RNA binding protein Sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation

Microbiology and Molecular Biology Reviews

Volumn 67, Issue 3, 2003, Pages 343-359

  Penalva, Luiz O F ^a   Sánchez, Lucas ^b  

^a DUKE UNIVERSITY   (United States)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA BINDING PROTEIN;

DROSOPHILA; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; GENETIC CODE; INSECT GENETICS; MALE; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; RNA SPLICING; RNA TRANSLATION; SEX DETERMINATION; SXL GENE;

AMINO ACID SEQUENCE; ANIMALS; DOSAGE COMPENSATION, GENETIC; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MALE; MOLECULAR SEQUENCE DATA; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEX DETERMINATION (GENETICS); TRANSCRIPTION, GENETIC;

ARACHNIDA; HEXAPODA; INSECTA;

EID: 0141789672     PISSN: 10922172     EISSN: None     Source Type: Journal    
DOI: 10.1128/MMBR.67.3.343-359.2003     Document Type: Review

References (136)

1. Albrecht, E. B., and H. K. Salz. 1993. The Drosophila sex determination gene snf is utilized for the establishment of the female-specific splicing pattern of Sex-lethal. Genetics 134:801-807.
2. Amrein, H., M. Gorman, and R. Nothiger. 1988. The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55:1025-1035.
3. Amrein, H. 2000. Multiple RNA-protein interactions in Drosophila dosage compensation. Genome Biol. 1:1030.1-1030.5.
4. Bachiller, D., and L. Sánchez. 1991. Production of XO clones in XX females of Drosophila. Genet. Res. 57:23-28.
5. Bashaw, G. J., and B. S. Baker. 1995. The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. Development 121:3245-3258.
6. Bashaw, G. J., and B. S. Baker. 1997. The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell 89:789-798.
7. Bell, L. R., E. M. Maine, P. Schedl, and T. W. Cline. 1988. Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similar to RNA binding proteins. Cell 55:1037-1046.
8. Bell, L. R., J. I. Horabin, P. Schedl, and T. W. Cline. 1991. Positive autoregulation of Sex-lethal, by alternative splicing maintains the female determined state in Drosophila. Cell 65:229-239.
9. Bernstein, M., and T. W. Cline. 1994. Differential effects of Sex-lethal mutations on dosage compensation early in Drosophila development. Genetics 136:1051-1061.
10. Blanchette, M., and B. Chabot. 1999. Modulation of exon skipping by high-affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J. 18:1939-1952.
11. Boggs, R. T., P. Gregor, S. Idriss, J. M. Belote, and M. McKeown. 1987. Regulation of sexual differentiation in D. melanogaster via alternative splicing of RNA from the transformer gene. Cell 50:739-747.
12. Bopp, D., L. R. Bell, T. W. Cline, and P. Schedl. 1991. Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev. 5:403-425.
13. Bopp, D., J. I. Horabin, R. A. Lersh, T. W. Cline, and P. Schedl. 1993. Expression of Sex-lethal gene is controlled at multiple levels during the Drosophila oogenesis. Development 118:797-812.
14. Bopp, D., G. Calhoun, J. I. Horabin, M. Samuels, and P. Schedl. 1996. Sex-specific control of Sex-lethal is a conserved mechanism for sex determination in the genus Drosophila. Development 122:971-982.
15. Bopp, D., C. Schutt, J. Puro, H. Huang, and R. Nothiger. 1999. Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene Sex-lethal. Development 126:5785-5794.
16. Brand, S., and H. M. Bourbon. 1993. The developmentally-regulated Drosophila gene rox8 encodes an RRM-type RNA binding protein structurally related to human TIA-1-type nucleolysins. Nucleic Acids Res. 21:3699-3704.
17. Burnette, J. M., A. R. Hatton, and A. J. Lopez. 1999. Trans-acting factors required for inclusion of regulated exons in the Ultrabithorax mRNAs of Drosophila melanogaster. Genetics 151:1517-1529.
18. Burtis, K. C., and B. S. Baker. 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997-1010.
19. Catteruccia, F., T. Nolan, T. G. Loukeris, C. Blass, C. Savakis, F. C. Kafatos, and A. Crisanti. 2000. Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405:959-962.
20. Chase, B. A., and B. S. Baker. 1995. A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics 139:1649-1661.
21. Chu, E., and C. J. Allegra. 1996. The role of thymidylate synthase as an RNA binding protein. Bioessays 18:191-198.
22. Cline, T. W. 1978. Two closely-linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90:683-698.
23. Cline, T. W. 1984. Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107:231-277.
24. Cline, T. W. 1986. A female specific lethal lesion in an X-linked positive regulator of the Drosophila sex determination gene Sex-lethal. Genetics 113:642-663.
25. Cline, T. W. 1993. The Drosophila sex determination signal: how do flies count to two? Trends Genet. 9:385-390.
26. + gene dose effects. Proc. Natl. Acad. Sci. USA 96:14451-14458.
27. Cline, T. W., and B. J. Meyer. 1996. Vive la difference: males vs females in flies vs worms. Annu. Rev. Genet. 30:637-702.
28. Cronmiller, C., and T. Cline. 1987. The Drosophila sex determination gene daughterless has different functions in the germ line versus the soma. Cell 48:479-487.
29. Dabeva, M. D., and J. R. Warner. 1993. Ribosomal protein L32 of Saccharomyces cerevisiae regulates both splicing and translation of its own transcript. J. Biol. Chem. 268:19669-19674.
30. Deshpande, G., G. Calhoun, and P.D. Schedl. 1999. The N-terminal domain of Sxl protein disrupts Sxl autoregulation in females and promotes female-specific splicing of tra in males. Development 126:2842-2853.
31. Finley, K. D., B. J. Taylor, M. Milstein, and M. McKeown. 1997. dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94:913-918.
32. Finley, K. D., P. T. Edeen, M. Foss, E. Gross, N. Ghbeish, R. H. Palmer, B. J. Taylor, and M. McKeown. 1998. dissatisfaction encodes a tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior. Neuron 21:1363-1374.
33. Flickinger, T. W., and H. K. Salz. 1994. The Drosophila sex determination gene snf encodes a nuclear protein with sequences and functional similarity to the mammalian U1A snRNP protein. Genes Dev. 8:914-925.
34. Forch, P., O. Puig, N. Kedersha, C. Martinez, S. Granneman, B. Seraphin, P. Anderson, and J. Valcárcel. 2000. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 6:1089-1098.
35. Forch, P., L. Merendino, C. Martinez, and J. Valcárcel. 2001. Modulation of msl-2 5′ splice site recognition by Sex-lethal. RNA 7:1185-1191.
36. Gebauer, F., L. Merendino, M. W. Hentze, and J. Valcárcel. 1998. The Drosophila splicing regulator Sex-lethal directly inhibits translation of male-specific-lethal 2 mRNA. RNA 4:142-150.
37. Gebauer, F., D. F. Corona, T. Preiss, P. B. Becker, and M. W. Hentze. 1999. Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 5′ and 3′ UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J. 18:6146-6154.
38. Gergen, J. P. 1987. Dosage compensation in Drosophila: evidence that Daughterless and Sex-lethal control X chromosome activity at the blastoderm stage of embryogenesis. Genetics 117:477-485.
39. Gorlich, D., M. Dabrowski, F. R. Bischoff, J. Kutay, P. Bork, E. Hartmann, S. Prehn, and E. Izaurralde. 1997. A novel class of RanGTP binding proteins. J. Cell Biol. 138:65-80.
40. Graham, P., J. K. Penn, and P. Schedl. 2003. Masters change, slaves remain. Bioessays 25:1-4.
41. Granadino, B., S. Campuzano, and L. Sánchez. 1990. The Drosophila melanogaster fl(2)d gene is needed for the female-specific splicing of Sex-lethal RNA. EMBO J. 9:2597-2602.
42. Granadino, B., A. B. San Juán, P, Santamaría, and L. Sánchez. 1992. Evidence of a dual function in fl(2)d a gene needed for Sex-lethal expression in Drosophila melanogaster. Genetics 130:597-612.
43. Granadino, B., P. Santamaria, and L. Sánchez. 1993. Sex determination in the germ line of Drosophila melanogaster: activation of the gene Sex-lethal. Development 118:813-816.
44. Granadino, B., L. O. F. Penalva, and L. Sánchez. 1996. The gene fl(2)d is needed for the sex-specific splicing of transformer pre-mRNA but not for double-sex pre-mRNA in Drosophila melanogaster. Mol. Gen. Genet. 253:26-31.
45. Granadino, B., L. O. F. Penalva, M. R. Green, J. Valcárcel, and L. Sánchez. 1997. Distinct mechanisms of splicing regulation in vivo by the Drosophila protein Sex-lethal. Proc. Natl. Acad. Sci. USA 94:7343-7348.
46. Hager, J. H., and T. W. Cline. 1997. Induction of female Sex-lethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. Development 124:5033-5048.
47. Harper, D. S., L. D. Fresco, and J. D. Keene. 1992. RNA binding specificity of a Drosophila snRNP protein that shares sequence homology with mammalian U1-A and U2-B″ proteins. Nucleic Acids Res. 20:3645-3650.
48. Hastie, N. D. 2001. Life, sex, and WT1 isoforms-three amino acids can make all the difference. Cell 106:391-394.
49. Heinrichs, V., L. C. Ryner, and B. S. Baker. 1998. Regulation of sex-specific selection of fruitless 5′ splice sites by Transformer and Transformer-2. Mol. Cell. Biol. 18:450-458.
50. Heintzen, C., M. Nater, K. Apel, and D. Staiger. 1997. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94:8515-8520.
51. Hilfiker, A., and R. Nöthiger. 1991. The temperature-sensitive mutation vir (virilizer) identifies a new gene involved in sex determination of Drosophila. Roux's Arch. Dev. Biol. 200:240-248.
52. Hilfiker, A., H. Amrein, A. Dübendorfer, and R. Nöthiger. 1995. The gene virilizer is required for female-specific splicing controlled by Sxl, the master gene for sexual development in Drosophila. Development 121:4017-4026.
53. Horabin, J. I., and P. Schedl. 1993. 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. 13:7734-7746.
54. Horabin, J., D. Bopp, J. Waterbury, and P. Schedl. 1995. Selection and maintenance of sexual identity in the Drosophila germline. Genetics 142:1521-1535.
55. Horabin, J. I., and P. Schedl. 1996. Splicing of the Drosophila Sex-lethal early transcripts involves exon skipping that is independent of Sex-lethal protein. RNA 2:1-10.
56. Hoshijima, K., K. Inoue, I. Higuchi, H. Sakamoto, and Y. Shimura. 1991. Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252:833-836.
57. Inoue, K., K. Hoshijima, H. Sakamoto, and Y. Shimura. 1990. Binding of the Drosophila Sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature 344:461-463.
58. Inoue, K., K. Hoshijima, I. Higuchi, H. Sakamoto, and Y. Shimura. 1992. Binding of the Drosophila transformer and transformer-2 proteins to the regulatory elements of doublesex primary transcript for sex-specific RNA processing. Proc. Natl. Acad. Sci. USA 89:8092-8096.
59. Irvine, D., C. Tuerk, and L. Gold. 1991. SELEXION. Systematic evolution of ligands by exponential enrichment with integrated optimization by nonlinear analysis. J. Mol. Biol. 222:739-761.
60. Ito, H., K. Fujitani, K. Usui, K. Shimizu-Nishikawa, S. Tanaka, and D. Yamamoto. 1996. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl. Acad. Sci. USA 93:9687-9692.
61. Kanaar, R., A. L. Lee, D. Z. Rudner, D. E. Wemmer, and D. C. Rio. 1995. Interaction of the Sex-lethal RNA binding domains with RNA. EMBO J. 14:4530-4539.
62. Kenan, D. J., C. C. Query, and J. D. Keene. 1991. RNA recognition: towards identifying determinants of specificity. Trends Biochem. Sci. 16:214-220.
63. Kelley, R. L., I. Solovyeva, L. M. Lyman, R. Richman, V. Solovyev, and M. I. Kuroda. 1995. Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81:867-877.
64. Kelley, R. L., J. Wang, L. Bell, and M. I. Kuroda. 1997. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387:195-199.
65. Kennedy, D., T. Ramsdale, J. Mattick, and M. Little. 1996. An RNA recognition motif in Wilms' tumour protein (WT1) revealed by structural modelling. Nat. Genet. 12:329-331.
66. Kennerdel, J. R., and R. W. Carthew. 1998. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95:1017-1026.
67. Keyes, L. N., T. W. Cline, and P. Schedl. 1992. The primary sex determination signal of Drosophila acts at the level of transcription. Cell 68:933-943.
68. Lallena, M. J., K. J. Chalmers, S. Llamazares, A. I. Lamond, and J. Valcárcel. 2002. Splicing regulation at the second catalytic step by Sex-lethal involves 3′ splice site recognition by SPF45. Cell 3:285-296.
69. Lee, S. B., and D. A. Haber. 2001. Wilms tumor and the WT1 gene. Exp. Cell Res. 264:74-99.
70. Le Hir, H., A. Nott, and M. J. Moore. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28:215-220.
71. Lisbin, M. J., J. Qiu, and K. White. 2001. The neuron-specific RNA-binding protein ELAV regulates neuroglian alternative splicing in neurons and binds directly to its pre-mRNA. Genes Dev. 15:2546-2561.
72. Little, N. A., N. D. Hastie, and R. C. Davies. 2000. Identification of WTAP, a novel Wilms' tumour 1-associating protein. Hum. Mol. Genet. 9:2231-2239.
73. Lu, S., and B. R. Cullen. 2003. Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA 9:618-630.
74. Lucchesi, J. C., and T. Skripsky. 1981. The link between dosage compensation and sex differentiation in Drosophila melanogaster. Chromosoma 82:217-227.
75. Meise, M., D. HilfikerKleiner, A. Dubendorfer, C. Brunner, R. Nothiger, and D. Bopp. 1998. Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125:1487-1494.
76. Merendino, L., S. Guth, D. Bilbao, C. Martinez, and J. Valcarcel. 1999. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3′ splice site AG. Nature 402:838-842.
77. Müller-Holtkamp, F. 1995. The Sex-lethal gene in Chrysomya rufifacies is highly conserved in sequence and exon-intron organization. J. Mol. Evol. 42:467-477.
78. Nagengast, A. A., S. M. Stitzinger, C. H. Tseng, S. M. Mount, and H. K. Salz. 2003. Sex-lethal splicing autoregulation in vivo: interactions between SEX-LETHAL, the U1 snRNP and U2AF underlie male exon skipping. Development 130:463-471.
79. Niessen, M., R. Schneiter, and R. Nothiger. 2001. Molecular identification of virilizer, a gene required for the expression of the sex-determining gene Sex-lethal in Drosophila melanogaster. Genetics 157:679-688.
80. Nöthiger, R., M. Jonglez, M. Leuthold, P. Meier-Gersch-Willer, and T. Weber. 1989. Sex determination in the germ line of Drosophila depends on genetic signals and inductive somatic factors. Development 107:505-518.
81. Oliver, B., N. Perrimon, and A. P. Mahowald. 1988. Genetic evidence that the sans-fille locus is involved in Drosophila sex determination. Genetics 120:159-171.
82. Oliver, B., Y. J. Kim, and B. S. Baker. 1993. Sex-lethal, master and slave: A hierarchy of germ line sex determination in Drosophila. Development 119:897-908.
83. Oliver, B. 2002. Genetic control of germline sexual dimorphism in Drosophila. Int. Rev. Cytol. 219:1-60.
84. O'Neil, M. T., and J. M. Belote. 1992. Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131:113-128.
85. Ortega, A., M. Niksic, A. Bachi, M. Wilm, L. Sanchez, N. Hastie, and J. Valcarcel. 2003. Biochemical function of female-lethal (2)D/Wilms' tumor suppressor-1-associated proteins in alternative pre-mRNA splicing. J. Biol. Chem. 278:3040-3047.
86. Pannuti, A., and J. C. Lucchesi. 2000. Recycling to remodel: evolution of dosage-compensation complexes. Curr. Opin. Genet. Dev. 10:644-650.
87. Pauli, D., B. Oliver, and A. Mahowald. 1993. The role of the ovarian tumor locus in Drosophila melanogaster germ line sex determination. Development 119:123-134.
88. Penalva, L. O. F., H. Sakamoto, A. NavarroSabate, E. Sakashita, B. A. Granadino, C. Segarra, and L. Sánchez. 1996. Regulation of the gene Sex-lethal: A comparative analysis of Drosophila melanogaster and Drosophila subobscura. Genetics 144:1653-1664.
89. Penalva, L. O. F., M. F. Ruiz, A. Ortega, B. Granadino, L. Vicente, C. Segarra, J. Valcárcel, and L. Sanchez. 2000. The Drosophila fl(2)d gene, required for female-specific splicing of Sxl and tra pre-mRNAs, encodes a novel nuclear protein with a HQ-rich domain. Genetics 155:129-139.
90. Penalva, L. O. F., M. J. Lallena, and J. Valcárcel. 2001. Switch in 3′ splice site recognition between exon definition and splicing catalysis is important for Sex-lethal autoregulation. Mol. Cell. Biol. 21:1986-1996.
91. Pultz, M. A., G. S. Carson, and B. S. Baker. 1994. A genetic analysis of hermaphrodite, a pleiotropic sex determination gene in Drosophila melanogaster. Genetics 136:195-207.
92. Pultz, M., and B. Baker. 1995. The dual role of hermaphrodite in the Drosophila sex determination regulatory hierarchy. Development 121:99-111.
93. Ryner, L. C., S. F. Goodwin, D. H. Castrillon, A. Anand, A. Villella, B. S. Baker, J. C. Hall, B. J. Taylor, and S. A. Wasserman. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079-1089.
94. Saccone, G., I. Peluso, D. Artiaco, E. Giordano, D. Bopp, and L. C. Polito. 1998. The Ceratitis capitata homologue of the Drosophila sex-determining gene Sex lethal is structurally conserved, but not sex-specifically regulated. Development 125:1495-1500.
95. Saccone, G., A. Pane, and L. C. Polito. 2002. Sex determination in flies, fruitflies and butterflies. Genetica 116:15-23.
96. Sakamoto, H., K. Inoue, I. Higuchi, Y. Ono, and Y. Shimura. 1992. Control of Drosophila Sex-lethal pre-mRNA splicing by its own female-specific product. Nucleic Acids Res. 20:5533-5540.
97. Sakashita, E., and H. Sakamoto. 1994. Characterization of RNA binding specificity of the Drosophila Sex-lethal protein by in vitro ligand selection. Nucleic Acids Res. 22:4082-4086.
98. Sakashita, E., and H. Sakamoto. 1996. Protein-RNA and protein-protein interactions of the Drosophila Sex-lethal mediated by its RNA-binding domains. J. Biochem. 120:1028-1033.
99. Salz, H. K., E. M. Maine, L. N. Keyes, M. E. Samuels, T. W. Cline, and P. Schedl. 1989. The Drosophila female-specific sex-determination gene, Sex-lethal, has stage-, tissue-, and sex-specific RNAs suggesting multiple modes of regulation. Genes Dev. 3:708-719.
100. Salz, H. K. 1992. The genetic analysis of snf: a Drosophila sex determination gene requires for activation of Sex-lethal in both the germline and the soma. Genetics 130:547-554.
101. Salz, H. K., and T. W. Flickinger. 1996. Both loss-of-function and gain-of-function mutations in snf define a role for snRNP proteins in regulating Sex-lethal pre-mRNA splicing in Drosophila development. Genetics 144:95-108.
102. Samuels, M., G. Deshpande, and P. Schedl. 1998. Activities of the Sex-lethal protein in RNA binding and protein:protein interactions. Nucleic Acids Res. 26:2625-2637.
103. Samuels, M. E., P. Schedl, and T. W. Cline. 1991. The complex set of late transcripts from the Drosophila sex determination gene Sex-lethal encodes multiple related polypeptides. Mol. Cell. Biol. 11:3584-3602.
104. Samuels, M. E., D. Bopp, R. A. Colvin, R. F. Roscigno, M. A. Garcia-Blanco, and P. Schedl. 1994. RNA binding by Sxl proteins in vitro and in vivo. Mol. Cell. Biol. 14:4975-4990.
105. Samson, M. L. 1998. Evidence for 3′ untranslated region-dependent autoregulation of the Drosophila gene encoding the neuronal nuclear RNA-binding protein ELAV. Genetics 150:723-733.
106. Sánchez, L., and R. Nöthiger. 1983. Sex determination and dosage compensation in Drosophila melanogaster. production of male clones in XX females. EMBO J. 2:485-491.
107. Sánchez, L., B. Granadino, and M. Torres. 1994. Sex determination in Drosophila melanogaster: X-linked genes involved in the initial step of Sex-lethal activation. Dev. Genet. 15:251-264.
108. Sánchez, L., P. López, and B. Granadino. 1998. Early events associated with sex determination in Drosophila melanogaster, p. 98-119. In R. Chatterjee and L. Sánchez (ed.), Genome analysis in eukaryotes: developmental and evolutionary aspects. Narosa Publishing House-Springer Verlag, New Delhi, India.
109. Schaeffer, C., B. Bardoni, J. L. Mandel, B. Ehresmann, C. Ehresmann, and H. Moine. 2001. The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20:4803-4813.
110. Schüpbach, T. 1985. Normal female germ cell differentiation requires the female X chromosome to autosome ratio and expression of Sex-lethal in Drosophila melanogaster. Genetics 109:529-548.
111. Schütt, C., A. Hilfiker, and R. Nothiger. 1998. Virilizer regulates Sex-lethal in the germline of Drosophila melanogaster. Development 125:1501-1507.
112. Schütt, C., and R. Nothiger. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development. 127:667-677.
113. Sievert, V., S. Kuhn, and W. Traut. 1997. Expression of the sex Determination cascade genes Sex-lethal and doublesex in the phorid fly Megaselia scalaris Genome 40:211-214.
114. Sievert, V., S. Kuhn, A. Paululat, and W. Traut. 2000. Sequence conservation and expression of the Sex-lethal homologue in the fly Megaselia scalaris. Genome 43:382-390.
115. Singh, R., J. Valcárcel, and M. R. Green. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268:1173-1176.
116. Sosnowski, B. A., J. M. Belote, and M. McKeown. 1989. Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell 58:449-459.
117. Starr, D. J., and T. W. Cline. 2002. A host parasite interaction rescues Drosophila oogenesis defects. Nature 428:76-79.
118. Steinmann-Zwicky, M. 1988. Sex determination in Drosophila: the X chromosomal gene liz is required for Sxl activity. EMBO J. 7:3889-3898.
119. Steinmann-Zwicky, M., H. Schmid, and R. Nöthiger. 1989. Cell-autonomous and inductive signals can determine the sex of the germ line of Drosophila by regulating the gene Sxl. Cell 57:157-166.
120. Steinmann-Zwicky, M. 1993. Sex determination in Drosophila: sis-b, a major numerator element of the X:A signal ratio in the soma, does not contribute to the X:A ratio in the germ line. Development 117:763-767.
121. Stuckenholz, C., Y. Kageyama, and M. I. Kuroda. 1999. Guilt by association: non-coding RNAs, chromosome-specific proteins and dosage compensation in Drosophila. Trends Genet. 15:454-458.
122. Tenenbaum, S. A., C. C. Carson, P. J. Lager, and J. D. Keene. 2000. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 97:14085-14090.
123. Tian, Q., M. Streuli, H. Saito, S. F. Schlossman, and P. Anderson. 1991. A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell 67:629-639.
124. Torres, M., and L. Sánchez. 1991. The sisterless-b function of the Drosophila gene scute is restricted to the state when the X:A ratio signal determines the activity of Sex-lethal. Development 113:715-722.
125. Tsai, D. E., D. S. Harper, and J. D. Keene. 1991. U1-snRNP-A protein selects a ten nucleotides consensus sequence from a degenerate RNA pool presented in various structural contexts. Nucleic Acids Res. 19:4931-4936.
126. Valcárcel, J., R. Singh, P. D. Zamore, and M. R. Green. 1993. The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362:171-175.
127. Vied, C., N. Halachmi, A. Salzberg, and J. I. Horabin. 2003. Antizyme is a target of Sex-lethal in the Drosophila germline and appears to act downstream of Hedgehog to regulate Sex-lethal and Cyclin B. Dev. Biol. 253:214-229.
128. Wang, J., and L. R. Bell. 1994. The Sex-lethal amino terminus mediates cooperative interactions in RNA binding and is essential for splicing regulation. Genes Dev. 8:2072-2085.
129. Wang, J., Z. Dong, and L. R. Bell. 1997. Sex-lethal interactions with protein and RNA. Roles of glycine-rich and RNA binding domains J. Biol. Chem. 272:22227-22235.
130. Waterbury, J. A., J. I. Horabin, D. Bopp, and P. Schedl. 2000. Sex determination in the Drosophila germline is dictated by the sexual identity of the surrounding soma. Genetics 155:1742-1756.
131. Wu, J., and J. Bag. 1998. Negative control of the poly(A)-binding protein mRNA translation is mediated by the adenine-rich region of its 5′-untranslated region. J. Biol. Chem. 273:34535-34542.
132. Yang, D., H. Lu, Y. Hong, T. Jinks, P. Estes, and J. Erickson. 2001. Interpretation of X chromosome dose at Sex-lethal requires non-E-box sites for the basic helix-loop-helix proteins SisB and Daughterless. Mol. Cell. Biol. 21:1581-1592.
133. Yanowitz, J. L., G. Deshpande, G. Calhoun, and P. D. Schedl. 1999. An N-terminal truncation uncouples the sex-transforming and dosage compensation functions of Sex-lethal. Mol. Cell. Biol. 19:3018-3028.
134. Zarkower, D. 2001. Establishing sexual dimorphism: conservation amidst diversity? Nat. Rev. Genet. 2:175-185.
135. Zhou, S., Y. Yang, M. J. Scott, A. Pannuti, K. C. Fehr, A. Eisen, E. V. Koonin, D. L. Fouts, R. Wrightsman, J. E. Manning, et al. 1995. Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J. 14:2884-2895.
136. Zhu, C., J. Urano, and L. R. Bell. 1997. The Sex-lethal early splicing pattern uses a default mechanism dependent on the alternative 5′ splice sites. Mol. Cell. Biol. 17:1674-1681.