Alternative titles; symbols
HGNC Approved Gene Symbol: CR1
Cytogenetic location: 1q32.2 Genomic coordinates (GRCh38): 1:207,496,157-207,641,765 (from NCBI)
| Location | Phenotype |
Phenotype MIM number |
Inheritance |
Phenotype mapping key |
|---|---|---|---|---|
| 1q32.2 | [Blood group, Knops system] | 607486 | 3 | |
| {Malaria, severe, resistance to} | 611162 | 3 |
CR1 is a multiple modular protein that binds C3b (120700)/C4b (120820)-opsonized foreign antigens. By doing so, CR1 mediates the immune adherence phenomenon, a fundamental event for destroying microbes and initiating an immunologic response (Smith et al., 2002).
Donius et al. (2013) noted that the Cr1 and Cr2 proteins are generated through alternative splicing of the single mouse Cr2 gene, in contrast with the distinct CR1 and CR2 (120650) genes found in humans and other primates. Donius et al. (2013) showed that Cr1 was the dominant isoform in mouse follicular dendritic cells (FDCs), whereas Cr2 was preferentially expressed by mouse B cells.
Although C3BR was assigned to chromosome 6 by somatic cell hybrid studies (Curry et al., 1976), the immunoelectrophoretic polymorphism does not show linkage to HLA. Atkinson (1983) counseled caution in interpretation of the studies of Curry et al. (1976) because the ligands used were no longer considered acceptable reagents for identifying the receptors, the C3bi receptor (unknown in 1976) may account for all or part of the rosette data, and the Raji cell does not have the CR1 C3b/C4b receptor.
Rodriguez de Cordoba et al. (1985) concluded that factor H (HF; 134370), C4BP (120830), C3BR, and C3DR (CR2; 120650) represent a linked cluster of genes for proteins regulating the activation of C3. They called the cluster RCA for regulators of complement activation. They showed, furthermore, that RCA segregates independently of HLA, the C2, C4, Bf cluster (on 6p), and C3 (on 19p).
Weis et al. (1987) mapped both CR1 and CR2 to chromosome 1q32 by use of partial cDNA clones in in situ hybridization and in Southern analysis of DNA from somatic cell hybrids. Using cDNA probes, Hing et al. (1988) assigned the genes for HF and C3-binding protein to chromosome 1q. Weis et al. (1987) indicated that C3b receptor is the same as C4b receptor (see 120830); it may be, however, that the 2 are closely related proteins determined by closely linked genes on chromosome 1.
Smith et al. (2002) reported the structure of the principal C3b/C4b-binding site (residues 901 to 1,095) of CR1, which revealed 3 complement control protein modules (modules 15 to 17) in an extended head-to-tail arrangement, with flexibility at the 16-17 junction. Structure-guided mutagenesis identified a positively charged surface region on module 15 that is critical for C4b binding.
In studying Treponema pallidum, Nelson (1953) observed a phenomenon he called immune adherence. Immune adherence is the specific attachment of primate red cells to antigen-antibody complexes in the presence of complement and involves the binding of complement-fixing immune complexes to the immune-adherence receptor, CR1, normally present on human red cells.
CR2 is part of an activating signal complex with CD19 (107265) and CD81 (186845) that transduces a positive signal upon coligation with surface IgM on B cells. Jozsi et al. (2002) showed that aggregated C3, mimicking multimeric C3b, strongly binds to CR1 and inhibits, in a dose-dependent manner, the anti-IgM-induced tyrosine phosphorylation of cytoplasmic proteins, intracellular calcium increase, and proliferation of B lymphocytes. This inhibitory activity occurred even in the presence of IL2 (147680) and IL15 (600554). Jozsi et al. (2002) concluded that CR1 plays a role opposite that of CR2 in the regulation of B-cell activation.
Plasmodium falciparum is responsible for the most severe form of malaria (see 611162) in humans. By incubating erythrocytes with increasing amounts of anti-CR1 antibodies or soluble CR1, followed by immunoprecipitation analysis, Tham et al. (2010) showed that the P. falciparum merozoite ligand PfRh4 bound to CR1. Levels of PfRh4 binding correlated with CR1 expression on the erythrocyte surface, which is controlled by the CR1 exon 22 SNP (120620.0001). Binding was reduced in individuals homozygous for low CR1 expression. Parasite invasion of neuraminidase-treated erythrocytes was also reduced. Tham et al. (2010) concluded that CR1 is an erythrocyte receptor used by P. falciparum PfRh4 for sialic acid-independent invasion.
Reviews
Wilson et al. (1987) reviewed CR1 and the other cell membrane proteins that bind C3 and C4.
CR1 Polymorphisms
Nowak (1987) demonstrated polymorphism of CR1 using the hemagglutination assay with human aggregated IgG and guinea pig complement. Among normal men, 3 phenotypes were distinguished: a high phenotype corresponding to strong agglutination, an intermediate phenotype producing weak agglutination, and a low phenotype that gave no agglutination. In a group of 517 normal men in Poland, these 3 phenotypes occurred in 63.8, 30.6, and 5.6%, respectively. These findings gave an estimated gene frequency of 0.791 and 0.209 for the high and low CR1 alleles, respectively.
Using monoclonal antibodies, Dykman et al. (1983) demonstrated polymorphism of C3BR of red cells. In U.S. whites, the frequency of the A and B alleles was found to be 0.83 and 0.17, respectively. Heterozygotes showed differential expression of the 2 gene products in different cell types. The A allele determines a 190-kD protein, whereas the B allele determines a 220-kD protein. In red cells of heterozygotes, the latter is preferentially expressed. The Bgb blood group, which was raised in a multiparous woman, is an expression of this same protein. Its genetics was always confusing because of the anomalous expression in red cells in heterozygotes. There is cross-reactivity with HLA-B17.
Wilson et al. (1986) identified a HindIII-generated RFLP using a C1 cDNA that correlated with the number of CR1 sites on erythrocytes. They concluded that the genomic polymorphism linked to the CR1 gene was associated with a cis-acting regulatory element for the expression of CR1 on erythrocytes.
Holers et al. (1987) identified an mRNA size polymorphism that correlated with the molecular weight polymorphism of the CR1 gene product. This finding, in addition to the report of several homologous repeats in CR1, is consistent with the hypothesis that the molecular weight polymorphism is determined at the genomic level and was generated by unequal crossing-over.
CR1 is a single-chain glycoprotein with 4 allotypic variants that differ in molecular mass by increments of 40 to 50 kD. The 2 most common variants are termed F and S (or A and B) allotypes and are 250 and 290 kD, respectively. The corresponding CR1 transcripts from various allotypes show incremental differences of 1.3 to 1.5 kD. Wong et al. (1989) described the organization of the S and F alleles of CR1.
CR1 Polymorphisms and Systemic Lupus Erythematosus
The occurrence of excessive amounts of antigen-antibody complexes in systemic lupus erythematosus (SLE; 152700) could be the consequence of either overproduction of autoantibodies (as through polyclonal B-cell activation or altered suppressor T-cell function) or impaired catabolism. A defect in cellular C3b receptors involved in the clearance of immune complexes that have activated the immune system and are coated with C3b has been found and has been thought to be inherited (Miyakawa et al., 1981). Both Miyakawa et al. (1981) and Iida et al. (1982) found CR1 deficiency in systemic lupus erythematosus (SLE; 152700).
Wilson et al. (1982) showed that the number of C3b receptors on erythrocytes is genetically regulated. Receptor sites on red cells were decreased in SLE patients and their relatives; spouses of SLE patients had normal values. Three phenotypes were demonstrated in the normal population: HH (5,500-8,500 sites per cell), HL (3,000-5,499 sites per cell) and LL (less than 3,000 sites per cell). Among normal subjects, the 3 phenotypes were present in a frequency of 34, 54, and 12%, respectively; the figures were 5, 42, and 53% for SLE patients. Hardy-Weinberg and pedigree analyses were consistent with codominant inheritance of high and low alleles. Wilson (1982) concluded that the locus for the C3b receptor numerical phenotype is separate from the structural locus for C3b receptor; of 6 pairs of HLA-identical sibs, 4 were discordant for the numerical phenotype.
Wilson et al. (1985) implicated autoantibodies to the C3b/C4b receptor and absence of this receptor in the clinical manifestations of SLE.
In a review, Wilson et al. (1987) discussed the mechanism by which inherited and acquired abnormalities of CR1 might participate in the pathogenesis of SLE.
Moldenhauer et al. (1987) concluded that inherited deficiency of CR1 does not cause susceptibility to SLE. Deficiency of CR1 was found on red cells of patients with SLE; however, the 2 alleles defined by the RFLP identified using a cDNA probe for CR1 showed the same frequency in normals and in patients with SLE.
Nath et al. (2005) performed a metaanalysis of several studies that had tested the association of CR1 or interleukin-10 (IL10; 124092) polymorphisms with SLE. The CR1 metaanalysis revealed the association of the S structural variant of CR1 with SLE; the IL10 metaanalysis showed the association of the IL10 G11 allele and SLE in whole populations and of the promoter -1082A-G polymorphism and SLE in Asians.
CR1 Polymorphisms and Resistance to Malaria
The Knops blood group system (607486) is a system of antigens located on CR1. Rowe et al. (1997) demonstrated that CR1 is involved in malarial rosetting, a process associated with cerebral malaria (see 611162), which is the major cause of mortality in Plasmodium falciparum malaria. They showed that rosette formation was considerably reduced with Sl(a-) Knops phenotype RBCs, indicating that this antigen on CR1 is involved in rosetting. Because Sl(a-) is more common in persons of African ancestry, a protective role was suggested (Moulds and Moulds, 2000).
CR1-deficient RBCs show greatly reduced rosetting, leading Cockburn et al. (2004) to hypothesize that if rosetting is a direct cause of malaria pathology, CR1-deficient individuals should be protected against severe disease. They showed that RBC CR1 deficiency occurs in up to 80% of healthy individuals from the malaria-endemic regions of Papua New Guinea. This RBC CR1 deficiency is associated with polymorphisms in the CR1 gene and, unexpectedly, with alpha-thalassemia, a common genetic disorder in Melanesian populations. Analysis of a case-control study demonstrated that the CR1 polymorphisms and alpha-thalassemia independently confer protection against severe malaria. Thus, Cockburn et al. (2004) identified CR1 as a new malaria resistance gene and provided compelling evidence that rosetting is an important parasite virulence phenotype that should be a target for drug and vaccine development.
CR1 Polymorphisms and Other Diseases
Ohi et al. (1986) found CR1 deficiency in 2 cases of mesangiocapillary glomerulonephritis.
Eumycetoma is a tumorous fungal infection, typically of the hands or feet, characterized by the infiltration of large numbers of neutrophils. It is caused by Madurella mycetomatis, a pathogen that is abundant in the soil and on the vegetation of Sudan, where the disease is common. Van de Sande et al. (2007) noted that ELISA has shown near universal IgG seropositivity in mycetoma patients and controls from endemic areas, but no seropositivity in European controls, implying that most individuals in endemic areas are exposed to the pathogen, but only a small percentage develop disease. Van de Sande et al. (2007) studied 11 SNPs in genes involved in neutrophil function in 125 Sudanese mycetoma patients and 140 ethnically and geographically matched controls and found significant differences in allele distributions for SNPs in IL8 (146930), IL8RB (146928), TSP4 (THBS4; 600715), NOS2 (163730), and CR1. Serum IL8 was significantly higher in patients compared with controls, while nitrite/nitrate levels were lower in patients and seemed to be associated with delayed wound healing. Van de Sande et al. (2007) concluded that there is a genetic predisposition toward susceptibility to mycetoma.
For a discussion of a possible association between variation in the CR1 gene and Alzheimer disease, see 104300.
Fairweather et al. (2006) found that mice deficient in both Cr1 and Cr2 had increased acute myocarditis and pericardial fibrosis due to coxsackievirus B3 (CVB3), leading to early progression to dilated cardiomyopathy and heart failure. Increased inflammation was not associated with increased viral replication. Immunofluorescence microscopy demonstrated increased numbers of macrophages, higher Il1b (147720) levels, and immune complex deposition in the heart. The mouse complement regulatory protein, Crry, was increased in cardiac macrophages, while immature B cells were increased in mutant mice after CVB3 infection. Fairweather et al. (2006) concluded that CR1/CR2 expression is not necessary for CVB3 clearance, but it is involved in protection against immune-mediated damage to the heart.
Donius et al. (2013) found that mice with specific deletion of the Cr1 isoform of the Cr2 gene (i.e., Cr1-knockout mice) had normal quantity of Cr2 protein on B cells and normal function and development of B-cell subsets. However, the quantity of Cr1 protein on FDCs was minimal in Cr1-knockout mice. Immunization experiments demonstrated that Cr1-knockout mice produced reduced antibody levels against a high dose of T-dependent, but not T-independent, antigens compared with controls. Germinal centers (GCs) from immunized Cr1-knockout mice generated fewer activated B cells in response to T-dependent antigens. However, Cr1-knockout mice did not suffer from reduced immunity to Streptococcus pneumoniae, as did Cr1/Cr2-knockout mice.
In a follow-up to Donius et al. (2013), Donius et al. (2014) found that immunized Cr1-knockout mice had normal initial generation of activated GC B cells, but they were unable to maintain these cells, indicating that Cr1 expression on B cells was required for GC B-cell maintenance but not initiation. Cr1 deletion also resulted in reduction of antigen-specific IgM titer and IgM memory B cells, but not antigen-specific IgG.
Xiang et al. (1999) identified 3 single-nucleotide polymorphisms (SNPs) in the CR1 gene that are associated with CR1 expression levels in Caucasians. One of these, the CR1 exon 22 SNP (A/G at nucleotide 3650), showed the strongest association with RBC CR1 levels in populations from 2 malaria-endemic sites in Papua New Guinea (PNG) and in Edinburgh, UK. In all 3 populations the exon 22 genotype had a highly significant effect on RBC CR1 level, with carriers of the G3650 low (L) expression allele having significantly lower CR1 levels than HH individuals. The RBC CR1 levels of HL individuals were intermediate between those of HH and LL individuals, as expected for codominant alleles. The frequency of the CR1 L allele in the malarious regions of PNG were the highest described in the world. Its frequency in the nonmalarious Eastern Highlands Province of PNG were significantly lower than in the malarious regions. Cockburn et al. (2004) showed that RBC CR1 deficiency as reflected by the LL genotype occurs in up to 80% of healthy individuals from the malaria-endemic regions of PNG. Although the polymorphism in the CR1 gene was associated with alpha-thalassemia, a common genetic disorder in Melanesian populations, analysis of a case-control study demonstrated that CR1 polymorphisms and alpha-thalassemia independently confer protection against severe malaria (611162).
Tham et al. (2010) showed that levels of binding between the P. falciparum merozoite ligand PfRh4 and CR1 correlated with CR1 expression on the erythrocyte surface, as controlled by the CR1 exon 22 SNP. Binding was reduced in individuals homozygous for the L allele compared with those homozygous for the H allele.
Atkinson, J. P. Personal Communication. St. Louis, Mo. 3/7/1983.
Cockburn, I. A., Mackinnon, M. J., O'Donnell, A., Allen, S. J., Moulds, J. M., Baisor, M., Bockarie, M., Reeder, J. C., Rowe, J. A. A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc. Nat. Acad. Sci. 101: 272-277, 2004. [PubMed: 14694201] [Full Text: https://doi.org/10.1073/pnas.0305306101]
Curry, R. A., Dierich, M. P., Pellegrino, M. A., Hoch, H. A. Evidence for linkage between HLA antigens and receptors for complement components C3b and C3d in human-mouse hybrids. Immunogenetics 3: 465-471, 1976.
Donius, L. R., Handy, J. M., Weis, J. J., Weis, J. H. Optimal germinal center B cell activation and T-dependent antibody responses require expression of the mouse complement receptor Cr1. J. Immun. 191: 434-447, 2013. [PubMed: 23733878] [Full Text: https://doi.org/10.4049/jimmunol.1203176]
Donius, L. R., Weis, J. J., Weis, J. H. Murine complement receptor 1 is required for germinal center B cell maintenance but not initiation. Immunobiology 219: 440-449, 2014. [PubMed: 24636730] [Full Text: https://doi.org/10.1016/j.imbio.2014.02.007]
Dykman, T. R., Cole, J. L., Iida, K., Atkinson, J. P. Polymorphism of human erythrocyte C3b/C4b receptor. Proc. Nat. Acad. Sci. 80: 1698-1702, 1983. [PubMed: 6572933] [Full Text: https://doi.org/10.1073/pnas.80.6.1698]
Dykman, T. R., Cole, J. L., Iida, K., Atkinson, J. P. Structural heterogeneity of the C3b/C4b receptor (CR1) on human peripheral blood cells. J. Exp. Med. 157: 2160-2165, 1983. [PubMed: 6222138] [Full Text: https://doi.org/10.1084/jem.157.6.2160]
Dykman, T. R., Hatch, J. A., Atkinson, J. P. Polymorphism of the human C3b/C4b receptor: identification of a third allele and analysis of receptor phenotypes in families and patients with systemic lupus erythematosus. J. Exp. Med. 159: 691-703, 1984. [PubMed: 6230413] [Full Text: https://doi.org/10.1084/jem.159.3.691]
Fairweather, D., Frisancho-Kiss, S., Njoku, D. B., Nyland, J. F., Kaya, Z., Yusung, S. A., Davis, S. E., Frisancho, J. A., Barrett, M. A., Rose, N. R. Complement receptor 1 and 2 deficiency increases coxsackievirus B3-induced myocarditis, dilated cardiomyopathy, and heart failure by increasing macrophages, IL-1-beta, and immune complex deposition in the heart. J. Immun. 176: 3516-3524, 2006. [PubMed: 16517720] [Full Text: https://doi.org/10.4049/jimmunol.176.6.3516]
Gerdes, J., Hansmann, M.-L., Stein, H., Naiem, M., Mason, D. Y. Ultrastructural localization of human complement C3b receptors in the human kidney as determined by immunoperoxidase staining with the monoclonal antibody C3RTo5. Virchows Arch. B Cell Path. Incl. Molec. Path. 40: 1-7, 1982. [PubMed: 6126949] [Full Text: https://doi.org/10.1007/BF02932845]
Hing, S., Day, A. J., Linton, S. J., Ripoche, J., Sim, R. B., Reid, K. B., Solomon, E. Assignment of complement components C4 binding protein (C4BP) and factor H (FH) to human chromosome 1q, using cDNA probes. Ann. Hum. Genet. 52: 117-122, 1988. [PubMed: 2977721] [Full Text: https://doi.org/10.1111/j.1469-1809.1988.tb01086.x]
Holers, V. M., Chaplin, D. D., Leykam, J. F., Gruner, B. A., Kumar, V., Atkinson, J. P. Human complement C3b/C4b receptor (CR1) mRNA polymorphism that correlates with the CR1 allelic molecular weight polymorphism. Proc. Nat. Acad. Sci. 84: 2459-2463, 1987. [PubMed: 3031685] [Full Text: https://doi.org/10.1073/pnas.84.8.2459]
Iida, K., Mornaghi, R., Nussenzweig, V. Complement receptor (CR1) deficiency in erythrocytes from patients with systemic lupus erythematosus. J. Exp. Med. 155: 1427-1438, 1982. [PubMed: 6978375] [Full Text: https://doi.org/10.1084/jem.155.5.1427]
Jozsi, M., Prechl, J., Bajtay, Z., Erdei, A. Complement receptor type 1 (CD35) mediates inhibitory signals in human B lymphocytes. J. Immun. 168: 2782-2788, 2002. [PubMed: 11884446] [Full Text: https://doi.org/10.4049/jimmunol.168.6.2782]
Miyakawa, Y., Yamada, A., Kosaka, K., Tsuda, F., Kosugi, E., Mayumi, M. Defective immune-adherence (C3b) receptor on erythrocytes from patients with systemic lupus erythematosus. Lancet 318: 493-497, 1981. Note: Originally Volume II. [PubMed: 6115248] [Full Text: https://doi.org/10.1016/s0140-6736(81)90882-5]
Moldenhauer, F., David, J., Fielder, A. H. L., Lachmann, P. J., Walport, M. J. Inherited deficiency of erythrocyte complement receptor type 1 does not cause susceptibility to systemic lupus erythematosus. Arthritis Rheum. 30: 961-966, 1987. [PubMed: 2959289] [Full Text: https://doi.org/10.1002/art.1780300901]
Moulds, J. M., Moulds, J. J. Blood group associations with parasites, bacteria, and viruses. Transfus. Med. Rev. 14: 302-311, 2000. [PubMed: 11055075] [Full Text: https://doi.org/10.1053/tmrv.2000.16227]
Nath, S. K., Harley, J. B., Lee, Y. H. Polymorphisms of complement receptor 1 and interleukin-10 genes and systemic lupus erythematosus: a meta-analysis. Hum. Genet. 118: 225-234, 2005. [PubMed: 16133175] [Full Text: https://doi.org/10.1007/s00439-005-0044-6]
Nelson, R. A. The immune-adherence phenomenon: an immunologically specific reaction between microorganisms and erythrocytes leading to enhanced phagocytosis. Science 118: 733-737, 1953. [PubMed: 13122009] [Full Text: https://doi.org/10.1126/science.118.3077.733]
Nowak, J. S. Genetic variability of complement receptor on human erythrocytes. J. Genet. 66: 133-138, 1987.
Ohi, H., Ikezawa, T., Watanabe, S., Seki, M., Mizutani, Y., Nawa, N., Hatano, M. Two cases of mesangiocapillary glomerulonephritis with CR1 deficiency. (Letter) Nephron 43: 307 only, 1986. [PubMed: 3736743] [Full Text: https://doi.org/10.1159/000183861]
Rodriguez de Cordoba, S., Lublin, D. M., Rubinstein, P., Atkinson, J. P. Human genes for three complement components that regulate the activation of C3 are tightly linked. J. Exp. Med. 161: 1189-1195, 1985. [PubMed: 3157763] [Full Text: https://doi.org/10.1084/jem.161.5.1189]
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, 1997. [PubMed: 9230440] [Full Text: https://doi.org/10.1038/40888]
Smith, B. O., Mallin, R. L., Krych-Goldberg, M., Wang, X., Hauhart, R. E., Bromek, K., Uhrin, D., Atkinson, J. P., Barlow, P. N. Structure of the C3b binding site of CR1 (CD35), the immune adherence receptor. Cell 108: 769-780, 2002. [PubMed: 11955431] [Full Text: https://doi.org/10.1016/s0092-8674(02)00672-4]
Tham, W.-H., Wilson, D. W., Lopaticki, S., Schmidt, C. Q., Tetteh-Quarcoo, P. B., Barlow, P. N., Richard, D., Corbin, J. E., Beeson, J. G., Cowman, A. F. Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc. Nat. Acad. Sci. 107: 17327-17332, 2010. [PubMed: 20855594] [Full Text: https://doi.org/10.1073/pnas.1008151107]
van de Sande, W. W. J., Fahal, A., Verbrugh, H., van Belkum, A. Polymorphisms in genes involved in innate immunity predispose toward mycetoma susceptibility. J. Immun. 179: 3065-3074, 2007. [PubMed: 17709521] [Full Text: https://doi.org/10.4049/jimmunol.179.5.3065]
Weis, J. H., Morton, C. C., Bruns, G. A. P., Weis, J. J., Klickstein, L. B., Wong, W. W., Fearon, D. T. A complement receptor locus: genes encoding C3b/C4b receptor and C3d/Epstein-Barr virus receptor map to 1q32. J. Immun. 138: 312-315, 1987. [PubMed: 3782802] [Full Text: https://www.jimmunol.org/lookup/pmidlookup?view=long&pmid=3782802]
Wilson, J. G., Andriopoulos, N. A., Fearon, D. T. CR1 and the cell membrane proteins that bind C3 and C4: a basic and clinical review. Immun. Res. 6: 192-209, 1987. [PubMed: 2960763] [Full Text: https://doi.org/10.1007/BF02918091]
Wilson, J. G., Jack, R. M., Wong, W. W., Schur, P. H., Fearon, D. T. Autoantibody to the C3b/C4b receptor and absence of this receptor from erythrocytes of a patient with systemic lupus erythematosus. J. Clin. Invest. 76: 182-190, 1985. [PubMed: 4019777] [Full Text: https://doi.org/10.1172/JCI111944]
Wilson, J. G., Murphy, E. E., Wong, W. W., Klickstein, L. B., Weis, J. H., Fearon, D. T. 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. [PubMed: 3014040] [Full Text: https://doi.org/10.1084/jem.164.1.50]
Wilson, J. G., Wong, W. W., Schur, P. H., Fearon, D. T. Mode of inheritance of decreased C3b receptors on erythrocytes of patients with systemic lupus erythematosus. New Eng. J. Med. 307: 981-986, 1982. [PubMed: 7110302] [Full Text: https://doi.org/10.1056/NEJM198210143071604]
Wilson, J. G. Personal Communication. Boston, Mass. 10/25/1982.
Wong, W. W., Cahill, J. M., Rosen, M. D., Kennedy, C. A., Bonaccio, E. T., Morris, M. J., Wilson, J. G., Klickstein, L. B., Fearon, D. T. Structure of the human CR1 gene: molecular basis of the structural and quantitative polymorphisms and identification of a new CR1-like allele. J. Exp. Med. 169: 847-863, 1989. [PubMed: 2564414] [Full Text: https://doi.org/10.1084/jem.169.3.847]
Wong, W. W., Klickstein, L. B., Smith, J. A., Weis, J. H., Fearon, D. T. Identification of a partial cDNA clone for the human receptor for complement fragments C3b/C4b. Proc. Nat. Acad. Sci. 82: 7711-7715, 1985. [PubMed: 2933745] [Full Text: https://doi.org/10.1073/pnas.82.22.7711]
Xiang, L., Rundles, J. R., Hamilton, D. R., Wilson, J. G. Quantitative allele of CR1: coding sequence analysis and comparison of haplotypes in two ethnic groups. J. Immun. 163: 4939-4945, 1999. [PubMed: 10528197]