The Pediatric Cell Atlas: Defining the Growth Phase of Human Development at Single-Cell Resolution

Deanne M Taylor; Bruce J Aronow; Kai Tan; Kathrin Bernt; Nathan Salomonis; Casey S Greene; Alina Frolova; Sarah E Henrickson; Andrew Wells; Liming Pei; Jyoti K Jaiswal; Jeffrey Whitsett; Kathryn E Hamilton; Sonya A MacParland; Judith Kelsen; Robert O Heuckeroth; S Steven Potter; Laura A Vella; Natalie A Terry; Louis R Ghanem; Benjamin C Kennedy; Ingo Helbig; Kathleen E Sullivan; Leslie Castelo-Soccio; Arnold Kreigstein; Florian Herse; Martijn C Nawijn; Gerard H Koppelman; Melissa Haendel; Nomi L Harris; Jo Lynne Rokita; Yuanchao Zhang; Aviv Regev; Orit Rozenblatt-Rosen; Jennifer E Rood; Timothy L Tickle; Roser Vento-Tormo; Saif Alimohamed; Monkol Lek; Jessica C Mar; Kathleen M Loomes; David M Barrett; Prech Uapinyoying; Alan H Beggs; Pankaj B Agrawal; Yi-Wen Chen; Amanda B Muir; Lana X Garmire; Scott B Snapper; Javad Nazarian; Steven H Seeholzer; Hossein Fazelinia; Larry N Singh; Robert B Faryabi; Pichai Raman; Noor Dawany; Hongbo Michael Xie; Batsal Devkota; Sharon J Diskin; Stewart A Anderson; Eric F Rappaport; William Peranteau; Kathryn A Wikenheiser-Brokamp; Sarah Teichmann; Douglas Wallace; Tao Peng; Yang-Yang Ding; Man S Kim; Yi Xing; Sek Won Kong; Carsten G Bönnemann; Kenneth D Mandl; Peter S White

doi:10.1016/j.devcel.2019.03.001

The Pediatric Cell Atlas: Defining the Growth Phase of Human Development at Single-Cell Resolution

Dev Cell. 2019 Apr 8;49(1):10-29. doi: 10.1016/j.devcel.2019.03.001. Epub 2019 Mar 28.

Authors

Deanne M Taylor¹, Bruce J Aronow², Kai Tan³, Kathrin Bernt⁴, Nathan Salomonis⁵, Casey S Greene⁶, Alina Frolova⁷, Sarah E Henrickson⁸, Andrew Wells⁹, Liming Pei¹⁰, Jyoti K Jaiswal¹¹, Jeffrey Whitsett¹², Kathryn E Hamilton¹³, Sonya A MacParland¹⁴, Judith Kelsen¹³, Robert O Heuckeroth¹⁵, S Steven Potter¹⁶, Laura A Vella¹⁷, Natalie A Terry¹³, Louis R Ghanem¹³, Benjamin C Kennedy¹⁸, Ingo Helbig¹⁹, Kathleen E Sullivan⁸, Leslie Castelo-Soccio²⁰, Arnold Kreigstein²¹, Florian Herse²², Martijn C Nawijn²³, Gerard H Koppelman²⁴, Melissa Haendel²⁵, Nomi L Harris²⁶, Jo Lynne Rokita²⁷, Yuanchao Zhang²⁸, Aviv Regev²⁹, Orit Rozenblatt-Rosen³⁰, Jennifer E Rood³⁰, Timothy L Tickle³¹, Roser Vento-Tormo³², Saif Alimohamed⁵, Monkol Lek³³, Jessica C Mar³⁴, Kathleen M Loomes¹³, David M Barrett⁴, Prech Uapinyoying³⁵, Alan H Beggs³⁶, Pankaj B Agrawal³⁷, Yi-Wen Chen¹¹, Amanda B Muir¹³, Lana X Garmire³⁸, Scott B Snapper³⁹, Javad Nazarian¹¹, Steven H Seeholzer⁴⁰, Hossein Fazelinia⁴¹, Larry N Singh⁴², Robert B Faryabi⁴³, Pichai Raman²⁷, Noor Dawany²⁷, Hongbo Michael Xie²⁷, Batsal Devkota²⁷, Sharon J Diskin⁴, Stewart A Anderson⁴⁴, Eric F Rappaport⁴⁵, William Peranteau⁴⁶, Kathryn A Wikenheiser-Brokamp⁴⁷, Sarah Teichmann⁴⁸, Douglas Wallace⁴⁹, Tao Peng⁵⁰, Yang-Yang Ding⁴, Man S Kim²⁷, Yi Xing⁵¹, Sek Won Kong⁵², Carsten G Bönnemann⁵³, Kenneth D Mandl⁵², Peter S White⁵

Affiliations

¹ Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, and the Department of Pediatrics, The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA. Electronic address: taylordm@email.chop.edu.
² Department of Biomedical Informatics, University of Cincinnati College of Medicine, and Cincinnati Children's Hospital Medical Center, Division of Biomedical Informatics, Cincinnati, OH 45229, USA. Electronic address: Bruce.Aronow@cchmc.org.
³ Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, and the Department of Pediatrics, The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA. Electronic address: tank1@email.chop.edu.
⁴ Division of Oncology, Department of Pediatrics, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA; Center for Childhood Cancer Research, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁵ Department of Biomedical Informatics, University of Cincinnati College of Medicine, and Cincinnati Children's Hospital Medical Center, Division of Biomedical Informatics, Cincinnati, OH 45229, USA.
⁶ Childhood Cancer Data Lab, Alex's Lemonade Stand Foundation, Philadelphia, PA 19102, USA; Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
⁷ Institute of Molecular Biology and Genetics, National Academy of Science of Ukraine, Kyiv 03143, Ukraine.
⁸ Division of Allergy Immunology, Department of Pediatrics, The Children's Hospital of Philadelphia and the Institute for Immunology, the University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
⁹ Department of Pathology and Laboratory Medicine, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
¹⁰ Department of Pathology and Laboratory Medicine, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA; Center for Mitochondrial and Epigenomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
¹¹ Department of Genomics and Precision Medicine, George Washington University School of Medicine and Health Sciences, Washington, DC, USA; Center for Genetic Medicine Research, Children's National Medical Center, NW, Washington, DC, 20010-2970, USA.
¹² Cincinnati Children's Hospital Medical Center, Section of Neonatology, Perinatal and Pulmonary Biology, Perinatal Institute, Cincinnati, OH 45229, USA.
¹³ Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
¹⁴ Multi-Organ Transplant Program, Toronto General Hospital Research Institute, Departments of Laboratory Medicine and Pathobiology and Immunology, University of Toronto, Toronto, ON, Canada.
¹⁵ Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
¹⁶ Division of Developmental Biology, Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229, USA.
¹⁷ Division of Infectious Diseases, Department of Pediatrics, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
¹⁸ Division of Neurosurgery, Department of Surgery, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
¹⁹ Division of Neurology, Department of Pediatrics, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA; Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
²⁰ Department of Pediatrics, Section of Dermatology, The Children's Hospital of Philadelphia and University of Pennsylvania Perleman School of Medicine, Philadelphia, PA 19104, USA.
²¹ Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
²² Experimental and Clinical Research Center, A Joint Cooperation Between the Charité Medical Faculty and the Max-Delbrueck Center for Molecular Medicine, Berlin, Germany.
²³ Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen, and Groningen Research Institute for Asthma and COPD (GRIAC), Groningen, the Netherlands.
²⁴ University of Groningen, University Medical Center Groningen, Beatrix Children's Hospital, Department of Pediatric Pulmonology and Pediatric Allergology, and Groningen Research Institute for Asthma and COPD (GRIAC), Groningen, the Netherlands.
²⁵ Oregon Clinical & Translational Research Institute, Oregon Health & Science University, Portland, OR, USA; Linus Pauling Institute, Oregon State University, Corvallis, OR, USA.
²⁶ Environmental Genomics and Systems Biology Division, E. O. Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
²⁷ Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
²⁸ Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Genetics, Rutgers University, Piscataway, NJ 08854, USA.
²⁹ Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Howard Hughes Medical Institute, Koch Institure of Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02140, USA.
³⁰ Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
³¹ Data Sciences Platform, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
³² Wellcome Sanger Institute, Wellcome Trust Genome Campus, Hinxton, South Cambridgeshire CB10 1SA, UK.
³³ Department of Genetics, Yale University School of Medicine, New Haven, CT 06520-8005, USA.
³⁴ Australian Institute for Bioengineering and Nanotechnology, the University of Queensland, Brisbane, QLD 4072, Australia.
³⁵ National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA; Center for Genetic Medicine Research, Children's National Medical Center, NW, Washington, DC, 20010-2970, USA.
³⁶ Division of Genetics and Genomics, The Manton Center for Orphan Disease Research, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.
³⁷ The Manton Center for Orphan Disease Research, Divisions of Newborn Medicine and of Genetics and Genomics, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.
³⁸ Department of Computational Medicine & Bioinformatics, The University of Michigan Medical School, University of Michigan, Ann Arbor, MI, USA.
³⁹ Division of Gastroenterology, Hepatology, and Nutrition, Boston Children's Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁴⁰ Protein and Proteomics Core Facility, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁴¹ Protein and Proteomics Core Facility, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁴² Center for Mitochondrial and Epigenomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁴³ Department of Pathology and Laboratory Medicine, The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
⁴⁴ Department of Psychiatry, The Children's Hospital of Philadelphia, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA.
⁴⁵ Nucleic Acid PCR Core Facility, The Children's Hospital of Philadelphia Research Institute, Philadelphia, PA 19104, USA.
⁴⁶ Department of Surgery, Division of General, Thoracic, and Fetal Surgery, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁴⁷ Department of Pathology & Laboratory Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA; Divisions of Pathology & Laboratory Medicine and Pulmonary Biology in the Perinatal Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229, USA.
⁴⁸ Wellcome Sanger Institute, Wellcome Trust Genome Campus, Hinxton, South Cambridgeshire CB10 1SA, UK; European Molecular Biology Laboratory - European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, South Cambridgeshire CB10 1SA, UK; Cavendish Laboratory, Theory of Condensed Matter, 19 JJ Thomson Ave, Cambridge CB3 1SA, UK.
⁴⁹ Center for Mitochondrial and Epigenomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Genetics, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
⁵⁰ Department of Biomedical and Health Informatics, The Children's Hospital of Philadelphia, and the Department of Pediatrics, The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA.
⁵¹ Department of Pathology and Laboratory Medicine, The Children's Hospital of Philadelphia and The University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA; Center for Computational and Genomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁵² Computational Health Informatics Program, Boston Children's Hospital, Departments of Biomedical Informatics and Pediatrics, Harvard Medical School, Boston, MA 02115, USA.
⁵³ National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA; Department of Genomics and Precision Medicine, George Washington University School of Medicine and Health Sciences, Washington, DC, USA.

Abstract

Single-cell gene expression analyses of mammalian tissues have uncovered profound stage-specific molecular regulatory phenomena that have changed the understanding of unique cell types and signaling pathways critical for lineage determination, morphogenesis, and growth. We discuss here the case for a Pediatric Cell Atlas as part of the Human Cell Atlas consortium to provide single-cell profiles and spatial characterization of gene expression across human tissues and organs. Such data will complement adult and developmentally focused HCA projects to provide a rich cytogenomic framework for understanding not only pediatric health and disease but also environmental and genetic impacts across the human lifespan.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Review

MeSH terms

Embryonic Development / genetics*
Gene Expression Profiling
Gene Expression Regulation, Developmental / genetics
Gene Regulatory Networks / genetics*
Humans
Pediatrics / trends*
Single-Cell Analysis / methods*
Tissue Distribution / genetics

Abstract

Publication types

MeSH terms

Grants and funding