Reciprocal regulation of actin cytoskeleton remodelling and cell migration by Ca2+ and Zn2+: Role of TRPM2 channels

Journal of Cell Science

Volumn 129, Issue 10, 2016, Pages 2016-2029

  Li, Fangfang ^a   Abuarab, Nada ^a   Sivaprasadarao, Asipu ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Actin cytoskeleton dynamics; Ca2+; Cell migration; Focal adhesion; Lysosomal trafficking; TRPM2 channel; Zn2+

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; CALCIUM ION; HYDROGEN PEROXIDE; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL M2; ZINC ION; CALCIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM2 PROTEIN, HUMAN; ZINC;

ACTIN FILAMENT; ARTICLE; CANCER CELL; CELL MIGRATION; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; FEMALE; FOCAL ADHESION; HELA CELL LINE; HUMAN; HUMAN CELL; LYSOSOME; MALE; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS FIBER; CALCIUM SIGNALING; CELL DEATH; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PSEUDOPODIUM; TRANSCRIPTION INITIATION;

ACTIN CYTOSKELETON; CALCIUM; CALCIUM SIGNALING; CELL DEATH; CELL MOVEMENT; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROGEN PEROXIDE; LYSOSOMES; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PSEUDOPODIA; TRANSCRIPTIONAL ACTIVATION; TRPM CATION CHANNELS; ZINC;

EID: 84970993231     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.179796     Document Type: Article

References (58)

1. Bohil, A. B., Robertson, B. W. and Cheney, R. E. (2006). Myosin-X is a molecular motor that functions in filopodia formation. Proc. Natl. Acad. Sci. USA 103, 12411-12416.
2. Brundage, R. A., Fogarty, K. E., Tuft, R. A. and Fay, F. S. (1991). Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 254, 703-706.
3. Chen, Y.-F., Chiu,W.-T., Chen, Y.-T., Lin, P.-Y., Huang, H.-J., Chou, C.-Y., Chang, H.-C., Tang, M.-J. and Shen, M.-R. (2011). Calcium store sensor stromalinteraction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc. Natl. Acad. Sci. USA 108, 15225-15230.
4. Dourdin, N., Bhatt, A. K., Dutt, P., Greer, P. A., Arthur, J. S. C., Elce, J. S. and Huttenlocher, A. (2001). Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts. J. Biol. Chem. 276, 48382-48388.
5. Duncan, L. M., Deeds, J., Hunter, J., Shao, J., Holmgren, L. M., Woolf, E. A., Tepper, R. I. and Shyjan, A. W. (1998). Down-regulation of the novel gene melastatin correlates with potential for melanoma metastasis. Cancer Res. 58, 1515-1520.
6. Eide, D. J. (2006). Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722.
7. Ellis, S. and Mellor, H. (2000). The novel Rho-family GTPase Rif regulates coordinated actin-based membrane rearrangements. Curr. Biol. 10, 1387-1390.
8. Fabian, A., Fortmann, T., Dieterich, P., Riethmüller, C., Schön, P., Mally, S., Nilius, B. and Schwab, A. (2008). TRPC1 channels regulate directionality of migrating cells. Pflügers Arch. 457, 475-484.
9. Fan, L., Pellegrin, S., Scott, A. and Mellor, H. (2010). The small GTPase Rif is an alternative trigger for the formation of actin stress fibers in epithelial cells. J. Cell Sci. 123, 1247-1252.
10. Gardel, M. L., Schneider, I. C., Aratyn-Schaus, Y. and Waterman, C. M. (2010). Mechanical integration of actin and adhesion dynamics in cell migration. Annu. Rev. Cell Dev. Biol. 26, 315-333.
11. Giannone, G., Dubin-Thaler, B. J., Rossier, O., Cai, Y., Chaga, O., Jiang, G., Beaver, W., Döbereiner, H.-G., Freund, Y., Borisy, G. et al. (2007). Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561-575.
12. 2+]i and cell shape, polarity, and locomotion by InsP3, DAG, and protein kinase C in newt eosinophils. J. Cell Biol. 127, 489-503.
13. Giorgio, M., Trinei, M., Migliaccio, E. and Pelicci, P. G. (2007). Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8, 722-728.
14. Hurd, T. R., DeGennaro, M. and Lehmann, R. (2012). Redox regulation of cell migration and adhesion. Trends Cell Biol. 22, 107-115.
15. Johnson, H. W. and Schell, M. J. (2009). Neuronal IP3 3-kinase is an F-actinbundling protein: role in dendritic targeting and regulation of spine morphology. Mol. Biol. Cell 20, 5166-5180.
16. Klyubin, I. V., Kirpichnikova, K. M. and Gamaley, I. A. (1996). Hydrogen peroxideinduced chemotaxis of mouse peritoneal neutrophils. Eur. J. Cell Biol. 70, 347-351.
17. 2+-induced toxicity. J. Cell Sci. 127, 3094-3103.
18. Lamalice, L., Le Boeuf, F. and Huot, J. (2007). Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794.
19. 2+-release channel in β-Cells. Sci. Signal. 2, ra23.
20. 2+ release triggers pancreatic beta cell death. Biochem. J. 466, 537-546.
21. Mathews, M. T. and Berk, B. C. (2008). PARP-1 inhibition prevents oxidative and nitrosative stress-induced endothelial cell death via transactivation of the VEGF receptor 2. Arterioscler. Thromb. Vasc. Biol. 28, 711-717.
22. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
23. Michels, J., Vitale, I., Saparbaev, M., Castedo, M. and Kroemer, G. (2014). Predictive biomarkers for cancer therapy with PARP inhibitors. Oncogene 33, 3894-3907.
24. Monet, M., Lehen'kyi, V., Gackiere, F., Firlej, V., Vandenberghe, M., Roudbaraki, M., Gkika, D., Pourtier, A., Bidaux, G., Slomianny, C. et al. (2010). Role of cationic channel TRPV2 in promoting prostate cancer migration and progression to androgen resistance. Cancer Res. 70, 1225-1235.
25. Naito, Y., Yamada, T., Ui-Tei, K., Morishita, S. and Saigo, K. (2004). siDirect: highly effective, target-specific siRNA design software for mammalian RNA interference. Nucleic Acids Res. 32, W124-W129.
26. Niethammer, P., Grabher, C., Look, A. T. and Mitchison, T. J. (2009). A tissuescale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996-999.
27. Nilius, B. and Szallasi, A. (2014). Transient receptor potential channels as drug targets: fromthe science of basic research to the art of medicine. Pharmacol. Rev. 66, 676-814.
28. Nobes, C. D. and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
29. Polytarchou, C., Hatziapostolou, M. and Papadimitriou, E. (2005). Hydrogen peroxide stimulates proliferation and migration of human prostate cancer cells through activation of activator protein-1 and up-regulation of the heparin affin regulatory peptide gene. J. Biol. Chem. 280, 40428-40435.
30. Potier, M., Gonzalez, J. C., Motiani, R. K., Abdullaev, I. F., Bisaillon, J. M., Singer, H. A. and Trebak, M. (2009). Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 23, 2425-2437.
31. Prevarskaya, N., Skryma, R. and Shuba, Y. (2011). Calcium in tumour metastasis: new roles for known actors. Nat. Rev. Cancer 11, 609-618.
32. Ridley, A. J. (2001). Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722.
33. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
34. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
35. Sensi, S. L., Paoletti, P., Bush, A. I. and Sekler, I. (2009). Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 10, 780-791.
36. Sigal, Y. J., Quintero, O. A., Cheney, R. E. and Morris, A. J. (2007). Cdc42 and ARP2/3-independent regulation of filopodia by an integral membrane lipidphosphatase- related protein. J. Cell Sci. 120, 340-352.
37. Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: where motility begins. Trends Cell Biol. 12, 112-120.
38. Somlyo, A. V., Bradshaw, D., Ramos, S., Murphy, C., Myers, C. E. and Somlyo, A. P. (2000). Rho-kinase inhibitor retards migration and in vivo dissemination of human prostate cancer cells. Biochem. Biophys. Res. Commun. 269, 652-659.
39. Sumoza-Toledo, A. and Penner, R. (2011). TRPM2: a multifunctional ion channel for calcium signalling. J. Physiol. 589, 1515-1525.
40. 2+ release. FASEB J. 25, 3529-3542.
41. Takahashi, N., Kozai, D., Kobayashi, R., Ebert, M. and Mori, Y. (2011). Roles of TRPM2 in oxidative stress. Cell Calcium 50, 279-287.
42. Takatani-Nakase, T., Matsui, C., Maeda, S., Kawahara, S. and Takahashi, K. (2014). High glucose level promotes migration behavior of breast cancer cells through zinc and its transporters. PLoS ONE 9, e90136.
43. Tian, D., Jacobo, S. M. P., Billing, D., Rozkalne, A., Gage, S. D., Anagnostou, T., Pavenstädt, H., Hsu, H.-H., Schlondorff, J., Ramos, A. and Greka, A. (2010). Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci. Signal. 3, ra77.
44. Tojkander, S., Gateva, G. and Lappalainen, P. (2012). Actin stress fibers - assembly, dynamics and biological roles. J. Cell Sci. 125, 1855-1864.
45. 2+, diacylglycerol and STIM1 signalling system regulates directed cell migration. Nat. Cell Biol. 16, 133-144.
46. Turner, C. E. (2000). Paxillin and focal adhesion signalling. Nat. Cell Biol. 2, E231-E236.
47. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. and Horwitz, A. R. (2009). Nonmuscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790.
48. Waning, J., Vriens, J., Owsianik, G., Stüwe, L., Mally, S., Fabian, A., Frippiat, C., Nilius, B. and Schwab, A. (2007). A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium 42, 17-25.
49. Wei, C., Wang, X., Chen, M., Ouyang, K., Song, L.-S. and Cheng, H. (2009). Calcium flickers steer cell migration. Nature 457, 901-905.
50. Wei, C., Wang, X., Zheng, M. and Cheng, H. (2012). Calcium gradients underlying cell migration. Curr. Opin. Cell Biol. 24, 254-261.
51. Wiggins, H. and Rappoport, J. (2010). An agarose spot assay for chemotactic invasion. Biotechniques 48, 121-124.
52. 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.
53. 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.
54. 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.
55. Yang, W., Manna, P. T., Zou, J., Luo, J., Beech, D. J., Sivaprasadarao, A. and Jiang, L.-H. (2011). Zinc inactivates melastatin transient receptor potential 2 channels via the outer pore. J. Biol. Chem. 286, 23789-23798.
56. Yoo, S. K., Starnes, T. W., Deng, Q. and Huttenlocher, A. (2011). Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature 480, 109-112.
57. Zeng, Z., Inoue, K., Sun, H., Leng, T., Feng, X., Zhu, L. and Xiong, Z.-G. (2015). TRPM7 regulates vascular endothelial cell adhesion and tube formation. Am. J. Physiol. Cell Physiol. 308, C308-C318.
58. Zhao, H., Ruberu, K., Li, H. and Garner, B. (2013). Analysis of subcellular [57Co] cobalamin distribution in SH-SY5Y neurons and brain tissue. J. Neurosci. Methods 217, 67-74.