Heterozygous FOXN1 Variants Cause Low TRECs and Severe T Cell Lymphopenia, Revealing a Crucial Role of FOXN1 in Supporting Early Thymopoiesis

The American Journal of Human Genetics - Tập 105 - Trang 549-561 - 2019
Marita Bosticardo1, Yasuhiro Yamazaki1, Jennifer Cowan2, Giuliana Giardino3, Cristina Corsino1, Giulia Scalia4, Rosaria Prencipe3, Melanie Ruffner5, David A. Hill5, Inga Sakovich6, Irma Yemialyanava6, Jonathan S. Tam7, Nurcicek Padem8, Melissa E. Elder9, John W. Sleasman10, Elena Perez11, Hana Niebur12, Christine M. Seroogy13, Svetlana Sharapova6, Jennifer Gebbia14
1Laboratory of Clinical Immunology and Microbiology, IDGS, DIR, NIAID, NIH, Bethesda, MD 20892, USA
2Laboratory of Genome Integrity, CCR, NCI, NIH, Bethesda, MD 20892, USA
3Department of Translational Medical Sciences Federico II University, Naples 80138, Italy
4Laboratory of Clinical research and Advanced Diagnostics, CEINGE Biotecnologie Avanzate, Naples 80131, Italy
5Division of Allergy and Immunology, Department of Pediatrics, Children’s Hospital Philadelphia, Philadelphia, PA 19104, USA
6Immunology Lab, Belarusian Research Center for Pediatric Oncology, Hematology and Immunology, Minsk 223053, Belarus
7Division of Clinical Immunology and Allergy, Children’s Hospital Los Angeles, Los Angeles, CA 90027, USA
8Division of Allergy and Immunology, Lurie Children’s Hospital, Chicago, IL 60611, USA
9Division of Allergy, Immunology and Rheumatology, Department of Pediatrics, University of Florida, Gainesville, FL 32610, USA
10Division of Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Duke University School of Medicine, Durham, NC 27705, USA
11Allergy Associates of the Palm Beaches, North Palm Beach, FL 33408, USA
12Division of Pediatric Allergy and Immunology, University of Nebraska Medical Center, Omaha, NE 68198, USA
13Division of Allergy, Immunology and Rheumatology, Department of Pediatrics, University of Wisconsin School of Medicine and Public Health, Madison, WI 53792, USA
14Department of Pediatric Allergy and Immunology, University of Miami Miller School of Medicine, Miami, FL 33136, USA

Tài liệu tham khảo

Gordon, 2001, Gcm2 and Foxn1 mark early parathyroid- and thymus-specific domains in the developing third pharyngeal pouch, Mech. Dev., 103, 141, 10.1016/S0925-4773(01)00333-1 Flanagan, 1966, ‘Nude’, a new hairless gene with pleiotropic effects in the mouse, Genet. Res., 8, 295, 10.1017/S0016672300010168 D’Assante, 2016, Unraveling the Link Between Ectodermal Disorders and Primary Immunodeficiencies, Int. Rev. Immunol., 35, 25 Farley, 2013, Dynamics of thymus organogenesis and colonization in early human development, Development, 140, 2015, 10.1242/dev.087320 Žuklys, 2016, Foxn1 regulates key target genes essential for T cell development in postnatal thymic epithelial cells, Nat. Immunol., 17, 1206, 10.1038/ni.3537 Nowell, 2011, Foxn1 regulates lineage progression in cortical and medullary thymic epithelial cells but is dispensable for medullary sublineage divergence, PLoS Genet., 7, e1002348, 10.1371/journal.pgen.1002348 Chen, 2009, Foxn1 is required to maintain the postnatal thymic microenvironment in a dosage-sensitive manner, Blood, 113, 567, 10.1182/blood-2008-05-156265 Cheng, 2010, Postnatal tissue-specific disruption of transcription factor FoxN1 triggers acute thymic atrophy, J. Biol. Chem., 285, 5836, 10.1074/jbc.M109.072124 Gallo, 2017, FOXN1 Deficiency: from the Discovery to Novel Therapeutic Approaches, J. Clin. Immunol., 37, 751, 10.1007/s10875-017-0445-z Pignata, 1996, Congenital Alopecia and nail dystrophy associated with severe functional T-cell immunodeficiency in two sibs, Am. J. Med. Genet., 65, 167, 10.1002/(SICI)1096-8628(19961016)65:2<167::AID-AJMG17>3.0.CO;2-O Frank, 1999, Exposing the human nude phenotype, Nature, 398, 473, 10.1038/18997 Adriani, 2004, Ancestral founder mutation of the nude (FOXN1) gene in congenital severe combined immunodeficiency associated with alopecia in southern Italy population, Ann. Hum. Genet., 68, 265, 10.1046/j.1529-8817.2004.00091.x Markert, 2011, First use of thymus transplantation therapy for FOXN1 deficiency (nude/SCID): a report of 2 cases, Blood, 117, 688, 10.1182/blood-2010-06-292490 Chou, 2014, A novel mutation in FOXN1 resulting in SCID: a case report and literature review, Clin. Immunol., 155, 30, 10.1016/j.clim.2014.08.005 Radha Rama Devi, 2017, FOXN1 Italian founder mutation in Indian family: Implications in prenatal diagnosis, Gene, 627, 222, 10.1016/j.gene.2017.06.033 Auricchio, 2005, Nail dystrophy associated with a heterozygous mutation of the nude/SCID human FOXN1 (WHN) gene, Arch. Dermatol., 141, 647, 10.1001/archderm.141.5.647 Shearer, 2003, Lymphocyte subsets in healthy children from birth through 18 years of age: the Pediatric AIDS Clinical Trials Group P1009 study, J. Allergy Clin. Immunol., 112, 973, 10.1016/j.jaci.2003.07.003 Gray, 2007, Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire, J. Exp. Med., 204, 2521, 10.1084/jem.20070795 Kyewski, 2006, A central role for central tolerance, Annu. Rev. Immunol., 24, 571, 10.1146/annurev.immunol.23.021704.115601 Nehls, 1994, New member of the winged-helix protein family disrupted in mouse and rat nude mutations, Nature, 372, 103, 10.1038/372103a0 Kaufmann, 1996, Five years on the wings of fork head, Mech. Dev., 57, 3, 10.1016/0925-4773(96)00539-4 Newman, 2018, The structural basis for forkhead box family specificity revealed by the crystal structure of human FOXN1 in complex with DNA, bioRxiv Bajoghli, 2009, Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates, Cell, 138, 186, 10.1016/j.cell.2009.04.017 Tan, 2002, Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells, J. Exp. Med., 195, 1523, 10.1084/jem.20020066 Nehls, 1996, Two genetically separable steps in the differentiation of thymic epithelium, Science, 272, 886, 10.1126/science.272.5263.886 Bleul, 2000, Chemokines define distinct microenvironments in the developing thymus, Eur. J. Immunol., 30, 3371, 10.1002/1521-4141(2000012)30:12<3371::AID-IMMU3371>3.0.CO;2-L Rodewald, 1995, Intrathymically expressed c-kit ligand (stem cell factor) is a major factor driving expansion of very immature thymocytes in vivo, Immunity, 3, 313, 10.1016/1074-7613(95)90116-7 Rodewald, 1997, Pro-thymocyte expansion by c-kit and the common cytokine receptor γ chain is essential for repertoire formation, Immunity, 6, 265, 10.1016/S1074-7613(00)80329-5 Tsukamoto, 2005, Lack of Delta like 1 and 4 expressions in nude thymus anlages, Cell. Immunol., 234, 77, 10.1016/j.cellimm.2005.06.009 Hozumi, 2008, Delta-like 4 is indispensable in thymic environment specific for T cell development, J. Exp. Med., 205, 2507, 10.1084/jem.20080134 Zampieri, 2015, Reconfiguration of DNA methylation in aging, Mech. Ageing Dev., 151, 60, 10.1016/j.mad.2015.02.002 Scheiff, 1978, The thymus of Nu/+ mice, Anat. Embryol. (Berl.), 153, 115, 10.1007/BF00343368 Kojima, 1984, NFS/N-nu/ + mice can macroscopically be distinguished from NFS/N- +/+ littermates by their thymic size and shape, Exp. Cell Biol., 52, 107 Pignata, 2001, Human equivalent of the mouse Nude/SCID phenotype: long-term evaluation of immunologic reconstitution after bone marrow transplantation, Blood, 97, 880, 10.1182/blood.V97.4.880 Albuquerque, 2012, Human FOXN1-deficiency is associated with αβ double-negative and FoxP3+ T-cell expansions that are distinctly modulated upon thymic transplantation, PLoS ONE, 7, e37042, 10.1371/journal.pone.0037042 Levy, 2012, Vitiligo post-greffe thymique chez un enfant porteur d’un déficit en Foxn1, Ann. Dermatol. Venereol., 139, 468, 10.1016/j.annder.2012.03.014