Towards long term cultivation of Drosophila wing imaginal discs in vitro

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Handke, Björn ^a   Szabad, János ^b   Lidsky, Peter V ^a,d   Hafen, Ernst ^c   Lehner, Christian F ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF SZEGED   (Hungary)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE INSULIN; CELL PROTEIN; DP PROTEIN; INSULIN LIKE PEPTIDE 2; MATRIGEL; PEPTIDE; RAS PROTEIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG; YORKIE PROTEIN; CULTURE MEDIUM; DROSOPHILA PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL COUNT; CELL CYCLE PROGRESSION; CELL POPULATION; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; DISSECTION; DROSOPHILA; EMBRYO; FAT BODY; FORELIMB; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION; HEMOLYMPH; IMAGINAL DISC; IN VITRO STUDY; ISOLATION PROCEDURE; MITOSIS; NONHUMAN; PROTEIN EXPRESSION; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; TISSUE CULTURE; UAS EGFP GENE; ANIMAL; CELL CYCLE; CULTURE MEDIUM; DEVELOPMENTAL BIOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MORPHOGENESIS; PROCEDURES;

ANIMALS; CELL CYCLE; COCULTURE TECHNIQUES; CULTURE MEDIA; DEVELOPMENTAL BIOLOGY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMOLYMPH; IMAGINAL DISCS; IN VITRO TECHNIQUES; LARVA; MORPHOGENESIS; WING;

EID: 84929940677     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107333     Document Type: Article

References (103)

1. Garcia-Bellido A, Merriam JR (1971) Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev Biol 24: 61-87.
2. Madhavan M, Schneiderman HA (1977) Histological analysis of the dynamics of growth imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Roux's Archives of Developmental Biology 183: 269-305.
3. Dahmann C, Oates AC, Brand M (2011) Boundary formation and maintenance in tissue development. Nat Rev Genet 12: 43-55.
4. Restrepo S, Zartman JJ, Basler K (2014) Coordination of Patterning and Growth by the Morphogen DPP. Curr Biol 24: R245-255.
5. Vincent JP, Fletcher AG, Baena-Lopez LA (2013) Mechanisms and mechanics of cell competition in epithelia. Nat Rev Mol Cell Biol 14: 581-591.
6. Worley MI, Setiawan L, Hariharan IK (2012) Regeneration and transdetermination in Drosophila imaginal discs. Annu Rev Genet 46: 289-310.
7. Bryant PJ, Levinson P (1985) Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev Biol 107: 355-363.
8. Fain MJ, Stevens B (1982) Alterations in the cell cycle of Drosophila imaginal disc cells precede metamorphosis. Dev Biol 92: 247-258.
9. McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132: 5033-5042.
10. Widmann TJ, Dahmann C (2009) Dpp signaling promotes the cuboidal-tocolumnar shape transition of Drosophila wing disc epithelia by regulating Rho1. J Cell Sci 122: 1362-1373.
11. Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature 255: 614-617.
12. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, et al. (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11: 213-221.
13. Johnston LA, Edgar BA (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394: 82-84.
14. Teleman AA (2010) Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem J 425: 13-26.
15. Fristrom DK, Fristrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez Arias A, editors. The Development of Drosophila melanogaster: Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 843-897.
16. Schubiger M, Palka J (1987) Changing spatial patterns of DNA replication in the developing wing of Drosophila. Developmental Biology 123: 145-153.
17. Ghannad-Rezaie M, Wang X, Mishra B, Collins C, Chronis N (2012) Microfluidic chips for in vivo imaging of cellular responses to neural injury in Drosophila larvae. PLoS ONE 7: E29869.
18. Heemskerk I, Lecuit T, LeGoff L (2014) Dynamic clonal analysis based on chronic in vivo imaging allows multiscale quantification of growth in the Drosophila wing disc. Development 141: 2339-2348.
19. Nienhaus U, Aegerter-Wilmsen T, Aegerter CM (2012) In-vivo imaging of the Drosophila wing imaginal disc over time: Novel insights on growth and boundary formation. PLoS ONE 7: E47594.
20. Aldaz S, Escudero LM, Freeman M (2010) Live imaging of Drosophila imaginal disc development. Proc Natl Acad Sci U S A 107: 14217-14222.
21. Aldaz S, Escudero LM, Freeman M (2013) Dual role of myosin II during Drosophila imaginal disc metamorphosis. Nat Commun 4: 1761.
22. Gibson MC, Patel AB, Nagpal R, Perrimon N (2006) The emergence of geometric order in proliferating metazoan epithelia. Nature 442: 1038-1041.
23. Kicheva A, Pantazis P, Bollenbach T, Kalaidzidis Y, Bittig T, et al. (2007) Kinetics of morphogen gradient formation. Science 315: 521-525.
24. Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ, et al. (2009) Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr Biol 19: 1950-1955.
25. Legoff L, Rouault H, Lecuit T (2013) A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc. Development 140: 4051-4059.
26. Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, et al. (2011) Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes Dev 25: 131-136.
27. Mao Y, Tournier AL, Hoppe A, Kester L, Thompson BJ, et al. (2013) Differential proliferation rates generate patterns of mechanical tension that orient tissue growth. EMBO J 32: 2790-2803.
28. Nakajima Y, Meyer EJ, Kroesen A, McKinney SA, Gibson MC (2013) Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 500: 359-362.
29. Ohsawa S, Sugimura K, Takino K, Igaki T (2012) Imaging cell competition in Drosophila imaginal discs. Methods Enzymol 506: 407-413.
30. Zartman J, Restrepo S, Basler K (2013) A high-throughput template for optimizing Drosophila organ culture with response-surface methods. Development 140: 667-674.
31. Hadorn E (1963) Differenzierungsleistungen Wiederholt Fragmentierter Teilstucke Mannlicher Genitalscheiben Von Drosophila Melanogaster Nach Kultur in Vivo. Developmental Biology 7: 617.
32. Davis KT, Shearn A (1977) In vitro growth of imaginal disks from Drosophila melanogaster. Science 196: 438-440.
33. Robb JA (1969) Maintenance of imaginal discs of Drosophila melanogaster in chemically defined media. J Cell Biol 41: 876-885.
34. Currie DA, Milner MJ, Evans CW (1988) The Growth and Differentiation Invitro of Leg and Wing Imaginal Disk Cells from Drosophila-Melanogaster. Development 102: 805-814.
35. Ui K, Togashi S, Ueda R, Miyake T (1987) Establishment and Characterization of Cell-Lines from Drosophila Imaginal Discs-Iii. Japanese Journal of Genetics 62: 563-563.
36. Ui K, Ueda R, Miyake T (1987) Cell-Lines from Imaginal Disks of Drosophila-Melanogaster. In Vitro Cellular & Developmental Biology 23: 707-711.
37. Nijhout HF, Grunert LW (2002) Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc Natl Acad Sci U S A 99: 15446-15450.
38. Nijhout HF, Smith WA, Schachar I, Subramanian S, Tobler A, et al. (2007) The control of growth and differentiation of the wing imaginal disks of Manduca sexta. Dev Biol 302: 569-576.
39. Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A 98: 15050-15055.
40. Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA (1998) Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183-1193.
41. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, et al. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12: 557-570.
42. Halfar K, Rommel C, Stocker H, Hafen E (2001) Ras controls growth, survival and differentiation in the Drosophila eye by different thresholds of MAP kinase activity. Development 128: 1687-1696.
43. Oh H, Irvine KD (2009) In vivo analysis of Yorkie phosphorylation sites. Oncogene 28: 1916-1927.
44. Caussinus E, Colombelli J, Affolter M (2008) Tip-Cell Migration Controls Stalk-Cell Intercalation during Drosophila Tracheal Tube Elongation. Current Biology 18: 1727-1734.
45. Yoffe KB, Manoukian AS, Wilder EL, Brand AH, Perrimon N (1995) Evidence for Engrailed-Independent Wingless Autoregulation in Drosophila. Developmental Biology 170: 636-650.
46. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
47. Ng M, Diaz-Benjumea FJ, Cohen SM (1995) Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development 121: 589-599.
48. Calleja M, Moreno E, Pelaz S, Morata G (1996) Visualization of gene expression in living adult Drosophila. Science 274: 252-255.
49. Wieschaus E, Marsh JL, Gehring W (1978) Fs(1)K10, a Germline-Dependent Female Sterile Mutation Causing Abnormal Chorion Morphology in Drosophila-Melanogaster. Wilhelm Rouxs Archives of Developmental Biology 184: 75-82.
50. Rizki TM, Rizki RM, Grell EH (1980) A Mutant Affecting the Crystal Cells in Drosophila-Melanogaster. Wilhelm Rouxs Archives of Developmental Biology 188: 91-99.
51. Woodruff RC, Ashburner M (1979) Genetics of a Small Autosomal Region of Drosophila-Melanogaster Containing the Structural Gene for Alcohol-Dehydrogenase .1. Characterization of Deficiencies and Mapping of Adh and Visible Mutations. Genetics 92: 117-132.
52. Handke B, Poernbacher I, Goetze S, Ahrens CH, Omasits U, et al. (2013) The hemolymph proteome of fed and starved Drosophila larvae. PLoS One 8: E67208.
53. Echalier G, Ohanessian A (1969) [Isolation, in tissue culture, of Drosophila melangaster cell lines]. C R Acad Sci Hebd Seances Acad Sci D 268: 1771-1773.
54. Yanagawa S, Lee JS, Ishimoto A (1998) Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to wingless signaling. J Biol Chem 273: 32353-32359.
55. Martin PF (1982) Direct Determination of the Growth-Rate of Drosophila Imaginal Disks. Journal of Experimental Zoology 222: 97-102.
56. Llimargas M, Strigini M, Katidou M, Karagogeos D, Casanova J (2004) Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 131: 181-190.
57. Graves BJ, Schubiger G (1982) Cell cycle changes during growth and differentiation of imaginal discs in Drosophila melanogaster. Developmental Biology 93: 104-117.
58. James AA, Bryant PJ (1981) Mutations causing pattern deficiencies and duplications in the imaginal wing disk of Drosophila melanogaster. Dev Biol 85: 39-54.
59. Salic A, Mitchison TJ (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A 105: 2415-2420.
60. Adler PN, MacQueen M (1981) Partial coupling of the cell cycles of neighboring imaginal disc cells. Exp Cell Res 133: 452-456.
61. Gonzalez M, Martin-Ruiz I, Jimenez S, Pirone L, Barrio R, et al. (2011) Generation of stable Drosophila cell lines using multicistronic vectors. Scientific Reports 1.
62. Havens CG, Walter JC (2011) Mechanism of CRL4(Cdt2), a PCNA-dependent E3 ubiquitin ligase. Genes Dev 25: 1568-1582.
63. Primorac I, Musacchio A (2013) Panta rhei: The APC/C at steady state. J Cell Biol 201: 177-189.
64. Sigrist S, Jacobs H, Stratmann R, Lehner CF (1995) Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J 14: 4827-4838.
65. Leonhardt H, Rahn HP, Weinzierl P, Sporbert A, Cremer T, et al. (2000) Dynamics of DNA replication factories in living cells. J Cell Biol 149: 271-280.
66. Dimova DK, Stevaux O, Frolov MV, Dyson NJ (2003) Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 17: 2308-2320.
67. Duronio RJ, O'Farrell PH (1995) Developmental control of the G1 to S transition in Drosophila -cyclin E is a limiting downstream target of E2F. Genes Dev 9: 1456-1468.
68. Galko MJ, Krasnow MA (2004) Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol 2: E239.
69. Martin P, Parkhurst SM (2004) Parallels between tissue repair and embryo morphogenesis. Development 131: 3021-3034.
70. Stronach B (2005) Dissecting JNK signaling, one KKKinase at a time. Dev Dyn 232: 575-584.
71. Bosch M, Serras F, Martin-Blanco E, Baguna J (2005) JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev Biol 280: 73-86.
72. Igaki T (2009) Correcting developmental errors by apoptosis: Lessons from Drosophila JNK signaling. Apoptosis 14: 1021-1028.
73. Forristal CE, Wright KL, Hanley NA, Oreffo RO, Houghton FD (2010) Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139: 85-97.
74. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, et al. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91.
75. Ozturk SS, Palsson BO (1990) Effects of dissolved oxygen on hybridoma cell growth, metabolism, and antibody production kinetics in continuous culture. Biotechnol Prog 6: 437-446.
76. Guha A, Lin L, Kornberg TB (2009) Regulation of Drosophila matrix metalloprotease Mmp2 is essential for wing imaginal disc: Trachea association and air sac tubulogenesis. Dev Biol 335: 317-326.
77. Karim FD, Chang HC, Therrien M, Wassarman DA, Laverty T, et al. (1996) A screen for genes that function downstream of ras1 during Drosophila eye development. Genetics 143: 315-329.
78. Karim FD, Rubin GM (1998) Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 125: 1-9.
79. Prober DA, Edgar BA (2000) Ras1 promotes cellular growth in the Drosophila wing. Cell 100: 435-446.
80. Brumby AM, Richardson HE (2003) scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J 22: 5769-5779.
81. Pagliarini RA, Xu T (2003) A genetic screen in Drosophila for metastatic behavior. Science 302: 1227-1231.
82. Willecke M, Toggweiler J, Basler K (2011) Loss of PI3K blocks cell-cycle progression in a Drosophila tumor model. Oncogene 30: 4067-4074.
83. Wu M, Pastor-Pareja JC, Xu T (2010) Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 463: 545-548.
84. Simcox A, Mitra S, Truesdell S, Paul L, Chen T, et al. (2008) Efficient genetic method for establishing Drosophila cell lines unlocks the potential to create lines of specific genotypes. PLoS Genet 4: E1000142.
85. Yu FX, Guan KL (2013) The Hippo pathway: Regulators and regulations. Genes Dev 27: 355-371.
86. Dushay MS (2009) Insect hemolymph clotting. Cell Mol Life Sci 66: 2643-2650.
87. Karlsson C, Korayem AM, Scherfer C, Loseva O, Dushay MS, et al. (2004) Proteomic analysis of the Drosophila larval hemolymph clot. J Biol Chem 279: 52033-52041.
88. Rizki TM, Rizki RM, Bellotti RA (1985) Genetics of a Drosophila Phenoloxidase. Molecular & General Genetics 201: 7-13.
89. Kim SH, Turnbull J, Guimond S (2011) Extracellular matrix and cell signalling: The dynamic cooperation of integrin, proteoglycan and growth factor receptor. Journal of Endocrinology 209: 139-151.
90. Taipale J, KeskiOja J (1997) Growth factors in the extracellular matrix. FASEB Journal 11: 51-59.
91. Yan D, Lin X (2009) Shaping morphogen gradients by proteoglycans. Cold Spring Harb Perspect Biol 1: A002493.
92. Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, et al. (2011) Selforganizing optic-cup morphogenesis in three-dimensional culture. Nature 472: 51-U73.
93. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, et al. (2013) Cerebral organoids model human brain development and microcephaly. Nature 501: 373-+.
94. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-U147.
95. Pastor-Pareja JC, Xu T (2011) Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev Cell 21: 245-256.
96. Barnes D, Sato G (1980) Serum-Free Cell-Culture -A Unifying Approach. Cell 22: 649-655.
97. Morris LX, Spradling AC (2011) Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138: 2207-2215.
98. Prasad M, Jang ACC, Starz-Gaiano M, Melani M, Montell DJ (2007) A protocol for culturing Drosophila melanogaster stage 9 egg chambers for live imaging. Nat Protoc 2: 2467-2473.
99. Sheng XR, Matunis E (2011) Live imaging of the Drosophila spermatogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development 138: 3367-3376.
100. Glatter T, Schittenhelm RB, Rinner O, Roguska K, Wepf A, et al. (2011) Modularity and hormone sensitivity of the Drosophila melanogaster insulin receptor/target of rapamycin interaction proteome. Mol Syst Biol 7.
101. Beadle GW, Ephrussi B (1936) The Differentiation of Eye Pigments in Drosophila as Studied by Transplantation. Genetics 21: 225-247.
102. Ursprung H (1962) The effect of heat age on the developmental capacity of the sagittal halves of male genital disks in Drosophila melanogaster. Developmental Biol 22-39.
103. Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ (1995) The Drosophila tumor-suppressor gene warts encodes a homolog of human myotonic-dystrophy kinase and is required for the control of cell-shape and proliferation. Genes Dev 9: 534-546.