No Evidence that Knops Blood Group Polymorphisms Affect Complement Receptor 1 Clustering on Erythrocytes

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Swann, O V ^a   Harrison, E M ^a   Opi, D H ^a,b,d   Nyatichi, E ^b   Macharia, A ^b   Uyoga, S ^b   Williams, T N ^b,c   Rowe, J A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d BURNET INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD GROUP ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; CR1 PROTEIN, HUMAN;

CHILD; CLUSTER ANALYSIS; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; FEMALE; GENE DOSAGE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; HUMAN; KENYA; MALE; PHYSIOLOGY;

BLOOD GROUP ANTIGENS; CHILD; CLUSTER ANALYSIS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; FEMALE; GENE DOSAGE; GENOTYPE; HUMANS; KENYA; MALE; POLYMORPHISM, GENETIC; RECEPTORS, COMPLEMENT 3B;

EID: 85038609252     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-17664-9     Document Type: Article

References (70)

1. Fearon, D. T. Human Complement Receptors for C3b (CR1) and C3d (CR2). J. Invest. Dermatol. 85, 53s-57s, https://doi.org/10.1111/1523-1747.ep12275473 (1985)
2. Vik, D. P. & Wong, W. W. Structure of the gene for the F allele of complement receptor type 1 and sequence of the coding region unique to the S allele. J. Immunol. 151, 6214-6224 (1993)
3. Dykman, T. R., Hatch, J. A., Aqua, M. S. & Atkinson, J. P. Polymorphism of the C3b/C4b receptor (CR1): characterization of a fourth allele. J. Immunol. 134, 1787-1789 (1985)
4. Wong, W. W. Structural and Functional Correlation of the Human Complement Receptor Type 1. J. Invest. Dermatol. 94, 64s-67s, https://doi.org/10.1111/1523-1747.ep12875150 (1990)
5. Moulds, J. M., Moulds, J. J., Brown, M. & Atkinson, J. P. 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 Sang 62, 230-235 (1992)
6. Wilson, J. G. et al. Identification of a restriction fragment length polymorphism by a CR1 cDNA that correlates with the number of CR1 on erythrocytes. J. Exp. Med. 164, 50-59 (1986)
7. Herrera, A. H., Xiang, L., Martin, S. G., Lewis, J. & Wilson, J. G. Analysis of complement receptor type 1 (CR1) expression on erythrocytes and of CR1 allelic markers in Caucasian and African American populations. Clin. Immunol. Immunopathol. 87, 176-183 (1998)
8. Rowe, J. A. et al. Erythrocyte CR1 expression level does not correlate with a HindIII restriction fragment length polymorphism in Africans; implications for studies on malaria susceptibility. Genes Immun. 3, 497-500, https://doi.org/10.1038/sj.gene.6363899 (2002)
9. Iida, K. & Nussenzweig, V. Complement receptor is an inhibitor of the complement cascade. J. Exp. Med. 153, 1138-1150, https://doi.org/10.1084/jem.153.5.1138 (1981)
10. Medof, M. E. & Nussenzweig, V. Control of the function of substrate-bound C4b-C3b by the complement receptor Cr1. J. Exp. Med. 159, 1669-1685 (1984)
11. Krych-Goldberg, M. et al. Decay accelerating activity of complement receptor type 1 (CD35). Two active sites are required for dissociating C5 convertases. J. Biol. Chem. 274, 31160-31168 (1999)
12. Klickstein, L. B. et al. Identification of distinct C3b and C4b recognition sites in the human C3b/C4b receptor (CR1, CD35) by deletion mutagenesis. J. Exp. Med. 168, 1699-1717 (1988)
13. Krych, M., Hourcade, D. & Atkinson, J. P. Sites within the complement C3b/C4b receptor important for the specificity of ligand binding. Proc. Nat. Acad. Sci. USA 88, 4353-4357 (1991)
14. Klickstein, L. B., Barbashov, S. F., Liu, T., Jack, R. M. & Nicholson-Weller, A. Complement receptor type 1 (CR1, CD35) is a receptor for C1q. Immunity 7, 345-355 (1997)
15. Ghiran, I. et al. Complement Receptor 1/Cd35 Is a Receptor for Mannan-Binding Lectin. J. Exp. Med. 192, 1797-1808, https://doi.org/10.1084/jem.192.12.1797 (2000)
16. Moulds, J. M. et al. Molecular identification of Knops blood group polymorphisms found in long homologous region D of complement receptor 1. Blood 97, 2879-2885, https://doi.org/10.1182/blood.V97.9.2879 (2001)
17. Tetteh-Quarcoo, P. B. et al. 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, https://doi.org/10.1371/journal.pone.0034820 (2012)
18. Moulds, J. M. The Knops blood-group system: A review. Immunohematol. 26, 2-7 (2010)
19. Rowe, J. A., Moulds, J. M., Newbold, C. I. & Miller, L. H. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388, 292-295, https://doi.org/10.1038/40888 (1997)
20. Thathy, V., Moulds, J., Guyah, B., Otieno, W. & Stoute, J. Complement receptor 1 polymorphisms associated with resistance to severe malaria in Kenya. Malaria J. 4, 54, https://doi.org/10.1186/1475-2875-4-54 (2005)
21. Zimmerman, P. A. et al. CR1 Knops blood group alleles are not associated with severe malaria in the Gambia. Genes Immun 4, 368-373, https://doi.org/10.1038/sj.gene.6363980 (2003)
22. Hansson, H. H. et al. Human genetic polymorphisms in the Knops blood group are not associated with a protective advantage against Plasmodium falciparum malaria in Southern Ghana. Malaria J. 12, 400, https://doi.org/10.1186/1475-2875-12-400 (2013)
23. Schifferli, J. A. & Taylor, R. P. Physiological and pathological aspects of circulating immune complexes. Kidney Int. 35, 993-1003 (1989)
24. Emlen, W., Carl, V. & Burdick, G. Mechanism of transfer of immune complexes from red blood cell CR1 to monocytes. Clin. Exp. Immunol. 89, 8-17 (1992)
25. Paccaud, J. P., Carpentier, J. L. & Schifferli, J. A. Direct evidence for the clustered nature of complement receptors type 1 on the erythrocyte membrane. J. Immunol 141, 3889-3894 (1988)
26. Chevalier, J. & Kazatchkine, M. D. Distribution in clusters of complement receptor type one (CR1) on human erythrocytes. J. Immunol. 142, 2031-2036 (1989)
27. Paccaud, J. P., Carpentier, J. L. & Schifferli, J. A. Difference in the clustering of complement receptor type 1 (CR1) on polymorphonuclear leukocytes and erythrocytes: effect on immune adherence. Euro. J. Immunol. 20, 283-289, https://doi.org/10.1002/eji.1830200209 (1990)
28. Ghiran, I., Glodek, A. M., Weaver, G., Klickstein, L. B. & Nicholson-Weller, A. Ligation of erythrocyte CR1 induces its clustering in complex with scaffolding protein FAP-1. Blood 112, 3465-3473, https://doi.org/10.1182/blood-2008-04-151845 (2008)
29. Glodek, A. M. et al. Ligation of complement receptor 1 increases erythrocyte membrane deformability. Blood 116, 6063-6071, https://doi.org/10.1182/blood-2010-04-273904 (2010)
30. Lapin, Z. J., Höppener, C., Gelbard, H. A. & Novotny, L. Near-field quantification of complement receptor 1 (CR1/CD35) protein clustering in human erythrocytes. J Neuroimmune Pharmacol. 7, 539-543, https://doi.org/10.1007/s11481-012-9346-3 (2012)
31. Melhorn, M. I. et al. CR1-mediated ATP Release by Human Red Blood Cells Promotes CR1 Clustering and Modulates the Immune Transfer Process. J. Biol. Chem. 288, 31139-31153, https://doi.org/10.1074/jbc.M113.486035 (2013)
32. Cosio, F. G., Shen, X. P. & Hebert, L. A. Immune complexes bind preferentially to specific subpopulations of human erythrocytes. Clin. Immunol. Immunopathol. 55, 337-354 (1990)
33. Taylor, R. P., Pocanic, F., Reist, C. & Wright, E. L. Complement-opsonized IgG antibody/dsDNA immune complexes bind to CR1 clusters on isolated human erythrocytes. Clin. Immunol. Immunopathol. 61, 143-160 (1991)
34. Krych-Goldberg, M., Moulds, J. M. & Atkinson, J. P. Human complement receptor type 1 (CR1) binds to a major malarial adhesin. Trends Mol. Med. 8, 531-537 (2002)
35. Biryukov, S. et al. Complement and Antibody-mediated Enhancement of Red Blood Cell Invasion and Growth of Malaria Parasites. EBioMedicine 9, 207-216, https://doi.org/10.1016/j.ebiom.2016.05.015 (2016)
36. Mibei, E. K., Otieno, W. O., Orago, A. S. & Stoute, J. A. Distinct pattern of class and subclass antibodies in immune complexes of children with cerebral malaria and severe malarial anaemia. Parasite Immunol. 30, 334-341, https://doi.org/10.1111/j.1365-3024.2008.01030.x (2008)
37. Jancar, S. & Sanchez Crespo, M. Immune complex-mediated tissue injury: A multistep paradigm. Trends Immunol. 26, 48-55, https://doi.org/10.1016/j.it.2004.11.007 (2005)
38. Debets, J. M. et al. Fc-receptor cross-linking induces rapid secretion of tumor necrosis factor (cachectin) by human peripheral blood monocytes. J. Immunol. 141, 1197-1201 (1988)
39. Kwiatkowski, D. et al. TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 1201-1204 (1990)
40. Opi, D. H., Uyoga, S., Orori, E. N., Williams, T. N. & Rowe, J. A. Red blood cell complement receptor one level varies with Knops blood group, α(+)thalassaemia and age among Kenyan children. Genes Immun. 17, 171-178, https://doi.org/10.1038/gene.2016.2 (2016)
41. Waitumbi, J. N., Donvito, B., Kisserli, A., Cohen, J. H. M. & Stoute, J. A. Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J. Infect. Dis. 190, 1183-1191, https://doi.org/10.1086/423140 (2004)
42. Cockburn, I. A. et al. A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc. Nat. Acad. Sci. USA 101, 272-277, https://doi.org/10.1073/pnas.0305306101 (2004)
43. Chen, C. H. et al. Antibody CR1-2B11 recognizes a non-polymorphic epitope of human CR1 (CD35). Clin. Exp. Immunol 148, 546-554, https://doi.org/10.1111/j.1365-2249.2007.03355.x (2007)
44. Nickells, M. et al. Mapping epitopes for 20 monoclonal antibodies to CR1. Clin. Exp. Immunol. 112, 27-33 (1998)
45. Rowe, A., Obeiro, J., Newbold, C. I. & Marsh, K. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun. 63, 2323-2326 (1995)
46. Rowe, J. A. et al. 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. J. Immunol. 165, 6341-6346 (2000)
47. Spadafora, C. et al. Complement receptor 1 is a sialic acid-independent erythrocyte receptor of Plasmodium falciparum. PLoS Pathog. 6, e1000968, https://doi.org/10.1371/journal.ppat.1000968 (2010)
48. Tham, W.-H. et al. Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc. Nat. Acad. Sci. USA 107, 17327-17332, https://doi.org/10.1073/pnas.1008151107 (2010)
49. Tham, W.-H. et al. Plasmodium falciparum uses a key functional site in complement receptor type-1 for invasion of human erythrocytes. Blood 118, 1923-1933, https://doi.org/10.1182/blood-2011-03-341305 (2011)
50. Park, H. J. et al. Using mutagenesis and structural biology to map the binding site for the Plasmodium falciparum merozoite protein PfRh4 on the human immune adherence receptor. J. Biol. Chem., https://doi.org/10.1074/jbc.M113.520346 (2013)
51. Lim, N. T. et al. Characterization of Inhibitors and Monoclonal Antibodies That Modulate the Interaction between Plasmodium falciparum Adhesin PfRh4 with Its Erythrocyte Receptor Complement Receptor 1. J. Biol. Chem. 290, 25307-25321, https://doi.org/10.1074/jbc.M115.657171 (2015)
52. Jacquet, M. et al. Deciphering complement receptor type 1 interactions with recognition proteins of the lectin complement pathway. J. Immunol. 190, 3721-3731, https://doi.org/10.4049/jimmunol.1202451 (2013)
53. Garred, P. et al. Mannose-binding lectin is a disease modifier in clinical malaria and may function as opsonin for Plasmodium falciparum-infected erythrocytes. Infect. Immun. 71, 5245-5253 (2003)
54. Holmberg, V. et al. Mannose-binding lectin variant associated with severe malaria in young African children. Microbes Infect. 10, 342-348, https://doi.org/10.1016/j.micinf.2007.12.008 (2008)
55. Korir, J. C., Nyakoe, N. K., Awinda, G. & Waitumbi, J. N. Complement Activation by Merozoite Antigens of Plasmodium falciparum. PLoS ONE 9, https://doi.org/10.1371/journal.pone.0105093 (2014)
56. Williams, T. N. et al. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J. Infect. Dis. 192, 178-186, https://doi.org/10.1086/430744 (2005)
57. Scott, J. A. G. et al. Profile: The Kilifi Health and Demographic Surveillance System (KHDSS). Int. J. Epidemiol. 41, 650-657, https://doi.org/10.1093/ije/dys062 (2012)
58. O'Meara, W. P. et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372, 1555-1562, https://doi.org/10.1016/S0140-6736(08)61655-4 (2008)
59. Fry, A. E. et al. Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum. Mol. Gene.t 17, 567-576, https://doi.org/10.1093/hmg/ddm331 (2008)
60. Waterfall, C. M. & Cobb, B. D. Single tube genotyping of sickle cell anaemia using PCR-based SNP analysis. Nucleic Acids Res. 29, E119 (2001)
61. Chong, S. S., Boehm, C. D., Higgs, D. R. & Cutting, G. R. Single-tube multiplex-PCR screen for common deletional determinants of alpha-thalassemia. Blood 95, 360-362 (2000)
62. Rowe, J. A. et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc. Nat. Acad. Sci. USA 104, 17471-17476, https://doi.org/10.1073/pnas.0705390104 (2007)
63. Otenio, W. et al. Sickle Cell Trait (HbAS) is Associated with Increased Expression of Erythrocyte Complement Regulatory Proteins CR1 and CD55 Levels in Children. Int. J. Trop. Dis. 3, 133-147 (2013)
64. Pascual, M., Lutz, H. U., Steiger, G., Stammler, P. & Schifferli, J. A. Release of vesicles enriched in complement receptor 1 from human erythrocytes. J. Immunol. 151, 397-404 (1993)
65. Cockburn, I. A., Donvito, B., Cohen, J. H. M. & Rowe, J. A. A simple method for accurate quantification of complement receptor 1 on erythrocytes preserved by fixing or freezing. J. Immunol. Methods 271, 59-64 (2002)
66. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org (2008)
67. Wickham, H. The Split-Apply-Combine Strategy for Data Analysis. J. Stat. Software 40 (2011)
68. Wickham, H. Ggplot2: elegant graphics for data analysis. (Springer, 2009)
69. lme4: Linear mixed-effects models using Eigen and S4 v. R package version 1.0-4 (2013)
70. Schmidt, C. Q., Kennedy, A. T. & Tham W.-H. More than just immune evasion: Hijacking complement by Plasmodium falciparum. Molecular Immunology 67(1), 71-84 (2015).