Novel Cell Types, Neurosecretory Cells, and Body Plan of the Early-Diverging Metazoan Trichoplax adhaerens
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Background Trichoplax adhaerens is the best-known member of the phylum Placozoa, one of the earliest-diverging metazoan phyla. It is a small disk-shaped animal that glides on surfaces in warm oceans to feed on algae. Prior anatomical studies of Trichoplax revealed that it has a simple three-layered organization with four somatic cell types.Results We reinvestigate the cellular organization of Trichoplax using advanced freezing and microscopy techniques to identify localize and count cells. Six somatic cell types are deployed in stereotyped positions. A thick ventral plate, comprising the majority of the cells, includes ciliated epithelial cells, newly identified lipophil cells packed with large lipid granules, and gland cells. Lipophils project deep into the interior, where they alternate with regularly spaced fiber cells whose branches contact all other cell types, including cells of the dorsal and ventral epithelium. Crystal cells, each containing a birefringent crystal, are arrayed around the rim. Gland cells express several proteins typical of neurosecretory cells, and a subset of them, around the rim, also expresses an FMRFamide-like neuropeptide.Conclusions Structural analysis of Trichoplax with significantly improved techniques provides an advance in understanding its cell types and their distributions. We find two previously undetected cell types, lipohil and crystal cells, and an organized body plan in which different cell types are arranged in distinct patterns. The composition of gland cells suggests that they are neurosecretory cells and could control locomotor and feeding behavior.
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Newly identified 'lipophil' cells are characterized by a larger number of smaller vesicles, and a single large inclusion at the apical side with an acidic and lipophilic content.
“Instead, newly identified ‘lipophil’ cells are characterized by a larger number of smaller vesicles, and a single large inclusion at the apical side with an acidic and lipophilic content (Fig. 2d) (Smith et al. 2015; Smith et al. 2014).”
From A non-bilaterian perspective on the development and evolution of animal digestive systems (2019) · cites this paper as Smith et al. 2014
This long period of rudimentary nervous system development likely involved the deployment of genes now associated with the nervous system in proto-nervous system tissues, similar to Trichoplax today.
“This long period of rudimentary nervous system development likely involved the deployment of genes now associated with the nervous system in proto-nervous system tissues, similar to Trichoplax today [13,53,58].”
From Early metazoan life: divergence, environment and ecology (2015) · cites this paper as [58]
Trichoplax has neurosecretory cells concentrated in the periphery of the ventral epithelium that express typical neural proteins including syntaxin, synapsin, synaptobrevin and a FMRFamide-like neuropeptide.
“While Trichoplax has no obvious neurons, it does have neurosecretory cells concentrated in the periphery of the ventral epithelium [50]. These cells express typical neural proteins including syntaxin, synapsin, synaptobrevin and a FMRFamide-like neuropeptide [47].”
From Where is my mind? How sponges and placozoans may have lost neural cell types (2015) · cites this paper as [47]
Trichoplax is thought to consist of six different cell types, none of which present an obvious similarity to a neural cell type.
“Trichoplax is thought to consist of six different cell types, none of which present an obvious similarity to a neural cell type [47].”
From Where is my mind? How sponges and placozoans may have lost neural cell types (2015) · cites this paper as [47]
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Cites
Microscopic anatomy of invertebrates
Harrison, F. W. (1991) · Wiley-Liss eBooks · Cited by 2,736 · see citing works
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
Chapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D., et al. (2010) · Nature · doi:10.1038/nature08830 · Cited by 810 · see citing works
The Genome of the Ctenophore <i>Mnemiopsis leidyi</i> and Its Implications for Cell Type Evolution
Ryan, J. F., Pang, K., Schnitzler, C. E., Nguyen, A.-D., Moreland, R. T., Simmons, D. K., Koch, B. J., Francis, W. R., Havlak, P., Program, N. C. S., et al. (2013) · Science · doi:10.1126/science.1242592 · Cited by 702 · see citing works
Invertebrate Zoology: A Functional Evolutionary Approach
Ruppert, E. E., Fox, R. S., & Barnes, R. D. (2003) · Cited by 626 · see citing works
Global view of the evolution and diversity of metazoan neuropeptide signaling
Jékely, G. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221833110 · Cited by 451 · see citing works
The Capsaspora genome reveals a complex unicellular prehistory of animals
Suga, H., Chen, Z., de Mendoza, A., Sebé-Pedrós, A., Brown, M. W., Kramer, E., Carr, M., Kerner, P., Vervoort, M., Sánchez-Pons, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3325 · Cited by 317 · see citing works
The neuroendocrine system of invertebrates: a developmental and evolutionary perspective
Hartenstein, V. (2006) · Journal of Endocrinology · doi:10.1677/joe.1.06964 · Cited by 284 · see citing works
Review lecture: On the organization of reflecting surfaces in some marine animals
Denton, E. J. (1970) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1970.0037 · Cited by 270 · see citing works
Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes.
Ornberg, R., & Reese, T. S. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.90.1.40 · Cited by 210 · see citing works
Self-citationMetazoan opsin evolution reveals a simple route to animal vision
Feuda, R., Hamilton, S. C., McInerney, J. O., & Pisani, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204609109 · Cited by 186 · see citing works
My favorite animal, <i>Trichoplax adhaerens</i>
Schierwater, B. (2005) · BioEssays · doi:10.1002/bies.20320 · Cited by 161 · see citing works
Impulse conduction in a sponge
Leys, S. P., Mackie, G. O., & Meech, R. W. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.9.1139 · Cited by 156 · see citing works
Cnidarian chemical neurotransmission, an updated overview
Kass-Simon, G., & Pierobon, P. (2007) · Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2006.09.008 · Cited by 150 · see citing works
Studies on hexactinellid sponges. I. Histology of Rhabdocalyptus dawsoni (Lambe, 1873)
Mackie, G. O., & Singla, C. L. (1983) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1983.0028 · Cited by 142 · see citing works
Neuropeptides regulate swimming depth of Platynereis larvae
Conzelmann, M., Offenburger, S.-L., Asadulina, A., Keller, T., Münch, T. A., & Jékely, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109085108 · Cited by 136 · see citing works
Characterization of endoplasmic reticulum by co-localization of BiP and dicarbocyanine dyes
Terasaki, M., & Reese, T. S. (1992) · Journal of Cell Science · doi:10.1242/jcs.101.2.315 · Cited by 134 · see citing works
Self-citationThe Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary
Jakob, W., Sagasser, S., Dellaporta, S. L., Holland, P. W. H., Kuhn, K., & Schierwater, B. (2004) · Development Genes and Evolution · doi:10.1007/s00427-004-0390-8 · Cited by 116 · see citing works
New Insights into the Evolution of Metazoan Cadherins
Hulpiau, P., & Roy, F. M. V. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq233 · Cited by 115 · see citing works
Epithelia, an Evolutionary Novelty of Metazoans
Leys, S. P., & Riesgo, A. (2011) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21442 · Cited by 107 · see citing works
Origin and early evolution of neural circuits for the control of ciliary locomotion
Jékely, G. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.2027 · Cited by 103 · see citing works
Guanine‐Based Photonic Crystals in Fish Scales Form from an Amorphous Precursor
Gur, D., Politi, Y., Sivan, B., Fratzl, P., Weiner, S., & Addadi, L. (2013) · Angewandte Chemie International Edition · doi:10.1002/anie.201205336 · Cited by 85 · see citing works
Driscoll, T., Gillespie, J. J., Nordberg, E. K., Azad, A. F., & Sobral, B. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt036 · Cited by 79 · see citing works
Control of planula migration by LWamide and RFamide neuropeptides inHydractinia echinata
Katsukura, Y., Andō, H., David, C. N., Grimmelikhuijzen, C. J. P., & Sugiyama, T. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.00974 · Cited by 75 · see citing works
Ruthmann, A., Behrendt, G., & Wahl, R. (1986) · Zoomorphology · doi:10.1007/bf00312113 · Cited by 72 · see citing works
Mackie, G. O., Lawn, I. D., & de Ceccatty, M. P. (1983) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1983.0029 · Cited by 61 · see citing works
Conaco, C., Neveu, P. A., Zhou, H., Arcila, M. L., Degnan, B. M., Degnan, B. M., & Kosik, K. S. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-209 · Cited by 57 · see citing works
Ringrose, J. H., van den Toorn, H., Eitel, M., Post, H., Neerincx, P. B. T., Schierwater, B., Altelaar, M. A. F., & Heck, A. J. R. (2013) · Nature Communications · doi:10.1038/ncomms2424 · Cited by 55 · see citing works
Self-citationDynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence
Ueda, T., Koya, S., & Maruyama, Y. K. (1999) · Biosystems · doi:10.1016/s0303-2647(99)00066-0 · Cited by 54 · see citing works
Martinelli, C., & Spring, J. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0353-5 · Cited by 50 · see citing works
Schuchert, P. (1993) · Acta Zoologica · doi:10.1111/j.1463-6395.1993.tb01227.x · Cited by 49 · see citing works
Ultrastructural analyses support different morphological lineages in the phylum placozoa Grell, 1971
Guidi, L., Eitel, M., Cesarini, E., Schierwater, B., & Balsamo, M. (2011) · Journal of Morphology · doi:10.1002/jmor.10922 · Cited by 45 · see citing works
Self-citationInvertebrate FMRFamide Related Peptides
Krajniak, K. G. (2013) · Protein and Peptide Letters · doi:10.2174/0929866511320060005 · Cited by 34 · see citing works
Shiny spheres of placozoans (Trichoplax) function in anti‐predator defense
Jackson, A. M., & Buss, L. W. (2009) · Invertebrate Biology · doi:10.1111/j.1744-7410.2009.00177.x · Cited by 29 · see citing works
Trichoplax adhaerens F.E. Schulze (placozoa) in the scanning electron microscope
Rassat, J., & Ruthmann, A. (1979) · Zoomorphology · doi:10.1007/bf02568675 · Cited by 29 · see citing works
Expression pattern of the homeobox gene Not in the basal metazoan Trichoplax adhaerens
Martinelli, C., & Spring, J. (2004) · Gene Expression Patterns · doi:10.1016/j.modgep.2004.01.002 · Cited by 27 · see citing works
Transepithelial Cytophagy by Trichoplax adhaerens F. E. Schulze (Placozoa) Feeding on Yeast
Wenderoth, H. (1986) · Zeitschrift für Naturforschung C · doi:10.1515/znc-1986-0316 · Cited by 26 · see citing works
Birefringent Granules in Placozoans (Trichoplax adhaerens)
Pearse, V. B., Uehara, T., & Miller, R. L. (1994) · Transactions of the American Microscopical Society · doi:10.2307/3226631 · Cited by 19 · see citing works
Nanoscale Imaging of Protein Molecules at the Postsynaptic Density
Chen, X., Winters, C. A., Azzam, R. N., Sousa, A. A., Leapman, R. D., & Reese, T. S. (2014) · Neuromethods · doi:10.1007/978-1-4614-9179-8_1 · Cited by 9 · see citing works
Self-citationGrell, K. G., & Benwitz, G. (1975) · PubMed · Cited by 8 · see citing works
Nanoscale imaging of synapses : new concepts and opportunities
Nägerl, U. V., & Triller, A. (2014) · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [19]19. Pearse, V.B., Uehara, T., and Miller, R.L. (1994). Birefringent granules in placozoans. Trans. Am. Microsc. Soc. 113, 385-389.
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- Authors
- Smith, C. L., Varoqueaux, F., Kittelmann, M., Azzam, R. N., Cooper, B., Winters, C. A., Eitel, M., Fasshauer, D., & Reese, T. S.
- Affiliations
- National Institutes of Health (US)
- Max Planck Institute of Experimental Medicine (DE)
- University of Veterinary Medicine Hannover, Foundation (DE)
- University of Lausanne (CH)
- Corresponding author
- Smith, Carolyn L.
- Fasshauer, Dirk
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 24
- Issue
- 14
- Pages
- 1565-1572
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4128346
- OpenAlex
- W2158723722
- Cited by
- 254
- References
- 43
- Citations by year
- 2026: 7 · 2025: 26 · 2024: 22 · 2023: 21 · 2022: 16 · 2021: 34 · 2020: 16 · 2019: 27 · 2018: 21 · 2017: 19 · 2016: 17 · 2015: 22 · 2014: 6
- FWCI
- 15.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- IRIS (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Funders
- National Institutes of Health (Z99 NS999999)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Trichoplax adhaerens, Placozoa, cell types, neurosecretory cells, body plan, crystal cells, gland cells, ciliated epithelium, fiber cells, early-diverging metazoans, cell localization
- MeSH terms
- Animals, Cytoplasmic Granules, Epithelial Cells, Epithelium, Neurons, Neurosecretion, Placozoa
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