Distinct regulatory programs establish widespread sex-specific alternative splicing in Drosophila melanogaster

RNA

Volumn 17, Issue 3, 2011, Pages 453-468

  Hartmann, Britta ^a,b,c   Castelo, Robert ^b,d   Miñana, Belén ^a,b   Peden, Erin ^e   Blanchette, Marco ^f,h   Rio, Donald C ^f   Singh, Ravinder ^e   Valcárcel, Juan ^a,g  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSITY OF FREIBURG   (Germany)

^d INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^e UNIVERSITY OF COLORADO   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^h STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Alternative splicing; Drosophila; Hrp40; Sex

Indexed keywords

RNA BINDING PROTEIN; SEX LETHAL PROTEIN; TRANSFORMER PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; BIOINFORMATICS; DROSOPHILA MELANOGASTER; FEMALE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; SEX DIFFERENTIATION;

ALTERNATIVE SPLICING; ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GENES, REGULATOR; MALE; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA-BINDING PROTEINS; SEX FACTORS;

DROSOPHILA MELANOGASTER;

EID: 79951529353     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2460411     Document Type: Article

References (80)

1. Anne J, Ollo R, Ephrussi A, Mechler BM. 2007. Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila. Development 134: 137-146. (Pubitemid 46152714)
2. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
3. Baker BS. 1989. Sex in flies: the splice of life. Nature 340: 521-524.
4. Baker BS, Ridge KA. 1980. Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94: 383-423.
5. Baker BS, Burtis K, Goralski T, Mattox W, Nagoshi R. 1989. Molecular genetic aspects of sex determination in Drosophila melanogaster. Genome 31: 638-645.
6. Bashaw GJ, Baker BS. 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.
7. Bell LR, Horabin JI, Schedl P, Cline TW. 1991. Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65: 229-239. (Pubitemid 121006054)
8. Ben-Dov C, Hartmann B, Lundgren J, Valcarcel J. 2008. Genome-wide analysis of alternative pre-mRNA splicing. J Biol Chem 283: 1229-1233.
9. Blanchette M, Green RE, Brenner SE, Rio DC. 2005. Global analysis of positive and negative pre-mRNA splicing regulators in Drosophila. Genes Dev 19: 1306-1314. (Pubitemid 41003020)
10. Blanchette M, Green RE, MacArthur S, Brooks AN, Brenner SE, Eisen MB, Rio DC. 2009. Genome-wide analysis of alternative pre-mRNA splicing and RNA-binding specificities of the Drosophila hnRNP A/B family members. Mol Cell 33: 438-449.
11. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y. 2010. Sex-specific and lineage-specific alternative splicing in primates. Genome Res 20: 180-189.
12. Blencowe B, Brenner S, Hughes T, Morris Q. 2009. Post-transcriptional gene regulation: RNA-protein interactions, RNA processing, mRNA stability and localization. Pac Symp Biocomput 2009: 545-548.
13. Bopp D, Calhoun G, Horabin JI, Samuels M, Schedl P. 1996. Sex-specific control of Sex-lethal is a conserved mechanism for sex determination in the genus Drosophila. Development 122: 971-982.
14. Burtis KC, Baker BS. 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997-1010.
15. Calarco JA, Xing Y, Caceres M, Calarco JP, Xiao X, Pan Q, Lee C, Preuss TM, Blencowe BJ. 2007. Global analysis of alternative splicing differences between humans and chimpanzees. Genes Dev 21: 2963-2975. (Pubitemid 350133443)
16. Chapman T. 2001. Seminal fluid-mediated fitness traits in Drosophila. Heredity 87: 511-521. (Pubitemid 34067638)
17. Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10: 741-754.
18. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, Hemmings BA, Dixon JE. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci 97: 6499-6503. (Pubitemid 30412742)
19. Cline TW. 1984. Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107: 231-277. (Pubitemid 14079518)
20. Cline TW. 1993. The Drosophila sex determination signal: how do flies count to two? Trends Genet 9: 385-390.
21. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R. 2008. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452: 473-477. (Pubitemid 351450846)
22. Ellegren H, Parsch J. 2007. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8: 689-698. (Pubitemid 47281991)
23. Forch P, Valcarcel J. 2003. Splicing regulation in Drosophila sex determination. Prog Mol Subcell Biol 2003: 127-151.
24. Forch P, Merendino L, Martinez C, Valcarcel J. 2001. Modulation of msl-2 5′ splice site recognition by Sex-lethal. RNA 7: 1185-1191. (Pubitemid 32831349)
25. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80. doi: 10.1184/gb-2004-5-10-r80.
26. Gonsalvez GB, Rajendra TK, Tian L, Matera AG. 2006. The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance. Curr Biol 16: 1077-1089. (Pubitemid 43815752)
27. Hartmann B, Castelo R, Blanchette M, Boue S, Rio DC, Valcarcel J. 2009. Global analysis of alternative splicing regulation by insulin and wingless signaling in Drosophila cells. Genome Biol 10: R11. doi: 10.1186/gb-2009-10-1- r11.
28. Heinrichs V, Ryner LC, Baker BS. 1998. Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer- 2. Mol Cell Biol 18: 450-458.
29. Hughes TA. 2006. Regulation of gene expression by alternative untranslated regions. Trends Genet 22: 119-122. (Pubitemid 43290014)
30. Inoue K, Hoshijima K, Sakamoto H, Shimura Y. 1990. Binding of the Drosophila Sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature 344: 461-463.
31. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
32. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. 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 93: 9687-9692. (Pubitemid 26296670)
33. Kelley RL, Wang J, Bell L, Kuroda MI. 1997. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387: 195-199. (Pubitemid 27209436)
34. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006. (Pubitemid 34662293)
35. Khusial PR, Vaidya K, Zieve GW. 2005. The symmetrical dimethylarginine post-translational modification of the SmD3 protein is not required for snRNP assembly and nuclear transport. Biochem Biophys Res Commun 337: 1119-1124. (Pubitemid 41509192)
36. Kim E, Magen A, Ast G. 2007. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res 35: 125-131. (Pubitemid 46189837)
37. Lallena MJ, Chalmers KJ, Llamazares S, Lamond AI, Valcarcel J. 2002. Splicing regulation at the second catalytic step by Sexlethal involves 3′ splice site recognition by SPF45. Cell 109: 285-296. (Pubitemid 34606872)
38. Lasko P. 2000. The Drosophila melanogaster genome: translation factors and RNA binding proteins. J Cell Biol 150: F51-F56. (Pubitemid 30491346)
39. Lee S, Nahm M, Lee M, Kwon M, Kim E, Zadeh AD, Cao H, Kim HJ, Lee ZH, Oh SB, et al. 2007. The F-actin-microtubule crosslinker Shot is a platform for Krasavietz-mediated translational regulation of midline axon repulsion. Development 134: 1767-1777. (Pubitemid 46796573)
40. Liu H, Kubli E. 2003. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci 100: 9929-9933. (Pubitemid 37087045)
41. Louis M, Holm L, Sánchez L, Kaufman M. 2003. A theoretical model for the regulation of Sex-lethal, a gene that controls sex determination and dosage compensation in Drosophila melanogaster. Genetics 165: 1355-1384. (Pubitemid 38020255)
42. McGlincy NJ, Smith CW. 2008. Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem Sci 33: 385-393.
43. McIntyre LM, Bono LM, Genissel A, Westerman R, Junk D, Telonis- Scott M, Harshman L, Wayne ML, Kopp A, Nuzhdin SV. 2006. Sex-specific expression of alternative transcripts in Drosophila. Genome Biol 7: R79. doi: 10.1186/gb-2006-7-8-r79.
44. McKeown M, Madigan SJ. 1992. Sex determination and differentiation in invertebrates: Drosophila and Caenorhabditis elegans. Curr Opin Cell Biol 4: 948-954.
45. Merendino L, Guth S, Bilbao D, Martinez C, Valcarcel J. 1999. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3′ splice site AG. Nature 402: 838-841.
46. Mount SM, Salz HK. 2000. Pre-messenger RNA processing factors in the Drosophila genome. J Cell Biol 150: F37-F44.
47. Nagengast AA, Stitzinger SM, Tseng CH, Mount SM, Salz HK. 2003. Sex-lethal splicing autoregulation in vivo: interactions between SEX-LETHAL, the U1 snRNP and U2AF underlie male exon skipping. Development 130: 463-471. (Pubitemid 36231266)
48. Nagoshi RN, McKeown M, Burtis KC, Belote JM, Baker BS. 1988. The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 53: 229-236.
49. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
50. Pan Q, Shai O, Misquitta C, Zhang W, Saltzman AL, Mohammad N, Babak T, Siu H, Hughes TR, Morris QD, et al. 2004. Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Mol Cell 16: 929-941. (Pubitemid 40018403)
51. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
52. Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, Lu J, Doctolero M, Vainer M, Chan C, Malley J, et al. 2004. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol 5: R40. doi: 10.1186/gb-2004-5-6-r40.
53. Park JW, Parisky K, Celotto AM, Reenan RA, Graveley BR. 2004. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc Natl Acad Sci 101: 15974-15979. (Pubitemid 39507912)
54. Penalva LO, Sanchez L. 2003. RNA binding protein Sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67: 343-359. (Pubitemid 37122524)
55. Penn JK, Graham P, Deshpande G, Calhoun G, Chaouki AS, Salz HK, Schedl P. 2008. Functioning of the Drosophila Wilms'-tumor- 1-associated protein homolog, Fl(2)d, in Sex-lethal-dependent alternative splicing. Genetics 178: 737-748. (Pubitemid 351398788)
56. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi: 10.1093/nar/29.9.e45.
57. Pfreundt U, James DP, Tweedie S, Wilson D, Teichmann SA, Adryan B. 2010. FlyTF: improved annotation and enhanced functionality of the Drosophila transcription factor database. Nucleic Acids Res 38: D443-D447.
58. Polycarpou-Schwarz M, Gunderson SI, Kandels-Lewis S, Seraphin B, Mattaj IW. 1996. Drosophila SNF/D25 combines the functions of the two snRNP proteins U1A and U2B′ that are encoded separately in human, potato, and yeast. RNA 2: 11-23. (Pubitemid 26371308)
59. Ribeiro C, Dickson BJ. 2010. Sex peptide receptor and neuronal TOR/ S6K signaling modulate nutrient balancing in Drosophila. Curr Biol 20: 1000-1005.
60. RobidaMD, Rahn A, Singh R. 2007. Genome-wide identification of alternatively spliced mRNA targets of specific RNA-binding proteins. PLoS ONE 2: e520. doi: 10.1371/journal.pone.0000520.
61. Ryner LC, Baker BS. 1991. Regulation of doublesex pre-mRNA processing occurs by 3′-splice site activation. Genes Dev 5: 2071-2085.
62. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
63. Salz HK, Flickinger TW. 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.
64. Schupbach T, Wieschaus E. 1986. Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113: 443-448. (Pubitemid 16074695)
65. Schutt C, Nothiger R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127: 667-677. (Pubitemid 30129014)
66. Silver JD, Ritchie ME, Smyth GK. 2009. Microarray background correction: maximum likelihood estimation for the normal-exponential convolution. Biostatistics 10: 352-363.
67. Singh R, Valcarcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268: 1173-1176.
68. Sinha R, Allemand E, Zhang Z, Karni R, Myers MP, Krainer AR. 2010. Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF. Mol Cell Biol 30: 2762-2774.
69. Smyth GK 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 3. doi: 10.2202/1544-6115.1027.
70. Stitzinger SM, Conrad TR, Zachlin AM, Salz HK. 1999. Functional analysis of SNF, the Drosophila U1A/U2B″ homolog: identification of dispensable and indispensable motifs for both snRNP assembly and function in vivo. RNA 5: 1440-1450. (Pubitemid 29530488)
71. Stolc V, Gauhar Z, Mason C, Halasz G, van Batenburg MF, Rifkin SA, Hua S, Herreman T, Tongprasit W, Barbano PE, et al. 2004. A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306: 655-660. (Pubitemid 39440907)
72. Su WL, Modrek B, GuhaThakurta D, Edwards S, Shah JK, Kulkarni AV, Russell A, Schadt EE, Johnson JM, Castle JC. 2008. Exon and junction microarrays detect widespread mouse strain- and sex-bias expression differences. BMC Genomics 9: 273. doi: 10.1186/1471-2164-9-273.
73. Tarone AM, Nasser YM, Nuzhdin SV. 2005. Genetic variation for expression of the sex determination pathway genes in Drosophila melanogaster. Genet Res 86: 31-40. (Pubitemid 41430672)
74. Telonis-Scott M, Kopp A,WayneML, Nuzhdin SV,McIntyre LM. 2009. Sex-specific splicing in Drosophila: widespread occurrence, tissue specificity and evolutionary conservation. Genetics 181: 421-434.
75. Thomson T, Lasko P. 2005. Tudor and its domains: germ cell formation from a Tudor perspective. Cell Res 15: 281-291. (Pubitemid 41642884)
76. Tian M, Maniatis T. 1994. A splicing enhancer exhibits both constitutive and regulated activities. Genes Dev 8: 1703-1712. (Pubitemid 24236248)
77. Valcárcel J, Singh R, Zamore PD, Green MR. 1993. The protein Sexlethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362: 171-175. (Pubitemid 23085259)
78. Wahl MC, Will CL, Luhrmann R. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718.
79. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
80. Xing Y, Lee C. 2007. Relating alternative splicing to proteome complexity and genome evolution. Adv Exp Med Biol 2007: 36-49.