A feeder-free differentiation system identifies autonomously proliferating b cell precursors in human bone marrow

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1044-1054

  Kraus, Helene ^a,b   Kaiser, Sandra ^a   Aumann, Konrad ^a   Bönelt, Peter ^a   Salzer, Ulrich ^a   Vestweber, Dietmar ^c   Erlacher, Miriam ^a   Kunze, Mirjam ^a   Burger, Meike ^a   Pieper, Kathrin ^a   Sic, Heiko ^a   Rolink, Antonius ^d   Eibel, Hermann ^a   Rizzi, Marta ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 7;

ARTICLE; B CELL CULTURE; BONE MARROW; CD34 SELECTION; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; FEEDER CELL; HUMAN; HUMAN CELL; HUMORAL IMMUNE DEFICIENCY; IN VITRO STUDY; PRE B LYMPHOCYTE; PRIORITY JOURNAL;

ADULT; ANIMALS; B-LYMPHOCYTES; BONE MARROW; CELL CULTURE TECHNIQUES; CELL DIVISION; CELL LINEAGE; CELLS, CULTURED; COCULTURE TECHNIQUES; DNA-BINDING PROTEINS; FETAL BLOOD; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELLS; HETEROGRAFTS; HOMEOSTASIS; HUMANS; IMMUNOGLOBULIN M; IMMUNOPHENOTYPING; INTERLEUKIN-7; LYMPHOPOIESIS; MICE; RADIATION CHIMERA; RECEPTORS, INTERLEUKIN-2; TIME FACTORS; YOUNG ADULT;

EID: 84893374134     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301815     Document Type: Article

References (56)

1. van Zelm, M. C., M. van der Burg, D. de Ridder, B. H. Barendregt, E. F. de Haas, M. J. Reinders, A. C. Lankester, T. Révész, F. J. Staal, and J. J. van Dongen. 2005. Ig gene rearrangement steps are initiated in early human precursor B cell subsets and correlate with specific transcription factor expression. J. Immunol. 175: 5912-5922.
2. Herzog, S., M. Reth, and H. Jumaa. 2009. Regulation of B-cell proliferation and differentiation by pre-B-cell receptor signalling. Nat. Rev. Immunol. 9: 195-205.
3. Scheeren, F. A., A. U. van Lent, M. Nagasawa, K. Weijer, H. Spits, N. Legrand, and B. Blom. 2010. Thymic stromal lymphopoietin induces early human B-cell proliferation and differentiation. Eur. J. Immunol. 40: 955-965.
4. Ghia, P., E. ten Boekel, E. Sanz, A. de la Hera, A. Rolink, and F. Melchers. 1996. Ordering of human bone marrow B lymphocyte precursors by single-cell polymerase chain reaction analyses of the rearrangement status of the immunoglobulin H and L chain gene loci. J. Exp. Med. 184: 2217-2229.
5. Nutt, S. L., and B. L. Kee. 2007. The transcriptional regulation of B cell lineage commitment. Immunity 26: 715-725.
6. Singh, H., K. L. Medina, and J. M. Pongubala. 2005. Contingent gene regulatory networks and B cell fate specification. Proc. Natl. Acad. Sci. USA 102: 4949-4953.
7. Macallan, D. C., D. L. Wallace, Y. Zhang, H. Ghattas, B. Asquith, C. de Lara, A. Worth, G. Panayiotakopoulos, G. E. Griffin, D. F. Tough, and P. C. Beverley. 2005. B-cell kinetics in humans: rapid turnover of peripheral blood memory cells. Blood 105: 3633-3640.
8. Cheshier, S. H., S. J. Morrison, X. Liao, and I. L. Weissman. 1999. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 96: 3120-3125.
9. Johnson, K. M., K. Owen, and P. L. Witte. 2002. Aging and developmental transitions in the B cell lineage. Int. Immunol. 14: 1313-1323.
10. Min, H., E. Montecino-Rodriguez, and K. Dorshkind. 2006. Effects of aging on the common lymphoid progenitor to pro-B cell transition. J. Immunol. 176: 1007-1012.
11. van Zelm, M. C., T. Szczepanski, M. van der Burg, and J. J. van Dongen. 2007. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J. Exp. Med. 204: 645-655.
12. Zhang, Q., R. Iida, T. Yokota, and P. W. Kincade. 2013. Early events in lymphopoiesis: an update. Curr. Opin. Hematol. 20: 265-272.
13. Ghia, P., E. ten Boekel, A. G. Rolink, and F. Melchers. 1998. B-cell development: a comparison between mouse and man. Immunol. Today 19: 480-485.
14. Grabstein, K. H., T. J. Waldschmidt, F. D. Finkelman, B. W. Hess, A. R. Alpert, N. E. Boiani, A. E. Namen, and P. J. Morrissey. 1993. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J. Exp. Med. 178: 257-264.
15. Puel, A., S. F. Ziegler, R. H. Buckley, and W. J. Leonard. 1998. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat. Genet. 20: 394-397.
16. Noguchi, M., H. Yi, H. M. Rosenblatt, A. H. Filipovich, S. Adelstein, W. S. Modi, O. W. McBride, and W. J. Leonard. 1993. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73: 147-157.
17. Macchi, P., A. Villa, S. Giliani, M. G. Sacco, A. Frattini, F. Porta, A. G. Ugazio, J. A. Johnston, F. Candotti, J. J. O'Shea, et al. 1995. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 377: 65-68.
18. Giliani, S., L. Mori, G. de Saint Basile, F. Le Deist, C. Rodriguez-Perez, C. Forino, E. Mazzolari, S. Dupuis, R. Elhasid, A. Kessel, et al. 2005. Interleukin-7 receptor alpha (IL-7Ralpha) deficiency: cellular and molecular bases. Analysis of clinical, immunological, and molecular features in 16 novel patients. Immunol. Rev. 203: 110-126.
19. Espeli, M., B. Rossi, S. J. Mancini, P. Roche, L. Gauthier, and C. Schiff. 2006. Initiation of pre-B cell receptor signaling: common and distinctive features in human and mouse. Semin. Immunol. 18: 56-66.
20. Fedoriw, Y., T. D. Samulski, A. M. Deal, C. H. Dunphy, A. Sharf, T. C. Shea, J. S. Serody, and S. Sarantopoulos. 2012. Bone marrow B cell precursor number after allogeneic stem cell transplantation and GVHD development. Biol. Blood Marrow Transplant. 18: 968-973.
21. Venhoff, N., N. M. Effelsberg, U. Salzer, K. Warnatz, H. H. Peter, D. Lebrecht, M. Schlesier, R. E. Voll, and J. Thiel. 2012. Impact of rituximab on immunoglobulin concentrations and B cell numbers after cyclophosphamide treatment in patients with ANCA-Associated vasculitides. PLoS ONE 7: e37626.
22. Zhu, L. P., T. R. Cupps, G. Whalen, and A. S. Fauci. 1987. Selective effects of cyclophosphamide therapy on activation, proliferation, and differentiation of human B cells. J. Clin. Invest. 79: 1082-1090.
23. Fluckiger, A. C., E. Sanz, M. Garcia-Lloret, T. Su, Q. L. Hao, R. Kato, S. Quan, A. de la Hera, G. M. Crooks, O. N. Witte, and D. J. Rawlings. 1998. In vitro reconstitution of human B-cell ontogeny: from CD34(+) multipotent progenitors to Ig-secreting cells. Blood 92: 4509-4520.
24. Ichii, M., K. Oritani, T. Yokota, M. Nishida, I. Takahashi, T. Shirogane, S. Ezoe, N. Saitoh, R. Tanigawa, P. W. Kincade, and Y. Kanakura. 2008. Regulation of human B lymphopoiesis by the transforming growth factor-beta superfamily in a newly established coculture system using human mesenchymal stem cells as a supportive microenvironment. Exp. Hematol. 36: 587-597.
25. Kurosaka, D., T. W. LeBien, and J. A. Pribyl. 1999. Comparative studies of different stromal cell microenvironments in support of human B-cell development. Exp. Hematol. 27: 1271-1281.
26. Rawlings, D. J., S. G. Quan, R. M. Kato, and O. N. Witte. 1995. Long-term culture system for selective growth of human B-cell progenitors. Proc. Natl. Acad. Sci. USA 92: 1570-1574.
27. Ichii, M., K. Oritani, T. Yokota, D. C. Schultz, J. L. Holter, Y. Kanakura, and P. W. Kincade. 2010. Stromal cell-free conditions favorable for human B lymphopoiesis in culture. J. Immunol. Methods 359: 47-55.
28. Kienzler, A. K., M. Rizzi, M. Reith, S. L. Nutt, and H. Eibel. 2013. Inhibition of human B-cell development into plasmablasts by histone deacetylase inhibitor valproic acid. J. Allergy Clin. Immunol. 131: 1695-1699.
29. Aumann, K., A. V. Frey, A. M. May, D. Hauschke, C. Kreutz, J. P. Marx, J. Timmer, M. Werner, and H. L. Pahl. 2013. Subcellular mislocalization of the transcription factor NF-E2 in erythroid cells discriminates prefibrotic primary myelofibrosis from essential thrombocythemia. Blood 122: 93-99.
30. van der Burg, M., H. Kreyenberg, A. Willasch, B. H. Barendregt, S. Preuner, F. Watzinger, T. Lion, E. Roosnek, J. Harvey, M. Alcoceba, et al; EU-supported EuroChimerism Consortium project QLRT-2001-01485. 2011. Standardization of DNA isolation from low cell numbers for chimerism analysis by PCR of short tandem repeats. Leukemia 25: 1467-1470.
31. van Dongen, J. J., A. W. Langerak, M. Bruggemann, P. A. Evans, M. Hummel, F. L. Lavender, E. Delabesse, F. Davi, E. Schuuring, R. García-Sanz, et al. 2003. 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.
32. Ning, H., G. Lin, T. F. Lue, and C. S. Lin. 2011. Mesenchymal stem cell marker Stro-1 is a 75 kd endothelial antigen. Biochem. Biophys. Res. Commun. 413: 353-357.
33. Parrish, Y. K., I. Baez, T. A. Milford, A. Benitez, N. Galloway, J. W. Rogerio, E. Sahakian, M. Kagoda, G. Huang, Q. L. Hao, et al. 2009. IL-7 dependence in human B lymphopoiesis increases during progression of ontogeny from cord blood to bone marrow. J. Immunol. 182: 4255-4266.
34. Taguchi, T., H. Takenouchi, Y. Shiozawa, J. Matsui, N. Kitamura, Y. Miyagawa, Y. U. Katagiri, T. Takahashi, H. Okita, J. Fujimoto, and N. Kiyokawa. 2007. Interleukin-7 contributes to human pro-B-cell development in a mouse stromal cell-dependent culture system. Exp. Hematol. 35: 1398-1407.
35. Conget, P. A., and J. J. Minguell. 1999. Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J. Cell. Physiol. 181: 67-73.
36. Ren, G., X. Zhao, L. Zhang, J. Zhang, A. L'Huillier, W. Ling, A. I. Roberts, A. D. Le, S. Shi, C. Shao, and Y. Shi. 2010. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J. Immunol. 184: 2321-2328.
37. Ichii, M., K. Oritani, T. Yokota, Q. Zhang, K. P. Garrett, Y. Kanakura, and P. W. Kincade. 2010. The density of CD10 corresponds to commitment and progression in the human B lymphoid lineage. PLoS ONE 5: e12954.
38. Dworzak, M. N., G. Fritsch, G. Froschl, D. Printz, and H. Gadner. 1998. Fourcolor flow cytometric investigation of terminal deoxynucleotidyl transferasepositive lymphoid precursors in pediatric bone marrow: CD79a expression precedes CD19 in early B-cell ontogeny. Blood 92: 3203-3209.
39. LeBien, T. W., and T. F. Tedder. 2008. B lymphocytes: how they develop and function. Blood 112: 1570-1580.
40. Arakawa-Hoyt, J., M. A. Dao, F. Thiemann, Q. L. Hao, D. C. Ertl, K. I. Weinberg, G. M. Crooks, and J. A. Nolta. 1999. The number and generative capacity of human B lymphocyte progenitors, measured in vitro and in vivo, is higher in umbilical cord blood than in adult or pediatric bone marrow. Bone Marrow Transplant. 24: 1167-1176.
41. Oettinger, M. A., D. G. Schatz, C. Gorka, and D. Baltimore. 1990. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248: 1517-1523.
42. Lin, Y. C., S. Jhunjhunwala, C. Benner, S. Heinz, E. Welinder, R. Mansson, M. Sigvardsson, J. Hagman, C. A. Espinoza, J. Dutkowski, et al. 2010. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11: 635-643.
43. Cobaleda, C., A. Schebesta, A. Delogu, and M. Busslinger. 2007. Pax5: the guardian of B cell identity and function. Nat. Immunol. 8: 463-470.
44. Rolink, A., A. Kudo, H. Karasuyama, Y. Kikuchi, and F. Melchers. 1991. Long-term proliferating early pre B cell lines and clones with the potential to develop to surface Ig-positive, mitogen reactive B cells in vitro and in vivo. EMBO J. 10: 327-336.
45. Prieyl, J. A., and T. W. LeBien. 1996. Interleukin 7 independent development of human B cells. Proc. Natl. Acad. Sci. USA 93: 10348-10353.
46. Shultz, L. D., M. A. Brehm, J. V. Garcia-Martinez, and D. L. Greiner. 2012. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 12: 786-798.
47. von Freeden-Jeffry, U., P. Vieira, L. A. Lucian, T. McNeil, S. E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181: 1519-1526.
48. Billips, L. G., C. A. Nunez, F. E. Bertrand, III, A. K. Stankovic, G. L. Gartland, P. D. Burrows, and M. D. Cooper. 1995. Immunoglobulin recombinase gene activity is modulated reciprocally by interleukin 7 and CD19 in B cell progenitors. J. Exp. Med. 182: 973-982.
49. Conley, M. E., D. Mathias, J. Treadaway, Y. Minegishi, and J. Rohrer. 1998. Mutations in btk in patients with presumed X-linked agammaglobulinemia. Am. J. Hum. Genet. 62: 1034-1043.
50. Minegishi, Y., J. Rohrer, E. Coustan-Smith, H. M. Lederman, R. Pappu, D. Campana, A. C. Chan, and M. E. Conley. 1999. An essential role for BLNK in human B cell development. Science 286: 1954-1957.
51. Mullighan, C. G. 2012. Molecular genetics of B-precursor acute lymphoblastic leukemia. J. Clin. Invest. 122: 3407-3415.
52. Staron, M., Y. Yang, B. Liu, J. Li, Y. Shen, J. C. Zúniga- Pflucker, H. L. Aguila, I. Goldschneider, and Z. Li. 2010. gp96, an endoplasmic reticulum master chaperone for integrins and Toll-like receptors, selectively regulates early T and B lymphopoiesis. Blood 115: 2380-2390.
53. Voermans, C., P. M. Rood, P. L. Hordijk, W. R. Gerritsen, and C. E. van der Schoot. 2000. Adhesion molecules involved in transendothelial migration of human hematopoietic progenitor cells. Stem Cells 18: 435-443.
54. Jung, Y., J. Wang, A. Havens, Y. Sun, J. Wang, T. Jin, and R. S. Taichman. 2005. Cell-to-cell contact is critical for the survival of hematopoietic progenitor cells on osteoblasts. Cytokine 32: 155-162.
55. Arana, E., A. Vehlow, N. E. Harwood, E. Vigorito, R. Henderson, M. Turner, V. L. Tybulewicz, and F. D. Batista. 2008. Activation of the small GTPase Rac2 via the B cell receptor regulates B cell adhesion and immunological-synapse formation. Immunity 28: 88-99.
56. Imhof, B. A., C. Schlienger, K. Handloser, B. Hesse, M. Slanicka, and R. Gisler. 1991. Monoclonal antibodies that block adhesion of B cell progenitors to bone marrow stroma in vitro prevent B cell differentiation in vivo. Eur. J. Immunol. 21: 2043-2049.