The Role of Mast Cells in Molding the Tumor Microenvironment

Overview

Journal Cancer Microenviron

Publisher Springer

Specialty Oncology

Date 2014 Sep 8

PMID 25194694

Citations 38

Authors

A Rigoni

M P Colombo

C Pucillo

Affiliations

Soon will be listed here.

Abstract

Mast cells (MCs) are granulocytic immune cells that reside in tissues exposed to the external environment. MCs are best known for their activity in allergic reactions, but they have been involved in different physiological and pathological conditions. In particular, MC infiltration has been shown in several types of human tumors and in animal cancer models. Nevertheless, the role of MCs in the tumor microenvironment is still debated because they have been associated either to good or poor prognosis depending on tumor type and tissue localization. This dichotomous role relies on MC capacity to secrete a broad spectrum of molecules with modulatory functions, which may condition the final tumor outcome also promoting angiogenesis and tissue remodeling. In this review, we analyze the multifaceted role of mast cell in tumor progression and inhibition considering their ability to interact with: i) immune cells, ii) tumor cells and iii) the extracellular matrix. Eventually, the current MC targeting strategies to treat cancer patients are discussed. Deciphering the actual role of MCs in tumor onset and progression is crucial to identify MC-targeted treatments aimed at killing cancer cells or at making the tumor vulnerable to selected anti-cancer drugs.

Citing Articles

Single-cell transcriptomics reveals stage- and side-specificity of gene modules in colorectal cancer.

Rahiminejad S, Mukund K, Maurya M, Subramaniam S Res Sq. 2024; .

PMID: 38826219 PMC: 11142301. DOI: 10.21203/rs.3.rs-4402565/v1.

Diagnostic and prognostic significance of mast cell markers in HIV/AIDS: Current insights and future directions.

Obeagu E Medicine (Baltimore). 2024; 103(20):e38117.

PMID: 38758896 PMC: 11098248. DOI: 10.1097/MD.0000000000038117.

Cellular interactions in tumor microenvironment during breast cancer progression: new frontiers and implications for novel therapeutics.

Akinsipe T, Mohamedelhassan R, Akinpelu A, Pondugula S, Mistriotis P, Avila L Front Immunol. 2024; 15:1302587.

PMID: 38533507 PMC: 10963559. DOI: 10.3389/fimmu.2024.1302587.

Mast Cell: A Mysterious Character in Skin Cancer.

Alda S, Ceausu R, Gaje P, Raica M, Cosoroaba R In Vivo. 2023; 38(1):58-68.

PMID: 38148067 PMC: 10756458. DOI: 10.21873/invivo.13410.

The regulatory network of the chemokine CCL5 in colorectal cancer.

Zhang X, Zhang X, Wang Y, Fang Y, Li M, Liu X Ann Med. 2023; 55(1):2205168.

PMID: 37141250 PMC: 10161960. DOI: 10.1080/07853890.2023.2205168.

References

Souza H, Elia C, Spencer J, MacDonald T . Expression of lymphocyte-endothelial receptor-ligand pairs, alpha4beta7/MAdCAM-1 and OX40/OX40 ligand in the colon and jejunum of patients with inflammatory bowel disease. Gut. 1999; 45(6):856-63. PMC: 1727744. DOI: 10.1136/gut.45.6.856. View

Monteleone I, Pallone F, Monteleone G . Aryl hydrocarbon receptor and colitis. Semin Immunopathol. 2013; 35(6):671-5. DOI: 10.1007/s00281-013-0396-2. View

Metz M, Grimbaldeston M, Nakae S, Piliponsky A, Tsai M, Galli S . Mast cells in the promotion and limitation of chronic inflammation. Immunol Rev. 2007; 217:304-28. DOI: 10.1111/j.1600-065X.2007.00520.x. View

Theoharides T, Conti P . Mast cells: the Jekyll and Hyde of tumor growth. Trends Immunol. 2004; 25(5):235-41. DOI: 10.1016/j.it.2004.02.013. View

Schmidt D, Kao W . The interrelated role of fibronectin and interleukin-1 in biomaterial-modulated macrophage function. Biomaterials. 2006; 28(3):371-82. DOI: 10.1016/j.biomaterials.2006.08.041. View

Ammendola M, Sacco R, Donato G, Zuccala V, Russo E, Luposella M . Mast cell positivity to tryptase correlates with metastatic lymph nodes in gastrointestinal cancer patients treated surgically. Oncology. 2013; 85(2):111-6. DOI: 10.1159/000351145. View

Heijmans J, Buller N, Muncan V, van den Brink G . Role of mast cells in colorectal cancer development, the jury is still out. Biochim Biophys Acta. 2010; 1822(1):9-13. DOI: 10.1016/j.bbadis.2010.12.001. View

Abdel-Majid R, Marshall J . Prostaglandin E2 induces degranulation-independent production of vascular endothelial growth factor by human mast cells. J Immunol. 2004; 172(2):1227-36. DOI: 10.4049/jimmunol.172.2.1227. View

Morgan R, McAllister B, Cross L, Green D, Kornfeld H, Center D . Histamine 4 receptor activation induces recruitment of FoxP3+ T cells and inhibits allergic asthma in a murine model. J Immunol. 2007; 178(12):8081-9. DOI: 10.4049/jimmunol.178.12.8081. View

10.

Pittoni P, Tripodo C, Piconese S, Mauri G, Parenza M, Rigoni A . Mast cell targeting hampers prostate adenocarcinoma development but promotes the occurrence of highly malignant neuroendocrine cancers. Cancer Res. 2011; 71(18):5987-97. DOI: 10.1158/0008-5472.CAN-11-1637. View

11.

Grimbaldeston M, Chen C, Piliponsky A, Tsai M, Tam S, Galli S . Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol. 2005; 167(3):835-48. PMC: 1698741. DOI: 10.1016/S0002-9440(10)62055-X. View

12.

Gu Y, Hogenesch J, Bradfield C . The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol. 2000; 40:519-61. DOI: 10.1146/annurev.pharmtox.40.1.519. View

13.

Pittoni P, Piconese S, Tripodo C, Colombo M . Tumor-intrinsic and -extrinsic roles of c-Kit: mast cells as the primary off-target of tyrosine kinase inhibitors. Oncogene. 2010; 30(7):757-69. DOI: 10.1038/onc.2010.494. View

14.

Pierotti M, Tamborini E, Negri T, Pricl S, Pilotti S . Targeted therapy in GIST: in silico modeling for prediction of resistance. Nat Rev Clin Oncol. 2011; 8(3):161-70. DOI: 10.1038/nrclinonc.2011.3. View

15.

Fakhrjou A, Niroumand-Oscoei S, Somi M, Ghojazadeh M, Naghashi S, Samankan S . Prognostic value of tumor-infiltrating mast cells in outcome of patients with esophagus squamous cell carcinoma. J Gastrointest Cancer. 2013; 45(1):48-53. DOI: 10.1007/s12029-013-9550-2. View

16.

Frossi B, Gri G, Tripodo C, Pucillo C . Exploring a regulatory role for mast cells: 'MCregs'?. Trends Immunol. 2010; 31(3):97-102. DOI: 10.1016/j.it.2009.12.007. View

17.

Elenkov I, Webster E, Papanicolaou D, Fleisher T, Chrousos G, Wilder R . Histamine potently suppresses human IL-12 and stimulates IL-10 production via H2 receptors. J Immunol. 1998; 161(5):2586-93. View

18.

Piconese S, Gri G, Tripodo C, Musio S, Gorzanelli A, Frossi B . Mast cells counteract regulatory T-cell suppression through interleukin-6 and OX40/OX40L axis toward Th17-cell differentiation. Blood. 2009; 114(13):2639-48. DOI: 10.1182/blood-2009-05-220004. View

19.

Tripodo C, Gri G, Piccaluga P, Frossi B, Guarnotta C, Piconese S . Mast cells and Th17 cells contribute to the lymphoma-associated pro-inflammatory microenvironment of angioimmunoblastic T-cell lymphoma. Am J Pathol. 2010; 177(2):792-802. PMC: 2913370. DOI: 10.2353/ajpath.2010.091286. View

20.

Moennikes O, Loeppen S, Buchmann A, Andersson P, Ittrich C, Poellinger L . A constitutively active dioxin/aryl hydrocarbon receptor promotes hepatocarcinogenesis in mice. Cancer Res. 2004; 64(14):4707-10. DOI: 10.1158/0008-5472.CAN-03-0875. View