CLIC4 is a tumor suppressor for cutaneous squamous cell cancer

Carcinogenesis

Volumn 33, Issue 5, 2012, Pages 986-995

  Suh, K Stephen ^a,b   Malik, Mariam ^a   Shukla, Anjali ^a   Ryscavage, Andrew ^a   Wright, Lisa ^a   Jividen, Kasey ^a   Crutchley, John M ^a   Dumont, Rebecca A ^a   Fernandez Salas, Ester ^a,c   Webster, Joshua D ^a   Simpson, R Mark ^a   Yuspa, Stuart H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HACKENSACK UNIVERSITY MEDICAL CENTER   (United States)

^c ALLERGAN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; CHLORIDE INTRACELLULAR CHANNEL 4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; EPIDERMIS; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MALE; MOUSE; NEWBORN; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CARCINOMA;

EID: 84860475420     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs115     Document Type: Article

References (50)

1. Suh, K.S. et al. (2005) Intracellular chloride channels: critical mediators of cell viability and potential targets for cancer therapy. Curr. Pharm. Des., 11, 2753-2764.
2. Singh, H. et al. (2006) Redox regulation of CLIC1 by cysteine residues associated with the putative channel pore. Biophys. J., 90, 1628-1638.
3. Littler, D.R. et al. (2005) Crystal structure of the soluble form of the redoxregulated chloride ion channel protein CLIC4. FEBS J., 272, 4996-5007.
4. Littler, D.R. et al. (2010) The enigma of the CLIC proteins: ion channels, redox proteins, enzymes, scaffolding proteins? FEBS Lett., 584, 2093-2101.
5. Oakley, A.J. (2005) Glutathione transferases: new functions. Curr. Opin. Struct. Biol., 15, 716-723.
6. Suh, K.S. et al. (2007) Reciprocal modifications of CLIC4 in tumor epithelium and stroma mark malignant progression of multiple human cancers. Clin. Cancer Res., 13, 121-131.
7. Ashley, R.H. (2003) Challenging accepted ion channel biology: p64 and the CLIC family of putative intracellular anion channel proteins. Mol. Membr. Biol., 20, 1-11.
8. Suh, K.S. et al. (2007b) CLIC4, skin homeostasis and cutaneous cancer: surprising connections. Mol. Carcinog., 46, 599-604.
9. Ponsioen, B. et al. (2009) Spatiotemporal regulation of chloride intracellular channel protein CLIC4 by RhoA. Mol. Biol. Cell, 20, 4664-4672.
10. Boyer, L.A. et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell, 122, 947-956.
11. Myers, K. et al. (2004) Identification of chloride intracellular channel proteins in spermatozoa. FEBS Lett., 566, 136-140.
12. Qian, Z. et al. (1999) Molecular cloning and characterization of a mitogenactivated protein kinase-associated intracellular chloride channel. J. Biol. Chem., 274, 1621-1627.
13. Suh, K.S. et al. (2005) Antisense suppression of the chloride intracellular channel family induces apoptosis, enhances tumor necrosis factor α -induced apoptosis, and inhibits tumor growth. Cancer Res., 65, 562-571.
14. Paradisi, S. et al. (2008) Blockade of chloride intracellular ion channel 1 stimulates Abeta phagocytosis. J. Neurosci. Res., 86, 2488-2498.
15. Jalilian, C. et al. (2008) Redox potential and the response of cardiac ryanodine receptors to CLIC-2, a member of the glutathione S-transferase structural family. Antioxid. Redox Signal., 10, 1675-1686.
16. Berry, K.L. et al. (2006) Mapping functional domains of chloride intracellular channel (CLIC) proteins in vivo. J. Mol. Biol., 359, 1316-1333.
17. Littler, D.R. et al. (2008) Comparison of vertebrate and invertebrate CLIC proteins: the crystal structures of Caenorhabditis elegans EXC-4 and Drosophila melanogaster DmCLIC. Protein, 71, 364-378.
18. Fernandez-Salas, E. et al. (1999) p53 and tumor necrosis factor a regulate the expression of a mitochondrial chloride channel protein. J. Biol. Chem., 274, 36488-36497.
19. Suh, K.S. et al. (2004) The organellular chloride channel protein CLIC4/mtCLIC translocates to the nucleus in response to cellular stress and accelerates apoptosis. J. Biol. Chem., 279, 4632-4641.
20. Chuang, J.Z. et al. (1999) A 29 kDa intracellular chloride channel p64H1 is associated with large dense-core vesicles in rat hippocampal neurons. J. Neurosci., 19, 2919-2928.
21. Fernandez-Salas, E. et al. (2002) mtCLIC/CLIC4, an organellular chloride channel protein, is increased by DNA damage and participates in the apoptotic response to p53. Mol. Cell. Biol., 22, 3610-3620.
22. Shiio, Y. et al. (2006) Quantitative proteomic analysis of myc-induced apoptosis: a direct role for Myc induction of the mitochondrial chloride ion channel, mtCLIC/CLIC4. J. Biol. Chem., 281, 2750-2756.
23. Suginta, W. et al. (2001) Chloride intracellular channel protein CLIC4 (p64H1) binds directly to brain dynamin I in a complex containing actin, tubulin and 14-3-3 isoforms. Biochem. J., 359, 55-64.
24. Berryman, M.A. et al. (2003) CLIC4 is enriched at cell-cell junctions and colocalizes with AKAP350 at the centrosome and midbody of cultured mammalian cells. Cell Motil. Cytoskeleton, 56, 159-172.
25. Bohman, S. et al. (2005) Proteomic analysis of vascular endothelial growth factor-induced endothelial cell differentiation reveals a role for chloride intracellular channel 4 (CLIC4) in tubular morphogenesis. J. Biol. Chem., 280, 42397-42404.
26. Ulmasov, B. et al. (2009) Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway. Am. J. Pathol., 174, 1084-1096.
27. Suh, K.S. et al. (2007c) CLIC4 mediates and is required for Ca2+-induced keratinocyte differentiation. J. Cell Sci., 120, 2631-2640.
28. Kitamura, A. et al. (2001) Expression of p68 RNA helicase is closely related to the early stage of adipocyte differentiation of mouse 3T3-L1 cells. Biochem. Biophys. Res. Commun., 287, 435-439.
29. Malik, M. et al. (2010) S-nitrosylation regulates nuclear translocation of chloride intracellular channel protein CLIC4. J. Biol. Chem., 285, 23818-23828.
30. Shukla, A. et al. (2009) TGF-beta signalling is regulated by Schnurri-2-dependent nuclear translocation of CLIC4 and consequent stabilization of phospho-Smad2 and 3. Nat. Cell Biol., 11, 777-784.
31. Lichti, U. et al. (2008) Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat. Protoc., 3, 7799-7810.
32. Darwiche, N. et al. (2007) Expression profile of skin papillomas with high cancer risk displays a unique genetic signature that clusters with squamous cell carcinomas and predicts risk for malignant conversion. Oncogene, 26, 6885-6895.
33. Connolly, E.C. et al. (2011) The complexities of TGF-b action during mammary and squamous cell carcinogenesis. Curr. Pharm. Biotechnol., 33, 2138-2149.
34. Trachootham, D. et al. (2008) Redox regulation of cell survival. Antioxid. Redox Signal., 10, 1343-1374.
35. Powis, G. et al. (2007) Thioredoxin signaling as a target for cancer therapy. Curr. Opin. Pharmacol., 7, 392-397.
36. Yoo, M.H. et al. (2010) Alteration of thioredoxin reductase 1 levels in elucidating cancer etiology. Methods Enzymol., 474, 255-275.
37. Tonissen, K.F. et al. (2009) Thioredoxin system inhibitors as mediators of apoptosis for cancer therapy. Mol. Nutr. Food Res., 53, 87-103.
38. Morris, R.J. et al. (2004) Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol., 22, 411-417.
39. Ahlborn, G.J. et al. (2008) Dose response evaluation of gene expression profiles in the skin of K6/ODC mice exposed to sodium arsenite. Toxicol. Appl. Pharmacol., 227, 400-416.
40. Ronnov-Jessen, L. et al. (2002) Differential expression of a chloride intracellular channel gene, CLIC4, in transforming growth factor-beta1-mediated conversion of fibroblasts to myofibroblasts. Am. J. Pathol., 161, 471-480.
41. Chen, L. et al. (2004) Light damage induced changes in mouse retinal gene expression. Exp. Eye Res., 79, 239-247.
42. Bae, S.M. et al. (2004) Expression profiling of the cellular processes in uterine leiomyomas: omic approaches and IGF-2 association with leiomyosarcomas. Cancer Res. Treat., 36, 31-42.
43. Liu, M. et al. (2005) Genes transactivated by hepatitis C virus core protein, a microarray assay. World J. Gastroenterol., 11, 3351-3356.
44. Alonso, S.R. et al. (2007) A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res., 67, 3450-3460.
45. Sukiennicki, T.L. et al. (2006) Distinct molecular program imposed on CD4+ T cell targets by CD4+CD25+ regulatory T cells. J. Immunol., 177, 6952-6961.
46. Ogawa, S. et al. (2005) Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell, 122, 707-721.
47. Mynott, A.V. et al. (2011) Crystal structure of importin-a bound to a peptide bearing the nuclear localisation signal from chloride intracellular channel protein 4. FEBS J., 278, 1662-1675.
48. Trachootham, D. et al. (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell, 10, 241-252.
49. Yoo, M.H. et al. (2007) Targeting thioredoxin reductase 1 reduction in cancer cells inhibits self-sufficient growth and DNA replication. PLoS One, 2, e1112.
50. Huh, Y.J. et al. (2006) Regulation of osteoclast differentiation by the redoxdependent modulation of nuclear import of transcription factors. Cell Death Differ., 13, 1138-1146.