Phylogenetic aspects of cloacal epithelium development in vertebrates

Abstract

BACKGROUND: The study of embryonic tissue and organ development from the perspective of comparative evolutionary histology enables the tracing of gradual changes in histogenetic processes and their continuity among vertebrate species. Data on the phylogenetic aspects of cloacal epithelium development remain fragmentary. Data on the histological structure of the epithelial lining of the anorectal canal (ARC) and cloacal subdivisions in embryogenesis across vertebrates (amphibians, birds, mammals) and humans are scarce in the scientific literature, with only a few published studies available. Research in this area is of particular relevance as it contributes to refining the theory of critical periods of embryogenesis and understanding the mechanisms of congenital malformations in humans.

AIM: To provide a comparative morphological characterization of the epithelial lining of the cloaca in cloacal vertebrates and the epithelial lining of the anorectal part of the digestive tract in rat and human embryos, based on the concept of heteromorphy.

METHODS: A single-center, observational, retrospective, uncontrolled study was conducted. The study material included the caudal region of the ARC in cloacal vertebrates (adult frogs, 13-day-old chicken embryos) and mammals (rat embryos at 9, 15, and 18 days of development). Additionally, histological specimens of human embryos (7–8 weeks of intrauterine development) were analyzed. Samples were fixed, dehydrated in alcohol, embedded in paraffin, and sectioned for Hematoxylin and Eosin staining, as well as Feulgen staining. Statistical analysis was performed, including calculations of the mean (M) and standard error of the mean (m).

RESULTS: The study revealed that different parts of the cloaca in vertebrates exhibit morphometric differences in their epithelial lining. The urinary part of the cloaca in vertebrates with a cloaca and chicken embryos is characterized by a heteromorphic structure. In mammalian embryogenesis (rat embryos), the formation of the cloacal membrane involves interacting histological systems derived from various embryonic primordia, including the peridermal epithelium, the allantoic epithelium adjacent to the periderm, and the gut-type epithelium of the hindgut. In human antenatal development, ARC formation is marked by the emergence of interaction zones between epithelial layers, which differ in structure and tinctorial properties.

CONCLUSION: Comparative analysis indicates that the embryogenesis of vertebrates, particularly in rats and humans, exhibits specific similarities in the composition of the epithelial lining of the ARC and the cloacal epithelium of amphibians and birds. The bilayered urothelium-like epithelium serves as a transient structure during embryonic development.

Keywords

cloaca / cloacal membrane / hindgut / epithelial lining / embryonic histogenesis / anorectal canal / phylogeny

References

[1] Knorre AG. Embryonic histogenesis: Morphological essays. Leningrad: Medicine; 1971. (In Russ.)

[2] Blumberg AZh. Experimental-histological study of skin and intestinal epithelium types in the adjacent area [dissertation]. Leningrad; 1949. (In Russ.)

[3] Khlopin NG. General biological and experimental foundations of histology. Moscow: Izdatel’stvo Akademii Nauk SSSR; 1946. (In Russ.)

[4] Borisov IN, Dunaev PV, Bazhanov AN. Phylogenetic foundations of tissue organization in animals. Novosibirsk: Nauka; 1986. (In Russ.)

[5] Danilov RK, Komarova AS, Zheglova MY, Odintsova IA. On the question of tissue derivatives of the vertebrate cloacae. In: Questions of morphology of the XXI century: Proceedings of the 26th All-Russian scientific conference “Histogenesis, Reactivity and Tissue Regeneration”. St. Petersburg, 16–17 May 2024. Saint Petersburg: Limited liability company “Izdatel’stvo DEAN”; 2024. EDN: CAJPBP

[6] Danilov RK, Zheglova MYu. Formation of heterogeneity of the epithelial lining of the utero-vaginal tract in prenatal development in humans. Current problems in morphology: embryonic and reparative histogenesis, phylohistogenesis. Saint Petersburg: Izdatel’stvo SPbGPMU; 2014. (In Russ.)

[7] Hoshi M, Reginensi A, Joens MS, et al. Reciprocal spatiotemporally controlled apoptosis regulates Wolffian duct cloaca fusion. J Am Soc Nephrol. 2018;29(3):775–783. doi: 10.1681/ASN.2017040380

[8] Kruepunga N, Hikspoors JPJM, Mekonen HK, et al. The development of the cloaca in the human. J Anat. 2018;233(6):724–739. doi: 10.1111/joa.12882

[9] Komarova AS. The structural features of the epithelial lining of the cloaca in mature tailless amphibians of Rana temporaria species. In: Innovative technologies for studying histogenesis, reactivity and tissue regeneration (Proceedings of the Military Medical Academy). Saint Petersburg: Kirov Military Medical Academy; 2024. EDN: FAJOGS

[10] Shevlyuk NN. The main patterns of transformation in organs of reproductive system during the evolution of vertebrates. Journal of Anatomy and Histopathology. 2023;12(3):103–112. doi: 10.18499/2225-7357-2023-12-3-103-112 EDN: ZLRTGT

[11] Solovyev GS, Pantelyev SM, Shidin VA, Yanin VL. Divergence of organogenesis and divergent mechanism of organ evolution. Morphology. 2019;155(2):266. (In Russ.) EDN: LHKKJU

[12] Gică N, Apostol L, Huluţă I, et al. Cloacal dysgenesis sequence. Diagnostics (Basel). 2023;13(23):3529. doi: 10.3390/diagnostics13233529

[13] Li Y, Liu P, Wang W, et al. A novel genotype-phenotype between persistent-cloaca-related VACTERL and mutations of 8p23 and 12q23. Pediatr Res. 2023;95(5):1246–1253. doi: 10.1038/s41390-023-02928-0

[14] Singh S, Kayastha A, Thapa A, et al. Omphalocele, exstrophy of cloaca, imperforate anus, and spinal defects complex: a case report. JNMA J Nepal Med Assoc. 2023;61(260):375–378. doi: 10.31729/jnma.8048

[15] Fritsch H, Zehm S, Illig R, et al. New insights into the development and differentiation of the human anorectal epithelia. Are there clinical consequences? Int J Colorectal Dis. 2010;25(10):1231–1242. doi: 10.1007/s00384-010-0986-6

[16] Danilov RK, editor. Handbook of Histology. 2nd ed. Saint Petersburg: SpetsLit; 2011. (In Russ.)

[17] Thomas DFM. The embryology of persistent cloaca and urogenital sinus malformation. Asian J Androl. 2020;22(2):124–128. doi: 10.4103/aja.aja_72_19

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