Abstract
Calcium is a key regulator of many physiological processes that are perturbed in cancer, such as migration, proliferation and apoptosis. The proteins STIM and Orai mediate store-operated calcium entry (SOCE), the main pathway for calcium entry in non-excitable cells. Changes in the expression and function of STIM and Orai have been found in a range of cancer types and thus implicated in disease progression. Here we discuss the role of STIM, Orai and the SOCE pathway in the progression of melanoma and explore how the heterogeneous nature of melanoma may explain the lack of consensus in the field regarding the role of SOCE in the progression of this disease.
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Anastas, J.N., Kulikauskas, R.M., Tamir, T., Rizos, H., Long, G.V., von Euw, E.M., Yang, P.T., Chen, H.W., Haydu, L., Toroni, R.A., Lucero, O.M., Chien, A.J., and Moon, R.T. (2014). Wnt5a enhances resistance of melanoma cells to targeted braf inhibitors. J Clin Invest 124, 2877–2890.
Berridge, M.J., and Irvine, R.F. (1984). Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315–321.
Berridge, M.J., Lipp, P., and Bootman, M.D. (2000). The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1, 11–21.
Carafoli, E. (1991). Calcium pump of the plasma membrane. Physiol Rev 71, 129–153
Dissanayake, S.K., and Weeraratna, A.T. (2008). Detecting PKC phosphorylation as part of the wnt/calcium pathway in cutaneous melanoma. Methods Mol Biol, 468, 157–172.
Feldman, B., Fedida-Metula, S., Nita, J., Sekler, I., and Fishman, D. (2010). Coupling of mitochondria to store-operated Ca2+-signaling sustains constitutive activation of protein kinase B/Akt and augments survival of malignant melanoma cells. Cell Calcium 47, 525–537.
Flourakis, M., Lehen’kyi, V., Beck, B., Raphaël, M., Vandenberghe, M., Abeele, F.V., Roudbaraki, M., Lepage, G., Mauroy, B., Romanin, C., Shuba, Y., Skryma, R., and Prevarskaya, N. (2010). Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis 1, e75.
Goodsell, D.S. (2001). The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 6, 298–299.
Hooper, R., Zhang, X., Webster, M., Go, C., Kedra, J., Marchbank, K., Gill, D.L., Weeraratna, A.T., Trebak. M., and Soboloff, J. (2015). Novel protein kinase C-mediated control of Orai1 function in invasive melanoma. Mol Cell Biol 35, 2790–2798.
Hou, M.F., Kuo, H.C., Li, J.H., Wang, Y.S., Chang, C.C., Chen, K.C., Chen, W.C., Chiu, C.C., Yang, S., and Chang, W.C. (2011). Orai1/CRACM1 overexpression suppresses cell proliferation via attenuation of the store-operated calcium influx-mediated signalling pathway in a549 lung cancer cells. Biochim Biophys Acta, 1810, 1278–1284.
Kawasaki, T., Ueyama, T., Lange, I., Feske, S., and Saito, N. (2010). Protein kinase C-induced phosphorylation of orai1 regulates the intracellular Ca2+ level via the store-operated Ca2+ channel. J Biol Chem 285, 25720–25730.
Liotta, L.A., and Stetler-Stevenson, W.G. (1991). Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res 51, 5054s–5059s.
Miller, A.J., Du, J., Rowan, S., Hershey, C.L., Widlund, H.R., and Fisher, D.E. (2004). Transcriptional regulation of the melanoma prognostic marker melastatin (TRPM1) by MITF in melanocytes and melanoma. Cancer Res 64, 509–516.
Motiani, R.K., Hyzinski-Garcia, M.C., Zhang, X., Henkel, M.M., Abdullaev, I.F., Kuo, Y.H., Matrougui, K., Mongin, A.A., and Trebak, M. (2013). STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch 465, 1249–1260.
Pan, Z., and Ma, J.J. (2015). Open Sesame: treasure in store-operated calcium entry pathway. Sci China Life Sci 58, 48–53.
Raposo, G., and Marks, M.S. (2007). Melanosomes—dark organelles enlighten endosomal membrane transport. Nat Rev Mol Cell Biol 8, 786–797.
Schadendorf, D., Fisher, D.E., Garbe, C., Gershenwald, J.E., Grob, J.J., Halpern, A., Herlyn, M., Marchetti, M.A., McArthur, G., Ribas, A., Roesch, A., and Hauschild, A. (2015). Melanoma. Nat Rev Dis Primers, 1, 1–20.
Schafer, C., Rymarczyk, G., Ding, L., Kirber, M.T., and Bolotina, V.M. (2012). Role of molecular determinants of store-operated Ca2+ entry (Orai1, phospholipase A2 group 6, and STIM1) in focal adhesion formation and cell migration. J Biol Chem, 287, 40745–40757.
Stanisz, H., Saul, S., Muller, C.S., Kappl, R., Niemeyer, B.A., Vogt, T., Hoth, M., Roesch, A., and Bogeski, I. (2014). Inverse regulation of melanoma growth and migration by Orai1/STIM2-dependent calcium entry. Pigment Cell Melanoma Res 27, 442–453.
Sun, J., Lu, F., He, H., Messina, J., Mathew, R., Wang, D., Sarnaik, A.A., Chang, W.C., Kim, M., Cheng, H., and Yang, S. (2014). STIM1-and Orai1-mediated Ca2+ oscillation orchestrates invadopodium formation and melanoma invasion. J Cell Biol 207, 535–548.
Tsai, F.C., Seki, A., Yang, H.W., Hayer, A., Carrasco, S., Malmersjö, S., and Meyer, T. (2014). A polarized Ca2+, diacylglycerol and stim1 signalling system regulates directed cell migration. Nat Cell Biol, 16, 133–144.
Soboloff, J., Rothberg, B.S., Madesh, M.,and Gill, D.L. (2012). Stim proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13, 549–565.
Vashisht, A., Trebak, M., and Motiani, R.K. (2015). STIM and Orai proteins as novel targets for cancer therapy. A review in the theme: cell and molecular processes in cancer metastasis. Am J Physiol Cell Physiol 309, C457–C469.
Umemura, M., Baljinnyam, E., Feske, S., de Lorenzo, M.S., Xie, L.H., Feng, X., Oda, K., Makino, A., Fujita, T., Yokoyama, U., Iwatsubo, M., Chen, S., Goydos, J.S., Ishikawa, Y., and Iwatsubo, K. (2014). Store-operated Ca2+ entry (SOCE) regulates melanoma proliferation and cell migration. PloS One 9, e89292.
Venkatachalam, K., and Montell, C. (2007). Trp channels. Annu Rev Biochem, 76, 387–417.
Wang, J.Y., Sun, J., Huang, M.Y., Wang, Y.S., Hou, M.F., Sun, Y., He, H., Krishna, N., Chiu, S.J., Lin, S., Yang, S., and Chang, W.C. (2015). STIM1 overexpression promotes colorectal cancer progression, cell motility and COX-2 expression. Oncogene, 34, 4358–4367
Webster, M.R., and Weeraratna, A.T. (2013). A wnt-er migration: the confusing role of beta-catenin in melanoma metastasis. Sci Signal, 6, pe11.
Xu, H., Martinoia, E., and Szabo, I. (2015). Organellar channels and transporters. Cell Calcium 58, 1–10.
Xu, J.M., Zhou, Y., Gao, L., Zhou, S.X., Liu, W.H., and Li, X.A. (2016). Stromal interaction molecule 1 plays an important role in gastric cancer progression. Oncol Rep 35, 3496–3504.
Yamamura, H., Ugawa, S., Ueda, T., Morita, A., and Shimada, S. (2008). TRPM8 activation suppresses cellular viability in human melanoma. Am J Physiol Cell Physiol 295, C296–C301.
Yang, S., Zhang, J.J., and Huang, X.Y. (2009). Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15, 124–134.
Zhu, N., Qin, L., Luo, Z., Guo, Q., Yang, L., and Liao, D. (2014). Challenging role of Wnt5a and its signaling pathway in cancer metastasis (review). Exp Ther Med 8, 3–8.
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Hooper, R., Zaidi, M.R. & Soboloff, J. The heterogeneity of store-operated calcium entry in melanoma. Sci. China Life Sci. 59, 764–769 (2016). https://doi.org/10.1007/s11427-016-5087-5
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DOI: https://doi.org/10.1007/s11427-016-5087-5