Chronic Trypanosoma congolense infections in mice cause a sustained disruption of the B-cell homeostasis in the bone marrow and spleen

Parasite Immunology

Volumn 36, Issue 5, 2014, Pages 187-198

  Obishakin, E ^a,b   de Trez, C ^a,b   Magez, S ^a,b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

B cell depletion; ELISA Enzyme linked immunosorbent assay; Flow cytometry; Trypanosoma congolense; Trypanosomosis; Vaccination

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; PARASITE ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; BONE MARROW; C57BL 6 MOUSE; CELL MATURATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE SEVERITY; EXPERIMENTAL INFECTION; FEMALE; HOMEOSTASIS; LYMPHOCYTE DEPLETION; LYMPHOPOIESIS; MOLECULAR CLONING; MOUSE; MOUSE MODEL; NAGANA; NONHUMAN; PARASITE VIRULENCE; PARASITEMIA; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SPLEEN; SURVIVAL;

B-CELL DEPLETION; ELISA/ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; TRYPANOSOMA CONGOLENSE; TRYPANOSOMOSIS; VACCINATION;

ANIMALS; ANTIBODIES, PROTOZOAN; B-LYMPHOCYTES; BONE MARROW; BONE MARROW CELLS; CELL COUNT; FEMALE; HOMEOSTASIS; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; PARASITEMIA; SPLEEN; TRYPANOSOMA CONGOLENSE; TRYPANOSOMIASIS, AFRICAN; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA; VIRULENCE;

EID: 84897938123     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12099     Document Type: Article

References (54)

1. Bockstal V, Guirnalda P, Caljon G, et al. T. brucei infection reduces B lymphopoiesis in bone marrow and truncates compensatory splenic lymphopoiesis through transitional B-cell apoptosis. PLoS Pathog 2011; 7: e1002089.
2. Coustou V, Guegan F, Plazolles N & Baltz T. Complete in vitro life cycle of Trypanosoma congolense: development of genetic tools. PLoS Negl Trop Dis 2010; 4: e618.
3. Peacock L, Cook S, Ferris V, Bailey M & Gibson W. The life cycle of Trypanosoma (Nannomonas) congolense in the tsetse fly. Parasit Vectors 2012; 5: 109.
4. Baral TN, De Baetselier P, Brombacher F & Magez S. Control of Trypanosoma evansi infection is IgM mediated and does not require a type I inflammatory response. J Infect Dis 2007; 195: 1513-1520.
5. Saerens D, Stijlemans B, Baral TN, et al. Parallel selection of multiple anti-infectome nanobodies without access to purified antigens. J Immunol Methods 2008; 329: 138-150.
6. Ojok L, Kaeufer-Weiss I & Weiss E. Distribution of Trypanosoma congolense in infected multimammate rats (Mastomys coucha): light and electron microscopical studies. Vet Parasitol 2002; 105: 327-336.
7. Morrison L & MacLeod A. African trypanosomiasis. Parasite Immunol 2011; 33: 421-422.
8. Kuriakose S, Muleme HM, Onyilagha C, Singh R, Jia P & Uzonna JE. Diminazene aceturate (Berenil) modulates the host cellular and inflammatory responses to Trypanosoma congolense infection. PLoS ONE 2012; 7: e48696.
9. La Greca F & Magez S. Vaccination against trypanosomiasis: can it be done or is the trypanosome truly the ultimate immune destroyer and escape artist? Hum Vaccin 2011; 7: 1225-1233.
10. Lu W, Wei G, Pan W & Tabel H. Trypanosoma congolense infections: induced nitric oxide inhibits parasite growth in vivo. J Parasitol Res 2011; 2011: 316067.
11. Antoine-Moussiaux N, Büscher P & Desmecht D. Host-parasite interactions in trypanosomiasis: on the way to an antidisease strategy. Infect Immun 2009; 77: 1276-1284.
12. Vickerman K. Antigenic variation in the trypanosome. Nature 1978; 273: 613-617.
13. Askonas B. Macrophages as mediators of immunosuppression in murine African trypanosomiasis. Curr Top Microbiol Immunol 1985; 117: 119-127.
14. Schleifer KW & Mansfield JM. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J Immunol 1993; 151: 5492-5503.
15. Darji A, Lucas R, Magez S, et al. Mechanisms underlying trypanosome-elicited immunosuppression. Ann Soc Belg Med Trop 1992; 72: 27-38.
16. Blom-Potar MC, Chamond N, Cosson A, et al. Trypanosoma vivax infections: pushing ahead with mouse models for the study of Nagana. II. Immunobiological dysfunctions. PLoS Negl Trop Dis 2010; 4: e793.
17. Radwanska M, Guirnalda P, De Trez C, Ryffel B, Black S & Magez S. Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog 2008; 4: e1000078.
18. Magez S, Radwanska M, Drennan M, et al. Interferon-γ and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 infections. J Infect Dis 2006; 193: 1575-1583.
19. Guilliams M, Oldenhove G, Noel W, et al. African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation. J Immunol 2007; 179: 2748-2757.
20. Ogunremi O & Tabel H. Genetics of resistance to Trypanosoma congolense in inbred mice: efficiency of apparent clearance of parasites correlates with long-term survival. J Parasitol 1995; 81: 876-881.
21. Namangala B, de Baetselier P, Brijs L, et al. Attenuation of Trypanosoma brucei is associated with reduced immunosuppression and concomitant production of Th2 lymphokines. J Infect Dis 2000; 181: 1110-1120.
22. Loder F & Mutschler B, Ray RJ, et al. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J Exp Med 1999; 190: 75-90.
23. Teague BN, Pan Y, Mudd PA, et al. Cutting edge: Transitional T3 B cells do not give rise to mature B cells, have undergone selection, and are reduced in murine lupus. J Immunol 2007; 178: 7511-7515.
24. Lopes-Carvalho T & Kearney JF. Development and selection of marginal zone B cells. Immunol Rev 2004; 197: 192-205.
25. Martin F & Kearney JF. Marginal-zone B cells. Nat Rev Immunol 2002; 2: 323-335.
26. Cariappa A, Mazo IB, Chase C, et al. Perisinusoidal B cells in the bone marrow participate in T-independent responses to blood-borne microbes. Immunity 2005; 23: 397-407.
27. Pillai S & Cariappa A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat Rev Immunol 2009; 9: 767-777.
28. Cariappa A, Chase C, Liu H, Russell P & Pillai S. Naive recirculating B cells mature simultaneously in the spleen and bone marrow. Blood 2007; 109: 2339-2345.
29. Cambier JC, Gauld SB, Merrell KT & Vilen BJ. B-cell anergy: from transgenic models to naturally occurring anergic B cells? Nat Rev Immunol 2007; 7: 633-643.
30. Stefan M, Magdalena R. Trypanosomes and Trypanosomiasis. Vienna, Springer, 2014. 294.
31. Morrison WI, Roelants GE, Mayor-Withey KS & Murray M. Susceptibility of inbred strains of mice to Trypanosoma congolense: correlation with changes in spleen lymphocyte populations. Clin Exp Immunol 1978; 32: 25-40.
32. Geysen D, Delespaux V & Geerts S. PCR-RFLP using Ssu-rDNA amplification as an easy method for species-specific diagnosis of Trypanosoma species in cattle. Vet Parasitol 2003; 110: 171-180.
33. Lanham SM. Separation of trypanosomes from the blood of infected rats and mice by anion-exchangers. Nature 1968; 218: 1273-1274.
34. Lanham SM & Godfrey DG. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol 1970; 28: 521-534.
35. Pletinckx K, Stijlemans B, Pavlovic V, et al. Similar inflammatory DC maturation signatures induced by TNF or Trypanosoma brucei antigens instruct default Th2-cell responses. Eur J Immunol 2011; 41: 3479-3494.
36. Magez S, Stijlemans B, Caljon G, Eugster H-P & De Baetselier P. Control of experimental Trypanosoma brucei infections occurs independently of lymphotoxin-α induction. Infect Immun 2002; 70: 1342-1351.
37. Borst P. Molecular genetics of antigenic variation. Immunol Today 1991; 12: A29-A33.
38. Roelants GE & Pinder M. Immunobiology of African trypanosomiasis. Contemp Top Immunobiol 1984; 12: 225-274.
39. Frevert U & Reinwald E. Trypanosoma congolense bloodstream forms evade complement lysis in vitro by shedding of immune complexes. Eur J Cell Biol 1990; 52: 264-269.
40. Mansfield JM & Kreier JP. Autoimmunity in experimental Trypanosoma congolense infections of rabbits. Infect Immun 1972; 5: 648-656.
41. Buza J, Sileghem M, Gwakisa P & Naessens J. CD5+ B lymphocytes are the main source of antibodies reactive with non-parasite antigens in Trypanosoma congolense-infected cattle. Immunology 1997; 92: 226-233.
42. Tabel H. Activation of the alternative pathway of bovine complement by Trypanosoma congolense. Parasite Immunol 1982; 4: 329-335.
43. Wei G, Bull H, Zhou X & Tabel H. Intradermal infections of mice by low numbers of African trypanosomes are controlled by innate resistance but enhance susceptibility to reinfection. J Infect Dis 2011; 203: 418-429.
44. Cerutti A, Cols M & Puga I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol 2013; 13: 118-132.
45. Tabel H, Wei G & Shi M. T cells and immunopathogenesis of experimental African trypanosomiasis. Immunol Rev 2008; 225: 128-139.
46. Shi M, Wei G, Pan W & Tabel H. Trypanosoma congolense infections: antibody-mediated phagocytosis by Kupffer cells. J Leukoc Biol 2004; 76: 399-405.
47. Bockstal V, Geurts N & Magez S. Acute disruption of bone marrow b lymphopoiesis and apoptosis of transitional and marginal zone b cells in the spleen following a blood-stage Plasmodium chabaudi infection in mice. J Parasitol Res 2011; 2011: 534697.
48. Achtman AH, Khan M, MacLennan ICM & Langhorne J. Plasmodium chabaudi chabaudi infection in mice induces strong B cell responses and striking but temporary changes in splenic cell distribution. J Immunol 2003; 171: 317-324.
49. Ojok L, Kaeufer-Weiss I & Weiss E. Bone marrow response to acute and chronic Trypanosoma congolense infection in multimammate rats (Mastomys coucha). J Comp Pathol 2001; 124: 149-158.
50. Traggiai E, Casati A, Frascoli M, et al. Selective preservation of bone marrow mature recirculating but not marginal zone B cells in murine models of chronic inflammation. PLoS ONE 2010; 5: e11262.
51. Anosa V & Kaneko J. Pathogenesis of Trypanosoma brucei infection in deer mice (Peromyscus maniculatus): hematologic, erythrocyte biochemical, and iron metabolic aspects. Am J Vet Res 1983; 44: 639.
52. Taiwo V, Adejinmi J & Oluwaniyi J. Non-immune control of trypanosomosis: in vitro oxidative burst of PMA-and trypanosome-stimulated neutrophils of Boran and N'Dama cattle. Onderstepoort J Vet Res 2002; 69: 43.
53. Nagaoka H, Gonzalez-Aseguinolaza G, Tsuji M & Nussenzweig MC. Immunization and infection change the number of recombination activating gene (rag)-expressing B cells in the periphery by altering immature lymphocyte production. J Exp Med 2000; 191: 2113-2120.
54. Ueda Y, Yang K, Foster SJ, Kondo M & Kelsoe G. Inflammation controls B lymphopoiesis by regulating chemokine CXCL12 expression. J Exp Med 2004; 199: 47-58.