Lethal Influenza in Two Related Adults with Inherited GATA2 Deficiency

Journal of Clinical Immunology

Volumn 38, Issue 4, 2018, Pages 513-526

  Sologuren, Ithaisa ^a   Martínez Saavedra, María Teresa ^a   Solé Violán, Jordi ^a,b   de Borges de Oliveira, Edgar ^c,d   Betancor, Eva ^e   Casas, Inmaculada ^f   Oleaga Quintas, Carmen ^c,d   Martínez Gallo, Mónica ^g   Zhang, Shen Ying ^c,d,h   Pestano, Jose ^e   Colobran, Roger ^g,i   Herrera Ramos, Estefanía ^a   Pérez, Carmen ^a   López Rodríguez, Marta ^a   Ruiz Hernández, José Juan ^a   Franco, Nieves ^j   Ferrer, José María ^a,b   Bilbao, Cristina ^a   Andújar Sánchez, Miguel ^k   Álvarez Fernández, Mercedes ^j   Ciancanelli, Michael J ^h   Rodríguez de Castro, Felipe ^a   Casanova, Jean Laurent ^c,d,h,l   Bustamante, Jacinta ^a,c,d,h   Rodríguez Gallego, Carlos ^a   more..

^a HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^f INSTITUTO DE SALUD CARLOS III   (Spain)

^g HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^h ROCKEFELLER UNIVERSITY   (United States)

ⁱ UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^j HOSPITAL DE MÓSTOLES   (Spain)

^k HOSPITAL UNIVERSITARIO INSULAR DE GRAN CANARIA   (Spain)

^l HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

GATA2; H1N1; Immunodeficiency; immunological memory; influenza A virus

Indexed keywords

ADP RIBOSYL CYCLASE/CYCLIC ADP RIBOSE HYDROLASE 1; CD19 ANTIGEN; CD20 ANTIGEN; CD24 ANTIGEN; CD27 ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; CD57 ANTIGEN; CEFTRIAXONE; CXCL9 CHEMOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN D; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 8; LEVOFLOXACIN; LUCIFERASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; OSELTAMIVIR; PROTEIN; RESIDUE 396 PROTEIN; TRANSCRIPTION FACTOR GATA 2; UNCLASSIFIED DRUG; ZANAMIVIR; BIOLOGICAL MARKER; CYTOKINE;

ACINETOBACTER INFECTION; ACUTE RESPIRATORY FAILURE; ADULT; ADULT RESPIRATORY DISTRESS SYNDROME; ALLELE; ANTIBODY BLOOD LEVEL; ARTICLE; ARTIFICIAL VENTILATION; B LYMPHOCYTE; BLOOD SAMPLING; BONE MARROW BIOPSY; CD4 CD8 RATIO; CELL CLONING; CELL EXPANSION; CYTOKINE PRODUCTION; CYTOKINE STORM; DRUG WITHDRAWAL; ELECTROPHORESIS; EPSTEIN BARR VIRUS; FEMALE; FIBROSING ALVEOLITIS; FLU LIKE SYNDROME; GENE EXPRESSION; GENE TRANSFER; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; HEK293T CELL LINE; HERPES SIMPLEX VIRUS; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXEMIA; IMMUNOLOGICAL PROCEDURES; INFECTIOUS COMPLICATION; INFLUENZA A (H1N1); INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H7N9); INTENSIVE CARE; KLEBSIELLA PNEUMONIAE INFECTION; LUNG ALVEOLUS PROTEINOSIS; LUNG BIOPSY; LUNG INFILTRATE; LUPUS LIKE SYNDROME; MACROPHAGE; MALE; MIDDLE AGED; MISSENSE MUTATION; MONOCYTE; MONOCYTOPENIA; MYELODYSPLASTIC SYNDROME; NATURAL KILLER CELL; NEUTROPENIA; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; RECRUITMENT MANEUVER; REGULATORY T LYMPHOCYTE; RESPIRATORY FAILURE; RUBELLA VIRUS; SANGER SEQUENCING; SECONDARY INFECTION; SEPTIC SHOCK; T LYMPHOCYTE; T-CELL GENE REARRANGEMENT; THORAX RADIOGRAPHY; THROAT CULTURE; TRANSCRIPTION FACTOR GATA 2 DEFICIENCY; VARICELLA ZOSTER VIRUS; VIRUS PNEUMONIA; YOUNG ADULT; BLOOD; CASE REPORT; COMPLICATION; DNA MUTATIONAL ANALYSIS; FATALITY; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; INFLUENZA; INFLUENZA A VIRUS; LYMPHOCYTE SUBPOPULATION; METABOLISM; MUTATION; PEDIGREE; VIROLOGY;

BIOMARKERS; CYTOKINES; DNA MUTATIONAL ANALYSIS; FATAL OUTCOME; FEMALE; GATA2 DEFICIENCY; GATA2 TRANSCRIPTION FACTOR; HUMANS; IMMUNOPHENOTYPING; INFLUENZA A VIRUS; INFLUENZA, HUMAN; LYMPHOCYTE SUBSETS; MALE; MUTATION; PEDIGREE;

EID: 85048125487     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-018-0512-0     Document Type: Article

References (51)

1. Peiris JS, Cheung CY, Leung CY, Nicholls JM. Innate immune responses to influenza AH5N1: friend or foe? Trends Immunol. 2009;30:574–84.
2. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 2003;289:179–86.
3. Bautista E, Chotpitayasunondh T, Gao Z, et al. Clinical aspects of pandemic 2009 influenza A (H1N1) virus infection. N Engl J Med. 2010;362:1708–19.
4. Wu JT, Leung K, Perera RA, et al. Inferring influenza infection attack rate from seroprevalence data. PLoS Pathog. 2014;10:e1004054.
5. Hayward AC, Fragaszy EB, Bermingham A, Wang L, Copas A, Edmunds WJ, et al. Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study. Lancet Respir Med. 2014;2:445–54.
6. Dawood FS, Iuliano AD, Reed C, Meltzer MI, Shay DK, Cheng PY, et al. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis. 2012;12:687–95.
7. Albright FS, Orlando P, Pavia AT, Jackson GG, Cannon Albright LA. Evidence for a heritable predisposition to death due to influenza. J Infect Dis. 2008;197:18–24.
8. Fukuyama S, Kawaoka Y. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol. 2011;23:481–6.
9. Ciancanelli MJ, Abel L, Zhang SY, Casanova JL. Host genetics of severe influenza: from mouse Mx1 to human IRF7. Curr Opin Immunol. 2016;38:109–20.
10. Ciancanelli MJ, Huang SX, Luthra P, et al. Infectious disease. Life-threatening influenza and impaired interferon amplification in human IRF7 deficiency. Science. 2015;348:448–53.
11. Bigley V, Haniffa M, Doulatov S, Wang XN, Dickinson R, McGovern N, et al. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J Exp Med. 2011;208:227–34.
12. Pasquet M, Bellanné-Chantelot C, Tavitian S, et al. High frequency of GATA2 mutations in patients with mild chronic neutropenia evolving to MonoMac syndrome, myelodysplasia, and acute myeloid leukemia. Blood. 2013;121:822–9.
13. Hsu AP, Sampaio EP, Khan J, Calvo KR, Lemieux JE, Patel SY, et al. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood. 2011;118:2653–5.
14. Dickinson RE, Griffin H, Bigley V, Reynard LN, Hussain R, Haniffa M, et al. Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood. 2011;118:2656–8.
15. Ostergaard P, Simpson MA, Connell FC, Steward CG, Brice G, Woollard WJ, et al. Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat Genet. 2011;43:929–31.
16. Hahn CN, Chong CE, Carmichael CL, Wilkins EJ, Brautigan PJ, Li XC, et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat Genet. 2011;43:1012–7.
17. Spinner MA, Sanchez LA, Hsu AP, Shaw PA, Zerbe CS, Calvo KR, et al. GATA2 deficiency: a protean disorder of hematopoiesis, lymphatics, and immunity. Blood. 2014;123:809–21.
18. Dickinson RE, Milne P, Jardine L, Zandi S, Swierczek SI, McGovern N, et al. The evolution of cellular deficiency in GATA2 mutation. Blood. 2014;123:863–74.
19. Ganapathi KA, Townsley DM, Hsu AP, Arthur DC, Zerbe CS, Cuellar-Rodriguez J, et al. GATA2 deficiency-associated bone marrow disorder differs from idiopathic aplastic anemia. Blood. 2015;125:56–70.
20. Ho CK, Strauss JF 3rd. Activation of the control reporter plasmids pRL-TK and pRL-SV40 by multiple GATA transcription factors can lead to aberrant normalization of transfection efficiency. BMC Biotechnol. 2004;4:10.
21. Pérez-Lago L, Navarro Y, Montilla P, Comas I, Herranz M, Rodríguez-Gallego C, et al. Persistent infection by a mycobacterium tuberculosis strain that was theorized to have advantageous properties, as it was responsible for a massive outbreak. J Clin Microbiol. 2015;53:3423–9.
22. Centers for Disease Control. CDC Protocol of Real-Time RTPCR for Influenza AH1N1; 2009.
23. WHO Global Influenza Surveillance Network. Manual for the laboratory diagnosis and virological surveillance of influenza. Chapter 2G pp. 63-77. Switzerland: WHO Press; 2011.
24. Douek DC, McFarland RD, Keiser PH, Gage EA, Massey JM, Haynes BF, et al. Changes in thymic function with age and during the treatment of HIV infection. Nature. 1998;396:690–5.
25. Herrera-Ramos E, López-Rodríguez M, Ruíz-Hernández JJ, Horcajada J, Borderías L, Lerma E, et al. Surfactant protein A genetic variants associate with severe respiratory insufficiency in pandemic influenza a virus infection. Crit Care. 2014;18:R127.
26. López-Rodríguez M, Herrera-Ramos E, Solé-Violán J, Ruíz-Hernández JJ, Borderías L, Horcajada JP, et al. IFITM3 and severe influenza virus infection. No evidence of genetic association. Eur J Clin Microbiol Infect Dis. 2016;35:1811–7.
27. Vinh DC, Patel SY, Uzel G, Anderson VL, Freeman AF, Olivier KN, et al. Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia. Blood. 2010;115:1519–29.
28. Hsu AP, McReynolds LJ, Holland SM. GATA2 deficiency. Curr Opin Allergy Clin Immunol. 2015;15:104–9.
29. Chou J, Lutskiy M, Tsitsikov E, Notarangelo LD, Geha RS, Dioun A. Presence of hypogammaglobulinemia and abnormal antibody responses in GATA2 deficiency. J Allergy Clin Immunol. 2014;134:223–6.
30. Nováková M, Žaliová M, Suková M, et al. Loss of B cells and their precursors is the most constant feature of GATA-2 deficiency in childhood myelodysplastic syndrome. Haematologica. 2016;101:707–16.
31. Sridhar S, Begom S, Bermingham A, Hoschler K, Adamson W, Carman W, et al. Cellular immune correlates of protection against symptomatic pandemic influenza. Nat Med. 2013;19:1305–12.
32. Wilkinson TM, Li CK, Chui CS, et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med. 2012;18:274–80.
33. Trammell RA, Liberati TA, Toth LA. Host genetic background and the innate inflammatory response of lung to influenza virus. Microbes Infect. 2012;14:50–8.
34. Huang Y, Zaas AK, Rao A, Dobigeon N, Woolf PJ, Veldman T, et al. Temporal dynamics of host molecular responses differentiate symptomatic and asymptomatic influenza a infection. PLoS Genet. 2011;7:e1002234.
35. Teijaro JR, Walsh KB, Cahalan S, Fremgen DM, Roberts E, Scott F, et al. Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell. 2011;146:980–91.
36. Cohen JI, Dropulic L, Hsu AP, Zerbe CS, Krogmann T, Dowdell K, et al. Association of GATA2 deficiency with severe primary Epstein-Barr virus (EBV) infection and EBV-associated cancers. Clin Infect Dis. 2016;63:41–7.
37. Spinner MA, Ker JP, Stoudenmire CJ, et al. GATA2 deficiency underlying severe blastomycosis and fatal herpes simplex virus-associated hemophagocytic lymphohistiocytosis. J Allergy Clin Immunol. 2016;137:638–40.
38. Ishii E. Hemophagocytic lymphohistiocytosis in children: pathogenesis and treatment. Front Pediatr. 2016;4:47.
39. Collin M, Dickinson R, Bigley V. Haematopoietic and immune defects associated with GATA2 mutation. Br J Haematol. 2015;169:173–87.
40. Belkaid Y, Tarbell K. Regulatory T cells in the control of host-microorganism interactions (*). Annu Rev Immunol. 2009;27:551–89.
41. Antunes I, Kassiotis G. Suppression of innate immune pathology by regulatory T cells during Influenza A virus infection of immunodeficient mice. J Virol. 2010;84:12564–75.
42. Lee MN, Ye C, Villani AC, Raj T, Li W, Eisenhaure TM, et al. Common genetic variants modulate pathogen-sensing responses in human dendritic cells. Science. 2014;343:1246980.
43. Li GM, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng NY, et al. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci U S A. 2012;109:9047–52.
44. Li Y, Myers JL, Bostick DL, Sullivan CB, Madara J, Linderman SL, et al. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J Exp Med. 2013;210:1493–500.
45. Fonville JM, Wilks SH, James SL, Fox A, Ventresca M, Aban M, et al. Antibody landscapes after influenza virus infection or vaccination. Science. 2014;346:996–1000.
46. Skowronski DM, Hottes TS, McElhaney JE, et al. Immuno-epidemiologic correlates of pandemic H1N1 surveillance observations: higher antibody and lower cell-mediated immune responses with advanced age. J Infect Dis. 2011;203:158–67.
47. Mace EM, Orange JS. Genetic causes of human NK cell deficiency and their effect on NK cell subsets. Front Immunol. 2016;7:545.
48. Dropulic LK, Cohen JI. Severe viral infections and primary immunodeficiencies. Clin Infect Dis. 2011;53:897–909.
49. Sancho-Shimizu V, Perez de Diego R, Jouanguy E, Zhang SY, Casanova JL. Inborn errors of anti-viral interferon immunity in humans. Curr Opin Virol. 2011;1:487–96.
50. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, et al. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med. 2011;365:127–38.
51. Alcais A, Quintana-Murci L, Thaler DS, Schurr E, Abel L, Casanova JL. Life-threatening infectious diseases of childhood: single-gene inborn errors of immunity? Ann N Y Acad Sci. 2010;1214:18–33.