Spermatid Cyst Polarization in Depends upon and the CPEB Family Translational Regulator

English version České info

After completion of meiosis, the 64 cells in the spermatid cyst begin differentiating into sperm. Sperm are highly polarized cells and a critical step in their differentiation is spermatid cyst polarization. Spermatids are also polarized within the testis, with the heads of the elongating spermatids located basally, while the tails extend apically. We show that aPKC accumulates preferentially on the apical side of the cyst during polarization and is required to correctly orient cyst polarization with respect to the apical-basal axis of the testis. Unexpectedly, aPKC activity is spatially restricted by a mechanism that depends upon the CPEB family translational regulator orb2. orb2 is required to asymmetrically localize and activate the translation of apkc mRNAs during spermatid differentiation. In addition to correctly orienting the direction of cyst polarization, orb2 is required for the process of polarization itself. One of the orb2 regulatory targets in this process is its own mRNA, and this autoregulatory activity depends, in turn, upon apkc.

Vyšlo v časopise: Spermatid Cyst Polarization in Depends upon and the CPEB Family Translational Regulator. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004380
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004380

Souhrn

Zdroje

1. MunroE, BowermanB (2009) Cellular symmetry breaking during Caenorhabditis elegans development. Cold Spring Harb Perspect Biol 1: a003400.

2. Etemad-MoghadamB, GuoS, KemphuesKJ (1995) Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83: 743–752.

3. WattsJL, Etemad-MoghadamB, GuoS, BoydL, DraperBW, et al. (1996) par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122: 3133–3140.

4. TabuseY, IzumiY, PianoF, KemphuesKJ, MiwaJ, et al. (1998) Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125: 3607–3614.

5. HaoY, BoydL, SeydouxG (2006) Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev Cell 10: 199–208.

6. HurovJB, WatkinsJL, Piwnica-WormsH (2004) Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr Biol 14: 736–741.

7. SchneiderSQ, BowermanB (2003) Cell polarity and the cytoskeleton in the Caenorhabditis elegans zygote. Annu Rev Genet 37: 221–249.

8. DoeCQ (2001) Cell polarity: the PARty expands. Nat Cell Biol 3: E7–9.

9. JanYN, JanLY (2001) Asymmetric cell division in the Drosophila nervous system. Nat Rev Neurosci 2: 772–779.

10. BetschingerJ, KnoblichJA (2004) Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr Biol 14: R674–685.

11. ChiaW, SomersWG, WangH (2008) Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J Cell Biol 180: 267–272.

12. TokuyasuKT, PeacockWJ, HardyRW (1972) Dynamics of spermiogenesis in Drosophila melanogaster. I. Individualization process. Z Zellforsch Mikrosk Anat 124: 479–506.

13. Fuller MT (1993) Spermatogenesis. The Development of Drosophila. M. Martinez-Arias and M. Bate ed. Cold Spring Harbor, New York: Cold Spring Harbor Press. pp. 71–147.

14. TokuyasuKT (1975) Dynamics of spermiogenesis in Drosophila melanogaster. VI. Significance of “onion” nebenkern formation. J Ultrastruct Res 53: 93–112.

15. TokuyasuKT (1974) Dynamics of spermiogenesis in Drosophila melanogaster. 3. Relation between axoneme and mitochondrial derivatives. Exp Cell Res 84: 239–250.

16. FabianL, BrillJA (2012) Drosophila spermiogenesis: Big things come from little packages. Spermatogenesis 2: 197–212.

17. RollsMM, AlbertsonR, ShihHP, LeeCY, DoeCQ (2003) Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J Cell Biol 163: 1089–1098.

18. WodarzA, RamrathA, GrimmA, KnustE (2000) Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol 150: 1361–1374.

19. FabianL, WeiHC, RollinsJ, NoguchiT, BlankenshipJT, et al. (2010) Phosphatidylinositol 4,5-bisphosphate directs spermatid cell polarity and exocyst localization in Drosophila. Mol Biol Cell 21: 1546–1555.

20. NoguchiT, MillerKG (2003) A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130: 1805–1816.

21. White-CooperH (2012) Tissue, cell type and stage-specific ectopic gene expression and RNAi induction in the Drosophila testis. Spermatogenesis 2: 11–22.

22. NiJQ, ZhouR, CzechB, LiuLP, HolderbaumL, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407.

23. BarreauC, BensonE, GudmannsdottirE, NewtonF, White-CooperH (2008) Post-meiotic transcription in Drosophila testes. Development 135: 1897–1902.

24. ChangJS, TanL, SchedlP (1999) The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev Biol 215: 91–106.

25. ChangJS, TanL, WolfMR, SchedlP (2001) Functioning of the Drosophila orb gene in gurken mRNA localization and translation. Development 128: 3169–3177.

26. ChristersonLB, McKearinDM (1994) orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev 8: 614–628.

27. MendezR, RichterJD (2001) Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2: 521–529.

28. RichterJD (2007) CPEB: a life in translation. Trends Biochem Sci 32: 279–285.

29. XuS, HaferN, AgunwambaB, SchedlP (2012) The CPEB Protein Orb2 Has Multiple Functions during Spermatogenesis in Drosophila melanogaster. PLoS Genet 8: e1003079.

30. HaferN, XuS, BhatKM, SchedlP (2011) The Drosophila CPEB protein Orb2 has a novel expression pattern and is important for asymmetric cell division and nervous system function. Genetics 189: 907–921.

31. Mastushita-SakaiT, White-GrindleyE, SamuelsonJ, SeidelC, SiK (2010) Drosophila Orb2 targets genes involved in neuronal growth, synapse formation, and protein turnover. Proc Natl Acad Sci U S A 107: 11987–11992.

32. KelemanK, KruttnerS, AleniusM, DicksonBJ (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 10: 1587–1593.

33. EberhartCG, MainesJZ, WassermanSA (1996) Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature 381: 783–785.

34. TanL, ChangJS, CostaA, SchedlP (2001) An autoregulatory feedback loop directs the localized expression of the Drosophila CPEB protein Orb in the developing oocyte. Development 128: 1159–1169.

35. FanW, XuX, ShenY, FengH, LiA, et al. (2014) Prediction of protein kinase-specific phosphorylation sites in hierarchical structure using functional information and random forest. Amino Acids 46: 1069–1078.

36. ZuoX, FogelgrenB, LipschutzJH (2011) The small GTPase Cdc42 is necessary for primary ciliogenesis in renal tubular epithelial cells. J Biol Chem 286: 22469–22477.

37. HarrisKP, TepassU (2010) Cdc42 and vesicle trafficking in polarized cells. Traffic 11: 1272–1279.

38. HuttererA, BetschingerJ, PetronczkiM, KnoblichJA (2004) Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev Cell 6: 845–854.

39. HughesJR, BullockSL, Ish-HorowiczD (2004) Inscuteable mRNA localization is dynein-dependent and regulates apicobasal polarity and spindle length in Drosophila neuroblasts. Curr Biol 14: 1950–1956.

40. Horne-BadovinacS, BilderD (2008) Dynein regulates epithelial polarity and the apical localization of stardust A mRNA. PLoS Genet 4: e8.

41. FuerstenbergS, BroadusJ, DoeCQ (1998) Asymmetry and cell fate in the Drosophila embryonic CNS. Int J Dev Biol 42: 379–383.

42. MedioniC, MowryK, BesseF (2012) Principles and roles of mRNA localization in animal development. Development 139: 3263–3276.

43. van EedenF, St JohnstonD (1999) The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr Opin Genet Dev 9: 396–404.

44. PapagiannouliF, MechlerBM (2009) discs large regulates somatic cyst cell survival and expansion in Drosophila testis. Cell Res 19: 1139–1149.

45. NiJQ, LiuLP, BinariR, HardyR, ShimHS, et al. (2009) A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182: 1089–1100.

46. ChengMH, MainesJZ, WassermanSA (1998) Biphasic subcellular localization of the DAZL-related protein boule in Drosophila spermatogenesis. Dev Biol 204: 567–576.

47. WangYC, KhanZ, KaschubeM, WieschausEF (2012) Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 484: 390–393.