The monovalent cation leak in overhydrated stomatocytic red blood cells results from amino acid substitutions in the Rh-associated glycoprotein

Blood

Volumn 113, Issue 6, 2009, Pages 1350-1357

  Bruce, Lesley J ^a   Guizouarn, Hélène ^b   Burton, Nicholas M ^a,c   Gabillat, Nicole ^b   Poole, Joyce ^a   Flatt, Joanna F ^a   Brady, R Leo ^c   Borgese, Franck ^b   Delaunay, Jean ^d,e   Stewart, Gordon W ^f  

^a NHS BLOOD AND TRANSPLANT   (United Kingdom)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d BICÊTRE HOSPITAL   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLYCOPROTEIN; ISOLEUCINE; MONOVALENT CATION; PHENYLALANINE; RH ASSOCIATED GLYCOPROTEIN; SERINE; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PLASMA PROTEIN; RHAG PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DNA DETERMINATION; ERYTHROCYTE; FEMALE; GENE MUTATION; HEMOLYTIC ANEMIA; HETEROZYGOSITY; HUMAN; MALE; NITROSOMONAS EUROPAEA; NONHUMAN; OOCYTE; OVERHYDRATED HEREDITARY STOMATOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STOMATOCYTOSIS; WILD TYPE; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; BLOOD GROUP RHESUS SYSTEM; CHEMICAL STRUCTURE; CYTOLOGY; ERYTHROCYTE MEMBRANE; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANEMIA, HEMOLYTIC; ANIMALS; BLOOD PROTEINS; CATIONS, MONOVALENT; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HUMANS; IMMUNOBLOTTING; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NITROSOMONAS EUROPAEA; OOCYTES; PROTEIN CONFORMATION; RH-HR BLOOD-GROUP SYSTEM; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS LAEVIS;

EID: 60849116982     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-07-171140     Document Type: Article

References (40)

1. Lock SP, Sephton Smith R, Hardisty RM. Stomatocytosis: a hereditary haemolytic anomaly associated with haemolytic anaemia. Br J Haematol. 1961;7:303-314.
2. Stewart GW. Hemolytic disease due to membrane ion channel disorders. Curr Opin Hematol. 2004;11:244-250.
3. Fricke B, Parsons SF, Knöpfle G, von Düring M, Stewart GW. Stomatin is mis-trafficked in the erythrocytes of overhydrated hereditary stomato-cytosis, and is absent from normal primitive yolk sac-derived erythrocytes. Br J Haematol. 2005; 131:265-277.
4. Turner EJ, Jarvis HG, Chetty MC, et al. ATP-dependent vesiculation in red cell membranes from different hereditary stomatocytosis variants. Br J Haematol. 2003;120:894-902.
5. Bruce LJ, Robinson HC, Guizouarn H, et al. Monovalent cation leaks in human red cells caused by single amino-acid substitutions in the transport domain of the band 3 chloride-bicarbonate exchanger, AE1. Nat Genet. 2005;37:1258-1263.
6. Bruce LJ, Beckmann R, Ribeiro ML, et al.Aband 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood. 2003;101: 4180-4188.
7. Khademi S, O'Connell J 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM. Mechanism of ammonia transport byAmt/MEP/Rh: structure of AmtB at 1.35 A. Science. 2004;305: 1587-1594.
8. Zheng L, Kostrewa D, Berneche S, Winkler FK, Li XD. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc Natl Acad Sci U S A. 2004;101:17090-17095.
9. Lupo D, Li XD, Durand A, et al. The 1.3-Å resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins. Proc Natl Acad Sci USA. 2007;104:19303-19308.
10. Li X, Jayachandran S, Nguyen HH, Chan MK. Structure of the Nitrosomonas europaea Rh protein. Proc Natl Acad Sci USA. 2007;104:19279-19284.
11. Fricke B, Argent AC, Chetty MC, et al. The "stomatin" gene and protein in overhydrated hereditary stomatocytosis. Blood. 2003;102:2268-2277.
12. Fricke B, Jarvis HG, Reid CD, et al. Four new cases of stomatin-deficient hereditary stomatocytosis syndrome: association of the stomatin-deficient cryohydrocytosis variant with neurological dysfunction. Br J Haematol. 2004;125:796-803.
13. Meadow SR. Stomatocytosis. Proc R Soc Med. 1967;60:13-15.
14. -)-cotransport in a case of congenital stomatocytosis. Br J Haematol. 1989;71: 141-146.
15. Ridgwell K, Spurr NK, Laguda B, MacGeoch C, Avent ND, Tanner MJ. Isolation of cDNA clones for a 50 kDa glycoprotein of the human erythrocyte membrane associated with Rh (rhesus) blood-group antigen expression. Biochem J. 1992;287:223-228.
16. null disease. J Biol Chem. 1998;273:2207-2213.
17. Young MT, Tanner MJ. Distinct regions of human glycophorin A enhance human red cell anion exchanger (band 3; AE1) transport function and surface trafficking. J Biol Chem. 2003;278:32954-32961.
18. Ridgwell K, Eyers SA, Mawby WJ, Anstee DJ, Tanner MJ. Studies on the glycoprotein associated with Rh (rhesus) blood group antigen expression in the human red blood cell membrane. J Biol Chem. 1994;269:6410-6416.
19. Martial S, Guizouarn H, Gabillat N, Pellissier B, Borgese F. Importance of several cysteine residues for the chloride conductance of trout anion exchanger 1 (tAE1). J Cell Physiol. 2007;213:70-78.
20. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993;234:779-815.
21. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. Procheck: a program to check the stereochemical quality of protein structures. J Appl Crystallog. 1993;26:283-291.
22. Davis IW, Murray LW, Richardson JS, Richardson DC. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 2004;32:W615-W619.
23. Bruce LJ. Red cell membrane transport abnormalities. Curr Opin Hematol. 2008;15:184-190.
24. Tilley L, Gaskell A, Poole J, Daniels G. Duclosnegative and Ol(a+) blood group phenotypes are associated with amino acid substitutions in the external loops of the Rh-associated glycoprotein [abstract]. Vox Sang. 2008;95:37. Abstract 3CS18-03.
25. Conroy MJ, Bullough PA, Merrick M, Avent ND. Modelling the human rhesus proteins: implications for structure and function. Br J Haematol. 2005;131:543-551.
26. Huang CH, Peng J. Evolutionary conservation and diversification of Rh family genes and proteins. Proc Natl Acad Sci USA. 2005;102:15512-15517.
27. Marcus Y. Ion solvation. Chicester, UK: Wiley; 1985.
28. Hemker MB, Cheroutre G, van Zwieten R, et al. The Rh complex exports ammonium from human red blood cells. Br J Haematol. 2003;122:333-340.
29. Ripoche P, Bertrand O, Gane P, et al. Human Rhesus-associated glycoprotein mediates facilitated transport of NH(3) into red blood cells. Proc Natl Acad Sci USA. 2004;101:17222-17227.
30. Benjelloun F, Bakouh N, Fritsch J, et al. Expression of the human erythroid Rh glycoprotein (RhAG) enhances both NH3 and NH4+ transport in HeLa cells. Pflugers Arch. 2005;450:155-167.
31. Marini AM, Matassi G, Raynal V, Andre B, Cartron JP, Chérif-Zahar B. The human Rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nat Genet. 2000;26:341-344.
32. Westhoff CM, Wylie DE. Transport characteristics of mammalian Rh and Rh glycoproteins expressed in heterologous systems. Transfus Clin Biol. 2006;13:132-138.
33. Szekely D, Chapman BE, Bubb WA, Kuchel PW. Rapid exchange of fluoroethylamine via the Rhesus complex in human erythrocytes: 19F NMR magnetization transfer analysis showing competition by ammonia and ammonia analogues. Biochemistry. 2006;45:9354-9361.
34. 3 gas transport in red cell ghosts: a stopped-flow analysis. Transfus Clin Biol. 2006;13:117-122.
35. Kustu S, Inwood W. Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. Transfus Clin Biol. 2006; 13:103-110.
36. Endeward V, Cartron JP, Ripoche P, Gros G. RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J. 2008;22:64-73.
37. Missner A, Kügler P, Saparov SM, et al. Carbon dioxide transport through membranes. J Biol Chem. 2008;283:25340-25347.
38. Fong RN, Kim K-S, Yoshihara C, Inwood WB, Kustu S. The W148L substitution in the Escherichia coli ammonium channel AmtB increases flux and indicates that the substrate is an ion. Proc Natl Acad Sci U SA. 2007;104:18706-18711.
39. Montel-Hagen A. Erythrocyte Glut1 triggers dehydroascorbic acid uptake in mammals unable to synthesize vitamin C. Cell. 2008;132:1039-1048.
40. Mentzer WC Jr, Smith WB, Goldstone J, Shohet SB. Hereditary stomatocytosis: membrane and metabolism studies. Blood. 1975;46:659-669.