Blood Reviews
Volume 20, Issue 2 , Pages 93-110 , March 2006

Rh proteins: Key structural and functional components of the red cell membrane

References 

  1. Mollison PL, Engelfriet CP, Contreras M. Blood Transfusion in Clinical Medicine, 9th edition. London; 1993.
  2. Agre P, Cartron JP. Molecular biology of the Rh antigens. Blood. 1991;78:551–563
  3. Cartron JP, Agre P. Rh blood group antigens: protein and gene structure. Semin Hematol. 1993;30:193–208
  4. Anstee DJ, Tanner MJ. Biochemical aspects of the blood group Rh (rhesus) antigens. Baillieres Clin Haematol. 1993;6:401–422
  5. Cartron JP. Defining the Rh blood group antigens. Biochemistry and molecular genetics. Blood Rev. 1994;8:199–212
  6. Cartron JP, Bailly P, Le Van Kim C, Cherif-Zahar B, Matassi G, Bertrand O, et al. Insights into the structure and function of membrane polypeptides carrying blood group antigens. Vox Sang. 1998;74(Suppl 2):29–64
  7. Huang CH. Molecular insights into the Rh protein family and associated antigens. Curr Opin Hematol. 1997;4:94–103
  8. Avent ND, Reid ME. The Rh blood group system: a review. Blood. 2000;95:375–387
  9. Lomas-Francis C, Reid ME. The Rh blood group system: the first 60 years of discovery. Immunohematol. 2000;16:7–17
  10. Avent ND. Molecular biology of the Rh blood group system. J Pediatr Hematol Oncol. 2001;23:394–402
  11. Wagner FF, Flegel WA. Review: the molecular basis of the Rh blood group phenotypes. Immunohematol. 2004;20:23–36
  12. Cartron JP. RH blood group system and molecular basis of Rh-deficiency. Baillieres Best Pract Res Clin Haematol. 1999;12:655–689
  13. Huang CH, Liu PZ, Cheng JG. Molecular biology and genetics of the Rh blood group system. Semin Hematol. 2000;37:150–165
  14. Levine P, Stetson RE. An unusual case of intragroup agglutination. Journal of the American Medical Association. 1939;113:126–127
  15. Daniels G. A century of human blood groups. Wien Klin Wochenschr. 2001;113:781–786
  16. Wagner FF, Flegel WA. RHD gene deletion occurred in the Rhesus box. Blood. 2000;95:3662–3668
  17. Colin Y, Cherif-Zahar B, Le Van Kim C, Raynal V, Van Huffel V, Cartron JP. Genetic basis of the RhD-positive and RhD-negative blood group polymorphism as determined by Southern analysis. Blood. 1991;78:2747–2752
  18. Wagner FF, Frohmajer A, Flegel WA. RHD positive haplotypes in D negative Europeans. BMC Genet. 2001;2:10
  19. Singleton BK, Green CA, Avent ND, Martin PG, Smart E, Daka A, et al. The presence of an RHD pseudogene containing a 37 base pair duplication and a nonsense mutation in africans with the Rh D-negative blood group phenotype. Blood. 2000;95:12–18
  20. Le van Kim C, Mouro I, Cherif-Zahar B, Raynal V, Cherrier C, Cartron JP, et al. Molecular cloning and primary structure of the human blood group RhD polypeptide. Proc Natl Acad Sci U S A. 1992;89:10925–10929
  21. Cartron JP, Rouillac C, Le Van Kim C, Mouro I, Colin Y. Tentative model for the mapping of D epitopes on the RhD polypeptide. Transfus Clin Biol. 1996;3:497–503
  22. Scott ML, Voak D, Liu W, Jones JW, Avent ND. Epitopes on Rh proteins. Vox Sang. 2000;78(Suppl 2):117–120
  23. Avent ND, Liu W, Scott ML, Jones JW, Voak D. Site directed mutagenesis of the human Rh D antigen: molecular basis of D epitopes. Vox Sang. 2000;78(Suppl 2):83–89
  24. Liu W, Avent ND, Jones JW, Scott ML, Voak D. Molecular configuration of Rh D epitopes as defined by site-directed mutagenesis and expression of mutant Rh constructs in K562 erythroleukemia cells. Blood. 1999;94:3986–3996
  25. Avent ND, Finning KM, Liu W, Scott ML. Molecular biology of partial D phenotypes. Transfus Clin Biol. 1996;3:511–516
  26. Rouillac C, Colin Y, Hughes-Jones NC, Beolet M, D’Ambrosio AM, Cartron JP, et al. Transcript analysis of D category phenotypes predicts hybrid Rh D-CE-D proteins associated with alteration of D epitopes. Blood. 1995;85:2937–2944
  27. Westhoff CM. The Rh blood group system in review: a new face for the next decade. Transfusion. 2004;44:1663–1673
  28. Tippett P. Depressed Rh phenotypes. Rev Fr Transfus Immunohematol. 1978;21:135–150
  29. Flegel WA, Khull SR, Wagner FF. Primary anti-D immunization by weak D type 2 RBCs. Transfusion. 2000;40:428–434
  30. Fairbanks G, Steck TL, Wallach DF. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 1971;10:2606–2617
  31. Wagner FF, Gassner C, Muller TH, Schonitzer D, Schunter F, Flegel WA. Molecular basis of weak D phenotypes. Blood. 1999;93:385–393
  32. Wagner FF, Frohmajer A, Ladewig B, Eicher NI, Lonicer CB, Muller TH, et al. Weak D alleles express distinct phenotypes. Blood. 2000;95:2699–2708
  33. Mouro I, Colin Y, Cherif-Zahar B, Cartron JP, Le Van Kim C. Molecular genetic basis of the human Rhesus blood group system. Nat Genet. 1993;5:62–65
  34. Smythe JS, Avent ND, Judson PA, Parsons SF, Martin PG, Anstee DJ. Expression of RHD and RHCE gene products using retroviral transduction of K562 cells establishes the molecular basis of Rh blood group antigens. Blood. 1996;87:2968–2973
  35. Salvignol I, Calvas P, Socha WW, Colin Y, Le Van Kim C, Bailly P, et al. Structural analysis of the RH-like blood group gene products in nonhuman primates. Immunogenetics. 1995;41:271–281
  36. Westhoff CM, Silberstein LE, Wylie DE. Evidence supporting the requirement for two proline residues for expression of c. Transfusion. 2000;40:321–324
  37. Noizat-Pirenne F, Mouro I, Gane P, Okubo Y, Hori Y, Rouger P, et al. Heterogeneity of blood group RhE variants revealed by serological analysis and molecular alteration of the RHCE gene and transcript. Br J Haematol. 1998;103:429–436
  38. Chen YX, Peng J, Novaretti M, Reid ME, Huang CH. Deletion of arginine codon 229 in the Rhce gene alters e and f but not c antigen expression. Transfusion. 2004;44:391–398
  39. Mouro I, Colin Y, Sistonen P, Le Pennec PY, Cartron JP, Le Van Kim C. Molecular basis of the RhCW (Rh8) and RhCX (Rh9) blood group specificities. Blood. 1995;86:1196–1201
  40. Strobel E, Noizat-Pirenne F, Hofmann S, Cartron JP, Bauer MF. The molecular basis of the Rhesus antigen Ew. Transfusion. 2004;44:407–409
  41. Noizat-Pirenne F, Le Pennec PY, Mouro I, Rouzaud AM, Juszczak G, Roussel M, et al. Molecular background of D (C) (e) haplotypes within the white population. Transfusion. 2002;42:627–633
  42. 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(Pt 1):223–228
  43. Cherif-Zahar B, Raynal V, Gane P, Mattei MG, Bailly P, Gibbs B, et al. Candidate gene acting as a suppressor of the RH locus in most cases of Rh-deficiency. Nat Genet. 1996;12:168–173
  44. Miller YE, Daniels GL, Jones C, Palmer DK. Identification of a cell-surface antigen produced by a gene on human chromosome 3 (cen-q22) and not expressed by Rhnull cells. Am J Hum Genet. 1987;41:1061–1070
  45. Huang CH, Chen Y, Reid ME, Seidl C. Rhnull disease: the amorph type results from a novel double mutation in RhCe gene on D-negative background. Blood. 1998;92:664–671
  46. Cherif-Zahar B, Matassi G, Raynal V, Gane P, Mempel W, Perez C, et al. Molecular defects of the RHCE gene in Rh-deficient individuals of the amorph type. Blood. 1998;92:639–646
  47. Eyers SA, Ridgwell K, Mawby WJ, Tanner MJ. Topology and organization of human Rh (rhesus) blood group-related polypeptides. J Biol Chem. 1994;269:6417–6423
  48. Hartel-Schenk S, Agre P. Mammalian red cell membrane Rh polypeptides are selectively palmitoylated subunits of a macromolecular complex. J Biol Chem. 1992;267:5569–5574
  49. Huang CH. The human Rh50 glycoprotein gene. Structural organization and associated splicing defect resulting in Rh (null) disease. J Biol Chem. 1998;273:2207–2213
  50. Sieff C, Bicknell D, Caine G, Robinson J, Lam G, Greaves MF. Changes in cell surface antigen expression during hemopoietic differentiation. Blood. 1982;60:703–713
  51. Dunstan RA. Status of major red cell blood group antigens on neutrophils, lymphocytes and monocytes. Br J Haematol. 1986;62:301–309
  52. Gahmberg CG. Molecular characterization of the human red cell Rho (D) antigen. Embo J. 1983;2:223–227
  53. de Vetten MP, Agre P. The Rh polypeptide is a major fatty acid-acylated erythrocyte membrane protein. J Biol Chem. 1988;263:18193–18196
  54. Nicolas V, Le Van Kim C, Gane P, Birkenmeier C, Cartron JP, Colin Y, et al. Rh-RhAG/ankyrin-R, a new interaction site between the membrane bilayer and the red cell skeleton, is impaired by Rh (null)-associated mutation. J Biol Chem. 2003;278:25526–25533
  55. Moore S, Green C. The identification of specific Rhesus-polypeptide-blood-group-ABH-active-glycoprotein complexes in the human red-cell membrane. Biochem J. 1987;244:735–741
  56. Bony V, Gane P, Bailly P, Cartron JP. Time-course expression of polypeptides carrying blood group antigens during human erythroid differentiation. Br J Haematol. 1999;107:263–274
  57. Southcott MJ, Tanner MJ, Anstee DJ. The expression of human blood group antigens during erythropoiesis in a cell culture system. Blood. 1999;93:4425–4435
  58. Senes A, Engel DE, DeGrado WF. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol. 2004;14:465–479
  59. Mouro-Chanteloup I, D’Ambrosio AM, Gane P, Le Van Kim C, Raynal V, Dhermy D, et al. Cell-surface expression of RhD blood group polypeptide is posttranscriptionally regulated by the RhAG glycoprotein. Blood. 2002;100:1038–1047
  60. Brown EJ, Frazier WA. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 2001;11:130–135
  61. Pettersen RD. CD47 and death signaling in the immune system. Apoptosis. 2000;5:299–306
  62. Gao AG, Lindberg FP, Finn MB, Blystone SD, Brown EJ, Frazier WA. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J Biol Chem. 1996;271:21–24
  63. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Science. 2000;288:2051–2054
  64. Mouro-Chanteloup I, Delaunay J, Gane P, Nicolas V, Johansen M, Brown EJ, et al. Evidence that the red cell skeleton protein 4.2 interacts with the Rh membrane complex member CD47. Blood. 2003;101:338–344
  65. Oldenborg PA, Gresham HD, Lindberg FP. CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med. 2001;193:855–862
  66. Oldenborg PA, Gresham HD, Chen Y, Izui S, Lindberg FP. Lethal autoimmune hemolytic anemia in CD47-deficient nonobese diabetic (NOD) mice. Blood. 2002;99:3500–3504
  67. Oldenborg PA. Role of CD47 in erythroid cells and in autoimmunity. Leuk Lymphoma. 2004;45:1319–1327
  68. Lindberg FP, Bullard DC, Caver TE, Gresham HD, Beaudet AL, Brown EJ. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science. 1996;274:795–798
  69. Bailly P, Hermand P, Callebaut I, Sonneborn HH, Khamlichi S, Mornon JP, et al. The LW blood group glycoprotein is homologous to intercellular adhesion molecules. Proc Natl Acad Sci U S A. 1994;91:5306–5310
  70. Bailly P, Tontti E, Hermand P, Cartron JP, Gahmberg CG. The red cell LW blood group protein is an intercellular adhesion molecule which binds to CD11/CD18 leukocyte integrins. Eur J Immunol. 1995;25:3316–3320
  71. Hermand P, Huet M, Callebaut I, Gane P, Ihanus E, Gahmberg CG, et al. Binding sites of leukocyte beta 2 integrins (LFA-1, Mac-1) on the human ICAM-4/LW blood group protein. J Biol Chem. 2000;275:26002–26010
  72. Mankelow TJ, Spring FA, Parsons SF, Brady RL, Mohandas N, Chasis JA, et al. Identification of critical amino-acid residues on the erythroid intercellular adhesion molecule-4 (ICAM-4) mediating adhesion to alpha V integrins. Blood. 2004;103:1503–1508
  73. Hermand P, Gane P, Huet M, Jallu V, Kaplan C, Sonneborn HH, et al. Red cell ICAM-4 is a novel ligand for platelet-activated alpha IIbbeta 3 integrin. J Biol Chem. 2003;278:4892–4898
  74. Hermand P, Gane P, Callebaut I, Kieffer N, Cartron JP, Bailly P. Integrin receptor specificity for human red cell ICAM-4 ligand. Critical residues for alphaIIbeta3 binding. Eur J Biochem. 2004;271:3729–3740
  75. Zennadi R, Hines PC, De Castro LM, Cartron JP, Parise LV, Telen MJ. Epinephrine Acts Via Erythroid Signaling Pathways to Activate Sickle Cell Adhesion to Endothelium Via LW-{alpha}v{beta}3 Interactions. Blood. 2004;
  76. Blumenfeld OO, Huang CH. Molecular genetics of the glycophorin gene family, the antigens for MNSs blood groups: multiple gene rearrangements and modulation of splice site usage result in extensive diversification. Hum Mutat. 1995;6:199–209
  77. Cartron JP, Rahuel C. MNSs and major glycophorins of human erythrocytes. Transfus Clin Biol. 1995;2:251–258
  78. 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
  79. Bruce LJ, Beckmann R, Ribeiro ML, Peters LL, Chasis JA, Delaunay J, et al. A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood. 2003;101:4180–4188
  80. Bowman JM. RhD hemolytic disease of the newborn. N Engl J Med. 1998;339:1775–1777
  81. Kumpel BM, Elson CJ. Mechanism of anti-D-mediated immune suppression–a paradox awaiting resolution?. Trends Immunol. 2001;22:26–31
  82. Hartwell EA. Use of Rh immune globulin: ASCP practice parameter. American Society of Clinical Pathologists. Am J Clin Pathol. 1998;110:281–292
  83. Bennett PR, Le Van Kim C, Colin Y, Warwick RM, Cherif-Zahar B, Fisk NM, et al. Prenatal determination of fetal RhD type by DNA amplification. N Engl J Med. 1993;329:607–610
  84. Lo YM, Hjelm NM, Fidler C, Sargent IL, Murphy MF, Chamberlain PF, et al. Prenatal diagnosis of fetal RhD status by molecular analysis of maternal plasma. N Engl J Med. 1998;339:1734–1738
  85. Rouillac-Le Sciellour C, Puillandre P, Gillot R, Baulard C, Métral S, Le Van Kim C, et al. Large scale prediagnosis study of fetal RhD genotyping by PCR on plasma DNA from Rh-negative pregnant women. Molecular Diagnosis 2004;in press.
  86. Costa JM, Gautier E, Benachi A. [Genetic analysis of the fetus using maternal blood]. Gynecol Obstet Fertil. 2004;32:646–650
  87. Finning K, Martin P, Daniels G. A clinical service in the UK to predict fetal Rh (Rhesus) D blood group using free fetal DNA in maternal plasma. Ann N Y Acad Sci. 2004;1022:119–123
  88. Finning KM, Martin PG, Soothill PW, Avent ND. Prediction of fetal D status from maternal plasma: introduction of a new noninvasive fetal RHD genotyping service. Transfusion. 2002;42:1079–1085
  89. Chiu RW, Lo YM. Non-invasive prenatal diagnosis: on the horizon?. Pharmacogenomics. 2003;4:191–200
  90. Rijn der RJ, Christianens GC, Bassers B, Van der Smagt JJ, Van der Shoot CE, de Hass M. Clinical applications of cell-free fetal DNA from material plasma. Obset Gynecol. 2004;103:157–164
  91. Li Y, Zimmermann B, Zhong XY, Gupta AK, Holzgreve W, Hahn S. Determination of RHD zygosity using real-time quantitative PCR. Swiss Med Wkly. 2003;133:442–445
  92. Mohandas N, Chasis JA. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol. 1993;30:171–192
  93. Discher DE, Mohandas N, Evans EA. Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science. 1994;266:1032–1035
  94. Delaunay J. Molecular basis of red cell membrane disorders. Acta Haematol. 2002;108:210–218
  95. Nunomura W, Takakuwa Y, Parra M, Conboy J, Mohandas N. Regulation of protein 4.1R, p55, and glycophorin C ternary complex in human erythrocyte membrane. J Biol Chem. 2000;275:24540–24546
  96. Bhattacharyya R, Das AK, Moitra PK, Pal B, Mandal I, Basu J. Mapping of a palmitoylatable band 3-binding domain of human erythrocyte membrane protein 4.2. Biochem J. 1999;340(Pt 2):505–512
  97. Ridgwell K, Tanner MJ, Anstee DJ. The Rhesus (D) polypeptide is linked to the human erythrocyte cytoskeleton. FEBS Lett. 1984;174:7–10
  98. Gahmberg CG, Karhi KK. Association of Rho(D) polypeptides with the membrane skeleton in Rho(D)-positive human red cells. J Immunol. 1984;133:334–337
  99. Gane P, Le Van Kim C, Bony V, El Nemer W, Mouro I, Nicolas V, et al. Flow cytometric analysis of the association between blood group-related proteins and the detergent-insoluble material of K562 cells and erythroid precursors. Br J Haematol. 2001;113:680–688
  100. Murphy SC, Samuel BU, Harrison T, Speicher KD, Speicher DW, Reid ME, et al. Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood. 2003;
  101. Dahl KN, Westhoff CM, Discher DE. Fractional attachment of CD47 (IAP) to the erythrocyte cytoskeleton and visual colocalization with Rh protein complexes. Blood. 2003;101:1194–1199
  102. Gimm A, Mouro I, Lambin P, Mohandas N, Cartron JP. Direct evidence for in situ interaction between Rh complex and membrane skeleton in intact red cells. Vox Sanguinis. 2000;78(Suppl1):14;(abstract)
  103. Dahl KN, Parthasarathy R, Westhoff CM, Layton DM, Discher DE. Protein 4.2 is critical to CD47-membrane skeleton attachment in human red cells. Blood. 2004;103:1131–1136
  104. Bruce LJ, Ghosh S, King MJ, Layton DM, Mawby WJ, Stewart GW, et al. Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex. Blood. 2002;100:1878–1885
  105. Nicolas V, Le Van Kim C, Cartron JP, Colin Y, Mouro-Chanteloup I. Critical residues for Rh/RhAG binding to ankyrin-R are mutated in some weak-D variants. Vox Sang. 2004;87:9
  106. Cartron JP, Colin Y. Bases moléculaires du systême RH et du syndrome Rhnull. Hématologie. 1997;3:207–220
  107. Delaunay J. Red cell membrane and erythropoiesis genetic defects. Hematol J. 2003;4:225–232
  108. Matassi G, Cherif-Zahar B, Raynal V, Rouger P, Cartron JP. Organization of the human RH50A gene (RHAG) and evolution of base composition of the RH gene family. Genomics. 1998;47:286–293
  109. Kitano T, Sumiyama K, Shiroishi T, Saitou N. Conserved evolution of the Rh50 gene compared to its homologous Rh blood group gene. Biochem Biophys Res Commun. 1998;249:78–85
  110. Matassi G, Cherif-Zahar B, Pesole G, Raynal V, Cartron JP. The members of the RH gene family (RH50 and RH30) followed different evolutionary pathways. J Mol Evol. 1999;48:151–159
  111. Carritt B, Kemp TJ, Poulter M. Evolution of the human RH (rhesus) blood group genes: a 50 year old prediction (partially) fulfilled. Hum Mol Genet. 1997;6:843–850
  112. Blancher A, Klein J, Socha WW. Molecular biology and evolution of blood group and MHC antigens in primates. Berlin: Springer-Verlag; 1997;
  113. Kitano T, OOta S, Saitou N. Molecular evolutionary analyses of the Rh blood group genes and Rh50 genes in mammals. Zoological Studies. 1999;38:379–386
  114. Huang CH, Liu Z, Apoil PA, Blancher A. Sequence, organization, and evolution of Rh50 glycoprotein genes in nonhuman primates. J Mol Evol. 2000;51:303–304
  115. Innan H. A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes. Proc Natl Acad Sci U S A. 2003;100:8793–8798
  116. Marini AM, Urrestarazu A, Beauwens R, Andre B. The Rh (rhesus) blood group polypeptides are related to NH4+ transporters. Trends Biochem Sci. 1997;22:460–461
  117. Lorenz MC, Heitman J. Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics. 1998;150:1443–1457
  118. Liu Z, Chen Y, Mo R, Hui C, Cheng JF, Mohandas N, et al. Characterization of human RhCG and mouse Rhcg as novel nonerythroid Rh glycoprotein homologues predominantly expressed in kidney and testis. J Biol Chem. 2000;275:25641–25651
  119. Liu Z, Peng J, Mo R, Hui C, Huang CH. Rh type B glycoprotein is a new member of the Rh superfamily and a putative ammonia transporter in mammals. J Biol Chem. 2001;276:1424–1433
  120. Marini AM, Matassi G, Raynal V, Andre B, Cartron JP, Cherif-Zahar B. The human Rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nat Genet. 2000;26:341–344
  121. Huang CH, Liu PZ. New insights into the Rh superfamily of genes and proteins in erythroid cells and nonerythroid tissues. Blood Cells Mol Dis. 2001;27:90–101
  122. Westhoff CM, Siegel DL, Burd CG, Foskett JK. Mechanism of genetic complementation of ammonium transport in yeast by human erythrocyte Rh-associated glycoprotein (RhAG. J Biol Chem. 2004;
  123. Westhoff CM, Ferreri-Jacobia M, Mak DO, Foskett JK. Identification of the erythrocyte Rh blood group glycoprotein as a mammalian ammonium transporter. J Biol Chem. 2002;277:12499–12502
  124. Nakhoul NL, DeJong H, Abdulnour-Nakhoul SM, Boulpaep EL, Hering-Smith K, Hamm LL. Characteristics of Renal Rhbg as an NH4+ Transporter. Am J Physiol Renal Physiol. 2004;
  125. Ludewig U. Electroneutral ammonium transport by basolateral rhesus B glycoprotein. J Physiol. 2004;559:751–759
  126. Bakouh N, Benjelloun F, Hulin P, Brouillard F, Edelman A, Cherif-Zahar B, et al. NH3 is involved in the NH4+ transport induced by the functional expression of the human RhC glycoprotein. J Biol Chem. 2004;
  127. Burckhardt BC, Fromter E. Pathways of NH3/NH4+ permeation across Xenopus laevis oocyte cell membrane. Pflugers Arch. 1992;420:83–86
  128. Cougnon M, Bouyer P, Hulin P, Anagnostopoulos T, Planelles G. Further investigation of ionic diffusive properties and of NH4+ pathways in Xenopus laevis oocyte cell membrane. Pflugers Arch. 1996;431:658–667
  129. Labotka RJ, Lundberg P, Kuchel PW. Ammonia permeability of erythrocyte membrane studied by 14N and 15N saturation transfer NMR spectroscopy. Am J Physiol. 1995;268:C686–C699
  130. Ripoche P, Bertrand O, Gane P, Birkenmeier C, Colin Y, Cartron JP. Human Rhesus-associated glycoprotein mediates facilitated transport of NH3 into red blood cells. Proc Natl Acad Sci U S A. 2004;101:17222–17227
  131. Hemker MB, Cheroutre G, van Zwieten R, Maaskant-van Wijk PA, Roos D, Loos JA, et al. The Rh complex exports ammonium from human red blood cells. Br J Haematol. 2003;122:333–340
  132. Handlogten ME, Hong SP, Westhoff CM, Weiner ID. Basolateral ammonium transport by the mouse inner medullary collecting duct cell (mIMCD-3). Am J Physiol Renal Physiol. 2004;287:F628–F638
  133. Zidi-Yahiaoui N, Mouro-Chanteloup I, D’Ambrosio A, Lopez C, Gane P, Le Van Kim C, et al. Human Rhesus B and Rhesus C glycoproteins: Properties of facilitated ammonium transport on recombinant kidney cells. Biochem J, in press.
  134. Khademi S, O’Connell J, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM. Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science. 2004;305:1587–1594
  135. Conroy MJ, Jamieson SJ, Blakey D, Kaufmann T, Engel A, Fotiadis D, et al. Electron and atomic force microscopy of the trimeric ammonium transporter AmtB. EMBO Rep. 2004;
  136. Blakey D, Leech A, Thomas GH, Coutts G, Findlay K, Merrick M. Purification of the Escherichia coli ammonium transporter AmtB reveals a trimeric stoichiometry. Biochem J. 2002;364:527–535
  137. 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;
  138. Soupene E, Ramirez RM, Kustu S. Evidence that fungal MEP proteins mediate diffusion of the uncharged species NH(3) across the cytoplasmic membrane. Mol Cell Biol. 2001;21:5733–5741
  139. Forster RE, Gros G, Lin L, Ono Y, Wunder M. The effect of 4,4’-diisothiocyanato-stilbene-2,2’-disulfonate on CO2 permeability of the red blood cell membrane. Proc Natl Acad Sci U S A. 1998;95:15815–15820
  140. Soupene E, Lee H, Kustu S. Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proc Natl Acad Sci U S A. 2002;99:3926–3931
  141. Soupene E, King N, Feild E, Liu P, Niyogi KK, Huang CH, et al. Rhesus expression in a green alga is regulated by CO(2). Proc Natl Acad Sci U S A. 2002;99:7769–7773
  142. Asamizu E, Miura K, Kucho K, Inoue Y, Fukuzawa H, Ohyama K, et al. Generation of expressed sequence tags from low-CO2 and high-CO2 adapted cells of Chlamydomonas reinhardtii. DNA Res. 2000;7:305–307
  143. Soupene E, Inwood W, Kustu S. From The Cover: Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. Proc Natl Acad Sci U S A. 2004;101:7787–7792
  144. Benghezal M, Gotthardt D, Cornillon S, Cosson P. Localization of the Rh50-like protein to the contractile vacuole in Dictyostelium. Immunogenetics. 2001;52:284–288
  145. Kosenko E, Kaminsky YG, Felipo V, Minana MD, Grisolia S. Chronic hyperammonemia prevents changes in brain energy and ammonia metabolites induced by acute ammonium intoxication. Biochim Biophys Acta. 1993;1180:321–326
  146. Huizenga JR, Tangerman A, Gips CH. Determination of ammonia in biological fluids. Ann Clin Biochem. 1994;31(Pt 6):529–543
  147. Eladari D, Cheval L, Quentin F, Bertrand O, Mouro I, Cherif-Zahar B, et al. Expression of RhCG, a new putative NH (3)/NH (4)(+) transporter, along the rat nephron. J Am Soc Nephrol. 2002;13:1999–2008
  148. Quentin F, Eladari D, Cheval L, Lopez C, Goossens D, Colin Y, et al. RhBG and RhCG, the putative ammonia transporters, are expressed in the same cells in the distal nephron. J Am Soc Nephrol. 2003;14:545–554
  149. Verlander JW, Miller RT, Frank AE, Royaux IE, Kim YH, Weiner ID. Localization of the ammonium transporter proteins RhBG and RhCG in mouse kidney. Am J Physiol Renal Physiol. 2003;284:F323–F337
  150. Weiner ID, Miller RT, Verlander JW. Localization of the ammonium transporters, Rh B glycoprotein and Rh C glycoprotein, in the mouse liver. Gastroenterology. 2003;124:1432–1440
  151. Knepper MA, Packer R, Good DW. Ammonium transport in the kidney. Physiol Rev. 1989;69:179–249
  152. Humphreys BD, Chernova MN, Jiang L, Zhang Y, Alper SL. NH4Cl activates AE2 anion exchanger in Xenopus oocytes at acidic pHi. Am J Physiol. 1997;272:C1232–C1240
  153. Franch HA. Modification of the epidermal growth factor response by ammonia in renal cell hypertrophy. J Am Soc Nephrol. 2000;11:1631–1638
  154. Nakhoul NL, Hering-Smith KS, Abdulnour-Nakhoul SM, Hamm LL. Ammonium interaction with the epithelial sodium channel. Am J Physiol Renal Physiol. 2001;281:F493–F502
  155. Chernova MN, Stewart AK, Jiang L, Friedman DJ, Kunes YZ, Alper SL. Structure-function relationships of AE2 regulation by Ca (i) (2+)-sensitive stimulators NH (4+) and hypertonicity. Am J Physiol Cell Physiol. 2003;284:C1235–C1246
  156. Knepper MA, Agre P. Structural biology. The atomic architecture of a gas channel. Science. 2004;305:1573–1574

PII: S0268-960X(05)00029-9

doi: 10.1016/j.blre.2005.04.002

Blood Reviews
Volume 20, Issue 2 , Pages 93-110 , March 2006

Article Tools

* Image Usage & Resolution