Lipid rafts couple store-operated Ca2+ entry to constitutive activation of PKB/Akt in a Ca2+/calmodulin-, Src- and PP2A-mediated pathway and promote melanoma tumor growth

Carcinogenesis

Volumn 33, Issue 4, 2012, Pages 740-750

  Fedida Metula, Shlomit ^a   Feldman, Ben ^a   Koshelev, Valeria ^a   Levin Gromiko, Uliana ^a   Voronov, Elena ^a   Fishman, Daniel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; ANTINEOPLASTIC AGENT; CALCIUM; CALCIUM ION; CALMODULIN; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; METHYL BETA CYCLODEXTRIN; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTALENESULFONAMIDE; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; SMALL INTERFERING RNA; STEROID RECEPTOR COACTIVATOR 1; STROMAL INTERACTION MOLECULE 1; UNCLASSIFIED DRUG;

ABLATION THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE DISRUPTION; LIPID RAFT; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SRC HOMOLOGY DOMAIN; SURVIVAL RATE; TUMOR GROWTH; TUMOR LOCALIZATION;

EID: 84859566521     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs021     Document Type: Article

References (62)

1. Madhunapantula, S. V. et al. (2009) The PTEN-AKT3 signaling cascade as a therapeutic target in melanoma. Pigment Cell Melanoma Res., 22, 400-419.
2. Davies, M. A. et al. (2009) Integrated molecular and clinical analysis of AKTactivation in metastatic melanoma. Clin. Cancer Res., 15, 7538-7546.
3. Westermarck, J. et al. (2008) Multiple pathways regulated by the tumor suppressor PP2A in transformation. Trends Mol. Med., 14, 152-160.
4. Jiang, C. C. et al. (2011) MEK-independent survival of B-RAFV600E melanoma cells selected for resistance to apoptosis induced by the RAF inhibitor PLX4720. Clin. Cancer Res., 17, 721-730.
5. Nazarian, R. et al. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature, 468, 973-977.
6. Cheung, M. et al. (2008) Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res., 68, 3429-3439.
7. Paraiso, K. H. et al. (2011) PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res., 71, 2750-2760.
8. Shao, Y. et al. (2010) Akt3-mediated resistance to apoptosis in B-RAFtargeted melanoma cells. Cancer Res., 70, 6670-6681.
9. Patra, S. K. (2009) Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim. Biophys. Acta, 1785, 182-206.
10. Freeman, M. R. et al. (2010) The Rafts of the Medusa: cholesterol targeting in cancer therapy. Oncogene, 29, 3745-3747.
11. Baruthio, F. et al. (2008) Proteomic analysis of membrane rafts of melanoma cells identifies protein patterns characteristic of the tumor progression stage. Proteomics, 8, 4733-4747.
12. Li, Y. C. et al. (2006) Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesteroldepleting agents. Am. J. Pathol., 168, 1107-1118.
13. Ohkawa, Y. et al. (2010) Ganglioside GD3 enhances adhesion signals and augments malignant properties of melanoma cells by recruiting integrins to glycolipid-enriched microdomains. J. Biol. Chem., 285, 27213-27223.
14. Park, E. K. et al. (2009) Cholesterol depletion induces anoikis-like apoptosis via FAK down-regulation and caveolae internalization. J. Pathol., 218, 337-349.
15. Jahn, T. et al. (2007) Lipid rafts are required for Kit survival and proliferation signals. Blood, 110, 1739-1747.
16. Adam, R. M. et al. (2007) Cholesterol sensitivity of endogenous and myristoylated Akt. Cancer Res., 67, 6238-6246.
17. Fedida-Metula, S. et al. (2008) Targeting lipid rafts inhibits protein kinase B by disrupting calcium homeostasis and attenuates malignant properties of melanoma cells. Carcinogenesis, 29, 1546-1554.
18. Feldman, B. et al. (2010) Coupling of mitochondria to store-operated Ca(2+)-signaling sustains constitutive activation of protein kinase B/Akt and augments survival of malignant melanoma cells. Cell Calcium, 47, 525-537.
19. Dong, B. et al. (2007) Ca(2+)/calmodulin directly interacts with the pleckstrin homology domain of AKT1. J. Biol. Chem., 282, 25131-25140.
20. Perez-Garcia, M. J. et al. (2004) Glial cell line-derived neurotrophic factor increases intracellular calcium concentration. Role of calcium/calmodulin in the activation of the phosphatidylinositol 3-kinase pathway. J. Biol. Chem., 279, 6132-6142.
21. Kleene, R. et al. (2010) NCAM-induced neurite outgrowth depends on binding of calmodulin to NCAM and on nuclear import of NCAM and fak fragments. J. Neurosci., 30, 10784-10798.
22. Hayashi, N. et al. (2004) Myristoylation-regulated direct interaction between calcium-bound calmodulin and N-terminal region of pp60v-src. J. Mol. Biol., 338, 169-180.
23. Fecchi, K. et al. (2011) Human melanoma cells express FGFR/Src/Rho signaling that entails an adhesion-independent caveolin-1 membrane association. Int. J. Cancer doi: 10. 1002/ijc. 26092
24. Arcaro, A. et al. (2007) Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signaling. Cell. Signal., 19, 1081-1092.
25. Chen, J. et al. (1994) Tyrosine phosphorylation of protein phosphatase 2A in response to growth stimulation and v-src transformation of fibroblasts. J. Biol. Chem., 269, 7957-7962.
26. Ito, A. et al. (2003) A mutation in protein phosphatase type 2A as a cause of melanoma progression. Histol. Histopathol., 18, 1313-1319.
27. Pani, B. et al. (2008) Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J. Biol. Chem., 283, 17333-17340.
28. Galan, C. et al. (2010) Lipid rafts modulate the activation but not the maintenance of store-operated Ca(2+) entry. Biochim. Biophys. Acta, 1803, 1083-1093.
29. Liao, Y. et al. (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC: orai complex may mediate store and receptor operated Ca2+ entry. Proc. Natl Acad. Sci. USA, 106, 3202-3206.
30. Szejtli, J. (2004) Past present and future of cyclodextrin research. Pure Appl. Chem., 76, 1825-1845.
31. Bagrodia, S. et al. (1991) Altered tyrosine 527 phosphorylation and mitotic activation of p60c-src. Nature, 349, 172-175.
32. Peterson, B. Z. et al. (1999) Calmodulin is the Ca2+ sensor for Ca2+dependent inactivation of L-Type calcium channels. Neuron, 22, 549-558.
33. Prakriya, M. et al. (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature, 443, 230-233.
34. Robinzon, S. et al. (2009) Impaired cholesterol biosynthesis in a neuronal cell line persistently infected with measles virus. J. Virol., 83, 5495-5504.
35. Homsi, J. et al. (2009) Src activation in melanoma and Src inhibitors as therapeutic agents in melanoma. Melanoma Res., 19, 167-175.
36. Barisic, S. et al. (2010) Tyrosine phosphatase inhibition triggers sustained canonical serine-dependent NFkappaB activation via Src-dependent blockade of PP2A. Biochem. Pharmacol., 80, 439-447.
37. Hu, X. et al. (2009) Src kinase up-regulates the ERK cascade through inactivation of protein phosphatase 2A following cerebral ischemia. BMC Neurosci., 10, 74.
38. Liu, W. et al. (2003) Protein phosphatase 2A-linked and -unlinked caspasedependent pathways for downregulation of Akt kinase triggered by 4-hydroxynonenal. Cell Death Differ., 10, 772-781.
39. Osawa, M. et al. (1998) Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J. Mol. Biol., 276, 165-176.
40. Chen, K. F. et al. (2010) CIP2A mediates effects of bortezomib on phospho-Akt and apoptosis in hepatocellular carcinoma cells. Oncogene, 29, 6257-6266.
41. Switzer, C. H. et al. (2011) Targeting SET/I2PP2A oncoprotein functions as a multi-pathway strategy for cancer therapy. Oncogene, 30, 2504-2513.
42. Wong, L. L. et al. (2009) Tyrosine phosphorylation of PP2A is regulated by HER-2 signalling and correlates with breast cancer progression. Int. J. Oncol., 34, 1291-1301.
43. Katz, S. et al. (2011) Activation of the PI3K/Akt signaling pathway through P2Y(2) receptors by extracellular ATP is involved in osteoblastic cell proliferation. Arch. Biochem. Biophys., 513, 144-152.
44. Lewis, R. S. (2011) Store-operated calcium channels: new perspectives on mechanism and function. Cold Spring Harb. Perspect. Biol. doi: 10. 1101/ cshperspect. a003970
45. Yang, S. et al. (2009) Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell, 15, 124-134.
46. Faouzi, M. et al. (2011) Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells. J. Cell. Physiol., 226, 542-551.
47. Koslowski, M. et al. (2008) MS4A12 is a colon-selective store-operated calcium channel promoting malignant cell processes. Cancer Res., 68, 3458-3466.
48. Wang, J. Y. et al. (2012) Involvement of store-operated calcium signaling in EGF-mediated COX-2 gene activation in cancer cells. Cell. Signal., 24, 162-169.
49. Hou, M. F. et al. (2011) Orai1/CRACM1 overexpression suppresses cell proliferation via attenuation of the store-operated calcium influx-mediated signalling pathway in A549 lung cancer cells. Biochim. Biophys. Acta, 1810, 1278-1284.
50. Huang, W. C. et al. (2011) Histamine regulates cyclooxygenase 2 gene activation through Orai1-mediated NFκB activation in lung cancer cells. Cell Calcium, 50, 27-35.
51. El Boustany, C. et al. (2008) Capacitative calcium entry and transient receptor potential canonical 6 expression control human hepatoma cell proliferation. Hepatology, 47, 2068-2077.
52. Wu, N. et al. (2006) Arrestin binding to calmodulin: a direct interaction between two ubiquitous signaling proteins. J. Mol. Biol., 364, 955-963.
53. Sánchez-González, P. et al. (2010) Calmodulin-mediated regulation of the epidermal growth factor receptor. FEBS J., 277, 327-342.
54. Lee, J. H. et al. (2008) Calmodulin dynamically regulates the trafficking of the metabotropic glutamate receptor mGluR5. Proc. Natl Acad. Sci. USA, 105, 12575-12580.
55. Hogan, P. G. et al. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev., 17, 2205-2232.
56. Dolmetsch, R. E. et al. (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature, 392, 933-936.
57. Flockhart, R. J. et al. (2009) NFAT signalling is a novel target of oncogenic BRAF in metastatic melanoma. Br. J. Cancer, 101, 1448-1455.
58. Romashkova, J. A. et al. (1999) NF-kappaB is a target of AKT in antiapoptotic PDGF signalling. Nature, 401, 86-90.
59. Yoeli-Lerner, M. et al. (2009) Akt/protein kinase b and glycogen synthase kinase-3beta signaling pathway regulates cell migration through the NFAT1 transcription factor. Mol. Cancer Res., 7, 425-432.
60. Bar-On, P. et al. (2006) Effects of the cholesterol-lowering compound methyl-beta-cyclodextrin in models of alpha-synucleinopathy. J. Neurochem., 98, 1032-1045.
61. Liu, B. et al. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc. Natl Acad. Sci. USA, 106, 2377-2382.
62. Ramirez, C. M. et al. (2010)Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res., 68, 309-315.