Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease

Jacinta Bustamante; Andres A. Arias; Guillaume Vogt; Capucine Picard; Lizbeth Blancas Galicia; Carolina Prando; Audrey V. Grant; Christophe C. Marchal; Marjorie Hubeau; Ariane Chapgier; Ludovic De Beaucoudrey; Anne Puel; Jacqueline Feinberg; Ethan Valinetz; Lucile Jannière; Céline Besse; Anne Boland; Jean Marie Brisseau; Stéphane Blanche; Olivier Lortholary; Claire Fieschi; Jean François Emile; Stéphanie Boisson-Dupuis; Saleh Al-Muhsen; Bruce Woda; Peter E. Newburger; Antonio Condino-Neto; Mary C. Dinauer; Laurent Abel; Jean Laurent Casanova

doi:10.1038/ni.1992

Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease

Jacinta Bustamante, Andres A. Arias, Guillaume Vogt, Capucine Picard, Lizbeth Blancas Galicia, Carolina Prando, Audrey V. Grant, Christophe C. Marchal, Marjorie Hubeau, Ariane Chapgier, Ludovic De Beaucoudrey, Anne Puel, Jacqueline Feinberg, Ethan Valinetz, Lucile Jannière, Céline Besse, Anne Boland, Jean Marie Brisseau, Stéphane Blanche, Olivier LortholaryClaire Fieschi, Jean François Emile, Stéphanie Boisson-Dupuis, Saleh Al-Muhsen, Bruce Woda, Peter E. Newburger, Antonio Condino-Neto, Mary C. Dinauer, Laurent Abel, Jean Laurent Casanova

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Abstract

Germline mutations in CYBB, the human gene encoding the gp91^phox subunit of the phagocyte NADPH oxidase, impair the respiratory burst of all types of phagocytes and result in X-linked chronic granulomatous disease (CGD). We report here two kindreds in which otherwise healthy male adults developed X-linked recessive Mendelian susceptibility to mycobacterial disease (MSMD) syndromes. These patients had previously unknown mutations in CYBB that resulted in an impaired respiratory burst in monocyte-derived macrophages but not in monocytes or granulocytes. The macrophage-specific functional consequences of the germline mutation resulted from cell-specific impairment in the assembly of the NADPH oxidase. This 'experiment of nature' indicates that CYBB is associated with MSMD and demonstrates that the respiratory burst in human macrophages is a crucial mechanism for protective immunity to tuberculous mycobacteria.

Original language	English
Pages (from-to)	213-221
Number of pages	9
Journal	Nature immunology
Volume	12
Issue number	3
DOIs	https://doi.org/10.1038/ni.1992
State	Published - Mar 2011

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Bustamante, J., Arias, A. A., Vogt, G., Picard, C., Galicia, L. B., Prando, C., Grant, A. V., Marchal, C. C., Hubeau, M., Chapgier, A., De Beaucoudrey, L., Puel, A., Feinberg, J., Valinetz, E., Jannière, L., Besse, C., Boland, A., Brisseau, J. M., Blanche, S., ... Casanova, J. L. (2011). Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nature immunology, 12(3), 213-221. https://doi.org/10.1038/ni.1992

@article{58d6f2e749164032aba65f756875b57b,

title = "Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease",

abstract = "Germline mutations in CYBB, the human gene encoding the gp91phox subunit of the phagocyte NADPH oxidase, impair the respiratory burst of all types of phagocytes and result in X-linked chronic granulomatous disease (CGD). We report here two kindreds in which otherwise healthy male adults developed X-linked recessive Mendelian susceptibility to mycobacterial disease (MSMD) syndromes. These patients had previously unknown mutations in CYBB that resulted in an impaired respiratory burst in monocyte-derived macrophages but not in monocytes or granulocytes. The macrophage-specific functional consequences of the germline mutation resulted from cell-specific impairment in the assembly of the NADPH oxidase. This 'experiment of nature' indicates that CYBB is associated with MSMD and demonstrates that the respiratory burst in human macrophages is a crucial mechanism for protective immunity to tuberculous mycobacteria.",

author = "Jacinta Bustamante and Arias, {Andres A.} and Guillaume Vogt and Capucine Picard and Galicia, {Lizbeth Blancas} and Carolina Prando and Grant, {Audrey V.} and Marchal, {Christophe C.} and Marjorie Hubeau and Ariane Chapgier and {De Beaucoudrey}, Ludovic and Anne Puel and Jacqueline Feinberg and Ethan Valinetz and Lucile Janni{\`e}re and C{\'e}line Besse and Anne Boland and Brisseau, {Jean Marie} and St{\'e}phane Blanche and Olivier Lortholary and Claire Fieschi and Emile, {Jean Fran{\c c}ois} and St{\'e}phanie Boisson-Dupuis and Saleh Al-Muhsen and Bruce Woda and Newburger, {Peter E.} and Antonio Condino-Neto and Dinauer, {Mary C.} and Laurent Abel and Casanova, {Jean Laurent}",

note = "Funding Information: We thank the family members for participating in this study; J. Curnutte (3-V Biosciences) for EBV-B cells from CGD controls; D. Roos (University of Amsterdam) for mAb 449; F. Morel (Grenoble University) for mAb 7A2; M. Quinn (Montana State University) for mAb 54.1; all members of the two branches of the laboratory of Human Genetics of Infectious Diseases for discussions; and T. Leclerc, Y. Rose, M. de Suremain, M. Kezadi, and N. Stull for technical assistance. Supported by Institut National de la Sant{\'e} et de la Recherche M{\'e}dicale (J.B.), the European Union (NEOTIM EEA05095KKA to J.B., and HOMITB HEALTH-F3-2008-200732), the March of Dimes (RO5050KK to J.B.), Funda{\c c}{\~a}o de Amparo a Pesquisa do Estado de S{\~a}o Paulo (A.C.-N.), Conselho Nacional de Desenvolvimento Cientifico e Tecnol{\'o}gico (A.C.-N.), Fondation BNP-Paribas, Fondation Schlumberger, Institut Universitaire de France, Agence Nationale de Recherche, The Rockefeller University Center for Clinical and Translational Science (5UL1RR024143-03), The Rockefeller University, the National Institutes of Health (AI 079788 and DK54369 to P.E.N., and HL045635 to M.C.D.), the Riley Children{\textquoteright}s Foundation (M.C.D.) and the Howard Hughes Medical Institute (J.-L.C.).",

year = "2011",

month = mar,

doi = "10.1038/ni.1992",

language = "English",

volume = "12",

pages = "213--221",

journal = "Nature immunology",

issn = "1529-2908",

number = "3",

}

Bustamante, J, Arias, AA, Vogt, G, Picard, C, Galicia, LB, Prando, C, Grant, AV, Marchal, CC, Hubeau, M, Chapgier, A, De Beaucoudrey, L, Puel, A, Feinberg, J, Valinetz, E, Jannière, L, Besse, C, Boland, A, Brisseau, JM, Blanche, S, Lortholary, O, Fieschi, C, Emile, JF, Boisson-Dupuis, S, Al-Muhsen, S, Woda, B, Newburger, PE, Condino-Neto, A, Dinauer, MC, Abel, L & Casanova, JL 2011, 'Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease', Nature immunology, vol. 12, no. 3, pp. 213-221. https://doi.org/10.1038/ni.1992

TY - JOUR

T1 - Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease

AU - Bustamante, Jacinta

AU - Arias, Andres A.

AU - Vogt, Guillaume

AU - Picard, Capucine

AU - Galicia, Lizbeth Blancas

AU - Prando, Carolina

AU - Grant, Audrey V.

AU - Marchal, Christophe C.

AU - Hubeau, Marjorie

AU - Chapgier, Ariane

AU - De Beaucoudrey, Ludovic

AU - Puel, Anne

AU - Feinberg, Jacqueline

AU - Valinetz, Ethan

AU - Jannière, Lucile

AU - Besse, Céline

AU - Boland, Anne

AU - Brisseau, Jean Marie

AU - Blanche, Stéphane

AU - Lortholary, Olivier

AU - Fieschi, Claire

AU - Emile, Jean François

AU - Boisson-Dupuis, Stéphanie

AU - Al-Muhsen, Saleh

AU - Woda, Bruce

AU - Newburger, Peter E.

AU - Condino-Neto, Antonio

AU - Dinauer, Mary C.

AU - Abel, Laurent

AU - Casanova, Jean Laurent

N1 - Funding Information: We thank the family members for participating in this study; J. Curnutte (3-V Biosciences) for EBV-B cells from CGD controls; D. Roos (University of Amsterdam) for mAb 449; F. Morel (Grenoble University) for mAb 7A2; M. Quinn (Montana State University) for mAb 54.1; all members of the two branches of the laboratory of Human Genetics of Infectious Diseases for discussions; and T. Leclerc, Y. Rose, M. de Suremain, M. Kezadi, and N. Stull for technical assistance. Supported by Institut National de la Santé et de la Recherche Médicale (J.B.), the European Union (NEOTIM EEA05095KKA to J.B., and HOMITB HEALTH-F3-2008-200732), the March of Dimes (RO5050KK to J.B.), Fundação de Amparo a Pesquisa do Estado de São Paulo (A.C.-N.), Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (A.C.-N.), Fondation BNP-Paribas, Fondation Schlumberger, Institut Universitaire de France, Agence Nationale de Recherche, The Rockefeller University Center for Clinical and Translational Science (5UL1RR024143-03), The Rockefeller University, the National Institutes of Health (AI 079788 and DK54369 to P.E.N., and HL045635 to M.C.D.), the Riley Children’s Foundation (M.C.D.) and the Howard Hughes Medical Institute (J.-L.C.).

PY - 2011/3

Y1 - 2011/3

N2 - Germline mutations in CYBB, the human gene encoding the gp91phox subunit of the phagocyte NADPH oxidase, impair the respiratory burst of all types of phagocytes and result in X-linked chronic granulomatous disease (CGD). We report here two kindreds in which otherwise healthy male adults developed X-linked recessive Mendelian susceptibility to mycobacterial disease (MSMD) syndromes. These patients had previously unknown mutations in CYBB that resulted in an impaired respiratory burst in monocyte-derived macrophages but not in monocytes or granulocytes. The macrophage-specific functional consequences of the germline mutation resulted from cell-specific impairment in the assembly of the NADPH oxidase. This 'experiment of nature' indicates that CYBB is associated with MSMD and demonstrates that the respiratory burst in human macrophages is a crucial mechanism for protective immunity to tuberculous mycobacteria.

AB - Germline mutations in CYBB, the human gene encoding the gp91phox subunit of the phagocyte NADPH oxidase, impair the respiratory burst of all types of phagocytes and result in X-linked chronic granulomatous disease (CGD). We report here two kindreds in which otherwise healthy male adults developed X-linked recessive Mendelian susceptibility to mycobacterial disease (MSMD) syndromes. These patients had previously unknown mutations in CYBB that resulted in an impaired respiratory burst in monocyte-derived macrophages but not in monocytes or granulocytes. The macrophage-specific functional consequences of the germline mutation resulted from cell-specific impairment in the assembly of the NADPH oxidase. This 'experiment of nature' indicates that CYBB is associated with MSMD and demonstrates that the respiratory burst in human macrophages is a crucial mechanism for protective immunity to tuberculous mycobacteria.

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U2 - 10.1038/ni.1992

DO - 10.1038/ni.1992

M3 - Article

C2 - 21278736

AN - SCOPUS:79951647077

SN - 1529-2908

VL - 12

SP - 213

EP - 221

JO - Nature immunology

JF - Nature immunology

IS - 3

ER -

Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease

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