Sexual reproduction is thought to be a highly divergent process due to fast evolution and speciation. For example, sperm from one species can seldom fertilize eggs from another species, indicating that different molecular machinery for fertilization is applied in different species. In contrast to this divergent view, ovulation, the process of liberating mature eggs from the ovary, is a general phenomenon throughout the Metazoa. We provide evidence that basic mechanisms of ovulation are conserved. Like mammalian follicles, Drosophila follicles consist of single oocytes surrounded by a layer of follicle cells. Drosophila follicles degrade their posterior follicle cells to allow the oocyte to rupture into the oviduct during ovulation. The residual postovulatory follicles reside in the ovary, accumulate yellowish pigmentation, and produce the steroid hormone ecdysone, features which resemble the mammalian corpus luteum. We also showed that matrix metalloproteinase, a type of proteinase proposed to degrade the mammalian follicle wall during ovulation, is required in Drosophila for posterior follicle cell degradation and ovulation. These findings are particularly important because this simple genetic model system will speed up the identification of many conserved regulators required for regulating matrix metalloproteinase activity and ovulation in human, processes that influence ovarian cancer formation and cancer metastasis.
Vyšlo v časopise: Matrix Metalloproteinase 2 Is Required for Ovulation and Corpus Luteum Formation in. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004989 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004989
1. Conti M, Hsieh M, Musa Zamah A, Oh JS (2012) Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol 356 : 65–73. doi: 10.1016/j.mce.2011.11.002 22101318
2. Espey LL, Richards JS (2006) Ovulation. In: Neill JD, editor. Physiology of Reproduction. Amsterdam: Academic Press, Vol. 1. pp. 425–474.
3. Fan H-Y, Liu Z, Mullany LK, Richards JS (2012) Consequences of RAS and MAPK activation in the ovary: The good, the bad and the ugly. Mol Cell Endocrinol 356 : 74–79. doi: 10.1016/j.mce.2011.12.005 22197887
4. Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN (1998) Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol 145 : 47–54. doi: 10.1016/S0303–7207(98)00168–3 9922098
5. Ohnishi J, Ohnishi E, Shibuya H, Takahashi T (2005) Functions for proteinases in the ovulatory process. Biochim Biophys Acta BBA—Proteins Proteomics 1751 : 95–109. doi: 10.1016/j.bbapap.2005.05.002 25626174
6. Curry TE, Osteen KG (2003) The Matrix Metalloproteinase System: Changes, Regulation, and Impact throughout the Ovarian and Uterine Reproductive Cycle. Endocr Rev 24 : 428–465. doi: 10.1210/er.2002–0005 12920150
7. Curry T, Smith M (2006) Impact of Extracellular Matrix Remodeling on Ovulation and the Folliculo-Luteal Transition. Semin Reprod Med 24 : 228–241. doi: 10.1055/s-2006–948552 16944420
8. McCord LA, Li F, Rosewell KL, Brännström M, Curry TE (2012) Ovarian Expression and Regulation of the Stromelysins During the Periovulatory Period in the Human and the Rat. Biol Reprod 86 : 78. doi: 10.1095/biolreprod.111.095588 22116802
9. Gill SE, Kassim SY, Birkland TP, Parks WC (2010) Mouse Models of MMP and TIMP Function. In: Clark IM, editor. Matrix Metalloproteinase Protocols. Methods in Molecular Biology. Totowa, NJ: Humana Press, Vol. 622. pp. 31–52. Available: http://link.springer.com/10.1007/978-1-60327-299-5. Accessed 2 June 2014. doi: 10.1007/978-1-60327-299-5_2 20135274
10. Spradling AC (1993) Developmental genetics of oogenesis. In: Bate M, Martinez-Arias A, editors. The Development of Drosophila melanogaster. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, Vol. I. pp. 1–70.
11. Yang CH, Belawat P, Hafen E, Jan LY, Jan YN (2008) Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319 : 1679–1683. doi: 10.1126/science.1151842 18356529
12. Lee H-G, Seong C-S, Kim Y-C, Davis RL, Han K-A (2003) Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. Dev Biol 264 : 179–190. doi: 10.1016/j.ydbio.2003.07.018 14623240
13. Monastirioti M (2003) Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev Biol 264 : 38–49. doi: 10.1016/j.ydbio.2003.07.019 14623230
14. Lee HG, Rohila S, Han KA (2009) The octopamine receptor OAMB mediates ovulation via Ca2+/calmodulin-dependent protein kinase II in the Drosophila oviduct epithelium. PLoS One 4: e4716. doi: 10.1371/journal.pone.0004716 19262750
15. Yapici N, Kim YJ, Ribeiro C, Dickson BJ (2008) A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451 : 33–37. doi: 10.1038/nature06483 18066048
16. Hasemeyer M, Yapici N, Heberlein U, Dickson BJ (2009) Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61 : 511–518. doi: 10.1016/j.neuron.2009.01.009 19249272
17. Rubinstein CD, Wolfner MF (2013) Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc Natl Acad Sci 110 : 17420–17425. doi: 10.1073/pnas.1220018110 24101486
18. Yang C, Rumpf S, Xiang Y, Gordon MD, Song W, et al. (2009) Control of the Postmating Behavioral Switch in Drosophila Females by Internal Sensory Neurons. Neuron 61 : 519–526. doi: 10.1016/j.neuron.2008.12.021 19249273
19. Sun J, Spradling AC (2013) Ovulation in Drosophila is controlled by secretory cells of the female reproductive tract. Elife 2. Available: http://elife.elifesciences.org/content/2/e00415.short. Accessed 13 March 2014.
20. Duggavathi R, Volle DH, Mataki C, Antal MC, Messaddeq N, et al. (2008) Liver receptor homolog 1 is essential for ovulation. Genes Dev 22 : 1871–1876. doi: 10.1101/gad.472008 18628394
21. Zhang C, Large MJ, Duggavathi R, Demayo FJ, Lydon JP, et al. (2013) Liver receptor homolog-1 is essential for pregnancy. Nat Med. doi: 10.1038/nm.3435 24466584
22. Büning J (1994) The Insect Ovary: Ultrastructure, Previtellogenic Growth and Evolution. Springer. 424 p.
23. Sun J, Deng W-M (2007) Hindsight Mediates the Role of Notch in Suppressing Hedgehog Signaling and Cell Proliferation. Dev Cell 12 : 431–442. doi: 10.1016/j.devcel.2007.02.003 17336908
24. Petryk A, Warren JT, Marqués G, Jarcho MP, Gilbert LI, et al. (2003) Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc Natl Acad Sci 100 : 13773–13778. doi: 10.1073/pnas.2336088100 14610274
25. Warren JT, Petryk A, Marqués G, Parvy J-P, Shinoda T, et al. (2004) Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: a P450 enzyme critical in ecdysone biosynthesis. Insect Biochem Mol Biol 34 : 991–1010. doi: 10.1016/j.ibmb.2004.06.009 15350618
26. Domanitskaya E, Anllo L, Schüpbach T (2014) Phantom, a cytochrome P450 enzyme essential for ecdysone biosynthesis, plays a critical role in the control of border cell migration in Drosophila. Dev Biol 386 : 408–418. doi: 10.1016/j.ydbio.2013.12.013 24373956
27. Page-McCaw A (2008) Remodeling the model organism: matrix metalloproteinase functions in invertebrates. Semin Cell Dev Biol 19 : 14–23. doi: 10.1016/j.semcdb.2007.06.004 17702617
28. Brännström M, Woessner JF Jr, Koos RD, Sear CH, LeMaire WJ (1988) Inhibitors of mammalian tissue collagenase and metalloproteinases suppress ovulation in the perfused rat ovary. Endocrinology 122 : 1715–1721. doi: 10.1210/endo-122–5–1715 2452070
29. Reich R, Tsafriri A, Mechanic GL (1985) The involvement of collagenolysis in ovulation in the rat. Endocrinology 116 : 522–527. doi: 10.1210/endo-116–2–522 2981665
30. Chaffin CL, VandeVoort CA (2013) Follicle growth, ovulation, and luteal formation in primates and rodents: A comparative perspective. Exp Biol Med 238 : 539–548. doi: 10.1177/1535370213489437 23856905
31. Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T (2005) Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci U S A 102 : 8442–8447. doi: 10.1073/pnas.0502423102 15941829
32. Watt J (1915) Contributions to Embryology. Carnegie Institution of Washington Publication no. 222. 85–86 p.
33. Tootle TL, Williams D, Hubb A, Frederick R, Spradling A (2011) Drosophila Eggshell Production: Identification of New Genes and Coordination by Pxt. PLoS ONE 6: e19943. doi: 10.1371/journal.pone.0019943 21637834
34. Parks S, Spradling AC (1987) Spatially regulated expression of chorion genes during Drosophila oogenesis. Genes Dev 1 : 497–509. doi: 10.1101/gad.1.5.497.
35. Harshman LG, Loeb AM, Johnson BA (1999) Ecdysteroid titers in mated and unmated Drosophila melanogaster females. J Insect Physiol 45 : 571–577. doi: 10.1016/S0022–1910(99)00038–4 12770342
36. Sawada M, Carlson JC (1996) Intracellular regulation of progesterone secretion by the superoxide radical in the rat corpus luteum. Endocrinology 137 : 1580–1584. doi: 10.1210/endo.137.5.8612488 8612488
37. Schweigert FJ (2003) Research note: changes in the concentration of beta-carotene, alpha-tocopherol and retinol in the bovine corpus luteum during the ovarian cycle. Arch Für Tierernähr 57 : 307–310. 4740118
38. Jenett A, Rubin GM, Ngo T-TB, Shepherd D, Murphy C, et al. (2012) A GAL4-Driver Line Resource for Drosophila Neurobiology. Cell Rep 2 : 991–1001. doi: 10.1016/j.celrep.2012.09.011 23063364
39. Uhlirova M, Bohmann D (2006) JNK-and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J 25 : 5294–5304. 17082773
40. Glasheen BM, Kabra AT, Page-McCaw A (2009) Distinct functions for the catalytic and hemopexin domains of a Drosophila matrix metalloproteinase. Proc Natl Acad Sci U A 106 : 2659–2664. doi: 10.1073/pnas.0804171106 19196956
41. Page-McCaw A, Serano J, Sante JM, Rubin GM (2003) Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development. Dev Cell 4 : 95–106. doi: 10.1016/S1534-5807(02)00400-8 12530966
42. Venken KJ, Schulze KL, Haelterman NA, Pan H, He Y, et al. (2011) MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat Methods 8 : 737–743. 21985007
43. Srivastava A, Pastor-Pareja JC, Igaki T, Pagliarini R, Xu T (2007) Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc Natl Acad Sci U A 104 : 2721–2726. doi: 10.1073/pnas.0611666104 17301221
44. Sun J, Spradling AC (2012) NR5A Nuclear Receptor Hr39 Controls Three-Cell Secretory Unit Formation in Drosophila Female Reproductive Glands. Curr Biol 22 : 862–871. doi: 10.1016/j.cub.2012.03.059 22560612
45. Vidal M, Salavaggione L, Ylagan L, Wilkins M, Watson M, et al. (2010) A role for the epithelial microenvironment at tumor boundaries: evidence from Drosophila and human squamous cell carcinomas. Am J Pathol 176 : 3007–3014. doi: 10.2353/ajpath.2010.090253 20363916
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
