Enamel decussation pattern originates from directional sliding of ameloblasts

Vladislav Rakultsev , Josef Lavicky , Marcos Gonzalez Lopez , Klara Cigosova , Igor Adameyko , Jan Krivanek

International Journal of Oral Science ›› 2026, Vol. 18 ›› Issue (1) : 7

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International Journal of Oral Science ›› 2026, Vol. 18 ›› Issue (1) :7 DOI: 10.1038/s41368-025-00412-5
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Enamel decussation pattern originates from directional sliding of ameloblasts

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Abstract

Enamel, the inorganic tissue covering the crowns of teeth, is known for its remarkable resilience and hardness. These properties originate from its high proportion of mineralized matrix and complex internal microarchitecture. On an ultrastructural level, it consists of directionally arranged enamel prisms. Continuously growing rodent incisors are an exemplary case of this phenomenon. Their enamel has a consistent decussation pattern, providing teeth with extremely high resistance and ensuring they remain constantly sharp. While the decussation pattern has been described in detail, mechanisms behind its formation have not been experimentally proven. Here, we show that the highly organized enamel micropattern is generated by directional epithelial sliding of enamel-forming ameloblasts in vivo. Our results detail how enamel micropatterning stems from individual cell cluster segregation and subsequent reciprocal interweaving. Based on this determination, we introduce and experimentally demonstrate a new model of enamel decussation pattern formation.

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Vladislav Rakultsev, Josef Lavicky, Marcos Gonzalez Lopez, Klara Cigosova, Igor Adameyko, Jan Krivanek. Enamel decussation pattern originates from directional sliding of ameloblasts. International Journal of Oral Science, 2026, 18(1): 7 DOI:10.1038/s41368-025-00412-5

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References

[1]

Weatherell JA. Composition of dental enamel. Br. Med. Bull., 1975, 31: 115-119

[2]

Chai H, Lee JJW, Constantino PJ, Lucas PW, Lawn BR. Remarkable resilience of teeth. Proc. Natl Acad. Sci. USA, 2009, 106: 7289-7293

[3]

Yahyazadehfar M, Bajaj D, Arola DD. Hidden contributions of the enamel rods on the fracture resistance of human teeth. Acta Biomater., 2013, 9: 4806-4814

[4]

Balic, A. & Thesleff, I. Tissue Interactions Regulating Tooth Development and Renewal. in Current Topics in Developmental Biology Vol. 115, 157–186 (Elsevier, 2015).

[5]

Hu JCC, Chun YHP, Al Hazzazzi T, Simmer JP. Enamel formation and amelogenesis imperfecta. Cells Tissues Organs, 2007, 186: 78-85

[6]

Thesleff I. Epithelial-mesenchymal signalling regulating tooth morphogenesis. J. Cell Sci., 2003, 116: 1647-1648

[7]

Yu T, Klein OD. Molecular and cellular mechanisms of tooth development, homeostasis and repair. Development, 2020, 147: dev184754

[8]

Lavicky Jet al.. The development of dentin microstructure is controlled by the type of adjacent epithelium. J. Bone Miner. Res., 2022, 37: 323-339

[9]

Matsuo S, Ichikawa H, Wakisaka S, Akai M. Changes of cytochemical properties in the Golgi apparatus during in vivo differentiation of the ameloblast in developing rat molar tooth germs. Anat. Rec., 1992, 234: 469-478

[10]

Rönnholm E. An electron microscopic study of the amelogenesis in human teeth. J. Ultrastruct. Res., 1962, 6: 229-248

[11]

Warshawsky H. A freeze-fracture study of the topographic relationship between inner enamel-secretory ameloblasts in the rat incisor. Am. J. Anat., 1978, 152: 153-207

[12]

Line S, Novaes P. The development and evolution of mammalian enamel: structural and functional aspects. Braz. J. Morphol. Sci., 2005, 22: 67-72

[13]

Lynch, C. D., O’Sullivan, V. R., Dockery, P., McGillycuddy, C. T. & Sloan, A. J. Hunter-Schreger Band patterns in human tooth enamel. J. Anat. 106–115 https://doi.org/10.1111/j.1469-7580.2010.01255.x (2010).

[14]

Boyde A. Electron microscopic observations relating to the nature and development of prism decussation in mammalian dental enamel. Bull. Group. Int. Rech. Sci. Stomatol., 1969, 12: 151-207

[15]

Boyde A. The development of enamel structure. Proc. R. Soc. Med., 1967, 60: 923-928

[16]

Boyde, A. The Structure and Development of Mammalian Enamel (University of London, 1964).

[17]

Warshawsky H, Smith CE. Morphological classification of rat incisor ameloblasts. Anat. Rec., 1974, 179: 423-445

[18]

Warshawsky H, Smith CE. A three-dimensional reconstruction of the rods in rat maxillary incisor enamel. Anat. Rec., 1971, 169: 585-591

[19]

Koenigswald WV, Rensberger JM, Pretzschner HU. Changes in the tooth enamel of early Paleocene mammals allowing increased diet diversity. Nature, 1987, 328: 150-152

[20]

Bajaj D, Arola D. Role of prism decussation on fatigue crack growth and fracture of human enamel. Acta Biomater., 2009, 5: 3045-3056

[21]

Liu S, Xu Y, An B, Zhang D. Interaction of rod decussation and crack growth in enamel. Comput. Methods Biomech. Biomed. Engin., 2023, 26: 700-709

[22]

Pro JW, Barthelat F. Discrete element models of tooth enamel, a complex three-dimensional biological composite. Acta Biomater., 2019, 94: 536-552

[23]

Smith CE, Hu Y, Hu JC, Simmer JP. Characteristics of the transverse 2D uniserial arrangement of rows of decussating enamel rods in the inner enamel layer of mouse mandibular incisors. J. Anat., 2019, 235: 912-930

[24]

Yang D, Bharatiya M, Grine FE. Hunter-Schreger Band configuration in human molars reveals more decussation in the lateral enamel of ‘functional’ cusps than ‘guiding’ cusps. Arch. Oral. Biol., 2022, 142: 105524

[25]

Renvois‚ E, Michon F. An Evo-Devo perspective on ever-growing teeth in mammals and dental stem cell maintenance. Front. Physiol., 2014, 5: 324

[26]

Krivanek J, Adameyko I, Fried K. Heterogeneity and developmental connections between cell types inhabiting teeth. Front. Physiol., 2017, 8: 376

[27]

Møinichen CB, Lyngstadaas SP, Risnes S. Morphological characteristics of mouse incisor enamel. J. Anat., 1996, 189(Pt 2): 325-333

[28]

Smith CE, Hu Y, Hu JC-C, Simmer JP. Quantitative analysis of the core 2D arrangement and distribution of enamel rods in cross-sections of mandibular mouse incisors. J. Anat., 2019, 234: 274-290

[29]

Hua LCet al.. Dental development and microstructure of bamboo rat incisors. Biosurf. Biotribol., 2015, 1: 263-269

[30]

Krivanek Jet al.. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat. Commun., 2020, 11 4816

[31]

Sharir Aet al.. A large pool of actively cycling progenitors orchestrates self-renewal and injury repair of an ectodermal appendage. Nat. Cell Biol., 2019, 21: 1102-1112

[32]

Chiba Yet al.. Single-cell RNA-sequencing from mouse incisor reveals dental epithelial cell-type specific genes. Front. Cell Dev. Biol., 2020, 8: 841

[33]

Sanz-Navarro, M. et al. Plasticity within the niche ensures the maintenance of a Sox2+ stem cell population in the mouse incisor. Development dev.155929 https://doi.org/10.1242/dev.155929 (2017).

[34]

Juuri Eet al.. Sox2+ stem cells contribute to all epithelial lineages of the tooth via Sfrp5+ progenitors. Dev. Cell, 2012, 23: 317-328

[35]

Zhang Let al.. Expression pattern of Sox2 during mouse tooth development. Gene Expr. Patterns, 2012, 12: 273-281

[36]

Li Det al.. Sox2 controls asymmetric patterning of ameloblast lineage commitment by regulation of FGF signaling in the mouse incisor. J. Mol. Histol., 2021, 52: 1035-1042

[37]

Gonzalez Lopez Met al.. Spatiotemporal monitoring of hard tissue development reveals unknown features of tooth and bone development. Sci. Adv., 2023, 9 eadi0482

[38]

Krivanek J, Buchtova M, Fried K, Adameyko I. Plasticity of dental cell types in development, regeneration, and evolution. J. Dent. Res., 2023, 102: 589-598

[39]

Osborn JW. A 3-dimensional model to describe the relation between prism directions, parazones and diazones, and the Hunter-Schreger bands in human tooth enamel. Arch. Oral. Biol., 1990, 35: 869-878

[40]

Pagella P, de Vargas Roditi L, Stadlinger B, Moor AE, Mitsiadis TA. A single-cell atlas of human teeth. iScience, 2021, 24: 102405

[41]

Athwal HKet al.. Sox10 regulates plasticity of epithelial progenitors toward secretory units of exocrine glands. Stem Cell Rep., 2019, 12: 366-380

[42]

Dravis Cet al.. Sox10 regulates stem/progenitor and mesenchymal cell states in mammary epithelial cells. Cell Rep., 2015, 12: 2035-2048

[43]

Jing Jet al.. Expression and localization of Sox10 during hair follicle morphogenesis and induced hair cycle. Int. J. Med. Sci., 2021, 18: 3498-3505

[44]

Tomokiyo Aet al.. A multipotent clonal human periodontal ligament cell line with neural crest cell phenotypes promotes neurocytic differentiation, migration, and survival. J. Cell. Physiol., 2012, 227: 2040-2050

[45]

Wang Det al.. Sox10+ adult stem cells contribute to biomaterial encapsulation and microvascularization. Sci. Rep., 2017, 7 40295

[46]

Wong CEet al.. Neural crest–derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J. Cell Biol., 2006, 175: 1005-1015

[47]

Yu Wet al.. The duct of von Ebner’s glands is a source of Sox10+ taste bud progenitors and susceptible to pathogen infections. Front. Cell Dev. Biol., 2024, 12: 1460669

[48]

Kastriti MEet al.. Schwann cell precursors represent a neural crest-like state with biased multipotency. EMBO J., 2022, 41: e108780

[49]

Jessen KR, Mirsky R. Schwann cell precursors; multipotent glial cells in embryonic nerves. Front. Mol. Neurosci., 2019, 12: 69

[50]

Lai Xet al.. SOX10 ablation severely impairs the generation of postmigratory neural crest from human pluripotent stem cells. Cell Death Dis., 2021, 12 814

[51]

Huang Tet al.. Direct interaction of Sox10 with Cadherin-19 mediates early sacral neural crest cell migration: implications for enteric nervous system development defects. Gastroenterology, 2022, 162: 179-192.e11

[52]

Alloing-Séguier L, Marivaux L, Barczi J-F, Lihoreau F, Martinand-Mari C. Relationships between enamel prism decussation and organization of the ameloblast layer in rodent incisors. Anat. Rec., 2019, 302: 1195-1209

[53]

Cox BN. How the tooth got its stripes: patterning via strain-cued motility. J. R. Soc. Interface, 2013, 10: 20130266

[54]

Inaki Met al.. Chiral cell sliding drives left-right asymmetric organ twisting. eLife, 2018, 7 e32506

[55]

Sato Ket al.. Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis. Nat. Commun., 2015, 6 10074

[56]

Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature, 2004, 429: 667-671

[57]

Okuda S, Kuranaga E, Sato K. Apical junctional fluctuations lead to cell flow while maintaining epithelial integrity. Biophys. J., 2019, 116: 1159-1170

[58]

Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol., 2009, 10: 445-457

[59]

Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z. Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev. Cell, 2008, 14: 570-581

[60]

Lu Yet al.. Asymmetric stratification-induced polarity loss and coordinated individual cell movements drive directional migration of vertebrate epithelium. Cell Rep., 2020, 33: 108246

[61]

Nishikawa S. Cytoskeleton, intercellular junctions, planar cell polarity, and cell movement in amelogenesis. J. Oral. Biosci., 2017, 59: 197-204

[62]

Renteria C, Fernández-Arteaga JM, Grimm J, Ossa EA, Arola D. Mammalian enamel: a universal tissue and diverse source of inspiration. Acta Biomater., 2021, 136: 402-411

[63]

Marsico Cet al.. Characterizing the microstructures of mammalian enamel by synchrotron phase contrast microCT. Acta Biomater., 2024, 178: 208-220

[64]

Simmer JPet al.. A genetic model for the secretory stage of dental enamel formation. J. Struct. Biol., 2021, 213: 107805

[65]

Gan L, Liu Y, Cui DX, Pan Y, Wan M. New insight into dental epithelial stem cells: identification, regulation, and function in tooth homeostasis and repair. World J. Stem Cells, 2020, 12: 1327-1340

[66]

Laranjeira Cet al.. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J. Clin. Invest., 2011, 121: 3412-3424

[67]

Madisen Let al.. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 2010, 13: 133-140

[68]

Snippert HJet al.. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell, 2010, 143: 134-144

[69]

Susaki EAet al.. Advanced CUBIC protocols for whole-brain and whole-body clearing and imaging. Nat. Protoc., 2015, 10: 1709-1727

[70]

Krivanek J., Lavicky J., Bouderlique T. & Adameyko I. Rapid isolation of single cells from mouse and human teeth. J. Vis. Exp. 63043 https://doi.org/10.3791/63043-v (2021).

[71]

Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat. Methods, 2012, 9: 671-675

Funding

Grantová Agentura České Republiky (Grant Agency of the Czech Republic)(23-06160S)

Lékařská fakulta, Masarykova univerzita (Faculty of Medicine, Masaryk University)(MUNI/A/1738/2024)

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