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Resolution of Three Nonproliferative Immature Splenic B Cell Subsets Reveals Multiple Selection Points During Peripheral B Cell Maturation¹

David Allman^2,*, R. Coleman Lindsley^*, William DeMuth^*, Kristina Rudd^*, Susan A. Shinton and Richard R. Hardy

^* Department of Pathology and Laboratory Medicine and Abramson Family Cancer Research Institute, University of Pennsylvania School of Medicine, Philadelphia, PA 19104; and Institute for Cancer Research, Fox Chase Cancer Center, Philadelphia, PA 19111

Although immature/transitional peripheral B cells may remain susceptible to selection pressures before full maturation, the nature and timing of these selection events remain unclear. We show that correlated expression of surface (s) IgM (sIgM), CD23, and AA4 defines three nonproliferative subpopulations of immature/transitional peripheral B cells. We designate these populations transitional (T) 1 (AA4⁺CD23^-sIgM^high), T2 (AA4⁺CD23⁺sIgM^high), and T3 (AA4⁺CD23⁺sIgM^low). Cells within all three subsets are functionally immature as judged by their failure to proliferate following sIgM cross-linking in vitro, and their rapid rate of turnover in vivo as assessed by 5-bromo-2'-deoxyuridine labeling. These labeling studies also reveal measurable cell loss at both the T1-T2 and T2-T3 transitions, suggesting the existence of multiple selection points within the peripheral immature B cell pool. Furthermore, we find that Btk-deficient (xid) mice exhibit an incomplete developmental block at the T2-T3 transition within the immature B cell pool. This contrasts markedly with lyn^-/- mice, which exhibit depressed numbers but normal ratios of each immature peripheral B cell subset and severely reduced numbers of mature B cells. Together, these data provide evidence for multiple selection points among immature peripheral B cells, suggesting that the B cell repertoire is shaped by multiple unique selection events that occur within the immature/transitional peripheral B cell pool.

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				Z. SM. Rahman, S. P. Rao, S. L. Kalled, and T. Manser Normal Induction but Attenuated Progression of Germinal Center Responses in BAFF and BAFF-R Signaling-Deficient Mice J. Exp. Med., October 20, 2003; 198(8): 1157 - 1169. [Abstract] [Full Text] [PDF]

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				S. H. Smith and M. P. Cancro Cutting Edge: B Cell Receptor Signals Regulate BLyS Receptor Levels in Mature B Cells and Their Immediate Progenitors J. Immunol., June 15, 2003; 170(12): 5820 - 5823. [Abstract] [Full Text] [PDF]

				I. J. Amanna, J. P. Dingwall, and C. E. Hayes Enforced bcl-xL Gene Expression Restored Splenic B Lymphocyte Development in BAFF-R Mutant Mice J. Immunol., May 1, 2003; 170(9): 4593 - 4600. [Abstract] [Full Text] [PDF]

				D. Tarlinton, A. Light, D. Metcalf, R. P. Harvey, and L. Robb Architectural Defects in the Spleens of Nkx2-3-Deficient Mice Are Intrinsic and Associated with Defects in Both B Cell Maturation and T Cell-Dependent Immune Responses J. Immunol., April 15, 2003; 170(8): 4002 - 4010. [Abstract] [Full Text] [PDF]

				R. Mehr, G. Shahaf, A. Sah, and M. Cancro Asynchronous differentiation models explain bone marrow labeling kinetics and predict reflux between the pre- and immature B cell pools Int. Immunol., March 1, 2003; 15(3): 301 - 312. [Abstract] [Full Text] [PDF]

				H. Dalwadi, B. Wei, M. Schrage, T. T. Su, D. J. Rawlings, and J. Braun B Cell Developmental Requirement for the G{alpha}i2 Gene J. Immunol., February 15, 2003; 170(4): 1707 - 1715. [Abstract] [Full Text] [PDF]

				K. Hayakawa, M. Asano, S. A. Shinton, M. Gui, L.-J. Wen, J. Dashoff, and R. R. Hardy Positive Selection of Anti-Thy-1 Autoreactive B-1 Cells and Natural Serum Autoantibody Production Independent from Bone Marrow B Cell Development J. Exp. Med., January 6, 2003; 197(1): 87 - 99. [Abstract] [Full Text] [PDF]

				D. C. Otero, A. N. Anzelon, and R. C. Rickert CD19 Function in Early and Late B Cell Development: I. Maintenance of Follicular and Marginal Zone B Cells Requires CD19-Dependent Survival Signals J. Immunol., January 1, 2003; 170(1): 73 - 83. [Abstract] [Full Text] [PDF]

				J. B. Petro, R. M. Gerstein, J. Lowe, R. S. Carter, N. Shinners, and W. N. Khan Transitional Type 1 and 2 B Lymphocyte Subsets Are Differentially Responsive to Antigen Receptor Signaling J. Biol. Chem., December 6, 2002; 277(50): 48009 - 48019. [Abstract] [Full Text] [PDF]