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ste-A fortiori, even at 10 lm, the four diacylhydrazine ligands did not causesignificant changes in expression of endogenous genes in 293 cells andtherefore should have minimum pleiotropi

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endogenous gene expression in 293 cells

Siva K Panguluri1, Bing Li2*, Robert E Hormann2and Subba R Palli1

1 Department of Entomology, College of Agriculture, University of Kentucky, Lexington, KY, USA

2 Intrexon Corporation, Norristown, PA, USA

Gene therapy is used to correct a defect in the

expres-sion of a gene by transferring a gene expresexpres-sion

cas-sette containing a promoter, a terminator, and the

coding region of a gene whose absence or defect causes

a disease Current technology uses constitutive

promot-ers, such as the cytomegalovirus promoter, for

expres-sion of transgenes Such an ‘always on’ arrangement is

not desirable because it can exacerbate pleiotropiceffects and also leaves no option for remediation in theevent of medical complications due to transgeneexpression To address this issue, regulated expression

of the additive or corrective gene becomes attractivefor various gene therapy applications Despite extracomplexity, the regulated expression system can

Keywords

diacylhydrazine; ecdysone; gene therapy;

microarray; RSL-1

Correspondence

S R Palli, Department of Entomology,

College of Agriculture, University of

Kentucky, Lexington, KY 40546 USA

Fax: +1 859 323 1120

Tel: +1 859 257 4962

E-mail: rpalli@uky.edu

*Present address

MicroBiotiX, Inc., Worcester, MA, USA

(Received 24 June 2007, revised 13 August

2007, accepted 4 September 2007)

doi:10.1111/j.1742-4658.2007.06089.x

Regulated gene expression may substantially enhance gene therapy lated with structural differences between insect ecdysteroids and mamma-lian steroids, the ecdysteroids appear to have a benign pharmacologywithout adversely interfering with mammalian signaling systems Conse-quently, the ecdysone receptor-based gene switches are attractive for appli-cation in medicine In the present study, the effect of inducers of ecdysonereceptor switches on the expression of endogenous genes in HEK 293 cellswas determined Four ligand chemotypes, represented by a tetrahydroquin-oline (RG-120499), one amidoketone (RG-121150), two ecdysteroids[20-hydroxyecdysone (20E) and ponasterone A (Pon A)], and four diacyl-hydrazines (RG-102240, RG-102277, RG-102398 and RG-100864), weretested in HEK 293 cells The cells were exposed to ligands at concentra-tions of 1 lm (RG-120499) or 10 lm (all others) for 72 h and the totalRNA was isolated and analyzed using microarrays Microarray datashowed that the tetrahydroquinoline ligand, RG-120499 caused cell death

Corre-at concentrCorre-ations‡ 10 lm At 1 lm, this ligand caused changes in theexpression of genes such as TNF, MAF, Rab and Reprimo At 10 lm, theamidoketone, RG-121150, induced changes in the expression of genes such

as v-jun, FBJ and EGR, but was otherwise noninterfering Of the two roids tested, 20E did not affect gene expression, but Pon A caused somechanges in the expression of endogenous genes At lower concentrationspharmacologically relevant for gene therapy, intrinsic gene expressioneffects of ecdysteroids and amidoketones may actually be insignificant

ste-A fortiori, even at 10 lm, the four diacylhydrazine ligands did not causesignificant changes in expression of endogenous genes in 293 cells andtherefore should have minimum pleiotropic effects when used as ligandsfor the ecdysone receptor gene switch

Abbreviations

AMK, amidoketone; qRT-PCR, quantitative real-time reverse transcription PCR; STAT 6, signal transducer and activator of transcription 6; THQ, tetrahydroquinoline.

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substantially raise the level of safety and might even

be essential to control the expression levels of proteins

that have narrow therapeutic indices, such as

cyto-kinins and hormones

The main purpose of a regulated gene expression

system is to control the timing and levels of transgene

expression in vivo Whether the expressed protein

remains within the cell or, more commonly, is secreted

and⁄ or distributed in extracellular compartments, it

will undergo elimination according to pharmacokinetc

principles [1] Thus, too little protein will be

subthera-peutic, too much will be potentially toxic Therefore, a

successful therapy would be characterized by regulated

expression of the transgene finely tuned to the

chang-ing clinical state of a patient

Several gene switches have been developed for

regu-lating the expression of transgenes in humans [2]

More specifically, ecdysone receptor (EcR) gene

switches for medicinal purposes have been reported by

several laboratories [3–9] Among these switches,

EcR-based gene switches display particularly low basal

activity in the absence of an inducer and strong

induc-ible activity in the presence of an inducer [2,8,10]

The relative structural dissimilarity of ecdysteroidsand mammalian steroids might suggest that binding ofthe former to vertebrate steroid receptors would be tooweak for pharmacological effects, particularly adverseones In support of this proposition, humans consumesignificant amounts of phytoecdysteroids contained indietary vegetables seemingly without any apparentdetrimental effects [11] However, Oehme et al [12]reported recently that ecdysteroids and ecdysonemimics can induce and⁄ or suppress endogenous genes

in RKO and other mammalian cells and promoteapoptosis

A more comprehensive understanding of possiblepleiotropic effects of ligand inducers and⁄ or the switchcomponents is essential for successful use of the EcRgene switch for in vivo applications such as gene ther-apy The diacylhydrazine [13,14] nonsteroidal ecdysoneagonists, such as Rheoswitch ligand 1 (RSL-1; Fig 1),are reported to be an excellent inducer for EcR geneswitches, supporting up to 9000-fold induction ofreporter activity [15] Other steroidal ligands, such asponasterone A (Pon A; Fig 1), have also beenreported as potential inducers of EcR-based gene

O

O O

Diacylhydrazines (DAH) RG-100864 R 1 =Cl R 2 =H

R = OH

R = H

RG-102398 R 1 =2-CH 3 , 3-OCH 3

R 2 =3,5-di-CH 3 RG-102240 R 1 =2-CH 2 CH 3 , 3-OCH 3

R 2 =3,5-di-CH 3 RG-102277 R 1 =2-CH 2 CH 3 , 3-OCH 3

R 2 =3-CH 3 , 5-C(O)NH 2

N O

HN F

F

F

N H

O O

Fig 1 EcR ligands analyzed by microarray and qRT-PCR analysis.

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switches [8,14] In addition, other chemotypes, such

as amidoketones (AMK) and tetrahydroquinolines

(THQ), are also being developed as inducers of EcR

gene switches [16–20] (Fig 1)

The main goal of the present study was to determine

the intrinsic gene expression effects of EcR switch

in-ducers in mammalian cells We studied the effect of

eight EcR ligands: four diacylhydrazines, two

ecdyster-oids, one THQ and one AMK ligand (Fig 1) on the

expression of endogenous genes in HEK 293 cells

using microarray and quantitative real-time reverse

transcription PCR (qRT-PCR) THQ ligand caused

changes in the expression of genes such as TNF, MAF,

Rab and Reprimo The AMK ligand induced changes

in the expression of genes such as v-jun, FBJ and

EGR 20-Hydroxyecdysone (20E) did not affect gene

expression, but Pon A caused some changes in the

expression of endogenous genes At lower ligand

con-centrations applicable for therapeutic use, potential

pleiotropic effects may or may not be observed The

four diacylhydrazine ligands did not cause significant

changes in the expression of endogenous genes

Results and Discussion

THQ ligand, RG-120499, affects 293 cells via many

pathways

Incubation of 293 cells with the THQ compound

RG-120499 at 10 lm for 3 days resulted in the death of

70% of the cells as indicated by observation of cell

morphology To determine the possible genes and

path-ways that are affected by this ligand, we performed a

microarray experiment using RNA isolated from

293 cells treated with 1 lm RG-120499 A total of 1171

genes were up-regulated and 443 genes were

down-regulated in 293 cells treated with this compound

compared to the cells treated with dimethylsulfoxide

(Fig 2A) Among these, 115 genes showed P£ 0.01

with a two-fold or more greater in expression levels in

ligand-treated cells compared to the levels in

dimethyl-sulfoxide-treated cells (Table 1) Among these 115

genes, 55 genes showed signal detection values of more

than 100 We selected v-maf, TNF, PNAS13, Rab,

Rep-rimo, DNAH and KIF9 genes for PCR The

qRT-PCR data (Fig 2B,C) showed that v-maf, TNF,

PNAS13and DNAH mRNA levels increased, and Rab

and Reprimo mRNA levels decreased in RG-120499

treated cells, compared to the levels in

dimethylsulfox-ide-treated cells The microarray and qRT-PCR data

showed perfect correlation for these six genes The

two-fold down-regulation of the KIF9 gene observed in

microarray analyses was not confirmed by qRT-PCR

because this method showed a ten-fold up-regulation ofthis gene in the presence of RG-102499

MAF [v-maf musculoaponeurotic fibrosarcomaoncogene homolog (avian)] is a basic-leucine zippertranscription factor that plays crucial roles in gene reg-ulation, differentiation, oncogenesis and development

in many organisms [21] v-maf is a viral oncogeneencoding a leucine zipper motif that forms heterodi-mers with the protein products of maf-related genes orother proteins such as fos, jun and myc oncogenes thathave leucine zipper motifs [22] Our microarray andqRT-PCR data showed that, in 293 cells, RG-120499up-regulates v-maf gene expression by 2.4- and2.3-fold, respectively Nishizawa et al [22] have dem-onstrated that the human cellular counterpart of thev-maf (c-maf) gene is conserved across species Addi-tionally, Massrieh et al [21] reported that the MAFtranscription factor transcript levels are induced byproinflammatory cytokines in PHM1-31 myometrialcells and that MAF transcription factor mRNA israpidly induced by IL-1B and TNF in primarymyometrial and PHM1-13 cells Our data also indicateup-regulation of the TNF gene in microarray andqRT-PCR data (by 2.2- and 5.5-fold, respectively), anobservation consistent with TNF-induced up-regulation

of MAF transcript levels Zheng et al [23] reportedthat the tumor necrosis factor (TNF) can mediatemature T-cell receptor-induced apoptosis through thep75 TNF receptor This may be the possible reasonfor the death of 293 cells when treated with 10 lmRG-120499 ligand

In addition to the aforementioned up-regulatedgenes, two genes, namely, Rab and Reprimo, weredown-regulated by this THQ ligand in 293 cells, asobserved by both microarray and qRT-PCR tech-niques The Rab proteins constitute a subfamily ofRas-related GTP-binding proteins that are localized indistinct intracellular compartments [24] Mutations inthe Rab gene can alter the morphology of entire organ-elles by blocking protein transport along the exocyticand endocytic pathways because Rab proteins plays akey role in membrane trafficking [25] Barbosa et al.[26] reported that mutations in the Rab gene(s) cancause irregularities in the protein transport machineryleading to the formation of giant lysosomes in mousebeige (bg) mutant and other mutant mice It has beensuggested that Chediak–Higashi syndrome, a rareautosomal recessive disorder in humans, is the conse-quence of a mutation to a homolog of bg Our micro-array and qRT-PCR data indicate that the rab gene wasdown-regulated in 293 cells by two- and 23-fold, respec-tively, by the THQ, RG-120499 Mutation studies of theRabgene suggest that the Rab gene down-regulation by

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this ligand may be a reason for cell death in addition to

modulation of the v-maf and TNF genes

Tumor suppressor genes that encode transcriptional

factors can affect a variety of cellular mechanisms

underlying growth, differentiation, and apoptosis

[27,28] Also, when cells were exposed to DNA

dam-age-inducing agents or other noxious stress, the p53

protein, which is the most commonly mutated gene in

human cancer, is induced and⁄ or activated, resulting in

cell cycle arrest or apoptosis [29–31] Reprimo is a

highly glycosylated protein, which will localize in the

cytoplasm and induce G2 arrest of the cell cycle when

expressed ectopically [32] In the present study, it was

observed that RG-120499 down-regulates the Reprimo

gene by two-fold as measured by both microarray and

qRT-PCR techniques From these observations and

previous reports, we suggest that the down-regulation

of the Reprimo gene may cause loss of DNA repair,which, in turn, is passed on to the next generations,thereby accumulating DNA defects RG-120499 modu-lates the expression of other genes as well ThePNAS123 gene (transformation related protein 11) isup-regulated by 2.7- and 4.3-fold as measured bymicroarray and qRT-PCR, respectively The pathways

in which these genes are involved are not known

RG-120499 also triggers five- and 23-fold up-regulation ofthe DNAH (human axonemal dynein heavy chain)gene as measured by microarray and qRT-PCR tech-niques, respectively DNAH is a microtubule associ-ated motor protein that moves cilia and flagella[33,34] Afzelius [35,36] showed that patients sufferingfrom Kartagener syndrome have cilia lacking dynein

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arms This disease is characterized by chronic

respira-tory tract infections, altered position of internal

organs, and infertility arising from immotile sperm

Milisav and Affara [37] reported that the human

dynein-related gene DNEL2 may play an important

role specifically in sperm motility and is not involved

in the movement of cilia In summary, the use of the

THQ gene switch ligand RG-120499 may cause

signifi-cant changes in the expression of host genes

AMK, RG-121150, affects gene expression in

293 cells

The affect of the AMK RG-121150 on gene expression

in 293 cells was analyzed using microarray and

qRT-PCR In microarray analysis, a total of 636 genes were

up-regulated and 604 genes were down-regulated by

this ligand (Fig 3A) Among these genes, 71 genes

showed P£ 0.01 and a two-fold or greater change in

expression (Table 1) Among 71 genes, 24 genes

showed signal detection values greater than 100

Among these are hypothetical proteins, nuclear

pro-teins, transcriptional factors, glycogen phosphorylase,

hormone degrading enzymes, kinases and some solute

carrier proteins To validate microarray data with

qRT-PCR, the primers for early growth response gene

(EGR), FBJ, v-jun, and a hypothetical protein genewere designed For three of the four genes, the micro-array data was confirmed by qRT-PCR The datashowed that the hypothetical protein gene was up-regu-lated by two- and 1.5-fold in microarray and qRT-PCRexperiments, respectively EGR and v-jun showed sup-pression of their expression by the ligand in analyses byboth methods (Fig 3B,C) The gene FBJ mRNA levelswere down-regulated in microarray experiments and up-regulated in qRT-PCR experiments

The EGR gene product is a transcription factor thatplays a role in differentiation and growth EGR genesare transiently and coordinately induced upon activa-tion of peripheral blood T lymphocytes [38,39] TheseEGR genes are also expressed in a wide range of celltypes, including lymphoid cells, myeloid cells such asthymocytes, B cells, monocytes, and nonlymphoid cellssuch as fibroblasts, kidney cells and neurons [40,41].Huang et al [42,43] showed that the expression of theEGR gene exogenously in various tumor cells unex-pectedly and markedly reduces growth and tumorige-nicity, whereas the suppression of endogenous EGR

by antisense RNA enhances growth and promotesphenotypic transformation From our microarray andqRT-PCR data, the AMK RG-121150 caused down-regulation of this EGR gene by five- and six-fold,

Table 1 Differentially expressed genes in 293 cells treated with different ligands.

Up-regulated Down-regulated Total Up-regulated Down-regulated Total

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respectively, indicating a possible effect RG-121150 on

this pathway Overall, these studies showed that AMK

ligand RG-121150 could cause significant changes in

the expression of genes in host cells However, the

cor-responding toxicological potential could be

substan-tially mitigated or even erased by the likelihood that

actual gene therapy dosage would be significantly

lower than the 10 lm studied here Likewise, judicious

choice of the specific member of the AMK chemotype

may confer intrinsic benignity

Ecdysteroid ligand, 20E, shows little effect on

293 cells but Pon A affects cell division

Two steroid ligands Pon A and 20E were tested in

293 cells to determine their effect on gene expression

using microarray and qRT-PCR In 20E-treated

293 cells, a total of 542 genes were up-regulated and

627 genes were down-regulated compared to sulfoxide-treated cells (Fig 4A) Out of these, 51 genesshowed P£ 0.01 and a change in gene expression oftwo-fold or greater (Table 1) Among these 51 genes,only five genes had signal detection values greater than

dimethyl-100 We selected signal transducer and activator oftranscription 6 (STAT6) genes to perform qRT-PCRanalyses Although the STAT6 gene was down-regu-lated by 20E in microarray analysis, the qRT-PCRanalyses showed that the mRNA levels did not change

in treated cells compared to untreated cells(Fig 4B,C) Experiments in our laboratory (S R Palli,unpublished results) showed that, in mammalian cells,20E does not induce reporter genes placed under the

k Amido ketone Amido ketone Amido ketone

Fig 3 AMK RG-121150 affects endogene expression in 293 cells (A) The V-plot of differentially expressed genes from microarray analysis The P-values of t-test are plotted against fold suppression or induction The horizontal bar in the plot represents the nominal significant level 0.001 for the t-test under the assumption that each gene has a unique variance The vertical bars represent the genes that are minimum of two- fold up- or down-regulated compared to the control dimethylsulfoxide (DMSO) (B) The signal values of hypothetical protein, EGR, v-jun and FBJ genes from microarray The signal values from the microarray analysis were plotted for each gene are indicated as mean ± SD (n ¼ 3) The numbers above the bar represents the fold changes with this ligand against dimethylsulfoxide (C) The relative expressions of hypothetical protein, EGR, v-jun and FBJ gene transcript levels in qRT-PCR The relative expression values from the qRT-PCR analysis were plotted for each gene are indicated as mean ± SD (n ¼ 3) The numbers above the bar represents the fold changes with this ligand against dimethylsulfoxide.

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control of the EcR gene switch The microarray data

corroborate evidence for an overall benign influence of

20E on gene expression and metabolism in mammalian

cells [44] It is conceivable that 20E is excluded by

mammalian cells, or perhaps some other factors in the

mammalian cells inhibit the activity of 20E

A total of 639 genes were up-regulated and 638 were

down-regulated in 293 cells treated with Pon A

com-pared to the cells treated with dimethylsulfoxide

(Fig 5A) Among these, 41 genes showed P£ 0.01 and

two-fold or greater induction (up⁄ down-regulated;

Table 1) Only three genes showed signal detection

val-ues greater than 100 Out of these three genes, we

selected tousled-like kinase (Tlk) gene for qRT-PCR

analysis The data from both methods showed that the

Tlk gene was induced by Pon A by two-fold

(Fig 5B,C) In proliferating human cells, Tlks are

maximally active during the S phase but rapidly vated in response to inhibitors of DNA replication[45] Sillje and Nigg [46] showed that the Asf1 (anti-silencing function 1) proteins are phosphorylated byTlks both in vivo and in vitro during the S phase anddephosphorylated with inactivation of Tlks Constan-tino et al [47] used the ecdysone inducible gene expres-sion system in hematopoietic cells and found that thetwo steroids, muristerone A and Pon A, altered thesignaling pathways induced by IL-3 in the pro-B cell-line, Ba⁄ F3 Indeed, they also showed that these ecdy-steroids potentiate the IL-3-dependent activation ofthe PI 3-kinase⁄ Akt pathway, an effect that could ulti-mately interfere with the growth, and⁄ or survival ofthese cells Our data do not reveal any affect of Pon A

inacti-on the PI 3-kinase⁄ Akt pathway in 293 cells A ble reason is that these genes might be expressed only

e Expression 0.002

0.001

0 -2.86

20E DMSO

STAT6

20E DMSO

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analy-in a particular type of cells, such as hematopoietic cells,

but not 293 cells These observations, in conjunction

with our microarray and qRT-PCR data, indicate that

Pon A may affect cell division in mammalian cells

Diacylhydrazine ligands do not induce significant

changes in gene expression

Diacylhydrazine nonsteroidal ligands have been

sub-jected to extensive studies concerning their

toxicologi-cal effects on vertebrates for the purposes of

Environmental Protection Agency registration as

com-mercial insecticides [48,49] We selected four

represen-tatives from the diacylhydrazine gene switch

chemotype for evaluation of their effects on expression

of endogenous genes in 293 cells: the lepidopteran

insecticide, methoxyfenozide (RG-102398); the

coleopt-eran insecticide, halofenozide (RG-100864); the

Rheo-Switch ligand RSL-1 (RG-102240, also known as

GSTM-E); and, finally, a more polar and water-solublevariant of RSL-1, namely RG-102277 First, we deter-mined the effect of dimethylsulfoxide itself on theexpression of genes in 293 cells The expressions of atotal of 43 genes were modulated with P£ 0.01 with atwo-fold change in expression Among the affectedgenes, 38 were up-regulated and five of them weredown-regulated Interestingly, only 13 up-regulatedgenes and one down-regulated gene showed signaldetection values of more than 100 in the dimethylsulf-oxide-treated 293 cells In our experience, the genesthat show signal detection values less than 100 are notreliable indicators of gene expression; therefore, we didnot consider these in our analyses

Cells treated with the diacylhydrazine RG-102240resulted in up-regulation of a total of 865 genes; on theother hand, 411 genes were down-regulated in 293 cellstreated with RG-102240 (Fig 6A) From these, we con-sidered for further analysis only the genes with P£ 0.01

e Expression 0.000502

PonADMSO

TLK

PonADMSO

1 x1.5 x4 x8 x16

Fig 5 Steroidal ligand Pon A may affect cell division in 293 cells (A) The V-plot of differentially expressed genes from microarray analysis The P-values of t-test are plotted against fold suppression or induction The horizontal bar in the plot represents the nominal significant level 0.001 for the t-test under the assumption that each gene has a unique variance The vertical bars represent the genes that are minimum of two-fold up- or down-regulated compared to the control dimethylsulfoxide (DMSO) (B) The signal values of Tlk gene from microarray The signal values from the microarray analysis were plotted for each gene are indicated as mean ± SD (n ¼ 3) The numbers above the bar rep- resents the fold changes with this ligand against dimethylsulfoxide (C) The relative expression of Tlk transcripts as determined by qRT-PCR The relative expression values from the qRT-PCR analysis were plotted for each gene are indicated as mean ± SD (n ¼ 3) The numbers above the bar represents the fold changes with this ligand against dimethylsulfoxide.

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with a two-fold change in expression compared to the

expression in dimethylsulfoxide-treated cells A total of

46 genes met these criteria However, only six of these

genes showed signal detection values greater than 100

(Table 1) The annotations for these genes were

devel-oped by using NIH david ease software (http://david

niaid.nih.gov/david/ease.htm) Only two out of six were

annotated; these were identified as DAB2 interacting

protein gene and kinesin family member-9 (KIF9)

The reliability of microarray results depends on

sev-eral factors such as array production, RNA extraction,

probe labeling, hybridization conditions and image

analysis [50–53] Therefore, the genes identified as

dif-ferentially expressed by this method must be validated

with another method such as qRT-PCR, which is

quantitative, rapid, and requires 1000-fold less RNA

than conventional assays [54] For this reason, wedesigned primers for DAB2 interacting protein geneand KIF9 from their cDNA sequences for qRT-PCRanalysis Their expression levels were measured indimethylsulfoxide- and RG-102240-treated 293 cellsand compared to microarray data The DAB2 interact-ing protein gene showed two-fold down-regulation bymicroarray and a four-fold increase by qRT-PCRanalysis in RG-102240-treated cells compared tothe expression in dimethylsulfoxide-treated cells(Fig 6B,C) The KIF9 gene showed 3.9-fold down-reg-ulation by microarray and 2.8-fold down-regulation byqRT-PCR analysis in RG-102240-treated cells com-pared to the expression in dimethylsulfoxide-treatedcells (Fig 6B,C) The Drosophila melanogaster Dab(Disabled) interacting protein is the mammalian ortho-

0.0040.0030.0020.0010

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logue of D melanogaster DabIP The DabIP

partici-pates in a signaling complex containing various

pro-teins involved in brain development as well as other

aspects of adult brain function [55] Although the

microarray showed two-fold down-regulation of the

Dab gene, the qRT-PCR data showed four-fold

up-regulation The reasons for difference in the fold

regulation between the two techniques are not readily

apparent KIF9 protein is found to interact with

Ras-like GTPase Gem and is involved in cell shape

remod-eling [56] Both microarray data and qRT-PCR data,

showed similar results (3.9-fold and 2.8-fold

down-reg-ulation, respectively) in KIF9 gene expression levels

Over-expression of the KIF9 mutant did not cause any

significant difference in Gem-induced cell elongation

and it does not appear to be essential for the

Gem-induced phenotypic changes [56] From these tions, it can be concluded that, although the RSL-1ligand down-regulates the KIF9 gene, there may not besignificant changes in cell shape remodeling

observa-Treatment of HEK 293 cells with RG-102398resulted in a total of 598 down-regulated and 388up-regulated genes (Fig 7A) Among these, 52 genesindicated P£ 0.01 and a change in expression of two-fold or greater compared to dimethylsulfoxide-treatedcells (Table 1) Only three genes [ribosomal protein L13(RPL), hypothetical protein gene FLJ38705 and leptinreceptor] out of these 52 showed signal detection valuesgreater than 100 The qRT-PCR and microarray anal-ysis of RPL gene expression are weakly correlated.The RPL gene was down-regulated by two-fold bymicroarray, but was up-regulated 1.25-fold by

-2.27-2.05

Zink Finger RPL

Zink Finger RPL

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