Calcium in tumour metastasis: New roles for known actors

Nature Reviews Cancer

Volumn 11, Issue 8, 2011, Pages 609-618

  Prevarskaya, Natalia ^a,b   Skryma, Roman ^a,b   Shuba, Yaroslav ^c  

^a Université des Sciences et Technologies de Lille   (France)

^b UNIV LILLE   (France)

^c BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CALVASCULIN; G PROTEIN COUPLED RECEPTOR; STROMAL INTERACTION MOLECULE 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

BREAST CANCER; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANCER CELL; CANCER CELL CULTURE; CANCER MORTALITY; CANCER PATIENT; CARCINOGENESIS; CELL FUNCTION; CELL INVASION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CYTOSOL; ENDOPLASMIC RETICULUM; FIBROSARCOMA; GLIOBLASTOMA; HEPATOBLASTOMA; HUMAN; MELANOMA; MELANOMA CELL; METASTASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN METABOLISM; REVIEW;

CALCIUM; CELL MOVEMENT; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS;

EID: 79960759956     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3105     Document Type: Review

References (81)

1. Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57-70 (2000). (Pubitemid 30046295)
2. Brooks, S. A., Lomax-Browne, H. J., Carter, T. M., Kinch, C. E. & Hall, D. M. Molecular interactions in cancer cell metastasis. Acta Histochem.112, 3-25 (2010).
3. Pomorski, P. Calcium regulation of cell migration. Postepy Biochem.55,163-170 (2009) (in Polish).
4. Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev. Mol. Cell Biol. 4, 517-529 (2003). (Pubitemid 36773404)
5. 2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521-555 (2000). (Pubitemid 32037516)
6. Collingridge, G. L., Olsen, R. W., Peters, J. & Spedding, M. A nomenclature for ligand-gated ion channels. Neuropharmacology 56, 2-5 (2009).
7. Montell, C. & Rubin, G. M. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2, 1313-1323 (1989).
8. Venkatachalam, K. & Montell, C. TRP channels. Annu. Rev. Biochem. 76, 387-417 (2007).
9. Hewavitharana, T., Deng, X., Soboloff, J. & Gill, D. L. Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 42,173-182 (2007). (Pubitemid 47029604)
10. Hogan, P. G., Lewis, R. S. & Rao, A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533 (2010).
11. 2+ entry channel. J. Biol. Chem. 275, 9114-9119 (2000). (Pubitemid 30185125)
12. Shuttleworth, T. J. Arachidonic acid, ARC channels, and Orai proteins. Cell Calcium 45, 602-610 (2009).
13. Feng, M. et al. Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 143, 84-98 (2010).
14. Berridge, M. J., Lipp, P. & Bootman, M. D. The versatility and universality of calcium signalling. Nature Rev. Mol. Cell Biol. 1, 11-21 (2000).
15. Protasi, F. Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front. Biosci. 7, d650-d658 (2002).
16. 2+ mobilizing second messenger-cyclic ADP-ribose. J. Cell. Mol. Med. 10, 407-422 (2006). (Pubitemid 44870188)
17. Taylor, C. W. & Thorn, P. Calcium signalling: IP3 rises again.and again. Curr. Biol. 11, R352-R355 (2001). (Pubitemid 32418153)
18. Calcraft, P. J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600 (2009).
19. 2+ signaling in interleukin-8-treated lymphokine-activated killer cells. J. Biol. Chem. 285, 21877-21887 (2010).
20. Nabeshima, K., Inoue, T., Shimao, Y. & Sameshima, T. Matrix metalloproteinases in tumor invasion: role for cell migration. Pathol. Int. 52, 255-264 (2002). (Pubitemid 34587810)
21. Yoon, S. O., Park, S. J., Yun, C. H. & Chung, A. S. Roles of matrix metalloproteinases in tumor metastasis and angiogenesis. J. Biochem. Mol. Biol. 36, 128-137 (2003).
22. Brundage, R. A., Fogarty, K. E., Tuft, R. A. & Fay, F. S. Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 254, 703-706 (1991). (Pubitemid 21917391)
23. Hahn, K., DeBiasio, R. & Taylor, D. L. Patterns of elevated free calcium and calmodulin activation in living cells. Nature 359, 736-738 (1992).
24. Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 302, 1704-1709 (2003). (Pubitemid 37505725)
25. Pettit, E. J. & Fay, F. S. Cytosolic free calcium and the cytoskeleton in the control of leukocyte chemotaxis. Physiol. Rev. 78, 949-967 (1998). (Pubitemid 28491946)
26. 2+ channels controls the trailing tail contraction in growth factor-induced fibroblast cell migration. J. Biol. Chem. 280, 27130-27137 (2005). (Pubitemid 41040751)
27. Agle, K. A., Vongsa, R. A. & Dwinell, M. B. Calcium mobilization triggered by the chemokine CXCL12 regulates migration in wounded intestinal epithelial monolayers. J. Biol. Chem. 285, 16066-16075 (2010).
28. Li, S. & Hua, Z. C. FAK expression regulation and therapeutic potential. Adv. Cancer Res. 101, 45-61 (2008).
29. Kim, M. H., Lee, Y. J., Kim, M. O., Kim, J. S. & Han, H. J. Effect of leukotriene D4 on mouse embryonic stem cell migration and proliferation: involvement of PI3K/Akt as well as GSK-3β/β-catenin signaling pathways. J. Cell. Biochem. 111, 686-698 (2010).
30. 2+/calmodulin-dependent kinase II. J. Biol. Chem. 280, 24212-24220 (2005). (Pubitemid 40884911)
31. Easley, C. A., Brown, C. M., Horwitz, A. F. & Tombes, R. M. CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin. Cell Motil. Cytoskeleton. 65, 662-674 (2008).
32. Giannone, G. et al. Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J. Biol. Chem. 279, 28715-28723 (2004). (Pubitemid 38900156)
33. Chan, K. T., Bennin, D. A. & Huttenlocher, A. Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). J. Biol. Chem. 285, 11418-11426 (2010).
34. 2+-and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377, 75-79 (1995).
35. 2+-induced regulation of ion channel and MAP kinase functions. Nature 376, 737-745 (1995).
36. Boye, K. & Maelandsmo, G. M. S100A4 and metastasis: a small actor playing many roles. Am. J. Pathol. 176, 528-535 (2010).
37. Tarabykina, S. et al. Metastasis-associated protein S100A4: spotlight on its role in cell migration. Curr. Cancer Drug Targets 7, 217-228 (2007). (Pubitemid 46699073)
38. Kim, E. J. & Helfman, D. M. Characterization of the metastasis-associated protein, S100A4. Roles of calcium binding and dimerization in cellular localization and interaction with myosin. J. Biol. Chem. 278, 30063-3073 (2003).
39. Schneider, M., Hansen, J. L. & Sheikh, S. P. S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J. Mol. Med. 86, 507-522 (2008).
40. Saleem, M. et al. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc. Natl Acad. Sci. USA 103, 14825-14830 (2006). (Pubitemid 44527813)
41. Mueller, A., Bδchi, T., Hφchli, M., Schδfer, B. W. & Heizmann, C. W. Subcellular distribution of S100 proteins in tumor cells and their relocation in response to calcium activation. Histochem. Cell Biol. 111, 453-459 (1999). (Pubitemid 29302025)
42. Lee, J., Ishihara, A., Oxford, G., Johnson, B. & Jacobson, K. Regulation of cell movement is mediated by stretch-activated calcium channels. Nature 400, 382-386 (1999). (Pubitemid 29344206)
43. 2+-dependent regulation of cell adhesiveness. J. Cell Sci. 118, 369-379 (2005). (Pubitemid 40277349)
44. Hamill, O. P. Twenty odd years of stretch-sensitive channels. Pflugers Arch. 453, 333-351 (2006). (Pubitemid 44764235)
45. Wei, C. et al. Calcium flickers steer cell migration. Nature 457, 901-905 (2009).
46. Wei, C. et al. Flickering calcium microdomains signal turning of migrating cells. Can. J. Physiol. Pharmacol. 88, 105-110 (2010).
47. Su, L. T. et al. TRPM7 regulates cell adhesion by controlling the calcium-dependent protease calpain. J. Biol. Chem. 281, 11260-11270 (2006).
48. Le, Q. T., Denko, N. C. & Giaccia, A. J. Hypoxic gene expression and metastasis. Cancer Metastasis Rev. 23, 293-310 (2004). (Pubitemid 38881813)
49. 2+ influx. Cell Calcium. 47, 425-432 (2010).
50. Waning, J. et al. A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium 42, 17-25 (2007). (Pubitemid 46760451)
51. Monet, M. et al. Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim. Biophys. Acta 1793, 528-539 (2009).
52. Monet, M. et al. Role of cationic channel TRPV2 in promoting prostate cancer migration and progression to androgen resistance. Cancer Res. 70, 1225-1235 (2010).
53. Wondergem, R., Ecay, T. W., Mahieu, F., Owsianik, G. & Nilius, B. HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem. Biophys. Res. Commun. 372, 210-215 (2008).
54. 2+, BK channel activity and cell migration. J. Biomed. Sci. 16, 90 (2009).
55. Duncan, L. M. et al. Down-regulation of the novel gene melastatin correlates with potential for melanoma metastasis. Cancer Res. 58, 1515-1520 (1998). (Pubitemid 28193617)
56. Devi, S. et al. Calcium homeostasis in human melanocytes: role of transient receptor potential melastatin 1 (TRPM1) and its regulation by ultraviolet light. Am. J. Physiol. Cell Physiol. 297, C679-C687 (2009).
57. Yang, Z. H., Wang, X. H., Wang, H. P. & Hu, L. Q. Effects of TRPM8 on the proliferation and motility of prostate cancer PC-3 cells. Asian J. Androl. 11, 157-165 (2009).
58. Yang, S., Zhang, J. J. & Huang, X. Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 15, 124-134 (2009).
59. McAndrew, D. et al. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol. Cancer Ther. 10, 448-460 (2011)).
60. Bisaillon, J. M. et al. Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am. J. Physiol. Cell Physiol. 298, C993-C1005 (2010).
61. Flourakis, M. et al. Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis. 1, e75 (2010).
62. Prevarskaya, N., Skryma, R. & Shuba, Y. Ion channels and the hallmarks of cancer. Trends Mol. Med. 16, 107-121 (2010).
63. Martini, A., Bruno, R., Mazzulla, S., Nocita, A. & Martino, G. Angiotensin II regulates endothelial cell migration through calcium influx via T-type calcium channel in human umbilical vein endothelial cells. Acta Physiol. 198, 449-455 (2010).
64. Huang, J. B., Kindzelskii, A. L., Clark, A. J. & Petty, H. R. Identification of channels promoting calcium spikes and waves in HT1080 tumor cells: their apparent roles in cell motility and invasion. Cancer Res. 64, 2482-2489 (2004). (Pubitemid 38523903)
65. Kang, S. S. et al. Caffeine-mediated inhibition of calcium release channel inositol 1,4,5-trisphosphate receptor subtype 3 blocks glioblastoma invasion and extends survival. Cancer Res. 70, 1173-1183 (2010).
66. 2+ channel in rat cerebellum is inhibited by caffeine. Biochem. J. 282, 309-312 (1992).
67. 2+-dependent mechanism. Cancer Res. 70, 5607-5617 (2010).
68. Peng, H. H., Hodgson, L., Henderson, A. J. & Dong, C. Involvement of phospholipase C signaling in melanoma cell-induced endothelial junction disassembly. Front. Biosci. 10, 1597-1606 (2005). (Pubitemid 40529023)
69. Denmeade, S. R. & Isaacs, J. T. The SERCA pump as a therapeutic target: making a "smart bomb" for prostate cancer. Cancer Biol. Ther. 4, 14-22 (2005). (Pubitemid 41350924)
70. Jurkat-Rott, K. & Lehmann-Horn, F. The impact of splice isoforms on voltage-gated calcium channel α1 subunits. J. Physiol. 554, 609-619 (2004). (Pubitemid 38219878)
71. Vαzquez, E. & Valverde, M. A. A review of TRP channels splicing. Semin. Cell Dev. Biol. 17, 607-617 (2006). (Pubitemid 46138164)
72. Latour, I. et al. Expression of T-type calcium channel splice variants in human glioma. Glia 48, 112-119 (2004). (Pubitemid 39545943)
73. Liu, X., Chang, Y., Reinhart, P. H., Sontheimer, H. & Chang, Y. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J. Neurosci. 22, 1840-1849 (2002). (Pubitemid 35386302)
74. Onkal, R. & Djamgoz, M. B. Molecular pharmacology of voltage-gated sodium channel expression in metastatic disease: clinical potential of neonatal Nav1.5 in breast cancer. Eur. J. Pharmacol. 625, 206-219 (2009).
75. 2+-selective cation channel TRPV6 in human prostate cancer: a novel prognostic marker for tumor progression. Oncogene. 22, 7858-7861 (2003). (Pubitemid 37485545)
76. 2+ channel expression. Biochem. Biophys. Res. Commun. 322, 1359-1363 (2004). (Pubitemid 39164665)
77. Bidaux, G. et al. Evidence for specific TRPM8 expression in human prostate secretory epithelial cells: functional androgen receptor requirement. Endocr. Relat. Cancer 12, 367-382 (2005). (Pubitemid 40903086)
78. Bidaux, G. et al. Prostate cell differentiation status determines transient receptor potential melastatin member 8 channel subcellular localization and function. J. Clin. Invest. 117, 1647-1657 (2007). (Pubitemid 46871349)
79. Horimoto, M. et al. A novel strategy for cancer therapy by mutated mammalian degenerin gene transfer. Cancer Gene Ther. 7, 1341-1347 (2000).
80. Waldmann, R., Champigny, G., Voilley, N., Lauritzen, I. & Lazdunski, M. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. J. Biol. Chem. 271,10433-10436 (1996). (Pubitemid 26145774)
81. Mitra, S. K., Hanson, D. A. & Schlaepfer, D. D. Focal adhesion kinase: in command and control of cell motility. Nature Rev. Mol. Cell Biol. 6, 56-68 (2005). (Pubitemid 40064899)