Genetic Basis for Developmental Homeostasis of Germline Stem Cell Niche Number: A Network of Tramtrack-Group Nuclear BTB Factors

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Bartoletti, Mathieu ^a,b   Rubin, Thomas ^b,d   Chalvet, Fabienne ^a,b,c   Netter, Sophie ^a,b   Dos Santos, Nicolas ^b   Poisot, Emilie ^b   Paces Fessy, Mélanie ^a,b   Cumenal, Delphine ^a   Peronnet, Frédérique ^a   Pret, Anne Marie ^a,b   Théodore, Laurent ^a,b,c  

^a CNRS   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BTB NUCLEAR FACTOR; NUCLEAR FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL STRUCTURES; ANIMAL TISSUE; ARTICLE; BATMAN GENE; BRIC A BRAC GENE; CELL SELECTION; CONTROLLED STUDY; DEVELOPMENT; DROSOPHILA MELANOGASTER; FEMALE; GENE; GENE CONTROL; GENE DOSAGE; GENE INTERACTION; GENE LOCUS; GENE REGULATORY NETWORK; GERM LINE; GERMLINE STEM CELL NICHE NUMBER; HOMEOSTASIS; IMAGO; NONHUMAN; OVARIOLE; OVARY DEVELOPMENT; PIPSQUEAK GENE; PUPA (LIFE CYCLE STAGE); STEM CELL NICHE; TERMINAL FILAMENT; TRITHORAX LIKE GENE;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; HOMEOSTASIS; MORPHOGENESIS; NUCLEAR PROTEINS; OVARY; STEM CELL NICHE; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER SUBGROUP;

EID: 84869832958     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049958     Document Type: Article

References (73)

1. King RC (1970) Ovarian development in Drosophila melanogaster: New York: Academic Press.
2. Hodin J, Riddiford LM, (2000) Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in drosophilids (Insecta: Diptera). Evolution 54: 1638-1653.
3. Green DA, 2nd, Sarikaya DP, Extavour CG (2011) Counting in oogenesis. Cell and tissue research 344: 207-212.
4. Williamson A, Lehmann R, (1996) Germ cell development in Drosophila. Annu Rev Cell Dev Biol 12: 365-391.
5. Camara N, Whitworth C, Van Doren M, (2008) The creation of sexual dimorphism in the Drosophila soma. Current topics in developmental biology 83: 65-107.
6. Sahut-Barnola I, Godt D, Laski FA, Couderc JL, (1995) Drosophila ovary morphogenesis: analysis of terminal filament formation and identification of a gene required for this process. Dev Biol 170: 127-135.
7. Godt D, Laski FA, (1995) Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric a brac. Development 121: 173-187.
8. Sahut-Barnola I, (1996) Terminal filament cell organization in the larval ovary of Drosophila melanogaster: ultrastructural observations and pattern of divisions. Roux's Arch Dev Biol 205: 356-363.
9. Chen J, Godt D, Gunsalus K, Kiss I, Goldberg M, et al. (2001) Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat Cell Biol 3: 204-209.
10. Zhu CH, Xie T, (2003) Clonal expansion of ovarian germline stem cells during niche formation in Drosophila. Development 130: 2579-2588.
11. Dansereau DA, Lasko P, (2008) The development of germline stem cells in Drosophila. Methods in molecular biology 450: 3-26.
12. Ward EJ, Shcherbata HR, Reynolds SH, Fischer KA, Hatfield SD, et al. (2006) Stem cells signal to the niche through the Notch pathway in the Drosophila ovary. Current biology 16: 2352-2358.
13. Song X, Call GB, Kirilly D, Xie T, (2007) Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development 134: 1071-1080.
14. Hsu HJ, Drummond-Barbosa D, (2011) Insulin signals control the competence of the Drosophila female germline stem cell niche to respond to Notch ligands. Developmental biology 350: 290-300.
15. Decotto E, Spradling AC, (2005) The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Developmental cell 9: 501-510.
16. Rojas-Rios P, Guerrero I, Gonzalez-Reyes A, (2012) Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila. PLoS biology 10: e1001298.
17. Kirilly D, Wang S, Xie T, (2011) Self-maintained escort cells form a germline stem cell differentiation niche. Development 138: 5087-5097.
18. Konig A, Yatsenko AS, Weiss M, Shcherbata HR, (2011) Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation. The EMBO journal 30: 1549-1562.
19. 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.
20. Xie T, Spradling AC, (1998) decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94: 251-260.
21. Xie T, Spradling AC, (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290: 328-330.
22. Song X, Wong MD, Kawase E, Xi R, Ding BC, et al. (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131: 1353-1364.
23. David JR, Bocquet C, (1975) Similarities and differences in latitudinal adaptation of two Drosophila sibling species. Nature 257: 588-590.
24. Louis J, David JR, (1986) Ecological specialization in the Drosophila melanogester species group: A case study of D. sechellia. Acta Oecol (OECOL GEN) 7 (3): 215-229.
25. Coyne JA, Rux J, David JR, (1991) Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet Res 57: 113-122.
26. Markow TA, O'Grady PM, (2007) Drosophila biology in the genomic age. Genetics 177: 1269-1276.
27. Delpuech J-M NB, Chiche J, Pla E, Vouidibio J, David JR, (1995) Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster: ovarian size and developmental temperature. Evolution 49 (4): 670-675.
28. Thomas-Orillard M, (1984) Modifications of Mean Ovariole Number, Fresh Weight of Adult Females and Developmental Time in DROSOPHILA MELANOGASTER Induced by Drosophila C Virus. Genetics 107: 635-644.
29. Gibert P, Capy P, Imasheva A, Moreteau B, Morin JP, et al. (2004) Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120: 165-179.
30. Bergland AO, Genissel A, Nuzhdin SV, Tatar M, (2008) Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180: 567-582.
31. Orgogozo V, Broman KW, Stern DL, (2006) High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 173: 197-205.
32. Wayne ML, McIntyre LM, (2002) Combining mapping and arraying: An approach to candidate gene identification. Proceedings of the National Academy of Sciences of the United States of America 99: 14903-14906.
33. Wayne ML, Hackett JB, Dilda CL, Nuzhdin SV, Pasyukova EG, et al. (2001) Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster. Genetical research 77: 107-116.
34. Sarikaya DP, Belay AA, Ahuja A, Dorta A, Green DA, et al. (2012) The roles of cell size and cell number in determining ovariole number in Drosophila. Developmental biology 363: 279-289.
35. Hodin J, Riddiford LM, (2000) Parallel alterations in the timing of ovarian ecdysone receptor and ultraspiracle expression characterize the independent evolution of larval reproduction in two species of gall midges (Diptera: Cecidomyiidae). Dev Genes Evol 210: 358-372.
36. Gancz D, Lengil T, Gilboa L, (2011) Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLoS Biol 9: e1001202.
37. Forbes AJ, Lin H, Ingham PW, Spradling AC, (1996) hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122: 1125-1135.
38. Bolivar J, Pearson J, Lopez-Onieva L, Gonzalez-Reyes A, (2006) Genetic dissection of a stem cell niche: the case of the Drosophila ovary. Dev Dyn 235: 2969-2979.
39. Couderc JL, Godt D, Zollman S, Chen J, Li M, et al. (2002) The bric a brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129: 2419-2433.
40. Zollman S, Godt D, Prive GG, Couderc JL, Laski FA, (1994) The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A 91: 10717-10721.
41. Bardwell VJ, Treisman R, (1994) The POZ domain: a conserved protein-protein interaction motif. Genes Dev 8: 1664-1677.
42. Albagli O, Dhordain P, Deweindt C, Lecocq G, Leprince D, (1995) The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ 6: 1193-1198.
43. Pointud JC, Larsson J, Dastugue B, Couderc JL, (2001) The BTB/POZ domain of the regulatory proteins Bric a brac 1 (BAB1) and Bric a brac 2 (BAB2) interacts with the novel Drosophila TAF(II) factor BIP2/dTAF(II)155. Dev Biol 237: 368-380.
44. Bonchuk A, Denisov S, Georgiev P, Maksimenko O, (2011) Drosophila BTB/POZ domains of "ttk group" can form multimers and selectively interact with each other. Journal of molecular biology 412: 423-436.
45. Horowitz H, Berg CA, (1996) The Drosophila pipsqueak gene encodes a nuclear BTB-domain-containing protein required early in oogenesis. Development 122: 1859-1871.
46. Farkas G, Gausz J, Galloni M, Reuter G, Gyurkovics H, et al. (1994) The Trithorax-like gene encodes the Drosophila GAGA factor. Nature 371: 806-808.
47. Faucheux M, Roignant JY, Netter S, Charollais J, Antoniewski C, et al. (2003) batman Interacts with polycomb and trithorax group genes and encodes a BTB/POZ protein that is included in a complex containing GAGA factor. Mol Cell Biol 23: 1181-1195.
48. Lehmann M, Siegmund T, Lintermann KG, Korge G, (1998) The pipsqueak protein of Drosophila melanogaster binds to GAGA sequences through a novel DNA-binding domain. J Biol Chem 273: 28504-28509.
49. Schwendemann A, Lehmann M, (2002) Pipsqueak and GAGA factor act in concert as partners at homeotic and many other loci. Proc Natl Acad Sci U S A 99: 12883-12888.
50. Mishra K, Chopra VS, Srinivasan A, Mishra RK, (2003) Trl-GAGA directly interacts with lola like and both are part of the repressive complex of Polycomb group of genes. Mech Dev 120: 681-689.
51. Huang DH, Chang YL, Yang CC, Pan IC, King B, (2002) pipsqueak encodes a factor essential for sequence-specific targeting of a polycomb group protein complex. Mol Cell Biol 22: 6261-6271.
52. Gibert JM, Peronnet F, Schlotterer C, (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet 3: e30.
53. Kumar S, (2011) Remote homologue identification of Drosophila GAGA factor in mouse. Bioinformation 7: 29-32.
54. Sing A, Pannell D, Karaiskakis A, Sturgeon K, Djabali M, et al. (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138: 885-897.
55. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE, (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140: 99-110.
56. Matharu NK, Hussain T, Sankaranarayanan R, Mishra RK, (2010) Vertebrate homologue of Drosophila GAGA factor. Journal of molecular biology 400: 434-447.
57. Dos-Santos N, Rubin T, Chalvet F, Gandille P, Cremazy F, et al. (2008) Drosophila retinal pigment cell death is regulated in a position-dependent manner by a cell memory gene. Int J Dev Biol 52: 21-31.
58. Horowitz H, Berg CA, (1995) Aberrant splicing and transcription termination caused by P element insertion into the intron of a Drosophila gene. Genetics 139: 327-335.
59. Ferres-Marco D, Gutierrez-Garcia I, Vallejo DM, Bolivar J, Gutierrez-Avino FJ, et al. (2006) Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature 439: 430-436.
60. Greenberg AJ, Schedl P, (2001) GAGA factor isoforms have distinct but overlapping functions in vivo. Mol Cell Biol 21: 8565-8574.
61. Chalvet F, Bartoletti M, Théodore L, (2011) Ovary phenotype and expression of bab1 and bab2 paralogs in the ovary of two mutants of the bab locus in Drosophila melanogaster. Drosophila info service 94: 158-162.
62. Song X, Zhu CH, Doan C, Xie T, (2002) Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296: 1855-1857.
63. Gibert JM, Peronnet F, Schlotterer C, (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS genetics 3: e30.
64. Faucheux M, Netter S, Bloyer S, Moussa M, Boissonneau E, et al. (2001) Advantages of a P-element construct containing MtnA sequences for the identification of patterning and cell determination genes in Drosophila melanogaster. Mol Genet Genomics 265: 14-22.
65. Siegmund T, Lehmann M, (2002) The Drosophila Pipsqueak protein defines a new family of helix-turn-helix DNA-binding proteins. Development genes and evolution 212: 152-157.
66. Lehmann M, (2004) Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure. Trends Genet 20: 15-22.
67. Bickel RD, Kopp A, Nuzhdin SV, (2011) Composite effects of polymorphisms near multiple regulatory elements create a major-effect QTL. PLoS Genet 7: e1001275.
68. Capella IC, Hartfelder K, (1998) Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. J Insect Physiol 44: 385-391.
69. Hodin J, Riddiford LM, (1998) The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev Genes Evol 208: 304-317.
70. Kopp A, Duncan I, Godt D, Carroll SB, (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408: 553-559.
71. Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, et al. (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134: 610-623.
72. Gibert JM, Karch F, Schlotterer C, (2011) Segregating variation in the polycomb group gene cramped alters the effect of temperature on multiple traits. PLoS Genet 7: e1001280.
73. Ma Y, Creanga A, Lum L, Beachy PA, (2006) Prevalence of off-target effects in Drosophila RNA interference screens. Nature 443: 359-363.