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Published in: Clinical and Experimental Medicine 1/2016

01-02-2016 | Original Article

Age-related differences in human palatine tonsillar B cell subsets and immunoglobulin isotypes

Authors: Jino Lee, Dong-Yeop Chang, Sang-Wook Kim, Yoon Seok Choi, Sea-Yuong Jeon, Vito Racanelli, Dae Woo Kim, Eui-Cheol Shin

Published in: Clinical and Experimental Medicine | Issue 1/2016

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Abstract

The tonsils provide defense of the upper aerodigestive tract against pathogens. Although long known to undergo functional changes with age, the precise changes occurring within tonsillar B cell populations remain undefined. In the present study, we investigated age-related changes in palatine tonsillar B cell subsets and immunoglobulin (Ig) isotypes. Palatine tonsils were obtained from forty-two tonsillectomy patients without tonsillitis who were divided into three groups: young children (4–9 years), adolescents (10–19 years), and adults (20–60 years). Tonsillar B cells were then analyzed by flow cytometry. Using expression of CD38 and IgD to define B cell subsets, we found that the frequency of germinal center (GC) B cells in the tonsils was significantly higher, and the frequency of memory B cells lower, in young children as compared to adolescents and adults. Within the GC B cell subsets, adults had a higher frequency of IgA+ cells and a lower frequency of IgM+ cells as compared to individuals in the younger age groups. Moreover, young children had a higher frequency of IgG+ cells in the GC B cell subsets than did individuals in the older age groups. We also observed an abundance of IgM+ cells among memory B cells and plasmablasts in young children and IgA+ cells in adults. In summary, the proportion of GC B cells in palatine tonsillar B cells decreases with age, while the proportion of memory B cells increases with age. In addition, Ig isotypes in tonsils preferentially switch from IgM to IgA as individuals age.
Literature
1.
go back to reference Surjan L Jr. Tonsils and lympho-epithelial structures in the pharynx as immuno-barriers. Acta Otolaryngol. 1987;103:369.PubMed Surjan L Jr. Tonsils and lympho-epithelial structures in the pharynx as immuno-barriers. Acta Otolaryngol. 1987;103:369.PubMed
2.
go back to reference Brandtzaeg P. Immunobarriers of the mucosa of the upper respiratory and digestive pathways. Acta Otolaryngol. 1988;105:172.CrossRefPubMed Brandtzaeg P. Immunobarriers of the mucosa of the upper respiratory and digestive pathways. Acta Otolaryngol. 1988;105:172.CrossRefPubMed
3.
go back to reference Korsrud FR, Brandtzaeg P. Immune systems of human nasopharyngeal and palatine tonsils: histomorphometry of lymphoid components and quantification of immunoglobulin-producing cells in health and disease. Clin Exp Immunol. 1980;39:361.PubMedPubMedCentral Korsrud FR, Brandtzaeg P. Immune systems of human nasopharyngeal and palatine tonsils: histomorphometry of lymphoid components and quantification of immunoglobulin-producing cells in health and disease. Clin Exp Immunol. 1980;39:361.PubMedPubMedCentral
4.
go back to reference Brandtzaeg P. Immunology of tonsils and adenoids: everything the ENT surgeon needs to know. Int J Pediatr Otorhinolaryngol. 2003;67(Suppl 1):S69.CrossRefPubMed Brandtzaeg P. Immunology of tonsils and adenoids: everything the ENT surgeon needs to know. Int J Pediatr Otorhinolaryngol. 2003;67(Suppl 1):S69.CrossRefPubMed
5.
go back to reference Van Kempen MJ, Rijkers GT, Van Cauwenberge PB. The immune response in adenoids and tonsils. Int Arch Allergy Immunol. 2000;122:8.CrossRefPubMed Van Kempen MJ, Rijkers GT, Van Cauwenberge PB. The immune response in adenoids and tonsils. Int Arch Allergy Immunol. 2000;122:8.CrossRefPubMed
6.
go back to reference Quiding-Jarbrink M, Granstrom G, Nordstrom I, Holmgren J, Czerkinsky C. Induction of compartmentalized B-cell responses in human tonsils. Infect Immun. 1995;63:853.PubMedPubMedCentral Quiding-Jarbrink M, Granstrom G, Nordstrom I, Holmgren J, Czerkinsky C. Induction of compartmentalized B-cell responses in human tonsils. Infect Immun. 1995;63:853.PubMedPubMedCentral
7.
go back to reference Wilson S, Norton P, Haverson K, Leigh J, Bailey M. Development of the palatine tonsil in conventional and germ-free piglets. Dev Comp Immunol. 2005;29:977.CrossRefPubMed Wilson S, Norton P, Haverson K, Leigh J, Bailey M. Development of the palatine tonsil in conventional and germ-free piglets. Dev Comp Immunol. 2005;29:977.CrossRefPubMed
8.
go back to reference Akcay A, Kara CO, Dagdeviren E, Zencir M. Variation in tonsil size in 4- to 17-year-old schoolchildren. J Otolaryngol. 2006;35:270.CrossRefPubMed Akcay A, Kara CO, Dagdeviren E, Zencir M. Variation in tonsil size in 4- to 17-year-old schoolchildren. J Otolaryngol. 2006;35:270.CrossRefPubMed
9.
go back to reference Papaioannou G, Kambas I, Tsaoussoglou M, Panaghiotopoulou-Gartagani P, Chrousos G, Kaditis AG. Age-dependent changes in the size of adenotonsillar tissue in childhood: implications for sleep-disordered breathing. J Pediatr. 2013;162:269.CrossRefPubMed Papaioannou G, Kambas I, Tsaoussoglou M, Panaghiotopoulou-Gartagani P, Chrousos G, Kaditis AG. Age-dependent changes in the size of adenotonsillar tissue in childhood: implications for sleep-disordered breathing. J Pediatr. 2013;162:269.CrossRefPubMed
12.
go back to reference Choi YS. Differentiation and apoptosis of human germinal center B-lymphocytes. Immunol Res. 1997;16(2):161–74.CrossRefPubMed Choi YS. Differentiation and apoptosis of human germinal center B-lymphocytes. Immunol Res. 1997;16(2):161–74.CrossRefPubMed
13.
go back to reference Mattila PS, Tarkkanen J. Age-associated changes in the cellular composition of the human adenoid. Scand J Immunol. 1997;45(4):423–7.CrossRefPubMed Mattila PS, Tarkkanen J. Age-associated changes in the cellular composition of the human adenoid. Scand J Immunol. 1997;45(4):423–7.CrossRefPubMed
14.
go back to reference Kolar GR, Mehta D, Wilson PC, Capra JD. Diversity of the Ig repertoire is maintained with age in spite of reduced germinal centre cells in human tonsil lymphoid tissue. Scand J Immunol. 2006;64(3):314–24.CrossRefPubMed Kolar GR, Mehta D, Wilson PC, Capra JD. Diversity of the Ig repertoire is maintained with age in spite of reduced germinal centre cells in human tonsil lymphoid tissue. Scand J Immunol. 2006;64(3):314–24.CrossRefPubMed
15.
go back to reference Gonzalez-Garcia I, Ocana E, Jimenez-Gomez G, Campos-Caro A, Brieva JA. Immunization-induced perturbation of human blood plasma cell pool: progressive maturation, IL-6 responsiveness, and high PRDI-BF1/BLIMP1 expression are critical distinctions between antigen-specific and nonspecific plasma cells. J Immunol. 2006;176(7):4042–50.CrossRefPubMed Gonzalez-Garcia I, Ocana E, Jimenez-Gomez G, Campos-Caro A, Brieva JA. Immunization-induced perturbation of human blood plasma cell pool: progressive maturation, IL-6 responsiveness, and high PRDI-BF1/BLIMP1 expression are critical distinctions between antigen-specific and nonspecific plasma cells. J Immunol. 2006;176(7):4042–50.CrossRefPubMed
16.
go back to reference Dorner T, Radbruch A. Antibodies and B cell memory in viral immunity. Immunity. 2007;27(3):384–92.CrossRefPubMed Dorner T, Radbruch A. Antibodies and B cell memory in viral immunity. Immunity. 2007;27(3):384–92.CrossRefPubMed
17.
go back to reference Valles-Ayoub Y, Govan HL III, Braun J. Evolving abundance and clonal pattern of human germinal center B cells during childhood. Blood. 1990;76(1):17–23.PubMed Valles-Ayoub Y, Govan HL III, Braun J. Evolving abundance and clonal pattern of human germinal center B cells during childhood. Blood. 1990;76(1):17–23.PubMed
18.
go back to reference Yamanaka N, Matsuyama H, Harabuchi Y, Kataura A. Distribution of lymphoid cells in tonsillar compartments in relation to infection and age. A quantitative study using image analysis. Acta Otolaryngol. 1992;112(1):128–37.CrossRefPubMed Yamanaka N, Matsuyama H, Harabuchi Y, Kataura A. Distribution of lymphoid cells in tonsillar compartments in relation to infection and age. A quantitative study using image analysis. Acta Otolaryngol. 1992;112(1):128–37.CrossRefPubMed
19.
20.
go back to reference Bourges D, Wang CH, Chevaleyre C, Salmon H. T and IgA B lymphocytes of the pharyngeal and palatine tonsils: differential expression of adhesion molecules and chemokines. Scand J Immunol. 2004;60(4):338–50.CrossRefPubMed Bourges D, Wang CH, Chevaleyre C, Salmon H. T and IgA B lymphocytes of the pharyngeal and palatine tonsils: differential expression of adhesion molecules and chemokines. Scand J Immunol. 2004;60(4):338–50.CrossRefPubMed
21.
go back to reference Paganelli R, Scala E, Quinti I, Ansotegui IJ. Humoral immunity in aging. Aging Clin Exp Res. 1994;6(3):143–50.CrossRef Paganelli R, Scala E, Quinti I, Ansotegui IJ. Humoral immunity in aging. Aging Clin Exp Res. 1994;6(3):143–50.CrossRef
22.
go back to reference McDonald KG, McDonough JS, Dieckgraefe BK, Newberry RD. Dendritic cells produce CXCL13 and participate in the development of murine small intestine lymphoid tissues. Am J Pathol. 2010;176(5):2367–77.CrossRefPubMedPubMedCentral McDonald KG, McDonough JS, Dieckgraefe BK, Newberry RD. Dendritic cells produce CXCL13 and participate in the development of murine small intestine lymphoid tissues. Am J Pathol. 2010;176(5):2367–77.CrossRefPubMedPubMedCentral
23.
go back to reference Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, Browning JL, Lipp M, Cyster JG. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature. 2000;406(6793):309–14.CrossRefPubMed Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, Browning JL, Lipp M, Cyster JG. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature. 2000;406(6793):309–14.CrossRefPubMed
24.
go back to reference Velaga S, Herbrand H, Friedrichsen M, Jiong T, Dorsch M, Hoffmann MW, Förster R, Pabst O. Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses. J Immunol. 2009;182(5):2610–9.CrossRefPubMed Velaga S, Herbrand H, Friedrichsen M, Jiong T, Dorsch M, Hoffmann MW, Förster R, Pabst O. Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses. J Immunol. 2009;182(5):2610–9.CrossRefPubMed
25.
go back to reference Kunkel EJ, Campbell DJ, Butcher EC. Chemokines in lymphocyte trafficking and intestinal immunity. Microcirculation. 2003;10(3–4):313–23.CrossRefPubMed Kunkel EJ, Campbell DJ, Butcher EC. Chemokines in lymphocyte trafficking and intestinal immunity. Microcirculation. 2003;10(3–4):313–23.CrossRefPubMed
26.
go back to reference McDonald KG, McDonough JS, Wang C, Kucharzik T, Williams IR, Newberry RD. CC chemokine receptor 6 expression by B lymphocytes is essential for the development of isolated lymphoid follicles. Am J Pathol. 2007;170(4):1229–40.CrossRefPubMedPubMedCentral McDonald KG, McDonough JS, Wang C, Kucharzik T, Williams IR, Newberry RD. CC chemokine receptor 6 expression by B lymphocytes is essential for the development of isolated lymphoid follicles. Am J Pathol. 2007;170(4):1229–40.CrossRefPubMedPubMedCentral
27.
go back to reference Ogra PL. Effect of tonsillectomy and adenoidectomy on nasopharyngeal antibody response to poliovirus. N Engl J Med. 1971;284(2):59–64.CrossRefPubMed Ogra PL. Effect of tonsillectomy and adenoidectomy on nasopharyngeal antibody response to poliovirus. N Engl J Med. 1971;284(2):59–64.CrossRefPubMed
28.
go back to reference Cantani A, Bellioni P, Salvinelli F, Businco L. Serum immunoglobulins and secretory IgA deficiency in tonsillectomized children. Ann Allergy. 1986;57(6):413–6.PubMed Cantani A, Bellioni P, Salvinelli F, Businco L. Serum immunoglobulins and secretory IgA deficiency in tonsillectomized children. Ann Allergy. 1986;57(6):413–6.PubMed
29.
go back to reference D’Amelio R, Palmisano L, Le Moli S, Seminara R, Aiuti F. Serum and salivary IgA levels in normal subjects: comparison between tonsillectomized and non-tonsillectomized subjects. Int Arch Allergy Appl Immunol. 1982;68(3):256–9.CrossRefPubMed D’Amelio R, Palmisano L, Le Moli S, Seminara R, Aiuti F. Serum and salivary IgA levels in normal subjects: comparison between tonsillectomized and non-tonsillectomized subjects. Int Arch Allergy Appl Immunol. 1982;68(3):256–9.CrossRefPubMed
30.
go back to reference Lenander-Lumikari M, Tenovuo J, Puhakka HJ, Malvaranta T, Ruuskanen O, Meurman O, Meurman P, Vilja P. Salivary antimicrobial proteins and mutans streptococci in tonsillectomized children. Pediatr Dent. 1992;14(2):86–91.PubMed Lenander-Lumikari M, Tenovuo J, Puhakka HJ, Malvaranta T, Ruuskanen O, Meurman O, Meurman P, Vilja P. Salivary antimicrobial proteins and mutans streptococci in tonsillectomized children. Pediatr Dent. 1992;14(2):86–91.PubMed
31.
go back to reference Childers NK, Powell WD, Tong G, Kirk K, Wiatrak B, Michalek SM. Human salivary immunoglobulin and antigen-specific antibody activity after tonsillectomy. Oral Microbiol Immunol. 2001;16(5):265–9.CrossRefPubMed Childers NK, Powell WD, Tong G, Kirk K, Wiatrak B, Michalek SM. Human salivary immunoglobulin and antigen-specific antibody activity after tonsillectomy. Oral Microbiol Immunol. 2001;16(5):265–9.CrossRefPubMed
32.
go back to reference Ikinciogullari A, Dogu F, Ikinciogullari A, Egin Y, Babacan E. Is immune system influenced by adenotonsillectomy in children? Int J Pediatr Otorhinolaryngol. 2002;66(3):251–7.CrossRefPubMed Ikinciogullari A, Dogu F, Ikinciogullari A, Egin Y, Babacan E. Is immune system influenced by adenotonsillectomy in children? Int J Pediatr Otorhinolaryngol. 2002;66(3):251–7.CrossRefPubMed
33.
go back to reference Van den Akker EH, Sanders EA, van Staaij BK, Rijkers GT, Rovers MM, Hoes AW, Schilder AG. Long-term effects of pediatric adenotonsillectomy on serum immunoglobulin levels: results of a randomized controlled trial. Ann Allergy Asthma Immunol. 2006;97(2):251–6.CrossRefPubMed Van den Akker EH, Sanders EA, van Staaij BK, Rijkers GT, Rovers MM, Hoes AW, Schilder AG. Long-term effects of pediatric adenotonsillectomy on serum immunoglobulin levels: results of a randomized controlled trial. Ann Allergy Asthma Immunol. 2006;97(2):251–6.CrossRefPubMed
Metadata
Title
Age-related differences in human palatine tonsillar B cell subsets and immunoglobulin isotypes
Authors
Jino Lee
Dong-Yeop Chang
Sang-Wook Kim
Yoon Seok Choi
Sea-Yuong Jeon
Vito Racanelli
Dae Woo Kim
Eui-Cheol Shin
Publication date
01-02-2016
Publisher
Springer International Publishing
Published in
Clinical and Experimental Medicine / Issue 1/2016
Print ISSN: 1591-8890
Electronic ISSN: 1591-9528
DOI
https://doi.org/10.1007/s10238-015-0338-5

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