Drosophila eggshell production: Identification of new genes and coordination by Pxt

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Tootle, Tina L ^a   Williams, Dianne ^b   Hubb, Alexander ^a   Frederick, Rebecca ^b   Spradling, Allan ^b  

^a UNIVERSITY OF IOWA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; ECDYSONE; LIPID; PROSTAGLANDIN SYNTHASE; DROSOPHILA PROTEIN; ECDYSTEROID 26 HYDROXYLASE, DROSOPHILA; ECDYSTEROID 26-HYDROXYLASE, DROSOPHILA; MESSENGER RNA; PEROXIDASE; PXT PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL MATURATION; CONTROLLED STUDY; CYP18A1 GENE; DOWN REGULATION; DROSOPHILA; EGG SHELL; FEMALE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; GENETIC IDENTIFICATION; GENETIC TRANSCRIPTION; HORMONE METABOLISM; NONHUMAN; OVARY FOLLICLE; PXT GENE; SIGNAL TRANSDUCTION; SOMATIC CELL GENETICS; ANIMAL; ANIMAL EMBRYO; CHORION; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OOCYTE; PRENATAL DEVELOPMENT; TIME;

ANIMALS; CHORION; CYTOCHROME P-450 ENZYME SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; MUTATION; OVARIAN FOLLICLE; OVUM; PEROXIDASES; RNA, MESSENGER; TIME FACTORS;

EID: 79957570660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019943     Document Type: Article

References (59)

1. Spradling AC, (1993) Developmental genetics of oogenesis. In: Martinez-Arias B, editors. The development of Drosophila melanogaster Cold Spring Harbor Laboratory Press pp. 1-70.
2. Waring GL, (2000) Morphogenesis of the eggshell in Drosophila. Int Rev Cytol 198: 67-108.
3. Cavaliere V, Bernardi F, Romani P, Duchi S, Gargiulo G, (2008) Building up the Drosophila eggshell: first of all the eggshell genes must be transcribed. Dev Dyn 237: 2061-2072.
4. Berg CA, (2008) Tube formation in Drosophila egg chambers. Tissue Eng Part A 14: 1479-1488.
5. Wu X, Tanwar PS, Raftery LA, (2008) Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19: 271-282.
6. Stevens LM, Beuchle D, Jurcsak J, Tong X, Stein D, (2003) The Drosophila embryonic patterning determinant torsolike is a component of the eggshell. Curr Biol 13: 1058-1063.
7. Ray RP, Schupbach T, (1996) Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev 10: 1711-1723.
8. LeMosy EK, Hashimoto C, (2000) The nudel protease of Drosophila is required for eggshell biogenesis in addition to embryonic patterning. Dev Biol 217: 352-361.
9. Kolahi KS, White PF, Shreter DM, Classen AK, Bilder D, et al. (2009) Quantitative analysis of epithelial morphogenesis in Drosophila oogenesis: New insights based on morphometric analysis and mechanical modeling. Dev Biol 331: 129-139.
10. Yakoby N, Bristow CA, Gong D, Schafer X, Lembong J, et al. (2008) A combinatorial code for pattern formation in Drosophila oogenesis. Dev Cell 15: 725-737.
11. Fakhouri M, Elalayli M, Sherling D, Hall JD, Miller E, et al. (2006) Minor proteins and enzymes of the Drosophila eggshell matrix. Dev Biol 293: 127-141.
12. Parks S, Spradling A, (1987) Spatially regulated expression of chorion genes during Drosophila oogenesis. Genes Dev 1: 497-509.
13. Tolias PP, Konsolaki M, Halfon MS, Stroumbakis ND, Kafatos FC, (1993) Elements controlling follicular expression of the s36 chorion gene during Drosophila oogenesis. Mol Cell Biol 13: 5898-5906.
14. Yakoby N, Lembong J, Schupbach T, Shvartsman SY, (2008) Drosophila eggshell is patterned by sequential action of feedforward and feedback loops. Development 135: 343-351.
15. Nogueron MI, Mauzy-Melitz D, Waring GL, (2000) Drosophila dec-1 eggshell proteins are differentially distributed via a multistep extracellular processing and localization pathway. Dev Biol 225: 459-470.
16. Pascucci T, Perrino J, Mahowald AP, Waring GL, (1996) Eggshell assembly in Drosophila: processing and localization of vitelline membrane and chorion proteins. Dev Biol 177: 590-598.
17. Polesello C, Tapon N, (2007) Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr Biol 17: 1864-1870.
18. Buszczak M, Freeman MR, Carlson JR, Bender M, Cooley L, et al. (1999) Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126: 4581-4589.
19. Hackney JF, Pucci C, Naes E, Dobens L, (2007) Ras signaling modulates activity of the Ecdysone Receptor EcR during cell migration in the drosophila ovary. Dev Dyn 236: 1213-1226.
20. Bernardi F, Romani P, Tzertzinis G, Gargiulo G, Cavaliere V, (2009) EcR-B1 and Usp nuclear hormone receptors regulate expression of the VM32E eggshell gene during Drosophila oogenesis. Dev Biol 328: 541-551.
21. Binelli M, Murphy BD, (2010) Coordinated regulation of follicle development by germ and somatic cells. Reprod Fertil Dev 22: 1-12.
22. Downs SM, Longo FJ, (1983) Prostaglandins and preovulatory follicular maturation in mice. J Exp Zool 228: 99-108.
23. Machado E, Swevers L, Sdralia N, Medeiros MN, Mello FG, et al. (2007) Prostaglandin signaling and ovarian follicle development in the silkmoth, Bombyx mori. Insect Biochem Mol Biol 37: 876-885.
24. Lister AL, Van Der Kraak G, (2008) An investigation into the role of prostaglandins in zebrafish oocyte maturation and ovulation. Gen Comp Endocrinol 159: 46-57.
25. Tootle TL, Spradling AC, (2008) Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 135: 839-847.
26. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, et al. (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91: 197-208.
27. Takahashi T, Morrow JD, Wang H, Dey SK, (2006) Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem 281: 37117-37129.
28. Guittard E, Blais C, Maria A, Parvy JP, Pasricha S, et al. (2011) CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev Biol 349: 35-45.
29. Cox RT, Spradling AC, (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130: 1579-1590.
30. Claycomb JM, Benasutti M, Bosco G, Fenger DD, Orr-Weaver TL, (2004) Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev Cell 6: 145-155.
31. Syed ZA, Hard T, Uv A, van Dijk-Hard IF, (2008) A potential role for Drosophila mucins in development and physiology. PLoS One 3: e3041.
32. Spradling AC, Mahowald AP, (1979) Identification and genetic localization of mRNAs from ovarian follicle cells of Drosophila melanogaster. Cell 16: 589-598.
33. Chintapalli VR, Wang J, Dow JA, (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720.
34. Bernardi F, Duchi S, Cavaliere V, Donati A, Andrenacci D, et al. (2007) Egfr signaling modulates VM32E gene expression during Drosophila oogenesis. Dev Genes Evol 217: 529-540.
35. Robinson DS, King NR, Bowen DJ, (1968) The occurrence of neutral and acidic mucins in the reproductive tract of the laying hen. Histochemie 13: 97-104.
36. Lagow E, DeSouza MM, Carson DD, (1999) Mammalian reproductive tract mucins. Hum Reprod Update 5: 280-292.
37. Jonchere V, Rehault-Godbert S, Hennequet-Antier C, Cabau C, Sibut V, et al. (2010) Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 11: 57-76.
38. Petri WH, Wyman AR, Kafatos FC, (1976) Specific protein synthesis in cellular differentiation. III. The eggshell proteins of Drosophila melanogaster and their program of synthesis. Dev Biol 49: 185-199.
39. Konstandi OA, Papassideri IS, Stravopodis DJ, Kenoutis CA, Hasan Z, et al. (2005) The enzymatic component of Drosophila melanogaster chorion is the Pxd peroxidase. Insect Biochem Mol Biol 35: 1043-1057.
40. Li J, Hodgeman BA, Christensen BM, (1996) Involvement of peroxidase in chorion hardening in Aedes aegypti. Insect Biochem Mol Biol 26: 309-317.
41. Yoshiga T, Okano K, Mita K, Shimada T, Matsumoto S, (2000) cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene 246: 339-345.
42. Szafer-Glusman E, Giansanti MG, Nishihama R, Bolival B, Pringle J, et al. (2008) A role for very-long-chain fatty acids in furrow ingression during cytokinesis in Drosophila spermatocytes. Curr Biol 18: 1426-1431.
43. Eppig JJ, (2001) Oocyte control of ovarian follicular development and function in mammals. Reproduction 122: 829-838.
44. Eppig JJ, Wigglesworth K, Pendola FL, (2002) The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 99: 2890-2894.
45. Gilchrist RB, Ritter LJ, Armstrong DT, (2004) Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82-83: 431-446.
46. Fuchs AR, (1987) Prostaglandin F2 alpha and oxytocin interactions in ovarian and uterine function. J Steroid Biochem 27: 1073-1080.
47. Slonina D, Kowalik MK, Subocz M, Kotwica J, (2009) The effect of ovarian steroids on oxytocin-stimulated secretion and synthesis of prostaglandins in bovine myometrial cells. Prostaglandins Other Lipid Mediat 90: 69-75.
48. Brodie AM, Lu Q, Long BJ, Fulton A, Chen T, et al. (2001) Aromatase and COX-2 expression in human breast cancers. J Steroid Biochem Mol Biol 79: 41-47.
49. Howe LR, (2007) Inflammation and breast cancer. Cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res 9: 210.
50. Zhao Y, Agarwal VR, Mendelson CR, Simpson ER, (1996) Estrogen biosynthesis proximal to a breast tumor is stimulated by PGE2 via cyclic AMP, leading to activation of promoter II of the CYP19 (aromatase) gene. Endocrinology 137: 5739-5742.
51. Karuppu D, Kalus A, Simpson ER, Clyne C, (2002) Aromatase and prostaglandin inter-relationships in breast adipose tissue: significance for breast cancer development. Breast Cancer Res Treat 76: 103-109.
52. Prosperi JR, Robertson FM, (2006) Cyclooxygenase-2 directly regulates gene expression of P450 Cyp19 aromatase promoter regions pII, pI.3 and pI.7 and estradiol production in human breast tumor cells. Prostaglandins Other Lipid Mediat 81: 55-70.
53. Bulun SE, (2009) Endometriosis. N Engl J Med 360: 268-279.
54. Attar E, Bulun SE, (2006) Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum Reprod Update 12: 49-56.
55. Attar E, Tokunaga H, Imir G, Yilmaz MB, Redwine D, et al. (2009) Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab 94: 623-631.
56. Bulin C, Albrecht U, Bode JG, Weber AA, Schror K, et al. (2005) Differential effects of vasodilatory prostaglandins on focal adhesions, cytoskeletal architecture, and migration in human aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 25: 84-89.
57. Ebert AD, Bartley J, David M, (2005) Aromatase inhibitors and cyclooxygenase-2 (COX-2) inhibitors in endometriosis: new questions-old answers? Eur J Obstet Gynecol Reprod Biol 122: 144-150.
58. Carney GE, Bender M, (2000) The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis. Genetics 154: 1203-1211.
59. Gaziova I, Bonnette PC, Henrich VC, Jindra M, (2004) Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development 131: 2715-2725.