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. 2000 Aug;155(4):1809–1819. doi: 10.1093/genetics/155.4.1809

The Drosophila cystoblast differentiation factor, benign gonial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles.

B Ohlstein 1, C A Lavoie 1, O Vef 1, E Gateff 1, D M McKearin 1
PMCID: PMC1461197  PMID: 10924476

Abstract

Selection of asymmetric cell fates can involve both intrinsic and extrinsic factors. Previously we have identified the bag-of-marbles (bam) gene as an intrinsic factor for cystoblast fate in Drosophila germline cells and shown that it requires active product from the benign gonial cell neoplasm (bgcn) gene. Here we present the cloning and characterization of bgcn. The predicted Bgcn protein is related to the DExH-box family of RNA-dependent helicases but lacks critical residues for ATPase and helicase functions. Expression of the bgcn gene is extremely limited in ovaries but, significantly, bgcn mRNA is expressed in a very limited number of germline cells, including the stem cells. Also, mutations in bgcn dominantly enhance a bam mutant phenotype, further corroborating the interdependence of these two genes' functions. On the basis of known functions of DExH-box proteins, we propose that Bgcn and Bam may be involved in regulating translational events that are necessary for activation of the cystoblast differentiation program.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aubourg S., Kreis M., Lecharny A. The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res. 1999 Jan 15;27(2):628–636. doi: 10.1093/nar/27.2.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BROWN E. H., KING R. C. STUDIES ON THE EVENTS RESULTING IN THE FORMATION OF AN EGG CHAMBER IN DROSOPHILA MELANOGASTER. Growth. 1964 Mar;28:41–81. [PubMed] [Google Scholar]
  4. Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
  5. Christerson L. B., McKearin D. M. orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev. 1994 Mar 1;8(5):614–628. doi: 10.1101/gad.8.5.614. [DOI] [PubMed] [Google Scholar]
  6. Cooley L., Verheyen E., Ayers K. chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell. 1992 Apr 3;69(1):173–184. doi: 10.1016/0092-8674(92)90128-y. [DOI] [PubMed] [Google Scholar]
  7. Curtis D., Treiber D. K., Tao F., Zamore P. D., Williamson J. R., Lehmann R. A CCHC metal-binding domain in Nanos is essential for translational regulation. EMBO J. 1997 Feb 17;16(4):834–843. doi: 10.1093/emboj/16.4.834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Forbes A., Lehmann R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development. 1998 Feb;125(4):679–690. doi: 10.1242/dev.125.4.679. [DOI] [PubMed] [Google Scholar]
  9. Gateff E. Gonial cell neoplasm of genetic origin affecting both sexes of drosophila melanogaster. Prog Clin Biol Res. 1982;85(Pt B):621–632. [PubMed] [Google Scholar]
  10. Gross C. H., Shuman S. The QRxGRxGRxxxG motif of the vaccinia virus DExH box RNA helicase NPH-II is required for ATP hydrolysis and RNA unwinding but not for RNA binding. J Virol. 1996 Mar;70(3):1706–1713. doi: 10.1128/jvi.70.3.1706-1713.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. King F. J., Lin H. Somatic signaling mediated by fs(1)Yb is essential for germline stem cell maintenance during Drosophila oogenesis. Development. 1999 May;126(9):1833–1844. doi: 10.1242/dev.126.9.1833. [DOI] [PubMed] [Google Scholar]
  12. Kiyatkin N., Dulubova I., Grishin E. Cloning and structural analysis of alpha-latroinsectotoxin cDNA. Abundance of ankyrin-like repeats. Eur J Biochem. 1993 Apr 1;213(1):121–127. doi: 10.1111/j.1432-1033.1993.tb17741.x. [DOI] [PubMed] [Google Scholar]
  13. Lavoie C. A., Ohlstein B., McKearin D. M. Localization and function of Bam protein require the benign gonial cell neoplasm gene product. Dev Biol. 1999 Aug 15;212(2):405–413. doi: 10.1006/dbio.1999.9346. [DOI] [PubMed] [Google Scholar]
  14. León A., McKearin D. Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Mol Biol Cell. 1999 Nov;10(11):3825–3834. doi: 10.1091/mbc.10.11.3825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lin H., Spradling A. C. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development. 1997 Jun;124(12):2463–2476. doi: 10.1242/dev.124.12.2463. [DOI] [PubMed] [Google Scholar]
  16. Lin H., Spradling A. C. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993 Sep;159(1):140–152. doi: 10.1006/dbio.1993.1228. [DOI] [PubMed] [Google Scholar]
  17. Lin H. The self-renewing mechanism of stem cells in the germline. Curr Opin Cell Biol. 1998 Dec;10(6):687–693. doi: 10.1016/s0955-0674(98)80108-7. [DOI] [PubMed] [Google Scholar]
  18. Lukacsovich T., Asztalos Z., Juni N., Awano W., Yamamoto D. The Drosophila melanogaster 60A chromosomal division is extremely dense with functional genes: their sequences, genomic organization, and expression. Genomics. 1999 Apr 1;57(1):43–56. doi: 10.1006/geno.1999.5746. [DOI] [PubMed] [Google Scholar]
  19. McKearin D. M., Spradling A. C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990 Dec;4(12B):2242–2251. doi: 10.1101/gad.4.12b.2242. [DOI] [PubMed] [Google Scholar]
  20. McKearin D., Ohlstein B. A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development. 1995 Sep;121(9):2937–2947. doi: 10.1242/dev.121.9.2937. [DOI] [PubMed] [Google Scholar]
  21. McKearin D. The Drosophila fusome, organelle biogenesis and germ cell differentiation: if you build it.... Bioessays. 1997 Feb;19(2):147–152. doi: 10.1002/bies.950190209. [DOI] [PubMed] [Google Scholar]
  22. Morrison S. J., Shah N. M., Anderson D. J. Regulatory mechanisms in stem cell biology. Cell. 1997 Feb 7;88(3):287–298. doi: 10.1016/s0092-8674(00)81867-x. [DOI] [PubMed] [Google Scholar]
  23. Pause A., Méthot N., Sonenberg N. The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol Cell Biol. 1993 Nov;13(11):6789–6798. doi: 10.1128/mcb.13.11.6789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. doi: 10.1016/b978-0-409-90042-2.50028-3. [DOI] [PubMed] [Google Scholar]
  25. Robinson D. N., Cooley L. Examination of the function of two kelch proteins generated by stop codon suppression. Development. 1997 Apr;124(7):1405–1417. doi: 10.1242/dev.124.7.1405. [DOI] [PubMed] [Google Scholar]
  26. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  27. Saraste M., Sibbald P. R., Wittinghofer A. The P-loop--a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 1990 Nov;15(11):430–434. doi: 10.1016/0968-0004(90)90281-f. [DOI] [PubMed] [Google Scholar]
  28. Schultz J., Milpetz F., Bork P., Ponting C. P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857–5864. doi: 10.1073/pnas.95.11.5857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sedgwick S. G., Smerdon S. J. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci. 1999 Aug;24(8):311–316. doi: 10.1016/s0968-0004(99)01426-7. [DOI] [PubMed] [Google Scholar]
  30. Sidén-Kiamos I., Saunders R. D., Spanos L., Majerus T., Treanear J., Savakis C., Louis C., Glover D. M., Ashburner M., Kafatos F. C. Towards a physical map of the Drosophila melanogaster genome: mapping of cosmid clones within defined genomic divisions. Nucleic Acids Res. 1990 Nov 11;18(21):6261–6270. doi: 10.1093/nar/18.21.6261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
  32. Stroumbakis N. D., Li Z., Tolias P. P. RNA- and single-stranded DNA-binding (SSB) proteins expressed during Drosophila melanogaster oogenesis: a homolog of bacterial and eukaryotic mitochondrial SSBs. Gene. 1994 Jun 10;143(2):171–177. doi: 10.1016/0378-1119(94)90093-0. [DOI] [PubMed] [Google Scholar]
  33. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wang C., Dickinson L. K., Lehmann R. Genetics of nanos localization in Drosophila. Dev Dyn. 1994 Feb;199(2):103–115. doi: 10.1002/aja.1001990204. [DOI] [PubMed] [Google Scholar]
  35. Wei W., Twell D., Lindsey K. A novel nucleic acid helicase gene identified by promoter trapping in Arabidopsis. Plant J. 1997 Jun;11(6):1307–1314. doi: 10.1046/j.1365-313x.1997.11061307.x. [DOI] [PubMed] [Google Scholar]
  36. Wharton R. P., Sonoda J., Lee T., Patterson M., Murata Y. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell. 1998 May;1(6):863–872. doi: 10.1016/s1097-2765(00)80085-4. [DOI] [PubMed] [Google Scholar]
  37. Wieschaus E., Szabad J. The development and function of the female germ line in Drosophila melanogaster: a cell lineage study. Dev Biol. 1979 Jan;68(1):29–46. doi: 10.1016/0012-1606(79)90241-0. [DOI] [PubMed] [Google Scholar]
  38. Xie T., Spradling A. C. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell. 1998 Jul 24;94(2):251–260. doi: 10.1016/s0092-8674(00)81424-5. [DOI] [PubMed] [Google Scholar]
  39. Zaccai M., Lipshitz H. D. Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote. 1996 May;4(2):159–166. doi: 10.1017/s096719940000304x. [DOI] [PubMed] [Google Scholar]
  40. Zhang S., Grosse F. Domain structure of human nuclear DNA helicase II (RNA helicase A). J Biol Chem. 1997 Apr 25;272(17):11487–11494. doi: 10.1074/jbc.272.17.11487. [DOI] [PubMed] [Google Scholar]
  41. de Cuevas M., Lilly M. A., Spradling A. C. Germline cyst formation in Drosophila. Annu Rev Genet. 1997;31:405–428. doi: 10.1146/annurev.genet.31.1.405. [DOI] [PubMed] [Google Scholar]
  42. de la Cruz J., Kressler D., Linder P. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci. 1999 May;24(5):192–198. doi: 10.1016/s0968-0004(99)01376-6. [DOI] [PubMed] [Google Scholar]

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