Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process

Takebe T, Enomura M, Yoshizawa E, Kimura M, Koike H, Ueno Y, et al. Vascularized and complex organ buds from diverse tissues via mesenchymal Cell-Driven condensation. Cell Stem Cell. 2015;16(5):556–65.

CAS  PubMed  Google Scholar 

Shyer AE, Rodrigues AR, Schroeder GG, Kassianidou E, Kumar S, Harland RM. Emergent cellular self-organization and mechanosensation initiate follicle pattern in the avian skin. Science. 2017;357(6353):811–5.

CAS  PubMed  PubMed Central  Google Scholar 

Giffin JL, Gaitor D, Franz-Odendaal TA. The forgotten skeletogenic condensations: A comparison of early skeletal development amongst vertebrates. J Dev Biol. 2019;7(1).

Mammoto T, Mammoto A, Torisawa YS, Tat T, Gibbs A, Derda R, et al. Mechanochemical control of mesenchymal condensation and embryonic tooth organ formation. Dev Cell. 2011;21(4):758–69.

CAS  PubMed  PubMed Central  Google Scholar 

Hall BK, Miyake T. Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Int J Dev Biol. 1995;39(6):881–93.

CAS  PubMed  Google Scholar 

Sui BD, Zheng CX, Zhao WM, Xuan K, Li B, Jin Y. Mesenchymal condensation in tooth development and regeneration: a focus on translational aspects of organogenesis. Physiol Rev. 2023;103(3):1899–964.

CAS  PubMed  Google Scholar 

Yang S, Palmquist KH, Nathan L, Pfeifer CR, Schultheiss PJ, Sharma A, et al. Morphogens enable interacting supracellular phases that generate organ architecture. Science. 2023;382(6673):eadg5579.

CAS  PubMed  Google Scholar 

Jing J, Feng J, Yuan Y, Guo T, Lei J, Pei F, et al. Spatiotemporal single-cell regulatory atlas reveals neural crest lineage diversification and cellular function during tooth morphogenesis. Nat Commun. 2022;13(1):4803.

CAS  PubMed  PubMed Central  Google Scholar 

Mammoto T, Ingber DE. Mechanical control of tissue and organ development. Development. 2010;137(9):1407–20.

CAS  PubMed  PubMed Central  Google Scholar 

Mercker M, Hartmann D, Marciniak-Czochra A. A mechanochemical model for embryonic pattern formation: coupling tissue mechanics and morphogen expression. PLoS ONE. 2013;8(12):e82617.

PubMed  PubMed Central  Google Scholar 

Villeneuve C, Hashmi A, Ylivinkka I, Lawson-Keister E, Miroshnikova YA, Perez-Gonzalez C, et al. Mechanical forces across compartments coordinate cell shape and fate transitions to generate tissue architecture. Nat Cell Biol. 2024;26(2):207–18.

CAS  PubMed  PubMed Central  Google Scholar 

Khatib NS, Monsen J, Ahmed S, Huang Y, Hoey DA, Nowlan NC. Mechanoregulatory role of TRPV4 in prenatal skeletal development. Sci Adv. 2023;9(4):eade2155.

CAS  PubMed  PubMed Central  Google Scholar 

Yang S, Huang F, Zhang F, Sheng X, Fan W, Dissanayaka WL. Emerging roles of YAP/TAZ in tooth and surrounding: from development to regeneration. Stem Cell Rev Rep. 2023;19(6):1659–75.

PubMed  Google Scholar 

Lappalainen P, Kotila T, Jegou A, Romet-Lemonne G. Biochemical and mechanical regulation of actin dynamics. Nat Rev Mol Cell Biol. 2022;23(12):836–52.

CAS  PubMed  Google Scholar 

Roh-Johnson M, Shemer G, Higgins CD, McClellan JH, Werts AD, Tulu US, et al. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science. 2012;335(6073):1232–5.

CAS  PubMed  PubMed Central  Google Scholar 

Seetharaman S, Etienne-Manneville S. Cytoskeletal crosstalk in cell migration. Trends Cell Biol. 2020;30(9):720–35.

CAS  PubMed  Google Scholar 

Sakamoto R, Murrell MP. F-actin architecture determines the conversion of chemical energy into mechanical work. Nat Commun. 2024;15(1):3444.

CAS  PubMed  PubMed Central  Google Scholar 

Li TD, Bieling P, Weichsel J, Mullins RD, Fletcher DA. The molecular mechanism of load adaptation by branched actin networks. Elife. 2022;11.

Clarke DN, Martin AC. Actin-based force generation and cell adhesion in tissue morphogenesis. Curr Biol. 2021;31(10):R667–80.

CAS  PubMed  PubMed Central  Google Scholar 

Wang J. Perspectives on the landscape and flux theory for describing emergent behaviors of the biological systems. J Biol Phys. 2022;48(1):1–36.

PubMed  Google Scholar 

Gao G, Li X, Jiang Z, Osorio L, Tang YL, Yu X, et al. Isthmin-1 (Ism1) modulates renal branching morphogenesis and mesenchyme condensation during early kidney development. Nat Commun. 2023;14(1):2378.

CAS  PubMed  PubMed Central  Google Scholar 

Liu S. Mesenchymal stem cell engineering. Methods Mol Biol. 2024;2766:169–74.

CAS  PubMed  Google Scholar 

Saraswathibhatla A, Indana D, Chaudhuri O. Cell-extracellular matrix mechanotransduction in 3D. Nat Rev Mol Cell Biol. 2023;24(7):495–516.

CAS  PubMed  PubMed Central  Google Scholar 

Huang D, Li Y, Ma Z, Lin H, Zhu X, Xiao Y, et al. Collagen hydrogel viscoelasticity regulates MSC chondrogenesis in a ROCK-dependent manner. Sci Adv. 2023;9(6):eade9497.

CAS  PubMed  PubMed Central  Google Scholar 

Li Y, Zhong Z, Xu C, Wu X, Li J, Tao W, et al. 3D micropattern force triggers YAP nuclear entry by transport across nuclear pores and modulates stem cells paracrine. Natl Sci Rev. 2023;10(8):nwad165.

CAS  PubMed  PubMed Central  Google Scholar 

Sart S, Tsai AC, Li Y, Ma T. Three-dimensional aggregates of mesenchymal stem cells: cellular mechanisms, biological properties, and applications. Tissue Eng Part B Rev. 2014;20(5):365–80.

PubMed  Google Scholar 

Zimmermann B. Assembly and disassembly of gap junctions during mesenchymal cell condensation and early chondrogenesis in limb buds of mouse embryos. J Anat. 1984;138(Pt 2):351–63.

PubMed  PubMed Central  Google Scholar 

Glimm T, Zhang J, Shen Y-Q, Newman SA. Reaction–Diffusion systems and external morphogen gradients: the Two-Dimensional case, with an application to skeletal pattern formation. Bull Math Biol. 2011;74(3):666–87.

PubMed  Google Scholar 

Barna M, Niswander L. Visualization of cartilage formation: insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell. 2007;12(6):931–41.

CAS  PubMed  Google Scholar 

Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, Dahn R, et al. Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science. 2012;338(6113):1476–80.

CAS  PubMed  PubMed Central  Google Scholar 

Bhat R, Lerea KM, Peng H, Kaltner H, Gabius HJ, Newman SA. A regulatory network of two galectins mediates the earliest steps of avian limb skeletal morphogenesis. BMC Dev Biol. 2011;11:6.

CAS  PubMed  PubMed Central  Google Scholar 

Newman SA, Bhat R. Activator-inhibitor dynamics of vertebrate limb pattern formation. Birth Defects Res C Embryo Today. 2007;81(4):305–19.

CAS  PubMed  Google Scholar 

Glimm T, Kazmierczak B, Newman SA, Bhat R. A two-galectin network establishes mesenchymal condensation phenotype in limb development. Math Biosci. 2023;365:109054.

CAS  PubMed  Google Scholar 

Hall BK, Miyake T. All for one and one for all: condensations and the initiation of skeletal development. BioEssays. 2000;22(2):138–47.

CAS  PubMed  Google Scholar 

Vainio S, Thesleff I. Sequential induction of syndecan, Tenascin and cell proliferation associated with mesenchymal cell condensation during early tooth development. Differentiation. 1992;50(2):97–105.

CAS  PubMed  Google Scholar 

Tomasek JJ, Mazurkiewicz JE, Newman SA. Nonuniform distribution of fibronectin during avian limb development. Dev Biol. 1982;90(1):118–26.

CAS  PubMed  Google Scholar 

Dessau W, von der Mark H, von der Mark K, Fischer S. Changes in the patterns of collagens and fibronectin during limb-bud chondrogenesis. J Embryol Exp Morphol. 1980;57:51–60.

CAS  PubMed  Google Scholar 

Krivanek J, Soldatov RA, Kastriti ME, Chontorotzea T, Herdina AN, Petersen J, et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat Commun. 2020;11(1):4816.

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