Expression patterns of keratin family members during tooth development and the role of keratin 17 in cytodifferentiation of stratum intermedium and stellate reticulum.
cell differentiation
keratin
scRNA‐seq
stellate reticulum
stratum intermedium
tooth development
Journal
Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222
Informations de publication
Date de publication:
16 Jul 2024
16 Jul 2024
Historique:
revised:
05
06
2024
received:
02
02
2024
accepted:
09
07
2024
medline:
17
7
2024
pubmed:
17
7
2024
entrez:
17
7
2024
Statut:
aheadofprint
Résumé
Keratins are typical intermediate filament proteins of the epithelium that exhibit highly specific expression patterns related to the epithelial type and stage of cellular differentiation. They are important for cytoplasmic stability and epithelial integrity and are involved in various intracellular signaling pathways. Several keratins are associated with enamel formation. However, information on their expression patterns during tooth development remains lacking. In this study, we analyzed the spatiotemporal expression of keratin family members during tooth development using single-cell RNA-sequencing (scRNA-seq) and microarray analysis. scRNA-seq datasets from postnatal Day 1 mouse molars revealed that several keratins are highly expressed in the dental epithelium, indicating the involvement of keratin family members in cellular functions. Among various keratins, keratin 5 (Krt5), keratin 14 (Krt14), and keratin 17 (Krt17) are highly expressed in the tooth germ; KRT17 is specifically expressed in the stratum intermedium (SI) and stellate reticulum (SR). Depletion of Krt17 did not affect cell proliferation in the dental epithelial cell line SF2 but suppressed their differentiation ability. These results suggest that Krt17 is essential for SI cell differentiation. Furthermore, scRNA-seq results indicated that Krt5, Krt14, and Krt17 exhibited distinct expression patterns in ameloblast, SI, and SR cells. Our findings contribute to the elucidation of novel mechanisms underlying tooth development.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e31387Subventions
Organisme : Japan Society for the Promotion of Science
Informations de copyright
© 2024 The Author(s). Journal of Cellular Physiology published by Wiley Periodicals LLC.
Références
Al Thamin, S., Chiba, Y., Yoshizaki, K., Tian, T., Jia, L., Wang, X., Saito, K., Li, J., Yamada, A., & Fukumoto, S. (2021). Transcriptional regulation of the basic helix‐loop‐helix factor AmeloD during tooth development. Journal of Cellular Physiology, 236(11), 7533–7543. https://doi.org/10.1002/jcp.30389
Chamcheu, J. C., Siddiqui, I. A., Syed, D. N., Adhami, V. M., Liovic, M., & Mukhtar, H. (2011). Keratin gene mutations in disorders of human skin and its appendages. Archives of Biochemistry and Biophysics, 508(2), 123–137. https://doi.org/10.1016/j.abb.2010.12.019
Chiba, Y., Saito, K., Martin, D., Boger, E. T., Rhodes, C., Yoshizaki, K., Nakamura, T., Yamada, A., Morell, R. J., Yamada, Y., & Fukumoto, S. (2020). Single‐cell RNA‐sequencing from mouse incisor reveals dental epithelial cell‐type specific genes. Frontiers in Cell and Developmental Biology, 8, 841. https://doi.org/10.3389/fcell.2020.00841
Chiba, Y., Yoshizaki, K., Tian, T., Miyazaki, K., Martin, D., Saito, K., Yamada, A., & Fukumoto, S. (2021). Integration of single‐cell RNA‐ and CAGE‐seq reveals tooth‐enriched genes. Journal of Dental Research, 101(5), 542–550. https://doi.org/10.1177/00220345211049785
Duverger, O., Beniash, E., & Morasso, M. I. (2016). Keratins as components of the enamel organic matrix. Matrix Biology, 52–54, 260–265. https://doi.org/10.1016/j.matbio.2015.12.007
Duverger, O., Carlson, J. C., Karacz, C. M., Schwartz, M. E., Cross, M. A., Marazita, M. L., Shaffer, J. R., & Morasso, M. I. (2018). Genetic variants in pachyonychia congenita‐associated keratins increase susceptibility to tooth decay. PLoS Genetics, 14(1), e1007168. https://doi.org/10.1371/journal.pgen.1007168
Franceschetti, A., & Jadassohn, W. (1954). A propos de l’«incontinentia pigmenti», délimitation de deux syndromes différents figurant sous le même terme. Dermatology, 108(1), 1–28.
Fuchs, E. (1995). Keratins and the skin. Annual Review of Cell and Developmental Biology, 11, 123–154. https://doi.org/10.1146/annurev.cb.11.110195.001011
Hao, Y., Hao, S., Andersen‐Nissen, E., Mauck, 3rd W. M., Zheng, S., Butler, A., Lee, M. J., Wilk, A. J., Darby, C., Zager, M., Hoffman, P., Stoeckius, M., Papalexi, E., Mimitou, E. P., Jain, J., Srivastava, A., Stuart, T., Fleming, L. M., Yeung, B., … Satija, R. (2021). Integrated analysis of multimodal single‐cell data. Cell, 184(13), 3573–3587.e29. https://doi.org/10.1016/j.cell.2021.04.048
Harada, H., Ichimori, Y., Yokohama‐Tamaki, T., Ohshima, H., Kawano, S., Katsube, K., & Wakisaka, S. (2006). Stratum intermedium lineage diverges from ameloblast lineage via Notch signaling. Biochemical and Biophysical Research Communications, 340(2), 611–616. https://doi.org/10.1016/j.bbrc.2005.12.053
Jernvall, J., & Thesleff, I. (2000). Reiterative signaling and patterning during mammalian tooth morphogenesis. Mechanisms of Development, 92(1), 19–29. https://doi.org/10.1016/s0925-4773(99)00322-6
Jheon, A. H., Mostowfi, P., Snead, M. L., Ihrie, R. A., Sone, E., Pramparo, T., Attardi, L. D., & Klein, O. D. (2011). PERP regulates enamel formation via effects on cell‐cell adhesion and gene expression. Journal of Cell Science, 124(Pt), 745–754. https://doi.org/10.1242/jcs.078071
Jheon, A. H., Prochazkova, M., Meng, B., Wen, T., Lim, Y. J., Naveau, A., Espinoza, R., Cox, T. C., Sone, E. D., Ganss, B., Siebel, C. W., & Klein, O. D. (2016). Inhibition of notch signaling during mouse incisor renewal leads to enamel defects. Journal of Bone and Mineral Research, 31(1), 152–162. https://doi.org/10.1002/jbmr.2591
Jia, L., Chiba, Y., Saito, K., Yoshizaki, K., Tian, T., Han, X., Mizuta, K., Chiba, M., Wang, X., Al Thamin, S., Yamada, A., & Fukumoto, S. (2022). The tooth‐specific basic helix‐loop‐helix factor AmeloD promotes differentiation of ameloblasts. Journal of Cellular Physiology, 237(2), 1597–1606. https://doi.org/10.1002/jcp.30639
Kaimal, V., Bardes, E. E., Tabar, S. C., Jegga, A. G., & Aronow, B. J. (2010). ToppCluster: A multiple gene list feature analyzer for comparative enrichment clustering and network‐based dissection of biological systems. Nucleic Acids Research, 38, W96–W102. https://doi.org/10.1093/nar/gkq418
Lacruz, R. S., Habelitz, S., Wright, J. T., & Paine, M. L. (2017). Dental enamel formation and implications for oral health and disease. Physiological Reviews, 97(3), 939–993. https://doi.org/10.1152/physrev.00030.2016
Lähdeniemi, I. A. K., Misiorek, J. O., Antila, C. J. M., Landor, S. K. J., Stenvall, C. G. A., Fortelius, L. E., Bergström, L. K., Sahlgren, C., & Toivola, D. M. (2017). Keratins regulate colonic epithelial cell differentiation through the Notch1 signalling pathway. Cell Death & Differentiation, 24(6), 984–996. https://doi.org/10.1038/cdd.2017.28
McDonald, R. M. (1976). Natal teeth and steatocystoma multiplex complicated by hidradenitis suppurativa. A new syndrome. Archives of Dermatology, 112(8), 1132–1134.
Mikami, Y., Fujii, S., Nagata, K., Wada, H., Hasegawa, K., Abe, M., Yoshimoto, R. U., Kawano, S., Nakamura, S., & Kiyoshima, T. (2017). GLI‐mediated Keratin 17 expression promotes tumor cell growth through the anti‐apoptotic function in oral squamous cell carcinomas. Journal of Cancer Research and Clinical Oncology, 143(8), 1381–1393. https://doi.org/10.1007/s00432-017-2398-2
Moll, R., Divo, M., & Langbein, L. (2008). The human keratins: Biology and pathology. Histochemistry and Cell Biology, 129(6), 705–733. https://doi.org/10.1007/s00418-008-0435-6
Munne, P. M., Tummers, M. J., Järvinen, E., Thesleff, I., & Jernvall, J. (2009). Tinkering with the inductive mesenchyme: Sostdc1 uncovers the role of dental mesenchyme in limiting tooth induction. Development, 136(3): 393–402.
Nakai, M., Tatemoto, Y., Mori, H., & Mori, M. (1986). Distribution profiles of keratin proteins during rat amelogenesis. Histochemistry, 85(2), 89–94. https://doi.org/10.1007/bf00491753
Nakamura, T., Chiba, Y., Naruse, M., Saito, K., Harada, H., & Fukumoto, S. (2016). Globoside accelerates the differentiation of dental epithelial cells into ameloblasts. International Journal of Oral Science, 8(4), 205–212. https://doi.org/10.1038/ijos.2016.35
Nakatomi, M., Ida‐Yonemochi, H., Nakatomi, C., Saito, K., Kenmotsu, S., Maas, R. L., & Ohshima, H. (2018). Msx2 prevents stratified squamous epithelium formation in the enamel organ. Journal of dental research, 97(12), 1355–1364. doi:10.1177/0022034518777746
Närhi, K., Tummers, M., Ahtiainen, L., Itoh, N., Thesleff, I., & Mikkola, M. L. (2012). Sostdc1 defines the size and number of skin appendage placodes. Developmental Biology, 364(2), 149–161. https://doi.org/10.1016/j.ydbio.2012.01.026
Oh, S. W., Kim, M. Y., Lee, J. S., & Kim, S. C. (2006). Keratin 17 mutation in pachyonychia congenita type 2 patient with early onset steatocystoma multiplex and Hutchinson‐like tooth deformity. The Journal of Dermatology, 33(3), 161–164. https://doi.org/10.1111/j.1346-8138.2006.00037.x
Pan, X., Hobbs, R. P., & Coulombe, P. A. (2013). The expanding significance of keratin intermediate filaments in normal and diseased epithelia. Current Opinion in Cell Biology, 25(1), 47–56. https://doi.org/10.1016/j.ceb.2012.10.018
Ravindranath, R. M. H., Basilrose, Sr. R. M., Ravindranath, N. H., & Vaitheesvaran, B. (2003). Amelogenin interacts with cytokeratin‐5 in ameloblasts during enamel growth. Journal of Biological Chemistry, 278(22), 20293–20302. https://doi.org/10.1074/jbc.M211184200
Ravindranath, R. M. H., Tam, W. Y., Bringas, Jr. P., Santos, V., & Fincham, A. G. (2001). Amelogenin‐cytokeratin 14 interaction in ameloblasts during enamel formation. Journal of Biological Chemistry, 276(39), 36586–36597. https://doi.org/10.1074/jbc.M104656200
Sakamoto, K., Aragaki, T., Morita, K., Kawachi, H., Kayamori, K., Nakanishi, S., Omura, K., Miki, Y., Okada, N., Katsube, K., Takizawa, T., & Yamaguchi, A. (2011). Down‐regulation of keratin 4 and keratin 13 expression in oral squamous cell carcinoma and epithelial dysplasia: A clue for histopathogenesis. Histopathology (Oxford), 58(4), 531–542. https://doi.org/10.1111/j.1365-2559.2011.03759.x
Sakamoto, K., Fujii, T., Kawachi, H., Miki, Y., Omura, K., Morita, K., Kayamori, K., Katsube, K., & Yamaguchi, A. (2012). Reduction of NOTCH1 expression pertains to maturation abnormalities of keratinocytes in squamous neoplasms. Laboratory Investigation, 92(5), 688–702. https://doi.org/10.1038/labinvest.2012.9
Smith, F. J. D., Corden, L. D., Rugg, E. L., Ratnavel, R., Leigh, I. M., Moss, C., Tidman, M. J., Hohl, D., Huber, M., Kunkeler, L., Munro, C. S., Birgitte Lane, E., & Irwin McLean, W. H. (1997). Missense mutations in keratin 17 cause either pachyonychia congenita type 2 or a phenotype resembling steatocystoma multiplex. Journal of Investigative Dermatology, 108(2), 220–223. https://doi.org/10.1111/1523-1747.ep12335315
Soderquist, N. A. (1968). Pachyonychia congenita with epidermal cysts and other congenital dyskeratoses. Archives of Dermatology, 97(1), 31–33.
Vasioukhin, V., Degenstein, L., Wise, B., & Fuchs, E. (1999). The magical touch: Genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proceedings of the National Academy of Sciences United States of America, 96(15), 8551–8556. https://doi.org/10.1073/pnas.96.15.8551
Wang, X., Chiba, Y., Jia, L., Yoshizaki, K., Saito, K., Yamada, A., Qin, M., & Fukumoto, S. (2020). Expression patterns of claudin family members during tooth development and the role of claudin‐10 (Cldn10) in cytodifferentiation of stratum intermedium. Frontiers in Cell and Developmental Biology, 8, 595593. https://doi.org/10.3389/fcell.2020.595593
Yoshizaki, K., Hu, L., Nguyen, T., Sakai, K., Ishikawa, M., Takahashi, I., Fukumoto, S., DenBesten, P. K., Bikle, D. D., Oda, Y., & Yamada, Y. (2017). Mediator 1 contributes to enamel mineralization as a coactivator for Notch1 signaling and stimulates transcription of the alkaline phosphatase gene. Journal of Biological Chemistry, 292(33), 13531–13540. https://doi.org/10.1074/jbc.M117.780866
Zhang, X., Yin, M., & Zhang, L. (2019). Keratin 6, 16 and 17‐critical barrier alarmin molecules in skin wounds and psoriasis. Cells, 8(8), 807. https://doi.org/10.3390/cells8080807