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An Epigenetic Model for Pigment Patterning Based on Mechanical and Cellular Interactions LORENA CABALLERO1,2,3∗, MARIANA BEN´ITEZ3,4,5, ELENA R

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An Epigenetic Model for Pigment Patterning Based on Mechanical and Cellular Interactions LORENA CABALLERO1,2,3∗, MARIANA BEN´ITEZ3,4,5, ELENA R RESEARCH ARTICLE An Epigenetic Model for Pigment Patterning Based on Mechanical and Cellular Interactions LORENA CABALLERO1,2,3∗, MARIANA BEN´ITEZ3,4,5, ELENA R. ALVAREZ-BUYLLA3,6, SERGIO HERNANDEZ´ 3, 7 1,3 ALEJANDRO V. ARZOLA , AND GERMINAL COCHO 1Departamento de Sistemas Complejos Instituto de F´ısica, Universidad Nacional Autonoma´ de Mexico,´ Ciudad de Mexico,´ DF, Mexico´ 2Posgrado en Ciencias Biologicas,´ Universidad Nacional Autonoma´ de Mexico,´ Ciudad de Mexico,´ DF, Mexico´ 3C3, Centro de Ciencias de la Complejidad, Universidad Nacional Autonoma´ de Mexico,´ Ciudad de Mexico,´ DF, Mexico´ 4Department of Functional Genomics and Proteomics, Masaryk University, Brno, Czech Republic 5CEITEC-Central European Institute of Technology, Masaryk University, Brno, Czech Republic 6Laboratorio de Genetica´ Molecular Desarrollo y Evolucion´ en Plantas Instituto de Ecolog´ıa, Universidad Nacional Autonoma´ de Mexico,´ Ciudad de Mexico,´ DF, Mexico´ 7Institute of Scientific Instruments Academy of Sciences of the Czech Republic, Brno, Czech Republic ABSTRACT Pigment patterning in animals generally occurs during early developmental stages and has eco- logical, physiological, ethological, and evolutionary significance. Despite the relative simplicity of color patterns, their emergence depends upon multilevel complex processes. Thus, theoretical models have become necessary tools to further understand how such patterns emerge. Recent studies have reevaluated the importance of epigenetic, as well as genetic factors in developmen- tal pattern formation. Yet epigenetic phenomena, specially those related to physical constraints that might be involved in the emergence of color patterns, have not been fully studied. In this article, we propose a model of color patterning in which epigenetic aspects such as cell migra- tion, cell–tissue interactions, and physical and mechanical phenomena are central. This model considers that motile cells embedded in a fibrous, viscoelastic matrix—mesenchyme—can deform it in such a way that tension tracks are formed. We postulate that these tracks act, in turn, as guides for subsequent cell migration and establishment, generating long-range phenomenolog- ical interactions. We aim to describe some general aspects of this developmental phenomenon with a rather simple mathematical model. Then we discuss our model in the context of available experimental and morphological evidence for reptiles, amphibians, and fishes, and compare it with other patterning models. We also put forward novel testable predictions derived from our model, regarding, for instance, the localization of the postulated tension tracks, and we propose new experiments. Finally, we discuss how the proposed mechanism could constitute a dynamic patterning module accounting for pattern formation in many animal lineages. J. Exp. Zool. (Mol. Dev. Evol.) 318:209–223, 2012. © 2012 Wiley Periodicals, Inc. ´ ´ J. Exp. Zool. How to cite this article: Caballero L, Benıtez M, Alvarez-Buylla ER, Hernandez S, Arzola AV, (Mol. Dev. Evol.) Cocho G. 2012. An epigenetic model for pigment patterning based on mechanical and cellular 318:209–223, 2012 interactions. J. Exp. Zool. (Mol. Dev. Evol.) 318:209–223. © 2012 WILEY PERIODICALS, INC. 210 CABALLERO ET AL. Morphogenetic mechanisms and pattern formation have tradi- tion of organic organization in terms of internal dynamics and tionally been central topics in developmental biology, and more interaction, focusing on process and change” (Van Speybroeck recently in the search of explanations for pattern formation and et al., 2002: p. 33). The related term epigenetics, which combines evolution at the molecular genetic level (e.g., Parichy, 2006). epigenesis and genetics, was proposed by Waddington to rep- In this context, a valuable strategy for understanding the basic resent “a true synthesis between developmental processes and phenomena involved in the emergence, maintenance, and evolu- genetic action, which together bring the organism into being” tion of developmental patterns is to look for potentially generic (Van Speybroeck et al., 2002: p. 33). mechanisms by using modeling or other theoretical approaches. Based on this understanding of the epigenetic phenomena, we Color pattern formation has already been studied with generic analyze some physical mechanisms critical to the establishment dynamic reaction–diffusion (RD) models (Turing ’52; Gierer and of color patterns in the skin of reptiles, fishes, and amphibians, Meinhardt ’72). However, such models generally do not take and postulate them as potentially generic processes across evo- into account the cellular and tissue environments in which color lutionary lineages. These generic mechanisms could explain, at patterns arise (see, however, Cocho et al., ’87a,b; Moreira and least partially, some of the repeated patterns observed in ver- Deutsch, 2005; Deutsch and Dormann, 2005). In this article, we tebrates. In this case, we will consider the epigenetic processes postulate a simple mathematical model that considers that long- of pigment-cell migration and attraction, and the adhesive and range forces can emerge from viscoelastic and tensile properties mechanical interactions between pigments cells and the mes- of the mesenchymatic tissue, and that these forces, in conjunc- enchyme. tion with cell–cell interactions, may give rise to color patterns Pigment pattern formation can be traced to early stages in like those observed in different animal lineages. We, neverthe- the development of fishes, amphibians, and reptiles, and like less, do not argue that RD models and the model we postulate many key developmental processes, it involves the arrangement here necessarily exclude each other. of epithelial sheets and cells in relation with the mesenchyme Developmental biology recognizes that the emergence of new (Schock¨ and Perrimon, 2002). It is important to mention that patterns results from interactions among diverse molecular, cel- the mesenchyme, the embryonic tissue on which pigment cells lular, and environmental processes, and that epigenetic interac- (chromatophores) migrate during color patterning, is a fibrous tions play an essential role in development (Newman and Muller¨ tissue with few cells. This makes the mesenchyme a matrix 2000). It is important to note that in this work we use the term that is biphasic (consisting of both solid and uid fractions) and epigenetic to refer to a wide range of mechanisms, and not only viscoelastic (exhibiting both viscous and elastic characteristics to refer to heritable DNA modifications, such as methylation. We when deformed), which can show heterogeneous compression or regard as epigenetic mechanisms processes such as cell commu- tension patterns (Grinnell and Petroll, 2010). Given such prop- nication, cell–environment interactions, tensegrity, which gives erties of the mesenchymatic tissue, cells migrating and adhering structural stability to a system by means of tension–compression to it can reorient its fibers and deform the matrix in a way such or attraction–repulsion mechanisms, and other physicochemi- that tension lines are formed. This phenomenon has been ob- cal mechanisms (Waddington, ’62; Newman and Muller,¨ 2000; served in both in vivo and in vitro experimental setups (Table 1). Ingber, 2000, 2006, 2010). According to van Speybroeck and Moreover, it has been shown that such lines become guides for coauthors (2002) “epigenesis can be seen to approach the ques- subsequent cell migration and accumulation (Weiss, ’59; Grin- nell and Petroll, 2010; Fig. 1, Table 1). Contract grant sponsor: Posgrado en Ciencias Biologicas;´ Contract grant We hypothesize that the migration of chromatophores on the sponsor: Centro de Ciencias de la Complejidad, C3; Contract grant spon- mesenchyme, which is mediated by different types of junctions, sor: CONACyT, contract grant numbers: 81433, 81542, 90565; Contract such as the adherens junctions (Schock¨ and Perrimon 2002; Ya- grant sponsor: Red de CONACyT Complejidad, Ciencia y Sociedad; Contract mada et al., 2005), deforms the mesenchyme and gives rise to grant sponsor: PAPIIT, contract grant numbers: IN210408, IN229009-3, tension tracks to which chromatophores will tend to migrate and IN223607-3. where these cells will be more likely to establish. In a recent re- The present address of Mariana Ben´ıtez is Department of Functional Ge- view, Grinnell and Petroll (2010) offer a comprehensive account nomics and Proteomics, Institute of Experimental Biology, Faculty of Sci- ence, Masaryk University, CZ-625 00 Brno, Czech Republic of the mechanisms involved in the adhesion and migration of ∗Correspondence to: Lorena Caballero, Departamento de Sistemas Com- cells embedded in a viscoelastic matrix, and mention that cell plejos, Instituto de F´ısica, Universidad Nacional Autonoma´ de Mexico,´ traction and contraction can deform viscoelastic tissues by es- Posgrado en Ciencias Biologicas,´ Universidad Nacional Autonoma´ de tablishing adhesive interactions and locally contracting the ma- Mexico,´ Ciudad de Mexico,´ DF, Mexico,´ Mexico´ 04510 . E-mail: lrnca- trix. Importantly, this deformation results in long-range forces [email protected] Received 28 February 2011; Revised 2 August 2011; Accepted 2 Novem- regulating subsequent cell migration and establishment (Weiss, ber 2011 ’59; Fig. 1). Published online 4 December 2011 in Wiley Online Library (wileyonline Almost 30 years ago, Oster and Murray (Oster et al., ’83; Mur- library.com). DOI: 10.1002/jez.22007 ray et al., ’83; Murray et al., ’88)
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