Overexpression of the ZIP1 zinc transporter induces an osteogenic phenotype in mesenchymal stem cells

Bone

Volumn 38, Issue 2, 2006, Pages 181-198

  Tang, Zhihui ^a   Sahu, Surasri Nandan ^a   Khadeer, Mohammed Abdul ^a   Bai, Guang ^a   Franklin, Renty B ^a   Gupta, Anandarup ^a  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

ALP, alkaline phosphatase; AR, Alizarin red; BGM, basal growth medium; LIV 1; MSCs, mesenchymal stem cells; OPN, osteopontin; OSM, osteogenic medium; rAd, recombinant adenovirus; ZIP1, Zrt Irt like protein

Indexed keywords

ALIZARIN RED S; ALKALINE PHOSPHATASE; COMPLEMENTARY DNA; OSTEOPONTIN; SIALOPROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX2; ZINC TRANSPORTER;

ARTICLE; BREAST CANCER; CANCER CELL; CELL DIFFERENTIATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PHENOTYPE; PROMYELOCYTIC LEUKEMIA; UNINDEXED SEQUENCE;

EID: 31544464940     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2005.08.010     Document Type: Article

References (56)

1. D. Beyersmann, and H. Haase Functions of zinc in signaling, proliferation and differentiation of mammalian cells Biometals 14 2001 331 341
2. L. Rink, and P. Gabriel Zinc and the immune system Proc. Nutr. Soc. 59 2000 541 552
3. J.K. Chesters Biochemical functions of zinc in animals World Rev. Nutr. Diet. 32 1978 135 164
4. M. Andrews, and C. Gallagher-Allred The role of zinc in wound healing Adv. Wound Care 12 1999 137 138
5. J. Eberle, S. Schmidmayer, R.G. Erben, M. Stangassinger, and H.P. Roth Skeletal effects of zinc deficiency in growing rats J. Trace Elem. Med. Biol. 13 1999 21 26
6. Y. Nishi Zinc and growth J. Am. Coll. Nutr. 15 1996 340 344
7. E.M. Alhava, H. Olkkonen, J. Puittinen, and V.M. Nokso-Koivisto Zinc content of human cancellous bone Acta Orthop. Scand. 48 1977 1 4
8. J. Ovesen, B. Moller-Madsen, J.S. Thomsen, G. Danscher, and L. Mosekilde The positive effects of zinc on skeletal strength in growing rats Bone 29 2001 565 570
9. S. Gomez, R. Rizzo, M. Pozzi-Mucelli, E. Bonucci, and F. Vittur Zinc mapping in bone tissues by histochemistry and synchrotron radiation-induced X-ray emission: correlation with the distribution of alkaline phosphatase Bone 25 1999 33 38
10. N. Tsuzuike, Y. Segawa, E. Tagashira, and M. Yamaguchi β-alanyl-l-histidinato zinc enhances various bone-regulating factors' effects on bone alkaline phosphatase activity in tissue culture Pharmacology 47 1993 66 72
11. M. Hashizume, and M. Yamaguchi Effect of β-alanyl-l-histidinato zinc on differentiation of osteoblastic MC3T3-E1 cells: increases in alkaline phosphatase activity and protein concentration Mol. Cell. Biochem. 131 1994 19 24
12. M. Yamaguchi, and K. Ozaki A new zinc compound, β-alanyl-l- histidinato zinc, stimulates bone growth in weanling rats Res. Exp. Med. (Berl) 190 1990 105 110
13. T. Matsui, and M. Yamaguchi Zinc modulation of insulin-like growth factor's effect in osteoblastic MC3T3-E1 cells Peptides 16 1995 1063 1068
14. T. Takada, N. Suzuki, E. Ito-Kato, Y. Noguchi, M. Ito, and M. Maeno Effect of β-alanyl-l-histidinato zinc on the differentiation of C2C12 cells Life Sci. 76 2004 509 520
15. J.P. Rodriguez, and G. Rosselot Effects of zinc on cell proliferation and proteoglycan characteristics of epiphyseal chondrocytes J. Cell. Biochem. 82 2001 501 511
16. M. Yamaguchi β-alanyl-l-histidinato zinc and bone resorption Gen. Pharmacol. 26 1995 1179 1183
17. S. Kishi, and M. Yamaguchi Inhibitory effect of zinc compounds on osteoclast-like cell formation in mouse marrow cultures Biochem. Pharmacol. 48 1994 1225 1230
18. B.S. Moonga, and D.W. Dempster Zinc is a potent inhibitor of osteoclastic bone resorption in vitro J. Bone Miner. Res. 10 1995 453 457
19. M.L. Guerinot The ZIP family of metal transporters Biochim. Biophys. Acta 1465 2000 190 198
20. C.E. Outten, and T.V. O'Halloran Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis Science 292 2001 2488 2492
21. K.M. Taylor, and R.I. Nicholson The LZT proteins; the LIV-1 subfamily of zinc transporters Biochim. Biophys. Acta 1611 2003 16 30
22. R.D. Palmiter, T.B. Cole, and S.D. Findley ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration EMBO J. 15 1996 1784 1791
23. R. Nath, R. Kambadur, S. Gulati, V.K. Paliwal, and M. Sharma Molecular aspects, physiological function, and clinical significance of metallothioneins Crit. Rev. Food Sci. Nutr. 27 1988 41 85
24. K. Inoue, K. Matsuda, M. Itoh, H. Kawaguchi, H. Tomoike, and T. Aoyagi Osteopenia and male-specific sudden cardiac death in mice lacking a zinc transporter gene, Znt5 Hum. Mol. Genet. 11 2002 1775 1784
25. T. Suzuki, K. Ishihara, H. Migaki, W. Matsuura, A. Kohda, and K. Okumura Zinc transporters, ZnT5 and ZnT7, are required for the activation of alkaline phosphatases, zinc-requiring enzymes that are glycosylphosphatidylinositol- anchored to the cytoplasmic membrane J. Biol. Chem. 280 2005 637 643
26. L.A. Gaither, and D.J. Eide The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells J. Biol. Chem. 276 2001 22258 22264
27. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
28. L.C. Costello, Y. Liu, R.B. Franklin, and M.C. Kennedy Zinc inhibition of mitochondrial aconitase and its importance in citrate metabolism of prostate epithelial cells J. Biol. Chem. 272 1997 28875 28881
29. R.B. Franklin, J. Ma, J. Zou, Z. Guan, B.I. Kukoyi, and P. Feng Human ZIP1 is a major zinc uptake transporter for the accumulation of zinc in prostate cells J. Inorg. Biochem. 96 2003 435 442
30. K.M. Taylor, H.E. Morgan, A. Johnson, L.J. Hadley, and R.I. Nicholson Structure-function analysis of LIV-1, the breast cancer-associated protein that belongs to a new subfamily of zinc transporters J. Biochem. 375 2003 51 59
31. R.D. Anderson, R.E. Haskell, H. Xia, B.J. Roessler, and B.L. Davidson A simple method for the rapid generation of recombinant adenovirus vectors Gene Ther. 7 2000 1034 1038
32. A. Liu, P.W. Hoffman, W. Lu, and G. Bai NF-κB site interacts with Sp factors and up-regulates the NR1 promoter during neuronal differentiation J. Biol. Chem. 279 2004 17449 17458
33. C.A. Gregory, W.G. Gunn, A. Peister, and D.J. Prockop An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction Anal. Biochem. 329 2004 77 84
34. A. Liu, Z. Zhuang, P.W. Hoffman, and G. Bai Functional analysis of the rat N-methyl-d-aspartate receptor 2A promoter: multiple transcription starts points, positive regulation by Sp factors, and translational regulation J. Biol. Chem. 278 2003 26423 26434
35. H. Hackl, F.S. Cabo, A. Sturn, O. Wolkenhauer, and Z. Trajanoski Analysis of DNA microarray data Curr. Top Med. Chem. 4 2004 1357 1370
36. K.M. Taylor, S. Hiscox, and R.I. Nicholson Zinc transporter LIV-1: a link between cellular development and cancer progression Trends Endocrinol. Metab. 15 2004 461 463
37. B. Milon, D. Dhermy, D. Pountney, M. Bourgeois, and C. Beaumont Differential subcellular localization of hZip1 in adherent and non-adherent cells FEBS Lett. 507 2001 241 246
38. F. Wang, J. Dufner-Beattie, B.E. Kim, M.J. Petris, G. Andrews, and D.J. Eide Zinc-stimulated endocytosis controls activity of the mouse ZIP1 and ZIP3 zinc uptake transporters J. Biol. Chem. 279 2004 24631 24639
39. C.P. Kirschke, and L. Huang ZnT7, a novel mammalian zinc transporter, accumulates zinc in the Golgi apparatus J. Biol. Chem. 278 2003 4096 4102
40. C.A. Simmons, S. Matlis, A.J. Thornton, S. Chen, C.Y. Wang, and D.J. Mooney Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway J. Biomech. 36 2003 1087 1096
41. R. Ikeda, K. Yoshida, S. Tsukahara, Y. Sakamoto, H. Tanaka, and K. Furukawa The promyelotic leukemia zinc finger promotes osteoblastic differentiation of human mesenchymal stem cells as an upstream regulator of CBFA1 J. Biol. Chem. 280 2005 8523 8530
42. P. Bianco, M. Riminucci, S. Gronthos, and P.G. Robey Bone marrow stromal stem cells: nature, biology, and potential applications Stem Cells 19 2001 180 192
43. M. Doi, A. Nagano, and Y. Nakamura Genome-wide screening by cDNA microarray of genes associated with matrix mineralization by human mesenchymal stem cells in vitro Biochem. Biophys. Res. Commun. 290 2002 381 390
44. F. Liu, L. Malaval, and J.E. Aubin Global amplification polymerase chain reaction reveals novel transitional stages during osteoprogenitor differentiation J. Cell Sci. 116 2003 1787 1796
45. R. Zohar, S. Cheifetz, C.A. McCulloch, and J. Sodek Analysis of intracellular osteopontin as a marker of osteoblastic cell differentiation and mesenchymal cell migration Eur. J. Oral Sci. 106 Suppl. 1 1998 401 407
46. J.D. Termine, H.K. Kleinman, S.W. Whitson, K.M. Conn, M.L. McGarvey, and G.R. Martin Osteonectin, a bone-specific protein linking mineral to collagen Cell 26 1981 99 105
47. W. Yang, S.J. Hyllner, and S. Christakos Interrelationship between signal transduction pathways and 1,25(OH)2D3 in UMR106 osteoblastic cells Am. J. Physiol. Endocrinol. Metab. 281 2001 E162 E170
48. W. Lutz, M.F. Burritt, D.E. Nixon, P.C. Kao, and R. Kumar Zinc increases the activity of vitamin D-dependent promoters in osteoblasts Biochem. Biophys. Res. Commun. 271 2000 1 7
49. A. Oshima, H. Tanabe, T. Yan, G.N. Lowe, C.A. Glackin, and A. Kudo A novel mechanism for the regulation of osteoblast differentiation: transcription of periostin, a member of the fasciclin I family, is regulated by the bHLH transcription factor, twist J. Cell. Biochem. 86 2002 792 804
50. J. Litvin, A.H. Selim, M.O. Montgomery, K. Lehmann, M.C. Rico, and H. Devlin Expression and function of periostin-isoforms in bone J. Cell. Biochem. 92 2004 1044 1061
51. F. Lecanda, P.M. Warlow, S. Sheikh, F. Furlan, T.H. Steinberg, and R. Civitelli Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction J. Cell. Biol. 151 2000 931 944
52. J.P. Stains, and R. Civitelli Cell-to-cell interactions in bone Biochem. Biophys. Res. Commun. 328 2005 721 727
53. P. Bialek, B. Kern, X. Yang, M. Schrock, D. Sosic, and N. Hong A twist code determines the onset of osteoblast differentiation Dev. Cell 6 2004 423 435
54. J.P. Rodriguez, S. Rios, and M. Gonzalez Modulation of the proliferation and differentiation of human mesenchymal stem cells by copper J. Cell. Biochem. 85 2002 92 100
55. E.E. Golub Enzymes in mineralizing systems: state of the art Connect Tissue Res. 35 1996 183 188
56. R.J. Majeska, J.T. Ryaby, and T.A. Einhorn Direct modulation of osteoblastic activity with estrogen J. Bone Jt. Surg. Am. 76 1994 713 721