Nutrient transport in the mammary gland: Calcium, trace minerals and water soluble vitamins

Journal of Mammary Gland Biology and Neoplasia

Volumn 19, Issue 1, 2014, Pages 73-90

  Montalbetti, Nicolas ^a   Dalghi, Marianela G ^a   Albrecht, Christiane ^a   Hediger, Matthias A ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

ABC transporters; Calcium transporters and breast cancer; SLC transporters

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; CARRIER PROTEIN; FERROPORTIN 1; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; TRACE ELEMENT; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; VITAMIN; WATER SOLUBLE VITAMIN;

ARTICLE; BASOLATERAL MEMBRANE; BREAST CANCER; BREAST EPITHELIUM; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; HUMAN; IRON TRANSPORT; MAMMARY GLAND; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MINERALS; TRACE ELEMENTS; VITAMINS;

EID: 84896490783     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-014-9317-9     Document Type: Article

References (174)

1. Fromter E, Diamond J. Route of passive ion permeation in epithelia. Nat New Biol. 1972;235(53):9-13.
2. Itoh M, Bissell MJ. The organization of tight junctions in epithelia: implications for mammary gland biology and breast tumorigenesis. J Mammary Gland Biol Neoplasia. 2003;8(4):449-62.
3. Nguyen DA, Neville MC. Tight junction regulation in the mammary gland. J Mammary Gland Biol Neoplasia. 1998;3(3):233-46.
4. McManaman JL, Neville MC. Mammary physiology and milk secretion. Adv Drug Deliv Rev. 2003;55(5):629-41.
5. Neville MC et al. Studies in human lactation - milk volume and nutrient composition during weaning and lactogenesis. Am J Clin Nutr. 1991;54(1):81-92.
6. Neville MC, Peaker M. Secretion of calcium and phosphorus into milk. J Physiol Lond. 1979;290(May):59-67.
7. Neville MC, Peaker M. Calcium fluxes in mouse mammary tissue in vitro: intracellular and extracellular calcium pools. J Physiol. 1982;323:497-517.
8. Shennan DB, Peaker M. Transport of milk constituents by the mammary gland. Physiol Rev. 2000;80(3):925-51.
9. Gao B et al. Functional properties of a new voltage-dependent calcium channel alpha(2)delta auxiliary subunit gene (CACNA2D2). J Biol Chem. 2000;275(16):12237-42.
10. Bertolesi GE et al. The Ca(2+) channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxic mechanisms. Mol Pharmacol. 2002;62(2):210-9.
11. Baldi C, Vazquez G, Boland R. Capacitative calcium influx in human epithelial breast cancer and non-tumorigenic cells occurs through Ca2+ entry pathways with different permeabilities to divalent cations. J Cell Biochem. 2003;88(6):1265-72.
12. Hoenderop JG et al. Molecular identification of the apical Ca2+ channel in 1, 25-dihydroxyvitamin D3-responsive epithelia. J Biol Chem. 1999;274(13):8375-8.
13. Peng JB et al. Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption. J Biol Chem. 1999;274(32):22739-46.
14. Hoenderop JG et al. Function and expression of the epithelial Ca(2+) channel family: comparison of mammalian ECaC1 and 2. J Physiol. 2001;537(Pt 3):747-61.
15. Loffing J et al. Distribution of transcellular calcium and sodium transport pathways along mouse distal nephron. Am J Physiol Renal Physiol. 2001;281(6):F1021-7.
16. Zhuang L et al. Calcium-selective ion channel, CaT1, is apically localized in gastrointestinal tract epithelia and is aberrantly expressed in human malignancies. Lab Invest. 2002;82(12):1755-64.
17. Sudlow AW, Burgoyne RD. A hypo-osmotically induced increase in intracellular Ca2+ in lactating mouse mammary epithelial cells involving Ca2+ influx. Pflugers Arch. 1997;433(5):609-16.
18. Enomoto K et al. Mechanically induced electrical responses in murine mammary epithelial cells in primary culture. FEBS Lett. 1987;223(1):82-6.
19. Enomoto K et al. Mechanically induced electrical and intracellular calcium responses in normal and cancerous mammary cells. Cell Calcium. 1992;13(8):501-11.
20. Enomoto K et al. Proliferation-associated increase in sensitivity of mammary epithelial cells to inositol-1,4,5-trisphosphate. Cell Biochem Funct. 1993;11(1):55-62.
21. Flezar M, Heisler S. P2-purinergic receptors in human breast tumor cells: coupling of intracellular calcium signaling to anion secretion. J Pharmacol Exp Ther. 1993;265(3):1499-510.
22. VanHouten JN, Neville MC, Wysolmerski JJ. The calcium-sensing receptor regulates plasma membrane calcium adenosine triphosphatase isoform 2 activity in mammary epithelial cells: a mechanism for calcium-regulated calcium transport into milk. Endocrinology. 2007;148(12):5943-54.
23. Buxton IL, Yokdang N, Matz RM. Purinergic mechanisms in breast cancer support intravasation, extravasation and angiogenesis. Cancer Lett. 2010;291(2):131-41.
24. Neville MC et al. Calcium partitioning in human and bovine milk. J Dairy Sci. 1994;77(7):1964-75.
25. Van Baelen K et al. The Ca2+/Mn2+ pumps in the Golgi apparatus. Biochim Biophys Acta. 2004;1742(1-3):103-12.
26. Wuytack F, Raeymaekers L, Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium. 2002;32(5-6):279-305.
27. Wootton LL et al. The expression, activity and localisation of the secretory pathway Ca2+-ATPase (SPCA1) in different mammalian tissues. Biochim Biophys Acta. 2004;1664(2):189-97.
28. Vanoevelen J et al. The secretory pathway Ca2+/Mn2+-ATPase 2 is a Golgi-localized pump with high affinity for Ca2+ ions. J Biol Chem. 2005;280(24):22800-8.
29. Hu Z et al. Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat Genet. 2000;24(1):61-5.
30. Faddy HM et al. Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem Biophys Res Commun. 2008;369(3):977-81.
31. Reinhardt TA et al. Ca(2+)-ATPase protein expression in mammary tissue. Am J Physiol Cell Physiol. 2000;279(5):C1595-602.
32. Duncan JS, Burgoyne RD. Characterization of the effects of Ca2+ depletion on the synthesis, phosphorylation and secretion of caseins in lactating mammary epithelial cells. Biochem J. 1996;317(Pt 2):487-93.
33. Ginger MR, Grigor MR. Comparative aspects of milk caseins. Comp Biochem Physiol B Biochem Mol Biol. 1999;124(2):133-45.
34. Oda K. Calcium depletion blocks proteolytic cleavages of plasma protein precursors which occur at the Golgi and/or trans-Golgi network. Possible involvement of Ca(2+)-dependent Golgi endoproteases. J Biol Chem. 1992;267(24):17465-71.
35. Taylor RS et al. Characterization of the Golgi complex cleared of proteins in transit and examination of calcium uptake activities. Mol Biol Cell. 1997;8(10):1911-31.
36. Reinhardt TA et al. Null mutation in the gene encoding plasma membrane Ca2+-ATPase isoform 2 impairs calcium transport into milk. J Biol Chem. 2004;279(41):42369-73.
37. James P et al. Identification and primary structure of a calmodulin binding domain of the Ca2+ pump of human erythrocytes. J Biol Chem. 1988;263(6):2905-10.
38. Reinhardt TA, Horst RL. Ca2+-ATPases and their expression in the mammary gland of pregnant and lactating rats. Am J Physiol. 1999;276(4 Pt 1):C796-802.
39. Strehler EE, Zacharias DA. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev. 2001;81(1):21-50.
40. Jackisch C et al. Delayed micromolar elevation in intracellular calcium precedes induction of apoptosis in thapsigargin-treated breast cancer cells. Clin Cancer Res. 2000;6(7):2844-50.
41. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4(7):517-29.
42. Carafoli E et al. Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol. 2001;36(2):107-260.
43. Michalak M, Mariani P, Opas M. Calreticulin, a multifunctional Ca2+ binding chaperone of the endoplasmic reticulum. Biochem Cell Biol. 1998;76(5):779-85.
44. Lin P et al. The mammalian calcium-binding protein, nucleobindin (CALNUC), is a Golgi resident protein. J Cell Biol. 1998;141(7):1515-27.
45. Lin P et al. Overexpression of CALNUC (nucleobindin) increases agonist and thapsigargin releasable Ca2+ storage in the Golgi. J Cell Biol. 1999;145(2):279-89.
46. Bolanz KA, Hediger MA, Landowski CP. The role of TRPV6 in breast carcinogenesis. Mol Cancer Ther. 2008;7(2):271-9.
47. Lee WJ et al. Expression of plasma membrane calcium pump isoform mRNAs in breast cancer cell lines. Cell Signal. 2002;14(12):1015-22.
48. Dhennin-Duthille I et al. High expression of transient receptor potential channels in human breast cancer epithelial cells and tissues: correlation with pathological parameters. Cell Physiol Biochem. 2011;28(5):813-22.
49. Li M et al. Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proc Natl Acad Sci U S A. 1997;94(7):3425-30.
50. VanHouten J et al. PMCA2 regulates apoptosis during mammary gland involution and predicts outcome in breast cancer. Proc Natl Acad Sci U S A. 2010;107(25):11405-10.
51. Peters AA et al. Calcium channel TRPV6 as a potential therapeutic target in estrogen receptor-negative breast cancer. Mol Cancer Ther. 2012;11(10):2158-68.
52. Lonnerdal B. Effects of maternal dietary intake on human milk composition. J Nutr. 1986;116(4):499-513.
53. Siimes MA, Vuori E, Kuitunen P. Breast milk iron-A declining concentration during the course of lactation. Acta Paediatr Scand. 1979;68(1):29-31.
54. Vaughan LA, Weber CW, Kemberling SR. Longitudinal changes in the mineral content of human milk. Am J Clin Nutr. 1979;32(11):2301-6.
55. Keen CL et al. Developmental changes in composition of rat milk: trace elements, minerals, protein, carbohydrate and fat. J Nutr. 1981;111(2):226-36.
56. Lonnerdal B. Copper nutrition during infancy and childhood. Am J Clin Nutr. 1998;67(5 Suppl):1046S-53S.
57. Krebs NF et al. The effects of a dietary zinc supplement during lactation on longitudinal changes in maternal zinc status and milk zinc concentrations. Am J Clin Nutr. 1985;41(3):560-70.
58. Domellof M et al. Iron, zinc, and copper concentrations in breast milk are independent of maternal mineral status. Am J Clin Nutr. 2004;79(1):111-5.
59. Hannan MA et al. Maternal milk concentration of zinc, iron, selenium, and iodine and its relationship to dietary intakes. Biol Trace Elem Res. 2009;127(1):6-15.
60. Vuori E et al. The effects of the dietary intakes of copper, iron, manganese, and zinc on the trace element content of human milk. Am J Clin Nutr. 1980;33(2):227-31.
61. Griffin IJ, Abrams SA. Iron and breastfeeding. Pediatr Clin North Am. 2001;48(2):401-13.
62. Dallman PR. Progress in the prevention of iron deficiency in infants. Acta Paediatr Scand Suppl. 1990;365:28-37.
63. Casey C, SAa.ZP. Handbook of milk composition. Academic Press;1995
64. Ohgami RS et al. Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat Genet. 2005;37(11):1264-9.
65. Knutson MD. Steap proteins: implications for iron and copper metabolism. Nutr Rev. 2007;65(7):335-40.
66. Lambe T et al. Identification of a Steap3 endosomal targeting motif essential for normal iron metabolism. Blood. 2009;113(8):1805-8.
67. Fleming MD et al. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A. 1998;95(3):1148-53.
68. Touret N et al. Dynamic traffic through the recycling compartment couples the metal transporter Nramp2 (DMT1) with the transferrin receptor. J Biol Chem. 2003;278(28):25548-57.
69. Canonne-Hergaux F et al. Characterization of the iron transporter DMT1 (NRAMP2/DCT1) in red blood cells of normal and anemic mk/mk mice. Blood. 2001;98(13):3823-30.
70. Gruenheid S et al. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes. J Exp Med. 1999;189(5):831-41.
71. Gunshin H et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 1997;388(6641):482-8.
72. Nevo Y, Nelson N. The NRAMP family of metal-ion transporters. Biochim Biophys Acta. 2006;1763(7):609-20.
73. Zhao N et al. ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J Biol Chem. 2010;285(42):32141-50.
74. Pinilla-Tenas JJ et al. Zip14 is a complex broad-scope metal-ion transporter whose functional properties support roles in the cellular uptake of zinc and nontransferrin-bound iron. Am J Physiol Cell Physiol. 2011;301(4):C862-71.
75. Liuzzi JP et al. Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc Natl Acad Sci U S A. 2006;103(37):13612-7.
76. Dong XP et al. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature. 2008;455(7215):992-6.
77. Lopin KV et al. Fe(2)(+) block and permeation of CaV3.1 (alpha1G) T-type calcium channels: candidate mechanism for non-transferrin-mediated Fe(2)(+) influx. Mol Pharmacol. 2012;82(6):1194-204.
78. Kumfu S et al. T-type calcium channel as a portal of iron uptake into cardiomyocytes of beta-thalassemic mice. Eur J Haematol. 2011;86(2):156-66.
79. Loh TT. Iron in the lactating mammary gland of the rat. Proc Soc Exp Biol Med. 1970;134(4):1070-2.
80. Loh TT, Kaldor I. Studies on the transfer of plasma iron to milk in the lactating rat. Aust J Exp Biol Med Sci. 1976;54(6):587-92.
81. Zhang P et al. The effect of serum iron concentration on iron secretion into mouse milk. J Physiol. 2000;522(Pt 3):479-91.
82. Moutafchiev DA, Shisheva AC, Sirakov LM. Binding of transferrin-iron to the plasma membrane of a lactating rabbit mammary gland cell. Int J Biochem. 1983;15(5):755-8.
83. Sigman M, Lonnerdal B. Characterization of transferrin receptors on plasma membranes of lactating rat mammary tissue. J Nutr Biochem. 1990;1(5):239-43.
84. Grigor MR, Wilde CJ, Flint DJ. Transferrin receptor activity in rat mammary epithelial cells. Biochem Int. 1988;17(4):747-54.
85. Schulman HM et al. Transferrin receptor and ferritin levels during murine mammary gland development. Biochim Biophys Acta. 1989;1010(1):1-6.
86. Sigman M, Lonnerdal B. Relationship of milk iron and the changing concentration of mammary tissue transferrin receptors during the course of lactation. J Nutr Biochem. 1990;1(11):572-6.
87. Sigman M, Lonnerdal B. Response of rat mammary gland transferrin receptors to maternal dietary iron during pregnancy and lactation. Am J Clin Nutr. 1990;52(3):446-50.
88. Leong WI, Lonnerdal B. Iron transporters in rat mammary gland: effects of different stages of lactation and maternal iron status. Am J Clin Nutr. 2005;81(2):445-53.
89. Gilchrist SE, Alcorn J. Lactation stage-dependent expression of transporters in rat whole mammary gland and primary mammary epithelial organoids. Fundam Clin Pharmacol. 2010;24(2):205-14.
90. Hubert N, Hentze MW. Previously uncharacterized isoforms of divalent metal transporter (DMT)-1: implications for regulation and cellular function. Proc Natl Acad Sci U S A. 2002;99(19):12345-50.
91. Montalbetti N et al. Mammalian iron transporters: families SLC11 and SLC40. Mol Aspects Med. 2013;34(2-3):270-87.
92. Kelleher SL, Lonnerdal B. Low vitamin a intake affects milk iron level and iron transporters in rat mammary gland and liver. J Nutr. 2005;135(1):27-32.
93. Agrawal RM, Tripathi AM, Agarwal KN. Cord blood haemoglobin, iron and ferritin status in maternal anaemia. Acta Paediatr Scand. 1983;72(4):545-8.
94. Sisson TR, Lund CJ. The influence of maternal iron deficiency on the newborn. Am J Clin Nutr. 1958;6(4):376-85.
95. Umbreit JN et al. Paraferritin: a protein complex with ferrireductase activity is associated with iron absorption in rats. Biochemistry. 1996;35(20):6460-9.
96. Shi H et al. A cytosolic iron chaperone that delivers iron to ferritin. Science. 2008;320(5880):1207-10.
97. Abboud S, Haile DJ. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem. 2000;275(26):19906-12.
98. Donovan A et al. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature. 2000;403(6771):776-81.
99. McKie AT et al. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell. 2000;5(2):299-309.
100. Pinnix ZK et al. Ferroportin and iron regulation in breast cancer progression and prognosis. Sci Transl Med. 2010;2(43):43ra56.
101. Ward PP et al. Iron status in mice carrying a targeted disruption of lactoferrin. Mol Cell Biol. 2003;23(1):178-85.
102. Delaby C et al. Presence of the iron exporter ferroportin at the plasma membrane of macrophages is enhanced by iron loading and down-regulated by hepcidin. Blood. 2005;106(12):3979-84.
103. Canonne-Hergaux F et al. Comparative studies of duodenal and macrophage ferroportin proteins. Am J Physiol Gastrointest Liver Physiol. 2006;290(1):G156-63.
104. Lymboussaki A et al. The role of the iron responsive element in the control of ferroportin1/IREG1/MTP1 gene expression. J Hepatol. 2003;39(5):710-5.
105. Knutson MD et al. Iron loading and erythrophagocytosis increase ferroportin 1 (FPN1) expression in J774 macrophages. Blood. 2003;102(12):4191-7.
106. Yang F et al. Regulation of reticuloendothelial iron transporter MTP1 (Slc11a3) by inflammation. J Biol Chem. 2002;277(42):39786-91.
107. Zoller H et al. Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology. 2001;120(6):1412-9.
108. Frazer DM et al. Hepcidin expression inversely correlates with the expression of duodenal iron transporters and iron absorption in rats. Gastroenterology. 2002;123(3):835-44.
109. Gambling L et al. Effect of iron deficiency on placental transfer of iron and expression of iron transport proteins in vivo and in vitro. Biochem J. 2001;356(Pt 3):883-9.
110. Zhang DL et al. A ferroportin transcript that lacks an iron-responsive element enables duodenal and erythroid precursor cells to evade translational repression. Cell Metab. 2009;9(5):461-73.
111. Cianetti L et al. Expression of alternative transcripts of ferroportin-1 during human erythroid differentiation. Haematologica. 2005;90(12):1595-606.
112. Ganz T, Nemeth E. Iron imports. IV. Hepcidin and regulation of body iron metabolism. Am J Physiol Gastrointest Liver Physiol. 2006;290(2):G199-203.
113. Nemeth E et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004;306(5704):2090-3.
114. Aydin S et al. Concentrations of preptin, salusins and hepcidins in plasma and milk of lactating women with or without gestational diabetes mellitus. Peptides. 2013;49:123-30.
115. De Domenico I et al. Ferroxidase activity is required for the stability of cell surface ferroportin in cells expressing GPI-ceruloplasmin. EMBO J. 2007;26(12):2823-31.
116. Harris ZL et al. Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux. Proc Natl Acad Sci U S A. 1999;96(19):10812-7.
117. Xu X et al. Aceruloplasminemia: an inherited neurodegenerative disease with impairment of iron homeostasis. Ann N Y Acad Sci. 2004;1012:299-305.
118. Anderson GJ et al. The ceruloplasmin homolog hephaestin and the control of intestinal iron absorption. Blood Cells Mol Dis. 2002;29(3):367-75.
119. Petrak J, Vyoral D. Hephaestin-A ferroxidase of cellular iron export. Int J Biochem Cell Biol. 2005;37(6):1173-8.
120. Vulpe CD et al. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat Genet. 1999;21(2):195-9.
121. Jaeger JL, Shimizu N, Gitlin JD. Tissue-specific ceruloplasmin gene expression in the mammary gland. Biochem J. 1991;280(Pt 3):671-7.
122. Donley SA et al. Copper transport to mammary gland and milk during lactation in rats. Am J Physiol Endocrinol Metab. 2002;283(4):E667-75.
123. Cerveza PJ et al. Milk ceruloplasmin and its expression by mammary gland and liver in pigs. Arch Biochem Biophys. 2000;373(2):451-61.
124. Chen H et al. Identification of zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J Nutr. 2010;140(10):1728-35.
125. Emery T. Iron oxidation by casein. Biochem Biophys Res Commun. 1992;182(3):1047-52.
126. Lonnerdal B. Trace element transport in the mammary gland. Annu Rev Nutr. 2007;27:165-77.
127. Ashkenazi A et al. The syndrome of neonatal copper deficiency. Pediatrics. 1973;52(4):525-33.
128. Cordano A. Clinical manifestations of nutritional copper deficiency in infants and children. Am J Clin Nutr. 1998;67(5 Suppl):1012S-6S.
129. Rauch H. Toxic milk, a new mutation affecting cooper metabolism in the mouse. J Hered. 1983;74(3):141-4.
130. Lee J, Prohaska JR, Thiele DJ. Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc Natl Acad Sci U S A. 2001;98(12):6842-7.
131. De Feo CJ et al. Three-dimensional structure of the human copper transporter hCTR1. Proc Natl Acad Sci U S A. 2009;106(11):4237-42.
132. Aller SG, Unger VM. Projection structure of the human copper transporter CTR1 at 6-A resolution reveals a compact trimer with a novel channel-like architecture. Proc Natl Acad Sci U S A. 2006;103(10):3627-32.
133. Lee J et al. Biochemical characterization of the human copper transporter Ctr1. J Biol Chem. 2002;277(6):4380-7.
134. Puig S et al. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem. 2002;277(29):26021-30.
135. Kelleher SL, Lonnerdal B. Mammary gland copper transport is stimulated by prolactin through alterations in Ctr1 and Atp7A localization. Am J Physiol Regul Integr Comp Physiol. 2006;291(4):R1181-91.
136. Kelleher SL, Lonnerdal B. Marginal maternal Zn intake in rats alters mammary gland Cu transporter levels and milk Cu concentration and affects neonatal Cu metabolism. J Nutr. 2003;133(7):2141-8.
137. Maryon EB, Molloy SA, Kaplan JH. Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1. Am J Physiol Cell Physiol. 2013;304(8):C768-79.
138. Harris ED. Cellular copper transport and metabolism. Annu Rev Nutr. 2000;20:291-310.
139. Lutsenko S et al. Function and regulation of human copper-transporting ATPases. Physiol Rev. 2007;87(3):1011-46.
140. Ackland ML et al. Expression of menkes copper-transporting ATPase, MNK, in the lactating human breast: possible role in copper transport into milk. J Histochem Cytochem. 1999;47(12):1553-62.
141. Michalczyk AA et al. Defective localization of the Wilson disease protein (ATP7B) in the mammary gland of the toxic milk mouse and the effects of copper supplementation. Biochem J. 2000;352(Pt 2):565-71.
142. Buiakova OI et al. Null mutation of the murine ATP7B (Wilson disease) gene results in intracellular copper accumulation and late-onset hepatic nodular transformation. Hum Mol Genet. 1999;8(9):1665-71.
143. Llanos RM et al. Copper transport during lactation in transgenic mice expressing the human ATP7A protein. Biochem Biophys Res Commun. 2008;372(4):613-7.
144. La Fontaine S, Mercer JF. Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Arch Biochem Biophys. 2007;463(2):149-67.
145. Council NR. Nutrition during lactation. Washington, DC: The National Academies Press; 1991.
146. Endo M et al. Vitamin contents in rat milk and effects of dietary vitamin intakes of dams on the vitamin contents in their milk. J Nutr Sci Vitaminol (Tokyo). 2011;57(3):203-8.
147. Hediger MA et al. The ABCs of membrane transporters in health and disease (SLC series): introduction. Mol Aspects Med. 2013;34(2-3):95-107.
148. van Herwaarden AE et al. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Mol Cell Biol. 2007;27(4):1247-53.
149. Jonker JW et al. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med. 2005;11(2):127-9.
150. Yonezawa A, Inui K. Novel riboflavin transporter family RFVT/SLC52: identification, nomenclature, functional characterization and genetic diseases of RFVT/SLC52. Mol Aspects Med. 2013;34(2-3):693-701.
151. Subramanian VS et al. Role of cysteine residues in cell surface expression of the human riboflavin transporter-2 (hRFT2) in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2011;301(1):G100-9.
152. Subramanian VS et al. Differential expression of human riboflavin transporters -1, -2, and -3 in polarized epithelia: a key role for hRFT-2 in intestinal riboflavin uptake. Biochim Biophys Acta. 2011;1808(12):3016-21.
153. Adkins Y, Lonnerdal B. High affinity binding of the transcobalamin II-cobalamin complex and mRNA expression of haptocorrin by human mammary epithelial cells. Biochim Biophys Acta. 2001;1528(1):43-8.
154. Sandberg DP, Begley JA, Hall CA. The content, binding, and forms of vitamin B12 in milk. Am J Clin Nutr. 1981;34(9):1717-24.
155. Zhao R, Goldman ID. Folate and thiamine transporters mediated by facilitative carriers (SLC19A1-3 and SLC46A1) and folate receptors. Mol Aspects Med. 2013;34(2-3):373-85.
156. Boulware MJ et al. Polarized expression of members of the solute carrier SLC19A gene family of water-soluble multivitamin transporters: implications for physiological function. Biochem J. 2003;376(Pt 1):43-8.
157. Neufeld EJ et al. Thiamine-responsive megaloblastic anemia syndrome: a disorder of high-affinity thiamine transport. Blood Cells Mol Dis. 2001;27(1):135-8.
158. Sweet R, Paul A, Zastre J. Hypoxia induced upregulation and function of the thiamine transporter, SLC19A3 in a breast cancer cell line. Cancer Biol Ther. 2010;10(11):1101-11.
159. de Carvalho FD, Quick M. Surprising substrate versatility in SLC5A6: Na+-coupled I- transport by the human Na+/multivitamin transporter (hSMVT). J Biol Chem. 2011;286(1):131-7.
160. Wang H et al. Human placental Na+-dependent multivitamin transporter. Cloning, functional expression, gene structure, and chromosomal localization. J Biol Chem. 1999;274(21):14875-83.
161. Gopal E et al. Transport of nicotinate and structurally related compounds by human SMCT1 (SLC5A8) and its relevance to drug transport in the mammalian intestinal tract. Pharm Res. 2007;24(3):575-84.
162. Coady MJ et al. Establishing a definitive stoichiometry for the Na+/monocarboxylate cotransporter SMCT1. Biophys J. 2007;93(7):2325-31.
163. Miyauchi S et al. Functional identification of SLC5A8, a tumor suppressor down-regulated in colon cancer, as a Na(+)-coupled transporter for short-chain fatty acids. J Biol Chem. 2004;279(14):13293-6.
164. Biondi C et al. Expression and characterization of vitamin C transporter in the human trophoblast cell line HTR-8/SVneo: effect of steroids, flavonoids and NSAIDs. Mol Hum Reprod. 2007;13(1):77-83.
165. Corpe CP et al. 6-Bromo-6-deoxy-L-ascorbic acid: an ascorbate analog specific for Na+-dependent vitamin C transporter but not glucose transporter pathways. J Biol Chem. 2005;280(7):5211-20.
166. Mackenzie B, Illing AC, Hediger MA. Transport model of the human Na+-coupled L-ascorbic acid (vitamin C) transporter SVCT1. Am J Physiol Cell Physiol. 2008;294(2):C451-9.
167. Tsukaguchi H et al. A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature. 1999;399(6731):70-5.
168. Zhao R et al. Mechanisms of membrane transport of folates into cells and across epithelia. Annu Rev Nutr. 2011;31:177-201.
169. Matherly LH, Goldman DI. Membrane transport of folates. Vitam Horm. 2003;66:403-56.
170. Borst P, Elferink RO. Mammalian ABC transporters in health and disease. Annu Rev Biochem. 2002;71:537-92.
171. Ifergan I, Assaraf YG. Molecular mechanisms of adaptation to folate deficiency. Vitam Horm. 2008;79:99-143.
172. Sorensen MT et al. Cell turnover and activity in mammary tissue during lactation and the dry period in dairy cows. J Dairy Sci. 2006;89(12):4632-9.
173. Mani O et al. Differential expression and localization of lipid transporters in the bovine mammary gland during the pregnancy-lactation cycle. J Dairy Sci. 2009;92(8):3744-56.
174. Picciano MF. Handbook of milk composition. San Diego: Academic; 1995.