Placental Plasmodium falciparum infection: Causes and consequences of in utero sensitization to parasite antigens

Molecular and Biochemical Parasitology

Volumn 151, Issue 1, 2007, Pages 1-8

  Broen, Kelly ^a   Brustoski, Kim ^b   Engelmann, Ilka ^c   Luty, Adrian J F ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cellular immunology; In utero sensitization; Malaria; Neonatal; Pregnancy

Indexed keywords

CD20 ANTIGEN; FANSIDAR; GAMMA INTERFERON; HLA ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; MALARIA VACCINE; PARASITE ANTIGEN; PROTEIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ASEXUAL REPRODUCTION; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL MATURATION; CYTOKINE PRODUCTION; DENDRITIC CELL; DEVELOPMENTAL STAGE; ENDEMIC DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EXPOSURE; FILARIASIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INFANCY; INFECTION RISK; INFECTION SENSITIVITY; INNATE IMMUNITY; INTERFERON PRODUCTION; INTRAUTERINE INFECTION; MALARIA; NATURAL KILLER CELL; PARASITE DEVELOPMENT; PLACENTAL TRANSFER; PLASMODIUM FALCIPARUM; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SCHISTOSOMIASIS; SENSITIZATION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; UMBILICAL CORD BLOOD; VACCINATION;

ANIMALS; ANTIGENS, PROTOZOAN; DISEASE TRANSMISSION, VERTICAL; FEMALE; HUMANS; MALARIA, FALCIPARUM; PLACENTA; PLASMODIUM FALCIPARUM; UTERUS;

PLASMODIUM FALCIPARUM; VERMES;

EID: 33845317258     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2006.10.001     Document Type: Review

References (89)

1. Brabin B.J., Romagosa C., Abdelgalil S., et al. The sick placenta-the role of malaria. Placenta 25 (2004) 359-378
2. Hviid L. The immuno-epidemiology of pregnancy-associated malaria: a variant surface antigen-specific perspective. Parasite Immunol 26 (2004) 477-486
3. Beeson J.G., and Duffy P.E. The immunology and pathogenesis of malaria during pregnancy. Curr Top Microbiol Immunol 297 (2005) 187-227
4. Duffy P.E., and Fried M. Malaria in pregnancy: deadly parasite, susceptible host (2001), Taylor and Francis, London
5. Steketee R.W., Nahlen B.L., Parise M.E., and Menendez C. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64 Suppl (2001) 28-35
6. Le Hesran J.Y., Cot M., Personne P., et al. Maternal placental infection with Plasmodium falciparum and malaria morbidity during the first 2 years of life. Am J Epidemiol 146 (1997) 826-831
7. Cot M., Le Hesran J.Y., Staalsoe T., Fievet N., Hviid L., and Deloron P. Maternally transmitted antibodies to pregnancy-associated variant antigens on the surface of erythrocytes infected with Plasmodium falciparum: relation to child susceptibility to malaria. Am J Epidemiol 157 (2003) 203-209
8. Mutabingwa T.K., Bolla M.C., Li J.L., et al. Maternal malaria and gravidity interact to modify infant susceptibility to malaria. PLoS Med 2 (2005) e407
9. Desowitz R.S. Prenatal immune priming in malaria: antigen-specific blastogenesis of cord blood lymphocytes from neonates born in a setting of holoendemic malaria. Ann Trop Med Parasitol 82 (1988) 121-125
10. Rasheed F.N., Bulmer J.N., De Francisco A., et al. Relationships between maternal malaria and malarial immune responses in mothers and neonates. Parasite Immunol 17 (1995) 1-10
11. Fievet N., Ringwald P., Bickii J., et al. Malaria cellular immune responses in neonates from Cameroon. Parasite Immunol 18 (1996) 483-490
12. King C.L., Malhotra I., Wamachi A., et al. Acquired immune responses to Plasmodium falciparum merozoite surface protein-1 in the human fetus. J Immunol 168 (2002) 356-364
13. Brustoski K., Moller U., Kramer M., et al. IFN-gamma and IL-10 mediate parasite-specific immune responses of cord blood cells induced by pregnancy-associated Plasmodium falciparum malaria. J Immunol 174 (2005) 1738-1745
14. Brustoski K., Kramer M., Moller U., Kremsner P.G., and Luty A.J.F. Neonatal and maternal immunological responses to conserved epitopes within the DBL-gamma3 chondroitin sulfate A-binding domain of Plasmodium falciparum erythrocyte membrane protein 1. Infect Immun 73 (2005) 7988-7995
15. Malhotra I., Mungai P., Muchiri E., et al. Distinct Th1- and Th2-type prenatal cytokine responses to Plasmodium falciparum erythrocyte invasion ligands. Infect Immun 73 (2005) 3462-3470
16. Brustoski K., Moller U., Kramer M., et al. Reduced cord blood immune effector-cell responsiveness mediated by CD4+ cells induced in utero as a consequence of placental Plasmodium falciparum infection. J Infect Dis 193 (2006) 146-154
17. Achidi E.A., Perlmann H., Salimonu L.S., Asuzu M.C., Perlmann P., and Berzins K. Antibodies to Pf155/RESA and circumsporozoite protein of Plasmodium falciparum in paired maternal-cord sera from Nigeria. Parasite Immunol 17 (1995) 535-540
18. Malhotra I., Ouma J.H., Wamachi A., et al. Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 71 (2003) 5231-5237
19. Malhotra I., Mungai P.L., Wamachi A.N., et al. Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. J Infect Dis 193 (2006) 1005-1013
20. Malhotra I., Mungai P., Wamachi A., et al. Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162 (1999) 6843-6848
21. Soboslay P.T., Geiger S.M., Drabner B., et al. Prenatal immune priming in onchocerciasis-Onchocerca volvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clin Exp Immunol 117 (1999) 130-137
22. Adkins B. T-cell function in newborn mice and humans. Immunol Today 20 (1999) 330-335
23. Marshall-Clarke S., Reen D., Tasker L., and Hassan J. Neonatal immunity: how well has it grown up?. Immunol Today 21 (2000) 35-41
24. Fadel S., and Sarzotti M. Cellular immune responses in neonates. Int Rev Immunol 19 (2000) 173-193
25. Garcia A.M., Fadel S.A., Cao S., and Sarzotti M. T cell immunity in neonates. Immunol Res 22 (2000) 177-190
26. Siegrist C.A. Neonatal and early life vaccinology. Vaccine 19 (2001) 3331-3346
27. Ridge J.P., Fuchs E.J., and Matzinger P. Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271 (1996) 1723-1726
28. Rainsford E., and Reen D.J. Interleukin 10, produced in abundance by human newborn T cells, may be the regulator of increased tolerance associated with cord blood stem cell transplantation. Br J Haematol 116 (2002) 702-709
29. Han P., McDonald T., and Hodge G. Potential immaturity of the T-cell and antigen-presenting cell interaction in cord blood with particular emphasis on the CD40-CD40 ligand costimulatory pathway. Immunology 113 (2004) 26-34
30. Jonuleit H., Schmitt E., Schuler G., Knop J., and Enk A.H. Induction of interleukin 10-producing, non-proliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 192 (2000) 1213-1222
31. Redd S.C., Wirima J.J., Steketee R.W., Breman J.G., and Heymann D.L. Transplacental transmission of Plasmodium falciparum in rural Malawi. Am J Trop Med Hyg 55 Suppl. 1 (1996) 57-60
32. Druilhe P., Monjour L., and Gentilini M. Transplacental passage of soluble plasmodial antigens. Induction of a specific immune tolerance?. Nouv Presse Med 5 (1976) 1430-1431
33. Crocker I.P., Tanner O.M., Myers J.E., Bulmer J.N., Walraven G., and Baker P.N. Syncytiotrophoblast degradation and the pathophysiology of the malaria-infected placenta. Placenta 25 (2004) 273-282
34. Bonner P.C., Zhou Z., Mirel L.B., et al. Placental malaria diminishes development of antibody responses to Plasmodium falciparum epitopes in infants residing in an area of western Kenya where P. falciparum is endemic. Clin Diagn Lab Immunol 12 (2005) 375-379
35. De Souza J.B., Williamson K.H., Otani T., and Playfair J.H. Early gamma interferon responses in lethal and non-lethal murine blood-stage malaria. Infect Immun 65 (1997) 1593-1598
36. Mohan K., Moulin P., and Stevenson M.M. Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J Immunol 159 (1997) 4990-4998
37. Choudhury H.R., Sheikh N.A., Bancroft G.J., Katz D.R., and De Souza J.B. Early non-specific immune responses and immunity to blood-stage non-lethal Plasmodium yoelii malaria. Infect Immun 68 (2000) 6127-6132
38. Hensmann M., and Kwiatkowski D. Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun 69 (2001) 2364-2371
39. Artavanis-Tsakonas K., and Riley E.M. Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169 (2002) 2956-2963
40. Engelmann I., Santamaria A., Kremsner P.G., and Luty A.J. Activation status of cord blood gamma delta T cells reflects in utero exposure to Plasmodium falciparum antigen. J Infect Dis 191 (2005) 1612-1622
41. Vleugels M.P., Brabin B., Eling W.M., and de Graaf R. Cortisol and Plasmodium falciparum infection in pregnant women in Kenya. Trans R Soc Trop Med Hyg 83 (1989) 173-177
42. Gatti G., Cavallo R., Sartori M.L., et al. Inhibition by cortisol of human natural killer (NK) cell activity. J Steroid Biochem 26 (1987) 49-58
43. Callewaert D.M., Moudgil V.K., Radcliff G., and Waite R. Hormone specific regulation of natural killer cells by cortisol. Direct inactivation of the cytotoxic function of cloned human NK cells without an effect on cellular proliferation. FEBS Lett 285 (1991) 108-110
44. Zhou J., Olsen S., Moldovan J., et al. Glucocorticoid regulation of natural cytotoxicity: effects of cortisol on the phenotype and function of a cloned human natural killer cell line. Cell Immunol 178 (1997) 108-116
45. Bouyou-Akotet M.K., Adegnika A.A., Agnandji S.T., et al. Cortisol and susceptibility to malaria during pregnancy. Microbes Infect 7 (2005) 1217-1223
46. Bouyou-Akotet M.K., Issifou S., Meye J.F., et al. Depressed natural killer cell cytotoxicity against Plasmodium falciparum-infected erythrocytes during first pregnancies. Clin Infect Dis 38 (2004) 342-347
47. Barshes N.R., Goodpastor S.E., and Goss J.A. Pharmacologic immunosuppression. Front Biosci 9 (2004) 411-420
48. Ordi J., Menendez C., Ismail M.R., et al. Placental malaria is associated with cell-mediated inflammatory responses with selective absence of natural killer cells. J Infect Dis 183 (2001) 1100-1107
49. Tsuji M., Mombaerts P., Lefrancois L., Nussenzweig R.S., Zavala F., and Tonegawa S. Gamma delta T cells contribute to immunity against the liver stages of malaria in alpha beta T-cell-deficient mice. Proc Natl Acad Sci USA 91 (1994) 345-349
50. van der Heyde H.C., Elloso M.M., Chang W.L., Kaplan M., Manning D.D., and Weidanz W.P. Gamma delta T cells function in cell-mediated immunity to acute blood-stage Plasmodium chabaudi adami malaria. J Immunol 154 (1995) 3985-3990
51. Elloso M.M., van der Heyde H.C., vande Waa J.A., Manning D.D., and Weidanz W.P. Inhibition of Plasmodium falciparum in vitro by human gamma delta T cells. J Immunol 153 (1994) 1187-1194
52. Troye-Blomberg M., Worku S., Tangteerawatana P., et al. Human gamma delta T cells that inhibit the in vitro growth of the asexual blood stages of the Plasmodium falciparum parasite express cytolytic and proinflammatory molecules. Scand J Immunol 50 (1999) 642-650
53. Roussilhon C., Agrapart M., Guglielmi P., Bensussan A., Brasseur P., and Ballet J.J. Human TcR gamma delta+ lymphocyte response on primary exposure to Plasmodium falciparum. Clin Exp Immunol 95 (1994) 91-97
54. Worku S., Bjorkman A., Troye-Blomberg M., Jemaneh L., Farnert A., and Christensson B. Lymphocyte activation and subset redistribution in the peripheral blood in acute malaria illness: distinct gammadelta+ T cell patterns in Plasmodium falciparum and P. vivax infections. Clin Exp Immunol 108 (1997) 34-41
55. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu Rev Immunol 20 (2002) 197-216
56. Pichyangkul S., Yongvanitchit K., Kum-arb U., et al. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J Immunol 172 (2004) 4926-4933
57. Coban C., Ishii K.J., Kawai T., et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201 (2005) 19-25
58. Krishnegowda G., Hajjar A.M., Zhu J., et al. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 280 (2005) 8606-8616
59. Mockenhaupt F.P., Cramer J.P., Hamann L., et al. Toll-like receptor (TLR) polymorphisms in African children: common TLR-4 variants predispose to severe malaria. Proc Natl Acad Sci USA 103 (2006) 177-182
60. Mockenhaupt F.P., Hamann L., von Gaertner C., et al. Common polymorphisms of toll-like receptors 4 and 9 are associated with the clinical manifestation of malaria during pregnancy. J Infect Dis 194 (2006) 184-188
61. Ismaili J., van der Sande M., Holland M.J., et al. Plasmodium falciparum infection of the placenta affects newborn immune responses. Clin Exp Immunol 133 (2003) 414-421
62. Fievet N., Moussa M., Tami G., et al. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta. J Infect Dis 183 (2001) 1530-1534
63. Suguitan Jr. A.L., Leke R.G., Fouda G., et al. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis 188 (2003) 1074-1082
64. Abrams E.T., Milner Jr. D.A., Kwiek J., et al. Risk factors and mechanisms of preterm delivery in Malawi. Am J Reprod Immunol 52 (2004) 174-183
65. Walther M., Tongren J.E., Andrews L., et al. Upregulation of TGF-beta, FOXP3, and CD4 + CD25 + regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23 (2005) 287-296
66. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy. Immunol Today 18 (1997) 478-482
67. Fried M., Muga R.O., Misore A.O., and Duffy P.E. Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. J Immunol 160 (1998) 2523-2530
68. Moormann A.M., Sullivan A.D., Rochford R.A., et al. Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J Infect Dis 180 (1999) 1987-1993
69. Rogerson S.J., Brown H.C., Pollina E., et al. Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infect Immun 71 (2003) 267-270
70. Suguitan Jr. A.L., Leke R.G., Fouda G., et al. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis 188 (2003) 1074-1082
71. Suguitan Jr. A.L., Cadigan T.J., Nguyen T.A., et al. Malaria associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. Am J Trop Med Hyg 69 (2003) 574-581
72. Abrams E.T., Kwiek J.J., Mwapasa V., et al. Malaria during pregnancy and foetal haematological status in Blantyre, Malawi. Malar J 4 (2005) 39
73. Steinman R.M., Hawiger D., and Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 21 (2003) 685-711
74. Smits H.H., de Jong E.C., Wierenga E.A., and Kapsenberg M.L. Different faces of regulatory DCs in homeostasis and immunity. Trends Immunol 26 (2005) 123-129
75. Goriely S., Vincart B., Stordeur P., et al. Deficient IL-12(p35) gene expression by dendritic cells derived from neonatal monocytes. J Immunol 166 (2001) 2141-2146
76. Levings M.K., Gregori S., Tresoldi E., Cazzaniga S., Bonini C., and Roncarolo M.G. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25 + CD4 + Tr cells. Blood 105 (2005) 1162-1169
77. Steinbrink K., Graulich E., Kubsch S., Knop J., and Enk A.H. CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99 (2002) 2468-2476
78. Jakobsen P.H., Rasheed F.N., Bulmer J.N., Theisen M., Ridley R.G., and Greenwood B.M. Inflammatory reactions in placental blood of Plasmodium falciparum-infected women and high concentrations of soluble E-selectin and a circulating P. falciparum protein in the cord sera. Immunology 93 (1998) 264-269
79. Roncarolo M.G., Levings M.K., and Traversari C. Differentiation of T regulatory cells by immature dendritic cells. J Exp Med 193 (2001) F5-F9
80. Belkaid Y., Piccirillo C.A., Mendez S., Shevach E.M., and Sacks D.L. CD4 + CD25 + regulatory T cells control Leishmania major persistence and immunity. Nature 420 (2002) 502-507
81. Mendez S., Reckling S.K., Piccirillo C.A., Sacks D., and Belkaid Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med 200 (2004) 201-210
82. Taylor M.D., LeGoff L., Harris A., Malone E., Allen J.E., and Maizels R.M. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 174 (2005) 4924-4933
83. Abrams E.T., Brown H., Chensue S.W., et al. Host response to malaria during pregnancy: placental monocyte recruitment is associated with elevated beta chemokine expression. J Immunol 170 (2003) 2759-2764
84. Chaisavaneeyakorn S., Moore J.M., Mirel L., et al. Levels of macrophage inflammatory protein 1 alpha (MIP-1 alpha) and MIP-1 beta in intervillous blood plasma samples from women with placental malaria and human immunodeficiency virus infection. Clin Diagn Lab Immunol 10 (2003) 631-636
85. Bouyou-Akotet M.K., Kombila M., Kremsner P.G., and Mavoungou E. Cytokine profiles in peripheral, placental and cord blood in pregnant women from an area endemic for Plasmodium falciparum. Eur Cytokine Netw 15 (2004) 120-125
86. Hill J., and Kazembe P. Reaching the Abuja target for intermittent preventive treatment of malaria in pregnancy in African women: a review of progress and operational challenges. Trop Med Int Health 11 (2006) 409-418
87. Hill J., Lines J., and Rowland M. Insecticide-treated nets. Adv Parasitol 61 (2006) 77-128
88. Breitling L.P., Fendel R., Mordmueller B., Adegnika A.A., Kremsner P.G., and Luty A.J.F. Cord blood dendritic cell subsets in African newborns exposed to Plasmodium falciparum in utero. Infect Immun 74 (2006) 5725-5729
89. Hopman, et al. Submitted for publication.