Autosomal recessive bestrophinopathy is not associated with the loss of bestrophin-1 anion channel function in a patient with a novel BEST1 mutation

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 8, 2015, Pages 4619-4630

  Johnson, Adiv A ^a   Bachman, Lori A ^a   Gilles, Benjamin J ^a   Cross, Samuel D ^a   Stelzig, Kimberly E ^a   Resch, Zachary T ^a   Marmorstein, Lihua Y ^a   Pulido, Jose S ^a   Marmorstein, Alan D ^a  

^a MAYO CLINIC   (United States)

Author keywords

Best1; iPSC RPE; Localization; Oligomerization

Indexed keywords

AMINO ACID; ANION CHANNEL; BEST1 PROTEIN, HUMAN; CHLORIDE CHANNEL; DNA; EYE PROTEIN;

ADENOVIRIDAE; ADOLESCENT; ANIMAL CELL; ARTICLE; AUTOSOMAL RECESSIVE BESTROPHINOPATHY; BESTROPHIN 1 GENE; CALCIUM CURRENT; CARBOXY TERMINAL SEQUENCE; CASE REPORT; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CONVERGENT STRABISMUS; ELECTRON MICROSCOPY; ELECTROOCULOGRAPHY; EYE FUNDUS; FEMALE; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE LOCATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MACULAR DEGENERATION; MDCK CELL LINE; OLIGOMERIZATION; OPTICAL COHERENCE TOMOGRAPHY; PHAGOCYTOSIS; PHOTORECEPTOR OUTER SEGMENT; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RETINA DISEASE; RETINA PIGMENT CELL; VISUAL ACUITY; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; BIOSYNTHESIS; CELL MEMBRANE; DNA MUTATIONAL ANALYSIS; EYE DISEASE; FLUORESCENCE ANGIOGRAPHY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PATCH CLAMP TECHNIQUE; PATHOLOGY; RECESSIVE GENE; RETINAL PIGMENT EPITHELIUM; ULTRASTRUCTURE;

ADOLESCENT; BLOTTING, WESTERN; CELL MEMBRANE; CHLORIDE CHANNELS; DNA; DNA MUTATIONAL ANALYSIS; EYE DISEASES, HEREDITARY; EYE PROTEINS; FEMALE; FLUORESCEIN ANGIOGRAPHY; FUNDUS OCULI; GENE EXPRESSION REGULATION; GENES, RECESSIVE; HEK293 CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MUTATION; PATCH-CLAMP TECHNIQUES; RETINAL DISEASES; RETINAL PIGMENT EPITHELIUM;

EID: 84939794591     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-16910     Document Type: Article

References (49)

1. Petrukhin K, Koisti MJ, Bakall B, et al. Identification of the gene responsible for Best macular dystrophy. Nat Genet. 1998; 19:241–247
2. Marquardt A, Stohr H, Passmore LA, Kramer F, Rivera A, Weber BH. Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best’s disease). Hum Mol Genet. 1998;7:1517–1525
3. Burgess R, Millar ID, Leroy BP, et al. Biallelic mutation of BEST1 causes a distinct retinopathy in humans. Am J Hum Genet 2008;82:19–31
4. Marmorstein AD, Cross HE, Peachey NS. Functional roles of bestrophins in ocular epithelia. Prog Retin Eye Res. 2009;28: 206–226
5. Boon CJ, Klevering BJ, Leroy BP, Hoyng CB, Keunen JE, den Hollander AI. The spectrum of ocular phenotypes caused by mutations in the BEST1 gene. Prog Retin Eye Res. 2009;28: 187–205
6. Marmorstein AD, Marmorstein LY, Rayborn M, Wang X, Hollyfield JG, Petrukhin K. Bestrophin, the product of the Best vitelliform macular dystrophy gene (VMD2), localizes to the basolateral plasma membrane of the retinal pigment epithelium. Proc Natl Acad Sci U S A. 2000;97:12758–12763
7. Milenkovic VM, Rivera A, Horling F, Weber BH. Insertion and topology of normal and mutant bestrophin-1 in the endoplasmic reticulum membrane. J Biol Chem. 2007;282:1313–1321
8. Dickson VK, Pedi L, Long SB. Structure and insights into the function of a Ca-activated Cl channel. Nature. 2014;516:213–218
9. Yang T, Liu Q, Kloss B, et al. Structure and selectivity in bestrophin ion channels. Science. 2014;346:355–359
10. Johnson AA, Lee YS, Chadburn AJ, et al. Disease-causing mutations associated with four bestrophinopathies exhibit disparate effects on the localization, but not the oligomerization, of Bestrophin-1. Exp Eye Res. 2014;121:74–85
11. Johnson AA, Lee YS, Stanton JB, et al. Differential effects of Best disease causing missense mutations on bestrophin-1 trafficking. Hum Mol Genet. 2013;22:4688–4697
12. Sun H, Tsunenari T, Yau KW, Nathans J. The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci U S A. 2002;99:4008–4013
13. Stanton JB, Goldberg AF, Hoppe G, Marmorstein LY, Marmorstein AD. Hydrodynamic properties of porcine bestrophin-1 in Triton X-100. Biochim Biophys Acta. 2006;1758:241–247
14. Bharill S, Fu Z, Palty R, Isacoff EY. Stoichiometry and specific assembly of Best ion channels. Proc Natl Acad Sci U S A. 2014; 111:6491–6496
15. Hartzell HC, Qu Z, Yu K, Xiao Q, Chien LT. Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol Rev. 2008;88:639–672
16. Xiao Q, Hartzell HC, Yu K. Bestrophins and retinopathies Pflugers Arch. 2010;460:559–569
17. Marmorstein AD, Kinnick TR, Stanton JB, Johnson AA, Lynch RM, Marmorstein LY. Bestrophin-1 influences transepithelial electrical properties and Ca(2þ) signaling in human retinal pigment epithelium. Mol Vis. 2015;21:347–359
18. Milenkovic A, Brandl C, Milenkovic VM, et al. Bestrophin 1 is indispensable for volume regulation in human retinal pigment epithelium cells. Proc Natl Acad Sci U S A. 2015;112:E2630–E2639
19. Lee S, Yoon BE, Berglund K, et al. Channel-mediated tonic GABA release from glia. Science. 2010;330:790–796
20. Woo DH, Han KS, Shim JW, et al. TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell. 2012;151:25–40
21. Yu K, Lujan R, Marmorstein A, Gabriel S, Hartzell HC Bestrophin-2 mediates bicarbonate transport by goblet cells in mouse colon. J Clin Invest. 2010;120:1722–1735
22. Cui CY, Childress V, Piao Y, et al. Forkhead transcription factor FoxA1 regulates sweat secretion through Bestrophin 2 anion channel and Na-K-Cl cotransporter 1. Proc Natl Acad Sci U S A. 2012;109:1199–1203
23. Marmorstein LY, Wu J, McLaughlin P, et al. The light peak of the electroretinogram is dependent on voltage-gated calcium channels and antagonized by bestrophin (best-1). J Gen Physiol. 2006;127:577–589
24. Rosenthal R, Bakall B, Kinnick T, et al. Expression of bestrophin-1, the product of the VMD2 gene, modulates voltage-dependent Ca2þchannels in retinal pigment epithelial cells. FASEB J. 2006;20:178–180
25. Yu K, Xiao Q, Cui G, Lee A, Hartzell HC. The best diseaselinked Cl- channel hBest1 regulates Ca V 1 (L-type) Ca2þ channels via src-homology-binding domains. J Neurosci. 2008; 28:5660–5670
26. Zhang Y, Stanton JB, Wu J, et al. Suppression of Ca2þsignaling in a mouse model of Best disease. Hum Mol Genet. 2010;19: 1108–1118
27. Singh R, Shen W, Kuai D, et al. iPS cell modeling of Best disease: insights into the pathophysiology of an inherited macular degeneration. Hum Mol Genet. 2013;22:593–607
28. Gomez NM, Tamm ER, Straubeta O. Role of bestrophin-1 in store-operated calcium entry in retinal pigment epithelium Pflugers Arch. 2013;465:481–495
29. Neussert R, Muller C, Milenkovic VM, Strauss O. The presence of bestrophin-1 modulates the Ca2þ recruitment from Ca2þ stores in the ER. Pflugers Arch. 2010;460:163–175
30. Strauss O, Muller C, Reichhart N, Tamm ER, Gomez NM. The role of bestrophin-1 in intracellular Ca(2þ) signaling. Adv Exp Med Biol. 2014;801:113–119
31. Milenkovic VM, Rohrl E, Weber BH, Strauss O. Diseaseassociated missense mutations in bestrophin-1 affect cellular trafficking and anion conductance. J Cell Sci. 2011;124:2988–2996
32. Iannaccone A, Kerr NC, Kinnick TR, Calzada JI, Stone EM Autosomal recessive best vitelliform macular dystrophy: report of a family and management of early-onset neovascular complications. Arch Ophthalmol. 2011;129:211–217
33. Maruotti J, Wahlin K, Gorrell D, Bhutto I, Lutty G, Zack DJ. A simple and scalable process for the differentiation of retinal pigment epithelium from human pluripotent stem cells. Stem Cells Transl Med. 2013;2:341–354
34. Finnemann SC, Bonilha VL, Marmorstein AD, Rodriguez- Boulan E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc Natl Acad Sci U S A 1997;94:12932–12937
35. Rohani L, Johnson AA, Arnold A, Stolzing A. The aging signature: a hallmark of induced pluripotent stem cells? Aging Cell. 2014;13:2–7
36. Davidson AE, Millar ID, Burgess-Mullan R, et al. Functional characterization of bestrophin-1 missense mutations associated with autosomal recessive bestrophinopathy. Invest Ophthalmol Vis Sci. 2011;52:3730–3736
37. Brandl C, Zimmermann SJ, Milenkovic VM, et al. In-depth characterisation of retinal pigment epithelium (RPE) cells derived from human induced pluripotent stem cells (hiPSC) Neuromolecular Med. 2014;16:551–564
38. Abramoff MD, Mullins RF, Lee K, et al. Human photoreceptor outer segments shorten during light adaptation. Invest Ophthalmol Vis Sci. 2013;54:3721–3728
39. Kay CN, Abramoff MD, Mullins RF, et al. Three-dimensional distribution of the vitelliform lesion, photoreceptors, and retinal pigment epithelium in the macula of patients with best vitelliform macular dystrophy. Arch Ophthalmol. 2012;130: 357–364
40. Qu Z, Cui Y, Hartzell C. A short motif in the C-terminus of mouse bestrophin 3 [corrected] inhibits its activation as a Cl channel. FEBS Lett. 2006;580:2141–2146
41. Marmorstein LY, McLaughlin PJ, Stanton JB, Yan L, Crabb JW, Marmorstein AD. Bestrophin interacts physically and functionally with protein phosphatase 2A. J Biol Chem. 2002;277: 30591–30597
42. Xiao Q, Prussia A, Yu K, Cui YY, Hartzell HC. Regulation of bestrophin Cl channels by calcium: role of the C terminus. J Gen Physiol. 2008;132:681–692
43. Qu Z, Chien LT, Cui Y, Hartzell HC. The anion-selective pore of the bestrophins, a family of chloride channels associated with retinal degeneration. J Neurosci. 2006;26:5411–5419
44. Davidson AE, Millar ID, Urquhart JE, et al. Missense mutations in a retinal pigment epithelium protein, bestrophin-1, cause retinitis pigmentosa. Am J Hum Genet. 2009;85:581–592
45. Reichhart N, Milenkovic VM, Halsband CA, Cordeiro S, Strauss O. Effect of bestrophin-1 on L-type Ca2þ channel activity depends on the Ca2þ channel beta-subunit. Exp Eye Res 2010;91:630–639
46. Milenkovic VM, Krejcova S, Reichhart N, Wagner A, Strauss O Interaction of bestrophin-1 and Ca2þ channel beta-subunits: identification of new binding domains on the bestrophin-1 Cterminus PLoS One. 2011;6:e19364
47. Pomares E, Bures-Jelstrup A, Ruiz-Nogales S, Corcostegui B, Gonzalez-Duarte R, Navarro R. Nonsense-mediated decay as the molecular cause for autosomal recessive bestrophinopathy in two unrelated families. Invest Ophthalmol Vis Sci. 2012;53: 532–537
48. Bitner H, Mizrahi-Meissonnier L, Griefner G, Erdinest I, Sharon D, Banin E. A homozygous frameshift mutation in BEST1 causes the classical form of Best disease in an autosomal recessive mode. Invest Ophthalmol Vis Sci. 2011;52:5332–5338
49. Davidson AE, Sergouniotis PI, Burgess-Mullan R, et al. A synonymous codon variant in two patients with autosomal recessive bestrophinopathy alters in vitro splicing of BEST1 Mol Vis. 2010;16:2916–2922