Skip to main content
    • Aa
    • Aa
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 8
  • Cited by
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.

    Ahouidi, Ambroise D. Amambua-Ngwa, Alfred Awandare, Gordon A. Bei, Amy K. Conway, David J. Diakite, Mahamadou Duraisingh, Manoj T. Rayner, Julian C. and Zenonos, Zenon A. 2016. Malaria Vaccine Development: Focusing Field Erythrocyte Invasion Studies on Phenotypic Diversity. Trends in Parasitology, Vol. 32, Issue. 4, p. 274.

    Cheeseman, Ian H. Miller, Becky Tan, John C. Tan, Asako Nair, Shalini Nkhoma, Standwell C. De Donato, Marcos Rodulfo, Hectorina Dondorp, Arjen Branch, Oralee H. Mesia, Lastenia Ruiz Newton, Paul Mayxay, Mayfong Amambua-Ngwa, Alfred Conway, David J. Nosten, François Ferdig, Michael T. and Anderson, Tim J. C. 2016. Population Structure Shapes Copy Number Variation in Malaria Parasites. Molecular Biology and Evolution, Vol. 33, Issue. 3, p. 603.

    Morrison, W. Ivan Connelley, Timothy Hemmink, Johanneke D. and MacHugh, Niall D. 2015. Understanding the Basis of Parasite Strain-Restricted Immunity toTheileria parva. Annual Review of Animal Biosciences, Vol. 3, Issue. 1, p. 397.

    Bei, Amy K. and Duraisingh, Manoj T. 2012. Functional analysis of erythrocyte determinants of Plasmodium infection. International Journal for Parasitology, Vol. 42, Issue. 6, p. 575.

    Standley, Claire J. Mugisha, Lawrence Verweij, Jaco J. Adriko, Moses Arinaitwe, Moses Rowell, Candia Atuhaire, Aaron Betson, Martha Hobbs, Emma van Tulleken, Christoffer R. Kane, Richard A. van Lieshout, Lisette Ajarova, Lilly Kabatereine, Narcis B. and Stothard, J. Russell 2011. Confirmed Infection with Intestinal Schistosomiasis in Semi-Captive Wild-Born Chimpanzees on Ngamba Island, Uganda. Vector-Borne and Zoonotic Diseases, Vol. 11, Issue. 2, p. 169.

    Ahouidi, Ambroise D. Bei, Amy K. Neafsey, Daniel E. Sarr, Ousmane Volkman, Sarah Milner, Dan Cox-Singh, Janet Ferreira, Marcelo U. Ndir, Omar Premji, Zul Mboup, Souleymane and Duraisingh, Manoj T. 2010. Population genetic analysis of large sequence polymorphisms in Plasmodium falciparum blood-stage antigens. Infection, Genetics and Evolution, Vol. 10, Issue. 2, p. 200.

    Geraudie, Perrine Gerbron, Marie and Minier, Christophe 2010. Seasonal variations and alterations of sex steroid levels during the reproductive cycle of male roach (Rutilus rutilus). Marine Environmental Research, Vol. 69, p. S53.

    Sullivan, D. 2010. Uncertainty in Mapping Malaria Epidemiology: Implications for Control. Epidemiologic Reviews, Vol. 32, Issue. 1, p. 175.


Erythrocyte invasion profiles are associated with a common invasion ligand polymorphism in Senegalese isolates of Plasmodium falciparum

  • P. M. LANTOS (a1), A. D. AHOUIDI (a2), A. K. BEI (a1), C. V. JENNINGS (a1), O. SARR (a2), O. NDIR (a2), D. F. WIRTH (a1), S. MBOUP (a2) and M. T. DURAISINGH (a1)
  • DOI:
  • Published online: 01 January 2009

Plasmodium falciparum parasites use multiple ligand-receptor interactions to invade human erythrocytes. Variant expression levels of members of the PfRh and PfEBA ligand families are associated with the use of different erythrocyte receptors, defining invasion pathways. Here we analyse a major polymorphism, a large sequence deletion in the PfRh2b ligand, and erythrocyte invasion profiles in uncultured Senegalese isolates. Parasites vary considerably in their use of sialic acid-containing and protease-sensitive erythrocyte receptors for invasion. The erythrocyte selectivity index was not related to invasion pathway usage, while parasite multiplication rate was associated with enhanced use of a trypsin-resistant invasion pathway. PfRh2b protein was expressed in all parasite isolates, although the PfRh2b deletion was present in a subset (~68%). Parasites with the PfRh2b deletion were found to preferentially utilize protease-resistant pathways for erythrocyte invasion. Sialic acid-independent invasion is reduced in parasites with the PfRh2b deletion, but only in isolates derived from blood group O patients. Our results suggest a significant role for PfRh2b sequence polymorphism in discriminating between alternative erythrocyte receptors for invasion and as a possible determinant of virulence.

Corresponding author
*Corresponding author: Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02115, USA. Tel: +1 617 432 2675. Fax: +1 617 436 4766. E-mail:
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

J. Baum , A. G. Maier , R. T. Good , K. M. Simpson and A. F. Cowman (2005). Invasion by Plasmodium falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathogens 1, e37.

J. Baum , M. Pinder and D. J. Conway (2003). Erythrocyte invasion phenotypes of Plasmodium falciparum in The Gambia. Infection and Immunity 71, 18561863.

A. K. Bei , C. D. Membi , J. C. Rayner , M. Mubi , B. Ngasala , A. A. Sultan , Z. Premji and M. T. Duraisingh (2007). Variant merozoite protein expression is associated with erythrocyte invasion phenotypes in Plasmodium falciparum isolates from Tanzania. Molecular and Biochemical Parasitology 153, 6671.

K. Chotivanich , R. Udomsangpetch , J. A. Simpson , P. Newton , S. Pukrittayakamee , S. Looareesuwan and N. J. White (2000). Parasite multiplication potential and the severity of falciparum malaria. Journal of Infectious Diseases 181, 12061209.

A. F. Cowman and B. S. Crabb (2006). Invasion of red blood cells by malaria parasites. Cell 124, 755766.

C. M. Cserti and W. H. Dzik (2007). The ABO blood group system and Plasmodium falciparum malaria. Blood 110, 22502258.

A. M. Deans , S. Nery , D. J. Conway , O. Kai , K. Marsh and J. A. Rowe (2007). Invasion pathways and malaria severity in Kenyan Plasmodium falciparum clinical isolates. Infection and Immunity 75, 30143020.

S. A. Dolan , L. H. Miller and T. E. Wellems (1990). Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. Journal of Clinical Investigation 86, 618624.

S. A. Dolan , J. L. Proctor , D. W. Alling , Y. Okubo , T. E. Wellems and L. H. Miller (1994). Glycophorin B as an EBA-175 independent Plasmodium falciparum receptor of human erythrocytes. Molecular and Biochemical Parasitology 64, 5563.

M. T. Duraisingh , A. G. Maier , T. Triglia and A. F. Cowman (2003 a). Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and -independent pathways. Proceedings of the National Academy of Sciences, USA 100, 47964801.

M. T. Duraisingh , T. Triglia , S. A. Ralph , J. C. Rayner , J. W. Barnwell , G. I. McFadden and A. F. Cowman (2003 b). Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO Journal 22, 10471057.

D. Gaur , J. R. Storry , M. E. Reid , J. W. Barnwell and L. H. Miller (2003). Plasmodium falciparum is able to invade erythrocytes through a trypsin-resistant pathway independent of glycophorin B. Infection and Immunity 71, 67426746.

T. W. Gilberger , J. K. Thompson , T. Triglia , R. T. Good , M. T. Duraisingh and A. F. Cowman (2003). A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. Journal of Biological Chemistry 278, 1448014486.

T. J. Hadley , F. W. Klotz , G. Pasvol , J. D. Haynes and M. H. McGinniss (1987). Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion. Journal of Clinical Investigation 80, 11901193.

D. G. Jay (1986). Glycosylation site of band 3, the human erythrocyte anion-exchange protein. Biochemistry 25, 554556.

C. V. Jennings , A. D. Ahouidi , M. Zilversmit , A. Bei , J. Rayner , O. Sarr , O. Ndir , D. F. Wirth , S. Mboup and M. T. Duraisingh (2007). Molecular analysis of erythrocyte invasion in Plasmodium falciparum isolates from Senegal. Infection and Immunity 75, 35313538.

O. Kaneko , J. Mu , T. Tsuboi , X. Su and M. Torii (2002). Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins. Molecular and Biochemical Parasitology 121, 275278.

C. A. Lobo , K. De Frazao , M. Rodriguez , M. Reid , M. Zalis and S. Lustigman (2004). Invasion profiles of Brazilian field isolates of Plasmodium falciparum: phenotypic and genotypic analyses. Infection and Immunity 72, 58865891.

C. A. Lobo , M. Rodriguez , M. Reid and S. Lustigman (2003). Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101, 46284631.

C. A. Lobo , M. Rodriguez , C. J. Struchiner , M. G. Zalis and S. Lustigman (2006). Associations between defined polymorphic variants in the PfRH ligand family and the invasion pathways used by Plasmodium falciparum field isolates from Brazil. Molecular and Biochemical Parasitology 149, 246251.

A. G. Maier , M. T. Duraisingh , J. C. Reeder , S. S. Patel , J. W. Kazura , P. A. Zimmerman and A. F. Cowman (2003). Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nature Medicine 9, 8792.

D. S. Peterson and T. E. Wellems (2000). EBL-1, a putative erythrocyte binding protein of Plasmodium falciparum, maps within a favored linkage group in two genetic crosses. Molecular and Biochemical Parasitology 105, 105113.

J. C. Rayner , M. R. Galinski , P. Ingravallo and J. W. Barnwell (2000). Two Plasmodium falciparum genes express merozoite proteins that are related to Plasmodium vivax and Plasmodium yoelii adhesive proteins involved in host cell selection and invasion. Proceedings of the National Academy of Sciences, USA 97, 96489653.

J. C. Rayner , E. Vargas-Serrato , C. S. Huber , M. R. Galinski and J. W. Barnwell (2001). A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. Journal of Experimental Medicine 194, 15711581.

B. Sim , P. A. Orlandi , J. D. Haynes , F. W. Klotz , J. M. Carter , D. Camus , M. E. Zegans and J. D. Chulay (1990). Primary structure of the 175K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion. Journal of Cell Biology 111, 18771884.

B. K. L. Sim , C. E. Chitnis , K. Wasniowska , T. J. Hadley and L. H. Miller (1994). Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264, 19411944.

J. A. Simpson , K. Silamut , K. Chotivanich , S. Pukrittayakamee and N. J. White (1999). Red cell selectivity in malaria: a study of multiple-infected erythrocytes. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 165168.

J. Stubbs , K. M. Simpson , T. Triglia , D. Plouffe , C. J. Tonkin , M. T. Duraisingh , A. G. Maier , E. A. Winzeler and A. F. Cowman (2005). Molecular mechanism for switching of Plasmodium falciparum invasion pathways into human erythrocytes. Science 309, 13841387.

H. M. Taylor , M. Grainger and A. A. Holder (2002). Variation in the expression of a Plasmodium falciparum protein family implicated in erythrocyte invasion. Infection and Immunity 70, 57795789.

J. K. Thompson , T. Triglia , M. B. Reed and A. F. Cowman (2001). A novel ligand from Plasmodium falciparum that binds to a sialic acid-containing receptor on the surface of human erythrocytes. Molecular Microbiology 41, 4758.

T. Triglia , M. T. Duraisingh , R. T. Good and A. F. Cowman (2005). Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum. Molecular Microbiology 55, 162174.

T. Triglia , J. Thompson , S. R. Caruana , M. Delorenzi , T. Speed and A. F. Cowman (2001). Identification of proteins from Plasmodium falciparum that are homologous to reticulocyte binding proteins in Plasmodium vivax. Infection and Immunity 69, 10841092.

S. Viriyakosol , N. Siripoon , X. P. Zhu , W. Jarra , A. Seugorn , K. N. Brown and G. Snounou (1994). Plasmodium falciparum: selective growth of subpopulations from field samples following in vitro culture, as detected by the polymerase chain reaction. Experimental Parasitology 79, 517525.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *