Reduction of anion exchanger 2 expression induces apoptosis of human hepatocellular carcinoma cells

Molecular and Cellular Biochemistry

Volumn 327, Issue 1-2, 2009, Pages 135-144

  Hwang, Jin Ming ^a   Kao, Shao Hsuan ^a   Hsieh, Yi Hsien ^a   Li, Kuen Lin ^a   Wang, Pei Hsi ^a   Hsu, Li Song ^a   Liu, Jer Yuh ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Anion exchanger 2; Antisense oligonucleotide; Hepatocellular carcinoma

Indexed keywords

ANION TRANSPORT PROTEINS; ANTIPORTERS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION; HUMANS; LIVER NEOPLASMS; RNA, MESSENGER;

EID: 67349095907     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-009-0051-3     Document Type: Article

References (53)

1. Bosch FX, Ribes J, Borras J (1999) Epidemiology of primary liver cancer. Semin Liver Dis 19:271-285. doi: 10.1055/s-2007-1007117
2. Teo EK, Fock KM (2001) Hepatocellular carcinoma: An Asian perspective. Dig Dis 19:263-268. doi: 10.1159/000050692
3. El-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340:745-750. doi: 10.1056/ NEJM199903113401001
4. Taylor-Robinson SD, Foster GR, Arora S et al (1997) Increase in primary liver cancer in the UK, 1979-94. Lancet 350:1142-1143. doi: 10.1016/ S0140-6736(05)63789-0
5. Chao Y, Chan WK, Birkhofer MJ et al (1998) Phase II and pharmacokinetic study of paclitaxel therapy for unresectable hepatocellular carcinoma patients. Br J Cancer 78:34-39
6. Tang ZY (2001) Hepatocellular carcinoma-cause, treatment and metastasis. World J Gastroenterol 7:445-454
7. Alper SL (2002) Genetic diseases of acid-base transporters. Annu Rev Physiol 64:899-923. doi: 10.1146/annurev.physiol.64.092801.141759
8. Alper SL (2006) Molecular physiology of SLC4 anion exchangers. Exp Physiol 91:153-161. doi: 10.1113/expphysiol.2005.031765
9. Romero MF (2005) Molecular pathophysiology of SLC4 bicarbonate transporters. Curr Opin Nephrol Hypertens 14:495-501. doi: 10.1097/ 01.mnh.0000168333.01831.2c
10. Stewart AK, Kurschat CE, Burns D et al (2007) Transmembrane domain histidines contribute to regulation of AE2-mediated anion exchange by pH. Am J Physiol Cell Physiol 292:C909-C918. doi: 10.1152/ ajpcell.00265.2006
11. Tanner MJ (1997) The structure and function of band 3 (AE1): Recent developments. Mol Membr Biol 14:155-165. doi: 10.3109/09687689709048178 Review
12. Stuart-Tilley A, Sardet C, Pouyssegur J et al (1994) Immunolocalization of anion exchanger AE2 and cation exchanger NHE-1 in distinct adjacent cells of gastric mucosa. Am J Physiol 266:C559-C568
13. Alper SL, Stuart-Tilley A, Simmons CF et al (1994) The fodrin-ankyrin cytoskeleton of choroid plexus preferentially colocalizes with apical Na+ K(+)-ATPase rather than with basolateral anion exchanger AE2. J Clin Invest 93:1430-1438. doi: 10.1172/JCI117120
14. Alper SL, Rossmann H, Wilhelm S et al (1999) Expression of AE2 anion exchanger in mouse intestine. Am J Physiol 277:G321-G332
15. Stuart-Tilley AK, Shmukler BE, Brown D et al (1998) Immunolocalization and tissue-specific splicing of AE2 anion exchanger in mouse kidney. J Am Soc Nephrol 9:946-959
16. Dudeja PK, Hafez N, Tyagi S et al (1999) Expression of the Na+/H+ and Cl-/HCO-3 exchanger isoforms in proximal and distal human airways. Am J Physiol 276:L971-L978
17. Humphreys BD, Jiang L, Chernova MN et al (1995) Hypertonic activation of AE2 anion exchanger in Xenopus oocytes via NHE-mediated intracellular alkalinization. Am J Physiol 268:C201-C209
18. Fejes-Toth G, Rusvai E, Cleaveland ES et al (1998) Regulation of AE2 mRNA expression in the cortical collecting duct by acid/base balance. Am J Physiol 274:F596-F601
19. Garcia C, Montuenga LM, Medina JF et al (1998) In situ detection of AE2 anion-exchanger mRNA in the human liver. Cell Tissue Res 291:481-488. doi: 10.1007/s004410051017
20. Martinez-Anso E, Castillo JE, Diez J et al (1994) Immunohistochemical detection of chloride/bicarbonate anion exchangers in human liver. Hepatology 19:1400-1406
21. Wu TT, Hsieh YH, Wu CC et al (2006) Overexpression of anion exchanger 2 in human hepatocellular carcinoma. Chin J Physiol 49:192-198
22. Liu CJ, Hwang JM, Wu TT et al (2008) Anion exchanger inhibitor DIDS induces human poorly-differentiated malignant hepatocellular carcinoma HA22T cell apoptosis. Mol Cell Biochem 308:117-125. doi: 10.1007/ s11010-007-9619-y
23. Aden DP, Fogel A, Plotkin S et al (1979) Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 282:615-616. doi: 10.1038/282615a0
24. Alexander JJ, McElligott S, Saunders R (1978) Antibody to hepatitis B surface antigen is not cytotoxic to antigen-secreting hepatocytes. S Afr Med J 54:973-974
25. Chang C, Lin Y, Ol TW et al (1983) Induction of plasma protein secretion in a newly established human hepatoma cell line. Mol Cell Biol 3:1133-1137
26. Chuma M, Sakamoto M, Yasuda J et al (2004) Overexpression of cortactin is involved in motility and metastasis of hepatocellular carcinoma. J Hepatol 41:629-636. doi: 10.1016/j.jhep.2004.06.018
27. Farazi PA, DePinho RA (2006) Hepatocellular carcinoma pathogenesis: From genes to environment. Nat Rev Cancer 6:674-687. doi: 10.1038/nrc1934
28. Hsieh YH, Wu TT, Huang CY et al (2007) p38 mitogen-activated protein kinase pathway is involved in protein kinase Calpha-regulated invasion in human hepatocellular carcinoma cells. Cancer Res 67:4320-4327. doi: 10.1158/0008-5472.CAN-06-2486
29. Tian J, Tang Z, Xue Q (1999) Expressions of the metastasis-associated factors of a new human hepatocellular carcinoma cell line with highly metastatic potential. Zhonghua Yi Xue Za Zhi 79:470-472
30. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid dinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159. doi: 10.1016/0003-2697(87)90021-2
31. De Petro G, Tavian D, Copeta A et al (1998) Expression of urokinase-type plasminogen activator (u-PA), u-PA receptor, and tissue-type PA messenger RNAs in human hepatocellular carcinoma. Cancer Res 58:2234-2239
32. Chandra D, Liu JW, Tang DG (2002) Early mitochondrial activation and cytochrome c up-regulation during apoptosis. J Biol Chem 277:50842-50854. doi: 10.1074/jbc.M207622200
33. Kondoh N, Wakatsuki T, Ryo A et al (1999) Identification and characterization of genes associated with human hepatocellular carcinogenesis. Cancer Res 59:4990-4996
34. Ray SK, Patel SJ, Welsh CT et al (2002) Molecular evidence of apoptotic death in malignant brain tumors including glioblastoma multiforme: upregulation of calpain and caspase-3. J Neurosci Res 69:197-206. doi: 10.1002/jnr.10265
35. Denker SP, Barber DL (2002) Ion transport proteins anchor and regulate the cytoskeleton. Curr Opin Cell Biol 14:214-220. doi: 10.1016/ S0955-0674(02)00304-6
36. Reshkin SJ, Bellizzi A, Caldeira S et al (2000) Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J 14:2185-2197. doi: 10.1096/fj.00-0029com
37. Rotin D, Steele-Norwood D, Grinstein S et al (1989) Requirement of the Na+/H+ exchanger for tumor growth. Cancer Res 49:205-211
38. Di Sario A, Bendia E, Omenetti A et al (2007) Selective inhibition of ion transport mechanisms regulating intracellular pH reduces proliferation and induces apoptosis in cholangiocarcinoma cells. Dig Liver Dis 39:60-69. doi: 10.1016/j.dld.2006.07.013
39. Rich IN, Worthington-White D, Garden OA et al (2000) Apoptosis of leukemic cells accompanies reduction in intracellular pH after targeted inhibition of the Na(+)/H(+) exchanger. Blood 95:1427-1434
40. Wong P, Kleemann HW, Tannock IF (2002) Cytostatic potential of novel agents that inhibit the regulation of intracellular pH. Br J Cancer 87:238-245. doi: 10.1038/sj.bjc.6600424
41. Sanchez-Alcazar JA, Khodjakov A, Schneider E (2001) Anticancer drugs induce increased mitochondrial cytochrome c expression that precedes cell death. Cancer Res 61:1038-1044
42. Dai DL, Martinka M, Bush JA et al (2004) Reduced Apaf-1 expression in human cutaneous melanomas. Br J Cancer 91:1089-1095
43. Zlobec I, Minoo P, Baker K et al (2007) Loss of APAF-1 expression is associated with tumour progression and adverse prognosis in colorectal cancer. Eur J Cancer 43:1101-1107. doi: 10.1016/j.ejca.2007.01.029
44. Doppler W, Jaggi R, Groner B (1987) Induction of v-mos and activated Ha-ras oncogene expression in quiescent NIH 3T3 cells causes intracellular alkalinisation and cell-cycle progression. Gene 54:147-153. doi: 10.1016/0378-1119(87)90357-X
45. Martinez-Zaguilan R, Seftor EA, Seftor RE et al (1996) Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis 14:176-186. doi: 10.1007/BF00121214
46. Kraus M, Wolf B (1996) Implications of acidic tumor microenvironment for neoplastic growth and cancer treatment: A computer analysis. Tumour Biol 17:133-154
47. Montcourrier P, Mangeat PH, Valembois C et al (1994) Characterization of very acidic phagosomes in breast cancer cells and their association with invasion. J Cell Sci 107(Pt 9):2381-2391
48. Webb SD, Sherratt JA, Fish RG et al (1999) Mathematical modelling of tumour acidity: Regulation of intracellular pH. J Theor Biol 196:237-250. doi: 10.1006/jtbi.1998.0836
49. Gillies RJ, Raghunand N, Karczmar GS et al (2002) MRI of the tumor microenvironment. J Magn Reson Imaging 16:430-450. doi: 10.1002/ jmri.10181
50. Radinsky R (1995) Modulation of tumor cell gene expression and phenotype by the organ-specific metastatic environment. Cancer Metastasis Rev 14:323-338. doi: 10.1007/BF00690601
51. Izumi H, Torigoe T, Ishiguchi H et al (2003) Cellular pH regulators: potentially promising molecular targets for cancer chemotherapy. Cancer Treat Rev 29:541-549. doi: 10.1016/S0305-7372(03)00106-3
52. Lee CH, Wu CL, Shiau AL et al (2007) Hypoxia-induced cytosine deaminase gene expression for cancer therapy. Hum Gene Ther 18:27-38. doi: 10.1089/ hum.2005.239
53. Scott KA, Holdsworth H, Balkwill FR et al (2000) Exploiting changes in the tumour microenvironment with sequential cytokine and matrix metalloprotease inhibitor treatment in a murine breast cancer model. Br J Cancer 83:1538-1543. doi: 10.1054/bjoc.2000.1487