Differential Effects of Environmental and Genetic Factors on T and B Cell Immune Traits

Cell Reports

Volumn 17, Issue 9, 2016, Pages 2474-2487

  Aguirre Gamboa, Raul ^a   Joosten, Irma ^b   Urbano, Paulo C M ^b   van der Molen, Renate G ^b   van Rijssen, Esther ^b   van Cranenbroek, Bram ^b   Oosting, Marije ^b   Smeekens, Sanne ^b   Jaeger, Martin ^b   Zorro, Maria ^a   Withoff, Sebo ^a   van Herwaarden, Antonius E ^b   Sweep, Fred C G J ^b   Netea, Romana T ^b   Swertz, Morris A ^a   Franke, Lude ^a   Xavier, Ramnik J ^c,d   Joosten, Leo A B ^b   Netea, Mihai G ^b   Wijmenga, Cisca ^a,e   Kumar, Vinod ^a   Li, Yang ^a   Koenen, Hans J P M ^b   more..

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; LONG UNTRANSLATED RNA; MYO1B PROTEIN, HUMAN; MYOSIN I; PDE4A PROTEIN, HUMAN; PHOSPHODIESTERASE IV;

ADULT; AGE; AGED; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; COHORT ANALYSIS; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; FEMALE; GENE LOCUS; GENETIC ASSOCIATION; HERITABILITY; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOGLOBULIN BLOOD LEVEL; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SEQUENCE ANALYSIS; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; ADOLESCENT; CELLULAR IMMUNITY; ENVIRONMENT; GENETICS; HUMAN CHROMOSOME; HUMORAL IMMUNITY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; NETHERLANDS; QUANTITATIVE TRAIT LOCUS; SEASON; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; AGED; B-LYMPHOCYTES; CHROMOSOMES, HUMAN; COHORT STUDIES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; ENVIRONMENT; FEMALE; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOGLOBULINS; LYMPHOCYTE COUNT; LYMPHOCYTE SUBSETS; MALE; MIDDLE AGED; MYOSIN TYPE I; NETHERLANDS; QUANTITATIVE TRAIT LOCI; SEASONS; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84996635686     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.10.053     Document Type: Article

References (49)

1. Akiyama, M., Suzuki, K., Yamaoka, K., Yasuoka, H., Takeshita, M., Kaneko, Y., Kondo, H., Kassai, Y., Miyazaki, T., Morita, R., et al. Number of Circulating Follicular Helper 2 T Cells Correlates With IgG4 and Interleukin-4 Levels and Plasmablast Numbers in IgG4-Related Disease. Arthritis Rheumatol. 67 (2015), 2476–2481.
2. Amadori, A., Zamarchi, R., De Silvestro, G., Forza, G., Cavatton, G., Danieli, G.A., Clementi, M., Chieco-Bianchi, L., Genetic control of the CD4/CD8 T-cell ratio in humans. Nat. Med. 1 (1995), 1279–1283.
3. Baumgarth, N., Herman, O.C., Jager, G.C., Brown, L., Herzenberg, L.A., Herzenberg, L.A., Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc. Natl. Acad. Sci. USA 96 (1999), 2250–2255.
4. Benjamini, Y., Hochberg, Y., Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J.R. Stat. Soc. 57 (1995), 289–300.
5. Brodin, P., Jojic, V., Gao, T., Bhattacharya, S., Angel, C.J.L., Furman, D., Shen-Orr, S., Dekker, C.L., Swan, G.E., Butte, A.J., et al. Variation in the human immune system is largely driven by non-heritable influences. Cell 160 (2015), 37–47.
6. Brüggemann, M., Williams, G.T., Bindon, C.I., Clark, M.R., Walker, M.R., Jefferis, R., Waldmann, H., Neuberger, M.S., Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J. Exp. Med. 166 (1987), 1351–1361.
7. Butterworth, M., McClellan, B., Allansmith, M., Influence of sex in immunoglobulin levels. Nature 214 (1967), 1224–1225.
8. Carr, E.J., Dooley, J., Garcia-Perez, J.E., Lagou, V., Lee, J.C., Wouters, C., Meyts, I., Goris, A., Boeckxstaens, G., Linterman, M.A., et al. The cellular composition of the human immune system is shaped by age and cohabitation. Nat. Immunol. 17 (2016), 461–468.
9. Cho, J.H., Feldman, M., Heterogeneity of autoimmune diseases: pathophysiologic insights from genetics and implications for new therapies. Nat. Med. 21 (2015), 730–738.
10. Coffman, R.L., Lebman, D.A., Shrader, B., Transforming growth factor beta specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes. J. Exp. Med. 170 (1989), 1039–1044.
11. R Core Team (2012). R: A language and environment for statistical computing. http://R-project.org/.
12. Dopico, X.C., Evangelou, M., Ferreira, R.C., Guo, H., Pekalski, M.L., Smyth, D.J., Cooper, N., Burren, O.S., Fulford, A.J., Hennig, B.J., et al. Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nat. Commun., 6, 2015, 7000.
13. Farber, D.L., Yudanin, N.A., Restifo, N.P., Human memory T cells: generation, compartmentalization and homeostasis. Nat. Rev. Immunol. 14 (2014), 24–35.
14. Fehrmann, R.S.N., Karjalainen, J.M., Krajewska, M., Westra, H.-J., Maloney, D., Simeonov, A., Pers, T.H., Hirschhorn, J.N., Jansen, R.C., Schultes, E.A., et al. Gene expression analysis identifies global gene dosage sensitivity in cancer. Nat. Genet. 47 (2015), 115–125.
15. Frasca, D., Diaz, A., Romero, M., Phillips, M., Mendez, N.V., Landin, A.M., Blomberg, B.B., Unique biomarkers for B-cell function predict the serum response to pandemic H1N1 influenza vaccine. Int. Immunol. 24 (2012), 175–182.
16. Hazeldine, J., Hampson, P., Lord, J.M., Reduced release and binding of perforin at the immunological synapse underlies the age-related decline in natural killer cell cytotoxicity. Aging Cell 11 (2012), 751–759.
17. Kanda, N., Tamaki, K., Estrogen enhances immunoglobulin production by human PBMCs. J. Allergy Clin. Immunol. 103 (1999), 282–288.
18. Kanda, N., Tsuchida, T., Tamaki, K., Testosterone inhibits immunoglobulin production by human peripheral blood mononuclear cells. Clin. Exp. Immunol. 106 (1996), 410–415.
19. Klein, U., Küppers, R., Rajewsky, K., Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood 89 (1997), 1288–1298.
20. Kurosaki, T., Kometani, K., Ise, W., Memory B cells. Nat. Rev. Immunol. 15 (2015), 149–159.
21. Le Garff-Tavernier, M., Béziat, V., Decocq, J., Siguret, V., Gandjbakhch, F., Pautas, E., Debré, P., Merle-Beral, H., Vieillard, V., Human NK cells display major phenotypic and functional changes over the life span. Aging Cell 9 (2010), 527–535.
22. LeMaoult, J., Szabo, P., Weksler, M.E., Effect of age on humoral immunity, selection of the B-cell repertoire and B-cell development. Immunol. Rev. 160 (1997), 115–126.
23. Li, Y., Oosting, M., Smeekens, S., Jaeger, M., Aguirre-Gamboa, R., Le, K.T.T., Deelen, P., Ricaño-Ponce, I., Schoffelen, T., Jansen, A.F.M., et al. A functional genomics approach to understand variation in cytokine production in humans. Cell 167 (2016), 1099–1110.
24. Maravillas-Montero, J.L., López-Ortega, O., Patiño-López, G., Santos-Argumedo, L., Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes. Eur. J. Immunol. 44 (2014), 877–886.
25. Mazur, M., Karczewski, J., Lodyga, M., Żaba, R., Adamski, Z., Inhibitors of phosphodiesterase 4 (PDE 4): A new therapeutic option in the treatment of psoriasis vulgaris and psoriatic arthritis. J. Dermatolog. Treat. 26 (2015), 326–328.
26. McIntyre, T.M., Klinman, D.R., Rothman, P., Lugo, M., Dasch, J.R., Mond, J.J., Snapper, C.M., Transforming growth factor beta 1 selectivity stimulates immunoglobulin G2b secretion by lipopolysaccharide-activated murine B cells. J. Exp. Med. 177 (1993), 1031–1037.
27. Orrù, V., Steri, M., Sole, G., Sidore, C., Virdis, F., Dei, M., Lai, S., Zoledziewska, M., Busonero, F., Mulas, A., et al. Genetic variants regulating immune cell levels in health and disease. Cell 155 (2013), 242–256.
28. Paternoster, L., Standl, M., Chen, C.-M., Ramasamy, A., Bønnelykke, K., Duijts, L., Ferreira, M.A., Alves, A.C., Thyssen, J.P., Albrecht, E., et al. Australian Asthma Genetics Consortium (AAGC) Genetics of Overweight Young Adults (GOYA) Consortium, EArly Genetics & Lifecourse Epidemiology (EAGLE) Consortium. Meta-analysis of genome-wide association studies identifies three new risk loci for atopic dermatitis. Nat. Genet. 44 (2011), 187–192.
29. Peter, D., Jin, S.L.C., Conti, M., Hatzelmann, A., Zitt, C., Differential expression and function of phosphodiesterase 4 (PDE4) subtypes in human primary CD4+ T cells: predominant role of PDE4D. J. Immunol. 178 (2007), 4820–4831.
30. Peters, J.H., Koenen, H.J.P.M., Fasse, E., Tijssen, H.J., Ijzermans, J.N.M., Groenen, P.J.T.A., Schaap, N.P.M., Kwekkeboom, J., Joosten, I., Human secondary lymphoid organs typically contain polyclonally-activated proliferating regulatory T cells. Blood 122 (2013), 2213–2223.
31. Quinn, J.J., Chang, H.Y., Unique features of long non-coding RNA biogenesis and function. Nat. Rev. Genet. 17 (2016), 47–62.
32. Restifo, N.P., Gattinoni, L., Lineage relationship of effector and memory T cells. Curr. Opin. Immunol. 25 (2013), 556–563.
33. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
34. Roederer, M., Quaye, L., Mangino, M., Beddall, M.H., Mahnke, Y., Chattopadhyay, P., Tosi, I., Napolitano, L., Terranova Barberio, M., Menni, C., et al. The genetic architecture of the human immune system: a bioresource for autoimmunity and disease pathogenesis. Cell 161 (2015), 387–403.
35. Rowley, M.J., Mackay, I.R., Measurement of antibody-producing capacity in man. I. The normal response to flagellin from Salmonella adelaide. Clin. Exp. Immunol. 5 (1969), 407–418.
36. Schirmer, M., Smeekens, S.P., Vlamakis, H., Jaeger, M., Oosting, M., Franzosa, E.A., Jansen, T., Jacobs, L., Bonder, M.J., Kurilshikov, A., Fu, J., et al. Linking the gut microbiome to inflammatory cytokine production capacity. Cell 167 (2016), 1125–1136.
37. Schroeder, H.W. Jr., Cavacini, L., Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125:2, Suppl 2 (2010), S41–S52.
38. Shabalin, A.A., Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics 28 (2012), 1353–1358.
39. Shaw, A.C., Goldstein, D.R., Montgomery, R.R., Age-dependent dysregulation of innate immunity. Nat. Rev. Immunol. 13 (2013), 875–887.
40. Snapper, C.M., Paul, W.E., Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236 (1987), 944–947.
41. Solana, R., Pawelec, G., Tarazona, R., Aging and innate immunity. Immunity 24 (2006), 491–494.
42. Tangye, S.G., Deenick, E.K., Palendira, U., Ma, C.S., T cell-B cell interactions in primary immunodeficiencies. Ann. N Y Acad. Sci. 1250 (2012), 1–13.
43. ter Horst, R., Jaeger, M., Smeekens, S.P., Oosting, M., Swertz, M.A., Li, Y., Kumar, V., Diavatopoulos, D.A., Jansen, A.F.M., Lemmers, H., et al. Host and environmental factors influencing individual human cytokine responses. Cell 167 (2016), 1111–1124.
44. Tigchelaar, E.F., Zhernakova, A., Dekens, J.A.M., Hermes, G., Baranska, A., Mujagic, Z., Swertz, M.A., Muñoz, A.M., Deelen, P., Cénit, M.C., et al. Cohort profile: LifeLines DEEP, a prospective, general population cohort study in the northern Netherlands: study design and baseline characteristics. BMJ Open, 5, 2015, e006772.
45. Tsang, J.S., Schwartzberg, P.L., Kotliarov, Y., Biancotto, A., Xie, Z., Germain, R.N., Wang, E., Olnes, M.J., Narayanan, M., Golding, H., et al. Baylor HIPC Center, CHI Consortium. Global analyses of human immune variation reveal baseline predictors of postvaccination responses. Cell 157 (2014), 499–513.
46. Venables, W.N., Ripley, B.D., Modern Applied Statistics with S. 2002, Springer, New York.
47. Weller, S., Braun, M.C., Tan, B.K., Rosenwald, A., Cordier, C., Conley, M.E., Plebani, A., Kumararatne, D.S., Bonnet, D., Tournilhac, O., et al. Human blood IgM “memory” B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104 (2004), 3647–3654.
48. Yang, J., Benyamin, B., McEvoy, B.P., Gordon, S., Henders, A.K., Nyholt, D.R., Madden, P.A., Heath, A.C., Martin, N.G., Montgomery, G.W., et al. Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42 (2010), 565–569.
49. Zaitlen, N., Kraft, P., Heritability in the genome-wide association era. Hum. Genet. 131 (2012), 1655–1664.