Contribution of high‐throughput DNA sequencing to the study of primary immunodeficiencies

Primary immunodeficiencies (PIDs) are inborn errors of the immune system. PIDs have been characterized immunologically for the last 60 years and genetically, principally by Sanger DNA sequencing, over the last 30 years. The advent of next‐generation sequencing (NGS) in 2011, with the development of whole‐exome sequencing in particular, has facilitated the identification of previously unknown genetic lesions. NGS is rapidly generating a stream of candidate variants for an increasing number of genetically undefined PIDs. The use of NGS technology is ushering in a new era, by facilitating the discovery and characterization of new PIDs in patients with infections and other phenotypes, thereby helping to improve diagnostic accuracy. This review provides a historical overview of the identification of PIDs before NGS, and the advances and limitations of the use of NGS for the diagnosis and characterization of PIDs.

[1]  G. Uzel,et al.  XMEN disease: a new primary immunodeficiency affecting Mg2+ regulation of immunity against Epstein-Barr virus. , 2014, Blood.

[2]  E. Cuppen,et al.  Targeted next-generation sequencing: a novel diagnostic tool for primary immunodeficiencies. , 2014, The Journal of allergy and clinical immunology.

[3]  Alain Laederach,et al.  Small RNAs derived from lncRNA RNase MRP have gene-silencing activity relevant to human cartilage-hair hypoplasia. , 2014, Human molecular genetics.

[4]  Nada Jabado,et al.  Phosphoinositide 3-Kinase δ Gene Mutation Predisposes to Respiratory Infection and Airway Damage , 2013, Science.

[5]  Winnie S. Liang,et al.  A Pilot Study Using Next-Generation Sequencing in Advanced Cancers: Feasibility and Challenges , 2013, PloS one.

[6]  J. B. Oliveira,et al.  Dominant-activating germline mutations in the gene encoding the PI(3)K catalytic subunit p110δ result in T cell senescence and human immunodeficiency , 2013, Nature Immunology.

[7]  Huanming Yang,et al.  Whole-genome and whole-exome sequencing of bladder cancer identifies frequent alterations in genes involved in sister chromatid cohesion and segregation , 2013, Nature Genetics.

[8]  Quinten Waisfisz,et al.  Best Practice Guidelines for the Use of Next‐Generation Sequencing Applications in Genome Diagnostics: A National Collaborative Study of Dutch Genome Diagnostic Laboratories , 2013, Human mutation.

[9]  T. Fleisher.  Ribosomal Protein SA Haploinsufficiency in Humans With Isolated Congenital Asplenia , 2013, Pediatrics.

[10]  S. Scherer,et al.  Detection of clinically relevant genetic variants in autism spectrum disorder by whole-genome sequencing. , 2013, American journal of human genetics.

[11]  Toshiro K. Ohsumi,et al.  Use of whole exome and genome sequencing in the identification of genetic causes of primary immunodeficiencies , 2012, Current opinion in allergy and clinical immunology.

[12]  V. Pascual,et al.  Immunodeficiency, auto-inflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency , 2012, Nature Immunology.

[13]  J. Casanova,et al.  Mycobacterial Disease and Impaired IFN-γ Immunity in Humans with Inherited ISG15 Deficiency , 2012, Science.

[14]  M. Gerstein,et al.  The Centers for Mendelian Genomics: A new large‐scale initiative to identify the genes underlying rare Mendelian conditions , 2012, American journal of medical genetics. Part A.

[15]  Bodo Grimbacher,et al.  Deleterious mutations in LRBA are associated with a syndrome of immune deficiency and autoimmunity. , 2012, American journal of human genetics.

[16]  E. Coustan-Smith,et al.  Agammaglobulinemia and absent B lineage cells in a patient lacking the p85α subunit of PI3K , 2012, The Journal of experimental medicine.

[17]  A. Borkhardt,et al.  Array‐Based Sequence Capture and Next‐Generation Sequencing for the Identification of Primary Immunodeficiencies , 2012, Scandinavian journal of immunology.

[18]  Eric O Long,et al.  Cold urticaria, immunodeficiency, and autoimmunity related to PLCG2 deletions. , 2012, The New England journal of medicine.

[19]  E. Cuppen,et al.  Multiplexed array-based and in-solution genomic enrichment for flexible and cost-effective targeted next-generation sequencing , 2011, Nature Protocols.

[20]  A. Fischer,et al.  Primary Immunodeficiency Diseases: An Update on the Classification from the International Union of Immunological Societies Expert Committee for Primary Immunodeficiency , 2011, Front. Immun..

[21]  D. Standley,et al.  A mutation in the immunoproteasome subunit PSMB8 causes autoinflammation and lipodystrophy in humans. , 2011, The Journal of clinical investigation.

[22]  M. Lenardo,et al.  Loss of MAGT1 abrogates the Mg2+ flux required for T cell signaling and leads to a novel human primary immunodeficiency. , 2011, Magnesium research.

[23]  Bernard Keavney,et al.  Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. , 2011, Blood.

[24]  Smita Y. Patel,et al.  Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. , 2011, Blood.

[25]  A. Smahi,et al.  Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. , 2011, The New England journal of medicine.

[26]  A. Fischer,et al.  Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis , 2011, The Journal of experimental medicine.

[27]  D. Douek,et al.  Second messenger role for Mg2+ revealed by human T-cell immunodeficiency , 2011, Nature.

[28]  A. Hoischen,et al.  STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. , 2011, The New England journal of medicine.

[29]  Nada Jabado,et al.  What can exome sequencing do for you? , 2011, Journal of Medical Genetics.

[30]  J. Casanova,et al.  Whole-exome sequencing-based discovery of STIM1 deficiency in a child with fatal classic Kaposi sarcoma , 2010, The Journal of experimental medicine.

[31]  S. Chanock,et al.  A custom 148 gene‐based resequencing chip and the SNP explorer software: new tools to study antibody deficiency , 2010, Human mutation.

[32]  J. B. Oliveira,et al.  Molecular- and Flow Cytometry-based Diagnosis of Primary Immunodeficiency Disorders , 2010, Current allergy and asthma reports.

[33]  M. Nowrousian.  Next-Generation Sequencing Techniques for Eukaryotic Microorganisms: Sequencing-Based Solutions to Biological Problems , 2010, Eukaryotic Cell.

[34]  P. Bork,et al.  A method and server for predicting damaging missense mutations , 2010, Nature Methods.

[35]  T. Fleisher,et al.  Mutation analysis in primary immunodeficiency diseases: case studies , 2009, Current opinion in allergy and clinical immunology.

[36]  F. Rieux-Laucat,et al.  STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. , 2009, The New England journal of medicine.

[37]  J. Lupski,et al.  The complete genome of an individual by massively parallel DNA sequencing , 2008, Nature.

[38]  Shigeaki Nonoyama,et al.  Primary immunodeficiency diseases: an update from the International Union of Immunological Societies Primary Immunodeficiency Diseases Classification Committee. , 2007, The Journal of allergy and clinical immunology.

[39]  W. Reith,et al.  MHC class II deficiency: a disease of gene regulation. , 2001, Medicine.

[40]  R. Aebersold,et al.  A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients , 1998, Nature Genetics.

[41]  P. Emery,et al.  RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency , 1997, The EMBO journal.

[42]  U. Pannicke,et al.  RAG Mutations in Human B Cell-Negative SCID , 1996, Science.

[43]  B. Roe,et al.  A transcription map of the DiGeorge and velo-cardio-facial syndrome minimal critical region on 22q11. , 1996, Human molecular genetics.

[44]  Dale A Ramsden,et al.  The RAG1 and RAG2 Proteins Establish the 12/23 Rule in V(D)J Recombination , 1996, Cell.

[45]  B. Durand,et al.  A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). , 1995, Genes & development.

[46]  U. Francke,et al.  Isolation of a novel gene mutated in Wiskott-Aldrich syndrome , 1994, Cell.

[47]  M. Gellert,et al.  Expression and V(D)J recombination activity of mutated RAG-1 proteins. , 1993, Nucleic acids research.

[48]  B. Mach,et al.  Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome) , 1993, Cell.

[49]  Carolyn J. Brown,et al.  The interleukin-2 receptor gamma chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1. , 1993, Human molecular genetics.

[50]  D J Rawlings,et al.  Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. , 1993, Science.

[51]  W. Leonard,et al.  Interleukin-2 receptor γ chain mutation results in X-linked severe combined immunodeficiency in humans , 1993, Cell.

[52]  Ornella Parolini,et al.  Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia , 1993, Cell.

[53]  J. Ott,et al.  Localization of the gene for the Wiskott-Aldrich syndrome between two flanking markers, TIMP and DXS255, on Xp11.22-Xp11.3. , 1991, Genomics.

[54]  David Baltimore,et al.  The V(D)J recombination activating gene, RAG-1 , 1989, Cell.

[55]  A. Fischer,et al.  Close linkage of the locus for X chromosome-linked severe combined immunodeficiency to polymorphic DNA markers in Xq11-q13. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[56]  A. Jesaitis,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. , 1987, The Journal of clinical investigation.

[57]  A. Monaco,et al.  Cloning the gene for an inherited human disorder—chronic granulomatous disease—on the basis of its chromosomal location , 1986, Nature.

[58]  Lloyd M. Smith,et al.  Fluorescence detection in automated DNA sequence analysis , 1986, Nature.

[59]  J. Haines,et al.  DNA linkage analysis of X chromosome-linked chronic granulomatous disease. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[60]  F. Sanger,et al.  Nucleotide sequence of bacteriophage φX174 DNA , 1977, Nature.

[61]  H. Huser,et al.  [Agammaglobulinemia & alymphocytosis with atrophy of lymphatic tissue]. , 1958, Helvetica paediatrica acta.

[62]  H. Cottier,et al.  [Familial lymphopenia with agammaglobulinemia & severe moniliasis: the essential lymphocytophthisis as a special form of early childhood agammaglobulinemia]. , 1958, Helvetica paediatrica acta.

[63]  R. Good,et al.  A fatal granulomatosus of childhood: the clinical study of a new syndrome. , 1957, Minnesota medicine.

[64]  R. Geha,et al.  LPS-responsive beige-like anchor (LRBA) gene mutation in a family with inflammatory bowel disease and combined immunodeficiency. , 2012, The Journal of allergy and clinical immunology.

[65]  M. Metzker.  Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[66]  Emily H Turner,et al.  Targeted Capture and Massively Parallel Sequencing of Twelve Human Exomes , 2009, Nature.

[67]  S. Henikoff,et al.  Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm , 2009, Nature Protocols.

[68]  J. Mullikin,et al.  Human adenylate kinase 2 deficiency causes a profound hematopoietic defect associated with sensorineural deafness , 2009, Nature Genetics.

[69]  U. Pannicke,et al.  Reticular dysgenesis (aleukocytosis) is caused by mutations in the gene encoding mitochondrial adenylate kinase 2 , 2009, Nature Genetics.

[70]  D. Vetrie,et al.  The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases , 1993, Nature.

[71]  S. Orkin,et al.  The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex , 1987, Nature.

[72]  A. Monaco,et al.  Cloning the gene for the inherited disorder chronic granulomatous disease on the basis of its chromosomal location. , 1986, Cold Spring Harbor symposia on quantitative biology.

[73]  F. Sanger,et al.  Nucleotide sequence of bacteriophage phi X174 DNA. , 1977, Nature.