Skip to main content Accessibility help

Rosetting revisited: a critical look at the evidence for host erythrocyte receptors in Plasmodium falciparum rosetting

  • Fiona McQuaid (a1) and J. Alexandra Rowe (a1)


Malaria remains a major cause of mortality in African children, with no adjunctive treatments currently available to ameliorate the severe clinical forms of the disease. Rosetting, the adhesion of infected erythrocytes (IEs) to uninfected erythrocytes, is a parasite phenotype strongly associated with severe malaria, and hence is a potential therapeutic target. However, the molecular mechanisms of rosetting are complex and involve multiple distinct receptor–ligand interactions, with some similarities to the diverse pathways involved in P. falciparum erythrocyte invasion. This review summarizes the current understanding of the molecular interactions that lead to rosette formation, with a particular focus on host uninfected erythrocyte receptors including the A and B blood group trisaccharides, complement receptor one, heparan sulphate, glycophorin A and glycophorin C. There is strong evidence supporting blood group A trisaccharides as rosetting receptors, but evidence for other molecules is incomplete and requires further study. It is likely that additional host erythrocyte rosetting receptors remain to be discovered. A rosette-disrupting low anti-coagulant heparin derivative is being investigated as an adjunctive therapy for severe malaria, and further research into the receptor–ligand interactions underlying rosetting may reveal additional therapeutic approaches to reduce the unacceptably high mortality rate of severe malaria.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Rosetting revisited: a critical look at the evidence for host erythrocyte receptors in Plasmodium falciparum rosetting
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Rosetting revisited: a critical look at the evidence for host erythrocyte receptors in Plasmodium falciparum rosetting
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Rosetting revisited: a critical look at the evidence for host erythrocyte receptors in Plasmodium falciparum rosetting
      Available formats


This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (, which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: J. Alexandra Rowe, E-mail:


Hide All
Adams, Y, Kuhnrae, P, Higgins, MK, Ghumra, A and Rowe, JA (2014) Rosetting Plasmodium falciparum-infected erythrocytes bind to human brain microvascular endothelial cells in vitro, demonstrating a dual adhesion phenotype mediated by distinct P. falciparum erythrocyte membrane protein 1 domains. Infection and Immunity 82, 949959.
Albrecht, L, Moll, K, Blomqvist, K, Normark, J, Chen, Q and Wahlgren, M (2011) Var gene transcription and PfEMP1 expression in the rosetting and cytoadhesive Plasmodium falciparum clone FCR3S1.2. Malaria Journal 10, 17.
Angeletti, D, Sandalova, T, Wahlgren, M and Achour, A (2015) Binding of subdomains 1/2 of PfEMP1-DBL1alpha to heparan sulfate or heparin mediates Plasmodium falciparum rosetting. PLoS ONE 10, e0118898.
Angus, BJ, Thanikkul, K, Silamut, K, White, NJ and Udomsangpetch, R (1996) Short report: rosette formation in Plasmodium ovale infection. American Journal of Tropical Medicine and Hygiene 55, 560561.
Band, G, Rockett, KA, Spencer, CC, Kwiatkowski, DP and Network, MGE (2015) A novel locus of resistance to severe malaria in a region of ancient balancing selection. Nature 526, 253257.
Barragan, A, Spillmann, D, Kremsner, PG, Wahlgren, M and Carlson, J (1999) Plasmodium falciparum: molecular background to strain-specific rosette disruption by glycosaminoglycans and sulfated glycoconjugates. Experimental Parasitology 91, 133143.
Barragan, A, Fernandez, V, Chen, Q, von Euler, A, Wahlgren, M and Spillmann, D (2000 a) The duffy-binding-like domain 1 of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) is a heparan sulfate ligand that requires 12 mers for binding. Blood 95, 35943599.
Barragan, A, Kremsner, PG, Wahlgren, M and Carlson, J (2000 b) Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infection and Immunity 68, 29712975.
Barrera, V, MacCormick, IJC, Czanner, G, Hiscott, PS, White, VA, Craig, AG, Beare, NAV, Culshaw, LH, Zheng, Y, Biddolph, SC, Milner, DA, Kamiza, S, Molyneux, ME, Taylor, TE and Harding, SP (2018) Neurovascular sequestration in paediatric P. falciparum malaria is visible clinically in the retina. Elife 7, e32208. doi: 10.7554/eLife.32208.
Baruch, DI, Gormely, JA, Ma, C, Howard, RJ and Pasloske, BL (1996) Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proceedings of the National Academy of Sciences USA 93, 34973502.
Bei, AK, Brugnara, C and Duraisingh, MT (2010) In vitro genetic analysis of an erythrocyte determinant of malaria infection. Journal of Infectious Diseases 202, 17221727.
Cabrera, A, Neculai, D and Kain, KC (2014) CD36 and malaria: friends or foes? A decade of data provides some answers. Trends in Parasitology 30, 436444.
Carlson, J and Wahlgren, M (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. Journal of Experimental Medicine 176, 13111317.
Carlson, J, Helmby, H, Hill, AV, Brewster, D, Greenwood, BM and Wahlgren, M (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336, 14571460.
Carlson, J, Ekre, HP, Helmby, H, Gysin, J, Greenwood, BM and Wahlgren, M (1992) Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. American Journal of Tropical Medicine and Hygiene 46, 595602.
Chen, Q, Heddini, A, Barragan, A, Fernandez, V, Pearce, SF and Wahlgren, M (2000) The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. Journal of Experimental Medicine 192, 110.
Ch'ng, JH, Moll, K, Quintana, MEP, Chan, SC, Masters, E, Moles, E, Liu, J, Eriksson, AB and Wahlgren, M (2016) Rosette-disrupting effect of an anti-plasmodial compound for the potential treatment of Plasmodium falciparum malaria complications. Scientific Reports 6, 29317.
Chotivanich, KT, Pukrittayakamee, S, Simpson, JA, White, NJ and Udomsangpetch, R (1998) Characteristics of Plasmodium vivax-infected erythrocyte rosettes. American Journal of Tropical Medicine and Hygiene 59, 7376.
Chung, WY, Gardiner, DL, Hyland, C, Gatton, M, Kemp, DJ and Trenholme, KR (2005) Enhanced invasion of blood group A1 erythrocytes by Plasmodium falciparum. Molecular and Biochemical Parasitology 144, 128130.
Chung, JE, Magis, W, Vu, J, Heo, SJ, Wartiovaara, K, Walters, MC, Kurita, R, Nakamura, Y, Boffelli, D, Martin, DIK, Corn, JE and DeWitt, MA (2019) CRISPR-Cas9 interrogation of a putative fetal globin repressor in human erythroid cells. PLoS ONE 14, e0208237.
Clough, B, Atilola, FA and Pasvol, G (1998) The role of rosetting in the multiplication of Plasmodium falciparum: rosette formation neither enhances nor targets parasite invasion into uninfected red cells. British Journal of Haematology 100, 99104.
Cockburn, IA, Mackinnon, MJ, O'Donnell, A, Allen, SJ, Moulds, JM, Baisor, M, Bockarie, M, Reeder, JC and Rowe, JA (2004) A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proceedings of the National Academy of Sciences USA 101, 272277.
Cowman, AF, Tonkin, CJ, Tham, WH and Duraisingh, MT (2017) The molecular basis of erythrocyte invasion by malaria parasites. Cell Host and Microbe 22, 232245.
Dankwa, S, Chaand, M, Kanjee, U, Jiang, RHY, Nobre, LV, Goldberg, JM, Bei, AK, Moechtar, MA, Grüring, C, Ahouidi, AD, Ndiaye, D, Dieye, TN, Mboup, S, Weekes, MP and Duraisingh, MT (2017) Genetic evidence for erythrocyte receptor glycophorin B expression levels defining a dominant Plasmodium falciparum invasion pathway into human erythrocytes. Infection and Immunity 85, e00074-17.
de Agostini, AI, Watkins, SC, Slayter, HS, Youssoufian, H and Rosenberg, RD (1990) Localization of anticoagulantly active heparan sulfate proteoglycans in vascular endothelium: antithrombin binding on cultured endothelial cells and perfused rat aorta. Journal of Cell Biology 111, 12931304.
Deans, AM and Rowe, JA (2006) Plasmodium falciparum: rosettes do not protect merozoites from invasion-inhibitory antibodies. Experimental Parasitology 112, 269273.
Degarege, A, Gebrezgi, MT, Ibanez, G, Wahlgren, M and Madhivanan, P (2019) Effect of the ABO blood group on susceptibility to severe malaria: a systematic review and meta-analysis. Blood Reviews 33, 5362.
Dondorp, AM, Pongponratn, E and White, NJ (2004) Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Tropica 89, 309317.
Doudna, JA and Charpentier, E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096.
Doumbo, OK, Thera, MA, Koné, AK, Raza, A, Tempest, LJ, Lyke, KE, Plowe, CV and Rowe, JA (2009) High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. American Journal of Tropical Medicine and Hygiene 81, 987993.
Frevert, U, Sinnis, P, Cerami, C, Shreffler, W, Takacs, B and Nussenzweig, V (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. Journal of Experimental Medicine 177, 12871298.
Fried, M and Duffy, PE (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272, 15021504.
Fry, AE, Griffiths, MJ, Auburn, S, Diakite, M, Forton, JT, Green, A, Richardson, A, Wilson, J, Jallow, M, Sisay-Joof, F, Pinder, M, Peshu, N, Williams, TN, Marsh, K, Molyneux, ME, Taylor, TE, Rockett, KA and Kwiatkowski, DP (2008) Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Human Molecular Genetics 17, 567576.
Fry, AE, Ghansa, A, Small, KS, Palma, A, Auburn, S, Diakite, M, Green, A, Campino, S, Teo, YY, Clark, TG, Jeffreys, AE, Wilson, J, Jallow, M, Sisay-Joof, F, Pinder, M, Griffiths, MJ, Peshu, N, Williams, TN, Newton, CR, Marsh, K, Molyneux, ME, Taylor, TE, Koram, KA, Oduro, AR, Rogers, WO, Rockett, KA, Sabeti, PC and Kwiatkowski, DP (2009) Positive selection of a CD36 nonsense variant in sub-Saharan Africa, but no association with severe malaria phenotypes. Human Molecular Genetics 18, 26832692.
Ghumra, A, Semblat, JP, McIntosh, RS, Raza, A, Rasmussen, IB, Braathen, R, Johansen, FE, Sandlie, I, Mongini, PK, Rowe, JA and Pleass, RJ (2008) Identification of residues in the Cmu4 domain of polymeric IgM essential for interaction with Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1). Journal of Immunology 181, 19882000.
Ghumra, A, Semblat, JP, Ataide, R, Kifude, C, Adams, Y, Claessens, A, Anong, DN, Bull, PC, Fennell, C, Arman, M, Amambua-Ngwa, A, Walther, M, Conway, DJ, Kassambara, L, Doumbo, OK, Raza, A and Rowe, JA (2012) Induction of strain-transcending antibodies against Group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathogens 8, e1002665.
Goel, S, Palmkvist, M, Moll, K, Joannin, N, Lara, P, Akhouri, RR, Moradi, N, Öjemalm, K, Westman, M, Angeletti, D, Kjellin, H, Lehtiö, J, Blixt, O, Ideström, L, Gahmberg, CG, Storry, JR, Hult, AK, Olsson, ML, von Heijne, G, Nilsson, I and Wahlgren, M (2015) RIFINs are adhesins implicated in severe Plasmodium falciparum malaria. Nature Medicine 21, 314317.
Handunnetti, SM, van Schravendijk, MR, Hasler, T, Barnwell, JW, Greenwalt, DE and Howard, RJ (1992) Involvement of CD36 on erythrocytes as a rosetting receptor for Plasmodium falciparum-infected erythrocytes. Blood 80, 20972104.
Hawksworth, J, Satchwell, TJ, Meinders, M, Daniels, DE, Regan, F, Thornton, NM, Wilson, MC, Dobbe, JG, Streekstra, GJ, Trakarnsanga, K, Heesom, KJ, Anstee, DJ, Frayne, J and Toye, AM (2018) Enhancement of red blood cell transfusion compatibility using CRISPR-mediated erythroblast gene editing. EMBO Molecular Medicine 10, e8454. doi: 10.15252/emmm.201708454.
Heddini, A, Pettersson, F, Kai, O, Shafi, J, Obiero, J, Chen, Q, Barragan, A, Wahlgren, M and Marsh, K (2001) Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infection and Immunity 69, 58495856.
Hviid, L and Jensen, AT (2015) Pfemp1 – a parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Advances in Parasitology 88, 5184.
Ito, N, Nishi, K, Kawahara, S, Okamura, Y, Hirota, T, Rand, S, Fechner, G and Brinkmann, B (1990) Difference in the ability of blood group-specific lectins and monoclonal antibodies to recognize the ABH antigens in human tissues. Histochemical Journal 22, 604614.
Jaskiewicz, E, Peyrard, T, Kaczmarek, R, Zerka, A, Jodlowska, M and Czerwinski, M (2018) The Gerbich blood group system: old knowledge, new importance. Transfusion Medicine Reviews 32, 111116.
Juillerat, A, Igonet, S, Vigan-Womas, I, Guillotte, M, Gangnard, S, Faure, G, Baron, B, Raynal, B, Mercereau-Puijalon, O and Bentley, GA (2010) Biochemical and biophysical characterisation of DBL1alpha1-varO, the rosetting domain of PfEMP1 from the VarO line of Plasmodium falciparum. Molecular and Biochemical Parasitology 170, 8492.
Juillerat, A, Lewit-Bentley, A, Guillotte, M, Gangnard, S, Hessel, A, Baron, B, Vigan-Womas, I, England, P, Mercereau-Puijalon, O and Bentley, GA (2011) Structure of a Plasmodium falciparum PfEMP1 rosetting domain reveals a role for the N-terminal segment in heparin-mediated rosette inhibition. Proceedings of the National Academy of Sciences USA 108, 52435248.
Kanjee, U, Grüring, C, Chaand, M, Lin, KM, Egan, E, Manzo, J, Jones, PL, Yu, T, Barker, R, Weekes, MP and Duraisingh, MT (2017) CRISPR/cas9 knockouts reveal genetic interaction between strain-transcendent erythrocyte determinants of. Proceedings of the National Academy of Sciences USA 114, E9356E9365.
Kaul, DK, Roth, EF, Nagel, RL, Howard, RJ and Handunnetti, SM (1991) Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78, 812819.
Kraemer, SM and Smith, JD (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Current Opinion in Microbiology 9, 374380.
Kun, JF, Schmidt-Ott, RJ, Lehman, LG, Lell, B, Luckner, D, Greve, B, Matousek, P and Kremsner, PG (1998) Merozoite surface antigen 1 and 2 genotypes and rosetting of Plasmodium falciparum in severe and mild malaria in Lambaréné, Gabon. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 110114.
Kurita, R, Suda, N, Sudo, K, Miharada, K, Hiroyama, T, Miyoshi, H, Tani, K and Nakamura, Y (2013) Establishment of immortalized human erythroid progenitor cell lines able to produce enucleated red blood cells. PLoS ONE 8, e59890.
Kyriacou, HM, Stone, GN, Challis, RJ, Raza, A, Lyke, KE, Thera, MA, Koné, AK, Doumbo, OK, Plowe, CV and Rowe, JA (2006) Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Molecular and Biochemical Parasitology 150, 211218.
Kyriacou, HM, Steen, KE, Raza, A, Arman, M, Warimwe, G, Bull, PC, Havlik, I and Rowe, JA (2007) In vitro inhibition of Plasmodium falciparum rosette formation by Curdlan sulfate. Antimicrobial Agents and Chemotherapy 51, 13211326.
Le Scanf, C, Vigan-Womas, I, Contamin, H, Guillotte, M, Bischoff, E and Mercereau-Puijalon, O (2008) Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey. Microbes and Infection 10, 447451.
Lee, WC, Malleret, B, Lau, YL, Mauduit, M, Fong, MY, Cho, JS, Suwanarusk, R, Zhang, R, Albrecht, L, Costa, FT, Preiser, P, McGready, R, Renia, L, Nosten, F and Russell, B (2014) Glycophorin C (CD236R) mediates vivax malaria parasite rosetting to normocytes. Blood 123, e100e109.
Leffler, EM, Band, G, Busby, GBJ, Kivinen, K, Le, QS, Clarke, GM, Bojang, KA, Conway, DJ, Jallow, M, Sisay-Joof, F, Bougouma, EC, Mangano, VD, Modiano, D, Sirima, SB, Achidi, E, Apinjoh, TO, Marsh, K, Ndila, CM, Peshu, N, Williams, TN, Drakeley, C, Manjurano, A, Reyburn, H, Riley, E, Kachala, D, Molyneux, M, Nyirongo, V, Taylor, T, Thornton, N, Tilley, L, Grimsley, S, Drury, E, Stalker, J, Cornelius, V, Hubbart, C, Jeffreys, AE, Rowlands, K, Rockett, KA, Spencer, CCA, Kwiatkowski, DP and Malaria Genomic Epidemiology Network (2017) Resistance to malaria through structural variation of red blood cell invasion receptors. Science 356, eaam6393. doi: 10.1126/science.aam6393.
Leitgeb, AM, Blomqvist, K, Cho-Ngwa, F, Samje, M, Nde, P, Titanji, V and Wahlgren, M (2011) Low anticoagulant heparin disrupts Plasmodium falciparum rosettes in fresh clinical isolates. American Journal of Tropical Medicine and Hygiene 84, 390396.
Leitgeb, AM, Charunwatthana, P, Rueangveerayut, R, Uthaisin, C, Silamut, K, Chotivanich, K, Sila, P, Moll, K, Lee, SJ, Lindgren, M, Holmer, E, Färnert, A, Kiwuwa, MS, Kristensen, J, Herder, C, Tarning, J, Wahlgren, M and Dondorp, AM (2017) Inhibition of merozoite invasion and transient de-sequestration by sevuparin in humans with Plasmodium falciparum malaria. PLoS ONE 12, e0188754.
Li, JS, Jaggers, J and Anderson, PA (2006) The use of TP10, soluble complement receptor 1, in cardiopulmonary bypass. Expert Reviews in Cardiovascular Therapy 4, 649654.
Lowe, BS, Mosobo, M and Bull, PC (1998) All four species of human malaria parasites form rosettes. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 526.
Lublin, DM, Griffith, RC and Atkinson, JP (1986) Influence of glycosylation on allelic and cell-specific Mr variation, receptor processing, and ligand binding of the human complement C3b/C4b receptor. Journal of Biological Chemistry 261, 57365744.
Luginbuhl, A, Nikolic, M, Beck, HP, Wahlgren, M and Lutz, HU (2007) Complement factor D, albumin, and immunoglobulin G anti-band 3 protein antibodies mimic serum in promoting rosetting of malaria-infected red blood cells. Infection and Immunity 75, 17711777.
Maier, AG, Duraisingh, MT, Reeder, JC, Patel, SS, Kazura, JW, Zimmerman, PA and Cowman, AF (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nature Medicine 9, 8792.
Malaria Genomic Epidemiology Network (2014) Reappraisal of known malaria resistance loci in a large multicenter study. Nature Genetics 46, 11971204.
Marín-Menéndez, A, Bardají, A, Martínez-Espinosa, FE, Bôtto-Menezes, C, Lacerda, MV, Ortiz, J, Cisteró, P, Piqueras, M, Felger, I, Müeller, I, Ordi, J, del Portillo, H, Menéndez, C, Wahlgren, M and Mayor, A (2013) Rosetting in Plasmodium vivax: a cytoadhesion phenotype associated with anaemia. PLoS Neglected Tropical Diseases 7, e2155.
Mayer, DC, Jiang, L, Achur, RN, Kakizaki, I, Gowda, DC and Miller, LH (2006) The glycophorin C N-linked glycan is a critical component of the ligand for the Plasmodium falciparum erythrocyte receptor BAEBL. Proceedings of the National Academy of Sciences USA 103, 23582362.
McGilvray, ID, Serghides, L, Kapus, A, Rotstein, OD and Kain, KC (2000) Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 96, 32313240.
McMorran, BJ, Wieczorski, L, Drysdale, KE, Chan, JA, Huang, HM, Smith, C, Mitiku, C, Beeson, JG, Burgio, G and Foote, SJ (2012) Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 338, 13481351.
Miller, LH, Baruch, DI, Marsh, K and Doumbo, OK (2002) The pathogenic basis of malaria. Nature 415, 673679.
Moll, K, Palmkvist, M, Ch'ng, J, Kiwuwa, MS and Wahlgren, M (2015) Evasion of immunity to Plasmodium falciparum: rosettes of blood group A impair recognition of PfEMP1. PLoS ONE 10, e0145120.
Moulds, JM (2010) The Knops blood-group system: a review. Immunohematology 26, 27.
Moulds, JM, Moulds, JJ, Brown, M and Atkinson, JP (1992) Antiglobulin testing for CR1-related (Knops/McCoy/Swain-Langley/York) blood group antigens: negative and weak reactions are caused by variable expression of CR1. Vox Sanguinis 62, 230235.
Nagayasu, E, Ito, M, Akaki, M, Nakano, Y, Kimura, M, Looareesuwan, S and Aikawa, M (2001) CR1 density polymorphism on erythrocytes of falciparum malaria patients in Thailand. American Journal of Tropical Medicine and Hygiene 64, 15.
Ndila, CM, Uyoga, S, Macharia, AW, Nyutu, G, Peshu, N, Ojal, J, Shebe, M, Awuondo, KO, Mturi, N, Tsofa, B, Sepulveda, N, Clark, TG, Band, G, Clarke, G, Rowlands, K, Hubbart, C, Jeffreys, A, Kariuki, S, Marsh, K, Mackinnon, M, Maitland, K, Kwiatkowski, DP, Rockett, KA, Williams, TN and Malaria, GENC (2018) Human candidate gene polymorphisms and risk of severe malaria in children in Kilifi, Kenya: a case-control association study. Lancet Haematology 5, e333e345.
Newbold, C, Warn, P, Black, G, Berendt, A, Craig, A, Snow, B, Msobo, M, Peshu, N and Marsh, K (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 57, 389398.
Niang, M, Bei, AK, Madnani, KG, Pelly, S, Dankwa, S, Kanjee, U, Gunalan, K, Amaladoss, A, Yeo, KP, Bob, NS, Malleret, B, Duraisingh, MT and Preiser, PR (2014) STEVOR is a Plasmodium falciparum erythrocyte binding protein that mediates merozoite invasion and rosetting. Cell Host & Microbe 16, 8193.
Nickells, M, Hauhart, R, Krych, M, Subramanian, VB, Geoghegan-Barek, K, Marsh, HC Jr. and Atkinson, JP (1998) Mapping epitopes for 20 monoclonal antibodies to CR1. Clinical and Experimental Immunology 112, 2733.
Ochola, LB, Siddondo, BR, Ocholla, H, Nkya, S, Kimani, EN, Williams, TN, Makale, JO, Liljander, A, Urban, BC, Bull, PC, Szestak, T, Marsh, K and Craig, AG (2011) Specific receptor usage in Plasmodium falciparum cytoadherence is associated with disease outcome. PLoS ONE 6, e14741.
Opi, DH, Swann, O, Macharia, A, Uyoga, S, Band, G, Ndila, CM, Harrison, E, Thera, MA, Kone, AK, Diallo, DA, Doumbo, OK, Lyke, KE, Plowe, C, Moulds, JM, Shebbe, M, Mturi, N, Peshu, N, Maitland, K, Raza, A, Kwiatkowski, DP, Rockett, KA, Williams, T and Rowe, JA (2018) Two complement receptor one alleles have opposing associations with cerebral malaria and interact with α + thalassaemia. Elife 7, e31579. doi: 10.7554/eLife.31579.
Panda, AK, Panda, M, Tripathy, R, Pattanaik, SS, Ravindran, B and Das, BK (2012) Complement receptor 1 variants confer protection from severe malaria in Odisha, India. PLoS ONE 7, e49420.
Patel, SS, Mehlotra, RK, Kastens, W, Mgone, CS, Kazura, JW and Zimmerman, PA (2001) The association of the glycophorin C exon 3 deletion with ovalocytosis and malaria susceptibility in the Wosera, Papua New Guinea. Blood 98, 34893491.
Pathak, V, Colah, R and Ghosh, K (2016) Correlation between ‘H’ blood group antigen and Plasmodium falciparum invasion. Annals of Hematology 95, 10671075.
Pipitaporn, B, Sueblinvong, T, Dharmkrong-at, A and Udomsangpetch, R (2000) Rosetting of Plasmodium falciparum required multiple components of the uninfected erythrocytes. Asian Pacific Journal of Allergy and Immunology 18, 2935.
Rampengan, TH (1991) Cerebral malaria in children. Comparative study between heparin, dexamethasone and placebo. Paediatrica Indonesiana 31, 5966.
Reddy, YN, Siedlecki, AM and Francis, JM (2017) Breaking down the complement system: a review and update on novel therapies. Current Opinion in Nephrology and Hypertension 26, 123128.
Ribacke, U, Moll, K, Albrecht, L, Ahmed Ismail, H, Normark, J, Flaberg, E, Szekely, L, Hultenby, K, Persson, KE, Egwang, TG and Wahlgren, M (2013) Improved in vitro culture of Plasmodium falciparum permits establishment of clinical isolates with preserved multiplication, invasion and rosetting phenotypes. PLoS ONE 8, e69781.
Ringwald, P, Peyron, F, Lepers, JP, Rabarison, P, Rakotomalala, C, Razanamparany, M, Rabodonirina, M, Roux, J and Le Bras, J (1993) Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infection and Immunity 61, 51985204.
Robinson, BA, Welch, TL and Smith, JD (2003) Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Molecular Microbiology 47, 12651278.
Rogerson, SJ, Reeder, JC, al-Yaman, F and Brown, GV (1994) Sulfated glycoconjugates as disrupters of Plasmodium falciparum erythrocyte rosettes. American Journal of Tropical Medicine and Hygiene 51, 198203.
Rout, R, Dhangadamajhi, G, Mohapatra, BN, Kar, SK and Ranjit, M (2011) High CR1 level and related polymorphic variants are associated with cerebral malaria in eastern-India. Infection Genetics and Evolution 11, 139144.
Rout, R, Dhangadamajhi, G, Ghadei, M, Mohapatra, BN, Kar, SK and Ranjit, M (2012) Blood group phenotypes A and B are risk factors for cerebral malaria in Odisha, India. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 538543.
Rowe, A, Berendt, AR, Marsh, K and Newbold, CI (1994) Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes. Experimental Parasitology 79, 506516.
Rowe, A, Obeiro, J, Newbold, CI and Marsh, K (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infection and Immunity 63, 23232326.
Rowe, JA, Moulds, JM, Newbold, CI and Miller, LH (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388, 292295.
Rowe, JA, Rogerson, SJ, Raza, A, Moulds, JM, Kazatchkine, MD, Marsh, K, Newbold, CI, Atkinson, JP and Miller, LH (2000) Mapping of the region of complement receptor (CR) 1 required for Plasmodium falciparum rosetting and demonstration of the importance of CR1 in rosetting in field isolates. Journal of Immunology 165, 63416346.
Rowe, JA, Obiero, J, Marsh, K and Raza, A (2002) Short report: positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. American Journal of Tropical Medicine and Hygiene 66, 458460.
Rowe, JA, Handel, IG, Thera, MA, Deans, AM, Lyke, KE, Koné, A, Diallo, DA, Raza, A, Kai, O, Marsh, K, Plowe, CV, Doumbo, OK and Moulds, JM (2007) Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proceedings of the National Academy of Sciences USA 104, 1747117476.
Rowe, JA, Claessens, A, Corrigan, RA and Arman, M (2009 a) Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Reviews in Molecular Medicine 11, e16.
Rowe, JA, Opi, DH and Williams, TN (2009 b) Blood groups and malaria: fresh insights into pathogenesis and identification of targets for intervention. Current Opinion in Hematology 16, 480487.
Saiwaew, S, Sritabal, J, Piaraksa, N, Keayarsa, S, Ruengweerayut, R, Utaisin, C, Sila, P, Niramis, R, Udomsangpetch, R, Charunwatthana, P, Pongponratn, E, Pukrittayakamee, S, Leitgeb, AM, Wahlgren, M, Lee, SJ, Day, NP, White, NJ, Dondorp, AM and Chotivanich, K (2017) Effects of sevuparin on rosette formation and cytoadherence of Plasmodium falciparum infected erythrocytes. PLoS ONE 12, e0172718.
Schmidt, CQ, Kennedy, AT and Tham, WH (2015) More than just immune evasion: Hijacking complement by Plasmodium falciparum. Molecular Immunology 67, 7184.
Scholander, C, Treutiger, CJ, Hultenby, K and Wahlgren, M (1996) Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nature Medicine 2, 204208.
Scully, EJ, Shabani, E, Rangel, GW, Gruring, C, Kanjee, U, Clark, MA, Chaand, M, Kurita, R, Nakamura, Y, Ferreira, MU and Duraisingh, MT (2019) Generation of an immortalized erythroid progenitor cell line from peripheral blood: a model system for the functional analysis of Plasmodium spp. invasion. American Journal of Hematology 94, 963974.
Semblat, JP, Ghumra, A, Czajkowsky, DM, Wallis, R, Mitchell, DA, Raza, A and Rowe, JA (2015) Identification of the minimal binding region of a Plasmodium falciparum IgM binding PfEMP1 domain. Molecular and Biochemical Parasitology 201, 7682.
Silverstein, RL and Febbraio, M (2009) CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Science Signaling 2, re3.
Sim, BK, Chitnis, CE, Wasniowska, K, Hadley, TJ and Miller, LH (1994) Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264, 19411944.
Sinha, S, Jha, GN, Anand, P, Qidwai, T, Pati, SS, Mohanty, S, Mishra, SK, Tyagi, PK, Sharma, SK, Venkatesh, V and Habib, S (2009) CR1 levels and gene polymorphisms exhibit differential association with falciparum malaria in regions of varying disease endemicity. Human Immunology 70, 244250.
Song, B, Fan, Y, He, W, Zhu, D, Niu, X, Wang, D, Ou, Z, Luo, M and Sun, X (2015) Improved hematopoietic differentiation efficiency of gene-corrected beta-thalassemia induced pluripotent stem cells by CRISPR/Cas9 system. Stem Cells and Development 24, 10531065.
Stevenson, L, Huda, P, Jeppesen, A, Laursen, E, Rowe, JA, Craig, A, Streicher, W, Barfod, L and Hviid, L (2015 a) Investigating the function of Fc-specific binding of IgM to Plasmodium falciparum erythrocyte membrane protein 1 mediating erythrocyte rosetting. Cellular Microbiology 17, 819831.
Stevenson, L, Laursen, E, Cowan, GJ, Bandoh, B, Barfod, L, Cavanagh, DR, Andersen, GR and Hviid, L (2015 b) α2-Macroglobulin can crosslink multiple Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) molecules and may facilitate adhesion of parasitized erythrocytes. PLoS Pathogens 11, e1005022.
Stoler-Barak, L, Moussion, C, Shezen, E, Hatzav, M, Sixt, M and Alon, R (2014) Blood vessels pattern heparan sulfate gradients between their apical and basolateral aspects. PLoS ONE 9, e85699.
Teeranaipong, P, Ohashi, J, Patarapotikul, J, Kimura, R, Nuchnoi, P, Hananantachai, H, Naka, I, Putaporntip, C, Jongwutiwes, S and Tokunaga, K (2008) A functional single-nucleotide polymorphism in the CR1 promoter region contributes to protection against cerebral malaria. Journal of Infectious Diseases 198, 18801891.
Tekeste, Z and Petros, B (2010) The ABO blood group and Plasmodium falciparum malaria in Awash, Metehara and Ziway areas, Ethiopia. Malaria Journal 9, 280.
Tetteh-Quarcoo, PB, Schmidt, CQ, Tham, WH, Hauhart, R, Mertens, HD, Rowe, A, Atkinson, JP, Cowman, AF, Rowe, JA and Barlow, PN (2012) Lack of evidence from studies of soluble protein fragments that Knops blood group polymorphisms in complement receptor-type 1 are driven by malaria. PLoS ONE 7, e34820.
Thathy, V, Moulds, JM, Guyah, B, Otieno, W and Stoute, JA (2005) Complement receptor 1 polymorphisms associated with resistance to severe malaria in Kenya. Malaria Journal 4, 54.
Theron, M, Cross, N, Cawkill, P, Bustamante, LY and Rayner, JC (2018) An in vitro erythrocyte preference assay reveals that Plasmodium falciparum parasites prefer Type O over Type A erythrocytes. Scientific Reports 8, 8133.
Thielen, AJF, Zeerleder, S and Wouters, D (2018) Consequences of dysregulated complement regulators on red blood cells. Blood Reviews 32, 280288.
Trakarnsanga, K, Griffiths, RE, Wilson, MC, Blair, A, Satchwell, TJ, Meinders, M, Cogan, N, Kupzig, S, Kurita, R, Nakamura, Y, Toye, AM, Anstee, DJ and Frayne, J (2017) An immortalized adult human erythroid line facilitates sustainable and scalable generation of functional red cells. Nature Communications 8, 14750.
Treutiger, CJ, Hedlund, I, Helmby, H, Carlson, J, Jepson, A, Twumasi, P, Kwiatkowski, D, Greenwood, BM and Wahlgren, M (1992) Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. American Journal of Tropical Medicine and Hygiene 46, 503510.
Treutiger, CJ, Scholander, C, Carlson, J, McAdam, KP, Raynes, JG, Falksveden, L and Wahlgren, M (1999) Rouleaux-forming serum proteins are involved in the rosetting of Plasmodium falciparum-infected erythrocytes. Experimental Parasitology 93, 215224.
Udomsangpetch, R, Wåhlin, B, Carlson, J, Berzins, K, Torii, M, Aikawa, M, Perlmann, P and Wahlgren, M (1989) Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. Journal of Experimental Medicine 169, 18351840.
Udomsangpetch, R, Webster, HK, Pattanapanyasat, K, Pitchayangkul, S and Thaithong, S (1992) Cytoadherence characteristics of rosette-forming Plasmodium falciparum. Infection and Immunity 60, 44834490.
Udomsangpetch, R, Todd, J, Carlson, J and Greenwood, BM (1993) The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. American Journal of Tropical Medicine and Hygiene 48, 149153.
Udomsanpetch, R, Thanikkul, K, Pukrittayakamee, S and White, NJ (1995) Rosette formation by Plasmodium vivax. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 635637.
Uyoga, S, Skorokhod, OA, Opiyo, M, Orori, EN, Williams, TN, Arese, P and Schwarzer, E (2012) Transfer of 4-hydroxynonenal from parasitized to non-parasitized erythrocytes in rosettes. Proposed role in severe malaria anemia. British Journal of Haematology 157, 116124.
van Schravendijk, M, Handunnetti, S, Barnwell, J and Howard, R (1992) Normal human erythrocytes express CD36, an adhesion molecule of monocytes, platelets and endothelial cells. Blood 80, 21052114.
Vigan-Womas, I, Guillotte, M, Le Scanf, C, Igonet, S, Petres, S, Juillerat, A, Badaut, C, Nato, F, Schneider, A, Lavergne, A, Contamin, H, Tall, A, Baril, L, Bentley, GA and Mercereau-Puijalon, O (2008) An in vivo and in vitro model of Plasmodium falciparum rosetting and autoagglutination mediated by varO, a group A var gene encoding a frequent serotype. Infection and Immunity 76, 55655580.
Vigan-Womas, I, Guillotte, M, Juillerat, A, Vallieres, C, Lewit-Bentley, A, Tall, A, Baril, L, Bentley, GA and Mercereau-Puijalon, O (2011) Allelic diversity of the Plasmodium falciparum erythrocyte membrane protein 1 entails variant-specific red cell surface epitopes. PLoS ONE 6, e16544.
Vigan-Womas, I, Guillotte, M, Juillerat, A, Hessel, A, Raynal, B, England, P, Cohen, JH, Bertrand, O, Peyrard, T, Bentley, GA, Lewit-Bentley, A and Mercereau-Puijalon, O (2012) Structural basis for the ABO blood-group dependence of Plasmodium falciparum rosetting. PLoS Pathogens 8, e1002781.
Vogt, AM, Barragan, A, Chen, Q, Kironde, F, Spillmann, D and Wahlgren, M (2003) Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood 101, 24052411.
Vogt, AM, Winter, G, Wahlgren, M and Spillmann, D (2004) Heparan sulphate identified on human erythrocytes: a Plasmodium falciparum receptor. Biochemical Journal 381, 593597.
Wahlgren, M, Carlson, J, Udomsangpetch, R and Perlmann, P (1989) Why do Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes? Parasitology Today 5, 183185.
Wang, CW and Hviid, L (2015) Rifins, rosetting, and red blood cells. Trends in Parasitology 31, 285286.
Warimwe, GM, Fegan, G, Musyoki, JN, Newton, CR, Opiyo, M, Githinji, G, Andisi, C, Menza, F, Kitsao, B, Marsh, K and Bull, PC (2012) Prognostic indicators of life-threatening malaria are associated with distinct parasite variant antigen profiles. Science Translational Medicine 4, 129ra145.
White, NJ, Turner, GD, Day, NP and Dondorp, AM (2013) Lethal malaria: Marchiafava and Bignami were right. Journal of Infectious Diseases 208, 192198.
Wilson, JG, Murphy, EE, Wong, WW, Klickstein, LB, Weis, JH and Fearon, DT (1986) Identification of a restriction fragment length polymorphism by a CR1 cDNA that correlates with the number of CR1 on erythrocytes. Journal of Experimental Medicine 164, 5059.
Wilson, MC, Trakarnsanga, K, Heesom, KJ, Cogan, N, Green, C, Toye, AM, Parsons, SF, Anstee, DJ and Frayne, J (2016) Comparison of the proteome of adult and cord erythroid cells, and changes in the proteome following reticulocyte maturation. Molecular and Cellular Proteomics 15, 19381946.
Wolofsky, KT, Ayi, K, Branch, DR, Hult, AK, Olsson, ML, Liles, WC, Cserti-Gazdewich, CM and Kain, KC (2012) ABO blood groups influence macrophage-mediated phagocytosis of Plasmodium falciparum-infected erythrocytes. PLoS Pathogens 8, e1002942.
World Health Organisation (1986) Severe and complicated malaria. World Health Organization Malaria Action Programme. Transactions of the Royal Society of Tropical Medicine and Hygiene 80(suppl.), 3–50.
Yam, XY, Niang, M, Madnani, KG and Preiser, PR (2017) Three is a crowd – new insights into rosetting in Plasmodium falciparum. Trends in Parasitology 33, 309320.



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed