publication . Article . Other literature type . 2016

Self-generated chemoattractant gradients: Attractant depletion extends the range and robustness of chemotaxis

David Knecht; Luke Tweedy; Robert Insall;
Open Access English
  • Published: 16 Mar 2016
  • Publisher: Public Library of Science
  • Country: United Kingdom
Abstract
A combination of experiment and simulation reveals self-generated chemotaxis—an emergent, fundamental, and widespread mechanism of directed cell migration that depends on removal or destruction of the chemotactic signal by the migrating cells themselves.
Subjects
free text keywords: Research Article, Biology and Life Sciences, Cell Biology, Cell Motility, Chemotaxis, Research and Analysis Methods, Bioassays and Physiological Analysis, Cell Analysis, Chemotaxis Assay, Organisms, Protists, Slime Molds, Dictyosteliomycota, Dictyostelium, Model Organisms, Protozoan Models, Cell Physiology, Receptor Physiology, Population Biology, Population Metrics, Population Density, Cell Migration, Developmental Biology, Directed Cell Migration, Biology (General), QH301-705.5, General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Neuroscience, General Agricultural and Biological Sciences
Related Organizations
34 references, page 1 of 3

1 Insall R. The interaction between pseudopods and extracellular signalling during chemotaxis and directed migration. Curr Opin Cell Biol. 2013;25:526–531. 10.1016/j.ceb.2013.04.009 23747069 [OpenAIRE] [PubMed] [DOI]

2 Moissoglu K, Majumdar R, Parent CA. Cell migration: sinking in a gradient. Curr Biol. 2014;24:R23–R25. 10.1016/j.cub.2013.10.075 24405672 [OpenAIRE] [PubMed] [DOI]

3 Muinonen-Martin AJ, Susanto O, Zhang Q et al Melanoma Cells Break Down LPA to Establish Local Gradients That Drive Chemotactic Dispersal. PLoS Biol. 2014;12:e1001966 10.1371/journal.pbio.1001966 25313567 [OpenAIRE] [PubMed] [DOI]

4 Sucgang R, Weijer CJ, Siegert F, Franke J, Kessin RH. Null mutations of the Dictyostelium cyclic nucleotide phosphodiesterase gene block chemotactic cell movement in developing aggregates. Dev Biol. 1997;192:181–192. 9405107 [OpenAIRE] [PubMed]

5 Sorkin A. Internalization of the epidermal growth factor receptor: role in signalling. Biochem Soc Trans. 2001;29:480–484. 11498013 [OpenAIRE] [PubMed]

6 Haugh JM. Deterministic model of dermal wound invasion incorporating receptor-mediated signal transduction and spatial gradient sensing. Biophys J. 2006;90:2297–2308. 16415056 [OpenAIRE] [PubMed]

7 Dona E, Barry JD, Valentin G et al Directional tissue migration through a self-generated chemokine gradient. Nature. 2013;503:285–289. 10.1038/nature12635 24067609 [OpenAIRE] [PubMed] [DOI]

8 Venkiteswaran G, Lewellis SW, Wang J, Reynolds E, Nicholson C, Knaut H. Generation and Dynamics of an Endogenous, Self-Generated Signaling Gradient across a Migrating Tissue. Cell. 2013;155:674–687. 10.1016/j.cell.2013.09.046 24119842 [OpenAIRE] [PubMed] [DOI]

9 Goetzl EJ, An S. Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 1998;12:1589–1598. 9837849 [OpenAIRE] [PubMed]

10 Houben AJ, Moolenaar WH. Autotaxin and LPA receptor signaling in cancer. Cancer Metastasis Rev. 2011;30:557–565. 10.1007/s10555-011-9319-7 22002750 [OpenAIRE] [PubMed] [DOI]

11 Laevsky G, Knecht DA. Under-agarose folate chemotaxis of Dictyostelium discoideum amoebae in permissive and mechanically inhibited conditions. Biotechniques. 2001;31:1140–2, 1144, 1146 11730020 [OpenAIRE] [PubMed]

12 Choi JW, Herr DR, Noguchi K et al LPA r eceptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol. 2010;50:157–186. 10.1146/annurev.pharmtox.010909.105753 20055701 [OpenAIRE] [PubMed] [DOI]

13 Bernstein RL, Tabler M, Vestweber D, Van Driel R. Extracellular folate deaminase of Dictyostelium discoideum. Biochim Biophys Acta. 1981;677:295–302. 6271253 [PubMed]

14 Kuwayama H, Ishida S, Van Haastert PJ. Non-chemotactic Dictyostelium discoideum mutants with altered cGMP signal transduction. J Cell Biol. 1993;123:1453–1462. 7902839 [OpenAIRE] [PubMed]

15 Zigmond SH. Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes. Nature. 1974;249:450–452. 4834231 [PubMed]

34 references, page 1 of 3
Abstract
A combination of experiment and simulation reveals self-generated chemotaxis—an emergent, fundamental, and widespread mechanism of directed cell migration that depends on removal or destruction of the chemotactic signal by the migrating cells themselves.
Subjects
free text keywords: Research Article, Biology and Life Sciences, Cell Biology, Cell Motility, Chemotaxis, Research and Analysis Methods, Bioassays and Physiological Analysis, Cell Analysis, Chemotaxis Assay, Organisms, Protists, Slime Molds, Dictyosteliomycota, Dictyostelium, Model Organisms, Protozoan Models, Cell Physiology, Receptor Physiology, Population Biology, Population Metrics, Population Density, Cell Migration, Developmental Biology, Directed Cell Migration, Biology (General), QH301-705.5, General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Neuroscience, General Agricultural and Biological Sciences
Related Organizations
34 references, page 1 of 3

1 Insall R. The interaction between pseudopods and extracellular signalling during chemotaxis and directed migration. Curr Opin Cell Biol. 2013;25:526–531. 10.1016/j.ceb.2013.04.009 23747069 [OpenAIRE] [PubMed] [DOI]

2 Moissoglu K, Majumdar R, Parent CA. Cell migration: sinking in a gradient. Curr Biol. 2014;24:R23–R25. 10.1016/j.cub.2013.10.075 24405672 [OpenAIRE] [PubMed] [DOI]

3 Muinonen-Martin AJ, Susanto O, Zhang Q et al Melanoma Cells Break Down LPA to Establish Local Gradients That Drive Chemotactic Dispersal. PLoS Biol. 2014;12:e1001966 10.1371/journal.pbio.1001966 25313567 [OpenAIRE] [PubMed] [DOI]

4 Sucgang R, Weijer CJ, Siegert F, Franke J, Kessin RH. Null mutations of the Dictyostelium cyclic nucleotide phosphodiesterase gene block chemotactic cell movement in developing aggregates. Dev Biol. 1997;192:181–192. 9405107 [OpenAIRE] [PubMed]

5 Sorkin A. Internalization of the epidermal growth factor receptor: role in signalling. Biochem Soc Trans. 2001;29:480–484. 11498013 [OpenAIRE] [PubMed]

6 Haugh JM. Deterministic model of dermal wound invasion incorporating receptor-mediated signal transduction and spatial gradient sensing. Biophys J. 2006;90:2297–2308. 16415056 [OpenAIRE] [PubMed]

7 Dona E, Barry JD, Valentin G et al Directional tissue migration through a self-generated chemokine gradient. Nature. 2013;503:285–289. 10.1038/nature12635 24067609 [OpenAIRE] [PubMed] [DOI]

8 Venkiteswaran G, Lewellis SW, Wang J, Reynolds E, Nicholson C, Knaut H. Generation and Dynamics of an Endogenous, Self-Generated Signaling Gradient across a Migrating Tissue. Cell. 2013;155:674–687. 10.1016/j.cell.2013.09.046 24119842 [OpenAIRE] [PubMed] [DOI]

9 Goetzl EJ, An S. Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 1998;12:1589–1598. 9837849 [OpenAIRE] [PubMed]

10 Houben AJ, Moolenaar WH. Autotaxin and LPA receptor signaling in cancer. Cancer Metastasis Rev. 2011;30:557–565. 10.1007/s10555-011-9319-7 22002750 [OpenAIRE] [PubMed] [DOI]

11 Laevsky G, Knecht DA. Under-agarose folate chemotaxis of Dictyostelium discoideum amoebae in permissive and mechanically inhibited conditions. Biotechniques. 2001;31:1140–2, 1144, 1146 11730020 [OpenAIRE] [PubMed]

12 Choi JW, Herr DR, Noguchi K et al LPA r eceptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol. 2010;50:157–186. 10.1146/annurev.pharmtox.010909.105753 20055701 [OpenAIRE] [PubMed] [DOI]

13 Bernstein RL, Tabler M, Vestweber D, Van Driel R. Extracellular folate deaminase of Dictyostelium discoideum. Biochim Biophys Acta. 1981;677:295–302. 6271253 [PubMed]

14 Kuwayama H, Ishida S, Van Haastert PJ. Non-chemotactic Dictyostelium discoideum mutants with altered cGMP signal transduction. J Cell Biol. 1993;123:1453–1462. 7902839 [OpenAIRE] [PubMed]

15 Zigmond SH. Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes. Nature. 1974;249:450–452. 4834231 [PubMed]

34 references, page 1 of 3
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