Stress Induction of Bm1 RNA in Silkworm Larvae: SINEs, an Unusual Class of Stress Genes

Overview

Journal Cell Stress Chaperones

Publisher Elsevier

Specialty Cell Biology

Date 2001 Oct 16

PMID 11599568

Citations 14

Authors

R H Kimura

P V Choudary

K K Stone

C W Schmid

Affiliations

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Abstract

This study surveys the induction of RNA polymerase III (Pol III)-directed expression of short interspersed element (SINE) transcripts by various stresses in an animal model, silkworm larvae. Sublethal heat shock and exposure to several toxic compounds increase the level of Bm1 RNA, the silkworm SINE transcript, while also transiently increasing expression of a well-characterized stress-induced transcript, Hsp70 messenger RNA (mRNA). In certain cases, the Bm1 RNA response coincides with that of Hsp70 mRNA, but more often Bm1 RNA responds later in recovery. Baculovirus infection and exposure to certain toxic compounds increase Bm1 RNA but not Hsp70 mRNA, showing that SINE induction is not necessarily coupled to transcription of this particular heat shock gene. SINEs behave as an additional class of stress-inducible genes in living animals but are unusual as stress genes because of their high copy number, genomic dispersion, and Pol III-directed transcription.

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References

Li T, Spearow J, Rubin C, Schmid C . Physiological stresses increase mouse short interspersed element (SINE) RNA expression in vivo. Gene. 1999; 239(2):367-72. DOI: 10.1016/s0378-1119(99)00384-4. View

Kimura R, Choudary P, Schmid C . Silk worm Bm1 SINE RNA increases following cellular insults. Nucleic Acids Res. 1999; 27(16):3380-7. PMC: 148573. DOI: 10.1093/nar/27.16.3380. View

Singh K, Carey M, Saragosti S, Botchan M . Expression of enhanced levels of small RNA polymerase III transcripts encoded by the B2 repeats in simian virus 40-transformed mouse cells. Nature. 1985; 314(6011):553-6. DOI: 10.1038/314553a0. View

Maeda S, Kawai T, Obinata M, Fujiwara H, Horiuchi T, Saeki Y . Production of human alpha-interferon in silkworm using a baculovirus vector. Nature. 1985; 315(6020):592-4. DOI: 10.1038/315592a0. View

Adams D, Eickbush T, Herrera R, Lizardi P . A highly reiterated family of transcribed oligo(A)-terminated, interspersed DNA elements in the genome of Bombyx mori. J Mol Biol. 1986; 187(4):465-78. DOI: 10.1016/0022-2836(86)90327-x. View

Fornace Jr A, Mitchell J . Induction of B2 RNA polymerase III transcription by heat shock: enrichment for heat shock induced sequences in rodent cells by hybridization subtraction. Nucleic Acids Res. 1986; 14(14):5793-811. PMC: 311592. DOI: 10.1093/nar/14.14.5793. View

Carey M, Singh K, Botchan M, Cozzarelli N . Induction of specific transcription by RNA polymerase III in transformed cells. Mol Cell Biol. 1986; 6(9):3068-76. PMC: 367041. DOI: 10.1128/mcb.6.9.3068-3076.1986. View

Wilson E, Condliffe D, Sprague K . Transcriptional properties of BmX, a moderately repetitive silkworm gene that is an RNA polymerase III template. Mol Cell Biol. 1988; 8(2):624-31. PMC: 363188. DOI: 10.1128/mcb.8.2.624-631.1988. View

Matsumoto K, TAKII T, Okada N . Characterization of a new termination signal for RNA polymerase III responsible for generation of a discrete-sized RNA transcribed from salmon total genomic DNA in a HeLa cell extract. J Biol Chem. 1989; 264(2):1124-31. View

10.

Jang K, Latchman D . The herpes simplex virus immediate-early protein ICP27 stimulates the transcription of cellular Alu repeated sequences by increasing the activity of transcription factor TFIIIC. Biochem J. 1992; 284 ( Pt 3):667-73. PMC: 1132590. DOI: 10.1042/bj2840667. View

11.

Jang K, Collins M, Latchman D . The human immunodeficiency virus tat protein increases the transcription of human Alu repeated sequences by increasing the activity of the cellular transcription factor TFIIIC. J Acquir Immune Defic Syndr (1988). 1992; 5(11):1142-7. View

12.

Panning B, SMILEY J . Activation of RNA polymerase III transcription of human Alu repetitive elements by adenovirus type 5: requirement for the E1b 58-kilodalton protein and the products of E4 open reading frames 3 and 6. Mol Cell Biol. 1993; 13(6):3231-44. PMC: 359768. DOI: 10.1128/mcb.13.6.3231-3244.1993. View

13.

Pryor W, Stone K . Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci. 1993; 686:12-27; discussion 27-8. DOI: 10.1111/j.1749-6632.1993.tb39148.x. View

14.

Liu W, Maraia R, Rubin C, Schmid C . Alu transcripts: cytoplasmic localisation and regulation by DNA methylation. Nucleic Acids Res. 1994; 22(6):1087-95. PMC: 307934. DOI: 10.1093/nar/22.6.1087. View

15.

Stone K, Bermudez E, Pryor W . Aqueous extracts of cigarette tar containing the tar free radical cause DNA nicks in mammalian cells. Environ Health Perspect. 1994; 102 Suppl 10:173-8. PMC: 1566999. DOI: 10.1289/ehp.94102s10173. View

16.

Stone K, Bermudez E, Zang L, Carter K, Queenan K, Pryor W . The ESR properties, DNA nicking, and DNA association of aged solutions of catechol versus aqueous extracts of tar from cigarette smoke. Arch Biochem Biophys. 1995; 319(1):196-203. DOI: 10.1006/abbi.1995.1282. View

17.

Liu W, Chu W, Choudary P, Schmid C . Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res. 1995; 23(10):1758-65. PMC: 306933. DOI: 10.1093/nar/23.10.1758. View

18.

Russanova V, Driscoll C, Howard B . Adenovirus type 2 preferentially stimulates polymerase III transcription of Alu elements by relieving repression: a potential role for chromatin. Mol Cell Biol. 1995; 15(8):4282-90. PMC: 230667. DOI: 10.1128/MCB.15.8.4282. View

19.

Schmid C . Alu: structure, origin, evolution, significance and function of one-tenth of human DNA. Prog Nucleic Acid Res Mol Biol. 1996; 53:283-319. DOI: 10.1016/s0079-6603(08)60148-8. View

20.

Gao G, Herrera R . Enrichment of middle repetitive element Bm-1 transcripts in translationally active RNA fractions of the silkmoth, Bombyx mori. Genetica. 1996; 97(2):173-82. DOI: 10.1007/BF00054624. View