#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Possibilities for the analysis of peripheral blood B cell subpopulations in a routine immunological laboratory


Authors: J. Štíchová 1;  J. Nechvátalová 1,2;  J. Litzman 1,2;  M. Vlková 1,2
Authors‘ workplace: Ústav klinické imunologie a alergologie, LF MU v Brně 1;  Ústav klinické imunologie a alergologie, Fakultní nemocnice u sv. Anny v Brně, Brno 2
Published in: Epidemiol. Mikrobiol. Imunol. 70, 2021, č. 4, s. 264-280
Category: Review Article

Overview

B cells play a vital role in the defence of the body against infectious agents. Apart from their ability to present antigen to T cells, B cells are mainly producers of antibodies. These play a crucial role in the effective elimination of infection and are also involved in the regulation of the immune response. The analysis of peripheral blood B cell subpopulations that makes it possible to monitor the development of B cells to the stage of antibody producing plasmablasts provides a valuable laboratory parameter which is important for both the study of the pathogenesis and diagnosis of some diseases. Laboratory analysis of B cell subpopulations is now a routinely available laboratory option thanks to the development of multicolour flow cytometry. This article summarizes the core knowledge which is currently applied to the analysis of B cell subpopulations in immunological laboratories.

Keywords:

B cell– flow cytometry – marginal zone of the spleen – germinal centre


Sources

1. Bousfiha A, Jeddane L, Picard C, et al. Human Inborn Errors of Immunity: 2019 Update of the IUIS Phenotypical Classification. J Clin Immunol, 2020;40(1):66–81.

2. Agematsu K, Futatani T, Hokibara S, et al. Absence of Memory B Cells in Patients with Common Variable Immunodeficiency. Clin Immunol, 2002;103(1):34–42.

3. Nechvatalova J, Pikulova Z, Stikarovska D, et al. B-lymphocyte Subpopulations in Patients with Selective IgA Deficiency. J Clin Immunol, 2012;32(3):441–448.

4. Novakova M, Zaliova M, Sukova M, et al. Loss of B cells and their precursors is the most constant feature of GATA-2 deficiency in childhood myelodysplastic syndrome. Haematologica, 2016;101(6):707–716.

5. Chovancova Z, Vlkova M, Litzman J, et al. Antibody forming cells and plasmablasts in peripheral blood in CVID patients after vaccination. Vaccine, 2011;29(24):4142–4150.

6. Wardowska A, Komorniczak M, Skoniecka A, et al. 2020. Alterations in peripheral blood B cells in systemic lupus erythematosus patients with renal insufficiency. Int Immunopharmacol, 2020;83:106451.

7. Bugatti S, Vitolo B, Caporali R, et al. B Cells in Rheumatoid Arthritis: From Pathogenic Players to Disease Biomarkers. Biomed Res Int, 2014;2014.

8. Hansen A, Daridon C, Dörner T. What do we know about memory B cells in primary Sjögren’s syndrome? Autoimmun Rev, 2010;9(9):600–603.

9. Wei Ch, Jenks S, Sanz I. Polychromatic flow cytometry in evaluating rheumatic disease patients. Arthritis Res Ther, 2015;17(1):46.

10. Hermiston ML, Xu Z, Weiss A. CD45: a critical regulator of signaling thresholds in immune cells. Annu Rev Immunol, 2003;21:107– 137.

11. Depoil D, Fleire S, Treanor BL, et al. CD19 is essential for B cell activation by promoting B cell receptor–antigen microcluster formation in response to membrane-bound ligand. Nat Immunol, 2008;9(1):63–72.

12. Quách TD, Rodríguez-Zhurbenko N, Hopkins TJ, et al. Distinctions among Circulating Antibody-Secreting Cell Populations, Including B-1 Cells, in Human Adult Peripheral Blood. J Immunol, 2016;196(3):1060–1069.

13. Walshe CA, Beers SA, French RR, et al. Induction of Cytosolic Calcium Flux by CD20 Is Dependent upon B Cell Antigen Receptor Signaling. J Biol Chem, 2008;283(25):16971–16984.

14. Burgueño-Bucio E, Mier-Aguilar AC, Soldevila G. The multiple faces of CD5. J Leukoc Biol, 2019;105(5):891–904.

15. Prieto JMB, Felippe JMB. Development, phenotype, and function of non-conventional B cells. Comp Immunol Microbiol Infect Dis, 2017;54:38–44.

16. Skrzypczynska KM, Zhu WJ, Weiss A. Positive Regulation of Lyn Kinase by CD148 Is Required for B Cell Receptor Signaling in B1 but Not B2 B Cells. Immunity, 2016;45(6):1232–1244.

17. Murphy K, Weaver C. Janeway’s immunobiology. New York and London: Garland Science; 2017.

18. Mensah FFK, Armstrong ChW, Reddy V, et al. CD24 Expression and B Cell Maturation Shows a Novel Link With Energy Metabolism: Potential Implications for Patients With Myalgic Encephalomyelitis/ Chronic Fatigue Syndrome. Front Immunol, 2018;9:2421.

19. Agematsu K, Hokibara S, Nagumo H, et al. CD27: a memory B-cell marker. Immunol Today, 2000;21(5):204–206.

20. Zhao, YJ, Lam CMCH, Lee HCH. The Membrane-Bound Enzyme CD38 Exists in Two Opposing Orientations. Sci Signa, 2012;5(241):ra67.

21. Loder BF, Bettina B, Ray JR, et al. B Cell Development in the Spleen Takes Place in Discrete Steps and Is Determined by the Quality of B Cell Receptor–Derived Signals. J Exp Med, 1999:190(1):75–90.

22. Kalina T, Flores-Montero J, Van Der Velden VHJ, et al. EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols. Leukemia, 2012;26(9):1986– 2010.

23. Wehr C, Kivioja T, Schmitt Ch, et al. The EUROclass trial: defining subgroups in common variable immunodeficiency. Blood, 2008; 111(1):77–85.

24. Buffa S, Pellicanò M, Bulati M, et al. A novel B cell population revealed by a CD38/CD24 gating strategy: CD38−CD24− B cells in centenarian offspring and elderly people. Age, 2013;35(5):2009– 2024.

25. Palanichamy A, Barnard J, Zheng B, et al. Novel Human Transitional B Cell Populations Revealed by B Cell Depletion Therapy. J Immunol, 2009:182(10):5982–5993.

26. Schroeder HW, Radbruch A, Berek C. 7 - B-Cell Development and Differentiation. In: Clinical Immunology (Fifth Edition) London: Elsevier; 2019. s. 107–118.

27. Klein U, Rajewsky K, Küppers R. Human Immunoglobulin (Ig) M+IgD+ Peripheral Blood B Cells Expressing the CD27 Cell Surface Antigen Carry Somatically Mutated Variable Region Genes: CD27 as a General Marker for Somatically Mutated (Memory) B Cells. J Ex Med, 1998;188(9):1679–1689.

28. Carsetti R, Köhler G, Lamers MC. Transitional B cells are the target of negative selection in the B cell compartment. J Exp Med, 1995;181(6):2129–2140.

29. Allman DM, Ferguson SE, Cancro MP. Peripheral B cell maturation. I. Immature peripheral B cells in adults are heat-stable antigenhi and exhibit unique signaling characteristics. J Immunol, 1992;149(8):2533–2540.

30. Garcia‐Prat M, Álvarez‐Sierra D, Aguiló‐Cucurull A, et al. Extended immunophenotyping reference values in a healthy pediatric population. Cytometry B Clin Cytom, 2019;96(3):223–233.

31. Marie-Cardine A, Divay F, Dutot I, et al. Transitional B cells in humans: Characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin Immunol, 2008;127(1):14–25.

32. Piątosa B, Wolska‐Kuśnierz B, Pac M, et al. B cell subsets in healthy children: Reference values for evaluation of B cell maturation process in peripheral blood. Cytometry B Clin Cytom, 2010;78B(6):372–381.

33. Tangye SG, Liu YJ, Aversa G, et al. 1998. Identification of Functional Human Splenic Memory B Cells by Expression of CD148 and CD27. J Ex Med, 1998;188(9):1691–1703.

34. Weller S, Braun MC, Tan BK, et al. Human blood IgM “memory” B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood, 2004;104(12):3647–3654.

35. Kruetzmann S, Rosado MM, Weber H, et al. Human Immunoglobulin M Memory B Cells Controlling Streptococcus pneumoniae Infections Are Generated in the Spleen. J Ex Med, 2003;197(7):939–945.

36. Weller S, Mamani-Matsuda M, Picard C, et al. Somatic diversification in the absence of antigen-driven responses is the hallmark of the IgM+IgD+CD27+ B cell repertoire in infants. J Ex Med, 2008;205(6):1331–1342.

37. Ticha O, Moos L, Wajant H, et al. 2018. Expression of Tumor Necrosis Factor Receptor 2 Characterizes TLR9-Driven Formation of Interleukin-10-Producing B Cells. Front Immunol, 2018;8:1951.

38. Weller S, Faili A, Garcia C, et al. CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc Natl Acad Sci USA, 2001; 98(3):1166– 1170.

39. Martinez-Gamboa L, Mei H, Loddenkemper CH, et al. Role of the spleen in peripheral memory B-cell homeostasis in patients with autoimmune thrombocytopenia purpura. Clin Immunol, 2009;130(2):199–212.

40. Scheeren FA, Nagasawa M, Weijer K, et al. T cell–independent development and induction of somatic hypermutation in human IgM+IgD+CD27+ B cells. J Ex Med, 2008;205(9):2033–2042.

41. Noviski M, Zikherman J. Control of autoreactive B cells by IgM and IgD B cell receptors: maintaining a fine balance. Curr Opin Immunol, 2018;55:67–74.

42. Sabouri Z, Perotti S, Spierings E, et al. IgD attenuates the IgM-induced anergy response in transitional and mature B cells. Nat Commun, 2016;7(1):13381.

43. Blanco E, Pérez-Andrés M, Arriba-Méndez S, et al. Defects in memory B-cell and plasma cell subsets expressing different immunoglobulin-subclasses in patients with CVID and immunoglobulin subclass deficiencies. J Allergy Clin Immunol, 2019;144(3):809–824.

44. Finocchi A, Di Cesare S, Romiti ML, et al. Humoral immune responses and CD27+ B cells in children with DiGeorge syndrome (22q11.2 deletion syndrome). Pediatr Allergy Immunol, 2006;17(5):382–388.

45. Klocperk A, Parackova Z, Bloomfield M, et al. Follicular Helper T Cells in DiGeorge Syndrome. Front Immunol, 2018;9:1730.

46. Palm Ak E, Henry C. Remembrance of Things Past: Long-Term B Cell Memory After Infection and Vaccination. Front Immunol, 2019;10:1787.

47. Vidarsson G, Dekkers G, Trispens T. IgG Subclasses and Allotypes: From Structure to Effector Functions. Front Immunol, 2014;5:520.

48. Lebon A, Verkaik NJ, Labout JAM, et al. Natural Antibodies against Several Pneumococcal Virulence Proteins in Children during the Pre-Pneumococcal-Vaccine Era: the Generation R Study. Infect Immun, 2011;79(4):1680–1687.

49. Grimsholm O, Piano Mortari E, Davydov AN, et al. The Interplay between CD27dull and CD27bright B Cells Ensures the Flexibility, Stability, and Resilience of Human B Cell Memory. Cell Rep, 2020;30(9):2963–2977.

50. Knox JJ, Myles A, Cancro MP. T-bet+ memory B cells: Generation, function, and fate. Immunol Rev, 2019;288(1):149–160.

51. Van Dongen JJM, Van Der Burg M, Kalina T, et al. EuroFlow-Based Flowcytometric Diagnostic Screening and Classification of Primary Immunodeficiencies of the Lymphoid System. Front Immunol, 2019;10:1271.

52. Van Der Burg M, Kalina T, Perez-Andres M. The EuroFlow PID Orientation Tube for Flow Cytometric Diagnostic Screening of Primary Immunodeficiencies of the Lymphoid System. Front Immunol, 2019;10:246.

53. Delmonte O, Schuetz C, Notarangelo L. RAG Deficiency: Two Genes, Many Diseases. J Clin Immunol, 2018;38(6):646–655.

54. Siala N, Azzabi O, Kebaier H, et al. Omenn syndrome: two case reports. Acta Dermatovenerol Croat, 2013;21(4):259– 262.

55. Puel A, Leonard JW. Mutations in the gene for the IL-7 receptor result in T–B+NK+ severe combined immunodeficiency disease. Curr Opin Immunol, 2000;12(4):468–473.

56. Ege M, Ma Y, Manfras B, et al. Omenn syndrome due to ARTEMIS mutations. Blood, 2005; 105(11):4179–4186.

57. Giliani S, Mori L, Basile G, et al. Interleukin-7 receptor α (IL-7Rα) deficiency: cellular and molecular bases. Analysis of clinical, immunological, and molecular features in 16 novel patients. Immunol Rev, 2005;203(1):110–126.

58. Rossberg S, Schwarz K, Meisel C, et al. Delayed Onset of (Severe) Combined Immunodeficiency (S)CID (T-B+NK+): Complete IL-7 Receptor Deficiency in a 22 Months Old Girl. Klin Padiatr, 2009;221(6):339–343.

59. Lim CHK, Abolhassani H, Appelberg KS, et al. IL2RG hypomorphic mutation: identification of a novel pathogenic mutation in exon 8 and a review of the literature. Allergy Asthma Clin Immunol, 2019;15(2).

60. Ma C, Pittaluga S, Avery TD, et al. Selective generation of functional somatically mutated IgM+CD27+, but not Ig isotype- switched, memory B cells in X-linked lymphoproliferative disease. J Clinl Invest, 2006;116(2):322–333.

61. Ma C, Hare JN, Nichols KE, et al. Impaired humoral immunity in X-linked lymphoproliferative disease is associated with defective IL-10 production by CD4+ T cells. J Clin Invest, 2005;115(4):1049–1059.

62. Cuss AK, Avery DT, Cannons LJ, et al. Expansion of Functionally Immature Transitional B Cells Is Associated with Human-Immunodeficient States Characterized by Impaired Humoral Immunity. J Immunol, 2006;176(3):1506–1516.

63. Menard L, Cantaert T, Chamberlain N, et al. Signaling lymphocytic activation molecule (SLAM)/SLAM-associated protein pathway regulates human B-cell tolerance. J Allergy Clin Immunol, 2014;133(4):1149–1161.

64. Sharifinejad N, Jamee M, Zaki-Dizaji M, et al. Clinical, Immunological, and Genetic Features in 49 Patients With ZAP-70 Deficiency: A Systematic Review. Front Immunol, 2020;11:831.

65. Engelhardt KR, Gertz EM, Keles S, et al. The extended clinical phenotype of 64 patients with dedicator of cytokinesis 8 deficiency. J Allergy Clin Immunol, 2015;136(2):402–412.

66. Somech R, Lev A, Grisaru-Soen G, et al. Purine nucleoside phosphorylase deficiency presenting as severe combined immune deficiency. Immunol Res, 2013;56(1):150–154.

67. Agematsu K, Nagumo H, Shinozaki K, et al. Absence of IgD- -CD27(+) memory B cell population in X-linked hyper-IgM syndrome. J Clin Invest, 1998;102(4):853–860.

68. Tsai H, Yu HH, Chien YH, et al. X-linked hyper-IgM syndrome with CD40LG mutation: Two case reports and literature review in Taiwanese patients. J Microbiol Immunol, 2015;48(1):113– 118.

69. Ameratunga R, Woon ST, Koopmans W, et al. Cellular and Molecular Characterisation of the Hyper Immunoglobulin M Syndrome Associated with Congenital Rubella Infection. J Clin Immunol, 2008;29(1):99–106.

70. Torres JM, Martinez-Barricarte R, García-Gómez S, et al. Inherited BCL10 deficiency impairs hematopoietic and nonhematopoietic immunity. J Clin Invest, 2014;124(12):5239–5248.

71. Çipe FE, Aydogmus C, Babayigit Hocaoglu A, et al. Cernunnos/ XLF Deficiency: A Syndromic Primary Immunodeficiency. Case Rep Pediatr, 2014;2014:614238.

72. Sharifinejad N, Jamee M, Zaki-Dizaji M, et al. Cernunnos deficiency: a case report. J Investig Allergol Clin Immunol, 2011;21(4):313–316.

73. Staples ER, McDermott EM, Reiman A, et al. Immunodeficiency in ataxia telangiectasia is correlated strongly with the presence of two null mutations in the ataxia telangiectasia mutated gene. Clin Exp Immunol, 2008;153(2):214–220.

74. Stefano AD, Boldt A, Schmiedel L, et al. Flow cytometry as an important tool in the diagnosis of immunodeficiencies demonstrated in a patient with ataxia-telangiectasia. Lab Medizin, 2016;40(4):255–261.

75. Pereira CTM, Bichuetti-Silva DC, Da Mota NVF, et al. B-cell subsets imbalance and reduced expression of CD40 in ataxia-telangiectasia patients. Allergol Immunopathol, 2018;46(5):438–446.

76. Heller S, Kölsch U, Magg T, et al. T Cell Impairment Is Predictive for a Severe Clinical Course in NEMO Deficiency. J Clin Immunol, 2020;40(3):421–434.

77. Chandrakasan S, Marsh AR, Uzel G, et al. Outcome of patients with NEMO deficiency following allogeneic hematopoietic cell transplant. J Allergy Clin Immunol, 2017;139(3):1040–1043.

78. Park JY, Shcherbina A, Rosen FS, et al. Phenotypic perturbation of B cells in the Wiskott–Aldrich syndrome. Clin Exp Immunol, 2005;139(2):297–305.

79. Simon KL, Anderson SM, Garabedian KE, et al. Molecular and phenotypic abnormalities of B lymphocytes in patients with Wiskott- Aldrich syndrome. J Allergy Clin Immunol, 2014;133(3):896– 899.

80. Castiello MC, Bosticardo M, Pala F, et al. Wiskott–Aldrich Syndrome protein deficiency perturbs the homeostasis of B-cell compartment in humans. J Autoimmun, 2014;50:42–50.

81. McCann LJ, McPartland J, Barge D, et al. Phenotypic Variations of Cartilage Hair Hypoplasia: Granulomatous Skin Inflammation and Severe T Cell Immunodeficiency as Initial Clinical Presentation in Otherwise Well Child with Short Stature. J Clin Immunol, 2014;34(1):42–48.

82. Kostjukovits S, Klemetti P, Valta H, et al. Analysis of clinical and immunologic phenotype in a large cohort of children and adults with cartilage-hair hypoplasia. J Allergy Clin Immunol, 2017;140(2):612–614.

83. Sullivan KE, McDonald-McGinn D, Driscoll AD, et al. Longitudinal Analysis of Lymphocyte Function and Numbers in the First Year of Life in Chromosome 22q11.2 Deletion Syndrome (DiGeorge Syndrome/Velocardiofacial Syndrome). Clin Diagn Lab Immunol, 1999;6(6):906–911.

84. Giardino G, Radwan N, Koletsi P, et al. Clinical and immunological features in a cohort of patients with partial DiGeorge syndrome followed at a single center. Blood, 2019;133(24):2586–2596.

85. Sigmon JR, Kasasbeh E, Krishnaswamy G. X-linked agammaglobulinemia diagnosed late in life: case report and review of the literature. Clin Mol Allergy, 2008;6(1):5.

86. Alkhairy OK, Perez-Becker R, Driessen JG, 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.

87. Van Montfrans JM, Hoepelman IMA, Otto S, et al. CD27 deficiency is associated with combined immunodeficiency and persistent symptomatic EBV viremia. J Allergy Clin Immunol, 2012;129(3):787–793.

88. Celiksoy MH, Yildiran A. A comparison of B cell subsets in primary immune deficiencies that progress with antibody deficiency and age-matched healthy children. Allergol Immunopathol, 2016;44(4):331–340.

89. Singh A, Joshi V, Jindal KA, et al. An updated review on activated PI3 kinase delta syndrome (APDS). Genes Dis, 2020;7(1):67–74.

90. Thouenon R, Moreno-Corona N, Poggi L, et al. Activated PI3Kinase Delta Syndrome – A Multifaceted Disease. Front Pediatr, 2021;9:652405.

91. Shim J, Park S, Chandrakasan S. Early B Cell Development Is Impaired in Patients with Active Hemophagocytic Lymphohistiocytosis. Blood, 2017;130(1):1006.

92. Speckmann C, Enders A, Woellner C, et al. Reduced memory B cells in patients with hyper IgE syndrome. Clin Immunol, 2008;129(3):448–454.

93. Een W, Krätz EC, McKenzie IC, et al. Impaired memory B-cell development and antibody maturation with a skewing toward IgE in patients with STAT3 hyper-IgE syndrome. Allergy, 2019;74(12):2394–2405.

94. Martin E, Minet N, Boschatca, et al. Impaired lymphocyte function and differentiation in CTPS1-deficient patients result from a hypomorphic homozygous mutation. JCI Insight, 2020;5(5):e133880.

95. Bleesing JJH, Brown RM, Straus, ES, et al. Immunophenotypic profiles in families with autoimmune lymphoproliferative syndrome. Blood, 2001;98(8):2466–2473.

96. Bleesing JJ, Souto-Carneiro MM, Savage JW, et al. Patients with Chronic Granulomatous Disease Have a Reduced Peripheral Blood Memory B Cell Compartment. J Immunol, 2006;176(11):7096–7103.

97. Moir S, De Ravin SS, Santich HB, et al. Humans with chronic granulomatous disease maintain humoral immunologic memory despite low frequencies of circulating memory B cells. Blood, 2012;120(24):4850–4858.

98. Novakova M, Janda A, Wlodarski WM, et al. Defect in B Cell Production Driven By GATA2 Mutation Results in Their Absolute Reduction and Mature Phenotype in Pediatric Patients. Blood, 2014;124(21):2746.

99. McGuire PJ, Cunningham-Rundles CH, Ochs H, et al. Oligoclonality, impaired class switch and B-cell memory responses in WHIM syndrome. Clin Immunol, 2010;135(3):412–421.

100. Kawai T, Malech LH. WHIM Syndrome: Congenital Immune Deficiency Disease. Curr opin hematol, 2009;16(1):20–26.

101. Gulino AV, Moratto D, Sozzani S, et al. Altered leukocyte response to CXCL12 in patients with warts hypogammaglobulinemia, infections, myelokathexis (WHIM) syndrome. Blood, 2004;104(2):444–452.

102. Romberg N, Morbach H, Lawrence GM, et al. Gain-of-function STAT1 mutations are associated with PD-L1 overexpression and a defect in B-cell survival. J Allergy Clin Immunol, 2013;131(6):1691–1693.

103. Nemoto K, Kawanami T, Hoshina T, et al. Impaired B-Cell Differentiation in a Patient With STAT1 Gain-of-Function Mutation. Front Immunol, 2020;11:557521.

104. Zhang W, Chen X, Gao G, et al. Clinical Relevance of Gain- and Loss-of-Function Germline Mutations in STAT1: A Systematic Review. Front Immunol, 2021;12:654406.

105. Weller S, Bonnet M, Delagreverie H, et al. IgM+IgD+CD27+ B cells are markedly reduced in IRAK-4–, MyD88-, and TIRAP- but not UNC-93B–deficient patients. Blood, 2012;120(25):4992–5001.

106. Nishimura S, Kobayashi Y, Ohnishi H, et al. IRAK4 Deficiency Presenting with Anti-NMDAR Encephalitis and HHV6 Reactivation. J Clin Immunol, 2021;41(1):125–135.

107. Gobin K, Hintermeyer M, Boisson B, et al. IRAK4 Deficiency in a Patient with Recurrent Pneumococcal Infections: Case Report and Review of the Literature. Front Pediatr, 2017;5:83.

108. Moura RA, Weinmann P, Pereira AP, et al. Alterations on peripheral blood B-cell subpopulations in very early arthritis patients. Rheumatology, 2010;49(6):1082–1092.

109. Wang Y, Lloyd AK, Melas I, et al. Rheumatoid arthritis patients display B-cell dysregulation already in the naïve repertoire consistent with defects in B-cell tolerance. Sci Rep, 2019;9(1):19995.

110. Fedele AL, Tolusso B, Gremese E, et al. Memory B cell subsets and plasmablasts are lower in early than in long-standing Rheumatoid Arthritis. BMC Immunol, 2014;15:28.

111. DÖRNER T, JACOBI MA, LEE J et al. Abnormalities of B cell subsets in patients with systemic lupus erythematosus. J Immunol Methods, 2011;363(2):187–197.

112. Henning S, Lambers MW, Doornbos-Van Der Meer B, et al. Proportions of B-cell subsets are altered in incomplete systemic lupus erythematosus and correlate with interferon score and IgG levels. Rheumatology, 2020;59(9):2616–2624.

113. Jin W, Luo Z, Yang H. Peripheral B Cell Subsets in Autoimmune Diseases: Clinical Implications and Effects of B Cell-Targeted Therapies. J Immunol Res, 2020;2020:e9518137.

114. Piper CHJM, Wilkinson GLM, Deakin TC, et al. CD19+CD24hiCD38hi B Cells Are Expanded in Juvenile Dermatomyositis and Exhibit a Pro-Inflammatory Phenotype After Activation Through Toll-Like Receptor 7 and Interferon-α. Front Immunol, 2018;9:1372.

115. Young-Glazer J, Cisneros A, Wilfong ME, et al. Jo-1 autoantigen- specific B cells are skewed towards distinct functional B cell subsets in anti-synthetase syndrome patients. Arthritis Res Ther, 2021;23:33.

116. Ibrahem HM. B-cell dysregulation in primary Sjögren’s syndrome: A review. Jpn Dent Sci Rev, 2019;55(1):139–144.

117. Le Pottier L, Devauchelle V, Pers JO, et al. The mosaic of B-cell subsets (with special emphasis on primary Sjögren’s syndrome). Autoimmun Rev, 2007;6(3):149–154.

118. Nocturne G, Mariette X. B cells in the pathogenesis of primary Sjögren syndrome. Nat Rev Rheumatol, 2018;14(3):133–145.

119. Kraaij MD, Van Laar JM. The role of B cells in systemic sclerosis. Biol: Targets Ther, 2008;2(3):389–395.

120. Soto L, Ferrier A, Aravena AO, et al. Systemic sclerosis patients present alterations in the expression of molecules involved in B cell regulation. Front Immunol, 2015;6:496.

121. Hajas A, Barath S, Szodoray P, et al. Derailed B cell homeostasis in patients with mixed connective tissue disease. Hum Immunol, 2013;74(7):833–841.

122. Alvarez-Rodriguez L, Riancho-Zarrabeitia L, Calvo-Alén J, et al. Peripheral B-Cell Subset Distribution in Primary Antiphospholipid Syndrome. Int J Mol Sci, 2018;19(2):589.

123. Reincke ME, Payne JK, Harder I, et al. The Antigen Presenting Potential of CD21low B Cells. Front Immunol, 2020;11:535784.

124. Hisada RYO, Kato M, Sugawara ERI, et al. Circulating plasmablasts contribute to antiphospholipid antibody production, associated with type I interferon upregulation. J Thromb Haemost, 2019;17(7):1134–1143.

125. Kamphuis LS, Van Zelm CM, Lam HK, et al. Perigranuloma Localization and Abnormal Maturation of B Cells: emerging key players in sarcoidosis? Am J Respir Crit Care Med, 2013;187(4):406– 416.

126. Saussine A, Tazi A, Feuillet S, et al. Active Chronic Sarcoidosis is Characterized by Increased Transitional Blood B Cells, Increased IL-10-Producing Regulatory B Cells and High BAFF Levels. PLoS One, 2012;7(8):e43588.

127. Timmermans WMC, Laar AMJ, Houwen BT, et al. B-Cell Dysregulation in Crohn’s Disease Is Partially Restored with Infliximab Therapy. PLoS One, 2016;11(7):e0160103.

128. Pararasa CH, Zhang N, Tull JT, et al. Reduced CD27−IgD− B Cells in Blood and Raised CD27−IgD− B Cells in Gut-Associated Lymphoid Tissue in Inflammatory Bowel Disease. Front Immunol, 2019;10:361.

129. Rabe H, Malmquist M, Barkman C, et al. Distinct patterns of naive, activated and memory T and B cells in blood of patients with ulcerative colitis or Crohn’s disease. Clin Exp Immunol, 2019;197(1):111–129.

130. Hosomi S, Oshitani N, Kamata N, et al. Increased numbers of immature plasma cells in peripheral blood specifically overexpress chemokine receptor CXCR3 and CXCR4 in patients with ulcerative colitis. Clin Exp Immunol, 2011;63(2):215–224.

131. Bures J. Memory B lymphocytes in peripheral blood in coeliac disease: a pilot study. Gastroenterol Hepatol, 2019;73(4):296– 302.

132. Renand A, Habes S, Mosnier JF, et al. Immune Alterations in Patients With Type 1 Autoimmune Hepatitis Persist Upon Standard Immunosuppressive Treatment. Hepatol Commun, 2018;2(8):972–985.

133. Ma L, Qin J, Ji H, et al. Tfh and plasma cells are correlated with hypergammaglobulinaemia in patients with autoimmune hepatitis. Liver Int, 2014;34(3):405–415.

134. Li Y, Wang W, Tang L, et al. Chemokine (C-X-C motif ) ligand 13 promotes intrahepatic chemokine (C-X-C motif ) receptor 5+ lymphocyte homing and aberrant B-cell immune responses in primary biliary cirrhosis. Hepatology, 2015;61(6):1998– 2007.

135. Zhang J, Zhang W, Leung SCP, et al. Ongoing activation of autoantigen- specific B cells in primary biliary cirrhosis. Hepatology, 2014;60(5):1708–1716.

136. Liu Y, Gong Y, Qu CH, et al. CD32b expression is down-regulated on double-negative memory B cells in patients with Hashimoto’s thyroiditis. Mol Cell Endocrinol, 2017;440:1–7.

137. Yu S, Qi Y, Wang H, et al. Dysfunction of CD24+CD38+ B cells in patients with Hashimoto’s thyroiditis is associated with a lack of interleukin 10. Int J Biochem Cell Biol, 2017;90:114–120.

138. Ruschil CH, Gabernet G, Lepennetier G, et al. Specific Induction of Double Negative B Cells During Protective and Pathogenic Immune Responses. Front Immunol, 2020;11:606338.

139. Van Der Weerd K, Van Hagen MP, Schrijver B, et al. The peripheral blood compartment in patients with Graves’ disease: activated T lymphocytes and increased transitional and pre-naive mature B lymphocytes. Clin Exp Immunol, 2013;174(2):256–264.

140. Mori H, Amino N, Iwatani Y, et al. Increase of peripheral B lymphocytes in Graves’ disease. Clin Exp Immunol, 1980;42(1):33–40.

141. Deng CH, Xiang Y, Tan T, et al. Altered Peripheral B-Lymphocyte Subsets in Type 1 Diabetes and Latent Autoimmune Diabetes in Adults. Diabetes Care, 2016;39(3):434–440.

142. Hanley P, Sutter AJ, Goodman GN, et al. Circulating B cells in type 1 diabetics exhibit fewer maturation-associated phenotypes. Clin Immunol, 2017;183:336–343.

143. Roberto P, Lobreglio G, Rosatelli CM, et al. Immunophenotypic Characterisation of Peripheral Blood Lymphocytes in Autoimmune Polyglandular Syndrome Type 1: Clinical Study and Review of the Literature. J Pediatr Endocrinol Metab, 2005;18(2):155–164.

144. Wolff ASB, Oftedal VEB, Kisand K, et al. Flow Cytometry Study of Blood Cell Subtypes Reflects Autoimmune and Inflammatory Processes in Autoimmune Polyendocrine Syndrome Type I. Scand J Immunol, 2010;71(6):459–467.

145. Kohler S, Keil POT, Swierzy M, et al. Disturbed B cell subpopulations and increased plasma cells in myasthenia gravis patients. J Neuroimmunol, 2013;264(1):114–119.

146. Hu Y, Wang J, Rao J, et al. Comparison of peripheral blood B cell subset ratios and B cell-related cytokine levels between ocular and generalized myasthenia gravis. Int Immunopharmacol, 2020;80:106130.

147. Kubota A, Izaki S, Fukaura H, et al. Circulating memory B cells are reduced in patients with late-onset myasthenia gravis. Clin Exp Neuroimmunol, 2015;6(3):322–329

148. Golinski ML, Demeules M, Derambure C, et al. CD11c+ B Cells Are Mainly Memory Cells, Precursors of Antibody Secreting Cells in Healthy Donors. Front Immunol, 2020;11:32.

149. Mouquet H, Musette P, Gougeon LM, et al. B-Cell Depletion Immunotherapy in Pemphigus: Effects on Cellular and Humoral Immune Responses. J Investe Dermatol, 2008;128(12):2859– 2869.

150. Lu J, Ding Y, Yi X, et al. CD19+ B cell subsets in the peripheral blood and skin lesions of psoriasis patients and their correlations with disease severity. Braz J Med Biol Res, 2016;49(9):e5374.

151. Czarnowicki T, Gonzalez J, Bonifacio MK, et al. Diverse activation and differentiation of multiple B-cell subsets in patients with atopic dermatitis but not in patients with psoriasis. J Allergy Clin Immunol, 2016;137(1):118–129.

152. Habib J, Deng J, Lava N, et al. Blood B Cell and Regulatory Subset Content in Multiple Sclerosis Patients. J mult Scler, 2015;2(2):1000139.

153. Yilmaz V, Tura AD, Ulusoy C, et al. Flow cytometry analysis of peripheral blood B cell distribution of patients with multiple sclerosis. Turk J Neurol, 2017;23:219–224.

154. Claes N, Fraussen J, Vanheusden M, et al. Age-Associated B Cells with Proinflammatory Characteristics Are Expanded in a Proportion of Multiple Sclerosis Patients. J Immunol, 2016;197(12):4576–4583.

Labels
Hygiene and epidemiology Medical virology Clinical microbiology

Article was published in

Epidemiology, Microbiology, Immunology

Issue 4

2021 Issue 4

Most read in this issue
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#