Caco-2 cell acquisition of dietary iron(III) invokes a nanoparticulate endocytic pathway
Dietary non-heme iron contains ferrous [Fe(II)] and ferric [Fe(III)] iron fractions and the latter should hydrolyze, forming Fe(III) oxo-hydroxide particles, on passing from the acidic stomach to less acidic duodenum. Using conditions to mimic the in vivo hydrolytic environment we confirmed the form...
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Published in | PloS one Vol. 8; no. 11; p. e81250 |
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Main Authors | , , , , , , , , , |
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Language | English |
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Abstract | Dietary non-heme iron contains ferrous [Fe(II)] and ferric [Fe(III)] iron fractions and the latter should hydrolyze, forming Fe(III) oxo-hydroxide particles, on passing from the acidic stomach to less acidic duodenum. Using conditions to mimic the in vivo hydrolytic environment we confirmed the formation of nanodisperse fine ferrihydrite-like particles. Synthetic analogues of these (~ 10 nm hydrodynamic diameter) were readily adherent to the cell membrane of differentiated Caco-2 cells and internalization was visualized using transmission electron microscopy. Moreover, Caco-2 exposure to these nanoparticles led to ferritin formation (i.e., iron utilization) by the cells, which, unlike for soluble forms of iron, was reduced (p=0.02) by inhibition of clathrin-mediated endocytosis. Simulated lysosomal digestion indicated that the nanoparticles are readily dissolved under mildly acidic conditions with the lysosomal ligand, citrate. This was confirmed in cell culture as monensin inhibited Caco-2 utilization of iron from this source in a dose dependent fashion (p<0.05) whilet soluble iron was again unaffected. Our findings reveal the possibility of an endocytic pathway for acquisition of dietary Fe(III) by the small intestinal epithelium, which would complement the established DMT-1 pathway for soluble Fe(II). |
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AbstractList | Dietary non-heme iron contains ferrous [Fe(II)] and ferric [Fe(III)] iron fractions and the latter should hydrolyze, forming Fe(III) oxo-hydroxide particles, on passing from the acidic stomach to less acidic duodenum. Using conditions to mimic the
in vivo
hydrolytic environment we confirmed the formation of nanodisperse fine ferrihydrite-like particles. Synthetic analogues of these (~ 10 nm hydrodynamic diameter) were readily adherent to the cell membrane of differentiated Caco-2 cells and internalization was visualized using transmission electron microscopy. Moreover, Caco-2 exposure to these nanoparticles led to ferritin formation (i.e., iron utilization) by the cells, which, unlike for soluble forms of iron, was reduced (
p
=0.02) by inhibition of clathrin-mediated endocytosis. Simulated lysosomal digestion indicated that the nanoparticles are readily dissolved under mildly acidic conditions with the lysosomal ligand, citrate. This was confirmed in cell culture as monensin inhibited Caco-2 utilization of iron from this source in a dose dependent fashion (
p
<0.05) whilet soluble iron was again unaffected. Our findings reveal the possibility of an endocytic pathway for acquisition of dietary Fe(III) by the small intestinal epithelium, which would complement the established DMT-1 pathway for soluble Fe(II). Dietary non-heme iron contains ferrous [Fe(II)] and ferric [Fe(III)] iron fractions and the latter should hydrolyze, forming Fe(III) oxo-hydroxide particles, on passing from the acidic stomach to less acidic duodenum. Using conditions to mimic the in vivo hydrolytic environment we confirmed the formation of nanodisperse fine ferrihydrite-like particles. Synthetic analogues of these (~ 10 nm hydrodynamic diameter) were readily adherent to the cell membrane of differentiated Caco-2 cells and internalization was visualized using transmission electron microscopy. Moreover, Caco-2 exposure to these nanoparticles led to ferritin formation (i.e., iron utilization) by the cells, which, unlike for soluble forms of iron, was reduced (p=0.02) by inhibition of clathrin-mediated endocytosis. Simulated lysosomal digestion indicated that the nanoparticles are readily dissolved under mildly acidic conditions with the lysosomal ligand, citrate. This was confirmed in cell culture as monensin inhibited Caco-2 utilization of iron from this source in a dose dependent fashion (p<0.05) whilet soluble iron was again unaffected. Our findings reveal the possibility of an endocytic pathway for acquisition of dietary Fe(III) by the small intestinal epithelium, which would complement the established DMT-1 pathway for soluble Fe(II). |
Audience | Academic |
Author | Pereira, Dora I A Faria, Nuno Prassmayer, Laura Aslam, Mohamad F Powell, Jonathan J Lönnerdal, Bo Brown, Andy P Bruggraber, Sylvaine F A Poots, Lynsey K Mergler, Bianca I |
AuthorAffiliation | 2 Department of Nutrition, University of California Davis, Davis, California, United States of America 1 Medical Research Council Human Nutrition Research (MRC HNR), Elsie Widdowson Laboratory, Cambridge, United Kingdom University of Birmingham, United Kingdom 3 Institute for Materials Research, School of Process, Environmental and Materials Engineering, University of Leeds, Leeds, United Kingdom |
AuthorAffiliation_xml | – name: University of Birmingham, United Kingdom – name: 2 Department of Nutrition, University of California Davis, Davis, California, United States of America – name: 3 Institute for Materials Research, School of Process, Environmental and Materials Engineering, University of Leeds, Leeds, United Kingdom – name: 1 Medical Research Council Human Nutrition Research (MRC HNR), Elsie Widdowson Laboratory, Cambridge, United Kingdom |
Author_xml | – sequence: 1 givenname: Dora I A surname: Pereira fullname: Pereira, Dora I A organization: Medical Research Council Human Nutrition Research (MRC HNR), Elsie Widdowson Laboratory, Cambridge, United Kingdom – sequence: 2 givenname: Bianca I surname: Mergler fullname: Mergler, Bianca I – sequence: 3 givenname: Nuno surname: Faria fullname: Faria, Nuno – sequence: 4 givenname: Sylvaine F A surname: Bruggraber fullname: Bruggraber, Sylvaine F A – sequence: 5 givenname: Mohamad F surname: Aslam fullname: Aslam, Mohamad F – sequence: 6 givenname: Lynsey K surname: Poots fullname: Poots, Lynsey K – sequence: 7 givenname: Laura surname: Prassmayer fullname: Prassmayer, Laura – sequence: 8 givenname: Bo surname: Lönnerdal fullname: Lönnerdal, Bo – sequence: 9 givenname: Andy P surname: Brown fullname: Brown, Andy P – sequence: 10 givenname: Jonathan J surname: Powell fullname: Powell, Jonathan J |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24278403$$D View this record in MEDLINE/PubMed |
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DocumentTitleAlternate | Dietary Iron(III) Uptake Invokes Endocytosis |
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Notes | These authors contribute equally to this work. Conceived and designed the experiments: DIAP BIM JJP. Performed the experiments: DIAP BIM LKP LP MFA. Analyzed the data: DIAP BIM MFA APB. Contributed reagents/materials/analysis tools: BL NF SFAB APB. Wrote the manuscript: DIAP APB JJP. Developed the hypothesis behind this research: JJP DIAP. Provided input on development of the hypothesis behind this research: SFAB NF APB. Had primary responsibility for final content: DIAP JJP. Read, provided input to and approved the manuscript: DIAP BIM NF SFAB MFA LKP LP BL APB JJP. Competing Interests: The authors declare no conflict of interest but D.I.A.P., N.F., S.F.A.B. and J.J.P. wish to note that they are inventors on a patent detailing novel Fe(III) poly oxo-hydroxide structures that may have potential as dietary supplements [Powell, J., S. Bruggraber, et al. (2008). Ligand modified poly oxo-hydroxy metal ion materials, their uses and processes for their preparation. W. I. P. Organization, U.K. WO/2008/096130]. This patent does not alter adherence to all PLOS ONE policies on sharing data or materials. |
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Snippet | Dietary non-heme iron contains ferrous [Fe(II)] and ferric [Fe(III)] iron fractions and the latter should hydrolyze, forming Fe(III) oxo-hydroxide particles,... |
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SubjectTerms | Caco-2 Cells Cell culture Citric acid Clathrin Computer simulation Councils Diet Divalent metal transporter-1 Duodenum Electron microscopy Endocytosis Epithelium Ferritin Ferritins - metabolism Glycoproteins Heme Humans Inhibition Internalization Intestine Iron Iron, Dietary - metabolism Laboratories Ligands Lysosomes - metabolism Medical research Metal Nanoparticles Molecular weight Monensin Nanoparticles Nanoparticles - chemistry Nanoparticles - ultrastructure Nutrition research Particulates Proteins Rodents Stomach Transmission electron microscopy |
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Title | Caco-2 cell acquisition of dietary iron(III) invokes a nanoparticulate endocytic pathway |
URI | https://www.ncbi.nlm.nih.gov/pubmed/24278403 https://www.proquest.com/docview/1460505157 https://pubmed.ncbi.nlm.nih.gov/PMC3836913 https://doaj.org/article/1bc1423b3da748a2b1466fd4796ad4b6 http://dx.doi.org/10.1371/journal.pone.0081250 |
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