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Micrognathia is a severe craniofacial deformity affecting appearance and survival. Previous studies revealed that multiple factors involved in the osteogenesis of mandibular bone have contributed to micrognathia, but concerned little on factors other than osteogenesis. In the current study, we found that ectopic activation of Fgf8 by Osr2-cre in the presumptive mesenchyme for masseter tendon in mice led to micrognathia, masseter regression, and the disrupted patterning and differentiation of masseter tendon. Since Myf5-cre;Rosa26R-Fgf8 mice exhibited the normal masseter and mandibular bone, the possibility that the micrognathia and masseter regression resulted directly from the over-expressed Fgf8 was excluded. Further investigation disclosed that a series of chondrogenic markers were ectopically activated in the developing Osr2-cre;Rosa26R-Fgf8 masseter tendon, while the mechanical sensing in the masseter and mandibular bone was obviously reduced. Thus, it suggested that the micrognathia in Osr2-cre;Rosa26R-Fgf8 mice resulted secondarily from the reduced mechanical force transmitted to mandibular bone. Consistently, when tenogenic or myogenic components were deleted from the developing mandibles, both the micrognathia and masseter degeneration took place with the decreased mechanical sensing in mandibular bone, which verified that the loss of mechanical force transmitted by masseter tendon could result in micrognathia. Furthermore, it appeared that the micrognathia resulting from the disrupted tenogenesis was attributed to the impaired osteogenic specification, instead of the differentiation in the periosteal progenitors. Our findings disclose a novel mechanism for mandibular morphogenesis, and shed light on the prevention and treatment for micrognathia.
Neuschulz, J., Wilhelm, L., Christ, H. & Braumann, B. Prenatal indices for mandibular retrognathia/micrognathia. J. Orofac. Orthop. 76, 30–40 (2015).
Kruse, T., Neuschulz, J., Wilhelm, L., Ritgen, J. & Braumann, B. Prenatal diagnosis of robin sequence: sensitivity, specificity, and clinical relevance of an index for micrognathia. Cleft. Palate Craniofac. J. 58, 1012–1019 (2021).
Logjes, R. J. H. et al. The ontogeny of Robin sequence. Am. J. Med. Genet. A 176, 1349–1368 (2018).
Hsieh, S. T. & Woo, A. S. Pierre Robin Sequence. Clin. Plast. Surg. 46, 249–259 (2019).
Izumi, K., Konczal, L., Mitchell, A. L. & Jones, M. C. Underlying genetic diagnosis of Pierre Robin sequence: retrospective chart review at two children’s hospitals and a systematic literature review. J. Pediatr. 160, 645–650 (2012).
Gomez-Ospina, N. & Bernstein, J. A. Clinical, cytogenic, and molecular outcomes in a series of 66 patients with Pierre Robin sequence and literature review: 22q11.2 deletion is less common than other chromosomal anomalies. Am. J. Med. Genet. 170A, 870–880 (2016).
Karempelis, P., Hagen, M., Morrell, N. & Roby, B. B. Associated syndromes in patients with Pierre Robin Sequence. Int. J. Pediatr. Otorhinolaryngol. 131, 109842 (2020).
Rosa, R. F. et al. Nager syndrome and Pierre Robin sequence. Pediatr. Int. 57, e69–e72 (2015).
Sakai, D., Dixon, J., Achilleos, A., Dixon, M. & Trainor, P. A. Prevention of Treacher Collins syndrome craniofacial anomalies in mouse models via maternal antioxidant supplementation. Nat. Commun. 7, 10328 (2016).
Morrow, B. E., McDonald-McGinn, D. M., Emanuel, B. S., Vermeesch, J. R. & Scambler, P. J. Molecular genetics of 22q11.2 deletion syndrome. Am. J. Med. Genet. A 176, 2070–2081 (2018).
Boothe, M., Morris, R. & Robin, N. Stickler Syndrome: a review of clinical manifestations and the genetics evaluation. J. Pers. Med. 10, 105 (2020).
Trang, H., Bourgeois, P. & Cheliout-Heraut, F. Neurocognition in congenital central hypoventilation syndrome: influence of genotype and ventilation method. Orphanet. J. Rare. Dis. 15, 322 (2020).
Bhatt, S., Diaz, R. & Trainor, P. A. Signals and switches in Mammalian neural crest cell differentiation. Cold. Spring Harb. Perspect. Biol. 5, a008326 (2013).
Dash, S. & Trainor, P. A. The development, patterning and evolution of neural crest cell differentiation into cartilage and bone. Bone 137, 115409 (2020).
Depew, M. J., Lufkin, T. & Rubenstein, J. L. Specification of jaw subdivisions by Dlx genes. Science 298, 381–385 (2002).
Ozeki, H., Kurihara, Y., Tonami, K., Watatani, S. & Kurihara, H. Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mech. Dev. 121, 387–395 (2004).
Depew, M. J., Simpson, C. A., Morasso, M. & Rubenstein, J. L. R. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J. Anat. 207, 501–561 (2005).
Sato, T. et al. An endothelin-1 switch specifies maxillomandibular identity. Proc. Natl Acad. Sci. USA 105, 18806–18811 (2008).
Funato, N., Kokubo, H., Nakamura, M., Yanagisawa, H. & Saga, Y. Specification of jaw identity by the Hand2 transcription factor. Sci. Rep. 6, 28405 (2016).
Beverdam, A. et al. Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis 34, 221–227 (2002).
Parada, C. & Chai, Y. Mandible and tongue development. Curr. Top. Dev. Biol. 115, 31–58 (2015).
Barbosa, A. C. et al. Hand transcription factors cooperatively regulate development of the distal midline mesenchyme. Dev. Biol. 310, 154–168 (2007).
Funato, N. et al. Hand2 controls osteoblast differentiation in the branchial arch by inhibiting DNA binding of Runx2. Development 136, 615–625 (2009).
Tavares, A. L. P. et al. Ectodermal-derived Endothelin1 is required for patterning the distal and intermediate domains of the mouse mandibular arch. Dev. Biol. 371, 47–56 (2012).
Shimo, T. et al. Expression and roles of connective tissue growth factor in Meckel’s cartilage development. Dev. Dyn. 231, 136–147 (2004).
Mori-Akiyama, Y., Akiyama, H., Rowitch, D. H. & de Crombrugghe, B. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc. Natl Acad. Sci. USA 100, 9360–9365 (2003).
Parada, C., Li, J., Iwata, J., Suzuki, A. & Chai, Y. CTGF mediates Smad-dependent transforming growth factor β signaling to regulate mesenchymal cell proliferation during palate development. Mol. Cel. Biol. 33, 3482–3493 (2013).
Newbern, J. et al. Mouse and human phenotypes indicate a critical conserved role for ERK2 signaling in neural crest development. Proc. Natl Acad. Sci. USA 105, 17115–17120 (2008).
Song, Z. et al. Mice with Tak1 deficiency in neural crest lineage exhibit cleft palate associated with abnormal tongue development. J. Biol. Chem. 288, 10440–10450 (2013).
Parada, C. et al. Disruption of the ERK/MAPK pathway in neural crest cells as a potential cause of Pierre Robin sequence. Development 142, 3734–3745 (2015).
Tan, T. Y., Kilpatrick, N. & Farlie, P. G. Developmental and genetic perspectives on Pierre Robin sequence. Am. J. Med. Genet. C. Semin. Med. Genet. 163, 295–305 (2013).
Rot-Nikcevic, I. et al. Myf5-/-;MyoD-/- amyogenic fetuses reveal the importance of early contraction and static loading by striated muscle in mouse skeletogenesis. Dev. Genes Evol. 216, 1–9 (2006).
Rot, I., Mardesic-Brakus, S., Costain, W. J., Saraga-Babic, M. & Kablar, B. Role of skeletal muscle in mandible development. Histol. Histopathol. 29, 1377–1394 (2014).
Gomez, C. et al. Absence of mechanical loading in utero influences bone mass and architecture but not innervation in Myod-Myf5-deficient mice. J. Anat. 210, 259–271 (2007).
Sharir, A., Stern, T., Rot, C., Shahar, R. & Zelzer, E. Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis. Development 138, 3247–3259 (2011).
Rolfe, R. A. et al. Abnormal fetal muscle forces result in defects in spinal curvature and alterations in vertebral segmentation and shape. J. Orthop. Res. 35, 2135–2144 (2017).
Yamamoto, M. et al. Morphological association between the muscles and bones in the craniofacial region. PLoS ONE 15, e0227301 (2020).
Blitz, E. et al. Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Dev. Cell. 17, 861–873 (2009).
Nassari, S., Duprez, D. & Fournier-Thibault, C. Non-myogenic contribution to muscle development and homeostasis: the role of connective tissues. Front. Cell. Dev. Biol. 5, 22 (2017).
Eloy-Trinquet, S., Wang, H., Edom-Vovard, F. & Duprez, D. Fgf signaling components are associated with muscles and tendons during limb development. Dev. Dyn. 238, 1195–1206 (2009).
Edom-Vovard, F., Schuler, B., Bonnin, M. A., Teillet, M. A. & Duprez, D. Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev. Biol. 247, 351–366 (2002).
Shao, M. et al. FGF8 signaling sustains progenitor status and multipotency of cranial neural crest-derived mesenchymal cells in vivo and in vitro. J. Mol. Cell. Biol. 7, 441–454 (2015).
Xu, J. et al. FGF8 signaling alters the osteogenic cell fate in the hard palate. J. Dent. Res. 97, 589–596 (2018).
Schmidt, L., Taiyab, A., Melvin, V. S., Jones, K. L. & Williams, T. Increased FGF8 signaling promotes chondrogenic rather than osteogenic development in the embryonic skull. Dis. Model. Mech. 11, dmm031526 (2018).
Salazar, V. S., Gamer, L. W. & Rosen, V. BMP signaling in skeletal development, disease and repair. Nat. Rev. Endocrinol. 12, 203–221 (2016).
Wu, W. et al. Altered FGF signaling pathways impair cell proliferation and elevation of palate shelves. PLoS ONE 10, e0136951 (2015).
Gao, Y., Lan, Y., Ovitt, C. E. & Jiang, R. Functional equivalence of the zinc finger transcription factors Osr1 and Osr2 in mouse development. Dev. Biol. 328, 200–209 (2009).
Orgeur, M. et al. Genome-wide strategies identify downstream target genes of chick connective tissue-associated transcription factors. Development 145, dev161208 (2018).
Gao, Y., Lan, Y., Liu, H. & Jiang, R. The zinc finger transcription factors Osr1 and Osr2 control synovial joint formation. Dev. Biol. 352, 83–91 (2011).
Besse, L. et al. Individual limb muscle bundles are formed through progressive steps orchestrated by adjacent connective tissue cells during primary myogenesis. Cell. Rep. 30, 3552–3565 (2020).
Liu, H. et al. Odd-skipped related-1 controls neural crest chondrogenesis during tongue development. Proc. Natl Acad. Sci. USA 110, 18555–18560 (2013).
Lan, Y., Kingsley, P. D., Cho, E. S. & Jiang, R. Osr2, a new mouse gene related to Drosophila odd-skipped, exhibits dynamic expression patterns during craniofacial, limb, and kidney development. Mech. Dev. 107, 175–179 (2001).
Zhang, Z., Lan, Y., Chai, Y. & Jiang, R. Antagonistic actions of Msx1 and Osr2 pattern mammalian teeth into a single row. Science 323, 1232–1234 (2009).
Brault, V. et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253–1264 (2001).
Lan, Y., Wang, Q., Ovitt, C. E. & Jiang, R. A unique mouse strain expressing Cre recombinase for tissue-specific analysis of gene function in palate and kidney development. Genesis 45, 618–624 (2007).
Li, J. et al. SMAD4-mediated WNT signaling controls the fate of cranial neural crest cells during tooth morphogenesis. Development 138, 1977–1989 (2011).
Deng, J. et al. Noggin overexpression impairs the development of muscles, tendons, and aponeurosis in soft palates by disrupting BMP-Smad and Shh-Gli1 signaling. Front. Cell. Dev. Biol. 9, 711334 (2021).
Lan, Y., Qin, C. & Jiang, R. Requirement of hyaluronan synthase-2 in craniofacial and palate development. J. Dent. Res. 98, 1367–1375 (2019).
Yoshimoto, Y. et al. Scleraxis is required for maturation of tissue domains for proper integration of the musculoskeletal system. Sci. Rep. 7, 45010 (2017).
Brent, A. E., Braun, T. & Tabin, C. J. Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development 132, 515–528 (2005).
Sugimoto, Y. et al. Scx+/Sox9+ progenitors contribute to the establishment of the junction between cartilage and tendon/ligament. Development 140, 2280–2288 (2013).
Blitz, E., Sharir, A., Akiyama, H. & Zelzer, E. Tendon-bone attachment unit is formed modularly by a distinct pool of Scx- and Sox9-positive progenitors. Development 140, 2680–2690 (2013).
Roberts, R. R. et al. FGF signaling patterns cell fate at the interface between tendon and bone. Development 146, dev170241 (2019).
Sharir, A., Stern, T., Rot, C., Shahar, R. & Zelzer, E. Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis. Development 138, 3247–3259 (2011).
Felsenthal, N. & Zelzer, E. Mechanical regulation of msuculoskeletal system development. Development 144, 4271–4283 (2017).
Rolfe, R. A. et al. Identification of mechanosensitive genes during skeletal development: alteration of genes associated with cytoskeletal rearrangement and cell signalling pathways. BMC Genomics 15, 48 (2014).
Esteves, de Lima, J., Bonnin, M. A., Birchmeier, C. & Duprez, D. Muscle contraction is required to maintain the pool of muscle progenitors via YAP and NOTCH during fetal myogenesis. eLife 5, e15593 (2016).
Qin, X. et al. Low shear stress induces ERK nuclear localization and YAP activation to control the proliferation of breast cancer cells. Biochem. Biophys. Res. Commun. 510, 219–223 (2019).
Huelter-Hassler, D., Tomakidi, P., Steinberg, T. & Jung, B. A. Orthodontic strain affects the Hippo-pathway effector YAP concomitant with proliferation in human periodontal ligament fibroblasts. Eur. J. Orthod. 39, 251–257 (2017).
Prasad, M. S., Charney, R. M. & García-Castro, M. I. Specification and formation of the neural crest: Perspectives on lineage segregation. Genesis 57, e23276 (2019).
Chen, J., Lan, Y., Baek, J. A., Gao, Y. & Jiang, R. Wnt/beta-catenin signaling plays an essential role in activation of odontogenic mesenchyme during early tooth development. Dev. Biol. 334, 174–185 (2009).
Lin, C. et al. Delineating a conserved genetic cassette promoting outgrowth of body appendages. PLoS Genet. 9, e1003231 (2013).
Wang, F. et al. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J. Mol. Diagn. 14, 22–29 (2012).
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