publication . Article . Other literature type . 2018

Interaction of the human erythrocyte Band 3 anion exchanger 1 (AE1, SLC4A1) with lipids and glycophorin A: Molecular organization of the Wright (Wr) blood group antigen.

Antreas C. Kalli; Reinhart A. F. Reithmeier;
Open Access English
  • Published: 16 Jul 2018 Journal: PLoS Computational Biology (issn: 1553-734X, eissn: 1553-7358, Copyright policy)
  • Publisher: Public Library of Science (PLoS)
  • Country: United Kingdom
Abstract
The Band 3 (AE1, SLC4A1) membrane protein is found in red blood cells and in kidney where it functions as an electro-neutral chloride/bicarbonate exchanger. In this study, we have used molecular dynamics simulations to provide the first realistic model of the dimeric membrane domain of human Band 3 in an asymmetric lipid bilayer containing a full complement of phospholipids, including phosphatidylinositol 4,5–bisphosphate (PIP2) and cholesterol, and its partner membrane protein Glycophorin A (GPA). The simulations show that the annular layer in the inner leaflet surrounding Band 3 was enriched in phosphatidylserine and PIP2 molecules. Cholesterol was also enrich...
Subjects
Medical Subject Headings: stomatognathic systemlipids (amino acids, peptides, and proteins)
free text keywords: Biology (General), QH301-705.5, Research Article, Biology and Life Sciences, Biochemistry, Biochemical Simulations, Computational Biology, Lipids, Cholesterol, Physical sciences, Chemistry, Chemical physics, Dimers (Chemical physics), Physics, Condensed Matter Physics, Solid State Physics, Crystallography, Crystal Structure, Cell Biology, Cellular Structures and Organelles, Cell Membranes, Cellular Types, Animal Cells, Blood Cells, Red Blood Cells, Membrane Proteins, Ecology, Modelling and Simulation, Computational Theory and Mathematics, Genetics, Ecology, Evolution, Behavior and Systematics, Molecular Biology, Cellular and Molecular Neuroscience
Funded by
WT
Project
  • Funder: Wellcome Trust (WT)
98 references, page 1 of 7

1 Reithmeier RAF, Casey JR, Kalli AC, Sansom MSP, Alguel Y, Iwata S. Band 3, the human red cell chloride/bicarbonate anion exchanger (AE1, SLC4A1), in a structural context. Biochim Biophys Acta—Biomembr. 2016;1858: 1507–1532. 10.1016/j.bbamem.2016.03.030 27058983 [OpenAIRE] [PubMed] [DOI]

2 Low PS. Structure and function of the cytoplasmic domain of Band 3: Centre of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta. 1986;864: 145–167. 10.1016/0304-4157(86)90009-2 2943319 [OpenAIRE] [PubMed] [DOI]

3 Lux SE, John KM, Kopito RR, Lodish HF. Cloning and characterization of band 3, the human erythrocyte anion-exchange protein (AE1). Proc Natl Acad Sci U S A. 1989;86: 9089–9093. 10.1073/pnas.86.23.9089 2594752 [OpenAIRE] [PubMed] [DOI]

4 Tanner MJ, Martin PG, High S. The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. Biochem J. 1988;256: 703–12. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1135473&tool=pmcentrez&rendertype=abstract 3223947 [OpenAIRE] [PubMed]

5 Jennings ML. Oligomeric structure and the anion transport function of human erythrocyte band 3 protein. J Mem Biol. 1984;80: 105–117. 10.1007/BF01868768 [DOI]

6 Casey JR, Reithmeier RAF. Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J Biol Chem. 1991;266: 15726–15737. Available: http://www.jbc.org/content/266/24/15726.abstractN2 1874731 [OpenAIRE] [PubMed]

7 Zhang D, Kiyatkin A, Bolin JT, Low PS. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood. 2000;96: 2925–33. Available: http://www.bloodjournal.org/content/96/9/2925.abstract 11049968 [PubMed]

8 Reithmeier RA. Fragmentation of the band 3 polypeptide from human erythrocyte membranes. J Biol Chem. 1979;254: 3054–3060. Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=429334 429334 [PubMed]

9 Wang DN, Kühlbrandt W, Sarabia V, Reithmeier RAF. Two-dimensional structure of the membrane domain of human Band 3, the anion transport protein of erythrocyte membrane. EMBO J. 1993;12: 2233–2239. Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC413451/8508760 [OpenAIRE] [PubMed]

10 Wang DN, Sarabia VE, Reithmeier RA, Kuhlbrandt W. Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, Band 3. EMBO J. 1994;13: 3230–3235. Available: http://www.ncbi.nlm.nih.gov/pubmed/8045253 8045253 [OpenAIRE] [PubMed]

11 Arakawa T, Kobayashi-Yurugi T, Alguel Y, Iwanari H, Hatae H, Iwata M, et al Crystal structure of the anion exchanger domain of human erythrocyte band 3. Science (80-). 2015;350: 680–684. 10.1126/science.aaa4335 26542571 [OpenAIRE] [PubMed] [DOI]

12 Tang XB, Fujinaga J, Kopito R, Casey JR. Topology of the region surrounding Glu681of human AE1 protein, the erythrocyte anion exchanger. J Biol Chem. 1998;273: 22545–22553. 10.1074/jbc.273.35.22545 9712881 [OpenAIRE] [PubMed] [DOI]

13 Zhu Q, Lee DWK, Casey JR. Novel topology in C-terminal region of the human plasma membrane anion exchanger, AE1. J Biol Chem. 2003;278: 3112–3120. 10.1074/jbc.M207797200 12446737 [PubMed] [DOI]

14 Fujinaga J, Tang XB, Casey JR. Topology of the membrane domain of human erythrocyte anion exchange protein, AE1. J Biol Chem. 1999;274: 6626–33. 10.1074/jbc.274.10.6626 10037758 [OpenAIRE] [PubMed] [DOI]

15 Popov M, Tam LY, Li J, Reithmeier RAF. Mapping the ends of transmembrane segments in a polytopic membrane protein. J Biol Chem. 1997;272: 18325–18332. 10.1074/jbc.272.29.18325 9218473 [OpenAIRE] [PubMed] [DOI]

98 references, page 1 of 7
Abstract
The Band 3 (AE1, SLC4A1) membrane protein is found in red blood cells and in kidney where it functions as an electro-neutral chloride/bicarbonate exchanger. In this study, we have used molecular dynamics simulations to provide the first realistic model of the dimeric membrane domain of human Band 3 in an asymmetric lipid bilayer containing a full complement of phospholipids, including phosphatidylinositol 4,5–bisphosphate (PIP2) and cholesterol, and its partner membrane protein Glycophorin A (GPA). The simulations show that the annular layer in the inner leaflet surrounding Band 3 was enriched in phosphatidylserine and PIP2 molecules. Cholesterol was also enrich...
Subjects
Medical Subject Headings: stomatognathic systemlipids (amino acids, peptides, and proteins)
free text keywords: Biology (General), QH301-705.5, Research Article, Biology and Life Sciences, Biochemistry, Biochemical Simulations, Computational Biology, Lipids, Cholesterol, Physical sciences, Chemistry, Chemical physics, Dimers (Chemical physics), Physics, Condensed Matter Physics, Solid State Physics, Crystallography, Crystal Structure, Cell Biology, Cellular Structures and Organelles, Cell Membranes, Cellular Types, Animal Cells, Blood Cells, Red Blood Cells, Membrane Proteins, Ecology, Modelling and Simulation, Computational Theory and Mathematics, Genetics, Ecology, Evolution, Behavior and Systematics, Molecular Biology, Cellular and Molecular Neuroscience
Funded by
WT
Project
  • Funder: Wellcome Trust (WT)
98 references, page 1 of 7

1 Reithmeier RAF, Casey JR, Kalli AC, Sansom MSP, Alguel Y, Iwata S. Band 3, the human red cell chloride/bicarbonate anion exchanger (AE1, SLC4A1), in a structural context. Biochim Biophys Acta—Biomembr. 2016;1858: 1507–1532. 10.1016/j.bbamem.2016.03.030 27058983 [OpenAIRE] [PubMed] [DOI]

2 Low PS. Structure and function of the cytoplasmic domain of Band 3: Centre of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta. 1986;864: 145–167. 10.1016/0304-4157(86)90009-2 2943319 [OpenAIRE] [PubMed] [DOI]

3 Lux SE, John KM, Kopito RR, Lodish HF. Cloning and characterization of band 3, the human erythrocyte anion-exchange protein (AE1). Proc Natl Acad Sci U S A. 1989;86: 9089–9093. 10.1073/pnas.86.23.9089 2594752 [OpenAIRE] [PubMed] [DOI]

4 Tanner MJ, Martin PG, High S. The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. Biochem J. 1988;256: 703–12. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1135473&tool=pmcentrez&rendertype=abstract 3223947 [OpenAIRE] [PubMed]

5 Jennings ML. Oligomeric structure and the anion transport function of human erythrocyte band 3 protein. J Mem Biol. 1984;80: 105–117. 10.1007/BF01868768 [DOI]

6 Casey JR, Reithmeier RAF. Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J Biol Chem. 1991;266: 15726–15737. Available: http://www.jbc.org/content/266/24/15726.abstractN2 1874731 [OpenAIRE] [PubMed]

7 Zhang D, Kiyatkin A, Bolin JT, Low PS. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood. 2000;96: 2925–33. Available: http://www.bloodjournal.org/content/96/9/2925.abstract 11049968 [PubMed]

8 Reithmeier RA. Fragmentation of the band 3 polypeptide from human erythrocyte membranes. J Biol Chem. 1979;254: 3054–3060. Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=429334 429334 [PubMed]

9 Wang DN, Kühlbrandt W, Sarabia V, Reithmeier RAF. Two-dimensional structure of the membrane domain of human Band 3, the anion transport protein of erythrocyte membrane. EMBO J. 1993;12: 2233–2239. Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC413451/8508760 [OpenAIRE] [PubMed]

10 Wang DN, Sarabia VE, Reithmeier RA, Kuhlbrandt W. Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, Band 3. EMBO J. 1994;13: 3230–3235. Available: http://www.ncbi.nlm.nih.gov/pubmed/8045253 8045253 [OpenAIRE] [PubMed]

11 Arakawa T, Kobayashi-Yurugi T, Alguel Y, Iwanari H, Hatae H, Iwata M, et al Crystal structure of the anion exchanger domain of human erythrocyte band 3. Science (80-). 2015;350: 680–684. 10.1126/science.aaa4335 26542571 [OpenAIRE] [PubMed] [DOI]

12 Tang XB, Fujinaga J, Kopito R, Casey JR. Topology of the region surrounding Glu681of human AE1 protein, the erythrocyte anion exchanger. J Biol Chem. 1998;273: 22545–22553. 10.1074/jbc.273.35.22545 9712881 [OpenAIRE] [PubMed] [DOI]

13 Zhu Q, Lee DWK, Casey JR. Novel topology in C-terminal region of the human plasma membrane anion exchanger, AE1. J Biol Chem. 2003;278: 3112–3120. 10.1074/jbc.M207797200 12446737 [PubMed] [DOI]

14 Fujinaga J, Tang XB, Casey JR. Topology of the membrane domain of human erythrocyte anion exchange protein, AE1. J Biol Chem. 1999;274: 6626–33. 10.1074/jbc.274.10.6626 10037758 [OpenAIRE] [PubMed] [DOI]

15 Popov M, Tam LY, Li J, Reithmeier RAF. Mapping the ends of transmembrane segments in a polytopic membrane protein. J Biol Chem. 1997;272: 18325–18332. 10.1074/jbc.272.29.18325 9218473 [OpenAIRE] [PubMed] [DOI]

98 references, page 1 of 7
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