ZIP4, a novel determinant of tumor invasion in hepatocellular carcinoma, contributes to tumor recurrence after liver transplantation

International Journal of Biological Sciences

Volumn 10, Issue 3, 2014, Pages 245-256

  Xu, Xiao ^a,c   Guo, Hai Jun ^a,b   Xie, Hai Yang ^a,b   Li, Jie ^a,b   Zhuang, Run Zhou ^a,b   Ling, Qi ^a,b   Zhou, Lin ^a,b   Wei, Xu Yong ^a,b   Liu, Zhi Kun ^a,b   Ding, Song Ming ^a,b   Chen, Kang Jie ^a,b   Xu, Zhi Yuan ^a,b   Zheng, Shu Sen ^a,c  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b BEIJING HOSPITAL   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Hepatocellular carcinoma; Liver transplantation; ZIP4

Indexed keywords

CATION TRANSPORT PROTEIN; SLC39A4 PROTEIN, HUMAN;

APOPTOSIS; CASE CONTROL STUDY; CELL CYCLE; CHINA; EPIDEMIOLOGY; FEMALE; HEPG2 CELL LINE; HUMAN; LIVER; LIVER CELL CARCINOMA; LIVER TRANSPLANTATION; LIVER TUMOR; MALE; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; TUMOR INVASION; TUMOR RECURRENCE;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; CATION TRANSPORT PROTEINS; CELL CYCLE; CHINA; FEMALE; HEP G2 CELLS; HUMANS; LIVER; LIVER NEOPLASMS; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL;

EID: 84896729119     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.7401     Document Type: Article

References (50)

1. Xu ZY, Ding SM, Zhou L, et al. FOXC1 contributes to microvascular invasion in primary hepatocellular carcinoma via regulating epithelial-mesenchymal transition. Int J Biol Sci. 2012;8:1130-1141.
2. Shim JH, Lee HC, Han S, et al. Hepatocyte nuclear factor 1beta is a novel prognostic marker independent of the Milan criteria in transplantable hepatocellular carcinoma: a retrospective analysis based on tissue microarrays. Liver Transpl. 2013;19:336-345.
3. Ng KK, Lo CM, Chan SC, et al. Liver transplantation for hepatocellular carcinoma: the Hong Kong experience. J Hepatobiliary Pancreat Sci. 2010;17:548-554.
4. Ringe B, Pichlmayr R, Wittekind C, et al. Surgical treatment of hepatocellular carcinoma: experience with liver resection and transplantation in 198 patients. World J Surg. 1991;15:270-285.
5. O'Grady JG, Polson RJ, Rolles K, et al. Liver transplantation for malignant disease. Results in 93 consecutive patients. Ann Surg. 1988;207:373-379.
6. Iwatsuki S, Gordon RD, Shaw BW, Jr. et al. Role of liver transplantation in cancer therapy. Ann Surg. 1985;202:401-407.
7. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334:693-699.
8. Volk ML, Vijan S, Marrero JA. A novel model measuring the harm of transplanting hepatocellular carcinoma exceeding Milan criteria. Am J Transplant. 2008;8:839-846.
9. Lei J, Yan L. Outcome comparisons among the Hangzhou, Chengdu, and UCSF criteria for hepatocellular carcinoma liver transplantation after successful downstaging therapies. J Gastrointest Surg. 2013;17:1116-1122.
10. Malago M, Sotiropoulos GC, Nadalin S et al. Living donor liver transplantation for hepatocellular carcinoma: a single-center preliminary report. Liver Transpl. 2006;12:934-940.
11. Gondolesi GE, Roayaie S, Munoz L, et al. Adult living donor liver transplantation for patients with hepatocellular carcinoma: extending UNOS priority criteria. Ann Surg. 2004;239:142-149.
12. Roayaie S, Frischer JS, Emre SH, et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters. Ann Surg. 2002;235:533-539.
13. Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology. 2001;33:1394-1403.
14. Liuzzi JP, Cousins RJ. Mammalian zinc transporters. Annu Rev Nutr. 2004;24:151-172.
15. Kim BE, Wang F, Dufner-Beattie J, et al. Zn2+-stimulated endocytosis of the mZIP4 zinc transporter regulates its location at the plasma membrane. J Biol Chem. 2004;279:4523-4530.
16. Liuzzi JP, Bobo JA, Lichten LA, et al. Responsive transporter genes within the murine intestinal-pancreatic axis form a basis of zinc homeostasis. Proc Natl Acad Sci U S A. 2004;101:14355-14360.
17. Eide DJ. The SLC39 family of metal ion transporters. Pflugers Arch. 2004;447:796-800.
18. Guerinot ML. The ZIP family of metal transporters. Biochim Biophys Acta. 2000;1465:190-198.
19. Murgia C, Vespignani I, Rami R, et al. The Znt4 mutation inlethal milk mice affects intestinal zinc homeostasis through the expression of other Zn transporters. Genes Nutr. 2006;1:61-70.
20. Taylor KM, Morgan HE, Johnson A, et al. Structure-function analysis of LIV-1, the breast cancer-associated protein that belongs to a new subfamily of zinc transporters. Biochem J. 2003;375:51-59.
21. Hogstrand C, Kille P, Nicholson RI, et al. Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med. 2009;15:101-111.
22. Zhao L, Chen W, Taylor KM, et al. LIV-1 suppression inhibits HeLa cell invasion by targeting ERK1/2-Snail/Slug pathway. Biochem Biophys Res Commun. 2007;363:82-88.
23. Taylor KM, Hiscox S, Nicholson RI. Zinc transporter LIV-1: a link between cellular development and cancer progression. Trends Endocrinol Metab. 2004;15:461-463.
24. Kagara N, Tanaka N, Noguchi S, et al. Zinc and its transporter ZIP10 are involved in invasive behavior of breast cancer cells. Cancer Sci. 2007;98:692-697.
25. Mao X, Kim BE, Wang F, et al. A histidine-rich cluster mediates the ubiquitination and degradation of the human zinc transporter, hZIP4, and protects against zinc cytotoxicity. J Biol Chem. 2007;282:6992-7000.
26. Dufner-Beattie J, Weaver BP, Geiser J, et al. The mouse acrodermatitis enteropathica gene Slc39a4 (Zip4) is essential for early development and heterozygosity causes hypersensitivity to zinc deficiency. Hum Mol Genet. 2007;16:1391-1399.
27. Wang FD, Kim BE, Dufner-Beattie J, et al. Acrodermatitis enteropathica mutations affect transport activity, localization and zinc-responsive trafficking of the mouse ZIP4 zinc transporter. Hum Mol Genet. 2004;13:563-571.
28. Dufner-Beattie J, Wang F, Kuo YM et al. The acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J Biol Chem. 2003;278:33474-33481.
29. Dufner-Beattie J, Langmade SJ, Wang F, et al. Structure, function, and regulation of a subfamily of mouse zinc transporter genes. J Biol Chem. 2003;278:50142-50150.
30. Kury S, Dreno B, Bezieau S, et al. Identification of SLC39A4, a gene involved in acrodermatitis enteropathica. Nat Genet. 2002;31:239-240.
31. Kury S, Devilder MC, Avet-Loiseau H, et al. Expression pattern, genomic structure and evaluation of the human SLC30A4 gene as a candidate for acrodermatitis enteropathica. Hum Genet. 2001;109:178-185.
32. Li M, Zhang Y, Bharadwaj U, et al. Down-regulation of ZIP4 by RNA interference inhibits pancreatic cancer growth and increases the survival of nude mice with pancreatic cancer xenografts. Clin Cancer Res. 2009;15:5993-6001.
33. Li M, Zhang Y, Liu Z, et al. Aberrant expression of zinc transporter ZIP4 (SLC39A4) significantly contributes to human pancreatic cancer pathogenesis and progression. Proc Natl Acad Sci U S A. 2007;104:18636-18641.
34. Zhang Y, Bharadwaj U, Logsdon CD, et al. ZIP4 regulates pancreatic cancer cell growth by activating IL-6/STAT3 pathway through zinc finger transcription factor CREB. Clin Cancer Res. 2010;16:1423-1430.
35. Chen QG, Zhang Z, Yang Q, et al. The role of zinc transporter ZIP4 in prostate carcinoma. Urol Oncol. 2011.
36. Weaver BP, Zhang Y, Hiscox S, et al. Zip4 (Slc39a4) expression is activated in hepatocellular carcinomas and functions to repress apoptosis, enhance cell cycle and increase migration. PLoS One. 2010;5.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
38. Cheng J, Xie HY, Xu X, et al. NDRG1 as a biomarker for metastasis, recurrence and of poor prognosis in hepatocellular carcinoma. Cancer Lett. 2011;310:35-45.
39. Wittekind C. [The new WHO classification of liver tumors--what is really new?]. Verh Dtsch Ges Pathol. 2001;85:212-218.
40. Greene FL. American Joint Committee on Cancer., American Cancer Society. AJCC cancer staging handbook: from the AJCC cancer staging manual. 6th ed. New York: Springer, 2002.
41. Chen KJ, Lin SZ, Zhou L, et al. Selective recruitment of regulatory T cell through CCR6-CCL20 in hepatocellular carcinoma fosters tumor progression and predicts poor prognosis. PLoS One. 2011;6:e24671.
42. Yau WL, Lam CS, Ng L, et al. Over-Expression of miR-106b Promotes Cell Migration and Metastasis in Hepatocellular Carcinoma by Activating Epithelial-Mesenchymal Transition Process. PLoS One. 2013;8:e57882.
43. Xue YJ, Xiao RH, Long DZ, et al. Overexpression of FoxM1 is associated with tumor progression in patients with clear cell renal cell carcinoma. J Transl Med. 2012;10:200.
44. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57-70.
45. Marsh JW, Dvorchik I, Bonham CA et al. Is the pathologic TNM staging system for patients with hepatoma predictive of outcome? Cancer. 2000;88:538-543.
46. Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: comparison of the proposed UCSF criteria with the Milan criteria and the Pittsburgh modified TNM criteria. Liver Transpl. 2002;8:765-774.
47. Ma XJ, Patel R, Wang X, et al. Molecular classification of human cancers using a 92-gene real-time quantitative polymerase chain reaction assay. Arch Pathol Lab Med. 2006;130:465-473.
48. Taylor KM, Morgan HE, Smart K, et al. The emerging role of the LIV-1 subfamily of zinc transporters in breast cancer. Mol Med. 2007;13:396-406.
49. Huang L, Kirschke CP, Zhang Y et al. The ZIP7 gene (Slc39a7) encodes a zinc transporter involved in zinc homeostasis of the Golgi apparatus. J Biol Chem. 2005;280:15456-15463.
50. Wang F, Dufner-Beattie J, Kim BE, et al. Zinc-stimulated endocytosis controls activity of the mouse ZIP1 and ZIP3 zinc uptake transporters. J Biol Chem. 2004;279:24631-24639.