Glycophorin C (CD236R) mediates vivax malaria parasite rosetting to normocytes

Blood

Volumn 123, Issue 18, 2014, Pages

  Lee, Wenn Chyau ^a   Malleret, Benoit ^b,c   Lau, Yee Ling ^a   Mauduit, Marjorie ^c   Fong, Mun Yik ^a   Cho, Jee Sun ^b   Suwanarusk, Rossarin ^c   Zhang, Rou ^b   Albrecht, Letusa ^d   Costa, Fabio T M ^d   Preiser, Peter ^e   McGready, Rose ^f,g   Renia, Laurent ^c   Nosten, Francois ^f,g   Russell, Bruce ^b  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

^d UNIVERSITY OF CAMPINAS   (Brazil)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^f MAHIDOL UNIVERSITY   (Thailand)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPHORIN C; ANTIBODY; CD235A ANTIGEN; CD236R ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; LYMPHOCYTE ANTIGEN; MEMBRANE PROTEIN; RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; EX VIVO STUDY; GENE SILENCING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MALARIA FALCIPARUM; MEROZOITE; MICROBIAL COLONIZATION; NONHUMAN; PATHOGENESIS; PLASMODIUM VIVAX MALARIA; PRIORITY JOURNAL; RETICULOCYTE; ROSETTE FORMATION; BLOOD GROUP ABO SYSTEM; BLOOD SMEAR; CELL INVASION; CLINICAL ARTICLE; CRYOPRESERVATION; HOST PARASITE INTERACTION; MEDIATOR; PARASITEMIA; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; RETICULOCYTE COUNT; THAILAND; UMBILICAL CORD BLOOD;

ANIMALS; ANTIBODIES, MONOCLONAL; CRYOPRESERVATION; ERYTHROCYTES; GENE KNOCKDOWN TECHNIQUES; GLYCOPHORIN; HUMANS; MALARIA, VIVAX; PLASMODIUM VIVAX; RECEPTORS, COMPLEMENT 3B; ROSETTE FORMATION; WORKFLOW;

EID: 84900440031     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-12-541698     Document Type: Article

References (43)

1. Lowe BS, Mosobo M, Bull PC. All four species of human malaria parasites form rosettes. Trans R Soc Trop Med Hyg. 1998;92 (5):526. (Pubitemid 28486479)
2. Rowe JA, Obiero J, Marsh K, Raza A. Short report: positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am J Trop Med Hyg. 2002;66 (5): 458-460.
3. Wahlgren M, Carlson J, Udomsangpetch R, Perlmann P. Why do Plasmodium falciparumminfected erythrocytes form spontaneous erythrocyte rosettes? Parasitol Today. 1989;5 (6): 183-185.
4. Rowe JA. Rosetting. In: Sherman IW, ed. Molecular approaches to malaria. Washington, DC: ASM Press; 2005:416-426
5. David PH, Handunnetti SM, Leech JH, Gamage P, Mendis KN. Rosetting: a new cytoadherence property of malaria-infected erythrocytes. Am J Trop Med Hyg. 1988;38 (2):289-297. (Pubitemid 18086108)
6. Handunnetti SM, David PH, Perera KL, Mendis KN. Uninfected erythrocytes form "rosettes" around Plasmodium falciparum infected erythrocytes. Am J Trop Med Hyg. 1989;40 (2): 115-118. (Pubitemid 19086534)
7. Angus BJ, Thanikkul K, Silamut K, White NJ, Udomsangpetch R. Short report: rosette formation in Plasmodium ovale infection. Am J Trop Med Hyg. 1996;55 (5):560-561. (Pubitemid 26392722)
8. Chotivanich KT, Pukrittayakamee S, Simpson JA, White NJ, Udomsangpetch R. Characteristics of Plasmodium vivax-infected erythrocyte rosettes. Am J Trop Med Hyg. 1998;59 (1):73-76. (Pubitemid 28304800)
9. Udomsangpetch R, Wåhlin B, Carlson J, et al. Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. J Exp Med. 1989;169 (5):1835-1840. (Pubitemid 19126838)
10. Udomsanpetch R, Thanikkul K, Pukrittayakamee S, White NJ. Rosette formation by Plasmodium vivax. Trans R Soc Trop Med Hyg. 1995;89 (6): 635-637. (Pubitemid 26016347)
11. al-Yaman F, Genton B, Mokela D, et al. Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg. 1995;89 (1): 55-58.
12. Carlson J, Holmquist G, Taylor DW, Perlmann P, Wahlgren M. Antibodies to a histidine-rich protein (PfHRP1) disrupt spontaneously formed Plasmodium falciparum erythrocyte rosettes. Proc Natl Acad Sci U S A. 1990;87 (7):2511-2515.
13. Ho M, Davis TM, Silamut K, Bunnag D, White NJ. Rosette formation of Plasmodium falciparuminfected erythrocytes from patients with acute malaria. Infect Immun. 1991;59 (6):2135-2139.
14. Treutiger CJ, Hedlund I, Helmby H, et al. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg. 1992;46 (5):503-510.
15. Udomsangpetch R, Todd J, Carlson J, Greenwood BM. The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. Am J Trop Med Hyg. 1993;48 (2): 149-153. (Pubitemid 23083728)
16. Udomsangpetch R, Webster HK, Pattanapanyasat K, Pitchayangkul S, Thaithong S. Cytoadherence characteristics of rosetteforming Plasmodium falciparum. Infect Immun. 1992;60 (11):4483-4490.
17. Wahlgren M, Carlson J, Helmby H, Hedlund I, Treutiger CJ. Molecular mechanisms and biological importance of Plasmodium falciparum erythrocyte rosetting. Mem Inst Oswaldo Cruz. 1992;87 (suppl 3):323-329.
18. Anstey NM, Handojo T, Pain MC, et al. Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and posttreatment alveolar-capillary inflammation. J Infect Dis. 2007;195 (4):589-596. (Pubitemid 46214403)
19. Anstey NM, Russell B, Yeo TW, Price RN. The pathophysiology of vivax malaria. Trends Parasitol. 2009;25 (5):220-227.
20. Baird JK. Severe and fatal vivax malaria challenges 'benign tertian malaria' dogma. Ann Trop Paediatr. 2009;29 (4):251-252.
21. Bammigatti C, Shetty S, Shetty S, Kumar A. Benign tertian malaria - a misnomer? Trop Doct. 2011;41 (3):168-169.
22. Borlon C, Russell B, Sriprawat K, et al. Cryopreserved Plasmodium vivax and cord blood reticulocytes can be used for invasion and short term culture. Int J Parasitol. 2012;42 (2):155-160.
23. Kitchen SF. The infection of reticulocytes by Plasmodium vivax. Am J Trop Med Hyg. 1938; S1-18:347-359.
24. Russell B, Suwanarusk R, Borlon C, et al. A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood. 2011; 118 (13):e74-e81.
25. Russell B, Suwanarusk R, Malleret B, et al. Human ex vivo studies on asexual Plasmodium vivax: the best way forward. Int J Parasitol. 2012; 42 (12):1063-1070.
26. Marín-Menéndez A, Bardají A, Martínez- Espinosa FE, et al. Rosetting in Plasmodium vivax: a cytoadhesion phenotype associated with anaemia. PLoS Negl Trop Dis. 2013;7 (4):e2155.
27. Rowe JA, Moulds JM, Newbold CI, Miller LH. P. falciparum rosetting mediated by a parasitevariant erythrocyte membrane protein and complement-receptor 1. Nature. 1997;388 (6639): 292-295. (Pubitemid 27317975)
28. Barragan A, Kremsner PG, Wahlgren M, Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun. 2000;68 (5):2971-2975. (Pubitemid 30253879)
29. Rowe JA, Handel IG, Thera MA, et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci U S A. 2007;104 (44):17471-17476. (Pubitemid 350219862)
30. Vigan-Womas I, Guillotte M, Juillerat A, et al. Structural basis for the ABO blood-group dependence of Plasmodium falciparum rosetting. PLoS Pathog. 2012;8 (7):e1002781.
31. Leitgeb AM, Blomqvist K, Cho-Ngwa F, et al. Low anticoagulant heparin disrupts Plasmodium falciparum rosettes in fresh clinical isolates. Am J Trop Med Hyg. 2011;84 (3):390-396.
32. Chotivanich K, Sritabal J, Udomsangpetch R, et al. Platelet-induced autoagglutination of Plasmodium falciparum-infected red blood cells and disease severity in Thailand. J Infect Dis. 2004;189 (6):1052-1055. (Pubitemid 38373098)
33. Janes JH, Wang CP, Levin-Edens E, et al. Investigating the host binding signature on the Plasmodium falciparum PfEMP1 protein family. PLoS Pathog. 2011;7 (5):e1002032.
34. Lee WC, Russell B, Lau YL, et al. Giemsa-stained wet mount based method for reticulocyte quantification: a viable alternative in resource limited or malaria endemic settings. PLoS ONE. 2013;8 (4):e60303.
35. Christofinis GJ, Miller H. A simplified method for cryopreservation of Plasmodium falciparum from continuous in vitro cultures. Ann Trop Med Parasitol. 1983;77 (2):123-126. (Pubitemid 13101227)
36. Blomqvist K. Thawing of glycerolyte-frozen parasites with NaCl. In: Moll K, Ljungström I, Perlmann H, Scherf A, Wahlgren M, eds. Methods in malaria research. 5th ed. Manassas, VA: MR4/ATCC; 2008:15.
37. Giarratana MC, Rouard H, Dumont A, et al. Proof of principle for transfusion of in vitrogenerated red blood cells. Blood. 2011; 118 (19):5071-5079.
38. Malleret B, Claser C, Ong AS, et al. A rapid and robust tri-color flow cytometry assay for monitoring malaria parasite development. Sci Rep. 2011;1:118.
39. Bei AK, Duraisingh MT. Functional analysis of erythrocyte determinants of Plasmodium infection. Int J Parasitol. 2012; 42 (6):575-582.
40. Bei AK, Brugnara C, Duraisingh MT. In vitro genetic analysis of an erythrocyte determinant of malaria infection. J Infect Dis. 2010;202 (11): 1722-1727.
41. Corish P, Tyler-Smith C. Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng. 1999;12 (12):1035-1040. (Pubitemid 30011478)
42. Clough B, Atilola FA, Pasvoi G. The role of rosetting in the multiplication of Plasmodium falciparum: rosette formation neither enhances nor targets parasite invasion into uninfected red cells. Br J Haematol. 1998; 100 (1):99-104. (Pubitemid 28051846)
43. Malleret B, Xu F, Mohandas N, et al. Significant biochemical, biophysical and metabolic diversity in circulating human cord blood reticulocytes. PLoS ONE. 2013;8 (10):e76062.