Similar results have been described for the mouse embryo [5]. Pathoembryogenesis of terminal myelocystocele: terminal balloon in secondary neurulation of the chick embryo. It therefore represents the equivalent of Hensens node in more rostral regions. Disordered secondary neurulation at each phase of development may cause corresponding lesions, such as failed junction with the primary neural tube (junctional neural tube defect and segmental spinal dysgenesis), dysgenesis or duplication of the caudal cell mass associated with disturbed activity of caudal mesenchymal tissue (caudal agenesis and caudal duplication syndrome), failed ingression of the primitive streak to the caudal cell mass (myelomeningocele), focal limited dorsal neuro-cutaneous nondisjunction (limited dorsal myeloschisis and congenital dermal sinus), neuro-mesenchymal adhesion (lumbosacral lipomatous malformation), and regression failure spectrum of the medullary cord (thickened filum and filar cyst, low-lying conus, retained medullary cord, terminal myelocele and terminal myelocystocele). The distribution of cell surface glycoconjugates during mouse secondary neurulation. 1 NT : primary neural tube, Jct Z : junctional zone between the primary and secondary neural tubes, CCM : caudal cell mass. If, however, the connection of the medullary cord persists only to the mesenchymal tissue, it may lead to LLM (Fig. As the proper development of the caudal mesenchyme composing the walls of the cloaca is important for the formation of the urorectal septum and its approximation to the area of the cloacal membrane, defects in the caudal mesenchyme may lead to various types of fistulous or occluded malformations involving the urogenital/anorectal organs [33]. Since the 18th century, patients manifesting various clinical anomalies of duplicated distal organs have rarely been reported [20]. Modified from Catala et al. This site needs JavaScript to work properly. As the tail is absent in both species, the medullary cord eventually degenerates. Kim KH, Wang KC, Lee JY. Secondary neurulation of human embryos: morphological During hindgut formation, mesenchymal cells grow into the cloaca and divide it into the urogenital sinus and anorectal canal [70]. What are the steps of Neurulation? - BYJU'S Axial section from a more rostral level than represented on Fig. The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate in response to local signaling cues. [24] with permission from Sage publications, Inc. Mesenchymal defects such as gastroschisis, omphalocele, bladder exstrophy, and anorectal stenosis were reported in CDupS [1,3,15]. Consequently, an open neural tube defect suggests that it is due to a process affecting primary neurulation. Another one, called secondary neurulation (SN), is seen in a posterior region of the body. 13 and 14 shows the complementary pattern observed after grafting. After inculation, grafted cells (recognized by QCPN antibody) develop and give riose to the dorsal part of the medullary cord (Med Cord) (arrows). [32] revealed the embryological background through research using chick embryos. The neural tube in the tail forms by the process known as secondary neurulation (SN), where undifferentiated mesenchymal cells change their shape to form a neural epithelium by mesenchymal-to-epithelial transition (MET) ( Criley 1969; Griffith et al. Regarding the spinal cord, insult during the earlier period of secondary neurulation will result in failed formation of the medullary cord. [48] to explain the pathoembryogenesis of SCMs. Epub 2022 Nov 21. Therefore, if apoptosis does not occur at a time when it should occur, it can cause an RMC to form [23,25,38]. This mode of body formation is called secondary formation and it is materialized by the phenomenon of secondary neurulation. [15] reported six patients with complex anomalies of the distal caudal end of the trunk and proposed the term CDupS. However, trumpet-like flaring, which is a terminal syringomyelic dilatation typically seen in TMCC, is not observed. Neurulation: Transverse sections that show the progression of the neural plate into the neural tube. Except for pure intradural lipomas (rare and prevalent at locations other than the lumbosacral area) and some LLMs of filar type, the main fat masses in LLMs are directly connected to subcutaneous fat. WebSolution Secondary neurulation: It is a morphological process that accounts for the formation of the caudal spinal cord in mammals including humans. Details of the surgical procedure are beyond the scope of this article. Thus, it is clearly established that the tail bud is not a mass of undifferentiated pluripotent cells but is made up of a juxtaposition of territories whose fate is different. Modified from Shimokita and Takahashi [58] with permission from Japanese Society of Developmental Biologists. Would you like email updates of new search results? In the area of Hensens node, the future secondary neural tube is located at the caudal midline part of Hensens node, whereas the future primary neural tube is located at the lateral sides, and secondary neurulation progresses in the caudal direction [13,58] (Fig. An approach to pathoembryogenesis from a different angle was attempted by Bannykh et al. Wei Y, Mikawa T. Fate diversity of primitive streak cells during heart field formation in ovo. However, patients with filar lesions have conditions such as a thickened filum terminale, fatty filum (filar lipoma) or filar cyst. 6). Secondary neurulation Understanding secondary neurulation and its associated processes, such as gastrulation and junctional neurulation, may uncover the previously unknown pathoembryogenesis of the lesions that therefore have not been properly classified. C : The primordium of the spinal cord is formed as a solid cellular structure (the so-called medullary cord). Involvement of the axially condensed tail bud mesenchyme in normal and abnormal human posterior neural tube development. What tissues are involved? Peripheral nervous system consists of cranial and spinal nerves, ganglia, plexuses, and 3) Frequently, the adhesion site is off the midline, and the developing laminae from both sides push the adhesion site to the midline rotating the spinal cord. Schoenwolf GC. However, this conception seems excessive to us according to our already published results. Nevertheless, after such surgical removal, the tail can form normally showing the regenerative capacities of this region [31,46]. Bijtel JH. The space between ventral neural tissue and notochord (No) is an artefact due to dehydration. Therefore early repair with resection is recommended. As mentioned above, if a transitional LLM is the result of differentiation error in the secondary neural tube, the fat tissue may be mainly present as an isolated lesion from the subcutaneous fat tissue and located at the ventral side of the spinal cord in the junctional zone (overlap zone between the primary and secondary neural tubes) because the secondary neural tube lies ventral to the primary neural tube in the junctional zone. [6]. This was done by Schumacher [37] in chick embryo (Fig. Schoenwolf GC, Nichols DH. Undoubtedly, the species for which secondary neurulation is best described is chick [7,8,16,32,35,37]. 2023;19(2):177-183. doi: 10.1038/s41567-022-01822-6. Kim JW, Wang KC, Chong S, Kim SK, Lee JY. In humans and chicks, secondary neurulation is known to occur by the elongation and cavitation of the caudal cell mass (CCM) into a medullary cord. Patients show two urethral, vaginal and anal orifices, although the bladder, uterus or rectum are only septated. Clinicians should be aware of the variability in the presentation and symptoms based on pathoembryogenesis for proper management of patients. Different entities are thought to arise depending on which stage the problem occurs during each process. 4 The tail bud is still limited by surface ectoderm (SE) dorsally and endoderm (End) ventrally. They need to internalize for undergoing neurulation; if this process is impaired, a defect affecting secondary neurulation would produce open neural tube defect. An official website of the United States government. Epub 2016 Oct 29. WebThis first study of molecular aspects of secondary NCC ontogeny has revealed that the mechanisms of neural crest generation occurring along the trunk region of the chick embryo are generally conserved and independent of the type of neurulation involved. In the mesodermal caudal eminence, a hollow space arises that becomes connected to the central canal of the neural tube. The rostral pole is located at the right of the figure. Gasser E. Der Primitivstreifen bei Vogelembryonen (Huhn und Gans). The study of chick embryos younger than the stage that I have just described, shows an overlap zone where the neural tube is formed by primary neurulation in its dorsal part while its ventral part is formed by secondary neurulation. During the third week of gestation the notochord sends signals to the overlying ectoderm, inducing it to become neuroectoderm. 8600 Rockville Pike Comparing Fig. In order to determine if the tail bud of birds is a homogeneous structure as imagined by David Holmdahl or if, on the contrary, it is composed by different territories (according to Jean Pasteels), we realized a fate map of this region in birds [7] . The presence of an overlapping zone between the primary and secondary neural tubes is previously well known [12,58]. steps 15). A detailed description of the terminal balloon from formation to disappearance was performed using chick embryos. 2022 Apr 21;10(5):965. doi: 10.3390/biomedicines10050965. Retethering after transection of a tight filum terminale, postoperative MRI may help to identify patients at risk. Al-Omari MH, Eloqayli HM, Qudseih HM, Al-Shinag MK. The lumens produced during primary and secondary neurulations are continuous [22-25,29,37] (Fig. Eine formgeschichtliche und materialgeschichtliche Analyse. There is no contribution of grafted cells to the neural tube (NT). In order to determine the relationships between primary and secondary neurulation in birds, we carried out a fate map of the territories of the rhomboid sinus [6] At the 6 somite stage in birds (Fig. Such a mechanism has not been demonstrated in mammals and should lead my readers to remain cautious about the generalization of this phenomenon to all vertebrate species. Economides KD, Zeltser L, Capecchi MR. Hoxb13 mutations cause overgrowth of caudal spinal cordand tail vertebrae. [32] by permission from Springer Nature. Based on the similarity of spinal cord pathology, they insisted that SSD, which was established as a separate entity by Scott et al. We thus show that part of the central nervous system also undergoes this same process. During primary neurulation, the folds of the groove fuse to form the neural tube. [40]) in which anorectal and urogenital anomalies may be associated. Lee JY, Kim SP, Kim SW, Park SH, Choi JW, Phi JH, et al. Multiple lumens can be evidenced in the secondary neural tube (A and B). Duplicated organs are mostly derivatives of the hindgut and CCM. Embryology, Neural Tube Article - StatPearls CDupS involves the gastrointestinal, genitourinary, spinal, musculoskeletal and cardiovascular systems. No potential conflict of interest relevant to this article was reported. Since this morphogenetic process occurs after the one affecting the neural plate, it is described as secondary neurulation. Analysis of the developing Xenopus tail bud reveals separate phases of gene expression during determination and outgrowth. 10). This information solved the enigmas of several dysraphic lesions, such as caudal agenesis, caudal duplication syndrome (CDupS), SSD, and LLM of transitional type, in which the main pathology seemed to occur during secondary neurulation, but the spine and spinal cord of lower thoracic and lumbar segments (previously regarded as products of primary neurulation) may be involved. Bertocchini F, Stern CD. The spinal level of this LDM was regarded as S1. The distal end (dome) of the balloon is stuck to the skin of chick embryos. It is assumed that the RMC is a medullary cord that remains as a result of regression failure in the process of secondary neurulation. Oiseaux. This second experiment validates our first result and proves that all the tissues that would generate the spinal cord by secondary neurulation are located in the superficial layer of the embryo. Furthermore, the close association with the activity of caudal mesenchymal tissue in secondary neurulation involves a wider range of surrounding structures than in primary neurulation. Each part of this article was primarily written by one of the coauthors and modified after discussion among the authors : Jeyul Yang (CCM duplication associated with disturbed activity of caudal mesenchymal tissue), Ji Yeoun Lee (hypoplasia or arrest of secondary neurulation associated with disturbed activity of caudal mesenchymal tissue, failed ingression of the primitive streak to the CCM), Kyung Hyun Kim (failed regression spectrum of the medullary cord) and Kyu-Chang Wang (failed junction with the primary neural tube, focal limited dorsal neuro-cutaneous nondisjunction, neuro-mesenchymal adhesion). In the originally compact cord, a hollow space arises that connects with the central canal and that finally becomes coated with neural epithelium. He considers the tail bud as a blastema made up of homogeneous and undifferentiated cells. He observed a few small cavities whose size is that of nuclei. The secondary neurulation is described as the event in which more caudal levels of the spinal cord are generated by connection and fusion of mesodermal cells (Sadler 2005). Gont LK, Steinbeisser H, Blumberg B, de Robertis EM. 14). Simultaneously, secondary neurulation, with key words such as the primitive streak, primitive node (Hensens node), gastrulation, junctional neurulation, caudal cell mass (CCM) and medullary cord, became one of the central topics of academic interest in this field. 6), two lumens develop inside the medullary cord. If fat or fibrous tissue grows into the filum and replaces glial tissue, it may create a fatty filum or thickened filum terminale (Fig. Such a superficial origin of tissues fated to formed caudal spinal cord has also been demonstrated for zebrafish [18] and amphibans [2,41,42]. Type III and type IV are the same as the previous caudal type (the failure of early secondary neurulation) and filar type (the failure of late secondary neurulation), respectively. Pang D, Zovickian J, Moes GS. The caudal neural plate was labelled with the carboxyfluorescein diacetate succimidyl ester (CFDA-SE). Following this reconstruction, we see that secondary lumens freely communicate with the primary lumen of the neural tube. 5), neural midline cells appear as a homogeneous rod of cells (the so-called medullary cord). [17], which had nonfunctional band-like structures instead of a functional spinal cord at the junctional zone, must have had localized insults at the place of junctional neurulation. However, as the tail bud is transplanted en bloc, it is not possible to demonstrate heterogeneity in the grafted structure using this type of experiments. 6, the two lumens fuse. The primitive streak is the site of gastrulation. The https:// ensures that you are connecting to the B : A T1 axial image at the level of the dotted line (A). Quail cells can be recognised by their condensed heterochromatin (arrowheads). 3), an axial section of the embryo shows mesenchymal tissue located between the surface ectoderm (forming the most dorsal region of the embryo) and the endoderm (its ventral region). Row RH, Tsotras SR, Goto H, Martin BL. D and E : If the spinal cord is distracted to the extraspinal side, a terminal myelocele (if the terminal balloon collapses, D) or terminal myelocystocele (if the terminal balloon persists, E) is formed. The next hypothesis would be that secondary neurulation error may also result in ONTDs. However, in reality, the fat tissue in the junctional zone in transitional-type LLMs is located at the dorsal side and connects with the subcutaneous fat. In our series, approximately 40% (11/28) of all LDM cases were located in the area of secondary neural tube. 13). Apart from duplication, CDupS shows mesenchymal defects, which are also characteristics of caudal agenesis. The exits from the spinal cord are located at the vertebral level of L1 or L2. Shedden PM, Wiley MJ. D and E : Dorso-ventral gradient of epithelialization. In addition, they emphasized the timing of errors according to the LLM type, but the nature of errors was not mentioned for types IIIV. Caudally to the level of sacral nerves 3 to 6, the graft yields the caudal notochord (arrowheads) and the floor plate (double arrow). Cambray N, Wilson V. Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. More rostrally (Fig. This mode of experimentation shows that the caudal bud in amphibians is formed by a mosaic of juxtaposed territories [2]. Retethering : a neurosurgical viewpoint. Childs Nerv Syst. 21). The space between CNH and ventral neural tissue is an artefact due to dehydration. Analysis of the embryonic sources and mechanisms of development of posterior levels of chick neural tubes. It is generally widely accepted that secondary neurulation abnormalities generate by definition closed neural tube defects. The patient can exhibit gait disturbance, pain, sensory deficit, urological dysfunction, scoliosis or foot deformities. They involve homotopic and isochronic transplants (the graft replaces the same anatomical region of the host, host and donor have the same age) that were either marked with tritiated thymidine [30] or by using the chimeric quail chicken system [34], a system that I will describe later. Arai H, Sato K, Okuda O, Miyajima M, Hishii M, Nakanishi H, et al. However, this heterogeneity might only reflect diversity of inductions. 8). [6]. A graft containing the latero-caudal part of the neural plate from a 6-somite quail embryo is placed at the same level in a chick host. The misexpression of chordin also led to an ectopic primitive streak [59]. Isolated lipoma of filum terminale in adults: MRI findings and clinical correlation. When the fat tissue is slender, parts of the fat tissue may easily fall off from the main fat mass, resulting in satellite lesions. There is no contribution of grafted cells to the neural tube (NT). A drawing showing the method to determine the spinal level of limited dorsal myeloschisis (LDM). 8600 Rockville Pike These processes contrast with the well known primary neurulation, which is achieved by View on Wiley ncbi.nlm.nih.gov Save to Library Create Alert Cite 41 Citations Citation Type Neurulation and the Neural Tube 17). PMC The formation of the hindgut begins at the fourth week of gestation from caudal folding of an embryo [39]. Enlargement of extraspinal cysts in spinal dysraphism : a reason for early untethering. Secondary neurulation is a morphological process described since the second half of the 19th century; it accounts for the formation of the caudal spinal cord in mammals including humans. WebSecondary neurulation, which begins at stage 12, is the differentiation of the caudal part of the neural tube from the caudal eminence (or end-bud) without the intermediate phase of a neural plate. They include the addition of lipomyelomeningoceles (an extraspinal extension with extraspinal herniation of the subarachnoid space) and a chaotic type (involving a placode and roots) [4,51]. It is the process by which the neural tube at the lower levels and Schoenwolf GC. QCPN antibody marks specifically the quail nucleus and not the chick one. Zhang T, Zhang HL, Wang da J, Tang XB, Jia HM, Bai YZ, et al. Development. End : endoderm, So : somatopleural mesoderm, Sp : splanchnopleural mesoderm. 7). 1882;6:207241. Although the majority of the data are from animals, not from humans and many theories are still conjectural, these changing concepts of normal and disordered secondary neurulation will provoke further advancements in our management strategies as well as in the pathoembryogenetic understanding of anomalous lesions in this area. 1994;181:70-82; discussion 82-9. doi: 10.1002/9780470514559.ch5. We speculated that parallel running of the CCM, or the late-stage primitive streak, would form mesenchymal cells between the two primordial body axes. Axial section of a sheep embryo (Maximilian Braun) [4]. Pathogenesis of lumbosacral lipoma: a test of the premature dysjunction theory. The, At more rostral level compared to Fig. Grafted cells contribute to neural tube (NT) (arrowheads) and somitic derivatives (arrows). Thereafter, modifications of the classification were proposed. Web1. Unable to load your collection due to an error, Unable to load your delegates due to an error. 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