Sex determination in Drosophila: The view from the top

Fly

Volumn 4, Issue 1, 2010, Pages 60-70

  Salz, Helen K ^a   Erickson, James W ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Alternative splicing; Dosage compensation; RNA binding proteins; Sexual dimorphism; Transcriptional activation; Translational regulation; X: A ratio; XSE

Indexed keywords

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 77952617125     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.4.1.11277     Document Type: Article

References (109)

1. Bridges CB. Non-Disjunction as Proof of the Chromosome Theory of Heredity. Genetics 1916; 1:107-63.
2. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, et al. FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 2009; 37:555-9.
3. Bell LR, Maine EM, Schedl P, Cline T.W. Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell 1988; 55:1037-46.
4. Salz HK, Maine EM, Keyes LN, Samuels ME, Cline T W, Schedl P. The Drosophila female-specific sex determination gene, Sex-lethal, has stage-, tissueand sex-specific R NAs suggesting multiple modes of regulation. Genes Dev 1989; 3:708-19.
5. Samuels ME, Schedl P, Cline TW. The complex set of late transcripts from the Drosophila sex determination gene Sex-lethal encodes multiple related polypeptides. Mol Cell Biol 1991; 11:3584-602.
6. Clery A, Blatter M, Allain FH. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 2008; 18:290-8.
7. Singh R, Valcarcel J, Green MR. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 1995; 268:1173-6.
8. Robida MD, Rahn A, Singh R. Genome-wide identification of alternatively spliced mRNA targets of specific RNA-binding proteins. PLoS ONE. 2007; 2:520.
9. Cline TW. Evidence that sisterless-a and sisterless-b are two of several discrete "numerator elements" of the X/A sex determination signal in Drosophila that switch Sxl between two alternative stable expression states. Genetics 1988; 119:829-62.
10. Duffy JB, Gergen JP. The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev 1991; 5:2176-87.
11. Jinks TM, Polydorides AD, Calhoun G, Schedl P. The JAK/STAT signaling pathway is required for the initial choice of sexual identity in Drosophila melanogaster. Mol Cell 2000; 5:581-7.
12. Sanchez L, Granadino B, Torres M. Sex determination in Drosophila melanogaster: X-linked genes involved in the initial step of Sex-lethal activation. Dev Genet 1994; 15:251-64.
13. Sefton L, Timmer JR, Zhang Y, Beranger F, Cline TW. An extracellular activator of the Drosophila JAK/STAT pathway is a sex-determination signal element. Nature 2000; 405:970-3.
14. Yang D, Lu H, Hong Y, Jinks TM, Estes PA, Erickson JW. Interpretation of X chromosome dose at Sexlethal requires non-E-box sites for the basic helixloop-helix proteins SISB and Daughterless. Mol Cell Biol 2001; 21:1581-92.
15. Erickson JW, Cline TW. A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev 1993; 7:1688-702.
16. Kramer SG, Jinks TM, Schedl P, Gergen JP. Direct activation of Sex-lethal transcription by the Drosophila Runt protein. Development 1999; 126:191-200.
17. Avila FW, Erickson JW. Drosophila JAK /STAT pathway reveals distinct initiation and reinforcement steps in early transcription of Sxl. Curr Biol 2007; 17: 643-8.
18. Barbash DA, Cline TW. Genetic and molecular analysis of the autosomal component of the primary sex determination signal of Drosophila melanogaster. Genetics 1995; 141:1451-71.
19. Erickson JW, Quintero JJ. Indirect effects of ploidy suggest X chromosome dose, not the X: A ratio, signals sex in Drosophila. PLoS Biol 2007; 5:332.
20. Lu H, Kozhina E, Mahadevaraju S, Yang D, Avila FW, Erickson JW. Maternal Groucho and bHLH repressors amplify the dose-sensitive X chromosome signal in Drosophila sex determination. Dev Biol 2008; 323:248-60.
21. Estes PA, Keyes LN, Schedl P. Multiple response elements in the Sex-lethal early promoter ensure its female-specific expression pattern. Mol Cell Biol 1995; 15:904-17.
22. Keyes LN, Cline TW, Schedl P. The primary sexdetermination signal of Drosophila acts at the level of transcription. Cell 1992; 68:933-43.
23. Barolo S, Levine M. hairy mediates dominant repression in the Drosophila embryo. EMBO J 1997; 16:2883-91.
24. Chen G, Courey AJ. Groucho/TLE family proteins and transcriptional repression. Gene 2000; 249:1-16.
25. Payankaulam S, Arnosti DN. Groucho corepressor functions as a cofactor for the Knirps short-range transcriptional repressor. Proc Natl Acad Sci USA 2009; 106:17314-9.
26. Sekiya T, Zaret KS. Repression by Groucho/TLE/ Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol Cell 2007; 28:291-303.
27. Buscarlet M, Stifani S. The 'Marx' of Groucho on development and disease. Trends Cell Biol 2007; 17:353-61.
28. Fischer A, Gessler M. Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res 2007; 35:4583-96.
29. Younger-Shepherd S, Vaessin H, Bier E, Jan LY, Jan Y N. deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell 1992; 70:1-20.
30. Bridges CB. Haploid Drosophila and the theory of genic balance. Science 1930; 72:405-6.
31. Bridges CB. Triploid intersexes in Drosophila melanogaster. Science 1921; 54:252-4.
32. Bridges CB. Haploidy in Drosophila Melanogaster. Proc Natl Acad Sci USA 1925; 11:706-10.
33. Wrischnik LA, Timmer JR, Megna LA, Cline TW. Recruitment of the proneural gene scute to the Drosophila sex-determination pathway. Genetics 2003; 165:2007-27.
34. Cline TW. The Drosophila sex determination signal: how do f lies count to two? Trends in Genetics 1993; 9:385-90.
35. Edgar BA, Kiehle CP, Schubiger G. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 1986; 44:365-72.
36. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development 2009; 136:3033-42.
37. Gonzalez AN, Lu H, Erickson JW. A shared enhancer controls a temporal switch between promoters during Drosophila primary sex determination. Proc Natl Acad Sci USA 2008; 105:18436-41.
38. Bernstein M, Lersch R A, Subrahmanyan L, Cline T W. Transposon insertions causing constitutive Sex-lethal activity in Drosophila melanogaster affect Sxl sex-specific transcript splicing. Genetics 1995; 139: 631-48.
39. Louis M, Holm L, Sanchez L, Kaufman M. A theoretical model for the regulation of Sex-lethal, a gene that controls sex determination and dosage compensation in Drosophila melanogaster. Genetics 2003; 165:1355-84.
40. Cline T W. Autoregulator y functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 1984; 107:231-77.
41. Bell LR, Horabin JI, Schedl P, Cline TW. Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 1991; 65:229-39.
42. Horabin JI, Schedl P. Regulated splicing of the Drosophila Sex-lethal male exon involves a blockage mechanism. Mol Cell Biol 1993; 13:1408-14.
43. Horabin JI, Schedl P. Sex-lethal autoregulation requires multiple cis-acting elements upstream and downstream of the male exon and appears to depend largely on controlling the use of the male exon 5' splice site. Mol Cell Biol 1993; 13:7734-46.
44. Flickinger TW, Salz HK. The Drosophila sex determination gene snf encodes a nuclear protein with sequence and functional similarity to the mammalian U1A snRNP protein. Genes Dev 1994; 8:914-25.
45. Nagengast A A, Stitzinger SM, Tseng C-H, Mount SM, Salz HK. Sex-lethal splicing autoregulation in vivo: interactions between SEX-LETHAL, the U1 snRNP and U2AF underlie male exon skipping. Development 2003; 130:463-71.
46. Johnson ML, Nagengast A A, Salz HK. PPS, a large multidomain protein, functions with Sex-lethal to regulate alternative splicing in Drosophila. PLoS Genetics 2010; in press.
47. Lallena MJ, Chalmers KJ, Llamazares S, Lamond AI, Valcarcel J. Splicing Regulation at the Second Catalytic Step by Sex-lethal Involves 3' Splice Site Recognition by SPF45. Cell 2002; 109:285-96.
48. Chaouki AS, Salz HK. Drosophila SPF45: a bifunctional protein with roles in both splicing and DNA repair. PLoS Genetics 2006; 2:178.
49. Wahl MC, Will CL, Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18.
50. Herold N, Will CL, Wolf E, Kastner B, Urlaub H, Luhrmann R. Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol Cell Biol 2009; 29:281-301.
51. Siera SG, Cline TW. Sexual back talk with evolutionary implications: stimulation of the Drosophila sex-determination gene Sex-lethal by its target transformer. Genetics 2008; 180:1963-81.
52. Allemand E, Batsche E, Muchardt C. Splicing, transcription and chromatin: a menage a trois. Curr Opin Genet Dev 2008; 18:145-51.
53. Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 2009; 10:741-54.
54. Horabin JI, Walthall S, Vied C, Moses M. A positive role for Patched in Hedgehog signaling revealed by the intracellular trafficking of Sex-lethal, the Drosophila sex determination master switch. Development 2003; 130:6101-9.
55. Vied C, Horabin JI. The sex determination master switch, Sex-lethal, responds to Hedgehog signaling in the Drosophila germline. Development 2001; 128:2649-60.
56. Horabin JI. Splitting the Hedgehog signal: sex and patterning in Drosophila. Development 2005; 132:4801-10.
57. Yanowitz JL, Deshpande G, Calhoun G, Schedl PD. An N-terminal truncation uncouples the sextransforming and dosage compensation functions of Sex-lethal. Mol Cell Biol 1999; 19:3018-28.
58. Wang Z, Lin H. Sex-lethal is a target of Brunomediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis. Dev Biol 2007; 302:160-8.
59. Sosnowski BA, Belote JM, McKeown M. Sex-specific aternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell 1989; 3:449-59.
60. Valcarcel J, Singh R, Zamore PD, Green MR. The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 1993; 362:171-5.
61. Deshpande G, Calhoun G, Schedl PD. The N-terminal domain of Sxl protein disrupts Sxl autoregulation in females and promotes female-specific splicing of tra in males. Development 1999; 126:2841-53.
62. Ortega A, Niksic M, Bachi A, Wilm M, Sanchez L, Hastie N, Valcarcel J. Biochemical function of female-lethal (2)D/Wilms' tumor suppressor-1associated proteins in alternative pre-mRNA splicing. J Biol Chem 2003; 278:3040-7.
63. Bashaw GJ, Baker BS. The regulation of the Drosophila msl-2 gene reveals a function for Sexlethal in translational control. Cell 1997; 89:789-98.
64. Kelley R L, Wang J, Bell L, Kuroda MI. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 1997; 387:195-9.
65. Gebauer F, Merendino L, Hentze MW, Valcarcel J. The Drosophila splicing regulator Sex-lethal directly inhibits translation of male-specific-lethal-2 mRNA. Rna 1998; 4:142-50.
66. Merendino L, Guth S, Bilbao D, Martinez C, Valcarcel J. Inhibition of msl-2 splicing by Sex-lethal reveals interction between U2AF35 and the 3' splice site AG. Nature 1999; 402:838-41.
67. Forch P, Merendino L, Martinez C, Valcarcel J. Modulation of msl-2 5' splice site recognition by Sexlethal. Rna 2001; 7:1185-91.
68. Beckmann K, Grskovic M, Gebauer F, Hentze MW. A dual inhibitory mechanism restricts msl-2 mRNA translation for dosage compensation in Drosophila. Cell 2005; 122:529-40.
69. Abaza I, Coll O, Patalano S, Gebauer F. Drosophila UNR is required for translational repression of male-specific lethal 2 mRNA during regulation of X-chromosome dosage compensation. Genes Dev 2006; 20:380-9.
70. Duncan K, Grskovic M, Strein C, Beckmann K, Niggeweg R, Abaza I, et al. Sex-lethal imparts a sexspecific function to UNR by recruiting it to the msl-2 mRNA 3' UTR: translational repression for dosage compensation. Genes Dev 2006; 20:368-79.
71. Patalano S, Mihailovich M, Belacortu Y, Paricio N, Gebauer F. Dual sex-specific functions of Drosophila Upstream of N-ras in the control of X chromosome dosage compensation. Development 2009; 136: 689-98.
72. Hunt SL, Hsuan JJ, Totty N, Jackson RJ. unr, a cellular cytoplasmic RNA-binding protein with five cold-shock domains, is required for internal initiation of translation of human rhinovirus RNA. Genes Dev 1999; 13:437-48.
73. Chang TC, Yamashita A, Chen CY, Yamashita Y, Zhu W, Durdan S, et al. UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant. Genes Dev 2004; 18:2010-23.
74. Patel GP, Ma S, Bag J. The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex. Nucleic Acids Res 2005; 33:7074-89.
75. Duncan KE, Strein C, Hentze MW. The SXLUNR corepressor complex uses a PABP-mediated mechanism to inhibit ribosome recruitment to msl-2 mRNA. Mol Cell 2009; 36:571-82.
76. Kopp A, Graze R M, Xu S, Carroll SB, Nuzhdin SV. Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 2003; 163:771-87.
77. Penn JK, Schedl P. The master switch gene sexlethal promotes female development by negatively regulating the N-signaling pathway. Dev Cell 2007; 12:275-86.
78. Hartenstein V, Posakony JW. A dual function of the Notch gene in Drosophila sensillum development. Dev Biol 1990; 142:13-30.
79. Gawande B, Robida MD, Rahn A, Singh R. Drosophila Sex-lethal protein mediates polyadenylation switching in the female germline. EMBO J 2006; 25:1263-72.
80. Kelley R.L., Solovyeva I, Lyman LM, Richman R, Solovyev V, Kuroda MI. Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 1995; 81:867-77.
81. Gergen JP. Dosage compensation in Drosophila: evidence that daughterless and Sex-lethal control X chromosome activity at the blastoderm stage of embryogenesis. Genetics 1987; 117:477-85.
82. Franke A, Dernburg A, Bashaw GJ, Baker BS. Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development 1996; 122:2751-60.
83. Rastelli L, Richman R, Kuroda MI. The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev 1995; 53:223-33.
84. Schupbach T. Normal female germ cell differentiation requires the female X chromosome to autosome ratio and expression of sex-lethal in Drosophila melanogaster. Genetics 1985; 109:529-48.
85. Hager JH, Cline TW. Induction of female Sexlethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. Development 1997; 124:5033-48.
86. Dansereau DA, Lasko P. The development of germline stem cells in Drosophila. Methods Mol Biol 2008; 450:3-26.
87. Staab S, Steinmann-Zwicky M. Somatic sex-determining signals act on X X germ cells in Drosophila embryos. Development 1996; 122:4065-71.
88. Janzer B, Steinmann-Zwicky M. Cell-autonomous and somatic signals control sex-specific gene expression in XY germ cells of Drosophila. Mech Dev 2001; 100:3-13.
89. Wawersik M, Milutinovich A, Casper AL, Matunis E, Williams B, Van Doren M. Somatic control of germline sexual development is mediated by the JAK/ STAT pathway. Nature 2005; 436:563-7.
90. Casper AL, Van Doren M. The establishment of sexual identity in the Drosophila germline. Development 2009; 136:3821-30.
91. Oliver B, Kim Y-J, Baker BS. Sex-lethal, master and slave: A hierarchy of germline sex determination in Drosophila. Development 1993; 119:897-908.
92. Waterbury JA, Horabin JI, Bopp D, Schedl P. Sex determination in the Drosophila germline is dictated by the sexual identity of the surrounding soma. Genetics 2000; 155:1741-56.
93. Bopp D, Bell LR, Cline TW, Schedl P. Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev 1991; 5:403-15.
94. Horabin JI, Bopp D, Waterbury J, Schedl P. Selection and maintenance of sexual identity in the Drosophila germline. Genetics 1995; 141:1521-35.
95. Cook KR. Regulation of recombination and oogenesis by the ovarian tumor, Sex-lethal and ovo genes of Drosophila melanogaster. 1993; Ph.D. Thesis, University of Iowa, Iowa City IA.
96. Bopp D, Schutt C, Puro J, Huang H, Nothiger R. Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene Sex-lethal. Development 1999; 126:5785-94.
97. Sun S, Cline TW. Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila. Genetics 2009; 181:1291-301.
98. Wei G, Oliver B, Pauli B, Mahowald AP. Evidence for sex transformation of germline cells in ovarian tumor mutants of Drosophila. Dev Biol 1994; 161:318-20.
99. Chau J, Kulnane LS, Salz HK. Sex-lethal facilitates the transition from germline stem cell to committed daughter cell in the Drosophila ovary. Genetics 2009; 182:121-32.
100. Li Y, Minor NT, Park JK, McKearin DM, Maines JZ. Bam and Bgcn antagonize Nanos-dependent germline stem cell maintenance. Proc Natl Acad Sci USA 2009; 106:9304-9.
101. Parisi MJ, Deng W, Wang Z, Lin H. The arrest gene is required for germline cyst formation during Drosophila oogenesis. Genesis 2001; 29:196-209.
102. Sugimura I, Lilly MA. Bruno inhibits the expression of mitotic cyclins during the prophase I meiotic arrest of Drosophila oocytes. Dev Cell 2006; 10:127-35.
103. Sanchez L. Sex-determining mechanisms in insects. Int J Dev Biol 2008; 52:837-56.
104. Hinman MN, Lou H. Diverse molecular functions of Hu proteins. Cell Mol Life Sci 2008; 65:3168-81.
105. Horabin JI, Schedl P. Splicing of the Drosophila Sex-lethal early transcripts involves exon skipping that is independent of Sex-lethal protein. RNA 1996; 2:1-10.
106. Zhu C, Urano J, Bell LR. The Sex-lethal early splicing pattern uses a default mechanism dependent on the alternative 5' splice sites. Mol Cell Biol 1997; 17:1674-81.
107. Salz HK, Mancebo RSY, Nagengast A A, Speck O, Psotka M, Mount SM. The Drosophila U1-70K protein is required for viability, but its arginine-rich domain is dispensable. Genetics 2004; 168:2059-65.
108. Penn JK, Graham P, Deshpande G, Calhoun G, Chaouki AS, Salz HK, Schedl P. Functioning of the Drosophila Wilms'-tumor-1-associated protein homolog, Fl(2)d, in Sex-lethal-dependent alternative splicing. Genetics 2008; 178:737-48.
109. Niessen M, Schneiter R, Nothiger R. Molecular identification of virilizer, a gene required for the expression of the sex-determining gene Sex-lethal in Drosophila melanogaster. Genetics 2001; 157: 679-88.