Yetley EA. 1982. Cell-mediated immunity in malnourished guinea pigs after Mycobacterium bovis BCG vaccination. Infect Immun 35:909-914.
8. McMurray DN, Carlomagno MA, Mintzer CL, Tetzlaff CL. 1985. Mycobacterium bovis BCG vaccine fails to protect protein-deficient guinea pigs against respiratory challenge with virulent Mycobacterium tuberculosis. Infect Immun 50:555-559.
9. Knudsen NP, Norskov-Lauritsen S, Dolganov GM, Schoolnik GK, Lindenstrøm T, Andersen P, Agger EM, Aagaard C. 2014. Tuberculosis vaccine with high predicted population coverage and compatibility with modern diagnostics. Proc Natl Acad Sci U S A http://dx.doi.org/10.1073/pnas.1314973111.
10. Ottenhoff TH, Kaufmann SH. 2012. Vaccines against tuberculosis: where are we and where do we need to go? PLoS Pathog 8:e1002607. http://dx.doi.org/10.1371/journal.ppat.1002607.
11. Aagaard C, Hoang T, Dietrich J, Cardona PJ, Izzo A, Dolganov G, Schoolnik GK, Cassidy JP, Billeskov R, Andersen P. 2011. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 17:189-194. http://dx.doi.org/10.1038/nm.2285.
12. Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, Lockhart S, Shea JE, McClain JB, Hussey GD, Hanekom WA, Mahomed H, McShane H, MVA85A 020 Trial Study Team. 2013. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 381:1021-1028. http://dx.doi.org/10.1016/S0140-6736(13)60177-4.
13. Orme IM. 2013. Vaccine development for tuberculosis: current progress. Drugs 73:1015-1024. http://dx.doi.org/10.1007/s40265-013-0081-8.
14. Andersen P, Woodworth JS. 2014. Tuberculosis vaccines-rethinking the current paradigm. Trends Immunol 35:387-395. http://dx.doi.org/10.1016/j.it.2014.04.006.
15. Drake TE. 1971. Thymolymphatic deficiency and depression of cell-mediated immunity in protein-calorie malnutrition. Lancet ii:1322-1323.
16. Chandra RK. 1997. Nutrition and the immune system: an introduction. Am J Clin Nutr 66:460S-463S.
17. Dai G, McMurray DN. 1998. Altered cytokine production and impaired antimycobacterial immunity in protein-malnourished guinea pigs. Infect Immun 66:3562-3568.
18. Mengheri E, Nobili F, Crocchioni G, Lewis JA. 1992. Protein starvation impairs the ability of activated lymphocytes to produce interferon-gamma. J Interferon Res 12:17-21. http://dx.doi.org/10.1089/jir.1992.12.17.
19. González-Martínez H, Rodriguez L, Najera O, Cruz D, Miliar A, Dominguez A, Sanchez F, Graniel J, González-Torres MC. 2008. Expression of cytokine mRNA in lymphocytes of malnourished children. J Clin Immunol 28:593-599. http://dx.doi.org/10.1007/s10875-008-9204-5.
20. González-Torres C, González-Martínez H, Miliar A, Najera O, Graniel J, Firo V, Alvarez C, Bonilla E, Rodriguez L. 2013. Effect of malnutrition on the expression of cytokines involved in Th1 cell differentiation. Nutrients 5:579-593. http://dx.doi.org/10.3390/nu5020579.
21. Saucillo DC, Gerriets VA, Sheng J, Rathmell JC, Maciver NJ. 2014. Leptin metabolically licenses T cells for activation to link nutrition and immunity. J Immunol 192:136-144. http://dx.doi.org/10.4049/jimmunol.1301158.
22. Palacio A, Lopez M, Perez-Bravo F, Monkeberg F, Schlesinger L. 2002. Leptin levels are associated with immune response in malnourished infants. J Clin Endocrinol Metab 87:3040-3046. http://dx.doi.org/10.1210/jcem.87.7.8636.
23. Soliman AT, El Zalabany MM, Salama M, Ansari BM. 2000. Serum leptin concentrations during severe protein-energy malnutrition: correlation with growth parameters and endocrine function. Metabolism 49:819-825. http://dx.doi.org/10.1053/meta.2000.6745.
24. Howard JK, Lord GM, Matarese G, Vendetti S, Ghatei MA, Ritter MA, Lechler RI, Bloom SR. 1999. Leptin protects mice from starvationinduced lymphoid atrophy and increases thymic cellularity in ob/ob mice. J Clin Invest 104:1051-1059. http://dx.doi.org/10.1172/JCI6762.
25. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. 1998. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394:897-901. http://dx.doi.org/10.1038/29795.
26. Hoang T, Aagaard C, Dietrich J, Cassidy JP, Dolganov G, Schoolnik GK, Lundberg CV, Agger EM, Andersen P. 2013. ESAT-6 (EsxA) and TB10.4 (EsxH) based vaccines for pre- and post-exposure tuberculosis vaccination. PLoS One 8:e80579. http://dx.doi.org/10.1371/journal.pone.0080579.
27. Agger EM, Rosenkrands I, Hansen J, Brahimi K, Vandahl BS, Aagaard C, Werninghaus K, Kirschning C, Lang R, Christensen D, Theisen M, Follmann F, Andersen P. 2008. Cationic liposomes formulated with synthetic mycobacterial cordfactor (CAF01): a versatile adjuvant for vaccines with different immunological requirements. PLoS One 3:e3116. http://dx.doi.org/10.1371/journal.pone.0003116.
28. Weinrich Olsen A, van Pinxteren LA, Meng Okkels L, Birk Rasmussen P, Andersen P. 2001. Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Infect Immun 69:2773-2778. http://dx.doi.org/10.1128/IAI.69.5.2773-2778.2001.
29. Hoang TT, Nansen A, Roy S, Billeskov R, Aagaard C, Elvang T, Dietrich J, Andersen P. 2009. Distinct differences in the expansion and phenotype of TB10.4 specific CD8 and CD4 T cells after infection with Mycobacterium tuberculosis. PLoS One 4:e5928. http://dx.doi.org/10.1371/journal.pone.0005928.
30. Lindenstrøm T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, Seder RA, Rosenkrands I, Andersen P. 2009. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 182:8047-8055. http://dx.doi.org/10.4049/jimmunol.0801592.
31. Mainali ES, McMurray DN. 1998. Protein deficiency induces alterations in the distribution of T-cell subsets in experimental pulmonary tuberculosis. Infect Immun 66:927-931.
32. Lin PL, Dietrich J, Tan E, Abalos RM, Burgos J, Bigbee C, Bigbee M, Milk L, Gideon HP, Rodgers M, Cochran C, Guinn KM, Sherman DR, Klein E, Janssen C, Flynn JL, Andersen P. 2012. The multistage vaccine H56 boosts the effects of BCG to protect cynomolgus macaques against active tuberculosis and reactivation of latent Mycobacterium tuberculosis infection. J Clin Invest 122:303-314. http://dx.doi.org/10.1172/JCI46252.
33. Boelaert JR, Gordeuk VR. 2002. Protein energy malnutrition and risk of tuberculosis infection. Lancet 360:1102. http://dx.doi.org/10.1016/S0140-6736(02)11169-X.
34. Keusch GT. 2003. The history of nutrition: malnutrition, infection and immunity. J Nutr 133:336S-340S.
35. Schaible UE, Kaufmann SH. 2007. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med 4:e115. http://dx.doi.org/10.1371/journal.pmed.0040115.
36. Cegielski JP, Arab L, Cornoni-Huntley J. 2012. Nutritional risk factors for tuberculosis among adults in the United States, 1971-1992. Am J Epidemiol 176:409-422. http://dx.doi.org/10.1093/aje/kws007.
37. Faber K. 1938. Tuberculosis and nutrition. Acta Tuberc Scand 12:306-309.
38. McMurray DN, Bartow RA. 1992. Immunosuppression and alteration of resistance to pulmonary tuberculosis in guinea pigs by protein undernutrition. J Nutr 122:738-743.
39. Nussler AK, Billiar TR. 1993. Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 54:171-178.
40. Ishikawa LL, Franca TG, Chiuso-Minicucci F, Zorzella-Pezavento SF, Marra NM, Pereira PC, Silva CL, Sartori A. 2009. Dietary restriction abrogates antibody production induced by a DNA vaccine encoding the mycobacterial 65 kDa heat shock protein. Genet Vaccines Ther 7:11. http://dx.doi.org/10.1186/1479-0556-7-11.
41. Sugawara I, Yamada H, Mizuno S. 2007. BCG vaccination enhances resistance to M. tuberculosis infection in guinea pigs fed a low casein diet. Tohoku J Exp Med 211:259-268. http://dx.doi.org/10.1620/tjem.211.259.
42. Malafaia G, Serafim TD, Silva ME, Pedrosa ML, Rezende SA. 2009. Protein-energy malnutrition decreases immune response to Leishmania chagasi vaccine in BALB/c mice. Parasite Immunol 31:41-49. http://dx.doi.org/10.1111/j.1365-3024.2008.01069.x.
43. Mussi-Pinhata MM, Goncalves AL, Foss NT. 1993. BCG vaccination of full-term infants with chronic intrauterine malnutrition: influence of immunization age on development of post-vaccination, delayed tuberculin hypersensitivity. Bull World Health Organ 71:41-48.
44. Roth A, Jensen H, Garly ML, Djana Q, Martins CL, Sodemann M, Rodrigues A, Aaby P. 2004. Low birth weight infants and Calmette-Guerin bacillus vaccination at birth: community study from Guinea-Bissau. Pediatr Infect Dis J 23:544-550. http://dx.doi.org/10.1097/01.inf.0000129693.81082.a0.
45. McMurray DN, Mintzer CL, Bartow RA, Parr RL. 1989. Dietary protein deficiency and Mycobacterium bovis BCG affect interleukin-2 activity in experimental pulmonary tuberculosis. Infect Immun 57:2606-2611.
46. Lindenstrøm T, Knudsen NP, Agger EM, Andersen P. 2013. Control of chronic Mycobacterium tuberculosis infection by CD4 KLRG1-IL-2-secreting central memory cells. J Immunol 190:6311-6319. http://dx.doi.org/10.4049/jimmunol.1300248.
47. Seder RA, Darrah PA, Roederer M. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8:247-258. http://dx.doi.org/10.1038/nri2274.
48. Iyer SS, Chatraw JH, Tan WG, Wherry EJ, Becker TC, Ahmed R, Kapasi ZF. 2012. Protein energy malnutrition impairs homeostatic proliferation of memory CD8 T cells. J Immunol 188:77-84. http://dx.doi.org/10.4049/jimmunol.1004027.
49. White SJ, Taylor MJ, Hurt RT, Jensen MD, Poland GA. 2013. Leptinbased adjuvants: an innovative approach to improve vaccine response. Vaccine 31:1666-1672. http://dx.doi.org/10.1016/j.vaccine.2013.01.032.
50. Carr EL, Kelman A, Wu GS, Gopaul R, Senkevitch E, Aghvanyan A, Turay AM, Frauwirth KA. 2010. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol 185:1037-1044. http://dx.doi.org/10.4049/jimmunol.0903586.
51. Horio Y, Osawa S, Takagaki K, Hishida A, Furuta T, Ikuma M. 2008. Glutamine supplementation increases Th1-cytokine responses in murine intestinal intraepithelial lymphocytes. Cytokine 44:92-95. http://dx.doi.org/10.1016/j.cyto.2008.06.011.
52. Scanga CA, Mohan VP, Tanaka K, Alland D, Flynn JL, Chan J. 2001. The inducible nitric oxide synthase locus confers protection against aerogenic challenge of both clinical and laboratory strains of Mycobacterium tuberculosis in mice. Infect Immun 69:7711-7717. http://dx.doi.org/10.1128/IAI.69.12.7711-7717.2001.
53. Chan J, Xing Y, Magliozzo RS, Bloom BR. 1992. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 175:1111-1122. http://dx.doi.org/10.1084/jem.175.4.1111.
54. Wu G, Flynn NE, Flynn SP, Jolly CA, Davis PK. 1999. Dietary protein or arginine deficiency impairs constitutive and inducible nitric oxide synthesis by young rats. J Nutr 129:1347-1354.
55. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77:4911-4927. http://dx.doi.org/10.1128/JVI.77.8.4911-4927.2003.
56. McMurray DN, Bartow RA, Mintzer C. 1990. Malnutrition-induced impairment of resistance against experimental pulmonary tuberculosis. Prog Clin Biol Res 325:403-412.