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Rhombomere-Specific Patterns of Apoptosis in the Tree Shrew Tupaia Belangeri

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Rhombomere-Specific Patterns of Apoptosis in the Tree Shrew Tupaia Belangeri Cell Tissue Res (2004) 316:1–13 DOI 10.1007/s00441-004-0855-0 REGULAR ARTICLE Wolfgang Knabe · Stefan Washausen · Guido Brunnett · Hans-Jrg Kuhn Rhombomere-specific patterns of apoptosis in the tree shrew Tupaia belangeri Received: 22 October 2003 / Accepted: 14 January 2004 / Published online: 24 February 2004 Springer-Verlag 2004 Abstract Whether rhombomere-specific patterns of ap- apoptotic patterns composed of apoptotic maxima in the optosis exist in the developing hindbrain of vertebrates is dorsal and lateral thirds of r1, r2, and r3. These rhom- under debate. We have investigated the sequence of bomere-specific patterns of apoptosis may therefore apoptotic events in three-dimensionally reconstructed represent a conserved character, at least in amniotes. hindbrains of Tupaia belangeri (8- to 19-somite em- bryos). Apoptotic cells were identified by structural Keywords Hindbrain · Development · Cell death · Neural criteria and by applying an in situ tailing technique to crest cells · Tree shrew, Tupaia belangeri · Scandentia visualize DNA fragmentation. Seven rhombomeres orig- inated from three pro-rhombomeres. Among pre-migra- tory neural crest cells in the dorsal thirds of the neural Introduction folds, the earliest apoptotic concentrations appeared in the developing third rhombomere (r3). Dorsal apoptotic The transient appearance of rhombomeres, which repet- maxima then persisted in r3, extended from r3 to r2, itively bulge along the rostrocaudal axis of the developing and also arose in r5. Transverse apoptotic bands increased hindbrain, is a shared feature of teleosts and, at least, the total amount of apoptotic cells in odd-numbered amniote embryos (Kuratani 1997). Distinct rhombomeres rhombomeres first in r3 and, with a delay, also in r5. This (1) reveal segment-specific patterns of gene expression, sequence of apoptotic events was paralleled by an (2) give rise to neural crest cells that populate distinct approximate rostrocaudal sequence of neural crest cell sites of the embryonic head, and (3) are connected with delamination from the even-numbered rhombomeres. specific branchiomotor nerves and sensory ganglia Thus, large-scale apoptosis in r3 and r5 helped to (Lumsden and Keynes 1989; Lumsden 1990, 1999). establish crest-free zones that segregated streams of Inter-rhombomeric boundaries are defined by combina- migrating neural crest cells adjacent to r2, r4, and r6. torial expression patterns of Hox genes (Duboule and The sequence of apoptotic events observed in the dorsal Dolle 1989; Graham et al. 1989; Wilkinson et al. 1989; thirds of rhombomeres matches that reported for the chick Moens and Prince 2002). Cell mingling between adjacent embryo. Other shared features are apoptotic peaks in the rhombomeres, except for some crossing “violator” clones position of a circumscribed ventricular protrusion of (Birgbauer and Fraser 1994), is restricted by specialized fusing parts of the neural folds in r1 and r2, and Y-shaped boundary cells and by repulsive interactions between cells from odd- and even-numbered rhombomeres that express This work was supported by the Deutsche Forschungsgemeinschaft cell-surface molecules of the ephrin (Eph) family of (KN 525/1–1, KN 525/1–2, BR 1185/4–1, and former Sonder- receptor tyrosine kinases or their membrane-bound ephrin forschungsbereich 89: Cardiology) ligands, respectively (Lumsden and Keynes 1989; Fraser W. Knabe ()) · S. Washausen · H.-J. Kuhn et al. 1990; Heymann et al. 1993, 1995; Birgbauer and Department of Anatomy/Embryology, Fraser 1994; Lumsden 1999; Cooke and Moens 2002). Georg August University, Cell mixing is also prevented between subpopulations Kreuzbergring 36, 37075 Gttingen, Germany of rhombomere-derived neural crest cells. In chick and e-mail: [email protected] mouse embryos, neural crest cells that colonize the Tel.: +49-551-392354 Fax: +49-551-397043 branchial arches 1, 2, and 3 delaminate from rhom- bomeres r1/r2, r4, and r6, respectively (Graham et al. G. Brunnett 1993; Barrow et al. 2000). The resulting streams of neural Department of Informatics, crest cells migrate in the mesenchyme adjacent to the Technical University, even-numbered rhombomeres and are separated by crest- 09107 Chemnitz, Germany 2 free zones adjacent to r3 and r5. Whether apoptosis plays expanding our reconstructive approach to the entire brain, a decisive role in establishing these crest-free zones is we have studied whether, in Tupaia belangeri, rhombo- currently under debate. In favor of this view is the mere-specific patterns of apoptosis exist and whether observation of large-scale apoptosis of pre-migratory these apoptotic events are spatially and temporally neural crest cells in r3 and r5 of chick embryos (Lumsden correlated with the delamination of neural crest cells. et al. 1991; Jeffs et al. 1992; Graham et al. 1993, 1994). Between Hamburger Hamilton (HH) stages 9 (HH9) and HH13 (Hamburger and Hamilton 1951), an “anteropos- Materials and methods terior wave” of apoptosis (Ellies et al. 2000) starts in the dorsal midline of r3 (8-somite embryo). In the 11-somite Animals embryo, apoptosis extends to r2 and also arises in r5 Tree shrews are basal eutherian mammals, and their relationship to (Ellies et al. 2000). In contrast, Farlie et al. (1999) state primates is under debate (Wible and Zeller 1994). Embryos of that apoptosis in rhombomeres of chick embryos (1) Tupaia belangeri (Scandentia, average gestation period: 43.7 days; varies widely numerically and in pattern, (2) tends to be Kuhn and Schwaier 1973) were collected at the German Primate centered at the r2/3 boundary, and (3) is not well Center (DPZ), Gttingen, and at the Battelle-Institute, Frankfurt/ Main, for unrelated projects of the former DFG Sonderforschungs- correlated with neural crest cell emigration from the bereich 89 (Cardiology). In accordance with German law, pregnant even-numbered rhombomeres. Correspondingly, both the Tupaia belangeri were killed by intraperitoneal injection of an presence of distinct apoptotic maxima in r1, r3, and r5 overdose of pentobarbitone sodium (Nembutal), arterially perfused (Serbedzija et al. 1996) and the absence of rhombomere- with Macrodex and 0.15% procaine hydrochloride (Novocain), and specific apoptotic patterns have been reported for embry- fixed with 4% glutaraldehyde/3% paraformaldehyde in phosphate buffer (pH 7.3). Embryos were removed from the uterine cavity, onic mice (Trainor et al. 2002). According to Trainor et further fixed in the same fixative, embedded in Araldite (Serva, al. (2002) “the patterns of cell death in the hindbrain do Heidelberg, Germany), and completely serially sectioned at a not correlate with the generation or migration of neural thickness of 1 m. Consecutive sections were alternately placed on crest” in mice. Trainor et al. (2002) concluded that the two sets of slides. Sections belonging to the first set, further referred to as the “working series” (Knabe et al. 2002), were stained distinctly different patterns of apoptosis observed in the with Heidenhain’s hematoxylin (Romeis 1989). Sections of the rhombomeres of mouse and chick embryos signify a second set (“reference series”) remained unstained and, for reasons difference in the mechanisms that contribute to the detailed below, provided external fiducials for the realignment patterning of cranial neural crest cells in these species. procedure (Knabe et al. 2002). In previous work, 12- to 16-day-old embryos (E12 to E16) of Tupaia belangeri, used for three- The present study aims to clarify whether the reported dimensional reconstructions of apoptotic patterns, were classified species-specific patterns and functions of apoptosis in the according to five arbitrary phases of optic cup formation (Knabe early developing hindbrain of chick and mouse embryos and Kuhn 1998, 1999; Knabe et al. 2000, 2002). In the present might reflect a distinguishing character between mam- study, several younger paraffin-embedded embryos were included mals and birds. We have investigated the sequence of (Table 1). apoptotic events in the early developing hindbrain of Tupaia belangeri (Scandentia), a species widely used as a Three-dimensional reconstruction model for basal primates and eutherian mammals in general. Our methods for producing three-dimensional The PC used for image acquisition was equipped with two 350 MHz CPUs (Pentium II, Intel, Leixlip, Ireland), 56 GB hard reconstructions of cellular events in the forebrain (Knabe disk memory, 640 MB working memory, and an accelerated and Kuhn 1998; Knabe et al. 2000) have been improved graphics port device with 16 MB memory (Viper TNT, Diamond, (1) by establishing the high resolution scanning system Santa Clara, USA). Three-dimensional reconstruction was carried “Huge Image” (Sss et al. 2002), (2) by introducing a out on two PCs with two graphics tablets (Intuos A3, Wacom, Krefeld, Germany). The first PC was equipped with a 1.2 GHz CPU procedure to re-align serial sections with the help of (Athlon, AMD, Munich, Germany), 200 GB hard disk memory external fiducials (Knabe et al. 2002), and (3) by (5T040H4 and 6E040L0, Maxtor EMEA, Massy Cedex, France; installing rapid triangulation algorithms to reconstruct WD1200BB, Western Digital, Lake Forest, USA), 1.5 GB SD- large embryonic surfaces (Brunnett et al. 2003). By RAM, and an accelerated graphics port device with 64 MB memory (PowerColor Geforce2 Ti, Astra Datentechnik, Hurth, Germany). Table 1 Details of the embryos of Tupaia belangeri from day 11 to Araldite, B Bouin’s solution, E eosin, G glutaraldehyde, H day 13 of ontogenetic development used to investigate the patterns Heidenhain’s hematoxylin, P paraformaldehyde, Pa paraffin) of apoptosis in three-dimensionally reconstructed hindbrains (A Code number of embryo Ontogenetic age Number of somites Fixation, embedding, in the collection (days after conception) thickness of sections, staining 1044A 11 8 B, Pa, 7 mm, HE 1044C 11 8 B, Pa, 7 mm, HE 194A 12 11 B, Pa, 10 mm, HE 754/1A 13 13 G/P, A, 1 mm, H 754/5B 13 13 G/P, A, 1 mm, H 948/8A 13 19 G/P, A, 1 mm, H 948/1B 13 19 G/P, A, 1 mm, H 3 The second PC was equipped with a 3.0 GHz CPU (Pentium 4, et al.
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