Cell segmentation-free inference of cell types from in situ transcriptomics data

Multiplexed fluorescence in situ hybridization techniques have enabled cell-type identification, linking transcriptional heterogeneity with spatial heterogeneity of cells. However, inaccurate cell segmentation reduces the efficacy of cell-type identification and tissue characterization. Here, we present a method called Spot-based Spatial cell-type Analysis by Multidimensional mRNA density estimation (SSAM), a robust cell segmentation-free computational framework for identifying cell-types and tissue domains in 2D and 3D. SSAM is applicable to a variety of in situ transcriptomics techniques and capable of integrating prior knowledge of cell types. We apply SSAM to three mouse brain tissue images: the somatosensory cortex imaged by osmFISH, the hypothalamic preoptic region by MERFISH, and the visual cortex by multiplexed smFISH. Here, we show that SSAM detects regions occupied by known cell types that were previously missed and discovers new cell types.

[1]  Aric Hagberg,et al.  Exploring Network Structure, Dynamics, and Function using NetworkX , 2008 .

[2]  Fabian J Theis,et al.  Diffusion pseudotime robustly reconstructs lineage branching , 2016, Nature Methods.

[3]  Long Cai,et al.  Giotto, a pipeline for integrative analysis and visualization of single-cell spatial transcriptomic data , 2019, bioRxiv.

[4]  Lucas Pelkmans,et al.  Image-based transcriptomics in thousands of single human cells at single-molecule resolution , 2013, Nature Methods.

[5]  Patrik L. Ståhl,et al.  Visualization and analysis of gene expression in tissue sections by spatial transcriptomics , 2016, Science.

[6]  Allon M Klein,et al.  Scrublet: Computational Identification of Cell Doublets in Single-Cell Transcriptomic Data. , 2019, Cell systems.

[7]  Fabian J. Theis,et al.  destiny: diffusion maps for large-scale single-cell data in R , 2015, Bioinform..

[8]  R. Satija,et al.  Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression , 2019, Genome Biology.

[9]  S. Teichmann,et al.  Exponential scaling of single-cell RNA-seq in the past decade , 2017, Nature Protocols.

[10]  Hans-Peter Kriegel,et al.  OPTICS: ordering points to identify the clustering structure , 1999, SIGMOD '99.

[11]  R. Satija,et al.  Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression , 2019, Genome Biology.

[12]  Michael Garland,et al.  Surface simplification using quadric error metrics , 1997, SIGGRAPH.

[13]  Chenglong Xia,et al.  Spatial transcriptome profiling by MERFISH reveals subcellular RNA compartmentalization and cell cycle-dependent gene expression , 2019, Proceedings of the National Academy of Sciences.

[14]  B. S. Manjunath,et al.  Accurate 3D Cell Segmentation Using Deep Features and CRF Refinement , 2019, 2019 IEEE International Conference on Image Processing (ICIP).

[15]  S. Teichmann,et al.  SpatialDE: identification of spatially variable genes , 2018, Nature Methods.

[16]  Erik Sundström,et al.  RNA velocity of single cells , 2018, Nature.

[17]  Michael L. Waskom,et al.  mwaskom/seaborn: v0.9.0 (July 2018) , 2018 .

[18]  Sanjay Tyagi,et al.  Mechanism of mRNA transport in the nucleus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Takeshi Sakurai,et al.  Identification of a population of sleep-active cerebral cortex neurons , 2008, Proceedings of the National Academy of Sciences.

[20]  Jeffrey M. Perkel,et al.  Starfish enterprise: finding RNA patterns in single cells , 2019, Nature.

[21]  Filippo Molinari,et al.  Automated Segmentation of Fluorescence Microscopy Images for 3D Cell Detection in human-derived Cardiospheres , 2019, Scientific Reports.

[22]  I. Amit,et al.  Single-cell spatial reconstruction reveals global division of labor in the mammalian liver , 2016, Nature.

[23]  Hannah A. Pliner,et al.  Reversed graph embedding resolves complex single-cell trajectories , 2017, Nature Methods.

[24]  Richard Bonneau,et al.  High-definition spatial transcriptomics for in situ tissue profiling , 2019, Nature Methods.

[25]  Philip Lijnzaad,et al.  CHETAH: a selective, hierarchical cell type identification method for single-cell RNA sequencing , 2019, bioRxiv.

[26]  Roland Eils,et al.  Cell segmentation-free inference of cell types from in situ transcriptomics data , 2019, Nature Communications.

[27]  Jens Hjerling-Leffler,et al.  Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system , 2016, Science.

[28]  Thomas A Caswell,et al.  matplotlib/matplotlib v3.1.3 , 2020 .

[29]  Paolo Cignoni,et al.  MeshLab: an Open-Source Mesh Processing Tool , 2008, Eurographics Italian Chapter Conference.

[30]  William J. Schroeder,et al.  Overview of Visualization , 2005, The Visualization Handbook.

[31]  Hans-Peter Kriegel,et al.  A Density-Based Algorithm for Discovering Clusters in Large Spatial Databases with Noise , 1996, KDD.

[32]  S. Linnarsson,et al.  Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq , 2015, Science.

[33]  S. Fortunato,et al.  Resolution limit in community detection , 2006, Proceedings of the National Academy of Sciences.

[34]  Erlend Hodneland,et al.  CellSegm - a MATLAB toolbox for high-throughput 3D cell segmentation , 2013, Source Code for Biology and Medicine.

[35]  Aaron Watters,et al.  Spatiotemporal dynamics of molecular pathology in amyotrophic lateral sclerosis , 2018, Science.

[36]  M. Rosenblatt Remarks on Some Nonparametric Estimates of a Density Function , 1956 .

[37]  Jisha John,et al.  A review on cell detection and segmentation in microscopic images , 2017, 2017 International Conference on Circuit ,Power and Computing Technologies (ICCPCT).

[38]  Wesam M. Ashour,et al.  EOPTICS “Enhancement Ordering Points to Identify the Clustering Structure” , 2012 .

[39]  F. Fujiyama,et al.  Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex , 2005 .

[40]  Carolina Wählby,et al.  In situ sequencing for RNA analysis in preserved tissue and cells , 2013, Nature Methods.

[41]  Peng Yin,et al.  SABER enables amplified and multiplexed imaging of RNA and DNA in cells and tissues , 2019, Nature Methods.

[42]  Hugues Hoppe,et al.  New quadric metric for simplifying meshes with appearance attributes , 1999, Proceedings Visualization '99 (Cat. No.99CB37067).

[43]  Kun Zhang,et al.  Fluorescent in situ sequencing (FISSEQ) of RNA for gene expression profiling in intact cells and tissues , 2015, Nature Protocols.

[44]  Fusheng Wang,et al.  Automated cell segmentation with 3D fluorescence microscopy images , 2015, 2015 IEEE 12th International Symposium on Biomedical Imaging (ISBI).

[45]  A. Einstein Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen [AdP 17, 549 (1905)] , 2005, Annalen der Physik.

[46]  Lars E. Borm,et al.  Spatial organization of the somatosensory cortex revealed by osmFISH , 2018, Nature Methods.

[47]  Sebastian J. Streichan,et al.  Identification of a neural crest stem cell niche by Spatial Genomic Analysis , 2017, Nature Communications.

[48]  Allan R. Jones,et al.  Conserved cell types with divergent features in human versus mouse cortex , 2019, Nature.

[49]  X. Zhuang,et al.  Spatially resolved, highly multiplexed RNA profiling in single cells , 2015, Science.

[50]  William E. Allen,et al.  Three-dimensional intact-tissue sequencing of single-cell transcriptional states , 2018, Science.

[51]  Richard Bonneau,et al.  High-density spatial transcriptomics arrays for in situ tissue profiling , 2019, bioRxiv.

[52]  M. Ankerst,et al.  OPTICS: Ordering Points To Identify the Clustering Structure , 1999, SIGMOD Conference.

[53]  V. A. Epanechnikov Non-Parametric Estimation of a Multivariate Probability Density , 1969 .

[54]  E. Parzen On Estimation of a Probability Density Function and Mode , 1962 .

[55]  William Schroeder,et al.  The Visualization Toolkit: An Object-Oriented Approach to 3-D Graphics , 1997 .

[56]  F. Fujiyama,et al.  Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex , 2005, The European journal of neuroscience.

[57]  Catherine E. Braine,et al.  Spatiotemporal dynamics of molecular pathology in amyotrophic lateral sclerosis , 2018, Science.

[58]  Timur Zhiyentayev,et al.  Single-cell in situ RNA profiling by sequential hybridization , 2014, Nature Methods.

[59]  Fabian J Theis,et al.  Current best practices in single‐cell RNA‐seq analysis: a tutorial , 2019, Molecular systems biology.

[60]  Christopher J. Cronin,et al.  Dynamics and Spatial Genomics of the Nascent Transcriptome by Intron seqFISH , 2018, Cell.

[61]  Paul Hoffman,et al.  Integrating single-cell transcriptomic data across different conditions, technologies, and species , 2018, Nature Biotechnology.

[62]  Fabian J Theis,et al.  The Human Cell Atlas , 2017, bioRxiv.

[63]  Lars E. Borm,et al.  Molecular Architecture of the Mouse Nervous System , 2018, Cell.

[64]  L. Cai,et al.  Giotto: a toolbox for integrative analysis and visualization of spatial expression data , 2021, Genome Biology.

[65]  Cole Trapnell,et al.  The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells , 2014, Nature Biotechnology.

[66]  Carolyn R. Bertozzi,et al.  Mammalian Y RNAs are modified at discrete guanosine residues with N-glycans , 2019, bioRxiv.

[67]  Michael M. Kazhdan,et al.  Poisson surface reconstruction , 2006, SGP '06.

[68]  Allan R. Jones,et al.  Shared and distinct transcriptomic cell types across neocortical areas , 2018, Nature.

[69]  Guo-Cheng Yuan,et al.  Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+ , 2019, Nature.

[70]  Leland McInnes,et al.  hdbscan: Hierarchical density based clustering , 2017, J. Open Source Softw..

[71]  R. Metzler,et al.  Manipulation and Motion of Organelles and Single Molecules in Living Cells. , 2017, Chemical reviews.

[72]  Eric S. Lander,et al.  Compressed sensing for imaging transcriptomics , 2019, bioRxiv.

[73]  Nimrod D. Rubinstein,et al.  Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region , 2018, Science.

[74]  Marcel J. T. Reinders,et al.  A comparison of automatic cell identification methods for single-cell RNA sequencing data , 2019, Genome Biology.

[75]  Kan Liu,et al.  Giotto, a toolbox for integrative analysis and visualization of spatial expression data , 2020 .

[76]  Christof Koch,et al.  Adult Mouse Cortical Cell Taxonomy by Single Cell Transcriptomics , 2016, Nature Neuroscience.

[77]  Evan Z. Macosko,et al.  Slide-seq: A scalable technology for measuring genome-wide expression at high spatial resolution , 2019, Science.

[78]  L. Cai,et al.  In Situ Transcription Profiling of Single Cells Reveals Spatial Organization of Cells in the Mouse Hippocampus , 2016, Neuron.

[79]  Michael M. Kazhdan,et al.  Screened poisson surface reconstruction , 2013, TOGS.

[80]  Atul J. Butte,et al.  Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage , 2018, Nature Immunology.

[81]  Joakim Lundeberg,et al.  Multidimensional transcriptomics provides detailed information about immune cell distribution and identity in HER2+ breast tumors , 2018, bioRxiv.