The ‘straight mouse’: defining anatomical axes in 3D embryo models

Abstract A primary objective of the eMouseAtlas Project is to enable 3D spatial mapping of whole embryo gene expression data to capture complex 3D patterns for indexing, visualization, cross-comparison and analysis. For this we have developed a spatio-temporal framework based on 3D models of embryos at different stages of development coupled with an anatomical ontology. Here we introduce a method of defining coordinate axes that correspond to the anatomical or biologically relevant anterior–posterior (A–P), dorsal–ventral (D–V) and left–right (L–R) directions. These enable more sophisticated query and analysis of the data with biologically relevant associations, and provide novel data visualizations that can reveal patterns that are otherwise difficult to detect in the standard 3D coordinate space. These anatomical coordinates are defined using the concept of a ‘straight mouse-embryo’ within which the anatomical coordinates are Cartesian. The straight embryo model has been mapped via a complex non-linear transform onto the standard embryo model. We explore the utility of this anatomical coordinate system in elucidating the spatial relationship of spatially mapped embryonic ‘Fibroblast growth factor’ gene expression patterns, and we discuss the importance of this technology in summarizing complex multimodal mouse embryo image data from gene expression and anatomy studies. Database URL: www.emouseatlas.org

[1]  M. Taketo,et al.  Wnt9b-dependent FGF signaling is crucial for outgrowth of the nasal and maxillary processes during upper jaw and lip development , 2012, Development.

[2]  Karl Theiler,et al.  The House Mouse: Atlas of Embryonic Development , 1972 .

[3]  Philippe Soriano,et al.  Fgfr1 regulates development through the combinatorial use of signaling proteins , 2015, Genes & development.

[4]  Charles Watson,et al.  The Mouse Nervous System. , 2012 .

[5]  V. French,et al.  Distal regeneration and symmetry. , 1981, Science.

[6]  D'arcy W. Thompson.  On Growth and Form , 1945 .

[7]  J. Golden,et al.  Patterning the developing diencephalon , 2007, Brain Research Reviews.

[8]  P. Trainor,et al.  Disrupting hedgehog and WNT signaling interactions promotes cleft lip pathogenesis. , 2014, The Journal of clinical investigation.

[9]  Richard Baldock,et al.  Kaufman’s Atlas of Mouse Development Supplement: With Coronal Sections , 2015 .

[10]  V. French,et al.  Pattern regulation in epimorphic fields. , 1976, Science.

[11]  J. Hecksher-Sørensen,et al.  Optical Projection Tomography as a Tool for 3D Microscopy and Gene Expression Studies , 2002, Science.

[12]  C. Tabin,et al.  Sonic hedgehog mediates the polarizing activity of the ZPA , 1993, Cell.

[13]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[14]  Albert Burger,et al.  Anatomical Ontologies: Linking Names to Places in Biology , 2008, Anatomy Ontologies for Bioinformatics.

[15]  G. Fuller,et al.  Nervus terminalis (cranial nerve zero) in the adult human. , 1990, Clinical neuropathology.

[16]  Bill Hill,et al.  Constrained distance transforms for spatial atlas registration , 2015, BMC Bioinformatics.

[17]  A. McMahon,et al.  Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. , 1995, Development.

[18]  Xiao Liu,et al.  Straightening Caenorhabditis elegans images , 2007, Bioinform..

[19]  M. Depew,et al.  Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. , 1999, Genes & development.

[20]  Chris Armit,et al.  Digital Graphical Resources and Developmental Anatomy in the Mouse , 2016 .

[21]  R. Baldock,et al.  eMouseAtlas informatics: embryo atlas and gene expression database , 2015, Mammalian Genome.

[22]  Richard Baldock,et al.  eMouseAtlas, EMAGE, and the spatial dimension of the transcriptome , 2012, Mammalian Genome.

[23]  Naohito Takatori,et al.  PII: S0925-4773(02)00150-8 , 2002 .

[24]  A. Reymond,et al.  A High-Resolution Anatomical Atlas of the Transcriptome in the Mouse Embryo , 2011, PLoS biology.

[25]  Chris Mungall,et al.  Nose to tail, roots to shoots: spatial descriptors for phenotypic diversity in the Biological Spatial Ontology , 2014, J. Biomed. Semant..

[26]  Joseph C. Pearson,et al.  Modulating Hox gene functions during animal body patterning , 2005, Nature Reviews Genetics.

[27]  B. Kingsbury.  Branchiomerism and the theory of head segmentation , 1926 .

[28]  E. Puelles,et al.  Molecular Regionalization of the Developing Neural Tube , 2012 .