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Forty years of the 93D puff of Drosophila melanogaster

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Abstract

The 93D puff of Drosophila melanogaster became attractive in 1970 because of its singular inducibility by benzamide and has since then remained a major point of focus in my laboratory. Studies on this locus in my and several other laboratories during the past four decades have revealed that (i) this locus is developmentally active, (ii) it is a member of the heat shock gene family but selectively inducible by amides, (iii) the 93D or heat shock RNA omega (hsrω) gene produces multiple nuclear and cytoplasmic large non-coding RNAs (hsrω-n, hsrω-pre-c and hsrω-c), (iv) a variety of RNA-processing proteins, especially the hnRNPs, associate with its >10 kb nuclear (hsrω-n) transcript to form the nucleoplasmic omega speckles, (v) its genomic architecture and hnRNP-binding properties with the nuclear transcript are conserved in different species although the primary base sequence has diverged rapidly, (vi) heat shock causes the omega speckles to disappear and all the omega speckle associated proteins and the hsrω-n transcript to accumulate at the 93D locus, (vii) the hsrω-n transcript directly or indirectly affects the localization/stability/activity of a variety of proteins including hnRNPs, Sxl, Hsp83, CBP, DIAP1, JNK-signalling members, proteasome constituents, lamin C, ISWI, HP1 and poly(ADP)-ribose polymerase and (viii) a balanced level of its transcripts is essential for the orderly relocation of various proteins, including hnRNPs, RNA pol II and HP1, to developmentally active chromosome regions during recovery from heat stress. In view of such multitudes of interactions, it appears that large non-coding RNAs like those produced by the hsrω gene may function as hubs to coordinate multiple cellular networks and thus play important roles in maintenance of cellular homeostasis.

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References

  • Akanksha, Mallik M, Fatima R and Lakhotia SC 2008 The hsromega(05241) allele of the noncoding hsromega gene of Drosophila melanogaster is not responsible for male sterility as reported earlier. J. Genet. 87 87–90

    PubMed  CAS  Google Scholar 

  • Anderson AR, Collinge JE, Hoffmann AA, Kellett M and Mckechnie SW 2003 Thermal tolerance trade-offs associated with the right arm of chromosome 3 and marked by the hsr-omega gene in Drosophila melanogaster. Heredity 90 195–202

    PubMed  CAS  Google Scholar 

  • Arao Y, Kuriyama R, Kayama F and Kato S 2000 A nuclear matrix-associated factor, SAF-B, interacts with specific isoforms of AUF1/hnRNP D. Arch. Biochem. Biophys. 380 228–236

    PubMed  CAS  Google Scholar 

  • Arya R, Mallik M and Lakhotia SC 2007 Heat shock genes – integrating cell survival and death. J. Biosci. 32 595–610

    PubMed  CAS  Google Scholar 

  • Ashburner M 1967 Patterns of puffing activity in the salivary gland chromosomes of Drosophila. I. Autosomal puffing patterns in a laboratory stock of Drosophila melanogaster. Chromosoma 21 398–428

    PubMed  CAS  Google Scholar 

  • Ashburner M 1970 Patterns of puffing activity in the salivary gland chromosomes of Drosophila. V. Responses to environmental treatments. Chromosoma 31 356–376

    PubMed  CAS  Google Scholar 

  • Ashburner M and Bonner JJ 1979 The induction of gene activity in Drosophilia by heat shock. Cell 17 241–254

    PubMed  CAS  Google Scholar 

  • Behnel HJ 1982 Comparative study of protein synthesis and heat shock puffing activity in Drosophila salivary glands treated with chloramphenicol. Exp. Cell. Res. 142

  • Belew K and Brady T 1981 Induction of tyrosine aminotransferase by pyridoxine in Drosophila hydei. Chromosoma 82 99–106

    PubMed  CAS  Google Scholar 

  • Bendena WG, Ayme-Southgate A, Garbe JC and Pardue ML 1991 Expression of heat-shock locus hsr-omega in nonstressed cells during development in Drosophila melanogaster. Dev. Biol. 144 65–77

    PubMed  CAS  Google Scholar 

  • Bendena WG, Fini ME, Garbe JC, Kidder GM, Lakhotia SC and Pardue ML 1989a hsrω: A different sort of heat shock locus; in Stress-induced proteins (eds) ML Pardue, J Ferimisco and S Lindquist (Alan R Liss, Inc) pp 3–14

  • Bendena WG, Garbe JC, Traverse KL, Lakhotia SC and Pardue ML 1989b Multiple inducers of the Drosophila heat shock locus 93D (hsrω): inducer-specific pattern of the three transcripts. J. Cell Biol. 108 2017–2028

    PubMed  CAS  Google Scholar 

  • Berendes HD and Beermann W 1969 Biochemical activity of interphase chromosomes (polytene chromosomes); in Handbook of molecular cytogenetics (ed) Lima-de-Faria (Amsterdam: London North Holland Publishing Company) pp 501–519

  • Bonner JJ and Pardue ML 1976 The effect of heat shock on RNA synthesis in Drosophila tissues. Cell 8 43–50

    PubMed  CAS  Google Scholar 

  • Brady T and Belew K 1981 Pyridoxine induced puffing (II-48C) and synthesis of a 40 KD protein in Drosophila hydei salivary glands. Chromosoma 82 89–98

    PubMed  CAS  Google Scholar 

  • Brand AH and Perrimon N 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 401–415

    PubMed  CAS  Google Scholar 

  • Buchenau P, Saumweber H and Arndt-Jovin DJ 1997 The dynamic nuclear redistribution of an hnRNP K-homologous protein during Drosophila embryo development and heat shock. Flexibility of transcription sites in vivo. J. Cell Biol. 137 291–303

    PubMed  CAS  Google Scholar 

  • Burma PK and Lakhotia SC 1984 Cytological identity of 93D-like and 87C-like heat shock loci in Drosophila pseudoobscura. Indian J. Exp. Biol. 22 577–580

    CAS  Google Scholar 

  • Burma PK and Lakhotia SC 1986 Expression of 93D heat shock puff of Drosophila melanogaster in deficiency genotype and its influence on activity of the 87C puff. Chromosoma 94 273–278

    Google Scholar 

  • Carmona MJ, Morcillo G, Galler R, Martinez-Salas E, de la Campa AG, Diez JL and Edstrom JE 1985 Cloning and molecular characterization of a telomeric sequence from a temperature-induced Balbiani ring. Chromosoma 92 108–115

    CAS  Google Scholar 

  • Collinge JE, Anderson AR, Weeks AR, Johnson TK and McKechnie SW 2008 Latitudinal and cold-tolerance variation associate with DNA repeat-number variation in the hsr-omega RNA gene of Drosophila melanogaster. Heredity 101 260–270

    PubMed  CAS  Google Scholar 

  • Compton JL and McCarthy BJ 1978 Induction of the Drosophila heat shock response in isolated polytene nuclei. Cell 14 191–201

    PubMed  CAS  Google Scholar 

  • Corona DF, 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 e232

    PubMed  Google Scholar 

  • Cutforth T and Rubin GM 1994 Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 7 1027–1036

    Google Scholar 

  • Dangli A and Bautz EK 1983 Differential distribution of nonhistone proteins from polytene chromosomes of Drosophila melanogaster after heat shock. Chromosoma 88 201–207

    PubMed  CAS  Google Scholar 

  • Dangli A, Grond C, Kloetzel P and Bautz EK 1983 Heat-shock puff 93 D from Drosophila melanogaster: accumulation of a RNP-specific antigen associated with giant particles of possible storage function. EMBO J. 2 1747–1751

    PubMed  CAS  Google Scholar 

  • Denegri M, Chiodi I, Corioni M, Cobianchi F, Riva S and Biamonti G 2001 Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors. Mol. Biol. Cell 12 3502–3514

    PubMed  CAS  Google Scholar 

  • Derksen J 1975 The submicroscopic structure of synthetically active units in a puff of Drosophila hydei giant chromosomes. Chromosoma 50 45–52

    PubMed  CAS  Google Scholar 

  • Derksen J, Berendes HD and Willart E 1973 Production and release of a locus-specific ribonucleoprotein product in polytene nuclei of Drosophila hydei. J. Cell Biol. 59 661–668

    PubMed  CAS  Google Scholar 

  • Doolittle WF and Sapienza C 1980 Selfish genes, the phenotype paradigm and genome evolution. Nature (London) 284 601–603

    CAS  Google Scholar 

  • Dustin P 1978 Microtubules (Berlin, Heidelberg, New York: Springer-Verlag)

    Google Scholar 

  • Edstrom JE and Beermann W 1962 The base composition of nucleic acids in chromosomes, puffs, nucleoli, and cytoplasm of Chironomus salivary gland cells. J. Cell Biol. 14 371–379

    PubMed  CAS  Google Scholar 

  • Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, Martinez P, Turiegano E, Benito J, et al. 2000 Identification of genes that modify ataxin-1-induced neurodegeneration. Nature (London) 408 101–106

    CAS  Google Scholar 

  • Fini ME, Bendena WG and Pardue ML 1989 Unusual behavior of the cytoplasmic transcript of hsr omega: an abundant, stress-inducible RNA that is translated but yields no detectable protein product. J. Cell Biol. 108 2045–2057

    PubMed  CAS  Google Scholar 

  • Garbe JC and Pardue ML 1986 Heat-shock locus 93D of Drosophila melanogaster: a spliced RNA most strongly conserved in the intron sequence. Proc. Natl. Acad. Sci. USA 83 1812–1816

    PubMed  CAS  Google Scholar 

  • Garbe JC, Bendena WG and Pardue ML 1989 Sequence evolution of the Drosophila heat shock locus hsr omega. I. The nonrepeated portion of the gene. Genetics 122 403–415

    PubMed  CAS  Google Scholar 

  • Garbe JC, Bendena WG, Alfano M and Pardue ML 1986 A Drosophila heat shock locus with a rapidly diverging sequence but a conserved structure. J. Biol. Chem. 261 16889–16894

    PubMed  CAS  Google Scholar 

  • Grossbach U 1969 Chromosome activity and biochemical cell differentiation in the salivary glands of Camptochironomus. Chromosoma 28 136–187

    PubMed  CAS  Google Scholar 

  • Gubenko IS and Baricheva EM 1979 Drosophila virilis puffs induced by temperature and other environmental factors. Genetika (USSR) 15 1399–1414

    CAS  Google Scholar 

  • Han SP, Tang YH and Smith R 2010 Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J. 430 379–392

    PubMed  CAS  Google Scholar 

  • 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 25–31

    PubMed  CAS  Google Scholar 

  • Henikoff S 1980 A more conventional view of the ‘ebony’ gene. Dros. Lnf. Serv. 55 61

    Google Scholar 

  • Hochstrasser M 1987 Chromosome structure in four wild-type polytene tissues of Drosophila melanogaster. The 87A and 87C heat shock loci are induced unequally in the midgut in a manner dependent on growth temperature. Chromosoma 95 197–208

    PubMed  CAS  Google Scholar 

  • Hogan NC, Traverse KL, Sullivan DE and Pardue ML 1994 The nucleus-limited Hsr-omega-n transcript is a polyadenylated RNA with a regulated intranuclear turnover. J. Cell Biol. 125 21–30

    PubMed  CAS  Google Scholar 

  • Hovemann B, Walldorf U and Ryseck RP 1986 Heat-shock locus 93D of Drosophila melanogaster: An RNA with limited coding capacity accumulates precursor transcripts after heat shock. Mol. Gen. Genet. 204 334–340

    CAS  Google Scholar 

  • Ji Y and Tulin AV 2009 Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res. 37 3501–3513

    PubMed  CAS  Google Scholar 

  • Johnson TK, Carrington LB, Hallas RJ and McKechnie SW 2009 Protein synthesis rates in Drosophila associate with levels of the hsr-omega nuclear transcript. Cell Stress Chaperones 14 569–577

    PubMed  CAS  Google Scholar 

  • 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 5508–5514

    PubMed  CAS  Google Scholar 

  • Jolly C and Morimoto RI 1999 Stress and the cell nucleus: dynamics of gene expression and structural reorganization. Gene Expr. 7 261–270

    PubMed  CAS  Google Scholar 

  • Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S and Vourc'h C 2004 Stress-induced transcription of satellite III repeats. J. Cell Biol. 164 25–33

    PubMed  CAS  Google Scholar 

  • Kar Chowdhury D and Lakhotia SC 1986 Different effects of 93D on 87C heat shock puff activity in Drosophila melanogaster and D. simulans. Chromosoma 94: 279–284

    Google Scholar 

  • Lakhotia SC 1970 Gene physiological studies on dosage compensation in Drosophila. PhD Thesis, University of Calcutta, Kolkata

  • Lakhotia SC 1974 EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. 3. Localisation of non-replicating chromatin in the chromocentre heterochromatin. Chromosoma 46 145–159

    PubMed  CAS  Google Scholar 

  • Lakhotia SC 1987 The 93D heat shock locus in Drosophila - a review. J. Genet. 66 139–157

    CAS  Google Scholar 

  • Lakhotia SC 1989 The 93D heat shock locus of Drosophila melanogaster: modulation by genetic and developmental factors. Genome 31 677–683

    PubMed  CAS  Google Scholar 

  • Lakhotia SC 1996 RNA polymerase II dependent genes that do not code for protein. Indian J. Biochem. Biophys. 33 93–102

    Google Scholar 

  • Lakhotia SC 1999 Non-coding RNAs: versatile roles in cell regulation. Curr. Sci. 77 479–480

    Google Scholar 

  • Lakhotia SC 2003 The non-coding, developmentally active and stress inducible hsrω gene of Drosophila melanogaster integrates post-transcriptional processing of other nuclear transcripts; in Noncoding RNAs: molecular biology and molecular medicine (eds) J Barciszweski and VA Erdmann (New York: Kluwer Academic/Plenum Publishers) pp 202–219

    Google Scholar 

  • Lakhotia SC and Jacob J 1974a Electron microscopic autoradiographic studies on polytene nuclei of Drosophila melanogaster: Part I. Replication and its relationship with nuclear membrane. Indian J. Exp. Biol. 12 389–394

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Jacob J 1974b EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. II. Organization and transcriptive activity of the chromocentre. Exp. Cell Res. 86 253–263

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mukherjee AS 1969 Chromosomal basis of dosage compensation in Drosophila. I. Cellular autonomy of hyperactivity of the male X-chromosome in salivary glands and sex differentiation. Genet. Res. 14 137–150

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mukherjee AS 1970a Chromosomal basis of dosage compensation in Drosophila. 3. Early completion of replication by the polytene X-chromosome in male: further evidence and its implications. J. Cell Biol. 47 18–33

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mukherjee AS 1970b Activation of a specific puff by benzamide in D. melanogaster. Dros. Inf. Serv. 45 108

    Google Scholar 

  • Lakhotia SC and Mukherjee T 1980 Specific activation of puff 93D of Drosophila melanogaster by benzamide and the effect of benzamide treatment on the heat shock induced puffing activity. Chromosoma 81 125–136

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mukherjee T 1982 Absence of novel translation products in relation to induced activity of the 93D puff in Drosophila melanogaster. Chromosoma 85 369–374

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mukherjee T 1984 Specific induction of the 93D puff in polytene nuclei of Drosophila melanogaster by colchicine. Indian J. Exp. Biol. 22 67–70

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Mutsuddi M 1996 Heat shock but not benzamide and colchicine response elements are present within the −844 bp upstream region of the hsr omega gene of Drosophila melanogaster. J. Biosci. 21 235–246

    CAS  Google Scholar 

  • Lakhotia SC and Ray P 1996 hsp83 mutation is a dominant enhancer of lethality associated with absence of the non-protein coding hsr omega locus in Drosophila melanogaster. J. Biosci. 21 207–219

    CAS  Google Scholar 

  • Lakhotia SC and Sharma A 1995 RNA metabolism in situ at the 93D heat shock locus in polytene nuclei of Drosophila melanogaster after various treatments Chromosome Res. 3 151–161

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Sharma A 1996 The 93D (hsrω) locus of Drosophila: non-coding gene with house-keeping functions. Genetica 97 339–348

    PubMed  CAS  Google Scholar 

  • Lakhotia SC and Singh AK 1982 Conservation of the 93D puff of Drosophila melanogaster in different species of Drosophila. Chromosoma 86 265–278

    Google Scholar 

  • Lakhotia SC and Singh AK 1985 Non-inducibility of the 93D heat shock puff in cold-reared larvae of Drosophila melanogaster. Chromosoma 92 48–54

    Google Scholar 

  • Lakhotia SC and Tapadia MG 1998 Genetic mapping of the amide response element/s of the hsrω locus of Drosophila melanogaster. Chromosoma 107 127–135

    PubMed  CAS  Google Scholar 

  • Lakhotia SC, Kar Chowdhuri D and Burma PK 1990 Mutations affecting β-alanine metabolism influence inducibility of the 93D puff by heat shock in Drosophila melanogaster. Chromosoma 99 296–305

    PubMed  CAS  Google Scholar 

  • Lakhotia SC, Rajendra TK and Prasanth KV 2001 Developmental regulation and complex organization of the promoter of the non-coding hsrω gene of Drosophila melanogaster. J. Biosci. 26 25–38

    PubMed  CAS  Google Scholar 

  • 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. 77 553–563

    CAS  Google Scholar 

  • Lakomek HJ, Plomann M, Specker C and Schwochau M 1991 Ankylosing spondylitis: an autoimmune disease? Ann. Rheum. Dis. 50 776–781

    PubMed  CAS  Google Scholar 

  • Leenders HJ, Derksen J, Mass PMJM and Berendes HD 1973 Selective induction of a giant puff in Drosophila hydei by vitamin B6 and derivatives. Chromosoma 41 447–460

    CAS  Google Scholar 

  • Lengyel JA, Ransom LJ, Graham ML and Pardue ML 1980 Transcription and metabolism of RNA from the Drosophila melanogaster heat shock puff site 93D. Chromosoma 80 237–252

    PubMed  CAS  Google Scholar 

  • Lewis M, Helmsing PJ and Ashburner M 1975 Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila. Proc. Natl. Acad. Sci. USA 72 3604–3608

    PubMed  CAS  Google Scholar 

  • Lindell TJ, Weinberg F, Morris PW, Roeder RG and Rutter WJ 1970 Specific inhibition of nuclear RNA polymerase II by alpha-amanitin. Science 170 447–449

    PubMed  CAS  Google Scholar 

  • Livak KJ, Freund R, Schweber M, Wensink PC and Meselson M 1978 Sequence organization and transcription at two heat shock loci in Drosophila. Proc. Natl. Acad. Sci. USA 75 5613–5617

    PubMed  CAS  Google Scholar 

  • Lyon MF 1961 Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature (London) 190 372–373

    CAS  Google Scholar 

  • Mallik M and Lakhotia SC 2007 Noncoding DNA is not “junk” but a necessity for origin and evolution of biological complexity. Proc. Natl. Acad. Sci. India Spl. Iss. 77(B) 43–50

    Google Scholar 

  • Mallik M and Lakhotia SC 2009a RNAi for the large non-coding hsromega transcripts suppresses polyglutamine pathogenesis in Drosophila models. RNA Biol. 6 464–478

    PubMed  CAS  Google Scholar 

  • Mallik M and Lakhotia SC 2009b The developmentally active and stress-inducible non-coding hsrω gene is a novel regulator of apoptosis in Drosophila. Genetics 183 831–852

    PubMed  CAS  Google Scholar 

  • Mallik M and Lakhotia SC 2010a Improved activities of CBP, hnRNPs and proteasome following down regulation of noncoding hsromega transcripts help suppress polyQ pathogenesis in fly models. Genetics 184 927–945

    PubMed  CAS  Google Scholar 

  • Mallik M and Lakhotia SC 2010b Modifiers and mechanisms of multi-system polyglutamine neurodegenerative disorders: lessons from fly models. J. Genet. 89 497–526

    PubMed  CAS  Google Scholar 

  • Mallik M and Lakhotia SC 2011 Misexpression of the developmentally active and stress-inducible non-coding hsrω gene in Drosophila has pleiotropic consequences. J. Biosci. 36 265–280

    PubMed  CAS  Google Scholar 

  • Mattern KA, van der Kraan I, Schul W, de Jong L and van Driel R 1999 Spatial organization of four hnRNP proteins in relation to sites of transcription, to nuclear speckles, and to each other in interphase nuclei and nuclear matrices of HeLa cells. Exp. Cell Res. 246 461–470

    PubMed  CAS  Google Scholar 

  • McColl G and McKechnie SW 1999 The Drosophila heat shock hsr-omega gene: an allele frequency cline detected by quantitative PCR. Mol. Biol. Evol. 16 1568–1574

    PubMed  CAS  Google Scholar 

  • McKechnie SW, Halford MM, McColl G and Hoffmann AA 1998 Both allelic variation and expression of nuclear and cytoplasmic transcripts of Hsr-omega are closely associated with thermal phenotype in Drosophila. Proc. Natl. Acad. Sci. USA 95 2423–2428

    PubMed  CAS  Google Scholar 

  • Mohler J and Pardue ML 1982 Deficiency mapping of' the 93D heat shock locus in Drosophila. Chromosoma 86 457–467

    PubMed  CAS  Google Scholar 

  • Mohler J and Pardue ML 1984 Mutational analysis of the region surrounding the 93D heat shock locus of Drosophila melanogaster. Genetics 106 249–265

    PubMed  CAS  Google Scholar 

  • Morcillo G, Diez JL, Carbajal Μ Ε and Tanguay R Μ 1993 Hsp90 associates with specific heat shock puffs (hsrω) in polytene chromosomes of Drosophila and Chironomus. Chromosoma 102 648–659

    PubMed  CAS  Google Scholar 

  • Morcillo G, Diez JL and Botella LM 1994 Heat shock activation of telomeric sequences in different tissues of Chironomus thummi. Exp. Cell Res. 211 163–167

    PubMed  CAS  Google Scholar 

  • Mukherjee AS and Beermann W 1965 Synthesis of ribonucleic acid by the X-chromosomes of Drosophila melanogaster and the problem of dosage compensation. Nature (London) 207 785–786

    CAS  Google Scholar 

  • Mukherjee T and Lakhotia SC 1979 3H-uridine incorporation in the puff 93D and in chromocentric heterochromatin of heat shocked salivary glands of Drosophila melanogaster. Chromosoma 74 75–82

    PubMed  CAS  Google Scholar 

  • Mukherjee T and Lakhotia SC 1981 Specific induction of the 93D puff in Drosophila melanogaster by a homogenate of heat shocked larval salivary glands. Indian J. Exp. Biol. 19 1–4

    CAS  Google Scholar 

  • Mukherjee T and Lakhotia SC 1982 Heat shock puff activity in salivary glands of Drosophila melanogaster larvae during recovery from anoxia at two different temperatures. Indian J. Exp. Biol. 20 437–439

    Google Scholar 

  • Muller HJ and Kaplan WD 1966 The dosage compensation of Drosophila and mammals as showing the accuracy of the normal type. Genet. Res. 8 41–59

    PubMed  CAS  Google Scholar 

  • 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. 17 303–311

    PubMed  CAS  Google Scholar 

  • Nath BB and Lakhotia SC 1991 Search for a Drosophila-93D-like locus in Chironomus and Anopheles. Cytobios 65 7–13

    PubMed  CAS  Google Scholar 

  • Onorati MC, Lazzaro S, Mallik M, Ingrassia AMR, Singh AK, Chaturvedi DP, Lakhotia SC and Corona DFV 2011 The ISWI chromatin remodeler organizes the hsrω ncRNA-containing omega speckle nuclear compartments. PLoS Genet. 7 e1002096. doi:10.1371/journal.pgen.1002096

    PubMed  CAS  Google Scholar 

  • Orgel LE and Crick FH 1980 Selfish DNA: the ultimate parasite. Nature (London) 284 604–607

    CAS  Google Scholar 

  • Pardue ML, Bendena WG, Fini ME, Garbe JC, Hogan NC and Traverse KL 1990 Hsr-omega, A novel gene encoded by a Drosophila heat shock puff. Biol. Bull. 179 77–86

    CAS  Google Scholar 

  • Perry RP and Kelley DE 1968 Persistent synthesis of 5S RNA when production of 28S and 18S ribosomal RNA is inhibited by low doses of actinomycin D. J. Cell Physiol. 72 235–246

    PubMed  CAS  Google Scholar 

  • Peters FP, Lubsen NH and Sondermeijer PJ 1980 Rapid sequence divergence in a heat shock locus of Drosophila. Chromosoma 81 271–280

    PubMed  CAS  Google Scholar 

  • Peters FP, Lubsen NH, Walldorf U, Moormann RJ and Hovemann B 1984 The unusual structure of heat shock locus 2-48B in Drosophila hydei. Mol. Gen. Genet. 197 392–398

    PubMed  CAS  Google Scholar 

  • Piacentini L, Fanti L, Berloco M, Perrini B and Pimpinelli S 2003 Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. J. Cell Biol. 161 707–714

    CAS  Google Scholar 

  • Prasanth KV and Spector DL 2007 Eukaryotic regulatory RNAs: an answer to the ‘genome complexity’ conundrum. Gene. Dev. 21 11–42

    PubMed  CAS  Google Scholar 

  • 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 3485–3497

    PubMed  CAS  Google Scholar 

  • Rajendra TK, Prasanth KV and Lakhotia SC 2001 Male sterility associated with over-expression of the non-coding hsrω gene in cyst cells of testis of Drosophila melanogaster. J. Genet. 80 97–110

    PubMed  CAS  Google Scholar 

  • Rao SRV and Lakhotia SC 1972 Chromosomes of Rattus (Rattus) blanfordi (Thomas), Muridae, Rodentia. J. Heredity 63 44–47

    CAS  Google Scholar 

  • Ray P 1997 Studies on interaction of the 93D (hsr-omega) locus with other genes during development of D. melanogaster. PhD Thesis, Banaras Hindu University, Varanasi

  • Ray P and Lakhotia SC 1998 Interaction of the non-protein-coding developmental and stress-inducible hsrω gene with Ras genes of Drosophila melanogaster. J. Biosci. 23 377–386

  • Rorth P 1996 A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc. Natl. Acad. Sci. USA 93 12418–12422

    PubMed  CAS  Google Scholar 

  • Ryseck RP, Walldorf U and Hovemann B 1985 Two major RNA products are transcribed from heat-shock locus 93D of Drosophila melanogaster. Chromosoma 93 17–20

    PubMed  CAS  Google Scholar 

  • Ryseck RP, Walldorf U, Hoffmann T and Hovemann B 1987 Heat shock loci 93D of Drosophila melanogaster and 48B of Drosophila hydei exhibit a common structural and transcriptional pattern. Nucleic Acids Res. 15 3317–3333

    PubMed  CAS  Google Scholar 

  • Samuels ME, Bopp D, Colvin RA, Roscigno RF, Garcia-Blanco MA and Schedl P 1994 RNA binding by Sxl proteins in vitro and in vivo. Mol. Cell Biol. 14 4975–4990

    PubMed  CAS  Google Scholar 

  • Santa-Cruz MC, Morcillo G and Diez JL 1984 Ultrastructure of a temperature-induced Balbiani ring in Chironomus thummi. Biol. Cell 52 205–211

    PubMed  CAS  Google Scholar 

  • 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 80 253–275

    PubMed  CAS  Google Scholar 

  • Scalenghe F and Ritossa F 1977 The puff inducible in region 93D is responsible for the synthesis of the major ‘heat-shock’ polypeptide in Drosophila melanogaster. Chromosoma 63 317–327

    CAS  Google Scholar 

  • Sengupta S 2005 Studies on a novel gene interacting with hsrω and their roles as modifiers in polyglutamine induced neurodegeneration in Drosophila melanogaster. PhD Thesis, Banaras Hindu University, Varanasi

  • Sengupta S and Lakhotia SC 2006 Altered expression of the noncoding hsrω gene enhances poly-Q-induced neurotoxicity in Drosophila. RNA Biol. 3 28–35

    PubMed  CAS  Google Scholar 

  • Shah VC, Lakhotia SC and Rao SRV 1973 Nature of heterochromatin. J. Sci. Industrial Res. 32 467–480

    Google Scholar 

  • Sharma A and Lakhotia SC 1995 In situ quantification of hsp70 and alpha-beta transcripts at 87A and 87C loci in relation to hsr-omega gene activity in polytene cells of Drosophila melanogaster. Chromosome Res. 3 386–393

    PubMed  CAS  Google Scholar 

  • Sims JL, Berger SJ and Berger NA 1983 Poly(ADP-ribose) Polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5'-triphosphate pools in DNA-damaged cells: mechanism of stimulation of unscheduled DNA synthesis. Biochemistry 22 5188–5194

    PubMed  CAS  Google Scholar 

  • Singh AK and Lakhotia SC 1983 Further observations on inducibility of 93D puff of Drosophila melanogaster by homogenate of heat shocked cells. Indian J. Exp. Biol. 21 363–366

    Google Scholar 

  • Singh AK and Lakhotia SC 1984 Lack of effect of microtubules positions on the 93D or 93D-like heat shock puffs in Drosophila. Indian J. Exp. Biol. 22 569–576

    CAS  Google Scholar 

  • Sirlin JL and Jacob J 1964 Sequential and reversible inhibition of synthesis of ribonucleic acid in the nucleolus and chromosomes: effect of benzamide and substituted benzimidazoles on dipteran salivary glands. Nature (London) 204 545–547

    CAS  Google Scholar 

  • Spector DL, Fu XD and Maniatis T 1991 Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 10 3467–3481.

    PubMed  CAS  Google Scholar 

  • Spradling A, Pardue ML and Penman S 1977 Messanger RNA in heat-shocked Drosophila cells. J. Mol. Biol. 109 559–587

    PubMed  CAS  Google Scholar 

  • Spruill WA, Hurwitz DR, Lucchesi JC and Steiner AL 1978 Association of cyclic GMP with gene expression of polytene chromosomes of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 75 1480–1484

    PubMed  CAS  Google Scholar 

  • Srikrishna S 2008 Studies on expression of hsrω non-coding RNA and its interacting proteins during oogenesis in Drosophila melanogaster. PhD Thesis, Banaras Hindu University, Varanasi

  • Srivastava JP and Bangia KK 1985 Specific induction of puff 93D in the polytene chromosomes of salivary glands of Drosophila melanogaster by paracetamol. J. Curr. Biosci. 2 48–50

    Google Scholar 

  • Tapadia MG and Lakhotia SC 1997 Specific induction of the hsr omega locus of Drosophila melanogaster by amides. Chromosome Res. 5 359–362

    PubMed  CAS  Google Scholar 

  • Tissieres A, Mitchell HK and Tracy UM 1974 Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J. Mol. Biol. 84 389–398

    PubMed  CAS  Google Scholar 

  • Walldorf U, Richter S, Ryseck RP, Steller H, Edstrom JE, Bautz EK and Hovemann B 1984 Cloning of heat-shock locus 93D from Drosophila melanogaster. EMBO J. 3 2499–2504

    PubMed  CAS  Google Scholar 

  • Westwood JT, Clos J and Wu C 1991 Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature (London) 353 822–827

    CAS  Google Scholar 

  • Wright TR 1987 The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv. Genet. 24 127–222

    PubMed  CAS  Google Scholar 

  • Zimowska G and Paddy MR 2002 Structures and dynamics of Drosophila Tpr inconsistent with a static, filamentous structure. Exp. Cell Res. 276 223–232

    PubMed  CAS  Google Scholar 

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Acknowledgements

I express my appreciation of the stimulating and enthusiastic work carried out by my former and present PhD students and of the various stimulating discussions with colleagues in the Cytogenetics Laboratory, all of which helped develop new ideas. The technical and other support by the different support staff in the laboratory has been invaluable. I thank Mary-Lou Pardue, Caroline Jolly and Davide F Corona for collaborating and sharing ideas/reagents. I thank H Saumweber for developing the remarkable collection of monoclonal antibodies against a large variety of nuclear proteins and making them available for our work and which were largely responsible for appreciation of the omega speckles. The generous and ‘no-questions-asked’ approach of the fly community in sharing fly stocks and other reagents has been a great support. I also thank the various funding agencies in India (University Grants Commission, Board of Research in Nuclear Sciences, Indian National Science Academy, Council of Scientific and Industrial Research, Department of Science & Technology and Department of Biotechnology) for supporting my research on various topics at different times. I also thank the anonymous reviewers of this manuscript for their very useful comments/suggestions.

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  1. Cytogenetics Laboratory, Department of Zoology, Banaras Hindu University, Varanasi, 221 005, India

    Subhash C Lakhotia

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[Lakhotia SC 2011 Forty years of the 93D puff of Drosophila melanogaster. J. Biosci. 36 399–423] DOI 10.1007/s12038-011-9078-1

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Lakhotia, S.C. Forty years of the 93D puff of Drosophila melanogaster . J Biosci 36, 399–423 (2011). https://doi.org/10.1007/s12038-011-9078-1

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