Emergent Stem Cell Homeostasis in the C. elegans Germline Is Revealed by Hybrid Modeling

Biophysical Journal

Volumn 109, Issue 2, 2015, Pages 428-438

  Hall, Benjamin A ^a,b   Piterman, Nir ^c   Hajnal, Alex ^d   Fisher, Jasmin ^b,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MICROSOFT RESEARCH   (United Kingdom)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS;

ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; GERM CELL; GONAD; HOMEOSTASIS; PHYSIOLOGY; STEM CELL; VIDEORECORDING;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; GERM CELLS; GONADS; HOMEOSTASIS; MODELS, BIOLOGICAL; STEM CELLS; VIDEO RECORDING;

EID: 84937557261     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.06.007     Document Type: Article

References (47)

1. J. Kimble, and S.L. Crittenden Germline proliferation and its control WormBook 2005 1 14
2. J.E. Kimble, and J.G. White On the control of germ cell development in Caenorhabditis elegans Dev. Biol. 81 1981 208 219
3. A.D. Lander, and J. Kimble T. Oskarsson What does the concept of the stem cell niche really mean today? BMC Biol. 10 2012 19
4. J. Maciejowski, and N. Ugel E.J. Hubbard Quantitative analysis of germline mitosis in adult C. elegans Dev. Biol. 292 2006 142 151
5. S.L. Crittenden, and K.A. Leonhard J. Kimble Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line Mol. Biol. Cell 17 2006 3051 3061
6. D.T. Byrd, and K. Knobel J. Kimble A DTC niche plexus surrounds the germline stem cell pool in Caenorhabditis elegans PLoS ONE 9 2014 e88372
7. S.L. Crittenden, and J. Kimble Analysis of the C. elegans germline stem cell region Methods Mol. Biol. 450 2008 27 44
8. N. Suh, and S.L. Crittenden J. Kimble FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline Genetics 181 2009 1249 1260
9. J. Kimble Molecular regulation of the mitosis/meiosis decision in multicellular organisms Cold Spring Harb. Perspect. Biol. 3 2011 a002683
10. M.H. Lee, and M. Ohmachi T. Schedl Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development Genetics 177 2007 2039 2062
11. E.J.A. Hubbard, and D. Greenstein The Caenorhabditis elegans gonad: a test tube for cell and developmental biology Dev. Dyn. 218 2000 2 22
12. S.W. Leacock, and V. Reinke Expression profiling of MAP kinase-mediated meiotic progression in Caenorhabditis elegans PLoS Gen 2 2006 e174
13. M. Ohmachi, and C.E. Rocheleau M.V. Sundaram C. elegans ksr-1 and ksr-2 have both unique and redundant functions and are required for MPK-1 ERK phosphorylation Curr. Biol 12 2002 427 433
14. D.S. Cha, and U.S. Datla M.H. Lee The Ras-ERK MAPK regulatory network controls dedifferentiation in Caenorhabditis elegans germline Biochim. Biophys. Acta 1823 2012 1847 1855
15. L. Galluzzi, and N. Joza G. Kroemer No death without life: vital functions of apoptotic effectors Cell Death Differ. 15 2008 1113 1123
16. A. Bailly, and A. Gartner Germ cell apoptosis and DNA damage responses Adv. Exp. Med. Biol. 757 2013 249 276
17. R. Rutkowski, and R. Dickinson A. Gartner Regulation of Caenorhabditis elegans p53/CEP-1-dependent germ cell apoptosis by Ras/MAPK signaling PLoS Genet. 7 2011 e1002238
18. E.A. Kritikou, and S. Milstein M.O. Hengartner C. elegans GLA-3 is a novel component of the MAP kinase MPK-1 signaling pathway required for germ cell survival Genes Dev. 20 2006 2279 2292
19. A. Gartner, P.R. Boag, and T.K. Blackwell Germline survival and apoptosis WormBook 2008 1 20
20. D.J. Killian, and E.J. Hubbard Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line Dev. Biol. 279 2005 322 335
21. J. Fisher, and T.A. Henzinger Executable cell biology Nat. Biotechnol. 25 2007 1239 1249
22. J. Fisher, and N. Piterman The executable pathway to biological networks Brief Funct. Genomics 9 2010 79 92
23. A. Sadot, and J. Fisher D. Harel Toward verified biological models IEEE/ACM Trans 5 2008 223 234
24. N. Bonzanni, and K.A. Feenstra E. Krepska What can formal methods bring to systems biology? FM 2009: Formal Methods 2009 Springer Berlin, Germany 16 22
25. N. Kam, and H. Kugler E.J.A. Hubbard A scenario-based approach to modeling development: a prototype model of C. elegans vulval fate specification Dev. Biol. 323 2008 1 5
26. N. Kam, I.R. Cohen, and D. Harel The immune system as a reactive system: modeling T cell activation with statecharts Human-Centric Computing Languages and Environments 2001 IEEE Piscataway, NJ 15 22
27. S. Efroni, D. Harel, and I.R. Cohen Toward rigorous comprehension of biological complexity: modeling, execution, and visualization of thymic T-cell maturation Genome Res. 13 2003 2485 2497
28. A. Clark, and V. Galpin J. Hillston Formal methods for checking the consistency of biological models Adv. Exp. Med. Biol. 736 2012 461 475
29. E.M. Clarke, O. Grumberg, and D.A. Peled Model Checking 1999 The MIT Press Cambridge, MA
30. A. Beyer, and R. Eberhard J. Fisher A dynamic physical model of cell migration, differentiation and apoptosis in Caenorhabditis elegans I.I. Goryanin, A.B. Goryachev, editors. Advances in Systems Biology 2012 Springer New York 211 233
31. T. Yamamoto, and N. Kanda Computational model for Brownian dynamics simulation of polymer/clay nanocomposites under flow J. Non-Newt. Fluid Mech. 181-182 2012 1 10
32. T. Yamamoto, T. Suga, and N. Mori Brownian dynamics simulation of orientational behavior, flow-induced structure, and rheological properties of a suspension of oblate spheroid particles under simple shear Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72 2005 021509
33. G. Rosser, and R.E. Baker A.G. Fletcher Modelling and analysis of bacterial tracks suggest an active reorientation mechanism in Rhodobacter sphaeroides J. R. Soc. Interface 11 2014 20140320
34. I. Ramis-Conde, and D. Drasdo M.A.J. Chaplain Modeling the influence of the E-cadherin-β-catenin pathway in cancer cell invasion: a multiscale approach Biophys. J. 95 2008 155 165
35. M.A. Schaub, T.A. Henzinger, and J. Fisher Qualitative networks: a symbolic approach to analyze biological signaling networks BMC Syst. Biol. 1 2007 4
36. W. Gunsteren, and H. Berendsen Algorithms for Brownian dynamics Mol. Phys. 45 1982 637 647
37. D. Benque, and S. Bourton M. Vardi BMA: visual tool for modeling and analyzing biological networks P. Madhusudan, S. Seshia, editors. Computer Aided Verification 2012 Springer Berlin, Germany 686 692
38. S. Nawaz, and P. Sánchez I.A. Schaap Cell visco-elasticity measured with AFM and optical trapping at sub-micrometer deformations PLoS ONE 7 2012 e45297
39. van der Spoel, D., E. Lindahl,..., H. J. C. Berendsen. 2010. GROMACS User Manual, Ver. 4.6 Beta1. www.gromacs.org.
40. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
41. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
42. E.R. Fearon, and B. Vogelstein A genetic model for colorectal tumorigenesis Cell 61 1990 759 767
43. T.L. Gumienny, and E. Lambie M.O. Hengartner Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline Development 126 1999 1011 1022
44. Y. Wang, and S. Wang L. Xie The roles of DNA damage-dependent signals and MAPK cascades in tributyltin-induced germline apoptosis in Caenorhabditis elegans Chemosphere 108 2014 231 238
45. R. Eberhard, and L. Stergiou M.O. Hengartner Ribosome synthesis and MAPK activity modulate ionizing radiation-induced germ cell apoptosis in Caenorhabditis elegans PLoS Genet. 9 2013 e1003943
46. A. Hajnal, and T. Berset The C. elegans MAPK phosphatase LIP-1 is required for the G(2)/M meiotic arrest of developing oocytes EMBO J. 21 2002 4317 4326
47. S.M. Pinto, and M.O. Hengartner Cleaning up the mess: cell corpse clearance in Caenorhabditis elegans Curr. Opin. Cell Biol. 24 2012 881 888