Permeation of Internal and External Monovalent Cations through the Catfish Cone Photoreceptor cGMP-gated Channel

The pe rmea t ion o f monova len t cations th rough the cGMP-gated channel of catfish cone ou te r segments was examined by measur ing permeabi l i ty and conduc tance ratios u n d e r bi ionic condit ions. For monova len t cations presented on the cytoplasmic side of the channel , the permeabi l i ty ratios with respect to extracel lular Na followed the sequence NH4 > K > Li > Rb = Na > Cs while the conductance ratios at +50 mV followed the sequence Na ~ NH4 > K > Rb > Li = Cs. These pa t te rns are broadly similar to the amph ib i an rod channel . The symmetry of the channe l was tested by present ing the test ion on the extracel lular side and using Na as the c o m m o n reference ion on the cytoplasmic side. U n d e r these bi ionic condi t ions, the permeabi l i ty ratios with respect to Na at the intracellular side followed the sequence NH4 > Li > K > Na > Rb > Cs while the conduc tance ratios at +50 mV followed the sequence NH4 > K ~ Na > Rb > Li > Cs. Thus, the channel is asymmetric with respect to external and internal cations. Und e r symmetrical 120 mM ionic condi t ions, the single-channel conduc tance at +50 mV ranged from 58 pS in NI-I4 to 15 pS for Cs and was in the order NI-I4 > Na > K > Rb > Cs. Unexpectedly , the s ingle-channel cur rent -vol tage re la t ion showed suffic ient outward rect if icat ion to account for the rect if icat ion observed in mult ichannel patches without invoking voltage d e p e n d e n c e in gating. The concen t ra t ion d e p e n d e n c e of the reversal potent ia l for K showed that ch lor ide was impermeant . Anomalous mole fraction behavior was no t observed, nor, over a l imi ted concent ra t ion range, were mul t ip le dissociat ion constants. An Eyring rate theory mode l with a single b ind ing site was sufficient to expla in these observations. I N T R O D U C T I O N T h e cGMP-ga ted c h a n n e l s o f r o d a n d c o n e o u t e r s egmen t s a r e r e s p o n s i b l e fo r crea t i ng the c h a n g e in t r a n s m e m b r a n e vol tage tha t occurs in r e s p o n s e to i l l u m i n a t i o n o f the p h o t o r e c e p t o r . T h e c h a n n e l s o f b o t h rods (Fesenko , Kolesnikov, a n d LyuAddress correspondence to Dr. L. W. Haynes, Department of Medical Physiology, University of Calgary, 330 Hospital Drive NW, Calgary, AB, T2N 4N1, Canada. J. GEN. PHYSIOL. 9 The Rockefeller University Press" 0022-1295/95/09/485/21 $2.00 Volume 106 September 1995 485-505 485 on A ril 9, 2017 D ow nladed fom Published September 1, 1995