Timely and spatially regulated maturation of B and T cell repertoire during human fetal development

Science Translational Medicine

Volumn 7, Issue 276, 2015, Pages

  Rechavi, Erez ^a,b   Lev, Atar ^a,b   Lee, Yu Nee ^c   Simon, Amos J ^a,b,d   Yinon, Yoav ^b,d   Lipitz, Schlomo ^b,d   Amariglio, Ninette ^d   Weisz, Boaz ^b,d   Notarangelo, Luigi D ^c,e,f   Somech, Raz ^a,b  

^a Jeffrey Modell Foundation Center   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SHEBA MEDICAL CENTER   (Israel)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; IMMUNOGLOBULIN HEAVY CHAIN; INTRON RECOMBINATION SIGNAL SEQUENCE K DELETING ELEMENT; SIGNAL JOINT KAPPA RECEPTOR EXCISION CIRCLE; T CELL RECEPTOR EXCISION CIRCLE; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG; ANTIBODY; ANTIGEN; COMPLEMENTARITY DETERMINING REGION; LYMPHOCYTE ANTIGEN RECEPTOR;

ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CELL MATURATION; CONTROLLED STUDY; FETUS; FETUS DEVELOPMENT; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; INFANT; NEXT GENERATION SEQUENCING; PREGNANCY; PREMATURITY; PRIORITY JOURNAL; SOMATIC HYPERMUTATION; T LYMPHOCYTE; VDJ RECOMBINATION; BLOOD; CHEMISTRY; COMPLEMENTARITY DETERMINING REGION; FEMALE; FETUS BLOOD; GENE REARRANGEMENT; IMMUNOLOGY; METABOLISM; TIME FACTOR;

ANTIBODIES; ANTIGENS; B-LYMPHOCYTES; COMPLEMENTARITY DETERMINING REGIONS; FEMALE; FETAL BLOOD; FETAL DEVELOPMENT; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; INFANT; PREGNANCY; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; T-LYMPHOCYTES; TIME FACTORS;

EID: 84923917237     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa0072     Document Type: Article

References (56)

1. N. P. Davies, A. G. Buggins, R. J. Snijders, E. Jenkins, D. M. Layton, K. H. Nicolaides, Blood leucocyte count in the human fetus. Arch. Dis. Child. 67, 399-403 (1992).
2. B. Thilaganathan, C. A. Mansur, G. Morgan, K. H. Nicolaides, Fetal T-lymphocyte subpopulations in normal pregnancies. Fetal Diagn. Ther. 7, 53-61 (1992).
3. B. Thilaganathan, K. H. Nicolaides, C. A. Mansur, R. J. Levinsky, G. Morgan, Fetal B lymphocyte subpopulations in normal pregnancies. Fetal Diagn. Ther. 8, 15-21 (1993).
4. P. G. Holt, C. A. Jones, The development of the immune system during pregnancy and early life. Allergy 55, 688-697 (2000).
5. E. Juretić, B. Užarevic, M. Petrovećki, A. Juretić, Two-color flow cytometric analysis of preterm and term newborn lymphocytes. Immunobiology 202, 421-428 (2000).
6. M. Prabhudas, B. Adkins, H. Gans, C. King, O. Levy, O. Ramilo, C. Siegrist, Challenges in infant immunity: Implications for responses to infection and vaccines. Nat. Immunol. 12, 189-194 (2011).
7. H. Schroeder, J. Wang, Preferential utilization of conserved immunoglobulin heavy chain variable gene segments during human fetal life. Proc. Natl. Acad. Sci. U.S.A. 87, 6146-6150 (1990).
8. V. Pascual, L. Verkruyse, M. L. Casey, J. D. Capra, Analysis of Ig H chain gene segment utilization in human fetal liver. Revisiting the "proximal utilization hypothesis". J. Immunol. 151, 4164-4172 (1993).
9. B. Baskin, K. B. Islam, C. I. Smith, Characterization of the CDR3 region of rearranged α heavy chain genes in human fetal liver. Clin. Exp. Immunol. 112, 44-47 (1998).
10. H. Robins, Immunosequencing: Applications of immune repertoire deep sequencing. Curr. Opin. Immunol. 25, 646-652 (2013).
11. L. Al-Harthi, G. Marchetti, C. M. Steffens, J. Poulin, R. Sékaly, A. Landay, Detection of T cell receptor circles (TRECs) as biomarkers for de novo T cell synthesis using a quantitative polymerase chain reaction-enzyme linked immunosorbent assay (PCR-ELISA). J. Immunol. Methods 237 187-197 (2000).
12. M. C. van Zelm, T. Szczepanski, M. van der Burg, J. J. M. van Dongen, Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J. Exp. Med. 204, 645-655 (2007).
13. W. A. Dik, K. Pike-Overzet, F. Weerkamp, D. de Ridder, E. F. de Haas, M. R. Baert, P. van der Spek, E. E. Koster, M. J. Reinders, J. J. van Dongen, A. W. Langerak, F. J. Staal, New insights on human T cell development by quantitative T cell receptor gene rearrangement studies and gene expression profiling. J. Exp. Med. 201, 1715-1723 (2005).
14. J. J. M. van Dongen, A. W. Langerak, M. Brüggemann, P. A S. Evans, M. Hummel, F. L. Lavender, E. Delabesse, F. Davi, E. Schuuring, R. García-Sanz, J. H. J. M. van Krieken, J. Droese, D. González, C. Bastard, H. E. White, M. Spaargaren, M. González, A. Parreira, J. L. Smith, G. J. Morgan, M. Kneba, E. A. Macintyre, Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: Report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 17, 2257-2317 (2003).
15. E. Simpson, Measurement of diversity. Nature 163, 688 (1949).
16. J. L. Xu, M. M. Davis, Diversity in the CDR3 region of VH is sufficient for most antibody specificities. Immunity 13, 37-45 (2000).
17. E. L. Reinherz, K. Tan, L. Tang, P. Kern, J. Liu, Y. Xiong, R. E. Hussey, A. Smolyar, B. Hare, R. Zhang, A. Joachimiak, H. C. Chang, G. Wagner, J. Wang, The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286, 1913-1921 (1999).
18. H. J. Schroeder, G. Ippolito, S. Shiokawa, Regulation of the antibody repertoire through control of HCDR3 diversity. Vaccine 16, 1383-1390 (1998).
19. H. W. Schroeder, Slow, programmed maturation of the immunoglobulin HCDR3 repertoire during the third trimester of fetal life. Blood 98, 2745-2751 (2001).
20. M. Zemlin, R. L. Schelonka, K. Bauer, H. W. Schroeder Jr., Regulation and chance in the ontogeny of B and T cell. Immunol. Res. 26, 265-278 (2002).
21. H. W. Schroeder Jr., J. L. Hillson, R. M. Perlmutter, Early restriction of the human antibody repertoire. Science 238, 791-793 (1987).
22. Z. Li, C. J. Woo, M. D. Iglesias-Ussel, D. Ronai, M. D. Scharff, The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18, 1-11 (2004).
23. A. Six, M. E. Mariotti-Ferrandiz, W. Chaara, S. Magadan, H.-P. Pham, M.-P. Lefranc, T. Mora, V. Thomas-Vaslin, A. M. Walczak, P. Boudinot, The past, present, and future of immune repertoire biology - The rise of next-generation repertoire analysis. Front. Immunol. 4, 413 (2013).
24. M. Zemlin, G. Hoersch, C. Zemlin, A. Pohl-Schickinger, M. Hummel, C. Berek, R. F. Maier, K. Bauer, The postnatal maturation of the immunoglobulin heavy chain IgG repertoire in human preterm neonates is slower than in term neonates. J. Immunol. 178, 1180-1188 (2007).
25. S. Li, M.-P. Lefranc, J. J. Miles, E. Alamyar, V. Giudicelli, P. Duroux, J. D. Freeman, V. D. A. Corbin, J.-P. Scheerlinck, M. A. Frohman, P. U. Cameron, M. Plebanski, B. Loveland, S. R. Burrows, A. T. Papenfuss, E. J. Gowans, IMGT/HighV QUEST paradigm for T cell receptor IMGT clonotype diversity and next generation repertoire immunoprofiling. Nat. Commun. 4, 2333 (2013).
26. K. J. L. Jackson, M. J. Kidd, Y. Wang, A. M. Collins, The shape of the lymphocyte receptor repertoire: Lessons from the B cell receptor. Front. Immunol. 4, 263 (2013).
27. M. Souto-Carneiro, G. Sims, J. Lee, P. E. Lipsky, Developmental changes in the human heavy chain CDR3. J. Immunol. 175, 7425-7436 (2005).
28. R. L. Schelonka, F. M. Raaphorst, D. Infante, E. Kraig, J. M. Teale, A. J. Infante, T cell receptor repertoire diversity and clonal expansion in human neonates. Pediatr. Res. 43, 396-402 (1998).
29. H3 genes and short diverse third complementarity-determining regions (CDR3) in human fetal B lymphocyte immunoglobulin heavy chain rearrangements. Eur. J. Immunol. 22, 247-251 (1992).
30. R. L. Schelonka, E. Szymanska, A. Vale, DH and JH usage in murine fetal liver mirrors that of human fetal liver. Immunogenetics 62, 653-666 (2010).
31. M. Zemlin, K. Bauer, M. Hummel, S. Pfeiffer, S. Devers, C. Zemlin, H. Stein, H. Versmold, The diversity of rearranged immunoglobulin heavy chain variable region genes in peripheral blood B cells of preterm infants is restricted by short third complementarity-determining regions but not by limited gene segment usage. Blood 97, 1511-1513 (2001).
32. P. Prabakaran, W. Chen, M. G. Singarayan, C. C. Stewart, E. Streaker, Y. Feng, D. S. Dimitrov, Expressed antibody repertoires in human cord blood cells: 454 sequencing and IMGT/HighV-QUEST analysis of germline gene usage, junctional diversity, and somatic mutations. Immunogenetics 64, 337-350 (2012).
33. D. Brugnoni, P. Airò, D. Graf, M. Marconi, M. Lebowitz, A. Plebani, S. Giliani, F. Malacarne, R. Cattaneo, A. G. Ugazio, Ineffective expression of CD40 ligand on cord blood T cells may contribute to poor immunoglobulin production in the newborn. Eur. J. Immunol. 24, 1919-1924 (1994).
34. S. Nonoyama, L. A. Penix, C. P. Edwards, D. B. Lewis, S. Ito, A. Aruffo, C. B. Wilson, H. D. Ochs, Diminished expression of CD40 ligand by activated neonatal T cells. J. Clin. Invest. 95, 66-75 (1995).
35. K. Kaur, S. Chowdhury, N. S. Greenspan, J. R. Schreiber, Decreased expression of tumor necrosis factor family receptors involved in humoral immune responses in preterm neonates. Blood 110, 2948-2954 (2007).
36. N. A. Bos, C. G. Meeuwsen, H. Hooijkaas, R. Benner, B. S. Wostmann, J. R. Pleasants, Early development of Ig-secreting cells in young of germ-free BALB/c mice fed a chemically defined ultrafiltered diet. Cell. Immunol. 105, 235-245 (1987).
37. C. A. Alford, J. Schaefer, W. J. Blankenship, J. V Straumfjord, G. Cassady, A correlative immunologic, microbiologic and clinical approach to the diagnosis of acute and chronic infections in newborn infants. N. Engl. J. Med. 277, 437-449 (1967).
38. Z. Szépfalusi, J. Pichler, S. Elsässer, K. van Duren, C. Ebner, G. Bernaschek, R. Urbanek, Transplacental priming of the human immune system with environmental allergens can occur early in gestation. J. Allergy Clin. Immunol. 106, 530-536 (2000).
39. R. Casas, B. Björkstén, Detection of Fel d 1-immunoglobulin G immune complexes in cord blood and sera from allergic and non-allergic mothers. Pediatr. Allergy Immunol. 12, 59-64 (2001).
40. J. Ridings, I. C. Nicholson, W. Goldsworthy, R. Haslam, D. M. Roberton, H. Zola, Somatic hypermutation of immunoglobulin genes in human neonates. Clin. Exp. Immunol. 108, 366-374 (1997).
41. +B cells. J. Exp. Med. 205, 2033-2042 (2008).
42. C. Mao, L. Jiang, M. Melo-Jorge, M. Puthenveetil, X. Zhang, M. C. Carroll, T. Kari-Imanishi, T cell-independent somatic hypermutation in murine B cells with an immature phenotype. Immunity 20, 133-144 (2004).
43. J. H. Han, S. Akira, K. Calame, B. Beutler, E. Selsing, T. Imanishi-Kari, Class switch recombination and somatic hypermutation in early mouse B cells are mediated by B cell and Toll-like receptors. Immunity 27, 64-75 (2007).
44. + memory B cell development. J. Exp. Med. 203, 393-400 (2006).
45. J. F. George, H. W. Schroeder, Developmental regulation of D beta reading frame and junctional diversity in T cell receptor-beta transcripts from human thymus. J. Immunol. 148, 1230-1239 (1992).
46. F. M. Raaphorst, E. L. Kaijzel, M. J. van Tol, J. M. Vossen, P. J. Van den Elsen, Non-random employment of Vβ6 and Jβ gene elements and conserved amino acid usage profiles in CDR3 regions of human fetal and adult TCR β chain rearrangements. Int. Immunol. 6, 1-9 (1994).
47. F. M. Raaphorst, J. Van Bergen, R. L. Van Den Bergh, M. Van Der Keur, R. De Krijger, J. Bruining, M. J. D. Van To, J. M. Vossen, P. J. Van Den Elsenl, Usage of TCRAV and TCRBV gene families in human fetal and adult TCR rearrangements. Immunogenetics 39, 343-350 (1994).
48. J. M. Murray, T. Messier, J. Rivers, J. P. O'Neill, V. E. Walker, P. M. Vacek, B. A. Finette, V(D)J recombinase-mediated TCR β locus gene usage and coding joint processing in peripheral T cells during perinatal and pediatric development. J. Immunol. 189, 2356-2364 (2012).
49. + T cell responses to cytomegalovirus and EBV. J. Immunol. 181, 7853-7862 (2008).
50. V. Venturi, K. Kedzierska, D. A. Price, P. C. Doherty, D. C. Douek, S. J. Turner, M. P. Davenport, Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc. Natl. Acad. Sci. U.S.A. 103, 18691-18696 (2006).
51. V. Venturi, M. F. Quigley, H. Y. Greenaway, P. C. Ng, Z. S. Ende, T. McIntosh, T. E. Asher, J. R. Almeida, S. Levy, D. A. Price, M. P. Davenport, D. C. Douek, A mechanism for TCR sharing between T cell subsets and individuals revealed by pyrosequencing. J. Immunol. 186, 4285-4294 (2011).
52. A. Lev, A. J. Simon, A. Broides, J. Levi, B. Z. Garty, E. Rosenthal, N. Amariglio, G. Rechavi, R. Somech, Thymic function in MHC class II-deficient patients. J. Allergy Clin. Immunol. 131, 831-839 (2013).
53. A. Lev, A. J. Simon, M. Bareket, B. Bielorai, D. Hutt, N. Amariglio, G. Rechavi, R. Somech, The kinetics of early T and B cell immune recovery after bone marrow transplantation in RAG-2-deficient SCID patients. PLOS One 7, e30494 (2012).
54. C. Wang, C. M. Sanders, Q. Yang, H. W. Schroeder, E. Wang, F. Babrzadeh, B. Gharizadeh, R. M. Myers, J. R. Hudson, R. W. Davis, J. Han, High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl. Acad. Sci. U.S.A. 107, 1518-1523 (2010).
55. T. Rogosch, S. Kerzel, K. H. Hoi, Z. Zhang, R. F. Maier, G. C. Ippolito, M. Zemlin, Immunoglobulin analysis tool: A novel tool for the analysis of human and mouse heavy and light chain transcripts. Front. Immunol. 3, 176 (2012).
56. Ø. Hammer, D. A. T. Harper, P. D. Ryan, PAST: Paleontological Statistics software package for education and data analysis. Palaeontol. Electron. 4, 1-9 (2001).