Cited by 196Cancer, Hypoxia, and MetabolismCancer Cells and MetastasisImmune cells in cancer

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Lactate is a mediator of metabolic cooperation between stromal carcinoma associated fibroblasts and glycolytic tumor cells in the tumor microenvironment

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Rattigan, Yanique I., Patel, Brijesh B., Ackerstaff, Ellen, Sukenick, George, Koutcher, Jason A., Glod, John W., Banerjee, Debabrata·2012·Experimental Cell Research

DOI 10.1016/j.yexcr.2011.11.014PMC PMC3402174

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Abstract

Human mesenchymal stem cells (hMSCs) are bone marrow-derived stromal cells, which play a role in tumor progression. We have shown earlier that breast cancer cells secrete higher levels of interleukin-6 (IL-6) under hypoxia, leading to the recruitment of hMSCs towards hypoxic tumor cells. We found that (i) MDA-MB-231 cells secrete significantly higher levels of lactate (3-fold more) under hypoxia (1% O(2)) than under 20% O(2) and (ii) lactate recruits hMSCs towards tumor cells by activating signaling pathways to enhance migration. The mRNA and protein expression of functional MCT1 in hMSCs is increased in response to lactate exposure. Thus, we hypothesized that hMSCs and stromal carcinoma associated fibroblasts (CAFs) in the tumor microenvironment have the capacity to take up lactate expelled from tumor cells and use it as a source of energy. Our (13)C NMR spectroscopic measurements indicate that (13)C-lactate is converted to (13)C-alpha ketoglutarate in hMSCs and CAFs supporting this hypothesis. To our knowledge this is the first in vitro model system demonstrating that hMSCs and CAFs can utilize lactate produced by tumor cells.

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Additional file 1 of 2P-FLIM unveils time-dependent metabolic shifts during osteogenic differentiation with a key role of lactate to fuel osteogenesis via glutaminolysis identified
Neto, N. G. B., Suku, M., Hoey, D. A., & Monaghan, M. G. (2023) · Figshare · doi:10.6084/m9.figshare.24797938
Additional file 4 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585433
Additional file 10 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585451
Additional file 14 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585463
Additional file 7 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585442
Additional file 2 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585427
Additional file 16 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585469
Additional file 5 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585436
Additional file 11 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585454
Additional file 12 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585457
Additional file 3 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585430
Additional file 15 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585466
Additional file 1 of Impaired anaplerosis is a major contributor to glycolysis inhibitor toxicity in glioma
Khadka, S., Arthur, K., Barekatain, Y., Behr, E., Washington, M., Ackroyd, J., Crowley, K., Suriyamongkol, P., Lin, Y.-H., Pham, C.-D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14850809
Additional file 6 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585439
Additional file 17 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585472
Additional file 13 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585460
Additional file 8 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585445
Additional file 9 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585448
Additional file 1 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585424
Additional file 18 of Osteosarcoma tumors maintain intra-tumoral transcriptional heterogeneity during bone and lung colonization
Rajan, S., Franz, E., McAloney, C. A., Vetter, T. A., Cam, M., Gross, A. C., Taslim, C., Wang, M., Cannon, M. V., Oles, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26585475
Advances in pyrimidine-like heterocyclic scaffolds: Innovative synthetic method for malic enzyme inhibition in pancreatic ductal adenocarcinoma (PDAC) - A comprehensive review
Mehta, S., Patel, I., & Patel, G. (2026) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2026.118657
Metabolic Constraints and Interactions Drive T-cell Function and Exhaustion in Cancer Progression
Tzeng, S., & Tsai, C.-H. (2026) · Journal of Medical Sciences · doi:10.4103/jmedsci.jmedsci_234_25
Targeting the metabolic environment to modulate T cell effector function
Matias, M. I. (2019) · theses.fr (ABES) · doi:10.70675/0582ddaaze61dz4707z9cb1zdb8fe1d82653
Caractérisation des récepteurs de l'inositol (1,4,5) trisphosphate dans le cancer mammaire humain invasif : nouvel outil diagnostique et pronostique?
Foulon, A. (2020) · theses.fr (ABES) · doi:10.70675/59a41e27z21a8z4dc1z8377zd1fa49137e4d
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Tafech, A. (2022) · theses.fr (ABES) · doi:10.70675/076075b7z825bz48cbz82d2z47b9e8a6846d
Metabolic Reprogramming in the Bladder Cancer Microenvironment: Bridging Fundamental Research and Therapeutic Avenues for Cancer-Associated Fibroblasts
da Silva, A. C. R., Baltazar, F., & Afonso, J. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-12166-0_5
Metabolic reprogramming and plasticity in breast Cancer: Mechanisms driving tumor progression, metastasis, and therapeutic resistance
Yuan, J., Zhang, H., Huang, J., Wang, B., Wang, M., & Yang, L. (2026) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2026.189733
Role of stromal fibroblasts in prostate carcinoma progression and metabolic reprogramming of cancer cells
Marini, A. (2014) · UnissResearch (Università degli Studi di Sassari)
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Authors: Rattigan, Y. I., Patel, B. B., Ackerstaff, E., Sukenick, G., Koutcher, J. A., Glod, J. W., & Banerjee, D.
Affiliations: Rutgers Cancer Institute (US)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Banerjee, Debabrata
ORCID: Ackerstaff, Ellen
Koutcher, Jason A.
Glod, John W.
Banerjee, Debabrata
Venue: Experimental Cell Research
Publisher: Elsevier BV
Published: 2012-02
Volume: 318
Issue: 4
Pages: 326-335
ISSN: 0014-4827 (ISSN-L)
DOI: 10.1016/j.yexcr.2011.11.014
PMC: PMC3402174
OpenAlex: W2106506721
Cited by: 196
References: 46
Citations by year: 2026: 7 · 2025: 10 · 2024: 27 · 2023: 16 · 2022: 13 · 2021: 15 · 2020: 20 · 2019: 10 · 2018: 9 · 2017: 16 · 2016: 11 · 2015: 15 · 2014: 12 · 2013: 9 · 2012: 6
FWCI: 2.94
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Experimental Cell Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (CA83084, P01 CA94060)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords: lactate, metabolic cooperation, human mesenchymal stem cells, tumor microenvironment, hypoxia, breast cancer, MDA-MB-231 cells, lactate transport, MCT1, alpha-ketoglutarate, interleukin-6, cell migration, 13C NMR
MeSH terms: Hypoxia, Breast Neoplasms, Carcinoma, Cell Communication, Female, Fibroblasts, Glycolysis, Humans, Stromal Cells, Lactic Acid, Paracrine Communication, Cell Line, Tumor, Metabolic Networks and Pathways, Tumor Microenvironment, Mesenchymal Stem Cells

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Lactate is a mediator of metabolic cooperation between stromal carcinoma associated fibroblasts and glycolytic tumor cells in the tumor microenvironment

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