- Email: [email protected]
M cone matrix sheaths in adult primate retina
Exp. Eye Res. (1995) 61, 763-766
LETTER TO THE E D I T O R S
Differential Peanut Agglutinin Lectin Labeling for S and L/M Cone Matrix Sheaths in Adult Primate Retina
A biochemically and structurally distinct domain of interphotoreceptor matrix that ensheaths cones, but not rods, has been identified on the basis of specific labeling by peanut agglutinin (PNA) lectin. This has been termed the cone matrix sheath (CMS) (Blanks and Johnson, 1984: Johnson, Hageman and Blanks, 1985, 1986; Hageman and Johnson, 1991). PNA preferentially binds to terminal galactose-N-acetyl galactosamine disaccharide residues of glycoconjugates (Lotan et al., 1975). Rods are surrounded by different matrix domain which binds wheat germ agglutinin (Sameshima, Uehara and Ohba, 1987; Hollyfield et al., 1990), a lectin that binds terminal Nacetyl glucosamine and sialic acid residues. The application of carbohydrate-specific lectins has proven to be a reliable marker to discriminate cones from rods. The primate retina contains red or long (L) wavelength, green or medium (M) wavelength, and blue or short (S) wavelength-sensitive cones (Nathans, Thomas and Hogness, 1986). S cones constitute about 10% in both monkey (deMonasterio et al., 1985) and h u m a n (Curcio et al., 1991) retina. In the ground squirrel retina (Szel et al., 1993) there is a difference in PNA labeling between the CMS of S and M cones, suggesting that PNA labeling not only can be used to discriminate the subtype of cones but also that different microenvironments surround S and M cones. In earlier studies of monkey retina using lectin binding (Sameshima, Uehara and Ohba, 1987: Blanks et al., 1988), no difference in PNA labeling between cones was reported. In the present study, we investigated the binding patterns of PNA to the CMS of Macaca monkey cones identified by immunocytochemical labeling by opsin antibody. Four adult Macaca monkeys were deeply anesthetized with barbiturate, the eyes were enucleated, the anterior segment removed and the posterior eyecup fixed in 4% paraformaldehyde in 0"1 M phosphate buffer containing 0.35% periodate and 0.05 % lysine. After overnight fixation, small pieces of retina were dehydrated in ethanol and propylene oxide and embedded in an Epon/Araldite resin mixture. Adjacent retinal blocks were cryoprotected and frozen sectioned at lO/~m. Serial 1/zm thick sections were cut from Epon blocks in both tangential and transverse planes of the retina, etched with sodium ethoxide for 20 min prior to reaction with reagents, and rinsed for 5 min in three changes of 0.1 M Tris buffer. In frozen and plastic sections non0014-4835/95/120763+04 $12.00/0
specific binding sites were blocked by incubating in 10% normal goat serum in Tris buffered saline (TBS) containing 0.2% TritonX 100 for 1 hr at room temperature. Sections were labeled with PNA-FITC (200/zg m1-1) in phosphate buffered saline (PBS); (E-Y Laboratories) for 45 min at 37°C in the dark, washed twice in PBS and coverslipped in glycerol. Some sections were treated with 0.25% trypsin for 2 0 60 sec before labeling by PNA-FITC. Adjacent serial sections were incubated in monoclonal antiserum OS2 which recognizes S opsin (Szel et al., 1993) ( 1 / 2 0 0 0 0 in TBS) for 2 4 h r at 4°C in a humid chamber with agitation. The sections were then washed overnight in TBS and the antibody binding visualized using a mouse IgG-avidin-biotinylatedperoxidase complex (Vector Laboratories) developed with diaminobenzidine and hydrogen peroxide. PNA binding in adult monkey retina is confined to cone CMS (Fig. 1). Figure l(a) is an en face frozen section at the outer segment level. It shows that the CMS of regularly-spaced single cones is stained slightly brighter than the majority of cones (arrows). This difference was more obvious in Epon sections [Fig. l(b) and (c), arrows], In vertical section single cones have a more intense CMS covering the outer and inner segment [Fig. l(b), arrows]. An en face Epon section through the photoreceptor layer at the outer segment level [Fig. l(c)] shows that a minority of cones which are arranged in hexagonal array (arrows) have an obviously heavier a n d / o r thicker CMS than the surrounding cones. To determine whether there was a correlation between CMS labeling intensity and cone subtypes, consecutive frozen or Epon sections were either immunoreacted with mab OS-2 to mark S cone outer segments or stained for PNA-FITC (Fig. 2). When the labeled S cone outer segments [Fig. 2(a), arrows] are compared with PNA-FITC [Fig. 2(b), arrows], it is clear that the S cones correlate with the thicker CMS. The effect of trypsinization on the CMS was studied in Epon sections (Fig. 3). When a vertical section was pretreated for 20 sec [Fig. 3(a)], most of the cones had lost almost all CMS labeling, but a few retained a brightly-labeled CMS [Fig 3(a), arrow]. The effect of trypsin pretreatment is more evident in a tangential section through the inner and outer segments [Fig. 3(b)]. The CMS is lost from almost all outer segments at the tip adjacent to the pigment epithelium (top of figure), although a thin rim persists on a few outer © 1995 Academic Press Limited
764
Q. Y A N ET AL.
FIG. 2. Consecutive adjacent Epon tangential sections were (a) immunoreacted with mab OS-2 and (b) labeled with PNA-FITC. The outer segment membrane of the S cones is dark due to OS-2 labeling [(a), arrows]. PNA-FITC shows heavier labeling for the CMS of the S cones [(b), arrows]. A double arrow indicates two closely adjacent cones in which the upper is an S cone [(a) and (b), double arrow]. Note the difference in the CMS of these two cones, x 300.
FIG. 1. The PNA binding pattern in adult Macaca monkey retina is shown on a frozen tangential section at the outer segment level (a). an Epon vertical section (b) and an Epon tangential section through the outer segment level (c). A regularly-spaced minority of cones have heavier labeling of PNA-FITC in their CMS. Some of these are marked by arrows, x 500.
segments [Fig. 3(b), arrowhead]. The CMS on most cone outer segments (middle of figure) and inner segments (bottom of figure) is strikingly reduced, but a few cones still have a heavily labeled CMS surrounding the outer segment (thick arrow) and inner segment (thin arrow). The similarity of the labeling pattern of OS-2 and PNA to Fig. 2 indicates that these are S
cones. W h e n trypsin pretreatment was increased to 60 seconds, the CMS on most cones disappeared but the outer segment m e m b r a n e remain labeled [Fig. 3(c)] while the CMS on S cones still persisted [Fig. 3(c), arrows]. In the primate retina plastic section PNA staining yielded reliable and consistent differences between the CMS of L/M and S cones. W h e n tissue from the same eyes was studied using frozen sections, the S cone CMS had brighter labeling, but the differences were not as striking nor as consistent. This indicates that the CMS difference was not due to tissue preparation, but dehydration m a y emphasize the difference. Monkey S cones had m u c h heavier binding of PNA to their CMS, indicating either that their CMS was thicker or that it had a higher concentration of terminal galactose-Nacetyl galactosamine disaccaride residues. The trypsin digestion also supported this conclusion. This observation is similar to CMS differences found between squirrel cones (Szel et al., 1993). In primates S cone inner segments are taller, larger and have a more cylindrical shape, their outer segments are shorter, and their synaptic pedicles are smaller t h a n L/M cones (deMonasterio et al., 1 9 8 5 : Curcio et al., 1 9 9 1 ; Ahnelt, Kolb and Pflug, 1987). Our finding of more intense PNA binding to the S cone CMS contributes a n o t h e r morphological difference. The CMS contains chondroitin 6-sulfate glycosa m i n o g l y c a n and glycoconjugates ( H a g e m a n and Johnson, 1986, 1991). SDS-polyacylamide gel electrophoresis and Western blotting of whole retinal extracts
PNA LABELING IN ADULT MONKEY CONES
765
FIG. 3. PNA labeling on Epon vertical (a) and tangential [(b) and (c)] sections after 20 sec [(a) and {b)] and 60 sec (c) trypsin pretreatment. Trypsinization removed the lectin label from the CMS in the majority of cones but their outer segment membranes still labeled. A few cones (arrows) retained a brightly labeled CMS. x 500.
found six m a j o r groups of P N A - b i n d i n g glycoproteins r a n g i n g b e t w e e n 30 a n d 88 kDa ( H a g e m a n a n d Johnson, 1986). F o u r of t h e m ( G P 3 9 / 4 0 . G P 4 2 / 4 5 , GP54 a n d GP60) were intensely labeled by PNA, with G P 5 4 being most sensitive to trypsin digestion. The differential P N A labeling p a t t e r n b e t w e e n S a n d L / M cones a n d the effect of trypsin digestion on PNA b i n d i n g c a n be interpreted in two w a y s w h i c h are n o t m u t u a l l y exclusive. One is t h a t the S cone CMS has the s a m e c a r b o h y d r a t e c o m p o n e n t s as L / M cone CMS, b u t S cones simply h a v e a larger total a m o u n t in a thicker CMS w h i c h takes l o n g e r to digest. The a l t e r n a t i v e is t h a t the L / M cone CMS c o n t a i n s m o r e trypsinsensitive GP54, a n d S cones h a v e m o r e of the o t h e r P N A - b i n d i n g c o m p o n e n t s . For the S cone, the CMS over the tip of o u t e r s e g m e n t m i g h t h a v e m o r e G P 5 4 w h i c h causes the rapid loss of PNA labeling after trypsinization. This s t u d y h a s s h o w n t h a t m o n k e y S cones h a v e a different glycoprotein m i c r o e n v i r o n m e n t t h a n L / M cones. S cones are k n o w n to be m o r e sensitive to e n v i r o n m e n t a l , light a n d a g i n g effects (Sperling, 1991), some of w h i c h could be m e d i a t e d by this differential m i c r o e n v i r o n m e n t lying b e t w e e n p h o t o receptors a n d p i g m e n t epithelium.
QI Y A N " KEELY B U M S T E D a A N I T A H E N D R I C K S O N a,b*
Departments of ~Biological Structure and b Ophthalmology, University of Washington, Seattle, WA 98195, U.S.A.
References
Acknowledgments
Ahnelt, P. K., Kolb, H. and Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. 1. Comp, Neurol. 255, 18-34. Blanks, J. C. and Johnson, L. V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 25. 546-57. Blanks, ]. C., Hageman, G. S.. Johnson, L. V. and Spee. C. (1988). Ultrastructural visualization of primate cone photoreceptor matrix sheaths. ]. Comp. Neurol. 270, 288-300. Curcio, C. A., Allen, K. A., Sloan, K. R,, Lerea, C. L., Hurley, J. B., Klock, I. B. and Milam, A. H. (1991J. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. I. Comp. Neurol. 312, 610-24, deMonasterio. F. M.. McCrane, E. P., Newlander, J. K. and Schein, S. ]. {1985). Density profle of blue-sensitive cones along the horizontal meridian of macaque retina. Invest. Ophthalmol. Vis. Sci. 26, 289-302. Hageman, G.S. and Johnson, L.V. (1986). Biochemical characterization of the major peanut agglutinin-binding glycoproteins in vertebrate retinae: a species comparison. ]. Comp. Neurol. 249, 499-510.
This research was supported by EY01208, EY04536 and Research to Prevent Blindness Inc.
* For correspondence at: BiologicalStructure SM20. University of Washington. Seattle. WA 98195. U.S.A.
Q. Y A N ET AL.
766
Hageman, G.S. and ]ohnson, L.V. (1991). Structure, composition and function of the retinal interphotoreceptor matrix. In Progress in Retinal Research. (Eds Osborne, N. N. and Chader, G. ].) Vol. 10, Pp. 207-49. Pergamon Press: Oxford. Hollyfield, ]. G., Rayborn, M. E., Landers, R. A. and Myers, K.M. (1990). Insoluble interphotoreceptor matrix domains surround rod photoreceptors in the human retina. Exp. Eye Res. 51, 107-10. Johnson, L.V., Hageman, G.S. and Blanks, ]. C. (1985). Restricted extracellular matrix domains ensheath cone photoreceptors in vertebrate retinae. In: The Interphotoreceptor Matrix in Health and Disease. (Eds Bridges, C. D. B. and Adler, A.].) Pp. 33-44. Plenum Press: New York, U.S.A. Johnson, L.V., Hageman, G.S. and Blanks, ]. C. (1986). Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 27, 129-35. Lotan, R., Skutelsky, E., Danon, D. and Sharon, N. (1975). The purification, composition, and specificity of anti-T
lectin from peanut (Arachis hypogaea). J. Biol. Chem. 250, 8518-23. Nathans, J., Thomas, D. and Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding blue, green and red pigments. Science 232, 193-202. Sameshima, M., Uehara, F. and Ohba, N. (1987). Specialization of the interphotoreceptor matrices around cone and rod photoreceptor cells in the monkey retina, as revealed by lectin cytochemistry. Exp. Eye Res. 45, 845-63. Sperling, H.G. (1991). Vulnerability of the blue-sensitive mechanism. In: Vision and Visual Dysfunction. (Ed. Dillon, J.C. Inherited and Acquired Colour Vision Deficiencies: Fundamental Aspects and Clinical Studies, Vol. 7. Pp. 72-87. CRC Press: Boca Raton, U.S.A. Szel, A., yon Schantz, M., Rohlich, P., Farber, D. B. and van Veen, T. (1993). Difference in PNA label intensity between short- and middle-wavelength sensitive cones in the ground squirrel retina. Invest. Ophthalmol. Vis. Sci. 34, 3641-5.
(Received Cleveland 10 April 1995 and accepted in revised form 19 July 1995)
LETTER TO THE E D I T O R S
Differential Peanut Agglutinin Lectin Labeling for S and L/M Cone Matrix Sheaths in Adult Primate Retina
A biochemically and structurally distinct domain of interphotoreceptor matrix that ensheaths cones, but not rods, has been identified on the basis of specific labeling by peanut agglutinin (PNA) lectin. This has been termed the cone matrix sheath (CMS) (Blanks and Johnson, 1984: Johnson, Hageman and Blanks, 1985, 1986; Hageman and Johnson, 1991). PNA preferentially binds to terminal galactose-N-acetyl galactosamine disaccharide residues of glycoconjugates (Lotan et al., 1975). Rods are surrounded by different matrix domain which binds wheat germ agglutinin (Sameshima, Uehara and Ohba, 1987; Hollyfield et al., 1990), a lectin that binds terminal Nacetyl glucosamine and sialic acid residues. The application of carbohydrate-specific lectins has proven to be a reliable marker to discriminate cones from rods. The primate retina contains red or long (L) wavelength, green or medium (M) wavelength, and blue or short (S) wavelength-sensitive cones (Nathans, Thomas and Hogness, 1986). S cones constitute about 10% in both monkey (deMonasterio et al., 1985) and h u m a n (Curcio et al., 1991) retina. In the ground squirrel retina (Szel et al., 1993) there is a difference in PNA labeling between the CMS of S and M cones, suggesting that PNA labeling not only can be used to discriminate the subtype of cones but also that different microenvironments surround S and M cones. In earlier studies of monkey retina using lectin binding (Sameshima, Uehara and Ohba, 1987: Blanks et al., 1988), no difference in PNA labeling between cones was reported. In the present study, we investigated the binding patterns of PNA to the CMS of Macaca monkey cones identified by immunocytochemical labeling by opsin antibody. Four adult Macaca monkeys were deeply anesthetized with barbiturate, the eyes were enucleated, the anterior segment removed and the posterior eyecup fixed in 4% paraformaldehyde in 0"1 M phosphate buffer containing 0.35% periodate and 0.05 % lysine. After overnight fixation, small pieces of retina were dehydrated in ethanol and propylene oxide and embedded in an Epon/Araldite resin mixture. Adjacent retinal blocks were cryoprotected and frozen sectioned at lO/~m. Serial 1/zm thick sections were cut from Epon blocks in both tangential and transverse planes of the retina, etched with sodium ethoxide for 20 min prior to reaction with reagents, and rinsed for 5 min in three changes of 0.1 M Tris buffer. In frozen and plastic sections non0014-4835/95/120763+04 $12.00/0
specific binding sites were blocked by incubating in 10% normal goat serum in Tris buffered saline (TBS) containing 0.2% TritonX 100 for 1 hr at room temperature. Sections were labeled with PNA-FITC (200/zg m1-1) in phosphate buffered saline (PBS); (E-Y Laboratories) for 45 min at 37°C in the dark, washed twice in PBS and coverslipped in glycerol. Some sections were treated with 0.25% trypsin for 2 0 60 sec before labeling by PNA-FITC. Adjacent serial sections were incubated in monoclonal antiserum OS2 which recognizes S opsin (Szel et al., 1993) ( 1 / 2 0 0 0 0 in TBS) for 2 4 h r at 4°C in a humid chamber with agitation. The sections were then washed overnight in TBS and the antibody binding visualized using a mouse IgG-avidin-biotinylatedperoxidase complex (Vector Laboratories) developed with diaminobenzidine and hydrogen peroxide. PNA binding in adult monkey retina is confined to cone CMS (Fig. 1). Figure l(a) is an en face frozen section at the outer segment level. It shows that the CMS of regularly-spaced single cones is stained slightly brighter than the majority of cones (arrows). This difference was more obvious in Epon sections [Fig. l(b) and (c), arrows], In vertical section single cones have a more intense CMS covering the outer and inner segment [Fig. l(b), arrows]. An en face Epon section through the photoreceptor layer at the outer segment level [Fig. l(c)] shows that a minority of cones which are arranged in hexagonal array (arrows) have an obviously heavier a n d / o r thicker CMS than the surrounding cones. To determine whether there was a correlation between CMS labeling intensity and cone subtypes, consecutive frozen or Epon sections were either immunoreacted with mab OS-2 to mark S cone outer segments or stained for PNA-FITC (Fig. 2). When the labeled S cone outer segments [Fig. 2(a), arrows] are compared with PNA-FITC [Fig. 2(b), arrows], it is clear that the S cones correlate with the thicker CMS. The effect of trypsinization on the CMS was studied in Epon sections (Fig. 3). When a vertical section was pretreated for 20 sec [Fig. 3(a)], most of the cones had lost almost all CMS labeling, but a few retained a brightly-labeled CMS [Fig 3(a), arrow]. The effect of trypsin pretreatment is more evident in a tangential section through the inner and outer segments [Fig. 3(b)]. The CMS is lost from almost all outer segments at the tip adjacent to the pigment epithelium (top of figure), although a thin rim persists on a few outer © 1995 Academic Press Limited
764
Q. Y A N ET AL.
FIG. 2. Consecutive adjacent Epon tangential sections were (a) immunoreacted with mab OS-2 and (b) labeled with PNA-FITC. The outer segment membrane of the S cones is dark due to OS-2 labeling [(a), arrows]. PNA-FITC shows heavier labeling for the CMS of the S cones [(b), arrows]. A double arrow indicates two closely adjacent cones in which the upper is an S cone [(a) and (b), double arrow]. Note the difference in the CMS of these two cones, x 300.
FIG. 1. The PNA binding pattern in adult Macaca monkey retina is shown on a frozen tangential section at the outer segment level (a). an Epon vertical section (b) and an Epon tangential section through the outer segment level (c). A regularly-spaced minority of cones have heavier labeling of PNA-FITC in their CMS. Some of these are marked by arrows, x 500.
segments [Fig. 3(b), arrowhead]. The CMS on most cone outer segments (middle of figure) and inner segments (bottom of figure) is strikingly reduced, but a few cones still have a heavily labeled CMS surrounding the outer segment (thick arrow) and inner segment (thin arrow). The similarity of the labeling pattern of OS-2 and PNA to Fig. 2 indicates that these are S
cones. W h e n trypsin pretreatment was increased to 60 seconds, the CMS on most cones disappeared but the outer segment m e m b r a n e remain labeled [Fig. 3(c)] while the CMS on S cones still persisted [Fig. 3(c), arrows]. In the primate retina plastic section PNA staining yielded reliable and consistent differences between the CMS of L/M and S cones. W h e n tissue from the same eyes was studied using frozen sections, the S cone CMS had brighter labeling, but the differences were not as striking nor as consistent. This indicates that the CMS difference was not due to tissue preparation, but dehydration m a y emphasize the difference. Monkey S cones had m u c h heavier binding of PNA to their CMS, indicating either that their CMS was thicker or that it had a higher concentration of terminal galactose-Nacetyl galactosamine disaccaride residues. The trypsin digestion also supported this conclusion. This observation is similar to CMS differences found between squirrel cones (Szel et al., 1993). In primates S cone inner segments are taller, larger and have a more cylindrical shape, their outer segments are shorter, and their synaptic pedicles are smaller t h a n L/M cones (deMonasterio et al., 1 9 8 5 : Curcio et al., 1 9 9 1 ; Ahnelt, Kolb and Pflug, 1987). Our finding of more intense PNA binding to the S cone CMS contributes a n o t h e r morphological difference. The CMS contains chondroitin 6-sulfate glycosa m i n o g l y c a n and glycoconjugates ( H a g e m a n and Johnson, 1986, 1991). SDS-polyacylamide gel electrophoresis and Western blotting of whole retinal extracts
PNA LABELING IN ADULT MONKEY CONES
765
FIG. 3. PNA labeling on Epon vertical (a) and tangential [(b) and (c)] sections after 20 sec [(a) and {b)] and 60 sec (c) trypsin pretreatment. Trypsinization removed the lectin label from the CMS in the majority of cones but their outer segment membranes still labeled. A few cones (arrows) retained a brightly labeled CMS. x 500.
found six m a j o r groups of P N A - b i n d i n g glycoproteins r a n g i n g b e t w e e n 30 a n d 88 kDa ( H a g e m a n a n d Johnson, 1986). F o u r of t h e m ( G P 3 9 / 4 0 . G P 4 2 / 4 5 , GP54 a n d GP60) were intensely labeled by PNA, with G P 5 4 being most sensitive to trypsin digestion. The differential P N A labeling p a t t e r n b e t w e e n S a n d L / M cones a n d the effect of trypsin digestion on PNA b i n d i n g c a n be interpreted in two w a y s w h i c h are n o t m u t u a l l y exclusive. One is t h a t the S cone CMS has the s a m e c a r b o h y d r a t e c o m p o n e n t s as L / M cone CMS, b u t S cones simply h a v e a larger total a m o u n t in a thicker CMS w h i c h takes l o n g e r to digest. The a l t e r n a t i v e is t h a t the L / M cone CMS c o n t a i n s m o r e trypsinsensitive GP54, a n d S cones h a v e m o r e of the o t h e r P N A - b i n d i n g c o m p o n e n t s . For the S cone, the CMS over the tip of o u t e r s e g m e n t m i g h t h a v e m o r e G P 5 4 w h i c h causes the rapid loss of PNA labeling after trypsinization. This s t u d y h a s s h o w n t h a t m o n k e y S cones h a v e a different glycoprotein m i c r o e n v i r o n m e n t t h a n L / M cones. S cones are k n o w n to be m o r e sensitive to e n v i r o n m e n t a l , light a n d a g i n g effects (Sperling, 1991), some of w h i c h could be m e d i a t e d by this differential m i c r o e n v i r o n m e n t lying b e t w e e n p h o t o receptors a n d p i g m e n t epithelium.
QI Y A N " KEELY B U M S T E D a A N I T A H E N D R I C K S O N a,b*
Departments of ~Biological Structure and b Ophthalmology, University of Washington, Seattle, WA 98195, U.S.A.
References
Acknowledgments
Ahnelt, P. K., Kolb, H. and Pflug, R. (1987). Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. 1. Comp, Neurol. 255, 18-34. Blanks, J. C. and Johnson, L. V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 25. 546-57. Blanks, ]. C., Hageman, G. S.. Johnson, L. V. and Spee. C. (1988). Ultrastructural visualization of primate cone photoreceptor matrix sheaths. ]. Comp. Neurol. 270, 288-300. Curcio, C. A., Allen, K. A., Sloan, K. R,, Lerea, C. L., Hurley, J. B., Klock, I. B. and Milam, A. H. (1991J. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. I. Comp. Neurol. 312, 610-24, deMonasterio. F. M.. McCrane, E. P., Newlander, J. K. and Schein, S. ]. {1985). Density profle of blue-sensitive cones along the horizontal meridian of macaque retina. Invest. Ophthalmol. Vis. Sci. 26, 289-302. Hageman, G.S. and Johnson, L.V. (1986). Biochemical characterization of the major peanut agglutinin-binding glycoproteins in vertebrate retinae: a species comparison. ]. Comp. Neurol. 249, 499-510.
This research was supported by EY01208, EY04536 and Research to Prevent Blindness Inc.
* For correspondence at: BiologicalStructure SM20. University of Washington. Seattle. WA 98195. U.S.A.
Q. Y A N ET AL.
766
Hageman, G.S. and ]ohnson, L.V. (1991). Structure, composition and function of the retinal interphotoreceptor matrix. In Progress in Retinal Research. (Eds Osborne, N. N. and Chader, G. ].) Vol. 10, Pp. 207-49. Pergamon Press: Oxford. Hollyfield, ]. G., Rayborn, M. E., Landers, R. A. and Myers, K.M. (1990). Insoluble interphotoreceptor matrix domains surround rod photoreceptors in the human retina. Exp. Eye Res. 51, 107-10. Johnson, L.V., Hageman, G.S. and Blanks, ]. C. (1985). Restricted extracellular matrix domains ensheath cone photoreceptors in vertebrate retinae. In: The Interphotoreceptor Matrix in Health and Disease. (Eds Bridges, C. D. B. and Adler, A.].) Pp. 33-44. Plenum Press: New York, U.S.A. Johnson, L.V., Hageman, G.S. and Blanks, ]. C. (1986). Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 27, 129-35. Lotan, R., Skutelsky, E., Danon, D. and Sharon, N. (1975). The purification, composition, and specificity of anti-T
lectin from peanut (Arachis hypogaea). J. Biol. Chem. 250, 8518-23. Nathans, J., Thomas, D. and Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding blue, green and red pigments. Science 232, 193-202. Sameshima, M., Uehara, F. and Ohba, N. (1987). Specialization of the interphotoreceptor matrices around cone and rod photoreceptor cells in the monkey retina, as revealed by lectin cytochemistry. Exp. Eye Res. 45, 845-63. Sperling, H.G. (1991). Vulnerability of the blue-sensitive mechanism. In: Vision and Visual Dysfunction. (Ed. Dillon, J.C. Inherited and Acquired Colour Vision Deficiencies: Fundamental Aspects and Clinical Studies, Vol. 7. Pp. 72-87. CRC Press: Boca Raton, U.S.A. Szel, A., yon Schantz, M., Rohlich, P., Farber, D. B. and van Veen, T. (1993). Difference in PNA label intensity between short- and middle-wavelength sensitive cones in the ground squirrel retina. Invest. Ophthalmol. Vis. Sci. 34, 3641-5.
(Received Cleveland 10 April 1995 and accepted in revised form 19 July 1995)