The hnRNP A1 homolog Hrp36 is essential for normal development, female fecundity, omega speckle formation and stress tolerance in Drosophila melanogaster
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  • 作者:Anand K Singh ; Subhash C Lakhotia
  • 关键词:93D ; hnRNP ; ISWI ; Megator ; noncoding RNA ; omega speckles ; thermo ; tolerance
  • 刊名:Journal of Biosciences
  • 出版年:2012
  • 出版时间:September 2012
  • 年:2012
  • 卷:37
  • 期:4
  • 页码:659-678
  • 全文大小:
  • 参考文献:Blanchette M, Green RE, MacArthuer S, Brooks AN, Brenner SE, Eisen MB and 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鈥?49PubMed CrossRef
    Boehm AK, Saunders A, Werner J and Lis JT 2003 Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock. Mol. Cell Biol. 23 7628鈥?637PubMed CrossRef
    Bonner JJ and Kerby RL 1982 RNA polymerase II transcribes all of the heat shock induced genes of Drosophila melanogaster. Chromosoma 85 93鈥?08PubMed CrossRef
    Borah S, Wong AC and Steitz JA 2009 Drosophila hnRNP A1 homologs Hrp36/Hrp38 enhance U2-type versus U12-type splicing to regulate alternative splicing of the prospero twintron. Proc. Natl. Acad. Sci. USA 106 2577鈥?582PubMed CrossRef
    Busch A and Hertel KJ 2012 Evolution of SR protein and hnRNP splicing regulatory factors. WIREs RNA 3 1鈥?2PubMed CrossRef
    Chaudhury A, Chander P and Howe PH 2010 Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles. RNA 16 1449鈥?462PubMed CrossRef
    Clouse KN, Ferguson SB and Schupbach T 2008 Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Dev. Biol. 313 713鈥?24PubMed CrossRef
    Corona DFV, Siriaco G, Armstrong JA, Snarskaya N, McClymont SA, Scott MP and Tamkun JW 2007 ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol. 5 e232PubMed CrossRef
    Daneholt B 2001 Assembly and transport of a premessenger RNP particle. Proc. Natl. Acad. Sci. USA 98 7012鈥?017PubMed CrossRef
    Dej KJ and Spradling AC 1999 The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis. Development 126 293鈥?03PubMed
    Dwivedi V, Anandan EM, Mony RS, Muraleedharan TS, Valiathan MS, Mutsuddi M and Lakhotia SC 2012 In vivo effects of traditional Ayurvedic formulations in Drosophila melanogaster model relate with therapeutic applications. PLos One 7 e37113PubMed CrossRef
    Geng C and Macdonald PM 2006 Imp associates with squid and Hrp48 and contributes to localized expression of gurken in the oocyte. Mol. Cell Biol. 26 9508鈥?516PubMed CrossRef
    Gerber M, Tenney K, Conaway JW, Conaway RC, Eissenberg JC and Shilatifard A 2005 Regulation of heat shock gene expression by RNA polymerase II elongation factor, Elongin A. J. Biol. Chem. 280 4017鈥?020PubMed CrossRef
    Goodrich JS, Clouse KN and Schupbach T 2004 Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development 131 1949鈥?958PubMed CrossRef
    Griffith BN, Walsh CM, Szeszel-Fedorowicz W, Timperman AT and Salati LM 2006 Identification of hnRNPs K, L and A2/B1 as candidate proteins involved in the nutritional regulation of mRNA splicing. Biochim. Biophys. Acta. 1759 552鈥?61PubMed CrossRef
    Guisbert KK, Duncan K, Li H and Guthrie C 2005 Functional specificity of shuttling hnRNPs revealed by genome-wide analysis of their RNA binding profiles. RNA 11 383鈥?93CrossRef
    Han SP, Kassahn KS, Skarshewski A, Ragan MA, Rothnagel JA and Smith R 2010 Functional implications of the emergence of alternative splicing in hnRNP A/B transcripts. RNA 16 1760鈥?768PubMed CrossRef
    Haynes SR, Cooper MT, Pype S and Stolow DT 1997 Involvement of a tissue-specific RNA recognition motif protein in Drosophila spermatogenesis. Mol. Cell Biol. 17 2708鈥?715PubMed
    Haynes SR, Johnson D, Raychaudhuri G and Beyer AL 1991 The Drosophila Hrb87F gene encodes a new member of the A and B hnRNP protein group. Nucleic Acids Res. 19 25鈥?1PubMed CrossRef
    Haynes SR, Raychaudhuri G and Beyer AL 1990 The Drosophila Hrb98DE locus encodes four protein isoforms homologous to the A1 protein of mammalian heterogeneous nuclear ribonucleoprotein complexes. Mol. Cell Biol. 10 316鈥?23PubMed
    He DC, Martin T and Penman S 1991 Localization of heterogeneous nuclear ribonucleoprotein in the interphase nuclear matrix core filaments and on perichromosomal filaments at mitosis. Proc. Natl. Acad. Sci. USA 88 7469鈥?473PubMed CrossRef
    He Y and Smith R 2009 Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B Cell. Mol. Life Sci. 66 1239鈥?256CrossRef
    Ji Y and Tulin AV 2009 Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res. 37 3501鈥?513PubMed CrossRef
    Ji Y and Tulin AV 2012 Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization. Nat. Commun. 3 760 doi: 10.1038 ncomms1759PubMed CrossRef
    Jolly C and Lakhotia SC 2006 Human sat III and Drosophila hsr omega transcripts: a common paradigm for regulation of nuclear RNA processing in stressed cells. Nucleic Acids Res. 34 5508鈥?514PubMed CrossRef
    King RC 1970 The meiotic behavior of the Drosophila oocyte. Int. Rev. Cytol. 28 125鈥?68PubMed CrossRef
    King RC, Riley SF, Cassidy JD, White PE and Paik YK 1981 Giant polytene chromosomes from the ovaries of a Drosophila mutant. Science 212 441鈥?43PubMed CrossRef
    King RC and Storto PD 1988 The role of the otu gene in Drosophila oogenesis. Bioessays 8 18鈥?4PubMed CrossRef
    Kozlova N, Braga J, Lundgren J, Rino J, Young P, Carmo-Fonseca M and Visa N 2006 Studies on the role of NonA in mRNA biogenesis. Exp. Cell Res. 312 2619鈥?630PubMed CrossRef
    Lakhotia SC 1974 EM Autoradiographic Studies on polytene nuclei of Drosophila melanogaster III. Localisation of non-replicating chromatin in the chromocentre heterochromatin. Chromosoma 46 145鈥?59PubMed CrossRef
    Lakhotia SC 1984 Replication in Drosophila chromosomes XII. Reconfirmation of underreplication of heterochromatin in polytene nuclei by cytofluorometry. Chromosoma 89 63鈥?7CrossRef
    Lakhotia SC 2003 Integration of transcriptional and translational activities in normal and stressed cells by the noncoding hsr-omega transcripts in Drosophila. Biol. Intl. 45 30鈥?3
    Lakhotia SC 2011 Forty years of the 93D puff of Drosophila melanogaster. J. Biosci. 36 399鈥?23PubMed CrossRef
    Lakhotia SC, Mallik M, Singh AK and Ray M 2012 The large noncoding hsromega-n transcripts are essential for thermotolerance and remobilization of hnRNPs, HP1 and RNA polymerase II during recovery from heat shock in Drosophila. Chromosoma 121 49鈥?0PubMed CrossRef
    Lakhotia SC, Rajendra TK and Prasanth KV 2001 Developmental regulation and complex organization of the promoter of the non-coding hsr(omega) gene of Drosophila melanogaster. J. Biosci. 26 25鈥?8PubMed CrossRef
    Lakhotia SC, Ray P, Rajendra TK and Prasanth KV 1999 The non-coding transcripts of hsr-omega gene in Drosophila: Do they regulate trafficking and availability of nuclear RNA-processing factors? Curr. Sci. 77 553鈥?63
    Lakhotia SC and Tapadia MG 1998 Genetic mapping of the amide response element(s) of the hsr omega locus of Drosophila melanogaster. Chromosoma 107 127鈥?35PubMed CrossRef
    Mallik M and Lakhotia SC 2009 The developmentally active and stress-inducible noncoding hsromega gene is a novel regulator of apoptosis in Drosophila. Genetics 183 831鈥?52PubMed CrossRef
    Mallik M and Lakhotia SC 2010 Improved activities of CREB binding protein, heterogeneous nuclear ribonucleoproteins and proteasome following downregulation of noncoding hsromega transcripts help suppress poly(Q) pathogenesis in fly models. Genetics 184 927鈥?45PubMed CrossRef
    Mallik M and Lakhotia SC 2011 Pleiotropic consequences of misexpression of the developmentally active and stress-inducible non-coding hsromega gene in Drosophila. J. Biosci. 36 265鈥?80PubMed CrossRef
    Manita D, Toba Y, Takakusagi Y, Matsumoto Y, Kusayanagi T, Takakusagi K, Tsukuda S, Takada K, Kanai Y, Kamisuki S, Sakaguchi K and Sugawara F 2011 Camptothecin (CPT) directly binds to human heterogeneous nuclear ribonucleoprotein A1 (hnRNP A1) and inhibits the hnRNP A1/topoisomerase I interaction. Bioorg. Med. Chem. 19 7690鈥?697PubMed CrossRef
    Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T and Chabot B 2007 hnRNP proteins and splicing control. Adv. Exp. Med. Biol. 623 123鈥?47PubMed CrossRef
    Mayeda A, Munroe SH, Xu RM and Krainer AR 1998 Distinct functions of the closely related tandem RNA-recognition motifs of hnRNP A1. RNA 4 1111鈥?123PubMed CrossRef
    Mutsuddi M and Lakhotia SC 1995 Spatial expression of the hsr-omega (93D) gene in different tissues of Drosophila melanogaster and identification of promoter elements controlling its developmental expression. Dev. Genet. 17 303鈥?11PubMed CrossRef
    Nilsen TW and Graveley BR 2010 Expansion of the eukaryotic proteome by alternative splicing. Nature 463 457鈥?63PubMed CrossRef
    Norvell A, Debec A, Finch D, Gibson L and Thoma B 2005 Squid is required for efficient posterior localization of oskar mRNA during Drosophila oogenesis. Dev. Genes Evol. 215 340鈥?49PubMed CrossRef
    Olson S, Blanchette M, Park J, Savva Y, Yeo GW, Yeakley JM, Rio DC and Graveley BR 2007 A regulator of Dscam mutually exclusive splicing fidelity. Nat. Struct. Mol. Biol. 14 1134鈥?140PubMed CrossRef
    Onorati MC, Lazzaro S, Mallik M, Ingrassia AM, Carreca AP, Singh AK, Chaturvedi DP, Lakhotia SC and Corona DFV 2011 The ISWI chromatin remodeler organizes the hsromega ncRNA-containing omega speckle nuclear compartments. PLoS Genet. 7 e1002096PubMed CrossRef
    Piacentini L, Fanti L, Negri R, Del Vescovo V, Fatica A, Altieri F and Pimpinelli S 2009 Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet. 5 e1000670PubMed CrossRef
    Prasanth KV, Rajendra TK, Lal AK and Lakhotia SC 2000 Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J. Cell Sci. 113 3485鈥?497PubMed
    Sala A, La Rocca G, Burgio G, Kotova E, Di Gesu D, Collesano M, Ingrassia AM, Tulin AV and Corona DFV 2008 The nucleosome-remodeling ATPase ISWI is regulated by poly-ADP-ribosylation. PLoS Biol. 6 e252PubMed CrossRef
    Saumweber H, Symmons P, Kabisch R, Will H and Bonhoeffer F 1980 Monoclonal antibodies against chromosomal proteins of Drosophila melanogaster: establishment of antibody producing cell lines and partial characterization of corresponding antigens. Chromosoma 80 253鈥?75PubMed CrossRef
    Sengupta S and Lakhotia SC 2006 Altered expressions of the noncoding hsromega gene enhances poly-Q-induced neurotoxicity in Drosophila. RNA Biol. 3 28鈥?5PubMed CrossRef
    Sofola OA, Jin P, Qin Y, Duan R, Liu H, de Haro M, Nelson DL and Botas J 2007 RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 55 565鈥?71PubMed CrossRef
    Steinhauer J and Kalderon D 2005 The RNA-binding protein Squid is required for the establishment of anteroposterior polarity in the Drosophila oocyte. Development 132 5515鈥?525PubMed CrossRef
    Velazquez JM and Lindquist S 1984 hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36 655鈥?62PubMed CrossRef
    Zeng C, Kim E, Warren SL and Berget SM 1997 Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 16 1401鈥?412PubMed CrossRef
    Zimowska G, Aris JP and Paddy MR 1997 A Drosophila Tpr protein homolog is localized both in the extrachromosomal channel network and to nuclear pore complexes. J. Cell Sci. 110 927鈥?44PubMed
    Zimowska G and Paddy MR 2002 Structures and dynamics of Drosophila Tpr inconsistent with a static, filamentous structure. Exp. Cell Res. 276 223鈥?32PubMed CrossRef
    Zu K, Sikes ML and Beyer AL 1998 Separable roles in vivo for the two RNA binding domains of a Drosophila A1-hnRNP homolog. RNA 4 1585鈥?598PubMed CrossRef
    Zu K, Sikes ML, Haynes SR and Beyer AL 1996 Altered levels of the Drosophila HRB87F/hrp36 hnRNP protein have limited effects on alternative splicing in vivo. Mol. Biol. Cell 7 1059鈥?073PubMed
  • 作者单位:Anand K Singh (1)
    Subhash C Lakhotia (1)

    1. Cytogenetics Laboratory, Department of Zoology, Banaras Hindu University, Varanasi, 221 005, India
  • 刊物类别:Life Sciences, general; Biomedicine general; Zoology; Plant Sciences; Microbiology; Cell Biology;
  • 刊物主题:Life Sciences, general; Biomedicine general; Zoology; Plant Sciences; Microbiology; Cell Biology;
  • 出版者:Springer India
  • ISSN:0973-7138
文摘
Hrp36/Hrb87F is one of the most abundant and well-characterized hnRNP A homolog in Drosophila and is shown to have roles in regulation of alternative splicing, heterochromatin formation, neurodegeneration, etc. Yet, hrp36 null individuals were reported to be viable and without any apparent phenotype, presumably because of overlapping functions provided by Hrp38 and related proteins. Here we show that loss of both copies of hrp36 gene slows down development with significant reduction in adult life span, decreased female fecundity and high sensitivity to starvation and thermal stresses. In the absence of Hrp36, the nucleoplasmic omega speckles are nearly completely disrupted. The levels of nuclear matrix protein Megator and the chromatin remodeller ISWI are significantly elevated in principal cells of larval Malpighian tubules, which also display additional endoreplication cycles and good polytene chromosomes. We suggest that besides the non-coding hsr蠅-n transcripts, the Hrp36 protein is also a core constituent of omega speckles. The heat-shock-induced association of other hnRNPs at the hsr蠅 locus is affected in hrp36 null cells, which may be one of the reasons for their high sensitivity to cell stress. Therefore, in spite of the functional redundancy provided by Hrp38, Hrp36 is essential for normal development and for survival under conditions of stress. Keywords 93D hnRNP ISWI Megator noncoding RNA omega speckles thermo-tolerance

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