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Early Development of the Cranial Nerves in a Primitive Vertebrate, the Sea Lamprey, Petromyzon Marinus L

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Early Development of the Cranial Nerves in a Primitive Vertebrate, the Sea Lamprey, Petromyzon Marinus L The Open Zoology Journal, 2008, 1, 37-43 37 Open Access Early Development of the Cranial Nerves in a Primitive Vertebrate, the Sea Lamprey, Petromyzon Marinus L. Antón Barreiro-Iglesias, María Pilar Gómez-López, Ramón Anadón and María Celina Rodicio* Department of Cell Biology and Ecology, Faculty of Biology, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain Abstract: The early development of the cranial nerves of the sea lamprey, Petromyzon marinus L., was studied in em- bryos and early prolarvae by immunocytochemical techniques with the marker for post-mitotic neurons acetylated - tubulin. The trigeminal and facial nerves were first observed in embryos 9 days post fertilisation. The glossopharyngeal and vagal nerves appeared later, which indicates a rostrocaudal gradient in differentiation of branchiomeric nerves. The anterior and posterior lateral line, octaval and hypoglossal nerves also appeared in early developmental stages, but the ocular motor nerves were not observed in prolarvae. The present results indicate that, in comparison with cranial nerves and ganglia organisation reported in larval and adult lampreys, organisational changes occur in the cranial nerves between the prolarval and larval stages. One important change is the disappearance of the pharyngeal branch of the facial nerve, which was not previously reported to be present in larval and adult lampreys, whereas it had been observed in earlier de- velopmental stages. Comparison of the present results with those from studies carried out in other vertebrate species, in- cluding the Japanese lamprey, suggests that the developmental pattern of the cranial nerves is conserved in agnathans and differs from that reported in other vertebrate groups. As maturation of lamprey eyes and extraocular muscles is completed at metamorphosis, there appears to be a correlation between the late development of eye-related cranial nerves in lampreys and the anatomical structures that they innervate. Keywords: Tubulin, agnathans, peripheral nervous system, cranial nerves, early development, whole-mount immunostaining. INTRODUCTION scientists study the lamprey nervous system using P. marinus as a model [12-20], but cranial nerve anatomical The cranial nerves in vertebrates are responsible for a data in the early developmental stages of this species are variety of behaviours, including olfaction, vision, taste, bal- lacking. In spite of the previous study on the Pacific lam- ance and eye movements. The cranial nerves of the brain- prey, a comparative analysis between the early development stem are composed of somatomotor, branchiomeric and oc- of cranial nerves in lampreys and in other vertebrates has not tavolateral nerves. Branchiomeric cranial nerves innervate yet been carried out. In the present study, we analysed the adjacent pharyngeal arches and show a segmental organisa- development of the cranial nerves in the sea lamprey, using tion, the somatomotor nerves are represented by the ocular antibodies against acetylated -tubulin, a neuronal marker motor nerves (oculomotor, trochlear and abducens), and the used in developmental studies in lamprey [8, 9, 21] and octavolateral nerves consist of the octaval and the anterior teleosts [1, 6]. The main objectives of the study were 1) to and posterior lateral line nerves. Lampreys are representa- compare the results for lamprey with those reported for other tives of the most primitive group of vertebrates, the agna- vertebrates, to determine the degree of conservation of de- thans, and their phylogenetic position makes them a key velopmental patterns in evolution and 2) to analyse the de- group for comparative studies. The development of the early gree of conservation of cranial nerve development between scaffold of axon tracts within the central nervous system has lampreys belonging to different genera. In addition, since the been previously studied in different vertebrate groups [1-8], organisation of the cranial nerves in the larval and adult sea but the early development of the cranial nerves is less stud- lamprey has previously been studied in detail [22-24], the ied. Development of the cranial nerves of the Pacific lam- present results also allowed comparison of the organisation prey, Lampetra japonica, has been investigated and dis- of the cranial nerves in embryonic/early prolarval sea lam- cussed in terms of their branchiomeric pattern [9], but it is prey stages and larvae. not known whether their development is the same in other species of lamprey in the Atlantic Ocean. Even though the MATERIALS AND METHODOLOGY two genera, Petromyzon and Lampetra, show many morpho- Animals logical and physiological similarities, a few differences re- main [10, 11]. In addition, in south Europe and North Amer- Embryos and prolarvae were obtained from in vitro fertil- ica, P. marinus is more easily accessible and some groups of ised eggs, which were taken from sexually mature adult sea lampreys caught in the River Ulla (north-western Spain). Fertilised eggs were reared in the laboratory under appropri- *Address correspondence to this author at the Department of Cell Biology ate conditions of darkness and temperature [25]. The stages and Ecology, Faculty of Biology, University of Santiago de Compostela, of embryos (E) and prolarvae (P) are indicated by days from 15782 Santiago de Compostela, Spain; Tel: 0034 981 56 31 00, Ext: 16946; Fax: 981 596904; E-mail: [email protected] fertilisation and hatching, respectively. Late embryos (E8- 1874-3366/08 2008 Bentham Open 38 The Open Zoology Journal, 2008, Volume 1 Barreiro-Iglesias et al. E12, n=15) and prolarvae (P0-P7; n=19) of sea lamprey (P. procedures specifically reveal early axons, no further con- marinus L.) were used. For group prolarvae, we adopted trols were included. Piavis’ stages of sea lamprey development [26]: hatchling (P0-P1), pigmentation (P2-P3), gill-cleft (P4-P7) and bur- RESULTS rowing (P8-P23). The experiments complied with European The organisation of the cranial nerves in a sea lamprey Union regulations on animal care and experimentation. P5 prolarvae is shown in Fig. (1). The sequential develop- ment of these nerves is presented in the series of photos in Tubulin Immunohistochemistry Fig. (2). The nomenclature for cranial nerves used here fol- Embryos and prolarvae were fixed in 4% paraformalde- lows that of [9]. hyde in 0.1 M phosphate buffer (pH 7.4) for 5h, washed in Tris-HCl (0.05 M, pH 7.4), dehydrated in methanol and stored at -20ºC in methanol. For whole-mount immunostain- ing, samples were incubated with proteinase K (Sigma, St. Louis, MO; 30g/ml in Tris-HCl) for 1-3 h at room tempera- ture and with acetone at -20ºC for 7 min. The samples were then pretreated with 5% H O in Tris-HCl to block endoge- 2 2 nous peroxidases before incubation in the monoclonal anti- acetylated -tubulin antibody (Sigma; dilution 1:500). Anti- body dilutions were made in Tris-HCl containing 2.92% NaCl, 0.5% Triton X-100 and 1% dimethyl sulfoxide under agitation for 5 to 6 days. After the incubation with the anti- tubulin antibody, the samples were incubated first with goat anti-mouse immunoglobulin G (Dako, Golstrup, Denmark; dilution 1:50) overnight, and then with mouse peroxidase- antiperoxidase complex (Sigma) for 24h. The immunoreac- tion was developed with 0.6 mg/ml 3-3´-diaminobenzidine (Sigma) and 0.003% H2O2 for 40-70 min. Samples were rinsed and cleared in a mixture of glycerol and water (1:1). Embryos and prolarvae were mounted on concavity well glass slides for observation with an Olympus BX51 micro- scope. Photomicrographs were taken with Olympus DP12 and Olympus DP70 digital cameras. Photomicrographs were adjusted for brightness and contrast with Corel Draw 12 software. Tubulin Immunofluorescence For immunofluorescence, samples were prepared as above, except that the primary antibody was diluted in a ratio of 1:250. The secondary antibody was FITC-coupled goat Fig. (1). Organisation of the sea lamprey cranial nerves in a P5 anti-mouse (Chemicon, Temecula, CA; diluted 1:50), for a 1 prolarva. A: Schematic drawing showing the organisation of the h exposure. The antibody dilutions were carried out in TBS cranial nerves in a P5 prolarva. The dotted line indicates the brain. containing 15% normal goat serum and 0.2% Triton X-100. Bb: Buccal branch, BCb: Buccinator branch, EO: Ectopic olfactory Photomicrographs were taken with a spectral confocal laser cells, EP: Eye primordium, ETX: Epibranchial tract of the vagal microscope (Leica TCS-SP2). The photomicrographs were nerve, gV1-gPLLN: Ganglia of the different nerves, Hb: Hyoman- converted to gray scale, inverted and adjusted for brightness dibular branch, Ib: Intestinal branch, ION: Infraoptic nerve, IXDb: and contrast using the Adobe Photoshop software. Dorsal branch of the IX nerve, Mb: Maxillary branch, mMb: Me- dial maxillary branch, N: Neuromast, OV: Otic vesicle, P: Pineal, Histology PbIX: Principal branch of the IX nerve, PHb: Pharyngeal branch, After tubulin immunostaining, some samples were cryo- PLLN: Posterior lateral line nerve, Rb/RN: Recurrent branch/nerve, protected in 30% sucrose containing 0.01 % of sodium azide, SbX: Sensory branch of the vagal nerve, SP: Spinal plexus, Tb: embedded in Tissue Tek (Sakura), frozen, cut on a cryostat Thyroid branch, V1: Deep ophthalmic nerve, Vb: Velar branch, X1- (40 μm thick), mounted on gelatin-subbed slides and ob- X6: Epibranchial branches, XII: Hypoglossal nerve. Black arrows served and photographed as above. For the immunofluores- indicate the ventral spinal roots. Curved arrows indicate the dorsal cence experiments, the sections were coverslipped with Vec- spinal roots. B: Lateral view of a P5 prolarva showing the organis- tashield (Vector Laboratories, Burlingame, CA). sation of the cranial nerves at this developmental stage. Abbrevia- tions as in A. Scale bar: 100 mm. Rostral is at the left in all the Controls figures. The primary anti-tubulin antibody [27] has previously been shown to label early differentiated neurons and their Olfactory ectopic cells are present in E9 embryos just processes in the embryonic nervous system [1, 6, 8].
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