Proliferation of Bone Marrow Pro-B Cells Is Dependent on Stimulation by the Pituitary/Thyroid Axis
Abstract
The frequency and absolute number of pro-B, pre-B, and B cells in the bone marrow of the hypothyroid strain of mice are significantly reduced compared with those of their normal littermates. To investigate why this is the case, various B cell developmental processes were examined in the thyroid hormone-deficient mice. These studies revealed that the frequency of pro-B cells in the S-G2/M phase of the cell cycle was significantly reduced in hypothyroid mice. That thyroid hormone deficiency was responsible for this proliferation defect was established by demonstrating that treatment of hypothyroid mice with thyroxine resulted in a specific increase in the frequency and total number of cycling pro-B cells. The latter effect was paralleled by increases in the frequency and number of bone marrow B lineage cells. Additional in vitro experiments revealed that at least some thyroid hormone effects were directly mediated on the bone marrow. Taken together, these data demonstrate that thyroid hormones are required for normal B cell production in the bone marrow through regulation of pro-B cell proliferation and establish a role for the pituitary/thyroid axis in B cell development.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Thyroid hormones are required for normal B-cell production in the bone marrow.
“Thyroid hormones are required for normal B-cell production in the bone marrow [130].”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [130]
Cites
Conditions controlling the proliferation of haemopoietic stem cells in vitro
Dexter, T. M., Allen, T., & Lajtha, L. G. (1977) · Journal of Cellular Physiology · doi:10.1002/jcp.1040910303 · Cited by 2,120 · see citing works
Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow.
Hardy, R. R., Carmack, C. E., Shinton, S. A., Kemp, J. D., & Hayakawa, K. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.173.5.1213 · Cited by 1,604 · see citing works
The c-erb-A gene encodes a thyroid hormone receptor
Weinberger, C., Thompson, C. C., Ong, E. S., Lebo, R. V., Gruol, D. J., & Evans, R. M. (1986) · Nature · doi:10.1038/324641a0 · Cited by 1,477 · see citing works
The c-erb-A protein is a high-affinity receptor for thyroid hormone
Sap, J., Múñoz, A., Damm, K., Goldberg, Y., Ghysdael, J., Leutz, A., Beug, H., & Vennström, B. (1986) · Nature · doi:10.1038/324635a0 · Cited by 1,314 · see citing works
Thyroid Hormone Receptors: Multiple Forms, Multiple Possibilities*
Lazar, M. A. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-2-184 · Cited by 1,061 · see citing works
Stimulation of B-cell progenitors by cloned murine interleukin-7
Namen, A. E., Lupton, S. D., Hjerrild, K., Wignall, J. M., Mochizuki, D. Y., Schmierer, A. E., Mosley, B., March, C. J., Urdal, D. L., Gillis, S. A., et al. (1988) · Nature · doi:10.1038/333571a0 · Cited by 803 · see citing works
Ordered rearrangement of immunoglobulin heavy chain variable region segments
Alt, F. W., Yancopoulos, G. D., Blackwell, T. K., Wood, C., Thomas, E., Boss, M., Coffman, R., Rosenberg, N., Tonegawa, S., & Baltimore, D. (1984) · The EMBO Journal · doi:10.1002/j.1460-2075.1984.tb01955.x · Cited by 733 · see citing works
Horseman, N. D., Zhao, W., Montecino‐Rodriguez, E., Tanaka, M., Nakashima, K., Engle, S. J., Smith, F., Markoff, E., & Dorshkind, K. (1997) · The EMBO Journal · doi:10.1093/emboj/16.23.6926 · Cited by 649 · see citing works
Self-citationSamuels, H. H., Stanley, F. M., & Casanova, J. (1979) · Endocrinology · doi:10.1210/endo-105-1-80 · Cited by 649 · see citing works
Long-term culture of B lymphocytes and their precursors from murine bone marrow.
Whitlock, C. A., & Witte, O. N. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.11.3608 · Cited by 599 · see citing works
Ligand induction of a transcriptionally active thyroid hormone receptor coactivator complex.
Fondell, J. D., Ge, H., & Roeder, R. G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8329 · Cited by 578 · see citing works
Keller, G. M., Paige, C. J., Gilboa, E., & Wagner, E. F. (1985) · Nature · doi:10.1038/318149a0 · Cited by 572 · see citing works
Abramson, S. B., Miller, R. G., & Phillips, R. (1977) · The Journal of Experimental Medicine · doi:10.1084/jem.145.6.1567 · Cited by 559 · see citing works
The Molecular Basis of Thyroid Hormone Action
Epstein, F. H., & Brent, G. A. (1994) · New England Journal of Medicine · doi:10.1056/nejm199409293311306 · Cited by 528 · see citing works
HODGSON, G. S., & Bradley, T. R. (1979) · Nature · doi:10.1038/281381a0 · Cited by 509 · see citing works
Regulation of hemopoiesis by bone marrow stromal cells and their products
Dorshkind, K. (1990) · Annual Review of Immunology · doi:10.1146/annurev.iy.08.040190.000551 · Cited by 504 · see citing works
Identification of a tHyroid Hormone Receptor That Is Pituitary-Specific
Hodin, R. A., Lazar, M. A., Wintman, B. I., Darling, D. S., Koenig, R. J., Larsen, P. R., Moore, D. D., & Chin, W. W. (1989) · Science · doi:10.1126/science.2539642 · Cited by 486 · see citing works
V(D)J Recombination: Molecular Biology and Regulation
Schatz, D. G., Oettinger, M. A., & Schlissel, M. S. (1992) · Annual Review of Immunology · doi:10.1146/annurev.iy.10.040192.002043 · Cited by 471 · see citing works
Koenig, R. J., Lazar, M. A., Hodin, R. A., Brent, G. A., Larsen, P. R., Chin, W. W., & Moore, D. D. (1989) · Nature · doi:10.1038/337659a0 · Cited by 430 · see citing works
Fraichard, A., Chassande, O., Plateroti, M., Roux, J. P., Trouillas, J., Dehay, C., Legrand, C., Gauthier, K. C., Kédinger, M., Malaval, L., et al. (1997) · The EMBO Journal · doi:10.1093/emboj/16.14.4412 · Cited by 349 · see citing works
Collins, L., & Dorshkind, K. A. (1987) · The Journal of Immunology · doi:10.4049/jimmunol.138.4.1082 · Cited by 340 · see citing works
Self-citationThyroid hormone receptors: multiple forms, multiple possibilities
Lazar, M. A. (1993) · Endocrine Reviews · doi:10.1210/er.14.2.184 · Cited by 322 · see citing works
Schmid, I., Uíttenbogaart, C. H., Keld, B., et al. (1994) · Journal of Immunological Methods · doi:10.1016/0022-1759(94)90390-5 · Cited by 315 · see citing works
Clark, R. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.2.0296 · Cited by 314 · see citing works
Forrest, D., Sjöberg, M., & Vennström, B. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb08270.x · Cited by 301 · see citing works
IL-2 receptor α chain (CD25JAC) expression defines a crucial stage in pre-B cell development
Rolink, A. G., Grawunder, U., Winkler, T., Karasuyama, H., & Melchers, F. (1994) · International Immunology · doi:10.1093/intimm/6.8.1257 · Cited by 294 · see citing works
Functional heterogeneity is associated with the cell cycle status of murine hematopoietic stem cells
Fleming, W., Alpern, E., Uchida, N., Ikuta, K., Spangrude, G. J., & Weissman, I. L. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.4.897 · Cited by 277 · see citing works
The surrogate light chain in B-cell development
Melchers, F., Karasuyama, H., Haasner, D., Bauer, S. R., Kudō, A., Sakaguchi, N., Jameson, B. A., & Rolink, A. G. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90060-x · Cited by 274 · see citing works
Cells And Molecules That Regulate B Lymphopoiesis In Bone Marrow
Kincade, P. W., Lee, G., Pietrangeli, C. E., Hayashi, S., & Gimble, J. M. (1989) · Annual Review of Immunology · doi:10.1146/annurev.iy.07.040189.000551 · Cited by 262 · see citing works
Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary.
Bradley, D. J., Young, W. S., & Weinberger, C. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.18.7250 · Cited by 250 · see citing works
Lazar, M. A., Hodin, R. A., Darling, D. S., & Chin, W. W. (1988) · Molecular Endocrinology · doi:10.1210/mend-2-10-893 · Cited by 250 · see citing works
Population Dynamics of Bone Marrow B Lymphocytes
Osmond, D. G. (1986) · Immunological Reviews · doi:10.1111/j.1600-065x.1986.tb01504.x · Cited by 206 · see citing works
Corcoran, A. E., Smart, F. M., Cowling, R. J., et al. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00543.x · Cited by 204 · see citing works
Identification of a point mutation in the thyrotropin receptor of the hyt/hyt hypothyroid mouse
Stein, S. A., Oates, E. L., Hall, C., Grumbles, R. M., Fernandez, L. M., Taylor, N., Puett, D., & Jin, S. (1994) · Molecular Endocrinology · doi:10.1210/mend.8.2.8170469 · Cited by 200 · see citing works
Inherited Primary Hypothyroidism in Mice
Beamer, W. G., Eicher, E. M., Maltais, L. J., & Southard, J. L. (1981) · Science · doi:10.1126/science.7209519 · Cited by 156 · see citing works
Sjöberg, M., Vennström, B., & Forrest, D. (1992) · Development · doi:10.1242/dev.114.1.39 · Cited by 155 · see citing works
Experimental Models for Understanding B Lymphocyte Formation
Kincade, P. W. (1987) · Advances in immunology · doi:10.1016/s0065-2776(08)60032-2 · Cited by 129 · see citing works
Lazar, M. A., Hodin, R. A., & Chin, W. W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.20.7771 · Cited by 129 · see citing works
Myelogenous production and maturation of B lymphocytes in the mouse.
Landreth, K. S., Rosse, C., & Clagett, J. A. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.127.5.2027 · Cited by 126 · see citing works
Transendothelial migration and trafficking of leukocytes in LFA-1-deficient mice
Andrew, D. P., Spellberg, J. P., Takimoto, H., Schmits, R., Mak, T. W., & Zukowski, M. M. (1998) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199806)28:06 · Cited by 124 · see citing works
Sex Hormones as Negative Regulators of Lymphopoiesis
Kincade, P. W., Medina, K. L., & Smithson, G. M. (1994) · Immunological Reviews · doi:10.1111/j.1600-065x.1994.tb00661.x · Cited by 115 · see citing works
The turnover of B-cell populations
Osmond, D. G. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90322-c · Cited by 113 · see citing works
Hastings, M. L., Milcarek, C., Martincic, K., Peterson, M. L., & Munroe, S. H. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.21.4296 · Cited by 112 · see citing works
Osmond, D. G., Rico-Vargas, S., Valenzona, H., et al. (1994) · Immunological Reviews · doi:10.1111/j.1600-065x.1994.tb00891.x · Cited by 79 · see citing works
Apoptosis during B lymphopoiesis in mouse bone marrow
Lu, L., & Osmond, D. G. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.11.5136 · Cited by 78 · see citing works
Gu, W., Du, G. G., Kopp, P. A., et al. (1995) · Endocrinology · doi:10.1210/endo.136.7.7789342 · Cited by 78 · see citing works
Wood, W. M., OCRAN, K. W., Gordon, D. F., & Ridgway, E. C. (1991) · Molecular Endocrinology · doi:10.1210/mend-5-8-1049 · Cited by 73 · see citing works
Dorshkind, K. A. (1986) · The Journal of Immunology · doi:10.4049/jimmunol.136.2.422 · Cited by 72 · see citing works
Self-citationDefective B cell development in Snell dwarf (dw/dw) mice can be corrected by thyroxine treatment
Montecino‐Rodriguez, E., Clark, R. T., Johnson, A. H., Collins, L., & Dorshkind, K. A. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.157.8.3334 · Cited by 62 · see citing works
Self-citationPrimary B cell development is impaired in mice with defects of the pituitary/thyroid axis
Montecino‐Rodriguez, E., CLARK, R. G., Powell-Braxton, L., & Dorshkind, K. A. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.6.2712 · Cited by 62 · see citing works
Self-citationRolink, A. G., & Melchers, F. (1993) · Advances in immunology · doi:10.1016/s0065-2776(08)60499-x · Cited by 60 · see citing works
Molecular Biology of B-Cell and T-Cell Development
Monroe, J. G. (1998) · Humana Press eBooks · doi:10.1007/978-1-4757-2778-4 · Cited by 49 · see citing works
Thyroid Hormone Receptor Variant α2
Yang, Y.-Z., Burgos-Trinidad, M., Wu, Y., & Koenig, R. J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.45.28235 · Cited by 49 · see citing works
Borghesi, L., Smithson, G. M., & Kincade, P. W. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.9.4171 · Cited by 47 · see citing works
Effects of 5-fluorouracil on B lymphocyte lineage cells.
Větvička, V., Kincade, P. W., & Witte, P. L. (1986) · The Journal of Immunology · doi:10.4049/jimmunol.137.8.2405 · Cited by 38 · see citing works
Dorshkind, K. A. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.146.12.4204 · Cited by 37 · see citing works
Self-citationThe erbA/thyroid hormone receptor genes in development of the central nervous system.
Forrest, D. (1994) · PubMed · Cited by 33 · see citing works
Henderson, A. J., Narayanan, R., Collins, L., et al. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.6.1973 · Cited by 31 · see citing works
Toms, S. A., Hercbergs, A. A., Liu, J., et al. (1998) · PubMed · Cited by 18 · see citing works
Regulation of Lymphocyte Development by Microenvironmental and Systemic Factors
Montecino‐Rodriguez, E., & Dorshkind, K. A. (1998) · Humana Press eBooks · doi:10.1007/978-1-4757-2778-4_11 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Interaction of the endocrine system with inflammation: a function of energy and volume regulation
Straub, R. H. (2014) · Arthritis Research & Therapy · doi:10.1186/ar4484 · Cited by 121 · see citing works
“duction in the bone marrow [130].”
Hyperthyroidism-driven bone loss depends on BMP receptor Bmpr1a expression in osteoblasts
Lademann, F., Rijntjes, E., Köhrle, J., Tsourdi, E., Hofbauer, L. C., & Rauner, M. (2024) · Communications Biology · doi:10.1038/s42003-024-06227-0 · Cited by 8 · see citing works
- Authors
- Foster, M. P., Montecino-Rodriguez, E., & Dorshkind, K.
- Affiliations
- University of California, Los Angeles (US)
- Department of Pathology and Laboratory Medicine and Jonsson Comprehensive Cancer Center, School of Medicine, University of California , Los Angeles, CA 90095
- ORCID
- Dorshkind, Kenneth
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-12-01
- Volume
- 163
- Issue
- 11
- Pages
- 5883-5890
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2155455544
- Cited by
- 75
- References
- 60
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 4 · 2022: 7 · 2021: 4 · 2020: 6 · 2019: 6 · 2018: 1 · 2017: 2 · 2015: 3 · 2014: 5 · 2013: 5 · 2012: 1
- FWCI
- 0.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA-16 042, P30CA016042)
- National Institute of Allergy and Infectious Diseases (AI21256)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- pro-B cells, B cell development, thyroid hormones, hypothyroidism, thyroxine, pituitary-thyroid axis, bone marrow, cell cycle, B-cell lineage, B cell proliferation
- MeSH terms
- Animals, B-Lymphocytes, Bone Marrow, Cell Division, Cells, Cultured, Fluorouracil, Hematopoietic Stem Cells, Hypothyroidism, Immunoglobulin M, Mice, Mutant Strains, Pituitary Gland, Receptors, Antigen, B-Cell, Thyroid Gland, Thyroid Hormones, Triiodothyronine, Apoptosis, Leukocyte Common Antigens, Cell Lineage, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review