Identification and Characterization of a Juvenile Hormone (JH) Response Region in the JH Esterase Gene from the Spruce Budworm, Choristoneura fumiferana

Using a differential display of mRNA technique we discovered that the juvenile hormone (JH) esterase gene (Cfjhe) from Choristoneura fumiferana is directly induced by juvenile hormone I (JH I), and the JH I induction is suppressed by 20-hydroxyecdysone (20E). To study the mechanism of action of these two hormones in the regulation of expression of this gene, we cloned the 1270-bp promoter region of the Cfjhe gene and identified a 30-bp region that is located between –604 and –574 and is sufficient to support both JH I induction and 20E suppression. This 30-bp region contains two conserved hormone response element half-sites separated by a 4-nucleotide spacer similar to the direct repeat 4 element and is designated as a putative juvenile hormone response element (JHRE). In CF-203 cells, a luciferase reporter placed under the control of JHRE and a minimal promoter was induced by JH I in a dose- and time-dependent manner. Moreover, 20E suppressed this JH I-induced luciferase activity in a dose- and time-dependent manner. Nuclear proteins isolated from JH I-treated CF-203 cells bound to JHRE and the binding was competed by a 100-fold excess of the cold probe but not by 100-fold excess of double-stranded oligonucleotides of unrelated sequence. JH I induced/modified nuclear proteins prior to their binding to JHRE and 20E suppressed this JH I induction/modification. These results suggest that the 30-bp JHRE identified in the Cfjhe gene promoter is sufficient to support JH induction and 20E suppression of the Cfjhe gene. Using a differential display of mRNA technique we discovered that the juvenile hormone (JH) esterase gene (Cfjhe) from Choristoneura fumiferana is directly induced by juvenile hormone I (JH I), and the JH I induction is suppressed by 20-hydroxyecdysone (20E). To study the mechanism of action of these two hormones in the regulation of expression of this gene, we cloned the 1270-bp promoter region of the Cfjhe gene and identified a 30-bp region that is located between –604 and –574 and is sufficient to support both JH I induction and 20E suppression. This 30-bp region contains two conserved hormone response element half-sites separated by a 4-nucleotide spacer similar to the direct repeat 4 element and is designated as a putative juvenile hormone response element (JHRE). In CF-203 cells, a luciferase reporter placed under the control of JHRE and a minimal promoter was induced by JH I in a dose- and time-dependent manner. Moreover, 20E suppressed this JH I-induced luciferase activity in a dose- and time-dependent manner. Nuclear proteins isolated from JH I-treated CF-203 cells bound to JHRE and the binding was competed by a 100-fold excess of the cold probe but not by 100-fold excess of double-stranded oligonucleotides of unrelated sequence. JH I induced/modified nuclear proteins prior to their binding to JHRE and 20E suppressed this JH I induction/modification. These results suggest that the 30-bp JHRE identified in the Cfjhe gene promoter is sufficient to support JH induction and 20E suppression of the Cfjhe gene. Although the biological actions of Juvenile hormones (JHs) 1The abbreviations used are: JH, juvenile hormone; 20E, 20-hydroxyecdysone; Cfjhe, juvenile hormone esterase gene; RXR, retinoid X receptor; FXR, farnesoid X-activated receptor; DTT, dithiothreitol; JHRE, juvenile hormone response element; RE, response element; DR4, direct repeat 4; EMSA, electrophoretic mobility shift assay; USP, ultraspiracle. 1The abbreviations used are: JH, juvenile hormone; 20E, 20-hydroxyecdysone; Cfjhe, juvenile hormone esterase gene; RXR, retinoid X receptor; FXR, farnesoid X-activated receptor; DTT, dithiothreitol; JHRE, juvenile hormone response element; RE, response element; DR4, direct repeat 4; EMSA, electrophoretic mobility shift assay; USP, ultraspiracle. in insect development and reproduction are well documented, the molecular mechanisms underlying JH action are poorly understood (1Riddiford L.M. Adv. Insect Physiol. 1994; 24: 213-274Crossref Scopus (502) Google Scholar, 2Wyatt G. Davey K. Adv. Insect Physiol. 1996; 26: 1-155Crossref Scopus (429) Google Scholar, 3Jones G. Annu. Rev. Entomol. 1995; 40: 147-169Crossref PubMed Scopus (82) Google Scholar, 4Cusson M. Palli S.R. Canadian Entomologist. 2000; 132: 263-280Crossref Scopus (21) Google Scholar, 5Gilbert L.I. Granger N.A. Roe R.M. Insect Biochem. Mol. Biol. 2000; 30: 617-644Crossref PubMed Scopus (346) Google Scholar). Several possible modes of actions have been proposed for JH. Direct action of JH in regulation of genes such as jhp21 (6Zhang J. Saleh D.S. Wyatt G.R. Mol. Cell. Endocrinol. 1996; 122: 15-20Crossref PubMed Scopus (36) Google Scholar), juvenile hormone esterase (7Wroblewski V.J. Harshman L.G. Hanzlik T.N. Hammock B.D. Arch. Biochem. Biophys. 1990; 278: 461-466Crossref PubMed Scopus (55) Google Scholar, 8Feng Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar), calmodulin (9Iyengar A.R. Kunkel J.G. Dev. Biol. 1995; 170: 314-320Crossref PubMed Scopus (16) Google Scholar), vitellogenin (10Comas D. Piulachs M.D. Belles X. Insect Biochem. Mol. Biol. 1999; 29: 821-827Crossref PubMed Scopus (52) Google Scholar), and several others have been reported (11Hirai M. Yuda M. Shinoda T. Chinzei Y. Insect Biochem. Mol. Biol. 1998; 28: 181-189Crossref PubMed Scopus (26) Google Scholar, 12Dubrovsky E.B. Dubrovskaya V.A. Bilderback A.L. Berger E.M. Dev. Biol. 2000; 224: 486-495Crossref PubMed Scopus (82) Google Scholar). Through indirect action, JH was shown to modulate 20-hydroxyecdysone (20E) action by affecting the expression of genes in a 20E-induced cascade (13Zhou B. Hiruma K. Shinoda T. Riddiford L.M. Dev. Biol. 1998; 203: 233-244Crossref PubMed Scopus (159) Google Scholar, 14Zhou X. Riddiford L.M. Development. 2002; 129: 2259-2269PubMed Google Scholar). Totally different from the above genomic actions, in ovarian follicular epithelium, JH acts through a membrane receptor to bring about rapid enzyme activation without the need for new transcription (15Sevala V.L. Davey K.G. Experientia. 1989; 45: 355-356Crossref Scopus (78) Google Scholar). Numerous attempts have been made to identify JH receptors. Palli et al. (16Palli S. Hiruma K. Riddiford L. Insect Biochem. 1991; 21: 7-15Crossref Scopus (39) Google Scholar) used human retinoic acid receptor cDNA as a probe and identified a steroid/thyroid superfamily member from Manduca sexta. Further characterization of this cDNA revealed that this is not a JH receptor but, rather, an ecdysone-induced transcription factor that plays a critical role in ecdysone signal transduction and is related to Drosophila hormone receptor 3 (17Koelle M.R. Segraves W.A. Hogness D.S. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 6167-6171Crossref PubMed Scopus (158) Google Scholar), subsequently named Manduca hormone receptor 3 (18Palli S.R. Hiruma K. Riddiford L.M. Dev. Biol. 1992; 150: 306-318Crossref PubMed Scopus (113) Google Scholar). The 29-kDa nuclear protein identified in M. sexta epidermis turned out to be a low affinity JH-binding protein (19Palli S.R. Touhara K. Charles J.P. Bonning B.C. Atkinson J.K. Trowell S.C. Hiruma K. Goodman W.G. Kyriakides T. Prestwich G.D. Hammock B.D. Riddiford L.M. Proc. Natl. Acad. Sci. U. S. A. 1994; 91: 6191-6195Crossref PubMed Scopus (57) Google Scholar, 20Charles J.-P. Wojtasek H. Lentz A.J. Thomas B.A. Bonning B.C. Palli S.R. Parker A.G. Dorman G. Hammock B.D. Prestwich G.D. Riddiford L.M. Adv. Insect Physiol. 1996; 31: 371-393Google Scholar). The mammalian retinoid X receptor (RXR) forms a heterodimer with several nuclear receptors including the farnesoid X-activated receptor (FXR). JH III but not JH acid or methoprene can bind/activate the FXR and RXR heterodimer (21Forman B.M. Goode E. Chen J. Oro A.E. Bradley D.J. Perlmann T. Noonan D.J. Burka L.T. McMorris T. Lamph W.W. Evans R.M. Weinberger C. Cell. 1995; 81: 687-693Abstract Full Text PDF PubMed Scopus (937) Google Scholar). Methoprene and methoprene acid but not JH III can activate RXR (22Harmon M.A. Boehm M.F. Heyman R.A. Mangelsdorf D.J. Proc. Natl. Acad. Sci. U. S. A. 1995; 92: 6157-6160Crossref PubMed Scopus (197) Google Scholar). These two studies suggested that RXR or its insect homologue ultraspiracle (USP) could play an important role in signal transduction of JH or JH-related compounds. Jones and Sharp (23Jones G. Sharp P.A. Proc. Natl. Acad. Sci. U. S. A. 1997; 94: 13499-13503Crossref PubMed Scopus (237) Google Scholar) showed that both JH III and JHB3 bind to a USP homodimer from Drosophila melanogaster. Subsequent studies showed that USP from D. melanogaster can bind to the DR12 response element and a reporter gene placed under the control of the DR12 response element fused to the jhe core promoter was induced by JH III (24Xu Y. Fang F. Chu Y. Jones D. Jones G. Eur. J. Biochem. 2002; 269: 6026-6036Crossref PubMed Scopus (67) Google Scholar). A D. melanogaster mutant tolerant to methoprene (Met) was identified (25Wilson T.G. Fabian J. Dev. Biol. 1986; 118: 190-201Crossref PubMed Scopus (185) Google Scholar). An 85-kDa protein isolated from Met flies showed a 6-fold lower affinity than the wild-type protein for JH III (26Shemshedini L. Lanoue M. Wilson T.G. J. Biol. Chem. 1990; 265: 1913-1918Abstract Full Text PDF PubMed Google Scholar). The Met gene was cloned and found to be a member of the basic helix-loop-helix-PER-AHR/ARNT-SIM (PAS) family of transcriptional regulators (27Ashok M. Turner C. Wilson T.G. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2761-2766Crossref PubMed Scopus (243) Google Scholar). Met is not a vital gene, as shown by the production of a null mutant allele that is viable (28Wilson T.G. Ashok M. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 14040-14044Crossref PubMed Scopus (99) Google Scholar), but this finding could reflect functional redundancy of Met. The Met gene product was detected in several tissues, including known JH response tissues (29Pursley S. Ashok M. Wilson T.G. Insect Biochem. Mol. Biol. 2000; 30: 839-845Crossref PubMed Scopus (57) Google Scholar). To clone JH receptor cDNA, several approaches, including characterization of JH response gene promoters to identify JH response elements to be used for screening expression libraries to isolate JH receptors, are being pursued. Several JH-responsive including and protein have been identified (9Iyengar A.R. Kunkel J.G. Dev. Biol. 1995; 170: 314-320Crossref PubMed Scopus (16) Google Scholar, M. Yuda M. Shinoda T. Chinzei Y. Insect Biochem. Mol. Biol. 1998; 28: 181-189Crossref PubMed Scopus (26) Google Scholar, Wyatt G.R. Biochem. Mol. Biol. 1995; Google Scholar). JH response gene, was identified in and a response element been identified in the promoter region of this gene (6Zhang J. Saleh D.S. Wyatt G.R. Mol. Cell. Endocrinol. 1996; 122: 15-20Crossref PubMed Scopus (36) Google Scholar). of protein that to this response element to the that this protein is a transcription factor by JH and that in regulation of expression of JH response genes S. J. M. Chinzei Y. H. Wyatt G.R. Mol. Cell. Endocrinol. 2002; PubMed Scopus Google Scholar). of these genes a of induction in response to JH that not be directly by a In Manduca sexta cells, a JH-binding protein gene is induced by JH I of and to be a response gene Goodman W.G. Mol. Cell. Endocrinol. 1999; PubMed Scopus (21) Google Scholar). CF-203 cells from of Choristoneura fumiferana and to both 20E and JH Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar, S.S. Mol. Biol. 1995; Google Scholar, S.R. Ladd T.R. A.R. Sohi S.S. Retnakaran A. Dev. 1997; PubMed Scopus Google Scholar, S.R. Ladd T.R. Sohi S.S. Retnakaran A. Insect Biochem. Mol. Biol. 1996; 26: PubMed Scopus (55) Google Scholar). have used differential display of technique and identified Cfjhe gene as a JH response gene Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar). This gene is directly induced by JH I the hormone in the of protein The expression of Cfjhe gene is suppressed by 20E in the of induction by JH I and suppression by 20E are dose- and time-dependent Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar). the Cfjhe gene is of the of genes expression is directly by both JH and and characterization of the promoter region of Cfjhe gene is for the mechanism of JH induction and 20E suppression of Cfjhe gene a C. fumiferana genomic and identified a 1270-bp that is located of the Cfjhe gene transcription of this 1270-bp genomic reporter in CF-203 cells identified a 30-bp region located between –604 and –574 that is sufficient to support both JH induction and 20E suppression of JH induction of Cfjhe gene. Nuclear proteins isolated from CF-203 cells that to JH bound to this 30-bp JH response CF-203 a was from the of C. fumiferana S.S. Mol. Biol. 1995; Google Scholar). 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Ladd T.R. Sohi S.S. Retnakaran A. Insect Biochem. Mol. Biol. 1996; 26: PubMed Scopus (55) Google Scholar). Cfjhe identify JH and 20E response in the Cfjhe we a C. fumiferana genomic with Cfjhe gene cDNA as a probe and identified genomic with an of of by and the Cfjhe gene cDNA as a probe identified a genomic a 1270-bp region that is located to the transcription This genomic was and from both The of this genomic showed a conserved transcription from the mRNA Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar) and a to the transcription A of the 1270-bp to that is to the transcription and showed a with half-sites of several known response elements including and both half-sites of of these showed a with the 1270-bp sequence. of the putative are shown in This a repeat of separated by in This 1270-bp showed with the found in the region of jhe M. Jones G. Dev. 1994; PubMed Scopus Google Scholar). a hormone response element that is similar to identified in T. jhe promoter is not found in the Cfjhe of the JH to of the 1270-bp Cfjhe promoter region and cloned luciferase reporter The is to the transcription of The that is between transcription and of mRNA was in These in CF-203 The that the Cfjhe promoter region from to to to and to showed to induction of luciferase reporter activity in the of JH I with the activity in the of the the that the Cfjhe promoter region from to showed and the that to not induction of reporter activity in the of JH These results showed that the JH I response region in the Cfjhe promoter is located between and from the transcription The hormone 20-hydroxyecdysone (20E) not reporter activity through of the but was to JH I-induced reporter activity both hormones These results showed that the region of the Cfjhe promoter that between and was to support both JH induction and 20E suppression as for Cfjhe gene Q.L. 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Biol. 1995; Google Scholar) the luciferase reporter gene is by 30-bp JHRE fused to the Cfjhe gene core to or CF-203 The cells to JH 20E, or JH I shown in the 30-bp region from the Cfjhe promoter is sufficient to support JH I induction as well as 20E suppression of JH I-induced reporter The luciferase reporter in was not induced by JH I or 20E or both in response and of JH I JH I induction of reporter activity through the 30-bp Cfjhe promoter is both JH I dose- and The induction of reporter activity as low as JH I and with the of JH I and of JH I was a in reporter activity of JH I This be to the of hormone to the The induction of reporter activity with an in and by the hormone was a in reporter activity by and Nuclear from CF-203 to JHRE from the Cfjhe promoter to nuclear proteins that are in CF-203 cells, we an electrophoretic mobility shift Nuclear from JH I-treated and CF-203 cells, and the nuclear proteins with double-stranded oligonucleotides 30-bp JHRE shown in the nuclear proteins isolated from JH I-treated CF-203 cells bound to the JHRE, and the binding was competed by a 100-fold excess cold probe but not by a 100-fold excess double-stranded oligonucleotides of unrelated that the binding is To nuclear proteins that bind to JHRE need prior to JH, we CF-203 cells in the of or JH I for and and the nuclear proteins isolated and by Nuclear proteins from the cells that to JH but not from the cells that to bound to JHRE that JH I or nuclear proteins that bind to JHRE To 20E JH I of nuclear proteins prior to their binding to JHRE, we CF-203 cells in or 20E or of JH I and 20E for the nuclear proteins isolated and for their binding to JHRE by shown in nuclear proteins isolated from JH I-treated cells bound to JHRE, but the nuclear proteins isolated from 20E, or 20E JH I cells not bind to These that JH I nuclear proteins prior to their binding to JHRE and that 20E can this action of JH used in the in a new of for of 30-bp JHRE to Nuclear JHRE and to identify critical for binding to nuclear we mutant of 30-bp JHRE and used in Nuclear proteins isolated from CF-203 cells bound to the 30-bp JHRE and the binding was competed by excess cold probe A excess of a 30-bp a to A in the or in both the half-sites or in the showed These results showed that in repeat elements are important for binding of nuclear proteins to this To the of to the repeat oligonucleotides of the the of JHRE These oligonucleotides showed in as in to the repeat elements showed with the cold The 30-bp JHRE we identified through promoter two the of the a that these two The JHRE competed well for the binding of 30-bp JHRE to nuclear The above results showed that the in the repeat is critical for binding of nuclear proteins to These results showed that of the that are to the are not important in binding of nuclear proteins to JHRE that the two direct repeat elements with a 4-nucleotide spacer is the binding for nuclear we of JHRE conserved in the element to for is or and A or In mutant the was to a found in hormone response of these by showed that and showed with the These in conserved of the element in was to mutant the A in was to and mutant the in to A and the elements to competed well with the probe for binding of nuclear proteins A and These suggest that the element in the 30-bp JHRE is for binding to nuclear proteins isolated from CF-203 To the in the element that is critical for binding of nuclear proteins is important for JH I induction of a reporter gene placed under the control of JHRE, we of the in element and as well as the in found to A of mutant and in CF-203 cells showed that both in element was to A and JH I induction of reporter gene by with The suppression by 20E in these 20E was to JH I-induced reporter the to in not JH I induction or 20E suppression. These suggest that the in the element in the Cfjhe promoter are important for JH I induction of this gene. The of study is the of a 30-bp JHRE the Cfjhe promoter that is sufficient for JH induction and 20E suppression of this induction for Cfjhe gene. Several of support this the luciferase gene was placed under the control of this 30-bp JHRE and the Cfjhe core promoter to JH I induced reporter in 20E suppressed this JH I-induced reporter nuclear proteins isolated from CF-203 cells to JH I bound to this 30-bp of the 1270-bp Cfjhe promoter not support JH I these that the identified 30-bp JHRE is for the JH induction and 20E suppression for the Cfjhe gene Q.L. Ladd T.R. Tomkins B.L. Sundaram M. Sohi S.S. Retnakaran A. Davey K.G. Palli S.R. Mol. Cell. Endocrinol. 1999; 148: 95-108Crossref PubMed Scopus (80) Google Scholar). The 30-bp JHRE contains two direct of with a spacer and these elements with the element A or A or or or and A or showed that the two and A that are in the elements to A and its with probe for binding to nuclear proteins that these two are critical for binding of nuclear proteins to these showed that the oligonucleotides two hormone response element elements that are separated by a 4-nucleotide spacer competed well with 30-bp JHRE probe for binding of nuclear proteins isolated from CF-203 These results suggest that the elements in the Cfjhe promoter are in binding of nuclear proteins isolated from CF-203 In the mutant of the 1270-bp Cfjhe promoter in the in of the element in the 30-bp JHRE was to A and JH I induction by the of to A in element found of Cfjhe promoter not JH I induction of luciferase gene by the Cfjhe These suggest that the elements in the promoter region of the Cfjhe gene are in JH The JHRE found in the promoter region of gene, from L. (6Zhang J. Saleh D.S. Wyatt G.R. Mol. Cell. Endocrinol. 1996; 122: 15-20Crossref PubMed Scopus (36) Google Scholar, S. J. M. Chinzei Y. H. Wyatt G.R. Mol. Cell. Endocrinol. 2002; PubMed Scopus Google Scholar) known hormone response elements the repeat elements with receptor and ultraspiracle bind to both and elements K. Segraves W.A. J. Biol. Chem. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar). The in of the two repeat in JHRE is similar to of the binding identified in the promoter region of the vitellogenin gene from V.A. D. A. PubMed Scopus Google Scholar). To the family of transcription can bind to JHRE identified in the Cfjhe we in made protein K. J. Biol. Chem. 1994; 269: Full Text PDF PubMed Google Scholar). These not the protein that the nuclear proteins binding to JHRE are not similar to protein not Nuclear proteins isolated from CF-203 cells that to JH I but not to bound to the 30-bp JH response region of the Cfjhe promoter that JH I the expression of mRNA or the nuclear proteins prior to their binding to of 3 to JH I is sufficient to the nuclear protein binding to JHRE, we the that the nuclear proteins that bind to JHRE are than their mRNA expression being induced by JH Nuclear proteins that bind to the JHRE in the promoter region of jhp21 gene from L. are through protein that from binding to JHRE S. J. M. Chinzei Y. H. Wyatt G.R. Mol. Cell. Endocrinol. 2002; PubMed Scopus Google Scholar). is that the nuclear proteins that bind to JHRE in the Cfjhe promoter are and nuclear proteins not be to bind to to JH I in of nuclear proteins to their binding to are in to this The identified JHRE be for for through their to bring about the expression of Cfjhe gene. The JHRE identified be for to for new JH for and and for with the CF-203 and of for for the of an for an the of

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