Oncogenic K-Ras suppresses IP3-dependent Ca2+ release through remodelling of the isoform composition of IP3Rs and ER luminal Ca2+levels in colorectal cancer cell lines

Journal of Cell Science

Volumn 127, Issue 7, 2014, Pages 1607-1619

  Pierro, Cristina ^a   Cook, Simon J ^a   Foets, Thomas C F ^a   Bootman, Martin D ^a,b   Roderick, H Llewelyn ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b OPEN UNIVERSITY   (United Kingdom)

Author keywords

Cancer; Inositol 1,4,5 trisphosphate; K Ras; Mitochondria

Indexed keywords

CALCIUM; G PROTEIN COUPLED RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ISOPROTEIN; PROTEIN TYROSINE KINASE; RAS PROTEIN;

ALLELE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANCER CELL CULTURE; CANCER SURVIVAL; CELL FATE; COLORECTAL CANCER; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE DELETION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MITOCHONDRION; ONCOGENE K RAS; PHENOTYPE; PRIORITY JOURNAL; COLORECTAL TUMOR; GENETICS; HCT116 CELL LINE; METABOLISM; ONCOGENE RAS; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CALCIUM; CALCIUM SIGNALING; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; ENDOPLASMIC RETICULUM; GENES, RAS; HCT116 CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; PROTEIN ISOFORMS; RAS PROTEINS;

EID: 84897375103     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.141408     Document Type: Article

References (99)

1. Almirza, W. H., Peters, P. H., van Meerwijk, W. P., van Zoelen, E. J. and Theuvenet, A. P. (2010). Different roles of inositol 1,4,5-trisphosphate receptor subtypes in prostaglandin F(2alpha)-induced calcium oscillations and pacemaking activity of NRK fibroblasts. Cell Calcium 47, 544-553.
2. Arbabian, A., Brouland, J. P., Apati, A., Paszty, K., Hegedus, L., Enyedi, A., Chomienne, C. and Papp, B. (2012). Modulation of endoplasmic reticulum calcium pump expression during lung cancer cell differentiation. FEBS J. 280, 5408-5418.
3. Barbacid, M. (1987). ras genes. Annu. Rev. Biochem. 56, 779-827. Baumgartner, H. K., Gerasimenko, J. V., Thorne, C., Ferdek, P., Pozzan, T., Tepikin, A. V., Petersen, O. H., Sutton, R., Watson, A. J. and Gerasimenko, O. V. (2009). Calcium elevation in mitochondria is the main Ca2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J. Biol. Chem. 284, 20796-20803.
4. Baumgartner, H. K., Gerasimenko, J. V., Thorne, C., Ferdek, P., Pozzan, T., Tepikin, A. V., Petersen, O. H., Sutton, R., Watson, A. J. and Gerasimenko, O. V. (2009). Calcium elevation in mitochondria is the main Ca2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J. Biol. Chem. 284, 20796-20803
5. Belden, S. and Flaherty, K. T. (2012). MEK and RAF inhibitors for BRAF-mutated cancers. Expert Rev. Mol. Med. 14, e17.
6. Bergner, A. and Huber, R. M. (2008). Regulation of the endoplasmic reticulum Ca(2+)-store in cancer. Anticancer. Agents Med. Chem. 8, 705-709.
7. Bergner, A., Kellner, J., Tufman, A. and Huber, R. M. (2009). Endoplasmic reticulum Ca2+-homeostasis is altered in small and non-small cell lung cancer cell lines. J. Exp. Clin. Cancer Res. 28, 25.
8. Berridge, M. J. (2006). Calcium microdomains: organization and function. Cell Calcium 40, 405-412.
9. Berridge, M. J., Bootman, M. D. and Lipp, P. (1998). Calcium-a life and death signal. Nature 395, 645-648.
10. 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.
11. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529.
12. Blackshaw, S., Sawa, A., Sharp, A. H., Ross, C. A., Snyder, S. H. and Khan, A. A. (2000). Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J. 14, 1375-1379.
13. Bollag, G. and McCormick, F. (1991). Regulators and effectors of ras proteins. Annu. Rev. Cell Biol. 7, 601-632.
14. Bootman, M. D., Roderick, H. L., O'Connor, R., Berridge, M. J. and Edward, A. D. (2003). Intracellular calcium signaling. In Handbook of Cell Signaling, pp. 51-56. Burlington, MA: Academic Press.
15. Brouland, J. P., Gélébart, P., Kovàcs, T., Enouf, J., Grossmann, J. and Papp, B. (2005). The loss of sarco/endoplasmic reticulum calcium transport ATPase 3 expression is an early event during the multistep process of colon carcinogenesis. Am. J. Pathol. 167, 233-242.
16. Bunney, T. D. and Katan, M. (2006). Phospholipase C epsilon: linking second messengers and small GTPases. Trends Cell Biol. 16, 640-648.
17. Bunney, T. D., Harris, R., Gandarillas, N. L., Josephs, M. B., Roe, S. M., Sorli, S. C., Paterson, H. F., Rodrigues-Lima, F., Esposito, D., Ponting, C. P. et al. (2006). Structural and mechanistic insights into ras association domains of phospholipase C epsilon. Mol. Cell 21, 495-507.
18. Cárdenas, C., Miller, R. A., Smith, I., Bui, T., Molgó, J., Müller, M., Vais, H., Cheung, K. H., Yang, J., Parker, I. et al. (2010). Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142, 270-283.
19. Caroppo, R., Colella, M., Colasuonno, A., DeLuisi, A., Debellis, L., Curci, S. and Hofer, A. M. (2003). A reassessment of the effects of luminal [Ca2+] on inositol 1,4,5-trisphosphate-induced Ca2+ release from internal stores. J. Biol. Chem. 278, 39503-39508.
20. Chen, R., Valencia, I., Zhong, F., McColl, K. S., Roderick, H. L., Bootman, M. D., Berridge, M. J., Conway, S. J., Holmes, A. B., Mignery, G. A. et al. (2004). Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J. Cell Biol. 166, 193-203.
21. Collins, T. J., Lipp, P., Berridge, M. J. and Bootman, M. D. (2001). Mitochondrial Ca(2+) uptake depends on the spatial and temporal profile of cytosolic Ca(2+) signals. J. Biol. Chem. 276, 26411-26420.
22. Collins, T. J., Berridge, M. J., Lipp, P. and Bootman, M. D. (2002). Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21, 1616-1627.
23. Conway, S. J., Thuring, J. W., Andreu, S., Kvinlaug, B. T., Llewelyn Roderick, H. L., Bootman, M. D. and Holmes, A. B. (2006). The synthesis of membrane permeant derivatives of myo-inositol 1,4,5-trisphosphate. Aust. J. Chem. 59, 887-893.
24. Cook, S. J. and Lockyer, P. J. (2006). Recent advances in Ca(2+)-dependent RAS regulation and cell proliferation. Cell Calcium 39, 101-112.
25. Crépin, A., Bidaux, G., Vanden-Abeele, F., Dewailly, E., Goffin, V., Prevarskaya, N. and Slomianny, C. (2007). Prolactin stimulates prostate cell proliferation by increasing endoplasmic reticulum content due to SERCA 2b over-expression. Biochem. J. 401, 49-55.
26. Csordá s, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A. and Hajnóczky, G. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921.
27. Csordás, G., Várnai, P., Golenár, T., Roy, S., Purkins, G., Schneider, T. G., Balla, T. and Hajnóczky, G. (2010). Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol. Cell 39, 121- 132.
28. Cullen, P. J. and Lockyer, P. J. (2002). Integration of calcium and ras signalling. Nat. Rev. Mol. Cell Biol. 3, 339-348.
29. Cully, M. and Downward, J. (2008). SnapShot: ras signaling. Cell 133, 1292-
30. De Marchi, U., Campello, S., Szabo, I., Tombola, F., Martinou, J. C. and Zoratti, M. (2004). Bax does not directly participate in the Ca(2+)-induced permeability transition of isolated mitochondria. J. Biol. Chem. 279, 37415-37422.
31. Dolmetsch, R. E., Xu, K. and Lewis, R. S. (1998). Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936.
32. Downward, J. (2003a). Role of receptor tyrosine kinases in G-protein-coupled receptor regulation of ras: transactivation or parallel pathways? Biochem. J. 376, e9-e10.
33. Downward, J. (2003b). Targeting ras signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22.
34. Drawnel, F. M., Wachten, D., Molkentin, J. D., Maillet, M., Aronsen, J. M., Swift, F., Sjaastad, I., Liu, N., Catalucci, D., Mikoshiba, K. et al. (2012). Mutual antagonism between IP(3)RII and miRNA-133a regulates calcium signals and cardiac hypertrophy. J. Cell Biol. 199, 783-798.
35. Duchen, M. R. (2000). Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 529, 57-68.
36. Giacomello, M., Drago, I., Bortolozzi, M., Scorzeto, M., Gianelle, A., Pizzo, P. and Pozzan, T. (2010). Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of storeoperated Ca2+ channels. Mol. Cell 38, 280-290.
37. Giorgi, C., Ito, K., Lin, H. K., Santangelo, C., Wieckowski, M. R., Lebiedzinska, M., Bononi, A., Bonora, M., Duszynski, J., Bernardi, R. et al. (2010). PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 330, 1247-1251.
38. Grynkiewicz, G., Poenie, M. and Tsien, R. Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
39. Hagar, R. E., Burgstahler, A. D., Nathanson, M. H. and Ehrlich, B. E. (1998). Type III InsP3 receptor channel stays open in the presence of increased calcium. Nature 396, 81-84.
40. Hajnóczky, G. and Csordás, G. (2010). Calcium signalling: fishing out molecules of mitochondrial calcium transport. Curr. Biol. 20, R888-R891.
41. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57- 70.
42. Hanahan, D. and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
43. Hanson, C. J., Bootman, M. D., Distelhorst, C. W., Maraldi, T. and Roderick, H. L. (2008a). The cellular concentration of Bcl-2 determines its pro- or antiapoptotic effect. Cell Calcium 44, 243-258.
44. Hanson, C. J., Bootman, M. D., Distelhorst, C. W., Wojcikiewicz, R. J. and Roderick, H. L. (2008b). Bcl-2 suppresses Ca(2+) release through inositol 1,4,5-trisphosphate receptors and inhibits Ca(2+) uptake by mitochondria without affecting ER calcium store content. Cell Calcium 44, 324-338.
45. Harzheim, D., Movassagh, M., Foo, R. S.-Y., Ritter, O., Tashfeen, A., Conway, S. J., Bootman, M. D. and Roderick, H. L. (2009). Increased InsP3Rs in the junctional sarcoplasmic reticulum augment Ca2+ transients and arrhythmias associated with cardiac hypertrophy. Proc. Natl. Acad. Sci. USA 106, 11406- 11411.
46. Hashii, M., Nozawa, Y. and Higashida, H. (1993). Bradykinin-induced cytosolic Ca2+ oscillations and inositol tetrakisphosphate-induced Ca2+ influx in voltageclamped ras-transformed NIH/3T3 fibroblasts. J. Biol. Chem. 268, 19403-19410.
47. Hattori, M., Suzuki, A. Z., Higo, T., Miyauchi, H., Michikawa, T., Nakamura, T., Inoue, T. and Mikoshiba, K. (2004). Distinct roles of inositol 1,4,5-trisphosphate receptor types 1 and 3 in Ca2+ signaling. J. Biol. Chem. 279, 11967-11975.
48. Heighway, J., Betticher, D. C., Hoban, P. R., Altermatt, H. J. and Cowen, R. (1996). Coamplification in tumors of KRAS2, type 2 inositol 1,4,5 triphosphate receptor gene, and a novel human gene, KRAG. Genomics 35, 207-214.
49. Higazi, D. R., Fearnley, C. J., Drawnel, F. M., Talasila, A., Corps, E. M., Ritter, O., McDonald, F., Mikoshiba, K., Bootman, M. D. and Roderick, H. L. (2009). Endothelin-1-stimulated InsP3-induced Ca2+ release is a nexus for hypertrophic signaling in cardiac myocytes. Mol. Cell 33, 472-482.
50. Hovnanian, A. (2007). SERCA pumps and human diseases. Subcell. Biochem. 45, 337-363.
51. Humez, S., Legrand, G., Vanden-Abeele, F., Monet, M., Marchetti, P., Lepage, G., Crepin, A., Dewailly, E., Wuytack, F. and Prevarskaya, N. (2004). Role of endoplasmic reticulum calcium content in prostate cancer cell growth regulation by IGF and TNFalpha. J. Cell. Physiol. 201, 201-213.
52. Kahl, C. R. and Means, A. R. (2003). Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 24, 719-736.
53. Kasri, N. N., Holmes, A. M., Bultynck, G., Parys, J. B., Bootman, M. D., Rietdorf, K., Missiaen, L., McDonald, F., De Smedt, H., Conway, S. J. et al. (2004). Regulation of InsP3 receptor activity by neuronal Ca2+-binding proteins. EMBO J. 23, 312-321.
54. Kasri, N. N., Kocks, S. L., Verbert, L., Hébert, S. S., Callewaert, G., Parys, J. B., Missiaen, L. and De Smedt, H. (2006). Up-regulation of inositol 1,4,5-trisphosphate receptor type 1 is responsible for a decreased endoplasmicreticulum Ca2+ content in presenilin double knock-out cells. Cell Calcium 40, 41- 51.
55. Kelley, G. G., Reks, S. E., Ondrako, J. M. and Smrcka, A. V. (2001). Phospholipase C(epsilon): a novel ras effector. EMBO J. 20, 743-754.
56. Khan, A. A., Soloski, M. J., Sharp, A. H., Schilling, G., Sabatini, D. M., Li, S. H., Ross, C. A. and Snyder, S. H. (1996). Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273, 503-507.
57. Khan, M. T., Wagner, L., I. I, Yule, D. I., Bhanumathy, C. and Joseph, S. K. (2006). Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 281, 3731-3737.
58. Kittler, R., Putz, G., Pelletier, L., Poser, I., Heninger, A. K., Drechsel, D., Fischer, S., Konstantinova, I., Habermann, B., Grabner, H. et al. (2004). An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division. Nature 432, 1036-1040.
59. Korošec, B., Glavac, D., Rott, T. and Ravnik-Glavac, M. (2006). Alterations in the ATP2A2 gene in correlation with colon and lung cancer. Cancer Genet. Cytogenet. 171, 105-111.
60. Lang, F., Friedrich, F., Kahn, E., Wöll, E., Hammerer, M., Waldegger, S., Maly, K. and Grunicke, H. (1991). Bradykinin-induced oscillations of cell membrane potential in cells expressing the Ha-ras oncogene. J. Biol. Chem. 266, 4938- 4942.
61. Legrand, G., Humez, S., Slomianny, C., Dewailly, E., Vanden Abeele, F., Mariot, P., Wuytack, F. and Prevarskaya, N. (2001). Ca2+ pools and cell growth. Evidence for sarcoendoplasmic Ca2+-ATPases 2B involvement in human prostate cancer cell growth control. J. Biol. Chem. 276, 47608-47614.
62. Lipskaia, L., Hulot, J. S. and Lompré, A. M. (2009). Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation. Pflugers Arch. 457, 673-685.
63. Little, A. S., Smith, P. D. and Cook, S. J. (2013). Mechanisms of acquired resistance to ERK1/2 pathway inhibitors. Oncogene 32, 1207-1215.
64. Marchi, S., Marinello, M., Bononi, A., Bonora, M., Giorgi, C., Rimessi, A. and Pinton, P. (2012). Selective modulation of subtype III IP3R by Akt regulates ER Ca2+ release and apoptosis. Cell Death Dis. 3, e304.
65. Mendes, C. C., Gomes, D. A., Thompson, M., Souto, N. C., Goes, T. S., Goes, A. M., Rodrigues, M. A., Gomez, M. V., Nathanson, M. H. and Leite, M. F. (2005). The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J. Biol. Chem. 280, 40892-40900.
66. Miyakawa, T., Maeda, A., Yamazawa, T., Hirose, K., Kurosaki, T. and Iino, M. (1999). Encoding of Ca2+ signals by differential expression of IP3 receptor subtypes. EMBO J. 18, 1303-1308.
67. Monteith, G. R., McAndrew, D., Faddy, H. M. and Roberts-Thomson, S. J. (2007). Calcium and cancer: targeting Ca2+ transport. Nat. Rev. Cancer 7, 519- 530.
68. 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.
69. Motiani, R. K., Hyzinski-García, 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.
70. Oakes, S. A., Scorrano, L., Opferman, J. T., Bassik, M. C., Nishino, M., Pozzan, T. and Korsmeyer, S. J. (2005). Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102, 105-110.
71. Orrenius, S., Zhivotovsky, B. and Nicotera, P. (2003). Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4, 552-565.
72. Palmer, A. E., Jin, C., Reed, J. C. and Tsien, R. Y. (2004). Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc. Natl. Acad. Sci. USA 101, 17404-17409.
73. Peppiatt, C. M., Collins, T. J., Mackenzie, L., Conway, S. J., Holmes, A. B., Bootman, M. D., Berridge, M. J., Seo, J. T. and Roderick, H. L. (2003). 2- Aminoethoxydiphenyl borate (2-APB) antagonises inositol 1,4,5-trisphosphateinduced calcium release, inhibits calcium pumps and has a use-dependent and slowly reversible action on store-operated calcium entry channels. Cell Calcium 34, 97-108.
74. Pinton, P., Ferrari, D., Rapizzi, E., Di Virgilio, F., Pozzan, T. and Rizzuto, R. (2001). The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 20, 2690-2701.
75. Pinton, P., Giorgi, C., Siviero, R., Zecchini, E. and Rizzuto, R. (2008). Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27, 6407-6418.
76. Prasad, V., Boivin, G. P., Miller, M. L., Liu, L. H., Erwin, C. R., Warner, B. W. and Shull, G. E. (2005). Haploinsufficiency of Atp2a2, encoding the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 Ca2+ pump, predisposes mice to squamous cell tumors via a novel mode of cancer susceptibility. Cancer Res. 65, 8655-8661.
77. Rizzuto, R. and Pozzan, T. (2006). Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 86, 369-408.
78. Rizzuto, R., Pinton, P., Carrington, W., Fay, F. S., Fogarty, K. E., Lifshitz, L. M., Tuft, R. A. and Pozzan, T. (1998). Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280, 1763-1766.
79. Rizzuto, R., Pinton, P., Ferrari, D., Chami, M., Szabadkai, G., Magalhães, P. J., Di Virgilio, F. and Pozzan, T. (2003). Calcium and apoptosis: facts and hypotheses. Oncogene 22, 8619-8627.
80. Rizzuto, R., Duchen, M. R. and Pozzan, T. (2004). Flirting in little space: the ER/ mitochondria Ca2+ liaison. Sci. STKE 2004, re1.
81. Rizzuto, R., De Stefani, D., Raffaello, A. and Mammucari, C. (2012). Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 13, 566-578.
82. Roderick, H. L. and Cook, S. J. (2008). Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat. Rev. Cancer 8, 361-375.
83. Roderick, H. L., Campbell, A. K. and Llewellyn, D. H. (1997). Nuclear localisation of calreticulin in vivo is enhanced by its interaction with glucocorticoid receptors. FEBS Lett. 405, 181-185.
84. Sakakura, C., Hagiwara, A., Fukuda, K., Shimomura, K., Takagi, T., Kin, S., Nakase, Y., Fujiyama, J., Mikoshiba, K., Okazaki, Y. et al. (2003). Possible involvement of inositol 1,4,5-trisphosphate receptor type 3 (IP3R3) in the peritoneal dissemination of gastric cancers. Anticancer Res. 23 5A, 3691-3697.
85. Schulze, A., Nicke, B., Warne, P. H., Tomlinson, S. and Downward, J. (2004). The transcriptional response to Raf activation is almost completely dependent on mitogen-activated protein kinase kinase activity and shows a major autocrine component. Mol. Biol. Cell 15, 3450-3463.
86. Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D. and Lowe, S. W. (1997). Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88, 593-602.
87. Shirasawa, S., Furuse, M., Yokoyama, N. and Sasazuki, T. (1993). Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260, 85-88.
88. Szabadkai, G. and Duchen, M. R. (2008). Mitochondria: the hub of cellular Ca2+ signaling. Physiology (Bethesda) 23, 84-94.
89. Szado, T., Vanderheyden, V., Parys, J. B., De Smedt, H., Rietdorf, K., Kotelevets, L., Chastre, E., Khan, F., Landegren, U., Söderberg, O. et al. (2008). Phosphorylation of inositol 1,4,5-trisphosphate receptors by protein kinase B/Akt inhibits Ca2+ release and apoptosis. Proc. Natl. Acad. Sci. USA 105, 2427-2432.
90. Szatkowski, C., Parys, J. B., Ouadid-Ahidouch, H. and Matifat, F. (2010). Inositol 1,4,5-trisphosphate-induced Ca2+ signalling is involved in estradiolinduced breast cancer epithelial cell growth. Mol. Cancer 9, 156.
91. Thomas, D., Lipp, P., Tovey, S. C., Berridge, M. J., Li, W., Tsien, R. Y. and Bootman, M. D. (2000). Microscopic properties of elementary Ca2+ release sites in non-excitable cells. Curr. Biol. 10, 8-15.
92. Tuveson, D. A., Shaw, A. T., Willis, N. A., Silver, D. P., Jackson, E. L., Chang, S., Mercer, K. L., Grochow, R., Hock, H., Crowley, D. et al. (2004). Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5, 375-387.
93. Vartanian, S., Bentley, C., Brauer, M. J., Li, L., Shirasawa, S., Sasazuki, T., Kim, J. S., Haverty, P., Stawiski, E., Modrusan, Z. et al. (2013). Identification of mutant K-Ras-dependent phenotypes using a panel of isogenic cell lines. J. Biol. Chem. 288, 2403-2413.
94. Wakelam, M. J., Davies, S. A., Houslay, M. D., McKay, I., Marshall, C. J. and Hall, A. (1986). Normal p21N-ras couples bombesin and other growth factor receptors to inositol phosphate production. Nature 323, 173-176.
95. Weber, G. (2005). Down-regulation of increased signal transduction capacity in human cancer cells. Adv. Enzyme Regul. 45, 37-51.
96. Wu,W. K., Wang, X. J., Cheng, A. S., Luo, M. X., Ng, S. S., To, K. F., Chan, F. K., Cho, C. H., Sung, J. J. and Yu, J. (2013). Dysregulation and crosstalk of cellular signaling pathways in colon carcinogenesis. Crit. Rev. Oncol. Hematol. 86, 251-277.
97. Wuytack, F., Eggermont, J. A., Raeymaekers, L., Plessers, L. and Casteels, R. (1989). Antibodies against the non-muscle isoform of the endoplasmic reticulum Ca2(+)-transport ATPase. Biochem. J. 264, 765-769.
98. Wuytack, F., Papp, B., Verboomen, H., Raeymaekers, L., Dode, L., Bobe, R., Enouf, J., Bokkala, S., Authi, K. S. and Casteels, R. (1994). A sarco/endoplasmic reticulum Ca(2+)-ATPase 3-type Ca2+ pump is expressed in platelets, in lymphoid cells, and in mast cells. J. Biol. Chem. 269, 1410-1416.
99. Yoshida, J., Iwabuchi, K., Matsui, T., Ishibashi, T., Masuoka, T. and Nishio, M. (2012). Knockdown of stromal interaction molecule 1 (STIM1) suppresses storeoperated calcium entry, cell proliferation and tumorigenicity in human epidermoid carcinoma A431 cells. Biochem. Pharmacol. 84, 1592-1603.