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The 93D heat shock locus InDrosophila: A review

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Abstract

One of the major heat shock induced genes ofDrosophila melanogaster is located in the 93D6-7 bands of polytene chromosomes. The 93D locus shows many unique and intriguing features which are reviewed here. This locus is induced selectively and independently of the other heat shock loci by very diverse agents. The heat shock inducibility of this locus shows a remarkable dependence on the developmental history of the organism, its genetic background and other specific inducers of 93D. In all species ofDrosophila so far tested, one of the major heat shock loci is also selectively induced by the same set of 93D inducers and thus this locus is conserved in the genus. However, cloning and molecular characterisation of the primary DNA base sequence of the 93D ofD. melanogaster and the 93D-like locus ofD. hydei (the 2–48C locus) reveal that except for certain small stretches, the primary DNA base sequence of this locus has diverged rapidly. Interestingly, the structural organisation of the 93D ofD. melanogaster and 2–48C ofD. hydei is remarkably similar-both have a 5’ unique sequence followed on the 3’ end by a long stretch of a species-specific repetitive sequence apparently unique to the locus. Heat shock in both cases induces 3 major transcripts: a long 10–12 kb RNA covering the 5’ unique and 3’ repeat part, a 1.9–2.0 kb RNA complementary to the 5’ unique part and a 1.2 kb transcript which lacks the 0.7 kb “intron” of the 2 kb RNA. None of the transcripts in either species has any appreciable open reading frames, and other evidence also suggests that the 93D or 2–48C loci do not code for any polypeptide. Functions of 93D or 93D-like loci remain uncertain although the locus is essential for ecdysone-induced differentiation of imaginal disks and viability of flies. Strong evidence exists that the activity pattern of the 93D heat shock locus inD. melanogaster distinctly influences heat shock puffing of the 87C locus, one of the two duplicate loci carrying the coding sequences for the major 70 kd heat shock polypeptide; presently available evidence suggests that this effect on 87C puffing is mediated via the mid-repetitive and heat-inducibleaß sequences residing at the 87C locus. The strong conservation of its inducible properties, of the organisation rather than the primary DNA base sequence and of the pattern of heat shock transcripts of 93D locus in the genusDrosophila point to important but hitherto little understood functions of this locus. The structure of its transcripts may have vital regulatory roles.

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References

  • Abd-el-Wahab A and Sirlin J L 1959 Nucleolar RNA and hormone production in the ring gland of Drosophila.Exp. Cell Res. 18: 301–312

    Article  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 ofDrosophila melanogaster.Chromosoma 21: 398–428

    Article  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Atkinson B G and Walden D B (eds) 1985Changes in eukaryotic gene expression in response to environmental stimuli (New York: Academic Press)

    Google Scholar 

  • Babu A K, Shah V C and Lakhotia S C 1980 Effect of benzamide on mitosis and chromosomes in mammalian cells in vitro.Indian J. Exp. Biol. 18: 329–332

    PubMed  CAS  Google Scholar 

  • Behnel H J 1982 Comparative study of protein synthesis and heat shock puffing activity inD. melanogaster glands treated with chloramphenicol.Exp. Cell Res. 142: 223–228

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Berendes H D 1972 The control of puffing inDrosophila hydei. InDevelopmental studies on giant chromosomes (ed.) W Beermann (Berlin, Heidelberg, New York: Springer-Verlag) pp. 181–207

    Google Scholar 

  • Blackman R K and Meselson M 1986 Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp 82 gene.J. Mol. Biol. 188: 499–515

    Article  PubMed  CAS  Google Scholar 

  • Bonner J J and Kerby R L 1982 RNA polymerase II transcribes all of the heat shock induced genes ofDrosophila melanogaster.Chromosoma 85: 93–108

    Article  PubMed  CAS  Google Scholar 

  • Bonner J J and Pardue M L 1976a The effect of heat shock on RNA synthesis in Drosophila tissues.Cell 8: 43–50

    Article  PubMed  CAS  Google Scholar 

  • Bonner J J and Pardue M L 1976b Ecdysone stimulated RNA synthesis in imaginal disks ofDrosophila melanogaster.Chromosoma 58: 87–99

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Burdette W J and Anderson R 1965 Puffing of salivary glands after treatment with carbon dioxide.Nature (London) 208: 409–410

    Article  CAS  Google Scholar 

  • Burma P K and Lakhotia S C 1984 Cytological identity of 93D-like and 87C-like heat shock loci inDrosophila pseudoobscura.Indian J. Exp. Biol. 22: 577–580

    CAS  Google Scholar 

  • Burma P K and Lakhotia S C 1986a Expression of 93D heat shock puff ofDrosophila melanogaster in deficiency genotypes and its influence on the activity of the 87C puff.Chromosoma 94: 273–278

    Article  Google Scholar 

  • Burma P K and Lakhotia S C 1986b Sequence homology of 58C heat shock puff ofD. pseudoobscura with heat shock genes ofD. melanogaster. Xth All India Cell Biol. Conf. Abstr. (Ahmedabad: Gujerat University) p. 84

    Google Scholar 

  • Caizzi R and Ritossa F 1983 The enzyme glutamine synthetase I ofD. melanogaster is associated with a modified RNA.Biochem. Genet. 21: 267–285

    Article  PubMed  CAS  Google Scholar 

  • Carmona M J, Morcillo G, Galler R, Martinez-Sales, dela Campas A G, Diez J L and Edström J E 1985 Cloning and molecular characterization of a telomeric sequence from a temperature-induced balbiani ring.Chromosoma 92: 108–115

    Article  CAS  Google Scholar 

  • Cleaver J E, Milam K M and Morgan W F 1985 Do inhibitor studies demonstrate a role for poly(ADP-ribose) in DNA repair?Radiation Res. 101: 16–28

    Article  PubMed  CAS  Google Scholar 

  • Compton J L and McCarthy B J 1978 Induction of Drosophila heat shock response in isolated polytene nuclei.Cell 14: 191–201

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Derksen J 1975 Induced RNA production in different cell types of Drosophila.Cell Differ. 4: 1–10

    Article  PubMed  CAS  Google Scholar 

  • Derksen J, Berendes H D and Wiliart E 1973 Production and release of a locus specific ribonucleoprotein product in polytene nuclei ofD. hydei.J. Cell Biol. 59: 661–668

    Article  PubMed  CAS  Google Scholar 

  • Devlin R H, Grigliatti T A and Holm D G 1984 Dosage compensation is transcriptionally regulated in autosomal trisomics of Drosophila.Chromosoma 91: 65–73

    Article  CAS  Google Scholar 

  • Devlin R H, Grigliatti T A and Holm D G 1985 Gene dosage compensation in trisomics ofD. melanogaster.Dev. Genet. 6: 39–58

    Article  Google Scholar 

  • Devlin RH, Holm D G and Grigliatti. T A 1982 Autosomal dosage compensation inD. melanogaster strain trisomic for the left arm of chromosome 2.Proc. Natl. Acad. Sci. USA 79: 1200–1204

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Garbe J C, Bendena W G, Alfano M and Pardue M L 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 

  • Garbe J C and Pardue M L 1986 Heat shock locus 93D ofD. melanogaster; a spliced RNA most strongly conserved in the intron sequence.Proc. Natl. Acad. Sci. USA 83: 1812–1816

    Article  PubMed  CAS  Google Scholar 

  • Hellmund D and Serfling E 1984 Structure of hsp coding genes in Drosophila. InHeat shock response in eukaryotic cells (ed.) L Nover (Berlin, Heidelberg, New York: Springer-Verlag) pp. 18–27

    Google Scholar 

  • Henikoff S 1980 A more conventional view of the “ebony” gene.Drosoph. Inf. Serv. 55: 61–62

    Google Scholar 

  • Hotta Y and Shepard J 1973 Biochemical aspects of colchicine action on meiotic cells.Mol. Gen. Genet. 122: 243–260

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ish-Horowicz D, Holden J J and Gehring W J 1977 Deletions of two heat activated loci inD. melanogaster and their effects on heat induced protein synthesis.Cell 12: 643–652

    Article  PubMed  CAS  Google Scholar 

  • Kar Chowdhuri D and Lakhotia S C 1986a Different effects of 93D on 87C heat shock puff activity inD. melanogaster andD. simulans.Chromosoma 94: 279–284

    Article  Google Scholar 

  • Kar Chowdhuri D and Lakhotia S C 1986b Position effect variegation at the 93D heat shock gene inD. melanogaster Xth All India Cell Biol. Conf. Abs. (Ahmedabad: Gujerat University) p. 82

    Google Scholar 

  • Korohoda W and Wohlfarth-Bottermann K E 1976 Effects of relaxation and contraction stimulating solutions on the structure of cyloplasmic fibrils in plasmodia ofPhysarum polycephalum.Acta Protozool. 15: 195–202

    Google Scholar 

  • Lakhotia S C and Mukherjee A S 1970 Activation of a specific puff by benzamide inD. melanogaster.Drosoph. Inf. Serv. 45: 108

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lakhotia S C and Pardue M L 1986 The 93D effects on heat shock puffing at 87C inDrosophila melanogaster are due to changing levels of the transcripts.9th All India Cell Biol. Conf. Abstr. (Pune: Poona University) p. 68

    Google Scholar 

  • Lakhotia S C and Singh A K 1982 Conservation of the 93D puff ofD. melanogaster in different species of Drosophila.Chromosoma 86: 265–278

    Article  Google Scholar 

  • Lakhotia S C and Singh A K 1985 Non-inducibility of the 93D heat shock puff in cold-reared larvae ofD. melanogaster.Chromosoma 92: 48–54

    Article  Google Scholar 

  • Leenders H J, Derksen J, Mass P M J M and Berendes H D 1973 Selective induction of a giant puff inD. hydei by vitamin B6 and derivatives.Chromosoma 41: 447–460

    Article  CAS  Google Scholar 

  • Leenders H J and Knoppien W G 1973 Respiration of larval salivary gland of Drosophila in relation to the activity of the specific genome loci.J. Insect Physiol. 19: 1793–1800

    Article  PubMed  CAS  Google Scholar 

  • Lengyel J A, Ransom L J, Graham M L and Pardue M L 1980 Transcription and metabolism of RNA from theD. melanogaster puff site 93D.Chromosoma 80: 237–252

    Article  PubMed  CAS  Google Scholar 

  • Lubsen N H, Sondermeijer P J A, Pages M and Alonso C 1978In situ hybridization of nuclear and cytoplasmic RNA to locus 2-48BC inD. hydei.Chromosoma 65: 199–212

    Article  PubMed  CAS  Google Scholar 

  • Mohler J and Pardue M L 1982a Deficiency mapping of the 93D heat shock locus in Drosophila.Chromosoma 86: 457–467

    Article  PubMed  CAS  Google Scholar 

  • Mohler J and Pardue M L 1982b Genetic analysis of the region of the 93D heat-shock locus. InHeat shock from bacteria to man. (eds) M J Schlesinger, M Ashburner and A Tissieres (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory) pp. 77–82

    Google Scholar 

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

    PubMed  Google Scholar 

  • Mukherjee T and Lakhotia S C 19793H-uridine incorporation in the puff 93D and in chromocentric heterochromatin of heat shocked salivary glands ofD. melanogaster.Chromosoma 74: 75–82

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Nover L (ed.) 1984Heat shock response of eukaryotic cells (Berlin, Heidelberg, New York: Springer-Verlag) pp. 1–82

    Google Scholar 

  • Painter R B 1985 3-aminobenzamide does not affect radiation induced inhibition of DNA synthesis in human cells.Mutation Res. 143: 113–115

    PubMed  CAS  Google Scholar 

  • Pardue M L, Bendena W G and Garbe J C 1987 Heat shock: puffs and response to environmental stress. InResults and problems in cell differentiation (ed.) W Hennig (Berlin, Heidelberg: Springer-Verlag) 14: 121–131

    Google Scholar 

  • Peters F P A M N, Lubsen N H and Sondermeijer P J A 1980 Rapid sequence divergence in a heat shock locus of Drosophila.Chromosoma 81: 271–280

    Article  PubMed  CAS  Google Scholar 

  • Peters F P A M N, Lubsen N H, Walldorf U, Moormann R J M and Hovemann B 1984 The unusual structure of heat shock locus 2-48B inDrosophila hydei.Mol. Gen. Genet 197: 392–398

    Article  PubMed  CAS  Google Scholar 

  • Ritossa F 1962 A new puffing pattern induced by heat shock and DNP in Drosophila.Experientia 18: 571–573

    Article  CAS  Google Scholar 

  • Ritossa F 1964 Experimental activation of specific loci in polytene chromosomes of Drosophila.Exp. Cell Res. 35: 601–607

    Article  PubMed  CAS  Google Scholar 

  • Ryseck R P, Walldorf U and Hovemann B 1985 Two major RNA products are transcribed from heat shock locus 93D ofDrosophila melanogaster.Chromosoma 93: 17–20

    Article  PubMed  CAS  Google Scholar 

  • Salonen K, Paranko J and Parvinen M 1982 A colcemid sensitive mechanism involved in regulation of chromosome movement during meiotic pairing.Chromosoma 85: 611–618

    Article  PubMed  CAS  Google Scholar 

  • Santa-Cruz M C Morcillo G and Diez J L 1984 Ultrastructure of a temperature induced balbiani ring inChironomus thummi.Biol. Cell 52: 205–212

    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 inDrosophila melanogaster.Chromosoma 63: 317–327

    Article  CAS  Google Scholar 

  • Schlesinger M J, Ashburner M and Tissieres A (eds) 1982Heat shock from bacteria to man (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory)

    Google Scholar 

  • Singh A K and Lakhotia S C 1983 Further observations on inducibility of 93D puff ofDrosophila melanogaster by homogenate of heat shocked cells.Indian J. Exp. Biol. 21: 363–366

    Google Scholar 

  • Singh A K and Lakhotia S C 1984 Lack of effect of microtubule poisons on the 93D or 93D-like heat shock puffs in Drosophila.Indian J. Exp. Biol. 22: 569–576

    CAS  Google Scholar 

  • Singh O P and Gupta J P 1985 Differential induction of chromosome puffs in two cell types ofMelanogromyza obtusa.Chromosoma 91: 359–362

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Spradling A, Pardue M L and Penman S 1977 Messenger RNA in heat shocked Drosophila cells.J. Mol. Biol. 109: 559–587

    Article  PubMed  CAS  Google Scholar 

  • Spruill W A, Hurwitz D R, Lucchesi J C and Steiner A L 1978 Association of cyclic GMP with gene expression of polytene chromosomes of salivary glands ofDrosophila melanogaster.Proc. Nail. Acad. Sci. USA 75: 1480–1484

    Article  CAS  Google Scholar 

  • Srivastava J P and Bangia K K 1985 Specific activation of puff 93D in the polytene chromosomes of salivary glands ofDrosophila melanogaster by paracetamol.J. Curr. Biosci. 2: 48–50

    Google Scholar 

  • Swift H 1965 Nuclear morphology of the chromosome.In Vitro 1: 26–49

    Article  Google Scholar 

  • Walldorf U, Richter S, Ryseck R P, Steller H, Edstrom J E, Bautz E K F and Hovemann B 1984 Cloning of heat shock locus 93D fromDrosophila melanogaster.EMBO J. 3: 2499–2504

    PubMed  CAS  Google Scholar 

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

    S C Lakhotia

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Lakhotia, S.C. The 93D heat shock locus InDrosophila: A review. J. Genet. 66, 139–157 (1987). https://doi.org/10.1007/BF02931660

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