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Histological and Lectin Histochemical Studies on the Main and Accessory Olfactory Bulbs in the Japanese Striped Snake, Elaphe Quadrivirgata

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Histological and Lectin Histochemical Studies on the Main and Accessory Olfactory Bulbs in the Japanese Striped Snake, Elaphe Quadrivirgata FULL PAPER Anatomy Histological and Lectin Histochemical Studies on the Main and Accessory Olfactory Bulbs in the Japanese Striped Snake, Elaphe quadrivirgata Daisuke KONDOH1,2), Akimi WADA1), Daisuke ENDO1,2), Nobuaki NAKAMUTA1,2) and Kazuyuki TANIGUCHI1,2)* 1)Laboratory of Veterinary Anatomy, Faculty of Agriculture, Iwate University, Morioka, Iwate 020–8550, Japan 2)Department of Basic Veterinary Science, The United Graduate School of Veterinary Science, Gifu University, Gifu, Gifu 501–1193, Japan (Received 1 November 2012/Accepted 7 December 2012/Published online in J-STAGE 21 December 2012) ABSTRACT. The main and accessory olfactory bulbs were examined by histological methods and lectin histochemistry in the Japanese striped snake. As the results, the histological properties are similar between the main olfactory bulb and the accessory olfactory bulb. In lectin histochemistry, 21 lectins used in this study showed similar binding patterns in the main olfactory bulb and the accessory olfactory bulb. In detail, 15 lectins stained these olfactory bulbs with similar manner, and 6 lectins did not stain them at all. Two lectins, Lycopersicon esculentum lectin (LEL) and Solanum tuberosum lectin (STL), stained the nerve and glomerular layers and did not stain any other layers in both olfactory bulbs. Four lectins, Soybean agglutinin (SBA), Vicia villosa agglutinin (VVA), Peanut agglutinin (PNA) and Phaseolus vulgaris agglutinin-L (PHA-L) stained the nerve and glomerular layers more intensely than other layers in both olfactory bulbs. In addition, VVA showed the dot-like stainings in the glomeruli of both olfactory bulbs. These findings suggest that the degree of development and the properties of glycoconjugates are similar between the main olfactory bulb and the accessory olfactory bulb in the Japanese striped snake. KEY WORDS: histology, nervous system, reptiles, Squamates, vomeronasal system. doi: 10.1292/jvms.12-0484; J. Vet. Med. Sci. 75(5): 567–574, 2013 The olfactory system receives and detects chemical sub- environmental substances by the tongue-flicking and deliver stances in the external environment. This system is divided concentrated chemicals to the vomeronasal epithelium, and into 2 independent systems: the main olfactory system and the information acquired with the tongue-flicking is medi- the vomeronasal system. In the main olfactory system, the ated by both the main olfactory system and the vomeronasal receptor cells in the olfactory epithelium project their axons system [13, 36]. Topographically, the size of the accessory to the glomeruli in the main olfactory bulb to form synapse olfactory bulb is as large as that of the main olfactory bulb in with output neurons and intermediate neurons. On the other snakes [15, 16], although the size of the accessory olfactory hand, in the vomeronasal system, the receptor cells in the bulb is much smaller than that of the main olfactory bulb in vomeronasal epithelium project their axons to the glomeruli many other vertebrate species. Histologically, both the main in the accessory olfactory bulb [14]. Although the main ol- and accessory olfactory bulbs in snakes are divided into 6 factory system exists in all vertebrate species, the vomero- layers (the nerve, glomerular, mitral cell, internal plexiform, nasal system first appears in amphibians, is lost in several granule cell and ependymal cell layers), and the histological species such as crocodiles, birds, whales and humans, and properties of the constituent cells are similar between these has various morphological and histological features among olfactory bulbs [15, 16]. However, there are few detailed animal species [4]. The localization, size and laminar struc- reports on the sublamination and cell distribution in these ture of the main and accessory olfactory bulbs vary among layers of the main and accessory olfactory bulbs in snakes. species [25, 29] and appear to relate with behavioral patterns Lectins are proteins binding nonimmunologically with and living environment of each species. glycoconjugates [3] and are extensively used for the differ- Among all tetrapods, snakes and some lizards have the entiation of cell types on histological sections based on the most developed vomeronasal system [13], i.e. the vomerona- staining regions and the staining intensities [23]. In lizards sal system of snakes and lizards mediates not only species- with well-developed vomeronasal system, the lectin binding specific communications by pheromones, such as courtship patterns are similar between the main olfactory bulb and and aggregative behaviors [10, 21], but also non-species- the accessory olfactory bulb [6], although the lectin binding specific behaviors by odoriferous molecules, such as preda- patterns are different between these olfactory bulbs in many tory and defensive behaviors [22, 27, 36]. Snakes sample other species, such as amphibians [32–34] and mammals [26, 28, 31]. According to these reports on the lizards and many other species, the glycoconjugate moieties appear to *CORRESPONDENCE TO: TANIGUCHI, K., Laboratory of Veterinary be similar between the main olfactory bulb and the acces- Anatomy, Department of Veterinary Science, Faculty of Ag- sory bulb in the species with well-developed vomeronasal riculture, Iwate University, 3–18–8 Ueda, Morioka-shi, Iwate system, such as some lizards. Although snakes are equipped 020–8550, Japan. with the most developed vomeronasal system [13, 14] and e-mail: [email protected] belong to Squamata as well as lizards, there is no report on ©2013 The Japanese Society of Veterinary Science the lectin histochemistry on the main olfactory bulb and ac- 568 D. KONDOH ET AL. cessory olfactory bulb in snakes. Squamata and mammals correlation [9], all snakes were sexually mature. This study have evolved separately from primitive reptiles, and it is was approved and conducted according to the Guideline possible that the histochemical features of olfactory system for Animal Experiment of Iwate University. All procedures are different between these two groups. In this study, we ex- were approved by the local animal ethical committee of amined the main olfactory bulb and the accessory olfactory Iwate University. bulb of the Japanese striped snake, Elaphe quadrivirgata, Histology: The animals were anesthetized by intraperito- by histological methods and 21 lectins extensively-used for neal injection of pentobarbital (0.13–0.20 mg/g body weight) screening the differentiation of the glycoconjugate moieties and were sacrificed by cardiac perfusion with Ringer’s between the main olfactory system and the vomeronasal sys- solution followed by Zamboni’s fixative. After decapitation, tem in many species to detect possible similarities between brains were removed from heads, fixed in the same fixative these olfactory bulbs in snakes. for 3–4 hr, routinely embedded in paraffin and cut frontally or horizontally at 5 µm thickness. Some of these sections MATERIALS AND METHODS were stained with luxol fast blue/cresyl violet (staining of Klüver-Barrera), and other sections were processed for lec- Animals: Six snakes in the reproductive season (June) tin histochemistry. were studied (Table 1). They were kept in near-natural Lectin histochemistry: Several sections were processed conditions in the Japan Snake Institute (Ota, Japan) and for histochemistry with ABC method using 21 biotinylated purchased. Based on an age estimated by the body length lectins (Table 2) in the lectin screening kit I-III (Vector Lab- oratories, Burlingame, CA, U. S. A.). After deparaffinization and rehydration, sections were incubated with 0.3% H2O2 Table 1. Details of animals used in the present study in methanol to eliminate endogenous peroxidase. Sections were rinsed in phosphate-buffered saline (PBS, 0.01 M, pH Date TL (cm) W(g) Sex 7.4) and incubated with 1% bovine serum albumin to block No. 22 Jun-09 116 202.1 Male nonspecific reactions. After rinsing, sections were incubated No. 23 Jun-09 119 225.7 Female with biotinylated lectins at 4°C overnight, reacted with ABC No. 24 Jun-09 114 202.9 Male reagent (Vector) at room temperature for 30 min and col- No. 25 Jun-09 124 458.7 Male orized with 0.05 M Tris-HCl (pH 7.4) containing 0.006% No. 36 Jun-10 130 341.1 Male H2O2 and 0.02% 3–3′-diaminobenzidine tetrahydrochloride. No. 37 Jun-10 89 226.8 Female Staining intensities were judged as 5 grades: intense, mod- TL, Total length; W, Weight erate, weak, faint and negative staining. Control stainings Table 2. Concentrations and binding specificities of lectins used in the present study Concentration Lectins Abbreviation Binding specificity (mg ml-1) Wheat germ agglutinin WGA 1.0×10-2 GlcNAc, NeuAc -2 Succinylated-wheat germ agglutinin s-WGA 1.0×10 (GlcNAc)n -3 Lycopersicon esculentum lectin LEL 2.0×10 (GlcNAc)2-4 -2 Solanum tuberosum lectin STL 1.0×10 (GlcNAc)2-4 -3 Datura stramonium lectin DSL 4.0×10 (GlcNAc)2-4 Bandeiraea simplicifolia lectin-II BSL-II 5.0×10-2 GlcNAc Dolichos biflorus agglutinin DBA 5.0×10-2 Gal, GalNAc Soybean agglutinin SBA 1.0×10-2 Gal, GalNAc Bandeiraea simplicifolia lectin-I BSL-I 5.0×10-3 Gal, GalNAc Vicia villosa agglutinin VVA 1.0×10-2 Gal, GalNAc Sophora japonica agglutinin SJA 5.0×10-2 Gal, GalNAc Ricinus communis agglutinin-I RCA-120 2.0×10-3 Gal, GalNAc Jacalin 5.0×10-4 Gal, GalNAc Peanut agglutinin PNA 4.0×10-3 Gal Erythrina cristagalli lectin ECL 2.0×10-2 Gal, GalNAc Ulex europaeus agglutinin-I UEA-I 5.0×10-2 Fuc Concanavalin A ConA 3.3×10-3 Man, Glc Pisum sativum agglutinin PSA 4.0×10-3 Man, Glc Lens culinaris agglutinin LCA 4.0×10-3 Man, Glc Phaseolus vulgaris agglutinin-E PHA-E 5.0×10-3 Oligosaccharide Phaseolus vulgaris agglutinin-L PHA-L 2.5×10-3 Oligosaccharide Fuc: Fucose; Gal: Galactose; GalNAc: N-acetylgalactosamine; Glc: Glucose; GlcNAc: N-acetylglucosamine; Man: Mannose; NeuAc: N-acetylneuraminic acid. LECTIN BINDING IN SNAKE OLFACTORY BULB 569 were performed (a) by the preabsorption of lectins with each specific sugar residue (Table 2) or (b) by the use of PBS to replace ABC reagent.
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