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Duffy antigen system

 
Wikipedia: Duffy antigen system
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Duffy antigen
Identifiers
Symbol DARC
Entrez 2532
HUGO 4035
OMIM 110700
RefSeq NM_002036
UniProt Q16570
Other data
Locus Chr. 1 q21-q22

The Duffy antigen is a protein located on the surface of red blood cells and is named after the patient in which it was discovered. In humans, this protein is encoded by the DARC gene.[1]

The protein encoded by this gene is a glycosylated membrane protein and a non-specific receptor for several chemokines. The protein is also the receptor for the human malarial parasites Plasmodium vivax and Plasmodium knowlesi. Polymorphisms in this gene are the basis of the Duffy blood group system.[2]

The gene is also known as CCBP1, Glycoprotein D (GPD), Dfy and CD234.

Contents

History

In 1950 the Duffy antigen was discovered in a multiply transfused hemophiliac whose serum contained the first example of anti-Fya antibody.[3] In 1951 the antibody to a second antigen, Fyb, was discovered in serum. Using these two antibodies three common phenotypes were defined: Fy(a+b+), Fy(a+b-), and Fy(a-b+).

Genetics and genomics

The Duffy antigen gene (gp-Fy; CD234) is located on the long arm of chromosome 1 (1.q22-1.q23) and was cloned in 1993.[1] The gene was first localised to chromosome 1 in 1968 and was the first blood system antigen to be localised. It is a single copy gene and encodes a 336 amino acid acidic glycoprotein. The gene carries the antigenic determinants of the Duffy blood group system consisting of four alleles - FY*A and FY*B - coding for the Fya and Fyb antigens respectively, FY*X and FY*Fy, five phenotypes (Fy-a, Fy-b, Fy-o, Fy-x and Fy-y) and five antigens. Fya and Fyb differ by in a single amino acid at position 43: glycine in Fya and aspartic acid in Fyb. The genetic basis for the Fy(a-b-) phenotype is a point mutation in the erythroid specific promoter. Two isotypes have Teen identified.

The Duffy antigen/chemokine receptor gene (DARC) is composed of a single exon. Most Duffy negative blacks carry a silent Fy-b allele with a single T to C substitution at nucleotide -46, impairing the promoter activity in erythroid cells by disrupting a binding site for the GATA1 erythroid transcription factor. The gene is still transcribed in non erythroid cells in the presence of this mutation.

The Duffy negative phenotype occurs at low frequency among whites (~3.5%) and is due to a mutation that results in an unstable protein (Arg89Cys: C-> T at position 265).[4]

The silent allele has evolved at least twice in the black population of Africa and evidence for selection for this allele has been found.[5] The selection pressure involved here appears to be more complex than many text books might suggest.[6] An independent evolution of this phenotype occurred in Papua New Guinea has also been documented.[7]

A comparative study of this gene in seven mammalian species revealed significant differences between species.[8] The species examined included Pan troglodytes (chimpanzee), Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), Rattus norvegicus (brown rat), Mus musculus (mouse), Monodelphis domestica (opposum), Bos taurus (cow) and Canis familiaris (dog).

Three exons are present in humans and chimpanzees while only two exons occur in the other species. This additional exon is located at the 5' end and is entirely non coding. Both intron and exon size varies considerably between the species examined. Between the chimpanzee and the human 24 differences in the nucleotide sequence were noted. Of these 18 occurred in non coding regions. Of the remaining 6, 3 were synonymous and 3 non synonymous mutations. The significance of these mutations if any is not known.

Molecular biology

The Duffy antigen is expressed in greater quantities on reticulocytes than on mature erythrocytes.[9] While the Duffy antigen is expressed on erythrocytes it is also found on some epithelial cells, Purkinje cells of the cerebellum,[10] endothelial cells of thyroid capillaries, the post-capillary venules of some organs[11] and the large pulmonary venules.

The Duffy antigen has been found to act as a multispecific receptor for chemokines of both the C-C and C-X-C families, including:

  • melanoma growth stimulatory activity (MGSA, CXCL1/CXCL2),[12]
  • regulated upon activation normal T expressed and secreted (RANTES; CCL5)[13]
  • monocyte chemotatic protein-1 (MCP-1; CCL2)[14]

and the angiogenic CXC chemokines:

  • interleukin-8 (IL-8, CXCL8)
  • growth related gene alpha (GRO-α, CXCL1)
  • neutrophil activating peptide-2 (NAP-2, CXCL7)
  • ENA-78 (CXCL5)

Consequently the Fy protein is also known as DARC (Duffy Antigen Receptor for Chemokines). The chemokine binding site on the receptor appears to be localised to the amino terminus.[15] The antigen is predicted to have 7 transmembrane domains, an exocellular N-terminal domain and an endocellular C-terminal domain. Alignment with other seven transmembrane G-protein-coupled receptors shows that DARC lacks the highly conserved DRY motif in the second intracellular loop of the protein that is known to be associated with G-protein signaling. Consistent with this finding ligand binding by DARC does not induce G-protein coupled signal transduction nor a Ca2+ flux unlike other chemokine receptors. Based on these alignments the Duffy antigen is considered to be most similar to the interleukin-8B receptors.

In DARC-transfected cells, DARC is internalized following ligand binding and this led to the hypothesis that expression of DARC on the surface of erythrocytes, endothelial, neuronal cells and epithelial cells may act as a sponge and provide a mechanism by which inflammatory chemokines may be removed from circulation as well as their concentration modified in the local environment.[16] This hypothesis has also been questioned after knock out mice were created. These animals appeared healthy and had normal responses to infection. While the function of the Duffy antigen remains presently (2006) unknown, evidence is accumulating that suggests a role in neutrophil migration from the blood into the tissues[17] and in modulating the inflammatory response.[18][19][20][21][22][23][24][25][26][27]

The protein is also known to interact with the protein KAI1 (CD82) and may have a role in the control of cancer.

Population genetics

Differences in the racial distribution of the Duffy antigens were discovered in 1954, when it was found that the overwhelming majority of blacks had the erythrocyte phenotype Fy(a-b-): 68% in African Americans and 88-100% in African blacks (including more than 90% of West African blacks).[28] This phenotype is exceedingly rare in whites. Because the Duffy antigen is uncommon in those of Black African descent, the presence of this antigen has been used to detect genetic admixture. In a sample of unrelated African Americans (n = 235), Afro-Caribbeans (n = 90) and Colombians (n = 93), the frequency of the -46T (Duffy positive) allele was 21.7%, 12.2% and 74.7% respectively.[29]

While a possible role in the protection of humans from malaria had been previously suggested, this was only confirmed clinically in 1976.[30] Since then many surveys have been carried out to elucidate the prevalence of Duffy antigen alleles in different populations including:

  • The mutation Ala100Thr (G -> A in the first codon position - base number 298) within the FY*B allele was thought to be purely a Caucasian genotype, but has since been described in Brazilians. However, the study's authors point out that the Brazilian population has arisen from miscegenation between Portuguese, Black Africans, and Indians, which accounts for the presence of this mutation in a few members of Brazil's non-Caucasian groups. Two of the three Afro-Brazilian test subjects that were found to have the mutation (out of a total of 25 Afro-Brazilians tested) were also related to one another, as one was a mother and the other her daughter.[31]
  • This antigen along with other blood group antigens was used to identify the Basque people as a genetically separate group.[32] Its use in forensic science is under consideration.[33]
  • In a survey of 115 unrelated Tunisians using both serological and DNA based methods gave the following results: FY*X frequency 0.0174; FY*1 = 0.291 (expressed 0.260, silent 0.031); FY*2 = 0.709 (expressed 0.427; silent 0.282). FY*2 silent is the most common allele in West African blacks and the high prevalence in this sample was interpreted as historical admixture.[38]

Clinical significance

Historically the role of this antigen other than its importance as a receptor for plasmodium parasitic protozoa has not been appreciated. Recent work has identified a number of additional roles for this protein.

Asthma

Asthma is more common and tends to be more severe in those of African descent. There appears to be a correlation with both total IgE levels and asthma and mutations in the Duffy antigen.[39]

Benign ethnic neutropenia

A significant proportion (25-50%) of otherwise healthy African Americans are known to have a persistently lower white blood cell count than the normal range defined for individuals of European ancestry - a condition known as benign ethnic neutropenia. This condition is also found in Arab Jordanians, Black Beduin, Falashah Jews, Yemenite Jews and West Indians. This condition is associated with a reduced capacity to mobilize bone marrow neutrophil reserves in response to corticosteroids, despite normal cellularity and maturation of all cell lines in bone marrow aspirates. Strongly suggestive evidence has been found that links condition to a mutation in the Duffy gene.[40] Although the mechanism is as yet unknown, it is known that neutrophils are retained in the bone marrow through interaction of CXCL12 with its receptor CXCR4. A number of rare diseases are known in which disruption or desensitization of CXCR4 results in failure to release mature neutrophils from bone marrow.

Cancer

Interactions between the metastasis suppressor KAI1 on tumor cells and the cytokine receptor DARC on adjacent vascular cells suppresses tumor metastasis.[41]

HIV infection

A connection has been found between HIV susceptibility and the expression of the Duffy antigen. The absence of the DARC receptor appears to increase the susceptibility to infection by HIV. However once established, the absence of the DARC receptor appears to slow down the progression of the disease.[42]

The association between the Duffy antigen and HIV infection appears to be complex. Leukopenia (a low total white cell count) is associated with relatively poor survival in HIV infection and this association is more marked in caucasians than in negroids despite the (on average) lower white cell counts found in black Africans. This difference appears to correlate with a particular genotype (-46C/C) associated with the absence of the Duffy antigen.[43] This genotype has only been found in black Africans and their descendants. The strength of this association increases inversely with the total white cell count. The basis for this association is probably related to the role of the Duffy antigen in cytokinebinding but this has yet to be verified.

Malaria

On erythrocytes the Duffy antigen acts as a receptor for invasion by the human malarial parasites Plasmodium vivax and Plasmodium knowlesi; Duffy negative individuals whose erythrocytes do not express the receptor are believed to be resistant to merozoite invasion,[44] although it has been reported that P. vivax infection in Duffy negative children in Kenya, suggesting a role in resistance to disease, not infection.[45] This antigen may also play a role in erythrocyte invasion in the rodent malarial parasite Plasmodium yoelii. The epitope Fy6 is required for Plasmodium vivax invasion.[9]

Nancy Ma's night monkey (Aotus nancymaae) is used as an animal model of Plasmodium vivax infection. This species' erythrocytes posses the Duffy antigen and this antigen is used as the receptor for P. vivax on the erythrocytes in this species.[46]

Transfusion medicine

A Duffy negative blood recipient may have a transfusion reaction if the donor is Duffy positive.[29] Since most Duffy-negative people are of African descent, blood donations from people of black African origin are important to transfusion banks.

References

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  3. ^ Cutbush, Marie; Mollison, P.L.; Parkin, Dorothy M. (4 February 1950). "A New Human Blood Group" (PDF). Nature 165 (188-189): 188. doi:10.1038/165188b0. http://www.nature.com/nature/journal/v165/n4188/pdf/165188b0.pdf. Retrieved 2007-06-08. 
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  18. ^ Dawson TC, Lentsch AB, Wang Z, et al. (2000). "Exaggerated response to endotoxin in mice lacking the Duffy antigen/receptor for chemokines (DARC)". Blood 96 (5): 1681–4. PMID 10961863. 
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  22. ^ Segerer S, Regele H, MacK M, et al. (2000). "The Duffy antigen receptor for chemokines is up-regulated during acute renal transplant rejection and crescentic glomerulonephritis". Kidney Int. 58 (4): 1546–56. doi:10.1046/j.1523-1755.2000.00316.x. PMID 11012889. 
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  24. ^ Brühl H, Vielhauer V, Weiss M, Mack M, Schlöndorff D, Segerer S (2005). "Expression of DARC, CXCR3 and CCR5 in giant cell arteritis". Rheumatology (Oxford, England) 44 (3): 309–13. doi:10.1093/rheumatology/keh485. PMID 15572394. 
  25. ^ Middleton J, Americh L, Gayon R, et al. (2005). "A comparative study of endothelial cell markers expressed in chronically inflamed human tissues: MECA-79, Duffy antigen receptor for chemokines, von Willebrand factor, CD31, CD34, CD105 and CD146". J. Pathol. 206 (3): 260–8. doi:10.1002/path.1788. PMID 15887283. 
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  30. ^ Miller LH, Mason SJ, Clyde DF, McGinniss MH (August 1976). "The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy". N. Engl. J. Med. 295 (6): 302–4. PMID 778616. 
  31. ^ Estalote AC, Proto-Siqueira R, Silva WA, Zago MA, Palatnik M (2005). "The mutation G298A-->Ala100Thr on the coding sequence of the Duffy antigen/chemokine receptor gene in non-caucasian Brazilians". Genet. Mol. Res. 4 (2): 166–73. PMID 16110438. http://www.funpecrp.com.br/gmr/year2005/vol2-4/gmr0122_abstract.htm. 
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  40. ^ Reich D, Nalls MA, Kao WH, Akylbekova EL, Tandon A, Patterson N, Mullikin J, Hsueh WC, Cheng CY, Coresh J, Boerwinkle E, Li M, Waliszewska A, Neubauer J, Li R, Leak TS, Ekunwe L, Files JC, Hardy CL, Zmuda JM, Taylor HA, Ziv E, Harris TB, Wilson JG. (2009) Reduced neutrophil count in people of African descent is due to a regulatory variant in the Duffy antigen receptor for chemokines gene. PLoS Genet. 5(1):e1000360
  41. ^ Zijlstra A, Quigley JP (September 2006). "The DARC side of metastasis: shining a light on KAI1-mediated metastasis suppression in the vascular tunnel". Cancer Cell 10 (3): 177–8. doi:10.1016/j.ccr.2006.08.012. PMID 16959609. 
  42. ^ He W, Neil S, Kulkarni H, Wright E, Agan BK, Marconi VC, Dolan MJ, Weiss RA, Ahuja SK (July 2008). "Duffy antigen receptor for chemokines mediates trans-infection of HIV-1 from red blood cells to target cells and affects HIV-AIDS susceptibility". Cell Host Microbe 4 (1): 52–62. doi:10.1016/j.chom.2008.06.002. PMID 18621010. 
  43. ^ Kulkarni H, Marconi VC, He W, Landrum ML, Okulicz JF, Delmar J, Kazandjian D, Castiblanco J, Ahuja SS, Wright EJ, Weiss RA, Clark RA, Dolan MJ, Ahuja SK (July 2009). "The Duffy-null state is associated with a survival advantage in leukopenic HIV-infected persons of African ancestry". Blood. doi:10.1182/blood-2009-04-215186. PMID 19620399. 
  44. ^ Miller LH, Mason SJ, Clyde DF, McGinniss MH (1976). "The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy". N. Engl. J. Med. 295 (6): 302–4. PMID 778616. 
  45. ^ Ryan JR, Stoute JA, Amon J, et al. (2006). "Evidence for transmission of Plasmodium vivax among a duffy antigen negative population in Western Kenya". Am. J. Trop. Med. Hyg. 75 (4): 575–81. PMID 17038676. 
  46. ^ McHenry AM, Barnwell JW, Adams JH (October 2009). "Plasmodium vivax DBP binding to Aotus nancymaae erythrocytes is Duffy antigen dependent". J. Parasitol.: 1. doi:10.1645/GE-2281.1. PMID 19799492. 

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