Zip4 (Slc39a4) expression is activated in hepatocellular carcinomas and functions to repress apoptosis, enhance cell cycle and increase migration

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Weaver, Benjamin P ^a,e   Zhang, Yuxia ^b   Hiscox, Stephen ^c   Guo, Grace L ^a   Apte, Udayan ^a   Taylor, Kathryn M ^c   Sheline, Christian T ^d   Wang, Li ^b   Andrews, Glen K ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FARNESOID X RECEPTOR; HYDROXYUREA; MESSENGER RNA; PROTEIN ZIP4; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INVASION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL MIGRATION; CELL STRAIN MCF 7; CONTROLLED STUDY; CULTURE MEDIUM; ESSENTIAL GENE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KNOCKOUT MOUSE; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RNA INTERFERENCE; ZINC METABOLISM;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; CATION TRANSPORT PROTEINS; CELL CYCLE; CELL MOVEMENT; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASM METASTASIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ZINC;

MAMMALIA; MUS;

EID: 78049316349     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013158     Document Type: Article

References (52)

1. Berg JM, Shi YG (1996) The galvanization of biology: A growing appreciation for the roles of zinc. Science 271: 1081-1085.
2. Lichten LA, Cousins RJ (2009) Mammalian Zinc Transporters: Nutritional and Physiologic Regulation. Annu Rev Nutr 29: 153-176.
3. Devirgiliis C, Murgia C, Danscher G, Perozzi G (2004) Exchangeable zinc ions transiently accumulate in a vesicular compartment in the yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 323: 58-64.
4. Yamasaki S, Sakata-Sogawa K, Hasegawa A, Suzuki T, Kabu K, et al. (2007) Zinc is a novel intracellular second messenger. J Cell Biol 177: 637-645.
5. Haase H, Rink L (2009) Functional Significance of Zinc-Related Signaling Pathways in Immune Cells. Annu Rev Nutr 29: 133-152.
6. Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, et al. (2009) Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 29: 2890-2901.
7. Beyersmann D, Haase H (2001) Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 14: 331-341.
8. Haase H, Maret W (2005) Fluctuations of cellular, available zinc modulate insulin signaling via inhibition of protein tyrosine phosphatases. J Trace Elem Med Biol 19: 37-42.
9. vonBulow V, Dubben S, Engelhardt G, Hebel S, Plumakers B, et al. (2007) Zinc- Dependent Suppression of TNF-{alpha} Production Is Mediated by Protein Kinase A-Induced Inhibition of Raf-1, I{kappa}B Kinase beta, and NF- {kappa}B. J Immunol 179: 4180-4186.
10. Hogstrand C, Kille P, Nicholson RI, Taylor KM (2009) Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med 15: 101-111.
11. Franklin RB, Costello LC (2009) The important role of the apoptotic effects of zinc in the development of cancers. J Cell Biochem 106: 750-757.
12. Kambe T, Weaver BP, Andrews GK (2008) The genetics of essential metal homeostasis during development. Genesis 46: 214-228.
13. Li M, Zhang Y, Liu Z, Bharadwaj U, Wang H, et al. (2007) Aberrant expression of zinc transporter ZIP4 (SLC39A4) significantly contributes to human pancreatic cancer pathogenesis and progression. Proc Natl Acad Sci U S A 104: 18636-18641.
14. Li M, Zhang Y, Bharadwaj U, Zhai QJ, Ahern CH (2009) 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 15: 5993-6001.
15. Zhang Y, Bharadwaj U, Logsdon CD, Chen C, Yao Q, et al. (2010) ZIP4 regulates pancreatic cancer cell growth by activating IL-6/STAT3 pathway through zinc finger transcription factor CREB. Clin Cancer Res 16: 1423-1430.
16. Zhang Y, Chen C, Yao Q, Li M (2010) ZIP4 upregulates the expression of neuropilin-1, vascular endothelial growth factor, and matrix metalloproteases in pancreatic cancer cell lines and xenografts. Cancer Biol Ther 9: 236-242.
17. Taylor KM, Hiscox S, Nicholson RI (2004) Zinc transporter LIV-1: a link between cellular development and cancer progression. Trends Endocrinol Metab 15: 461-463.
18. Zhao L, Chen W, Taylor KM, Cai B, Li X (2007) LIV-1 suppression inhibits HeLa cell invasion by targeting ERK1/2-Snail/Slug pathway. Biochem Biophys Res Commun 363: 82-88.
19. Kagara N, Tanaka N, Noguchi S, Hirano T (2007) Zinc and its transporter ZIP10 are involved in invasive behavior of breast cancer cells. Cancer Sci 98: 692-697.
20. Dufner-Beattie J, Weaver BP, Geiser J, Bilgen M, Larson M, et al. (2007) The mouse acrodermatitis gene Slc39a4 (ZIP4) is essential for development and heterozygosity causes hypersensitivity to zinc deficiency. Hum Mol Genet 16: 1391-1399.
21. Schmitt S, Kury S, Giraud M, Dreno B, Kharfi M, et al. (2009) An update on mutations of the SLC39A4 gene in acrodermatitis enteropathica. Hum Mutat 30: 926-933.
22. Mathews WR, Wang F, Eide DJ, Van Doren M (2005) Drosophila fear of intimacy Encodes a Zrt/IRT-like Protein (ZIP) Family Zinc Transporter Functionally Related to Mammalian ZIP Proteins. J Biol Chem 280: 787-795.
23. Yamashita S, Miyagi C, Fukada T, Kagara N, Che YS, et al. (2004) Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 429: 298-302.
24. Kim I, Morimura K, Shah Y, Yang Q, Ward JM, et al. (2007) Spontaneous hepatocarcinogenesis in farnesoid X receptor-null mice. Carcinogenesis 28: 940-946.
25. Yang F, Huang X, Yi T, Yen Y, Moore DD, et al. (2007) Spontaneous development of liver tumors in the absence of the bile acid receptor farnesoid X receptor. Cancer Res 67: 863-867.
26. Dufner-Beattie J, Wang F, Kuo YM, Gitschier J, Eide D (2003) The Acrodermatitis Enteropathica Gene ZIP4 Encodes a Tissue-specific, Zincregulated Zinc Transporter in Mice. J Biol Chem 278: 33474-33481.
27. Weaver BP, Dufner-Beattie J, Kambe T, Andrews GK (2007) Novel zincresponsive post-transcriptional mechanisms reciprocally regulate expression of the mouse Slc39a4 and Slc39a5 zinc transporters (Zip4 and Zip5). Biol Chem 388: 1301-1312.
28. Kambe T, Andrews GK (2009) Novel proteolytic processing of the ectodomain of the zinc transporter ZIP4 (Slc39a4) during zinc deficiency is inhibited by acrodermatitis enteropathica mutations. Mol Cell Biol 29: 129-139.
29. Kajstura M, Halicka HD, Pryjma J, Darzynkiewicz Z (2007) Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete "sub-G1" peaks on DNA content histograms. Cytometry A 71: 125-131.
30. Taylor KM, Vichova P, Jordan N, Hiscox S, Hendley R, et al. (2008) ZIP7- mediated intracellular zinc transport contributes to aberrant growth factor signaling in antihormone-resistant breast cancer Cells. Endocrinology 149: 4912-4920.
31. Taylor KM (2008) A distinct role in breast cancer for two LIV-1 family zinc transporters. Biochem Soc Trans 36: 1247-1251.
32. Taylor KM, Morgan HE, Smart K, Zahari NM, Pumford S, et al. (2007) The emerging role of the LIV-1 subfamily of zinc transporters in breast cancer. Mol Med 13: 396-406.
33. Wang FD, Kim BE, Dufner-Beattie J, Petris MJ, Andrews G, et al. (2004) Acrodermatitis enteropathica mutations affect transport activity, localization and zinc-responsive trafficking of the mouse ZIP4 zinc transporter. Hum Mol Genet 13: 563-571.
34. Gurusamy K (2007) Trace element concentration in primary liver cancers-a systematic review. Biol Trace Elem Res 118: 191-206.
35. Liuzzi JP, Guo L, Chang SM, Cousins RJ (2009) Kruppel-like factor 4 regulates adaptive expression of the zinc transporter Zip4 in mouse small intestine. Am J Physiol Gastrointest Liver Physiol 296: G517-G523.
36. Andrews GK (2008) Regulation and function of Zip4, the acrodermatitis enteropathica gene. Biochem Soc Trans 36: 1242-1246.
37. Chai FG, Truong-Tran AQ, Ho LH, Zalewski PD (1999) Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: A review. Immunol Cell Biol 77: 272-278.
38. Yan M, Song Y, Wong CP, Hardin K, Ho E (2008) Zinc deficiency alters DNA damage response genes in normal human prostate epithelial cells. J Nutr 138: 667-673.
39. Barthel A, Ostrakhovitch EA, Walter PL, Kampkotter A, Klotz LO (2007) Stimulation of phosphoinositide 3-kinase/Akt signaling by copper and zinc ions: mechanisms and consequences. Arch Biochem Biophys 463: 175-182.
40. Jankowski-Hennig MA, Clegg MS, Daston GP, Rogers JM, Keen CL (2000) Zinc-deficient rat embryos have increased caspase 3-like activity and apoptosis. Biochem Biophys Res Commun 271: 250-256.
41. Wilson D, Varigos G, Ackland ML (2006) Apoptosis may underlie the pathology of zinc-deficient skin. Immunol Cell Biol 84: 28-37.
42. Ryu JM, Lee MY, Yun SP, Han HJ (2009) Zinc chloride stimulates DNA synthesis of mouse embryonic stem cells: involvement of PI3K/Akt, MAPKs, and mTOR. J Cell Physiol 218: 558-567.
43. Walter PL, Kampkotter A, Eckers A, Barthel A, Schmoll D, et al. (2006) Modulation of FoxO signaling in human hepatoma cells by exposure to copper or zinc ions. Arch Biochem Biophys 454: 107-113.
44. Fukada T, Civic N, Furuichi T, Shimoda S, Mishima K, et al. (2008) The zinc transporter SLC39A13/ZIP13 is required for connective tissue development; its involvement in BMP/TGF-beta signaling pathways. PLoS ONE 3: e3642.
45. He N, Park K, Zhang Y, Huang J, Lu S, et al. (2008) Epigenetic inhibition of nuclear receptor small heterodimer partner is associated with and regulates hepatocellular carcinoma growth. Gastroenterology 134: 793-802.
46. Huang ZL, Dufner-Beattie J, Andrews GK (2006) Expression and Regulation of SLC39A Family Zinc Transporters in the Developing Mouse Intestine. Dev Biol 295: 571-579.
47. Dufner-Beattie J, Kuo YM, Gitschier J, Andrews GK (2004) The adaptive response to dietary zinc in mice involves the differential cellular localization and zinc-regulation of the zinc transporters ZIP4 and ZIP5. J Biol Chem 279: 49082-49090.
48. Andrews GK, Lee DK, Ravindra R, Lichtlen P, Sirito M, et al. (2001) The transcription factors MTF-1 and USF1 cooperate to regulate mouse metallothioneinmetallothionein- I expression in response to the essential metal zinc in visceral endoderm cells during early development. EMBO J 20: 1114-1122.
49. Langmade SJ, Ravindra R, Daniels PJ, Andrews GK (2000) The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J Biol Chem 275: 34803-34809.
50. Araki T, Sasaki Y, Milbrandt J (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305: 1010-1013.
51. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872.
52. Zhang Y, Xu P, Park K, Choi Y, Moore DD, et al. (2008) Orphan receptor small heterodimer partner suppresses tumorigenesis by modulating cyclin D1 expression and cellular proliferation. Hepatology 48: 289-298.