Mechanisms of regulating cell topology in proliferating epithelia: Impact of division plane, mechanical forces, and cell memory

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Li, Yingzi ^a,b   Naveed, Hammad ^b   Kachalo, Sema ^b   Xu, Lisa X ^a,c   Liang, Jie ^b,c  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b University of Illinois at Chicago   (United States)

^c Chinese National Human Genome Center at Shanghai   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL DIVISION; CELL DIVISION PLANE; CELL MEMORY; CELL MOTION; CELL PROLIFERATION; CELL SHAPE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; EPITHELIUM CELL; EPITHELIZATION; FORCE; MECHANICAL FORCE; MECHANICAL MODEL; NONBIOLOGICAL MODEL; REGULATORY MECHANISM; SIMULATION;

ANIMALS; BIOMECHANICS; CELL DIVISION; CELL PROLIFERATION; CELL SHAPE; COMPUTER SIMULATION; EPITHELIAL CELLS; EPITHELIUM; MODELS, BIOLOGICAL;

EID: 84865083903     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043108     Document Type: Article

References (58)

1. Shraiman B, (2005) Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci U S A 102: 3318-3323.
2. Gong Y, Mo C, Fraser S, (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430: 689-693.
3. Baena-Lopez L, Baonza A, Garcia-Bellido A, (2005) The orientation of cell divisions determines the shape of drosophila organs. Curr Biol 15: 1640-1644.
4. Hanahan D, Weinberg R, (2000) The hallmarks of cancer. Cell 100: 57-70.
5. Bhowmick N, Neilson E, Moses H, (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337.
6. Hanahan D, Weinberg R, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
7. Gibson W, Gibson M, (2009) Cell topology, geometry, and morphogenesis in proliferating epithelia. Curr Top Dev Biol 89: 87-114.
8. Farhadifar R, Roper J, Aigouy B, Eaton S, Julicher F, (2007) The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17: 2095-2104.
9. Ingber D, (2002) Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation. Differentiation 70: 547-560.
10. Nagpal R, Patel A, Gibson M, (2008) Epithelial topology. Bioessays 30: 260-266.
11. Sahlin P, Jonsson H, (2010) A modeling study on how cell division affects properties of epithelial tissues under isotropic growth. PLoS One 5: e11750.
12. Honda H, (1978) Description of cellular patterns by dirichlet domains: the two-dimensional case. J Theor Biol 72: 523-543.
13. Weliky M, Oster G, (1990) The mechanical basis of cell rearrangement. i. epithelial morphogenesis during fundulus epiboly. Development 109: 373-386.
14. Lewis F, (1928) The correlation between cell division and the shapes and sizes of prismatic cells in the epidermis of cucumis. Anat Rec 38: 341-376.
15. Aegerter-Wilmsen T, Smith A, Christen A, Aegerter C, Hafen E, et al. (2010) Exploring the effects of mechanical feedback on epithelial topology. Development 137: 499-506.
16. Gibson M, Patel A, Nagpal R, Perrimon N, (2006) The emergence of geometric order in proliferating metazoan epithelia. Nature 442: 1038-1041.
17. Dubertret B, Rivier N, (1997) The renewal of the epidermis: a topological mechanism. Biophys J 73: 38-44.
18. Zallen J, Zallen R, (2004) Cell-pattern disordering during convergent extension in drosophila. J Phys: Condensed Matter 16: S5073-S5080.
19. Martinand-Mari C, Maury B, Rousset F, Sahuquet A, Mennessier G, et al. (2009) Topological control of life and death in non-proliferative epithelia. PLoS One 4: e4202.
20. Axelrod J, (2006) Cell shape in proliferating epithelia: a multifaceted problem. Cell 126: 643-645.
21. Lewis F, (1926) The effect of cell division on the shape and size of hexagonal cells. Anat Rec 33: 331-355.
22. Dubertret B, Aste T, Ohlenbusch HM, Rivier N, (1998) Two-dimensional froths and the dynamics of biological tissues. Phys Rev E 58: 6368-6378.
23. Classen A, Anderson K, Marois E, Eaton S, (2005) Hexagonal packing of drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9: 805-817.
24. Korn R, Spalding R, (1973) The geometry of plant epidermal cells. New Phytologist 72: 1357-1365.
25. Patel A, Gibson W, Gibson M, Nagpal R, (2009) Modeling and inferring cleavage patterns in proliferating epithelia. PLoS Comput Biol 5: e1000412.
26. Gibson W, Veldhuis J, Rubinstein B, Cartwright H, Perrimon N, et al. (2011) Control of the mitotic cleavage plane by local epithelial topology. Cell 144: 427-438.
27. Staple D, Farhadifar R, Roper J, Aigouy B, Eaton S, et al. (2010) Mechanics and remodelling of cell packings in epithelia. Eur Phys J E Soft Matter 33: 117-127.
28. Aegerter-Wilmsen T, Aegerter C, Hafen E, Basler K, (2007) Model for the regulation of size in the wing imaginal disc of drosophila. Mech Dev 124: 318-326.
29. Hufnagel L, Teleman A, Rouault H, Cohen S, Shraiman B, (2007) On the mechanism of wing size determination in fly development. Proc Natl Acad Sci U S A 104: 3835-3840.
30. Nienhaus U, Aegerter-Wilmsen T, Aegerter C, (2009) Determination of mechanical stress distribution in drosophila wing discs using photoelasticity. Mech Dev 126: 942-949.
31. Dumais J, (2007) Can mechanics control pattern formation in plants? Curr Opin Plant Biol 10: 58-62.
32. Thery M, Jimenez-Dalmaroni A, Racine V, Bornens M, Julicher F, (2007) Experimental and theoretical study of mitotic spindle orientation. Nature 447: 493-496.
33. Ingber D, (2003) Tensegrity i. cell structure and hierarchical systems biology. J Cell Sci 116: 1157-1173.
34. Burrill D, Silver P, (2010) Making cellular memories. Cell 140: 13-18.
35. Cao Y, Lu H, Liang J, (2010) Probability landscape of heritable and robust epigenetic state of lysogeny in phage lambda. Proc Natl Acad Sci U S A 107: 18445-18450.
36. Westermann S, Weber K, (2003) Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4: 938-947.
37. Strauss B, Adams R, Papalopulu N, (2006) A default mechanism of spindle orientation based on cell shape is sufficient to generate cell fate diversity in polarised xenopus blastomeres. Development 133: 3883-3893.
38. Shimizu H, Bode P, Bode H, (1995) Patterns of oriented cell division during the steady-state morphogenesis of the body column in hydra. Dev Dyn 204: 349-357.
39. Segalen M, Bellaiche Y, (2009) Cell division orientation and planar cell polarity pathways. Semin Cell Dev Biol 20: 972-977.
40. Aigouy B, Farhadifar R, Staple D, Sagner A, Roper J, et al. (2010) Cell flow reorients the axis of planar polarity in the wing epithelium of drosophila. Cell 142: 773-786.
41. Yarden Y, (2001) The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur J Cancer 37 Suppl 4: S3-8.
42. Jiao Y, Torquato S, (2011) Emergent behaviors from a cellular automaton model for invasive tumor growth in heterogeneous microenvironments. PLoS Comput Biol 7: e1002314.
43. Affolter M, Basler K, (2007) The decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 8: 663-674.
44. Schwank G, Basler K, (2010) Regulation of organ growth by morphogen gradients. Cold Spring Harb Perspect Biol 2: a001669.
45. Turner S, Sherratt J, (2002) Intercellular adhesion and cancer invasion: a discrete simulation using the extended potts model. J Theor Biol 216: 85-100.
46. Anderson A, (2005) A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion. Math Med Biol 22: 163-186.
47. Takeichi M, (1993) Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 5: 806-811.
48. Kumar S, Weaver V, (2009) Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 28: 113-127.
49. Naveed H, Li Y, Kachalo S, Liang J, (2010) Geometric order in proliferating epithelia: impact of rearrangements and cleavage plane orientation. Conf Proc IEEE Eng Med Biol Soc 2010: 3808-3811.
50. Li Y, Naveed H, Kachalo S, Xu L, Liang J, (2011) Mechanical forces mediate localized topological change in epithelia. Conf Proc IEEE Eng Med Biol Soc 2011: 178-181.
51. Oster G, Perelson A, (1987) The physics of cell motility. J Cell Sci Suppl 8: 35-54.
52. Ingber D, (2005) Mechanical control of tissue growth: function follows form. Proc Natl Acad Sci U S A 102: 11571-11572.
53. Wakatsuki T, Kolodney M, Zahalak G, Elson E, (2000) Cell mechanics studied by a reconstituted model tissue. Biophys J 79: 2353-2368.
54. Fleming E, Zajac M, Moschenross D, Montrose D, Rosenberg D, et al. (2007) Planar spindle orientation and asymmetric cytokinesis in the mouse small intestine. J Histochem Cytochem 55: 1173-1180.
55. den Elzen N, Buttery C, Maddugoda M, Ren G, Yap A, (2009) Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol Biol Cell 20: 3740-3750.
56. Besson S, Dumais J, (2011) Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci U S A 108: 6294-6299.
57. Brodland G, Veldhuis J, (2002) Computer simulations of mitosis and interdependencies between mitosis orientation, cell shape and epithelia reshaping. J Biomech 35: 673-681.
58. Feldman J, Geimer S, Marshall W, (2007) The mother centriole plays an instructive role in defining cell geometry. PLoS Biol 5: e149.