Neural control of body-plan axis in regenerating planaria.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
04 2019
Historique:
received: 04 10 2018
accepted: 26 02 2019
revised: 26 04 2019
pubmed: 17 4 2019
medline: 29 5 2019
entrez: 17 4 2019
Statut: epublish

Résumé

Control of axial polarity during regeneration is a crucial open question. We developed a quantitative model of regenerating planaria, which elucidates self-assembly mechanisms of morphogen gradients required for robust body-plan control. The computational model has been developed to predict the fraction of heteromorphoses expected in a population of regenerating planaria fragments subjected to different treatments, and for fragments originating from different regions along the anterior-posterior and medio-lateral axis. This allows for a direct comparison between computational and experimental regeneration outcomes. Vector transport of morphogens was identified as a fundamental requirement to account for virtually scale-free self-assembly of the morphogen gradients observed in planarian homeostasis and regeneration. The model correctly describes altered body-plans following many known experimental manipulations, and accurately predicts outcomes of novel cutting scenarios, which we tested. We show that the vector transport field coincides with the alignment of nerve axons distributed throughout the planarian tissue, and demonstrate that the head-tail axis is controlled by the net polarity of neurons in a regenerating fragment. This model provides a comprehensive framework for mechanistically understanding fundamental aspects of body-plan regulation, and sheds new light on the role of the nervous system in directing growth and form.

Identifiants

pubmed: 30990801
doi: 10.1371/journal.pcbi.1006904
pii: PCOMPBIOL-D-18-01679
pmc: PMC6485777
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1006904

Subventions

Organisme : NIH HHS
ID : S10 OD021624
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Bioessays. 2000 Aug;22(8):753-60
pubmed: 10918306
Mol Neurobiol. 2001 Aug-Dec;24(1-3):1-28
pubmed: 11831547
Physiol Rev. 2003 Jul;83(3):871-932
pubmed: 12843411
J Mol Neurosci. 2005;25(1):29-36
pubmed: 15781964
Exp Cell Res. 2005 Jun 10;306(2):299-308
pubmed: 15925584
Zoolog Sci. 2005 May;22(5):535-46
pubmed: 15930826
Dev Dyn. 2005 Sep;234(1):176-89
pubmed: 16059906
Dev Biol. 2005 Nov 15;287(2):314-35
pubmed: 16243308
J Neurosci. 2006 Apr 26;26(17):4567-76
pubmed: 16641236
J Neurosci. 1990 Jul;10(7):2176-89
pubmed: 1695944
Hum Mol Genet. 2006 Oct 15;15 Spec No 2:R227-34
pubmed: 16987888
Genes Dev. 2007 Mar 1;21(5):483-96
pubmed: 17344411
Science. 2008 Jan 18;319(5861):323-7
pubmed: 18063757
Phys Biol. 2008 Apr 10;5(1):015008
pubmed: 18403826
Zoolog Sci. 1998 Jun 1;15(3):433-40
pubmed: 18466009
Curr Opin Neurobiol. 2008 Jun;18(3):270-5
pubmed: 18778772
Science. 2008 Oct 17;322(5900):399-403
pubmed: 18927385
PLoS One. 2008;3(11):e3737
pubmed: 19011685
Bioessays. 2009 Jan;31(1):5-9
pubmed: 19154002
Nat Rev Neurosci. 2009 May;10(5):319-32
pubmed: 19377501
Int J Mol Sci. 2009 Apr 17;10(4):1729-72
pubmed: 19468337
Stem Cell Rev. 2009 Sep;5(3):231-46
pubmed: 19562527
Proc Natl Acad Sci U S A. 2009 Oct 6;106(40):17061-6
pubmed: 19805089
Science. 2009 Dec 4;326(5958):1406-10
pubmed: 19933103
Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22329-34
pubmed: 20018728
Dev Biol. 2010 Mar 1;339(1):188-99
pubmed: 20026026
Cold Spring Harb Perspect Biol. 2009 Sep;1(3):a001644
pubmed: 20066106
Cold Spring Harb Perspect Biol. 2010 Jan;2(1):a000505
pubmed: 20182600
Nat Cell Biol. 2010 Apr;12(4):341-50
pubmed: 20305650
J Biol Chem. 2010 Jul 30;285(31):24120-30
pubmed: 20511647
Birth Defects Res A Clin Mol Teratol. 2010 Aug;88(8):633-52
pubmed: 20544799
Dev Biol. 2010 Aug 15;344(2):979-91
pubmed: 20599901
Dev Biol. 2010 Nov 1;347(1):24-39
pubmed: 20707997
J Theor Biol. 2011 Jan 21;269(1):359-65
pubmed: 21044633
Prog Biophys Mol Biol. 2011 May;105(3):258-69
pubmed: 21187110
CSH Protoc. 2008 Oct 01;2008:pdb.prot5053
pubmed: 21356691
Science. 2011 May 13;332(6031):852-5
pubmed: 21566195
Development. 2011 Jun;138(12):2417-27
pubmed: 21610023
Biomed Opt Express. 2011 Aug 1;2(8):2383-91
pubmed: 21833375
J Vis Exp. 2011 Aug 31;(54):null
pubmed: 21897362
J Cell Biol. 2011 Oct 3;195(1):19-26
pubmed: 21949415
PLoS One. 2011;6(9):e24953
pubmed: 21949803
Cell Stem Cell. 2011 Nov 4;9(5):402-11
pubmed: 22056138
Genesis. 2012 Mar;50(3):176-85
pubmed: 22083727
PLoS Comput Biol. 2012;8(8):e1002654
pubmed: 22956897
Trends Neurosci. 2012 Nov;35(11):691-9
pubmed: 22989534
Curr Biol. 2012 Dec 4;22(23):2203-12
pubmed: 23122850
BMC Biol. 2012 Nov 08;10:88
pubmed: 23136835
Dev Genes Evol. 2013 Mar;223(1-2):67-84
pubmed: 23138344
Curr Opin Genet Dev. 2012 Dec;22(6):553-61
pubmed: 23200115
PLoS Biol. 2013;11(1):e1001465
pubmed: 23319891
Cilia. 2012 May 02;1(1):7
pubmed: 23351924
Dev Dyn. 2013 Jun;242(6):718-30
pubmed: 23441014
Front Physiol. 2013 Feb 25;4:21
pubmed: 23508686
J Neurosci. 2013 Mar 27;33(13):5584-9
pubmed: 23536073
Nature. 2013 May 30;497(7451):628-32
pubmed: 23624372
Cilia. 2013 Apr 29;2(1):6
pubmed: 23628112
Nature. 2013 Aug 1;500(7460):73-6
pubmed: 23883928
Cell Rep. 2013 Aug 29;4(4):633-41
pubmed: 23954785
J Neurosci. 2013 Sep 25;33(39):15362-75
pubmed: 24068803
Nat Cell Biol. 2013 Nov;15(11):1269-81
pubmed: 24121526
J R Soc Interface. 2014 Jan 08;11(92):20130918
pubmed: 24402915
Development. 2014 Feb;141(4):729-36
pubmed: 24496611
Biophys J. 2014 Feb 18;106(4):813-23
pubmed: 24559984
PLoS Pathog. 2014 Feb 20;10(2):e1003942
pubmed: 24586156
Zoology (Jena). 2014 Jun;117(3):161-2
pubmed: 24854393
Br J Pharmacol. 2015 Jan;172(1):173-84
pubmed: 25220136
Sci Rep. 2014 Sep 17;4:6388
pubmed: 25227263
Stem Cell Reports. 2014 Aug 12;3(2):339-52
pubmed: 25254346
Neuron. 2014 Oct 22;84(2):292-309
pubmed: 25374356
Nat Commun. 2015 Jan 05;6:5846
pubmed: 25556612
Cell Rep. 2015 Jan 13;10(2):253-65
pubmed: 25558068
Nature. 2015 Mar 12;519(7542):187-192
pubmed: 25731175
Dev Cell. 2015 Mar 23;32(6):719-30
pubmed: 25771893
Development. 2015 Apr 1;142(7):1203-11
pubmed: 25804733
Phys Rev Lett. 2015 Apr 3;114(13):138101
pubmed: 25884138
PLoS Comput Biol. 2015 Jun 04;11(6):e1004295
pubmed: 26042810
Oxid Med Cell Longev. 2015;2015:392476
pubmed: 26180588
Nature. 2015 Aug 20;524(7565):351-5
pubmed: 26214737
Development. 2015 Dec 15;142(24):4217-29
pubmed: 26525673
Int J Mol Sci. 2015 Nov 05;16(11):26543-54
pubmed: 26556349
Neural Regen Res. 2015 Dec;10(12):1901-5
pubmed: 26889161
Dev Neurobiol. 2017 May;77(5):643-673
pubmed: 27265625
Int J Parasitol Drugs Drug Resist. 2016 Dec;6(3):356-363
pubmed: 27397764
Front Bioeng Biotechnol. 2016 Jul 06;4:55
pubmed: 27458581
Regeneration (Oxf). 2015 Nov 26;3(1):3-25
pubmed: 27499876
Regeneration (Oxf). 2016 Jun 24;3(3):139-55
pubmed: 27606065
Elife. 2016 Sep 09;5:
pubmed: 27612382
Dev Cell. 2017 Feb 6;40(3):248-263.e4
pubmed: 28171748
Cold Spring Harb Perspect Biol. 2018 Feb 1;10(2):
pubmed: 28264820
Dev Cell. 2017 Mar 13;40(5):491-504.e5
pubmed: 28292427
Biophys J. 2017 May 23;112(10):2231-2243
pubmed: 28538159
Nat Commun. 2017 Sep 25;8(1):587
pubmed: 28943634
J R Soc Interface. 2017 Sep;14(134):
pubmed: 28954851
Theor Biol Med Model. 2017 Oct 10;14(1):19
pubmed: 28992816
Prog Biophys Mol Biol. 2018 Sep;137:52-68
pubmed: 29626560
J Cell Sci. 2018 Apr 13;131(8):null
pubmed: 29654160
Science. 2018 May 25;360(6391):
pubmed: 29674431
J Neurobiol. 1973;4(6):535-42
pubmed: 4130195
Mol Pharmacol. 1970 Nov;6(6):597-603
pubmed: 4322367
Exp Brain Res. 1973 Mar 19;16(5):501-6
pubmed: 4695778
J Neurosci. 1996 May 15;16(10):3154-65
pubmed: 8627354
Biol Bull. 1998 Jun;194(3):358-60
pubmed: 9664662
Mol Cell Biochem. 1998 Jul;184(1-2):169-82
pubmed: 9746320
Bioorg Med Chem Lett. 1998 Oct 20;8(20):2839-44
pubmed: 9873633

Auteurs

Alexis Pietak (A)

Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.

Johanna Bischof (J)

Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.
Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

Joshua LaPalme (J)

Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.
Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

Junji Morokuma (J)

Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.
Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

Michael Levin (M)

Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.
Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

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Classifications MeSH