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The Development of the Male Genitourinary System: II. the Origin and Formation of the Urethral Plate

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The Development of the Male Genitourinary System: II. the Origin and Formation of the Urethral Plate The British Association of Plastic Surgeons (2004) 57, 112–121 The development of the male genitourinary system: II. The origin and formation of the urethral plate P.J. Hynes*, J.P. Fraher Department of Anatomy, University College Cork, Cork, Ireland Received 10 May 2002; accepted 21 August 2003 KEYWORDS Summary The origin, extent and topographical relationships of the urethral plate and Urethral plate; its role in the pathogenesis of developmental anomalies (bladder extrophy, epispadias Epispadias; Hypospadias; and hypospadias) remain incompletely resolved. The commonly held view that the Cloaca; Urethra urethral plate (the forerunner of the urethra) arises through distal proliferation of the cells of the anterior wall of the cloaca cannot explain these anomalies. Given this and its newfound implications for hypospadias repair the development of the urethral plate is presented in detail. New insights into the origin of associated congenital defects are revealed. Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. The origin of the urethral plate and its role in another view considers that the urethral plate development of the urethra has been the subject of results from apposition of the walls of the divergent views. According to most investigators cloaca.13 – 15 Moreover, the relationship of the the endoderm of the anterior cloacal wall prolifer- urethral plate and the cloacal membrane and ates and forms the epithelial urethral plate, which their roles in the pathogenesis of developmental grows anteriorly in the mesoderm of the genital anomalies is poorly understood.10,12,16,17 Some tubercle. It remains in contact with the ectoderm believe that bladder extrophy and epispadias result covering the caudal median surface of the tubercle from excessive lengthening of the cloacal mem- 3,9,20 at the cloacal groove.1–8 The urethral plate is brane early in development. Whilst hypospa- considered to be the precursor of the glandar dias is considered by most to result from failure of 2,5,6,9,16,17,21 urethra only, the remainder of the penile urethra fusion of the urethral folds, van der 3 developing from the urogenital sinus itself. Others Putte postulates that it results from a defect in the propose that the urethral plate is the precursor of cloacal membrane. the whole penile urethra.9,10 According to another This study entails a re-assessment of normal hypothesis the ectoderm lining the cloacal groove development and aims to resolve these inconsis- proliferates to form the urethral plate and the tencies. A clear understanding of the origin and latter is therefore ectodermal in origin.11,12 Yet topography of the urethral plate is important because of its new-found implications for hypospa- 24,25 *Corresponding author. dias repair. The use of native urethral epi- E-mail address: [email protected] thelium in hypospadias repair in an attempt to S0007-1226/$ - see front matter Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2003.08.018 The development of the male genitourinary system: II. The origin and formation of the urethral plate 113 simulate normal urethral form requires a detailed rostral mesoderm of genital tubercle; up, urethral knowledge of this epithelium and its extent. plate; urs, urorectal septum; us, urogenital sinus. Materials and method Observations Details of the material used, including fixation, The cloaca and the formation of the genital embedding, sectioning, staining, image capture and tubercle processing, have been given previously.22 The same sets of serial sections were used to examine the At embryonic day 11 (E11) the membranous cloaca formation of the urethral plate. (mc) is separated from the amniotic cavity (ac) by Computer assisted three-dimensional recon- the cloacal membrane (cm) (Fig. 1(a)). As the latter structions were made from sections at 30 mm is traced rostrally the superficial dense mesoderm intervals, using a Kontron image analysis system. of the cloacal folds (cf) extends progressively As before (paper I), the final reconstruction was further medially between its two epithelial com- sectioned virtually so as to view the median sagittal ponents, the cloacal endoderm and surface ecto- structures from a right lateral perspective. The derm (Fig. 1(b) and (c)). With this, the width of the resulting images were stored in a Harvard Graphics cloacal membrane decreases correspondingly. As it programme. The dimensions of individual struc- does so, its depth increases progressively, due to an tures were measured directly from the calibrated increase in the number of its endodermal cell reconstructions (Fig. 9). layers. This mesodermal extension continues to increase Abbreviations used in text: ac, amniotic cavity; ap, in degree during E11, particularly rostrally and apical part of glans; c, corona; cd, cloacal duct; cf, caudally. Thus, the depth of the endodermal cloacal fold; cg, cloacal groove; cm, cloacal component of the cloacal membrane (cm) con- membrane; gt, genital tubercle; hg, hindgut; mc, tinues to increase whilst its breadth decreases (Fig. membranous cloaca; pc, phallic cloaca; pug, 2(a)–(c)). During this period also, the rostral cloaca primitive urethral groove; rc, rostral cloaca; rmgt, (rc) is becoming partitioned into the hindgut (hg) Fig. 1 (a) Reconstructed mid-sagittal section of an E11 specimen. (b) and (c) Light micrographs of transverse sections of an E11 specimen. Their levels are indicated in (a). As the membranous cloaca (mc) is traced rostrally the superficial mesoderm of the cloacal folds (cf) comes closer to the midline. With this the depth of the cloacal membrane increases. Key to labels in Figs. 1–8: ac, amniotic cavity. ap, apical part of glans. c, corona. cd, cloacal duct. cf, cloacal fold. cg, cloacal groove. cm, cloacal membrane. cs, coronal sulcus. dw, dorsal body wall. hg, hindgut. ic, intraembryonic coelom. iuw, infra-umbilical ventral wall. mc, membranous cloaca. md, mesonephric duct. pc, phallic cloaca. pf, preputial fold. pug, primitive urethral groove. rc, rostral cloaca. rmgt, rostral mesoderm of genital tubercle. t, tail. tg, tail gut. ud, urogenital duct. up, urethral plate. urs, urorectal septum. us, urogenital sinus. Arrowheads indicate apoptosis. Note: in Figs. 1(a)–6(a), red, yellow and grey represent ectoderm, endoderm and mesoderm, respectively. 114 P.J. Hynes, J.P. Fraher Fig. 2 (a) Reconstructed mid-sagittal section of a late E11 specimen. (b) and (c) Light micrographs of transverse sections of a late E11 specimen. Their levels are indicated in (a). The depth of the cloacal membrane (cm) continues to increase. Key to labels are given in caption of Fig. 1. Fig. 3 (a) Reconstructed mid-sagittal section of an E12 specimen. The rostral end of the now deep cloacal membrane (cm) is being displaced towards the tip of the GT by the RMGT. (b) and (c) Light micrographs of transverse sections of an E12 specimen. Their levels are indicated in (a). Key to labels are given in caption of Fig. 1. The development of the male genitourinary system: II. The origin and formation of the urethral plate 115 and the urogenital sinus (us) by the urorectal Formation of the urethral plate septum (urs) (Fig. 2(a)). As a result of continued growth of the rostral Initially, early in E12 the phallic cloaca (pc) extends mesoderm of the genital tubercle (rmgt) (Figs. from the caudal to the rostral surfaces of the 3(a) and 4(a)) during E12, by E13 it has genital tubercle (gt). Its membrane is continuous overgrown the cloacal fold mesoderm distally with the ectoderm of the cloacal groove (cg), which to form the tip of the genital tubercle (gt) and extends onto its distal, rostral surface (Fig. 3(a) and the apical part of the glans (ap) (Fig. 5(a)). With (b)). As the rmgt extends distally, it progressively this the membranous cloaca (mc) and the cuts off this continuity with the rostral surface (Fig. cloacal folds no longer reach the tip of the gt. 4(a)–(d)). As a result, by E13 it fails to reach quite Most of the membranous cloaca extends distally to the tip of the gt as the rmgt overgrows it to form in the caudal median region of the gt as the the apical part of the glans (ap) (Fig. 5(a) and (b)). phallic cloaca (pc) (Figs. 3(a) and (c), and 4(a) Over the same period the cloacal folds (cf) come and (c)). The rmgt forms the deep wall of the closer to the median plane and the cloacal latter, the cloacal folds (cf) form its lateral membrane (cm) continues to become deeper and walls, and its ventral and caudal walls are narrower (Fig. 3(a) and (b)). By late E12, the distal formed by the ventral part of the cloacal walls of the phallic cloaca (pc) come together to membrane (cm) (Fig. 4). The proximal part of comprise a solid, sagittally orientated, median the membranous cloaca, which lies superficial to plate of endoderm, the urethral plate (up) (Fig. the urorectal septum (urs), forms the cloacal 4(a) and (b)). This remains in continuity with the duct (cd) (Fig. 4(a)). ectoderm at the bottom of the cloacal groove (cg) Fig. 4 (a) Reconstructed mid-sagittal section of a late E12. The sidewalls of the distal part of the phallic cloaca are coming into apposition and the urethral plate (up) is beginning to form. (b)–(e) Light micrographs of transverse sections of late E12. Their levels are indicated in (a). A small median cyst-like cavity persists, separate from that of the phallic cloaca (a) and (c). Key to labels are given in caption of Fig. 1. 116 P.J. Hynes, J.P. Fraher Fig. 5 (a) Reconstructed mid-sagittal section of an E13 specimen. The corona (c) is evident and the RMGT has extended distal to the urethral plate (up) to form the apical part of the glans (ap).
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