XB-ART-48333
J R Soc Interface
2014 Mar 06;1192:20130918. doi: 10.1098/rsif.2013.0918.
Show Gene links
Show Anatomy links
A linear-encoding model explains the variability of the target morphology in regeneration.
Lobo D
,
Solano M
,
Bubenik GA
,
Levin M
.
???displayArticle.abstract???
A fundamental assumption of today's molecular genetics paradigm is that complex morphology emerges from the combined activity of low-level processes involving proteins and nucleic acids. An inherent characteristic of such nonlinear encodings is the difficulty of creating the genetic and epigenetic information that will produce a given self-assembling complex morphology. This 'inverse problem' is vital not only for understanding the evolution, development and regeneration of bodyplans, but also for synthetic biology efforts that seek to engineer biological shapes. Importantly, the regenerative mechanisms in deer antlers, planarian worms and fiddler crabs can solve an inverse problem: their target morphology can be altered specifically and stably by injuries in particular locations. Here, we discuss the class of models that use pre-specified morphological goal states and propose the existence of a linear encoding of the target morphology, making the inverse problem easy for these organisms to solve. Indeed, many model organisms such as Drosophila, hydra and Xenopus also develop according to nonlinear encodings producing linear encodings of their final morphologies. We propose the development of testable models of regeneration regulation that combine emergence with a top-down specification of shape by linear encodings of target morphology, driving transformative applications in biomedicine and synthetic bioengineering.
???displayArticle.pubmedLink??? 24402915
???displayArticle.pmcLink??? PMC3899861
???displayArticle.link??? J R Soc Interface
References [+] :
Aboobaker,
Planarian stem cells: a simple paradigm for regeneration.
2011, Pubmed
Aboobaker, Planarian stem cells: a simple paradigm for regeneration. 2011, Pubmed
Adami, What is complexity? 2002, Pubmed
Adell, Gradients in planarian regeneration and homeostasis. 2010, Pubmed
Agata, Brain regeneration from pluripotent stem cells in planarian. 2008, Pubmed
Agata, Intercalary regeneration in planarians. 2003, Pubmed
Astigiano, Fate of embryonal carcinoma cells injected into postimplantation mouse embryos. 2005, Pubmed
Backwell, What are the consequences of being left-clawed in a predominantly right-clawed fiddler crab? 2007, Pubmed
Baddour, Organ repair and regeneration: an overview. 2012, Pubmed
Baker, Master regulatory genes; telling them what to do. 2001, Pubmed
Ball, Forging patterns and making waves from biology to geology: a commentary on Turing (1952) 'The chemical basis of morphogenesis'. 2015, Pubmed
Beane, Bioelectric signaling regulates head and organ size during planarian regeneration. 2013, Pubmed
Beane, A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. 2011, Pubmed
Beloussov, Mechanically based generative laws of morphogenesis. 2008, Pubmed
Beloussov, Morphogenesis as a macroscopic self-organizing process. 2012, Pubmed
Beloussov, Life of Alexander G. Gurwitsch and his relevant contribution to the theory of morphogenetic fields. 1997, Pubmed
Bissell, The organizing principle: microenvironmental influences in the normal and malignant breast. 2002, Pubmed
Bonabeau, From classical models of morphogenesis to agent-based models of pattern formation. 1997, Pubmed
Bongard, Resilient machines through continuous self-modeling. 2006, Pubmed
Bongard, Automated reverse engineering of nonlinear dynamical systems. 2007, Pubmed
Brockes, Comparative aspects of animal regeneration. 2008, Pubmed
Broun, Formation of the head organizer in hydra involves the canonical Wnt pathway. 2005, Pubmed
Bruzzone, The cellular Internet: on-line with connexins. 1996, Pubmed
Bubenik, Trophic responses to trauma in growing antlers. 1965, Pubmed
Bubenik, The effect of neurogenic stimulation on the development and growth of bony tissues. 1982, Pubmed
Chakravarthy, On Hebbian-like adaptation in heart muscle: a proposal for 'cardiac memory'. 1997, Pubmed
Chang, Diversity, topographic differentiation, and positional memory in human fibroblasts. 2002, Pubmed
Chanson, Effects of n-alcohols on junctional coupling and amylase secretion of pancreatic acinar cells. 1989, Pubmed
Coen, The genetics of geometry. 2004, Pubmed
Cohen, Explaining a complex living system: dynamics, multi-scaling and emergence. 2007, Pubmed
Cooke, Scale of body pattern adjusts to available cell number in amphibian embryos. 1981, Pubmed , Xenbase
Crick, Diffusion in embryogenesis. 1970, Pubmed
Cui, Quantitative control of organ shape by combinatorial gene activity. 2010, Pubmed
Currey, The mechanical properties of red deer antler bone when used in fighting. 2009, Pubmed
Das, Ecdysteroid receptor signaling disruption obstructs blastemal cell proliferation during limb regeneration in the fiddler crab, Uca pugilator. 2013, Pubmed
Dinicola, A systems biology approach to cancer: fractals, attractors, and nonlinear dynamics. 2011, Pubmed
Eldar, Elucidating mechanisms underlying robustness of morphogen gradients. 2004, Pubmed
Frischer, An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. 1986, Pubmed
Gentile, The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. 2011, Pubmed
Goss, Problems of antlerogesis. 1970, Pubmed
Gu, Expression and localization of insulin-like growth factor-I in four parts of the red deer antler. 2007, Pubmed
Gunamalai, Hormonal coordination of molting and female reproduction by ecdysteroids in the mole crab Emerita asiatica (Milne Edwards). 2004, Pubmed
Haldi, Human melanoma cells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. 2006, Pubmed
Hamant, Developmental patterning by mechanical signals in Arabidopsis. 2008, Pubmed
Handberg-Thorsager, Stem cells and regeneration in planarians. 2008, Pubmed
Harding, Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. 1989, Pubmed
Hendrix, Reprogramming metastatic tumour cells with embryonic microenvironments. 2007, Pubmed
Hornby, Creating high-level components with a generative representation for body-brain evolution. 2002, Pubmed
Howard, Regulatory interactions between the segmentation genes fushi tarazu, hairy, and engrailed in the Drosophila blastoderm. 1986, Pubmed
Hueber, Improving Hox protein classification across the major model organisms. 2010, Pubmed
Imokawa, Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. 1997, Pubmed
Jablonka, Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. 2009, Pubmed
Jaeger, Life's attractors : understanding developmental systems through reverse engineering and in silico evolution. 2012, Pubmed
Joachimczak, Evolution of robustness to damage in artificial 3-dimensional development. 2012, Pubmed
Kierdorf, Deer antler regeneration: cells, concepts, and controversies. 2007, Pubmed
Kierdorf, Improbable appendages: Deer antler renewal as a unique case of mammalian regeneration. 2009, Pubmed
Kierdorf, Antler regrowth as a form of epimorphic regeneration in vertebrates - a comparative view. 2012, Pubmed
Kobayashi, Ectopic pharynxes arise by regional reorganization after anterior/posterior chimera in planarians. 1999, Pubmed
Kragl, Cells keep a memory of their tissue origin during axolotl limb regeneration. 2009, Pubmed
Kumar, Nerve dependence in tissue, organ, and appendage regeneration. 2012, Pubmed , Xenbase
Lecuit, Orchestrating size and shape during morphogenesis. 2007, Pubmed
Lee, The fate of human malignant melanoma cells transplanted into zebrafish embryos: assessment of migration and cell division in the absence of tumor formation. 2005, Pubmed
Levin, Large-scale biophysics: ion flows and regeneration. 2007, Pubmed
Levin, Bioelectric mechanisms in regeneration: Unique aspects and future perspectives. 2009, Pubmed
Levin, Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients. 2012, Pubmed
Levin, The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology and cancer. 2011, Pubmed
Levin, Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. 2012, Pubmed
Levin, Gap junctional communication in morphogenesis. 2007, Pubmed
Levin, Reprogramming cells and tissue patterning via bioelectrical pathways: molecular mechanisms and biomedical opportunities. 2013, Pubmed
Lewis, A gene complex controlling segmentation in Drosophila. 1978, Pubmed
Lewis, From signals to patterns: space, time, and mathematics in developmental biology. 2008, Pubmed , Xenbase
Li, Morphogenetic aspects of deer antler development. 2012, Pubmed
Lindenmayer, Mathematical models for cellular interactions in development. I. Filaments with one-sided inputs. 1968, Pubmed
Lobo, Evolution of form and function in a model of differentiated multicellular organisms with gene regulatory networks. 2010, Pubmed
Lobo, Evolutionary development of tensegrity structures. 2010, Pubmed
Lobo, Modeling planarian regeneration: a primer for reverse-engineering the worm. 2012, Pubmed
Lobo, Towards a bioinformatics of patterning: a computational approach to understanding regulative morphogenesis. 2013, Pubmed
Lobo, Planform: an application and database of graph-encoded planarian regenerative experiments. 2013, Pubmed
Mammoto, Mechanical control of tissue and organ development. 2010, Pubmed
Mariappan, Decapod crustacean chelipeds: an overview. 2000, Pubmed
MARSH, Electrical control of growth polarity in regenerating Dugesia tigrina. 1947, Pubmed
Martin, Parallels between tissue repair and embryo morphogenesis. 2004, Pubmed
Martinez-Arias, Parasegments and compartments in the Drosophila embryo. , Pubmed
McCaig, Electrical dimensions in cell science. 2009, Pubmed
Meinhardt, Modeling pattern formation in hydra: a route to understanding essential steps in development. 2012, Pubmed
Meinhardt, Pattern formation by local self-activation and lateral inhibition. 2000, Pubmed
Menshykau, Branch mode selection during early lung development. 2012, Pubmed
Mondia, Patterned femtosecond-laser ablation of Xenopus laevis melanocytes for studies of cell migration, wound repair, and developmental processes. 2011, Pubmed , Xenbase
Mondia, Long-distance signals are required for morphogenesis of the regenerating Xenopus tadpole tail, as shown by femtosecond-laser ablation. 2011, Pubmed , Xenbase
Nieto-Diaz, Deer antler innervation and regeneration. 2012, Pubmed
Nogi, Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. 2005, Pubmed
Nüsslein-Volhard, Mutations affecting segment number and polarity in Drosophila. 1980, Pubmed
Okasha, Emergence, hierarchy and top-down causation in evolutionary biology. 2012, Pubmed
Oviedo, Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. 2003, Pubmed
Oviedo, Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. 2010, Pubmed
Pai, Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. 2012, Pubmed , Xenbase
Pellettieri, Cell death and tissue remodeling in planarian regeneration. 2010, Pubmed
Prusinkiewicz, Computational models of plant development and form. 2012, Pubmed
Reddien, Fundamentals of planarian regeneration. 2004, Pubmed
Reinhardt, HyBMP5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra. 2004, Pubmed
Rinn, Anatomic demarcation by positional variation in fibroblast gene expression programs. 2006, Pubmed
Sachdeva, Bistable dynamics of cardiac cell models coupled by dynamic gap junctions linked to cardiac memory. 2010, Pubmed
Saló, The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). 2006, Pubmed
Sarnat, The brain of the planarian as the ancestor of the human brain. 1985, Pubmed
Schmidt, Distilling free-form natural laws from experimental data. 2009, Pubmed
Schneuwly, Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. , Pubmed
Seno, A mathematical modelling for the cheliped regeneration with handedness in fiddler crab. 2007, Pubmed
Singer, Trophic functions of the neuron. VI. Other trophic systems. Neurotrophic control of limb regeneration in the newt. 1974, Pubmed
Smith, HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. 2000, Pubmed
Soto, Emergentism as a default: cancer as a problem of tissue organization. 2005, Pubmed
Soto, The tissue organization field theory of cancer: a testable replacement for the somatic mutation theory. 2011, Pubmed
Stanley, A hypercube-based encoding for evolving large-scale neural networks. 2009, Pubmed
Stocum, Looking proximally and distally: 100 years of limb regeneration and beyond. 2011, Pubmed , Xenbase
Suttie, Regrowth of amputated velvet antlers with and without innervation. 1985, Pubmed
Tseng, Cracking the bioelectric code: Probing endogenous ionic controls of pattern formation. 2013, Pubmed
Vandenberg, V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. 2011, Pubmed , Xenbase
Vandenberg, Normalized shape and location of perturbed craniofacial structures in the Xenopus tadpole reveal an innate ability to achieve correct morphology. 2012, Pubmed , Xenbase
Wang, Regeneration, repair and remembering identity: the three Rs of Hox gene expression. 2009, Pubmed
WISLOCKI, The occurrence and function of nerves in the growing antlers of deer. 1946, Pubmed
Wolpert, Positional information and the spatial pattern of cellular differentiation. 1969, Pubmed