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, 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

REID AND BIRD

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

4-7

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

SLDOD GROUP ANTIGENS AND DISEASE

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-

49

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

50

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-

REID AND BIRD

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,

~!.OOD GROUP ANTIGENS AND DISEASE r,blę

51

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

1

MNSs Ch,RQ ABO MER2 In (C044)

1 1

2 4

6 9 11 11

Locatio"

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

Fy

11

Fy

43

Jk Ok"

18

q34 p15-pter p13 q11-12

19

p13.2~pter

Fy

11

H

q

P,

19 19 19 19 19 22

Xg

X

Kx

X

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

Chromosome

Le Se MNSs MNSs

11 11

ABO

11

Lu/Se

11

Kx Kx

44,45

Kx

11

45,13

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

Ge antigens are weak in protein 4.1-deficient individuals, but the genes encoding protein 4.1 and the proteinmrrrying Ge antigens are on different chromosomes (1 and 2, respectively). The weakened expression of Ge antigens is a reflection of a reChem J 250:407-414, 1988 10. Danieis GL, Shaw M-A, Judson PA, et al: A family demonstrating inheritance of the Leach phenotype: A Gerbichnegative phenotype associated with elliptocytosis. Vox Sang 50:117-121, 1986 11. MiKusick VA: Mendelian Inheritance in Man. Catalogs of autosomaI dominant, autosomal recessive, and X-linked phenotypes (00 7). Baltimore, MD, The Johns Hopkins University Press, 1986 12. Marsh WL, Redman CM: Recent developments in the Kell blood group system. Transf Med Rev 1:4-20, 1987 13. Bertelson CJ, Pogo AO, Chaudburi A, et al: Localization of the McLeod locus (XK) within Xp21 by deletion analysis. Am J Hum Genet 42:703-711, 1988 14. McGinniss MH: The ubiquitous nature ofhuman blood group antigens as evidenced by bacterial, viral and parasitic infections, in Garratty G (ed): BloOO Group Antigens and Disease. Arlington, VA, American Association of BloOO Hanks, 1983, pp 25-44 15. Pasvol G, Jungery M, Weatherall OJ, et al: Glycophorins as possible receptors for Plasmodium jalciparum. Lancet 2:847-851, 1982 16. Cartron JP, Prou O, Luitier M, et al: Susceptibility to

invasion by Plasmodium jalciparum of some human erytbrocytes carrying rare blood group antigens. Hr J Haematol 55:639-647, 1983 17. Miller GH, Hadley TJ, McGinnis MH, et al: Invasion of erythrocytes by Plasmodium jalciparum malaria parasites: Bvidence for receptor heterogeneity and two receptors. Blood 67:1519-1521, 1986 18. Pasvol G, Anstee OJ, Tanner MJA: Glycophorin C and the invasion of red celIs by Plasmodium jalciparum. Lancet 2:907, 1984 19. Crookston MC: An01nalous AHO, H and Ii phenotypes in disease in Garratty G (ed): Blood Group Antigens and Disease. Arlington, VA, American Association of Blood Banks, 1983, pp 67-84 20. Salmon CH, Cartron JP, Lopex M, et al: Level of the A, B and H blood group glycosyltransferases in red celI membranes from patients with malignant hemopathies. Blood Transf Immunolog Hemato127:625-637, 1984 21. Lopez M, Bonnet-Gajdos M, Reviron M, et al: An acute leukaemia augurOO before clinical signs by blood group antigen abnonnalities and low levels of A and H blood group transferase activities on erythrocytes. Br J Haematol 63:535-539, 1986 22. Bird GWG: Blood groups: Determinants of recognition and of susceptibility to disease, in Garratty G (ed); Blood GIoup Antigens and Disease. Arlington, VA, American Association ofBlood Banks, 1983, pp 1-24 23. Feizi T, Childs RA: Carbohydrate structures of glycoproteins and glycolipids as differentiation antigeris, tumourassociated antigens and components of receptor systems. Trends Biochem Sci 10:24-29, 1985 24. Fukuda M: CelI surface glycoconjugates as oncodifferentiation markers in hematopoietic celIs.Biochem Biophys Acta 780:119-150, 1985 25. Thiel B, GUpte SC, KisslingK: Changes in 'A' antigenic sites in haematological disorders. An immunoautoradiographic study. Acta Haematol 73:65-70, 1985 26. Vowden P,Lowe AD, Lennox ES, et al: The expression of ABH and Y bloOO group antigens in benign and malignant breast tissue; The preservation of the H and Y antigens in malignant epithelium. Br J Cancer 53:313-319, 1986 27. Bishop 1M: The molecular genetics of cancer. Science 235:305-311, 1987 28. Mannessier L, Rouger P, Johnson CL, et al: Acquired loss ofred celi Wj antigen in a patient with Hodgkin's Disease. Vox Sang 50:240-244, 1986 29. Dahr W, Uhlenbruck G, Gunson RH, et al: Molecular basis for Tn-polyagglutinability. Vox Sang 29:36-50, 1975 30. Cartron JP, Cartron J, Andreu G, et al: Selective deficiency of 3-I3-D-galactosyltransferase (T-transferase).in Tnpolyagglutinable erythrocytes. Lancet 1:856-857, 1987 31. Beck ML: Blood group antigens acquired de novo, in

BLOOO GROUP ANTIGENS AND OłSEASE

Garratty G (ed): Antigens and Disease. Arlington, VA, Ameriean Association of Blood Banks, 1983, pp 45-66 32. Doinel C, Andreu G, Cartron IP, et al: Tk polyagglutination produeed in vitro by endo-13-galaetosidase. Vox Sang 38:94-98, 1980 33. Gerbal A, Ropars C, Gerbal R, et al: Aequired B antigen disappearanee by in vitro aeetylation associated with Al activity restoration. Vox Sang 31:64-66, 1976 34. Hiliman RS, Giblett ER: Red eell rnernbrane alteration associated with "rn;rrrow streSS." l Clin Invest 44:1730-1736, 1965 35. Mawby WJ, Tanner MJA, Anstee DJ, et al: Ineornplete glycosylation of erythroeyte membrane proteins in eongenital dyserythropoietie anaemia Type li (CAD II). Br J Haernatol 55:357-368, 1983 36. Reid ME, Takakuwa y, Tchemia G, et al: Protein 4.1 binds to sialoglycoprotein 13 and regulates its rnembrane content in human erythrocytes. Blood (suppl 1), 70:42a, 1987 (abstr) 37. Sondag D, Alloisio N, Blanehard D, et al: Gerbich reactivity in 4.10 hereditary elliptocytosis and protein 4.1 level in blood group Gerbieh deficieney. Br J Haematol 65:43-50, 1987 38. Booth PB, Serjeantson S, Woodfield DG, et al: Seleetive depression of blood group antigens associated with hereditary ovaloeytosis among Melanesians. Vox Sang 32:99-110, 1977 39. Petz LD, Garratty G: Aequired irnmune hemolytie anemias. New York, NY, Churchill Livingstone, 1980 40. Ninorniya H, Abe T, Shichishima T, et al: Decayaccelerating factor (DAF) on the blood eeU mernbrane in patients with paroxysrnal nocturnal baemoglobinuria (PNH): Measurernent by enzyme-linked irnmunosorbent assay (ELISA). Br J HaematoI69:81-87, 1988 41. Parsons SF, Spring FA, Merry AH, et al: Evidence that Crorner-related blood group antigens are carried on decay accelerating (DAF) suggests that the Inab phenotype is anovel form of DAF deficiency. XX Congress of the International Society of Blood Transfusion in Association with British Blood Transfusion Society, London, England, 1988, p 116 42. Telen MJ, HaU SE, Green A, et al: Identifieation of human blood group antigens on decay accelerating factor and dernonstration of a null phenotype. Clin Res 36:421A, 1988 (letter) 43. Griffiths KR, Zwi MB, McLeod JG, et al: Chrornosome l linkage studies in Charcot-Marie-Tooth neuropathy type I. Arn J Hum Genet 42:756-771, 1988 44. Frey D, Machler M, Seger R, et al: Gene deletion in a patient with chronic granulornatous disease and McLeod SYndrome: Fine mapping of tbe Xk gene locus. Blood 71:252-255, 1988 45. Orkin SH: X-linked ehronie granulornatous disease: From chromosomai position to the in vivo gene product. TIG 3:71-73, 1987 46. Sobel ID, Myers PG, Kaye D, et al: Adherence of Can-

55 dida albicans to burnan vaginal and buceal epithelial cells. J Infect Dis 143:76-82, 1981 47. Blaekwell CC, Jonsdottir K, Hanson M, et al: Nonsecretion of ABO antigens predisposing to infeetion by Neisseria meningitidis and Streptococcus pneumoniae. Lancet 2:284-285, 1986 48. Blaekwell CC, Jonsdottir K, Hanson M, et al: Nonsecretion of ABO blood group antigens predisposing to infection by Haemophilus influenzae. Lancet 2:687, 1986 49. Nowicki B, Moulds J, Hall R, et al: A hemagglutinin of Uropathogenic Eschericbia coli recognises the Dr blood group antigen. lnfeet Immun 56:1057-1060, 1988 50. Cartwright RA, Adib R, Appleyard I, et al: ABO, MNSs and Rhesus blood groups in bladder eancer. Br J Uroi 55:377383, 1983 51. Mantbrope R, Staub NL, Peterson JM, et al: Lewis blood type frequency in patients withprimary Sjogren's syndrome. A prospective study including analysis for AIAzBO, secretor, MNSs, P, Duffy, Kell, Lutheran and Rhesus blood groups. Scand J Rheumatol 14:159-162, 1985 52. Gill JC, Endres-Brooks J, Bauer Pl, et al: The effect of ABO blood group on the diagnosis of von Willebrand disease. Blood 69: 1691-1695, 1987 53. Shinebaurn R, Blackwell CC, Forester PJG, et al: Nonseeretion of ABO blood group antigens as a host Suseeptibility faetor in the spondyloartbropathies. Br Med l 294:208-210, 1987 54. Mollison PL, Engelfriet CP, Contreras M: Blood Transfusion in Clinical Medicine (ed 8). Boston, MA, Blackwell Seientific Publications, 1987 55. Mollison PL: Some aspects of Rh hemolytic disease and its prevention, in Garratty G (ed): Hemolytic Disease of the Newbom. Arlington, VA, Arnerican Association of Blood Banks, 1984, pp 1-32 56. Vengelen-Tyler V: The serologieal investigation of hemolytic disease of the newbom caused by antibodies other than anti-D, in Garratty G (ed): Hernolytic Disease of the newbom. Arlington, VA, Arnerican Association of Blood Banks, 1984, pp 145-172 57. Cantin G, Lyonnais J: Anti-PP1pk and early abortion. Transfusion 23:250-351, 1983 58. Toy PTCY, Reid M, Bums M: Positive direct antiglobulin test associated with hyperglobulinemia in acquired immunodeficiency syndrome (AIDS). Arn J Hematol 19:145-150, 1985 59. Pruzanski W, Roelcke D, Donnelly E, et al: Persistent cold agg1utinins in AIDS and related disorders. Acta Haematol 75:171-173, 1986 60. G;rrratty G: The signiflcance of IgG on the red celi sur· face. Transf Med Rev 1:47-57, 1987 61. White WL, Miller GE, Kaehny WD: Formaldehyde in tbe pathogenesis of hemodialysis-related anti-N antibodies. Transfusion 17:443-447, 1977

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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