Drug treatment of malaria infections can reduce levels of protection transferred to offspring via maternal immunity

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1737, 2012, Pages 2487-2496

  Staszewski, Vincent ^a   Reece, Sarah E ^a   O’Donnell, Aidan J ^a   Cunningham, Emma J A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Anti malarial drugs; Immunoglobulins; Maternal effects; Neonatal immunology; Passive immunity; Plasmodium chabaudi

Indexed keywords

PLASMODIUM CHABAUDI; RODENTIA;

ANTIMALARIAL AGENT; PROTOZOON ANTIBODY;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; COMPARATIVE STUDY; DRUG EFFECT; FEMALE; IMMUNOLOGY; MALARIA; MORTALITY; MOUSE; PARASITEMIA; PASSIVE IMMUNIZATION; PLASMODIUM CHABAUDI; PREGNANCY;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIMALARIALS; FEMALE; IMMUNITY, MATERNALLY-ACQUIRED; MALARIA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PARASITEMIA; PLASMODIUM CHABAUDI; PREGNANCY;

EID: 84865589537     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2011.1563     Document Type: Article

References (63)

1. Grindstaff J. L., Brodie E. D., Ketterson E. D. 2003 Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. Lond. B 270, 2309–2319. doi:10.1098/rspb.2003.2485 (doi:10.1098/rspb.2003.2485)
2. Price T. 1998 Maternal and parental effects in birds: effects on offspring fitness. In Maternal effects as adaptations (eds Mousseau T. A., Fox C. W.), pp. 202–226. New York, NY: Oxford University Press.
3. Boulinier T., Staszewski V. 2008 Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol. Evol. 23, 282–288. (doi:10.1016/j.tree.2007.12.006)
4. Frank S. A. 2002 Immunology and evolution of infectious disease. Princeton, NJ: Princeton University Press.
5. Hasselquist D., Nilsson J.-A. 2009 Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil. Trans. R. Soc. B 364, 51–60. (doi:10.1098/rstb.2008.0137)
6. Alizon S., van Baalen M. 2008 Acute or chronic? Within-host models with immune dynamics, infection outcome, and parasite evolution. Am. Nat. 172, 244–256. (doi:10.1086/592404)
7. Thakar J., Poss M., Albert R., Long G., Zhang R. 2010 Dynamic models of immune responses: what is the ideal level of detail? Theor. Biol. Med. Model 7, 35. (doi:10.1186/1742-4682-7-35)
8. Schmid-Hempel P., Frank S. A. 2007 Pathogenesis, virulence, and infective dose. PLoS Pathol. 3, e147. (doi:10.1371/journal.ppat.0030147)
9. Hudson P. J., Rizzoli A., Grenfell B. T., Heesterbeek H., Dobson A. P. 2002 The ecology of wildlife diseases. Oxford, UK: Oxford University Press.
10. Goldsby R. A., Kindt T. J., Osborne B. A. 2000 Kuby immunology. New York, NY: W. H. Freeman and Company.
11. Griffin A., Baraho-Hassan D., McSorley S. J. 2009 Successful treatment of bacterial infection hinders development of acquired immunity. J. Immunol. 183, 1263–1270. (doi:10.4049/jimmunol.0900772)
12. Mduluza T., Mutapi F., Ruwona T., Kaluka D., Midzi N., Ndhlovu P. D. 2009 Similar cellular responses after treatment with either praziquantel or oxamniquine in Schistosoma mansoni infection. Malawi Med. J. 21, 176–182.
13. Mutapi F., Burchmore R., Mduluza T., Foucher A., Harcus Y., Nicoll G., Midzi N., Turner C. M., Maizels R. M. 2005 Praziquantel treatment of individuals exposed to Schistosoma haematobium enhances serological recognition of defined parasite antigens. J. Infect. Dis. 192, 1108–1118. (doi:10.1086/432553)
14. Hviid L., Staalsoe T. 2004 Malaria immunity in infants: a special case of a general phenomenon? Trends Parasitol. 20, 66–72. (doi:10.1016/j.pt.2003.11.009)
15. Gol'dberg E. D., Masnaya N. V., Churin A. A. 2005 Immunity parameters in mice of different strains. Bull. Exp. Biol. Med. 140, 219–221. (doi:10.1007/s10517-005-0450-8)
16. Wargo A. R., Huijben S., de Roode J. C., Shepherd J., Read A. F. 2007 Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl Acad. Sci. USA 104, 19914–19919.
17. Terry R. J. 1956 Transmission of antimalarial immunity (Plasmodium berghei) from mother rats to their young during lactation. Trans. R. Soc. Trop. Med. Hyg. 50, 41–46. (doi:10.1016/0035-9203(56)90006-2)
18. Bruce-Chwatt L. J. 1954 Plasmodium berghei in the placenta of mice and rats: transmission of specific immunity from mother rats to litters. Nature 173, 353–354. (doi:10.1038/173353a0)
19. Palmer T. T. 1978 Plasmodium berghei infection in pregnant rats: effects on antibody response and course of infection in offspring. J. Parasitol. 64, 493–496. (doi:10.2307/3279791)
20. Hviid L., Marinho C. R. F., Staalsoe T., Penha-Gonçalves C. 2010 Of mice and women: rodent models of placental malaria. Trends Parasitol. 26, 412–419. doi:10.1016/j.pt.2010.04.010
21. Stanisic D. I., Martin L. B., Good M. F. 2003 The role of the 19-kDa region of merozoite surface protein 1 and whole-parasite-specific maternal antibodies in directing neonatal pups’ responses to rodent malaria infection. J. Immunol. 171, 5461–5469.
22. Shutler D., Reece S. E., Mullie A., Billingsley P. F., Read A. F. 2005 Rodent malaria parasites Plasmodium chabaudi and P. vinckei do not increase their rates of gametocytogenesis in response to mosquito probing. Proc. R. Soc. B 22, 2397–2402. doi:10.1098/rspb.2005.3232
23. Kicska G. A., Ting L. M., Schramm V. L., Kim K. 2003 Effect of dietary p-aminobenzoic acid on murine Plasmodium yoelii infection. J. Infect. Dis. 188, 1776–1881. doi:10.1086/379373
24. Cheesman S., Raza A., Carter R. 2006 Mixed strain infections and strain-specific protective immunity in the rodent malaria parasite Plasmodium chabaudi chabaudi in mice. Infect. Immunol. 74, 2996–3001. (doi:10.1128/IAI.74.5.2996-3001.2006)
25. Mideo N., Barclay V. C., Chan B. H. K., Savill N. J., Read A. F., Day T. 2008 Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. Am. Nat. 172, E214–E238. doi:10.1086/591684
26. Beale G. H., Carter R., Walliker D. 1978 Genetics. In Rodent malaria (eds Killick-Kendrick R., Peters W.), pp. 213–245. London, UK: Academic Press.
27. Mota M. M., Brown K. N., Holder A. A., Jarra W. 1998 Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infect. Immunol. 66, 4080–4086.
28. Nahrevanian H., Dascombe M. J. 2001 Nitric oxide and reactive nitrogen intermediates during lethal and nonlethal strains of murine malaria. Parasite Immunol. 23, 491–501. doi:10.1046/j.1365-3024.2001.00406.x
29. Achtman A. H., Stephens R., Cadman E. T., Harrison V., Langhorne J. 2007 Malaria-specific antibody responses and parasite persistence after infection of mice with Plasmodium chabaudi chabaudi. Parasite Immunol. 29, 435–444. doi:10.1111/j.1365-3024.2007.00960.x
30. R Development Core Team 2010 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
31. Burnham K. P., Anderson D. R. 2002 Model selection and multimodel inference. New York, NY: Springer.
32. Gasparini J., Bize P., Piault R., Wakamatsu K., Blount J. D., Ducrest A.-L., Roulin A. 2009 Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J. Anim. Ecol. 78, 608–616. doi:10.1111/j.1365-2656.2008.01521.x
33. Hanssen S. A. 2006 Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87, 2440–2446. doi:10.1890/0012-9658(2006)87[2440:COAICA]2.0.CO;2
34. Raberg L., Nilsson J.-A., Illmonen P., Stjerman M., Hasselquist D. 2000 The cost of an immune response: vaccination reduces parental effort. Ecol. Lett. 3, 382–386. doi:10.1046/j.1461-0248.2000.00154.x
35. Bonneaud C., Mazuc J., Gonzalez G., Haussy C., Chastel O., Faivre B., Sorci G. 2003 Assessing the cost of mounting an immune response. Am. Nat. 161, 367–379. (doi:10.1086/346134)
36. Marzal A., Reviriego M., de Lope F., Moller A. P. 2007 Fitness costs of an immune response in the house martin (Delichon urbica). Behav. Ecol. Sociobiol. 61, 1573–1580. doi:10.1007/s00265-007-0389-z
37. Williams T. J., Christians J. K., Aiken J. J., Evanson M. 1999 Enhanced immune function does not depress reproductive output. Proc. R. Soc. Lond. B 266, 753–757. (doi:10.1098/rspb.1999.0701)
38. Gil D., Marzal A., de Lope F., Puerta M., Moller A. P. 2006 Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system. Behav. Ecol. Sociobiol. 60, 96–100. doi:10.1007/s00265-005-0145-1
39. Mousseau T. A., Fox C. W. 1998 Maternal effects as adaptations. Oxford, UK: Oxford University Press.
40. Staszewski V., McCoy K. D., Boulinier T. 2008 Variable exposure and immunological response to Lyme disease Borrelia among North Atlantic seabird species. Proc. R. Soc. B 275, 2101–2109. doi:10.1098/rspb.2008.0515
41. Staszewski V., Siitari H. 2010 Antibody injection in the egg yolk: maternal antibodies affect humoral immune response of the offspring. Funct. Ecol. 24, 1333–1341. doi:10.1111/j.1365-2435.2010.01745.x
42. May K., et al. 2009 Antibody-dependent transplacental transfer of malaria blood-stage antigen using a human ex vivo placental perfusion model. PLoS ONE 4, e7986. doi:10.1371/journal.pone.0007986
43. Soulard V., et al. 2011 Placental malaria-associated suppression of parasite-specific immune response in neonates has no major impact on systemic CD4 T cell homeostasis. Infect. Immun. 79, 2801–2809. doi:10.1128/IAI.00203-11
44. Malhotra I., Dent A., Mungai P., Wamachi A., Ouma J. H., Narum D. L., Muchri E., Tisch D. J., King C. L. 2009 Can prenatal malaria exposure produce an immune tolerant phenotype? A prospective birth cohort study in Kenya. Plos Medicine 6, e1000116. doi:10.1371/journal.pmed.1000116
45. Desowitz R. S. 1971 Plasmodium berghei-enhanced protective immunity after vaccination of white rats born of immune mothers. Science 172, 1151. doi:10.1126/science.172.3988.1151
46. Lindström K. M. 1999 Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343–348. doi:10.1016/S0169-5347(99)01639-0
47. Krist M. 2004 Maternal effects and offspring performance: in search of the best method. Oikos 106, 422–426. doi:10.1111/j.0030-1299.2004.13373.x
48. Mutapi F. 2001 Heterogeneities in anti-schistosome humoral responses following chemotherapy. Trends Parasitol. 17, 518–524. doi:10.1016/S1471-4922(01)02118-3
49. Jimenez J. C., Pinon A., Dive D., Capron M., Dei-Cas E., Convit J. 2009 Antibody response in children infected with Giardia intestinalis before and after treatment with secnidazole. Am. J. Trop. Med. Hyg. 80, 11–15.
50. Bardaji A., Sigauque B., Sanz S., Maixenchs M., Ordi J., Aponte J. J., Mabunda S., Alonso P. L., Menéndez C. 2011 Impact of malaria at the end of pregnancy on infant mortality and morbidity. J. Infect. Dis. 203, 691–699. doi:10.1093/infdis/jiq049
51. Müller W., Groothuis T. G. G., Dijkstra C., Siitari H., Alatalo R. V. 2004 Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Funct. Ecol. 18, 719–724. doi:10.1111/j.0269-8463.2004.00902.x
52. Gasparini J., McCoy K. D., Haussy C., Tveraa T., Boulinier T. 2001 Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B 268, 647–650. doi:10.1098/rspb.2000.1411
53. Buechler K., Fitze P. S., Gottstein B., Jacot A., Richner H. 2002 Parasite-induced maternal response in a natural bird population. J. Anim. Ecol. 71, 247–252. doi:10.1046/j.1365-2656.2002.00591.x
54. Staszewski V., McCoy K. D., Tveraa T., Boulinier T. 2007 Interannual dynamics of antibody levels in naturally infected individuals of a long-lived colonial birds. Ecology 88, 3183–3191. doi:10.1890/07-0098.1
55. Kallio E. R., Begon M., Henttonen H., Koskela E., Mappes T., Vaheri A., Vapalahti O. 2010 Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proc. R. Soc. B 277, 3783–3791. doi:10.1098/rspb.2010.1022
56. Troye-Blomberg M., Berzins K., Perlmann P. 1994 T-cell control of immunity to the asexual blood stage of the malaria parasite. Crit. Rev. Immunol. 14, 131–155.
57. Stevenson M. M., Tam M. F. 1993 Differential induction of helper T cell subsets during blood stage Plasmodium chabaudi as infection in resistant and susceptible mice. Clin. Exp. Immunol. 92, 77–83. doi:10.1111/j.1365-2249.1993.tb05951.x
58. Slade S. J., Langhorne J. 1989 Production of interferon gamma during infection of mice with Plasmodium chabaudi chabaudi. Immunobiology 179, 353–365. doi:10.1016/S0171-2985(89)80041-5
59. Jacobs P., Radzioch D., Stevenson M. M. 1996 A Th1-associated increase in tumor necrosis factor alpha expression in the spleen correlates with resistance to blood-stage malaria in mice. Infect. Immunol. 64, 535–541.
60. Langhorne J., Gillard S., Simon B., Slade S., Eichmann K. 1989 Frequencies of CD4+ T cells reactive with Plasmodium chabaudi chabaudi: distinct response kinetics for cells with Th1 and Th2 characteristics during infection. Int. Immunol. 1, 416–424. doi:10.1093/intimm/1.4.416
61. Helmby H., Troye-Blomberg M. 2000 Differential immunoglobulin E and cytokine responses in Balb/C and C57Bl/6 mice during repeated infections with blood-stage Plasmodium chabaudi malaria. Parasite Immunol. 22, 185–190. doi:10.1046/j.1365-3024.2000.00295.x
62. Peters L. L., Barker J. E. 2011 Hematology and clotting time survey in 43 inbred strains of mice. MPD:6202. Mouse Phenome Database web site. Bar Harbor, Maine USA: The Jackson Laboratory, See http://phenome.jax.org.
63. Addison B., Klasing K. C., Robinson W. D., Austin S. H., Ricklefs R. E. 2009 Ecological and life-history factors influencing the evolution of maternal antibody allocation: a phylogenetic comparison. Proc. R. Soc. B 276, 3979–3987. doi:10.1098/rspb.2009.1296