A mathematical model of collective cell migration in a three-dimensional, heterogeneous environment

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Stonko, David P ^a   Manning, Lathiena ^a   Starz Gaiano, Michelle ^a   Peercy, Bradford E ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL COUNT; CELL MIGRATION; CELL MOTION; CELL POPULATION; CELL SIZE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; IN VIVO STUDY; MATHEMATICAL MODEL; NONHUMAN; OOCYTE DEVELOPMENT; ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; CELL POLARITY; COMPUTER SIMULATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MARKOV CHAIN; OOCYTE; PHYSIOLOGY; STATISTICAL MODEL;

ANIMALIA;

ANIMALS; CELL ADHESION; CELL LINEAGE; CELL MOVEMENT; CELL POLARITY; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; MODELS, BIOLOGICAL; MODELS, STATISTICAL; OOCYTES; OOGENESIS; STOCHASTIC PROCESSES;

EID: 84928911029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122799     Document Type: Article

References (51)

1. Starz-Gaiano M, Melani M, Wang X, Meinhardt H, Montell DJ. Feedback Inhibition of JAK/STAT Signaling by Apontic Is Required to Limit an Invasive Cell Population. Developmental Cell. 2008; 14(5):726-738. Available from: http://www.sciencedirect.com/science/article/pii/S1534580708001135. doi: 10.1016/j.devcel.2008.03.005 PMID: 18477455
2. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, et al. Cell Migration: Integrating Signals from Front to Back. Science. 2003; 302(5651):1704-1709. Available from: http://www.sciencemag.org/content/302/5651/1704.abstract. doi: 10.1126/science.1092053 PMID: 14657486
3. Montell DJ, Yoon WH, Starz-Gaiano M. Group choreography: mechanisms orchestrating the collective movement of border cells. Nature Reviews Molecular Cell Biology. 2012; 13(10):631-645. doi: 10.1038/nrm3433 PMID: 23000794
4. Wright N, Hoffmann W, Otto W, Rio MC, Thim L. Rolling in the clover: trefoil factor family (TFF)-domain peptides, cell migration and cancer. FEBS Letters. 1997; 408(2):121-123. Available from: http://www.sciencedirect.com/science/article/pii/S0014579397004249. doi: 10.1016/S0014-5793(97)00424-9 PMID: 9187350
5. Ridley AJ. Rho GTPases and cell migration. Journal of Cell Science. 2001; 114(15):2713-2722. Available from: http://jcs.biologists.org/content/114/15/2713.abstract PMID: 11683406
6. Webb DJ, Parsons JT, Horwitz AF. Adhesion assembly, disassembly and turnover in migrating cellsover and over and over again. Nature cell biology. 2002; 4(4):E97-E100. doi: 10.1038/ncb0402-e97 PMID: 11944043
7. Van Haastert PJ, Devreotes PN. Chemotaxis: signalling the way forward. Nature reviews Molecular cell biology. 2004; 5(8):626-634. doi: 10.1038/nrm1435 PMID: 15366706
8. Aman A, Piotrowski T. Cell migration during morphogenesis. Developmental Biology. 2010; 341(1):20-33. Special Section: Morphogenesis. Available from: http://www.sciencedirect.com/science/article/pii/S0012160609013608. doi: 10.1016/j.ydbio.2009.11.014 PMID: 19914236
9. Theveneau E, Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Developmental biology. 2012; 366(1):34-54. doi: 10.1016/j.ydbio.2011.12.041 PMID: 22261150
10. Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. The Journal of cell biology. 2010; 188(1):11-19. doi: 10.1083/jcb.200909003 PMID: 19951899
11. Hudson AM, Cooley L. Methods for studying oogenesis. Methods. 2014; 68(1):207-17. doi: 10.1016/j.ymeth.2014.01.005 PMID: 24440745
12. Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. A Systematic Analysis of Human Disease-Associated Gene Sequences In Drosophila melanogaster. Genome Research. 2001; 11(6):1114-1125. Available from: http://genome.cshlp.org/content/11/6/1114.abstract. doi: 10.1101/gr.169101 PMID: 11381037
13. Silver DL, Geisbrecht ER, Montell DJ. Requirement for JAK/STAT signaling throughout border cell migration in Drosophila. Development. 2005; 132(15):3483-3492. doi: 10.1242/dev.01910 PMID: 16000386
14. McDonald JA, Pinheiro EM, Montell DJ. PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development. 2003; 130(15):3469-3478. Available from: http://dev.biologists.org/content/130/15/3469.abstract. doi: 10.1242/dev.00574 PMID: 12810594
15. Duchek P, Somogyi K, Jékely G, Beccari S, Rørth P. Guidance of Cell Migration by the Drosophila PDGF/VEGF Receptor. Cell. 2001; 107(1):17-26. doi: 10.1016/S0092-8674(01)00502-5 PMID: 11595182
16. Duchek P, Rørth P. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science. 2001; 291(5501):131-133. doi: 10.1126/science.291.5501.131 PMID: 11141565
17. Cai D, Chen SC, Prasad M, He L, Wang X, Choesmel-Cadamuro V, et al. Mechanical Feedback through E-Cadherin Promotes Direction Sensing during Collective Cell Migration. Cell. 2014; 157(5):1146-1159. doi: 10.1016/j.cell.2014.03.045 PMID: 24855950
18. Niewiadomska P, Godt D, Tepass U. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. The Journal of cell biology. 1999; 144(3):533-547. doi: 10.1083/jcb.144.3.533 PMID: 9971747
19. Prasad M, Montell DJ. Cellular and molecular mechanisms of border cell migration analyzed using time-lapse live-cell imaging. Developmental cell. 2007; 12(6):997-1005. doi: 10.1016/j.devcel.2007.03.021 PMID: 17543870
20. Bianco A, Poukkula M, Cliffe A, Mathieu J, Luque CM, Fulga TA, et al. Two distinct modes of guidance signalling during collective migration of border cells. Nature. 2007; 448(7151):362-365. doi: 10.1038/nature05965 PMID: 17637670
21. Thompson RN, Yates CA, Baker RE. Modeling Cell Migration and Adhesion During Development. Bulletin of Mathematical Biology. 2012; 74(12):2793-2809. Available from: http://dx.doi.org/10.1007/s11538-012-9779-0 PMID: 23081728
22. Yamao M, Naoki H, Ishii S. Multi-Cellular Logistics of Collective Cell Migration. PLoS ONE. 2011; 6(12):1-11. doi: 10.1371/journal.pone.0027950
23. Rangarajan R, Zaman MH. Modeling cell migration in 3D: Status and challenges. Cell Adhesion & Migration. 2008; 2(2):106-109. doi: 10.4161/cam.2.2.6211
24. Danuser G, Allard J, Mogilner A. Mathematical Modeling of Eukaryotic Cell Migration: Insights Beyond Experiments. Annual review of cell and developmental biology. 2013; 29:501-528. doi: 10.1146/annurev-cellbio-101512-122308 PMID: 23909278
25. Etienne-Manneville S. Neighborly relations during collective migration. Current opinion in cell biology. 2014; 30:51-59. doi: 10.1016/j.ceb.2014.06.004 PMID: 24997300
26. Iglesias PA, Devreotes PN. Navigating through models of chemotaxis. Current opinion in cell biology. 2008; 20(1):35-40. doi: 10.1016/j.ceb.2007.11.011 PMID: 18207721
27. Mogilner A. Mathematics of cell motility: have we got its number? Journal of mathematical biology. 2009; 58(1-2):105-134. doi: 10.1007/s00285-008-0182-2 PMID: 18461331
28. Mitchison TJ, Cramer LP. Actin-Based Cell Motility and Cell Locomotion. Cell. 1996; 84(3):371-379. Available from: http://www.sciencedirect.com/science/article/pii/S0092867400812817. doi: 10.1016/S0092-8674(00)81281-7 PMID: 8608590
29. Pollard TD, Borisy GG. Cellular Motility Driven by Assembly and Disassembly of Actin Filaments. Cell. 2003; 112(4):453-465. Available from: http://www.sciencedirect.com/science/article/pii/S009286740300120X. doi: 10.1016/S0092-8674(03)00120-X PMID: 12600310
30. Bretscher MS. Getting Membrane Flow and the Cytoskeleton to Cooperate in Moving Cells. Cell. 1996; 87(4):601-606. Available from: http://www.sciencedirect.com/science/article/pii/S009286740081380X. doi: 10.1016/S0092-8674(00)81380-X PMID: 8929529
31. Arciero J, Swigon D. Equation-Based Models of Wound Healing and Collective Cell Migration. In: Vodovotz Y, An G, editors. Complex Systems and Computational Biology Approaches to Acute Inflammation. Springer New York; 2013. p. 185-207.
32. Vedel S, Tay S, Johnston DM, Bruus H, Quake SR. Migration of cells in a social context. Proceedings of the National Academy of Sciences. 2013; 110(1):129-134. doi: 10.1073/pnas.1204291110
33. Dalle Nogare D, Somers K, Rao S, Matsuda M, Reichman-Fried M, Raz E, et al. Leading and trailing cells cooperate in collective migration of the zebrafish posterior lateral line primordium. Development. 2014; 141(16):3188-3196. doi: 10.1242/dev.106690 PMID: 25063456
34. Osterfield M, Du X, Schüpbach T, Wieschaus E, Shvartsman SY. Three-Dimensional Epithelial Morphogenesis in the Developing Drosophila Egg. Developmental cell. 2013; 24(4):400-410. doi: 10.1016/j.devcel.2013.01.017 PMID: 23449472
35. Fletcher AG, Osterfield M, Baker RE, Shvartsman SY. Vertex Models of Epithelial Morphogenesis. Biophysical Journal. 2014; 106:2291-2304. doi: 10.1016/j.bpj.2013.11.4498 PMID: 24896108
36. Ramis-Conde I, Drasdo D, Anderson AR, Chaplain MA. Modeling the Influence of the E-Cadherin-β-Catenin Pathway in Cancer Cell Invasion: A Multiscale Approach. Biophysical journal. 2008; 95(1):155-165. doi: 10.1529/biophysj.107.114678 PMID: 18339758
37. Zaman MH, Kamm RD, Matsudaira P, Lauffenburger DA. Computational model for cell migration in three-dimensional matrices. Biophysical journal. 2005; 89(2):1389-1397. doi: 10.1529/biophysj.105.060723 PMID: 15908579
38. Zaman MH, Trapani LM, Sieminski AL, MacKellar D, Gong H, Kamm RD, et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proceedings of the National Academy of Sciences. 2006; 103(29):10889-10894. doi: 10.1073/pnas.0604460103
39. Frascoli F, Hughes BD, Zaman MH, Landman KA. A computational model for collective cellular motion in three dimensions: general framework and case study for cell pair dynamics. PloS one. 2013; 8(3): e59249. doi: 10.1371/journal.pone.0059249 PMID: 23527148
40. Vargas DA, Zaman MH. Computational model for migration of a cell cluster in three-dimensional matrices. Annals of biomedical engineering. 2011; 39(7):2068-2079. doi: 10.1007/s10439-011-0290-9 PMID: 21424851
41. Prasad M, Jang AC, Starz-Gaiano M, Melani M, Montell DJ. A protocol for culturing Drosophila melanogaster stage 9 egg chambers for live imaging. Nature protocols. 2007; 2(10):2467-2473. doi: 10.1038/nprot.2007.363 PMID: 17947988
42. Ashburner M, et al. Drosophila. A laboratory handbook. Cold Spring Harbor Laboratory Press; 1989.
43. Van De Bor V, Zimniak G, Cérézo D, Schaub S, Noselli S. Asymmetric localisation of cy-tokine mRNA is essential for JAK/STAT activation during cell invasiveness. Development. 2011; 138(7):1383-1393. doi: 10.1242/dev.056184 PMID: 21350010
44. Groen CM, Spracklen AJ, Fagan TN, Tootle TL. Drosophila Fascin is a novel downstream target of prostaglandin signaling during actin remodeling. Molecular biology of the cell. 2012; 23(23):4567-4578. doi: 10.1091/mbc.E12-05-0417 PMID: 23051736
45. Du Roure O, Saez A, Buguin A, Austin RH, Chavrier P, Siberzan P, et al. Force mapping in epithelial cell migration. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(7):2390-2395. doi: 10.1073/pnas.0408482102 PMID: 15695588
46. Ladoux B, Anon E, Lambert M, Rabodzey A, Hersen P, Buguin A, et al. Strength dependence of cadherin-mediated adhesions. Biophysical journal. 2010; 98(4):534-542. doi: 10.1016/j.bpj.2009.10.044 PMID: 20159149
47. Kraning-Rush CM, Carey SP, Califano JP, Reinhart-King CA. Quantifying traction stresses in adherent cells. Methods Cell Biol. 2012; 110:139-178. doi: 10.1016/B978-0-12-388403-9.00006-0 PMID: 22482948
48. Stonko DP. Force-Based Biophysical Model of Border Cell Migration: Unraveling the mechanism of collective cell migration. Senior Thesis. 2013;.
49. Stonko D, Starz-Gaiano M, Peercy BE. Implementing a Numerical Package to Model Collective Cell Migration. Technical Report. 2014;(HPCF-2014-2).
50. Peifer M, Orsulic S, Sweeton D, Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development. 1993; 118(4):1191-1207. PMID: 8269848
51. Monahan AJ, Starz-Gaiano M. Socs36E attenuates STAT signaling to optimize motile cell specification in the Drosophila ovary. Developmental biology. 2013; 379(2):152-166. doi: 10.1016/j.ydbio.2013.03.022 PMID: 23583584