Extracellular acidity strengthens mesenchymal stem cells to promote melanoma progression

References

• Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25:2739-49; PMID:17656645; http://dx.doi.org/10.1634/stemcells.2007-0197
   PubMed Web of Science ®Google Scholar
• Kumar S, Chanda D, Ponnazhagan S. Therapeutic potential of genetically modified mesenchymal stem cells. Gene Ther 2008; 15:711-5; PMID:18356815; http://dx.doi.org/10.1038/gt.2008.35
   PubMed Web of Science ®Google Scholar
• Cuiffo BG, Karnoub AE. Mesenchymal stem cells in tumor development: emerging roles and concepts. Cell Adh Migr 2012; 6:220-30; PMID:22863739; http://dx.doi.org/10.4161/cam.20875
   PubMed Web of Science ®Google Scholar
• Goldstein RH, Reagan MR, Anderson K, Kaplan DL, Rosenblatt M. Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis. Cancer Res 2010; 70:10044-50; PMID:21159629; http://dx.doi.org/10.1158/0008-5472.CAN-10-1254
   PubMed Web of Science ®Google Scholar
• Khakoo AY, Pati S, Anderson SA, Reid W, Elshal MF, Rovira II, Nguyen AT, Malide D, Combs CA, Hall G et al Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 2006; 203:1235-47; PMID:16636132; http://dx.doi.org/10.1084/jem.20051921
   PubMed Web of Science ®Google Scholar
• Zhu Y, Sun Z, Han Q, Liao L, Wang J, Bian C, Li J, Yan X, Liu Y, Shao C, Zhao RC. Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia 2009; 23:925-33; PMID: 19148141; http://dx.doi.org/10.1038/leu.2008.384
   PubMed Web of Science ®Google Scholar
• Zhu W, Xu W, Jiang R, Qian H, Chen M, Hu J, Cao W, Han C, Chen Y Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp Mol Pathol 2006; 80:267-74; PMID:16214129; http://dx.doi.org/10.1016/j.yexmp.2005.07.004
   PubMed Web of Science ®Google Scholar
• Barcellos-de-Souza P, Gori V, Bambi F, Chiarugi P. Tumor microenvironment: bone marrow-mesenchymal stem cells as key players. Biochim Biophys Acta 2013; 1836:321-35; PMID:24183942
   PubMed Web of Science ®Google Scholar
• Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449:557-63; PMID:17914389; http://dx.doi.org/10.1038/nature06188
   PubMed Web of Science ®Google Scholar
• Mele V, Muraro MG, Calabrese D, Pfaff D, Amatruda N, Amicarella F, Kvinlaug B, Bocelli-Tyndall C, Martin I, Resink TJ, et al. Mesenchymal stromal cells induce epithelial-to-mesenchymal transition in human colorectal cancer cells through the expression of surface-bound TGF-β. Int J Cancer 2014; 134:2583-94; PMID:24214914; http://dx.doi.org/10.1002/ijc.28598
   PubMed Web of Science ®Google Scholar
• Ye H, Cheng J, Tang Y, Liu Z, Xu C, Liu Y, Sun Y. Human bone marrow-derived mesenchymal stem cells produced TGFbeta contributes to progression and metastasis of prostate cancer. Cancer Invest 2012; 30:513-8; PMID:22646310; http://dx.doi.org/10.3109/07357907.2012.692171
   PubMed Web of Science ®Google Scholar
• Peppicelli S, Bianchini F, Calorini L. Extracellular acidity, a “reappreciated” trait of tumor environment driving malignancy: perspectives in diagnosis and therapy. Cancer Metastasis Rev 2014; 33:823-32; PMID:24984804; http://dx.doi.org/10.1007/s10555-014-9506-4
   PubMed Web of Science ®Google Scholar
• Fais S, Venturi G, Gatenby B. Microenvironmental acidosis in carcinogenesis and metastases: new strategies in prevention and therapy. Cancer Metastasis Rev 2014; 33:1095-108; PMID:25376898; http://dx.doi.org/10.1007/s10555-014-9531-3
   PubMed Web of Science ®Google Scholar
• Gupta SC, Singh R, Pochampally R, Watabe K, Mo YY. Acidosis promotes invasiveness of breast cancer cells through ROS-AKT-NF-κB pathway. Oncotarget 2014; 5:12070-82; PMID:25504433
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324:1029-33; PMID:19460998; http://dx.doi.org/10.1126/science.1160809
   PubMed Web of Science ®Google Scholar
• Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004; 4:891-9; PMID:15516961; http://dx.doi.org/10.1038/nrc1478
   PubMed Web of Science ®Google Scholar
• Pouysségur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006; 441:437-43; PMID:Can't; http://dx.doi.org/10.1038/nature04871
   PubMed Web of Science ®Google Scholar
• Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 2008; 8:705-13; PMID:19143055; http://dx.doi.org/10.1038/nrc2468
   PubMed Web of Science ®Google Scholar
• Reshetnyak YK, Yao L, Zheng S, Kuznetsov S, Engelman DM, Andreev OA. Measuring Tumor Aggressiveness and Targeting Metastatic Lesions with Fluorescent pHLIP. Molecular Imaging and Biology: MIB: the Official Publication of the Academy of Molecular Imaging 2011; 13:1146-56; http://dx.doi.org/10.1007/s11307-010-0457-z
   PubMed Web of Science ®Google Scholar
• Wike-Hooley JL, Haveman J, Reinhold HS. The relevance of tumour pH to the treatment of malignant disease. Radiother Oncol 1984; 2:343-66; PMID:6097949; http://dx.doi.org/10.1016/S0167-8140(84)80077-8
   PubMed Web of Science ®Google Scholar
• Laurenzana A, Biagioni A, Bianchini F, Peppicelli S, Chillà A, Margheri F, Luciani C, Pimpinelli N, Del Rosso M, Calorini L, et al. Inhibition of uPAR-TGFβ crosstalk blocks MSC-dependent EMT in melanoma cells. J Mol Med (Berl) 2015; 93(7):783-94; PMID:25694039; http://dx.doi.org/10.1007/s00109-015-1266-2
   PubMed Web of Science ®Google Scholar
• Peppicelli S, Bianchini F, Contena C, Tombaccini D, Calorini L. Acidic pH via NF-κB favours VEGF-C expression in human melanoma cells. Clin Exp Metastasis 2013; 30:957-67; PMID:23784694; http://dx.doi.org/10.1007/s10585-013-9595-4
   PubMed Web of Science ®Google Scholar
• Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989; 49:6449-65; PMID:2684393
   PubMed Web of Science ®Google Scholar
• Song G, Ouyang G, Bao S. The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med. 2005 Jan-Mar; 9(1):59-71
   Google Scholar
• Krengel S, Grotelüschen F, Bartsch S, Tronnier M. Cadherin expression pattern in melanocytic tumors more likely depends on the melanocyte environment than on tumor cell progression. J Cutan Pathol 2004; 31:1-7; PMID:14675278; http://dx.doi.org/10.1046/j.0303-6987.2004.0106.x
   PubMed Web of Science ®Google Scholar
• Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000; 148:779-90; PMID:10684258; http://dx.doi.org/10.1083/jcb.148.4.779
   PubMed Web of Science ®Google Scholar
• Alonso SR, Tracey L, Ortiz P, Pérez-Gómez B, Palacios J, Pollán M, Linares J, Serrano S, Sáez-Castillo AI, Sánchez L, et al. A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res 2007; 67:3450-60; PMID:17409456; http://dx.doi.org/10.1158/0008-5472.CAN-06-3481
   PubMed Web of Science ®Google Scholar
• Peppicelli S, Bianchini F, Torre E, Calorini L. Contribution of acidic melanoma cells undergoing epithelial-to-mesenchymal transition to aggressiveness of non-acidic melanoma cells. Clin Exp Metastasis 2014; 31:423-33; PMID:24469963
   PubMed Web of Science ®Google Scholar
• Amiri KI, Richmond A. Role of nuclear factor-kappa B in melanoma. Cancer Metastasis Rev 2005; 24:301-13; PMID:15986139; http://dx.doi.org/10.1007/s10555-005-1579-7
   PubMed Web of Science ®Google Scholar
• Wu Y, Deng J, Rychahou PG, Qiu S, Evers BM, Zhou BP. Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion. Cancer Cell 2009; 15:416-28; PMID:19411070; http://dx.doi.org/10.1016/j.ccr.2009.03.016
   PubMed Web of Science ®Google Scholar
• Poser I, Domínguez D, de Herreros AG, Varnai A, Buettner R, Bosserhoff AK. Loss of E-cadherin expression in melanoma cells involves up-regulation of the transcriptional repressor Snail. J Biol Chem 2001; 276:24661-6; PMID:11323412; http://dx.doi.org/10.1074/jbc.M011224200
   PubMed Web of Science ®Google Scholar
• Freudlsperger C, Bian Y, Contag Wise S, Burnett J, Coupar J, Yang X, Chen Z, Van Waes C. TGF-β and NF-κB signal pathway cross-talk is mediated through TAK1 and SMAD7 in a subset of head and neck cancers. Oncogene 2013; 32:1549-59; PMID:22641218; http://dx.doi.org/10.1038/onc.2012.171
   PubMed Web of Science ®Google Scholar
• Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, Moretti M, De Smaele E, Beg AA, Tergaonkar V, et al. NF-κB controls Energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 2011; 13:1272-9; PMID:21968997; http://dx.doi.org/10.1038/ncb2324
   PubMed Web of Science ®Google Scholar
• Kato Y, Lambert CA, Colige AC, Mineur P, Noël A, Frankenne F, Foidart JM, Baba M, Hata R, Miyazaki K, et al. Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J Biol Chem 2005; 280:10938-44; PMID:15657063; http://dx.doi.org/10.1074/jbc.M411313200
   PubMed Web of Science ®Google Scholar
• Han G, Lu SL, Li AG, He W, Corless CL, Kulesz-Martin M, Wang XJ. Distinct mechanisms of TGF-beta1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. J Clin Invest 2005; 115:1714-23; PMID:15937546; http://dx.doi.org/10.1172/JCI24399
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011; 10:767-77; PMID:21921921; http://dx.doi.org/10.1038/nrd3554
   PubMed Web of Science ®Google Scholar
• Ohkouchi S, Block GJ, Katsha AM, Kanehira M, Ebina M, Kikuchi T, Saijo Y, Nukiwa T, Prockop DJ. Mesenchymal stromal cells protect cancer cells from ROS-induced apoptosis and enhance the Warburg effect by secreting STC1. Mol Ther 2012; 20:417-23; PMID:22146344; http://dx.doi.org/10.1038/mt.2011.259
   PubMed Web of Science ®Google Scholar
• Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008; 118:3930-42; PMID:19033663
   PubMed Web of Science ®Google Scholar
• Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 2009; 8:3984-4001; PMID:19923890; http://dx.doi.org/10.4161/cc.8.23.10238
   PubMed Web of Science ®Google Scholar
• Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, De Donatis A, Lanciotti M, Serni S, Cirri P, Chiarugi P. Reciprocal metabolic reprogramming through lactate shuttle coordinately influences tumor-stroma interplay. Cancer Res 2012; 72: 5130-40; PMID:22850421; http://dx.doi.org/10.1158/0008-5472.CAN-12-1949
   PubMed Web of Science ®Google Scholar
• Bonuccelli G, Avnet S, Grisendi G, Salerno M, Granchi D, Dominici M, Kusuzaki K, Baldini N. Role of mesenchymal stem cells in osteosarcoma and metabolic reprogramming of tumor cells. Oncotarget 2014; 5:7575-88; PMID:25277190
   PubMed Web of Science ®Google Scholar
• Cerezo M, Tichet M, Abbe P, Ohanna M, Lehraiki A, Rouaud F, Allegra M, Giacchero D, Bahadoran P, Bertolotto C, et al. Metformin blocks melanoma invasion and metastasis development in AMPK/p53-dependent manner. Mol Cancer Ther 2013; 12:1605-15; PMID:23741061; http://dx.doi.org/10.1158/1535-7163.MCT-12-1226-T
   PubMed Web of Science ®Google Scholar
• Rattan R, Ali Fehmi R, Munkarah A. Metformin: an emerging new therapeutic option for targeting cancer stem cells and metastasis. J Oncol 2012; 2012:928127; PMID:22701483; http://dx.doi.org/10.1155/2012/928127
   PubMedGoogle Scholar
• Blandino G, Valerio M, Cioce M, Mori F, Casadei L, Pulito C, Sacconi A, Biagioni F, Cortese G, Galanti S, et al. Metformin elicits anticancer effects through the sequential modulation of DICER and c-MYC. Nat Commun 2012; 3:865; PMID:22643892; http://dx.doi.org/10.1038/ncomms1859
   PubMed Web of Science ®Google Scholar
• Del Barco S, Vazquez-Martin A, Cufí S, Oliveras-Ferraros C, Bosch-Barrera J, Joven J, Martin-Castillo B, Menendez JA. Metformin: multi-faceted protection against cancer. Oncotarget 2011; 2:896-917; PMID:22203527
   PubMed Web of Science ®Google Scholar
• Borthwick LA, Gardner A, De Soyza A, Mann DA, Fisher AJ. Transforming Growth Factor-β1 (TGF-β1) Driven Epithelial to Mesenchymal Transition (EMT) is Accentuated by Tumour Necrosis Factor α (TNFα) via Crosstalk Between the SMAD and NF-κB Pathways. Cancer Microenviron 2012; 5:45-57; PMID:21792635; http://dx.doi.org/10.1007/s12307-011-0080-9
   PubMedGoogle Scholar
• Graham RM, Thompson JW, Webster KA. Inhibition of the vacuolar ATPase induces Bnip3-dependent death of cancer cells and a reduction in tumor burden and metastasis. Oncotarget 2014; 5:1162-73; PMID:24811485
   PubMed Web of Science ®Google Scholar
• Chen TR. In situ detection of mycoplasma contamination in cell cultures by fluorescent Hoechst 33258 stain. Exp Cell Res 1977; 104:255-62; PMID:65285; http://dx.doi.org/10.1016/0014-4827(77)90089-1
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression datausing real-time quantitativePCR andthe2; -Delta Delta C(T) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar