Development of the myelin sheath of the hypogastric nerves in a human foetus aged 23 weeks
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1 O R I G I N A L A R T I C L E Folia Morphol. Vol. 63, No. 3, pp Copyright 2004 Via Medica ISSN Development of the myelin sheath of the hypogastric nerves in a human foetus aged 23 weeks Małgorzata Bruska, Adam Piotrowski Department of Anatomy, University School of Medical Sciences, Poznań, Poland [Received 30 April 2004; Accepted 28 June 2004] The formation of the myelin sheath of the human hypogastric nerves was studied by electron microscopy in a foetus of 23 weeks of postovulatory age (220 mm C-R length). In the investigated foetus the hypogastric nerves were mainly composed of bundles of unmyelinated fibres. The myelinated fibres were seen to be at different stages of myelination. Well myelinated fibres had thick compact laminated myelin. The number of myelin lamellae on a single fibre was 22. Key words: human neuroembryology, hypogastric nerves, myelination, ultrastructure INTRODUCTION The hypogastric nerves arise from the lower part of the intermesenteric plexus, and terminate in the pelvic plexuses located laterally to the rectum. They contain sympathetic and parasympathetic nerve fibres. Fibres arising from these nerves reach the urinary bladder, uterus, ureter, prostate, uterine tube and blood vessels. Connections between the hypogastric nerves and pelvic nerves have also been observed [15]. Myelin is produced by lemmocytes which move the axons around to form compact lamellae [11]. An important role in the early phases of myelin wrapping is played by myelin basic protein (MBP) [4, 11] and the protein for peripheral myelination is peripheral myelin protein 22 kda (PMP 22/gas 3) [16]. Myelination in certain cranial nerves [1, 2, 10, 12 14, 17, 20] and peripheral nerves [5 8] was described in an earlier study. The aim of the present study is to trace the myelin formation of the hypogastric nerves in a human foetus aged 23 weeks. MATERIAL AND METHODS A human foetus of 220 mm C-R length, aged 23 weeks was used for the study. The hypogastric nerves were removed immediately after operation and immersed in chilled 1.2% glutaraldehyde for 1 h. The material was then placed for 2 h in 2% glutaraldehyde buffered to ph 7.4 with cacodylate. After being washed in cacodylate buffer for 24 h, parts of the hypogastric nerves were fixed in 1% osmium tetroxide. Thin and semithin sections were made on Reichert ultramicrotome. The semithin sections were contrasted with uranyl acetate and lead citrate. The thin sections were examined in JEM 7A and Philips electron microscopes. RESULTS In the human foetus of 220 mm C-R length the hypogastric nerves were composed mainly of bundles of unmyelinated fibres surrounded by lemmocyte processes (Fig. 1). The bundles of axons were separated by endoneural spaces containing collagenous fibres, fibro- Address for correspondence: Prof. Małgorzata Bruska, Department of Anatomy, University School of Medical Sciences, ul. Święcickiego 6, Poznań, Poland, tel: ext. 564, fax: , mbruska@usoms.poznan.pl 289
2 Folia Morphol., 2004, Vol. 63, No. 3 Figure 1. The left hypogastric nerve in a human foetus at 23 weeks; Ax axon, Bv blood vessels, Col collageous fibres, My myelin sheath micrometres (Fig. 4). The organelles in the axons consisted primarily of neurofilaments, microtubules and mitochondria (Fig. 4). blasts and blood vessels (Fig. 1 3). Dark lemmocytes were observed between the nerve processes (Fig. 5). The diameter of the axons varied from 0.2 to
3 Małgorzata Bruska et al., Human foetal hypogastric nerves Figure 2. Lemmocytes (L) and their processes surround differing numbers of axons (Ax) of the left hypogastric nerve in a human foetus at 23 weeks; Col collagenous fibres and 20 axons (Fig. 1 5). The lemmocytes were rich in organelles. The thin cytoplasm contained particularly free ribosomes and mitochondria (Fig. 5). Lemmocyte processes invaded the bundles and divided them into smaller complexes (Fig. 2, 3). These lemmocyte-axon complexes contained between 291
4 Folia Morphol., 2004, Vol. 63, No. 3 Figure 3. Bundle of nerve fibres of a hypogastric nerve in a foetus at 23 weeks; Ax axon, Col collagenous fibres, L lemmocyte, Lp lemmocyte process, Per perineurium In the investigated foetus the myelinating axons at the very beginning of myelination had one or one and a half turns of lemmocyte processes (Fig. 5). In some areas of the hypogastric nerves there were single myelinated fibres at different phases of myelination (Fig. 1, 5). 292
5 Małgorzata Bruska et al., Human foetal hypogastric nerves Figure 4. The right hypogastric nerve in a human foetus at 23 weeks; Ax axon, Lp lemmocyte process These first turns were irregular and showed major variations in their contours. Within the bundles of axons of the hypogastric nerves axonal growth cones were present (Fig. 6). These were large profiles containing growth cones vesicles, neurofilaments and smooth endoplasmic reticulum. The well myelinated fibres had a compact myelin 293
6 Folia Morphol., 2004, Vol. 63, No. 3 Figure 5. Myelinogenesis of the left hypogastric nerve in a foetus at 23 weeks; Ax axon. My myelin sheath sheath. The number of myelin lamellae on a single fibre could be as many as 22 (Fig. 7, 8). Small ganglia and single ganglionic cells were observed in the hypogastric nerves (Fig. 9, 10). These cells had oval or irregular nuclei with dispersed chromatin and nucleoli. The ganglionic cells were separated by lemmocytes and nerve fibres, and were surrounded by the processes of satellite cells (Fig. 11). 294
7 Małgorzata Bruska et al., Human foetal hypogastric nerves Figure 6. Axonal growth cones (Axg) in a hypogastric nerve in a foetus at 23 weeks DISCUSSION The present investigations showed that the hypogastric nerves in human foetuses are made up predominantly of unmyelinated fibres. During the development of the cranial and spinal nerves a large number of myelinated fibres are observed at this stage. This was shown in earlier studies on the myelination of the hypoglossal [2], phrenic [21], and trigeminal nerves [1] and in the vagus nerve [20]. The sympathetic trunk [3] is made up predominantly of unmyelinated fibres, as is the greater splanchnic nerve [19]. The myelinated fibres are at different stages of myelination. The studies performed reveal that in the 23 rd week of the foetal period the myelination of the hypogastric nerves is well in progress. At this period of development the compact myelin sheath is being formed. This is in accordance with the results of other authors [8, 12, 13]. In the present study the formation of the myelin sheath observed resembled that in other human nerves [7 10, 17, 18]. 295
8 Folia Morphol., 2004, Vol. 63, No. 3 Figure 7. Well myelinated fibres in a hypogastric nerve in a foetus at 23 weeks; Ax axon, My myelin sheath
9 Małgorzata Bruska et al., Human foetal hypogastric nerves Figure 8. Well myelinated fibres in a hypogastric nerve in a foetus at 23 weeks; My myelin sheath
10 Folia Morphol., 2004, Vol. 63, No. 3 Figure 9. Ganglion cells in hypogastric nerves in a foetus at 23 weeks; Gc ganglion cell
11 Małgorzata Bruska et al., Human foetal hypogastric nerves Figure 10. Ganglion cell (Gc) in the right hypogastric nerve in a foetus at 23 weeks
12 Folia Morphol., 2004, Vol. 63, No. 3 Figure 11. Ganglion cell in the left hypogastric nerve in a foetus at 23 weeks; Gc ganglion cell, Col collagenous fibres, Per perineurium
13 Małgorzata Bruska et al., Human foetal hypogastric nerves REFERENCES 1. Bruska M (2003) An ultrastructural study of the myelination of the trigeminal ganglion in human fetuses aged 10 to 23 weeks. Folia Morphol, 62: Bruska M, Woźniak W (1984) Myelination of the hypogossal nerve in human fetuses of 137 and 220 mm crown rump length. Folia Morphol, 43: Bruska M, Woźniak W (1997) Progress in myelin formation of the thoracic sympathetic aged 17 weeks. Folia Morphol, 56: Carson JH, Nielson MW, Barbarese E (1983) Development regulation of myelin basic protein expression in the brain. Der Biol, 96: Cravioto H (1965) The role of Schwann cells in the development of human peripheral nerves. J Ultrastr Res, 12: Davison AN, Duckett S, Oxberry M (1973) Correlative morphological and biochemical studies of the human fetal sciatic nerve. Brain Res, 58: Dunn JS (1970) Developing myelin in human peripheral nerves. Scott Med J, 15: Gamble HJ (1966) Further electron microscope study of human foetal peripheral nerves. J Anat, 100: Gamble HJ, Breathnach AS (1965) An electron microscope study of human peripheral nerves. J Anat, 99: Gamble HJ, Fenton J, Allsopp G (1978) Electron microscope observations on the changing relationships between unmyelimated axons and Schwann cells in human fetal nerves. J Anat, 127: Mikoshiba K, Okano H, Tanura T, Ikenaka K (1991) Structure and function of myelin protein genes. Annu Rev Neurosc, 14: Mustafa G, Gamble HJ (1978) Observations on the development of the connective tissues of the developing human nerve. J Anat, 127: Mustafa GY, Gamble HJ (1979) Changes in axonal numbers in developing human trochlear nerve. J Anat, 128: Schröder JM, Bohl J, von Bardeleben U (1988) Changes of the ratio between myelin thickness and axon diameter in human developing sural, femoral, ulnar, facial and trochlear nerves. Acta Neruopathol, 76: Słabikowski A, Woźniak W, Bruska M (1996) Origin and topography of the pelvic nerves in human embryos and fetuses. Folia Morphol, 55: Spreyer P, Kuhn G, Hanemann CO, Gillen C, Schaal H, Kuhn R, Lemke G, Müller HW (1991) Axon regulated expression of a Schwann cell transcript that is homologous to a growth arrest specific gene. EMBO J, 10: Woźniak W (1982) Compact myelin formation in the human nerves during intra-uterine development. Folia Morphol, 41: Woźniak W (1983) Axon diameter and myelin formation in the developing human nerves. Folia Morphol, 42; Woźniak W, Bruska M (1986) Fine structure and myelination of the greater splanchnic nerves in human fetus. Folia Morphol, 45: Woźniak W, O Rahilly R (1981) Fine structure and myelination vagus nerve. Acta Anat, 109: Woźniak W. O Rahilly R, Bruska M (1982) Myelination of the human fetal phrenic nerve. Acta Anat, 112:
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