Crossref journal-article
The Company of Biologists
Development (237)
Abstract

ABSTRACT The establishment of dorsoventral polarity in the Drosophila oocyte and future embryo is dependent on the efficient transport of K10 mRNA from nurse cells into the oocyte. To investigate the cis-requirements of K10 mRNA transport, we used a transgenic fly assay to analyze the expression patterns of a series of K10 deletion variants. Such studies identify a 44 nucleotide sequence within the K10 3′ untranslated region that is required and sufficient for K10 mRNA transport and subsequent localization to the oocyte’s anterior cortex. An inspection of the 44 nucleotide transport/localization sequence (TLS) reveals a strong potential for the formation of a stem-loop secondary structure. Nucleotide substitutions that interfere with the predicted base-pairing of the TLS block mRNA transport and anterior localization. Conversely, mutations that alter the base composition of the TLS while maintaining predicted base-pairing do not block mRNA transport or anterior localization. We conclude that K10 mRNA transport and anterior localization is mediated by a 44 nucleotide stem-loop structure. A similar putative stemloop structure is found in the 3′ untranslated region of the Drosophila orb mRNA, suggesting that the same factors mediate the transport and anterior localization of both K10 and orb mRNAs. Apart from orb, the K10 TLS is not found in any other localized mRNA, raising the possibility that the transport and localization of other mRNAs, e.g., bicoid, oskar and gurken, are mediated by novel sets of cisand trans-acting factors. Moreover, we find that the K10 TLS overrides the activity of oskar cis-regulatory elements that mediate the late stage movement of the mRNA to the posterior pole. We propose the existence of a family of cisregulatory elements that mediate mRNA transport into the oocyte, only some of which are compatible with the elements that mediate late stage movements.

Bibliography

Serano, T. L., & Cohen, R. S. (1995). A small predicted stem-loop structure mediates oocyte localization of Drosophila K10 mRNA. Development, 121(11), 3809–3818.

Authors 2
  1. Thomas L. Serano (first)
  2. Robert S. Cohen (additional)
References 46 Referenced 86
  1. 10.1016/0022-2836(79)90268-7 / J. Mol. Biol / Solvent-accessible surfaces of nucleic acids by Alden (1979)
  2. 10.1002/j.1460-2075.1988.tb03004.x / EMBO J / The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo by Berleth (1988)
  3. 10.1242/dev.114.3.653 / Development / Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg by Cheung (1992)
  4. 10.1016/S0960-9822(00)00068-3 / Curr. Biol / Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte by Clark (1994)
  5. 10.1016/0092-8674(85)90247-8 / Cell / Separate regulatory elements for the heat-inducible and ovarian expression of the Drosophila hsp26 gene by Cohen (1985)
  6. {'key': '2025011515123948000_DEVELOP_121_11_3809C6', 'article-title': 'mRNA localization and function of the Drosophila fs(1)K10 gene', 'volume-title': 'In RNA Localization', 'author': 'Cohen', 'year': '1995'} / In RNA Localization / mRNA localization and function of the Drosophila fs(1)K10 gene by Cohen (1995)
  7. 10.1126/science.7939713 / Science / Cytoskeletal functions during Drosophila oogenesis by Cooley (1994)
  8. 10.1002/bies.950151004 / BioEssays / Localized RNAs and their functions by Ding (1993)
  9. 10.1016/0092-8674(91)90137-N / Cell / oskar organizes the germ plasm and directs localization of the posterior determinant nanos by Ephrussi (1991)
  10. 10.1016/0003-2697(83)90418-9 / Anal. Biochem / A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity by Feinberg (1983)
  11. 10.1016/0092-8674(94)90013-2 / Cell / Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner by Ferrandon (1994)
  12. 10.1242/dev.114.2.481 / Development / Identification and characterization of Drosophila female germ line transcriptional control elements by Frank (1992)
  13. 10.1002/j.1460-2075.1987.tb04822.x / EMBO J / Oocyte-specific transcription of fs(1)K10: a Drosophila gene affecting dorsal-ventral developmental polarity by Haenlin (1987)
  14. {'volume-title': 'Ovarian Development in Drosophila melanogaster', 'year': '1970', 'author': 'King', 'key': '2025011515123948000_DEVELOP_121_11_3809C14'} / Ovarian Development in Drosophila melanogaster by King (1970)
  15. 10.1016/0092-8674(91)90136-M / Cell / oskar mRNA is localized to the posterior pole of the Drosophila oocyte by Kim-Ha (1991)
  16. 10.1242/dev.119.1.169 / Development / Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA by Kim-Ha (1993)
  17. 10.1242/dev.115.1.75 / Development / The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos by Lantz (1992)
  18. {'key': '2025011515123948000_DEVELOP_121_11_3809C18', 'first-page': '2235', 'article-title': 'Multiple cis-acting target sequences are required for orb mRNA localization during Drosophila oogenesis', 'volume': '14', 'author': 'Lantz', 'year': '1994', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Multiple cis-acting target sequences are required for orb mRNA localization during Drosophila oogenesis by Lantz (1994)
  19. {'volume-title': 'The Genome of Drosophila melanogaster', 'year': '1992', 'author': 'Lindsley', 'key': '2025011515123948000_DEVELOP_121_11_3809C19'} / The Genome of Drosophila melanogaster by Lindsley (1992)
  20. 10.1242/dev.110.1.161 / Development / bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure by Macdonald (1990)
  21. {'key': '2025011515123948000_DEVELOP_121_11_3809C21', 'first-page': '413', 'article-title': 'The means to the ends: localization of maternal messenger RNAs', 'volume': '3', 'author': 'Macdonald', 'year': '1992', 'journal-title': 'Sem. Dev. Biol'} / Sem. Dev. Biol / The means to the ends: localization of maternal messenger RNAs by Macdonald (1992)
  22. 10.1038/336595a0 / Nature / Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos by Macdonald (1988)
  23. 10.1242/dev.118.4.1233 / Development / RNA regulatory element BLE1 directs the early steps of bicoid mRNA localization by Macdonald (1993)
  24. 10.1016/S0092-8674(05)80093-5 / Cell / The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFa-like protein by Neuman-Silberberg (1993)
  25. 10.1016/0092-8674(93)90479-A / Cell / Sorting of membrane proteins in the secretory pathway by Pelham (1993)
  26. 10.1016/B978-0-409-90042-2.50028-3 / In Vectors: A Survey of Molecular Cloning Vectors and Their Uses / Vectors for P-mediated transformation in Drosophila by Pirrotta (1988)
  27. 10.1242/dev.113.1.55 / Development / Microtubules mediate the localization of bicoid mRNA during Drosophila oogenesis by Pokrywka (1991)
  28. 10.1006/dbio.1995.1030 / Dev. Biol / Microtubules are a general component of mRNA localization systems in Drosophila oocytes by Pokrywka (1995)
  29. 10.1101/gad.2.7.891 / Genes Dev / Role of the oocyte nucleus in determination of the dorsoventral polarity of Drosophila as revealed by molecular analysis of the K10 gene by Prost (1988)
  30. 10.1038/243150a0 / Nature / Double helix at atomic resolution by Rosenberg (1973)
  31. 10.1126/science.6289436 / Science / Genetic transformation of Drosophila with transposable element vectors by Rubin (1982)
  32. 10.1093/genetics/129.4.1119 / Genetics / Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology by Schüpbach (1991)
  33. 10.1073/pnas.73.3.804 / Proc. Natl. Acad. Sci. USA / Sequence-specific recognition of double helical nucleic acids by proteins by Seeman (1976)
  34. 10.1016/0378-1119(94)90804-4 / Gene / P element transformation vectors for studying Drosophila melanogaster oogenesis and early embryogenesis by Serano (1994)
  35. 10.1016/0925-4773(95)00363-0 / Mech. Dev / The role of fs(1)K10 in the localization of the mRNA of the TGFα homolog gurken within the Drosophila oocyte by Serano (1995)
  36. 10.1016/S0022-2836(83)80241-1 / J. Mol. Biol / Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B by Southgate (1983)
  37. 10.1126/science.6289435 / Science / Transposition of cloned P elements into Drosophila germ line chromosomes by Spadling (1982)
  38. 10.1016/0092-8674(95)90324-0 / Cell / The intracellular localization of messenger RNAs by St Johnston (1995)
  39. 10.1242/dev.107.Supplement.13 / Development / Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte by St Johnston (1989)
  40. 10.1073/pnas.89.22.10979 / Proc. Natl. Acad. Sci. USA / A conserved double-stranded RNA-binding domain by St Johnston (1992)
  41. 10.1016/0092-8674(91)90365-6 / Cell / Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation by Suter (1991)
  42. 10.1007/BF00291041 / Chromosoma / A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback by Tautz (1989)
  43. 10.1242/dev.115.4.923 / Development / Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport by Theurkauf (1992)
  44. 10.1242/dev.118.4.1169 / Development / A central role for microtubules in the differentiation of Drosophila oocytes by Theurkauf (1993)
  45. 10.1126/science.7690496 / Science / Major groove accessibility of RNA by Weeks (1993)
  46. 10.1016/0092-8674(83)90299-4 / Cell / Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock by Zimmerman (1983)
Dates
Type When
Created 4 years, 4 months ago (April 25, 2021, 10:12 p.m.)
Deposited 7 months, 2 weeks ago (Jan. 15, 2025, 10:12 a.m.)
Indexed 3 weeks, 1 day ago (Aug. 7, 2025, 4:50 p.m.)
Issued 29 years, 9 months ago (Nov. 1, 1995)
Published 29 years, 9 months ago (Nov. 1, 1995)
Published Online 29 years, 9 months ago (Nov. 1, 1995)
Published Print 29 years, 9 months ago (Nov. 1, 1995)
Funders 0

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@article{Serano_1995, title={A small predicted stem-loop structure mediates oocyte localization of Drosophila K10 mRNA}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.11.3809}, DOI={10.1242/dev.121.11.3809}, number={11}, journal={Development}, publisher={The Company of Biologists}, author={Serano, Thomas L. and Cohen, Robert S.}, year={1995}, month=nov, pages={3809–3818} }