Down regulation of the TCR complex CD3ζ-chain on CD3+ T cells: A potential mechanism for helminth-mediated immune modulation

Frontiers in Immunology

Volumn 6, Issue FEB, 2015, Pages

  Appleby, Laura J ^a,d   Nausch, Norman ^a,e   Heard, Francesca ^a   Erskine, Louise ^a   Bourke, Claire D ^a,f   Midzi, Nicholas ^b,c   Mduluza, Takafira ^c   Allen, Judith E ^a   Mutapi, Francisca ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b National Institute for Health Research   (Zimbabwe)

^c UNIVERSITY OF ZIMBABWE   (Zimbabwe)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^f QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Antibody; CD3 ; Downmodulation; Helminth; Human; Pathology; Schistosomiasis; T cells

Indexed keywords

CD3 ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; PRAZIQUANTEL; T LYMPHOCYTE RECEPTOR;

ADOLESCENT; ADULT; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; CD3+ T LYMPHOCYTE; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CHILD; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DISEASE TRANSMISSION; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOASSAY; IMMUNOMODULATION; INFECTION PREVENTION; INFECTION RATE; LINEAR REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; RECEPTOR DOWN REGULATION; RECOMMENDED DRUG DOSE; SCHISTOSOMIASIS HAEMATOBIA; SCHOOL CHILD; SIGNAL TRANSDUCTION;

EID: 84926624703     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00051     Document Type: Article

References (67)

1. Kenneth M, Paul T, Mark W, Charles J. Janeway's Immunobiology. New York, NY: Garland Science (2012).
2. Irving BA, Weiss A. The cytoplasmic domain of the T cell receptor γ chain is sufficient to couple to receptor-associated signal transduction pathways. Cell (1991) 64:891-901. doi:10.1016/0092-8674(91)90314-O
3. Baniyash M. TCR γ-chain downregulation: curtailing an excessive inflammatory immune response. Nat Rev Immunol (2004) 4:675-87. doi:10.1038/nri1434
4. Zea AH, Ochoa MT, Ghosh P, Longo DL, Alvord WG, Valderrama L, et al. Changes in expression of signal transduction proteins in T lymphocytes of patients with leprosy. Infect Immun (1998) 66:499-504.
5. Brundula V, Rivas LJ, Blasini AM, Paris M, Salazar S, Stekman IL, et al. Diminished levels of T cell receptor zeta chains in peripheral blood T lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum (1999) 42:1908-16. doi:10.1002/1529-0131(199909)42:9<1908::AID-ANR17>3.0.CO;2-7
6. Schule J, Bergkvist L, Hakansson L, Gustafsson B, Hakansson A. Down-regulation of the CD3-zeta chain in sentinel node biopsies from breast cancer patients. Breast Cancer Res Treat (2002) 74:33-40. doi:10.1023/A:1016009913699
7. Colley DG, Secor WE. Immunology of human schistosomiasis. Parasite Immunol (2014) 36:347-57. doi:10.1111/pim.12087
8. Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM. Immunopathogenesis of schistosomiasis. Immunol Rev (2004) 201:156-67. doi:10.1111/j.0105-2896.2004.00176.x
9. Caldas IR, Campi-Azevedo AC, Oliveira LF, Silveira AM, Oliveira RC, Gazzinelli G. Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection. Acta Trop (2008) 108:109-17. doi:10.1016/j.actatropica.2008.05.027
10. Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest (1999) 104:777-85. doi:10.1172/JCI7325
11. Gause WC, Wynn TA, Allen JE. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nat Rev Immunol (2013) 13:607-14. doi:10.1038/nri3476
12. Hesse M, Piccirillo CA, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M, et al. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol (2004) 172:3157-66. doi:10.4049/jimmunol.172.5.3157
13. Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, Kamgno J, et al. Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis (2008) 197:1204-12. doi:10.1086/586717
14. Hoffmann KF, James SL, Cheever AW, Wynn TA. Studies with double cytokine-deficient mice reveal that highly polarized Th1-and Th2-type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni. J Immunol (1999) 163:927-38.
15. Grogan J, Kremsner P, Deelder A, Yazdanbakhsh M. Antigen-specific proliferation and interferon-gamma and interleukin-5 production are down-regulated during Schistosoma haematobium infection. J Infect Dis (1998) 177:1433-7. doi:10.1086/517832
16. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, et al. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog (2009) 5:e1000371. doi:10.1371/journal.ppat.1000371
17. Yazdanbakhsh M. Common features of T cell reactivity in persistent helminth infections: lymphatic filariasis and schistosomiasis. Immunol Lett (1999) 65:109-15. doi:10.1016/S0165-2478(98)00133-3
18. Nutman TB, Kumaraswami V. Regulation of the immune response in lymphatic filariasis: perspectives on acute and chronic infection with Wuchereria bancrofti in South India. Parasite Immunol (2001) 23:389-99. doi:10.1046/j.1365-3024.2001.00399.x
19. Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol (2003) 3:733-44. doi:10.1038/nri1183
20. Graham AL, Allen JE, Read AF. Evolutionary causes and consequences of immunopathology. Annu Rev Ecol Evol Syst (2005) 36:373-97. doi:10.2307/30033809
21. Allen JE, Lawrence RA, Maizels RM. APC from mice harbouring the filarial nematode, Brugia malayi, prevent cellular proliferation but not cytokine production. Int Immunol (1996) 8:143-51. doi:10.1093/intimm/8.1.143
22. Grogan JL, Kremsner PG, Deelder AM, Yazdanbakhsh M. Elevated proliferation and interleukin-4 release from CD4+ cells after chemotherapy in human Schistosoma haematobium infection. Eur J Immunol (1996) 26:1365-70. doi:10.1002/eji.1830260628
23. Mduluza T, Ndhlovu P, Midzi N, Scott J, Mutapi F, Mary C, et al. Contrasting cellular responses in Schistosoma haematobium infected and exposed individuals from areas of high and low transmission in Zimbabwe. Immunol Lett (2003) 88:249-56. doi:10.1016/S0165-2478(03)00088-9
24. Elias D, Akuffo H, Pawlowski A, Haile M, Schon T, Britton S. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine (2005) 23:1326-34. doi:10.1016/j.vaccine.2004.09.038
25. Elliott AM, Kizza M, Quigley MA, Ndibazza J, Nampijja M, Muhangi L, et al. The impact of helminths on the response to immunization and on the incidence of infection and disease in childhood in Uganda: design of a randomized, double-blind, placebo-controlled, factorial trial of deworming interventions delivered in pregnancy and early childhood. Clin Trials (2007) 4:42-57. doi:10.1177/1740774506075248
26. Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol (2003) 24:302-6. doi:10.1016/S1471-4906(03)00132-7
27. Smits HH, Hartgers FC, Yazdanbakhsh M. Helminth infections: protection from atopic disorders. Curr Allergy Asthma Rep (2005) 5:42-50. doi:10.1007/s11882-005-0053-5
28. Koloski NA, Bret L, Radford-Smith G. Hygiene hypothesis in inflammatory bowel disease: a critical review of the literature. World J Gastroenterol (2008) 14:165-73. doi:10.3748/wjg.14.165
29. Fiasse R, Dewit O, Latinne D. Is endemic helminthiasis in sub-Saharan Africa the sole reason for the low prevalence of inflammatory bowel disease? Impacts on public health. [French]. J Afr Hepatogastroenterol (2009) 3:58-66. doi:10.1007/s12157-009-0077-x
30. Appleby LJ, Nausch N, Midzi N, Mduluza T, Allen JE, Mutapi F. Sources of heterogeneity in human monocyte subsets. Immunol Lett (2013) 152:32-41. doi:10.1016/j.imlet.2013.03.004
31. Midzi N, Sangweme D, Zinyowera S, Mapingure MP, Brouwer KC, Munatsi A, et al. The burden of polyparasitism among primary schoolchildren in rural and farming areas in Zimbabwe. Trans R Soc Trop Med Hyg (2008) 102:1039-45. doi:10.1016/j.trstmh.2008.05.024
32. WHO. Preventative Chemotherapy in Helminthiasis: Coordinated Use of Antihelminthic Drugs in Control Interventions: A Manual for Health Professionals and Programme Managers. Geneva: World Health Organization (2006).
33. Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo (1972) 14:397-400.
34. Mott K. A reusable polyamide filter for diagnosis of S. haematobium infection by urine filtration. Bull Soc Pathol Exot Filiales (1983) 76:101-4.
35. Mutapi F, Burchmore R, Foucher A, Harcus Y, Nicoll G, Midzi N, et al. Praziquantel treatment of people exposed to Schistosoma haematobium enhances serological recognition of defined parasite antigens. J Infect Dis (2005) 192:1108-18. doi:10.1086/432553
36. Mutapi F, Mduluza T, Gomez-Escobar N, Gregory WF, Fernandez C, Midzi N, et al. Immuno-epidemiology of human Schistosoma haematobium infection: preferential lgG3 antibody responsiveness to a recombinant antigen dependent on age and parasite burden. BMC Infect Dis (2006) 6:96. doi:10.1186/1471-2334-6-96
37. Nausch N, Louis D, Lantz O, Peguillet I, Trottein F, Chen IY, et al. Age-related patterns in human myeloid dendritic cell populations in people exposed to Schistosoma haematobium infection. PLoS Negl Trop Dis (2012) 6:e1824. doi:10.1371/journal.pntd.0001824
38. Anderson RM, May RM. Infectious Diseases of Humans: Dynamics and Control/Roy M. Anderson and Robert M. May. Oxford: Oxford University Press (1991). 1991 p.
39. Chandiwana SK, Woolhouse MEJ. Heterogeneities in water contact patterns and the epidemiology of Schistosoma haematobium. Parasitology (1991) 103:363-70. doi:10.1017/S0031182000059874
40. Mutapi F, Roddam A. p-values for pathogens: statistical inference from infectious-disease data. Lancet Infect Dis (2002) 2:219-30. doi:10.1016/S1473-3099(02)00240-2
41. Zea AH, Rodriguez PC, Culotta KS, Hernandez CP, Desalvo J, Ochoa JB, et al. L-Arginine modulates CD3γ expression and T cell function in activated human T lymphocytes. Cell Immunol (2004) 232:21-31. doi:10.1016/j.cellimm.2005.01.004
42. Mutapi F, Hagan P, Ndhlovu P, Woolhouse M. Comparison of humoral responses to Schistosoma haematobium in areas with high and low levels of infection. Parasite Immunol (1997) 19:255-63. doi:10.1046/j.1365-3024.1997.d01-206.x
43. Mutapi F, Ndhlovu P, Hagan P, Spicer J, Mduluza T, Turner C, et al. Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J Infect Dis (1998) 178:289-93. doi:10.1086/517456
44. Milner T, Reilly L, Nausch N, Midzi N, Mduluza T, Maizels R, et al. Circulating cytokine levels and antibody responses to human Schistosoma haematobium: IL-5 and IL-10 levels depend upon age and infection status. Parasite Immunol (2010) 32:710-21. doi:10.1111/j.1365-3024.2010.01235.x
45. Hagan P, Blumenthal U, Dunne D, Simpson A, Wilkins H. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature (1991) 349:243-5. doi:10.1038/349243a0
46. Webster M, Fulford AJ, Braun G, Ouma JH, Kariuki HC, Havercroft JC, et al. Human immunoglobulin E responses to a recombinant 22.6-kilodalton antigen from Schistosoma mansoni adult worms are associated with low intensities of reinfection after treatment. Infect Immun (1996) 64:4042-6.
47. Stavitsky AB, Olds GR, Peterson LB. Regulation of egg antigen-induced in vitro proliferative response by splenic suppressor T cells in murine Schistosoma japonicum infection. Infect Immun (1985) 49:635-40.
48. Sartono E, Kruize YCM, Kurniawan A, Maizels RM, Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. J Infect Dis (1997) 175:1276-80. doi:10.1086/593701
49. Su Z, Segura M, Morgan K, Loredo-Osti JC, Stevenson MM. Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect Immun (2005) 73:3531-9. doi:10.1128/IAI.73.6.3531-3539.2005
50. Hoffmann KF, Cheever AW, Wynn TA. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J Immunol (2000) 164:6406-16. doi:10.4049/jimmunol.164.12.6406
51. Wiskocil R, Weiss A, Imboden J, Kamin-Lewis R, Stobo J. Activation of a human T cell line: a two-stimulus requirement in the pretranslational events involved in the coordinate expression of interleukin 2 and gamma-interferon genes. J Immunol (1985) 134:1599-603.
52. Ceuppens JL, Baroja ML, Lorre K, Van Damme J, Billiau A. Human T cell activation with phytohemagglutinin. The function of IL-6 as an accessory signal. J Immunol (1988) 141:3868-74.
53. Ndhlovu P, Cadman H, Vennervald B, Christensen N, Chidimu N, Chandiwana S. Age-related antibody profiles in Schistosoma haematobium in a rural community in Zimbabwe. Parasite Immunol (1996) 18:181-91. doi:10.1046/j.1365-3024.1996.d01-78.x
54. Mutapi F, Bourke C, Harcus Y, Midzi N, Mduluza T, Turner CM, et al. Differential recognition patterns of Schistosoma haematobium adult worm antigens by the human antibodies IgA, IgE, IgG1 and IgG4. Parasite Immunol (2011) 33:181-92. doi:10.1111/j.1365-3024.2010.01270.x
55. Silveira AM, Bethony J, Gazzinelli A, Kloos H, Fraga LA, Alvares MC, et al. High levels of IgG4 to Schistosoma mansoni egg antigens in individuals with periportal fibrosis. Am J Trop Med Hyg (2002) 66:542-9.
56. Woolhouse M, Hagan P. Seeking the ghost of worms past. Nat Med (1999) 5:1225-7. doi:10.1038/15169
57. Butterworth AE, Fulford AJ, Dunne DW, Ouma JH, Sturrock RF. Longitudinal studies on human schistosomiasis. Philos Trans R Soc Lond B Biol Sci (1988) 321:495-511. doi:10.1098/rstb.1988.0105
58. Woolhouse M, Taylor P, Matanhire D, Chandiwana S. Acquired immunity and epidemiology of Schistosoma haematobium. Nature (1991) 351:757-9. doi:10.1038/351757a0
59. Mutapi F, Imai N, Nausch N, Bourke CD, Rujeni N, Mitchell KM, et al. Schistosome infection intensity is inversely related to auto-reactive antibody levels. PLoS One (2011) 6:e19149. doi:10.1371/journal.pone.0019149
60. Rujeni N, Nausch N, Bourke CD, Midzi N, Mduluza T, Taylor DW, et al. Atopy is inversely related to schistosome infection intensity: a comparative study in Zimbabwean villages with distinct levels of Schistosoma haematobium infection. Int Arch Allergy Immunol (2012) 158:288-98. doi:10.1159/000332949
61. Borkow G, Bentwich Z. Chronic parasite infections cause immune changes that could affect successful vaccination. Trends Parasitol (2008) 24:243-5. doi:10.1016/j.pt.2008.02.009
62. Ezernitchi AV, Vaknin I, Cohen-Daniel L, Levy O, Manaster E, Halabi A, et al. TCR γ down-regulation under chronic inflammation is mediated by myeloid suppressor cells differentially distributed between various lymphatic organs. J Immunol (2006) 177:4763-72. doi:10.4049/jimmunol.177.7.4763
63. Rodríguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev (2008) 222:180-91. doi:10.1111/j.1600-065X.2008.00608.x
64. Everts B, Adegnika AA, Kruize YC, Smits HH, Kremsner PG, Yazdanbakhsh M. Functional impairment of human myeloid dendritic cells during Schistosoma haematobium infection. PLoS Negl Trop Dis (2010) 4:e667. doi:10.1371/journal.pntd.0000667
65. Jenkins SJ, Allen JE. Similarity and diversity in macrophage activation by nematodes, trematodes, and cestodes. J Biomed Biotechnol (2010) 2010:262609. doi:10.1155/2010/262609
66. Munder M. Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol (2009) 158:638-51. doi:10.1111/j.1476-5381.2009.00291.x
67. Darcy CJ, Minigo G, Piera KA, Davis JS, McNeil YR, Chen Y, et al. Neutrophils with myeloid derived suppressor function deplete arginine and constrain T cell function in septic shock patients. Crit Care (2014) 18:R163. doi:10.1186/cc14003