Research progress of relationship between chloride intracellular channel protein 1 and colonic cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YU Jing , ZHOU Chengji , CHENG Long ,  WANG Pan

Department of Gastrointestinal Surgery and Department of General Surgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;

Corresponding author：

WANG Pan, Email: ncwangpan@163.com

Keywords：

colonic cancer; chloride intracellular channel protein 1; tumor metastasis

DOI：

10.7507/1007-9424.201801114

Video：

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Objective To summarize research progress of relationship between chloride intracellular channel protein 1 (CLIC1) and colonic cancer. Method The related literatures in recent years on the relationship between the CLIC1 and the colonic cancer were reviewed and analyzed. Results The CLIC1 could play its physiological function as a chloride ion channel, with a wide tissue distribution and high expression in many tumor tissues. The abnormal expression of CLIC1 could result in many diseases and participate in many processes such as the occurrence, development, metastasis, and treatment of the colonic cancer. Conclusions CLIC1 might be a biomarker for early diagnosis and a target for gene therapy of colonic cancer, key genes regulated its expression, signal transduction pathways involved in occurrence and progression of colonic cancer, and interaction with other related molecules are still unclear, and further study is needed.

Citation： YU Jing, ZHOU Chengji, CHENG Long, WANG Pan. Research progress of relationship between chloride intracellular channel protein 1 and colonic cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2018, 25(9): 1141-1145. doi: 10.7507/1007-9424.201801114 Copy

1.	Jia N, Dong S, Zhao G, et al. CLIC1 overexpression is associated with poor prognosis in pancreatic ductal adenocarcinomas. J Cancer Res Ther, 2016, 12(2): 892-896.
2.	Hossain KR, Holt SA, Le Brun AP, et al. X-ray and neutron reflectivity study shows that CLIC1 undergoes cholesterol-dependent structural reorganization in lipid monolayers. Langmuir, 2017, 33(43): 12497-12509.
3.	Hossain KR, Al Khamici H, Holt SA, et al. Cholesterol promotes interaction of the protein CLIC1 with phospholipid monolayers at the air-water interface. Membranes (Basel), 2016, 6(1): pii: E15.
4.	Jones PM, Curmi PM, Valenzuela SM, et al. Computational analysis of the soluble form of the intracellular chloride ion channel protein CLIC1. Biomed Res Int, 2013, 2013: 170586.
5.	Al Khamici H, Hossain KR, Cornell BA, et al. Investigating sterol and redox regulation of the ion channel activity of CLIC1 using tethered bilayer membranes. Membranes (Basel), 2016, 6(4): pii: E51.
6.	Peter B, Ngubane NC, Fanucchi S, et al. Membrane mimetics induce helix formation and oligomerization of the chloride intracellular channel protein 1 transmembrane domain. Biochemistry, 2013, 52(16): 2739-2749.
7.	Hare JE, Goodchild SC, Breit SN, et al. Interaction of human chloride intracellular channel protein 1(CLIC1) with lipid bilayers: A fluorescence study. Biochemistry, 2016, 55(27): 3825-3833.
8.	Liu B, Billington CK, Henry AP, et al. Chloride intracellular channel 1(CLIC1) contributes to modulation of cyclic AMP-activated whole-cell chloride currents in human bronchial epithelial cells. Physiol Rep, 2018, 6(2).
9.	Agarwal A, Kasinathan A, Ganesan R, et al. Curcumin induces apoptosis and cell cycle arrest via the activation of reactive oxygen species-independent mitochondrial apoptotic pathway in Smad4 and p53 mutated colon adenocarcinoma HT29 cells. Nutr Res, 2018, 51: 67-81.
10.	Tulk BM, Kapadia S, Edwards JC. CLIC1 inserts from the aqueous phase into phospholipid membranes, where it functions as an anion channel. Am J Physiol Cell Physiol, 2002, 282(5): C1103-C1112.
11.	Littler DR, Harrop SJ, Fairlie WD, et al. The intracellular chloride ion channel protein CLIC1 undergoes a redox-controlled structural transition. J Biol Chem, 2004, 279(10): 9298-9305.
12.	Singh H, Ashley RH. Redox regulation of CLIC1 by cysteine residues associated with the putative channel pore. Biophys J, 2006, 90(5): 1628-1638.
13.	Fanucchi S, Adamson RJ, Dirr HW. Formation of an unfolding intermediate state of soluble chloride intracellular channel protein CLIC1 at acidic pH. Biochemistry, 2008, 47(44): 11674-11681.
14.	Achilonu I, Fanucchi S, Cross M, et al. Role of individual histidines in the pH-dependent global stability of human chloride intracellular channel 1. Biochemistry, 2012, 51(5): 995-1004.
15.	Gururaja Rao S, Ponnalagu D, Sukur S, et al. Identification and characterization of a bacterial homolog of chloride intracellular channel (CLIC) protein. Sci Rep, 2017, 7(1): 8500.
16.	Al Khamici H, Brown LJ, Hossain KR, et al. Members of the chloride intracellular ion channel protein family demonstrate glutaredoxin-like enzymatic activity. PLoS One, 2015, 10(1): e115699.
17.	Valenzuela SM, Alkhamici H, Brown LJ, et al. Regulation of the membrane insertion and conductance activity of the metamorphic chloride intracellular channel protein CLIC1 by cholesterol. PLoS One, 2013, 8(2): e56948.
18.	Zhu J, Xu Y, Ren G, et al. Tanshinone ⅡA sodium sulfonate regulates antioxidant system, inflammation, and endothelial dysfunction in atherosclerosis by downregulation of CLIC1. Eur J Pharmacol, 2017, 815: 427-436.
19.	Domingo-Fernández R, Coll RC, Kearney J, et al. The intracellular chloride channel proteins CLIC1 and CLIC4 induce IL-1β transcription and activate the NLRP3 inflammasome. J Biol Chem, 2017, 292(29): 12077-12087.
20.	Ulmasov B, Bruno J, Oshima K, et al. CLIC1 null mice demonstrate a role for CLIC1 in macrophage superoxide production and tissue injury. Physiol Rep, 2017, 5(5): pii: e13169.
21.	Ulmasov B, Bruno J, Woost PG, et al. Tissue and subcellular distribution of CLIC1. BMC Cell Biol, 2007, 8: 8.
22.	Wang W, Xu X, Wang W, et al. The expression and clinical significance of CLIC1 and HSP27 in lung adenocarcinoma. Tumour Biol, 2011, 32(6): 1199-1208.
23.	Wei X, Li J, Xie H, et al. Chloride intracellular channel 1 participates in migration and invasion of hepatocellular carcinoma by targeting maspin. J Gastroenterol Hepatol, 2015, 30(1): 208-216.
24.	Chen CD, Wang CS, Huang YH, et al. Overexpression of CLIC1 in human gastric carcinoma and its clinicopathological significance. Proteomics, 2007, 7(1): 155-167.
25.	Yu W, Qu H, Cao G, et al. MtHsp70-CLIC1-pulsed dendritic cells enhance the immune response against ovarian cancer. Biochem Biophys Res Commun, 2017, 494(1-2): 13-19.
26.	Setti M, Savalli N, Osti D, et al. Functional role of CLIC1 ion channel in glioblastoma-derived stem/progenitor cells. J Natl Cancer Inst, 2013, 105(21): 1644-1655.
27.	Chang YH, Wu CC, Chang KP, et al. Cell secretome analysis using hollow fiber culture system leads to the discovery of CLIC1 protein as a novel plasma marker for nasopharyngeal carcinoma. J Proteome Res, 2009, 8(12): 5465-5474.
28.	Taguchi A, Rho JH, Yan Q, et al. MAPRE1 as a plasma biomarker for early-stage colorectal cancer and adenomas. Cancer Prev Res (Phila), 2015, 8(11): 1112-1119.
29.	杨小松, 池畔. 细胞内氯离子通道蛋白1蛋白表达与结直肠癌发生、发展及预后的关系. 中国普外基础与临床杂志, 2011, 18(7): 745-749.
30.	Petrova DT, Asif AR, Armstrong VW, et al. Expression of chloride intracellular channel protein 1(CLIC1) and tumor protein D52(TPD52) as potential biomarkers for colorectal cancer. Clin Biochem, 2008, 41(14-15): 1224-1236.
31.	Albini A, Bruno A, Noonan DM, et al. Contribution to tumor angiogenesis from innate immune cells within the tumor microenvironment: implications for immunotherapy. Front Immunol, 2018, 9: 527.
32.	Pal M, Bhattacharya S, Kalyan G, et al. Cadherin profiling for therapeutic interventions in epithelial mesenchymal transition (EMT) and tumorigenesis. Exp Cell Res, 2018, 368(2): 137-146.
33.	Jentsch TJ, Lutter D, Planells-Cases R, et al. VRAC: molecular identification as LRRC8 heteromers with differential functions. Pflugers Arch, 2016, 468(3): 385-393.
34.	Hoffmann EK, Sorensen BH, Sauter DP, et al. Role of volume-regulated and calcium-activated anion channels in cell volume homeostasis, cancer and drug resistance. Channels (Austin), 2015, 9(6): 380-396.
35.	Green BJ, Panagiotakopoulou M, Pramotton FM, et al. Pore shape defines paths of metastatic cell migration. Nano Lett, 2018, 18(3): 2140-2147.
36.	Wang P, Zhang C, Yu P, et al. Regulation of colon cancer cell migration and invasion by CLIC1-mediated RVD. Mol Cell Biochem, 2012, 365(1-2): 313-321.
37.	王攀, 张超, 刘涛, 等. CLIC-1 mRNA及蛋白在结肠癌的表达及临床意义. 第三军医大学学报, 2011, 33(22): 2407-2409.
38.	Wang P, Zeng Y, Liu T, et al. Chloride intracellular channel 1 regulates colon cancer cell migration and invasion through ROS/ERK pathway. World J Gastroenterol, 2014, 20(8): 2071-2078.
39.	Gurski LA, Knowles LM, Basse PH, et al. Relocation of CLIC1 promotes tumor cell invasion and colonization of fibrin. Mol Cancer Res, 2015, 13(2): 273-280.
40.	Arnold MW. Colon cancer: The road traveled. Surg Oncol Clin N Am, 2018, 27(2): xv-xviii.
41.	Liang J, Shaulov Y, Savage-Dunn C, et al. Chloride intracellular channel proteins respond to heat stress in Caenorhabditis elegans. PLoS One, 2017, 12(9): e0184308.h.
42.	Fujimoto M, Inoue T, Kito H, et al. Transcriptional repression of HER2 by ANO1 Cl- channel inhibition in human breast cancer cells with resistance to trastuzumab. Biochem Biophys Res Commun, 2017, 482(1): 188-194.
43.	He YM, Zhang ZL, Liu QY, et al. Effect of CLIC1 gene silencing on proliferation, migration, invasion and apoptosis of human gallbladder cancer cells. J Cell Mol Med, 2018, 22(5): 2569-2579.
44.	Nanaware PP, Ramteke MP, Somavarapu AK, et al. Discovery of multiple interacting partners of gankyrin, a proteasomal chaperone and an oncoprotein-evidence for a common hot spot site at the interface and its functional relevance. Proteins, 2014, 82(7): 1283-1300.
45.	Chernet BT, Levin M. Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range. Oncotarget, 2014, 5(10): 3287-3306.
46.	Wang W, Wan M, Liao D, et al. Identification of potent chloride intracellular channel protein 1 inhibitors from traditional Chinese medicine through structure-based virtual screening and molecular dynamics analysis. Biomed Res Int, 2017, 2017: 4751780.

1. Jia N, Dong S, Zhao G, et al. CLIC1 overexpression is associated with poor prognosis in pancreatic ductal adenocarcinomas. J Cancer Res Ther, 2016, 12(2): 892-896.
2. Hossain KR, Holt SA, Le Brun AP, et al. X-ray and neutron reflectivity study shows that CLIC1 undergoes cholesterol-dependent structural reorganization in lipid monolayers. Langmuir, 2017, 33(43): 12497-12509.
3. Hossain KR, Al Khamici H, Holt SA, et al. Cholesterol promotes interaction of the protein CLIC1 with phospholipid monolayers at the air-water interface. Membranes (Basel), 2016, 6(1): pii: E15.
4. Jones PM, Curmi PM, Valenzuela SM, et al. Computational analysis of the soluble form of the intracellular chloride ion channel protein CLIC1. Biomed Res Int, 2013, 2013: 170586.
5. Al Khamici H, Hossain KR, Cornell BA, et al. Investigating sterol and redox regulation of the ion channel activity of CLIC1 using tethered bilayer membranes. Membranes (Basel), 2016, 6(4): pii: E51.
6. Peter B, Ngubane NC, Fanucchi S, et al. Membrane mimetics induce helix formation and oligomerization of the chloride intracellular channel protein 1 transmembrane domain. Biochemistry, 2013, 52(16): 2739-2749.
7. Hare JE, Goodchild SC, Breit SN, et al. Interaction of human chloride intracellular channel protein 1(CLIC1) with lipid bilayers: A fluorescence study. Biochemistry, 2016, 55(27): 3825-3833.
8. Liu B, Billington CK, Henry AP, et al. Chloride intracellular channel 1(CLIC1) contributes to modulation of cyclic AMP-activated whole-cell chloride currents in human bronchial epithelial cells. Physiol Rep, 2018, 6(2).
9. Agarwal A, Kasinathan A, Ganesan R, et al. Curcumin induces apoptosis and cell cycle arrest via the activation of reactive oxygen species-independent mitochondrial apoptotic pathway in Smad4 and p53 mutated colon adenocarcinoma HT29 cells. Nutr Res, 2018, 51: 67-81.
10. Tulk BM, Kapadia S, Edwards JC. CLIC1 inserts from the aqueous phase into phospholipid membranes, where it functions as an anion channel. Am J Physiol Cell Physiol, 2002, 282(5): C1103-C1112.
11. Littler DR, Harrop SJ, Fairlie WD, et al. The intracellular chloride ion channel protein CLIC1 undergoes a redox-controlled structural transition. J Biol Chem, 2004, 279(10): 9298-9305.
12. Singh H, Ashley RH. Redox regulation of CLIC1 by cysteine residues associated with the putative channel pore. Biophys J, 2006, 90(5): 1628-1638.
13. Fanucchi S, Adamson RJ, Dirr HW. Formation of an unfolding intermediate state of soluble chloride intracellular channel protein CLIC1 at acidic pH. Biochemistry, 2008, 47(44): 11674-11681.
14. Achilonu I, Fanucchi S, Cross M, et al. Role of individual histidines in the pH-dependent global stability of human chloride intracellular channel 1. Biochemistry, 2012, 51(5): 995-1004.
15. Gururaja Rao S, Ponnalagu D, Sukur S, et al. Identification and characterization of a bacterial homolog of chloride intracellular channel (CLIC) protein. Sci Rep, 2017, 7(1): 8500.
16. Al Khamici H, Brown LJ, Hossain KR, et al. Members of the chloride intracellular ion channel protein family demonstrate glutaredoxin-like enzymatic activity. PLoS One, 2015, 10(1): e115699.
17. Valenzuela SM, Alkhamici H, Brown LJ, et al. Regulation of the membrane insertion and conductance activity of the metamorphic chloride intracellular channel protein CLIC1 by cholesterol. PLoS One, 2013, 8(2): e56948.
18. Zhu J, Xu Y, Ren G, et al. Tanshinone ⅡA sodium sulfonate regulates antioxidant system, inflammation, and endothelial dysfunction in atherosclerosis by downregulation of CLIC1. Eur J Pharmacol, 2017, 815: 427-436.
19. Domingo-Fernández R, Coll RC, Kearney J, et al. The intracellular chloride channel proteins CLIC1 and CLIC4 induce IL-1β transcription and activate the NLRP3 inflammasome. J Biol Chem, 2017, 292(29): 12077-12087.
20. Ulmasov B, Bruno J, Oshima K, et al. CLIC1 null mice demonstrate a role for CLIC1 in macrophage superoxide production and tissue injury. Physiol Rep, 2017, 5(5): pii: e13169.
21. Ulmasov B, Bruno J, Woost PG, et al. Tissue and subcellular distribution of CLIC1. BMC Cell Biol, 2007, 8: 8.
22. Wang W, Xu X, Wang W, et al. The expression and clinical significance of CLIC1 and HSP27 in lung adenocarcinoma. Tumour Biol, 2011, 32(6): 1199-1208.
23. Wei X, Li J, Xie H, et al. Chloride intracellular channel 1 participates in migration and invasion of hepatocellular carcinoma by targeting maspin. J Gastroenterol Hepatol, 2015, 30(1): 208-216.
24. Chen CD, Wang CS, Huang YH, et al. Overexpression of CLIC1 in human gastric carcinoma and its clinicopathological significance. Proteomics, 2007, 7(1): 155-167.
25. Yu W, Qu H, Cao G, et al. MtHsp70-CLIC1-pulsed dendritic cells enhance the immune response against ovarian cancer. Biochem Biophys Res Commun, 2017, 494(1-2): 13-19.
26. Setti M, Savalli N, Osti D, et al. Functional role of CLIC1 ion channel in glioblastoma-derived stem/progenitor cells. J Natl Cancer Inst, 2013, 105(21): 1644-1655.
27. Chang YH, Wu CC, Chang KP, et al. Cell secretome analysis using hollow fiber culture system leads to the discovery of CLIC1 protein as a novel plasma marker for nasopharyngeal carcinoma. J Proteome Res, 2009, 8(12): 5465-5474.
28. Taguchi A, Rho JH, Yan Q, et al. MAPRE1 as a plasma biomarker for early-stage colorectal cancer and adenomas. Cancer Prev Res (Phila), 2015, 8(11): 1112-1119.
29. 杨小松, 池畔. 细胞内氯离子通道蛋白1蛋白表达与结直肠癌发生、发展及预后的关系. 中国普外基础与临床杂志, 2011, 18(7): 745-749.
30. Petrova DT, Asif AR, Armstrong VW, et al. Expression of chloride intracellular channel protein 1(CLIC1) and tumor protein D52(TPD52) as potential biomarkers for colorectal cancer. Clin Biochem, 2008, 41(14-15): 1224-1236.
31. Albini A, Bruno A, Noonan DM, et al. Contribution to tumor angiogenesis from innate immune cells within the tumor microenvironment: implications for immunotherapy. Front Immunol, 2018, 9: 527.
32. Pal M, Bhattacharya S, Kalyan G, et al. Cadherin profiling for therapeutic interventions in epithelial mesenchymal transition (EMT) and tumorigenesis. Exp Cell Res, 2018, 368(2): 137-146.
33. Jentsch TJ, Lutter D, Planells-Cases R, et al. VRAC: molecular identification as LRRC8 heteromers with differential functions. Pflugers Arch, 2016, 468(3): 385-393.
34. Hoffmann EK, Sorensen BH, Sauter DP, et al. Role of volume-regulated and calcium-activated anion channels in cell volume homeostasis, cancer and drug resistance. Channels (Austin), 2015, 9(6): 380-396.
35. Green BJ, Panagiotakopoulou M, Pramotton FM, et al. Pore shape defines paths of metastatic cell migration. Nano Lett, 2018, 18(3): 2140-2147.
36. Wang P, Zhang C, Yu P, et al. Regulation of colon cancer cell migration and invasion by CLIC1-mediated RVD. Mol Cell Biochem, 2012, 365(1-2): 313-321.
37. 王攀, 张超, 刘涛, 等. CLIC-1 mRNA及蛋白在结肠癌的表达及临床意义. 第三军医大学学报, 2011, 33(22): 2407-2409.
38. Wang P, Zeng Y, Liu T, et al. Chloride intracellular channel 1 regulates colon cancer cell migration and invasion through ROS/ERK pathway. World J Gastroenterol, 2014, 20(8): 2071-2078.
39. Gurski LA, Knowles LM, Basse PH, et al. Relocation of CLIC1 promotes tumor cell invasion and colonization of fibrin. Mol Cancer Res, 2015, 13(2): 273-280.
40. Arnold MW. Colon cancer: The road traveled. Surg Oncol Clin N Am, 2018, 27(2): xv-xviii.
41. Liang J, Shaulov Y, Savage-Dunn C, et al. Chloride intracellular channel proteins respond to heat stress in Caenorhabditis elegans. PLoS One, 2017, 12(9): e0184308.h.
42. Fujimoto M, Inoue T, Kito H, et al. Transcriptional repression of HER2 by ANO1 Cl- channel inhibition in human breast cancer cells with resistance to trastuzumab. Biochem Biophys Res Commun, 2017, 482(1): 188-194.
43. He YM, Zhang ZL, Liu QY, et al. Effect of CLIC1 gene silencing on proliferation, migration, invasion and apoptosis of human gallbladder cancer cells. J Cell Mol Med, 2018, 22(5): 2569-2579.
44. Nanaware PP, Ramteke MP, Somavarapu AK, et al. Discovery of multiple interacting partners of gankyrin, a proteasomal chaperone and an oncoprotein-evidence for a common hot spot site at the interface and its functional relevance. Proteins, 2014, 82(7): 1283-1300.
45. Chernet BT, Levin M. Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range. Oncotarget, 2014, 5(10): 3287-3306.
46. Wang W, Wan M, Liao D, et al. Identification of potent chloride intracellular channel protein 1 inhibitors from traditional Chinese medicine through structure-based virtual screening and molecular dynamics analysis. Biomed Res Int, 2017, 2017: 4751780.

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Research progress of relationship between chloride intracellular channel protein 1 and colonic cancer

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