publication . Article . 2018

An Autocrine Proliferation Repressor Regulates Dictyostelium discoideum Proliferation and Chemorepulsion Using the G Protein-Coupled Receptor GrlH

Yu Tang; Yuantai Wu; Sarah E. Herlihy; Francisco J. Brito-Aleman; Jose H. Ting; Chris Janetopoulos; Richard H. Gomer; Scott D. Emr;
Open Access
  • Published: 01 Feb 2018 Journal: mBio, volume 9 (eissn: 2150-7511, Copyright policy)
  • Publisher: American Society for Microbiology
Abstract
IMPORTANCE Little is known about how eukaryotic cells can count themselves and thus regulate the size of a tissue or density of cells. In addition, little is known about how eukaryotic cells can sense a repellant signal and move away from the source of the repellant, for instance, to organize the movement of cells in a developing embryo or to move immune cells out of a tissue. In this study, we found that a eukaryotic microbe uses G protein-coupled receptors to mediate both cell density sensing and chemorepulsion.
Subjects
free text keywords: Secretion, G protein-coupled receptor, Autocrine signalling, Biology, Chemorepulsion, Genetics, Receptor, Cell biology, Dictyostelium discoideum, biology.organism_classification, G protein, Repressor, Microbiology, QR1-502, Research Article, cell density sensing, Dictyostelium, G-protein-coupled receptors, cell proliferation, quorum sensing
Funded by
NIH| Elucidation of a eukaryotic chemorepulsion mechanism
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM118355-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Elucidation of a Dictyostelium chalone
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM102280-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
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34 references, page 1 of 3

1.Weiss P, Kavanau JL 1957 A model of growth and growth control in mathematical ter ms. J Gen Physiol 41:1–47. doi:10.1085/jgp.41.1.1.13463267 [OpenAIRE] [PubMed] [DOI]

2.Elgjo K, Reichelt KL 2004 Chalones: from aqueous extracts to oligopeptides. Cell Cycle 3:1208–1211. doi:10.4161/cc.3.9.1087.15326370 [OpenAIRE] [PubMed] [DOI]

3.Bullough WS, Laurence EB 1968 Melanocyte chalone and mitotic control in melanomata. Nature 220:137–138. doi:10.1038/220137a0.5684821 [OpenAIRE] [PubMed] [DOI]

4.Bullough WS, Laurence EB 1968 Control of mitosis in mouse and hamster melanomata by means of the melanocyte chalone. Eur J Canc er 4:607–615. doi:10.1016/0014-2964(68)90045-5.5717957 [OpenAIRE] [PubMed] [DOI]

5.Brock DA, Gomer RH 2005 A secreted factor represses cell proliferation in Dictyostelium. Development 132:4553–4562. doi:10.1242/dev.02032.16176950 [OpenAIRE] [PubMed] [DOI]

6.Bakthavatsalam D, Brock DA, Nikravan NN, Houston KD, Hatton RD, Gomer RH 2008 The secreted Dictyostelium protein CfaD is a chalone. J Cell Sci 121:2473–2480. doi:10.1242/jcs.026682.18611962 [OpenAIRE] [PubMed] [DOI]

7.Choe JM, Bakthavatsalam D, Phillips JE, Gomer RH 2009 Dictyostelium cells bind a secreted autocrine factor that represses cell proliferation. BMC Biochem 10:4. doi:10.1186/1471-2091-10-4.19187549 [OpenAIRE] [PubMed] [DOI]

8.Bakthavatsalam D, Choe JM, Hanson NE, Gomer RH 2009 A Dictyostelium chalone uses G proteins to regulate proliferation. BMC Biol 7:44. doi:10.1186/1741-7007-7-44.19635129 [OpenAIRE] [PubMed] [DOI]

9.Phillips JE, Huang E, Shaulsky G, Gomer RH 2011 The putative bZIP transcription factor BzpN slows proliferation and functions in the regulation of cell density by autocrine signals in Dictyostelium. PLoS One 6:e21765. doi:10.1371/journal.pone.0021765.21760904 [OpenAIRE] [PubMed] [DOI]

10.Phillips JE, Gomer RH 2010 The ROCO kinase QkgA is necessary for proliferation inhibition by autocrine signals in Dictyostelium discoideum. Eukaryot Cell 9:1557–1565. doi:10.1128/EC.00121-10.20709790 [OpenAIRE] [PubMed] [DOI]

11.Bakthavatsalam D, White MJ, Herlihy SE, Phillips JE, Gomer RH 2014 A retinoblastoma orthologue is required for the sensing of a chalone in Dictyostelium discoideum. Eukaryot Cell 13:376–382. doi:10.1128/EC.00306-13.24390142 [OpenAIRE] [PubMed] [DOI]

12.Phillips JE, Gomer RH 2012 A secreted protein is an endogenous chemorepellant in Dictyostelium discoideum. Proc Natl Acad Sci U S A 109:10990–10995. doi:10.1073/pnas.1206350109.22711818 [OpenAIRE] [PubMed] [DOI]

13.Herlihy SE, Tang YT, Gomer RH 2013 A Dictyostelium secreted factor requires a PTEN-like phosphatase to slow proliferation and induce chemorepulsion. PLoS One 8:e59365. doi:10.1371/journal.pone.0059365.23555023 [OpenAIRE] [PubMed] [DOI]

14.Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, et al.2005 The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57. doi:10.1038/nature03481.15875012 [OpenAIRE] [PubMed] [DOI]

15.Heidel AJ, Lawal HM, Felder M, Schilde C, Helps NR, Tunggal B, Rivero F, John U, Schleicher M, Eichinger L, Platzer M, Noegel AA, Schaap P, Glöckner G 2011 Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communicati on. Genome Res 21:1882–1891. doi:10.1101/gr.121137.111.21757610 [OpenAIRE] [PubMed] [DOI]

34 references, page 1 of 3
Related research
Abstract
IMPORTANCE Little is known about how eukaryotic cells can count themselves and thus regulate the size of a tissue or density of cells. In addition, little is known about how eukaryotic cells can sense a repellant signal and move away from the source of the repellant, for instance, to organize the movement of cells in a developing embryo or to move immune cells out of a tissue. In this study, we found that a eukaryotic microbe uses G protein-coupled receptors to mediate both cell density sensing and chemorepulsion.
Subjects
free text keywords: Secretion, G protein-coupled receptor, Autocrine signalling, Biology, Chemorepulsion, Genetics, Receptor, Cell biology, Dictyostelium discoideum, biology.organism_classification, G protein, Repressor, Microbiology, QR1-502, Research Article, cell density sensing, Dictyostelium, G-protein-coupled receptors, cell proliferation, quorum sensing
Funded by
NIH| Elucidation of a eukaryotic chemorepulsion mechanism
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM118355-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Elucidation of a Dictyostelium chalone
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM102280-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
Download fromView all 3 versions
mBio
Article . 2018
Provider: Crossref
mBio
Article
Provider: UnpayWall
mBio
Article . 2018
34 references, page 1 of 3

1.Weiss P, Kavanau JL 1957 A model of growth and growth control in mathematical ter ms. J Gen Physiol 41:1–47. doi:10.1085/jgp.41.1.1.13463267 [OpenAIRE] [PubMed] [DOI]

2.Elgjo K, Reichelt KL 2004 Chalones: from aqueous extracts to oligopeptides. Cell Cycle 3:1208–1211. doi:10.4161/cc.3.9.1087.15326370 [OpenAIRE] [PubMed] [DOI]

3.Bullough WS, Laurence EB 1968 Melanocyte chalone and mitotic control in melanomata. Nature 220:137–138. doi:10.1038/220137a0.5684821 [OpenAIRE] [PubMed] [DOI]

4.Bullough WS, Laurence EB 1968 Control of mitosis in mouse and hamster melanomata by means of the melanocyte chalone. Eur J Canc er 4:607–615. doi:10.1016/0014-2964(68)90045-5.5717957 [OpenAIRE] [PubMed] [DOI]

5.Brock DA, Gomer RH 2005 A secreted factor represses cell proliferation in Dictyostelium. Development 132:4553–4562. doi:10.1242/dev.02032.16176950 [OpenAIRE] [PubMed] [DOI]

6.Bakthavatsalam D, Brock DA, Nikravan NN, Houston KD, Hatton RD, Gomer RH 2008 The secreted Dictyostelium protein CfaD is a chalone. J Cell Sci 121:2473–2480. doi:10.1242/jcs.026682.18611962 [OpenAIRE] [PubMed] [DOI]

7.Choe JM, Bakthavatsalam D, Phillips JE, Gomer RH 2009 Dictyostelium cells bind a secreted autocrine factor that represses cell proliferation. BMC Biochem 10:4. doi:10.1186/1471-2091-10-4.19187549 [OpenAIRE] [PubMed] [DOI]

8.Bakthavatsalam D, Choe JM, Hanson NE, Gomer RH 2009 A Dictyostelium chalone uses G proteins to regulate proliferation. BMC Biol 7:44. doi:10.1186/1741-7007-7-44.19635129 [OpenAIRE] [PubMed] [DOI]

9.Phillips JE, Huang E, Shaulsky G, Gomer RH 2011 The putative bZIP transcription factor BzpN slows proliferation and functions in the regulation of cell density by autocrine signals in Dictyostelium. PLoS One 6:e21765. doi:10.1371/journal.pone.0021765.21760904 [OpenAIRE] [PubMed] [DOI]

10.Phillips JE, Gomer RH 2010 The ROCO kinase QkgA is necessary for proliferation inhibition by autocrine signals in Dictyostelium discoideum. Eukaryot Cell 9:1557–1565. doi:10.1128/EC.00121-10.20709790 [OpenAIRE] [PubMed] [DOI]

11.Bakthavatsalam D, White MJ, Herlihy SE, Phillips JE, Gomer RH 2014 A retinoblastoma orthologue is required for the sensing of a chalone in Dictyostelium discoideum. Eukaryot Cell 13:376–382. doi:10.1128/EC.00306-13.24390142 [OpenAIRE] [PubMed] [DOI]

12.Phillips JE, Gomer RH 2012 A secreted protein is an endogenous chemorepellant in Dictyostelium discoideum. Proc Natl Acad Sci U S A 109:10990–10995. doi:10.1073/pnas.1206350109.22711818 [OpenAIRE] [PubMed] [DOI]

13.Herlihy SE, Tang YT, Gomer RH 2013 A Dictyostelium secreted factor requires a PTEN-like phosphatase to slow proliferation and induce chemorepulsion. PLoS One 8:e59365. doi:10.1371/journal.pone.0059365.23555023 [OpenAIRE] [PubMed] [DOI]

14.Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, et al.2005 The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57. doi:10.1038/nature03481.15875012 [OpenAIRE] [PubMed] [DOI]

15.Heidel AJ, Lawal HM, Felder M, Schilde C, Helps NR, Tunggal B, Rivero F, John U, Schleicher M, Eichinger L, Platzer M, Noegel AA, Schaap P, Glöckner G 2011 Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communicati on. Genome Res 21:1882–1891. doi:10.1101/gr.121137.111.21757610 [OpenAIRE] [PubMed] [DOI]

34 references, page 1 of 3
Related research
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