The evolution of cell types in animals: emerging principles from molecular studies

Arendt, Detlev

doi:10.1038/nrg2416

Cited by 527Developmental Biology and Gene RegulationMarine Invertebrate Physiology and EcologyGenomics and Phylogenetic Studies

The evolution of cell types in animals: emerging principles from molecular studies

Arendt, Detlev·2008·Nature Reviews Genetics

DOI 10.1038/nrg2416

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Abstract

Cell types are fundamental units of multicellular life but their evolution is obscure. How did the first cell types emerge and become distinct in animal evolution? What were the sets of cell types that existed at important evolutionary nodes that represent eumetazoan or bilaterian ancestors? How did these ancient cell types diversify further during the evolution of organ systems in the descending evolutionary lines? The recent advent of cell type molecular fingerprinting has yielded initial insights into the evolutionary interrelationships of cell types between remote animal phyla and has allowed us to define some first principles of cell type diversification in animal evolution.

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Cells within an organism can be grouped into types, with cells of a type sharing similar structure and function distinct from other types.
“Studies over the past century have revealed that cells within an organism can be grouped into types – cells within a type exhibit similar structure and function that are distinct from cells in other types (Arendt, 2008).”
From What is a cell type and how to define it? (2022) · cites this paper as Arendt, 2008

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Hwang, J. S., Ohyanagi, H., Hayakawa, S., Osato, N., Nishimiya‐Fujisawa, C., Ikeo, K., David, C. N., Fujisawa, T., & Gojobori, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703331104 · Cited by 89 · see citing works
Phylogenetic relationship of muscle tissues deduced from superimposition of gene trees
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The origins of colour vision in vertebrates
Collin, S. P., & Trezise, A. E. O. (2004) · Clinical and Experimental Optometry · doi:10.1111/j.1444-0938.2004.tb05051.x · Cited by 82 · see citing works
Motor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms.
Thor, S., & Thomas, J. B. (2002) · Current Opinion in Genetics and Development · doi:10.1016/s0959-437x(02)00340-4 · Cited by 77 · see citing works
The blood/vascular system in a phylogenetic perspective
Hartenstein, V., & Mandal, L. (2006) · BioEssays · doi:10.1002/bies.20497 · Cited by 77 · see citing works
FGF8/17/18 functions together with FGF9/16/20 during formation of the notochord in Ciona embryos
Yasuo, H., & Hudson, C. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.075 · Cited by 76 · see citing works
The Question of Functional Homology of Hatschek's Pit of Amphioxus (Branchiostoma belcheri) and the Vertebrate Adenohypophysis(Endocrinology)
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Repression of Six3 by a corepressor regulates rhodopsin expression
Manavathi, B., Peng, S., Rayala, S. K., Talukder, A. H., Wang, M. H., Wang, R., Balasenthil, S., Agarwal, N. A., Frishman, L. J., & Kumar, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705878104 · Cited by 67 · see citing works
Wnt Signaling Induces Vulva Development in the Nematode Pristionchus pacificus
Tian, H., Schlager, B., Xiao, H., & Sommer, R. J. (2008) · Current Biology · doi:10.1016/j.cub.2007.12.048 · Cited by 63 · see citing works
Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications
Nordström, K., Larsson, T., & Larhammar, D. (2004) · Genomics · doi:10.1016/j.ygeno.2003.11.008 · Cited by 62 · see citing works
Developmental and evolutionary aspects of the basic helix–loop–helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish
Seipel, K., Yanze, N., & Schmid, V. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.035 · Cited by 62 · see citing works
The evolution of neurosecretory centers in bilaterian forebrains: insights from protostomes
Tessmar-Raible, K. (2007) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2007.04.007 · Cited by 53 · see citing works
CHX10 Targets a Subset of Photoreceptor Genes
Dorval, K. M., Bobechko, B. P., Fujieda, H., Chen, S., Zack, D. J., & Bremner, R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509470200 · Cited by 53 · see citing works
Note on the Infusoria flagellata and the Spongiae ciliatae
James‐Clark, H. (1871) · American Journal of Science · doi:10.2475/ajs.s3-1.2.113 · Cited by 52 · see citing works
Genetic network of the eye in Platyhelminthes: expression and functional analysis of some players during planarian regeneration
Saló, E., Pineda, D., Marsal, M., González, J., Gremigni, V., & Batistoni, R. (2002) · Gene · doi:10.1016/s0378-1119(01)00863-0 · Cited by 51 · see citing works
Expression of the amphioxus Pit-1 gene (AmphiPOU1F1/Pit-1) exclusively in the developing preoral organ, a putative homolog of the vertebrate adenohypophysis
Candiani, S., Holland, N. D., Oliveri, D., Parodi, M., & Pestarino, M. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.023 · Cited by 51 · see citing works
Transcriptional regulation of neuronal phenotype in mammals
Ma, Q. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.113449 · Cited by 50 · see citing works
Key transitions during the evolution of animal phototransduction: novelty, "tree-thinking," co-option, and co-duplication
Plachetzki, D. C., & Oakley, T. H. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm050 · Cited by 50 · see citing works
New genes in the evolution of the neural crest differentiation program
Martínez‐Morales, J. R., Henrich, T., Ramialison, M., & Wittbrodt, J. (2007) · Genome biology · doi:10.1186/gb-2007-8-3-r36 · Cited by 50 · see citing works
Genes and homology in nervous system evolution: Comparing gene functions, expression patterns, and cell type molecular fingerprints
Arendt, D. (2005) · Theory in Biosciences · doi:10.1007/bf02814483 · Cited by 48 · see citing works
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Hierarchical phylogenetics as a quantitative analytical framework for evolutionary developmental biology
Serb, J. M., & Oakley, T. H. (2005) · BioEssays · doi:10.1002/bies.20291 · Cited by 47 · see citing works
cDNA microarray analysis reveals fundamental differences in the expression profiles of primary human monocytes, monocyte-derived macrophages, and alveolar macrophages
Li, J., Pritchard, D. K., Wang, X., Park, D. R., Bumgarner, R. E., Schwartz, S. M., & Liles, W. C. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0206124 · Cited by 44 · see citing works
Equivalent progenitor cells in the zebrafish anterior preplacodal field give rise to adenohypophysis, lens, and olfactory placodes
Toro, S., & Varga, Z. M. (2007) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2007.04.003 · Cited by 43 · see citing works
Cytology and Evolution
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New insights into the evolutionary history of photoreceptor cells
Plachetzki, D. C., Serb, J. M., & Oakley, T. H. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.07.001 · Cited by 42 · see citing works
The role of TGFβ signaling in the formation of the dorsal nervous system is conserved betweenDrosophilaand chordates
Rusten, T. E., Cantera, R., Kafatos, F. C., & Barrio, R. (2002) · Development · doi:10.1242/dev.129.15.3575 · Cited by 32 · see citing works
Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors
Oakley, T. H., Plachetzki, D. C., & Rivera, A. S. (2007) · Arthropod Structure & Development · doi:10.1016/j.asd.2007.08.002 · Cited by 31 · see citing works
Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii
Altincicek, B., & Vilcinskas, A. (2007) · Frontiers in Zoology · doi:10.1186/1742-9994-4-18 · Cited by 29 · see citing works
Making mesoderm--upstream and downstream of Xbra
Smith, J. C. (2001) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11291849 · Cited by 28 · see citing works
Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata).
Ms, R., & Anadón, R. (1991) · PubMed · Cited by 23 · see citing works
Strategies for studying microtubule transport in the neuron
Baas, P. W. (2000) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(20000115)48:2 · Cited by 18 · see citing works
Mucus secretion and transport in amphioxus larvae: organization and ultrastructure of the food trapping system, and implications for head evolution
Lacalli, T. C. (2007) · Acta Zoologica · doi:10.1111/j.1463-6395.2007.00310.x · Cited by 13 · see citing works
Insights into the Coupling of Duplication Events and Macroevolution from an Age Profile of Animal Transmembrane Gene Families
Ding, G., Kang, J., Liu, Q., Shi, T., Pei, G., & Li, Y. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020102 · Cited by 11 · see citing works

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eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses
Huerta‐Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S. K., Cook, H., Mende, D. R., Letunić, I., Rattei, T., Jensen, L. J., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1085 · Cited by 4,943 · see citing works
A census of human transcription factors: function, expression and evolution
Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A., & Luscombe, N. M. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2538 · Cited by 1,573 · see citing works
Single-cell sequencing-based technologies will revolutionize whole-organism science
Shapiro, E., Biezuner, T., & Linnarsson, S. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3542 · Cited by 1,177 · see citing works
The origin and evolution of cell types
Arendt, D., Musser, J. M., Baker, C. V. H., Bergman, A., Cepko, C., Erwin, D. H., Pavlicev, M., Schlosser, G., Widder, S., Laubichler, M. D., et al. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.127 · Cited by 764 · see citing works
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Tissue biology perspective on macrophages
Okabe, Y., & Medzhitov, R. M. (2015) · Nature Immunology · doi:10.1038/ni.3320 · Cited by 633 · see citing works
Annotating non-coding regions of the genome.
Alexander, R. P., Fang, G., Rozowsky, J., Snyder, M., & Gerstein, M. B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2814 · Cited by 464 · see citing works
What is a cell type and how to define it?
Zeng, H. (2022) · Cell · doi:10.1016/j.cell.2022.06.031 · Cited by 439 · see citing works
High-throughput spatial mapping of single-cell RNA-seq data to tissue of origin
Achim, K., Pettit, J.-B., Saraiva, L. R., Gavriouchkina, D., Larsson, T., Arendt, D., & Marioni, J. C. (2015) · Nature Biotechnology · doi:10.1038/nbt.3209 · Cited by 395 · see citing works
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The Origin of Animal Multicellularity and Cell Differentiation
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Biological Autonomy
Bergareche, Á. J. M., & Mossio, M. (2015) · History, philosophy and theory of the life sciences · doi:10.1007/978-94-017-9837-2 · Cited by 501 · see citing works
Biocompatibility characteristics of the metal organic framework ZIF-8 for therapeutical applications
Hoop, M., Walde, C. F., Riccò, R., Mushtaq, F., Terzopoulou, A., Chen, X., deMello, A. J., Doonan, C. J., Falcaro, P., Nelson, B. J., et al. (2018) · Applied Materials Today · doi:10.1016/j.apmt.2017.12.014 · Cited by 350 · see citing works
The origin of Metazoa: a unicellular perspective
Sebé-Pedrós, A., Degnan, B. M., & Ruiz-Trillo, I. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.21 · Cited by 332 · see citing works
Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium.
Tomer, R., Denes, A. S., Tessmar-Raible, K., & Arendt, D. (2010) · Cell · doi:10.1016/j.cell.2010.07.043 · Cited by 317 · see citing works
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From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system
Arendt, D., Tosches, M. A., & Marlow, H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.15 · Cited by 279 · see citing works
Self-citation
Eye evolution and its functional basis
NILSSON, D.-E. (2013) · Visual Neuroscience · doi:10.1017/s0952523813000035 · Cited by 267 · see citing works
Disentangling neural cell diversity using single-cell transcriptomics
Poulin, J.-F., Tasic, B., Hjerling-Leffler, J., Trimarchi, J. M., & Awatramani, R. (2016) · Nature Neuroscience · doi:10.1038/nn.4366 · Cited by 293 · see citing works
Neuro-Immune Interactions at Barrier Surfaces
Veiga‐Fernandes, H., & Mucida, D. (2016) · Cell · doi:10.1016/j.cell.2016.04.041 · Cited by 290 · see citing works
Evolution of oxytocin pathways in the brain of vertebrates
Knobloch, H. S., & Grinevich, V. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00031 · Cited by 259 · see citing works
Cerebellar nuclei evolved by repeatedly duplicating a conserved cell-type set
Kebschull, J. M., Richman, E. B., Ringach, N., Friedmann, D., Albarran, E., Kolluru, S. S., Jones, R. C., Allen, W. E., Wang, Y., Cho, S. W., et al. (2020) · Science · doi:10.1126/science.abd5059 · Cited by 253 · see citing works
The evolution of eyes and visually guided behaviour
Nilsson, D.-E. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0083 · Cited by 258 · see citing works
Phenotypic convergence: distinct transcription factors regulate common terminal features
Konstantinides, N., Kapuralin, K., Fadil, C., Barboza, L., Satija, R., & Desplan, C. (2018) · Cell · doi:10.1016/j.cell.2018.05.021 · Cited by 226 · see citing works
On the Independent Origins of Complex Brains and Neurons
Moroz, L. L. (2009) · Brain, Behavior and Evolution · doi:10.1159/000258665 · Cited by 209 · see citing works
Evolution of transcription factor binding in metazoans — mechanisms and functional implications
Villar, D., Flicek, P., & Odom, D. T. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3481 · Cited by 206 · see citing works
Specialization Can Drive the Evolution of Modularity
Espinosa‐Soto, C., & Wagner, A. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000719 · Cited by 206 · see citing works
Network Plasticity in Adaptive Filtering and Behavioral Habituation
Ramaswami, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.035 · Cited by 194 · see citing works
Vitamin A Metabolism in Rod and Cone Visual Cycles
Saari, J. C. (2012) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071811-150748 · Cited by 189 · see citing works
The saccus vasculosus of fish is a sensor of seasonal changes in day length
Nakane, Y., Ikegami, K., Iigo, M., Ono, H., Takeda, K., Takahashi, D., Uesaka, M., Kimijima, M., Hashimoto, R., Arai, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3108 · Cited by 189 · see citing works
Cephalopod Brains: An Overview of Current Knowledge to Facilitate Comparison With Vertebrates
Shigeno, S., Andrews, P. L. R., Ponte, G., & Fiorito, G. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00952 · Cited by 182 · see citing works
Regulated aggregative multicellularity in a close unicellular relative of metazoa
Sebé-Pedrós, A., Irimia, M., del Campo, J., Parra-Acero, H., Russ, C., Nusbaum, C., Blencowe, B. J., & Ruiz‐Trillo, I. (2013) · eLife · doi:10.7554/elife.01287 · Cited by 171 · see citing works
What nervous systems do: early evolution, input–output, and the skin brain thesis
Keijzer, F., van Duijn, M., & Lyon, P. (2013) · Adaptive Behavior · doi:10.1177/1059712312465330 · Cited by 173 · see citing works
Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution
Arnold, C. D., Gerlach, D., Spies, D., Matts, J. A., Sytnikova, Y. A., Pagani, M., Lau, N. C., & Stark, A. (2014) · Nature Genetics · doi:10.1038/ng.3009 · Cited by 175 · see citing works
Evolution of functional specialization and division of labor
Rueffler, C., Hermisson, J., & Wagner, G. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110521109 · Cited by 168 · see citing works
Dissecting phylogenetic signal and accounting for bias in whole-genome data sets: a case study of the Metazoa
Borowiec, M. L., Lee, E. K., Chiu, J. C., & Plachetzki, D. C. (2015) · doi:10.1101/013946 · Cited by 172 · see citing works
Independent origins of neurons and synapses: insights from ctenophores
Moroz, L. L., & Kohn, A. B. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0041 · Cited by 171 · see citing works
Origins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168 · see citing works
Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits
Colquitt, B. M., Merullo, D. P., Konopka, G., Roberts, T. F., & Brainard, M. S. (2021) · Science · doi:10.1126/science.abd9704 · Cited by 169 · see citing works
A pan-grass transcriptome reveals patterns of cellular divergence in crops
Guillotin, B., Rahni, R., Passalacqua, M. J., Mohammed, M. A., Xu, X., Raju, S. K. K., Ortiz‐Ramírez, C., Jackson, D. P., Groen, S. C., Gillis, J. A., et al. (2023) · Nature · doi:10.1038/s41586-023-06053-0 · Cited by 164 · see citing works
Molecular Signatures of the Three Stem Cell Lineages in Hydra and the Emergence of Stem Cell Function at the Base of Multicellularity
Hemmrich, G., Khalturin, K., Böhm, A.-M., Puchert, M., Anton‐Erxleben, F., Wittlieb, J., Klostermeier, U. C., Rosenstiel, P. C., Oberg, H., Domazet‐Lošo, T., et al. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss134 · Cited by 159 · see citing works
Mitochondria-rough-ER contacts in the liver regulate systemic lipid homeostasis
Anastasia, I., Ilacqua, N., Raimondi, A., Lemieux, P., Ghandehari‐Alavijeh, R., Faure, G., Mekhedov, S., Williams, K. J., Caicci, F., Valle, G., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108873 · Cited by 148 · see citing works
Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: Ancient association of “germline genes” with stemness
Alié, A., Leclère, L., Jager, M., Dayraud, C., Chang, P., Guyader, H. L., Quéinnec, É., & Manuel, M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.10.019 · Cited by 147 · see citing works
Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates
Nakane, Y., & Yoshimura, T. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00115 · Cited by 141 · see citing works
Neuroimmune regulation during intestinal development and homeostasis
Veiga‐Fernandes, H., & Pachnis, V. (2017) · Nature Immunology · doi:10.1038/ni.3634 · Cited by 144 · see citing works
Synthetic multistability in mammalian cells
Zhu, R., del Rio-Salgado, J. M., Garcia-Ojalvo, J., & Elowitz, M. B. (2022) · Science · doi:10.1126/science.abg9765 · Cited by 144 · see citing works
The genome of the jellyfish Aurelia and the evolution of animal complexity
Gold, D. A., Katsuki, T., Li, Y., Yan, X., Regulski, M., Ibberson, D., Holstein, T. W., Steele, R. E., Jacobs, D. K., & Greenspan, R. J. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0719-8 · Cited by 142 · see citing works
The origin of animal body plans: a view from fossil evidence and the regulatory genome
Erwin, D. H. (2020) · Development · doi:10.1242/dev.182899 · Cited by 133 · see citing works
From damage response to action potentials: early evolution of neural and contractile modules in stem eukaryotes
Brunet, T., & Arendt, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0043 · Cited by 129 · see citing works
Self-citation
Pigmentation Pathway Evolution after Whole-Genome Duplication in Fish
Braasch, I., Brunet, F., Volff, J., & Schartl, M. (2009) · Genome Biology and Evolution · doi:10.1093/gbe/evp050 · Cited by 127 · see citing works
Evolution of neuronal types and families
Arendt, D., Bertucci, P. Y., Achim, K., & Musser, J. M. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.01.022 · Cited by 121 · see citing works
Self-citation
Deciphering the transcriptional cis-regulatory code
Yáñez-Cuna, J. O., Kvon, E. Z., & Stark, A. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.09.007 · Cited by 124 · see citing works
Seahorse Brood Pouch Transcriptome Reveals Common Genes Associated with Vertebrate Pregnancy
Whittington, C. M., Griffith, O. W., Qi, W., Thompson, M. B., & Wilson, A. B. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv177 · Cited by 124 · see citing works
The pre-vertebrate origins of neurogenic placodes
Abitua, P. B., Gainous, T. B., Kaczmarczyk, A. N., Winchell, C. J., Hudson, C., Kamata, K., Nakagawa, M., Tsuda, M., Kusakabe, T. G., & Levine, M. (2015) · Nature · doi:10.1038/nature14657 · Cited by 123 · see citing works
High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species
He, Q., Bardet, A. F., Patton, B., Purvis, J., Johnston, J. J., Paulson, A., Gogol, M., Stark, A., & Zeitlinger, J. (2011) · Nature Genetics · doi:10.1038/ng.808 · Cited by 121 · see citing works
Homeoprotein Phox2b commands a somatic-to-visceral switch in cranial sensory pathways
D’Autréaux, F., Coppola, E., Hirsch, M., Birchmeier, C., & Brunet, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110416108 · Cited by 123 · see citing works
Evolution of the vertebrate skeleton: morphology, embryology, and development
Hirasawa, T., & Kuratani, S. (2015) · Zoological Letters · doi:10.1186/s40851-014-0007-7 · Cited by 120 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
Self-citation
Investigating Evolutionary Conservation of Dendritic Cell Subset Identity and Functions
Manh, T. V., Bertho, N., Hosmalin, A., Schwartz-Cornil, I., & Dalod, M. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00260 · Cited by 120 · see citing works
Single-Cell Analysis Uncovers Clonal Acinar Cell Heterogeneity in the Adult Pancreas
Wollny, D., Zhao, S., Everlien, I., Lun, X., Brunken, J., Brüne, D., Ziebell, F., Tabansky, I., Weichert, W., Marciniak-Czochra, A. K., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.10.002 · Cited by 114 · see citing works
On the evolution of chaperones and cochaperones and the expansion of proteomes across the Tree of Life
Rebeaud, M. E., Mallik, S., Goloubinoff, P., & Tawfik, D. S. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020885118 · Cited by 116 · see citing works
Neural mechanisms underlying the evolvability of behaviour
Katz, P. S. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0336 · Cited by 117 · see citing works
Eye evolution: common use and independent recruitment of genetic components
Vopálenský, P., & Kozmík, Z. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0079 · Cited by 116 · see citing works
Evolutionary cell biology: Two origins, one objective
Lynch, M., Field, M. C., Goodson, H. V., Malik, H. S., Pereira‐Leal, J. B., Roos, D. S., Turkewitz, A. P., & Sazer, S. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415861111 · Cited by 110 · see citing works
Neuronal connectome of a sensory-motor circuit for visual navigation
Randel, N., Asadulina, A., Bezares-Calderón, L. A., Verasztó, C., Williams, E. A., Conzelmann, M., Shahidi, R., & Jékely, G. (2014) · eLife · doi:10.7554/elife.02730 · Cited by 119 · see citing works
Evolution of central neural circuits: state of the art and perspectives
Roberts, R. J. V., Pop, S., & Prieto-Godino, L. L. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00644-y · Cited by 108 · see citing works
Notch activity in the nervous system: to switch or not switch?
Cau, E., & Blader, P. (2009) · Neural Development · doi:10.1186/1749-8104-4-36 · Cited by 109 · see citing works
Evolution of vertebrate rod and cone phototransduction genes
Larhammar, D., Nordström, K., & Larsson, T. (2009) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0077 · Cited by 113 · see citing works
Posterior elongation in the annelid Platynereis dumerilii involves stem cells molecularly related to primordial germ cells
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Authors: Arendt, D.
Affiliations: European Molecular Biology Laboratory (DE)
Corresponding author: Arendt, Detlev
ORCID: Arendt, Detlev
Venue: Nature Reviews Genetics
Publisher: Springer Science and Business Media LLC
Published: 2008-11
Volume: 9
Issue: 11
Pages: 868-882
ISSN: 1471-0056 (ISSN-L)
1471-0064
DOI: 10.1038/nrg2416
OpenAlex: W2072977772
Cited by: 525
References: 126
Citations by year: 2026: 25 · 2025: 33 · 2024: 44 · 2023: 50 · 2022: 30 · 2021: 33 · 2020: 37 · 2019: 27 · 2018: 26 · 2017: 28 · 2016: 24 · 2015: 45 · 2014: 31 · 2013: 19 · 2012: 17
FWCI: 1.44
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Genetics (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords: cell type evolution, animal evolution, multicellularity
MeSH terms: Animals, Cell Differentiation, Endocrine System, Biological Evolution, Immune System, Nervous System, Phylogeny, DNA Fingerprinting, Cell Lineage

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The evolution of cell types in animals: emerging principles from molecular studies

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