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Research Article| Volume 12, ISSUE 2, P277-304, June 1992

Chronic Granulomatous Disease: Diagnosis and Classification at the Molecular Level

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      Chronic granulomatous disease (CGD) is caused by the failure of phagocytes to produce microbicidal derivatives of molecular oxygen, such as hydrogen peroxide. It is one of the best characterized of the phagocyte disorders and represents an important consideration in the differential diagnosis of recurrent infections. The clinical, biochemical, and molecular genetic aspects of CGD are reviewed in this context in this article.
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      References

        • Abo A.
        • Pick E.
        • Hall A.
        • et al.
        Activation of the NADPH oxidase involves the small GTP-binding protein p21racl.
        Nature. 1991; 353: 668
        • Agwu D.E.
        • McPhail L.C.
        • Sozzani S.
        • et al.
        Phosphatidic acid as a second messenger in human polymorphonuclear leukocytes. Effects on activation of NADPH oxidase.
        J Clin Invest. 1991; 88: 531
        • Aliabadi H.
        • Gonzalez R.
        • Quie P.G.
        Urinary tract disorders in patients with chronic granulomatous disease.
        N Engl J Med. 1989; 321: 706
        • Ament M.E.
        • Ochs H.D.
        Gastrointestinal manifestations of chronic granulomatous disease.
        N Engl J Med. 1973; 288: 382
        • Anderson D.C.
        • Schmalsteig F.C.
        • Finegold M.J.
        • et al.
        The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: Their quantitative definition and relation to leukocyte dysfunction and clinical features.
        J Infect Dis. 1985; 152: 668
        • Amaout M.A.
        Structure and function of the leukocyte adhesion molecules CD11/CD18.
        Blood. 1990; 75: 1037
        • Babior B.M.
        The respiratory burst oxidase.
        Hematol/Oncol Clin North Am. 1988; 2: 201-212
        • Babior B.M.
        • Kuver R.
        • Cumutte J.T.
        Kinetics of activation of the respiratory burst oxidase in a fully soluble system from human neutrophils.
        J Biol Chem. 1988; 263: 1713
        • Badwey J.A.
        • Cumutte J.T.
        • Robinson J.M.
        • et al.
        Effects of free fatty acids on release of superoxide and on change of shape by human neutrophils: Reversibility by albumin.
        J Biol Chem. 1984; 259: 7870
        • Baehner R.L.
        • Johnston R.B.
        • Nathan D.G.
        Comparative study of the metabolic and bactericidal characteristics of severely glucose-6-phosphate dehydrogenase deficient polymorphonuclear leukocytes and leukocytes from children with chronic granulomatous disease.
        J Reticuloendothel Soc. 1972; 12: 150
        • Baehner R.L.
        • Kunkel L.M.
        • Monaco A.P.
        • et al.
        DNA linkage analysis of X chromosome-linked chronic granulomatous disease.
        Proc Natl Acad Sri USA. 1986; 83: 3398
        • Baehner R.L.
        • Nathan D.G.
        Quantitative nitroblue tetrazolium test in chronic granulomatous disease.
        N Engl J Med. 1968; 278: 971
        • Battat L.
        • Francke U.
        Nsi I RFLP at the X-linked chronic granulomatous disease locus (CYBB.
        Nucleic Acids Res. 1989; 17: 3619
        • Bej A.K.
        • Mahbubani M.H.
        • Atlas R.M.
        Amplification of nucleic acids by polymerase chain reaction (PCR) and other methods and their applications.
        CRC Crit Rev Biochem Molec Biol. 1991; 26: 301
        • Bemiller L.S.
        • Rost J.R.
        • Ku-Balai T.L.
        • et al.
        The production of intracellular oxidants by stimulated neutrophils correlates with the clinical severity of chronic granulomatous disease (CGD.
        Blood. 1991; 78: 377a
        • Bertelson C.J.
        • Pogo A.O.
        • Chaudhuri A.
        • et al.
        Localization of the McLeod Locus (XK) within XP21 by deletion analysis.
        Am J Hum Genet. 1988; 42: 703
        • Bolscher B.G.J.M.
        • de Boer M.
        • de Klein A.
        • et al.
        Point mutations in the β-subunit of cytochrome b558 leading to X-linked chronic granulomatous disease.
        Blood. 1991; 77: 2482
        • Bolscher B.G.J.M.
        • de Boer M.
        • de Klein A.
        • et al.
        Mutations in the beta subunit of cytochrome b556 leading to X-linked chronic granulomatous disease (abstract.
        Eur J Clin Invest. 1991; 21: 40
        • Borregaard N.
        • Bang J.
        • Berthelesen J.G.
        • et al.
        Prenatal diagnosis of chronic granulomatous disease.
        Lancet. 1982; 1: 114
        • Borregaard N.
        • Heiple J.M.
        • Simons E.R.
        • et al.
        Subcellular localization of the ^-cytochrome component of the human neutrophil microbicidal oxidase: Translocation during activation.
        J Cell Biol. 1983; 97: 52
        • Borregaard N.
        • Tauber A.I.
        Subcellular localization of the human neutrophil NADPH oxidase: ^-cytochrome and associated flavoprotein.
        J Biol Chem. 1984; 259: 47
        • Boulay F.
        • Mery L.
        • Tardif M.
        • et al.
        Expression cloning of a receptor for C5a anaphylatoxin on differentiated HL-60 cells.
        Biochemistry. 1991; 30: 2993
        • Boulay F.
        • Tardif M.
        • Brouchon L.
        • et al.
        The human N-formylpeptide receptor. Characterization of two cDNA isolates and evidence for a new subfamily of G-protein-coupled receptors.
        Biochemistry. 1990; 29: 11123
        • Boxer L.A.
        • Oliver J.M.
        • Spielberg S.P.
        • et al.
        Protection of granulocytes by vitamin E in glutathione synthetase deficiency.
        N Engl J Med. 1979; 301: 901
        • Bromberg Y.
        • Pick E.
        Activation of NADPH-dependent superoxide production in a cell-free system by sodium dodecyl sulfate.
        J Biol Chem. 1985; 260: 13539
        • Casimir C.M.
        • Bu-Ghanim H.N.
        • Rodaway A.R.F.
        • et al.
        Autosomal recessive chronic granulomatous disease caused by deletion at a dinucleotide repeat.
        Proc Natl Acad Sei USA. 1991; 88: 2753
        • Chanock S.J.
        • Barrett D.M.
        • Cumutte J.T.
        • et al.
        Gene structure of the cytosolic component, phox-47 and mutations in autosomal recessive chronic granulomatous disease.
        Blood. 1991; 78: 165a
        • Chin T.W.
        • Stiehm E.R.
        • Falloon J.
        • et al.
        Corticosteroids in treatment of obstructive lesions of chronic granulomatous disease.
        J Pediatr. 1987; 111: 349
        • Clark R.A.
        The human neutrophil respiratory burst oxidase.
        J Infect Dis. 1990; 161: 1140
        • Clark R.A.
        • Malech H.L.
        • Gallin J.T.
        • et al.
        Genetic variants of chronic granulomatous disease: Prevalence of deficiencies of two cytosolic components of the NADPH oxidase system.
        N Engl J Med. 1989; 321: 647
        • Clark R.A.
        • Volpp B.D.
        • Leidal K.G.
        • et al.
        Two cytosolic components of the human neutrophil respiratory burst oxidase translocate to the plasma membrane during cell activation.
        J Clin Invest. 1990; 85: 714
        • Cohen M.S.
        • Leong P.A.
        • Simpson D.M.
        Phagocytic cells in periodontal defense: Periodontal status of patients with chronic granulomatous disease of childhood.
        J Periodontal. 1985; 56: 611
        • Cooper M.R.
        • Dechatelet L.R.
        • McCall C.E.
        • et al.
        Complete deficiency of leukocyte glucose-6-phosphate dehydrogenase with defective bactericidal activity.
        J Clin Invest. 1972; 51: 769
        • Cross A.R.
        • Jones O.T.G.
        Enzymic mechanisms of superoxide production.
        Biochim Biophys Acta. 1991; 1057: 281
        • Cumutte J.T.
        Activation of human neutrophil nicotinamide adenine dinucleotide phosphate, reduced (triphosphopyridine nucleotide, reduced) oxidase by arachidonic acid in a cell-free system.
        J Clin Invest. 1985; 75: 1740
        • Cumutte J.T.
        Recent advances in chronic granulomatous disease.
        Curr Op Pediatr. 1990; 2: 907
        • Cumutte J.T.
        Molecular basis of the autosomal recessive forms of chronic granulomatous disease.
        Immunodef Rev. 1991; (in press)
        • Cumutte J.T.
        Disorders of phagocyte function.
        in: Hoffman R. Benz Jr., E.J. Shattil S.J. Hematology: Basic Principles and Practice. Churchill Livingstone, New York1991: 571-589
        • Cumutte J.T.
        • Babior B.M.
        Chronic granulomatous disease.
        in: Harris H. Hirschhorn K. Advances in Human Genetics. Plenum, New York1987: 229-297
        • Cumutte J.T.
        • Berkow R.L.
        • Roberts R.L.
        • et al.
        Chronic granulomatous disease due to a defect in the cytosolic factor required for nicotinamide adenine dinucleotide phosphate oxidase activation.
        J Clin Invest. 1988; 81: 606
        • Cumutte J.T.
        • Kipnes R.S.
        • Babior B.M.
        Defect in pyridine nucleotide dependent superoxide production by a particulate fraction from the granulocytes of patients with chronic granulomatous disease.
        N Engl J Med. 1975; 293: 628
        • Cumutte J.T.
        • Kuver R.
        • Scott P.J.
        Activation of neutrophil NADPH oxidase in a cell-free system. Partial purification of components and characterization of the activation process.
        J Biol Chem. 1987; 262: 5563
        • de Saint-Basile G.
        • Bohler M.C.
        • Fischer A.
        • et al.
        Xp21 DNA microdeletion in a patient with chronic granulomatous disease, retinitis pigmentosa, and McLeod phenotype.
        Hum Genet. 1990; 80: 85
        • Dinauer M.C.
        • Cumutte J.T.
        • Rosen H.
        • et al.
        A missense mutation in the neutrophil cytochrome b heavy chain in cytochrome-positive X-linked chronic granulomatous disease.
        J Clin Invest. 1989; 84: 2012
        • Dinauer M.C.
        • Orkin S.H.
        • Brown R.
        • et al.
        The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex.
        Nature. 1987; 327: 717
        • Dinauer M.C.
        • Pierce E.A.
        • Bruns G.A.P.
        • et al.
        Human neutrophil cytochrome b light chain (p22-phox): Gene structure, chromosomal location, and mutations in cytochrome-negative autosomal recessive chronic granulomatous disease.
        J Clin Invest. 1990; 86: 1729
        • Eklund E.A.
        • Marshall M.
        • Gibbs J.B.
        • et al.
        Resolution of a low molecular weight G protein in neutrophil cytosol required for NADPH oxidase activation and reconstitution by recombinant Krev-1 protein.
        J Biol Chem. 1991; 266: 13964
        • Ezekowitz R.A.B.
        • Orkin S.H.
        • Newburger P.E.
        Recombinant interferon gamma augments phagocyte superoxide production and X-chronic granulomatous disease gene expression in X-linked variant chronic granulomatous disease.
        J Clin Invest. 1987; 80: 1009
        • Francke U.
        Random X inactivation resulting in mosaic nullisomy of region Xp21→p21.3 associated with heterozygosity for ornithine transcarbamylase deficiency and for chronic granulomatous disease.
        Cytogenet Cell Genet. 1984; 38: 298
        • Francke U.
        • Hsieh C.-L.
        • Foellmer B.E.
        • et al.
        Genes for two autosomal recessive forms of chronic granulomatous disease assigned to lq25 (NCF2) and 7ql 1.23 (NCF1.
        Am J Hum Genet. 1990; 47: 483
        • Francke U.
        • Ochs H.D.
        • De Martinville B.
        • et al.
        Minor Xp21 chromosome deletion in a male associated with expression of Duchenne muscular dystrophy, chronic granulomatous disease, retinitis pigmentosa, and McLeod syndrome.
        Am J Hum Genet. 1985; 37: 250
        • Frey D.
        • Machler M.
        • Seger R.
        • et al.
        Gene deletion in a patient with chronic granulomatous disease and McLeod syndrome: Fine mapping of the Xk gene locus.
        Blood. 1988; 71: 252
        • Gabig T.G.
        • Lefker B.A.
        Deficient flavoprotein component of the NADPH-dependent O22-generating oxidase in neutrophils from three male patients with chronic granulomatous disease.
        J Clin Invest. 1984; 73: 701
        • Gerard N.P.
        • Gerard C.
        The chemotactic receptor for human C5a anaphylatoxin.
        Nature. 1991; 349: 614
        • Glass G.A.
        • DeLisle D.M.
        • DeTogni P.
        • et al.
        The respiratory burst oxidase of human neutrophils: Further studies of the purified enzyme.
        J Biol Chem. 1986; 261: 13247
        • Golbus M.S.
        • McGonigle K.F.
        • Goldberg J.D.
        • et al.
        Fetal tissue sampling: The San Francisco experience with 190 pregnancies.
        West J Med. 1989; 150: 423
        • Gray G.R.
        • Klebanoff S.J.
        • Stamatoyannopoulos G.
        • et al.
        Neutrophil dysfunction, chronic granulomatous disease and non-spherocytic haemolytic anaemia caused by complete deficiency of glucose-6-phosphate dehydrogenase.
        Lancet. 1973; 2: 530
        • Gyllensten U.B.
        PCR and DNA sequencing.
        Bio Tech. 1989; 7: 700
        • Hassan N.F.
        • Campbell D.E.
        • Douglas S.D.
        Phorbol myristate acetate induced oxidation of 2’,7’-dichlorofluorescin by neutrophils from patients with chronic granulomatous disease.
        J Leukoc Biol. 1988; 43: 317
        • Heinrich S.D.
        • Finney T.
        • Craver R.
        • et al.
        Aspergillus osteomyelitis in patients who have chronic granulomatous disease.
        J Bone Joint Surg [Am]. 1991; 73: 456
        • Heyworth P.G.
        • Cumutte J.T.
        • Rosen H.
        • et al.
        Neutrophil nicotinamide adenine dinucleotide phosphate oxidase assembly. Translocation of p>A7-phox and p67-phox requires interaction between p-A7-phox and cytochrome b558.
        J Clin Invest. 1991; 87: 352
        • Heyworth P.G.
        • Tolley J.O.
        • Smith R.M.
        • et al.
        The cytosolic components of the NADPH oxidase system exist as two complexes in the unstimulated neutrophil (abstract.
        Blood. 1990; 76: 183a
        • Huu T.P.
        • Dumez Y.
        • Marquetty C.
        • et al.
        Prenatal diagnosis of chronic granulomatous disease (CGD) in four high risk male fetuses.
        Prenat Diag. 1987; 7: 253
        • Innis M.A.
        • Gelfand D.H.
        Optimization of PCRs. PCR Protocols.
        A Guide to Methods and Applications. Academic Press, San Diego, CA1990: 3-12
        • Johansen K.S.
        Nitroblue tetrazolium slide test: Use of phorbol-myristate-acetate-stimu-lated NBT-reduction slide test for routine and prenatal detection of chronic granulomatous disease and diagnosis of heterozygous carriers.
        Acta Pathol Microbiol Immunol Scand. 1983; 91: 349
        • Kenney R.T.
        • Leto T.L.
        A Hindlll polymorphism in the human NCF2 gene.
        Nucleic Acids Res. 1990; 18: 7193
        • Knaus U.G.
        • Heyworth P.G.
        • Evans T.
        • et al.
        Rac 2 is a regulator of phagocyte oxygen radical production.
        Science. 1991; 254: 1512-1515
        • Koch C.A.
        • Anderson D.
        • Moran M.F.
        • et al.
        SH2 and SH3 domains: Elements that control interactions of cytoplasmic signaling proteins.
        Science. 1991; 252: 668
        • Larson R.S.
        • Springer T.A.
        Structure and function of leukocyte integrins.
        Immunol Rev. 1990; 114: 181
        • Lehrer R.I.
        • Ganz T.
        Antimicrobial polypeptides of human neutrophils.
        Blood. 1990; 76: 2169
        • Lehrer R.I.
        • Ganz T.
        • Selsted M.E.
        • et al.
        Neutrophils and host defense.
        Ann Intern Med. 1988; 109: 127
        • Leto T.L.
        • Lomax K.J.
        • Volpp B.D.
        • et al.
        Cloning of a 67-kDa neutrophil oxidase factor with similarity to a non-catalytic region of p60csrc.
        Science. 1990; 248: 727
        • Levinsky R.J.
        • Harvey B.
        • Nicolaides K.
        • et al.
        Antenatal diagnosis of chronic granulomatous disease.
        Lancet. 1986; 1: 504
        • Levinsky R.J.
        • Harvey B.A.M.
        • Rodeck C.H.
        • et al.
        Phorbol myristate acetate stimulated NBT test: A simple method suitable for antenatal diagnosis of chronic granulomatous disease.
        Clin Exp Immunol. 1983; 54: 595
        • Lew D.P.
        • Southwick F.S.
        • Stossel T.P.
        • et al.
        A variant of chronic granulomatous disease: Deficient oxidative metabolism due to a low affinity NADPH-oxidase.
        N Engl J Med. 1981; 305: 1329
        • Linch D.C.
        • Levinsky R.J.
        Prenatal diagnosis of immunodeficiency disorders.
        Br Med Bull. 1983; 39: 399
        • Lohr G.W.
        • Waller H.D.
        Glucose-6-phosphate dehydrogenase.
        in: Bergmeyer H.U. Methods of Enzymatic Analysis. Academic Press, New York1974: 636
        • Lomax K.J.
        • Leto T.L.
        • Nunoi H.
        • et al.
        Recombinant 47kD cytosol factor restores NADPH oxidase in chronic granulomatous disease.
        Science. 1989; 245: 409
        • Loos J.A.
        • Roos D.
        • Weening R.S.
        • et al.
        Familial deficiency of glutathione reductase in human blood cells.
        Blood. 1976; 48: 53
        • Mandell G.L.
        • Hook E.W.
        Leukocyte bactericidal activity in chronic granulomatous disease: Correlation of bacterial hydrogen peroxide production and susceptibility in intracellular killing.
        J Bacteriol. 1969; 100: 531
        • Manzi S.
        • Urbach A.H.
        • McCune A.B.
        • et al.
        Systemic lupus erythematosus in a boy with chronic granulomatous disease: Case report and review of the literature.
        Arthritis Rheum. 1991; 34: 101
        • Marlin S.D.
        • Morton C.C.
        • Anderson D.C.
        • et al.
        LFA-1 immunodeficiency disease: Definition of the genetic defect and chromosomal mapping of alpha and beta subunits by complementation in hybrid cells.
        J Exp Med. 1986; 164: 355
        • Matthay K.K.
        • Golbus M.S.
        • Wara D.W.
        • et al.
        Prenatal diagnosis of chronic granulomatous disease.
        Am J Med Genet. 1984; 17: 737
        • McPhail L.C.
        • Shirley P.S.
        • Clayton C.C.
        • et al.
        Activation of the respiratory burst enzyme from human neutrophils in a cell-free system.
        J Clin Invest. 1985; 75: 1735
        • Mills E.L.
        • Rholl K.S.
        • Quie P.G.
        X-linked inheritance in females with chronic granulomatous disease.
        J Clin Invest. 1980; 66: 332
        • Muhlebach T.J.
        • Robinson W.
        • Seger R.A.
        • et al.
        A second NsiI RFLP at the CYBB locus.
        Nucleic Acids Res. 1990; 18
        • Mulholland M.W.
        • Delaney J.P.
        • Simmons R.L.
        Gastrointestinal complications of chronic granulomatous disease: Surgical implications.
        Surgery. 1983; 94: 569
        • Murphy P.M.
        • Tiffany H.L.
        Cloning of complementary DNA encoding a functional human interleukin-8 receptor.
        Science. 1991; 253: 1280
        • Nakamura M.
        • Imajoh-Ohmi S.
        • Kanegasaki S.
        • et al.
        Prenatal diagnosis of cytochrome-deficient chronic granulomatous disease.
        Lancet. 1990; 1: 118
        • Nauseef W.M.
        Myeloperoxidase deficiency.
        Hematol/Oncol Clin North Am. 1988; 2: 135-158
        • Newburger P.E.
        • Cohen H.J.
        • Rothchild S.B.
        • et al.
        Prenatal diagnosis of chronic granulomatous disease.
        N Engl J Med. 1979; 300: 178
        • Newburger P.E.
        • Luscinskas F.W.
        • Ryan T.
        • et al.
        Variant chronic granulomatous disease: Modulation of the neutrophil by severe infection.
        Blood. 1986; 68: 914
        • Nunoi H.
        • Rotrosen D.
        • Gallin J.I.
        • et al.
        Two forms of autosomal chronic granulomatous disease lack distinct neutrophil cytosol factors.
        Science. 1988; 242: 1298
        • O’Neil K.M.
        • Herman J.H.
        • Modlin J.F.
        • et al.
        Pseudomonas cepacia: An emerging pathogen in chronic granulomatous disease.
        J Pediatr. 1986; 108: 940
        • Ochs H.D.
        • Igo R.P.
        The NBT slide test: A simple screening method for detecting chronic granulomatous disease and female carriers.
        J Pediatr. 1973; 83: 77
        • Ohno Y.
        • Buescher E.S.
        • Roberts R.
        • et al.
        Reevaluation of cytochrome b and flavin adenine dinucleotide in neutrophils from patients with chronic granulomatous disease and description of a family with probable autosomal recessive inheritance of cytochrome bdeficiency.
        Blood. 1986; 67: 1132
        • Okamura N.
        • Malawista S.E.
        • Roberts R.L.
        • et al.
        Phosphorylation of the oxidase-related 48K phosphoprotein family in the unusual autosomal cytochrome-negative and X-linked cytochrome-positive types of chronic granulomatous disease.
        Blood. 1988; 72: 811
        • Orita M.
        • Iwahana H.
        • Kanazawa H.
        • et al.
        Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms.
        Proc Natl Acad Sei USA. 1989; 86: 2766
        • Orita M.
        • Suzuki Y.
        • Sekiya T.
        • et al.
        Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction.
        Genomics. 1989; 5: 874
        • Orkin S.H.
        Molecular genetics of chronic granulomatous disease.
        Ann Rev Immunol. 1989; 7: 277
        • Parkos C.A.
        • Allen R.A.
        • Cochrane C.G.
        • et al.
        Purified cytochrome b from human granulocyte plasma membrane is comprised of two polypeptides with relative molecular weights of 91,000 and 22,000.
        J Clin Invest. 1987; 80: 732
        • Parkos C.A.
        • Dinauer M.C.
        • Jesaitis A.J.
        • et al.
        Absence of both the 91kD and 22kD subunits of human neutrophil cytochrome b in two genetic forms of chronic granulomatous disease.
        Blood. 1989; 73: 1416
        • Parkos C.A.
        • Dinauer M.C.
        • Walker L.E.
        • et al.
        Primary structure and unique expression of the 22-kilodalton light chain of human neutrophil cytochrome b.
        Proc Natl Acad Sei USA. 1988; 85: 3319
        • Parry M.F.
        • Root R.K.
        • Metcalf J.A.
        • et al.
        Myeloperoxidase deficiency: Prevalence and clinical significance.
        Ann Intern Med. 1981; 95: 293
        • Pelham A.
        • O’Reilly M.-A.J.
        • Malcolm S.
        • et al.
        RFLP and deletion analysis for X-linked chronic granulomatous disease using the cDNA probe: Potential for improved prenatal diagnosis and carrier determination.
        Blood. 1990; 76: 820
        • Quinn M.T.
        • Parkos C.A.
        • Walker L.
        • et al.
        Association of a Ras-related protein with cytochrome b of human neutrophils.
        Nature. 1989; 342: 198
        • Regelman W.
        • Hayes N.
        • et al.
        Chronic granulomatous disease: Historical perspectives and the clinical experience at the University of Minnesota Hospitals.
        in: Gallin J.I. Fauci A.S. Advances in Host Defense Mechanisms. vol 3. Raven Press, New York1982: 3 (Chronic Granulomatous Disease)
        • Roesler J.
        • Hecht M.
        • Freihorst J.
        • et al.
        Diagnosis of chronic granulomatous disease and of its mode of inheritance of dihydrorhodamine 123 and flow microcytofiuorometry.
        Eur J Pediatr. 1991; 150: 161
        • Roos D.
        • Weening R.S.
        • Voetman A.A.
        • et al.
        Protection of phagocytic leukocytes by endogenous glutathione: Studies in a family with glutathione reductase deficiency.
        Blood. 1979; 53: 851
        • Rothe G.
        • Valet G.
        Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2’,7’-dichlorofluorescin.
        J Leukoc Biol. 1990; 47: 440
        • Rotrosen D.
        • Kleinberg M.E.
        • Nunoi H.
        • et al.
        Evidence for a functional cytoplasmic domain of phagocyte oxidase cytochrome b556.
        J Biol Chem. 1990; 265: 8745
        • Rotrosen D.
        • Leto T.L.
        Phosphorylation of neutrophil 47-kDa cytosolic oxidase factor: Translocation to membrane is associated with distinct phosphorylation events.
        J Biol Chem. 1990; 265: 19910
        • Royer-Pokora B.
        • Kunkel L.M.
        • Monaco A.P.
        • et al.
        Cloning the gene for an inherited human disorder—chronic granulomatous disease—on the basis of its chromosomal location.
        Nature. 1986; 322: 32
        • Sadler K.L.
        • Badwey J.A.
        Second messengers involved in superoxide production by neutrophils: Function and metabolism.
        Hematol/Oncol Clin North Am. 1988; 2: 185-200
        • Segal A.W.
        Absence of both cytochrome fr-245 subunits from neutrophils in X-linked chronic granulomatous disease.
        Nature. 1987; 326: 88
        • Segal A.W.
        • Cross A.R.
        • Garcia R.C.
        • et al.
        Absence of cytochrome b-245 in chronic granulomatous disease: A multicenter European evaluation of its incidence and relevance.
        N Engl J Med. 1983; 308: 245
        • Segal A.W.
        • Heyworth P.G.
        • Cockcroft S.
        • et al.
        Stimulated neutrophils from patients with autosomal recessive chronic granulomatous disease fail to phosphorylate a Mr-44,000 protein.
        Nature. 1985; 316: 547
        • Seger R.
        • Steinmann B.
        Prenatal diagnosis of chronic granulomatous disease: Unreliability of fibroblast nitroblue tetrazolium test.
        Lancet. 1981; 1: 1216
        • Seger R.A.
        • Tiefenauer L.
        • Matsunaga T.
        • et al.
        Chronic granulomatous disease due to granulocytes with abnormal NADPH oxidase activity and deficient cytochrome-b.
        Blood. 1983; 61: 423
        • Shurin S.B.
        • Cohen H.J.
        • Whitin J.C.
        • et al.
        Impaired granulocyte superoxide production and prolongation of the respiratory burst due to a low-affinity NADPH-dependent oxidase.
        Blood. 1983; 62: 564
        • Skalnik D.G.
        • Strauss E.C.
        • Orkin S.H.
        CCAAT displacement protein as a depressor of the myelomonocytic specific gp9l-phox promoter.
        J Biol Chem. 1991; 266: 16736
        • Smith R.M.
        • Cumutte J.T.
        Molecular basis of chronic granulomatous disease.
        Blood. 1991; 77: 673
        • Spielberg S.P.
        • Boxer L.A.
        • Oliver J.M.
        • et al.
        Oxidative damage to neutrophils in glutathione synthetase deficiency.
        Br J Haematol. 1979; 42: 215
        • Spinardi L.
        • Mazars R.
        • Theillet C.
        Protocols for an improved detection of point mutations by SSCP.
        Nucleic Acids Res. 1991; 19: 4009
        • Springer T.A.
        Adhesion receptors of the immune system.
        Nature. 1990; 346: 425
        • Tauber A.I.
        • Borregaard N.
        • Simons E.
        • et al.
        Chronic granulomatous disease: A syndrome of phagocyte oxidase deficiencies.
        Medicine. 1983; 62: 286
        • Teahan C.
        • Rowe P.
        • Parker P.
        • et al.
        The X-linked chronic granulomatous disease gene codes for the beta-chain of cytochrome b-245.
        Nature. 1987; 327: 720
        • Todd III., R.F.
        • Freyer D.R.
        The CD11/CD18 leukocyte glycoprotein deficiency.
        Hematol Oncol Clin North Am. 1988; 2: 13-31
        • Unkeless J.C.
        Function and heterogeneity of human Fc receptors for immunoglobulin G.
        J Clin Invest. 1989; 83: 355
        • Van Tuinen P.
        • Johnson K.R.
        • Ledbetter S.A.
        • et al.
        Localization of myeloperoxidase to the long arm of human chromosome 17: Relationship to the 15,17 translocation of acute promyelocytic leukemia.
        Oncogene. 1987; 1: 319
        • Vives Corrons J.L.
        • Feliu E.
        • Pujades M.A.
        • et al.
        Severe glucose-6-phosphate dehydrogenase (G6PD) deficiency associated with chronic hemolytic anemia, granulocyte dysfunction, and increased susceptibility to infection: Description of a new molecular variant (G6PD Barcelona.
        Blood. 1982; 59: 428
        • Volpp B.D.
        • Nauseef W.M.
        • Donelson J.E.
        • et al.
        Cloning of the cDNA and functional expression of the 47-kilodalton cytosolic component of the human neutrophil respiratory burst oxidase.
        Proc Natl Acad Sei USA. 1989; 86: 7195
        • Weening R.S.
        • Corbeel L.
        • de Boer M.
        • et al.
        Cytochrome b deficiency in an autosomal form of chronic granulomatous disease. A third form of chronic granulomatous disease recognized by monocyte hybridization.
        J Clin Invest. 1985; 75: 915
        • White T.J.
        • Amheim N.
        • Erlich H.A.
        The polymerase chain reaction.
        Trends in Genetics. 1989; 5: 185