Human inborn errors of immunity to infection affecting cells other than leukocytes: from the immune system to the whole organism

Current Opinion in Immunology

Volumn 59, Issue , 2019, Pages 88-100

  Zhang, Shen Ying ^a,b,c   Jouanguy, Emmanuelle ^a,b,c   Zhang, Qian ^a   Abel, Laurent ^a,b,c   Puel, Anne ^a,b,c   Casanova, Jean Laurent ^a,b,c,d  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN L1; DARC PROTEIN; FUCOSYLTRANSFERASE; FUT2 PROTEIN; MEMBRANE RECEPTOR; UNCLASSIFIED DRUG; ACKR1 PROTEIN, HUMAN; CELL SURFACE RECEPTOR; COMPLEMENT; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE;

BRAIN CORTEX; BRAIN NERVE CELL; COMPLEMENT SYSTEM; EPITHELIUM CELL; ERYTHROCYTE; GENETIC RESISTANCE; GENETIC VARIABILITY; HERPES SIMPLEX VIRUS; HUMAN; HUMAN GENETICS; IMMUNE SYSTEM; IMMUNOPATHOLOGY; INFECTION RESISTANCE; INFECTION SENSITIVITY; INFLUENZA VIRUS; INTESTINE EPITHELIUM CELL; KERATINOCYTE; LEUKOCYTE; LIVER CELL; LUNG EPITHELIUM; NONHUMAN; NOROVIRUS INFECTION; PLASMODIUM VIVAX MALARIA; PROTEIN EXPRESSION; PROTEIN SECRETION; PYOGENIC BACTERIUM; REVIEW; ROTAVIRUS INFECTION; TRYPANOSOMA; WART VIRUS; ANIMAL; BLOOD GROUP DUFFY SYSTEM; IMMUNOLOGY; METABOLISM; NEWBORN; NEWBORN DISEASE;

ANIMALS; APOLIPOPROTEIN L1; COMPLEMENT SYSTEM PROTEINS; DUFFY BLOOD-GROUP SYSTEM; EPITHELIAL CELLS; ERYTHROCYTES; FUCOSYLTRANSFERASES; HEPATOCYTES; HUMANS; IMMUNE SYSTEM; IMMUNE SYSTEM DISEASES; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; INFECTIONS; LEUKOCYTES; RECEPTORS, CELL SURFACE;

EID: 85065795632     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2019.03.008     Document Type: Review

References (215)

1. Vickaryous, M.K., Hall, B.K., Human cell type diversity, evolution, development, and classification with special reference to cells derived from the neural crest. Biol Rev Camb Philos Soc 81 (2006), 425–455.
2. Silverstein, A., A History of Immunology. edn 2, 2009.
3. Pasteur L: Oeuvres complètes de Louis Pasteur, réunies par Pasteur Vallery-Radot. Paris: Masson et Cie, 1922-1939.
4. Landsteiner, K., The Specificity of Serological Reactions. 1932, The Rockefeller Institute for Medical Research New York; Charles C Thomas Springfield, Illinois Baltimore Maryland.
5. Mazumdar, P.M.H., Species and Specificity. An Interpretation of the History of Immunology, 202–213, 1995, Cambridge University Press, Cambridge, 214–236.
6. Nathan, C., Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6 (2006), 173–182.
7. Mass, E., Ballesteros, I., Farlik, M., Halbritter, F., Gunther, P., Crozet, L., Jacome-Galarza, C.E., Handler, K., Klughammer, J., Kobayashi, Y., et al. Specification of tissue-resident macrophages during organogenesis. Science, 353, 2016.
8. Perdiguero, E.G., Geissmann, F., The development and maintenance of resident macrophages. Nat Immunol 17 (2016), 2–8.
9. Fearon, D.T., Locksley, R.M., The instructive role of innate immunity in the acquired immune response. Science 272 (1996), 50–53.
10. Silverstein, A.M., Cellular versus humoral immunology: a century-long dispute. Nat Immunol 4 (2003), 425–428.
11. Rota, I.A., Dhalla, F., FOXN1 deficient nude severe combined immunodeficiency. Orphanet J Rare Dis, 12, 2017, 6.
12. Mehr, S., Hsu, P., Campbell, D., Immunodeficiency in CHARGE syndrome. Am J Med Genet C Semin Med Genet 175 (2017), 516–523.
13. Bolze, A., Boisson, B., Bosch, B., Antipenko, A., Bouaziz, M., Sackstein, P., Chaker-Margot, M., Barlogis, V., Briggs, T., Colino, E., et al. Incomplete penetrance for isolated congenital asplenia in humans with mutations in translated and untranslated RPSA exons. Proc Natl Acad Sci U S A 115 (2018), E8007–E8016.
14. Borzutzky, A., Crompton, B., Bergmann, A.K., Giliani, S., Baxi, S., Martin, M., Neufeld, E.J., Notarangelo, L.D., Reversible severe combined immunodeficiency phenotype secondary to a mutation of the proton-coupled folate transporter. Clin Immunol 133 (2009), 287–294.
15. Zhao, R., Min, S.H., Qiu, A., Sakaris, A., Goldberg, G.L., Sandoval, C., Malatack, J.J., Rosenblatt, D.S., Goldman, I.D., The spectrum of mutations in the PCFT gene, coding for an intestinal folate transporter, that are the basis for hereditary folate malabsorption. Blood 110 (2007), 1147–1152.
16. Piel, F.B., Steinberg, M.H., Rees, D.C., Sickle cell disease. N Engl J Med, 377, 2017, 305.
17. Booth, C., Inusa, B., Obaro, S.K., Infection in sickle cell disease: a review. Int J Infect Dis 14 (2010), e2–e12.
18. Massip-Copiz, M.M., Santa-Coloma, T.A., Extracellular pH and lung infections in cystic fibrosis. Eur J Cell Biol 97 (2018), 402–410.
19. Kiedrowski, M.R., Bomberger, J.M., Viral-bacterial co-infections in the cystic fibrosis respiratory tract. Front Immunol, 9, 2018, 3067.
20. Lu, M., Saddi, V., Britton, P.N., Selvadurai, H., Robinson, P.D., Pandit, C., Marais, B.J., Fitzgerald, D.A., Disease caused by non-tuberculous mycobacteria in children with cystic fibrosis. Paediatr Respir Rev 29 (2019), 42–52.
21. Schwarz, C., Hartl, D., Eickmeier, O., Hector, A., Benden, C., Durieu, I., Sole, A., Gartner, S., Milla, C.E., Barry, P.J., Progress in definition, prevention and treatment of fungal infections in cystic fibrosis. Mycopathologia 183 (2018), 21–32.
22. Plasschaert, L.W., Zilionis, R., Choo-Wing, R., Savova, V., Knehr, J., Roma, G., Klein, A.M., Jaffe, A.B., A single-cell atlas of the airway epithelium reveals the CFTR-rich pulmonary ionocyte. Nature 560 (2018), 377–381.
23. Brousse, V., Buffet, P., Rees, D., The spleen and sickle cell disease: the sick(led) spleen. Br J Haematol 166 (2014), 165–176.
24. Emond, M.J., Louie, T., Emerson, J., Zhao, W., Mathias, R.A., Knowles, M.R., Wright, F.A., Rieder, M.J., Tabor, H.K., Nickerson, D.A., et al. Exome sequencing of extreme phenotypes identifies DCTN4 as a modifier of chronic Pseudomonas aeruginosa infection in cystic fibrosis. Nat Genet 44 (2012), 886–889.
25. Casanova, J.L., Abel, L., The human model: a genetic dissection of immunity to infection in natural conditions. Nat Rev Immunol 4 (2004), 55–66.
26. Quintana-Murci, L., Alcais, A., Abel, L., Casanova, J.L., Immunology in natura: clinical, epidemiological and evolutionary genetics of infectious diseases. Nat Immunol 8 (2007), 1165–1171.
27. Casanova, J.L., Abel, L., Quintana-Murci, L., Immunology taught by human genetics. Cold Spring Harb Symp Quant Biol 78 (2013), 157–172.
28. Miller, L.H., Mason, S.J., Clyde, D.F., McGinniss, M.H., The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295 (1976), 302–304.
29. Barnwell, J.W., Nichols, M.E., Rubinstein, P., In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169 (1989), 1795–1802.
30. Miller, L.H., Mason, S.J., Dvorak, J.A., McGinniss, M.H., Rothman, I.K., Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189 (1975), 561–563.
31. Tournamille, C., Colin, Y., Cartron, J.P., Le Van Kim, C., Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 10 (1995), 224–228.
32. Howes, R.E., Patil, A.P., Piel, F.B., Nyangiri, O.A., Kabaria, C.W., Gething, P.W., Zimmerman, P.A., Barnadas, C., Beall, C.M., Gebremedhin, A., et al. The global distribution of the Duffy blood group. Nat Commun, 2, 2011, 266.
33. McManus, K.F., Taravella, A.M., Henn, B.M., Bustamante, C.D., Sikora, M., Cornejo, O.E., Population genetic analysis of the DARC locus (Duffy) reveals adaptation from standing variation associated with malaria resistance in humans. PLoS Genet, 13, 2017, e1006560 Population genetic study of the DARC locus estimating the age of the most recent common ancestor carrying the most common FY*O null mutation to be ∼42 000 years. This mutation swept to fixation in Africa from a very low frequency (0.1%), with one of the strongest selection coefficients in the human genome.
34. Casanova, J.L., Abel, L., Human genetics of infectious diseases: unique insights into immunological redundancy. Semin Immunol 36 (2018), 1–12 A classification of human genes into four groups, according to their redundancy in host defense. This is of potential interest to biologists testing immunological hypotheses experimentally and physicians managing patients with immunological or infectious conditions.
35. Menard, D., Barnadas, C., Bouchier, C., Henry-Halldin, C., Gray, L.R., Ratsimbasoa, A., Thonier, V., Carod, J.F., Domarle, O., Colin, Y., et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A 107 (2010), 5967–5971.
36. Niangaly, A., Karthigayan, G., Amed, O., Coulibaly, D., Sa, J.M., Adams, M., Travassos, M.A., Ferrero, J., Laurens, M.B., Kone, A.K., et al. Plasmodium vivax Infections over 3 years in Duffy blood group negative Malians in Bandiagara, Mali. Am J Trop Med Hyg 97 (2017), 744–752.
37. Le Pendu, J., Ruvoen-Clouet, N., Kindberg, E., Svensson, L., Mendelian resistance to human norovirus infections. Semin Immunol 18 (2006), 375–386.
38. Marionneau, S., Cailleau-Thomas, A., Rocher, J., Le Moullac-Vaidye, B., Ruvoen, N., Clement, M., Le Pendu, J., ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83 (2001), 565–573.
39. Huang, P., Xia, M., Tan, M., Zhong, W., Wei, C., Wang, L., Morrow, A., Jiang, X., Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J Virol 86 (2012), 4833–4843.
40. Lindesmith, L., Moe, C., Marionneau, S., Ruvoen, N., Jiang, X., Lindblad, L., Stewart, P., LePendu, J., Baric, R., Human susceptibility and resistance to Norwalk virus infection. Nat Med 9 (2003), 548–553.
41. Thorven, M., Grahn, A., Hedlund, K.O., Johansson, H., Wahlfrid, C., Larson, G., Svensson, L., A homozygous nonsense mutation (428G→A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J Virol 79 (2005), 15351–15355.
42. Nordgren, J., Sharma, S., Bucardo, F., Nasir, W., Gunaydin, G., Ouermi, D., Nitiema, L.W., Becker-Dreps, S., Simpore, J., Hammarstrom, L., et al. Both Lewis and secretor status mediate susceptibility to rotavirus infections in a rotavirus genotype-dependent manner. Clin Infect Dis 59 (2014), 1567–1573.
43. Payne, D.C., Currier, R.L., Staat, M.A., Sahni, L.C., Selvarangan, R., Halasa, N.B., Englund, J.A., Weinberg, G.A., Boom, J.A., Szilagyi, P.G., et al. Epidemiologic association between fut2 secretor status and severe rotavirus gastroenteritis in children in the United States. JAMA Pediatr 169 (2015), 1040–1045.
44. Marionneau, S., Ruvoen, N., Le Moullac-Vaidye, B., Clement, M., Cailleau-Thomas, A., Ruiz-Palacois, G., Huang, P., Jiang, X., Le Pendu, J., Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122 (2002), 1967–1977.
45. Ma, X., Li, D.D., Sun, X.M., Guo, Y.Q., Xiang, J.Y., Wang, W.H., Zhang, L.X., Gu, Q.J., Duan, Z.J., Binding patterns of rotavirus genotypes P[4], P[6], and P[8] in China with histo-blood group antigens. PLoS One, 10, 2015, e0134584.
46. Le Pendu, J., Nystrom, K., Ruvoen-Clouet, N., Host-pathogen co-evolution and glycan interactions. Curr Opin Virol 7 (2014), 88–94.
47. Kambhampati, A., Payne, D.C., Costantini, V., Lopman, B.A., Host genetic susceptibility to enteric viruses: a systematic review and metaanalysis. Clin Infect Dis 62 (2016), 11–18.
48. Barbe, L., Le Moullac-Vaidye, B., Echasserieau, K., Bernardeau, K., Carton, T., Bovin, N., Nordgren, J., Svensson, L., Ruvoen-Clouet, N., Le Pendu, J., Histo-blood group antigen-binding specificities of human rotaviruses are associated with gastroenteritis but not with in vitro infection. Sci Rep, 8, 2018, 12961 This study shows that fucosylation is not a requirement for in vitro infection of transformed cells by P[4] and P[8] rotavirus strains, suggesting that HBGAs could enhance viral replication and development of disease but may not be essential for infection per se.
49. Zhang, D., Tan, M., Zhong, W., Xia, M., Huang, P., Jiang, X., Human intestinal organoids express histo-blood group antigens, bind norovirus VLPs, and support limited norovirus replication. Sci Rep, 7, 2017, 12621.
50. McGovern, D.P., Jones, M.R., Taylor, K.D., Marciante, K., Yan, X., Dubinsky, M., Ippoliti, A., Vasiliauskas, E., Berel, D., Derkowski, C., et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet 19 (2010), 3468–3476.
51. Takeuchi, M., Mizuki, N., Meguro, A., Ombrello, M.J., Kirino, Y., Satorius, C., Le, J., Blake, M., Erer, B., Kawagoe, T., et al. Dense genotyping of immune-related loci implicates host responses to microbial exposure in Behcet's disease susceptibility. Nat Genet 49 (2017), 438–443.
52. Santos-Cortez, R.L.P., Chiong, C.M., Frank, D.N., Ryan, A.F., Giese, A.P.J., Bootpetch Roberts, T., Daly, K.A., Steritz, M.J., Szeremeta, W., et al. FUT2 variants confer susceptibility to familial otitis media. Am J Hum Genet 103 (2018), 679–690.
53. Ferrer-Admetlla, A., Sikora, M., Laayouni, H., Esteve, A., Roubinet, F., Blancher, A., Calafell, F., Bertranpetit, J., Casals, F., A natural history of FUT2 polymorphism in humans. Mol Biol Evol 26 (2009), 1993–2003.
54. Rausch, P., Rehman, A., Kunzel, S., Hasler, R., Ott, S.J., Schreiber, S., Rosenstiel, P., Franke, A., Baines, J.F., Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci U S A 108 (2011), 19030–19035.
55. Walport, M.J., Complement. First of two parts. N Engl J Med 344 (2001), 1058–1066.
56. Alper, C.A., Abramson, N., Johnston, R.B. Jr., Jandl, J.H., Rosen, F.S., Increased susceptibility to infection associated with abnormalities of complement-mediated functions and of the third component of complement (C3). N Engl J Med 282 (1970), 349–354.
57. Miller, M.E., Seals, J., Kaye, R., Levitsky, L.C., A familial, plasma associated defect of phagocytosis: a new cause of recurrent bacterial infections. Lancet ii (1968), 60–63.
58. Figueroa, J.E., Densen, P., Infectious diseases associated with complement deficiencies. Clin Microbiol Rev 4 (1991), 359–395.
59. Ram, S., Lewis, L.A., Rice, P.A., Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin Microbiol Rev 23 (2010), 740–780.
60. Klemperer, M.R., Woodworth, H.C., Rosen, F.S., Austen, K.F., Hereditary deficiency of the second component of complement (C’2) in man. J Clin Invest 45 (1966), 880–890.
61. Klemperer, M.R., Austen, K.F., Rosen, F.S., Hereditary deficiency of the second component of complement (C’2) in man: further observations on a second kindred. J Immunol 98 (1967), 72–78.
62. Sarma, J.V., Ward, P.A., The complement system. Cell Tissue Res 343 (2011), 227–235.
63. Hajishengallis, G., Reis, E.S., Mastellos, D.C., Ricklin, D., Lambris, J.D., Novel mechanisms and functions of complement. Nat Immunol 18 (2017), 1288–1298 A comprehensive review of recent advances in the field of complement. It provides an updated view of new and previously unanticipated functions of complement in health and disease.
64. Alper, C.A., Johnson, A.M., Birtch, A.G., Moore, F.D., Human C’3: evidence for the liver as the primary site of synthesis. Science 163 (1969), 286–288.
65. Morris, K.M., Aden, D.P., Knowles, B.B., Colten, H.R., Complement biosynthesis by the human hepatoma-derived cell line HepG2. J Clin Invest 70 (1982), 906–913.
66. Perlmutter, D.H., Colten, H.R., Molecular immunobiology of complement biosynthesis: a model of single-cell control of effector-inhibitor balance. Annu Rev Immunol 4 (1986), 231–251.
67. Baumann, H., Richards, C., Gauldie, J., Interaction among hepatocyte-stimulating factors, interleukin 1, and glucocorticoids for regulation of acute phase plasma proteins in human hepatoma (HepG2) cells. J Immunol 139 (1987), 4122–4128.
68. Mier, J.W., Dinarello, C.A., Atkins, M.B., Punsal, P.I., Perlmutter, D.H., Regulation of hepatic acute phase protein synthesis by products of interleukin 2 (IL 2)-stimulated human peripheral blood mononuclear cells. J Immunol 139 (1987), 1268–1272.
69. Morgan, B.P., Gasque, P., Extrahepatic complement biosynthesis: where, when and why?. Clin Exp Immunol 107 (1997), 1–7.
70. Tenner, A.J., Volkin, D.B., Complement subcomponent C1q secreted by cultured human monocytes has subunit structure identical with that of serum C1q. Biochem J 233 (1986), 451–458.
71. Gulati, P., Lemercier, C., Guc, D., Lappin, D., Whaley, K., Regulation of the synthesis of C1 subcomponents and C1-inhibitor. Behring Inst Mitt, 1993, 196–203.
72. Choy, L.N., Rosen, B.S., Spiegelman, B.M., Adipsin and an endogenous pathway of complement from adipose cells. J Biol Chem 267 (1992), 12736–12741.
73. White, R.T., Damm, D., Hancock, N., Rosen, B.S., Lowell, B.B., Usher, P., Flier, J.S., Spiegelman, B.M., Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue. J Biol Chem 267 (1992), 9210–9213.
74. Maves, K.K., Weiler, J.M., Properdin: approaching four decades of research. Immunol Res 12 (1993), 233–243.
75. Wurzner, R., Joysey, V.C., Lachmann, P.J., Complement component C7. Assessment of in vivo synthesis after liver transplantation reveals that hepatocytes do not synthesize the majority of human C7. J Immunol 152 (1994), 4624–4629.
76. Alper, C.A., Raum, D., Awdeh, Z.L., Petersen, B.H., Taylor, P.D., Starzl, T.E., Studies of hepatic synthesis in vivo of plasma proteins, including orosomucoid, transferrin, alpha 1-antitrypsin, C8, and factor B. Clin Immunol Immunopathol 16 (1980), 84–89.
77. Ross, S.C., Densen, P., Complement deficiency states and infection: epidemiology, pathogenesis and consequences of neisserial and other infections in an immune deficiency. Medicine (Baltimore) 63 (1984), 243–273.
78. Schur, P.H., Inherited complement component abnormalities. Annu Rev Med 37 (1986), 333–346.
79. Schifferli, J.A., Peters, D.K., Complement, the immune-complex lattice, and the pathophysiology of complement-deficiency syndromes. Lancet 2 (1983), 957–959.
80. Hannema, A.J., Kluin-Nelemans, J.C., Hack, C.E., Eerenberg-Belmer, A.J., Mallee, C., van Helden, H.P., SLE like syndrome and functional deficiency of C1q in members of a large family. Clin Exp Immunol 55 (1984), 106–114.
81. Meyer, O., Hauptmann, G., Tappeiner, G., Ochs, H.D., Mascart-Lemone, F., Genetic deficiency of C4, C2 or C1q and lupus syndromes. Association with anti-Ro (SS-A) antibodies. Clin Exp Immunol 62 (1985), 678–684.
82. Gelfand, E.W., Rao, C.P., Minta, J.O., Ham, T., Purkall, D.B., Ruddy, S., Inherited deficiency of properdin and C2 in a patient with recurrent bacteremia. Am J Med 82 (1987), 671–675.
83. Sjoholm, A.G., Hallberg, T., Oxelius, V.A., Hammarstrom, L., Smith, C.I., Lindgren, F., C2 deficiency, moderately low IgG2 concentrations and lack of the G2m(23) allotype marker in a child with repeated bacterial infections. Acta Paediatr Scand 76 (1987), 533–538.
84. Hauptmann, G., Goetz, J., Uring-Lambert, B., Grosshans, E., Component deficiencies. 2. The fourth component. Prog Allergy 39 (1986), 232–249.
85. Uring-Lambert, B., Mascart-Lemone, F., Tongio, M.M., Goetz, J., Hauptmann, G., Molecular basis of complete C4 deficiency. A study of three patients. Hum Immunol 24 (1989), 125–132.
86. Grumach, A.S., Vilela, M.M., Gonzalez, C.H., Starobinas, N., Pereira, A.B., Dias-da-Silva, W., Carneiro-Sampaio, M.M., Inherited C3 deficiency of the complement system. Braz J Med Biol Res 21 (1988), 247–257.
87. Fijen, C.A., Kuijper, E.J., Hannema, A.J., Sjoholm, A.G., van Putten, J.P., Complement deficiencies in patients over ten years old with meningococcal disease due to uncommon serogroups. Lancet 2 (1989), 585–588.
88. Botto, M., Fong, K.Y., So, A.K., Rudge, A., Walport, M.J., Molecular basis of hereditary C3 deficiency. J Clin Invest 86 (1990), 1158–1163.
89. Borzy, M.S., Houghton, D., Mixed-pattern immune deposit glomerulonephritis in a child with inherited deficiency of the third component of complement. Am J Kidney Dis 5 (1985), 54–59.
90. Barrett, D.J., Boyle, M.D., Restoration of complement function in vivo by plasma infusion in factor I (C3b inactivator) deficiency. J Pediatr 104 (1984), 76–81.
91. Rasmussen, J.M., Teisner, B., Brandslund, I., Svehag, S.E., A family with complement factor I deficiency. Scand J Immunol 23 (1986), 711–715.
92. Nielsen, H.E., Christensen, K.C., Koch, C., Thomsen, B.S., Heegaard, N.H., Tranum-Jensen, J., Hereditary, complete deficiency of complement factor H associated with recurrent meningococcal disease. Scand J Immunol 30 (1989), 711–718.
93. Alper, C.A., Colten, H.R., Rosen, F.S., Rabson, A.R., Macnab, G.M., Gear, J.S., Homozygous deficiency of C3 in a patient with repeated infections. Lancet 2 (1972), 1179–1181.
94. Botto, M., Fong, K.Y., So, A.K., Barlow, R., Routier, R., Morley, B.J., Walport, M.J., Homozygous hereditary C3 deficiency due to a partial gene deletion. Proc Natl Acad Sci U S A 89 (1992), 4957–4961.
95. Wang, X., Fleischer, D.T., Whitehead, W.T., Haviland, D.L., Rosenfeld, S.I., Leddy, J.P., Snyderman, R., Wetsel, R.A., Inherited human complement C5 deficiency. Nonsense mutations in exons 1 (Gln1 to Stop) and 36 (Arg1458 to Stop) and compound heterozygosity in three African-American families. J Immunol 154 (1995), 5464–5471.
96. Wurzner, R., Hobart, M.J., Fernie, B.A., Mewar, D., Potter, P.C., Orren, A., Lachmann, P.J., Molecular basis of subtotal complement C6 deficiency. A carboxy-terminally truncated but functionally active C6. J Clin Invest 95 (1995), 1877–1883.
97. Kaufmann, T., Hansch, G., Rittner, C., Spath, P., Tedesco, F., Schneider, P.M., Genetic basis of human complement C8 beta deficiency. J Immunol 150 (1993), 4943–4947.
98. Kojima, T., Horiuchi, T., Nishizaka, H., Fukumori, Y., Amano, T., Nagasawa, K., Niho, Y., Hayashi, K., Genetic basis of human complement C8 alpha-gamma deficiency. J Immunol 161 (1998), 3762–3766.
99. Westberg, J., Fredrikson, G.N., Truedsson, L., Sjoholm, A.G., Uhlen, M., Sequence-based analysis of properdin deficiency: identification of point mutations in two phenotypic forms of an X-linked immunodeficiency. Genomics 29 (1995), 1–8.
100. Biesma, D.H., Hannema, A.J., van Velzen-Blad, H., Mulder, L., van Zwieten, R., Kluijt, I., Roos, D., A family with complement factor D deficiency. J Clin Invest 108 (2001), 233–240.
101. Lim, D., Gewurz, A., Lint, T.F., Ghaze, M., Sepheri, B., Gewurz, H., Absence of the sixth component of complement in a patient with repeated episodes of meningococcal meningitis. J Pediatr 89 (1976), 42–47.
102. Petersen, B.H., Graham, J.A., Brooks, G.F., Human deficiency of the eighth component of complement. The requirement of C8 for serum Neisseria gonorrhoeae bactericidal activity. J Clin Invest 57 (1976), 283–290.
103. Hiemstra, P.S., Langeler, E., Compier, B., Keepers, Y., Leijh, P.C., van den Barselaar, M.T., Overbosch, D., Daha, M.R., Complete and partial deficiencies of complement factor D in a Dutch family. J Clin Invest 84 (1989), 1957–1961.
104. Rosenfeld, S.I., Kelly, M.E., Leddy, J.P., Hereditary deficiency of the fifth component of complement in man. I. Clinical, immunochemical, and family studies. J Clin Invest 57 (1976), 1626–1634.
105. Harriman, G.R., Esser, A.F., Podack, E.R., Wunderlich, A.C., Braude, A.I., Lint, T.F., Curd, J.G., The role of C9 in complement-mediated killing of Neisseria. J Immunol 127 (1981), 2386–2390.
106. Snyderman, R., Durack, D.T., McCarty, G.A., Ward, F.E., Meadows, L., Deficiency of the fifth component of complement in human subjects. Clinical, genetic and immunologic studies in a large kindred. Am J Med 67 (1979), 638–645.
107. Lee, T.J., Utsinger, P.D., Snyderman, R., Yount, W.J., Sparling, P.F., Familial deficiency of the seventh component of complement associated with recurrent bacteremic infections due to Neisseria. J Infect Dis 138 (1978), 359–368.
108. Sjoholm, A.G., Braconier, J.H., Soderstrom, C., Properdin deficiency in a family with fulminant meningococcal infections. Clin Exp Immunol 50 (1982), 291–297.
109. Owen, E.P., Wurzner, R., Leisegang, F., Rizkallah, P., Whitelaw, A., Simpson, J., Thomas, A.D., Harris, C.L., Giles, J.L., Hellerud, B.C., et al. A complement C5 gene mutation, c.754G>A:p.A252T, is common in the Western Cape, South Africa and found to be homozygous in seven percent of Black African meningococcal disease cases. Mol Immunol 64 (2015), 170–176.
110. Nishizaka, H., Horiuchi, T., Zhu, Z.B., Fukumori, Y., Volanakis, J.E., Genetic bases of human complement C7 deficiency. J Immunol 157 (1996), 4239–4243.
111. Nagata, M., Hara, T., Aoki, T., Mizuno, Y., Akeda, H., Inaba, S., Tsumoto, K., Ueda, K., Inherited deficiency of ninth component of complement: an increased risk of meningococcal meningitis. J Pediatr 114 (1989), 260–264.
112. Petersen, B.H., Lee, T.J., Snyderman, R., Brooks, G.F., Neisseria meningitidis and Neisseria gonorrhoeae bacteremia associated with C6, C7, or C8 deficiency. Ann Intern Med 90 (1979), 917–920.
113. Page, N.M., Butlin, D.J., Lomthaisong, K., Lowry, P.J., The human apolipoprotein L gene cluster: identification, classification, and sites of distribution. Genomics 74 (2001), 71–78.
114. Duchateau, P.N., Pullinger, C.R., Orellana, R.E., Kunitake, S.T., Naya-Vigne, J., O'Connor, P.M., Malloy, M.J., Kane, J.P., Apolipoprotein L, a new human high density lipoprotein apolipoprotein expressed by the pancreas. Identification, cloning, characterization, and plasma distribution of apolipoprotein L. J Biol Chem 272 (1997), 25576–25582.
115. Duchateau, P.N., Pullinger, C.R., Cho, M.H., Eng, C., Kane, J.P., Apolipoprotein L gene family: tissue-specific expression, splicing, promoter regions; discovery of a new gene. J Lipid Res 42 (2001), 620–630.
116. Vanhollebeke, B., Truc, P., Poelvoorde, P., Pays, A., Joshi, P.P., Katti, R., Jannin, J.G., Pays, E., Human Trypanosoma evansi infection linked to a lack of apolipoprotein L-I. N Engl J Med 355 (2006), 2752–2756.
117. Fontaine, F., Lecordier, L., Vanwalleghem, G., Uzureau, P., Van Reet, N., Fontaine, M., Tebabi, P., Vanhollebeke, B., Buscher, P., Perez-Morga, D., et al. APOLs with low pH dependence can kill all African trypanosomes. Nat Microbiol 2 (2017), 1500–1506 This study shows that the difference in trypanolytic activity between recombinant APOL3 and APOL1 is accounted for by their different dependence on acidic pH.
118. Pays, E., Vanhollebeke, B., Uzureau, P., Lecordier, L., Perez-Morga, D., The molecular arms race between African trypanosomes and humans. Nat Rev Microbiol 12 (2014), 575–584.
119. Vanhamme, L., Paturiaux-Hanocq, F., Poelvoorde, P., Nolan, D.P., Lins, L., Van Den Abbeele, J., Pays, A., Tebabi, P., Van Xong, H., Jacquet, A., et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422 (2003), 83–87.
120. Perez-Morga, D., Vanhollebeke, B., Paturiaux-Hanocq, F., Nolan, D.P., Lins, L., Homble, F., Vanhamme, L., Tebabi, P., Pays, A., Poelvoorde, P., et al. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309 (2005), 469–472.
121. Kennedy, P.G., Human African trypanosomiasis of the CNS: current issues and challenges. J Clin Invest 113 (2004), 496–504.
122. Chappuis, F., Loutan, L., Simarro, P., Lejon, V., Buscher, P., Options for field diagnosis of human African trypanosomiasis. Clin Microbiol Rev 18 (2005), 133–146.
123. Checchi, F., Filipe, J.A., Barrett, M.P., Chandramohan, D., The natural progression of Gambiense sleeping sickness: what is the evidence?. PLoS Negl Trop Dis, 2, 2008, e303.
124. Uzureau, P., Uzureau, S., Lecordier, L., Fontaine, F., Tebabi, P., Homble, F., Grelard, A., Zhendre, V., Nolan, D.P., Lins, L., et al. Mechanism of Trypanosoma brucei gambiense resistance to human serum. Nature 501 (2013), 430–434.
125. Xong, H.V., Vanhamme, L., Chamekh, M., Chimfwembe, C.E., Van Den Abbeele, J., Pays, A., Van Meirvenne, N., Hamers, R., De Baetselier, P., Pays, E., A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95 (1998), 839–846.
126. Genovese, G., Friedman, D.J., Ross, M.D., Lecordier, L., Uzureau, P., Freedman, B.I., Bowden, D.W., Langefeld, C.D., Oleksyk, T.K., Uscinski Knob, A.L., et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329 (2010), 841–845.
127. Cooper, A., Ilboudo, H., Alibu, V.P., Ravel, S., Enyaru, J., Weir, W., Noyes, H., Capewell, P., Camara, M., Milet, J., et al. APOL1 renal risk variants have contrasting resistance and susceptibility associations with African trypanosomiasis. eLife, 6, 2017.
128. Lowy, D.R., Peter, M., et al. Papillomaviruses. Knipe, D.M., Howley, P.M., Griffin, D.E., Lamb, R.A., Martin, M.A., Roizman, B., (eds.) Fields Virology, edn 4, 2001, Lippincott Williams & Wilkins, Philadelphia, 2231–2246.
129. Orth, G., Papillomaviruses-human (Papovaviridae). General features. Granoff, A., Webster, R.G., (eds.) Encyclopedia of Virology, edn 2, 1999, Academic Press, London, 1105–1114.
130. Casanova, J.L., Severe infectious diseases of childhood as monogenic inborn errors of immunity. Proc Natl Acad Sci U S A 112 (2015), E7128–7137.
131. Casanova, J.L., Human genetic basis of interindividual variability in the course of infection. Proc Natl Acad Sci U S A 112 (2015), E7118–E7127.
132. Orth, G., Genetics of epidermodysplasia verruciformis: insights into host defense against papillomaviruses. Semin Immunol 18 (2006), 362–374.
133. Lewandowsky, F., Lutz, W., Ein Fall einer bisher nicht beschriebenen Hauterkrankung (Epidermodysplasia verruciformis). Arch Dermatol Syphilol 141 (1922), 193–203.
134. Cockayne, E., Inherited Abnormalities of the Skin and its Appendages. 1933, Oxford University Press, London.
135. Lutz, W., A propos de l’épidermodysplasie verruciforme. Dermatologica, 1946, 30–43.
136. Lutzner, M.A., Epidermodysplasia verruciformis. An autosomal recessive disease characterized by viral warts and skin cancer. A model for viral oncogenesis. Bull Cancer, 1978, 169–182.
137. Burger, B., Itin, P.H., Epidermodysplasia verruciformis. Curr Probl Dermatol 45 (2014), 123–131.
138. Orth, G., Host defenses against human papillomaviruses: lessons from epidermodysplasia verruciformis. Curr Top Microbiol Immunol 321 (2008), 59–83.
139. de Jong, S.J., Imahorn, E., Itin, P., Uitto, J., Orth, G., Jouanguy, E., Casanova, J.L., Burger, B., Epidermodysplasia verruciformis: inborn errors of immunity to human beta-papillomaviruses. Front Microbiol, 9, 2018, 1222.
140. Huang, S., Wu, J.H., Lewis, D.J., Rady, P.L., Tyring, S.K., A novel approach to the classification of epidermodysplasia verruciformis. Int J Dermatol 57 (2018), 1344–1350.
141. Orth, G., Jablonska, S., Breitburd, F., Favre, M., Croissant, O., The human papillomaviruses. Bull Cancer 65 (1978), 151–164.
142. Antonsson, A., Erfurt, C., Hazard, K., Holmgren, V., Simon, M., Kataoka, A., Hossain, S., Hakangard, C., Hansson, B.G., Prevalence and type spectrum of human papillomaviruses in healthy skin samples collected in three continents. J Gen Virol 84 (2003), 1881–1886.
143. Antonsson, A., Karanfilovska, S., Lindqvist, P.G., Hansson, B.G., General acquisition of human papillomavirus infections of skin occurs in early infancy. J Clin Microbiol 41 (2003), 2509–2514.
144. Youssefian, L., Vahidnezhad, H., Mahmoudi, H., Saeidian, A.H., Daneshpazhooh, M., Kamyab Hesari, K., Zeinali, S., de Jong, S.J., Orth, G., Blanchet-Bardon, C., et al. Epidermodysplasia verruciformis: genetic heterogeneity and EVER1 and EVER2 mutations revealed by genome-wide analysis. J Invest Dermatol 139 (2019), 241–244.
145. Ramoz, N., Rueda, L.A., Bouadjar, B., Montoya, L.S., Orth, G., Favre, M., Mutations in two adjacent novel genes are associated with epidermodysplasia verruciformis. Nat Genet 32 (2002), 579–581.
146. Ramoz, N., Taieb, A., Rueda, L.A., Montoya, L.S., Bouadjar, B., Favre, M., Orth, G., Evidence for a nonallelic heterogeneity of epidermodysplasia verruciformis with two susceptibility loci mapped to chromosome regions 2p21-p24 and 17q. J Invest Dermatol 114 (2000), 1148–1153.
147. Arnold, A.W., Burger, B., Kump, E., Rufle, A., Tyring, S.K., Kempf, W., Hausermann, P., Itin, P.H., Homozygosity for the c.917A→T (p.N306l) polymorphism in the EVER2/TMC8 gene of two sisters with epidermodysplasia verruciformis Lewandowsky-Lutz originally described by Wilhelm Lutz. Dermatology 222 (2011), 81–86.
148. Imahorn, E., Yuksel, Z., Spoerri, I., Gurel, G., Imhof, C., Saracoglu, Z.N., Koku Aksu, A.E., Rady, P.L., Tyring, S.K., Kempf, W., et al. Novel TMC8 splice site mutation in epidermodysplasia verruciformis and review of HPV infections in patients with the disease. J Eur Acad Dermatol Venereol 31 (2017), 1722–1726.
149. Landini, M.M., Zavattaro, E., Borgogna, C., Azzimonti, B., De Andrea, M., Colombo, E., Marenco, F., Amantea, A., Landolfo, S., Gariglio, M., Lack of EVER2 protein in two epidermodysplasia verruciformis patients with skin cancer presenting previously unreported homozygous genetic deletions in the EVER2 gene. J Invest Dermatol 132 (2012), 1305–1308.
150. Crequer, A., Picard, C., Pedergnana, V., Lim, A., Zhang, S.Y., Abel, L., Majewski, S., Casanova, J.L., Jablonska, S., Orth, G., et al. EVER2 deficiency is associated with mild T-cell abnormalities. J Clin Immunol 33 (2013), 14–21.
151. Lazarczyk, M., Dalard, C., Hayder, M., Dupre, L., Pignolet, B., Majewski, S., Vuillier, F., Favre, M., Liblau, R.S., EVER proteins, key elements of the natural anti-human papillomavirus barrier, are regulated upon T-cell activation. PLoS One, 7, 2012, e39995.
152. Laffort, C., Le Deist, F., Favre, M., Caillat-Zucman, S., Radford-Weiss, I., Debre, M., Fraitag, S., Blanche, S., Cavazzana-Calvo, M., de Saint Basile, G., et al. Severe cutaneous papillomavirus disease after haemopoietic stem-cell transplantation in patients with severe combined immune deficiency caused by common gammac cytokine receptor subunit or JAK-3 deficiency. Lancet 363 (2004), 2051–2054.
153. Gaspar, H.B., Harwood, C., Leigh, I., Thrasher, A.J., Severe cutaneous papillomavirus disease after haematopoietic stem-cell transplantation in patients with severe combined immunodeficiency. Br J Haematol 127 (2004), 232–233.
154. de Jong, S.J., Crequer, A., Matos, I., Hum, D., Gunasekharan, V., Lorenzo, L., Jabot-Hanin, F., Imahorn, E., Arias, A.A., Vahidnezhad, H., et al. The human CIB1-EVER1-EVER2 complex governs keratinocyte-intrinsic immunity to beta-papillomaviruses. J Exp Med 215 (2018), 2289–2310 This report of autosomal recessive CIB1 deficiency, a novel genetic etiology of isolated epidermodysplasia verruciformis, clinically indistinguishable from EVER1 and EVER2 deficiency, suggests that the disruption of CIB1–EVER1–EVER2-dependent keratinocyte-intrinsic immunity underlies the selective susceptibility of these patients to β-human papillomaviruses.
155. Vahidnezhad, H., Youssefian, L., Saeidian, A.H., Mansoori, B., Jazayeri, A., Azizpour, A., Kamyab Hesari, K., Yousefi, M., Zeinali, S., Jouanguy, E., et al. A CIB1 splice-site founder mutation in families with typical epidermodysplasia verruciformis. J Invest Dermatol 139 (2019), 1195–1198.
156. Leisner, T.M., Freeman, T.C., Black, J.L., Parise, L.V., CIB1: a small protein with big ambitions. FASEB J 30 (2016), 2640–2650.
157. Yuan, W., Leisner, T.M., McFadden, A.W., Clark, S., Hiller, S., Maeda, N., O'Brien, D.A., Parise, L.V., CIB1 is essential for mouse spermatogenesis. Mol Cell Biol 26 (2006), 8507–8514.
158. Naik, M.U., Nigam, A., Manrai, P., Millili, P., Czymmek, K., Sullivan, M., Naik, U.P., CIB1 deficiency results in impaired thrombosis: the potential role of CIB1 in outside-in signaling through integrin alpha IIb beta 3. J Thromb Haemost 7 (2009), 1906–1914.
159. Heineke, J., Auger-Messier, M., Correll, R.N., Xu, J., Benard, M.J., Yuan, W., Drexler, H., Parise, L.V., Molkentin, J.D., CIB1 is a regulator of pathological cardiac hypertrophy. Nat Med 16 (2010), 872–879.
160. Zayed, M.A., Yuan, W., Leisner, T.M., Chalothorn, D., McFadden, A.W., Schaller, M.D., Hartnett, M.E., Faber, J.E., Parise, L.V., CIB1 regulates endothelial cells and ischemia-induced pathological and adaptive angiogenesis. Circ Res 101 (2007), 1185–1193.
161. Lazarczyk, M., Pons, C., Mendoza, J.A., Cassonnet, P., Jacob, Y., Favre, M., Regulation of cellular zinc balance as a potential mechanism of EVER-mediated protection against pathogenesis by cutaneous oncogenic human papillomaviruses. J Exp Med 205 (2008), 35–42.
162. Vuillier, F., Gaud, G., Guillemot, D., Commere, P.H., Pons, C., Favre, M., Loss of the HPV-infection resistance EVER2 protein impairs NF-kappaB signaling pathways in keratinocytes. PLoS One, 9, 2014, e89479.
163. Gaud, G., Guillemot, D., Jacob, Y., Favre, M., Vuillier, F., EVER2 protein binds TRADD to promote TNF-alpha-induced apoptosis. Cell Death Dis, 4, 2013, e499.
164. Bieniasz, P.D., Intrinsic immunity: a front-line defense against viral attack. Nat Immunol 5 (2004), 1109–1115.
165. Randow, F., MacMicking, J.D., James, L.C., Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340 (2013), 701–706.
166. Yan, N., Chen, Z.J., Intrinsic antiviral immunity. Nat Immunol 13 (2012), 214–222.
167. MacMicking, J.D., Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat Rev Immunol 12 (2012), 367–382.
168. Taubenberger, J.K., Hultin, J.V., Morens, D.M., Discovery and characterization of the 1918 pandemic influenza virus in historical context. Antivir Ther 12 (2007), 581–591.
169. Ciancanelli, M.J., Abel, L., Zhang, S.Y., Casanova, J.L., Host genetics of severe influenza: from mouse Mx1 to human IRF7. Curr Opin Immunol 38 (2016), 109–120.
170. Nair, H., Brooks, W.A., Katz, M., Roca, A., Berkley, J.A., Madhi, S.A., Simmerman, J.M., Gordon, A., Sato, M., Howie, S., et al. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet 378 (2011), 1917–1930.
171. Short, K.R., Kroeze, E., Fouchier, R.A.M., Kuiken, T., Pathogenesis of influenza-induced acute respiratory distress syndrome. Lancet Infect Dis 14 (2014), 57–69.
172. Skalka, A.M., Flint, S.J., Enquist, L.W., Racaniello, V.R., Principles of Virology. edn 4, 2015.
173. Picard, C., Bobby Gaspar, H., Al-Herz, W., Bousfiha, A., Casanova, J.L., Chatila, T., Crow, Y.J., Cunningham-Rundles, C., Etzioni, A., Franco, J.L., et al. International Union of Immunological Societies: 2017 primary immunodeficiency diseases committee report on inborn errors of immunity. J Clin Immunol 38 (2018), 96–128 This is the report of the classification of human inborn errors of immunity by the international committee of the IUIS.
174. Haller, O., Arnheiter, H., Pavlovic, J., Staeheli, P., The discovery of the antiviral resistance gene Mx: a story of great ideas, great failures, and some success. Annu Rev Virol 5 (2018), 33–51 A comprehensive review of the Mx-influenza saga, from the 1960s onward, by its main characters, who discovered the underlying gene and deciphered its mechanism of action.
175. Bigley, V., Haniffa, M., Doulatov, S., Wang, X.N., Dickinson, R., McGovern, N., Jardine, L., Pagan, S., Dimmick, I., Chua, I., et al. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J Exp Med 208 (2011), 227–234.
176. Sologuren, I., Martinez-Saavedra, M.T., Sole-Violan, J., de Borges de Oliveira, E. Jr., Betancor, E., Casas, I., Oleaga-Quintas, C., Martinez-Gallo, M., Zhang, S.Y., Pestano, J., et al. Lethal influenza in two related adults with inherited GATA2 deficiency. J Clin Immunol 38 (2018), 513–526.
177. Ciancanelli, M.J., Huang, S.X., Luthra, P., Garner, H., Itan, Y., Volpi, S., Lafaille, F.G., Trouillet, C., Schmolke, M., Albrecht, R.A., et al. Infectious disease. Life-threatening influenza and impaired interferon amplification in human IRF7 deficiency. Science 348 (2015), 448–453.
178. Hernandez, N., Melki, I., Jing, H., Habib, T., Huang, S.S.Y., Danielson, J., Kula, T., Drutman, S., Belkaya, S., Rattina, V., et al. Life-threatening influenza pneumonitis in a child with inherited IRF9 deficiency. J Exp Med 215 (2018), 2567–2585 Autosomal recessive IRF9 deficiency is the second genetic etiology of severe influenza pneumonitis in children. Cells from the patient do not activate IRF9-dependent and ISGF3-dependent genes in response to type I and III IFNs, thereby failing to control influenza virus in vitro and in vivo.
179. Duncan, C.J., Mohamad, S.M., Young, D.F., Skelton, A.J., Leahy, T.R., Munday, D.C., Butler, K.M., Morfopoulou, S., Brown, J.R., Hubank, M., et al. Human IFNAR2 deficiency: Lessons for antiviral immunity. Sci Transl Med, 7, 2015, 307ra154.
180. Dupuis, S., Jouanguy, E., Al-Hajjar, S., Fieschi, C., Al-Mohsen, I.Z., Al-Jumaah, S., Yang, K., Chapgier, A., Eidenschenk, C., Eid, P., et al. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat Genet 33 (2003), 388–391.
181. Averbuch, D., Chapgier, A., Boisson-Dupuis, S., Casanova, J.L., Engelhard, D., The clinical spectrum of patients with deficiency of signal transducer and activator of transcription-1. Pediatr Infect Dis J 30 (2011), 352–355.
182. Boisson-Dupuis, S., Kong, X.F., Okada, S., Cypowyj, S., Puel, A., Abel, L., Casanova, J.L., Inborn errors of human STAT1: allelic heterogeneity governs the diversity of immunological and infectious phenotypes. Curr Opin Immunol 24 (2012), 364–378.
183. Burns, C., Cheung, A., Stark, Z., Choo, S., Downie, L., White, S., Conyers, R., Cole, T., A novel presentation of homozygous loss-of-function STAT-1 mutation in an infant with hyperinflammation-A case report and review of the literature. J Allergy Clin Immunol Pract 4 (2016), 777–779.
184. Hambleton, S., Goodbourn, S., Young, D.F., Dickinson, P., Mohamad, S.M., Valappil, M., McGovern, N., Cant, A.J., Hackett, S.J., Ghazal, P., et al. STAT2 deficiency and susceptibility to viral illness in humans. Proc Natl Acad Sci U S A 110 (2013), 3053–3058.
185. Moens, L., Van Eyck, L., Jochmans, D., Mitera, T., Frans, G., Bossuyt, X., Matthys, P., Neyts, J., Ciancanelli, M., Zhang, S.Y., et al. A novel kindred with inherited STAT2 deficiency and severe viral illness. J Allergy Clin Immunol 139 (2017), 1995–1997 e1999.
186. Hernandez, N., Moens, L., Le Pen, J., Goudouris, E., Habib, T., Shirkani, A., Changi-Ashtiani, M., Rokni-Zadeh, H., Zijlmans, D., Jurado, A., et al. Inherited IFNAR1 deficiency in otherwise healthy patients with adverse reaction to measles and yellow fever live vaccines. J Exp Med, 2019 in press.
187. Swanson, P.A. 2nd, McGavern, D.B., Viral diseases of the central nervous system. Curr Opin Virol 11 (2015), 44–54.
188. Casanova, J.L., Abel, L., The genetic theory of infectious diseases: brief history and selected illustrations. Annu Rev Genome Hum Genet 14 (2013), 215–243.
189. Casrouge, A., Zhang, S.Y., Eidenschenk, C., Jouanguy, E., Puel, A., Yang, K., Alcais, A., Picard, C., Mahfoufi, N., Nicolas, N., et al. Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314 (2006), 308–312.
190. Guo, Y., Audry, M., Ciancanelli, M., Alsina, L., Azevedo, J., Herman, M., Anguiano, E., Sancho-Shimizu, V., Lorenzo, L., Pauwels, E., et al. Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity. J Exp Med 208 (2011), 2083–2098.
191. Herman, M., Ciancanelli, M., Ou, Y.H., Lorenzo, L., Klaudel-Dreszler, M., Pauwels, E., Sancho-Shimizu, V., Perez de Diego, R., Abhyankar, A., Israelsson, E., et al. Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J Exp Med 209 (2012), 1567–1582.
192. Perez de Diego, R., Sancho-Shimizu, V., Lorenzo, L., Puel, A., Plancoulaine, S., Picard, C., Herman, M., Cardon, A., Durandy, A., Bustamante, J., et al. Human TRAF3 adaptor molecule deficiency leads to impaired toll-like receptor 3 response and susceptibility to herpes simplex encephalitis. Immunity 33 (2010), 400–411.
193. Sancho-Shimizu, V., Perez de Diego, R., Lorenzo, L., Halwani, R., Alangari, A., Israelsson, E., Fabrega, S., Cardon, A., Maluenda, J., Tatematsu, M., et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 121 (2012), 4889–4902.
194. Zhang, S.Y., Jouanguy, E., Ugolini, S., Smahi, A., Elain, G., Romero, P., Segal, D., Sancho-Shimizu, V., Lorenzo, L., Puel, A., et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 317 (2007), 1522–1527.
195. Lim, H.K., Seppanen, M., Hautala, T., Ciancanelli, M.J., Itan, Y., Lafaille, F.G., Dell, W., Lorenzo, L., Byun, M., Pauwels, E., et al. TLR3 deficiency in herpes simplex encephalitis: high allelic heterogeneity and recurrence risk. Neurology 83 (2014), 1888–1897.
196. Lafaille, F.G., Pessach, I.M., Zhang, S.Y., Ciancanelli, M.J., Herman, M., Abhyankar, A., Ying, S.W., Keros, S., Goldstein, P.A., Mostoslavsky, G., et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 491 (2012), 769–793.
197. Andersen, L.L., Mork, N., Reinert, L.S., Kofod-Olsen, E., Narita, R., Jorgensen, S.E., Skipper, K.A., Honing, K., Gad, H.H., Ostergaard, L., et al. Functional IRF3 deficiency in a patient with herpes simplex encephalitis. J Exp Med 212 (2015), 1371–1379.
198. Zhang, S.Y., Casanova, J.L., Inborn errors underlying herpes simplex encephalitis: from TLR3 to IRF3. J Exp Med 212 (2015), 1342–1343.
199. Chapgier, A., Wynn, R.F., Jouanguy, E., Filipe-Santos, O., Zhang, S., Feinberg, J., Hawkins, K., Casanova, J.L., Arkwright, P.D., Human complete Stat-1 deficiency is associated with defective type I and II IFN responses in vitro but immunity to some low virulence viruses in vivo. J Immunol 176 (2006), 5078–5083.
200. Chapgier, A., Kong, X.F., Boisson-Dupuis, S., Jouanguy, E., Averbuch, D., Feinberg, J., Zhang, S.Y., Bustamante, J., Vogt, G., Lejeune, J., et al. A partial form of recessive STAT1 deficiency in humans. J Clin Invest 119 (2009), 1502–1514.
201. Niehues, T., Reichenbach, J., Neubert, J., Gudowius, S., Puel, A., Horneff, G., Lainka, E., Dirksen, U., Schroten, H., Döffinger, R., et al. A NEMO-deficient child with immunodeficiency yet without anhidrotic ectodermal dysplasia. J Allergy Clin Immunol 114 (2004), 1456–1462.
202. Puel, A., Reichenbach, J., Bustamante, J., Ku, C.L., Feinberg, J., Doffinger, R., Bonnet, M., Filipe-Santos, O., Beaucoudrey, L., Durandy, A., et al. The NEMO mutation creating the most-upstream premature stop codon is hypomorphic because of a reinitiation of translation. Am J Hum Genet 78 (2006), 691–701.
203. Audry, M., Ciancanelli, M., Yang, K., Cobat, A., Chang, H.H., Sancho-Shimizu, V., Lorenzo, L., Niehues, T., Reichenbach, J., Li, X.X., et al. NEMO is a key component of NF-kappaB- and IRF-3-dependent TLR3-mediated immunity to herpes simplex virus. J Allergy Clin Immunol 128 (2011), 610–617 e611-614.
204. Zimmer, B., Ewaleifoh, O., Harschnitz, O., Lee, Y.S., Peneau, C., McAlpine, J.L., Liu, B., Tchieu, J., Steinbeck, J.A., Lafaille, F., et al. Human iPSC-derived trigeminal neurons lack constitutive TLR3-dependent immunity that protects cortical neurons from HSV-1 infection. Proc Natl Acad Sci U S A 115 (2018), E8775–E8782 Following the 2012 report that TLR3-deficient iPSC-derived cortical neurons are more susceptible to HSV-1 infection than controls, this paper shows that control and TLR3-deficient iPSC-derived trigeminal neurons are equally susceptible to HSV-1. Collectively, these studies suggest that deficiency in the constitutive TLR3-dependent response of cortical neurons drives the pathogenesis of HSV-1 encephalitis.
205. Zhang, S.Y., Clark, N.E., Freije, C.A., Pauwels, E., Taggart, A.J., Okada, S., Mandel, H., Garcia, P., Ciancanelli, M.J., Biran, A., et al. Inborn errors of RNA lariat metabolism in humans with brainstem viral infection. Cell 172 (2018), 952–965 e918 This paper reports the discovery of autosomal recessive partial DBR1 deficiency in children with viral infections of the brainstem. DBR1 is the only known RNA lariat debranching enzyme, the expression of which normally peaks in the brainstem. Inborn errors of RNA lariat debranching underlies viral infection of the brainstem by disrupting brainstem-specific and cell-intrinsic immunity to viruses.
206. Chapman, K.B., Boeke, J.D., Isolation and characterization of the gene encoding yeast debranching enzyme. Cell 65 (1991), 483–492.
207. Ooi, S.L., Samarsky, D.A., Fournier, M.J., Boeke, J.D., Intronic snoRNA biosynthesis in Saccharomyces cerevisiae depends on the lariat-debranching enzyme: intron length effects and activity of a precursor snoRNA. RNA 4 (1998), 1096–1110.
208. Petfalski, E., Dandekar, T., Henry, Y., Tollervey, D., Processing of the precursors to small nucleolar RNAs and rRNAs requires common components. Mol Cell Biol 18 (1998), 1181–1189.
209. Murray, J.L., Sheng, J., Rubin, D.H., A role for H/ACA and C/D small nucleolar RNAs in viral replication. Mol Biotechnol 56 (2014), 429–437.
210. Sedger, L.M., microRNA control of interferons and interferon induced anti-viral activity. Mol Immunol 56 (2013), 781–793.
211. Han, B., Park, H.K., Ching, T., Panneerselvam, J., Wang, H., Shen, Y., Zhang, J., Li, L., Che, R., Garmire, L., et al. Human DBR1 modulates the recycling of snRNPs to affect alternative RNA splicing and contributes to the suppression of cancer development. Oncogene 36 (2017), 5382–5391.
212. Ulfendahl, P.J., Kreivi, J.P., Akusjarvi, G., Role of the branch site/3’-splice site region in adenovirus-2 E1A pre-mRNA alternative splicing: evidence for 5’- and 3’-splice site co-operation. Nucleic Acids Res 17 (1989), 925–938.
213. Plotch, S.J., Krug, R.M., In vitro splicing of influenza viral NS1 mRNA and NS1-beta-globin chimeras: possible mechanisms for the control of viral mRNA splicing. Proc Natl Acad Sci U S A 83 (1986), 5444–5448.
214. Perng, G.C., Jones, C., Towards an understanding of the herpes simplex virus type 1 latency-reactivation cycle. Interdiscip Perspect Infect Dis, 2010, 262415.
215. Galvis, A.E., Fisher, H.E., Fan, H., Camerini, D., Conformational changes in the 5’ end of the HIV-1 genome dependent on the debranching enzyme DBR1 during early stages of infection. J Virol, 91, 2017 pii: e01377-01317.