Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes

A. Molina-Cruz, R.J. DeJong, C. Ortega, A. Haile, E. Abban, J. Rodrigues, G. Jaramillo-Gutierrez, C. Barillas-Mury

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56 Citations (Scopus)

Abstract

Plasmodium falciparum lines differ in their ability to infect mosquitoes. The Anopheles gambiae L3-5 refractory (R) linemelanizesmost Plasmodium species, including the Brazilian P. falciparum 7G8 line, but it is highly susceptible to some African P. falciparum strains such as 3D7, NF54, and GB4. We investigatedwhether these lines differ in their ability to evade the mosquito immune system. Silencing key components of themosquito complement-like system[thioester-containing protein 1 (TEP1), leucine-rich repeat protein 1, and Anopheles Plasmodium-responsive leucine-rich repeat protein 1] prevented-melanization of 7G8 parasites, reverting the refractory phenotype. In contrast, it had no effect on the intensity of infection with NF54, suggesting that this line is able to evade TEP1-mediated lysis. When R females were coinfected with a line that is melanized (7G8) and a line that survives (3D7), the coinfection resulted inmixed infections with both live and encapsulated parasites on individualmidguts. This finding shows that survival of individual parasites is parasite-specific and not systemic in nature, because parasites can evade TEP1-mediated lysis even when other parasites aremelanized in the same midgut. When females from an extensive genetic cross between R and susceptible A. gambiae (G3) mosquitoes were infected with P. berghei, encapsulation was strongly correlated with the TEP1-R1 allele. However, P. falciparum 7G8 parasites were no longer encapsulated by females from this cross, indicating that the TEP1-R1 allele is not sufficient to melanize this line. Evasion of the A. gambiae immune system by P. falciparum may be the result of parasite adaptation to sympatric mosquito vectors and may be an important factor driving malaria transmission.
Original languageEnglish
Pages (from-to)E1957-E1962
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number28
DOIs
StatePublished - 2012

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Anopheles gambiae
Plasmodium falciparum
Culicidae
Malaria
Parasites
Plasmodium
Proteins
Immune System
Alleles
Genetic Crosses
Anopheles
Infection
Coinfection
Phenotype

Cite this

Molina-Cruz, A. ; DeJong, R.J. ; Ortega, C. ; Haile, A. ; Abban, E. ; Rodrigues, J. ; Jaramillo-Gutierrez, G. ; Barillas-Mury, C. / Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. In: Proceedings of the National Academy of Sciences of the United States of America. 2012 ; Vol. 109, No. 28. pp. E1957-E1962.
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abstract = "Plasmodium falciparum lines differ in their ability to infect mosquitoes. The Anopheles gambiae L3-5 refractory (R) linemelanizesmost Plasmodium species, including the Brazilian P. falciparum 7G8 line, but it is highly susceptible to some African P. falciparum strains such as 3D7, NF54, and GB4. We investigatedwhether these lines differ in their ability to evade the mosquito immune system. Silencing key components of themosquito complement-like system[thioester-containing protein 1 (TEP1), leucine-rich repeat protein 1, and Anopheles Plasmodium-responsive leucine-rich repeat protein 1] prevented-melanization of 7G8 parasites, reverting the refractory phenotype. In contrast, it had no effect on the intensity of infection with NF54, suggesting that this line is able to evade TEP1-mediated lysis. When R females were coinfected with a line that is melanized (7G8) and a line that survives (3D7), the coinfection resulted inmixed infections with both live and encapsulated parasites on individualmidguts. This finding shows that survival of individual parasites is parasite-specific and not systemic in nature, because parasites can evade TEP1-mediated lysis even when other parasites aremelanized in the same midgut. When females from an extensive genetic cross between R and susceptible A. gambiae (G3) mosquitoes were infected with P. berghei, encapsulation was strongly correlated with the TEP1-R1 allele. However, P. falciparum 7G8 parasites were no longer encapsulated by females from this cross, indicating that the TEP1-R1 allele is not sufficient to melanize this line. Evasion of the A. gambiae immune system by P. falciparum may be the result of parasite adaptation to sympatric mosquito vectors and may be an important factor driving malaria transmission.",
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Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. / Molina-Cruz, A.; DeJong, R.J.; Ortega, C.; Haile, A.; Abban, E.; Rodrigues, J.; Jaramillo-Gutierrez, G.; Barillas-Mury, C.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 28, 2012, p. E1957-E1962.

Research output: Contribution to journalArticle

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T1 - Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes

AU - Molina-Cruz, A.

AU - DeJong, R.J.

AU - Ortega, C.

AU - Haile, A.

AU - Abban, E.

AU - Rodrigues, J.

AU - Jaramillo-Gutierrez, G.

AU - Barillas-Mury, C.

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AB - Plasmodium falciparum lines differ in their ability to infect mosquitoes. The Anopheles gambiae L3-5 refractory (R) linemelanizesmost Plasmodium species, including the Brazilian P. falciparum 7G8 line, but it is highly susceptible to some African P. falciparum strains such as 3D7, NF54, and GB4. We investigatedwhether these lines differ in their ability to evade the mosquito immune system. Silencing key components of themosquito complement-like system[thioester-containing protein 1 (TEP1), leucine-rich repeat protein 1, and Anopheles Plasmodium-responsive leucine-rich repeat protein 1] prevented-melanization of 7G8 parasites, reverting the refractory phenotype. In contrast, it had no effect on the intensity of infection with NF54, suggesting that this line is able to evade TEP1-mediated lysis. When R females were coinfected with a line that is melanized (7G8) and a line that survives (3D7), the coinfection resulted inmixed infections with both live and encapsulated parasites on individualmidguts. This finding shows that survival of individual parasites is parasite-specific and not systemic in nature, because parasites can evade TEP1-mediated lysis even when other parasites aremelanized in the same midgut. When females from an extensive genetic cross between R and susceptible A. gambiae (G3) mosquitoes were infected with P. berghei, encapsulation was strongly correlated with the TEP1-R1 allele. However, P. falciparum 7G8 parasites were no longer encapsulated by females from this cross, indicating that the TEP1-R1 allele is not sufficient to melanize this line. Evasion of the A. gambiae immune system by P. falciparum may be the result of parasite adaptation to sympatric mosquito vectors and may be an important factor driving malaria transmission.

U2 - 10.1073/pnas.1121183109

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M3 - Article

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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