Literature DB >> 9256451

Desynchronization of cells on the developmental path triggers the formation of spiral waves of cAMP during Dictyostelium aggregation.

J Lauzeral1, J Halloy, A Goldbeter.   

Abstract

Whereas it is relatively easy to account for the formation of concentric (target) waves of cAMP in the course of Dictyostelium discoideum aggregation after starvation, the origin of spiral waves remains obscure. We investigate a physiologically plausible mechanism for the spontaneous formation of spiral waves of cAMP in D. discoideum. The scenario relies on the developmental path associated with the continuous changes in the activity of enzymes such as adenylate cyclase and phosphodiesterase observed during the hours that follow starvation. These changes bring the cells successively from a nonexcitable state to an excitable state in which they relay suprathreshold cAMP pulses, and then to autonomous oscillations of cAMP, before the system returns to an excitable state. By analyzing a model for cAMP signaling based on receptor desensitization, we show that the desynchronization of cells on this developmental path triggers the formation of fully developed spirals of cAMP. Developmental paths that do not correspond to the sequence of dynamic transitions no relay-relay-oscillations-relay are less able or fail to give rise to the formation of spirals.

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Year:  1997        PMID: 9256451      PMCID: PMC23083          DOI: 10.1073/pnas.94.17.9153

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  29 in total

1.  Positive genetic feedback governs cAMP spiral wave formation in Dictyostelium.

Authors:  H Levine; I Aranson; L Tsimring; T V Truong
Journal:  Proc Natl Acad Sci U S A       Date:  1996-06-25       Impact factor: 11.205

2.  Rotating spiral waves created by geometry.

Authors:  K Agladze; J P Keener; S C Müller; A Panfilov
Journal:  Science       Date:  1994-06-17       Impact factor: 47.728

3.  Adenylate cyclase activity in Dictyostelium discoideum amoebae and its changes during differentiation.

Authors:  C Klein
Journal:  FEBS Lett       Date:  1976-09-15       Impact factor: 4.124

4.  Spiral waves of chemical activity.

Authors:  A T Winfree
Journal:  Science       Date:  1972-02-11       Impact factor: 47.728

Review 5.  Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium.

Authors:  G Gerisch
Journal:  Annu Rev Biochem       Date:  1987       Impact factor: 23.643

6.  Pacemaker activity during aggregation in Dictyostelium discoideum.

Authors:  A J Durston
Journal:  Dev Biol       Date:  1974-04       Impact factor: 3.582

7.  Origin and evolution of circular waves and spirals in Dictyostelium discoideum territories.

Authors:  E Pálsson; E C Cox
Journal:  Proc Natl Acad Sci U S A       Date:  1996-02-06       Impact factor: 11.205

8.  Kinetics and concentration dependence of reversible cAMP-induced modification of the surface cAMP receptor in Dictyostelium.

Authors:  P N Devreotes; J A Sherring
Journal:  J Biol Chem       Date:  1985-05-25       Impact factor: 5.157

9.  Cell density-sensing in Dictyostelium by means of the accumulation rate, diffusion coefficient and activity threshold of a protein secreted by starved cells.

Authors:  I S Yuen; R H Gomer
Journal:  J Theor Biol       Date:  1994-04-07       Impact factor: 2.691

10.  Control of developmental transitions in the cyclic AMP signalling system of Dictyostelium discoideum.

Authors:  A Goldbeter; L A Segel
Journal:  Differentiation       Date:  1980       Impact factor: 3.880

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  17 in total

Review 1.  Oscillation patterns in negative feedback loops.

Authors:  Simone Pigolotti; Sandeep Krishna; Mogens H Jensen
Journal:  Proc Natl Acad Sci U S A       Date:  2007-04-05       Impact factor: 11.205

2.  Selection for spiral waves in the social amoebae Dictyostelium.

Authors:  E Pálsson; K J Lee; R E Goldstein; J Franke; R H Kessin; E C Cox
Journal:  Proc Natl Acad Sci U S A       Date:  1997-12-09       Impact factor: 11.205

Review 3.  Dissipative structures in biological systems: bistability, oscillations, spatial patterns and waves.

Authors:  Albert Goldbeter
Journal:  Philos Trans A Math Phys Eng Sci       Date:  2018-07-28       Impact factor: 4.226

4.  Predictability of spatio-temporal patterns in a lattice of coupled FitzHugh-Nagumo oscillators.

Authors:  Miriam Grace; Marc-Thorsten Hütt
Journal:  J R Soc Interface       Date:  2013-01-24       Impact factor: 4.118

5.  Clathrin Assembly Defines the Onset and Geometry of Cortical Patterning.

Authors:  Yang Yang; Ding Xiong; Anne Pipathsouk; Orion D Weiner; Min Wu
Journal:  Dev Cell       Date:  2017-11-20       Impact factor: 12.270

6.  Fold-change detection and scale invariance of cell-cell signaling in social amoeba.

Authors:  Keita Kamino; Yohei Kondo; Akihiko Nakajima; Mai Honda-Kitahara; Kunihiko Kaneko; Satoshi Sawai
Journal:  Proc Natl Acad Sci U S A       Date:  2017-05-11       Impact factor: 11.205

7.  Spatiotemporal variation of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators.

Authors:  U Rascher; M T Hütt; K Siebke; B Osmond; F Beck; U Lüttge
Journal:  Proc Natl Acad Sci U S A       Date:  2001-09-25       Impact factor: 11.205

8.  A cAMP signaling model explains the benefit of maintaining two forms of phosphodiesterase in Dictyostelium.

Authors:  Eiríkur Pálsson
Journal:  Biophys J       Date:  2009-11-04       Impact factor: 4.033

9.  Excitable waves and direction-sensing in Dictyostelium discoideum: steps towards a chemotaxis model.

Authors:  Arpan Bhowmik; Wouter-Jan Rappel; Herbert Levine
Journal:  Phys Biol       Date:  2016-01-29       Impact factor: 2.583

10.  Predicting the distribution of spiral waves from cell properties in a developmental-path model of Dictyostelium pattern formation.

Authors:  Daniel Geberth; Marc-Thorsten Hütt
Journal:  PLoS Comput Biol       Date:  2009-07-10       Impact factor: 4.475

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