Human mast cells promote colon cancer growth via bidirectional crosstalk: studies in 2D and 3D coculture models

References

• Moriarity A, O’Sullivan J, Kennedy J, Mehigan B, McCormick P. Current targeted therapies in the treatment of advanced colorectal cancer: a review. Ther Adv Med Oncol. 2016;8:276–293. doi: 10.1177/1758834016646734.
   PubMed Web of Science ®Google Scholar
• Passardi A, Canale M, Valgiusti M, Ulivi P. Immune checkpoints as a target for colorectal cancer treatment. Int J Mol Sci. 2017;18(6).
   Web of Science ®Google Scholar
• Boland PM, Ma WW. Immunotherapy for Colorectal Cancer. Cancers (Basel). 2017;9(5).
   Google Scholar
• Zhao B, Wang L, Qiu H, Zhang M, Sun L, Peng P, Yu Q, Yuan X. Mechanisms of resistance to anti-EGFR therapy in colorectal cancer. Oncotarget. 2017;8:3980–4000. doi: 10.18632/oncotarget.14012.
   PubMedGoogle Scholar
• Janakiram NB, Rao CV. The role of inflammation in colon cancer. Adv Exp Med Biol. 2014;816:25–52. doi: 10.1007/978-3-0348-0837-8_2.
   PubMed Web of Science ®Google Scholar
• Coussens LM, Zitvogel L, Palucka AK. Neutralizing tumor-promoting chronic inflammation: a magic bullet? Science (New York, NY). 2013;339:286–291. doi: 10.1126/science.1232227.
   Google Scholar
• Varricchi G, Galdiero MR, Loffredo S, Marone G, Iannone R, Marone G, Granata F. Are mast cells masters in cancer? Front Immunol. 2017;8:424. doi: 10.3389/fimmu.2017.00424.
   PubMed Web of Science ®Google Scholar
• Kalesnikoff J, Galli SJ. New developments in mast cell biology. Nat Immunol. 2008;9:1215–1223. doi: 10.1038/ni.f.216.
   PubMed Web of Science ®Google Scholar
• Theoharides TC, Conti P. Mast cells: the Jekyll and Hyde of tumor growth. Trends Immunol. 2004;25:235–241. doi: 10.1016/j.it.2004.02.013.
   PubMed Web of Science ®Google Scholar
• Acikalin MF, Oner U, Topcu I, Yasar B, Kiper H, Colak E. Tumour angiogenesis and mast cell density in the prognostic assessment of colorectal carcinomas. Digestive and Liver Disease: Official Journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver. 2005;37:162–169. doi: 10.1016/j.dld.2004.09.028.
   PubMedGoogle Scholar
• Ammendola M, Sacco R, Sammarco G, Donato G, Montemurro S, Ruggieri E, Patruno R, Marech I, Cariello M, Vacca A, et al. Correlation between serum tryptase, mast cells positive to tryptase and microvascular density in colo-rectal cancer patients: possible biological-clinical significance. PloS One. 2014;9:e99512. doi: 10.1371/journal.pone.0099512.
   PubMed Web of Science ®Google Scholar
• Gulubova M, Vlaykova T. Prognostic significance of mast cell number and microvascular density for the survival of patients with primary colorectal cancer. J Gastroenterol Hepatol. 2009;24:1265–1275. doi: 10.1111/j.1440-1746.2007.05009.x.
   PubMed Web of Science ®Google Scholar
• Malfettone A, Silvestris N, Saponaro C, Ranieri G, Russo A, Caruso S, Popescu O, Simone G, Paradiso A, Mangia A. High density of tryptase-positive mast cells in human colorectal cancer: a poor prognostic factor related to protease-activated receptor 2 expression. J Cell Mol Med. 2013;17:1025–1037. doi: 10.1111/jcmm.12073.
   PubMed Web of Science ®Google Scholar
• Nielsen HJ, Hansen U, Christensen IJ, Reimert CM, Brünner N, Moesgaard F. Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue. J Pathol. 1999;189:487–495. doi: 10.1002/(SICI)1096-9896(199912)189:4<487::AID-PATH484>3.0.CO;2-I.
   PubMed Web of Science ®Google Scholar
• Suzuki S, Ichikawa Y, Nakagawa K, Kumamoto T, Mori R, Matsuyama R, Takeda K, Ota M, Tanaka K, Tamura T, et al. High infiltration of mast cells positive to tryptase predicts worse outcome following resection of colorectal liver metastases. BMC Cancer. 2015;15:840. doi: 10.1186/s12885-015-1584-3.
   PubMed Web of Science ®Google Scholar
• Tan SY, Fan Y, Luo HS, Shen ZX, Guo Y, Zhao LJ. Prognostic significance of cell infiltrations of immunosurveillance in colorectal cancer. World Journal of Gastroenterology. 2005;11:1210–1214.
   PubMed Web of Science ®Google Scholar
• Wang S, Li L, Shi R, Liu X, Zhang J, Zou Z, Hao Z, Tao A. Mast cell targeted chimeric toxin can be developed as an adjunctive therapy in colon cancer treatment. Toxins (Basel). 2016;8(3).
   Google Scholar
• Huang B, Lei Z, Zhang G-M, Li D, Song C, Li B, Liu Y, Yuan Y, Unkeless J, Xiong H, et al. SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood. 2008;112:1269–1279. doi: 10.1182/blood-2008-03-147033.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Dobashi K. CC-chemokine CCL15 expression and possible implications for the pathogenesis of IgE-related severe asthma. Mediators Inflamm. 2012;2012:475253. doi: 10.1155/2012/475253.
   PubMed Web of Science ®Google Scholar
• Feder-Mengus C, Ghosh S, Reschner A, Martin I, Spagnoli GC. New dimensions in tumor immunology: what does 3D culture reveal? Trends Mol Med. 2008;14:333–340. doi: 10.1016/j.molmed.2008.06.001.
   PubMed Web of Science ®Google Scholar
• Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol. 2010;148:3–15. doi: 10.1016/j.jbiotec.2010.01.012.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674. doi: 10.1016/j.cell.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Reviews Immunol. 2010;10:826–837. doi: 10.1038/nri2873.
   PubMed Web of Science ®Google Scholar
• Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science (New York, NY). 2010;327:291–295. doi: 10.1126/science.1183021.
   Google Scholar
• Tang M, Diao J, Gu H, Khatri I, Zhao J, Cattral MS. Toll-like receptor 2 activation promotes tumor dendritic cell dysfunction by regulating IL-6 and IL-10 Receptor Signaling. Cell Rep. 2015;13:2851–2864. doi: 10.1016/j.celrep.2015.11.053.
   PubMed Web of Science ®Google Scholar
• Schaefer L. Complexity of danger: the diverse nature of damage-associated molecular patterns. J Biol Chem. 2014;289:35237–35245. doi: 10.1074/jbc.R114.619304.
   PubMed Web of Science ®Google Scholar
• Oldford SA, Haidl ID, Howatt MA, Leiva CA, Johnston B, Marshall JS. A critical role for mast cells and mast cell-derived IL-6 in TLR2-mediated inhibition of tumor growth. Journal of Immunology (Baltimore, Md. 1950;2010(185):7067–7076.
   Google Scholar
• Gounaris E, Erdman SE, Restaino C, Gurish MF, Friend DS, Gounari F, Lee DM, Zhang G, Glickman JN, Shin K, et al. Mast cells are an essential hematopoietic component for polyp development. Proc Natl Acad Sci U S A. 2007;104:19977–19982. doi: 10.1073/pnas.0704620104.
   PubMed Web of Science ®Google Scholar
• Wedemeyer J, Galli SJ. Decreased susceptibility of mast cell-deficient Kit(W)/Kit(W-v) mice to the development of 1, 2-dimethylhydrazine-induced intestinal tumors. Lab Invest. 2005;85:388–396. doi: 10.1038/labinvest.3700232.
   PubMed Web of Science ®Google Scholar
• Strouch MJ, Cheon EC, Salabat MR, Krantz SB, Gounaris E, Melstrom LG, Dangi-Garimella S, Wang E, Munshi HG, Khazaie K, et al. Crosstalk between mast cells and pancreatic cancer cells contributes to pancreatic tumor progression. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research. 2010;16:2257–2265. doi: 10.1158/1078-0432.CCR-09-1230.
   PubMed Web of Science ®Google Scholar
• Attarha S, Roy A, Westermark B, Tchougounova E. Mast cells modulate proliferation, migration and stemness of glioma cells through downregulation of GSK3beta expression and inhibition of STAT3 activation. Cell Signal. 2017;37:81–92. doi: 10.1016/j.cellsig.2017.06.004.
   PubMed Web of Science ®Google Scholar
• Roy A, Libard S, Weishaupt H, Gustavsson I, Uhrbom L, Hesselager G, Swartling FJ, Pontén F, Alafuzoff I, Tchougounova E. Mast cell infiltration in human brain metastases modulates the microenvironment and contributes to the metastatic potential. Front Oncol. 2017;7:115. doi: 10.3389/fonc.2017.00115.
   PubMed Web of Science ®Google Scholar
• Rudolph MI, Boza Y, Yefi R, Luza S, Andrews E, Penissi A, Garrido P, Rojas IG. The influence of mast cell mediators on migration of SW756 cervical carcinoma cells. J Pharmacol Sci. 2008;106:208–218.
   PubMed Web of Science ®Google Scholar
• Melillo RM, Guarino V, Avilla E, Galdiero MR, Liotti F, Prevete N, Rossi FW, Basolo F, Ugolini C, De Paulis A, et al. Mast cells have a protumorigenic role in human thyroid cancer. Oncogene. 2010;29:6203–6215. doi: 10.1038/onc.2010.348.
   PubMedGoogle Scholar
• Khan MW, Keshavarzian A, Gounaris E, Melson JE, Cheon EC, Blatner NR, Chen ZE, Tsai F-N, Lee G, Ryu H, et al. PI3K/AKT signaling is essential for communication between tissue-infiltrating mast cells, macrophages, and epithelial cells in colitis-induced cancer. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research. 2013;19:2342–2354. doi: 10.1158/1078-0432.CCR-12-2623.
   PubMed Web of Science ®Google Scholar
• Guhl S, Babina M, Neou A, Zuberbier T, Artuc M. Mast cell lines HMC-1 and LAD2 in comparison with mature human skin mast cells–drastically reduced levels of tryptase and chymase in mast cell lines. Exp Dermatol. 2010;19:845–847. doi: 10.1111/j.1600-0625.2010.01103.x.
   PubMed Web of Science ®Google Scholar
• Schmetzer O, Valentin P, Smorodchenko A, Domenis R, Gri G, Siebenhaar F, Metz M, Maurer M. A novel method to generate and culture human mast cells: peripheral CD34+ stem cell-derived mast cells (PSCMCs). J Immunol Methods. 2014;413:62–68. doi: 10.1016/j.jim.2014.07.003.
   PubMed Web of Science ®Google Scholar
• Yu Y, Blokhuis BR, Garssen J, Redegeld FA. Non-IgE mediated mast cell activation. Eur J Pharmacol. 2016;778:33–43. doi: 10.1016/j.ejphar.2015.07.017.
   PubMed Web of Science ®Google Scholar
• Inamoto S, Itatani Y, Yamamoto T, Minamiguchi S, Hirai H, Iwamoto M, Hasegawa S, Taketo MM, Sakai Y, Kawada K. Loss of SMAD4 promotes colorectal cancer progression by accumulation of myeloid-derived suppressor cells through the ccl15-ccr1 chemokine axis. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research. 2016;22:492–501. doi: 10.1158/1078-0432.CCR-15-0726.
   PubMed Web of Science ®Google Scholar
• Itatani Y, Kawada K, Fujishita T, Kakizaki F, Hirai H, Matsumoto T, Iwamoto M, Inamoto S, Hatano E, Hasegawa S, et al. Loss of SMAD4 from colorectal cancer cells promotes CCL15 expression to recruit CCR1+ myeloid cells and facilitate liver metastasis. Gastroenterology. 2013;145:1064–75.e11. doi: 10.1053/j.gastro.2013.07.033.
   PubMed Web of Science ®Google Scholar
• Melstrom LG, Bentrem DJ, Salabat MR, Kennedy TJ, Ding XZ, Strouch M, et al. Overexpression of 5-lipoxygenase in colon polyps and cancer and the effect of 5-LOX inhibitors in vitro and in a murine model. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research. 2008;14:6525–6530. doi:10.1158/1078-0432.CCR-07-4631.
   PubMed Web of Science ®Google Scholar
• Sainz B Jr., Martin B, Tatari M, Heeschen C, Guerra S. ISG15 is a critical microenvironmental factor for pancreatic cancer stem cells. Cancer Res. 2014;74:7309–7320. doi: 10.1158/0008-5472.CAN-14-1354.
   PubMed Web of Science ®Google Scholar
• Lin Q, Lim HS, Lin HL, Tan HT, Lim TK, Cheong WK, Cheah PY, Tang CL, Chow PKH, Chung MCM. Analysis of colorectal cancer glyco-secretome identifies laminin beta-1 (LAMB1) as a potential serological biomarker for colorectal cancer. Proteomics. 2015;15:3905–3920. doi: 10.1002/pmic.201500236.
   PubMed Web of Science ®Google Scholar
• Li TT, Ogino S, Qian ZR. Toll-like receptor signaling in colorectal cancer: carcinogenesis to cancer therapy. World Journal of Gastroenterology. 2014;20:17699–17708. doi: 10.3748/wjg.v20.i47.17699.
   PubMed Web of Science ®Google Scholar
• Lu CC, Kuo HC, Wang FS, Jou MH, Lee KC, Chuang JH. Upregulation of TLRs and IL-6 as a marker in human colorectal cancer. Int J Mol Sci. 2014;16:159–177. doi: 10.3390/ijms16010159.
   PubMed Web of Science ®Google Scholar
• Varadaradjalou S, Féger F, Thieblemont N, Hamouda NB, Pleau J-M, Dy M, Arock M. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human mast cells. Eur J Immunol. 2003;33:899–906. doi: 10.1002/eji.200323830.
   PubMed Web of Science ®Google Scholar
• Che XH, Chen CL, Ye XL, Weng GB, Guo XZ, Yu WY, Tao J, Chen Y-C, Chen X. Dual inhibition of COX-2/5-LOX blocks colon cancer proliferation, migration and invasion in vitro. Oncol Rep. 2016;35:1680–1688. doi: 10.3892/or.2015.4506.
   PubMed Web of Science ®Google Scholar
• Jensen SA, Vainer B, Bartels A, Brunner N, Sorensen JB. Expression of matrix metalloproteinase 9 (MMP-9) and tissue inhibitor of metalloproteinases 1 (TIMP-1) by colorectal cancer cells and adjacent stroma cells–associations with histopathology and patients outcome. European Journal Cancer (Oxford, England. 1990;2010(46):3233–3242.
   Google Scholar
• Song G, Xu S, Zhang H, Wang Y, Xiao C, Jiang T, Wu L, Zhang T, Sun X, Zhong L, et al. TIMP1 is a prognostic marker for the progression and metastasis of colon cancer through FAK-PI3K/AKT and MAPK pathway. J Exp Clin Cancer Res. 2016;35:148. doi: 10.1186/s13046-016-0427-7.
   PubMed Web of Science ®Google Scholar
• Groblewska M, Mroczko B, Gryko M, Pryczynicz A, Guzinska-Ustymowicz K, Kedra B, Kemona A, Szmitkowski M. Serum levels and tissue expression of matrix metalloproteinase 2 (MMP-2) and tissue inhibitor of metalloproteinases 2 (TIMP-2) in colorectal cancer patients. Tumour Biology: Journal Int Soc Oncodevelopmental Biol Med. 2014;35:3793–3802. doi: 10.1007/s13277-013-1502-8.
   PubMed Web of Science ®Google Scholar
• Boonstra MC, Verbeek FP, Mazar AP, Prevoo HA, Kuppen PJ, Van De Velde CJ, Vahrmeijer AL, Sier CF. Expression of uPAR in tumor-associated stromal cells is associated with colorectal cancer patient prognosis: a TMA study. BMC Cancer. 2014;14:269. doi: 10.1186/1471-2407-14-269.
   PubMed Web of Science ®Google Scholar
• Gordon-Weeks AN, Lim SY, Yuzhalin AE, Jones K, Muschel R. Macrophage migration inhibitory factor: a key cytokine and therapeutic target in colon cancer. Cytokine Growth Factor Rev. 2015;26:451–461. doi: 10.1016/j.cytogfr.2015.03.002.
   PubMed Web of Science ®Google Scholar
• Rossi FW, Prevete N, Rivellese F, Napolitano F, Montuori N, Postiglione L, Selleri C, De Paulis A. The Urokinase/Urokinase receptor system in mast cells: effects of its functional interaction with fMLF Receptors. Translational Medicine @ UniSa. 2016;15:34–41.
   PubMed Web of Science ®Google Scholar
• Qiao L, Wong BCY. Role of Notch signaling in colorectal cancer. Carcinogenesis. 2009;30:1979–1986. doi: 10.1093/carcin/bgp236.
   PubMed Web of Science ®Google Scholar
• D’Souza B, Meloty-Kapella L, Weinmaster G. Canonical and non-canonical notch ligands. Curr Top Dev Biol. 2010;92:73–129.
   Google Scholar
• Ribatti D, Crivellato E. Mast cells, angiogenesis, and tumour growth. Biochim Biophys Acta. 2012;1822(1):2–8.
   Google Scholar
• Ribatti D, Vacca A, Fau Nico B, Nico B, Fau Crivellato E, Crivellato E, Fau Roncali L, Roncali L, Dammacco F. The role of mast cells in tumour angiogenesis. Br J Haematol 2001;115:514–521.
   Google Scholar
• Detoraki A, Staiano RI, Granata F, Giannattasio G, Prevete N, de Paulis A, Ribatti D, Genovese A, Triggiani M, Marone G. Vascular endothelial growth factors synthesized by human lung mast cells exert angiogenic effects. J Allergy Clin Immunol. 2009;123:1142–9, 1149.e1-5.
   Web of Science ®Google Scholar
• Abdel-Majid RM, Marshall JS. Prostaglandin E2 induces degranulation-independent production of vascular endothelial growth factor by human mast cells. Journal of Immunology (Baltimore, Md. 1950;2004(172):1227–1236.
   Google Scholar
• Nakanishi M, Rosenberg DW. Multifaceted roles of PGE(2) in inflammation and cancer(). Semin Immunopathol. 2013;35:123–137. doi: 10.1007/s00281-012-0342-8.
   PubMed Web of Science ®Google Scholar
• Feng C, Beller EM, Bagga S, Boyce JA. Human mast cells express multiple EP receptors for prostaglandin E(2) that differentially modulate activation responses. Blood. 2006;107:3243–3250. doi: 10.1182/blood-2005-07-2772.
   PubMed Web of Science ®Google Scholar
• Torres-Atencio I, Ainsua-Enrich E, De Mora F, Picado C, Martin M. Prostaglandin E2 prevents hyperosmolar-induced human mast cell activation through prostanoid receptors EP2 and EP4. PloS One. 2014;9:e110870. doi: 10.1371/journal.pone.0110870.
   PubMed Web of Science ®Google Scholar
• Timmins NE, Nielsen LK. Generation of multicellular tumor spheroids by the hanging-drop method. Methods Mol Med. 2007;140:141–151.
   PubMedGoogle Scholar
• Berens EB, Holy JM, Riegel AT, Wellstein A. A cancer cell spheroid assay to assess Invasion in a 3D Setting. Journal of Visualized Experiments: JoVE. 2015. doi: 10.3791/53409.
   Web of Science ®Google Scholar