Associations Between Human Red Celi Blood Group Antigens and Disease Marion E. Reid and George W.G. E:lird

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LOOD GROUP anitgens are polymorphic, in~ . herired, structural characters that are located on proteins, glycoproteins, Ol' glycolipids on the outer sil1face of the red celi membrane. These antigens are important in homologous blood transfu· sion, matemo-fetal blood group imcotnpatibility, and organ transplantation. Blood group antigen prof11es have been used to predict inheritance of diseases that are encoded by genes closely linked to a blood group gene on the same chromosotne. Blood groops have been itnplicated in susceptibility Ol' resistance to disease. Certain diseases and II1icrobial infections alter blood group antigens or stiroulate. the prodlicuon of blood group antibod· ies. This review highlights sotne of these disease associations and describes the undetlying IIiechafiisms that have been elucidated by recent biochemical and genetic studies. Human· red celi blood group antigens and anti· bodies have been associated both with red celi dis· ·otders and other clinical conditions. i-3 The purpose of the present review is to sun1IIiarize the tnechanisms of those disease associations that have been elttcidared by recent biochen1ical and genetic studies. The discussion of associations between red cell blood groups and disease will be treated in two sections. The Iirst will describe associations involving blood gtoup antigens and will include genetic link:age and disease sosceptibility; the secpnd will discuss associations involving blood gtoup antibodies. . lo the interest of space, no attempt lias been l1lade to cite original reports when recent reviews have been available. the interested reader is re· . ferred to the cited reviews and terent publications for a comprehensive list of references. BLOOD GROUP ANTIGENS

1)iseases TOOt Result Ftom on Absente or Alteration ol ProteitlS TOOt Carty Blood .Group Antigens !he absence (Ol' altered form) of a protein on Which certain blood antigens are located can resułt in hematological disorders. An absence of the t:ranstnetnbrane proteins that carty Rh, Gerbich '{Ge) Ol' Kx blood group antigens, ali of which 'ttaTl!1fusioTl Medicine ReviewSi VoIIV, No 1 (January), 1990: Pll 47,55

interaet with the membrane skeleton, are associated, respectively, with stomatocytosis, elliptocytosis, and acanthocytosis (Table l). Hereditary stomatocytosis and hetnolytic ane· mia are found in individuals who inherit the rare Rhnu1l Ol' Rhmod blood types. The anemia fluctuates in severity. Rhnuu red cells lack Rh and LW blood group antigens, whereas RhrtJ.ód red cells express these antigens so weakly that they can only be detected by absorption and elution. Rhńul1 red cells apparently lack the polypeptides associated with Rh antigefis and with LW antigens. 4-7 The biochemical nature of the Rhmod phenotype has not been determined. Red celis from individuals with the type of he· reditary elliptocytosis (HE) that is associated with the Leach phenotype lack Ge blood group antigens because these red cells lack glycophorin C (siało· glycoprotein (SGP ~) and glycophorirt D (SGP 'Y) molecules on which Ge antigens are located.s Glycophorin C, in its interaction with the mernbrane skeleton, is involved in maintaining normal red celI deformability and IIiembrane mechanical stability.8 DNA fiom an individual with the Leach phenotype has an altered form ot the gene that ericodes glycophorin C. A deletion at the 3; end of the gene precludes synthesis of the cytoplasIIiic and transmembrane domains of glycophorin C. 9 Leach type red cells show a weakened expression of Kell blood group antigens but the reason for this is unknown. io The McLeod pheilOtype is characterized by weak expression of Kell blood group antigens, an

From the Departrnent ofLaboratory Medicinej San Francisco General Hospital and Medical Center, .San Francisco, CA, the Blood Group Reference Laboratory, 07iford, England, and the Regional Blo{)d Transfusion service,· Birmingham, Engłand.

This work Was supported by Public Health Service Transfusion Medicine Academic Award (KO·HL-O 1210) from the National Institutes oj Health. Address reprint requests to Marion E. Reid, PhD, FIMLS, Blood Group Reference Laboratóry, Southwestern Regitlnal Traiisfusion Centre, Sóuthmead Road, Bristol B5IO SND England. © 1990 W.B. Saunders Company.

Ó881-1963/90/040I-0007$0.3.0010 47


48 Table 1. Red Celi Blood Group Antigens Associated With Disease

References Diseases caused by absent or altered proteins that carry blood group antigens Hereditary stomatoeytosis Absent or weakened Rh Hereditary elliptoeytosis Absent Ge; weakened Kell Hereditary aeanthoeytosis Absent Kx; weakened Kell Blood group antigens associated with disease resistance Fy(a-b-) Malaria: P vivax p knowlesi Tn,Cad,En(a - ),U -, GePyelonephritis p Blood group antigen ehanges associated with disease leukemia Weakened A,B,I; enhanced i Hodgkin's disease Weakened A,B,lW, AnWj Aplastie anemia Weakened A, B Preleukemia Exposed Tn, weakened M,N Bacterial infection Exposed T, weakened M,N Bacterial infeetion Exposed Tk, weakened ABH,I,P, Aeąuired B, weakened A, Colon and bowel lesions Sacterial infeetion Acąuired B Thalassemia Enhaneed i Siekłe celi disease Enhanced i Dyserythropoiesis (HEMPAS) Enhanced i; weakened H Diamond Blackfan anemia Enhanced i Myeloblastie erythropoiesis Enhanced i Sideroblastie erythropoiesis Enhanced i Refractory anemia Enhanced i Weakened Ge Common HE lHE(4.1°)) Stomatocytie HE Weakened l,lW,Rh,Kpb,S,s,Jka AIHA Weakened target antigen (K,lW) PNH III cells Absent Cromer-related antigens

absence of Kx antigens, acanthocytosis, and heanemia in małes. The protein carrying Kx antigens is encoded by a gene located on the X chromosome and apparently affects the amount of the Kell protein that is in the red cell membrane. The McLeod phenotype occurs when this gene is altered. The autosomał gene encoding Kell protein is apparently normal because red cells from sons of men with the McLeod phenotype (who inherit an X chromosome with a normal Kx gene from their mothers) express Kell blood group antigens normally.5,11-13 mołytic

Blood Group Phenotypes Associated With Resistance to Disease Individuals with certain blood group phenotypes are afforded protection from specific diseases. For example, Fy(a - b -) individuals are resistant to certain malarial parasites, and individuals with the p blood type are resistant to microbes that cause pyelonephritis (Table 1). Individuals whose red cells lack Fya and Fyb


5,10 12 14 15-18 11

1,19,20,22 1,19,22,28 1,19,22 14,22,31 14,22,31 1,14,22,31 1,19,22,31 1,22,30,31 1,22 1,22 1,19,22 1,19,22 1,19,22 1,19,22 1,19,22

37 38 12,39 40-42

antigens are resistant to invasion by the malarial parasite Plasmodium vivax in vivo and to the simian malarial parasite Plasmodium knowlesi in vitro. P knowlesi parasites attach to red cells that lack Fya and Fyb antigens, but invasion does not occur becausę moving junctions between the parasite and the red cell membrane are not formed. 14 Red cells with altered O-linked oligosaccha~ rides, namely those possessing Cad 1 and Tnblood group antigens, resist invasion by some strains of Plasmodium jalciparumY-17 Red cells fram En(a - ) (glycophorin A-deficient), S-s-U- (glycophorin B-deficient), or the Leach type of Ge- (glycophorin C-deficient) individuals are partly resis:" tant to invasion by P jalciparum. 15 ,18 Collectively, these data suggest that an interaction between the parasite and O-linked oligosaccharides is a prerequisite for invasion of red cells. Studies using red cells with different blood groups have shown that malarial parasites require specific receptors in order to invade the red cell and that there is receptor heterogeneity, eg, some strains of P jalciparum do


invade En(a -) and sialidase-treated red cells, while other strains do not. 17 Individuals with the p blood group phenotype do not suffer from pyelonephritis caused by certain strains of Escherichia coli. The receptor for most pyelonephritogenie strains of E coli is the disaccharide, a-Gal(I-4)I3-Gal. This disaccharide is present on uroepithelial cells and red blood cells from a majority of people because it is part of the structures that carry pk, P and P l blood group antigens. Only individuals with the fare p blood group are known to lack this disaccharide. 11 Blood Group Antigen Changes That Are Induced by Certain Diseases

Changes in the expression ofblood group antigens occur in hoth inherited and acquired diseases. A change associated with an inherited disease is a characteristic and consistent finding of the disease; whereas a change associated with an acquired disease occurs during the development of the disease and returns to normal upon remission or recovery. Changes in expression of red cell blood group antigens can be induced by (1) aberrant glycosyltransferases that cause either a failure to add a carbohydrate or in the addition of carbohydrate, which masks the original specificity; (2) glycosidase cleavage of a carbohydrate residue or chain; (3) chromosome rearrangements; (4) deacetylase modification of carbohydrate; (5) adsotption of bacterial antigens; (6) incomplete biosynthesis; (7) reduction in the numher of copies of protein carrying a blood group antigen; and (8) unknown causes. Blood group antigens related to various diseases are listed in Table 1. Blood group antigen expression can be altered if a rearrangement of DNA occurs in the region of a gene encoding a blood group antigen. For example, the presence of Rh-negative red cells in the circulation of an Rh-positive male with myelofibrosis was due to deletion of part of the short arm of chromosome 1. The gene encoding the D blood group antigen is located on chromosome l at the p36-p34 region. II The weakened expression of A and B hlood group antigens in certain types of leukemia may be a consequence of chromosomaI translocation. Translocation of the long arm of chromosome 9 to chromosome 22 (the Philadelphia chromosome) occurs in over 90% of patients with chronie my-


eloid leukemia. This translocation can result in a reduction of A- or B-gene specified transferases because the genes encoding these transferases are located on the long arm of chromosame 9. A reduction in transferases will result in a weakened expression of A ar B antigens and a concurrent increased expression of H antigen on the patient's red cells. Weakened expression of A and B antigens is not known to be associated with lymphoid leukemias. 19-21 Weakened expression of A and B antigens on the red cells in certain types of leukemia may be caused by altered gene expression. In acute leukemias and carcinomas, malignant cells are less well differentiated than normal. Changes in the expression of blood group antigens in these eells may represent a dedifferentiation process, with the repression of genes that are normally aetivated during maturation, ar the reaetivation of genes that are norma1ly repressed during maturation. The weakened expression of A, B , LWa and AnWj antigens on red cells from patients with Hodgkin's disease, a malignant neoplasm, may be the result of this mechanism. Nontransfused patients with aplastic anemia have a reduced number of A ar B antigen sites per red eell eompared with the normai number.19.22-28 Another transferase deficiency, that of a galactosyltransferase (possihly the result of a genetic dysfunction in a mutant hemopoietic stem cell), results in exposure of cryptie Tn antigens. 29 ,30 Tn antigens are exposed when galactose and neuraminic acid are not attached to N-acetyl-galactosamine to eomplete the O-linked tetrasaccharides associated with normal glycophorin molecules. Only a proportion of red cells are affected, and this leads to a characteristie dual population of red cells. Tn has been reported in association with preleukemia and acute myelomonocytic leukemia but has also been found in apparently healthy individuals. 31 Exposure of blood group cryptantigens can OCeur during infection if the microbes produce exoglycosidases or endoglycosidases. T antigen is exposed when neuraminidase, secreted by certain microbes (Vibrio cholerae, Corynebacterium, Streptococcus pneumoniae and Clostridium perfringens), cleaves neuraminie acid from O-linked oligosaccharides. A concurrent weakening of M, N and other antigens may occur if neurarninie acid


is a structural part of the antigenic determinant. Another cryptantigen, Tk, is exposed by the action of endo-f3-galactosidase, produced by Bacteroides fragilis, whicb cleaves polylactosaminyl groups (f3Gal(1.4)f3GlcNAc(l.3)) resulting in exposure of N-acetyl-D-glucosaroine. Polylactosaminyl groups are an integral part of N-linked oligosaccharide structures and glycolipids and are, therefore, pre· cursor chains for ABH and Ii antigens. Cleavage of these polylactosaroinyl groups causes the weakened expression of these blood group antigens on red cells with exposed Tk antigens. 31 ,32 Bacterial deacetylase can result in the appear· ance of acquired B blood group antigens. This enzyme converts N-acetyl-galactosamine (the blood group A i1U1Uunodominant sugar) into galactosamine, which is sufficiently similar to galactose (the blood group B immunodominant sugar) to bind anti-B. 33 Tbus, the strengtb of the blood group A antigen deereases as that of the acquired B antigen increases. This type of acquired B antigen is associated with gastrointestinal malignancies, lesions of the colon or bawel wall, and severe infections, but can oecur in individuals witb no apparent malignancies or infections.31 Bacterial infections can also eause the appearance of acquired blood group antigens by tbe "passenger antigen" mecbanism. Blood group B antigen has been acquired by group A and group O type red eells by adsorption ofB-like materiał from E coli 0 86 and Proteus vulgaris. In vitro tests suggest that other bacteria may induce the appearance of blood group antigens. Ik (a + b ~ ) red cells incubated with Proteus mirabilis organh,ms in vitro became agglutinable by anti-Jkb , implying that tbey acquired a Jkb-like antigen. 14 ,3 1 . Inherited hematopoietic disorders such as homozygous (X.- or f3-thalassemia, sickle cell disease, hereditary erytbrobłastie mułtinuclearity with a positive acidified-serum test (HEMPAS) , and Diamond Blackfan congęnital hypoplastic anemia are assoeiated with an increased expression of i antigen. An inerease in this antigen also OCCurS in sOme acquired diseases, eg, myeloblastic or sideroblastic erythropoiesis and refractory anemia. !his is probably a consequence of incomplete biosynthesis. Tbis pbenomenon has been induced experimentally in normaI adults by repeated pblebotomy.34 The red cell membrane cbanges are a refleetion of an iIlcrease in the linear carbohy-


drate structures associated with glycolipids and complex type N-linked oligosaecharides,19,22,24,35 Red cells from patients witb common hereditary elliptocytosis due to protein 4.1 deficiency (HE [4.1°]) bave a weakened expression of Ge blood group antigens. This is due to the marked reduction of glycophorin C molecules in these red cell membranes. 36,37 The oval, rigid red cells from individuals witb stomatocytic HĘ, another type of hereditary elIiptocytosis found predominantly in Southeast Asians, have a weakened expression of many antigens, I, LWa, D, C, e, S, s, U, Kpb, Jka , Xga , Sd and En a • 38 Tbe reason for this is not koown. In rare cases of autoimmune hemolytic anemia (AIHA), the target antigen corresponding to the autoantibody specificity is profoundly weakened. The reasOn for this is unknown. In the case of Kell blood group antigens the mechanism apparentIy does not involve the biosyntbetic patbwaY be. cause, in two patients, transfused red cells also developed a weakened expression of Kell blood group antigens. 12 ,39 A population of red celIs from individllals with paroxysmal nocturnal hemoglobinuria (PNH) are sensitive to complement-mediated lysis. These red celIs (PNH III cells) are deficient in those glyco. proteins that attach to tbe red cell via a glycosylphosphatidylinositol taił, eg, decay-accelerating factor (PAF), lymphocyte function-associated antigen 3 (LFA·3) and acetylcholinesterase. DAF has recendy bęen shown to carry tbe Cromer-related blood group antigens. 40-42 Linkage olOenes Encoding Blood Group Antigen and Certain J)iseases

If a gene eneoding a diseąse is located on the same cbromosome in close enough proximity to a gene encoding a blood group antigen, the disease will be manifested every time the blood group antigen is inherited. II ,43 ExampIes are sbown in TabIe 2. Similarly, if an alteration of a cbromosome affects neighbouring genes tbat encode a blood group antigen and a disease, they will be associ. ated. For exampIe, deletions in the X chromosome bave been described tbat affect the genes eneoding KK antigens and eitber ebronic granuIomatous disease or mllseular dystrophy.11·13,44,45 Apparent associations may be due to functional interactions rather than gene linkage. For example,



2. Lipkage Betweep Gepas EpcodiP9 Blood Group

Tabl. 3. Locatlon ot Blood Group Genas on CłJromosomes

Aptfgeps ,pd Disease Blood Group Loci Refere"ces

Chromosome 1 Common HE (HE [4.1°]) 6-phosphoguconate dehydroQenase-deficiency a_fucosidase-cteficienev Invasive HIB disease Noninsulin-dependent djabetes Antithrombin III-deficiency Zonular pulverulent cataract Motor and sensory neuropathy Charcot-Marie-Tooth neuropathy

Rh Rh Rh Rh: Sc Rh Fy Fy

11 11 11 11 11 11 11

Chromosome 4 Selerotylosis Hypo- or dysfrbrinogenemia Chromosome 9 Nail patella syndrome Chromosome 19 Myotonie c;tystrophy X chromosome eGD Muscular dystrophy (Duchenne type) _Retinitis pigmentosa

Fy Rh

1 1

Se Rd Cromer-related (DAF) Ge


MNSs Ch,RQ ABO MER2 In (C044)

1 1

2 4

6 9 11 11


q12-q21 p34-p36 p32-p34 p22.1-p34 q32 q14-p21 q28-q31 p21.05-p23





Jk Ok"


q34 p15-pter p13 q11-12








19 19 19 19 19 22





(type 1) a-speetrin-deficiency (HE, HPP)



11 11





Kx Kx





Abbreviations: HE, hereditary elliptocytosis; HIB, Haemophilus influenzae type b dlsease; HPP, hereditary pyropoikilot,:ytosis; CGD, chronic granulomatous disease.

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Associations between human red cell blood group antigens and disease.

Associations Between Human Red Celi Blood Group Antigens and Disease Marion E. Reid and George W.G. E:lird · B LOOD GROUP anitgens are polymorphic,...
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