Antigen receptor-mediated changes in glucose metabolism in B lymphocytes: role of phosphatidylinositol 3-kinase signaling in the glycolytic control of growth

Doughty, Cheryl A.; Bleiman, Blair F.; Wagner, Dean J.; Dufort, Fay J.; Mataraza, Jennifer M.; Roberts, Mary F.; Chiles, Thomas C.

doi:10.1182/blood-2005-12-4788

Cited by 369T-cell and B-cell ImmunologyMetabolism, Diabetes, and CancerCancer, Hypoxia, and Metabolism

Antigen receptor-mediated changes in glucose metabolism in B lymphocytes: role of phosphatidylinositol 3-kinase signaling in the glycolytic control of growth

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Doughty, Cheryl A., Bleiman, Blair F., Wagner, Dean J., Dufort, Fay J., Mataraza, Jennifer M., Roberts, Mary F., Chiles, Thomas C.·2006·Blood

DOI 10.1182/blood-2005-12-4788PMC PMC1895797

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Abstract

The bioenergetic response of B lymphocytes is subject to rapid changes following antigen encounter in order to provide ATP and anabolic precursors necessary to support growth. However, the pathways involved in glucose acquisition and metabolism are unknown. We find that B lymphocytes rapidly increase glucose uptake and glycolysis following B-cell antigen receptor (BCR) crosslinking. Inhibition of glycolysis blocks BCR-mediated growth. Prior to S-phase entry, glucose metabolism shifts from primarily glycolytic to include the pentose phosphate pathway. BCR-induced glucose utilization is dependent upon phosphatidylinositol 3-kinase (PI-3K) activity as evidenced by inhibition of glucose uptake and glycolysis with LY294002 treatment of normal B cells and impaired glucose utilization in B cells deficient in the PI-3K regulatory subunit p85alpha. Activation of Akt is sufficient to increase glucose utilization in B cells. We find that glucose utilization is inhibited by coengagement of the BCR and FcgammaRIIB, suggesting that limiting glucose metabolism may represent an important mechanism underlying FcgammaRIIB-mediated growth arrest. Taken together, these findings demonstrate that both growth-promoting BCR signaling and growth-inhibitory FcgammaRIIB signaling modulate glucose energy metabolism. Manipulation of these pathways may prove to be useful in the treatment of lymphoproliferative disorders, wherein clonal expansion of B lymphocytes plays a role.

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Activated B cells greatly increase glucose and glutamine metabolism during clonal expansion, similar to T cells.
“Upon activation, B cells greatly enhance glucose and glutamine metabolism during clonal expansion comparable to T cells (Doughty et al., 2006; Garcia-Manteiga et al., 2011; Le et al., 2012).”
From Mitochondria in the Regulation of Innate and Adaptive Immunity (2015) · cites this paper as Doughty et al., 2006
TCR/CD28 stimulation of T cells, surface immunoglobulin stimulation on B cells, and TLR stimulation of macrophages and DCs all promote changes in aerobic glycolysis characteristic of the Warburg effect.
“TCR/CD28 stimulation of T cells (6), the stimulation of surface immunoglobulin on B cells (41), and TLR stimulation of macrophages and dendritic cells (DCs) (42, 43) all promote changes in aerobic glycolysis characteristic of the Warburg effect.”
From Fueling Immunity: Insights into Metabolism and Lymphocyte Function (2013) · cites this paper as [41]

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Authors: Doughty, C. A., Bleiman, B. F., Wagner, D. J., Dufort, F. J., Mataraza, J. M., Roberts, M. F., & Chiles, T. C.
Affiliations: Boston College (US)
ORCID: Mataraza, Jennifer M.
Roberts, Mary F.
Venue: Blood
Publisher: American Society of Hematology
Published: 2006-06-01
Volume: 107
Issue: 11
Pages: 4458-4465
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2005-12-4788
PMC: PMC1895797
OpenAlex: W2019383774
Cited by: 369
References: 53
Citations by year: 2026: 17 · 2025: 27 · 2024: 25 · 2023: 34 · 2022: 25 · 2021: 48 · 2020: 32 · 2019: 24 · 2018: 25 · 2017: 18 · 2016: 21 · 2015: 10 · 2014: 10 · 2013: 9 · 2012: 12
FWCI: 3.29
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: University of British Columbia
U.S. Public Health Service
National Institute of Allergy and Infectious Diseases (AI-49994)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: B cells, B cell receptor signaling, glucose metabolism, glycolysis, glucose uptake, phosphatidylinositol 3-kinase, Akt, p85α, Fc gamma receptor IIb, pentose phosphate pathway, cell growth, bioenergetics, lymphoproliferative disorders, clonal expansion
MeSH terms: Animals, B-Lymphocytes, Glucose, Glycolysis, Mice, Inbred BALB C, Receptors, Antigen, Receptors, Antigen, B-Cell, Signal Transduction, Antigens, CD, Receptors, IgG, Phosphatidylinositol 3-Kinases, Cell Growth Processes, Proto-Oncogene Proteins c-akt, Mice

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Antigen receptor-mediated changes in glucose metabolism in B lymphocytes: role of phosphatidylinositol 3-kinase signaling in the glycolytic control of growth

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