Mapping the zinc-transporting system in mammary cells: Molecular analysis reveals a phenotype-dependent zinc-transporting network during lactation

Journal of Cellular Physiology

Volumn 227, Issue 4, 2012, Pages 1761-1770

  Kelleher, Shannon L ^a   Velasquez, Vanessa ^a   Croxford, Thomas P ^a   McCormick, Nicholas H ^a   Lopez, Veronica ^a   Macdavid, Joshua ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER; ZIP10 PROTEIN; ZIP11 PROTEIN; ZIP3 PROTEIN; ZIP5 PROTEIN; ZIP7 PROTEIN; ZIP8 PROTEIN; ZNT2 PROTEIN; ZNT4 PROTEIN; ZNT9 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CELL; CELL COMPARTMENTALIZATION; CELL CULTURE; CIRCULATION; CONFOCAL MICROSCOPY; ENDOSOME; GENE EXPRESSION PROFILING; GOLGI COMPLEX; LACTATION; MAMMARY GLAND; MILK; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TRANSPORT; PROTEOMICS;

ANIMALS; CARRIER PROTEINS; EPITHELIAL CELLS; FEMALE; IMMUNOHISTOCHEMISTRY; LACTATION; MAMMARY GLANDS, ANIMAL; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, INBRED C57BL; MILK; MODELS, BIOLOGICAL; PHENOTYPE; PREGNANCY; RNA, MESSENGER; ZINC;

MUS;

EID: 84855724443     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22900     Document Type: Article

References (54)

1. Ackland ML, Mercer JF. 1992. The murine mutation, lethal milk, results in production of zinc-deficient milk. J Nutr 122:1214-1218.
2. Anchordoquy J, Picco S, Seoane A, Anchordoquy J, Ponzinibio M, Mattioli G, García PP, Furnus C. 2011. Analysis of apoptosis and DNA damage in bovine cumulus cells after exposure in vitro to different zinc concentrations. Cell Biol Int 35:593-597.
3. Aydemir TB, Liuzzi JP, McClellan S, Cousins RJ. 2009. Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-γ expression in activated human T cells. J Leukoc Biol 86:337-348.
4. Babina S, Kanyshkova T, Buneva V, Nevinsky G. 2004. Lactoferrin is the major deoxyribonuclease of human milk. Biochemistry 69:1006-1015.
5. Bhatnagar S, Taneja S. 2001. Zinc and cognitive development. Br J Nutr 85:S139-S145.
6. Blakeborough P, Salter D, Gurr M. 1983. Zinc binding in cow's milk and human milk. Biochem J 209:505-512.
7. Boyle K, Hadaschik D, Virtue S, Cawthorn W, Ridley S, O'Rahilly S, Siddle K. 2009. The transcription factors Egr1 and Egr2 have opposing influences on adipocyte differentiation. Cell Death Differ 16:782-789.
8. Brisken C, Rajaram R. 2006. Alveolar and lactogenic differentiation. J Mammary Gland Biol Neoplasia 11:239-248.
9. Bushway A, Park C, Keenan T. 1979. Effect of pregnancy and lactation on glycosyltransferase activities of rat mammary gland. Int J Biochem 10:147-154.
10. Chowanadisai W, Lonnerdal B, Kelleher SL. 2006. Identification of a mutation in SLC30A2 (ZnT-2) in women with low milk zinc concentration that results in transient neonatal zinc deficiency. J Biol Chem 281:39699-339707.
11. Colvin R, Holmes W, Fontaine C, Maret W. 2010. Cytosolic zinc buffering and muffling: Their role in intracellular zinc homeostasis. Metallomics 2:306-317.
12. Creamer BA, Sakamoto K, Schmidt JW, Triplett AA, Moriggl R, Wagner K-U. 2010. Stat5 promotes survival of mammary epithelial cells through transcriptional activation of a distinct promoter in akt1. Mol Cell Biol 30:2957-2970.
13. Croxford T, McCormick N, Kelleher S. 2011. Moderate zinc deficiency reduced testicular Zip6 and Zip10 abundance and impairs spermatogenesis in mice. J Nutr 141:359-365.
14. Cynis H, Rahfeld J-U, Stephan A, Kehlen A, Koch B, Wermann M, Demuth H-U, Schilling S. 2008. Isolation of an isoenzyme of human glutaminyl cyclase: Retention in the Golgi complex suggests involvement in the protein maturation machinery. J Mol Biol 379:966-980.
15. Dalziel M, Huang R, Dall'Olio F, Morris J, Taylor-Papadimitriou J, Lau J. 2001. Mouse ST6Gal sialyltransferase gene expression during mammary gland lactation. Glycobiology 11:407-412.
16. Eide DJ. 2006. Zinc transporters and the cellular trafficking of zinc. Biochimica Biophys Acta 1763:711-722.
17. Fukunaka A, Suzuki T, Kurokawa Y, Yamazaki T, Fujiwara N, Ishihara K, Migaki H, Okumura K, Masuda S, Yamaguchi-Iwai Y, Nagao M, Kambe T. 2009. Demonstration and characterization of the heterodimerization of ZnT5 and ZnT6 in the early secretory pathway. J Biol Chem 284:30798-30806.
18. Gaither LA, Eide DJ. 2000. Functional expression of the human hZIP2 zinc transporter. J Biol Chem 275:5560-5564.
19. Harzer G, Kauer H. 1980. Binding of zinc to casein. Am J Clin Nutr 35:981-987.
20. Hoac T, Lundh T, Purup S, Önning G, Sejrsen K, Åkesson B. 2007. Separation of selenium, zinc, and copper compounds in bovine whey using size exclusion chromatography linked to inductively coupled plasma mass spectrometry. J Agric Food Chem 55:4237-4243.
21. Huang L, Gitschier J. 1997. A novel gene involved in zinc transport is deficient in the lethal milk mouse. Nat Genet 17:292-297.
22. Huang L, Kirschke CP, Zhang Y, Yu YY. 2005. The ZIP7 gene (Slc39a7) encodes a zinc transporter involved in zinc homeostasis of the Golgi apparatus. J Biol Chem 280:15456-115463.
23. Jena BP. Porosome: The secretory portal in cells. Biochemistry 2009. 48:4009-4018.
24. Kasper G, Armin A, Weiser A, Rump A, Sparbier K, Dahl E, Hartmann A, Wild P, Schwidetzky U, Castaños-Vélez E, Lehmann K. 2005. Expression levels of the putative zinc transporter LIV-1 are associated with a better outcome of breast cancer patients. Int J Cancer 117:961-973.
25. Kelleher SL, Lonnerdal B. 2002. Zinc transporters in the mammary gland respond to marginal zinc and vitamin A intake during lactation in rats. J Nutr 132:3280-3285.
26. Kelleher SL, Lonnerdal B. 2003. Zn transporter levels and localization change throughout lactation in rat mammary gland and are regulated by Zn in mammary cells. J Nutr 133:3378-3385.
27. Kelleher SL, Lonnerdal B. 2005. Zip3 plays a major role in zinc uptake into mammary epithelial cells and is regulated by prolactin. Am J Physiol Cell Physiol 288:C1042-C1047.
28. Kelleher SL, Lopez V, Lonnerdal B, Dufner-Beattie J, Andrews GK. 2009. Zip3 (Slc39a3) functions in zinc reuptake from the alveolar lumen in lactating mammary gland. Am J Physiol Regul Integr Comp Physiol 297:R194-R201.
29. Lemire J, Mailloux R, Appanna VD. 2008. Zinc toxicity alters mitochondrial metabolism and leads to decreased ATP production in hepatocytes. J Appl Toxicol 28:175-182.
30. Linzell J, Mepham T, Peaker M. 1976. The secretion of citrate into milk. J Physiol 260:739-750.
31. Liuzzi JP, Bobo JA, Cui L, McMahon RJ, Cousins RJ. 2003. Zinc transporters 1, 2 and 4 are differentially expressed and localized in rats during pregnancy and lactation. J Nutr 133:342-351.
32. Liuzzi JP, Aydemir F, Nam H, Knutson MD, Cousins RJ. 2006. Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc Natl Acad Sci USA 103:13612-113617.
33. Lönnerdal B, Stanislowski A, Hurley L. 1980. Isolation of a low molecular weight zinc binding ligand from human milk. J Inorg Biochem 12:71-78.
34. Lopez V, Kelleher SL. 2009. Zinc transporter-2 (ZnT2) variants are localized to distinct sub-cellular compartments and functionally transport zinc. Biochem J 422:43-52.
35. Lopez V, Kelleher SL. 2010. Zip6-attenuation promotes epithelial-to-mesenchymal transition in ductal breast tumor (T47D) cells. Exp Cell Res 316:366-375.
36. Matsuura W, Yamazaki T, Yamaguchi-Iwai Y, Masuda S, Nagao M, Andrews G, Kambe T. 2009. SLC39A9 (ZIP9) regulates zinc homeostasis in the secretory pathway: Characterization of the ZIP subfamily I protein in vertebrate cells. Biosci Biotechnol Biochem 73:1142-1148.
37. McCormick N, Velasquez V, Finney L, Vogt S, Kelleher SL. 2010. X-Ray fluorescence microscopy reveals accumulation and secretion of discrete intracellular zinc pools in the lactating mouse mammary gland. PLoS One 5:e11078.
38. Menzies KK, Nicholas KR. 2007. The expression of [beta]-1, 3 galactosyltransferase and [beta]-1, 4 galactosyltransferase enzymatic activities in the mammary gland of the tammar wallaby (Macropus eugenii) during early lactation. Biochim Biophys Acta 1770:115-120.
39. Michalczyk A, Varigos G, Catto-Smith A, Blomeley RC, Ackland ML. 2003. Analysis of zinc transporter, hZnT4 (SIc30A4), gene expression in a mammary gland disorder leading to reduced zinc secretion into milk. Hum Genet 113:202-210.
40. Neville M. 2009. Classic Studies of Mammary Development and Milk Secretion: 1945-1980. J Mammary Gland Biol Neoplasia 14:193-197.
41. Palmiter RD, Huang L. 2004. Efflux and compartmentalizatin of zinc by members of the SLC30 family of solute carriers. Pflugers Arch 447:744-751.
42. Petris MJ, Mercer JFB. 1999. The Menkes protein (ATP7A:MNK) cycles via the plasma membrane both in basal and elevated extracellular copper using a C-termianl di-leucine endocytic signal. Hum Mol Genet 8:2107-2115.
43. Picciano M, Guthrie H. 1976. Copper, iron, and zinc contents of mature human milk. Am J Clin Nutr 29:242-254.
44. Qian L, Seo Y, Lopez V, Kelleher S. 2008. ZNT2 is regulated by prolactin through activation of the JAK2-STAT5 signaling pathway. Am J Physiol Cell Physiol 297:C369-C377.
45. Seo Y, Kelleher S. 2010. Functional analysis of two single nucleotide polymorphisms in SLC30A2 (ZnT2): Implications for mammary gland function and breast disease in women. Physiol Genomics 42A:219-227.
46. Seo Y, Lopez V, Kelleher S. 2011. A histidine-rich motif mediates mitochondrial localization of ZnT2 to modulate mitochondrial function. Am J Physiol Cell Physiol 300:C1479-C1489.
47. Shennan DB, Peaker M. 2000. Transport of milk constituents by the mammary gland. Physiological Rev 80:925-951.
48. Suzuki T, Ishihara K, Migaki H, Matsuura W, Kohda A, Okumura K, Nagao M, Yamaguchi-Iwai Y, Kambe T. 2005. 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 280:637-643.
49. Taylor KM. 2008. A distinct role in breast cancer for two LIV-1 family zinc transporters. Biochem Soc Trans 036:1247-1251.
50. Taylor KM, Morgan HE, Smart K, Zahari NM, Pumford S, Ellis IO, Robertson JF, Nicholson RI. 2007. The emerging role of the LIV-1 subfamily of zinc transporters in breast cancer. Mol Med 13:396-406.
51. Taylor KM, Vichova P, Jordan N, Hiscox S, Hendley R, Nicholson RI. 2008. ZIP7-mediated intracellular zinc transport contributes to aberrant growth factor signaling in antihormone-resistant breast cancer cells. Endocrinology 149:4912-4920.
52. Walker C, Black R. 2010. Zinc for the treatment of diarrhoea: effect on diarrhoea morbidity, mortality and incidence of future episodes. Int J Epidemiol 39:i63-i69.
53. Weaver BP, Dufner-Beattie J, Kambe T, Andrews GK. 2007. Novel zinc-responsive post-transcriptional mechanisms reciprocally regulate expression of the mouse Slc39a4 and Slc39a5 zinc transporters (Zip4 and Zip5). Biol Chem 388:1301-1312.
54. Zulak I, Keenan T. 1983. Citrate accumulation by a Golgi apparatus-rich fraction from lactating bovine mammary gland. Int J Biochem 15:747-750.