Mechanisms of regulating tissue elongation in Drosophila wing: Impact of oriented cell divisions, oriented mechanical forces, and reduced cell size

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Li, Yingzi ^a,b   Naveed, Hammad ^b,d   Kachalo, Sema ^b   Xu, Lisa X ^a,c,e   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)

^d Chinese Academy of Sciences   (China)

^e Science and Technology Commission of Shanghai Municipality   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL STRUCTURES; ARTICLE; CELL DIVISION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DROSOPHILA; INSECT CELL; MATHEMATICAL MODEL; MECHANICAL STRESS; MORPHOGENESIS; REGULATORY MECHANISM; TISSUE ELONGATION; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; COMPUTER SIMULATION; CYTOLOGY; DROSOPHILA MELANOGASTER; FORELIMB; GROWTH, DEVELOPMENT AND AGING;

ANIMALS; BIOMECHANICAL PHENOMENA; CELL DIVISION; CELL SIZE; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; MODELS, BIOLOGICAL; WING;

EID: 84896878227     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086725     Document Type: Article

References (81)

1. O'Brochta D, Bryant P (1985) A zone of non-proliferating cells at a lineage restriction boundary in drosophila. Nature 313: 138-141. (Pubitemid 15192338)
2. Gong Y, Mo C, Fraser S (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430: 689-693. (Pubitemid 39061686)
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. (Pubitemid 41323741)
4. Lecuit T, Lenne P (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8: 633-644. (Pubitemid 47108184)
5. Shraiman B (2005) Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci U S A 102: 3318-3323.
6. Hanahan D, Weinberg R (2000) The hallmarks of cancer. Cell 100: 57-70. (Pubitemid 30046295)
7. Bhowmick N, Neilson E, Moses H (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337. (Pubitemid 39551661)
8. Hanahan D, Weinberg R (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
9. Gibson M, Patel A, Nagpal R, Perrimon N (2006) The emergence of geometric order in proliferating metazoan epithelia. Nature 442: 1038-1041. (Pubitemid 44330260)
10. Milan M, Campuzano S, Garcia-Bellido A (1996) Cell cycling and patterned cell proliferation in the wing primordium of drosophila. Proc Natl Acad Sci U S A 93: 640-645. (Pubitemid 26041141)
11. Garcia-Bellido A, de Celis J (1992) Developmental genetics of the venation pattern of drosophila. Annu Rev Genet 26: 277-304. (Pubitemid 23022611)
12. Tree D, Ma D, Axelrod J (2002) A three-tiered mechanism for regulation of planar cell polarity. Semin Cell Dev Biol 13: 217-224. (Pubitemid 35304526)
13. Sagner A, Merkel M, Aigouy B, Gaebel J, Brankatschk M, et al. (2012) Establishment of global patterns of planar polarity during growth of the drosophila wing epithelium. Curr Biol 22: 1296-1301.
14. Canela-Xandri O, Sagues F, Casademunt J, Buceta J (2011) Dynamics and mechanical stability of the developing dorsoventral organizer of the wing imaginal disc. PLoS Comput Biol 7: e1002153.
15. Rauzi M, Lenne P (2011) Cortical forces in cell shape changes and tissue morphogenesis. Curr Top Dev Biol 95: 93-144.
16. Aegerter-Wilmsen T, Heimlicher M, Smith A, de Reuille P, Smith R, et al. (2012) Integrating force-sensing and signaling pathways in a model for the regulation of wing imaginal disc size. Development 139: 3221-3231.
17. 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.
18. Mao Y, Tournier A, Bates P, Gale J, Tapon N, et al. (2011) Planar polarization of the atypical myosin dachs orients cell divisions in drosophila. Genes Dev 25: 131-136.
19. Matakatsu H, Blair S (2004) Interactions between fat and dachsous and the regulation of planar cell polarity in the drosophila wing. Development 131: 3785-3794. (Pubitemid 39199385)
20. Simon M (2004) Planar cell polarity in the drosophila eye is directed by graded four-jointed and dachsous expression. Development 131: 6175-6184.
21. Cho E, Irvine K (2004) Action of fat, four-jointed, dachsous and dachs in distal-to-proximal wing signaling. Development 131: 4489-4500. (Pubitemid 39409690)
22. Lawrence P, Casal J, Struhl G (2004) Cell interactions and planar polarity in the abdominal epidermis of drosophila. Development 131: 4651-4664. (Pubitemid 39433453)
23. Matakatsu H, Blair S (2006) Separating the adhesive and signaling functions of the fat and dachsous protocadherins. Development 133: 2315-2324. (Pubitemid 44044553)
24. Wittmann T, Hyman A, Desai A (2001) The spindle: a dynamic assembly of microtubules and motors. Nat Cell Biol 3: E28-34. (Pubitemid 32114823)
25. Walczak C, Heald R (2008) Mechanisms of mitotic spindle assembly and function. Int Rev Cytol 265: 111-158. (Pubitemid 351215987)
26. Gatlin J, Bloom K (2010) Microtubule motors in eukaryotic spindle assembly and maintenance. Semin Cell Dev Biol 21: 248-254.
27. Stevermann L, Liakopoulos D (2012) Molecular mechanisms in spindle positioning: structures and new concepts. Curr Opin Cell Biol.
28. Eaton S, Wepf R, Simons K (1996) Roles for rac1 and cdc42 in planar polarization and hair outgrowth in the wing of drosophila. J Cell Biol 135: 1277-1289. (Pubitemid 27014599)
29. Turner C, Adler P (1998) Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in drosophila. Mech Dev 70: 181-192. (Pubitemid 28116492)
30. Shimada Y, Yonemura S, Ohkura H, Strutt D, Uemura T (2006) Polarized transport of frizzled along the planar microtubule arrays in drosophila wing epithelium. Dev Cell 10: 209-222. (Pubitemid 43174954)
31. Harumoto T, Ito M, Shimada Y, Kobayashi T, Ueda H, et al. (2010) Atypical cadherins dachsous and fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev Cell 19: 389-401.
32. Baskin T (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21: 203-222.
33. Dumais J (2007) Can mechanics control pattern formation in plants? Curr Opin Plant Biol 10: 58-62.
34. Neufeld T, de la Cruz A, Johnston L, Edgar B (1998) Coordination of growth and cell division in the drosophila wing. Cell 93: 1183-1193. (Pubitemid 28307423)
35. Su T, O'Farrell P (1998) Size control: cell proliferation does not equal growth. Curr Biol 8: R687-9. (Pubitemid 28451024)
36. 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.
37. 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.
38. Li Y, Naveed H, Kachalo S, Xu L, Liang J (2012) Mechanisms of regulating cell topology in proliferating epithelia: impact of division plane, mechanical forces, and cell memory. PLoS One 7: e43108.
39. Mizushima-Sugano J, Maeda T, Miki-Noumura T (1983) Flexural rigidity of singlet microtubules estimated from statistical analysis of their contour lengths and end-to-end distances. Biochim Biophys Acta 755: 257-262.
40. Burnside B (1971) Microtubules and microfilaments in newt neuralation. Dev Biol 26: 416-441.
41. Madreperla S, Adler R (1989) Opposing microtubule- and actin-dependent forces in the development and maintenance of structural polarity in retinal photoreceptors. Dev Biol 131: 149-160. (Pubitemid 19032133)
42. Brown M, Hallam J, Colucci-Guyon E, Shaw S (2001) Rigidity of circulating lymphocytes is primarily conferred by vimentin intermediate filaments. J Immunol 166: 6640-6646. (Pubitemid 32467205)
43. Ingber D (2003) Tensegrity i. cell structure and hierarchical systems biology. J Cell Sci 116: 1157-1173.
44. Chen C, Posy S, Ben-Shaul A, Shapiro L, Honig B (2005) Specificity of cell-cell adhesion by classical cadherins: Critical role for low-affinity dimerization through beta-strand swapping. Proc Natl Acad Sci U S A 102: 8531-8536. (Pubitemid 40862770)
45. Patel S, Ciatto C, Chen C, Bahna F, Rajebhosale M, et al. (2006) Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124: 1255-1268.
46. Shimoyama Y, Tsujimoto G, Kitajima M, Natori M (2000) Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem J 349: 159-167. (Pubitemid 30440178)
47. Evans A, Turner M, Sens P (2003) Interactions between proteins bound to biomembranes. Phys Rev E Stat Nonlin Soft Matter Phys 67: 041907.
48. Hotani H, Miyamoto H (1990) Dynamic features of microtubules as visualized by dark-field microscopy. Adv Biophys 26: 135-156.
49. Domnina L, Rovensky J, Vasiliev J, Gelfand I (1985) Effect of microtubule-destroying drugs on the spreading and shape of cultured epithelial cells. J Cell Sci 74: 267-282.
50. Harris A, Wild P, Stopak D (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208: 177-179. (Pubitemid 10072133)
51. 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. (Pubitemid 47181540)
52. 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. (Pubitemid 50014864)
53. 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. (Pubitemid 46400393)
54. 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.
55. Morin X, Bellaiche Y (2011) Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev Cell 21: 102-119.
56. Minc N, Burgess D, Chang F (2011) Influence of cell geometry on division-plane positioning. Cell 144: 414-426.
57. Halbleib J, Nelson W (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214. (Pubitemid 44904842)
58. Cerruti B, Puliafito A, Shewan A, Yu W, Combes A, et al. (2013) Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures. J Cell Biol 203: 359-372.
59. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, et al. (2000) Pharmacological properties of y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 57: 976-983. (Pubitemid 30253382)
60. Fankhauser G (1945) Maintenance of normal structure in heteroploid salamander larvae, through compensation of changes in cell size by adjustment of cell number and cell shape. J Exp Zool 100: 445-455.
61. Delgado-Benarroch L, Causier B,Weiss J, Egea-Cortines M (2009) FORMOSA controls cell division and expansion during floral development in antirrhinum majus. Planta 229: 1219-1229.
62. Bittig T, Wartlick O, Gonzalez-Gaitan M, Julicher F (2009) Quantification of growth asymmetries in developing epithelia. Eur Phys J E Soft Matter 30: 93-99.
63. Segalen M, Bellaiche Y (2009) Cell division orientation and planar cell polarity pathways. Semin Cell Dev Biol 20: 972-977.
64. Vladar E, Antic D, Axelrod J (2009) Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb Perspect Biol 1: a002964.
65. Fischer E, Legue E, Doyen A, Nato F, Nicolas J, et al. (2006) Defective planar cell polarity in polycystic kidney disease. Nat Genet 38: 21-23. (Pubitemid 43011877)
66. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, et al. (2008) Loss of fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 40: 1010-1015.
67. Wang Y (2009) Wnt/planar cell polarity signaling: a new paradigm for cancer therapy. Mol Cancer Ther 8: 2103-2109.
68. Jessen J (2009) Noncanonical wnt signaling in tumor progression and metastasis. Zebrafish 6: 21-28.
69. Cavallaro U, Schaffhauser B, Christofori G (2002) Cadherins and the tumour progression: is it all in a switch? Cancer Lett 176: 123-128. (Pubitemid 34136010)
70. Cavallaro U, Christofori G (2004) Cell adhesion and signalling by cadherins and ig-CAMs in cancer. Nat Rev Cancer 4: 118-132. (Pubitemid 38198740)
71. Kumar S, Weaver V (2009) Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 28: 113-127.
72. Turner S, Sherratt J (2002) Intercellular adhesion and cancer invasion: a discrete simulation using the extended potts model. J Theor Biol 216: 85-100. (Pubitemid 34748059)
73. Anderson A (2005) A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion. Math Med Biol 22: 163-186.
74. Takeichi M (1993) Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 5: 806-811.
75. Yamashita Y, Fuller M (2008) Asymmetric centrosome behavior and the mechanisms of stem cell division. J Cell Biol 180: 261-266. (Pubitemid 351185912)
76. Neumuller R, Knoblich J (2009) Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23: 2675-2699.
77. Lechler T, Fuchs E (2005) Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437: 275-280. (Pubitemid 41294492)
78. Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8: 677-687.
79. Cicalese A, Bonizzi G, Pasi C, Faretta M, Ronzoni S, et al. (2009) The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138: 1083-1095.
80. Knoblich J (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11: 849-860.
81. Cao Y, Liang C, Naveed H, Li Y, Chen M, et al. (2012) Modeling spatial population dynamics of stem cell lineage in tissue growth. Conf Proc IEEE Eng Med Biol Soc 2012: 5502-5505.