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Immune Responses of NIH Mice Infected with Avirulent and Virulent Strains of Plasmodium chabaudi adami Single and Mixed Infections

  • Namazi, M.J. (The University of Medical Sciences of Sabzevar) ;
  • Phillips, R.S. (Department of Infection and Immunity, Glasgow Biomedical Research Centre (GBRC), University of Glasgow)
  • Received : 2009.10.18
  • Accepted : 2010.02.20
  • Published : 2010.03.15

Abstract

An understanding of the nature of the immune response to asexual erythrocytic stages of malaria parasites will facilitate vaccine development by identifying which responses the vaccine should preferentially induce. The present study examined and compared the immune responses of NIH mice in either single or mixed infections with avirulent (DK) or virulent (DS) strains of Plasmodium chabaudi adami using the ELISA test for detecting and measurement of cytokines and antibody production. In both single and mixed infections, the study showed that both cell- and antibody-mediated responses were activated. In all experiments, an early relatively high level of IFN-$\gamma$ and IgG2a during the acute phase of the infection, and later elevation of IL-4 and IgG1, suggested that there was a sequential Th1/Th2 response. However, in the avirulent DK strain infection a stronger Th1 response was observed compared to the virulent DS strain-infection or in mixed infections. In the virulent DS infection, there was a stronger Th2 response compared to that in the DK and mixed infections. The faster proliferation rate of the virulent DS strain compared to the DK strain was also evident.

Keywords

References

  1. WHO. Malaria. http://www.who.int/mediacentre/factsheets/fs094/en/index.html. 2010.
  2. Wipasa J, Elliott S, Xu H, Good MF. Immunity to asexual blood stage malaria and vaccine approaches. Immunol Cell Biol 2002; 80: 401-414. https://doi.org/10.1046/j.1440-1711.2002.01107.x
  3. Babiker HA, Creasey AM, Bayoumi RA, Walliker D, Arnot DE. Genetic diversity of Plasmodium falciparum in a village in eastern Sudan. 1. Diversity of enzymes, 2D-PAGE proteins and antigens. Trans R Soc Trop Med Hyg 1991; 85: 572-577. https://doi.org/10.1016/0035-9203(91)90347-2
  4. Taylor-Robinson AW. Regulation of immunity to malaria: valuable lessons learned from murine models. Parasitol Today 1995; 11: 334-341. https://doi.org/10.1016/0169-4758(95)80186-3
  5. Langhorne J. The role of CD4(+) T-cells in the immune response to Plasmodium chabaudi. Parasitol Today 1989; 5: 362-364. https://doi.org/10.1016/0169-4758(89)90113-0
  6. Smith EC, Taylor-Robinson AW. Parasite-specific immunoglobulin isotypes during lethal and non-lethal murine malaria infections. Parasitol Res 2003; 89: 26-33.
  7. McDonald V, Phillips RS. Plasmodium chabaudi: Adoptive transfer of immunity with different spleen cell populations and development of protective activity in the serum of lethally irradiated recipient mice. Exp Parasitol 1980; 49: 26-33. https://doi.org/10.1016/0014-4894(80)90052-1
  8. De Souza JB, Ling IT, Ogun SA, Holder AA, Playfair JH. Cytokines and antibody subclass associated with protective immunity against blood-stage malaria in mice vaccinated with the C terminus of merozoite surface protein 1 plus a novel adjuvant. Infect Immun 1996; 64: 3532-3536.
  9. Jacobs P, Radzioch D, Stevenson MM. Nitric oxide expression in the spleen, but not in the liver, correlates with resistance to blood-stage malaria in mice. J Immunol 1995; 155: 5306-5313.
  10. Sam H, Stevenson MM. Early IL-12 p70, but not p40, production by splenic macrophages correlates with host resistance to bloodstage Plasmodium chabaudi AS malaria. Clin Exp Immunol 1999; 117: 343-349. https://doi.org/10.1046/j.1365-2249.1999.00966.x
  11. Stavnezer J. Antibody class switching. Adv Immunol 1996; 61: 79-146. https://doi.org/10.1016/S0065-2776(08)60866-4
  12. Ockenhouse CF, Shear HL. Oxidative killing of the intraerythrocytic malaria parasite Plasmodium yoelii by activated macrophages. J Immunol 1984; 132: 424-431.
  13. Su Z, Stevenson MM. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 2000; 68: 4399-4406. https://doi.org/10.1128/IAI.68.8.4399-4406.2000
  14. Yoneto T, Waki S, Takai T, Tagawa Yi, Iwakura Y, Mizuguchi J, Nariuchi H, Yoshimoto T. A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to bloodstage Plasmodium berghei XAT infection. J Immunol 2001; 166: 6236-6241. https://doi.org/10.4049/jimmunol.166.10.6236
  15. Balmer P, Alexander J, Phillips RS. Protective immunity to erythrocytic Plasmodium chabaudi AS infection involves IFN-gammamediated responses and a cellular infiltrate to the liver. Parasitology 2000; 121: 73-82. https://doi.org/10.1017/S0031182000006867
  16. Taylor-Robinson AW, Phillips RS. Th1 and Th2 CD4+ T cell clones specific for Plasmodium chabaudi but not for an unrelated antigen protect against blood stage P. chabaudi infection. Eur J Immunol 1994; 24: 158-164. https://doi.org/10.1002/eji.1830240124
  17. Taylor-Robinson AW, Smith EC. Modulation of experimental blood stage malaria through blockade of the B7/CD28 T-cell costimulatory pathway. Immunology 1999; 96: 498-504. https://doi.org/10.1046/j.1365-2567.1999.00718.x
  18. Langhorne J, Quin SJ, Sanni LA. Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem Immunol 2002; 80: 204-228. https://doi.org/10.1159/000058845
  19. Weidanz WP, Kemp JR, Batchelder JM, Cigel FK, Sandor M, Heyde HC. Plasticity of immune responses suppressing parasitemia during acute Plasmodium chabaudi malaria. J Immunol 1999; 162: 7383-7388.
  20. Rainczuk A, Scorza T, Smooker PM, Spithill TW. Induction of specific T-cell responses, opsonizing antibodies, and protection against Plasmodium chabaudi adami infection in mice vaccinated with genomic expression libraries expressed in targeted and secretory DNA vectors. Infect Immun 2003; 71: 4506-4515. https://doi.org/10.1128/IAI.71.8.4506-4515.2003
  21. Anders RF, Crewther PES, Edwards M, Margetts M, Matthew ML, Pollock B, Pye D. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine 1998; 16: 240-247. https://doi.org/10.1016/S0264-410X(97)88331-4
  22. Smooker PM, Setiady YY, Rainczuk A, Spithill TW. Expression library immunization protects mice against a challenge with virulent rodent malaria. Vaccine 2000; 18: 2533-2540. https://doi.org/10.1016/S0264-410X(00)00018-9
  23. Black J, Hommel M, Snounou G, Pinder M. Mixed infections with Plasmodium falciparum and P. malariae and fever in malaria. Lancet 1994; 343: 1095.
  24. Taylor LH, Walliker D, Read AF. Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 1997; 115: 121-132. https://doi.org/10.1017/S0031182097001145
  25. Snounou G, Bourne T, Jarra W, Viriyakosol S, Wood JC, Brown KN. Assessment of parasite population dynamics in mixed infections of rodent plasmodia. Parasitology 1992; 105: 363-374. https://doi.org/10.1017/S0031182000074539
  26. Maitland K, Williams TN, Newbold CI. Plasmodium vivax and P. falciparum: biological interactions and the possibility of cross-species immunity. Parasitol Today 1997; 13: 227-231. https://doi.org/10.1016/S0169-4758(97)01061-2
  27. Cox FE, Voller A. Cross-immunity between the malaria parasites of rodents. Ann Trop Med Parasitol 1966; 60: 297-303. https://doi.org/10.1080/00034983.1966.11686420
  28. McColm AA, Dalton L. Heterologous immunity in rodent malaria: comparison of the degree of cross-immunity generated by vaccination with that produced by exposure to live infection. Ann Trop Med Parasitol 1983; 77: 355-377. https://doi.org/10.1080/00034983.1983.11811724
  29. Jarra W, Brown KN. Protective immunity to malaria: Studies with cloned lines of Plasmodium chabaudi and P. berghei in CBA/Ca mice. I. The effectiveness and inter- and intra-species specificity of immunity induced by infection. Parasite Immunol 1985; 7: 595-606. https://doi.org/10.1111/j.1365-3024.1985.tb00103.x
  30. Jarra,W, Brown KN. Protective immunity to malaria: Studies with cloned lines of rodent malaria in CBA/Ca mice. IV. The specificity of mechanisms resulting in crisis and resolution of the primary acute phase parasitaemia of Plasmodium chabaudi chabaudi and P. yoelii yoelii. Parasite Immunol 1989; 11: 1-13. https://doi.org/10.1111/j.1365-3024.1989.tb00644.x
  31. Brown KN. The parasitology of malaria and the study of protective immunity. Immunol Lett 1990; 25: 97-99. https://doi.org/10.1016/0165-2478(90)90098-B
  32. Bruce MC, Donnelly CA, Alpers MP, Galinski MR, Barnwell JW, Walliker D, Day KP. Cross-species interactions between malaria parasites in humans. Science 2000; 287: 845-848. https://doi.org/10.1126/science.287.5454.845
  33. Daneshvar H, Hagan P, Phillips RS. Leishmania mexicana H-line attenuated under pressure of gentamicin, potentiates a Th1 response and control of cutaneous leishmaniasis in BALB/c mice. Parasite Immunol 2003; 25: 589-596. https://doi.org/10.1111/j.0141-9838.2004.00671.x
  34. McDonald V, Sherman IW. Plasmodium chabaudi: Humoral and cell-mediated responses of immunized mice. Exp Parasitol 1980; 49: 442-454. https://doi.org/10.1016/0014-4894(80)90078-8
  35. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science 1976; 193: 673-675. https://doi.org/10.1126/science.781840
  36. Cox FE. Acquired immunity to Plasmodium vinckei in mice. Parasitology 1966; 56: 719-732. https://doi.org/10.1017/S0031182000071742
  37. Glynn J R. Infecting dose and severity of malaria: a literature review of induced malaria. J Trop Med Hyg 1994; 97: 300-316.
  38. Timms RN, Colegrave B, Chan H, Read AF. The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 2001; 123: 1-11.
  39. Taylor-Robinson AW, Phillips RS. Infective dose modulates the balance between Th1- and Th2-regulated immune responses during blood-stage malaria infection. Scand J Immunol 1998; 48: 527-534. https://doi.org/10.1046/j.1365-3083.1998.00437.x
  40. Marsh K. Malaria: a neglected disease? Parasitology 1992; 104: S53-S69. https://doi.org/10.1017/S0031182000075247
  41. De Souza JB, Williamson KH, Otani T, Playfair JH. Early gamma interferon responses in lethal and nonlethal murine blood-stage malaria. Infect Immun 1997; 65: 1593-1598.
  42. Podoba JE, Stevenson MM. CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infect Immun 1991; 59: 51-58.
  43. Taylor-Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY. The role of TH1 and TH2 cells in a rodent malaria infection. Science 1993; 260: 1931-1934. https://doi.org/10.1126/science.8100366
  44. Kima PE, Srivastava IK, Long CA. Proteins with molecular masses of 25 to 40 kilodaltons elicit optimal protective responses against Plasmodium chabaudi adami infection. Infect Immun 1992; 60: 5065-5070.
  45. Stevenson MM, Tam MF. Differential induction of helper T cell subsets during blood-stage Plasmodium chabaudi AS infection in resistant and susceptible mice. Clin Exp Immunol 1993; 92: 77-83.
  46. Saul A. Models for the in-host dynamics of malaria revisited: errors in some basic models lead to large over-estimates of growth rates. Parasitology 1998; 117: 405-407. https://doi.org/10.1017/S0031182098003230
  47. Seder RA, Paul WE. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annl Rev Immunol 1994; 12: 635-673. https://doi.org/10.1146/annurev.iy.12.040194.003223
  48. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383: 787-793. https://doi.org/10.1038/383787a0
  49. von der Weid TM, Kopf, Kohler G, Langhorne J. The immune response to Plasmodium chabaudi malaria in interleukin-4-deficient mice. Eur J Immunol 1994; 24: 2285-2293. https://doi.org/10.1002/eji.1830241004
  50. van der Heyde HC, Pepper B, Batchelder J, Cigel F, Weidanz WP. The time course of selected malarial infections in cytokine-deficient mice. Exp Parasitol 1997; 85: 206-213. https://doi.org/10.1006/expr.1996.4132
  51. Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, Flavell RA, de Souza JB, Riley EM. IL-10 from CD4+ CD25-Foxp3-CD127- adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog 2008; 4: e1000004. https://doi.org/10.1371/journal.ppat.1000004
  52. Kelly MN, Kolls JK, Happel K, Schwartzman JD, Schwarzenberger P, Combe C, Moretto M, Khan IA. Interleukin-17/interleukin-17 receptor-mediated signalling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect Immun 2005; 73: 617-621. https://doi.org/10.1128/IAI.73.1.617-621.2005
  53. Rutitzky LI, Lopes da Rosa JR, Stadecker MJ. Severe CD4 T cellmediated immunopathology in murine schistosomiasis is dependent on IL-12p40 and correlates with high levels of IL-17. J Immunol 2005; 175: 3920-3926. https://doi.org/10.4049/jimmunol.175.6.3920

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