Mast Cells: Potential Positive and Negative Roles in Tumor Biology

Cancer Immunology Research - Tập 1 Số 5 - Trang 269-279 - 2013
Thomas Marichal1, Mindy Tsai1, Stephen J. Galli1
1Authors' Affiliations: Departments of 1Pathology and 2Microbiology and Immunology, Stanford University School of Medicine, Stanford, California

Tóm tắt

Abstract

Mast cells are immune cells that reside in virtually all vascularized tissues. Upon activation by diverse mechanisms, mast cells can secrete a broad array of biologically active products that either are stored in the cytoplasmic granules of the cells (e.g., histamine, heparin, various proteases) or are produced de novo upon cell stimulation (e.g., prostaglandins, leukotrienes, cytokines, chemokines, and growth factors). Mast cells are best known for their effector functions during anaphylaxis and acute IgE-associated allergic reactions, but they also have been implicated in a wide variety of processes that maintain health or contribute to disease. There has been particular interest in the possible roles of mast cells in tumor biology. In vitro studies have shown that mast cells have the potential to influence many aspects of tumor biology, including tumor development, tumor-induced angiogenesis, and tissue remodeling, and the shaping of adaptive immune responses to tumors. Yet, the actual contributions of mast cells to tumor biology in vivo remain controversial. Here, we review some basic features of mast cell biology with a special emphasis on those relevant to their potential roles in tumors. We discuss how using in vivo tumor models in combination with models in which mast cell function can be modulated has implicated mast cells in the regulation of host responses to tumors. Finally, we summarize data from studies of human tumors that suggest either beneficial or detrimental roles for mast cells in tumors. Cancer Immunol Res; 1(5); 269–79. ©2013 AACR.

Từ khóa


Tài liệu tham khảo

Ehrlich, 1878, Beiträge zur Theorie und Praxis der Histologischen Färbung [Thesis]

Westphal, 1891, Uber Mastzellen

Galli, 2012, IgE and mast cells in allergic disease, Nat Med, 18, 693, 10.1038/nm.2755

Galli, 2008, Immunomodulatory mast cells: negative, as well as positive, regulators of immunity, Nat Rev Immunol, 8, 478, 10.1038/nri2327

Reber, 2012, New models for analyzing mast cell functions in vivo, Trends Immunol, 33, 613, 10.1016/j.it.2012.09.008

Rodewald, 2012, Widespread immunological functions of mast cells: fact or fiction?, Immunity, 37, 13, 10.1016/j.immuni.2012.07.007

Gurish, 2012, Developmental origin and functional specialization of mast cell subsets, Immunity, 37, 25, 10.1016/j.immuni.2012.07.003

Galli, 2005, Mast cells as “tunable” effector and immunoregulatory cells: recent advances, Annu Rev Immunol, 23, 749, 10.1146/annurev.immunol.21.120601.141025

Kitamura, 1989, Heterogeneity of mast cells and phenotypic change between subpopulations, Annu Rev Immunol, 7, 59, 10.1146/annurev.iy.07.040189.000423

Galli, 2011, Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils, Nature Immunol, 12, 1035, 10.1038/ni.2109

Gilfillan, 2009, The tyrosine kinase network regulating mast cell activation, Immunol Rev, 228, 149, 10.1111/j.1600-065X.2008.00742.x

Detoraki, 2010, Angiogenesis and lymphangiogenesis in bronchial asthma, Allergy, 65, 946, 10.1111/j.1398-9995.2010.02372.x

Metz, 2007, Mast cells in the promotion and limitation of chronic inflammation, Immunol Rev, 217, 304, 10.1111/j.1600-065X.2007.00520.x

Kalesnikoff, 2008, New developments in mast cell biology, Nat Immunol, 9, 1215, 10.1038/ni.f.216

Pittoni, 2011, Tumor-intrinsic and -extrinsic roles of c-Kit: mast cells as the primary off-target of tyrosine kinase inhibitors, Oncogene, 30, 757, 10.1038/onc.2010.494

Valent, 2005, Mastocytosis: pathology, genetics, and current options for therapy, Leuk Lymph, 46, 35, 10.1080/10428190400010775

Rubin, 2007, Gastrointestinal stromal tumour, Lancet, 369, 1731, 10.1016/S0140-6736(07)60780-6

Galli, 1995, Regulation of mouse and human mast cell development, survival and function by stem cell factor, the ligand for the c-kit receptor, Int Arch Allergy Immunol, 107, 51, 10.1159/000236928

Bellone, 2006, KIT/stem cell factor expression in premalignant and malignant lesions of the colon mucosa in relationship to disease progression and outcomes, Int J Oncol, 29, 851

Yang, 2003, Neurofibromin-deficient Schwann cells secrete a potent migratory stimulus for Nf1+/− mast cells, J Clin Invest, 112, 1851, 10.1172/JCI19195

Huang, 2008, SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment, Blood, 112, 1269, 10.1182/blood-2008-03-147033

Zhang, 2000, Modulation of tumor angiogenesis by stem cell factor, Cancer Res, 60, 6757

Craig, 1989, Tryptase and chymase, markers of distinct types of human mast cells, Immunol Res, 8, 130, 10.1007/BF02919075

Samoszuk, 2005, Degranulating mast cells in fibrotic regions of human tumors and evidence that mast cell heparin interferes with the growth of tumor cells through a mechanism involving fibroblasts, BMC Cancer, 5, 121, 10.1186/1471-2407-5-121

Lazar-Molnar, 2002, Inhibition of human primary melanoma cell proliferation by histamine is enhanced by interleukin-6, Eur J Clin Invest, 32, 743, 10.1046/j.1365-2362.2002.01020.x

Sitohy, 2012, Anti-VEGF/VEGFR therapy for cancer: reassessing the target, Cancer Res, 72, 1909, 10.1158/0008-5472.CAN-11-3406

Boesiger, 1998, Mast cells can secrete vascular permeability factor/vascular endothelial cell growth factor and exhibit enhanced release after immunoglobulin E-dependent upregulation of fc ϵ receptor I expression, J Exp Med, 188, 1135, 10.1084/jem.188.6.1135

Grutzkau, 1998, Synthesis, storage, and release of vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) by human mast cells: implications for the biological significance of VEGF206, Mol Biol Cell, 9, 875, 10.1091/mbc.9.4.875

Sawatsubashi, 2000, Association of vascular endothelial growth factor and mast cells with angiogenesis in laryngeal squamous cell carcinoma, Virchows Archiv, 436, 243, 10.1007/s004280050037

Toth-Jakatics, 2000, Cutaneous malignant melanoma: correlation between neovascularization and peritumor accumulation of mast cells overexpressing vascular endothelial growth factor, Hum Pathol, 31, 955, 10.1053/hupa.2000.16658

Aoki, 2003, Mast cells in basal cell carcinoma express VEGF, IL-8 and RANTES, Int Arch Allergy Immunol, 130, 216, 10.1159/000069515

Imada, 2000, Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma, Eur Respir J, 15, 1087, 10.1034/j.1399-3003.2000.01517.x

Baram, 2001, Human mast cells release metalloproteinase-9 on contact with activated T cells: juxtacrine regulation by TNF-α, J Immunol, 167, 4008, 10.4049/jimmunol.167.7.4008

Coussens, 1999, Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis, Genes Dev, 13, 1382, 10.1101/gad.13.11.1382

Huang, 1998, Regulation and function of mast cell proteases in inflammation, J Clin Immunol, 18, 169, 10.1023/A:1020574820797

Blair, 1997, Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor, J Clin Invest, 99, 2691, 10.1172/JCI119458

Schreiber, 2011, Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion, Science, 331, 1565, 10.1126/science.1203486

Galli, 2005, Mast cells in the development of adaptive immune responses, Nat Immunol, 6, 135, 10.1038/ni1158

Lu, 2006, Mast cells are essential intermediaries in regulatory T-cell tolerance, Nature, 442, 997, 10.1038/nature05010

Dalton, 2012, The roles of mast cells in anticancer immunity, Cancer Immunol Immunother, 61, 1511, 10.1007/s00262-012-1246-0

Rao, 2008, Mast cells: multifaceted immune cells with diverse roles in health and disease, Ann N Y Acad Sci, 1143, 83, 10.1196/annals.1443.023

Chervenick, 1969, Decreased neutrophils and megakaryocytes in anemic mice of genotype W/W, J Cell Physiolo, 73, 25, 10.1002/jcp.1040730104

Nigrovic, 2008, Genetic inversion in mast cell-deficient Wsh mice interrupts corin and manifests as hematopoietic and cardiac aberrancy, Am J Pathol, 173, 1693, 10.2353/ajpath.2008.080407

Tsai, 2005, Using mast cell knock-in mice to analyze the roles of mast cells in allergic responses in vivo, Chem Immunol Allergy, 87, 179, 10.1159/000087644

Pittoni, 2011, Mast cell targeting hampers prostate adenocarcinoma development but promotes the occurrence of highly malignant neuroendocrine cancers, Cancer Res, 71, 5987, 10.1158/0008-5472.CAN-11-1637

Gounaris, 2007, Mast cells are an essential hematopoietic component for polyp development, Proc Natl Acad Sci U S A, 104, 19977, 10.1073/pnas.0704620104

Gounaris, 2009, T-regulatory cells shift from a protective anti-inflammatory to a cancer-promoting proinflammatory phenotype in polyposis, Cancer Res, 69, 5490, 10.1158/0008-5472.CAN-09-0304

Blatner, 2010, In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction, Proc Natl Acad Sci U S A, 107, 6430, 10.1073/pnas.0913683107

Colombo, 2009, Polyps wrap mast cells and Treg within tumorigenic tentacles, Cancer Res, 69, 5619, 10.1158/0008-5472.CAN-09-1351

Yang, 2008, Nf1-dependent tumors require a microenvironment containing Nf1+/− - and c-kit-dependent bone marrow, Cell, 135, 437, 10.1016/j.cell.2008.08.041

Yang, 2006, Nf1+/− mast cells induce neurofibroma like phenotypes through secreted TGF-beta signaling, Hum Mol Genet, 15, 2421, 10.1093/hmg/ddl165

Staser, 2010, Mast cells and the neurofibroma microenvironment, Blood, 116, 157, 10.1182/blood-2009-09-242875

Zhu, 2002, Neurofibromas in NF1: Schwann cell origin and role of tumor environment, Science, 296, 920, 10.1126/science.1068452

Dudeck, 2011, Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens, Immunity, 34, 973, 10.1016/j.immuni.2011.03.028

Lilla, 2011, Reduced mast cell and basophil numbers and function in Cpa3-Cre; Mcl-1fl/fl mice, Blood, 118, 6930, 10.1182/blood-2011-03-343962

Feyerabend, 2011, Cre-mediated cell ablation contests mast cell contribution in models of antibody- and T cell-mediated autoimmunity, Immunity, 35, 832, 10.1016/j.immuni.2011.09.015

Otsuka, 2011, Requirement of interaction between mast cells and skin dendritic cells to establish contact hypersensitivity, PLoS ONE, 6, e25538, 10.1371/journal.pone.0025538

Rabenhorst, 2012, Mast cells play a protumorigenic role in primary cutaneous lymphoma, Blood, 120, 2042, 10.1182/blood-2012-03-415638

Ribatti, 2003, Tumor vascularity and tryptase-positive mast cells correlate with a poor prognosis in melanoma, Eur J Clin Invest, 33, 420, 10.1046/j.1365-2362.2003.01152.x

Ribatti, 2003, Neovascularisation, expression of fibroblast growth factor-2, and mast cells with tryptase activity increase simultaneously with pathological progression in human malignant melanoma, Eur J Cancer, 39, 666, 10.1016/S0959-8049(02)00150-8

Beer, 2008, Mast cells have prognostic value in Merkel cell carcinoma, Am J Dermatopathol, 30, 27, 10.1097/DAD.0b013e31815c932a

Esposito, 2004, Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma, J Clin Pathol, 57, 630, 10.1136/jcp.2003.014498

Strouch, 2010, Crosstalk between mast cells and pancreatic cancer cells contributes to pancreatic tumor progression, Clin Cancer Res, 16, 2257, 10.1158/1078-0432.CCR-09-1230

Cai, 2011, Prognostic significance of mast cell count following curative resection for pancreatic ductal adenocarcinoma, Surgery, 149, 576, 10.1016/j.surg.2010.10.009

Elpek, 2001, The prognostic relevance of angiogenesis and mast cells in squamous cell carcinoma of the oesophagus, J Clin Pathol, 54, 940, 10.1136/jcp.54.12.940

Iamaroon, 2003, Increase of mast cells and tumor angiogenesis in oral squamous cell carcinoma, J Oral Pathol Med, 32, 195, 10.1034/j.1600-0714.2003.00128.x

Rojas, 2005, Characterization of mast cell subpopulations in lip cancer, J Oral Pathol Med, 34, 268, 10.1111/j.1600-0714.2004.00297.x

Glimelius, 2005, Angiogenesis and mast cells in Hodgkin lymphoma, Leukemia, 19, 2360, 10.1038/sj.leu.2403992

Molin, 2002, Mast cell infiltration correlates with poor prognosis in Hodgkin's lymphoma, Br J Haematol, 119, 122, 10.1046/j.1365-2141.2002.03768.x

Molica, 2003, Tryptase-positive mast cells predict clinical outcome of patients with early B-cell chronic lymphocytic leukemia, Eur J Haematol, 71, 137, 10.1034/j.1600-0609.2003.00110.x

Ribatti, 2003, Tryptase-positive mast cells correlate positively with bone marrow angiogenesis in B-cell chronic lymphocytic leukemia, Leukemia, 17, 1428, 10.1038/sj.leu.2402970

Ribatti, 2002, Correlation of bone marrow angiogenesis and mast cells with tryptase activity in myelodysplastic syndromes, Leukemia, 16, 1680, 10.1038/sj.leu.2402586

Taskinen, 2008, Prognostic influence of tumor-infiltrating mast cells in patients with follicular lymphoma treated with rituximab and CHOP, Blood, 111, 4664, 10.1182/blood-2007-11-125823

Ribatti, 2000, Angiogenesis and mast cell density with tryptase activity increase simultaneously with pathological progression in B-cell non-Hodgkin's lymphomas, Int J Cancer, 85, 171, 10.1002/(SICI)1097-0215(20000115)85:2%3C171::AID-IJC4%3E3.0.CO;2-W

Ribatti, 1999, Bone marrow angiogenesis and mast cell density increase simultaneously with progression of human multiple myeloma, Br J Cancer, 79, 451, 10.1038/sj.bjc.6690070

Nonomura, 2007, Decreased number of mast cells infiltrating into needle biopsy specimens leads to a better prognosis of prostate cancer, Br J Cancer, 97, 952, 10.1038/sj.bjc.6603962

Fleischmann, 2009, Immunological microenvironment in prostate cancer: high mast cell densities are associated with favorable tumor characteristics and good prognosis, Prostate, 69, 976, 10.1002/pros.20948

Johansson, 2010, Mast cells are novel independent prognostic markers in prostate cancer and represent a target for therapy, Am J Pathol, 177, 1031, 10.2353/ajpath.2010.100070

Fisher, 1989, Prognostic significance of eosinophils and mast cells in rectal cancer: findings from the National Surgical Adjuvant Breast and Bowel Project (protocol R-01), Hum Pathol, 20, 159, 10.1016/0046-8177(89)90180-9

Nielsen, 1999, Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue, J Pathol, 189, 487, 10.1002/(SICI)1096-9896(199912)189:4<487::AID-PATH484>3.0.CO;2-I

Tan, 2005, Prognostic significance of cell infiltrations of immunosurveillance in colorectal cancer, World J Gastroenterol, 11, 1210, 10.3748/wjg.v11.i8.1210

Acikalin, 2005, Tumour angiogenesis and mast cell density in the prognostic assessment of colorectal carcinomas, Dig Liver Dis, 37, 162, 10.1016/j.dld.2004.09.028

Yodavudh, 2008, Prognostic significance of microvessel density and mast cell density for the survival of Thai patients with primary colorectal cancer, J Med Assoc Thai, 91, 723

Gulubova, 2009, Prognostic significance of mast cell number and microvascular density for the survival of patients with primary colorectal cancer, J Gastroenterol Hepatol, 24, 1265, 10.1111/j.1440-1746.2007.05009.x

Tomita, 1999, Correlation between mast cells and survival rates in patients with pulmonary adenocarcinoma, Lung Cancer, 26, 103, 10.1016/S0169-5002(99)00076-8

Takanami, 2000, Mast cell density is associated with angiogenesis and poor prognosis in pulmonary adenocarcinoma, Cancer, 88, 2686, 10.1002/1097-0142(20000615)88:12<2686::AID-CNCR6>3.0.CO;2-6

Welsh, 2005, Macrophage and mast-cell invasion of tumor cell islets confers a marked survival advantage in non-small-cell lung cancer, J Clin Oncol, 23, 8959, 10.1200/JCO.2005.01.4910

Carlini, 2010, Mast cell phenotypes and microvessels in non-small cell lung cancer and its prognostic significance, Hum Pathol, 41, 697, 10.1016/j.humpath.2009.04.029

Aaltomaa, 1993, Mast cells in breast cancer, Anticancer Res, 13, 785

Dabiri, 2004, The presence of stromal mast cells identifies a subset of invasive breast cancers with a favorable prognosis, Mod Pathol, 17, 690, 10.1038/modpathol.3800094

Rajput, 2008, Stromal mast cells in invasive breast cancer are a marker of favourable prognosis: a study of 4,444 cases, Breast Cancer Res Treat, 107, 249, 10.1007/s10549-007-9546-3

della Rovere, 2007, Mast cells in invasive ductal breast cancer: different behavior in high and minimum hormone-receptive cancers, Anticancer Res, 27, 2465

Xiang, 2010, Mast cell tryptase promotes breast cancer migration and invasion, Oncol Rep, 23, 615

Ribatti, 2007, Angiogenesis and mast cells in human breast cancer sentinel lymph nodes with and without micrometastases, Histopathology, 51, 837, 10.1111/j.1365-2559.2007.02869.x

Palmu, 2002, Expression of C-KIT and HER-2 tyrosine kinase receptors in poor-prognosis breast cancer, Anticancer Res, 22, 411

Ali, 2009, Tryptase mast cells in malignant pleural mesothelioma as an independent favorable prognostic factor, J Thorac Oncol, 4, 348, 10.1097/JTO.0b013e3181989ddb

Hedstrom, 2007, Mast cell infiltration is a favourable prognostic factor in diffuse large B-cell lymphoma, Br J Haematol, 138, 68, 10.1111/j.1365-2141.2007.06612.x

Tuna, 2006, Association of mast cells with microvessel density in renal cell carcinomas, Eur Urol, 50, 530, 10.1016/j.eururo.2005.12.040

Dimitriadou, 1997, Mast cell-tumor cell interactions: for or against tumour growth and metastasis?, Anticancer Res, 17, 1541

Theoharides, 2004, Mast cells: the Jekyll and Hyde of tumor growth, Trends Immunol, 25, 235, 10.1016/j.it.2004.02.013

Galinsky, 2008, Mast cells and cancer–no longer just basic science, Crit Rev Oncol Hematol, 68, 115, 10.1016/j.critrevonc.2008.06.001

Mantovani, 2008, Cancer-related inflammation, Nature, 454, 436, 10.1038/nature07205

Mantovani, 2013, Tumor-associated macrophages as a paradigm of macrophage plasticity, diversity, and polarization: lessons and open questions, Arterioscler Thromb Vasc Biol, 33, 1478, 10.1161/ATVBAHA.113.300168

Biswas, 2010, Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm, Nat Immunol, 11, 889, 10.1038/ni.1937

Qian, 2010, Macrophage diversity enhances tumor progression and metastasis, Cell, 141, 39, 10.1016/j.cell.2010.03.014

Starkey, 1988, Mast-cell-deficient W/Wv mice exhibit a decreased rate of tumor angiogenesis, Int J Cancer, 42, 48, 10.1002/ijc.2910420110

Crowle, 1989, Mast cells and tumor-associated angiogenesis, 307

Wedemeyer, 2005, Decreased susceptibility of mast cell-deficient KitW/KitW-v mice to the development of 1, 2-dimethylhydrazine-induced intestinal tumors, Lab Invest, 85, 388, 10.1038/labinvest.3700232

Soucek, 2007, Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors, Nat Med, 13, 1211, 10.1038/nm1649

Sinnamon, 2008, A protective role of mast cells in intestinal tumorigenesis, Carcinogenesis, 29, 880, 10.1093/carcin/bgn040

Wasiuk, 2012, Mast cells impair the development of protective anti-tumor immunity, Cancer Immunol Immunother, 61, 2273, 10.1007/s00262-012-1276-7

Oka, 2012, Evidence questioning cromolyn's effectiveness and selectivity as a ‘mast cell stabilizer’ in mice, Lab Invest, 92, 1472, 10.1038/labinvest.2012.116