Diverse Fate of an Enigmatic Structure: 200 Years of Meckel's Cartilage

. 2020 ; 8 () : 821. [epub] 20200828

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid32984323

Meckel's cartilage was first described by the German anatomist Johann Friedrich Meckel the Younger in 1820 from his analysis of human embryos. Two hundred years after its discovery this paper follows the development and largely transient nature of the mammalian Meckel's cartilage, and its role in jaw development. Meckel's cartilage acts as a jaw support during early development, and a template for the later forming jaw bones. In mammals, its anterior domain links the two arms of the dentary together at the symphysis while the posterior domain ossifies to form two of the three ear ossicles of the middle ear. In between, Meckel's cartilage transforms to a ligament or disappears, subsumed by the growing dentary bone. Several human syndromes have been linked, directly or indirectly, to abnormal Meckel's cartilage formation. Herein, the evolution, development and fate of the cartilage and its impact on jaw development is mapped. The review focuses on developmental and cellular processes that shed light on the mechanisms behind the different fates of this cartilage, examining the control of Meckel's cartilage patterning, initiation and maturation. Importantly, human disorders and mouse models with disrupted Meckel's cartilage development are highlighted, in order to understand how changes in this cartilage impact on later development of the dentary and the craniofacial complex as a whole. Finally, the relative roles of tissue interactions, apoptosis, autophagy, macrophages and clast cells in the removal process are discussed. Meckel's cartilage is a unique and enigmatic structure, the development and function of which is starting to be understood but many interesting questions still remain.

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Ababneh K. T., Al-Khateeb T. H. (2009). Immunolocalization of proteoglycans in Meckel’s cartilage of the rat. Open Dent. J. 3 177–183. 10.2174/1874210600903010177 PubMed DOI PMC

Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E. N. (2002). Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129 4613–4625. PubMed

Aggarwal V. S., Carpenter C., Freyer L., Liao J., Petti M., Morrow B. E. (2010). Mesodermal Tbx1 is required for patterning the proximal mandible in mice. Dev. Biol. 344 669–681. 10.1016/j.ydbio.2010.05.496 PubMed DOI PMC

Amano K., Densmore M., Nishimura R., Lanske B. (2014). Indian hedgehog signaling regulates transcription and expression of collagen type X via Runx2/Smads interactions. J. Biol. Chem. 289 24898–24910. 10.1074/jbc.m114.570507 PubMed DOI PMC

Amano O., Doi T., Yamada T., Sasaki A., Sakiyama K., Kanegae H., et al. (2010). Meckel’s cartilage: discovery, embryology and evolution. J. Oral Biosci. 52 125–135. 10.2330/joralbiosci.52.125 DOI

Amin S., Matalova E., Simpson C., Yoshida H., Tucker A. S. (2007). Incudomalleal joint formation: the roles of apoptosis, migration and downregulation. BMC Dev. Biol. 7:134–146. 10.1186/1471-213X-7-134 PubMed DOI PMC

Amin S., Tucker A. S. (2006). Joint formation in the middle ear: lessons from the mouse and guinea pig. Dev. Dyn. 235 1326–1333. 10.1002/dvdy.20666 PubMed DOI

Anthwal N., Chai Y., Tucker A. S. (2008). The role of transforming growth factor B signalling in the patterning of the proximal processes of the murine dentary. Dev. Dyn. 237 1604–1613. 10.1002/dvdy.21567 PubMed DOI

Anthwal N., Fenelon J. C., Johnston S. D., Renfree M. B., Tucker A. S. (2020). Transient role of the middle ear as a jaw support in mammals. eLife 9:e57860. PubMed PMC

Anthwal N., Joshi L., Tucker A. S. (2013). Evolution of the mammalian middle ear and jaw: adaptations and novel structures. J. Anat. 222 147–160. 10.1111/j.1469-7580.2012.01526.x PubMed DOI PMC

Anthwal N., Urban D. J., Luo Z.-X., Sears K. E., Tucker A. S. (2017). Meckel’s cartilage breakdown offers clues to mammalian middle ear evolution. Nat. Ecol. Evol. 1:93. 10.1038/s41559-017-0093 PubMed DOI PMC

Arnott J. A., Lambi A. G., Mundy C., Hendesi H., Pixley R. A., Owen T. A., et al. (2011). The role of connective tissue growth factor (CTGF/CCN2) in skeletogenesis. Crit. Rev. Eukary. Gene Exp. 21 43–69. 10.1615/critreveukargeneexpr.v21.i1.40 PubMed DOI PMC

Bhaskar S. N., Weinmann J. P., Schour I. (1953). Role of Meckel’s cartilage in the development and growth of the rat mandible. J. Dent. Res. 32 398–410. 10.1177/00220345530320031401 PubMed DOI

Bi W., Huang W., Whitworth D. J., Deng J. M., Zhang Z., Behringer R. R., et al. (2001). Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc. Natl. Acad. Sci. 98 6698–6703. 10.1073/pnas.111092198 PubMed DOI PMC

Bildsoe H., Loebel D. A. F., Jones V. J., Hor A. C. C., Braithwaite A. W., Chen Y.-T., et al. (2013). The mesenchymal architecture of the cranial mesoderm of mouse embryos is disrupted by the loss of Twist1 function. Dev. Biol. 374 295–307. 10.1016/j.ydbio.2012.12.004 PubMed DOI PMC

Bilikova P., Svandova E., Vesela B., Doubek J., Poliard A., Matalova E. (2019). Coupling activation of pro-apoptotic caspases with autophagy in the Meckel’s cartilage. Physiol. Res. 68 135–140. 10.33549/physiolres.933947 PubMed DOI

Billmyre K. K., Klingensmith J. (2015). Sonic hedgehog from pharyngeal arch 1 epithelium is necessary for early mandibular arch cell survival and later cartilage condensation differentiation. Dev. Dyn. 244 564–576. 10.1002/dvdy.24256 PubMed DOI

Bohensky J., Shapiro I. M., Leshinsky S., Terkhorn S. P., Adams C. S., Srinivas V. (2014). HIF-1 regulation of chondrocyte apoptosis: induction of the autophagic pathway. Autophagy 3 207–214. 10.4161/auto.3708 PubMed DOI

Bonilla-Claudio M., Wang J., Bai Y., Klysik E., Selever J., Martin J. F. (2012). Bmp signaling regulates a dose-dependent transcriptional program to control facial skeletal development. Development 139 709–719. 10.1242/dev.073197 PubMed DOI PMC

Brazeau M. D., Friedman M. (2015). The origin and early phylogenetic history of jawed vertebrates. Nature 520 490–497. 10.1038/nature14438 PubMed DOI PMC

Carlevaro M. F., Cermelli S., Cancedda R., Descalzi Cancedda F. (2000). Vascular endothelial growth factor (VEGF) in cartilage neovascularization and chondrocyte differentiation: auto-paracrine role during endochondral bone formation. J. Cell Sci. 113 59–69. PubMed

Chai Y., Jiang X., Ito Y., Han J., Rowitch D. H., Soriano P., et al. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127 1671–1679. PubMed

Chai Y., Mah A., Crohin C., Groff S., Bringas P., Le T., et al. (1994). Specific transforming growth Factor-β subtypes regulate embryonic mouse Meckel’s cartilage and tooth development. Dev. Biol. 162 85–103. 10.1006/dbio.1994.1069 PubMed DOI

Chai Y., Shuler C., Devaney E., Grosschedl R., Slavkin H. C. (1998). A mouse mandibular culture model permits the study of neural crest cell migration and tooth development. Int. J. Dev. Biol. 42 87–94. PubMed

Chen G., Isham M., Yang J., Kishigami S., Fukada T., Scott G., et al. (2017). Specific and spatial labelling of P0-cre versus Wnt-1Cre in cranial neural crest in early mouse embryos. Genesis 55:10.1002/dvg.23034. 10.1002/dvg.23034 PubMed DOI PMC

Cheynet F., Guyot L., Richard O., Layoun W., Gola R. (2003). Discomallear and malleomandibular ligaments: anatomical study and clinical applications. Surg. Radiol. Anat. 25 152–157. 10.1007/s00276-003-0097-y PubMed DOI

Cruz C. V., Mattos C. T., Maia J. C., Granjeiro J. M., Reis M. F., Mucha J. N., et al. (2017). Genetics polymorphisms underlying the skeletal Class III phenotype. Am. J. Orthod. Dentofacial Orthop. 151 700–707. 10.1016/j.ajodo.2016.09.013 PubMed DOI

Davideau J.-L., Demri P., Hotton D., Gu T.-T., MacDougall M., Sharpe P., et al. (1999). Comparative study of MSX-2, DLX-5, and DLX-7 gene expression during early human tooth development. Pediatr. Res. 46 650–650. 10.1203/00006450-199912000-00015 PubMed DOI

DeLaurier A. (2019). Evolution and development of the fish jaw skeleton. Wiley Interdiscip. Rev. Dev. Biol. 8:e337. 10.1002/wdev.337 PubMed DOI PMC

Denker A. E., Haas A. R., Nicoll S. B., Tuan R. S. (1999). Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64 67–76. 10.1046/j.1432-0436.1999.6420067.x PubMed DOI

Depew M. J., Liu J. K., Long J. E., Presley R., Meneses J. J., Pedersen R. A., et al. (1999). Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126 3831–3846. PubMed

Depew M. J., Simpson C. A., Morasso M., Rubenstein J. L. R. (2005). Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J. Anat. 207 501–561. 10.1111/j.1469-7580.2005.00487.x PubMed DOI PMC

Depew M. J., Tucker A. S., Sharpe P. T. (2002). “Craniofacial development,” in Mouse Development: Patterning, Morphogenesis and Organogenesis, eds Rossant J., Tam P. P. L. (London: Academic Press; ), 421–498.

Ding M., Lu Y., Abbassi S., Li F., Li X., Song Y., et al. (2012). Targeting Runx2 expression in hypertrophic chondrocytes impairs endochondral ossification during early skeletal development. J. Cell. Physiol. 227 3446–3456. 10.1002/jcp.24045 PubMed DOI PMC

Donoghue P. C. J., Sansom I. J., Downs J. P. (2006). Early evolution of vertebrate skeletal tissues and cellular interactions, and the Canalization of skeletal development. J. Exp. Zool. Part B Mol. Dev. Evol. 306B 278–296. PubMed

Dudas M., Sridurongrit S., Nagy A., Okazaki K., Kaartinen V. (2004). Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mechan. Dev. 121 173–182. 10.1016/j.mod.2003.12.003 PubMed DOI

Duplan M., Komla-Ebri D., Heuzé Y., Estibals V., Gaudas E., Kaci N., et al. (2016). Meckel’s and condylar cartilages anomalies in achondroplasia result in defective development and growth of the mandible. Hum. Mol. Genet. 25 2997–3010. PubMed PMC

Eames B. F., Sharpe P. T., Helms J. A. (2004). Hierarchy revealed in the specification of three skeletal fates by Sox9 and Runx2. Dev. Biol. 274 188–200. 10.1016/j.ydbio.2004.07.006 PubMed DOI

Frommer J., Margolies M. R. (1971). Contribution of Meckel’s cartilage to ossification of the mandible in mice. J. Dent. Res. 50 1260–1267. 10.1177/00220345710500052801 PubMed DOI

Funato N., Kokubo H., Nakamura M., Yanagisawa H., Saga Y. (2016). Specification of jaw identity by the Hand2 transcription factor. Sci. Rep. 22:28405. PubMed PMC

Funato N., Nakamura M., Richardson J. A., Srivastava D., Yanagisawa H. (2015). Loss of Tbx1 induces bone phenotypes similar to cleidocranial dysplasia. Hum. Mol. Genet. 24 424–435. 10.1093/hmg/ddu458 PubMed DOI

Goret-Nicaise M., Lengele B., Dhem A. (1984). The function of Meckel’s and secondary cartilages in the histomorphogenesis of the cat mandibular symphysis. Arch. Anat. Microsc. Morphol. Exp. 73 291–303. PubMed

Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A. N., Kwiatkowski W., et al. (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420 636–642. 10.1038/nature01245 PubMed DOI

Harada Y., Ishizeki K. (1998). Evidence for transformation of chondrocytes and site-specific resorption during the degradation of Meckel’s cartilage. Anat. Embryol. 197 439–450. 10.1007/s004290050155 PubMed DOI

Herring S. W. (1993). Formation of the vertebrate face: epigenetic and functional influences. Am. Zool. 33 472–483. 10.1093/icb/33.4.472 PubMed DOI

Hunt P., Gulisano M., Cook M., Sham M.-H., Faiella A., Wilkinson D., et al. (1991). A distinct Hox code for the branchial region of the vertebrate head. Nature 353 861–864. 10.1038/353861a0 PubMed DOI

Ishizeki K. (2012). Imaging analysis of osteogenic transformation of Meckel’s chondrocytes from green fluorescent protein-transgenic mice during intrasplenic transplantation. Acta Histochem. 114 608–619. 10.1016/j.acthis.2011.11.008 PubMed DOI

Ishizeki K., Kagiya T., Fujiwara N., Otsu K., Harada H. (2009). Expression of osteogenic proteins during the intrasplenic transplantation of Meckel’s chondrocytes: a histochemical and immunohistochemical study. Arch. Histol. Cytol. 72 1–12. 10.1679/aohc.72.1 PubMed DOI

Ishizeki K., Nawa T., Takigawa M., Suzuki F. (1996). Mouse Meckel’s cartilage chondrocytes evoke bone-like matrix and further transform into osteocyte-like cells in culture. Anat. Rec. 245 25–35. 10.1002/(sici)1097-0185(199605)245:1<25::aid-ar5>3.0.co;2-e PubMed DOI

Ishizeki K., Saito H., Shinagawa T., Fujiwara N., Nawa T. (1999). Histochemical and immunohistochemical analysis of the mechanism of calcification of Meckel’s cartilage during mandible development in rodents. J. Anat. 194 265–277. 10.1046/j.1469-7580.1999.19420265.x PubMed DOI PMC

Ishizeki K., Takahashi N., Nawa T. (2001). Formation of the sphenomandibular ligament by Meckel’s cartilage in the mouse: possible involvement of epidermal growth factor as revealed by studies in vivo and in vitro. Cell Tiss. Res. 304 67–80. 10.1007/s004410100354 PubMed DOI

Ito Y., Bringas P., Mogharei A., Zhao J., Deng C., Chai Y. (2002). Receptor-regulated and inhibitory Smads are critical in regulating transforming growth factor β-mediated Meckel’s cartilage development. Dev. Dyn. 224 69–78. 10.1002/dvdy.10088 PubMed DOI

Ivkovic S., Yoon B. S., Popoff S. N., Safadi F. F., Libuda D. E., Stephenson R. C., et al. (2003). Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130 2779–2791. 10.1242/dev.00505 PubMed DOI PMC

Jeong J., Mao J., Tenzen T., Kottmann A. H., McMahon A. P. (2004). Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev. 18 937–951 10.1101/gad.1190304 PubMed DOI PMC

Kaback L. A., Soung D. Y., Naik A., Smith N., Schwarz E. M., O’Keefe R. J., et al. (2008). Osterix/Sp7 regulates mesenchymal stem cell mediated endochondral ossification. J. Cell. Physiol. 214 173–182. 10.1002/jcp.21176 PubMed DOI

Kaucka M., Zikmund T., Tesarova M., Gyllborg D., Hellander A., Jaros J., et al. (2017). Orientated clinal cell dynamics enables accurate growth and shaping of vertebrate cartilage. eLife 6:e25902. PubMed PMC

Keith A. (1910). Abnormal ossification of Meckel’s cartilage. J. Anat. Physiol. 44 151–152. PubMed PMC

Kobayashi T., Lyons K. M., McMahon A. P., Kronenberg H. M. (2005). BMP signaling stimulates cellular differentiation at multiple steps during cartilage development. Proc. Natl. Acad. Sci. U.S.A. 102 18023–18027. 10.1073/pnas.0503617102 PubMed DOI PMC

Koyama E., Leatherman J. L., Noji S., Pacifici M. (1996). Early chick limb cartilaginous elements possess polarizing activity and express hedgehog-related morphogenetic factors. Dev. Dyn. 207 344–354. PubMed

Le Douarin N. M., Dupin E. (1993). Cell lineage analysis in neural crest ontogeny. J. Neurobiol. 24 146–161. 10.1002/neu.480240203 PubMed DOI

Lei R., Zhang K., Liu K., Shao X., Ding Z., Wang F., et al. (2016). Transferrin receptor facilitates TGFb and BMP signaling activation to control craniofacial morphogenesis. Cell Death Dis. 7:e2282. 10.1038/cddis.2016.170 PubMed DOI PMC

Li F., Fu G., Liu Y., Miao X., Li Y., Yang X., et al. (2017). ISLET1-dependent β-Catenin/Hedgehog signaling is required for outgrowth of the lower jaw. Mol. Cell. Biol. 37:e00590-16. 10.1128/MCB.00590-16 PubMed DOI PMC

Liu W., Selever J., Murali D., Sun X., Brugger S. M., Ma L., et al. (2005). Threshold-specific requirements for Bmp4 in mandibular development. Dev. Biol. 283 282–293. 10.1016/j.ydbio.2005.04.019 PubMed DOI

Luo P., Gao F., Niu D., Sun X., Song Q., Guo C., et al. (2019). The role of autophagy in chondrocyte metabolism and osteoarthritis: a comprehensive research review. Biomed. Res. Int. 2019:5171602. 10.1155/2019/5171602 PubMed DOI PMC

Luo Z.-X. (2011). Developmental patterns in Mesozoic evolution of mammal ears. Annu. Rev. Ecol. Evol. Syst. 42 355–380. 10.1146/annurev-ecolsys-032511-142302 DOI

Luo Z.-X., Gatesy S. M., Jenkins F. A., Amaral W. W., Shubin N. H. (2015). Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution. Proc. Natl Acad. Sci. U.S.A. 112 E7101–E7109. PubMed PMC

Maier W., Ruf I. (2016). Evolution of the mammalian middle ear: a historical review. J. Anat. 228 270–283. 10.1111/joa.12379 PubMed DOI PMC

Malemud C. J. (2006). Matrix metalloproteinases: role in skeletal development and growth plate disorders. Front. Biosci. 11:1702–1715. 10.2741/1916 PubMed DOI

Mallat J. (2008). The evolution of the vertebrate Jaw: neoclassical ideas verses newer, development-based ideas. Zool. Sci. 25 990–998. 10.2108/zsj.25.990 PubMed DOI

Manocha S., Farokhnia N., Khosropanah S., Bertol J. W., Santiago Junior J., Fakhouri W. D. (2019). Systematic review of hormonal and genetic factors involved in the non-syndromic disorders of the lower jaw. Dev. Dyn. 248 162–172. 10.1002/dvdy.8 PubMed DOI

Mansour S., Offiah A. C., McDowall S., Sim P., Tolmie J., Hall C. (2002). The phenotype of survivors of campomelic dysplasia. J. Med. Genet. 39 597–602. 10.1136/jmg.39.8.597 PubMed DOI PMC

Mao F., Hu Y., Li C., Wang Y., Chase M. H., Smith A. K., et al. (2020). Integrated hearing and chewing modules decoupled in a Cretaceous stem therian mammal. Science 367 305–308. 10.1126/science.aay9220 PubMed DOI

Marchant C., Anderson P., Schwarz Q., Wisziak S. (2020). Vessel-derived angiocrine IGF1 promotes Meckel’s cartilage proliferation to drive jaw growth during embryogenesis. Development 147:dev190488. 10.1242/dev.190488 PubMed DOI PMC

Mckenzie J. (1958). The first arch syndrome. Arch. Dis. Child 33 477–486. PubMed PMC

Meckel J. F. (1820). Handbuch der menschlichen Anatomie. IV. Berlin: Lehre und Geschichte des Foetud.

Melnick M., Witcher D., Bringas P., Jr., Carlsson P., Jaskoll T. (2005). Meckel’s cartilage differentiation is dependent on hedgehog signaling. Cells Tissues Organs 179 146–157. 10.1159/000085950 PubMed DOI

Meng J., Hu Y., Wang Y., Li C. (2003). The ossified Meckel’s cartilage and internal groove in Mesozoic mammaliaforms: implications to origin of the definitive mammalian middle ear. Zool. J. Linn. Soc. 138 431–448. 10.1046/j.1096-3642.2003.00064.x DOI

Meng J., Wang Y., Li C. (2011). Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472 181–185. 10.1038/nature09921 PubMed DOI

Michigami T. (2014). Current understanding on the molecular basis of chondrogenesis. Clin. Pediatr. Endocrinol. 23, 1–8. PubMed PMC

Miettinen P. J., Chin J. R., Shum L., Slavkin H. C., Shuler C. F., Derynck R., et al. (1999). Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nat. Genet. 22 69–73. 10.1038/8773 PubMed DOI

Mikasa M., Rokutanda S., Komori H., Ito K., Tsang Y. S., Date Y., et al. (2011). Regulation of Tcf7 by Runx2 in chondrocyte maturation and proliferation. J. Bone Miner. Metab. 29 291–299. 10.1007/s00774-010-0222-z PubMed DOI

Mina M., Havens B. (2007). FGF signaling in mandibular skeletogenesis. Orthodont. Craniofac. Res. 10 59–66. 10.1111/j.1601-6343.2007.00385.x PubMed DOI

Miyashita T. (2016). Fishing for jaws in early vertebrate evolution: a new hypothesis of mandibular confinement. Biol. Rev. 91 611–657. 10.1111/brv.12187 PubMed DOI

Mori-Akiyama Y., Akiyama H., Rowitch D. H., de Crombrugghe B. (2003). Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc. Natl. Acad. Sci. U.S.A. 100 9360–9365. 10.1073/pnas.1631288100 PubMed DOI PMC

Murray S. A., Oram K. F., Gridley T. (2007). Multiple functions of Snail family genes during palate development in mice. Development 134 1789–1797. 10.1242/dev.02837 PubMed DOI

Nakamura T., Aikawa T., Iwamoto-Enomoto M., Iwamoto M., Higuchi Y., Maurizio P., et al. (1997). Induction of osteogenic differentiation by hedgehog proteins. Biochem. Biophys. Res. Commun. 237 465–469. 10.1006/bbrc.1997.7156 PubMed DOI

Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J. M., Behringer R. R., et al. (2002). The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108 17–29. 10.1016/s0092-8674(01)00622-5 PubMed DOI

Nishimura R., Wakabayashi M., Hata K., Matsubara T., Honma S., Wakisaka S., et al. (2012). Osterix regulates calcification and degradation of chondrogenic matrices through matrix metalloproteinase 13 (MMP13) expression in association with transcription factor Runx2 during endochondral ossification. J. Biol. Chem. 287 33179–33190. 10.1074/jbc.m111.337063 PubMed DOI PMC

Ogutcen-Toller M. (1995). The morphogenesis of the human discomalleolar and sphenomandibular ligaments. J. Craniomaxillofac. Surg. 23 42–46. 10.1016/s1010-5182(05)80254-9 PubMed DOI

Oka K., Oka S., Sasaki T., Ito Y., Bringas P., Nonaka K., et al. (2007). The role of TGF-β signaling in regulating chondrogenesis and osteogenesis during mandibular development. Dev. Biol. 303 391–404. 10.1016/j.ydbio.2006.11.025 PubMed DOI PMC

Ozeki H., Kurihara Y., Tonami K., Watatani S., Kurihara H. (2004). Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mech. Dev. 121 387–395. 10.1016/j.mod.2004.02.002 PubMed DOI

Parada C., Li J., Iwata J., Suzuki A., Chai Y. (2013). CTGF mediates smad-dependent transforming growth Factor β signalingto regulate mesenchymal cell proliferation during palate development. Mol. Cell. Biol. 33 3482–3493. 10.1128/mcb.00615-13 PubMed DOI PMC

Pron G., Galloway C., Armstrong D., Posnick J. (1993). Ear malformation and hearing loss in patients with treacher collins syndrome. Cleft Palate Craniofac. J. 30 97–103. 10.1597/1545-1569_1993_030_0097_emahli_2.3.co_2 PubMed DOI

Ramaesh T., Bard J. B. L. (2003). The growth and morphogenesis of the early mouse mandible: a quantitative analysis. J. Anat. 203 213–222. 10.1046/j.1469-7580.2003.00210.x PubMed DOI PMC

Reid B. S., Yang H., Melvin V. S., Taketo M. M., Williams T. (2011). Ectodermal WNT/β-catenin signaling shapes the mouse face. Dev. Biol. 349 261–269. 10.1016/j.ydbio.2010.11.012 PubMed DOI PMC

Richman J. M., Diewert V. M. (1988). The fate of Meckel’s cartilage chondrocytes in ocular culture. Dev. Biol. 129 48–60. 10.1016/0012-1606(88)90160-1 PubMed DOI

Ricks J. E., Ryder V. M., Bridgewater L. C., Schaalje B., Seegmiller R. E. (2002). Altered mandibular development precedes the time of palate closure in mice homozygous for disproportionate micromelia: an oral clefting model supporting the Pierre-Robin sequence. Teratology 65 116–120. 10.1002/tera.10022 PubMed DOI

Robledo R. F., Rajan L., Li X., Lufkin T. (2002). The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev. 16 1089–1101. 10.1101/gad.988402 PubMed DOI PMC

Rodriguez-Vazquez J. F., Merida-Velasco J. R., Merida-Velasco J. A., Sanchez-Montesinos I., Espin-Ferra J., Jimenez-Collado J. (1997). Development of Meckel’s cartilage in the symphyseal region in man. Anat. Rec. 249 249–254. 10.1002/(sici)1097-0185(199710)249:2<249::aid-ar12>3.0.co;2-o PubMed DOI

Ruest L. B., Clouthier D. E. (2009). Elucidating timing and function of endothelin-A receptor signaling during craniofacial development using neural crest cell-specific gene deletion and receptor antagonism. Dev. Biol. 328 94–108. 10.1016/j.ydbio.2009.01.005 PubMed DOI PMC

Sakakura Y., Hosokawa Y., Tsuruga E., Irie K., Yajima T. (2007). In situ localization of gelatinolytic activity during development and resorption of Meckel’s cartilage in mice. Eur. J. Oral Sci. 115 212–223. 10.1111/j.1600-0722.2007.00447.x PubMed DOI

Sakakura Y., Tsuruga E., Irie K., Hosokawa Y., Nakamura H., Yajima T. (2005). Immunolocalization of receptor activator of nuclear factor-kappaB ligand (RANKL) and osteoprotegerin (OPG) in Meckel’s cartilage compared with developing endochondral bones in mice. J. Anat. 207 325–337. 10.1111/j.1469-7580.2005.00466.x PubMed DOI PMC

Sanford L. P., Ormsby I., Sariola H., Friedman R., Boivin G. P., Cardell E. L., et al. (1997). TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124 2659–2670. PubMed PMC

Sato T., Kurihara Y., Asai R., Kawamura Y., Tonami K., Uchijima Y., et al. (2008). An endothelin-1 switch specifies maxillomandibular identity. Proc. Natl. Acad. Sci. U.S.A. 105 18806–18811. 10.1073/pnas.0807345105 PubMed DOI PMC

Savostin-Asling I., Asling C. W. (1975). Transmission and scanning electron microscope studies of calcified cartilage resorption. Anat. Rec. 183 373–391. 10.1002/ar.1091830303 PubMed DOI

Shibata S., Sakamoto Y., Baba O., Qin C., Murakami G., Cho B. H. (2013). An immunohistochemical study of matrix proteins in the craniofacial cartilage in midterm human fetuses. Eur. J. Histochem. 57:e39. 10.4081/ejh.2013.e39 PubMed DOI PMC

Shibata S., Suda N., Yoda S., Fukuoka H., Ohyama K., Yamashita Y., et al. (2004). Runx2-deficient mice lack mandibular condylar cartilage and have deformed Meckel’s cartilage. Anat. Embryol. 208 273–280. PubMed

Shibata S., Takahashi M., Fujikawa K. (2019). Histochemical and ultrastructural study of the developing gonial bone with evidence to intial ossification of the malleus and reduction of Meckel’s cartilage in mice. Anat. Rec. 302 1916–1933. 10.1002/ar.24201 PubMed DOI

Shimada K., Nakajima A., Ikeda K., Ishibashi K., Shimizu N., Ito K. (2011). CD47 regulates the TGF-β signaling pathway in osteoblasts and is distributed in Meckel’s cartilage. J. Oral Sci. 53 169–175. 10.2334/josnusd.53.169 PubMed DOI

Shimada M., Yamamoto M., Wakayama T., Iseki S., Amano O. (2003). Different expression of 25-kDa heat-shock protein (Hsp25) in Meckel’s cartilage compared with other cartilages in the mouse. Anat. Embryol. 206 163–173. 10.1007/s00429-002-0297-y PubMed DOI

Shimo T., Kanyama M., Wu C., Sugito H., Billings P. C., Abrams W. R., et al. (2004). Expression and roles of connective tissue growth factor in Meckel’s cartilage development. Dev. Dyn. 231 136–147. 10.1002/dvdy.20109 PubMed DOI

Silbermann M., von der Mark K. (1990). An immunohistochemical study of the distribution of matrical proteins in the mandibular condyle of neonatal mice. I. Collagens. J. Anat. 170 11–22. PubMed PMC

Song B., Song H., Wang W., Wang H., Peng H., Cui J., et al. (2017). Beclin 1 overexpression inhibits chondrocyte apoptosis and downregulates extracellular matrix metabolism in osteoarthritis. Mol. Med. Rep. 16 3958–3964. 10.3892/mmr.2017.7064 PubMed DOI PMC

Takahashi K., Nuckolls G. H., Takahashi I., Nonaka K., Nagata M., Ikura T., et al. (2001). Msx2 is a repressor of chondrogenic differentiation in migratory cranial neural crest cells. Dev. Dyn. 222 252–262. PubMed

Terao F., Takahashi I., Mitani H., Haruyama N., Sasano Y., Suzuki O., et al. (2011). Fibroblast growth factor 10 regulates Meckel’s cartilage formation during early mandibular morphogenesis in rats. Dev. Biol. 350 337–347. PubMed

Teshima T. H. N., Lourenco S. V., Tucker A. S. (2016). Multiple cranial organ defects after conditionally knocking out Fgf10 in the neural crest. Front. Physiol. 7:488. 10.3389/fphys.2016.00488 PubMed DOI PMC

Trichilis A., Wroblewski J. (1997). Expression of p53 and hsp70 in relation to apoptosis during Meckel’s cartilage development in the mouse. Anat. Embryol. 196 107–113. PubMed

Tsuzurahara F., Soeta S., Kawawa T., Baba K., Nakamura M. (2011). The role of macrophages in the disappearance of Meckel’s cartilage during mandibular development in mice. ActaHistochemica 113 194–200. PubMed

Tucker A. S., Watson R. P., Lettice L. A., Yamada G., Hill R. E. (2004). Bapx1 regulates patterning in the middle ear: altered regulatory role in the transition from the proxial jaw during vertebrate evolution. Development 131 1235–1245. PubMed

Urban D. J., Anthwal N., Luo Z.-X., Maier J. A., Sadier A., Tucker A. S., et al. (2017). A new developmental mechanism for the separation of the mammalian middle ear ossicles from the jaw. Proc. R. Soc. B Biol. Sci. 284:20162416. 10.1098/rspb.2016.2416 PubMed DOI PMC

Valcourt U., Gouttenoire J., Moustakas A., Herbage D., Mallein-Gerin F. (2002). Functions of transforming growth factor-β family Type I receptors and smad proteins in the hypertrophic maturation and osteoblastic differentiation of chondrocytes. J. Biol. Chem. 277 33545–33558. PubMed

Vu T. H., Shipley J. M., Bergers G., Berger J. E., Helms J. A., Hanahan D., et al. (1998). MMP-9/Gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93 411–422. PubMed PMC

Wang Y., Zheng Y., Chen D., Chen Y. P. (2013). Enhanced BMP signaling prevents degeneration and leads to endochondral ossification of Meckel’s cartilage in mice. Dev. Biol. 381 301–311. PubMed PMC

Wilson J., Tucker A. S. (2004). Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev. Biol. 266 138–150. PubMed

Wiszniak S., Mackenzie F. E., Anderson P., Kabbara S., Ruhrberg C., Schwarz Q. (2015). Neural crest cell-derived VEGF promotes embryonic jaw extension. Proc. Natl. Acad. Sci. U.S.A. 112 6086–6091. PubMed PMC

Woronowicz K. C., Schneider R. A. (2019). Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw. Evodevo 10:17. 10.1186/s13227-019-0131-8 PubMed DOI PMC

Wyganowska-Swiątkowska M., Przystanska A. (2011). The Meckel’s cartilage in human embryonic and early fetal periods. Anat. Sci. Int. 86 98–107. PubMed

Yahiro K., Higashihori N., Moriyama K. (2017). Histone methyltransferase Setdb1 is indispensable for Meckel’s cartilage development. Biochem. Biophys. Res. Commun. 482 883–888. PubMed

Yamashita S., Andoh M., Ueno-Kudoh H., Sato T., Miyaki S., Asahara H. (2009). Sox9 directly promotes Bapx1 gene expression to repress Runx2 in chondrocytes. Exp. Cell Res. 315 2231–2240. PubMed PMC

Yanagisawa H., Kapur R. P., Richardson J. A., Williams S. C., Clouthier D. E., Wit D., et al. (1998). Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 125 825–836. PubMed

Yang L., Tsang K. Y., Tang H. C., Chan D., Cheah K. S. (2014). Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc. Natl. Acad. Sci. U.S.A. 111 12097–12102. PubMed PMC

Yang R.-T., Zhang C., Liu Y., Zhou H.-H., Li Z.-B. (2012). Autophagy prior to chondrocyte cell death during the degeneration of Meckel’s cartilage. Anat. Rec. 295 734–741. PubMed

Yoon B. S., Ovchinnikov D. A., Yoshii I., Mishina Y., Behringer R. R., Lyons K. M. (2005). Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc. Natl. Acad. Sci. 102 5062–5067. PubMed PMC

Zehentner B. K., Dony C., Burtscher H. (1999). The transcription factor Sox9 is involved in BMP-2 signaling. J. Bone Mineral Res. 14 1734–1741. PubMed

Zelzer E., Mamluk R., Ferrara N., Johnson R. S., Schipani E., Olsen B. R. (2004). VEGFA is necessary for chondrocyte survival during bone development. Development 131 2161–2171. PubMed

Zhang H., Zhao X., Zhang Z., Chen W., Zhang X. (2013). An Immunohistochemistry Study of Sox9, Runx2, and osterix expression in the mandibular cartilages of newborn mouse. BioMed. Res. Int. 2013 1–11. PubMed PMC

Zhang Z., Wlodarczyk B. J., Niederreither K., Venugopalan S., Florez S., Finnell R. H., et al. (2011). Fuz regulates craniofacial development through tissue specific responses to signaling factors. PLoS One 6:e24608. 10.1371/journal.pone.0024608 PubMed DOI PMC

Zimmerman L. B., De Jesús-Escobar J. M., Harland R. M. (1996). The spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86 599–606. PubMed

Zou L., Zou X., Li H., Mygind T., Zeng Y., Lü N., et al. (2006). Molecular mechanism of osteochondroprogenitor fate determination during bone formation. Adv. Exp. Med. Biol. 585 431–441. PubMed

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