Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

Jian Sun; Yijun Lin; Nayoung Ha; Jianfei Zhang; Weiqi Wang; Xudong Wang; Qian Bian

doi:10.1016/j.jgg.2023.02.008

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

doi: 10.1016/j.jgg.2023.02.008

Jian Sun^a,b,
Yijun Lin^a,c,
Nayoung Ha^a,b,
Jianfei Zhang^a,b,
Weiqi Wang^a,b,
Xudong Wang^a,b, ,,
Qian Bian^a,c,d, ,

a. Department of Oral and Cranio-Maxillofacial Surgery, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China;
b. National Clinical Research Center for Oral Diseases, Shanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai 200011, China;
c. Shanghai Institute of Precision Medicine, Shanghai 200125, China;
d. Shanghai Key Laboratory of Reproductive Medicine, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China

基金项目:

31970585, 32170544, and 31801056 to Q.B.), the National Key Research and Development Program of China (2017YFC1001800 to X.W.

The authors thank the Flow Cytometry Lab and Bioimaging Facility at Shanghai Institute of Precision Medicine for help with experiments and Wu Zuo for the help with data processing. This work was supported by the National Natural Science Foundation of China (82071096 to X.W

2018YFC1004703 to Q.B), the Fundamental research program funding of Ninth People's Hospital affiliated to Shanghai Jiao Tong University School of Medicine (JYZZ179 to J.S.), the Innovative research team of high-level local universities in Shanghai (SHSMU-ZLCX20211700), and the SHIPM-pi fund No. JY201803 from Shanghai Institute of Precision Medicine, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine.

详细信息

通讯作者:
Xudong Wang,E-mail:xudongwang70@hotmail.com

Qian Bian,E-mail:qianbian@shsmu.edu.cn

计量
- 文章访问数: 228
- HTML全文浏览量: 93
- PDF下载量: 21
- 被引次数: 0
出版历程
- 收稿日期: 2022-10-10
- 录用日期: 2023-02-08
- 修回日期: 2023-01-15
- 刊出日期: 2023-02-24

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

Jian Sun^a,b,
Yijun Lin^a,c,
Nayoung Ha^a,b,
Jianfei Zhang^a,b,
Weiqi Wang^a,b,
Xudong Wang^{a,b
, ,},
Qian Bian^{a,c,d
, ,}

a. Department of Oral and Cranio-Maxillofacial Surgery, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China;
b. National Clinical Research Center for Oral Diseases, Shanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai 200011, China;
c. Shanghai Institute of Precision Medicine, Shanghai 200125, China;
d. Shanghai Key Laboratory of Reproductive Medicine, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China

Funds:

31970585, 32170544, and 31801056 to Q.B.), the National Key Research and Development Program of China (2017YFC1001800 to X.W.

摘要

摘要: During vertebrate embryonic development, neural crest-derived ectomesenchyme within the maxillary prominences undergoes precisely coordinated proliferation and differentiation to give rise to diverse craniofacial structures, such as tooth and palate. However, the transcriptional regulatory networks underpinning such an intricate process have not been fully elucidated. Here, we perform single-cell RNA-Seq to comprehensively characterize the transcriptional dynamics during mouse maxillary development from embryonic day (E) 10.5–E14.5. Our single-cell transcriptome atlas of ~28,000 cells uncovers mesenchymal cell populations representing distinct differentiating states and reveals their developmental trajectory, suggesting that the segregation of dental from the palatal mesenchyme occurs at E11.5. Moreover, we identify a series of key transcription factors (TFs) associated with mesenchymal fate transitions and deduce the gene regulatory networks directed by these TFs. Collectively, our study provides important resources and insights for achieving a systems-level understanding of craniofacial morphogenesis and abnormality.
- Craniofacial development /
- Single-cell RNA-Seq /
- Maxillary prominences /
- Gene regulatory network /
- Transcription factor
Abstract: During vertebrate embryonic development, neural crest-derived ectomesenchyme within the maxillary prominences undergoes precisely coordinated proliferation and differentiation to give rise to diverse craniofacial structures, such as tooth and palate. However, the transcriptional regulatory networks underpinning such an intricate process have not been fully elucidated. Here, we perform single-cell RNA-Seq to comprehensively characterize the transcriptional dynamics during mouse maxillary development from embryonic day (E) 10.5–E14.5. Our single-cell transcriptome atlas of ~28,000 cells uncovers mesenchymal cell populations representing distinct differentiating states and reveals their developmental trajectory, suggesting that the segregation of dental from the palatal mesenchyme occurs at E11.5. Moreover, we identify a series of key transcription factors (TFs) associated with mesenchymal fate transitions and deduce the gene regulatory networks directed by these TFs. Collectively, our study provides important resources and insights for achieving a systems-level understanding of craniofacial morphogenesis and abnormality.
- Craniofacial development /
- Single-cell RNA-Seq /
- Maxillary prominences /
- Gene regulatory network /
- Transcription factor

HTML全文

参考文献(48)

[1]	Aibar, S., Gonzalez-Blas, C.B., Moerman, T., Huynh-Thu, V.A., Imrichova, H., Hulselmans, G., Rambow, F., Marine, J.C., Geurts, P., Aerts, J., et al., 2017. Scenic: Single-cell regulatory network inference and clustering. Nat. Methods 14, 1083-1086.
[2]	Alappat, S., Zhang, Z.Y.,Chen, Y.P., 2003. Msx homeobox gene family and craniofacial development. Cell Res. 13, 429-442.
[3]	Barlow, A.J., Bogardi, J.P., Ladher, R.,Francis-West, P.H., 1999. Expression of chick barx-1 and its differential regulation by fgf-8 and bmp signaling in the maxillary primordia. Dev. Dyn. 214, 291-302.
[4]	Betancur, P., Bronner-Fraser, M.,Sauka-Spengler, T., 2010. Assembling neural crest regulatory circuits into a gene regulatory network. Annu. Rev. Cell Dev. Biol. 26, 581-603.
[5]	Birnbaum, K.D., 2018. Power in numbers: Single-cell rna-seq strategies to dissect complex tissues. Annu. Rev. Genet. 52, 203-221.
[6]	Bronner, M.E.,Simoes-Costa, M., 2016. The neural crest migrating into the twenty-first century. Curr. Top. Dev. Biol. 116, 115-134.
[7]	Bush, J.O.,Jiang, R., 2012. Palatogenesis: Morphogenetic and molecular mechanisms of secondary palate development. Development 139, 231-243.
[8]	Chen, J., Lan, Y., Baek, J.A., Gao, Y.,Jiang, R., 2009. Wnt/beta-catenin signaling plays an essential role in activation of odontogenic mesenchyme during early tooth development. Dev. Biol. 334, 174-185.
[9]	Dura, B., Choi, J.Y., Zhang, K., Damsky, W., Thakral, D., Bosenberg, M., Craft, J.,Fan, R., 2019. Scftd-seq: Freeze-thaw lysis based, portable approach toward highly distributed single-cell 3' mrna profiling. Nucleic Acids Res. 47, e16.
[10]	Francois, M., Caprini, A., Hosking, B., Orsenigo, F., Wilhelm, D., Browne, C., Paavonen, K., Karnezis, T., Shayan, R., Downes, M., et al., 2008. Sox18 induces development of the lymphatic vasculature in mice. Nature 456, 643-647.
[11]	Fuxman Bass, J.I., Diallo, A., Nelson, J., Soto, J.M., Myers, C.L.,Walhout, A.J., 2013. Using networks to measure similarity between genes: Association index selection. Nat. Methods 10, 1169-1176.
[12]	Gou, Y., Zhang, T.,Xu, J., 2015. Transcription factors in craniofacial development: From receptor signaling to transcriptional and epigenetic regulation. Curr. Top. Dev. Biol. 115, 377-410.
[13]	Gritli-Linde, A., 2007. Molecular control of secondary palate development. Dev. Biol. 301, 309-326.
[14]	Hafemeister, C.,Satija, R., 2019. Normalization and variance stabilization of single-cell rna-seq data using regularized negative binomial regression. Genome Biol. 20, 296.
[15]	Han, X., Feng, J., Guo, T., Loh, Y.E., Yuan, Y., Ho, T.V., Cho, C.K., Li, J., Jing, J., Janeckova, E., et al., 2021. Runx2-twist1 interaction coordinates cranial neural crest guidance of soft palate myogenesis. Elife 10.
[16]	Holleville, N., Mateos, S., Bontoux, M., Bollerot, K.,Monsoro-Burq, A.H., 2007. Dlx5 drives runx2 expression and osteogenic differentiation in developing cranial suture mesenchyme. Dev. Biol. 304, 860-874.
[17]	Hooper, J.E., Feng, W., Li, H., Leach, S.M., Phang, T., Siska, C., Jones, K.L., Spritz, R.A., Hunter, L.E.,Williams, T., 2017. Systems biology of facial development: Contributions of ectoderm and mesenchyme. Dev. Biol. 426, 97-114.
[18]	Kawasaki, K., Kawasaki, M., Watanabe, M., Idrus, E., Nagai, T., Oommen, S., Maeda, T., Hagiwara, N., Que, J., Sharpe, P.T., et al., 2015. Expression of sox genes in tooth development. Int. J. Dev. Biol. 59, 471-478.
[19]	Lan, Y., Xu, J.,Jiang, R., 2015. Cellular and molecular mechanisms of palatogenesis. Curr. Top. Dev. Biol. 115, 59-84.
[20]	Leach, S.M., Feng, W.,Williams, T., 2017. Gene expression profile data for mouse facial development. Data Brief. 13, 242-247.
[21]	Li, H., Jones, K.L., Hooper, J.E.,Williams, T., 2019. The molecular anatomy of mammalian upper lip and primary palate fusion at single cell resolution. Development 146.
[22]	Li, J., Parada, C.,Chai, Y., 2017. Cellular and molecular mechanisms of tooth root development. Development 144, 374-384.
[23]	Liu, B., Rooker, S.M.,Helms, J.A., 2010. Molecular control of facial morphology. Semin. Cell Dev. Biol. 21, 309-313.
[24]	Luecken, M.D.,Theis, F.J., 2019. Current best practices in single-cell rna-seq analysis: A tutorial. Mol. Syst. Biol. 15, e8746.
[25]	McGinnis, C.S., Murrow, L.M.,Gartner, Z.J., 2019. Doubletfinder: Doublet detection in single-cell rna sequencing data using artificial nearest neighbors. Cell Syst. 8, 329-337.e324.
[26]	Men, Y., Wang, Y., Yi, Y., Jing, D., Luo, W., Shen, B., Stenberg, W., Chai, Y., Ge, W.P., Feng, J.Q., et al., 2020. Gli1+ periodontium stem cells are regulated by osteocytes and occlusal force. Dev. Cell 54, 639-654.e636.
[27]	Pagani, F., Tratta, E., Dell'Era, P., Cominelli, M.,Poliani, P.L., 2021. Ebf1 is expressed in pericytes and contributes to pericyte cell commitment. Histochem. Cell Biol. 156, 333-347.
[28]	Pilling, D., Vakil, V., Cox, N.,Gomer, R.H., 2015. Tnf-α-stimulated fibroblasts secrete lumican to promote fibrocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 112, 11929-11934.
[29]	Randilini, A., Fujikawa, K.,Shibata, S., 2020. Expression, localization and synthesis of small leucine-rich proteoglycans in developing mouse molar tooth germ. Eur. J. Histochem. 64.
[30]	Sagar,Grun, D., 2020. Deciphering cell fate decision by integrated single-cell sequencing analysis. Annu. Rev. Biomed. Data Sci. 3, 1-22.
[31]	Santagati, F.,Rijli, F.M., 2003. Cranial neural crest and the building of the vertebrate head. Nat. Rev. Neurosci. 4, 806-818.
[32]	Sauka-Spengler, T.,Bronner-Fraser, M., 2008. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568.
[33]	Smith, T.M., Lozanoff, S., Iyyanar, P.P.,Nazarali, A.J., 2012. Molecular signaling along the anterior-posterior axis of early palate development. Front. Physiol. 3, 488.
[34]	Soldatov, R., Kaucka, M., Kastriti, M.E., Petersen, J., Chontorotzea, T., Englmaier, L., Akkuratova, N., Yang, Y., Haring, M., Dyachuk, V., et al., 2019. Spatiotemporal structure of cell fate decisions in murine neural crest. Science 364.
[35]	Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W.M., 3rd, Hao, Y., Stoeckius, M., Smibert, P.,Satija, R., 2019. Comprehensive integration of single-cell data. Cell 177, 1888-1902 e1821.
[36]	Sun, J., Ha, N., Liu, Z., Bian, Q.,Wang, X., 2022. A neural crest-specific overexpression mouse model reveals the transcriptional regulatory effects of dlx2 during maxillary process development. Front. Physiol. 13, 855959.
[37]	Suo, S., Zhu, Q., Saadatpour, A., Fei, L., Guo, G.,Yuan, G.C., 2018. Revealing the critical regulators of cell identity in the mouse cell atlas. Cell Rep. 25, 1436-1445 e1433.
[38]	Tirosh, I., Izar, B., Prakadan, S.M., Wadsworth, M.H., 2nd, Treacy, D., Trombetta, J.J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al., 2016. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell rna-seq. Science 352, 189-196.
[39]	Trainor, P.A., 2005. Specification of neural crest cell formation and migration in mouse embryos. Semin. Cell Dev. Biol. 16, 683-693.
[40]	Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N.J., Livak, K.J., Mikkelsen, T.S.,Rinn, J.L., 2014. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381-386.
[41]	Wilkie, A.O.,Morriss-Kay, G.M., 2001. Genetics of craniofacial development and malformation. Nat. Rev. Genet. 2, 458-468.
[42]	Williams, R.M., Candido-Ferreira, I., Repapi, E., Gavriouchkina, D., Senanayake, U., Ling, I.T.C., Telenius, J., Taylor, S., Hughes, J.,Sauka-Spengler, T., 2019. Reconstruction of the global neural crest gene regulatory network in vivo. Dev. Cell 51, 255-276 e257.
[43]	Wu, S.P., Dong, X.R., Regan, J.N., Su, C.,Majesky, M.W., 2013. Tbx18 regulates development of the epicardium and coronary vessels. Dev. Biol 383, 307-320.
[44]	Xu, J., Liu, H., Lan, Y., Adam, M., Clouthier, D.E., Potter, S.,Jiang, R., 2019. Hedgehog signaling patterns the oral-aboral axis of the mandibular arch. Elife 8.
[45]	Yu, G., Wang, L.G., Han, Y.,He, Q.Y., 2012. Clusterprofiler: An r package for comparing biological themes among gene clusters. Omics 16, 284-287.
[46]	Yuan, Y.,Chai, Y., 2019. Regulatory mechanisms of jaw bone and tooth development. Curr. Top. Dev. Biol. 133, 91-118.
[47]	Yuan, Y., Loh, Y.E., Han, X., Feng, J., Ho, T.V., He, J., Jing, J., Groff, K., Wu, A.,Chai, Y., 2020. Spatiotemporal cellular movement and fate decisions during first pharyngeal arch morphogenesis. Sci. Adv. 6.
[48]	Zalc, A., Sinha, R., Gulati, G.S., Wesche, D.J., Daszczuk, P., Swigut, T., Weissman, I.L.,Wysocka, J., 2021. Reactivation of the pluripotency program precedes formation of the cranial neural crest. Science 371.

施引文献

资源附件(0)

访问统计

点击查看大图

计量

文章访问数: 228
HTML全文浏览量: 93
PDF下载量: 21
被引次数: 0

姓名
邮箱
手机号码
标题
留言内容
验证码

留言板

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

doi: 10.1016/j.jgg.2023.02.008

通讯作者:
Xudong Wang,E-mail:xudongwang70@hotmail.com

Qian Bian,E-mail:qianbian@shsmu.edu.cn

计量

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

计量

目录

留言板

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

doi: 10.1016/j.jgg.2023.02.008

通讯作者: Xudong Wang,E-mail:xudongwang70@hotmail.com Qian Bian,E-mail:qianbian@shsmu.edu.cn

计量

出版历程

Single-cell RNA-Seq reveals transcriptional regulatory networks directing the development of mouse maxillary prominence

计量

出版历程

目录

通讯作者:
Xudong Wang,E-mail:xudongwang70@hotmail.com

Qian Bian,E-mail:qianbian@shsmu.edu.cn