Oligomerization of SLC4A11 protein and the severity of FECD and CHED2 corneal dystrophies caused by SLC4A11 mutations

Human Mutation

Volumn 33, Issue 2, 2012, Pages 419-428

  Vilas, Gonzalo L ^a   Loganathan, Sampath K ^a   Quon, Anita ^a   Sundaresan, Periasamy ^b   Vithana, Eranga N ^c,d   Casey, Joseph ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b ARAVIND MEDICAL RESEARCH FOUNDATION   (India)

^c SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Anion transport; CHED2; Congenital hereditary endothelial dystrophy; Cornea; ER retention; Fecd; Fuchs corneal endothelial dystrophy; Misfolding; SLC4A11

Indexed keywords

EPITOPE; PROTEIN; SLC4A11 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CELL MIGRATION; CELL SURFACE; CONGENITAL CORNEA DYSTROPHY; CONGENITAL HEREDITARY ENDOTHELIAL CORNEAL DYSTROPHY TYPE 2; CONTROLLED STUDY; DISEASE SEVERITY; FUCHS ENDOTHELIAL CORNEAL DYSTROPHY; GENE EXPRESSION; GENE MUTATION; HUMAN; IMMUNOPRECIPITATION; MISSENSE MUTATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; WILD TYPE;

ALLELES; AMINO ACID SUBSTITUTION; ANIMALS; ANION TRANSPORT PROTEINS; ANTIPORTERS; CELL LINE; CROSS-LINKING REAGENTS; DOGS; FUCHS' ENDOTHELIAL DYSTROPHY; GENE EXPRESSION; GENOTYPE; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MUTATION; PROTEIN MULTIMERIZATION; SUCCINIMIDES;

EID: 84857789238     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21655     Document Type: Article

References (44)

1. Aldahmesh MA, Khan AO, Meyer BF, Alkuraya FS. 2009. Mutational spectrum of SLC4A11 in autosomal recessive CHED in Saudi Arabia. Invest Ophthalmol Vis Sci. 50:4142-4145.
2. Aldave AJ, Yellore VS, Bourla N, Momi RS, Khan MA, Salem AK, Rayner SA, Glasgow BJ, Kurtz I. 2007. Autosomal recessive CHED associated with novel compound heterozygous mutations in SLC4A11. Cornea 26:896-900.
3. Alper SL. 2009. Molecular physiology and genetics of Na+-independent SLC4 anion exchangers. J Exp Biol 212(Pt 11):1672-1683.
4. Blodgett DM, Graybill C, Carruthers A. 2008. Analysis of glucose transporter topology and structural dynamics. J Biol Chem 283:36416-36424.
5. Casey JR, Reithmeier RAF. 1991. Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocytemembrane, by size exclusion high performance liquid chromatography: oligomeric stability and origin of heterogeneity. J Biol Chem 266:15726-15737.
6. Casula S, Zolotarev AS, Stuart-Tilley AK, Wilhelm S, Shmukler BE, Brugnara C, Alper SL. 2009. Chemical crosslinking studies with the mouse Kcc1 K-Cl cotransporter. Blood Cells Mol Dis 42:233-240.
7. Cheung JC, Cordat E, Reithmeier RA. 2005. Trafficking defects of the Southeast Asian ovalocytosis deletion mutant of anion exchanger 1 membrane proteins. Biochem J 392(Pt 3):425-434.
8. Cordat E. 2006. Unraveling trafficking of the kidney anion exchanger 1 in polarized MDCK epithelial cells. Biochem Cell Biol 84:949-959.
9. Cordat E, Casey JR. 2009. Bicarbonate transport in cell physiology and disease. Biochem J 417:423-439.
10. Cordat E, Kittanakom S, Yenchitsomanus PT, Li J, Du K, Lukacs GL, Reithmeier RA. 2006. Dominant and recessive distal renal tubular acidosis mutations of kidney anion exchanger 1 induce distinct trafficking defects inMDCK cells. Traffic 7:117-128.
11. Desir J, Abramowicz M. 2008. Congenital hereditary endothelial dystrophy with progressive sensorineural deafness (Harboyan syndrome). Orphanet J Rare Dis 3:28-36.
12. Desir J, Moya G, Reish O, Van Regemorter N, Deconinck H, David KL, Meire FM, Abramowicz M. 2007. Borate transporter SLC4A11 mutations cause both Harboyan syndrome and non-syndromic corneal endothelial dystrophy. J Med Genet 44:322-326.
13. Gaush CR, Hard WL, Smith TF. 1966. Characterization of an established line of canine kidney cells (MDCK). Proc Soc Exp Biol Med 122:931-935.
14. Hebert DN, Carruthers A. 1991. Cholate-solubilized erythrocyte glucose transporters exist as amixture of homodimers and homotetramers. Biochemistry 30(19):4654-4658.
15. Hemadevi B, Veitia RA, SrinivasanM, Arunkumar J, Prajna NV, Lesaffre C, Sundaresan P. 2008. Identification ofmutations in the SLC4A11 gene in patients with recessive congenital hereditary endothelial dystrophy. Arch Ophthalmol 126:700-708.
16. Jennings ML, Anderson MP, Monaghan R. 1986. Monoclonal antibodies against human erythrocyte Band 3 protein: localization of proteolytic cleavage sites and stilbenedisulfonate-binding lysine residues. J Biol Chem 261:9002-9010.
17. Jiao X, Sultana A, Garg P, Ramamurthy B, Vemuganti GK, Gangopadhyay N, Hejtmancik JF, Kannabiran C. 2007. Autosomal recessive corneal endothelial dystrophy (CHED2) is associated with mutations in SLC4A11. J Med Genet 44:64-68.
18. Kannabiran C. 2009. Genetics of corneal endothelial dystrophies. J Genet 88:487-494.
19. Kao L, Sassani P, Azimov R, Pushkin A, Abuladze N, Peti-Peterdi J, Liu W, Newman D, Kurtz I. 2008. Oligomeric structure and minimal functional unit of the electrogenic sodium bicarbonate cotransporter NBCe1-A. J Biol Chem 283:26782-26794.
20. Kedei N, Szabo T, Lile JD, Treanor JJ, Olah Z, Iadarola MJ, Blumberg PM. 2001. Analysis of the native quaternary structure of vanilloid receptor 1. J Biol Chem 276:28613-28619.
21. Kittanakom S, Cordat E, Akkarapatumwong V, Yenchitsomanus PT, Reithmeier RA. 2004. Trafficking defects of a novel autosomal recessive distal renal tubular acidosis mutant (S773P) of the human kidney anion exchanger (kAE1). J Biol Chem 279:40960-40971.
22. Klintworth GK. 2009. Corneal dystrophies. Orphanet J Rare Dis 4:7-45.
23. Kumar A, Bhattacharjee S, Prakash DR, Sadanand CS. 2007. Genetic analysis of two Indian families affected with congenital hereditary endothelial dystrophy: two novel mutations in SLC4A11. Mol Vis 13:39-46.
24. Laemmli UK. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680-685.
25. Okiyoneda T, Barriere H, Bagdany M, RabehWM, Du K, Hohfeld J, Young JC, Lukacs GL. 2010. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329:805-810.
26. Park M, Li Q, Shcheynikov N, Zeng W, Muallem S. 2004. NaBC1 is a ubiquitous electrogenic Na+-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Mol Cell 16:331-341.
27. Pascoe WS, Inukai K, Oka Y, Slot JW, James DE. 1996. Differential targeting of facilitative glucose transporters in polarized epithelial cells. Am J Physiol 271(2 Pt 1):C547-C554.
28. Pushkin A, Kurtz I. 2006. SLC4 base (HCO3 -, CO3 2-) transporters: classification, function, structure, genetic diseases, and knockout models. AmJ Physiol Renal Physiol 290:F580-F599.
29. Quilty JA, Cordat E, Reithmeier RA. 2002. Impaired trafficking of human kidney anion exchanger (kAE1) caused by hetero-oligomer formation with a truncated mutant associated with distal renal tubular acidosis. Biochem J 13:895-903.
30. Ramjeesingh M, Huan LJ, Garami E, Bear CE. 1999. Novel method for evaluation of the oligomeric structure of membrane proteins. Biochem J 342(Pt 1):119-123.
31. Ramprasad VL, Ebenezer ND, Aung T, Rajagopal R, Yong VH, Tuft SJ, Viswanathan D, El-Ashry MF, Liskova P, Tan DT, Bhattacharya SS, Kumaramanickavel G, Vithana EN. 2007. Novel SLC4A11mutations in patients with recessive congenital hereditary endothelial dystrophy (CHED2).Mutation in brief #958. Online. Hum Mutat 28:522-523.
32. Riazuddin SA, Vithana EN, Seet LF, Liu Y, Al-Saif A, Koh LW, Heng YM, Aung T, MeadowsDN, EghrariAO, GottschJD, Katsanis N. 2010.Missensemutations inthe sodium borate cotransporter SLC4A11 cause late-onset Fuchs corneal dystrophy. Hum Mutat 31:1261-1268.
33. Romero MF, Fulton CM, Boron WF. 2004. The SLC4 family of HCO3 - transporters. Pflugers Arch 447:496-509.
34. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529.
35. Ruetz S, Lindsey AE, Kopito RR. 1993. Function and biosynthesis of erythroid and nonerythroid anion exchangers. Soc Gen Physiol Ser 48:193-200.
36. Schroder M, Kaufman RJ. 2005. Themammalian unfolded protein response. Annu Rev Biochem 74:739-789.
37. Sultana A, Garg P, Ramamurthy B, Vemuganti GK, Kannabiran C. 2007. Mutational spectrum of the SLC4A11 gene in autosomal recessive congenital hereditary endothelial dystrophy. Mol Vis 13:1327-1332.
38. Vilas GL, Morgan PE, Loganathan SK, Quon A, Casey JR. 2011. A biochemical framework for SLC4A11, the plasmamembrane protein defective in corneal dystrophies. Biochemistry 50:2157-2169.
39. Vithana EN, Morgan P, Sundaresan P, Ebenezer ND, Tan DT, Mohamed MD, Anand S, Khine KO, Venkataraman D, Yong VH, Salto-Tellez M, Inglehearn CF, Aung T. 2006. Mutations in sodium-borate cotransporter SLC4A11 cause recessive congenital hereditary endothelial dystrophy (CHED2). Nat Genet 38:755-757.
40. Vithana EN, Morgan PE, Ramprasad V, TanDT, Yong VH, VenkataramanD, Venkatraman A, Yam GH, Nagasamy S, Law RW, Rajagopal R, Pang CP, Kumaramanickevel G, Casey JR, Aung T. 2008. SLC4A11 mutations in Fuchs endothelial corneal dystrophy. Hum Mol Genet 17:656-666.
41. Weiss JS, Moller HU, Lisch W, Kinoshita S, Aldave AJ, Belin MW, Kivela T, Busin M, Munier FL, Seitz B, Sutphin J, Bredrup C, Mannis MJ, Rapuano CJ, Van Rij G, KimEK, Klintworth GK. 2008. The IC3D classification of the corneal dystrophies. Cornea 27(SUPPL 2):S1-S83.
42. Zhu Q, Lee DWK, Casey JR. 2003. Novel Topology in C-terminal Region of the Human Plasma membrane anion exchanger, AE1. J Biol Chem 278:3112-3120.
43. Zolotarev AS, Shmukler BE, Alper SL. 1999. AE2 anion exchanger polypeptide is a homooligomer in pig gastric membranes: a chemical cross-linking study. Biochemistry 38:8521-8531.
44. Zuo S, Hellman U, Lundahl P. 2003. On the oligomeric state of the red blood cell glucose transporter GLUT1. Biochim Biophys Acta 1618:8-16.