Literature DB >> 11274408

How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum.

A F Marée1, P Hogeweg.   

Abstract

When individual amoebae of the cellular slime mold Dictyostelium discoideum are starving, they aggregate to form a multicellular migrating slug, which moves toward a region suitable for culmination. The culmination of the morphogenesis involves complex cell movements that transform a mound of cells into a globule of spores on a slender stalk. The movement has been likened to a "reverse fountain," whereby prestalk cells in the upper part form a stalk that moves downwards and anchors to the substratum, while prespore cells in the lower part move upwards to form the spore head. So far, however, no satisfactory explanation has been produced for this process. Using a computer simulation that we developed, we now demonstrate that the processes that are essential during the earlier stages of the morphogenesis are in fact sufficient to produce the dynamics of the culmination stage. These processes are cAMP signaling, differential adhesion, cell differentiation, and production of extracellular matrix. Our model clarifies the processes that generate the observed cell movements. More specifically, we show that periodic upward movements, caused by chemotactic motion, are essential for successful culmination, because the pressure waves they induce squeeze the stalk downwards through the cell mass. The mechanisms revealed by our model have a number of self-organizing and self-correcting properties and can account for many previously unconnected and unexplained experimental observations.

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Year:  2001        PMID: 11274408      PMCID: PMC31146          DOI: 10.1073/pnas.061535198

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


  18 in total

1.  Evolving mechanisms of morphogenesis: on the interplay between differential adhesion and cell differentiation.

Authors:  P Hogeweg
Journal:  J Theor Biol       Date:  2000-04-21       Impact factor: 2.691

Review 2.  Taking the plunge. Terminal differentiation in Dictyostelium.

Authors:  P Thomason; D Traynor; R Kay
Journal:  Trends Genet       Date:  1999-01       Impact factor: 11.639

3.  Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase.

Authors:  A J Harwood; N A Hopper; M N Simon; D M Driscoll; M Veron; J G Williams
Journal:  Cell       Date:  1992-05-15       Impact factor: 41.582

4.  Culmination in the slime mould Dictyostelium discoideum studied with a scanning electron microscope.

Authors:  D J Watts; T E Treffry
Journal:  J Embryol Exp Morphol       Date:  1976-04

5.  Dictyostelium development in the absence of cAMP.

Authors:  B Wang; A Kuspa
Journal:  Science       Date:  1997-07-11       Impact factor: 47.728

6.  [Vortex ring in a 3-dimensional active medium described by reaction-diffusion equations].

Authors:  A V Panfilov; A M Pertsov
Journal:  Dokl Akad Nauk SSSR       Date:  1984

7.  Migration and thermotaxis of dictyostelium discoideum slugs, a model study

Authors: 
Journal:  J Theor Biol       Date:  1999-08-07       Impact factor: 2.691

8.  Modulation of the cAMP relay in Dictyostelium discoideum by ammonia and other metabolites: possible morphogenetic consequences.

Authors:  G B Williams; E M Elder; M Sussman
Journal:  Dev Biol       Date:  1984-10       Impact factor: 3.582

Review 9.  Interacting signalling pathways regulating prestalk cell differentiation and movement during the morphogenesis of Dictyostelium.

Authors:  J Williams; N Hopper; A Early; D Traynor; A Harwood; T Abe; M N Simon; M Véron
Journal:  Dev Suppl       Date:  1993

10.  Periodic movements of Dictyostelium discoideum sorocarps.

Authors:  A J Durston; M H Cohen; D J Drage; M J Potel; A Robertson; D Wonio
Journal:  Dev Biol       Date:  1976-09       Impact factor: 3.582

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  53 in total

1.  Computing an organism.

Authors:  L A Segel
Journal:  Proc Natl Acad Sci U S A       Date:  2001-03-27       Impact factor: 11.205

2.  Pattern formation and traveling waves in myxobacteria: theory and modeling.

Authors:  O A Igoshin; A Mogilner; R D Welch; D Kaiser; G Oster
Journal:  Proc Natl Acad Sci U S A       Date:  2001-12-18       Impact factor: 11.205

Review 3.  Genetic control of morphogenesis in Dictyostelium.

Authors:  William F Loomis
Journal:  Dev Biol       Date:  2015-04-11       Impact factor: 3.582

4.  Cell population dynamics modulate the rates of tissue growth processes.

Authors:  Gang Cheng; Belgacem B Youssef; Pauline Markenscoff; Kyriacos Zygourakis
Journal:  Biophys J       Date:  2005-11-18       Impact factor: 4.033

5.  Cell elongation is key to in silico replication of in vitro vasculogenesis and subsequent remodeling.

Authors:  Roeland M H Merks; Sergey V Brodsky; Michael S Goligorksy; Stuart A Newman; James A Glazier
Journal:  Dev Biol       Date:  2005-12-01       Impact factor: 3.582

6.  On multiscale approaches to three-dimensional modelling of morphogenesis.

Authors:  R Chaturvedi; C Huang; B Kazmierczak; T Schneider; J A Izaguirre; T Glimm; H G E Hentschel; J A Glazier; S A Newman; M S Alber
Journal:  J R Soc Interface       Date:  2005-06-22       Impact factor: 4.118

7.  A continuum approach to modelling cell-cell adhesion.

Authors:  Nicola J Armstrong; Kevin J Painter; Jonathan A Sherratt
Journal:  J Theor Biol       Date:  2006-06-07       Impact factor: 2.691

Review 8.  Coordinated action of N-CAM, N-cadherin, EphA4, and ephrinB2 translates genetic prepatterns into structure during somitogenesis in chick.

Authors:  James A Glazier; Ying Zhang; Maciej Swat; Benjamin Zaitlen; Santiago Schnell
Journal:  Curr Top Dev Biol       Date:  2008       Impact factor: 4.897

9.  Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina.

Authors:  Jos Käfer; Takashi Hayashi; Athanasius F M Marée; Richard W Carthew; François Graner
Journal:  Proc Natl Acad Sci U S A       Date:  2007-11-14       Impact factor: 11.205

10.  Growth based morphogenesis of vertebrate limb bud.

Authors:  Yoshihiro Morishita; Yoh Iwasa
Journal:  Bull Math Biol       Date:  2008-07-31       Impact factor: 1.758

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