Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Expression of caspase 3 in ovarian follicle cells of the lizard Podarcis sicula

  • 314 Accesses

  • 1 Citations

Abstract

In this study, our aim was to determine whether caspase 3 plays a role, during previtellogenesis, in the ovarian follicular epithelium of the lizard Podarcis sicula. We investigated the presence and localization of proform and active caspase 3 by enzyme assay, Western blotting and immunocytochemistry. In parallel, a fragment of caspase 3 was cloned for the first time in this species, sequenced and used for in situ hybridization to localize messengers and analysed by a phylogenetic survey to shed light on its homology with reptilian caspases. Results demonstrated that: (1) the follicle cells expressed a caspase of the 3/7 group and the mRNA for caspase 3 was transcribed in the stem phase and was completely translated during cell differentiation; (2) the proform protein was stored during the differentiated (nurse) stage and activated at the end of previtellogenesis provoking the degeneration of cells; (3) the predicted protein sequence, although partial, had a strong similarity with the known reptilian caspases 3. The epithelial cells of the ovarian follicle, therefore, do not employ caspase 3 during the nurse stage but, instead, prepare for apoptosis long before the process actually begins. The relevance of this strategy is discussed.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

  2. Andreuccetti P, Taddei C, Filosa S (1978) Intercellular bridges between follicle cells and oocyte during the differentiation of follicular epithelium in Lacerta sicula. J Cell Sci 33:341–350

  3. Blanc C, Deveraux QL, Krajewski S, Janicke RU, Porter AG, Reed JC, Jaggi R, Marti A (2000) Caspase-3 is essential for procaspase-9 processing and cisplatin-induced apoptosis of MCF-7 breast cancer cells. Cancer Res 60:4386–4390

  4. Boccaccio GL, Carminatti H, Colman DR (1999) Subcellular fractionation and association with the cytoskeleton of messengers encoding myelin proteins. J Neurosci Res 58:480–491

  5. Chang HY, Yang X (2000) Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64:821–846

  6. Chen YR, Kori R, John B, Tan TH (2001) Caspase-mediated cleavage of actin-binding and SH3-domain-containing proteins cortactin, HS1, and HIP-55 during apoptosis. Biochem Biophys Res Commun 288:981–989

  7. De Caro M, Indolfi P, Iodice C, Spagnolo MS, Tammaro S, Motta CM (1998) How the ovarian follicles of Podarcis sicula recycles the DNA of its nurse regressing follicle cells. Mol Reprod Dev 51:421–429

  8. Kumar S (1997) The apoptotic cysteine protease CPP32. Int J Biochem Cell Biol 29:393–396

  9. Kumar S (2004) Migrate, differentiate, proliferate, or die: pleiotropic functions of an apical apoptotic caspase. Sci STKE 254:pe49

  10. Lechardeur D, Drzymala L, Sharma M, Zylka D, Kinach R, Pacia J, Hicks C, Usmani N, Rommens JM, Lukacs GL (2000) Determinants of the nuclear localization of the heterodimeric DNA fragmentation factor (ICAD/CAD). J Cell Biol 150:321–334

  11. Maurizii MG, Saverino O, Taddei C (1997) Cytokeratin cytoskeleton in the differentiating ovarian follicle of the lizard Podarcis sicula. Mol Reprod Dev 48:536–542

  12. Maurizii MG, Alibardi L, Taddei C (2000) Organization and characterization of the keratin cytoskeleton in the previtellogenic ovarian follicle of the lizard Podarcis sicula. Mol Reprod Dev 57:159–166

  13. Motta CM, Castriota Scanderbeg M, Filosa S, Andreuccetti P (1995) Role of pyriform cells during the growth of oocytes in the lizard Podarcis sicula. J Exp Zool 273:247–256

  14. Motta CM, Filosa S, Andreuccetti P (1996) Regression of the epithelium in late previtellogenic follicles of Podarcis sicula: a case of apoptosis. J Exp Zool 276:233–241

  15. Motta CM, Tammaro S, Cicale A, Indolfi P, Iodice C, Spagnuolo MS, Filosa S (2001) Storage in the yolk platelets of low MW DNA produced by the regressing follicle cells. Mol Reprod Dev 59:422–430

  16. Pondel MD, King ML (1988) Localized maternal mRNA related to transforming growth factor beta mRNA is concentrated in a cytokeratin-enriched fraction from Xenopus oocytes. Proc Natl Acad Sci USA 85:7612–7616

  17. Proskuryakov SY, Konoplyannikov AG, Gabai VL (2003) Necrosis: a specific form of programmed cell death? Exp Cell Res 283:1–16

  18. Rosati L, Prisco M, Coraggio F, Valiante S, Scudiero R, Laforgia V, Andreuccetti P, Agnese M (2014) PACAP and PAC1 receptor in the reproductive cycle of male lizard Podarcis sicula. Gen Comp Endocrinol 205:102–108

  19. Roy S, Bayly CI, Gareau Y, Houtzager VM, Kargman S, Keen SLC, Rowland K, Seiden IM, Thornberry NA, Nicholson DW (2001) Maintenance of caspase-3 proenzyme dormancy by an intrinsic “safety catch” regulatory tripeptide. Proc Natl Acad Sci USA 98:6132–6137

  20. Ruchaud S, Korfali N, Villa P, Kottke TJ, Dingwall C, Kaufmann SH, Earnshaw WC (2002) Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J 21:1967–1977

  21. Shimizu T, Pommier Y (1997) Camptothecin-induced apoptosis in p53-null human leukemia HL60 cells and their isolated nuclei: effects of the protease inhibitors Z-VAD-fmk and dichloroisocoumarin suggest an involvement of both caspases and serine proteases. Leukemia 11:1238–1244

  22. Simoniello P, Motta CM, Scudiero R, Trinchella F, Filosa S (2010) Spatiotemporal changes in metallothionein gene expression during embryogenesis in the wall lizard Podarcis sicula. J Exp Zool A Ecol Genet Physiol 313:410–420

  23. Slee EA, Adrain C, Martin SJ (1999) Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6:1067–1074

  24. Soldani C, Scovassi AI (2002) Poly (ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7:321–328

  25. Tammaro S, Simoniello P, Filosa S, Motta CM (2007) Block of mitochondrial apoptotic pathways in lizard ovarian follicle cells as an adaptation to their nurse function. Cell Tissue Res 327:625–635

  26. Tammaro S, Simoniello P, Filosa S, Motta CM (2008) cGnRH II involvement in pyriform cell apoptosis. Cell Tissue Res 332:337–347

  27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

  28. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

  29. Zheng Y, Wiens JJ (2016) Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol 94:537–547

Download references

Author information

Correspondence to Chiara Maria Motta.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tammaro, S., Simoniello, P., Ristoratore, F. et al. Expression of caspase 3 in ovarian follicle cells of the lizard Podarcis sicula . Cell Tissue Res 367, 397–404 (2017). https://doi.org/10.1007/s00441-016-2506-7

Download citation

Keywords

  • Caspase 3 expression
  • Apoptosis and tissue differentiation
  • Caspase 3 activation
  • Ovarian follicular epithelium remodelling
  • Pyriform cells