Sequence- or position-specific mutations in the carboxyl-terminal FL motif of the kidney sodium bicarbonate cotransporter (NBC1) disrupt its basolateral targeting and α-helical structure

Journal of Membrane Biology

Volumn 228, Issue 2, 2009, Pages 111-124

  Li, Hong C ^a,b   Collier, Joel H ^c   Shawki, Ali ^a   Rudra, Jai S ^c   Li, Emily Y ^a,b   MacKenzie, Bryan ^a   Soleimani, Manoocher ^a,b,d  

^a UNIVERSITY OF CINCINNATI   (United States)

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

^c UNIVERSITY OF CHICAGO   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acid base transporters; Epithelial transport; Intestinal and renal transport; Intracellular pH regulation

Indexed keywords

BICARBONATE SODIUM COTRANSPORTER; BICARBONATE SODIUM COTRANSPORTER 1; EPITOPE; MUTANT PROTEIN; PROTEIN DISULFIDE ISOMERASE; RNA; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE MUTATION; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; WILD TYPE; XENOPUS LAEVIS;

AMINO ACID MOTIFS; ANIMALS; BLOTTING, WESTERN; CELL LINE; CIRCULAR DICHROISM; DOGS; HUMANS; MICROSCOPY, CONFOCAL; MUTATION; OOCYTES; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; SODIUM-BICARBONATE SYMPORTERS; STRUCTURE-ACTIVITY RELATIONSHIP; XENOPUS LAEVIS;

EID: 63149161737     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-009-9164-6     Document Type: Article

References (54)

1. N Abuladze R Azimov D Newman P Sassani W Liu S Tatishchev A Pushkin I Kurtz 2005 Critical amino acid residues involved in the electrogenic sodium-bicarbonate cotransporter kNBC1-mediated transport J Physiol 565 717 730
2. SL Alper 2002 Genetic diseases of acid-base transporters Annu Rev Physiol 64 899 923
3. X Bai X Chen Z Feng K Hou P Zhang B Fu S Shi 2006 Identification of basolateral membrane targeting signal of human sodium-dependent dicarboxylate transporter 3 J Cell Physiol 206 821 830
4. S Barman A Ali EK Hui L Adhikary DP Nayak 2001 Transport of viral proteins to the apical membranes and interaction of matrix protein with glycoproteins in the assembly of influenza viruses Virus Res 77 61 69
5. V Bello JW Goding V Greengrass A Sali V Dubljevic C Lenoir G Trugnan M Maurice 2001 Characterization of a di-leucine-based signal in the cytoplasmic tail of the nucleotide-pyrophosphatase NPP1 that mediates basolateral targeting but not enocytosis Mol Biol Cell 12 3004 3015
6. D Bok MJ Schibler A Pushkin P Sassani N Abuladze Z Naser I Kurtz 2001 Immunolocalization of electrogenic sodium-bicarbonate cotransporters pNBC1 and kNBC1 in the rat eye Am J Physiol Renal Physiol 281 F920 F935
7. WF Boron 2006 Acid-base transport by the renal proximal tubule J Am Soc Nephrol 17 2368 2382
8. DA Brown JK Rose 1992 Sorting GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface Cell 68 533 544
9. - cotransporter J Biol Chem 272 19111 19114
10. MA Devonald AN Smith JP Poon G Ihrke FE Karet 2003 Non-polarized targeting of AE1 causes autosomal dominant distal renal tubular acidosis Nat Genet 33 125 127
11. D Dinour MH Chang J Satoh BL Smith N Angle A Knecht I Serban EJ Holtzman MF Romero 2004 A novel missense mutation in the sodium bicarbonate cotransporter (NBCe1/SLC4A4) causes proximal tubular acidosis and glaucoma through ion transport defects J Biol Chem 279 52238 52246
12. M Grati N Aggarwal EE Strehler RJ Wenthold 2006 Molecular determinants for differential membrane trafficking of PMCA1 and PMCA2 in mammalian hair cells J Cell Sci 119 2995 3007
13. NJ Greenfield 2006 Using circular dichroism spectra to estimate protein secondary structure Nat Protoc 1 2876 2890
14. A Gut F Kappeler N Hyka MS Balda HP Hauri K Matter 1998 Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins EMBO J 17 1919 1929
15. S Horita H Yamada J Inatomi N Moriyama T Sekine T Igarashi Y Endo M Dasouki M Ekim L Al-Gazali M Shimadzu G Seki T Fujita 2005 Functional analysis of NBC1 mutants associated with proximal renal tubular acidosis and ocular abnormalities J Am Soc Nephrol 16 2270 2278
16. W Hunziker C Fumey 1994 A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells EMBO J 13 2963 2969
17. T Igarashi J Inatomi T Sekine SH Cha Y Kanai M Kunimi K Tsukamoto H Satoh M Shimadzu F Tozawa T Mori M Shiobara G Seki H Endou 1999 Mutations in SLC4A4 cause permanent isolated proximal renal tubular acidosis with ocular abnormalities Nat Genet 23 264 266
18. - cotransporter gene (SLC4A4) in a patient with permanent isolated proximal renal tubular acidosis and bilateral glaucoma J Am Soc Nephrol 12 713 718
19. E Ikonen 2001 Roles of lipid rafts in membrane transport Curr Opin Cell Biol 13 470 477
20. A Kundu RT Avalos CM Sanderson DP Nayak 1996 Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells J Virol 70 6508 6515
21. - cotransporter NBC1 to the basolateral membrane J Biol Chem 279 43190 43197
22. - cotransporter NBC1 show abnormal trafficking in polarized kidney cells: a basis of proximal renal tubular acidosis Am J Physiol Renal Physiol 289 F61 F71
23. - cotransporter NBC1 that mediates basolateral targeting Am J Physiol Renal Physiol 292 F1245 F1255
24. S Lin HY Naim AC Rodriguez MG Roth 1998 Mutations in the middle of the transmembrane domain reverse the polarity of transport of the influenza virus hemagglutinin in MDCK epithelial cells J Cell Biol 142 51 57
25. Mackenzie B (1999) Selected techniques in membrane transport. In: Biomembrane transport. Academic Press, San Diego, pp 327-342
26. B Mackenzie H Takanaga N Hubert A Rolfs MA Hediger 2007 Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1) Biochem J 403 59 69
27. K Matter W Hunziker I Mellman 1992 Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants Cell 71 741 753
28. K Matter I Mellman 1994 Mechanisms of cell polarity: sorting and transport in epithelial cells Curr Opin Cell Biol 6 545 554
29. K Matter EM Yamamoto I Mellman 1994 Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells J Cell Biol 126 991 1004
30. KC Miranda T Khromykh P Christy TL Le CJ Gottardi AS Yap JL Stow RD Teasdale 2001 A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells J Biol Chem 276 22565 22572
31. TR Muth MJ Caplan 2003 Transport protein trafficking in polarized cells Annu Rev Cell Dev Biol 19 333 366
32. G Pena-Munzenmayer M Catalan I Cornejo CD Figueroa JE Melvin MI Niemeyer LP Cid FV Sepulveda 2005 Basolateral localization of native ClC-2 chloride channels in absorptive intestinal epithelial cells and basolateral sorting encoded by a CBS-2 domain di-leucine motif J Cell Sci 118 4243 4252
33. 2-) transporters: classification, function, structure, genetic diseases, and knockout models Am J Physiol Renal Physiol 290 F580 F599
34. RR Regeer D Markovich 2004 A dileucine motif targets the sulfate anion transporter sat-1 to the basolateral membrane in renal cell lines Am J Physiol Cell Physiol 287 C365 C372
35. MF Romero 2005 Molecular pathophysiology of SLC4 bicarbonate transporters Curr Opin Nephrol Hypertens 14 495 501
36. - cotransporter Nature 387 409 413
37. 3-transporters Pflugers Arch 447 495 509
38. E Roussa MF Romero BM Schmitt WF Boron SL Alper F Thevenod 1999 Immunolocalization of anion exchanger AE2 and Na(+)-HCO(-)(3) cotransporter in rat parotid and submandibular glands Am J Physiol 277 G1288 G1296
39. P Scheiffele J Peranen K Simons 1995 N-Glycans as apical sorting signals in epithelial cells Nature 378 96 98
40. - cotransporter in mammalian and amphibian kidney Am J Physiol Renal Physiol 276 F27 F38
41. H Sheikh CM Isacke 1996 A di-hydrophobic Leu-Val motif regulates the basolateral localization of CD44 in polarized Madin-Darby canine kidney epithelial cells J Biol Chem 271 12185 12190
42. K Simons E Ikonen 1997 Functional rafts in cell membrane Nature 387 569 572
43. - cotransporters (NBC): expression and regulation in the kidney J Nephrol 15 Suppl 5 S32 S40
44. - cotransporters (NBC) Minerva Urol Nefrol 55 131 140
45. - cotransporters (NBC): cloning and characterization J Membr Biol 183 71 84
46. M Tanemoto T Abe S Ito 2005 PDZ-binding and di-hydrophobic motifs regulate distribution of Kir4.1 channels in renal cells J Am Soc Nephrol 16 2608 2614
47. U Tepass G Tanentzapf R Ward R Fehon 2001 Epithelial cell polarity and cell junctions in Drosophila Annu Rev Genet 35 747 784
48. F Thevenod E Roussa BM Schmitt MF Romero 1999 Cloning and immunolocalization of a rat pancreatic Na(+) bicarbonate cotransporter Biochem Biophys Res Commun 264 291 298
49. DC Thomas CB Brewer MG Roth 1993 Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine J Biol Chem 268 3313 3320
50. AM Toye MD Parker CM Daly J Lu LV Virkki MF Pelletier WF Boron 2006 The human NBCe1-A mutant R881C, associated with proximal renal tubular acidosis, retains function but is mistargeted in polarized renal epithelia Am J Physiol Cell Physiol 291 C788 C801
51. T Usui M Hara H Satoh N Moriyama H Kagaya S Amano T Oshika Y Ishii N Ibaraki C Hara M Kunimi E Noiri K Tsukamoto J Inatomi H Kawakami H Endou T Igarashi A Goto T Fujita M Araie G Seki 2001 Molecular basis of ocular abnormalities associated with proximal renal tubular acidosis J Clin Invest 108 107 115
52. - cotransporter NBC4 in rat kidney and characterization of a novel NBC4 variant Am J Physiol Renal Physiol 284 F41 F50
53. H Yamada S Yamazaki N Moriyama C Hara S Horita Y Enomoto A Kudo H Kawakami Y Tanaka T Fujita G Seki 2003 Localization of NBC-1 variants in human kidney and renal cell carcinoma Biochem Biophys Res Commun 310 1213 1218
54. Z Zou B Chung T Nguyen S Mentone B Thomson D Biemesderfer 2004 Linking receptor-mediated endocytosis and cell signaling: evidence for regulated intramembrane proteolysis of megalin in proximal tubule J Biol Chem 279 34302 34310