Role of rare immune cells in common variable immunodeficiency.
CVID
common variable immunodeficiency
immunological defects
inborn errors of immunity
pathogenesis
primary immunodeficiency
rare immune cells
Journal
Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology
ISSN: 1399-3038
Titre abrégé: Pediatr Allergy Immunol
Pays: England
ID NLM: 9106718
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
revised:
10
12
2021
received:
09
08
2021
accepted:
17
12
2021
pubmed:
23
12
2021
medline:
8
4
2022
entrez:
22
12
2021
Statut:
ppublish
Résumé
Common variable immunodeficiency disorder (CVID) is a heterogeneous disorder and the most common symptomatic antibody deficiency disease characterized with hypogammaglobulinemia and a broad range of clinical manifestations. Multiple genetic, epigenetic, and immunological defects are involved in the pathogenesis of CVID. These immunological defects include abnormalities in the number and/or function of B lymphocytes, T lymphocytes, and other rare immune cells. Although some immune cells have a relatively lower proportion among total immune subsets in the human body, they could have important roles in the pathogenesis of immunological disorders like CVID. To the best of our knowledge, this is the first review that described the role of rare immune cells in the pathogenesis and clinical presentations of CVID.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13725Informations de copyright
© 2021 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.
Références
Yazdani R, Abolhassani H, Kiaee F, et al. Comparison of common monogenic defects in a large predominantly antibody deficiency cohort. J Allergy Clin Immunol Pract. 2019;7(3):864-878.e9.
Yazdani R, Habibi S, Sharifi L, et al. Common variable immunodeficiency: epidemiology, pathogenesis, clinical manifestations, diagnosis, classification, and management. J Investig Allergol Clin Immunol. 2020;30(1):14-34.
Aghamohammadi A, Abolhassani H, Moazzami K, et al. Correlation between common variable immunodeficiency clinical phenotypes and parental consanguinity in children and adults. J Investig Allergol Clin Immunol. 2010;20(5):372-379.
Cunningham-Rundles C, Bodian C. Common variable immunodeficiency: clinical and immunological features of 248 patients. Clin Immunol. 1999;92(1):34-48.
Azizi G, Abolhassani H, Hosein Asgardoon M, et al. The use of immunoglobulin therapy in primary immunodeficiency diseases. Endocr Metab Immune Disord Drug Targets. 2016;16(2):80-88.
Abolhassani H, Aghamohammadi A, Fang M, et al. Clinical implications of systematic phenotyping and exome sequencing in patients with primary antibody deficiency. Genet Med. 2019;21(1):243-251.
Abolhassani H, Lim CK, Aghamohammadi A, Hammarström L. Histocompatibility complex status and mendelian randomization analysis in unsolved antibody deficiency. Front Immunol. 2020;11:14. doi:10.3389/fimmu.2020.00014
Taubenheim N, von Hornung M, Durandy A, et al. Defined blocks in terminal plasma cell differentiation of common variable immunodeficiency patients. J Immunol. 2005;175(8):5498-5503.
Piqueras B, Lavenu-Bombled C, Galicier L, et al. Common variable immunodeficiency patient classification based on impaired B cell memory differentiation correlates with clinical aspects. J Clin Immunol. 2003;23(5):385-400. doi:10.1023/a:1025373601374
Li R, Zheng Y, Li Y, et al. Common variable immunodeficiency with genetic defects identified by whole exome sequencing. Biomed Res Int. 2018;2018:1-7.
Rae W. Indications to epigenetic dysfunction in the pathogenesis of common variable immunodeficiency. Arch Immunol Ther Exp. 2017;65(2):101-110.
Kopecký O, Lukešová Š. Genetic defects in common variable immunodeficiency. Int J Immunogenet. 2007;34(4):225-229.
Tallmadge RL, Shen L, Tseng CT, et al. Bone marrow transcriptome and epigenome profiles of equine common variable immunodeficiency patients unveil block of B lymphocyte differentiation. Clin Immunol. 2015;160(2):261-276.
Li J, Wei Z, Li YR, et al. Understanding the genetic and epigenetic basis of common variable immunodeficiency disorder through omics approaches. Biochimica Biophys Acta General Subjects. 2016;1860(11):2656-2663.
Zhou H, Hu H, Lai M. Non-coding RNAs and their epigenetic regulatory mechanisms. Biol Cell. 2010;102(12):645-655.
Rodríguez-Cortez VC, Del Pino-Molina L, Rodríguez-Ubreva J, et al. Monozygotic twins discordant for common variable immunodeficiency reveal impaired DNA demethylation during naïve-to-memory B-cell transition. Nat Commun. 2015;6:7335. doi:10.1038/ncomms8335
Langrish CL, Chen YI, Blumenschein WM, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med. 2005;201(2):233-240.
Chen K, Kolls JK. Interluekin-17a (il17a). Gene. 2017;614:8-14.
Rossi M, Bot A. The Th17 cell population and the immune homeostasis of the gastrointestinal tract. Int Rev Immunol. 2013;32(5-6):471-474.
Korn T, Bettelli E, Oukka M, et al. IL-17 and Th17 cells. Annu Rev Immunol. 2009;27:485-517.
Ivanov II, McKenzie BS, Zhou L, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell. 2006;126(6):1121-1133. doi:10.1016/j.cell.2006.07.035
Lee Y, Awasthi A, Yosef N, et al. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol. 2012;13(10):991-999.
Haak S, et al. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest. 2009;119(1):61-69.
Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity. 2008;28(4):454-467.
Iwakura Y, Ishigame H, Saijo S, et al. Functional specialization of interleukin-17 family members. Immunity. 2011;34(2):149-162.
Liang SC, Tan X-Y, Luxenberg DP, et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med. 2006;203(10):2271-2279.
Annunziato F, Cosmi L, Santarlasci V, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007;204(8):1849-1861.
Barbosa RR, Silva SP, Silva SL, et al. Primary B-cell deficiencies reveal a link between human IL-17-producing CD4 T-cell homeostasis and B-cell differentiation. PLoS One. 2011;6(8):e22848.
Ganjalikhani-Hakemi M, Yazdani R, Sherkat R, Homayouni V, Masjedi M, Hosseini M. Evaluation of the T helper 17 cell specific genes and the innate lymphoid cells counts in the peripheral blood of patients with the common variable immunodeficiency. J Res Med Sci. 2014;19(Suppl 1):S30-S35.
Azizi G, Mirshafiey A, Abolhassani H, et al. Circulating helper T-cell subsets and regulatory T cells in patients with common variable immunodeficiency without known monogenic disease. J Investig Allergol Clin Immunol. 2018;28(3):172-181.
Yang WY, Shao Y, Lopez-Pastrana J, et al. Pathological conditions re-shape physiological Tregs into pathological Tregs. Burns Trauma. 2015;3:1. doi:10.1186/s41038-015-0001-0
Lee YK, Turner H, Maynard CL, et al. Late developmental plasticity in the T helper 17 lineage. Immunity. 2009;30(1):92-107.
Jäger A, Dardalhon V, Sobel RA, et al. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol. 2009;183(11):7169-7177.
Kleinewietfeld M, Hafler DA. The plasticity of human Treg and Th17 cells and its role in autoimmunity. Semin Immunol. 2013;25:305-312.
Annunziato F, Cosmi L, Liotta F, et al. Defining the human T helper 17 cell phenotype. Trends Immunol. 2012;33(10):505-512.
Panzer M, Sitte S, Wirth S, et al. Rapid in vivo conversion of effector T cells into Th2 cells during helminth infection. J Immunol. 2012;188(2):615-623.
Bending D, De La Peña H, Veldhoen M, et al. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J Clin Invest. 2009;119(3):565-572.
Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity. 2009;30(5):646-655.
Mathur AN, et al. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood. 2006;108(5):1595-1601.
Hirota K, Duarte JH, Veldhoen M, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol. 2011;12(3):255-263.
Kamali AN, Noorbakhsh SM, Hamedifar H, et al. A role for Th1-like Th17 cells in the pathogenesis of inflammatory and autoimmune disorders. Mol Immunol. 2019;105:107-115.
Azizi G, Mirshafiey A, Abolhassani H, et al. The imbalance of circulating T helper subsets and regulatory T cells in patients with LRBA deficiency: Correlation with disease severity. J Cell Physiol. 2018;233(11):8767-8777.
Duhen T, Geiger R, Jarrossay D, et al. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol. 2009;10(8):857-863.
Ramirez J-M, Brembilla NC, Sorg O, et al. Activation of the aryl hydrocarbon receptor reveals distinct requirements for IL-22 and IL-17 production by human T helper cells. Eur J Immunol. 2010;40(9):2450-2459.
Jia L, Wu C. The biology and functions of Th22 cells. Adv Exp Med Biol. 2014;841:209-230.
Azizi G, Yazdani R, Mirshafiey A. Th22 cells in autoimmunity: a review of current knowledge. Eur Ann Allergy Clin Immunol. 2015;47(4):108-117.
Eyerich S, Eyerich K, Pennino D, et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest. 2009;119(12):3573-3585.
de Lollo C, de Moraes Vasconcelos D, da Silva Oliveira LM, et al. Impaired CD8+ T cell responses upon Toll-like receptor activation in common variable immunodeficiency. J Transl Med. 2016;14(1):138.
Azizi G, Abolhassani H, Mahdaviani SA, et al. Clinical, immunologic, molecular analyses and outcomes of iranian patients with LRBA deficiency: a longitudinal study. Pediatr Allergy Immunol. 2017;28(5):478-484.
Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell. 2000;101(5):455-458.
Cosmi L, Liotta F, Lazzeri E, et al. Human CD8+CD25+ thymocytes share phenotypic and functional features with CD4+CD25+ regulatory thymocytes. Blood. 2003;102(12):4107-4114.
Lu L, Cantor H. Generation and regulation of CD8(+) regulatory T cells. Cell Mol Immunol. 2008;5(6):401-406.
Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol. 2012;30:221-241.
Goschl L, Scheinecker C, Bonelli M. Treg cells in autoimmunity: from identification to treg-based therapies. Semin Immunopathol. 2019;41(3):301-314.
Sakaguchi S, Yamaguchi T, Nomura T, et al. Regulatory T cells and immune tolerance. Cell. 2008;133(5):775-787.
Chen WJ, Jin W, Hardegen N, et al. Conversion of peripheral CD4+ CD25− naive T cells to CD4+ CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. J Exp Med. 2003;198(12):1875-1886.
Shevach EM. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity. 2009;30(5):636-645.
Sakaguchi S, Miyara M, Costantino CM, et al. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol. 2010;10(7):490-500.
Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30:531-564.
Bilate AM, Lafaille JJ. Induced CD4+Foxp3+ regulatory T cells in immune tolerance. Annu Rev Immunol. 2012;30:733-758.
Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4(4):330-336.
Chinen T, Kannan AK, Levine AG, et al. An essential role for the IL-2 receptor in Treg cell function. Nat Immunol. 2016;17(11):1322-1333.
Yoshimura A, Muto G. TGF-beta function in immune suppression. Curr Top Microbiol Immunol. 2011;350:127-147.
Kriegel MA, Li MO, Sanjabi S, Wan YY, Flavell RA. Transforming growth factor-beta: recent advances on its role in immune tolerance. Curr Rheumatol Rep. 2006;8(2):138-144. doi:10.1007/s11926-006-0054-y
Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198(12):1875-1886. doi:10.1084/jem.20030152
McClymont SA, Putnam AL, Lee MR, et al. Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. J Immunol. 2011;186(7):3918-3926.
Jorn Bovenschen H, van de Kerkhof PC, van Erp PE, et al. Foxp3+ regulatory T cells of psoriasis patients easily differentiate into IL-17A-producing cells and are found in lesional skin. J Invest Dermatol. 2011;131(9):1853-1860.
Muratori L, Longhi MS. The interplay between regulatory and effector T cells in autoimmune hepatitis: implications for innovative treatment strategies. J Autoimmun. 2013;46:74-80.
Azizi G, Hafezi N, Mohammadi H, et al. Abnormality of regulatory T cells in common variable immunodeficiency. Cell Immunol. 2017;315:11-17.
Fevang B, Yndestad A, Sandberg WJ, et al. Low numbers of regulatory T cells in common variable immunodeficiency: association with chronic inflammation in vivo. Clin Exp Immunol. 2007;147(3):521-525. doi:10.1111/j.1365-2249.2006.03314.x
Genre J, Errante PR, Kokron CM, Toledo-Barros M, Câmara NO, Rizzo LV. Reduced frequency of CD4(+)CD25(HIGH)FOXP3(+) cells and diminished FOXP3 expression in patients with common variable immunodeficiency: a link to autoimmunity? Clin Immunol. 2009;132(2):215-221. doi:10.1016/j.clim.2009.03.519
Arumugakani G, Wood PM, Carter CR. Frequency of treg cells is reduced in CVID patients with autoimmunity and splenomegaly and is associated with expanded CD21lo B lymphocytes. J Clin Immunol. 2010;30(2):292-300.
Arandi N, Mirshafiey A, Abolhassani H, et al. Frequency and expression of inhibitory markers of CD4(+) CD25(+) FOXP3(+) regulatory T cells in patients with common variable immunodeficiency. Scand J Immunol. 2013;77(5):405-412. doi:10.1111/sji.12040
Sadati ZA, Motedayyen H, Sherkat R, et al. Comparison of the percentage of regulatory T cells and their p-STAT5 expression in allergic and non-allergic common variable immunodeficiency patients. Immunol Invest. 2019;48(1):52-63.
Kutukculer N, Azarsiz E, Aksu G, Karaca NE. CD4+CD25+Foxp3+ T regulatory cells, Th1 (CCR5, IL-2, IFN-γ) and Th2 (CCR4, IL-4, Il-13) type chemokine receptors and intracellular cytokines in children with common variable immunodeficiency. Int J Immunopathol Pharmacol. 2016;29(2):241-251. doi:10.1177/0394632015617064
Yesillik S, Agrawal S, Gollapudi S, et al. Phenotypic analysis of CD4+ Treg, CD8+ Treg, and breg cells in adult common variable immunodeficiency patients. Int Arch Allergy Immunol. 2019;180(2):150-158.
Azizi G, Abolhassani H, Kiaee F, et al. Autoimmunity and its association with regulatory T cells and B cell subsets in patients with common variable immunodeficiency. Allergol Immunopathol. 2018;46(2):127-135.
López-Herrera G, Segura-Méndez NH, O’Farril-Romanillos P, et al. Low percentages of regulatory T cells in common variable immunodeficiency (CVID) patients with autoimmune diseases and its association with increased numbers of CD4+CD45RO+ T and CD21(low) B cells. Allergol Immunopathol. 2019;47(5):457-466.
Yu GP, Chiang D, Song SJ, et al. Regulatory T cell dysfunction in subjects with common variable immunodeficiency complicated by autoimmune disease. Clin Immunol. 2009;131(2):240-253.
Mouillot G, Carmagnat M, Gérard L, et al. B-cell and T-cell phenotypes in CVID patients correlate with the clinical phenotype of the disease. J Clin Immunol. 2010;30(5):746-755.
Tangye SG, Al-Herz W, Bousfiha A, et al. Human inborn errors of immunity: 2019 update on the classification from the international union of immunological societies expert committee. J Clin Immunol. 2020;40(1):24-64.
Breitfeld D, Ohl L, Kremmer E, et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med. 2000;192(11):1545-1552.
Nurieva RI, Chung Y, Hwang D, et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity. 2008;29(1):138-149.
Crotty S. Follicular helper CD4 T cells (Tfh). Annu Rev Immunol. 2011;29:621-663.
He J, Tsai L, Leong Y, et al. Circulating precursor CCR7loPD-1hi CXCR5+ CD4+ T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure. Immunity. 2013;39(4):770-781.
Morita R, Schmitt N, Bentebibel S-E, et al. Human blood CXCR5+ CD4+ T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity. 2011;34(1):108-121.
Locci M, Havenar-Daughton C, Landais E, et al. Human circulating PD-1+ CXCR3− CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity. 2013;39(4):758-769.
Ma CS, Wong N, Rao G, et al. Monogenic mutations differentially affect the quantity and quality of T follicular helper cells in patients with human primary immunodeficiencies. J Allergy Clin Immunol. 2015;136(4):993-1006.e1. doi:10.1016/j.jaci.2015.05.036
Bogaert DJ, Dullaers M, Lambrecht BN, Vermaelen KY, De Baere E, Haerynck F. Genes associated with common variable immunodeficiency: one diagnosis to rule them all? J Med Genet. 2016;53(9):575-590. doi:10.1136/jmedgenet-2015-103690
Bossaller L, Burger J, Draeger R, et al. ICOS deficiency is associated with a severe reduction of CXCR5+CD4 germinal center Th cells. J Immunol. 2006;177(7):4927-4932. doi:10.4049/jimmunol.177.7.4927
Liu Y, Hanson S, Gurugama P, et al. Novel NFKB2 mutation in early-onset CVID. J Clin Immunol. 2014;34(6):686-690.
Romberg N, Chamberlain N, Saadoun D, et al. CVID-associated TACI mutations affect autoreactive B cell selection and activation. J Clin Investig. 2013;123(10):4283-4293.
Turpin D, Furudoi A, Parrens M, et al. Increase of follicular helper T cells skewed toward a Th1 profile in CVID patients with non-infectious clinical complications. Clin Immunol. 2018;197:130-138.
Coraglia A, Galassi N, Fernández Romero DS, et al. Common variable immunodeficiency and circulating TFH. J Immunol Res. 2016;2016:4951587. doi:10.1155/2016/4951587
Cunill V, Clemente A, Lanio N, et al. Follicular T cells from smB- common variable immunodeficiency patients are skewed toward a Th1 phenotype. Front Immunol. 2017;27(8):174. doi:10.3389/fimmu.2017.00174
Unger S, Seidl M, van Schouwenburg P, et al. The T(H)1 phenotype of follicular helper T cells indicates an IFN-γ-associated immune dysregulation in patients with CD21low common variable immunodeficiency. J Allergy Clin Immunol. 2018;141(2):730-740.
Le Coz C, Bengsch B, Khanna C, et al. Common variable immunodeficiency-associated endotoxemia promotes early commitment to the T follicular lineage. J Allergy Clin Immunol. 2019;144(6):1660-1673.
Yesillik S, Gupta S. Phenotypically defined subpopulations of circulating follicular helper T cells in common variable immunodeficiency. Immun Inflamm Dis. 2020;8(3):441-446.
Kasahara TM, Bento CAM, Gupta S. Phenotypic and functional analysis of T follicular cells in common variable immunodeficiency. Int Arch Allergy Immunol. 2020;181(8):635-647.
Fearon DT, Carroll MC, Carroll MC. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu Rev Immunol. 2000;18:393-422.
Wentink MWJ, Lambeck AJA, van Zelm MC, et al. CD21 and CD19 deficiency: two defects in the same complex leading to different disease modalities. Clin Immunol. 2015;161(2):120-127.
Yazdani R, Ganjalikhani-Hakemi M, Esmaeili M, et al. Impaired Akt phosphorylation in B-cells of patients with common variable immunodeficiency. Clin Immunol. 2017;175:124-132.
Wehr C, Kivioja T, Schmitt C, et al. The EUROclass trial: defining subgroups in common variable immunodeficiency. Blood. 2008;111(1):77-85.
Wehr C, Eibel H, Masilamani M, et al. A new CD21low B cell population in the peripheral blood of patients with SLE. Clin Immunol. 2004;113(2):161-171.
Warnatz K, Denz A, Dräger R, et al. Severe deficiency of switched memory B cells (CD27(+)IgM(−)IgD(−)) in subgroups of patients with common variable immunodeficiency: a new approach to classify a heterogeneous disease. Blood. 2002;99(5):1544-1551.
Warnatz K, Schlesier M. Flowcytometric phenotyping of common variable immunodeficiency. Cytometry B Clin Cytom. 2008;74(5):261-271.
Yazdani R, Seify R, Ganjalikhani-Hakemi M, et al. Comparison of various classifications for patients with common variable immunodeficiency (CVID) using measurement of B-cell subsets. Allergol Immunopathol. 2017;45(2):183-192.
Bonilla FA, Barlan I, Chapel H, et al. International consensus document (ICON): common variable immunodeficiency disorders. J Allergy Clin Immunol Pract. 2016;4(1):38-59.
Arumugakani G, Wood PM, Carter CR. Frequency of treg cells isreduced in CVID patients with autoimmunity and splenomegalyand is associated with expanded CD21lo B lymphocytes. J Clin Immunol. 2010;30:292-300.
Saadoun D, Terrier B, Bannock J, et al. Expansion of autoreactive unresponsive CD21-/low B cells in Sjögren's syndrome-associated lymphoproliferation. Arthritis Rheum. 2013;65(4):1085-1096. doi:10.1002/art.37828
Moratto D, Gulino AV, Fontana S, et al. Combined decrease of defined B and T cell subsets in a group of common variable immunodeficiency patients. Clin Immunol. 2006;121(2):203-214.
Friedmann D, Unger S, Keller B, et al. Bronchoalveolar lavage fluid reflects a TH1-CD21low B-cell interaction in CVID-related interstitial lung disease. Front Immunol. 2021;5(11):616832. doi:10.3389/fimmu.2020.616832
Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607-612.
Blair PA, Noreña LY, Flores-Borja F, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity. 2010;32(1):129-140.
Salomon S, Guignant C, Morel P, et al. Th17 and CD24(hi)CD27(+) regulatory B lymphocytes are biomarkers of response to biologics in rheumatoid arthritis. Arthritis Res Ther. 2017;19(1):33.
Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4⁺ T cells to T-regulatory cells. Cancer Res. 2011;71(10):3505-3515. doi:10.1158/0008-5472.CAN-10-4316
Zheng SG, Wang J, Wang P, Gray JD, Horwitz DA. IL-2 is essential for TGF-beta to convert naive CD4+CD25- cells to CD25+Foxp3+ regulatory T cells and for expansion of these cells. J Immunol. 2007;178(4):2018-2027. doi:10.4049/jimmunol.178.4.2018
Vlkova M, Ticha O, Nechvatalova J, et al. Regulatory B cells in CVID patients fail to suppress multifunctional IFN-γ+ TNF-α+ CD4+ T cells differentiation. Clin Immunol. 2015;160(2):292-300. doi:10.1016/j.clim.2015.06.013
Lim AI, Verrier T, Vosshenrich CAJ, et al. Developmental options and functional plasticity of innate lymphoid cells. Curr Opin Immunol. 2017;44:61-68.
Juelke K, Romagnani C. Differentiation of human innate lymphoid cells (ILCs). Curr Opin Immunol. 2016;38:75-85.
Bal SM, Golebski K, Spits H. Plasticity of innate lymphoid cell subsets. Nat Rev Immunol. 2020;20(9):552-565.
Eberl G, Colonna M, Di Santo JP, et al. Innate lymphoid cells: a new paradigm in immunology. Science. 2015;348(6237):aaa6566. 10.1126/science.aaa6566
Hazenberg MD, Spits H. Human innate lymphoid cells. Blood. 2014;124(5):700-709.
Yazdani R, Sharifi M, Shirvan AS, et al. Characteristics of innate lymphoid cells (ILCs) and their role in immunological disorders (an update). Cell Immunol. 2015;298(1-2):66-76.
Jiao Y, Huntington ND, Belz GT, Seillet C. Type 1 innate lymphoid cell biology: lessons learnt from natural killer cells. Front Immunol. 2016;12(7):426. doi:10.3389/fimmu.2016.00426
Meininger I, Carrasco A, Rao A, et al. Tissue-specific features of innate lymphoid cells. Trends Immunol. 2020;41(10):902-917.
Roediger B, Weninger W. Group 2 innate lymphoid cells in the regulation of immune responses. Adv Immunol. 2015;125:111-154.
Klose CS, Artis D. Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat Immunol. 2016;17(7):765-774.
Montaldo E, Juelke K, Romagnani C. Group 3 innate lymphoid cells (ILC3s): origin, differentiation, and plasticity in humans and mice. Eur J Immunol. 2015;45(8):2171-2182.
Trujillo CM, Muskus C, Arango J, Patiño PJ, Montoya CJ. Quantitative and functional evaluation of innate immune responses in patients with common variable immunodeficiency. J Investig Allergol Clin Immunol. 2011;21(3):207-215.
Ebbo M, Gérard L, Carpentier S, et al. Low circulating natural killer cell counts are associated with severe disease in patients with common variable immunodeficiency. EBioMedicine. 2016;6:222-230.
Kutukculer N, et al. A clinical and laboratory approach to the evaluation of innate immunity in pediatric CVID patients. Front Immunol. 2015;6:145.
Cols M, Rahman A, Maglione PJ, et al. Expansion of inflammatory innate lymphoid cells in patients with common variable immune deficiency. J Allergy Clin Immunol. 2016;137(4):1206-1215.e6.
Gottschalk TA, Tsantikos E, Hibbs ML. Pathogenic inflammation and its therapeutic targeting in systemic lupus erythematosus. Front Immunol. 2015;6:550.
Mace EM. Phosphoinositide-3-kinase signaling in human natural killer cells: new insights from primary immunodeficiency. Front Immunol. 2018;9:445.
Lougaris V, Patrizi O, Baronio M, et al. NFKB1 regulates human NK cell maturation and effector functions. Clin Immunol. 2017;175:99-108.
Yang LU, Xue X, Zeng T, et al. Novel biallelic TRNT1 mutations lead to atypical SIFD and multiple immune defects. Genes Dis. 2020;7(1):128-137.
Keller MD, Pandey R, Li D, et al. Mutation in IRF2BP2 is responsible for a familial form of common variable immunodeficiency disorder. J Allergy Clin Immunol. 2016;138(2):544-550 e4.
Geier CB, Kraupp S, Bra D, et al. Reduced numbers of circulating group 2 innate lymphoid cells in patients with common variable immunodeficiency. Eur J Immunol. 2017;47(11):1959-1969.
Magri G, Miyajima M, Bascones S, et al. Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat Immunol. 2014;15(4):354-364.
Moro K, Yamada T, Tanabe M, et al. Innate production of TH 2 cytokines by adipose tissue-associated c-Kit+ Sca-1+ lymphoid cells. Nature. 2010;463(7280):540-544.
Magri G, Cerutti A. Copycat innate lymphoid cells dampen gut inflammation. Cell Res. 2015;25(9):991-992.
Nussbaum JC, Van Dyken SJ, von Moltke J, et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013;502(7470):245-248.
Kamachi F, Isshiki T, Harada N, et al. ICOS promotes group 2 innate lymphoid cell activation in lungs. Biochem Biophys Res Comm. 2015;463(4):739-745.
Paclik D, Stehle C, Lahmann A, et al. ICOS regulates the pool of group 2 innate lymphoid cells under homeostatic and inflammatory conditions in mice. Eur J Immunol. 2015;45(10):2766-2772.
Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nat Immunol. 2006;7(3):293-301.
Suchanek O, Sadler R, Bateman EA, et al. Immunophenotyping of putative human B1 B cells in healthy controls and common variable immunodeficiency (CVID) patients. Clin Exp Immunol. 2012;170(3):333-341.
Abolhassani H. Specific immune response and cytokine production in CD70 Deficiency. Front Pediatr. 2021;9:615724.
Ghosh S, Köstel Bal S, Edwards ESJ, et al. Extended clinical and immunological phenotype and transplant outcome in CD27 and CD70 deficiency. Blood. 2020;136(23):2638-2655.
Abolhassani H, Edwards ESJ, Ikinciogullari A, et al. Combined immunodeficiency and Epstein-Barr virus-induced B cell malignancy in humans with inherited CD70 deficiency. J Exp Med. 2017;214(1):91-106.
Alkhairy OK, Perez-Becker R, Driessen GJ, et al. Novel mutations in TNFRSF7/CD27: clinical, immunologic, and genetic characterization of human CD27 deficiency. J Allergy Clin Immunol. 2015;136(3):703-712 e10.
Shortman K, Liu Y-J. Mouse and human dendritic cell subtypes. Nat Rev Immunol. 2002;2(3):151-161.
MacDonald KPA, Munster DJ, Clark GJ, et al. Characterization of human blood dendritic cell subsets. Blood. 2002;100(13):4512-4520.
Collin M, McGovern N, Haniffa M. Human dendritic cell subsets. Immunology. 2013;140(1):22-30.
Liu Y-J. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell. 2001;106(3):259-262.
Dubois B, Massacrier C, Vanbervliet B, et al. Critical role of IL-12 in dendritic cell-induced differentiation of naive B lymphocytes. J Immunol. 1998;161(5):2223-2231.
MacLennan IC, Vinuesa CG. Dendritic cells, BAFF, and APRIL: innate players in adaptive antibody responses. Immunity. 2002;17(3):235-238.
Jego G, Palucka AK, Blanck J-P, et al. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003;19(2):225-234.
Cerutti A, Qiao X, He B. Plasmacytoid dendritic cells and the regulation of immunoglobulin heavy chain class switching. Immunol Cell Biol. 2005;83(5):554-562.
Warnatz K, Voll R. Pathogenesis of autoimmunity in common variable immunodeficiency. Front Immunol. 2012;3(210). 10.3389/fimmu.2012.00210
Hall JC, Rosen A. Type I interferons: crucial participants in disease amplification in autoimmunity. Nat Rev Rheumatol. 2010;6(1):40-49.
Green NM, Marshak-Rothstein A. Toll-like receptor driven B cell activation in the induction of systemic autoimmunity. Semin Immunol. 2011;23(2):106-112.
Viallard JF, Camou F, André M, et al. Altered dendritic cell distribution in patients with common variable immunodeficiency. Arthritis Res Ther. 2005;7(5):R1052-R1055. doi:10.1186/ar1774
Taraldsrud E, Fevang B, Aukrust P, et al. Common variable immunodeficiency revisited: normal generation of naturally occurring dendritic cells that respond to Toll-like receptors 7 and 9. Clin Exp Immunol. 2014;175(3):439-448.
Yong PFK, Workman S, Wahid F, et al. Selective deficits in blood dendritic cell subsets in common variable immunodeficiency and X-linked agammaglobulinaemia but not specific polysaccharide antibody deficiency. Clin Immunol. 2008;127(1):34-42.
Sharifi L, Tavakolinia N, Kiaee F, et al. A review on defects of dendritic cells in common variable immunodeficiency. Endocr Metab Immune Disord Drug Targets. 2017;17(2):100-113.
Bayry J, Lacroix-Desmazes S, Kazatchkine MD, et al. Common variable immunodeficiency is associated with defective functions of dendritic cells. Blood. 2004;104(8):2441-2443. doi:10.1182/blood-2004-04-1325
Cunningham-Rundles C, Radigan L. Deficient IL-12 and dendritic cell function in common variable immune deficiency. Clin Immunol. 2005;115(2):147-153.
Cunningham-Rundles C, Radigan L, Knight AK, et al. TLR9 activation is defective in common variable immune deficiency. J Immunol. 2006;176(3):1978-1987.
Cytlak U, Resteu A, Bogaert D, et al. Ikaros family zinc finger 1 regulates dendritic cell development and function in humans. Nat Commun. 2018;9(1):1239.
Chien Y-H, Meyer C, Bonneville M. γδ T cells: first line of defense and beyond. Annu Rev Immunol. 2014;32:121-155.
Adams EJ, Gu S, Luoma AM. Human gamma delta T cells: evolution and ligand recognition. Cell Immunol. 2015;296(1):31-40.
Haas J, Ravens S, Düber S, et al. Development of interleukin-17-producing γδ T cells is restricted to a functional embryonic wave. Immunity. 2012;37(1):48-59.
Haas W, Pereira P, Tonegawa S. Gamma/delta cells. Annu Rev Immunol. 1993;11:637-685.
Foppoli M, Ferreri AJ. Gamma-delta t-cell lymphomas. Eur J Haematol. 2015;94(3):206-218.
Pauza CD, Poonia B, Li H, Cairo C, Chaudhry S. γδ T cells in HIV disease: past, present, and future. Front Immunol. 2015;5:687. doi:10.3389/fimmu.2014.00687
Paquin-Proulx D, Barsotti NS, Santos BAN, et al. Inversion of the Vδ1 to Vδ2 γδ T cell ratio in CVID is not restored by IVIg and is associated with immune activation and exhaustion. Medicine. 2016;95(30):e4304.
Powolny-Budnicka I, Riemann M, Tänzer S, Schmid RM, Hehlgans T, Weih F. RelA and RelB transcription factors in distinct thymocyte populations control lymphotoxin-dependent interleukin-17 production in γδ T cells. Immunity. 2011;34(3):364-374. doi:10.1016/j.immuni.2011.02.019
Kronenberg M. Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol. 2005;26:877-900.
Au-Yeung BB, Fowell DJ. A key role for Itk in both IFNγ and IL-4 production by NKT cells. J Immunol. 2007;179(1):111-119.
Carnaud C, Lee D, Donnars O, et al. Cutting edge: cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol. 1999;163(9):4647-4650.
Lang GA, Devera TS, Lang ML. Requirement for CD1d expression by B cells to stimulate NKT cell-enhanced antibody production. Blood. 2008;111(4):2158-2162.
Chan WL, Pejnovic N, Liew TV, et al. NKT cell subsets in infection and inflammation. Immunol Lett. 2003;85(2):159-163.
Yanagihara Y, Shiozawa K, Takai M, Kyogoku M, Shiozawa S. Natural killer (NK) T cells are significantly decreased in the peripheral blood of patients with rheumatoid arthritis (RA). Clin Exp Immunol. 1999;118(1):131-136.
Oishi Y, Sumida T, Sakamoto A, et al. Selective reduction and recovery of invariant Valpha24JalphaQ T cell receptor T cells in correlation with disease activity in patients with systemic lupus erythematosus. J Rheumatol. 2001;28(2):275-283.
Unutmaz D. NKT cells and HIV infection. Microbes Infect. 2003;5(11):1041-1047.
Carvalho KI, Melo KM, Bruno FR, et al. Skewed distribution of circulating activated natural killer T (NKT) cells in patients with common variable immunodeficiency disorders (CVID). PLoS One. 2010;5(9):e12652.
Sandberg JK, Stoddart CA, Brilot F, Jordan KA, Nixon DF. Development of innate CD4+ alpha-chain variable gene segment 24 (Valpha24) natural killer T cells in the early human fetal thymus is regulated by IL-7. Proc Natl Acad Sci U S A. 2004;101(18):7058-7063. doi:10.1073/pnas.0305986101
Arduini S, Dunne J, Conlon N, et al. Mucosal-associated invariant T cells are depleted and functionally altered in patients with common variable immunodeficiency. Clin Immunol. 2017;176:23-30.
Treiner E, Duban L, Bahram S, et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 2003;422(6928):164-169.
Kjer-Nielsen L, Patel O, Corbett AJ, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 2012;491(7426):717-723.
Ussher JE, Bilton M, Attwod E, et al. CD 161++ CD 8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+ IL-18 in a TCR-independent manner. Eur J Immunol. 2014;44(1):195-203.
Paquin-Proulx D, Santos BAN, Barsotti NS, et al. Loss of circulating mucosal-associated invariant T cells in common variable immunodeficiency is associated with immune activation and loss of Eomes and PLZF. ImmunoHorizons. 2017;1(7):142-155.
Leeansyah E, Ganesh A, Quigley MF, et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood. 2013;121(7):1124-1135.
Cambronero R, Sewell WAC, North ME, et al. Up-regulation of IL-12 in monocytes: a fundamental defect in common variable immunodeficiency. J Immunol. 2000;164(1):488-494.
North ME, Ivory K, Funauchi M, et al. Intracellular cytokine production by human CD4+ and CD8+ T cells from normal and immunodeficient donors using directly conjugated anti-cytokine antibodies and three-colour flow cytometry. Clin Exp Immunol. 1996;105(3):517-522.
Mannon PJ, Fuss IJ, Dill S, et al. Excess IL-12 but not IL-23 accompanies the inflammatory bowel disease associated with common variable immunodeficiency. Gastroenterology. 2006;131(3):748-756.
Timmermans WMC, van Laar JAM, van Hagen PM, et al. Immunopathogenesis of granulomas in chronic autoinflammatory diseases. Clin Transl Immunology. 2016;5(12):e118.
Aghamohammadi A, Abolhassani H, Hirbod-Mobarakeh A, et al. The uncommon combination of common variable immunodeficiency, macrophage activation syndrome, and cytomegalovirus retinitis. Viral Immunol. 2012;25(2):161-165.
Perelygina L, Plotkin S, Russo P, et al. Rubella persistence in epidermal keratinocytes and granuloma M2 macrophages in patients with primary immunodeficiencies. J Allergy Clin Immunol. 2016;138(5):1436-1439 e11.
Zhao Q, Jung LK. Frequency of CD19(+)CD24(hi)CD38(hi) regulatory B cells is decreased in peripheral blood and synovial fluid of patients with juvenile idiopathic arthritis: a preliminary study. Pediatr Rheumatol Online J. 2018;16:44.
Rodriguez-Zhurbenko N, Quach TD, Hopkins TJ, Rothstein TL, Hernandez AM. Human B-1 cells and B-1 cell antibodies change with advancing age. Front Immunol. 2019;10:483.
Valdez Y, Kyei SK, Poon GF, et al. Efficient enrichment of functional ILC subsets from human PBMC by immunomagnetic selection. J Immunol. 2018;200.
Schmid H, Schneidawind C, Jahnke S, et al. Culture-expanded human invariant natural killer T cells suppress T-cell alloreactivity and eradicate leukemia. Front Immunol. 2018;9:1817.
Chen P, Deng W, Li D, et al. Circulating mucosal-associated invariant T cells in a large cohort of healthy Chinese individuals from newborn to elderly. Front Immunol. 2019;10:260.
Hviid L, Akanmori BD, Loizon S, et al. High frequency of circulating γδ T cells with dominance of the Vδ1 subset in a healthy population. Int Immunol. 2000;12(6):797-805.