Naturally acquired antibodies specific for plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria

Tuan  Tran, Aissata Ongoiba, Jill Coursen, Cecile Crosnier, Ababacar Diouf, Chiung Yu Huang, Shanping Li, Safiatou Doumbo, Didier Doumtabe, Younoussou Kone, Aboudramane Bathily, Seydou Dia, Moussa Niangaly, Charles Dara, Jules Sangala, Louis H. Miller, Ogobara K. Doumbo, Kassoum Kayentao, Carole A. Long, Kazutoyo Miura & 3 others Gavin J. Wright, Boubacar Traore, Peter D. Crompton

Research output: Contribution to journalArticle

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Abstract

Background. Plasmodium falciparum reticulocyte-binding protein homologue 5 (PfRH5) is a blood-stage parasite protein essential for host erythrocyte invasion. PfRH5-specific antibodies raised in animals inhibit parasite growth in vitro, but the relevance of naturally acquired PfRH5-specific antibodies in humans is unclear.Methods. We assessed pre-malaria season PfRH5-specific immunoglobulin G (IgG) levels in 357 Malian children and adults who were uninfected with Plasmodium. Subsequent P. falciparum infections were detected by polymerase chain reaction every 2 weeks and malaria episodes by weekly physical examination and self-referral for 7 months. The primary outcome was time between the first P. falciparum infection and the first febrile malaria episode. PfRH5-specific IgG was assayed for parasite growth-inhibitory activity.Results. The presence of PfRH5-specific IgG at enrollment was associated with a longer time between the first blood-stage infection and the first malaria episode (PfRH5-seropositive median: 71 days, PfRH5-seronegative median: 18 days; P =. 001). This association remained significant after adjustment for age and other factors associated with malaria risk/exposure (hazard ratio,. 62; P =. 02). Concentrated PfRH5-specific IgG purified from Malians inhibited P. falciparum growth in vitro.Conclusions. Naturally acquired PfRH5-specific IgG inhibits parasite growth in vitro and predicts protection from malaria. These findings strongly support efforts to develop PfRH5 as an urgently needed blood-stage malaria vaccine.

Original languageEnglish (US)
Pages (from-to)789-798
Number of pages10
JournalJournal of Infectious Diseases
Volume209
Issue number5
DOIs
StatePublished - Mar 2014
Externally publishedYes

Fingerprint

Malaria
Parasites
Antibodies
Growth
Immunoglobulin G
Plasmodium falciparum
Plasmodium falciparum RH5 protein
Malaria Vaccines
Plasmodium
Age Factors
Physical Examination
Fever
Referral and Consultation
Erythrocytes
Polymerase Chain Reaction
Infection

Keywords

  • blood-stage immunity
  • endemic population
  • malaria
  • Plasmodium falciparum
  • prospective cohort study
  • RH5

ASJC Scopus subject areas

  • Infectious Diseases
  • Immunology and Allergy

Cite this

Naturally acquired antibodies specific for plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. / Tran, Tuan ; Ongoiba, Aissata; Coursen, Jill; Crosnier, Cecile; Diouf, Ababacar; Huang, Chiung Yu; Li, Shanping; Doumbo, Safiatou; Doumtabe, Didier; Kone, Younoussou; Bathily, Aboudramane; Dia, Seydou; Niangaly, Moussa; Dara, Charles; Sangala, Jules; Miller, Louis H.; Doumbo, Ogobara K.; Kayentao, Kassoum; Long, Carole A.; Miura, Kazutoyo; Wright, Gavin J.; Traore, Boubacar; Crompton, Peter D.

In: Journal of Infectious Diseases, Vol. 209, No. 5, 03.2014, p. 789-798.

Research output: Contribution to journalArticle

Tran, T, Ongoiba, A, Coursen, J, Crosnier, C, Diouf, A, Huang, CY, Li, S, Doumbo, S, Doumtabe, D, Kone, Y, Bathily, A, Dia, S, Niangaly, M, Dara, C, Sangala, J, Miller, LH, Doumbo, OK, Kayentao, K, Long, CA, Miura, K, Wright, GJ, Traore, B & Crompton, PD 2014, 'Naturally acquired antibodies specific for plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria', Journal of Infectious Diseases, vol. 209, no. 5, pp. 789-798. https://doi.org/10.1093/infdis/jit553
Tran, Tuan  ; Ongoiba, Aissata ; Coursen, Jill ; Crosnier, Cecile ; Diouf, Ababacar ; Huang, Chiung Yu ; Li, Shanping ; Doumbo, Safiatou ; Doumtabe, Didier ; Kone, Younoussou ; Bathily, Aboudramane ; Dia, Seydou ; Niangaly, Moussa ; Dara, Charles ; Sangala, Jules ; Miller, Louis H. ; Doumbo, Ogobara K. ; Kayentao, Kassoum ; Long, Carole A. ; Miura, Kazutoyo ; Wright, Gavin J. ; Traore, Boubacar ; Crompton, Peter D. / Naturally acquired antibodies specific for plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria. In: Journal of Infectious Diseases. 2014 ; Vol. 209, No. 5. pp. 789-798.
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abstract = "Background. Plasmodium falciparum reticulocyte-binding protein homologue 5 (PfRH5) is a blood-stage parasite protein essential for host erythrocyte invasion. PfRH5-specific antibodies raised in animals inhibit parasite growth in vitro, but the relevance of naturally acquired PfRH5-specific antibodies in humans is unclear.Methods. We assessed pre-malaria season PfRH5-specific immunoglobulin G (IgG) levels in 357 Malian children and adults who were uninfected with Plasmodium. Subsequent P. falciparum infections were detected by polymerase chain reaction every 2 weeks and malaria episodes by weekly physical examination and self-referral for 7 months. The primary outcome was time between the first P. falciparum infection and the first febrile malaria episode. PfRH5-specific IgG was assayed for parasite growth-inhibitory activity.Results. The presence of PfRH5-specific IgG at enrollment was associated with a longer time between the first blood-stage infection and the first malaria episode (PfRH5-seropositive median: 71 days, PfRH5-seronegative median: 18 days; P =. 001). This association remained significant after adjustment for age and other factors associated with malaria risk/exposure (hazard ratio,. 62; P =. 02). Concentrated PfRH5-specific IgG purified from Malians inhibited P. falciparum growth in vitro.Conclusions. Naturally acquired PfRH5-specific IgG inhibits parasite growth in vitro and predicts protection from malaria. These findings strongly support efforts to develop PfRH5 as an urgently needed blood-stage malaria vaccine.",
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author = "Tuan  Tran and Aissata Ongoiba and Jill Coursen and Cecile Crosnier and Ababacar Diouf and Huang, {Chiung Yu} and Shanping Li and Safiatou Doumbo and Didier Doumtabe and Younoussou Kone and Aboudramane Bathily and Seydou Dia and Moussa Niangaly and Charles Dara and Jules Sangala and Miller, {Louis H.} and Doumbo, {Ogobara K.} and Kassoum Kayentao and Long, {Carole A.} and Kazutoyo Miura and Wright, {Gavin J.} and Boubacar Traore and Crompton, {Peter D.}",
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T1 - Naturally acquired antibodies specific for plasmodium falciparum reticulocyte-binding protein homologue 5 inhibit parasite growth and predict protection from malaria

AU - Tran, Tuan 

AU - Ongoiba, Aissata

AU - Coursen, Jill

AU - Crosnier, Cecile

AU - Diouf, Ababacar

AU - Huang, Chiung Yu

AU - Li, Shanping

AU - Doumbo, Safiatou

AU - Doumtabe, Didier

AU - Kone, Younoussou

AU - Bathily, Aboudramane

AU - Dia, Seydou

AU - Niangaly, Moussa

AU - Dara, Charles

AU - Sangala, Jules

AU - Miller, Louis H.

AU - Doumbo, Ogobara K.

AU - Kayentao, Kassoum

AU - Long, Carole A.

AU - Miura, Kazutoyo

AU - Wright, Gavin J.

AU - Traore, Boubacar

AU - Crompton, Peter D.

PY - 2014/3

Y1 - 2014/3

N2 - Background. Plasmodium falciparum reticulocyte-binding protein homologue 5 (PfRH5) is a blood-stage parasite protein essential for host erythrocyte invasion. PfRH5-specific antibodies raised in animals inhibit parasite growth in vitro, but the relevance of naturally acquired PfRH5-specific antibodies in humans is unclear.Methods. We assessed pre-malaria season PfRH5-specific immunoglobulin G (IgG) levels in 357 Malian children and adults who were uninfected with Plasmodium. Subsequent P. falciparum infections were detected by polymerase chain reaction every 2 weeks and malaria episodes by weekly physical examination and self-referral for 7 months. The primary outcome was time between the first P. falciparum infection and the first febrile malaria episode. PfRH5-specific IgG was assayed for parasite growth-inhibitory activity.Results. The presence of PfRH5-specific IgG at enrollment was associated with a longer time between the first blood-stage infection and the first malaria episode (PfRH5-seropositive median: 71 days, PfRH5-seronegative median: 18 days; P =. 001). This association remained significant after adjustment for age and other factors associated with malaria risk/exposure (hazard ratio,. 62; P =. 02). Concentrated PfRH5-specific IgG purified from Malians inhibited P. falciparum growth in vitro.Conclusions. Naturally acquired PfRH5-specific IgG inhibits parasite growth in vitro and predicts protection from malaria. These findings strongly support efforts to develop PfRH5 as an urgently needed blood-stage malaria vaccine.

AB - Background. Plasmodium falciparum reticulocyte-binding protein homologue 5 (PfRH5) is a blood-stage parasite protein essential for host erythrocyte invasion. PfRH5-specific antibodies raised in animals inhibit parasite growth in vitro, but the relevance of naturally acquired PfRH5-specific antibodies in humans is unclear.Methods. We assessed pre-malaria season PfRH5-specific immunoglobulin G (IgG) levels in 357 Malian children and adults who were uninfected with Plasmodium. Subsequent P. falciparum infections were detected by polymerase chain reaction every 2 weeks and malaria episodes by weekly physical examination and self-referral for 7 months. The primary outcome was time between the first P. falciparum infection and the first febrile malaria episode. PfRH5-specific IgG was assayed for parasite growth-inhibitory activity.Results. The presence of PfRH5-specific IgG at enrollment was associated with a longer time between the first blood-stage infection and the first malaria episode (PfRH5-seropositive median: 71 days, PfRH5-seronegative median: 18 days; P =. 001). This association remained significant after adjustment for age and other factors associated with malaria risk/exposure (hazard ratio,. 62; P =. 02). Concentrated PfRH5-specific IgG purified from Malians inhibited P. falciparum growth in vitro.Conclusions. Naturally acquired PfRH5-specific IgG inhibits parasite growth in vitro and predicts protection from malaria. These findings strongly support efforts to develop PfRH5 as an urgently needed blood-stage malaria vaccine.

KW - blood-stage immunity

KW - endemic population

KW - malaria

KW - Plasmodium falciparum

KW - prospective cohort study

KW - RH5

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