Acute helminth infection enhances early macrophage mediated control of mycobacterial infection

Mucosal Immunology

Volumn 6, Issue 5, 2013, Pages 931-941

  Du Plessis, N ^a   Kleynhans, L ^a   Thiart, L ^a   Van Helden, P D ^a   Brombacher, F ^b,c   Horsnell, W G C ^b,c   Walzl, G ^a  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BOVINE TUBERCULOSIS; CD4+ T LYMPHOCYTE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DISEASE SEVERITY; FEMALE; HELMINTHIASIS; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; MEDIASTINUM LYMPH NODE; MOUSE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL;

ACUTE DISEASE; ADOPTIVE TRANSFER; ANIMALS; BACTERIAL LOAD; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COINFECTION; CYTOKINES; FEMALE; LUNG; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS; TH1-TH2 BALANCE; TUBERCULOSIS, PULMONARY;

EID: 84883141435     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.131     Document Type: Article

References (61)

1. Mauad, T. et al. Lung pathology in fatal novel human influenza A (H1N1) infection. Am. J. Respir. Crit. Care Med. 181, 72-79 (2010
2. Iverson, A.R. et al. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J. Infect. Dis. 203, 880-888 (2011
3. Brooker, S., Bethony, J. & Hotez, P.J. Human hookworm infection in the 21st Century. Adv. Parasitol. 58, 197-288 (2004
4. Savioli, L. & Albonico, M. Focus: Soil-transmitted helminthiasis. Nat. Rev. Microbiol. 2, 618-619 (2004
5. Maizels, R.M. et al. Helminth parasites-masters of regulation. Immunol. Rev. 201, 89-116 (2004
6. Brooker, S., Hotez, P.J. & Bundy, D.A.P. The global atlas of helminth infection: Mapping the way forward in neglected tropical disease control. PLoS Negl. Trop. Dis. 4, e779 (2010
7. Lienhardt, C. et al. Active tuberculosis in Africa is associated with reduced Th1 and increased Th2 activity in vivo. Eur. J. Immunol. 32, 1605-1613 (2002
8. Jackson, J.A., Friberg, I.M., Little, S. & Bradley, J.E. Review series on helminths, immune modulation and the hygiene hypothesis: Immunity against helminths and immunological phenomena in modern human populations: Coevolutionary legacies?. Immunology 126, 18-27 (2009
9. Kidd, P. Th1/Th2 balance: The hypothesis, its limitations, and implications for health and disease. Altern Med. Rev. 8, 223-246 (2003
10. Moreau, E. & Chauvin, A. Immunity against helminths: Interactions with the host and the intercurrent infections. J. Biomed. Biotechnol. 2010, 1-10 (2010
11. Elias, D., Akuffo, H. & Britton, S. Helminthes could influence the outcome of vaccines against TB in the tropics. Parasite Immunol. 28, 507-513 (2006
12. Elias, D.,Britton, S., Kassu, A. & Akuffo,H.Chronic helminth infections may negatively influence immunity against tuberculosis and other diseases of public health importance. Expert Rev. Anti-infective Ther. 5, 475-484 (2007
13. Rook, G.A.W. Th2 cytokines in susceptibility to tuberculosis. Curr. Mol. Med. 7, 327-337 (2007
14. Adams, J.F. et al. Decline in total serum IgE after treatment for tuberculosis. Lancet 353, 2030-2033 (1999
15. Elias, D. et al. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine 23, 1326-1334 (2005
16. Elias, D., Akuffo, H., Thors, C., Pawlowski, A. & Britton, S. Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin. Exp. Immunol. 139, 398-404 (2005
17. Elias, D. et al. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Gué rin (BCG) vaccination. Clin. Exp. Immunol. 123, 219-225 (2001
18. Erb, K.J., Trujillo, C., Fugate, M. & Moll, H. Infection with the helminth nippostrongylus brasiliensis does not interfere with efficient elimination of mycobacterium bovis BCG from the lungs of mice. Clin. Diagn. Lab. Immunol. 9, 727-730 (2002
19. Potian, J.A. et al. Preexisting helminth infection induces inhibition of innate pulmonary anti-tuberculosis defense by engaging the IL-4 receptor pathway. J. Exp. Med. 208, 1863-1874 (2011
20. Fulton, S.A., Martin, T.D., Redline, R.W. & Henry Boom, W. Pulmonary immune responses during primary mycobacteriumbovis-Calmette-Guerin bacillus infection in C57Bl/6 mice. Am. J. Respir. Cell Mol. Biol. 22, 333-343 (2000
21. Camberis, M., Le Gros, G. & Urban, J. Jr Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr. Protoc. Immunol. Chapter 19, Unit 19.12 (2003
22. Loukas, A. & Prociv, P. Immune responses in hookworm infections. Clin. Microbiol. Rev. 14, 689-703 (2001
23. Marsland, B.J., Kurrer, M., Reissmann, R., Harris, N.L. & Kopf, M. Nippostrongylus brasiliensis infection leads to the development of emphysema associated with the induction of alternatively activated macrophages. Eur. J. Immunol. 38, 479-488 (2008
24. Ramaswamy, K., De Sanctis, G.T., Green, F. & Befus, D. Pathology of pulmonary parasiticmigration: Morphological and bronchoalveolar cellular responses following Nippostrongylus brasiliensis infection in rats. J. Parasitol. 77, 302-312 (1991
25. Marsland, B.J., Camberis, M. & Le Gros, G. Secretory products from infective forms of Nippostrongylus brasiliensis induce a rapid allergic airway inflammatory response. Immunol. Cell Biol. 83, 40-47 (2005
26. Reece, J.J., Siracusa, M.C. & Scott, A.L. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect. Immun. 74, 4970-4981 (2006
27. Lawrence, R.A., Gray, C.A., Osborne, J. & Maizels, R.M. Nippostrongylus brasiliensis: Cytokine responses and nematode expulsion in normal and IL-4-deficient mice. Exp. Parasitol. 84, 65-73 (1996
28. Leversen, N.A., Sviland, L., Wiker, H.G. & Mustafa, T. Long-term persistence of BCG Pasteur in lungs of C57BL/6 mice following intranasal infection. Scand. J. Immunol. 75, 489-499 (2012
29. Mills, C.D., Kincaid, K., Alt, J.M., Heilman, M.J. & Hill, A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164, 6166-6173 (2000
30. Bot, A., Smith, K.A. & von Herrath, M. Molecular and cellular control of T1/T2 immunity at the interface between antimicrobial defense and immune pathology. DNA Cell Biol. 23, 341-350 (2004
31. Gallegos, A.M., Pamer, E.G. & Glickman, M.S. Delayed protection by ESAT-6-specific effector CD4+ T cells after airborne M. tuberculosis infection. J. Exp. Med. 205, 2359-2368 (2008
32. Gu, N. et al. Intelectin is required for IL-13-inducedmonocyte chemotactic protein-1 and -3 expression in lung epithelial cells and promotes allergic airway inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L290-L296 (2010
33. Jenkins, S.J. et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332, 1284-1288 (2011
34. Classen, A., Lloberas, J. & Celada, A. Macrophage activation: Classical versus alternative. Methods Mol. Biol. 531, 29-43 (2009
35. Hartgers, F.C. & Yazdanbakhsh, M. Co-infection of helminths and malaria: Modulation of the immune responses to malaria. Parasite Immunol. 28, 497-506 (2006
36. Brown, M. et al. Schistosoma mansoni, nematode infections, and progression to active tuberculosis among HIV-1-infected Ugandans. Am. J. Trop. Med. Hyg. 74, 819-825 (2006
37. Hoeve, M.A. et al. Plasmodium chabaudi limits early Nippostrongylus brasiliensis-induced pulmonary immune activation and Th2 polarization in co-infected mice. BMC Immunol. 10, 602009
38. Gordon, S. & Martinez, F.O. Alternative activation of macrophages: Mechanism and functions. Immunity 32, 593-604 (2010
39. Silva, M.T., Silva, M.N. & Appelberg, R. Neutrophil-macrophage cooperation in the host defence against mycobacterial infections. Microb. Pathog. 6, 369-380 (1989
40. Silva, M.T. When two is better than one: Macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 87, 93-106 (2010
41. Tan, B.H. et al. Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol. 177, 1864-1871 (2006
42. Mackaness, G.B. The influence of immunologically committed lymphoid cells on macrophage activity in vivo. J. Exp. Med. 129, 973-992 (1969
43. Sieve, A.N. et al. A novel IL-17-dependent mechanism of cross protection: Respiratory infection with mycoplasma protects against a secondary listeria infection. Eur. J. Immunol. 39, 426-438 (2009
44. Wolf, A.J. et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J. Exp. Med. 205, 105-115 (2008
45. Chackerian, A.A., Alt, J.M., Perera, T.V., Dascher, C.C. & Behar, S.M. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect. Immun. 70, 4501-4509 (2002
46. Gonzalez-Juarrero, M. et al. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect. Immun. 69, 1722-1728 (2001
47. Huffman, J.A., Hull, W.M., Dranoff, G., Mulligan, R.C. & Whitsett, J.A. Pulmonary epithelial cell expression of GM-CSF corrects the alveolar proteinosis in GM-CSF-deficient mice. J. Clin. Invest. 97, 649-655 (1996
48. Shibata, Y. et al. GM-CSF regulates alveolar macrophage differentiation and innate immunity in the lung through PU.1. Immunity 15, 557-567 (2001
49. Higgins, D.M. et al. Relative levels of M-CSF and GM-CSF influence the specific generation of macrophage populations during infection with Mycobacterium tuberculosis. J. Immunol. 180, 4892-4900 (2008
50. Peyron, P. et al. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog. 4, e10002042008
51. Vijayan, V.K. Tropical parasitic lung diseases. Indian J. Chest Dis. Allied Sci. 50 49-66 (2008
52. Donnelly, S., Dalton, J.P. & Loukas, A. Proteases in helminth- and allergeninduced inflammatory responses. Chem. Immunol. Allergy 90, 45-64 (2006
53. Inghammar, M. et al. COPD and the risk of tuberculosis-A populationbased Cohort study. PLoS ONE 5, e10138 (2010
54. Varin, A., Mukhopadhyay, S., Herbein, G. & Gordon, S. Alternative activation of macrophages by IL-4 impairs phagocytosis of pathogens but potentiates microbial-induced signalling and cytokine secretion. Blood 115, 353-362 (2010
55. Krysko, O. et al. Alternatively activated macrophages and impaired phagocytosis of S. aureus in chronic rhinosinusitis. Allergy 66, 396-403 (2011
56. Shapiro, S.D. et al. Neutrophil elastase contributes to cigarette smokeinduced emphysema in mice. Am. J. Pathol. 163, 2329-2335 (2003
57. Mearns, H. et al. Interleukin-4-promoted T helper 2 responses enhance Nippostrongylus brasiliensis-induced pulmonary pathology. Infect. Immun. 76 5535-5542 (2008
58. Anis, M.M., Fulton, S.A., Reba, S.M., Harding, C.V. & Boom, W.H. Modulation of naive CD4+ T-cell responses to an airway antigen during pulmonary mycobacterial infection. Infect. Immun. 75, 2260-2268 (2007
59. Hiraoka, M. et al. Lysosomal phospholipase A2 and phospholipidosis. Mol. Cell. Biol. 26, 6139-6148 (2006
60. Wiley John & Sons Current Protocols in Immunology-Current Protocols. Atohttp://cda.currentprotocols.com/WileyCDA/CPTitle/isbn-0471522767, descCd-tableOfContents.html4
61. Hamelin, M-È. et al. Pathogenesis of human metapneumovirus lung infection in BALB/c mice and cotton rats. J. Virol. 79, 8894-8903 (2005