Self-Generated Chemoattractant Gradients: Attractant Depletion Extends the Range and Robustness of Chemotaxis

PLoS Biology

Volumn 14, Issue 3, 2016, Pages

  Tweedy, Luke ^a   Knecht, David A ^b   Mackay, Gillian M ^a   Insall, Robert H ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CYCLIC AMP; CHEMOTACTIC FACTOR;

ARTICLE; CELL MOTILITY; CELL MOTION; CELL POPULATION; CHEMOTAXIS; CONCENTRATION (PARAMETERS); DICTYOSTELIUM DISCOIDEUM; MATHEMATICAL COMPUTING; NONHUMAN; POPULATION DISTRIBUTION; PROTEIN SECRETION; SELF GENERATED GRADIENT CHEMOTAXIS; DICTYOSTELIUM; METABOLISM;

CELL MOVEMENT; CHEMOTACTIC FACTORS; CHEMOTAXIS; DICTYOSTELIUM;

EID: 84962170794     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002404     Document Type: Article

References (34)

1. Insall R, The interaction between pseudopods and extracellular signalling during chemotaxis and directed migration. Curr Opin Cell Biol. 2013;25:526–531. doi: 10.1016/j.ceb.2013.04.00923747069
2. Moissoglu K, Majumdar R, Parent CA, Cell migration: sinking in a gradient. Curr Biol. 2014;24:R23–R25. doi: 10.1016/j.cub.2013.10.07524405672
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. doi: 10.1371/journal.pbio.100196625313567
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
5. Sorkin A, Internalization of the epidermal growth factor receptor: role in signalling. Biochem Soc Trans. 2001;29:480–484. 11498013
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
7. Dona E, Barry JD, Valentin G, et al. Directional tissue migration through a self-generated chemokine gradient. Nature. 2013;503:285–289. doi: 10.1038/nature1263524067609
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. doi: 10.1016/j.cell.2013.09.04624119842
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
10. Houben AJ, Moolenaar WH, Autotaxin and LPA receptor signaling in cancer. Cancer Metastasis Rev. 2011;30:557–565. doi: 10.1007/s10555-011-9319-722002750
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
12. Choi JW, Herr DR, Noguchi K, et al. LPA receptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol. 2010;50:157–186. doi: 10.1146/annurev.pharmtox.010909.10575320055701
13. Bernstein RL, Tabler M, Vestweber D, Van Driel R, Extracellular folate deaminase of Dictyostelium discoideum. Biochim Biophys Acta. 1981;677:295–302. 6271253
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
15. Zigmond SH, Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes. Nature. 1974;249:450–452. 4834231
16. De Wit RJ, Bulgakov R, Rinke de Wit TF, Konijn TM, Developmental regulation of the pathways of folate-receptor-mediated stimulation of cAMP and cGMP synthesis in Dictyostelium discoideum. Differentiation. 1986;32:192–199. 2878851
17. Abercrombie M, Heaysman J, Observations on the social behaviour of cells in tissue culture. Ii. Monolayering of fibroblasts. Exp Cell Res. 1954;6:293–306. 13173482
18. Carmona-Fontaine C, Matthews HK, Kuriyama S, et al. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature. 2008;456:957–961. doi: 10.1038/nature0744119078960
19. Liu CI, Cheng TL, Chen SZ, Huang YC, Chang WT, LrrA, a novel leucine-rich repeat protein involved in cytoskeleton remodeling, is required for multicellular morphogenesis in Dictyostelium discoideum. Dev Biol. 2005;285:238–251. 16051212
20. Van Haastert PJ, Jastorff B, Pinas JE, Konijn TM, Analogs of cyclic AMP as chemoattractants and inhibitors of Dictyostelium chemotaxis. J Bacteriol. 1982;149:99–105. 6274850
21. Muinonen-Martin AJ, Veltman DM, Kalna G, Insall RH, An improved chamber for direct visualisation of chemotaxis. PLoS ONE. 2010;5:e15309. doi: 10.1371/journal.pone.001530921179457
22. Zicha D, Dunn GA, Brown AF, A new direct-viewing chemotaxis chamber. J Cell Sci. 1991;99:769–775. 1770004
23. Bonner JT, Barkley DS, Hall EM, Konijn TM, Mason JW, O'Keefe G, 3rdWolfe PB, Acrasin, Acrasinase, and the sensitivity to acrasin in Dictyostelium discoideum. Dev Biol. 1969;20(1):72–87. 4307638
24. Darmon M, Barra J, Brachet P, The role of phosphodiesterase in aggregation of Dictyostelium discoideum. J Cell Sci. 1978;31:233–243. 209055
25. Jin M, Errede B, Behar M, et al. Yeast dynamically modify their environment to achieve better mating efficiency. Sci Signal. 2011;4:ra54. doi: 10.1126/scisignal.200176321868361
26. Insall RH, Nayler O, Kay RR, DIF-1 induces its own breakdown in Dictyostelium. EMBO J1992;11:2849–2854. 1322291
27. Zigmond SH, Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol. 1977;75(2):606–616. 264125
28. Endres RG, Wingreen NS, Accuracy of direct gradient sensing by single cells. Proc Natl Acad Sci U S A. 2008;105:15749–15754. doi: 10.1073/pnas.080468810518843108
29. Insall RH, Understanding eukaryotic chemotaxis: a pseudopod-centred view. Nat Rev Mol Cell Biol. 2010;11:453–458. doi: 10.1038/nrm290520445546
30. Tomchik KJ, Devreotes PN, Adenosine 3’,5’-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution—fluorography. Science. 1981;212:443–446. 6259734
31. Neilson MP, Veltman DM, van Haastert PJ, Webb SD, Mackenzie JA, Insall RH, Chemotaxis: a feedback-based computational model robustly predicts multiple aspects of real cell behaviour. PLoS Biol. 2011;9:e1000618. doi: 10.1371/journal.pbio.100061821610858
32. Tweedy L., Meier B., Stephan J., Heinrich D., Endres R. G., Distinct cell shapes determine accurate chemotaxis. Sci. Rep. 2013;3:2606. doi: 10.1038/srep0260624008441
33. Zaki M, Andrew N, Insall RH, Entamoeba histolytica cell movement: a central role for self-generated chemokines and chemorepellents. Proc Natl Acad Sci USA. 2006;103:18751–18756. 17132728
34. Muinonen-Martin AJ, Knecht DA, Veltman DM, Thomason PA, Kalna G, Insall RH, Measuring chemotaxis using direct visualization microscope chambers. Methods Mol Biol. 2013;1046:307–321. doi: 10.1007/978-1-62703-538-5_1823868596