Morphological Transformation of Sensory Ganglion Neurons and Satellite Cells
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Biomedical Reviews 2000; 11: 39-52. 39 MORPHOLOGICAL TRANSFORMATION OF SENSORY GANGLION NEURONS AND SATELLITE CELLS Seiji Matsuda1, Naoto Kobayashi1, Hiroyuki Wakisaka1, Shouichiro Saito1, Kyouko Saito1, Kyojy Miyawaki1, Katsumi Mominoki2, Kazuhiro Shigemoto3, Shingo Murakami4, and Takashi Fujiwara2 1Department of Anatomy, 2Laboratory Animal Center, 3Department of Hygiene, Ehime University School of Medicine, Shigenobu, Ehime, Japan, 4Department of Otolaryngology, Nagoya City University Medical School, Mizuho, Nagoya, Japan The development of sensory ganglion neurons and satellite cells examined by scanning electron microscopy after removal of the connective tissue is reviewed. Sensory neurons are bipolar at early stages of development and later became pseudounipolar. This maturation event starts earlier but proceeds more slowly in chick than in rat embryos. These may due to the difference in the extent and intimacy of satellite cell investments between these two animal species. The neuronal perikaryal projections are observed by scanning electron microscopy after removal of the connective tissue and satellite cells. The morphometric analysis reveals that perikaryal projections are more numerous on the surface of mature pseudounipolar neurons than on that of premature bipolar neurons; they increase in number as the neuronal cell bodies grow larger. This may support the hypothesis that perikaryal projections are structural devices for increasing the neuron-satellite interface and for improving the efficiency of metabolic exchange between these two cell types.The important role of satellite cells in neuronal maturation is discussed. Biomed Rev 2000; 11: 39-52. INTRODUCTION ganglion neurons, which were first thought to be a technical artifact or an instrument for the attachment between neurons Sensory ganglion neurons undergo a unique transformation and satellite cells, considerably enlarge the perikaryal surface from spindle-shaped bipolar to pseudounipolar cells during (6). By expanding the area available for exchange of development (1-5). Satellite cells are present from the begin- metabolites they may be important in neuronal metabolism in ning of this pseudounipolarization, but intricate networks of adult animals (6-8). We also supported the above hypothesis branching satellite cell processes only develop after about day by showing the neuronal shape- and size-dependent increase 17 in rat embryos (4). The important role of satellite cells in in perikaryal projections during development (5). the pseudounipolarization was reported in vitro (2) and in In this review we show the morphological change of sen- vivo (4). Perikaryal projections on the surface of sensory sory ganglion neurons, perikaryal projections and satellite cells Received 5 January 2000 and accepted 28 May 2000. Correspondence and reprint requests to Dr Seiji Matsuda, Department of Anatomy, Ehime University School of Medicine, Shigenobu, Ehime 791-02, Japan. Tel.: 81 89 960 5230, Fax: 81 89 960 5233, E-mail: [email protected] Biomed Rev 11, 2000 40 Matsuda, Kobayashi, Wakisaka, Saito, Saito, Miyawaki, et al to evaluate the functional significance of neuron-satellite cell COMPARISON OF PSEUDOUNIPOLARIZATION IN RAT interactions. AND CHICK PSEUDOUNIPOLARIZATION OF SENSORY NEURONS The development of each DRG is much different at early stages. Especially, as shown in Figure 2, the appearance differs Pseudounipolarization has been examined in histological considerably between the cervical and the thoracic ganglia. sections using classical silver impregnation methods (1,9-11), For this reason, we always used DRG of Th.2-7. by transmission electron microscopy (12,13), and more The examination of dissociated ganglion neurons gathered recently using immunohistochemistry for cytoskeletal markers on the Millipore filter facilitates the observation of the mor- (14,15). However, the precise time course of pseudounipo- phological characteristics of neurons with SEM. The propor- larization cannot be accurately determined, because the tions of different types of chick and rat neurons observed at neurons are visualized in only two dimensions and only a few different developmental stages are presented in Table 1, 2. can be seen in their entirety with the above methods. Further- Percentages of unipolar neurons at successive stage of devel- more, there is little detailed information about the development opment in chick and rat DRG are shown in Figure 3. From of dorsal root ganglion (DRG) neurons in birds, although these this figure, the formula to compare the early development of have been widely used as the source material for tissue culture chick and that of rat is estimated as follows: (chick embryo- studies (14). nal days)/2 + 10 days = rat embryonal days. Although it is not Scanning electron microscopy (SEM) has overcome some sure that this formula is applied widely, it is useful to at least compare the development of the spinal cord or the DRG in of these limitations of observing neurons. Using this tech- these two animal species. nique, the three-dimensional appearance of the neuronal cell Several marked differences are noted between the dissoci- bodies and processes in embryonic rat and chick DRG was ated chick and rat ganglion neurons during development. First, described (3-5,16,17). pseudounipolarization begins to take place during E8 to E10 In the early stages, most DRG neurons are spindle-shaped in the chick and around E14 in the rat (Fig. 3). Second, the bipolar; a few have an eccentrically bulging cytoplasm. The percentage of pseudounipolar neurons increase abruptly in angle formed by the extensions of the central and peripheral the prenatal rat after day E16, whereas in the chick, it in- processes of these neurons is greater than 90 degrees and the creases relatively gradually after day E10 (Fig. 3). Third, the central process is thinner than the peripheral one (Fig. 1a,b). percentage of bell-shaped bipolar neurons is higher in the rat The two processes approach each other as the cell body bulge during E14 to E17 than that in the chick throughout the em- more in a direction opposite to the initial segments of the bryonic periods (Tables 1, 2). Last, very few immature neu- processes. The extensions of these processes form an angle rons (3%) are found in the rat ganglia, one day after birth, less than 90 degrees, and thus the processes and cell body whereas in 2-day-old chicks many immature neurons (13% exhibit a bell-shaped conformation (Fig. 1c-f). At the same not unipolar) are still present (Fig.4). It is likely that in the developmental stages, there are some more advanced gan- chick, the estimated 13% immature neurons at post hatching glion neurons whose cell bodies elongate between the initial day 2 continue developing into mature forms, because such segments of two processes to form a primitive stem process bipolar neurons comprise only about 2% of the total in adult (Fig. 1f-h). Initially, the stem process is larger in diameter chick sensory ganglia (22,23). than the sum of the central and peripheral processes, shorter in length than the diameter of the cell body (Fig.1g) and gradu- ROLE OF SATELLITE CELLS IN PSEUDOUNIPOLARIZATION ally becomes thinner as it elongates (Fig. 1h). On the postna- tal days, the stem process is so long that the bifurcation of the The findings described above suggest that DRG neurons central and peripheral processes is hardly visible in SEM. remain in a more immature condition for longer during prenatal development in chicks than in rats. A possible explanation No sign of close apposition of the central process to the for this difference may be that the extent and intimacy of peripheral one is noted in any of the neurons examined and satellite cell investment is more developed in the rat than in the primitive stem processes are always thicker than the sum the chick (24,25). In line with this speculation, cultured chick of the diameters of the two individual processes. From these spinal ganglion neurons maintain bipolar form for periods of findings, one may exclude the possibility that both processes up to 1 month if grow in the absence of satellite cells or contact and fuse with each other to yield a common stem pro- Schwann cells (Fig. 5). However, when purified Schwann cells cess. A further elongation of the primitive stem process with- were added, the morphology of the neurons changed from the out fusion of the central and peripheral processes appears to bipolar to the pseudounipolar form (2). Moreover, the time result in the formation of a long-stem pseudounipolar neuron required for this change to occur is related to the number of (3,18-21). Schwann cells added; the more Schwann cells are added, the Biomed Rev 11, 2000 Development of sensory neurons and satellite cells 41 Figure. 1. Scanning electron micro- graphs of sensory neuron types at successive stages of development in the rat dorsal root ganglion. Spindle- shaped bipolar neuron on emb- ryonic day 14 (a), on day 16 (b). Bell- shaped intermediate neuroblasts on day 14 (c), on day 16 (d,f), on day 17 (e). Short-stem unipolar neuron on embryonic day 18 (g), on day 16 (h). Note that the connecting piece (arrow) elongates and a primitive stem process is formed (arrowhead). Bars, 5 µm. From Ref 3, with permission of Springer Verlag. Biomed Rev 11, 2000 42 Matsuda, Kobayashi, Wakisaka, Saito, Saito, Miyawaki, et al Figure 2. An embryonic rat spinal cord and dorsal root ganglia (DRG) stained with methylene blue. Note that the cervical DRG are much bigger than the thoracic DRG . Table 1. Percentage of different neuron types at successive Table 2. Percentage of different neuron types at succesive stages in chick dorsal root ganglion. stages in rat dorsal root ganglion. 6 8 10 14 18 P2 14 15 16 17 18 19 P1 Multipolar 35 1 Multipolar 21 Spindle shaped bipolar 31 12 5 2 1 1 Spindle shaped bipolar 434 1 Eccentric bipolar 66 69 73 27 10 6 Eccentric bipolar 56 30 18 13 2 1 1 Bell-shaped bipolar 14 12 13 11 6 Bell-shaped bipolar 31 46 47 24 8 5 2 Short stem unipolar 5465 Short stem unipolar 469 87125 Long stem unipolar 5537282 Long stem unipolar 3152155828292 Unipolar 0 0 10 57 78 87 Unipolar 7213063899497 Figure 3.