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Presence and foveal enrichment of rod opsin in the all cone Э retina of the American chameleon.

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THE ANATOMICAL RECORD 237:299-307 (1993)
Presence and Foveal Enrichment of Rod Opsin in the “All Cone”
Retina of the American Chameleon
DAVID S. McDEVITT, SAMIR K. BRAHMA, JEAN-CLAUDE JEANNY, AND
DAVID HICKS
Laboratories of Anatomy, Department of Animal Biology, University of Pennsylvania
School of Veterinary Medicine, Philadelphia, Pennsylvania 19104 (D.S.M.); Znstitut
National de la Santk et de la Recherche Mkdicale, Unite 118, 75016 Paris, France (D.S.M.,
J.-C.J., D.H.); and Hubrecht Laboratory, Netherlands Institute for Developmental Biology,
3584 CT Utrecht, The Netherlands (S.K.B.)
ABSTRACT
The retinal photoreceptors of the eye of the American chameleon,Anolis carolinensis, have been considered to be exclusively cones.
Its retina is unusual for possessing two foveas (areas associated with
heightened visual acuity),with the major, central fovea deeply incised and
very densely packed with photoreceptors. Immunoblotting and light- and
electron microscopic-immunocytochemistry, using several opsin monoclonal antibodies previously found specific for rods, demonstrated the
presence and localization of this protein in the Amlis retina. This visual
pigment appears sparsely in a subpopulation of photoreceptors in the periphery but overwhelmingly in the central fovea. Complementary results
with cone-specific antibody and lectin binding corroborated this spatial
organization. These results, as well as those with geckos, suggest that photoreceptor morphology is not an accurate guide among the lacertilians to
visual pigment content, and that this phylogenetic grouping may constitute
a crossroads in vertebrate photoreceptor evolution.
0 1993 Wiley-Liss, Inc.
Key words: Rhodopsin, Retina, Lizards, Photoreceptors, Evolution, A m lis carolinensis, Gekko gekko,Immunohistochemistry
The photoreceptors of the vertebrate eye have been
categorized as rods or cones, generally according to the
shape of their outer segments, since the 19th century.
It has become apparent, however, that this concept of a
“duplex” retina, ascribing specific and exclusive optical
properties and functions to each photoreceptor type, is
perhaps too simplistic (Underwood, 1968; Pedler, 1969;
Crescitelli, 1990). The visual pigments responsible for
transduction of light energy have been localized primarily in the outer segments of rods and cones, with
reports of presence also in the inner segment and cell
body (Hicks and Barnstable, 1987; St. Jules e t al.,
1990). The visual pigments constitute integral membrane proteins and are composed of a n apoprotein,
opsin (for rods and specific color sensitive cones) and a
chromophore covalently linked to its active-site lysine.
Light causes isomerization of the chromophore to a
trans configuration and initiation of the transduction
cascade involving cyclic GMP and transducin and leading to visual perception of light and color (Saari, 1990;
Stryer, 1991). Rod opsin is by far the most well characterized of the opsins, but analysis of visual pigment
protein genes in mammals has provided information on
the similarity and evolutionary conservation of other
opsins (Nathans et al., 1986; Applebury and Hargrave,
1986). The opsins are characterized by differing absorption maxima in the visible spectrum, ranging from
0 1993 WILEY-LISS, INC
blue-sensitive to red-sensitive, e.g., rod opsin at 500 nm
(Knowles and Dartnall, 1977). The different absorption
profiles are generated by changes in the apoprotein; in
all vertebrates (with the exception of certain fishes and
amphibia) the chromophore used is 11-cis retinal
(Crescitelli, 1990). Govardovskii et al. (1992), using immunocytochemistry, have proposed two distinct phylogenetic groupings of vertebrate visual pigments, those
belonging to amphibia and terrestial vertebrates, and
those to cartilaginous and bony fishes.
Anolis carolinensis, the American chameleon, a diurnal lizard native to the southeastern United States,
is popularly known for its ability to reversibly change
body color. It and other Anolis species, together with
raptorial birds, are unusual in possessing two foveas in
their retina (Underwood, 1951, 1970; Makaretz and
Levine, 1980; Fite and Lister, 1981). These, usually
deeply incised, eye structures are associated with
heightened visual acuity due to a concentration of photoreceptors (usually cones). A. carolinensis is considered, as all diurnal lizards, to have a n all-cone retina
Received April 23, 1993; accepted J u n e 3, 1993.
David Hicks is now at the Clinique Ophtalmologique, Hopitaux
Universitaires, BP 426, 67091 Strasbourg, France.
301
ROD OPSIN IN AN "ALL-CONE'' RETINA
by morphological criteria (Underwood, 1970; Crescitelli, 1972). We decided to investigate the possible presence and distribution of rod and cone photoreceptors in
this species. We have at our disposal monoclonal antibodies binding to different regions of the opsin apoprotein of rat and bovine rhodopsin: rho-4D2 to the N-terminal region (2-39) (Hicks and Molday, 1986); rho-4B4
to the F,-F, loop region (231-250) (MacKenzie and
Molday, 1982); and rho-1D4 to the C-terminal region
(341-348) (Molday and MacKenzie, 1983). All have
been previously demonstrated a s specific for rod opsin
and unreactive to cone opsin in the mammals and amphibia (Hicks and Molday, 1986; Molday, 1988; Bugra
et al., 1992). To identify cones, we used 1) the CSA-1
antibody originally derived by Johnson and Hageman
(1988) and subsequently shown to bind to red and
green, but not blue, sensitive cones (Rohlich et al.,
1989b) and 2) peanut agglutinin lectin, known to bind
to cone matrix sheaths (Blanks and Johnson, 1983).
The results presented not only indicate that this species' retina contains significant numbers of rod opsinpositive cells, but also that they are highly concentrated within the central fovea.
(1983); as a control, 50 mM D-galactose (Sigma Chemical Co., St. Louis, MO) was used to inhibit lectin binding. Immunopositive cells have been expressed per 100
countable cells in peripheral retina. Sections were
viewed on a Zeiss epifluorescence photomicroscope
equipped with FITC and rhodamine filter modules.
Immunoelectron Microscopy
Eyes from dark-adapted A . carolinensis were hemisected and fixed in 1.25% glutaraldehyde in 0.1 M
sodium cacodylate, pH 7.3, at 4°C. Small blocks of retina were freed as much as possible of adherent retinal
pigment epithelium and incubated in 1:20 rho-4D2 antibody overnight. Following washing in the same
buffer, blocks were successively incubated in goat antimouse IgG-Biotin (Amersham) and Extravidin-Dextran-gold (Hicks and Molday, 1986). After washing,
blocks were osmicated, dehydrated, and embedded in
Epon/Araldite resin. Ultrathin sections were collected,
counter-stained and examined under a JEOL 35s
transmission electron microscope.
lmmunoblotting
The opsins (0.5%SDS), prepared according to Knight
and Raymond (1990), and a mixture of low molecular
Adult male and female A . carolinensis (Charles Sul- weight proteins a s markers were co-fractionated on
livan, Nashville, TN 37211) were fed housefly larvae SDS polyacrylamide gel (12%) and then electrophoretand crickets, and kept for up to 6 months before sacri- ically transblotted to nitrocellulose membranes (Towfice. Gekko gekko, the Tokay gecko, and Plethodon ci- bin et al., 1979; McDevitt and Brahma, 1990). The
nereus, the red-backed salamander, were purchased lo- opsin lanes were then each reacted with the rho-4D2
cally. Their care was in accordance with institutional antibody (1:2,000), followed by washing in PBS, incuand D.H.E.W. guidelines. They were dark-adapted, bation in horseradish peroxidase-conjugated rabbit
anesthetized by chilling, and immediately sacrificed by anti-mouse immunoglobulins (Dakopatts), and the
decapitation. The eyes (28) were then removed, fixed in color developed with 3-3',5-5'tetramethyl benzidine
cold 3% paraformaldehyde in phosphate-buffered sa- (Sigma Chemical Co., St. Louis, MO). Marker proteins
line (PBS), mounted in O.C.T. (Miles Scientific), and were stained with 0.5%Amido Black.
frozen for cryostat sectioning (7 pm) and subsequent
RESULTS
immunofluorescence. No pre-treatment or blocking
Surprisingly, a population of photoreceptors in the
was found necessary for the sections which were exposed, in succession, to the mouse monoclonal antibod- retina of A . carolinensis exhibited a strong and unies rho-4D2, 1D4, 4B4, or CSA-1 (culture fluids used equivocal positive immunof luorescence for rod opsin,
without dilution or diluted 1:50), goat anti-mouse IgG- using the rho-4D2 antibody (Fig. 1); 17% of the photoBiotin (Amersham), and then Extravidin-Fluorescein receptors in the peripheral (nasal; non-foveal) retina
isothiocyanate (FITC-Sigma Chemical Co., St. Louis, were positive (see Fig. 4C), as were those of the temMO). For double-labelling, rhodamine was substituted poral fovea (very shallow in A . carolinensis; not
for FITC as fluorescent label. As a control in this and shown). Contrary to the other areas of the retina, the
other immunohistochemistry, non-immune mouse IgG central fovea had a n approximately 90-fold enrichment
or PBS was substituted for the primary antibody. Pea- of photoreceptor outer segments; because of this dennut agglutinin-FITC (Sigma Chemical Co., St. Louis, sity, i t was not feasible to identify and quantify indiMO) binding was according to Blanks and Johnson vidual outer segments (Makaretz and Levine, 1980;
Fite and Lister, 1981). It is clear, however, that outer
segments positive for rod opsin constitute a n overwhelming majority of those of the central fovea (Fig.
1D). Similar results, although the staining intensity
Fig. 1. Photomicrographs of sections through the deepest part of the
A . carolinensis central (CF) fovea: A and C (phase-contrast),for his- was less, were obtained with the rho-1D4 and rho-4B4
antibodies; these were not further employed.
tological reference to B and D (epifluorescence), respectively. Note in
A the displacement of most retinal layers from the fovea (arrow, outer
This specificity of labelling within the Anolis retina
limiting membrane), accompanied by extremely dense packing (C) of
was
confirmed by immunoelectron microscopy using
photoreceptors, whose attenuated inner (is) and outer segments (0s)
colloidal gold probes (Fig. 2). It can be seen that several
are enveloped by processes of the pigmented epithelium (p).B and D
(an enlargement of the central fovea in B), treated with rho-4D2 an- photoreceptor outer and inner segments completely
tibody, demonstrate the striking concentration of rod-opsin positive
negative for rod opsin are adjacent to positive inner
photoreceptors in the central fovea. gc, ganglion cell layer; ipl, inner
and
outer segments clearly exhibiting particles on the
plexiform layer; inl, inner nuclear layer; opl, outer plexiform layer;
onl, outer nuclear layer; pr, photoreceptor region; pe, pigmented epi- plasma membrane, e.g., as in Figure 2B,C. Underwood
(1951, 1970) has described three types of photorecepthelium; ch, choroid; sc, sclera. A and B, X 74; C and D, X 457.
MATERIALS AND METHODS
Preparation of Tissue and lmmunofluorescence
302
D.S. McDEVITT E T AL.
Fig. 2. Montage (A) of low power ( x 1,730)electron micrographs, A .
carolinensis peripheral retina. The retinal pigmented epithelium,
whose processes heavily invest and obscure the photoreceptors in this
organism, has been mechanically removed. Portions of six photoreceptors are visible, and only one exhibits immunoreactivity (arrows)
for rod opsin, a s evidenced by accumulation of immunogold particles
(insets B and C) on the external plasma membrane. Note in B and C
negative photoreceptors to either side of the rod opsin-positive one,
which we identify as a minor single cone. B: incomplete outer segment
contiguous with oil droplet ( x 11,900); C: ellipsoid area of inner segment with mitochondria ( x 16,700).
tors in the Anolis lineatopus retina: major single cones,
minor single cones, and double cones. As measured in
the peripheral (nasal) retina, the proportions of each
are 57%, 14%, and 29%, respectively (Underwood,
1970). Using his morphological criteria, we can iden-
tify those rho-4D2 immunopositive cells, e.g., Figure 2,
as his “minor single cones,” and their distribution
(17%) in A. carolinensis peripheral retina is in agreement with Underwood for this cell type. The very
heavy investment of A. carolinensis photoreceptors by
ROD OPSIN IN AN “ALL-CONE” RETINA
-0
94
67
+
43
*
,
,
30
2 0.1
A
B
C
Fig. 3. Imrnunoblot, with rho-4D2 diluted 1:2,000, of purified opsin
preparations (0.5%SDS) from rat (B) and A. carolinensis (C) retinas.
Under these conditions, the Anolis opsin and its presumptive dimer
(arrows) consistently migrate as approximately 35K and 70K, respectively, slightly larger than the rat opsin counterparts. A, marker
proteins; (o), origin.
Fig. 4. Photomicrographs of sections through the A . carolinensis
retina. A (phase-contrast) and B (epifluorescence) peripheral retina
treated with cone-specific antibody (CSA); C (epifluorescence),similar section treated with rho-4D2 (rod opsin) antibody. Many more cells
in the photoreceptor region (pr) stain a s cones rather than rods. D
303
pigment (see Figures) makes such identification at the
light microscopic level difficult.
Immunoblotting of purified rod opsin preparations
from rat and A . carolinensis retinas confirmed the presence of rod opsin in the chameleon retina and the specificity of the rho-4D2 antibody for use in this investigation (Fig. 3). The chameleon rod opsin demonstrates
slight phylogenetic variability in molecular weight
from that derived from the predominantly-rod rat retina, as reported for cow and frog (Molday and Molday,
1979).
A. carolinensis retina was similarly probed by immunofluorescence techniques with both a cone-specific
monoclonal antibody (CSA-1, gift of Dr. G. Hageman)
and peanut agglutinin (PNA).The results (Fig. 4)were
complementary to those obtained with the rod opsin
antibody. Most (70%) of the photoreceptor outer segments of the peripheral retina were positive for both
CSA and PNA. In the central foveal region, however,
no photoreceptors (CSA) and less than 5% (PNA; density of photoreceptors necessitated estimation of area
fluorescing) showed reactivity for these cone-specific
reagents. The slight difference in labeling Seen may be
due to differential recognition of a small slhset of cones
by PNA (Fig. 4; CSA data only). Double-labeling with
CSA and rho-4D2 also confirmed that each antibody
recognized a different population of photoreceptors
(phase-contrast)and E (epifluorescence)section through the region of
the central fovea (CF) treated with cone-specific antibody. Note complete lack of a positive reaction for cones, in an area similar to that in
Figure 1. A-E, x 183.Orientation: vitreous (interior) of the eye, to the
left; sclera (outer) layer of the eye, to the right.
304
D.S. McDEVITT ET AL.
Fig. 5. Photomicrographs ( x 183)of a section through A . carolinensis peripheral retina. A, phase contrast of B, epifluorescence. In B, the
section has been double-labelled with rho-4D2 (rhodamine label) and
CSA (FITC label) antibodies. The weakly fluorescing band of photo-
receptors (arrow) are CSA-positive, those strongly-fluorescing are
rho-4D2 positive; discrimination between labels is possible because of
the use of label-specific optical filtration. Orientation: sclera to the
left, vitreous to the right.
(Fig. 5). Since CSA recognizes red and green cones in
other vertebrates tested so far (Rohlich et al., 1989b),
we are confident that rho-4D2 positive cells contain
rhodopsin.
Because the nocturnal Tokay gecko, G. gekko, is considered to possess (very large) rods exclusively (Underwood, 1970), we have also examined this retina. We
have obtained results contradictory to that expected
from the morphological classification of its photo-receptors: in double-label immunofluorescence, both rod
opsin positive (as expected if “all r o d ) and cone positive cells could be identified (Fig. 6A). For comparison,
another putative “mostly-rod” retina from the nocturnal P. cinereus, the red-backed salamander, has been
included (Fig. 6B). The specific gecko photoreceptor
types reacting with each antibody in Figure 6A have
not been identified, but the low percentage (12%) of
rod-opsin positive cells found by us is in general agreement with that reported by Szel et al. (1986) for another nocturnal gecko, Teratoscincus.
ROD OPSIN IN AN “ALL-CONE” RETINA
305
Fig. 6. Epifluorescence photomicrographs of sections through the
peripheral retinae of A) G . gekko ( x 183) and B) P.cinereus ( x 457). In
A), the section has been double-labelled with rho-4D2 (rhodamine
label) and CSA (FITC label) antibodies. Those weakly fluorescing
photoreceptors are CSA-positive, those strongly fluorescing are rho-
4D2 positive; discrimination between labels is possible because of the
use of label-specific optical filtration. In B), all photoreceptor inner
and outer segments (here, very elongated in this nocturnal amphibian) are strongly rho-4D2 positive, as expected by habitat. Orientation: sclera to the left, vitreous to the right.
DISCUSSION
CSA-1 antibody, which has been shown to bind greenand red-sensitive cones in the pig retina (Rohlich et al.,
1989b) did not double-label any rho-4D2 positive cells
in Anolis retina (Fig. 5). Although no studies of CSA-1
specificity have been undertaken in this species, taken
altogether, these data lead us to conclude that a large
number of Anolis photoreceptor cells display rod-like
immunological characteristics.
Among the lizards, photoreceptor composition varies
widely. Studies of the geckos have led to the view that
their photoreceptors have undergone a morphological
evolution. Thus, what are ostensibly the rods of nocturnal geckos are the result of a “transmutation” from
the cones of the diurnal geckos. Indeed, a few diurnal
geckos are considered to have undergone a second
transmutation, of rods back to cones. The basis for this
hypothesis is differing photoreceptor organelle cytology, as well a s some visual pigment analyses (Walls,
1934; Underwood, 1968,1970; Pedler, 1969; Crescitelli,
1977, 1990). Szel et al. (1986), immunocytochemically,
and Govardovskii et al. (1984) and Crescitelli (1990),
microspectrophotometrically, have demonstrated the
presence of two photopigments in geckos, absorbing
near 520 nm and 467 nm (G. gekko) and occurring in
We have demonstrated here that the retina of A . carolinensis, formerly considered to be all-cone, contains a
large number of photoreceptors displaying immunoreactivity to monoclonal antibodies specific for
rhodopsin. The results presented here were obtained
using rho-4D2, a monoclonal antibody that labels only
rod photoreceptor cells in a variety of species: cow, rat,
mouse in the mammalia (Hicks and Molday, 1986;
Hicks e t al., 1989); chicken (Hicks, unpublished observation); and frog and newt (Hicks and Molday, 1986;
Bugra et al., 1992), a s well a s goldfish (Knight and
Raymond, 1990). Thus this antibody has been demonstrated to be a reliable marker of rod cells. In general,
the amino terminal of rhodopsin bears the least homology to cone opsins and other members of the opsin superfamily, and Rohlich et al. (1989a) have shown that
0 of 8 monoclonal antibodies binding to this region
cross-reacted with cones. Our confidence in the recognition of rod cells within Anolis retina by rho-4D2 is
further strengthened by the identical, albeit fainter,
staining pattern observed with rhodopsin antibodies
directed against two other distant epitopes, in the carboxyl terminal and F,-F, loop. Furthermore, use of the
306
D.S. McDEVITT ET AL.
different cells. In addition, Kojima et al. (1992) have
recently presented cDNA data that support the presence of cone visual pigments in G . gekko rod cells.
These results, as do ours, support the transmutation
hypothesis and indicate that photoreceptor morphology
is less conserved evolutionarily than photopigment
protein composition.
Little is known of the visual pigment&) of Anolis
species, in large part because of the very small size of
the photoreceptor outer segments. Yu and Fager (1982)
report two pigments with absorption maxima of 500
nm (indicative of rhodopsin) and 625 nm, yet conclude
that both are cone pigments, because of morphological
criteria. A phosphorylated A. carolinensis retinal protein comigrated with phosphorylated rat rod opsin, yet
a polyclonal rat opsin antibody (epitope uncharacterized) was negative in Anolis retinal immunoblots (Walter et al., 1986). In a classic study of opsin genomic
Southern blots, however, unexpected hybridization of a
bovine cDNA rod opsin probe with A. carolinensis DNA
(“puzzling” because supposedly all-cone) was noted
(Martin e t al., 1986). Lastly, the phototransduction
phosphodiesterase (PDE) complex in A. carolinensis is
similar in many features to that of mammalian rod
outer segments (Booth et al., 1991). Our results certainly confirm the existence of cones (photoreceptor
cells with cone-specific antigen and lectin-binding
properties) in the retina of A. carolinensis, yet, in
agreement with the single brief report (Yu and Fager,
1982) of two visual pigments, also demonstrate the
presence and localization of a visual pigment homologous with rod opsin. More strikingly, photoreceptors
expressing rod opsin constitute a n overwhelming proportion of those found packed into the central fovea of
A. carolinensis. The fovea is predominantly or all cone
in most birds and mammals, yet the foveas of the owl
and owl monkey are predominantly or all rod (Crescitelli, 1972; Kemp and Jackson, 1991). The usual association of rods and low light levels is not immediately
reconcilable with the concept of a rod-opsin packed
fovea in a diurnal lizard. If viewed however in the context of Anolis as a n evolutionary “half-way house” for
cones transmutating to rods or vice-versa, it is not surprising. We have seen this intimated in the geckos
(which do not possess a fovea). In addition, Okano et al.
(1992) report cDNA evidence in the chicken that supports visual pigment evolution in this direction, i.e.,
rhodopsin has evolved out of cone visual pigments.
For logistical reasons cited previously, the use of
other properties that might define a rod or cone, e.g.,
spectral absorbance, and sensitivity and rate of response to light, is not practical in A. carolinensis. Perhaps a rod could be defined as a vertebrate photoreceptor cell expressing rhodopsin, a cone as one expressing
one of the cone pigments, and insufficient evolutionary
time has passed to permit matching form (“rod/“cone”)
to function (rhodopsinicone pigments) in the lacertilians. As suggested by Goldsmith (1990), “the absorption spectrum is how we ordinarily distinguish one visual pigment from another, but natural selection
clearly has a wider set of criteria on which it works.”
Isolation of the lizard visual pigment genes and structural analysis of their products may provide us with
such criteria and confirm this grouping as a crossroads
in vertebrate photoreceptor evolution.
ACKNOWLEDGMENTS
We thank Andree Bouterie and L. Jonet for excellent
technical assistance, H. Coet for photography, Dr. G.
Hageman for the gift of Cone-Specific Antibody, and
Dr. Y. Courtois, Director, I.N.S.E.R.M. Unite 118, for
advice and support. This work was supported by the
I.N.S.E.R.M. (France) and N.I.H. grant T32 HD 07067,
and Association Claude Bernard, Fondation pour la
Recherche Medicale, and N.A.T.O. Collaborative Research Grant 890942 (D.S.McD.1.
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presence, retina, rod, cones, enrichment, fovea, american, opsin, chameleons
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