Macrophages are critical for cross-protective immunity conferred by babesia microti against babesia rodhaini infection in mice

Infection and Immunity

Volumn 80, Issue 1, 2012, Pages 311-320

  Li, Yan ^a   Terkawi, Mohamad Alaa ^a   Nishikawa, Yoshifumi ^a   Aboge, Gabriel Oluga ^a   Luo, Yuzi ^a   Ooka, Hideo ^a   Goo, Youn Kyoung ^a   Yu, Longzheng ^a   Cao, Shinuo ^a   Sun, Yongfeng ^a   Yamagishi, Junya ^a   Masatani, Tatsunori ^a   Yokoyama, Naoaki ^a   Igarashi, Ikuo ^a   Xuan, Xuenan ^a  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 8; NITRIC OXIDE; CYTOKINE; PROTOZOON ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BABESIA MICROTI INFECTION; BABESIA RODHAINI INFECTION; CONTROLLED STUDY; CROSS PROTECTION; CYTOKINE PRODUCTION; FEMALE; IMMUNIZATION; IN VIVO STUDY; INFECTION SENSITIVITY; LYMPHOCYTE DEPLETION; MACROPHAGE; MORTALITY; NATURAL KILLER CELL; NONHUMAN; PARASITEMIA; PARASITOSIS; PRIORITY JOURNAL; ANIMAL; BABESIA; BABESIOSIS; BAGG ALBINO MOUSE; BLOOD; IMMUNOLOGY; LEUKAPHERESIS; MOUSE; MOUSE MUTANT; PARASITOLOGY; SECRETION; SURVIVAL;

ANIMALS; ANTIBODIES, PROTOZOAN; BABESIA; BABESIOSIS; CROSS PROTECTION; CYTOKINES; FEMALE; LEUKOCYTE REDUCTION PROCEDURES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, SCID; PARASITEMIA; SURVIVAL ANALYSIS;

EID: 84863258192     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05900-11     Document Type: Article

References (58)

1. Aguilar-Delfin I, Homer MJ, Wettstein PJ, Persing DH. 2001. Innate resistance to Babesia infection is influenced by genetic background and gender. Infect. Immun. 69:7955-7958.
2. Aguilar-Delfin I, Wettstein PJ, Persing DH. 2003. Resistance to acute babesiosis is associated with interleukin-12- and gamma interferonmediated responses and requires macrophages and natural killer cells. Infect. Immun. 71:2002-2008.
3. Ahmed JS. 2002. The role of cytokines in immunity and immunopathogenesis of pirolasmoses. Parasitol. Res. 88(Suppl):S48-S50.
4. Allred DR, Cinque RM, Lane TJ, Ahrens KP. 1994. Antigenic variation of parasite-derived antigens on the surface of Babesia bovis-infected erythrocytes. Infect. Immun. 62:91-98.
5. Appelberg R. 2007. Neutrophils and intracellular pathogens: beyond phagocytosis and killing. Trends Microbiol. 15:87-92.
6. Barton ES, et al. 2007. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447:326-330.
7. Benach JL, Habicht GS, Holbrook TW, Cook JA. 1982. Glucan as an adjuvant for a murine Babesia microti immunization trial. Infect. Immun. 35:947-951.
8. Beutler B, Grau GE. 1993. Tumor necrosis factor in the pathogenesis of infectious diseases. Crit. Care Med. 21:S423- 435.
9. Brown WC, Palmer GH. 1999. Designing blood-stage vaccines against Babesia bovis and B. bigemina. Parasitol. Today 15:275-281.
10. Brown WC. 2001. Molecular approaches to elucidating innate and acquired immune responses to Babesia bovis, a protozoan parasite that causes persistent infection. Vet. Parasitol. 101:233-248.
11. Brown WC, Norimine J, Knowles DP, Goff WL. 2006. Immune control of Babesia bovis infection. Vet. Parasitol. 138:75- 87.
12. Chen D, Copeman DB, Burnell J, Hutchinson GW. 2000. Helper T cell and antibody responses to infection of CBA mice with Babesia microti. Parasite Immunol. 22:81- 88.
13. Clark IA, Richmond JE, Wills EJ, Allison AC. 1975. Immunity to intraerythrocytic protozoa. Lancet ii:1128-1129.
14. Clark IA, Alloson AC, Cox FE. 1976. Protection of mice against Babesia and Plasmodium with BCG. Nature 259:309-311.
15. Clark IA, Hunt NH. 1983. Evidence for reactive oxygen intermediates causing hemolysis and parasite death in malaria. Infect. Immun. 39:1- 6.
16. Clark IA, Hunt NH, Cowden WB. 1986. Oxygen-derived free radicals in the pathogenesis of parasitic disease. Adv. Parasitol. 25:1- 44.
17. Clark IA, Rockett KA, Cowden WB. 1992. TNF in malaria, p 303-328. InB. Beutler (ed.), Tumor necrosis factors: the molecules and their emerging role in medicine. Raven Press, Ltd, New York, NY.
18. Clark IA. 2001. Heterologous immunity revisited. Parasitology 122(Suppl):S51-S59.
19. Clawson ML, et al. 2002. Cellular immunity, but not gamma interferon, is essential for resolution of Babesia microti infection in BALB/c mice. Infect. Immun. 70:5304-5306.
20. Couper KN, et al. 2007. Macrophage-mediated but gamma interferonindependent innate immune responses control the primary wave of Plasmodium yoelii parasitemia. Infect. Immun. 75:5806-5818.
21. Couper KN, Blount DG, Riley EM. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180:5771-5777.
22. Cox FE. 1978. Heterologous immunity between piroplasms and malaria parasites: the simultaneous elimination of Plasmodium vinckei and Babesia microti from the blood of doubly infected mice. Parasitology 76:55- 60.
23. Gubernot DM, et al. 2009. Transfusion-transmitted babesiosis in the United States: summary of a workshop. Transfusion 49:2759-2771.
24. Hemmer RM, Ferrick DA, Conrad PA. 2000. Upregulation of tumor necrosis factor-alpha and interferon-gamma expression in the spleen and lungs of mice infected with the human Babesia isolate WA1. Parasitol. Res. 86:121-128.
25. - mice infected with the human Babesia WA1 parasite. J. Parasitol. 86:736-742.
26. Hildebrandt A, et al. 2007. First confirmed autochthonous case of human Babesia microti infection in Europe. Eur. J. Clin. Microbiol. Infect. Dis. 26:595- 601.
27. Homer MJ, Aguilar-Delfin I, Telford SR, III, Krause PJ, Persing DH. 2000. Babesiosis. Clin. Microbiol. Rev. 13:451- 469.
28. + T cells and gamma interferon in protective immunity against Babesia microti infection in mice. Infect. Immun. 67:4143- 4148.
29. Igarashi I, et al. 2000. Immunization with recombinant surface antigens p26 with Freund adjuvants against Babesia rodhaini infection. J. Vet. Med. Sci. 62:717-723.
30. Iseki H, et al. 2008. Babesia: the protective effects of killed Propionibacterium acnes on the infections of two rodent Babesia parasites in mice. Exp. Parasitol. 118:543-548.
31. Jacobs P, Radzioch D, Stevenson MM. 1996. A Th1-associated increase in tumor necrosis factor alpha expression in the spleen correlates with resistance to blood-stage malaria in mice. Infect. Immun. 64:535-541.
32. Jacobson RH, Parrodi F, Wright IG, Fitzgerald CJ, Dobson C. 1993. Babesia bovis: in vitro phagocytosis promoted by immune serum and by antibodies produced against protective antigens. Parasitol. Res. 79: 221-226.
33. Johnson WC, Cluff CW, Goff WL, Wyatt CR. 1996. Reactive oxygen and nitrogen intermediates and products from polyamine degradation are babesiacidal in vitro. Ann. N. Y. Acad. Sci. 791:136-147.
34. Kawabuchi T, et al. 2005. Isolation of a human erythrocyte-adapted substrain of Babesia rodhaini and analysis of the merozoite surface protein gene sequences. J. Vet. Med. Sci. 67:901-907.
35. Krause PJ, et al. 2003. Increasing health burden of human babesiosis in endemic sites. Am. J. Trop. Med. Hyg. 68:431- 436.
36. Krause PJ, et al. 2008. Persistent and relapsing babesiosis in immunocompromised patients. Clin. Infect. Dis. 46:370-376.
37. Leiby DA. 2011. Transfusion-transmitted Babesia spp.: bull's-eye on Babesia microti. Clin. Microbiol. Rev. 24:14-28.
38. Li C, Sanni LA, Omer F, Riley E, Langhorne J. 2003. Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect. Immun. 71:4850-4856.
39. Luyendyk J, Olivas OR, Ginger LA, Avery AC. 2002. Antigen-presenting cell function during Plasmodium yoelii infection. Infect. Immun. 70: 2941-2949.
40. Niikura M, Kamiya S, Kita K, Kobayashi F. 2008. Coinfection with nonlethal murine malaria parasites suppresses pathogenesis caused by Plasmodium berghei NK65. J. Immunol. 180:6877- 6884.
41. + cells in resistance against Neospora caninum infection in a murine model. J. Vet. Med. Sci. 72: 1275-1282.
42. Omer FM, de Souza JB, Riley EM. 2003. Differential induction of TGFbeta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections. J. Immunol. 171:5430-5436.
43. Ooka H, et al. 2011. Babesia microti: molecular and antigenic characterizations of a novel 94-kDa protein (BmP94). Exp. Parasitol. 127:287-293.
44. Ruebush MJ, Hanson WL. 1979. Susceptibility of five strains of mice to Babesia microti of human origin. J. Parasitol. 65:430-433.
45. + T-cell crossreactivity and heterologous immunity. Immunol. Rev. 211:164-181.
46. Shoda LK, et al. 2000. Babesia bovis-stimulated macrophages express interleukin-1β, interleukin-12, tumor necrosis factor alpha, and nitric oxide and inhibit parasite replication in vitro. Infect. Immun. 68: 5139-5145.
47. Stevenson MM, Ghadirian E, Phillips NC, Rae D, Podoba JE. 1989. Role of mononuclear phagocytes in elimination of Plasmodium chabaudi AS infection. Parasite Immunol. 11:529-544.
48. Stich RW, et al. 1998. Stimulation of nitric oxide production in macrophages by Babesia bovis. Infect. Immun. 66:4130-4136.
49. - mice: role for IFN-γ in activating apoptosis of hepatocytes. J. Immunol. 59: 1418-1428.
50. Terkawi MA, et al. 2008. C3 contributes to the cross-protective immunity induced by Babesia gibsoni phosphoriboprotein P0 against a lethal B. rodhaini infection. Parasite Immunol. 30:365-370.
51. Trinchieri G. 1995. Interleukin 12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigenspecific adaptive immunity. Annu. Rev. Immunol. 13:251-276.
52. Trinchieri G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
53. Van Duivenvoorde LM, et al. 2010. Suppression of Plasmodium cynomolgi in rhesus macaques by coinfection with Babesia microti. Infect. Immun. 78:1032-1039.
54. Van Rooijen N, Sanders A. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174:83-93.
55. Wei Q, et al. 2001. Human babesiosis in Japan: isolation of Babesia microti-like parasites from an asymptomatic transfusion donor and from a rodent from an area where babesiosis is endemic. J. Clin. Microbiol. 39:2178-2183.
56. Wood PR, Clark IA. 1984. Macrophages from Babesia and malaria infected mice are primed for monokine release. Parasite Immunol. 6:309-317.
57. Yoneto T, et al. 1999. Gamma interferon production is critical for protective immunity to infection with blood-stage Plasmodium berghei XAT but neither NO production nor NK cell activation is critical. Infect. Immun. 67:2349-2356.
58. Zivkovic D, Speksnijder JE, Kuil H, Seinen W. 1984. Immunity to Babesia in mice. II. Cross-protection between various Babesia and Plasmodium species and its relevance to the nature of Babesia immunity. Vet. Immunol. Immunopathol. 5:359-368.