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Keratins in the Epidermis of Chelonians, Lepidosaurians, and Archosaurians 1N 2 LORENZO ALIBARDI and ROGER H

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Keratins in the Epidermis of Chelonians, Lepidosaurians, and Archosaurians 1N 2 LORENZO ALIBARDI and ROGER H JOURNAL OF EXPERIMENTAL ZOOLOGY 293:27–38 (2002) Immunocytochemical Analysis of Beta (b)Keratins in the Epidermis of Chelonians, Lepidosaurians, and Archosaurians 1n 2 LORENZO ALIBARDI AND ROGER H. SAWYER 1Dipartimento di Biologia evoluzionistica sperimentale, University of Bologna, 40126, Bologna, Italy 2 Biological Sciences Department, University of South Carolina, Columbia, South Carolina 29208 ABSTRACT Beta (b) keratins are present only in the avian and reptilian epidermises. Although much is known about the biochemistry and molecular biology of the b keratins in birds, little is known for reptiles. In this study we have examined the distribution of b keratins in the adult epidermis of turtle, lizard, snake, tuatara, and alligator using light and electron immunocytochemistry with a well-characterized antiserum (anti-b1 antiserum) made against a known avian scale type b keratin. In lizard, snake, and tuatara epidermis this antiserum reacts strongly with the beta-layer, more weakly with the oberhautchen before it merges with the beta-layer, and least intensely with the mesos layer. In addition, the anti-b1 antiserum reacts speci¢cally with the setae of climbing pads in gekos, the plastron and carapace of turtles, and the stratum corneum of alligator epidermis. Electron microscopic studies con¢rm that the reaction of the anti-b1 antiserum is exclusively with characteristic bundles of the 3-nm b keratin ¢laments in the cells of the forming beta-layer, and with the densely packed electron-lucent areas of b keratin in the mature bet- layer.These immunocytochemical results suggest that the 3-nm b keratin ¢laments of the reptilian integument are phylogenetically related to those found in avian epidermal appendages. J. Exp. Zool. 293:27^38, 2002. r 2002 Wiley-Liss, Inc. Reptiles and birds are the only organisms known the similarity in chemical-physical properties of to possess b keratins in their epidermal tissues and reptilian and bird hard keratins to be due to func- their appendages (Baden and Maderson,’70; O’Guin tional convergence that indicates no phylogenetic and Sawyer,’82; O’Guin et al.,’82; Gregg and Rogers, relationship (Brush,’93). ’85; Frazer and Parry,’96; Sawyer et al., ’86, 2000). Microscopic, biochemical, and biophysical evi- These proteins are the major structural compo- dence of similarities between avian and reptilian b nents of the scales and claws of reptiles and birds keratins have been demonstrated in a few studies and the spurs, beaks, and feathers of birds. The b on lizard scales, turtle shells, and alligator claws. keratins have molecular weights ranging from 10^ Immunological similarity between avian and repti- 25 kDa. Alpha (a) keratins, present in the epidermis lian b keratins has been shown by Carver (’85,’88), of all vertebrates, have molecular weights ranging Carver and Sawyer (’87), Mays (’98), and Sawyer et from 40^68 kDa (Frazer et al., ’72; Baden et al., ’74; al. (2000). The ¢ne structure of cells known to con- Gregg and Rogers, ’85; Inglis et al., ’87; Shames tain b keratins displays interwoven and tightly et al., ’89, ’91; Presland et al., ’89a, b). It is believed packed bundles of 3-nm ¢laments in both reptiles that the b keratins are phylogenetically more recent and birds. Thus, an important step toward under- than a keratins, but their origin is unknown (Mar- standing the molecular evolution of these keratins shall and Gillespie, ’82; Gregg and Rogers, ’85; is to establish the immunological nature of these 3- Brush,’93,’96; Frazer and Parry,’96). Furthermore, nm ¢laments in adult reptiles relative to that of little is known about how and when they diverged in different epidermal appendages (Gillespie et al.,’82; Grant sponsor: University of Bologna. O’Guin and Sawyer, ’82; Shames et al., ’88, ’89, ’91; *Correspondence to: Dipartimento di Biologia evoluzionistica speri- mentale, University of Bologna, via Selmi 3, 40126, Bologna, Italy. Presland et al.,’89a, b; Whitbread et al.,’91; Sawyer E-mail: [email protected] et al., ’86, 2000). Wyld and Brush (’79, ’83) question Received 29 October 2001; Accepted 14 February 2002 Published online in Wiley InterScience (www.interscience.wiley. the reptilian origin of avian b keratins and consider com). DOI: 10.1002/jez.10145 r 2002 WILEY-LISS, INC. 28 L. ALIBARDI AND R.H. SAWYER birds. Here, we use an antiserum (designated anti- with 2% bovine serum albumin (BSA). Nonspecific b1) against a single polypeptide spot (spot #1), antigenic sites were blocked with 5% normal goat which was isolated from polyacrylamide following serum inTBS-BSA (30 min).The sections were incu- separation by two-dimensional gel electrophoresis bated overnight at 41Cintheprimaryantibody, (Shames et al.,’91; Sawyer et al., 2000).The polypep- anti-b1 (Shames et al., ’91; Sawyer et al., 2000), tide represented by spot #1 has been identi¢ed as rinsed repeatedly, and incubated for 1hr at room an avian scale keratin following hybrid selection of temperature with a goat anti-rabbit FITC-conju- mRNA with a known avian scale keratin sequence gated secondary antibody (Sigma, St. Louis, MO) and subsequent in vitro translation (Shames et al., in TBS. Controls were incubated with buffer only. ’89,’91). After prolonged rinsing, sections were mounted in We have examined epidermal tissues of represen- Fluoromount (EM Sciences, Fort Washington, PA) tatives of all extant clades of reptiles, lepidosauria and observed with a Zeiss, Jena, Germany epifluor- (lizards, snakes, tuatara), chelonia (turtle), and escence microscope. archosauria (crocodilians) for anti-b1-positive cells Because the tissues of S. punctatus were ¢xed in in which the presence of 3-nm ¢laments that react 10% acidic formalin, which may mask or destroy speci¢cally with the anti-b1 antiserum can be un- antigenic sites, they were handled as recommended ambiguously demonstrated. Our results indicate by Shi et al. (’91) to retrieve immunoreactivity. that the anti-b1 antiserum reacts with the beta- Thin sections were incubated at room tempera- layers and speci¢cally with the 3-nm ¢laments in ture for 15 min in TBS containing 0.1% Triton-X the epidermal cells of lepidosauria, chelonia, and and 1% cold-water ¢sh gelatin and then incubated archosauria.This study clearly shows that the b ker- overnight in the same bu¡er at 41Cwiththepri- atins of sauropsid reptiles and birds share common mary antibody (controls were incubated with the antigenic epitopes, and it strongly suggests a phylo- bu¡er only). After rinsing in bu¡er, grids were in- genetic relationship between the b keratins of the cubated for 1hr at room temperature with the sec- two groups. ondary antirabbit antibody conjugated to 10-nm gold beads (Sigma or Chemicon, Temecula, CA). MATERIALS AND METHODS After rinsing in the bu¡er, the grids were rinsed In this study, samples of skin, 2^4 mm long, were in distilled water, dried, and observed unstained collected from various reptilian species and imme- or slightly stained (5 min) with uranyl acetate. diately fixed.The species used were young adult tur- tles (Chrysemis picta,n¼ 5; and hatchlings of RESULTS Emydura macquarii,n¼ 2; carapace and plastron), alligator hatchlings (Alligator mississippiensis, Histology of reptilian epidermis n ¼ 2; dorsal and ventral body skin), adult salt- The histology of the epidermis of turtles, lizards, water crocodiles (Crocodylus porosus,n¼ 2; tail snakes, alligators, and the tuatara has been well skin), adult wall lizards (Podarcis muralis,n¼ 5; documented (Alexander, ’70; Maderson, ’85; Land- tail skin), adult geckos (Hemidactylus turcicus, mann, ’86; Matoltsy, ’87). In turtles the carapace n ¼ 5; and Sphaerodactylus argus,n¼ 2; digits), and plastron are formed by the proliferation of cu- posthatched snakes (Natrix natrix,n¼ 3; dorsal boidal basal cells that stratify to form the thick midbody and ventral skin), water pythons (Liasis stratum corneum. In lizards and snakes the epider- fuscus,n¼ 2; midbody scales), and tuatara (Spheno- mis may be in either the resting or renewal phase of don punctatus,n¼ 3; tail skin). Samples were fixed the shedding cycle. During the renewal phase the in either 4% paraformaldehyde in 0.1M phosphate germinative layer produces the oberhautchen, beta, buffer, pH 7.4, or in Carnoy’s fluid for 3^5 hours. mesos, alpha, lacunar, and clear layers.These layers After dehydration the tissues were embedded in constitute an epidermal generation and are re- Bioacryl resin (Scala et al., ’92) or Lowcryl K4M placed by a new inner epidermal generation at the (Polysciences,Warrington, PA). time of molting.The oberhautchen of the outer gen- Thick sections (1^4 mm) were collected on gelatin- eration detaches from the clear layer of the inner coated slides for light microscopic immunocyto- generation during molting, forming the so-called chemistry. For immunocytochemistry at the elec- shedding complex (Maderson,’85; Maderson et al., tron microscope level (immunogold), 50- to 90-nm- ’98). At the interface between the clear layer and thick sections were collected on nickel grids. For oberhautchen, the latter produces spines or micro- immunofluorescence, sections were incubated for ornamentation. The spines of the oberhautchen 3 min in 0.05 Tris buffered saline (TBS) at pH 7.6 may grow to be 60^100 mm in length, forming the HISTOLOGY OF REPTILIAN EPIDERMIS 29 setae of the climbing pads of geckos or anoline li- labeled, while the basal most layers were unlabeled zards (Maderson,’70; Alibardi,’97). (Fig. 1L). In Sphenodon several epidermal layers are pre- Finally, weak immunoreactivity was seen in sent but there is no de¢nitive shedding complex, the epidermis of tail scales from S. punctatus. This and the length of the shedding cycle is unknown immuno£uorescence was seen after microwave (Alibardi and Maderson, 2001). During epidermal oven retrieval (Shi et al., ’91) of immunoreactivity regeneration in lizards, following the injury an ex- (Fig.
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