The store-operated Ca2+ entry-mediated signaling is important for cancer spread

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 6, 2016, Pages 1427-1435

  Chen, Yih Fung ^a,b   Hsu, Keng Fu ^c   Shen, Meng Ru ^b,c  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Invasion; Metastasis; Migration; Orai; Store operated Ca2+ entry (SOCE); Stromal interaction molecule (STIM)

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; MYOSIN ADENOSINE TRIPHOSPHATASE; STROMAL INTERACTION MOLECULE 1; CALCIUM; MEMBRANE PROTEIN; ORAI1 PROTEIN, HUMAN; STIM1 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CALCIUM SIGNALING; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; METASTASIS; METASTASIS POTENTIAL; MIGRATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; STORE OPERATED CALCIUM ION ENTRY; TUMOR CELL; BIOLOGICAL MODEL; CELL MOTION; ENDOPLASMIC RETICULUM; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR INVASION;

CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MOVEMENT; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS;

EID: 84950131926     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.11.030     Document Type: Article

References (88)

1. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
2. Carafoli E. The calcium-signalling saga: tap water and protein crystals. Nat. Rev. Mol. Cell Biol. 2003, 4:326-332.
3. Rizzuto R., Pozzan T. When calcium goes wrong: genetic alterations of a ubiquitous signaling route. Nat. Genet. 2003, 34:135-141.
4. Monteith G.R., Davis F.M., Roberts-Thomson S.J. Calcium channels and pumps in cancer: changes and consequences. J. Biol. Chem. 2012, 287:31666-31673.
5. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
6. 2+ transport. Nat. Rev. Cancer 2007, 7:519-530.
7. Chen Y.F., Chen Y.T., Chiu W.T., Shen M.R. Remodeling of calcium signaling in tumor progression. J. Biomed. Sci. 2013, 20:23.
8. Parekh A.B. Store-operated CRAC channels: function in health and disease. Nat. Rev. Drug Discov. 2010, 9:399-410.
9. Gardel M.L., Schneider I.C., Aratyn-Schaus Y., Waterman C.M. Mechanical integration of actin and adhesion dynamics in cell migration. Annu. Rev. Cell Dev. Biol. 2010, 26:315-333.
10. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 2010, 11:633-643.
11. Kanchanawong P., Shtengel G., Pasapera A.M., Ramko E.B., Davidson M.W., Hess H.F., Waterman C.M. Nanoscale architecture of integrin-based cell adhesions. Nature 2010, 468:580-584.
12. Hanein D., Horwitz A.R. The structure of cell-matrix adhesions: the new frontier. Curr. Opin. Cell Biol. 2012, 24:134-140.
13. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
14. Small J.V., Resch G.P. The comings and goings of actin: coupling protrusion and retraction in cell motility. Curr. Opin. Cell Biol. 2005, 17:517-523.
15. Li R., Gundersen G.G. Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat. Rev. Mol. Cell Biol. 2008, 9:860-873.
16. Bravo-Cordero J.J., Hodgson L., Condeelis J. Directed cell invasion and migration during metastasis. Curr. Opin. Cell Biol. 2012, 24:277-283.
17. Murphy D.A., Courtneidge S.A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 2011, 12:413-426.
18. Linder S., Wiesner C., Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 2011, 27:185-211.
19. Mader C.C., Oser M., Magalhaes M.A., Bravo-Cordero J.J., Condeelis J., Koleske A.J., Gil-Henn H. An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res. 2011, 71:1730-1741.
20. Pan Y.R., Chen C.L., Chen H.C. FAK is required for the assembly of podosome rosettes. J. Cell Biol. 2011, 195:113-129.
21. Yamaguchi H., Yoshida S., Muroi E., Yoshida N., Kawamura M., Kouchi Z., Nakamura Y., Sakai R., Fukami K. Phosphoinositide 3-kinase signaling pathway mediated by p110alpha regulates invadopodia formation. J. Cell Biol. 2011, 193:1275-1288.
22. Beaty B.T., Sharma V.P., Bravo-Cordero J.J., Simpson M.A., Eddy R.J., Koleske A.J., Condeelis J. beta1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol. Biol. Cell 2013, 24:1661-1675. (S1661-1611).
23. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
24. Prevarskaya N., Skryma R., Shuba Y. Calcium in tumour metastasis: new roles for known actors. Nat. Rev. Cancer 2011, 11:609-618.
25. 2+ channels: impact on cell function. J. Physiol. 2008, 586:3043-3054.
26. 2+ pulses control local cycles of lamellipodia retraction and adhesion along the front of migrating cells. Curr. Biol. 2012, 22:837-842.
27. 2+ influx is an essential component of the positive-feedback loop that maintains leading-edge structure and activity in macrophages. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16176-16181.
28. Wei C., Wang X., Chen M., Ouyang K., Song L.S., Cheng H. Calcium flickers steer cell migration. Nature 2009, 457:901-905.
29. Blaser H., Reichman-Fried M., Castanon I., Dumstrei K., Marlow F.L., Kawakami K., Solnica-Krezel L., Heisenberg C.P., Raz E. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev. Cell 2006, 11:613-627.
30. Clark K., Langeslag M., Figdor C.G., van Leeuwen F.N. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 2007, 17:178-186.
31. 2+/calmodulin-dependent kinase II regulates vascular smooth muscle migration through matrix metalloproteinase 9. Am. J. Physiol. Heart Circ. Physiol. 2012, 302:H1953-H1964.
32. Franco S.J., Huttenlocher A. Regulating cell migration: calpains make the cut. J. Cell Sci. 2005, 118:3829-3838.
33. Broussard J.A., Webb D.J., Kaverina I. Asymmetric focal adhesion disassembly in motile cells. Curr. Opin. Cell Biol. 2008, 20:85-90.
34. Lysechko T.L., Cheung S.M., Ostergaard H.L. Regulation of the tyrosine kinase Pyk2 by calcium is through production of reactive oxygen species in cytotoxic T lymphocytes. J. Biol. Chem. 2010, 285:31174-31184.
35. Selitrennik M., Lev S. PYK2 integrates growth factor and cytokine receptors signaling and potentiates breast cancer invasion via a positive feedback loop. Oncotarget 2015, 6:22214-22246.
36. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
37. Putney J.W. Capacitative calcium entry: sensing the calcium stores. J. Cell Biol. 2005, 169:381-382.
38. Soboloff J., Rothberg B.S., Madesh M., Gill D.L. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 2012, 13:549-565.
39. 2+ channel function. J. Cell Biol. 2005, 169:435-445.
40. 2+ influx. Curr. Biol. 2005, 15:1235-1241.
41. Zhang S.L., Yeromin A.V., Zhang X.H., Yu Y., Safrina O., Penna A., Roos J., Stauderman K.A., Cahalan M.D. Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:9357-9362.
42. Feske S., Gwack Y., Prakriya M., Srikanth S., Puppel S.H., Tanasa B., Hogan P.G., Lewis R.S., Daly M., Rao A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006, 441:179-185.
43. Feske S., Gwack Y., Prakriya M., Srikanth S., Puppel S.H., Tanasa B., Hogan P.G., Lewis R.S., Daly M., Rao A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006, 441:179-185.
44. Shuttleworth T.J. Orai3-the 'exceptional' Orai?. J. Physiol. 2012, 590:241-257.
45. 2+ levels. Cell 2007, 131:1327-1339.
46. 2+ entry caused by mild store depletion. J. Physiol. 2013, 591:1433-1445.
47. Zheng L., Stathopulos P.B., Schindl R., Li G.Y., Romanin C., Ikura M. Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1337-1342.
48. Stathopulos P.B., Zheng L., Ikura M. Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J. Biol. Chem. 2009, 284:728-732.
49. 2+ entry. Curr. Biol. 2006, 16:1465-1470.
50. Wang X., Wang Y., Zhou Y., Hendron E., Mancarella S., Andrake M.D., Rothberg B.S., Soboloff J., Gill D.L. Distinct Orai-coupling domains in STIM1 and STIM2 define the orai-activating site. Nat. Commun. 2014, 5:3183.
51. 2+ oscillations and gene expression. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6969-6974.
52. Honnappa S., Gouveia S.M., Weisbrich A., Damberger F.F., Bhavesh N.S., Jawhari H., Grigoriev I., van Rijssel F.J., Buey R.M., Lawera A., Jelesarov I., Winkler F.K., Wuthrich K., Akhmanova A., Steinmetz M.O. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138:366-376.
53. Chen Y.T., Chen Y.F., Chiu W.T., Liu K.Y., Liu Y.L., Chang J.Y., Chang H.C., Shen M.R. Microtubule-associated histone deacetylase 6 supports the calcium store sensor STIM1 in mediating malignant cell behaviors. Cancer Res. 2013, 73:4500-4509.
54. 2+, diacylglycerol and STIM1 signalling system regulates directed cell migration. Nat. Cell Biol. 2014, 16:133-144.
55. Roberts-Thomson S.J., Peters A.A., Grice D.M., Monteith G.R. ORAI-mediated calcium entry: mechanism and roles, diseases and pharmacology. Pharmacol. Ther. 2010, 127:121-130.
56. Desvignes L., Weidinger C., Shaw P., Vaeth M., Ribierre T., Liu M., Fergus T., Kozhaya L., McVoy L., Unutmaz D., Ernst J.D., Feske S. STIM1 controls T cell-mediated immune regulation and inflammation in chronic infection. J. Clin. Invest. 2015, 125:2347-2362.
57. Picard C., McCarl C.A., Papolos A., Khalil S., Luthy K., Hivroz C., LeDeist F., Rieux-Laucat F., Rechavi G., Rao A., Fischer A., Feske S. STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N. Engl. J. Med. 2009, 360:1971-1980.
58. Oh-hora M. Calcium signaling in the development and function of T-lineage cells. Immunol. Rev. 2009, 231:210-224.
59. Nesin V., Wiley G., Kousi M., Ong E.C., Lehmann T., Nicholl D.J., Suri M., Shahrizaila N., Katsanis N., Gaffney P.M., Wierenga K.J., Tsiokas L. Activating mutations in STIM1 and ORAI1 cause overlapping syndromes of tubular myopathy and congenital miosis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:4197-4202.
60. Baba Y., Nishida K., Fujii Y., Hirano T., Hikida M., Kurosaki T. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat. Immunol. 2008, 9:81-88.
61. Vig M., DeHaven W.I., Bird G.S., Billingsley J.M., Wang H., Rao P.E., Hutchings A.B., Jouvin M.H., Putney J.W., Kinet J.P. Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat. Immunol. 2008, 9:89-96.
62. Nunes P., Cornut D., Bochet V., Hasler U., Oh-Hora M., Waldburger J.M., Demaurex N. STIM1 juxtaposes ER to phagosomes, generating Ca(2)(+) hotspots that boost phagocytosis. Curr. Biol. 2012, 22:1990-1997.
63. 2+ entry and endothelial tube formation. Circ. Res. 2011, 108:1190-1198.
64. Zou J.J., Gao Y.D., Geng S., Yang J. Role of STIM1/Orai1-mediated store-operated Ca(2)(+) entry in airway smooth muscle cell proliferation. J. Appl. Physiol. 2011, 110:1256-1263.
65. McAndrew D., Grice D.M., Peters A.A., Davis F.M., Stewart T., Rice M., Smart C.E., Brown M.A., Kenny P.A., Roberts-Thomson S.J., Monteith G.R. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol. Cancer Ther. 2011, 10:448-460.
66. Chen Y.F., Chiu W.T., Chen Y.T., Lin P.Y., Huang H.J., Chou C.Y., Chang H.C., Tang M.J., Shen M.R. 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. 2011, 108:15225-15230.
67. Chen Y.T., Chen Y.F., Chiu W.T., Wang Y.K., Chang H.C., Shen M.R. The ER Ca(2)(+) sensor STIM1 regulates actomyosin contractility of migratory cells. J. Cell Sci. 2013, 126:1260-1267.
68. Yang S., Zhang J.J., Huang X.Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 2009, 15:124-134.
69. Yang N., Tang Y., Wang F., Zhang H., Xu D., Shen Y., Sun S., Yang G. Blockade of store-operated Ca(2+) entry inhibits hepatocarcinoma cell migration and invasion by regulating focal adhesion turnover. Cancer Lett. 2013, 330:163-169.
70. Motiani R.K., Hyzinski-Garcia M.C., Zhang X., Henkel M.M., Abdullaev I.F., Kuo Y.H., Matrougui K., Mongin A.A., Trebak M. STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch. 2013, 465:1249-1260.
71. 2+ entry suppresses EGF-induced migration and eliminates extravasation from vasculature in nasopharyngeal carcinoma cell. Cancer Lett. 2013, 336:390-397.
72. Miyauchi A., Hruska K.A., Greenfield E.M., Duncan R., Alvarez J., Barattolo R., Colucci S., Zambonin-Zallone A., Teitelbaum S.L., Teti A. Osteoclast cytosolic calcium, regulated by voltage-gated calcium channels and extracellular calcium, controls podosome assembly and bone resorption. J. Cell Biol. 1990, 111:2543-2552.
73. Calle Y., Carragher N.O., Thrasher A.J., Jones G.E. Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J. Cell Sci. 2006, 119:2375-2385.
74. Siddiqui T.A., Lively S., Vincent C., Schlichter L.C. Regulation of podosome formation, microglial migration and invasion by Ca(2+)-signaling molecules expressed in podosomes. J. Neuroinflammation 2012, 9:250.
75. Sun J., Lu F., He H., Shen J., Messina J., Mathew R., Wang D., Sarnaik A.A., Chang W.C., Kim M., Cheng H., Yang S. STIM1- and Orai1-mediated Ca(2+) oscillation orchestrates invadopodium formation and melanoma invasion. J. Cell Biol. 2014, 207:535-548.
76. Bravo-Cordero J.J., Marrero-Diaz R., Megias D., Genis L., Garcia-Grande A., Garcia M.A., Arroyo A.G., Montoya M.C. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 2007, 26:1499-1510.
77. Ellis L.M., Hicklin D.J. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat. Rev. Cancer 2008, 8:579-591.
78. Motiani R.K., Zhang X., Harmon K.E., Keller R.S., Matrougui K., Bennett J.A., Trebak M. Orai3 is an estrogen receptor alpha-regulated Ca(2)(+) channel that promotes tumorigenesis. FASEB J. 2013, 27:63-75.
79. Zhang Z., Liu X., Feng B., Liu N., Wu Q., Han Y., Nie Y., Wu K., Shi Y., Fan D. STIM1, a direct target of microRNA-185, promotes tumor metastasis and is associated with poor prognosis in colorectal cancer. Oncogene 2014.
80. 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., Chang W.C. STIM1 overexpression promotes colorectal cancer progression, cell motility and COX-2 expression. Oncogene 2015, 34:4358-4367.
81. 2+ oscillations in human esophageal squamous cell carcinoma. Oncotarget 2014, 5:3455-3471.
82. Yoshida J., Iwabuchi K., Matsui T., Ishibashi T., Masuoka T., Nishio M. Knockdown of stromal interaction molecule 1 (STIM1) suppresses store-operated calcium entry, cell proliferation and tumorigenicity in human epidermoid carcinoma A431 cells. Biochem. Pharmacol. 2012, 84:1592-1603.
83. Ay A.S., Benzerdjeb N., Sevestre H., Ahidouch A., Ouadid-Ahidouch H. Orai3 constitutes a native store-operated calcium entry that regulates non small cell lung adenocarcinoma cell proliferation. PLoS One 2013, 8.
84. 2+ entry (SOCE) regulates melanoma proliferation and cell migration. PLoS One 2014, 9.
85. Kole R., Krainer A.R., Altman S. RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nat. Rev. Drug Discov. 2012, 11:125-140.
86. Weidinger C., Shaw P.J., Feske S. STIM1 and STIM2-mediated Ca(2+) influx regulates antitumour immunity by CD8(+) T cells. EMBO Mol. Med. 2013, 5:1311-1321.
87. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2011, 12:773-786.
88. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X.F., Yao T.P. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.