Ontogeny of the meniscus in the anuran Xenopus laevis.
geometric morphometrics
hindlimbs
histology
knee ontogeny
locomotion
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
Feb 2023
Feb 2023
Historique:
revised:
03
09
2022
received:
11
03
2022
accepted:
06
09
2022
pubmed:
13
9
2022
medline:
25
1
2023
entrez:
12
9
2022
Statut:
ppublish
Résumé
The anuran knee joint is subjected to the jump, one of the tetrapods' most demanding mechanical stresses. Consistent with this continuous effort, the knee of the anurans has a complex structure comparable to that of an amniote. Here, we describe the ontogeny of the Xenopus knee tissues and study the morphogenesis of the knee joint shape by performing a geometric morphometric analysis of specially selected anatomical structures: the menisci and the long bone epiphyses. A meniscus is a crescent-shaped fibrocartilaginous structure, with a triangular cross-section inserted between joints surfaces. A meniscus transmits load across the tibiofemoral joint by increasing congruity of the long bone epiphysis and decreasing the resulting stress exerted on the articular cartilage. We ask two questions: (1) what is the tissue composition along the ontogeny of the menisci of a swimming frog? (2) How do the menisci acquire the shape that will allow their adjustment? We studied the structures and tissue ontogeny of the knee of several specimens of Xenopus laevis and evaluated the congruity of the knee structures across the species ontogeny. Histological sections showed that the cavitation process responsible for separating the menisci and the epiphyses seems to be pivotal in shaping the conformity of these structures and the long bone epiphyses of the hindlimbs. The geometric morphometric analysis allowed us to interpret three phases of differentiation associated with limb functionality. The characteristic shape of the meniscus appears early in the ontogeny of the knee, simultaneously with the epiphysis contours.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
457-469Subventions
Organisme : Agencia Nacional de Promoción Científica y Tecnológica (FONCYT)
ID : Prestamo BID PICT 2016 2772
Organisme : Agencia Nacional de Promoción Científica y Tecnológica (FONCYT)
ID : Prestamo BID PICT 2018 0832
Organisme : Agencia Nacional de Promoción Científica y Tecnológica (FONCYT)
ID : Prestamo BID PICT 2019 03230
Organisme : Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)
ID : PIP 0389
Informations de copyright
© 2022 American Association for Anatomy.
Références
Abdala, V., Cristobal, L., Soliz, M. C., & Dos Santos, D. A. (2021). Geographical information system applied to a biological system: Pelvic girdle ontogeny as a morphoscape. Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.642255
Abdala, V., & Ponssa, M. L. (2012). Life in the slow line: The effect of reduced mobility on tadpole limb development. The Anatomical Record, 295, 5-17.
Abdala, V., Vera, M. C., & Ponssa, M. L. (2017). On the presence of the patella in frogs. The Anatomical Record, 300(10), 1747-1755. https://doi.org/10.1002/ar.23629
Ahmed, A. M., & Burke, D. L. (1983). In-vitro of measurement of static pressure distribution in synovial joints-Part I: Tibial surface of the knee. Journal of Biomechanical Engineering, 105(3), 216-225. https://doi.org/10.1115/1.3138409
Andrews, S., Shrive, N., & Ronsky, J. (2011). The shocking truth about meniscus. Journal of Biomechanics, 44, 2737-2740. https://doi.org/10.1016/j.jbiomech.2011.08.026
Beaupré, A., Choukroun, R., & Guidouin, R. (1986). Knee menisci. Correlation between microstructure and biomechanics. Clinical Orthopaedics and Related Research, 208, 72-75.
Bochyńska, A. I., Hannink, G., Grijpma, D. W., & Buma, P. (2016). Tissue adhesives for meniscus tear repair: An overview of current advances and prospects for future clinical solutions. Journal of Material Science: Materials in Medicine, 27(5), 85. https://doi.org/10.1007/s10856-016-5694-5
Bookstein, F. L. (1991). Thin-plate splines and the atlas problem for biomedical images. Information Processing in Medical Imaging, 511, 326-342. https://doi.org/10.1007/bfb0033763
Bookstein, F. L. (1997). Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. Medical Image Analysis, 1(3), 225-243. https://doi.org/10.1016/s1361-8415(97)85012-8
Borden, P., Nyland, J., Caborn, D. N. M., & Pienkowski, D. (2003). Biomechanical comparison of the fast-fix meniscal repair suture system with vertical mattress sutures and meniscus arrows. The American Journal of Sports Medicine, 31(3), 374-378. https://doi.org/10.1177/03635465030310030801
Canillas, F., Delgado-Martos, M. J., Touzal, A., Escario, A., Martos-Rodriguez, A., & Delgado-Baeza, E. (2011). An approach to comparative anatomy of the acetabulum from amphibians to primates. Anatomia, Histologia, Embryologia, 40, 466-473. https://doi.org/10.1111/j.1439-0264.2011.01095.x
Castania, V. A., Silveira, J. W. S., Issy, A. C., Pitol, D. L., Castania, M. L., Neto, A. D., Del Bel, E. A., & Defino, H. L. A. (2015). Advantages of a combined method of decalcification compared to EDTA. Microscopy Research and Technique, 78(2), 111-118. https://doi.org/10.1002/jemt.22451
Chazotte, B. (2012). Labeling Golgi with fluorescent ceramides. Cold Spring Harbor Protocols, 2012(8), pdb.prot070599. https://doi.org/10.1101/pdb.prot070599
Chevrier, A., Nelea, M., Hurtig, M. B., Hoemann, C. D., & Buschmann, M. D. (2009). Meniscus structure in human, sheep, and rabbit for animal models of meniscus repair. Journal of Orthopaedic Research, 27(9), 1197-1203. https://doi.org/10.1002/jor.20869
Colnot, C., Lu, C., Hu, D., & Helms, J. A. (2004). Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Developmental Biology, 269, 55-69. https://doi.org/10.1016/j.ydbio.2004.01.011
Cosden, R. S., Lattermann, C., Romine, S., Gao, J., Voss, S. R., & MacLeody, J. N. (2011). Intrinsic repair of full-thickness articular cartilage defects in the axolotl salamander. Osteoarthritis and Cartilage, 19, 200-205. https://doi.org/10.1016/j.joca.2010.11.005
Di Giancamillo, A., Deponti, D., Addis, A., Domeneghini, C., & Peretti, G. M. (2014). Meniscus maturation in the swine model: Changes occurring along with anterior to posterior and medial to lateral aspect during growth. Journal of Cellular and Molecular Medicine, 18(10), 1964-1974. https://doi.org/10.1111/jcmm.12367
Dye, S. F. (2003). Functional morphologic features of the human knee: An evolutionary perspective. Clinical Orthopaedics and Related Research, 410, 19-24. https://doi.org/10.1097/01.blo.0000063563.90853.23
Eames, B. F., de la Fuente, L., & Helms, J. A. (2003). Molecular ontogeny of the skeleton. Birth Defects Research Part C, 69, 93-101. https://doi.org/10.1002/bdrc.10016
Engebretsen, L., & Bahr, R. (2007). Dolor en la rodilla. In R. Bahr & S. Maelum (Eds.), Lesiones deportivas. Editorial Médica Panamericana.
Felisbino, S., & Carvalho, H. F. (2001). Growth cartilage calcification and formation of bone trabeculae are late and dissociated events in the endochondral ossification of Rana catesbeiana. Cell and Tissue Research, 306, 319-323. https://doi.org/10.1007/s004410100446
Felisbino, S. L., & Carvalho, H. F. (2000). The osteochondral ligament: A fibrous attachment between bone and articular cartilage in Rana catesbeiana. Tissue and Cell, 32(6), 527-536. https://doi.org/10.1016/s0040-8166(00)80009-9
Fox, A. J., Wanivenhaus, F., Burge, A. J., Warren, R. F., & Rodeo, S. A. (2015). The human meniscus: A review of anatomy, function, injury, and advances in treatment. Clinical Anatomy, 28(2), 269-287. https://doi.org/10.1002/ca.22456
Gardner, E., & O'Rahilly, R. (1968). The early development of the knee joint in staged human embryos. Journal of Anatomy, 102(2), 289-299.
Günther, M. M., Ishida, H., Kumakura, H., & Nakano, Y. (1991). The jump as a fast mode of locomotion in arboreal and terrestrial biotopes. Zeitschrift für Morphologie und Anthropologie, 78(3), 341-372.
Haines, R. W. (1942). The tetrapod knee joint. Journal of Anatomy, 76, 270-301.
Hall, B. K., & Miyake, T. (2000). All for one and one for all: Condensations and the initiation of skeletal development. BioEssays, 22, 138-147. https://doi.org/10.1002/(SICI)1521-1878(200002)22:2<138:AID-BIES5>3.0.CO;2-4
Hebling, A., Esquisatto, M. A. M., Aro, A. A., & Gomes, L. (2014). Morphological modifications of knee articular cartilage in bullfrogs (Lithobates catesbeianus) (Anura: Ranidae) during postmetamorphic maturation. Zoomorphology, 133, 245-256.
Klingenbergl, C. P. (2010). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353-357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Kurosawa, H., Fukubayashi, T., & Nakajima, H. (1980). Load-bearing mode of the knee joint: Physical behavior of the knee joint with or without menisci. Clinical Orthopaedics and Related Research, 149, 283-290.
Levy, I. M., Torzilli, P. A., & Warren, R. F. (1982). The effect of medial meniscectomy on anterior-posterior motion of the knee. The Journal of Bone and Joint Surgery, 64(6), 883-888.
Makris, E. A., Hadidi, P., & Athanasiou, K. A. (2011). The knee meniscus: Structure-function, pathophysiology, current repair techniques, and prospects for regeneration. Biomaterials, 32(30), 7411-7431. https://doi.org/10.1016/j.biomaterials.2011.06.037
Manzano, A., Abdala, V., Ponssa, M. L., & Soliz, M. (2013). Ontogeny and tissue differentiation of the pelvic girdle and hind limbs of anurans. Acta Zoologica, 94(4), 420-436. https://doi.org/10.1111/j.1463-6395.2012.00571.x
Masouros, S. D., McDermot, I. D., Amis, A. A., & Bull, A. M. J. (2008). Biomechanics of the meniscus-meniscal ligament construct of the knee. Knee Surgery, Sports, Traumatology Arthroscopy, 16, 1121-1132.
Meller, R., Schiborra, F., Brandes, G., Knobloch, K., Tschernig, T., Hankemeier, S., Haasper, C., Schmiedl, A., Jagodzinski, M., Krettek, C., & Willbold, E. (2009). Postnatal maturation of tendon, cruciate ligament, meniscus, and articular cartilage: A histological study in sheep. Annals of Anatomy, 191(6), 575-585. https://doi.org/10.1016/j.aanat.2009.08.005
Messner, J., & Gao, J. (1998). The menisci of the knee joint. Anatomical and functional characteristics, and a rationale for clinical treatment. Journal of Anatomy, 193, 161-178. https://doi.org/10.1046/j.1469-7580.1998.19320161.x
Mikic, B., Johnson, T. L., & Chhabra, A. B. (2000). Differential effects of embryonic immobilization on the development of fibrocartilaginous skeletal elements. Journal of Rehabilitation Research & Development, 37, 127-133.
Mo, X., Ge, W., Miraglia, M., Inglese, F., Zhao, D., Stefanini, C., & Romano, D. (2020). Jumping locomotion strategies: From animals to bioinspired robots. Applied Sciences, 10, 8607. https://doi.org/10.3390/app10238607
Muntz, L. (1975). Myogenesis in the trunk and leg during development of the tadpole of Xenopus laevis (Daudin 1802). Journal of Embryology and Experimental Morphology, 33, 757-774.
Nauwelaerts, S., & Aerts, P. (2006). Take-off and landing forces in jumping frogs. Journal of Experimental Biology, 209(1), 66-77. https://doi.org/10.1242/jeb.01969
Nieuwkoop, P. D., & Faber, J. (1967). Normal tables of Xenopus laevis (Daudin) Hubrecht laboratory. North Holland Publishing Co.
Nowlan, N. C., & Sharpe, J. (2014). Joint shape morphogenesis precedes cavitation of the developing hip joint. Journal of Anatomy, 224(4), 482-489. https://doi.org/10.1111/joa.12143
O'Rahilly, R., & Gardner, E. (1956). The development of the knee joint of the chick and its correlation with embryonic staging. Journal of Morphology, 98(1), 49-87. https://doi.org/10.1002/jmor.1050980103
Ovalle, W. K., & Nahirney, P. C. (2008). Netter' essential histology (2nd ed.). Elsevier.
Parsons, F. G. (1900). The joints of mammals compared to those of man: A course of lectures delivered at the Royal College of Surgeons of England Part II. Journal of Anatomy, 34, 301-323.
Pomikal, C., Blumer, R., & Streicher, J. (2011). Four-dimensional analysis of early pelvic girdle development in Rana temporaria. Journal of Morphology, 272, 287-301. https://doi.org/10.1002/jmor.10913
Ponssa, M. L., & Abdala, V. (2016). Phenotypical expression of reduced mobility during limb ontogeny in frogs: The knee-joint case. PeerJ, 4, e1730. https://doi.org/10.7717/peerj.1730
Ponssa, M. L., & Abdala, V. (2020). Sesamoids in Caudata and Gymnophiona (Lissamphibia): Absences and evidence. PeerJ, 8, e10595. https://doi.org/10.7717/peerj.10595
Přikryl, T., Aerts, P., Havelková, P., Herrel, A., & Rocek, Z. (2009). Pelvic and thigh musculature in frogs (Anura) and origin of anuran jumping locomotion. Journal of Anatomy, 214, 100-139. https://doi.org/10.1111/j.1469-7580.2008.01006.x
Proffen, B. L., McElfresh, M., Fleming, B. C., & Murray, M. M. (2012). A comparative anatomical study of the human knee and six animal species. The Knee, 19(4), 493-499. https://doi.org/10.1016/j.knee.2011.07.005
Ralphs, J. R., & Benjamin, M. (1994). The joint capsule: Structure, composition, aging and disease. Journal of Anatomy, 184, 503-509.
Rankin, C. C., Lintner, D. M., Noble, P. C., Paravic, V., & Greer, E. (2002). A biomechanical analysis of meniscal repair techniques. The American Journal of Sports Medicine, 30(4), 492-497. https://doi.org/10.1177/03635465020300040801
Rath, E., & Richmond, J. C. (2000). The menisci: Basic science and advances in treatment. British Journal of Sports Medicine, 34(4), 252-257. https://doi.org/10.1136/bjsm.34.4.252
Reese, S., Pfuderer, U. R., Bragulla, H., Loeffler, K., & Budras, K.-D. (2001). Topography, structure and function of the patella and the patelloid in marsupials. Anatomia, Histologia, Embryologia: Journal of Veterinary Medicine Series C, 30(5), 289-294.
Rohlf, F. J. (2015). The tps series of software. Hystrix, the Italian Journal of Mammalogy, 26, 9-12. https://doi.org/10.4404/hystrix-26.1-11264
Saavedra, M., Sepúlveda, M., Tuca, M. J., & Birrer, E. (2020). Discoid meniscus: Current concepts. EFORT Open Reviews, 5(7), 371-379. https://doi.org/10.1302/2058-5241.5.190023
Satoh, A., Sakamaki, K., Ide, H., & Tamura, K. (2005). Characteristics of initiation and early events for muscle development in the Xenopus limb bud. Developmental Dynamics, 234(4), 846-857. https://doi.org/10.1002/dvdy.20573
Sgaglione, N. A., Steadman, J. R., Shaffer, B., Miller, M. D., & Fu, F. H. (2003). Current concepts in meniscus surgery: Resection to replacement. Arthroscopy. The Journal of Arthroscopic and Related Surgery, 19(10), 161-188. https://doi.org/10.1016/j.arthro.2003.10.032
Slack, J. M. W. (1984). Regional biosynthetic markers in the early amphibian embryo. Journal of Embryology and Experimental Morphology, 80, 289-319.
Soliz, M., Tulli, M. J., & Abdala, V. (2017). Osteological postcranial traits in hylid anurans indicate a morphological continuum between swimming and jumping locomotor modes. Journal of Morphology, 278(3), 403-417. https://doi.org/10.1002/jmor.20651
Soren, A. (1985). On the etiology of congenital malformation of the meniscus. Archives of Orthopaedic and Traumatic Surgery, 104(5), 283-288. https://doi.org/10.1007/bf00435943
Tardieu, C. (1999). Ontogeny and phylogeny of femoro-tibial characters in humans and hominid fossils: Functional influence and genetic determinism. American Journal of Physical Anthropology, 110(3), 365-377. https://doi.org/10.1002/(sici)1096-8644(199911)110:3<365:aid-ajpa8>3.0.co;2-t
Thorlund, J. B., Hare, K. B., & Lohmander, L. S. (2014). Large increase in arthroscopic meniscus surgery in the middle-aged and older population in Denmark from 2000 to 2011. Acta Orthopaedica, 85(3), 287-292. https://doi.org/10.3109/17453674.2014.919558
Vera, M. C., Ferretti, J. L., Abdala, V., & Cointry, G. R. (2020). Biomechanical properties of anuran long bones: Correlations with locomotor modes and habitat use. Journal of Anatomy, 00, 1-14. https://doi.org/10.1111/joa.13161
Walker, P. S., & Eckman, M. J. (1975). The role of the menisci in force transmission across the knee. Clinical Orthopaedics and Related Research, 109, 184-192. https://doi.org/10.1097/00003086-197506000-00027