top of page

Mutant carbonic anhydrase 4 impairs pH regulation and causes retinal photoreceptor degeneration

Zhenglin Yang, Bernardo V. Alvarez, Christina Chakarova, Li Jiang, Goutam Karan, Jeanne M. Frederick, Yu Zhao, Yves Sauvé, Xi Li, Eberhart Zrenner, Bernd Wissinger, Anneke I. Den Hollander, Bradley Katz, Wolfgang Baehr, Frans P. Cremers,Joseph R. Casey, Shomi S. Bhattacharya, Kang Zhang


Human Molecular Genetics, Volume 14, Issue 2, 15 January 2005, Pages 255–265, https://doi.org/10.1093/hmg/ddi023


INTRODUCTION

Retinitis pigmentosa (RP) is the most prevalent group of inherited retinal degeneration, affecting approximately 1 in 3500 persons or a total of 1.8 million people worldwide (1,2). Clinical features of RP include night blindness, constriction and progressive loss of peripheral visual field affecting rod photoreceptors, followed by eventual loss of central vision (cones). RP may be transmitted as an autosomal dominant, recessive or X-linked trait (3,4). All known RP genes are expressed either in photoreceptors or in retinal pigment epithelium (RPE), and are, to the most part, involved in photoreceptor structure, phototransduction, photoreceptor development, the retinoid cycle or RNA splicing.


Retinal phototransduction is modulated by pH changes in its surrounding environment (5). It has been demonstrated that the amplitude of rod photoreceptor responses will decrease by ∼70% when the extracellular pH was decreased to 6.0 (6). Furthermore, there will also be a concomitant decrease in the Na+ conductance of rod photoreceptor outer segments (7). Despite exquisite sensitivity to the extracellular pH changes, photoreceptors paradoxically have a high rate of metabolism (8) and consequently high rate of endogenous acid production. As by-products of energy production in photoreceptors, a large amount of carbon dioxide and bicarbonate is generated from oxidative phosphorylation in mitochondria in the inner segments and lactic acid is generated from the inner and outer segments (9). Additional acid is generated from H+ release from cGMP turnover in the outer segment (10), and H+ influx due to Ca++/H+ exchanger activity in the plasma membrane of inner segment (11). The increase in acid load and lowering of intracellular pH are prevented by its removal from retina and RPE and release to blood stream in the choriocapillaris in the choroid, which is located adjacent to RPE and photoreceptors.



 

References

1.) Humphries, P., Kenna, P. and Farrar, G.J. (1992) On the molecular genetics of retinitis pigmentosa. Science, 256, 804–808. 2.) Rivolta, C., Sharon, D., DeAngelis, M.M. and Dryja, T.P. (2002) Retinitis pigmentosa and allied diseases: numerous diseases, genes, and inheritance patterns. Hum. Mol. Genet., 11, 1219–1227. 3.) Pacione, L.R., Szego, M.J., Ikeda, S., Nishina, P.M. and McInnes, R.R. (2003) Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations. Annu. Rev. Neurosci., 26, 657–700. 4.) Rattner, A., Sun, H. and Nathans, J. (1999) Molecular genetics of human retinal disease. Annu. Rev. Genet., 33, 89–131. 5.) Donner, K., Hemilä, S., Kalamkarov, G., Koskelainen, A., Pogozheva, I. and Rebrik, T. (1990) Sulfhydryl binding reagents increase the conductivity of the light-sensitive channel and inhibit phototransduction in retinal rods. Exp. Eye Res., 51, 97–105. 6.) Liebman, P.A., Mueller, P. and Pugh, E.N., Jr (1984) Protons suppress the dark current of frog retinal rods. J. Physiol. (Lond.), 347, 85–110. 7.) Gedney, C. and Ostroy, S.E. (1978) Hydrogen ion effects of the vertebrate photoreceptor. The pK's of ionizable groups affecting cell permeability. Arch. Biochem. Biophys., 188, 105–113. 8.) Wangsa-Wirawan, N.D. and Linsenmeier, R.A. (2003) Retinal oxygen: fundamental and clinical aspects. Arch. Ophthalmol., 121, 547–557. 9.) Winkler, B.S. (1986) Buffer dependence of retinal glycolysis and ERG potentials. Exp. Eye Res., 42, 585–593. 10.) Meyertholen, E.P., Wilson, M.J. and Ostroy, S.E. (1986) The effects of HEPES, bicarbonate and calcium on the cGMP content of vertebrate rod photoreceptors and the isolated electrophysiological effects of cGMP and calcium. Vision Res., 26, 521–533. 11 Krizaj, D. and Copenhagen, D.R. (1998) Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron, 21, 249–256.

Comentarios


bottom of page