The Rh gene family and renal ammonium transport

Current Opinion in Nephrology and Hypertension

Volumn 13, Issue 5, 2004, Pages 533-540

  Weiner, I David ^a,b  

^a Geriatric Research Education and Clinical Center   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Acidosis; Ammonium; Cation chloride cotransporter; Collecting duct; Intercalated cell; Rh proteins

Indexed keywords

AMMONIA; AMMONIA TRANSPORTER; CARRIER PROTEIN; GLYCOPROTEIN; UNCLASSIFIED DRUG;

ACID BASE BALANCE; BLOOD GROUP RH; BLOOD GROUP RHESUS SYSTEM; CELLULAR DISTRIBUTION; GENE FUNCTION; HUMAN; ION TRANSPORT; KIDNEY COLLECTING TUBULE; KIDNEY METABOLISM; KIDNEY TUBULE ABSORPTION; KIDNEY TUBULE EXCRETION; MOLECULAR PHYLOGENY; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW;

ANIMALS; BIOLOGICAL TRANSPORT; GLYCOPROTEINS; HUMANS; KIDNEY; KIDNEY TUBULES, COLLECTING; MEMBRANE TRANSPORT PROTEINS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 4344713582     PISSN: 10624821     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041552-200409000-00009     Document Type: Review

References (72)

1. Hamm LL, Simon EE. Roles and mechanisms of urinary buffer excretion. Am J Physiol 1987; 253:F595-F605.
2. Halperin ML, Jungas RL. Metabolic production and renal disposal of hydrogen ions. Kidney Int 1983; 24:709-713.
3. Carlisle EJ, Donnelly SM, Halperin ML. Renal tubular acidosis (RTA): recognize the ammonium defect and pHorget the urine pH. Pediatric Nephrol 1991; 5:242-248.
4. Nagami GT. Ammonia production and secretion by the proximal tubule. Am J Kidney Dis 1989; 14:258-261.
5. Simon EE, Merli C, Herndon J, et al. Effects of barium and 5-(N-ethyl-N-isopropyl)-amiloride on proximal tubule ammonia transport. Am J Physiol 1992; 262:F36-F39.
6. Hamm LL, Simon EE. Ammonia transport in the proximal tubule. Min Electrolyte Metab 1990; 16:283-290.
7. 3. Nature 1989; 339:478-480.
8. Amlal H, Paillard M, Bichara M. NH4+ transport pathways in cells of medullary thick ascending limb of rat kidney. NH4+ conductance and K+/ NH4+(H+) antiport. J Biol Chemistry 1994; 269:21962-21971.
9. Attmane-Elakeb A, Amlal H, Bichara M. Ammonium carriers in medullary thick ascending limb. Am J Physiol Renal Physiol 2001; 280:F1-F9.
10. Bettinelli A, Ciarmatori S, Cesareo L, et al. Phenotypic variability in Bartter syndrome type I. Pediatric Nephrol 2000; 14:940-945.
11. Rodriguez-Soriano J. Bartter and related syndromes: the puzzle is almost solved. Pediatric Nephrol 1998; 12:315-327.
12. Tannen RL, Sahai A. Biochemical pathways and modulators of renal ammoniagenesis. Min Electrolyte Metab 1990; 16:249-258.
13. DiGiovanni SR, Madsen KM, Luther AD, Knepper MA. Dissociation of ammoniagenic enzyme adaptation in rat S1 proximal tubules and ammonium excretion response. Am J Physiol 1994; 267:F407-F414.
14. Nagami GT. Enhanced ammonia secretion by proximal tubules from mice receiving NH(4)Cl: role of angiotensin II. Am J Physiol Renal Physiol 2002; 282:F472-F477.
15. Nagami GT, Sonu CM, Kurokawa K. Ammonia production by isolated mouse proximal tubules perfused in vitro: effect of metabolic acidosis. J Clin Invest 1986; 78:124-129.
16. Ambuhl PM, Amemiya M, Danczkay M, et al. Chronic metabolic acidosis increases NHE3 protein abundance in rat kidney. Am J Physiol 1996; 271:F917-F925.
17. Attmane-Elakeb A, Mount DB, Sibella V, et al. Stimulation by in vivo and in vitro metabolic acidosis of expression of rBSC-1, the Na+-K+(NH4+)-2Cl- cotransporter of the rat medullary thick ascending limb. J Biol Chem 1998; 273:33681-33691.
18. + intake. Am J Physiol 1990; 258:F1345-F1353.
19. Sajo IM, Goldstein MB, Sonnenberg H, et al. Sites of ammonia addition to tubular fluid in rats with chronic metabolic acidosis. Kidney Int 1982; 20:353-358.
20. + transport in the kidney. Kidney Int 1991; 40:S95-S102.
21. Flessner MF, Knepper MA. Ammonium transport in collecting ducts. Min Electrolyte Metab 1990; 16:299-307.
22. +. Am J Physiol 1991; 260:F264-F272.
23. Wall SM, Fischer MP. Contribution of the Na(+)-K(+)-2Cl(-) cotransporter (NKCC1) to transepithelial transport of H(+), NH(4)(+), K(+), and Na(+) in rat outer medullary collecting duct. J Am Soc Nephrol 2002; 13:827-835.
24. Melton LB, Vanatta JC. Ammonia transport by the urinary bladder of Bufo marinus. Comp Biochem Physiol A Physiol 1996; 115:153-158.
25. Talor Z, Lubansky HJ, Arruda JA. Relationship of K and ammonia transport by the turtle bladder. Min Electrolyte Metab 1987; 13:78-84.
26. Arruda JA, Dytko G, Withers L. Ammonia transport by the turtle urinary bladder. Am J Physiol 1984; 246:F635-F647.
27. Wall SM. NH4+ augments net acid-secretion by a ouabain-sensitive mechanism in isolated-perfused inner medullary collecting ducts. Am J Physiol 1996; 270:F432-F439.
28. Wall SM, Koger LM. NH+4 transport mediated by Na(+)-K(+)-ATPase in rat inner medullary collecting duct. Am J Physiol 1994; 267:F660-F670.
29. Knepper MA, Good DW, Burg MB. Mechanism of ammonia secretion by cortical collecting ducts of rabbits. Am J Physiol 1984; 247:F729-F738.
30. Dubois E, Grenson M. Methylamine/ammonia uptake systems in Saccharomyces cerevisiae: multiplicity and regulation. Mol Gen Genet 1979; 175:67-76.
31. Marini AM, Vissers S, Urrestarazu A, Andre B. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 1994; 13:3456-3463.
32. Ninnemann O, Jauniaux JC, Frommer WB. Identification of a high affinity NH4+ transporter from plants. EMBO J 1994; 13:3464-3471.
33. Marini AM, Soussi-Boudekou S, Vissers S, Andre B. A family of ammonium transporters in Saccnaromyces cerevisiae. Mol Cell Biol 1997; 17:4282-4293.
34. von Wiren N, Gazzarrini S, Gojon A, Frommer WB. The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 2000; 3:254-261.
35. Gazzarrini S, Lejay L, Gojon A, et al. Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 1999; 11:937-948.
36. Sohlenkamp C, Shelden M, Howitt S, Udvardi M. Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. FEBS Lett 2000; 467:273-278.
37. 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.
38. Marini AM, Matassi G, Raynal V, et al. The human rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nat Genet 2000; 26:341-344.
39. Liu Z, Chen Y, Mo R, 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.
40. Liu Z, Peng J, Mo R, et al. 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.
41. Liu Z, Huang CH. The mouse Rhl1 and Rhag genes: sequence, organization, expression, and chromosomal mapping. Biochem Genet 1999; 37:119-138.
42. Haussinger D. Hepatocyte heterogeneity in glutamine and ammonia metabolism and the role of an intercellular glutamine cycle during ureogenesis in perfused rat liver. Eur J Biochem 1983; 133:269-275.
43. 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. Although not a subject of this review, RhBG and RhCG are also expressed in the liver. RhBG is expressed by the perivenous hepatocyte cells that mediate high-affinity ammonia detoxification and conversion to glutamine. RhCG is expressed in bile duct epithelia, where it may mediate biliary ammonia secretion.
44. Brusilow SW, Gordes EH. Ammonia secretion in sweat. Am J Physiol 1968; 214:513-517.
45. Quentin F, Eladari D, Cheval L, 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. This study describes the localization of the Rh glycoprotein, RhBG, in the rat DCT, CNT and collecting duct, and shows that both RhBG and RhCG are expressed in the same cells, albeit at differing membranes, apical for RhCG and basolateral for RhBG.
46. Verlander JW, Miller RT, Frank AE, et al. Localization of the ammonium transporter proteins, Rh B glycoprotein and Rh C glycoprotein, in the mouse kidney. Am J Physiol Renal Physiol 2003; 284:F323-F337. This study demonstrates that RhBG and RhCG are expressed in the basolateral and apical membranes, respectively, in the mouse CNT and collecting duct. The CCD B-type intercalated cell does not express identifiable RhBG immunoreactivity, suggesting that it is unlikely to mediate ammonia secretion, and is consistent with this cell contributing to bicarbonate secretion and recovery from alkalosis.
47. Jalan R, Shawcross D, Davies N. The molecular pathogenesis of hepatic encephalopathy. Int J Biochem Cell Biol 2003; 35:1175-1181.
48. Cooper AJ, Plum F. Biochemistry and physiology of brain ammonia. Physiol Rev 1987; 67:440-519.
49. Eladari D, Cheval L, Quentin F, et al. Expression of RhCG, a new putative NH3/NH4+ transporter, along the rat nephron. J Am Soc Nephrol 2002; 13:1999-2008.
50. Flessner MF, Wall SM, Knepper MA. Ammonium and bicarbonate transport in rat outer medullary collecting ducts. Am J Physiol 1992; 262:F1-F7.
51. Star RA, Kurtz I, Mejia R, et al. Disequilibrium pH and ammonia transport in isolated perfused cortical collecting ducts. Am J Physiol 1987; 253:F1232-F1242.
52. Knepper MA, Good DW, Burg MB. Ammonia and bicarbonate transport by rat cortical collecting ducts perfused in vitro. Am J Physiol 1985; 249:F870-F877.
53. Ludewig U, von Wiren N, Frommer WB. Uniport of NH4+ by the root hair plasma membrane ammonium transporter LeAMT1:1. J Biol Chem 2002; 277:13548-13555.
54. 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.
55. 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.
56. +/hydrogen exchanger when heterologously expressed in Saccharomyces cerevisiae.
57. Westhoff CM, Ferreri-Jacobia M, Mak DD, Foskett JK. Identification of the erythrocyte Rh-blood group glycoprotein as a mammalian ammonium transporter. J Biol Chem 2002; 277:12499-12502.
58. 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. A genetic absence of RhAG leads to the decreased ability of erythrocytes to export ammonia, confirming the importance of RhAG in erythroid ammonia transport.
59. Nakhoul NL, Abdulnour-Nakhoul S, DeJong H, Hamm LL. Ammonium transport by Rhbg glycoprotein [Abstract]. Faseb J 2003; 17:A467.
60. Westhoff CM, Weiner ID, Foskett JK. Transport characteristics of the putative ammonium transporters, Rh B glycoprotein and Rh C glycoprotein, when expressed in the Xenopus oocyte [Abstract]. J Am Soc Nephrol 2003; 14:304A.
61. + transport activity.
62. Nakhoul NL, Palmer SA, Abdulnour-Nakhoul S, et al. Ammonium transport in oocytes expressing Rhcg [Abstract]. Faseb J 2002; 16:A53.
63. +/hydrogen exchange activity that may be mediated by RhBG.
64. Weiner ID, Handlogten ME. Apical ammonia transport by the mouse collecting duct, mIMCD-3, cell [Abstract]. Faseb J 2004; 18:A1017.
65. Soupene E, Inwood W, Kustu S. 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. The green algae, C. reinhardtii, has a Rh1 protein homologous to Rh glycoproteins that appears to be involved in carbon dioxide transport.
66. Soupene E, King N, Feild E, et al. Rhesus expression in a green alga is regulated by CO(2). Proc Natl Acad Sci U S A 2002; 99:7769-7773.
67. + at their potassium-binding site.
68. +.
69. Velazquez H, Silva T. Cloning and localization of KCC4 in rabbit kidney: expression in distal convoluted tubule. Am J Physiol Renal Physiol 2003; 285:F49-F58. In this study, KCC4 was widely expressed in the rabbit kidney, suggesting that it mediates an important role in renal ion transport.
70. Boettger T, Hubner CA, Maier H, et al. Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4. Nature 2002; 416:874-878. In this study, a failure to express KCC4 leads to deafness and an apparent distal renal tubular acidosis that appears to be caused by the failure of proton secretion.
71. Liapis H, Nag M, Kaji DM. K-Cl cotransporter expression in the human kidney. Am J Physiol 1998; 275:C1432-C1437.
72. Race JE, Makhlouf FN, Logue PJ, et al. Molecular cloning and functional characterization of KCC3, a new K-Cl cotransporter. Am J Physiol 1999; 277:C1210-C1219.