Emerging role of TRP channels in cell migration: From tumor vascularization to metastasis

Frontiers in Physiology

Volumn 4 NOV, Issue , 2013, Pages

  Pla, Alessandra Fiorio ^a,b   Gkika, Dimitra ^b  

^a UNIVERSITY OF TURIN   (Italy)

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

Author keywords

Cancer cells; Cell migration; Orai Stim1; TRP channels; Tumor angiogenesis

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; SMALL INTERFERING RNA; STROMAL INTERACTION MOLECULE 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL M1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2; VANILLOID RECEPTOR 4;

ANTINEOPLASTIC ACTIVITY; BLADDER CANCER; CALCIUM CELL LEVEL; CANCER GROWTH; CANCER INHIBITION; CELL MIGRATION; ENDOTHELIUM CELL; EPITHELIUM CELL; GENE SILENCING; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; LUNG ADENOCARCINOMA; METASTASIS; NASOPHARYNX CANCER; NONHUMAN; PANCREAS ADENOCARCINOMA; PROSTATE TUMOR; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR INVASION; TUMOR VASCULARIZATION; UTERINE CERVIX CANCER;

EID: 84889672076     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00311     Document Type: Review

References (117)

1. Abdullaev, I. F., Bisaillon, J. M., Potier, M., Gonzalez, J. C., Motiani, R. K., and Trebak, M. (2008). Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ. Res. 103, 1289-1299. doi: 10.1161/01.RES.0000338496.95579.56
2. Ambudkar, I. S., and Ong, H. L. (2007). Organization and function of TRPC channelosomes. Pflugers Arch. 455, 187-200. doi: 10.1007/s00424-007-0252-0
3. Antigny, F., Girardin, N., and Frieden, M. (2012). Transient receptor potential canonical channels are required for in vitro endothelial tube formation. J. Biol. Chem. 287, 5917-5927. doi: 10.1074/jbc.M111.295733
4. Aydar, E., Yeo, S., Djamgoz, M., and Palmer, C. (2009). Abnormal expression, localization and interaction of canonical transient receptor potential ion channels in human breast cancer cell lines and tissues: a potential target for breast cancer diagnosis and therapy. Cancer Cell Int. 9, 23. doi: 10.1186/1475-2867-9-23
5. Baldoli, E., Castiglioni, S., and Maier, J. A. M. (2013). Regulation and function of TRPM7 in human endothelial cells: TRPM7 as a potential novel regulator of endothelial function. PLoS ONE 8:e59891. doi: 10.1371/journal.pone.0059891
6. Baldoli, E., and Maier, J. A. M. (2012). Silencing TRPM7 mimics the effects of magnesium deficiency in human microvascular endothelial cells. Angiogenesis 15, 47-57. doi: 10.1007/s10456-011-9242-0
7. Bates-Withers, C., Sah, R., and Clapham, D. E. (2011). TRPM7, the Mg(2+) inhibited channel and kinase. Adv. Exp. Med. Biol. 704, 173-183. doi: 10.1007/978-94-007-0265-3_9
8. Beech, D. J. (2012). Orai1 calcium channels in the vasculature. Pflugers Arch. 463, 635-647. doi: 10.1007/s00424-012-1090-2
9. Bernaldo de Quirós, S., Merlo, A., Secades, P., Zambrano, I., de Santa María, I. S., Ugidos, N., et al. (2013). Identification of TRPC6 as a possible candidate target gene within an amplicon at 11q21-q22.2 for migratory capacity in head and neck squamous cell carcinomas. BMC Cancer 13:116. doi: 10.1186/1471-2407-13-116
10. Blázquez, C., González-Feria, L., Alvarez, L., Haro, A., Casanova, M. L., and Guzmán, M. (2004). Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res. 64, 5617-5623. doi: 10.1158/0008-5472.CAN-03-3927
11. Bödding, M. (2007). TRP proteins and cancer. Cell. Signal. 19, 617-624. doi: 10.1016/j.cellsig.2006.08.012
12. Bomben, V. C., and Sontheimer, H. W. (2008). Inhibition of transient receptor potential canonical channels impairs cytokinesis in human malignant gliomas. Cell Prolif. 41, 98-121. doi: 10.1111/j.1365-2184.2007.00504.x
13. Bomben, V. C., Turner, K. L., Barclay, T.-T. C., and Sontheimer, H. (2011). Transient receptor potential canonical channels are essential for chemotactic migration of human malignant gliomas. J. Cell. Physiol. 226, 1879-1888. doi: 10.1002/jcp.22518
14. Bussolati, B., Grange, C., and Camussi, G. (2011). Tumor exploits alternative strategies to achieve vascularization. FASEB J. 25, 2874-2882. doi: 10.1096/fj.10-180323
15. Cahalan, M. D., Zhang, S. L., Yeromin, A. V., Ohlsen, K., Roos, J., and Stauderman, K. A. (2007). Molecular basis of the CRAC channel. Cell Calcium 42, 133-144. doi: 10.1016/j.ceca.2007.03.002
16. Caprodossi, S., Amantini, C., Nabissi, M., Morelli, M. B., Farfariello, V., Santoni, M., et al. (2011). Capsaicin promotes a more aggressive gene expression phenotype and invasiveness in null-TRPV1 urothelial cancer cells. Carcinogenesis 32, 686-694. doi: 10.1093/carcin/bgr025
17. Caprodossi, S., Lucciarini, R., Amantini, C., Nabissi, M., Canesin, G., Ballarini, P., et al. (2008). Transient receptor potential vanilloid type 2 (TRPV2) expression in normal urothelium and in urothelial carcinoma of human bladder: correlation with the pathologic stage. Eur. Urol. 54, 612-620. doi: 10.1016/j.eururo.2007.10.016
18. Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936. doi: 10.1038/nature04478
19. Chantôme, A., Potier-Cartereau, M., Clarysse, L., Fromont, G., Marionneau-Lambot, S., Guéguinou, M., et al. (2013). Pivotal role of the lipid raft SK3-Orai1 complex in human cancer cell migration and bone metastases. Cancer Res. 73, 4852-4861. doi: 10.1158/0008-5472.CAN-12-4572
20. Chaudhuri, P., Colles, S. M., Bhat, M., Van Wagoner, D. R., Birnbaumer, L., and Graham, L. M. (2008). Elucidation of a TRPC6-TRPC5 channel cascade that restricts endothelial cell movement. Mol. Biol. Cell 19, 3203-3211. doi: 10.1091/mbc.E07-08-0765
21. Cheng, H.-W., James, A. F., Foster, R. R., Hancox, J. C., and Bates, D. O. (2006). VEGF activates receptor-operated cation channels in human microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 1768-1776. doi: 10.1161/01.ATV.0000231518.86795.0f
22. Cheng, J., Gu, Y.-J., Wang, Y., Cheng, S. H., and Wong, W.-T. (2011). Nanotherapeutics in angiogenesis: synthesis and in vivo assessment of drug efficacy and biocompatibility in zebrafish embryos. Int. J. Nanomed. 6, 2007-2021. doi: 10.2147/IJN.S20145
23. Cheng, K. T., Ong, H. L., Liu, X., and Ambudkar, I. S. (2013). Contribution and regulation of TRPC channels in store-operated Ca(2+) entry. Curr. Top. Membr. 71, 149-179. doi: 10.1016/B978-0-12-407870-3.00007-X
24. Chen, J.-P., Luan, Y., You, C.-X., Chen, X.-H., Luo, R.-C., and Li, R. (2010). TRPM7 regulates the migration of human nasopharyngeal carcinoma cell by mediating Ca(2+) influx. Cell Calcium 47, 425-432. doi: 10.1016/j.ceca.2010.03.003
25. Chen, Y.-F., Chiu, W.-T., Chen, Y.-T., Lin, P.-Y., Huang, H.-J., Chou, C.-Y., et al. (2011). Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 15225-15230. doi: 10.1073/pnas.1103315108
26. Chigurupati, S., Venkataraman, R., Barrera, D., Naganathan, A., Madan, M., Paul, L., et al. (2010). Receptor channel TRPC6 is a key mediator of notch-driven glioblastoma growth and invasiveness. Cancer Res. 70, 418-427. doi: 10.1158/0008-5472.CAN-09-2654
27. Clark, K., Langeslag, M., van Leeuwen, B., Ran, L., Ryazanov, A. G., Figdor, C. G., et al. (2006). TRPM7, a novel regulator of actomyosin contractility and cell adhesion. EMBO J. 25, 290-301. doi: 10.1038/sj.emboj.7600931
28. Clark, K., Middelbeek, J., and van Leeuwen, F. N. (2008). Interplay between TRP channels and the cytoskeleton in health and disease. Eur. J. Cell Biol. 87, 631-640. doi: 10.1016/j.ejcb.2008.01.009
29. Cuddapah, V. A., Turner, K. L., and Sontheimer, H. (2013). Calcium entry via TRPC1 channels activates chloride currents in human glioma cells. Cell Calcium 53, 187-194. doi: 10.1016/j.ceca.2012.11.013
30. Denmeade, S. R., and Isaacs, J. T. (2005). The SERCA pump as a therapeutic target: making a "smart bomb" for prostate cancer. Cancer Biol. Ther. 4, 14-22. doi: 10.4161/cbt.4.1.1505
31. De Petrocellis, L., Ligresti, A., Moriello, A. S., Allarà, M., Bisogno, T., Petrosino, S., et al. (2011). Effects of cannabinoids and cannabinoid-enriched cannabis extracts on TRP channels and endocannabinoid metabolic enzymes. Br. J. Pharmacol. 163, 1479-1494. doi: 10.1111/j.1476-5381.2010.01166.x
32. 2++ concentration. Stem Cells 29, 1898-1907. doi: 10.1002/stem.734
33. Duncan, L. M., Deeds, J., Hunter, J., Shao, J., Holmgren, L. M., Woolf, E. A., et al. (1998). Down-regulation of the novel gene melastatin correlates with potential for melanoma metastasis. Cancer Res. 58, 1515-1520.
34. El Boustany, C., Bidaux, G., Enfissi, A., Delcourt, P., Prevarskaya, N., and Capiod, T. (2008). Capacitative calcium entry and transient receptor potential canonical 6 expression control human hepatoma cell proliferation. Hepatology 47, 2068-2077. doi: 10.1002/hep.22263
35. Everaerts, W., Nilius, B., and Owsianik, G. (2010). The vanilloid transient receptor potential channel TRPV4: from structure to disease. Prog. Biophys. Mol. Biol. 103, 2-17. doi: 10.1016/j.pbiomolbio.2009.10.002
36. Fabian, A., Fortmann, T., Dieterich, P., Riethmüller, C., Schön, P., Mally, S., et al. (2008). TRPC1 channels regulate directionality of migrating cells. Pflugers Arch. 457, 475-484. doi: 10.1007/s00424-008-0515-4
37. Fang, D., and Setaluri, V. (2000). Expression and Up-regulation of alternatively spliced transcripts of melastatin, a melanoma metastasis-related gene, in human melanoma cells. Biochem. Biophys. Res. Commun. 279, 53-61. doi: 10.1006/bbrc.2000.3894
38. Fiorio Pla, A., Avanzato, D., Munaron, L., and Ambudkar, I. S. (2012a). Ion channels and transporters in cancer. 6. Vascularizing the tumor: TRP channels as molecular targets. Am. J. Physiol. Cell Physiol. 302, C9-C15. doi: 10.1152/ajpcell.00280.2011
39. Fiorio Pla, A., Ong, H. L., Cheng, K. T., Brossa, A., Bussolati, B., Lockwich, T., et al. (2012b). TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acid-activated actin remodeling. Oncogene 31, 200-212. doi: 10.1038/onc.2011.231
40. Gao, H., Chen, X., Du, X., Guan, B., Liu, Y., and Zhang, H. (2011). EGF enhances the migration of cancer cells by up-regulation of TRPM7. Cell Calcium 50, 559-568. doi: 10.1016/j.ceca.2011.09.003
41. Ge, R., Tai, Y., Sun, Y., Zhou, K., Yang, S., Cheng, T., et al. (2009). Critical role of TRPC6 channels in VEGF-mediated angiogenesis. Cancer Lett. 283, 43-51. doi: 10.1016/j.canlet.2009.03.023
42. Gkika, D., Flourakis, M., Lemonnier, L., and Prevarskaya, N. (2010). PSA reduces prostate cancer cell motility by stimulating TRPM8 activity and plasma membrane expression. Oncogene 29, 4611-4616. doi: 10.1038/onc.2010.210
43. Gkika, D., and Prevarskaya, N. (2009). Molecular mechanisms of TRP regulation in tumor growth and metastasis. Biochim. Biophys. Acta 1793, 953-958. doi: 10.1016/j.bbamcr.2008.11.010
44. Gkika, D., and Prevarskaya, N. (2011). TRP channels in prostate cancer: the good, the bad and the ugly. Asian J. Androl. 13, 673-676. doi: 10.1038/aja.2011.18
45. Guilbert, A., Dhennin-Duthille, I., Hiani, Y., El, Haren, N., Khorsi, H., Ouadid-Ahidouch, H., et al. (2008). Expression of TRPC6 channels in human epithelial breast cancer cells. BMC Cancer 8:125. doi: 10.1186/1471-2407-8-125
46. Hamdollah Zadeh, M. A., Glass, C. A., Magnussen, A., Hancox, J. C., and Bates, D. O. (2008). VEGF-mediated elevated intracellular calcium and angiogenesis in human microvascular endothelial cells in vitro are inhibited by dominant negative TRPC6. Microcirculation 15, 605-614. doi: 10.1080/10739680802220323
47. Hao, F., Tan, M., Xu, X., Han, J., Miller, D. D., Tigyi, G., et al. (2007). Lysophosphatidic acid induces prostate cancer PC3 cell migration via activation of LPA(1), p42 and p38alpha. Biochim. Biophys. Acta 1771, 883-892. doi: 10.1016/j.bbalip.2007.04.010
48. Hartmannsgruber, V., Heyken, W.-T., Kacik, M., Kaistha, A., Grgic, I., Harteneck, C., et al. (2007). Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS ONE 2:e827. doi: 10.1371/journal.pone.0000827
49. Hewavitharana, T., Deng, X., Soboloff, J., and Gill, D. L. (2007). Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 42, 173-182. doi: 10.1016/j.ceca.2007.03.009
50. Henshall, S. M., Afar, D. E. H., Hiller, J., Horvath, L. G., Quinn, D. I., Rasiah, K. K., et al. (2003). Survival analysis of genome-wide gene expression profiles of prostate cancers identifies new prognostic targets of disease relapse. Cancer Res. 63, 4196-4203.
51. Hisatsune, C., Kuroda, Y., Nakamura, K., Inoue, T., Nakamura, T., Michikawa, T., et al. (2004). Regulation of TRPC6 channel activity by tyrosine phosphorylation. J. Biol. Chem. 279, 18887-18894. doi: 10.1074/jbc.M311274200
52. 2+ entry, endothelial permeability, and angiogenesis. J. Biol. Chem. 285, 33082-33091. doi: 10.1074/jbc.M110.142034
53. Kitamura, K., Kangawa, K., Kawamoto, M., Ichiki, Y., Nakamura, S., Matsuo, H., et al. (1993). Adrenomedullin: a novel hypotensive peptide isolated from human pheochromocytoma. Biochem. Biophys. Res. Commun. 192, 553-560. doi: 10.1006/bbrc.1993.1451
54. Kuang, C., Yu, Y., Wang, K., Qian, D., Den, M., and Huang, L. (2012). Knockdown of transient receptor potential canonical-1 reduces the proliferation and migration of endothelial progenitor cells. Stem Cells Dev. 21, 487-496. doi: 10.1089/scd.2011.0027
55. Levy, C., Khaled, M., Iliopoulos, D., Janas, M. M., Schubert, S., Pinner, S., et al. (2010). Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol. Cell 40, 841-849. doi: 10.1016/j.molcel.2010.11.020
56. 2+ entry and endothelial tube formation. Circ. Res. 108, 1190-1198. doi: 10.1161/CIRCRESAHA.111.243352
57. 2+ entry is remodelled and controls in vitro angiogenesis in endothelial progenitor cells isolated from tumoral patients. PLoS ONE 7:e42541. doi: 10.1371/journal.pone.0042541
58. Lohela, M., and Werb, Z. (2010). Intravital imaging of stromal cell dynamics in tumors. Curr. Opin. Genet. Dev. 20, 72-78. doi: 10.1016/j.gde.2009.10.011
59. Matthews, B. D., Thodeti, C. K., Tytell, J. D., Mammoto, A., Overby, D. R., and Ingber, D. E. (2010). Ultra-rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface beta1 integrins. Integr. Biol. (Camb). 2, 435-442. doi: 10.1039/c0ib00034e
60. 2+ stores stimulates the translocation of vanilloid transient receptor potential 4-c1 heteromeric channels to the plasma membrane. Arterioscler. Thromb. Vasc. Biol. 30, 2249-2255. doi: 10.1161/ATVBAHA.110.212084
61. Ma, X., Cheng, K.-T., Wong, C.-O., O'Neil, R. G., Birnbaumer, L., Ambudkar, I. S., et al. (2011). Heteromeric TRPV4-C1 channels contribute to store-operated Ca(2+) entry in vascular endothelial cells. Cell Calcium 50, 502-509. doi: 10.1016/j.ceca.2011.08.006
62. Meng, X., Cai, C., Wu, J., Cai, S., Ye, C., Chen, H., et al. (2013). TRPM7 mediates breast cancer cell migration and invasion through the MAPK pathway. Cancer Lett. 333, 96-102. doi: 10.1016/j.canlet.2013.01.031
63. Middelbeek, J., Kuipers, A. J., Henneman, L., Visser, D., Eidhof, I., van Horssen, R., et al. (2012). TRPM7 is required for breast tumor cell metastasis. Cancer Res. 72, 4250-4261. doi: 10.1158/0008-5472.CAN-11-3863
64. Moffett, H. F., and Novina, C. D. (2007). A small RNA makes a Bic difference. Genome Biol. 8:221. doi: 10.1186/gb-2007-8-7-221
65. Monet, M., Gkika, D., Lehen'kyi, V., Pourtier, A., Vanden Abeele, F., Bidaux, G., et al. (2009). Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim. Biophys. Acta 1793, 528-539. doi: 10.1016/j.bbamcr.2009.01.003
66. Monet, M., Lehen'kyi, V., Gackiere, F., Firlej, V., Vandenberghe, M., Roudbaraki, M., et al. (2010). Role of cationic channel TRPV2 in promoting prostate cancer migration and progression to androgen resistance. Cancer Res. 70, 1225-1235. doi: 10.1158/0008-5472.CAN-09-2205
67. Monteith, G. R., Davis, F. M., and Roberts-Thomson, S. J. (2012). Calcium channels and pumps in cancer: changes and consequences. J. Biol. Chem. 287, 31666-31673. doi: 10.1074/jbc.R112.343061
68. Montell, C. (2011). The history of TRP channels, a commentary and reflection. Pflugers Arch. 461, 499-506. doi: 10.1007/s00424-010-0920-3
69. Motiani, R. K., Hyzinski-García, M. C., Zhang, X., Henkel, M. M., Abdullaev, I. F., Kuo, Y.-H., et al. (2013). STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch. 465, 1249-1260. doi: 10.1007/s00424-013-1254-8
70. Munaron, L., Genova, T., Avanzato, D., Antoniotti, S., and Fiorio Pla, A. (2013). Targeting calcium channels to block tumor vascularization. Recent Pat. Anticancer. Drug Discov. 8, 27-37. doi: 10.2174/1574892811308010027
71. Nakamura, M., Han, B., Nunobiki, O., and Kakudo, K. (2006). Adrenomedullin: a tumor progression factor via angiogenic control. Curr. Cancer Drug Targets 6, 635-643. doi: 10.2174/156800906778742442
72. Nikitenko, L. L., Fox, S. B., Kehoe, S., Rees, M. C. P., and Bicknell, R. (2006). Adrenomedullin and tumour angiogenesis. Br. J. Cancer 94, 1-7. doi: 10.1038/sj.bjc.6602832
73. Nilius, B., and Owsianik, G. (2011). The transient receptor potential family of ion channels. Genome Biol. 12, 218. doi: 10.1186/gb-2011-12-3-218
74. Nilius, B., Owsianik, G., Voets, T., and Peters, J. A. (2007). Transient receptor potential cation channels in disease. Physiol. Rev. 87, 165-217. doi: 10.1152/physrev.00021.2006
75. Okamoto, Y., Ohkubo, T., Ikebe, T., and Yamazaki, J. (2012). Blockade of TRPM8 activity reduces the invasion potential of oral squamous carcinoma cell lines. Int. J. Oncol. 40, 1431-1440. doi: 10.3892/ijo.2012.1340
76. Ong, H. L., Cheng, K. T., Liu, X., Bandyopadhyay, B. C., Paria, B. C., Soboloff, J., et al. (2007). Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J. Biol. Chem. 282, 9105-9116. doi: 10.1074/jbc.M608942200
77. Ouadid-Ahidouch, H., Dhennin-Duthille, I., Gautier, M., Sevestre, H., and Ahidouch, A. (2013). TRP channels: diagnostic markers and therapeutic targets for breast cancer. Trends Mol. Med. 19, 117-124. doi: 10.1016/j.molmed.2012.11.004
78. Oulidi, A., Bokhobza, A., Gkika, D., Vanden Abeele, F., Lehen'kyi, V., Ouafik, L., et al. (2013). TRPV2 Mediates adrenomedullin stimulation of prostate and urothelial cancer cell adhesion, migration and invasion. PLoS ONE 8:e64885. doi: 10.1371/journal.pone.0064885
79. Paravicini, T. M., Chubanov, V., and Gudermann, T. (2012). TRPM7: a unique channel involved in magnesium homeostasis. Int. J. Biochem. Cell Biol. 44, 1381-1384. doi: 10.1016/j.biocel.2012.05.010
80. Portella, G., Laezza, C., Laccetti, P., De Petrocellis, L., Di Marzo, V., and Bifulco, M. (2003). Inhibitory effects of cannabinoid CB1 receptor stimulation on tumor growth and metastatic spreading: actions on signals involved in angiogenesis and metastasis. FASEB J. 17, 1771-1773. doi: 10.1096/fj.02-1129fje
81. Prevarskaya, N., Skryma, R., and Shuba, Y. (2011). Calcium in tumour metastasis: new roles for known actors. Nat. Rev. Cancer 11, 609-618. doi: 10.1038/nrc3105
82. Raj, G. V., Sekula, J. A., Guo, R., Madden, J. F., and Daaka, Y. (2004). Lysophosphatidic acid promotes survival of androgen-insensitive prostate cancer PC3 cells via activation of NF-kappaB. Prostate 61, 105-113. doi: 10.1002/pros.20083
83. Ramer, R., and Hinz, B. (2008). Inhibition of cancer cell invasion by cannabinoids via increased expression of tissue inhibitor of matrix metalloproteinases-1. J. Natl. Cancer Inst. 100, 59-69. doi: 10.1093/jnci/djm268
84. Ramer, R., Merkord, J., Rohde, H., and Hinz, B. (2010). Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases-1. Biochem. Pharmacol. 79, 955-966. doi: 10.1016/j.bcp.2009.11.007
85. Ramsey, I. S., Delling, M., and Clapham, D. E. (2006). An introduction to TRP channels. Annu. Rev. Physiol. 68, 619-647. doi: 10.1146/annurev.physiol.68.040204.100431
86. 2++ for cancer cell proliferation and survival. Nat. Rev. Cancer 8, 361-375. doi: 10.1038/nrc2374
87. Rybarczyk, P., Gautier, M., Hague, F., Dhennin-Duthille, I., Chatelain, D., Kerr-Conte, J., et al. (2012). Transient receptor potential melastatin-related 7 channel is overexpressed in human pancreatic ductal adenocarcinomas and regulates human pancreatic cancer cell migration. Int. J. Cancer 131, E851-E861. doi: 10.1002/ijc.27487
88. Salido, G. M., Jardín, I., and Rosado, J. A. (2011). The TRPC ion channels: association with Orai1 and STIM1 proteins and participation in capacitative and non-capacitative calcium entry. Adv. Exp. Med. Biol. 704, 413-433. doi: 10.1007/978-94-007-0265-3_23
89. Schwab, A., Fabian, A., Hanley, P. J., and Stock, C. (2012). Role of ion channels and transporters in cell migration. Physiol. Rev. 92, 1865-1913. doi: 10.1152/physrev.00018.2011
90. Song, J., Wang, Y., Li, X., Shen, Y., Yin, M., Guo, Y., et al. (2013). Critical role of TRPC6 channels in the development of human renal cell carcinoma. Mol. Biol. Rep. 40, 5115-5122. doi: 10.1007/s11033-013-2613-4
91. Su, L.-T., Agapito, M. A., Li, M., Simonson, W. T. N., Huttenlocher, A., Habas, R., et al. (2006). TRPM7 regulates cell adhesion by controlling the calcium-dependent protease calpain. J. Biol. Chem. 281, 11260-11270. doi: 10.1074/jbc.M512885200
92. 2+ entry and proliferation of prostate cancer epithelial cells. Cancer Res. 66, 2038-2047. doi: 10.1158/0008-5472.CAN-05-0376
93. Thodeti, C. K., Matthews, B., Ravi, A., Mammoto, A., Ghosh, K., Bracha, A. L., et al. (2009). TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ. Res. 104, 1123-1130. doi: 10.1161/CIRCRESAHA.108.192930
94. Troidl, C., Troidl, K., Schierling, W., Cai, W.-J., Nef, H., Möllmann, H., et al. (2009). Trpv4 induces collateral vessel growth during regeneration of the arterial circulation. J. Cell. Mol. Med. 13, 2613-2621. doi: 10.1111/j.1582-4934.2008.00579.x
95. Tsavaler, L., Shapero, M. H., Morkowski, S., and Laus, R. (2001). Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res. 61, 3760-3769.
96. Valero, M. L., Mello de Queiroz, F., Stühmer, W., Viana, F., and Pardo, L. A. (2012). TRPM8 ion channels differentially modulate proliferation and cell cycle distribution of normal and cancer prostate cells. PLoS ONE 7:e51825. doi: 10.1371/journal.pone.0051825
97. Venkatachalam, K., and Montell, C. (2007). TRP channels. Annu. Rev. Biochem. 76, 387-417. doi: 10.1146/annurev.biochem.75.103004.142819
98. Vriens, J., Watanabe, H., Janssens, A., Droogmans, G., Voets, T., and Nilius, B. (2004). Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc. Natl. Acad. Sci. U.S.A. 101, 396-401. doi: 10.1073/pnas.0303329101
99. Wang, G. X., and Poo, M.-M. (2005). Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434, 898-904. doi: 10.1038/nature03478
100. Wang, Y., Wang, X., Yang, Z., Zhu, G., Chen, D., and Meng, Z. (2012). Menthol inhibits the proliferation and motility of prostate cancer DU145 cells. Pathol. Oncol. Res. 18, 903-910. doi: 10.1007/s12253-012-9520-1
101. Waning, J., Vriens, J., Owsianik, G., Stüwe, L., Mally, S., Fabian, A., et al. (2007). A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium 42, 17-25. doi: 10.1016/j.ceca.2006.11.005
102. Wei, C., Wang, X., Chen, M., Ouyang, K., Song, L.-S., and Cheng, H. (2009). Calcium flickers steer cell migration. Nature 457, 901-905. doi: 10.1038/nature07577
103. Wondergem, R., Ecay, T. W., Mahieu, F., Owsianik, G., and Nilius, B. (2008). HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem. Biophys. Res. Commun. 372, 210-215. doi: 10.1016/j.bbrc.2008.05.032
104. Yamaguchi, H., Wyckoff, J., and Condeelis, J. (2005). Cell migration in tumors. Curr. Opin. Cell Biol. 17, 559-564. doi: 10.1016/j.ceb.2005.08.002
105. Yang, N., Tang, Y., Wang, F., Zhang, H., Xu, D., Shen, Y., et al. (2013). Blockade of store-operated Ca(2+) entry inhibits hepatocarcinoma cell migration and invasion by regulating focal adhesion turnover. Cancer Lett. 330, 163-169. doi: 10.1016/j.canlet.2012.11.040
106. Yang, S., Zhang, J. J., and Huang, X.-Y. (2009a). Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15, 124-134. doi: 10.1016/j.ccr.2008.12.019
107. Yang, Z.-H., Wang, X.-H., Wang, H.-P., and Hu, L.-Q. (2009b). Effects of TRPM8 on the proliferation and motility of prostate cancer PC-3 cells. Asian J. Androl. 11, 157-165. doi: 10.1038/aja.2009.1
108. Yee, N. S., Zhou, W., and Lee, M. (2010). Transient receptor potential channel TRPM8 is over-expressed and required for cellular proliferation in pancreatic adenocarcinoma. Cancer Lett. 297, 49-55. doi: 10.1016/j.canlet.2010.04.023
109. Yeromin, A. V., Zhang, S. L., Jiang, W., Yu, Y., Safrina, O., and Cahalan, M. D. (2006). Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443, 226-229. doi: 10.1038/nature05108
110. Yogi, A., Callera, G. E., Antunes, T. T., Tostes, R. C., and Touyz, R. M. (2011). Transient receptor potential melastatin 7 (TRPM7) cation channels, magnesium and the vascular system in hypertension. Circ. J. 75, 237-245. doi: 10.1253/circj.CJ-10-1021
111. Yue, D., Wang, Y., Xiao, J.-Y., Wang, P., and Ren, C.-S. (2009). Expression of TRPC6 in benign and malignant human prostate tissues. Asian J. Androl. 11, 541-547. doi: 10.1038/aja.2009.53
112. Yu, P., Gu, S., Bu, J., and Du, J. (2010). TRPC1 is essential for in vivo angiogenesis in zebrafish. Circ. Res. 106, 1221-1232. doi: 10.1161/CIRCRESAHA.109.207670
113. Zhang, H., Zhou, L., Shi, W., Song, N., Yu, K., and Gu, Y. (2012). A mechanism underlying the effects of polyunsaturated fatty acids on breast cancer. Int. J. Mol. Med. 30, 487-494. doi: 10.3892/ijmm.2012.1022
114. 2+ entry suppresses EGF-induced migration and eliminates extravasation from vasculature in nasopharyngeal carcinoma cell. Cancer Lett. 336, 390-397. doi: 10.1016/j.canlet.2013.03.026
115. Zhang, L., and Barritt, G. J. (2006). TRPM8 in prostate cancer cells: a potential diagnostic and prognostic marker with a secretory function. Endocr. Relat. Cancer 13, 27-38. doi: 10.1677/erc.1.01093
116. Zhu, G., Wang, X., Yang, Z., Cao, H., Meng, Z., Wang, Y., et al. (2011). Effects of TRPM8 on the proliferation and angiogenesis of prostate cancer PC-3 cells in vivo. Oncol. Lett. 2, 1213-1217. doi: 10.3892/ol.2011.410
117. Zudaire, E., Martínez, A., and Cuttitta, F. (2003). Adrenomedullin and cancer. Regul. Pept. 112, 175-183. doi: 10.1016/S0167-0115(03)00037-5