Role of bestrophin-1 in store-operated calcium entry in retinal pigment epithelium

详细信息    查看全文

• 作者：Néstor Más Gómez (1)
  Ernst R. Tamm (2)
  Olaf Strauβ (1)
  
• 关键词：Bestrophin ; 1 ; Endoplasmic reticulum Ca2+ store ; Orai ; 1 ; Store ; operated calcium entry
• 刊名：Pfl眉gers Archiv - European Journal of Physiology
• 出版年：2013
• 出版时间：April 2013
• 年：2013
• 卷：465
• 期：4
• 页码：481-495
• 全文大小：795KB
• 参考文献：1. Abramoff MD, Magelhaes PJ, Ram SJ, Zhang S, Campochiaro PA, Zack DJ, Hughes BA (2004) Image processing with image. J Biophotonics Int 11(2):36?42
  2. Arden GB, Barrada A, Kelsey JH (1962) New clinical test of retinal function based upon the standing potential of the eye. Br J Ophthalmol 46(8):449-67 10.1136/bjo.46.8.449">CrossRef
  3. Bakall B, Marmorstein LY, Hoppe G, Peachey NS, Wadelius C, Marmorstein AD (2003) Expression and localization of bestrophin during normal mouse development. Invest Ophthalmol Vis Sci 44(8):3622-628 10.1167/iovs.03-0030">CrossRef
  4. Barro Soria R, Spitzner M, Schreiber R, Kunzelmann K (2009) Bestrophin-1 enables Ca2+-activated Cl<sup>?/sup> conductance in epithelia. J Biol Chem 284(43):29405-9412. doi:10.1074/jbc.M605716200 10.1074/jbc.M605716200">CrossRef
  5. Barro-Soria R, Aldehni F, Almaca J, Witzgall R, Schreiber R, Kunzelmann K (2010) ER-localized bestrophin 1 activates Ca2+-dependent ion channels TMEM16A and SK4 possibly by acting as a counterion channel. Pflugers Arch 459(3):485-97. doi:10.1007/s00424-009-0745-0 10.1007/s00424-009-0745-0">CrossRef
  6. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361(6410):315-25. doi:10.1038/361315a0 10.1038/361315a0">CrossRef
  7. Bok D (1993) The retinal pigment epithelium: a versatile partner in vision. J Cell Sci Suppl 17:189-95
  8. Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131(7):1327-339. doi:10.1016/j.cell.2007.11.039 10.1016/j.cell.2007.11.039">CrossRef
  9. Cahalan MD, Zhang SL, Yeromin AV, Ohlsen K, Roos J, Stauderman KA (2007) Molecular basis of the CRAC channel. Cell Calcium 42(2):133-44. doi:10.1016/j.ceca.2007.03.002 10.1016/j.ceca.2007.03.002">CrossRef
  10. Constable PA (2011) Nifedipine alters the light-rise of the electro-oculogram in man. Graefes Arch Clin Exp Ophthalmol 249(5):677-84. doi:10.1007/s00417-010-1604-6 10.1007/s00417-010-1604-6">CrossRef
  11. Cordeiro S, Strauss O (2010) Expression of Orai genes and I(CRAC) activation in the human retinal pigment epithelium. Graefes Arch Clin Exp Ophthalmol 249(1):47-4. doi:10.1007/s00417-010-1445-3 10.1007/s00417-010-1445-3">CrossRef
  12. Cordeiro S, Strauss O (2011) Expression of Orai genes and I(CRAC) activation in the human retinal pigment epithelium. Graefes Arch Clin Exp Ophthalmol 249(1):47-4. doi:10.1007/s00417-010-1445-3 10.1007/s00417-010-1445-3">CrossRef
  13. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441(7090):179-85. doi:10.1038/nature04702 10.1038/nature04702">CrossRef
  14. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 26(3):270-71. doi:10.1038/81555 10.1038/81555">CrossRef
  15. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260(6):3440-450
  16. Gu SM, Thompson DA, Srikumari CR, Lorenz B, Finckh U, Nicoletti A, Murthy KR, Rathmann M, Kumaramanickavel G, Denton MJ, Gal A (1997) Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet 17(2):194-97. doi:10.1038/ng1097-194 10.1038/ng1097-194">CrossRef
  17. Hartzell HC, Qu Z, Yu K, Xiao Q, Chien LT (2008) Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol Rev 88(2):639-72. doi:10.1152/physrev.00022.2007 10.1152/physrev.00022.2007">CrossRef
  18. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491-33. doi:10.1146/annurev.immunol.021908.132550 10.1146/annurev.immunol.021908.132550">CrossRef
  19. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355(6358):353-56. doi:10.1038/355353a0 10.1038/355353a0">CrossRef
  20. Jentsch TJ, Maritzen T, Zdebik AA (2005) Chloride channel diseases resulting from impaired transepithelial transport or vesicular function. J Clin Invest 115(8):2039-046. doi:10.1172/JCI25470 10.1172/JCI25470">CrossRef
  21. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15(13):1235-241. doi:10.1016/j.cub.2005.05.055 10.1016/j.cub.2005.05.055">CrossRef
  22. Marmorstein AD, Marmorstein LY, Rayborn M, Wang X, Hollyfield JG, Petrukhin K (2000) 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 97(23):12758-2763. doi:10.1073/pnas.220402097 10.1073/pnas.220402097">CrossRef
  23. Marmorstein LY, Wu J, McLaughlin P, Yocom J, Karl MO, Neussert R, Wimmers S, Stanton JB, Gregg RG, Strauss O, Peachey NS, Marmorstein AD (2006) The light peak of the electroretinogram is dependent on voltage-gated calcium channels and antagonized by bestrophin (best-1). J Gen Physiol 127(5):577-89. doi:10.1085/jgp.200509473 10.1085/jgp.200509473">CrossRef
  24. Marquardt A, Stohr H, Passmore LA, Kramer F, Rivera A, Weber BH (1998) Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best’s disease). Hum Mol Genet 7(9):1517-525 10.1093/hmg/7.9.1517">CrossRef
  25. Martins JR, Kongsuphol P, Sammels E, Dahimene S, Aldehni F, Clarke LA, Schreiber R, de Smedt H, Amaral MD (1812) Kunzelmann K F508del-CFTR increases intracellular Ca(2+) signaling that causes enhanced calcium-dependent Cl(? conductance in cystic fibrosis. Biochim Biophys Acta 11:1385-392. doi:10.1016/j.bbadis.2011.08.008
  26. Maw MA, Kennedy B, Knight A, Bridges R, Roth KE, Mani EJ, Mukkadan JK, Nancarrow D, Crabb JW, Denton MJ (1997) Mutation of the gene encoding cellular retinaldehyde-binding protein in autosomal recessive retinitis pigmentosa. Nat Genet 17(2):198-00. doi:10.1038/ng1097-198 10.1038/ng1097-198">CrossRef
  27. Mergler S, Strauss O (2002) Stimulation of L-type Ca(2+) channels by increase of intracellular InsP3 in rat retinal pigment epithelial cells. Exp Eye Res 74(1):29-0. doi:10.1006/exer.2001.1128S0014483501911285 10.1006/exer.2001.1128">CrossRef
  28. Milenkovic VM, Krejcova S, Reichhart N, Wagner A, Strauss O (2011) Interaction of bestrophin-1 and Ca2+ channel beta-subunits: identification of new binding domains on the bestrophin-1 C-terminus. PLoS One 6(4):e19364. doi:10.1371/journal.pone.0019364PONE-D-10-05789 10.1371/journal.pone.0019364">CrossRef
  29. Milenkovic VM, Rohrl E, Weber BH, Strauss O (2011) Disease-associated missense mutations in bestrophin-1 affect cellular trafficking and anion conductance. J Cell Sci 124(Pt 17):2988-996. doi:10.1242/jcs.085878 10.1242/jcs.085878">CrossRef
  30. Mullins RF, Oh KT, Heffron E, Hageman GS, Stone EM (2005) Late development of vitelliform lesions and flecks in a patient with best disease: clinicopathologic correlation. Arch Ophthalmol 123(11):1588-594. doi:10.1001/archopht.123.11.1588 10.1001/archopht.123.11.1588">CrossRef
  31. Neussert R, Muller C, Milenkovic VM, Strauss O (2010) The presence of bestrophin-1 modulates the Ca2+ recruitment from Ca2+ stores in the ER. Pflugers Arch 460(1):163-75. doi:10.1007/s00424-010-0840-2 10.1007/s00424-010-0840-2">CrossRef
  32. Parekh AB (2010) Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 9(5):399-10. doi:10.1038/nrd3136 10.1038/nrd3136">CrossRef
  33. Petrukhin K, Koisti MJ, Bakall B, Li W, Xie G, Marknell T, Sandgren O, Forsman K, Holmgren G, Andreasson S, Vujic M, Bergen AA, McGarty-Dugan V, Figueroa D, Austin CP, Metzker ML, Caskey CT, Wadelius C (1998) Identification of the gene responsible for Best macular dystrophy. Nat Genet 19(3):241-47. doi:10.1038/915 10.1038/915">CrossRef
  34. Reichhart N, Milenkovic VM, Halsband CA, Cordeiro S, Strauss O (2010) Effect of bestrophin-1 on L-type Ca2+ channel activity depends on the Ca2+ channel beta-subunit. Exp Eye Res 91(5):630-39. doi:10.1016/j.exer.2010.08.001 10.1016/j.exer.2010.08.001">CrossRef
  35. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169(3):435-45. doi:10.1083/jcb.200502019 10.1083/jcb.200502019">CrossRef
  36. Rosenthal R, Bakall B, Kinnick T, Peachey N, Wimmers S, Wadelius C, Marmorstein A, Strauss O (2006) Expression of bestrophin-1, the product of the VMD2 gene, modulates voltage-dependent Ca2+ channels in retinal pigment epithelial cells. FASEB J 20(1):178-80. doi:10.1096/fj.05-4495fje
  37. Schindl R, Bergsmann J, Frischauf I, Derler I, Fahrner M, Muik M, Fritsch R, Groschner K, Romanin C (2008) 2-Aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J Biol Chem 283(29):20261-0267. doi:10.1074/jbc.M803101200 10.1074/jbc.M803101200">CrossRef
  38. Singh A, Hildebrand ME, Garcia E, Snutch TP (2010) The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels. Br J Pharmacol 160(6):1464-475. doi:10.1111/j.1476-5381.2010.00786.x 10.1111/j.1476-5381.2010.00786.x">CrossRef
  39. Stanton JB, Goldberg AF, Hoppe G, Marmorstein LY, Marmorstein AD (2006) Hydrodynamic properties of porcine bestrophin-1 in Triton X-100. Biochim Biophys Acta 1758(2):241-47. doi:10.1016/j.bbamem.2006.01.024 10.1016/j.bbamem.2006.01.024">CrossRef
  40. Steinberg RH (1985) Interactions between the retinal pigment epithelium and the neural retina. Doc Ophthalmol 60(4):327-46 10.1007/BF00158922">CrossRef
  41. Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85(3):845-81. doi:10.1152/physrev.00021.2004 10.1152/physrev.00021.2004">CrossRef
  42. Sun H, Tsunenari T, Yau KW, Nathans J (2002) The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci U S A 99(6):4008-013. doi:10.1073/pnas.05269299999/6/4008 10.1073/pnas.052692999">CrossRef
  43. Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P, Yau KW, Nathans J (2003) Structure-function analysis of the bestrophin family of anion channels. J Biol Chem 278(42):41114-1125. doi:10.1074/jbc.M306150200M306150200 10.1074/jbc.M306150200">CrossRef
  44. Weingeist TA, Kobrin JL, Watzke RC (1982) Histopathology of Best’s macular dystrophy. Arch Ophthalmol 100(7):1108-114 10.1001/archopht.1982.01030040086016">CrossRef
  45. Wimmers S, Karl MO, Strauss O (2007) Ion channels in the RPE. Prog Retin Eye Res 26(3):263-01. doi:10.1016/j.preteyeres.2006.12.002 10.1016/j.preteyeres.2006.12.002">CrossRef
  46. Wu J, Marmorstein AD, Striessnig J, Peachey NS (2007) Voltage-dependent calcium channel CaV1.3 subunits regulate the light peak of the electroretinogram. J Neurophysiol 97(5):3731-735. doi:10.1152/jn.00146.2007 10.1152/jn.00146.2007">CrossRef
  47. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443(7108):226-29. doi:10.1038/nature05108 10.1038/nature05108">CrossRef
  48. Yu K, Qu Z, Cui Y, Hartzell HC (2007) Chloride channel activity of bestrophin mutants associated with mild or late-onset macular degeneration. Invest Ophthalmol Vis Sci 48(10):4694-705. doi:10.1167/iovs.07-0301 10.1167/iovs.07-0301">CrossRef
  49. Yu K, Xiao Q, Cui G, Lee A, Hartzell HC (2008) The best disease-linked Cl?/sup> channel hBest1 regulates Ca V 1 (L-type) Ca2+ channels via src-homology-binding domains. J Neurosci 28(22):5660-670. doi:10.1523/JNEUROSCI.0065-08.2008 10.1523/JNEUROSCI.0065-08.2008">CrossRef
  50. Zhang Y, Stanton JB, Wu J, Yu K, Hartzell HC, Peachey NS, Marmorstein LY, Marmorstein AD Suppression of Ca2+ signaling in a mouse model of Best disease. Hum Mol Genet 19 (6):1108-118. doi:10.1093/hmg/ddp583
  51. Zhang Y, Stanton JB, Wu J, Yu K, Hartzell HC, Peachey NS, Marmorstein LY, Marmorstein AD (2010) Suppression of Ca2+ signaling in a mouse model of Best disease. Hum Mol Genet 19(6):1108-118. doi:10.1093/hmg/ddp583 10.1093/hmg/ddp583">CrossRef
  52. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci U S A 103(24):9357-362. doi:10.1073/pnas.0603161103 10.1073/pnas.0603161103">CrossRef</sup>
  
• 作者单位：Néstor Más Gómez (1)
  Ernst R. Tamm (2)
  Olaf Strauβ (1)
  
  1. Experimental Ophthalmology, Eye Hospital, University Medical Center Regensburg, Franz-Josef-Strauss-Allee 11, 93053, Regensburg, Germany
  2. Institute of Human Anatomy and Embryology, University of Regensburg, Regensburg, Germany
  
• ISSN：1432-2013

文摘

The retinal pigment epithelium (RPE) expresses bestrophin-1 where mutant bestrophin cause retinal degenerations. Overexpression of bestrophin-1 demonstrated Ca2+-dependent Cl- channel function, whereas the RPE in bestrophin-1 knockout or mutant bestrophin-1 knock-in mice showed no change in Cl?/sup> conductance. To account for these apparently mutually exclusive findings, we investigated the function of endogenously expressed bestrophin-1 in a short-time RPE cell culture system by means of immunocytochemistry, Ca2+ imaging, and siRNA knockdown. Immunocytochemical quantification of bestrophin-1 localization demonstrated 2.5 times higher co-localization with the endoplasmic reticulum (ER) Ca2+-sensor protein, Stim-1, than with the membrane protein β-catenin, implicating it in store-operated Ca2+ entry (SOCE). Ca2+ release from ER stores under extracellular Ca2+-free conditions using thapsigargin (1?μM) to inhibit endoplasmic Ca2+ ATPase (SERCA) followed by re-adjustment of extracellular Ca2+ to physiological levels activated SOCE, which was insensitive to the blocker of numerous transient receptor potential channels and voltage-dependent Ca2+ channels SKF96563 (1?μM). SOCE was augmented at 5?μM and inhibited at 75?μM by 2-aminoethoxydiphenyl borate which indicates the involvement Orai-1 channels. In confirmation, SOCE was decreased by siRNA knockdown of Orai-1 expression. SOCE amplitude was strongly reduced by siRNA knockdown of bestrophin-1 expression, which was due to neither changes in Stim-1/Orai-1 expression nor Stim-1/bestrophin-1 interaction. The amount of Ca2+ released by SERCA inhibition was reduced after siRNA knockdown of bestrophin-1, but not of Orai-1. In conclusion we found that a proportion of bestrophin-1 is functionally localized to ER Ca2+ stores where it influences the amount of Ca2+ and therefore Ca2+ signals which result from activation of Orai-1 via Stim-1.