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Tumor-Derived Granulocyte-Macrophage Colony-Stimulating Factor Regulates Myeloid Inflammation and T Cell Immunity in Pancreatic Cancer
Open accessAbstract
Cancer-associated inflammation is thought to be a barrier to immune surveillance, particularly in pancreatic ductal adenocarcinoma (PDA). Gr-1(+) CD11b(+) cells are a key feature of cancer inflammation in PDA, but remain poorly understood. Using a genetically engineered mouse model of PDA, we show that tumor-derived granulocyte-macrophage colony-stimulating factor (GM-CSF) is necessary and sufficient to drive the development of Gr-1(+) CD11b(+) cells that suppressed antigen-specific T cells. In vivo, abrogation of tumor-derived GM-CSF inhibited the recruitment of Gr-1(+) CD11b(+) cells to the tumor microenvironment and blocked tumor development-a finding that was dependent on CD8(+) T cells. In humans, PDA tumor cells prominently expressed GM-CSF in vivo. Thus, tumor-derived GM-CSF is an important regulator of inflammation and immune suppression within the tumor microenvironment.
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“FAK inhibition-mediated reprogramming of the stroma was shown to overcome radiation resistance and sensitize the tumors to immunotherapy175”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [175]
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Zhao, Q., Lin, L., Du, G.-W., Wang, Z., Li, X., & Fang, J. (2020) · Immunopharmacology and Immunotoxicology · doi:10.1080/08923973.2020.1778722 · Cited by 4
Dhanisha, S. S., Salcedo-Noriega, M. F., Vaish, U., Kannan, A. B., Suryansh, S., Bhandari, S., Chatre, S., Jain, T., Dudeja, V., & Iyer, S. (2026) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2026.01.009 · Cited by 3
Myeloid diversity in tumors: Shaped by genes, location, and time
Nogales-Pons, M., Munárriz-Paños, M., Aceña-Gonzalo, T., & Casanova-Acebes, M. (2026) · The Journal of Experimental Medicine · doi:10.1084/jem.20252267 · Cited by 3
Divergent granulopoiesis at extramedullary sites safeguards antibacterial host defense
Silvestre-Roig, C., Chèvre, R., Farjia, M., Bender, A., Vöcking, L.-M., Richter, M., Hageb, A., Suerdieck, V., Cerro, F. J. A., Braster, Q., et al. (2026) · Science Immunology · doi:10.1126/sciimmunol.adw7077 · Cited by 11
Oncolytic viruses expressing MATEs facilitate target-independent T-cell activation in tumors
Peter, M., Mundt, B., Menze, A., Woller, N., Volk, V., Ernst, A. M., Öhler, L. A., Talbot, S. R., Wedemeyer, H. H., Falk, C. S., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-024-00187-y · Cited by 3
“The frequently used GM-CSF, also incorporated in T-Vec, is well-established for the maturation of dendritic cells, but may also promote MDSCs and immunosuppression in tumor tissue (Bayne et al, 2012).”
The Interplay Between DNA Repair and the Immune Microenvironment in Pancreatic Cancer
Ciner, A., Hosein, P. J., Jiang, Y., & Rassool, F. V. (2025) · Biomedicines · doi:10.3390/biomedicines13051031 · Cited by 3
“In PDAC, Bayne and colleagues highlighted the role of granulocyte–macrophage colony-stimulating factor in MDSC recruitment, T-cell dysfunction, and tumor growth in the KPC mouse model [36].”
Myeloid-derived suppressor cells in autoimmune diseases
Fujii, W., Ashihara, E., & Kawahito, Y. (2014) · Inflammation and Regeneration · doi:10.2492/inflammregen.34.124 · Cited by 3
Current approaches to immunotherapy in noncolorectal gastrointestinal malignancies
de Jesus, V. H. F., Felismino, T. C., Silva, M. J. D. B. E., Silva, V. S. E., & Riechelmann, R. P. (2018) · Clinics · doi:10.6061/clinics/2018/e510s · Cited by 3
“GM-CSF) that prevent effector T cells from infiltrating and destroying the tumor (40,41).”
BackgroundZhang, J., Späth, S. S., Weissman, S. M., & Katz, S. G. (2019) · Methods in molecular biology · doi:10.1007/978-1-0716-0203-4_10 · Cited by 3
Systemic Regulation of Metastatic Disease by Extracellular Vesicles and Particles
Wang, G., Kenific, C. M., Lieberman, G., Zhang, H., & Lyden, D. C. (2022) · Springer eBooks · doi:10.1007/978-3-031-09518-4_2 · Cited by 3
Role of tumor associated macrophages in regulating pancreatic cancer progression
Caso, R., & Miller, G. (2016) · World Journal of Immunology · doi:10.5411/wji.v6.i1.9 · Cited by 3
Innamarato, P., Morse, J. M., Mackay, A., Asby, S. C., Beatty, M. S., Blauvelt, J. L., Kidd, S., Mullinax, J. E., Sarnaik, A. A., & Pilon‐Thomas, S. (2021) · BMC Cancer · doi:10.1186/s12885-021-08522-z · Cited by 3
Tumor-Induced Myeloid-Derived Suppressor Cells
Sanctis, F. D., Bronte, V., & Ugel, S. (2017) · ASM Press eBooks · doi:10.1128/9781555819194.ch49 · Cited by 3
Immunohistochemical Assessment of Immune Cells in Mouse Tumor TissuePreprint
Bayne, L. J., & Vonderheide, R. H. (2013) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot077206 · Cited by 3
Self-citationNetrin G1 Ligand is a new stromal immunomodulator that promotes pancreatic cancerPreprint
Costa, D. B. V., Francescone, R., Franco‐Barraza, J., Luong, T., Graves, M., de Aquino, A. M., Steele, N. G., Gardiner, J. C., dos Santos, S. A. A., Ogier, C., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.15.594354 · Cited by 3
Molecular Mechanisms of Immune Resistance in Pancreatic Cancer: An Update
Pang, W. M., Lim, W., Ngai, Z. N., & Koh, R. Y. (2025) · Current Pharmaceutical Biotechnology · doi:10.2174/0113892010365485250330110031 · Cited by 2
Zhang, D., Huang, C., Zhou, L., Wang, B., Zhou, W. L., Xia, T., Shen, P., Li, S., & Gao, Y. (2025) · Chinese Medicine · doi:10.1186/s13020-025-01197-9 · Cited by 2
Adverse prognosis of GM-CSF expression in human cutaneous melanoma
García‐Martínez, E., Nieto‐Valle, A., Barrio‐Alonso, C., López-Navarro, B., Avilés-Izquierdo, J. A., Parra‐Blanco, V., Gutiérrez‐Seijo, A., Sánchez‐Mateos, P., & Samaniego, R. (2025) · Neoplasia · doi:10.1016/j.neo.2025.101240 · Cited by 2
The circadian gene Dec2 promotes pancreatic cancer progression and dormancy through immune evasion
Wang, L., Harris, C. R., Dudgeon, C., Prela, O., Cazarin, J., Shih, C.-H., Davidson, C., Casabianca, A., De, S., Narrow, W. C., et al. (2026) · Developmental Cell · doi:10.1016/j.devcel.2026.04.001 · Cited by 2
Targeting KRAS for cancer therapy
Jia, J., Liu, R., Adamide, T. A., Fernandez, I. E., & Stathopoulos, G. T. (2026) · British Journal of Pharmacology · doi:10.1111/bph.70546 · Cited by 3
Management of Advanced Pancreatic Cancer through Stromal Depletion and Immune Modulation
Liu, T., Cheng, S., Xu, Q., & Wang, Z. P. (2022) · Medicina · doi:10.3390/medicina58091298 · Cited by 2
“MDSCs increase the expression of tumor PD-L1 expression via the activation of EGFR/MAPK signaling pathway and result in CD8+ T cell exhaustion and T regulatory cell expansion [58,60], thus abrogation of tumor-derived GM-CSF secretion prohibits the MDSCs infiltration and blocks tumor development by increasing the numbe…”
BackgroundLiu, Z., Zhang, Y., & Wu, C. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115664 · Cited by 2
Chatterjee, A., Bandyopadhyay, A., Maiti, T. K., & Bhattacharyya, T. K. (2024) · Microsystems & Nanoengineering · doi:10.1038/s41378-024-00769-3 · Cited by 2
Regulatory T-Cells and Th17 Cells in Tumor Microenvironment
Kim, C. H. (2020) · Springer eBooks · doi:10.1007/978-3-030-30845-2_6 · Cited by 2
Inflammatory Dysregulation and Cancer: From Molecular Mechanisms to Therapeutic Opportunities
Steele, C. W., Jamieson, N. B., & Carter, C. R. (2014) · Springer eBooks · doi:10.1007/978-94-017-9421-3_17 · Cited by 2
Macrophage Differentiation and Activation States in the Tumor Microenvironment
Ginderachter, J. A. V. (2013) · Springer eBooks · doi:10.1007/978-94-007-6217-6_17 · Cited by 1
Desmoplastic Reaction In Pancreatic Ductal Adenocarcinoma
Aghamaliyev, U., Hajiyeva, Y., & Rückert, F. (2016) · Pancreas - Open Journal · doi:10.17140/poj-1-107 · Cited by 2
Saranaruk, P., Waraasawapati, S., Chamgramol, Y., Sawanyawisuth, K., Paungpan, N., Somphud, N., Wongkham, C., Okada, S., Wongkham, S., & Vaeteewoottacharn, K. (2023) · PeerJ · doi:10.7717/peerj.14883 · Cited by 2
“Cancer-promoting functions are established in breast, glioma, liver, and pancreatic cancers ( Bayne et al., 2012 ; Kohanbash et al., 2013 ; Lin et al., 2017 ; Reggiani et al., 2017 ; Revoltella, Menicagli & Campani, 2012 ), whereas cancer-preventing roles are demonstrated in bladder, cervical,…”
Immunotherapy for Pancreatic Cancer
Sunami, Y., Rieder, S., Michl, P., & Kleeff, J. H. (2023) · Springer eBooks · doi:10.1007/978-3-030-80962-1_223-1 · Cited by 3
Myeloid-Derived Suppressor Cells in Tumor-Induced T Cell Suppression and Tolerance
Serafini, P., & Bronte, V. (2014) · Springer eBooks · doi:10.1007/978-1-4899-8056-4_4 · Cited by 2
“either GM-CSF production or CD11b+Gr-1+ cell activity allowed to restore antitumor immunity [110], [111].”
BackgroundThe Role of the JAK/STAT Signalling Pathway in Immunoregulation of Gastrointestinal Cancers
Vaddi, K. (2017) · Springer eBooks · doi:10.1007/978-3-319-43063-8_7 · Cited by 2
Metadata
- Authors
- Bayne, L. J., Beatty, G. L., Jhala, N., Clark, C. E., Rhim, A. D., Stanger, B. Z., & Vonderheide, R. H.
- Affiliations
- University of Pennsylvania (US)
- Abramson Cancer Center (US)
- Corresponding author
- Vonderheide, Robert H.
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 21
- Issue
- 6
- Pages
- 822-835
- ISSN
- 1535-6108 (ISSN-L)
- PMC
- PMC3575028
- OpenAlex
- W2129176863
- Cited by
- 947
- References
- 45
- Citations by year
- 2026: 49 · 2025: 44 · 2024: 47 · 2023: 72 · 2022: 83 · 2021: 82 · 2020: 91 · 2019: 63 · 2018: 59 · 2017: 65 · 2016: 78 · 2015: 60 · 2014: 68 · 2013: 77 · 2012: 9
- FWCI
- 29.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 411 d)
- 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
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Abramson Family Cancer Research Institute
- National Institutes of Health (K08 088945, K12 CA076931)
- American Gastroenterological Association
- Cancer Research Institute
- Gabrielle’s Angel Foundation for Cancer Research
- Pennsylvania Department of Health
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- GM-CSF, pancreatic ductal adenocarcinoma, tumor inflammation, myeloid cells, tumor microenvironment, T cell suppression, CD8+ T cells, tumor immune evasion, tumor-derived cytokines
- MeSH terms
- Adenocarcinoma, Animals, Humans, Immunohistochemistry, Inflammation, Mice, Transgenic, Pancreatic Neoplasms, T-Lymphocytes, Granulocyte-Macrophage Colony-Stimulating Factor, Mice, Knockout, CD8-Positive T-Lymphocytes, Models, Immunological, Receptors, Chemokine, Carcinoma, Pancreatic Ductal, Myeloid Cells, RNA Interference, CD11b Antigen, Cell Line, Tumor, Mice, Tumor Microenvironment
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