The Transition from Proliferation to Differentiation in Colorectal Cancer Is Regulated by the Calcium Activated Chloride Channel A1

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Yang, Bo ^a   Cao, Lin ^b   Liu, Bin ^a   McCaig, Colin D ^b   Pu, Jin ^b  

^a 309TH HOSPITAL OF PLA   (China)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ACTIVATED CHLORIDE CHANNEL A1; CALCIUM ACTIVATED CHLORIDE CHANNEL A4; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN CACO 2; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN TISSUE; PROTEIN EXPRESSION; UPREGULATION;

ALKALINE PHOSPHATASE; BUTYRATES; CACO-2 CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHLORIDE CHANNELS; COLORECTAL NEOPLASMS; DOWN-REGULATION; ENTEROCYTES; GENE EXPRESSION REGULATION, NEOPLASTIC; GPI-LINKED PROTEINS; HUMANS; SUCRASE-ISOMALTASE COMPLEX; UP-REGULATION;

ANIMALIA;

EID: 84876076360     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060861     Document Type: Article

References (72)

1. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, et al. (2002) The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111: 241-250.
2. Gray LS, Perez-Reyes E, Gomora JC, Haverstick DM, Shattock M, et al. (2004) The role of voltage gated T-type Ca2+ channel isoforms in mediating "capacitative" Ca2+ entry in cancer cells. Cell Calcium 36: 489-497.
3. Ribiczey P, Tordai A, Andrikovics H, Filoteo AG, Penniston JT, et al. (2007) Isoform-specific up-regulation of plasma membrane Ca2+ATPase expression during colon and gastric cancer cell differentiation. Cell Calcium 42: 590-605.
4. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
5. Lehen'kyi V, Shapovalov G, Skryma R, Prevarskaya N, (2011) Ion channnels and transporters in cancer. 5. Ion channels in control of cancer and cell apoptosis. Am J Physiol Cell Physiol 301: C1281-1289.
6. Mu D, Chen L, Zhang X, See LH, Koch CM, et al. (2003) Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene. Cancer Cell 3: 297-302.
7. Takanami I, Inoue Y, Gika M, (2004) G-protein inwardly rectifying potassium channel 1 (GIRK 1) gene expression correlates with tumor progression in non-small cell lung cancer. BMC Cancer 4: 79.
8. Tsavaler L, Shapero MH, Morkowski S, Laus R, (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61: 3760-3769.
9. Schonherr R, (2005) Clinical relevance of ion channels for diagnosis and therapy of cancer. J Membr Biol 205: 175-184.
10. Anderson MP, Sheppard DN, Berger HA, Welsh MJ, (1992) Chloride channels in the apical membrane of normal and cystic fibrosis airway and intestinal epithelia. Am J Physiol 263: L1-14.
11. Okada Y, Shimizu T, Maeno E, Tanabe S, Wang X, et al. (2006) Volume-sensitive chloride channels involved in apoptotic volume decrease and cell death. J Membr Biol 209: 21-29.
12. Shen MR, Yang TP, Tang MJ, (2002) A novel function of BCL-2 overexpression in regulatory volume decrease. Enhancing swelling-activated Ca(2+) entry and Cl(-) channel activity. J Biol Chem 277: 15592-15599.
13. Lemonnier L, Shuba Y, Crepin A, Roudbaraki M, Slomianny C, et al. (2004) Bcl-2-dependent modulation of swelling-activated Cl- current and ClC-3 expression in human prostate cancer epithelial cells. Cancer Res 64: 4841-4848.
14. Cunningham SA, Awayda MS, Bubien JK, Ismailov, II, Arrate MP, et al. (1995) Cloning of an epithelial chloride channel from bovine trachea. J Biol Chem 270: 31016-31026.
15. Gandhi R, Elble RC, Gruber AD, Schreur KD, Ji HL, et al. (1998) Molecular and functional characterization of a calcium-sensitive chloride channel from mouse lung. J Biol Chem 273: 32096-32101.
16. Gruber AD, Elble RC, Ji HL, Schreur KD, Fuller CM, et al. (1998) Genomic cloning, molecular characterization, and functional analysis of human CLCA1, the first human member of the family of Ca2+-activated Cl- channel proteins. Genomics 54: 200-214.
17. Gruber AD, Pauli BU, (1999) Tumorigenicity of human breast cancer is associated with loss of the Ca2+-activated chloride channel CLCA2. Cancer Res 59: 5488-5491.
18. Elble RC, Pauli BU, (2001) Tumor suppression by a proapoptotic calcium-activated chloride channel in mammary epithelium. J Biol Chem 276: 40510-40517.
19. Bustin SA, Li SR, Dorudi S, (2001) Expression of the Ca2+-activated chloride channel genes CLCA1 and CLCA2 is downregulated in human colorectal cancer. DNA Cell Biol 20: 331-338.
20. Buhrke T, Lengler I, Lampen A, (2011) Analysis of proteomic changes induced upon cellular differentiation of the human intestinal cell line Caco-2. Dev Growth Differ 53: 411-426.
21. Bajka BH, Clarke JM, Cobiac L, Topping DL, (2008) Butyrylated starch protects colonocyte DNA against dietary protein-induced damage in rats. Carcinogenesis 29: 2169-2174.
22. Chung YS, Song IS, Erickson RH, Sleisenger MH, Kim YS, (1985) Effect of growth and sodium butyrate on brush border membrane-associated hydrolases in human colorectal cancer cell lines. Cancer Res 45: 2976-2982.
23. Siavoshian S, Segain JP, Kornprobst M, Bonnet C, Cherbut C, et al. (2000) Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut 46: 507-514.
24. Byrd JC, Alho H, (1987) Differentiation of PC12 pheochromocytoma cells by sodium butyrate. Brain Res 428: 151-155.
25. Blouin JM, Penot G, Collinet M, Nacfer M, Forest C, et al. (2011) Butyrate elicits a metabolic switch in human colon cancer cells by targeting the pyruvate dehydrogenase complex. Int J Cancer 128: 2591-2601.
26. Hilgers AR, Conradi RA, Burton PS, (1990) Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa. Pharm Res 7: 902-910.
27. Mariadason JM, Bordonaro M, Aslam F, Shi L, Kuraguchi M, et al. (2001) Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 61: 3465-3471.
28. Kinzler KW, Vogelstein B, (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170.
29. Doyon G, St-Jean S, Darsigny M, Asselin C, Boudreau F, (2009) Nuclear receptor co-repressor is required to maintain proliferation of normal intestinal epithelial cells in culture and down-modulates the expression of pigment epithelium-derived factor. J Biol Chem 284: 25220-25229.
30. van den Brink GR, Offerhaus GJ, (2007) The morphogenetic code and colon cancer development. Cancer Cell 11: 109-117.
31. Missero C, Di Cunto F, Kiyokawa H, Koff A, Dotto GP, (1996) The absence of p21Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev 10: 3065-3075.
32. Lee JY, Chien IC, Lin WY, Wu SM, Wei BH, et al. (2012) Fhl1 as a downstream target of Wnt signaling to promote myogenesis of C2C12 cells. Mol Cell Biochem 365: 251-262.
33. Dupasquier S, Abdel-Samad R, Glazer RI, Bastide P, Jay P, et al. (2009) A new mechanism of SOX9 action to regulate PKCalpha expression in the intestine epithelium. J Cell Sci 122: 2191-2196.
34. Cao L, Zhang XD, Liu X, Chen TY, Zhao M, (2010) Chloride channels and transporters in human corneal epithelium. Exp Eye Res 90: 771-779.
35. Connon CJ, Kawasaki S, Liles M, Koizumi N, Yamasaki K, et al. (2006) Gene expression and immunolocalisation of a calcium-activated chloride channel during the stratification of cultivated and developing corneal epithelium. Cell Tissue Res 323: 177-182.
36. Elble RC, Widom J, Gruber AD, Abdel-Ghany M, Levine R, et al. (1997) Cloning and characterization of lung-endothelial cell adhesion molecule-1 suggest it is an endothelial chloride channel. J Biol Chem 272: 27853-27861.
37. Gruber AD, Schreur KD, Ji HL, Fuller CM, Pauli BU, (1999) Molecular cloning and transmembrane structure of hCLCA2 from human lung, trachea, and mammary gland. Am J Physiol 276: C1261-1270.
38. Walia V, Yu Y, Cao D, Sun M, McLean JR, et al. (2012) Loss of breast epithelial marker hCLCA2 promotes epithelial-to-mesenchymal transition and indicates higher risk of metastasis. Oncogene 31: 2237-2246.
39. Thompson EB, (1998) The many roles of c-Myc in apoptosis. Annu Rev Physiol 60: 575-600.
40. Agnel M, Vermat T, Culouscou JM, (1999) Identification of three novel members of the calcium-dependent chloride channel (CaCC) family predominantly expressed in the digestive tract and trachea. FEBS Lett 455: 295-301.
41. McCaig CD, Song B, Rajnicek AM, (2009) Electrical dimensions in cell science. J Cell Sci 122: 4267-4276.
42. Bach SP, Renehan AG, Potten CS, (2000) Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 21: 469-476.
43. van der Flier LG, Clevers H, (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260.
44. Tanaka S, Terada K, Nohno T, (2011) Canonical Wnt signaling is involved in switching from cell proliferation to myogenic differentiation of mouse myoblast cells. J Mol Signal 6: 12.
45. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, et al. (1998) Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280: 596-599.
46. Yang J, Zhang W, Evans PM, Chen X, He X, et al. (2006) Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 281: 17751-17757.
47. Roediger WE, (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83: 424-429.
48. Ardawi MS, Newsholme EA, (1985) Fuel utilization in colonocytes of the rat. Biochem J 231: 713-719.
49. Leschelle X, Delpal S, Goubern M, Blottiere HM, Blachier F, (2000) Butyrate metabolism upstream and downstream acetyl-CoA synthesis and growth control of human colon carcinoma cells. Eur J Biochem 267: 6435-6442.
50. Kobayashi H, Tan EM, Fleming SE, (2003) Sodium butyrate inhibits cell growth and stimulates p21WAF1/CIP1 protein in human colonic adenocarcinoma cells independently of p53 status. Nutr Cancer 46: 202-211.
51. Kobayashi H, Tan EM, Fleming SE, (2004) Acetylation of histones associated with the p21WAF1/CIP1 gene by butyrate is not sufficient for p21WAF1/CIP1 gene transcription in human colorectal adenocarcinoma cells. Int J Cancer 109: 207-213.
52. Whitehead RH, Young GP, Bhathal PS, (1986) Effects of short chain fatty acids on a new human colon carcinoma cell line (LIM1215). Gut 27: 1457-1463.
53. Heo JI, Oh SJ, Kho YJ, Kim Jh, Kang HJ, et al. (2010) Butyrate-induced differentiation of PC12 cells to chromaffin cells involves cell adhesion and induction of extracellular proteins and cell adhesion proteins. Animal Cells and Systems 14: 261-266.
54. Comalada M, Bailon E, de Haro O, Lara-Villoslada F, Xaus J, et al. (2006) The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype. J Cancer Res Clin Oncol 132: 487-497.
55. Hodin RA, Meng S, Archer S, Tang R, (1996) Cellular growth state differentially regulates enterocyte gene expression in butyrate-treated HT-29 cells. Cell Growth Differ 7: 647-653.
56. Chirakkal H, Leech SH, Brookes KE, Prais AL, Waby JS, et al. (2006) Upregulation of BAK by butyrate in the colon is associated with increased Sp3 binding. Oncogene 25: 7192-7200.
57. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA, (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132: 1012-1017.
58. Kruh J, (1982) Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biochem 42: 65-82.
59. Davie JR, (2003) Inhibition of histone deacetylase activity by butyrate. J Nutr 133: 2485S-2493S.
60. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, et al. (2009) Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 682: 39-53.
61. Kouraklis G, Theocharis S, (2006) Histone deacetylase inhibitors: a novel target of anticancer therapy (review). Oncol Rep 15: 489-494.
62. Chen YX, Fang JY, Lu J, Qiu DK, (2004) Regulation of histone acetylation on the expression of cell cycle-associated genes in human colon cancer cell lines. Zhonghua Yi Xue Za Zhi 84: 312-317.
63. Yu DC, Waby JS, Chirakkal H, Staton CA, Corfe BM, (2010) Butyrate suppresses expression of neuropilin I in colorectal cell lines through inhibition of Sp1 transactivation. Mol Cancer 9: 276.
64. Ruemmele FM, Dionne S, Qureshi I, Sarma DS, Levy E, et al. (1999) Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP). Cell Death Differ 6: 729-735.
65. Ruemmele FM, Schwartz S, Seidman EG, Dionne S, Levy E, et al. (2003) Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut 52: 94-100.
66. Thangaraju M, Cresci GA, Liu K, Ananth S, Gnanaprakasam JP, et al. (2009) GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 69: 2826-2832.
67. Bordonaro M, Lazarova DL, Sartorelli AC, (2008) Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7: 1178-1183.
68. Scheppach W, Weiler F, (2004) The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care 7: 563-567.
69. Barrett T, Edgar R, (2006) Gene expression omnibus: microarray data storage, submission, retrieval, and analysis. Methods Enzymol 411: 352-369.
70. Hong Y, Ho KS, Eu KW, Cheah PY, (2007) A susceptibility gene set for early onset colorectal cancer that integrates diverse signaling pathways: implication for tumorigenesis. Clin Cancer Res 13: 1107-1114.
71. Hara T, Miyazaki M, Hakuno F, Takahashi S, Chida K, (2011) PKCeta promotes a proliferation to differentiation switch in keratinocytes via upregulation of p27Kip1 mRNA through suppression of JNK/c-Jun signaling under stress conditions. Cell Death Dis 2: e157.
72. Lee GY, Kenny PA, Lee EH, Bissell MJ, (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4: 359-365.