Role of accessory cells in B cell activation. II. The interaction of B cells with accessory cells results in the exclusive activation of an Lyb5+ B cell subpopulation

H. Boswell, A. Ahmed, I. Scher, A. Singer

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

The possibility was examined that different B cell subsets are activated by different cellular interactions. Primary anti-TNP PFC responses to TNP-KLH, TNP-Ficoll, TNP-BA, and TNP-LPS were generated in vitro from the same unfractionated and unprimed population of normal (DBA/2 X CBA/N)F1 male spleen cells, even though responses to these antigens differed in the cellular interactions each required. In addition to B cells, TNP-KLH responses required both adherent accessory cells and T-helper cells; responses to TNP-Ficoll required only accessory cells; responses to TNP-BA and TNP-LPS required neither accessory cells nor T-helper cells. Treatment of unfractionated spleen cells with anti-Lyb5.1 + C to eliminate Lyb5+ cells resulted in the complete abrogation of the accessory cell-dependent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-BA and TNP-LPS. Analysis of the cell type eliminated by treatment of spleen cells with anti-Lyb5 + C revealed that it was not an accessory cell, since treatment of accessory cell populations with anti-Lyb5 + C had no effect on their accessory cell function; rather, it was the cytotoxic elimination of a subset of B cells expressing the Lyb5 determinant that resulted in the functional abrogation of responsiveness to TNP-KLH and TNP-Ficoll. Thus, in vitro responses to TNP-KLH and TNP-Ficoll resulted entirely from the activation of Lyb5+ B cells alone. One explanation for the fact that these primary accessory cell-dependent responses only activated Lyb5+ B cells and not Lyb5- B cells was that only Lyb5+ B cells were responsive to accessory cell activation signals. To explore this possibility, accessory cells were pulsed with TNP-BA and assayed for their ability to present TNP-BA to B cells. Even though responses to TNP-BA suspension do not require accessory cells, accessory cells could be pulsed with TNP-BA and could function to present TNP-BA and B cells. In contrast to the activation of both Lyb5- and Lyb5+ B cells by TNP-BA free in suspension, TNP BA-presenting accessory cells activated Lyb5+ B cells exclusively. The failure of Lyb5- B cells to be activated by TNP-BA presented by accessory cells cannot be due to an innate inability of these cells to recognize TNP-BA as an antigen; rather, these results strongly support the concept that only Lyb5+ B cells are responsive to accessory cell activation signals. Finally, if the failure of TNP-KLH to activate Lyb5- B cells in vitro is similarly due to the inability of Lyb5- B cells to be activated by accessory cell activation signals, then in vitro activation of B cells by the T-helper cell-dependent response to this antigen also involved an interaction between accessory cells and B cells. To examine the possibility that the activation of Lyb5+ B cells by accessory cells presenting TNP-Ficoll occurred by a pathway identical to that resulting in the activation of Lyb5+ B cells by TNP-KLH, the effect of anti-Lyb7 serum on responses to TNP-Ficoll responses, it had no effect on TNP-KLH responses, suggesting that the activation of Lyb5+ B cells by T-helper cell-dependent and -independent responses could be distinguished by Lyb7-specific sera.

Original languageEnglish (US)
Pages (from-to)1340-1348
Number of pages9
JournalJournal of Immunology
Volume125
Issue number3
StatePublished - 1980
Externally publishedYes

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B-Lymphocytes
Helper-Inducer T-Lymphocytes
B-Lymphocyte Subsets
Spleen
Antigens
Suspensions
trinitrophenyl keyhole limpet hemocyanin
TNP-ficoll

ASJC Scopus subject areas

  • Immunology

Cite this

@article{6e38f1aa41df4375b4c2fa6533e076d3,
title = "Role of accessory cells in B cell activation. II. The interaction of B cells with accessory cells results in the exclusive activation of an Lyb5+ B cell subpopulation",
abstract = "The possibility was examined that different B cell subsets are activated by different cellular interactions. Primary anti-TNP PFC responses to TNP-KLH, TNP-Ficoll, TNP-BA, and TNP-LPS were generated in vitro from the same unfractionated and unprimed population of normal (DBA/2 X CBA/N)F1 male spleen cells, even though responses to these antigens differed in the cellular interactions each required. In addition to B cells, TNP-KLH responses required both adherent accessory cells and T-helper cells; responses to TNP-Ficoll required only accessory cells; responses to TNP-BA and TNP-LPS required neither accessory cells nor T-helper cells. Treatment of unfractionated spleen cells with anti-Lyb5.1 + C to eliminate Lyb5+ cells resulted in the complete abrogation of the accessory cell-dependent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-BA and TNP-LPS. Analysis of the cell type eliminated by treatment of spleen cells with anti-Lyb5 + C revealed that it was not an accessory cell, since treatment of accessory cell populations with anti-Lyb5 + C had no effect on their accessory cell function; rather, it was the cytotoxic elimination of a subset of B cells expressing the Lyb5 determinant that resulted in the functional abrogation of responsiveness to TNP-KLH and TNP-Ficoll. Thus, in vitro responses to TNP-KLH and TNP-Ficoll resulted entirely from the activation of Lyb5+ B cells alone. One explanation for the fact that these primary accessory cell-dependent responses only activated Lyb5+ B cells and not Lyb5- B cells was that only Lyb5+ B cells were responsive to accessory cell activation signals. To explore this possibility, accessory cells were pulsed with TNP-BA and assayed for their ability to present TNP-BA to B cells. Even though responses to TNP-BA suspension do not require accessory cells, accessory cells could be pulsed with TNP-BA and could function to present TNP-BA and B cells. In contrast to the activation of both Lyb5- and Lyb5+ B cells by TNP-BA free in suspension, TNP BA-presenting accessory cells activated Lyb5+ B cells exclusively. The failure of Lyb5- B cells to be activated by TNP-BA presented by accessory cells cannot be due to an innate inability of these cells to recognize TNP-BA as an antigen; rather, these results strongly support the concept that only Lyb5+ B cells are responsive to accessory cell activation signals. Finally, if the failure of TNP-KLH to activate Lyb5- B cells in vitro is similarly due to the inability of Lyb5- B cells to be activated by accessory cell activation signals, then in vitro activation of B cells by the T-helper cell-dependent response to this antigen also involved an interaction between accessory cells and B cells. To examine the possibility that the activation of Lyb5+ B cells by accessory cells presenting TNP-Ficoll occurred by a pathway identical to that resulting in the activation of Lyb5+ B cells by TNP-KLH, the effect of anti-Lyb7 serum on responses to TNP-Ficoll responses, it had no effect on TNP-KLH responses, suggesting that the activation of Lyb5+ B cells by T-helper cell-dependent and -independent responses could be distinguished by Lyb7-specific sera.",
author = "H. Boswell and A. Ahmed and I. Scher and A. Singer",
year = "1980",
language = "English (US)",
volume = "125",
pages = "1340--1348",
journal = "Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "3",

}

TY - JOUR

T1 - Role of accessory cells in B cell activation. II. The interaction of B cells with accessory cells results in the exclusive activation of an Lyb5+ B cell subpopulation

AU - Boswell, H.

AU - Ahmed, A.

AU - Scher, I.

AU - Singer, A.

PY - 1980

Y1 - 1980

N2 - The possibility was examined that different B cell subsets are activated by different cellular interactions. Primary anti-TNP PFC responses to TNP-KLH, TNP-Ficoll, TNP-BA, and TNP-LPS were generated in vitro from the same unfractionated and unprimed population of normal (DBA/2 X CBA/N)F1 male spleen cells, even though responses to these antigens differed in the cellular interactions each required. In addition to B cells, TNP-KLH responses required both adherent accessory cells and T-helper cells; responses to TNP-Ficoll required only accessory cells; responses to TNP-BA and TNP-LPS required neither accessory cells nor T-helper cells. Treatment of unfractionated spleen cells with anti-Lyb5.1 + C to eliminate Lyb5+ cells resulted in the complete abrogation of the accessory cell-dependent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-BA and TNP-LPS. Analysis of the cell type eliminated by treatment of spleen cells with anti-Lyb5 + C revealed that it was not an accessory cell, since treatment of accessory cell populations with anti-Lyb5 + C had no effect on their accessory cell function; rather, it was the cytotoxic elimination of a subset of B cells expressing the Lyb5 determinant that resulted in the functional abrogation of responsiveness to TNP-KLH and TNP-Ficoll. Thus, in vitro responses to TNP-KLH and TNP-Ficoll resulted entirely from the activation of Lyb5+ B cells alone. One explanation for the fact that these primary accessory cell-dependent responses only activated Lyb5+ B cells and not Lyb5- B cells was that only Lyb5+ B cells were responsive to accessory cell activation signals. To explore this possibility, accessory cells were pulsed with TNP-BA and assayed for their ability to present TNP-BA to B cells. Even though responses to TNP-BA suspension do not require accessory cells, accessory cells could be pulsed with TNP-BA and could function to present TNP-BA and B cells. In contrast to the activation of both Lyb5- and Lyb5+ B cells by TNP-BA free in suspension, TNP BA-presenting accessory cells activated Lyb5+ B cells exclusively. The failure of Lyb5- B cells to be activated by TNP-BA presented by accessory cells cannot be due to an innate inability of these cells to recognize TNP-BA as an antigen; rather, these results strongly support the concept that only Lyb5+ B cells are responsive to accessory cell activation signals. Finally, if the failure of TNP-KLH to activate Lyb5- B cells in vitro is similarly due to the inability of Lyb5- B cells to be activated by accessory cell activation signals, then in vitro activation of B cells by the T-helper cell-dependent response to this antigen also involved an interaction between accessory cells and B cells. To examine the possibility that the activation of Lyb5+ B cells by accessory cells presenting TNP-Ficoll occurred by a pathway identical to that resulting in the activation of Lyb5+ B cells by TNP-KLH, the effect of anti-Lyb7 serum on responses to TNP-Ficoll responses, it had no effect on TNP-KLH responses, suggesting that the activation of Lyb5+ B cells by T-helper cell-dependent and -independent responses could be distinguished by Lyb7-specific sera.

AB - The possibility was examined that different B cell subsets are activated by different cellular interactions. Primary anti-TNP PFC responses to TNP-KLH, TNP-Ficoll, TNP-BA, and TNP-LPS were generated in vitro from the same unfractionated and unprimed population of normal (DBA/2 X CBA/N)F1 male spleen cells, even though responses to these antigens differed in the cellular interactions each required. In addition to B cells, TNP-KLH responses required both adherent accessory cells and T-helper cells; responses to TNP-Ficoll required only accessory cells; responses to TNP-BA and TNP-LPS required neither accessory cells nor T-helper cells. Treatment of unfractionated spleen cells with anti-Lyb5.1 + C to eliminate Lyb5+ cells resulted in the complete abrogation of the accessory cell-dependent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-KLH and TNP-Ficoll but not the accessory cell-independent responses to TNP-BA and TNP-LPS. Analysis of the cell type eliminated by treatment of spleen cells with anti-Lyb5 + C revealed that it was not an accessory cell, since treatment of accessory cell populations with anti-Lyb5 + C had no effect on their accessory cell function; rather, it was the cytotoxic elimination of a subset of B cells expressing the Lyb5 determinant that resulted in the functional abrogation of responsiveness to TNP-KLH and TNP-Ficoll. Thus, in vitro responses to TNP-KLH and TNP-Ficoll resulted entirely from the activation of Lyb5+ B cells alone. One explanation for the fact that these primary accessory cell-dependent responses only activated Lyb5+ B cells and not Lyb5- B cells was that only Lyb5+ B cells were responsive to accessory cell activation signals. To explore this possibility, accessory cells were pulsed with TNP-BA and assayed for their ability to present TNP-BA to B cells. Even though responses to TNP-BA suspension do not require accessory cells, accessory cells could be pulsed with TNP-BA and could function to present TNP-BA and B cells. In contrast to the activation of both Lyb5- and Lyb5+ B cells by TNP-BA free in suspension, TNP BA-presenting accessory cells activated Lyb5+ B cells exclusively. The failure of Lyb5- B cells to be activated by TNP-BA presented by accessory cells cannot be due to an innate inability of these cells to recognize TNP-BA as an antigen; rather, these results strongly support the concept that only Lyb5+ B cells are responsive to accessory cell activation signals. Finally, if the failure of TNP-KLH to activate Lyb5- B cells in vitro is similarly due to the inability of Lyb5- B cells to be activated by accessory cell activation signals, then in vitro activation of B cells by the T-helper cell-dependent response to this antigen also involved an interaction between accessory cells and B cells. To examine the possibility that the activation of Lyb5+ B cells by accessory cells presenting TNP-Ficoll occurred by a pathway identical to that resulting in the activation of Lyb5+ B cells by TNP-KLH, the effect of anti-Lyb7 serum on responses to TNP-Ficoll responses, it had no effect on TNP-KLH responses, suggesting that the activation of Lyb5+ B cells by T-helper cell-dependent and -independent responses could be distinguished by Lyb7-specific sera.

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