Nucleic Acids Research, 2001, Vol. 29, No. 9 e45
© 2001 Oxford University Press
A new mathematical model for relative quantification in real-time RTPCR
Institute of Physiology, FML-Weihenstephan, Center of Life and Food Sciences, Technical University of Munich, Germany
Received December 18, 2000; Revised February 21, 2001; Accepted March 14, 2001.
| ABSTRACT |
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Use of the real-time polymerase chain reaction (PCR) to amplify cDNA products reverse transcribed from mRNA is on the way to becoming a routine tool in molecular biology to study low abundance gene expression. Real-time PCR is easy to perform, provides the necessary accuracy and produces reliable as well as rapid quantification results. But accurate quantification of nucleic acids requires a reproducible methodology and an adequate mathematical model for data analysis. This study enters into the particular topics of the relative quantification in real-time RTPCR of a target gene transcript in comparison to a reference gene transcript. Therefore, a new mathematical model is presented. The relative expression ratio is calculated only from the real-time PCR efficiencies and the crossing point deviation of an unknown sample versus a control. This model needs no calibration curve. Control levels were included in the model to standardise each reaction run with respect to RNA integrity, sample loading and inter-PCR variations. High accuracy and reproducibility (<2.5% variation) were reached in LightCycler PCR using the established mathematical model.
| INTRODUCTION |
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Reverse transcription (RT) followed by the polymerase chain reaction (PCR) is the technique of choice to analyse mRNA expression derived from various sources. Real-time RTPCR is highly sensitive and allows quantification of rare transcripts and small changes in gene expression. As well as this, it is easy to perform, provides the necessary accuracy and produces reliable as well as rapid quantification results. The simplest detection technique for newly synthesised PCR products in real-time PCR uses SYBR Green I fluorescence dye that binds specifically to the minor groove double-stranded DNA (1). The quantification method of choice depends on the target sequence, the expected range of mRNA amount present in the tissue, the degree of accuracy required and whether quantification needs to be relative or absolute (2). Generally two quantification types in real-time RT-PCR are possible. (i) A relative quantification based on the relative expression of a target gene versus a reference gene. To investigate the physiological changes in gene expression, the relative expression ratio is adequate for the most purposes. (ii) An absolute quantification, based either on an internal or an external calibration curve (1,3). Using such a calibration curve, the methodology has to be highly validated and the identical LightCycler PCR amplification efficiencies for standard material and target cDNA must be confirmed (46). Nevertheless, the generation of stable and reliable standard material, either recombinant DNA or recombinant RNA, is very time consuming and it must be precisely quantified (2,7,8). Furthermore, a normalisation of the target gene with an endogenous standard is recommended. Therefore, mainly non-regulated reference genes or housekeeping genes like glyceraldehyde-3-phosphate dehydrogenase (G3PDH or GAPDH), albumin, actins, tubulins, cyclophilin, 18S rRNA or 28S rRNA (9) were applicable. Housekeeping genes are present in all nucleated cell types since they are necessary for basis cell survival. The mRNA synthesis of these genes is considered to be stable and secure in various tissues, even under experimental treatments (911). But numerous studies have already shown that the housekeeping genes are regulated and vary under experimental conditions (1215). To circumvent the high expenditure of design and production of standard material, as well as optimisation and validation of a calibration curve based quantification model, and finally the need for normalisation of the target transcripts to an endogenous housekeeping transcript, a reliable and accurate relative quantification model in real-time RTPCR is needed.
This study enters into the particular topics of the relative quantification of a target gene in comparison to a reference gene. A new and simple mathematical model for data analysis was established, the application of the new model was tested and compared with available mathematical calculation models. Derived reproducibility, based on intra- and inter-test variation of this relative quantification and accuracy of the model will be discussed.
| MATERIALS AND METHODS |
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RNA source, total RNA extraction and RT
RNA extraction was performed as described previously (16) in bacterial Escherichia coli culture grown either in M9 minimal media (sample preparation) or LB rich media (control preparation), both with 0.4% glucose concentration (17). RNA integrity was electrophoretically verified by ethidium bromide staining and by OD260/OD280 nm absorption ratio >1.95. Escherichia coli total RNA (1 µg) was reverse transcribed with 100 U of Superscript II Plus RNase H Reverse Trancriptase (Gibco BRL Life Technologies, Gaithersburg, MD) using 100 µM random hexamer primers (Pharmacia Biotech, Uppsala, Sweden) according to the manufacturers instructions.
Optimisation of RTPCR
Highly purified salt-free primer for target gene1 (TyrA, tryptophan operon: forward primer, AAG CGT CTG GAA CTG GTT GC; reverse primer, AAA CGC TGT GCG TAA TCG CC), target gene 2 (PyrB, aspartate transcarbamylase: forward primer, GCT CCA ACC AAC ATC CGA; reverse primer, TTC ACG TTG GCG TAC TCG G) and reference gene (Gst, glutathione transferase: forward primer, CTT TGC CGT TAA CCC TAA GGG; reverse primer, GCT GCA ATG TGC TCT AAC CC) were generated (MWG Biotech, Ebersberg, Germany) and optimised to an equal annealing temperature of 60°C. Conditions for all PCRs were optimised in a gradient cycler (Mastercycler Gradient, Eppendorf, Germany) with regard to Taq DNA polymerase (Roche Diagnostics, Basel, Switzerland), forward and reverse primers, MgCl2 concentrations (Roche Diagnostics), dNTP concentrations (Roche Diagnostics) and various annealing temperatures (5565°C). RTPCR amplification products were separated on a 4% high resolution NuSieve agarose (FMC Bio Products, Rockland, ME) gel electrophoresis and analysed with the Image Master system (Pharmacia Biotech). Optimised results were transferred on the following LightCycler PCR protocol.
LightCycler real-time PCR
For LightCycler reaction a mastermix of the following reaction components was prepared to the indicated end-concentration: 13 µl water, 2.4 µl MgCl2 (4 mM), 0.8 µl forward primer (0.4 µM), 0.8 µl reverse primer (0.4 µM) and 2.0 µl LightCyler (Fast Start DNA Master SYBR Green I; Roche Diagnostics). LightCycler mastermix (19 µl) was filled in the LightCycler glass capillaries and 1 µl cDNA (3.2, 4.0, 4.8, 16, 20 or 24 ng reverse transcribed total RNA) was added as PCR template. Capillaries were closed, centrifuged and placed into the LightCycler rotor. The following LightCycler experimental run protocol was used: denaturation program (95°C for 10 min), amplification and quantification program repeated 40 times (95°C for 15 s, 60°C for 10 s, 72°C for 60 s with a single fluorescence measurement), melting curve program (6095°C with a heating rate of 0.1°C per second and a continuous fluorescence measurement) and finally a cooling step to 40°C. For the mathematical model it is necessary to determine the crossing points (CP) for each transcript. CP is defined as the point at which the fluorescence rises appreciably above the background fluorescence. Fit Point Method must be performed in the LightCycler software 3.3 (Roche Diagnostics), at which CP will be measured at constant fluorescence level (18).
| RESULTS |
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Confirmation of primer specificity
Specificity of RTPCR products was documented with high resolution gel electrophoresis and resulted in a single product with the desired length (TyrA, 978 bp; PyrB, 530 bp; and Gst, 402 bp). In addition a LightCycler melting curve analysis was performed which resulted in single product specific melting temperatures as follows: TyrA, 89.6°C; PyrB, 88.5°C; and Gst, 88.3°C. No primer-dimers were generated during the applied 40 real-time PCR amplification cycles.
Real-time PCR amplification efficiencies and linearity
Real-time PCR efficiencies were calculated from the given slopes in LightCycler software. The corresponding real-time PCR efficiency (E) of one cycle in the exponential phase was calculated according to the equation: E = 10[1/slope] (Fig. 1) (18). Investigated transcripts showed high real-time PCR efficiency rates; for TyrA, 2.09; PyrB, 2.16; and Gst, 1.99 in the investigated range from 0.40 to 50 ng cDNA input (n = 3) with high linearity (Pearson correlation coefficient r > 0.95).
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Intra- and inter-assay variation
To confirm accuracy and reproducibility of real-time PCR the intra-assay precision was determined in three repeats within one LightCycler run. Inter-assay variation was investigated in three different experimental runs performed on 3 days using three different premix cups of LightCycler, Fast Start DNA Master SYBR Green I kit (Roche Diagnostics). Determination of variation was done in 20 ng transcribed total RNA (Table 1). Test reproducibility for all investigated transcripts was low in inter-test experiments (<3.91%) and even lower in intra-test experiments (<2.16%). The calculation of test precision and test variability is based on the CP variation from the CP mean value.
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Mathematical model for relative quantification in real-time PCR
A new mathematical model was presented to determine the relative quantification of a target gene in comparison to a reference gene. The relative expression ratio (R) of a target gene is calculated based on E and the CP deviation of an unknown sample versus a control, and expressed in comparison to a reference gene.
1
Equation 1 shows a mathematical model of relative expression ratio in real-time PCR. The ratio of a target gene is expressed in a sample versus a control in comparison to a reference gene. Etarget is the real-time PCR efficiency of target gene transcript; Eref is the real-time PCR efficiency of a reference gene transcript;
CPtarget is the CP deviation of control sample of the target gene transcript;
CPref = CP deviation of control sample of reference gene transcript. The reference gene could be a stable and secure unregulated transcript, e.g. a house- keeping gene transcript. For the calculation of R, the individual real-time PCR efficiencies and the CD deviation (
CP) of the investigated transcripts must be known. Real-time PCR efficiencies were calculated, according to E = 10[1/slope] (18), as shown in Figure 1. CP deviations of control cDNA minus sample of the target gene and reference genes were calculated according to the derived CP values. Mean CP, variation of CP and
CP values between control and sample of investigated transcripts are listed in Table 2. The influence of differing cDNA input concentrations on
CP are also shown. Intended cDNA input concentration variation of control and sample were compared at different levels (low level, 3.2, 4.0, 4.8 ng cDNA; high level, 16, 20 and 24 ng cDNA). They resulted in stable and constant
CP cycle numbers. In Table 3 the corresponding ratios of target genes in comparison to the reference gene were calculated, through to the established mathematical model (equation 1). The expression ratios of target genes remain stable, even under intended ±20% cDNA variation and low and high cDNA input levels, performed in two runs. A minimal coefficient of variation (CV) of 2.50 and 1.74% was observed, respectively.
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Regulation of investigated gene transcripts
All investigated transcript expressions were regulated divergently (Table 3). The expression of Gst was constant, independent of media conditions, and therefore was chosen as endogenous standard or reference gene transcript Fig. 2. TyrA mRNA expression, measured in 20 ng cDNA, was up-regulated 49.1-fold (2.095.283) in M9 minimal compared to LB rich medium under high cDNA input conditions. Under the consideration of the reference gene expression the real up-regulation ratio was, on average, 58.5-fold. PyrB mRNA expression was down-regulated under M9 minimal medium conditions by a factor of 27.6 (2.164.311). With the normalisation of the endogenous standard transcript, the exact relative expression ratio can be calculated to 23.2.
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| DISCUSSION |
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RT followed by PCR is the most powerful tool to amplify small amounts of mRNA (19). Because of its high ramping rates, limited annealing and elongation time, the rapid cycle PCR in the LightCycler system offers stringent reaction conditions to all PCR components and leads to a primer sensitive and template specific PCR (20). The application of fluorescence techniques to real-time PCR combines the PCR amplification, product detection and quantification of newly synthesised DNA, as well as verification in the melting curve analysis. This led to the development of new kinetic RTPCR methodologies that are revolutionising the possibilities of mRNA quantification (21).
In this paper, we focused on the relative quantification of target gene transcripts in comparison to a reference gene transcript. A new mathematical model for data analysis was presented to calculate the relative expression ratio on the basis of the PCR efficiency and crossing point deviation of the investigated transcripts (equation 1). The concept of threshold fluorescence is the basis of an accurate and reproducible quantification using fluorescence-based RTPCR methods (22). Threshold fluorescence is defined as the point at which the fluorescence rises appreciably above the background fluorescence. In the Fit Point Method, the threshold fluorescence and therefore the DNA amount in the capillaries is identical for all samples. CP determination with the Second Derivative Maximum Method is not adequate for our mathematical model, because quantification is done at the point of most efficient real-time PCR where the second derivative is at its maximum (18).
A linear relationship between the CP, crossing the threshold fluorescence, and the log of the start molecules input in the reaction is given (18,23). Therefore, quantification will always occur during the exponential phase, and it will not be affected by any reaction components becoming limited in the plateau phase (7). In the established model the relative expression ratio of a target gene is normalised with the expression of an endogenous desirable unregulated reference gene transcript to compensate inter-PCR variations between the runs. The CP of the chosen reference gene is the same in the control and the sample (
CP = 0). Stable and constant reference gene mRNA levels are given. Under these considerations of an unregulated reference gene transcript, no normalisation is needed and equation 1 can be shortened to equation 2.
2
Equation 2 shows a mathematical model of relative expression ratio in real-time PCR under constant reference gene expression. CP values in the sample and control are equal and represent ideal housekeeping conditions (
CPref = 0, Eref = 1).
Two other mathematical models are available for the relative quantification during real-time PCR. The efficiency calibrated mathematical method for the relative expression ratio in real-time PCR is presented by Roche Diagnostics in a truncated form in an internal publication (24). The complete equation is, in principle, the same and the results are in identical relative expression ratio like our model (equation 3).
3
Efficiency calibrated mathematical method for the relative expression ratio in real-time PCR presented by Soong et al. (24). But the method of calculation in the described mathematical model is hard to understand. The second model available, the Deltadelta method for comparing relative expression results between treatments in real-time PCR (equation 4) is presented by PE Applied Biosystems (Perkin Elmer, Forster City, CA).
4
Equation 4 shows a mathematical deltadelta method for comparing relative expression results between treatments in real-time PCR developed by PE Applied Biosystems (Perkin Elmer). Optimal and identical real-time amplification efficiencies of target and reference gene of E = 2 are presumed. The deltadelta method is only applicable for a quick estimation of the relative expression ratio. For such a quick estimation, equation 1 can be shortened and transferred into equation 4, under the condition that Etarget = Eref = 2. Our presented formula combines both models in order to better understand the mode of CP data analysis and for a more reliable and exact relative gene expression.
Relative quantification is always based on a reference transcript. Normalisation of the target gene with an endogenous standard was done via the reference gene expression, to compensate inter-PCR variations. Beside this further control levels were included in the mathematical model to standardise each reaction run with respect to RNA integrity, RT efficiency or cDNA sample loading variations. The reproducibility of the RT step varies greatly between tissues, the applied RT isolation methodology (25) and the RT enzymes used (26). Different cDNA input concentrations were tested on low and high cDNA input ranges, to mimic different RT efficiencies (±20%) at different quantification levels. In the applied two-step RTPCR, using random hexamer primers, all possible interferences during RT will influence all target transcripts as well as the internal reference transcript in parallel. Occurring background interferences retrieved from extracted tissue components, like enzyme inhibitors, and cDNA synthesis efficiency were related to target and reference similarly. All products underwent identical reaction conditions during RT and variations only disappear during real-time PCR. Any source of error during RT will be compensated through the model itself. Widely distributed single-step RTPCR models are not applicable, because in each reaction set-up and for each investigated factor individual and slightly different RT conditions will occur. Therefore, the variation in a two-step RTPCR will always be lower, and the reproducibility of the assay will be higher, that in a single-step RTPCR (8). Reproducibility of the developed mathematical model was dependent on the exact determination of real-time amplification efficiencies and on the given low LightCycler CP variability. In our mathematical model the necessary reliability and reproducibility was given, which was confirmed by high accuracy and a relative error of <2.5% using low and high template concentration input.
| CONCLUSION |
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LightCycler real-time PCR using SYBR Green I fluorescence dye is a rapid and sensitive method to detect low amounts of mRNA molecules and therefore offers important physiological insights on mRNA expression level. The established mathematical model is presented in order to better understand the mode of analysis in relative quantification in real-time RTPCR. It is only dependent on
CP and amplification efficiency of the transcripts. No additional artificial nucleic acids, like recombinant nucleic acid constructs in external calibration curve models, are needed. Reproducibility of LightCycler RTPCR in general and the minimal error rate of the model allows for an accurate determination of the relative expression ratio. Even different cDNA input resulted in minor variations. Relative expression is adequate for the most relevant physiological expression changes. In future it is not necessary to establish more complex and time consuming quantification models based on calibration curves. For the differential display of mRNA the relative expression ratio is an ideal and simple tool for the verification of RNA or DNA array chip technology results. | ACKNOWLEDGEMENTS |
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The author thanks D.Schmidt for technical assistance. Primers, primer sequences and samples were kindly donated by Drs S.Wegener and W.Mann in collaboration with the BioChip division of MWG Biotech in Ebersberg, Germany.
| FOOTNOTES |
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* To whom correspondence should be addressed at present address: Institut für Physiologie, Weihenstephaner Berg 3, 85354 Freising, Weihenstephan, Germany. Tel: +49 8161 71 3511; Fax: +49 8161 71 4204; Email: pfaffl{at}weihenstephan.de
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S. Mansour, J. Bailly, S. Landaud, C. Monnet, A. S. Sarthou, M. Cocaign-Bousquet, S. Leroy, F. Irlinger, and P. Bonnarme Investigation of Associations of Yarrowia lipolytica, Staphylococcus xylosus, and Lactococcus lactis in Culture as a First Step in Microbial Interaction Analysis Appl. Envir. Microbiol., October 15, 2009; 75(20): 6422 - 6430. [Abstract] [Full Text] [PDF] |
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S. C. Chow, L. Y. Ching, A. M. F. Wong, and C. K. C. Wong Cloning and regulation of expression of the Na+-Cl--taurine transporter in gill cells of freshwater Japanese eels J. Exp. Biol., October 15, 2009; 212(20): 3205 - 3210. [Abstract] [Full Text] [PDF] |
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C. Collart, J. M. Ramis, T. A. Down, and J. C. Smith Smicl is required for phosphorylation of RNA polymerase II and affects 3'-end processing of RNA at the midblastula transition in Xenopus Development, October 15, 2009; 136(20): 3451 - 3461. [Abstract] [Full Text] [PDF] |
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M. Forlenza, S. Magez, J. P. Scharsack, A. Westphal, H. F. J. Savelkoul, and G. F. Wiegertjes Receptor-Mediated and Lectin-Like Activities of Carp (Cyprinus carpio) TNF-{alpha} J. Immunol., October 15, 2009; 183(8): 5319 - 5332. [Abstract] [Full Text] [PDF] |
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H. Hehnly, K. M. Longhini, J.-L. Chen, and M. Stamnes Retrograde Shiga Toxin Trafficking Is Regulated by ARHGAP21 and Cdc42 Mol. Biol. Cell, October 15, 2009; 20(20): 4303 - 4312. [Abstract] [Full Text] [PDF] |
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P. A. Harries, J.-W. Park, N. Sasaki, K. D. Ballard, A. J. Maule, and R. S. Nelson Differing requirements for actin and myosin by plant viruses for sustained intercellular movement PNAS, October 13, 2009; 106(41): 17594 - 17599. [Abstract] [Full Text] [PDF] |
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Y. Tsunoyama, G. Bernat, N. G. Dyczmons, D. Schneider, and M. Rogner Multiple Rieske Proteins Enable Short- and Long-term Light Adaptation of Synechocystis sp. PCC 6803 J. Biol. Chem., October 9, 2009; 284(41): 27875 - 27883. [Abstract] [Full Text] [PDF] |
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C. A. A. Penatti, D. M. Porter, and L. P. Henderson Chronic Exposure to Anabolic Androgenic Steroids Alters Neuronal Function in the Mammalian Forebrain via Androgen Receptor- and Estrogen Receptor-Mediated Mechanisms J. Neurosci., October 7, 2009; 29(40): 12484 - 12496. [Abstract] [Full Text] [PDF] |
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L. E. F. Almeida, P. D. Murray, H. R. Zielke, C. D. Roby, T. J. Kingsbury, and B. K. Krueger Autocrine Activation of Neuronal NMDA Receptors by Aspartate Mediates Dopamine- and cAMP-Induced CREB-Dependent Gene Transcription J. Neurosci., October 7, 2009; 29(40): 12702 - 12710. [Abstract] [Full Text] [PDF] |
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O. Peleg, G. Baneth, O. Eyal, J. Inbar, and S. Harrus Use of Chimeric DNA-RNA Primers in Quantitative PCR for Detection of Ehrlichia canis and Babesia canis Appl. Envir. Microbiol., October 1, 2009; 75(19): 6393 - 6398. [Abstract] [Full Text] [PDF] |
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S. Wang, K. Deng, S. Zaremba, X. Deng, C. Lin, Q. Wang, M. L. Tortorello, and W. Zhang Transcriptomic Response of Escherichia coli O157:H7 to Oxidative Stress Appl. Envir. Microbiol., October 1, 2009; 75(19): 6110 - 6123. [Abstract] [Full Text] [PDF] |
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R. Zhang, L. Zhou, Q. Li, J. Liu, W. Yao, and H. Wan Up-Regulation of Two Actin-Associated Proteins Prompts Pulmonary Artery Smooth Muscle Cell Migration under Hypoxia Am. J. Respir. Cell Mol. Biol., October 1, 2009; 41(4): 467 - 475. [Abstract] [Full Text] [PDF] |
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Y. Zhou, G. Cheng, L. Dieter, T. A. Hjalt, F. H. Andrade, J. S. Stahl, and H. J. Kaminski An Altered Phenotype in a Conditional Knockout of Pitx2 in Extraocular Muscle Invest. Ophthalmol. Vis. Sci., October 1, 2009; 50(10): 4531 - 4541. [Abstract] [Full Text] [PDF] |
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T. M. Filtz, D. R. Grubb, T. J. McLeod-Dryden, J. Luo, and E. A. Woodcock Gq-initiated cardiomyocyte hypertrophy is mediated by phospholipase C{beta}1b FASEB J, October 1, 2009; 23(10): 3564 - 3570. [Abstract] [Full Text] [PDF] |
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R. H. Hastings, P. R. Montgrain, R. Quintana, Y. Rascon, L. J. Deftos, and E. Healy Cell cycle actions of parathyroid hormone-related protein in non-small cell lung carcinoma Am J Physiol Lung Cell Mol Physiol, October 1, 2009; 297(4): L578 - L585. [Abstract] [Full Text] [PDF] |
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J. Munoz-Bertomeu, B. Cascales-Minana, J. M. Mulet, E. Baroja-Fernandez, J. Pozueta-Romero, J. M. Kuhn, J. Segura, and R. Ros Plastidial Glyceraldehyde-3-Phosphate Dehydrogenase Deficiency Leads to Altered Root Development and Affects the Sugar and Amino Acid Balance in Arabidopsis Plant Physiology, October 1, 2009; 151(2): 541 - 558. [Abstract] [Full Text] [PDF] |
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C.-C. Lan, R. Tang, I. Un San Leong, and D. R. Love Quantitative Real-Time RT-PCR (qRT-PCR) of Zebrafish Transcripts: Optimization of RNA Extraction, Quality Control Considerations, and Data Analysis CSH Protocols, October 1, 2009; 2009(10): pdb.prot5314 - pdb.prot5314. [Abstract] [Full Text] |
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C. T. Chan, F. Lovren, Y. Pan, and S. Verma Nocturnal haemodialysis is associated with improved vascular smooth muscle cell biology Nephrol. Dial. Transplant., September 17, 2009; (2009) gfp495v1. [Abstract] [Full Text] [PDF] |
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L. Kautz, D. Meynard, C. Besson-Fournier, V. Darnaud, T. Al Saati, H. Coppin, and M.-P. Roth BMP/Smad signaling is not enhanced in Hfe-deficient mice despite increased Bmp6 expression Blood, September 17, 2009; 114(12): 2515 - 2520. [Abstract] [Full Text] [PDF] |
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K. M. Wylie, J. E. Schrimpf, and L. A. Morrison Increased eIF2{alpha} Phosphorylation Attenuates Replication of Herpes Simplex Virus 2 vhs Mutants in Mouse Embryonic Fibroblasts and Correlates with Reduced Accumulation of the PKR Antagonist ICP34.5 J. Virol., September 15, 2009; 83(18): 9151 - 9162. [Abstract] [Full Text] [PDF] |
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S. Aharinejad, O. Andrukhova, M. Gmeiner, A. Thomas, A. Aliabadi, A. Zuckermann, K. Krenn, and M. Grimm Donor Serum SMARCAL1 Concentrations Predict Primary Graft Dysfunction in Cardiac Transplantation Circulation, September 15, 2009; 120(11_suppl_1): S198 - S205. [Abstract] [Full Text] [PDF] |
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S. Stefanovic, N. Abboud, S. Desilets, D. Nury, C. Cowan, and M. Puceat Interplay of Oct4 with Sox2 and Sox17: a molecular switch from stem cell pluripotency to specifying a cardiac fate J. Cell Biol., September 7, 2009; 186(5): 665 - 673. [Abstract] [Full Text] [PDF] |
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J. Wang, Q. Qiu, M. Haider, M. Bell, A. Gruslin, and J. K Christians Expression of pregnancy-associated plasma protein A2 during pregnancy in human and mouse J. Endocrinol., September 1, 2009; 202(3): 337 - 345. [Abstract] [Full Text] [PDF] |
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M F Machado, V M Portela, C A Price, I B Costa, P Ripamonte, R L Amorim, and J Buratini Jr Regulation and action of fibroblast growth factor 17 in bovine follicles J. Endocrinol., September 1, 2009; 202(3): 347 - 353. [Abstract] [Full Text] [PDF] |
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G. Garcia-Effron, S. Lee, S. Park, J. D. Cleary, and D. S. Perlin Effect of Candida glabrata FKS1 and FKS2 Mutations on Echinocandin Sensitivity and Kinetics of 1,3-{beta}-D-Glucan Synthase: Implication for the Existing Susceptibility Breakpoint Antimicrob. Agents Chemother., September 1, 2009; 53(9): 3690 - 3699. [Abstract] [Full Text] [PDF] |
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S. Almagro-Moreno and E. F. Boyd Sialic Acid Catabolism Confers a Competitive Advantage to Pathogenic Vibrio cholerae in the Mouse Intestine Infect. Immun., September 1, 2009; 77(9): 3807 - 3816. [Abstract] [Full Text] [PDF] |
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R. Goyal, A. Galffy, S. A. Field, C. P. Gheorghe, A. Mittal, and L. D. Longo Maternal Protein Deprivation: Changes in Systemic Renin-Angiotensin System of the Mouse Fetus Reproductive Sciences, September 1, 2009; 16(9): 894 - 904. [Abstract] [PDF] |
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H. M. Nef, H. Mollmann, C. Troidl, S. Kostin, S. Voss, P. Hilpert, C. B. Behrens, A. Rolf, J. Rixe, M. Weber, et al. Abnormalities in intracellular Ca2+ regulation contribute to the pathomechanism of Tako-Tsubo cardiomyopathy Eur. Heart J., September 1, 2009; 30(17): 2155 - 2164. [Abstract] [Full Text] [PDF] |
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J. Hedger, P. C. Holmquist, K. A. Leigh, K. Saraff, C. Pomykal, and M. L. Summers Illumination stimulates cAMP receptor protein-dependent transcriptional activation from regulatory regions containing class I and class II promoter elements in Synechocystis sp. PCC 6803 Microbiology, September 1, 2009; 155(9): 2994 - 3004. [Abstract] [Full Text] [PDF] |
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J. Ross, S. Bottardi, V. Bourgoin, A. Wollenschlaeger, E. Drobetsky, M. Trudel, and E. Milot Differential requirement of a distal regulatory region for pre-initiation complex formation at globin gene promoters Nucleic Acids Res., September 1, 2009; 37(16): 5295 - 5308. [Abstract] [Full Text] [PDF] |
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J. C. Raine and C. W. Hawryshyn Changes in thyroid hormone reception precede SWS1 opsin downregulation in trout retina J. Exp. Biol., September 1, 2009; 212(17): 2781 - 2788. [Abstract] [Full Text] [PDF] |
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U. Abdullah and P. J. Cullen The tRNA Modification Complex Elongator Regulates the Cdc42-Dependent Mitogen-Activated Protein Kinase Pathway That Controls Filamentous Growth in Yeast Eukaryot. Cell, September 1, 2009; 8(9): 1362 - 1372. [Abstract] [Full Text] [PDF] |
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M. THILL, S. BECKER, D. FISCHER, T. CORDES, A. HORNEMANN, K. DIEDRICH, D. SALEHIN, and M. FRIEDRICH Expression of Prostaglandin Metabolising Enzymes COX-2 and 15-PGDH and VDR in Human Granulosa Cells Anticancer Res, September 1, 2009; 29(9): 3611 - 3618. [Abstract] [Full Text] [PDF] |
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M. THILL, D. FISCHER, S. BECKER, T. CORDES, C. DITTMER, K. DIEDRICH, D. SALEHIN, and M. FRIEDRICH Prostaglandin Metabolizing Enzymes in Correlation with Vitamin D Receptor in Benign and Malignant Breast Cell Lines Anticancer Res, September 1, 2009; 29(9): 3619 - 3625. [Abstract] [Full Text] [PDF] |
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C. Yang, L. Su, Y. Wang, and L. Liu UTP regulation of ion transport in alveolar epithelial cells involves distinct mechanisms Am J Physiol Lung Cell Mol Physiol, September 1, 2009; 297(3): L439 - L454. [Abstract] [Full Text] [PDF] |
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V. Joshi and G. Jander Arabidopsis Methionine {gamma}-Lyase Is Regulated According to Isoleucine Biosynthesis Needs But Plays a Subordinate Role to Threonine Deaminase Plant Physiology, September 1, 2009; 151(1): 367 - 378. [Abstract] [Full Text] [PDF] |
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A. Kianianmomeni, K. Stehfest, G. Nematollahi, P. Hegemann, and A. Hallmann Channelrhodopsins of Volvox carteri Are Photochromic Proteins That Are Specifically Expressed in Somatic Cells under Control of Light, Temperature, and the Sex Inducer Plant Physiology, September 1, 2009; 151(1): 347 - 366. [Abstract] [Full Text] [PDF] |
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O. Klimchenko, M. Mori, A. DiStefano, T. Langlois, F. Larbret, Y. Lecluse, O. Feraud, W. Vainchenker, F. Norol, and N. Debili A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis Blood, August 20, 2009; 114(8): 1506 - 1517. [Abstract] [Full Text] [PDF] |
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A. Chen, I. Cuevas, P. A. Kenny, H. Miyake, K. Mace, C. Ghajar, A. Boudreau, M. Bissell, and N. Boudreau Endothelial Cell Migration and Vascular Endothelial Growth Factor Expression Are the Result of Loss of Breast Tissue Polarity Cancer Res., August 15, 2009; 69(16): 6721 - 6729. [Abstract] [Full Text] [PDF] |
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N. Mookherjee, D. N. D. Lippert, P. Hamill, R. Falsafi, A. Nijnik, J. Kindrachuk, J. Pistolic, J. Gardy, P. Miri, M. Naseer, et al. Intracellular Receptor for Human Host Defense Peptide LL-37 in Monocytes J. Immunol., August 15, 2009; 183(4): 2688 - 2696. [Abstract] [Full Text] [PDF] |
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S. Ehrlenbach, P. Willeit, S. Kiechl, J. Willeit, M. Reindl, K. Schanda, F. Kronenberg, and A. Brandstatter Influences on the reduction of relative telomere length over 10 years in the population-based Bruneck Study: introduction of a well-controlled high-throughput assay Int. J. Epidemiol., August 7, 2009; (2009) dyp273v1. [Abstract] [Full Text] [PDF] |
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I. K. Toumpoulis, J. T. Oxford, D. B. Cowan, C. E. Anagnostopoulos, C. K. Rokkas, T. P. Chamogeorgakis, D. C. Angouras, R. J. Shemin, M. Navab, M. Ericsson, et al. Differential expression of collagen type V and XI alpha-1 in human ascending thoracic aortic aneurysms. Ann. Thorac. Surg., August 1, 2009; 88(2): 506 - 513. [Abstract] [Full Text] [PDF] |
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A. Braeuning and A. Buchmann The Glycogen Synthase Kinase Inhibitor 3-(2,4-Dichlorophenyl)-4-(1-methyl-1H-indol-3-yl)-1H-pyrrole-2,5-dione (SB216763) Is a Partial Agonist of the Aryl Hydrocarbon Receptor Drug Metab. Dispos., August 1, 2009; 37(8): 1576 - 1580. [Abstract] [Full Text] [PDF] |
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M. Johnson, H. H. Phua, S. C. Bennett, J. M. Spence, and C. J. Farr Studying vertebrate topoisomerase 2 function using a conditional knockdown system in DT40 cells Nucleic Acids Res., August 1, 2009; 37(14): e98 - e98. [Abstract] [Full Text] [PDF] |
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Y. Koga, M. Pelizzola, E. Cheng, M. Krauthammer, M. Sznol, S. Ariyan, D. Narayan, A. M. Molinaro, R. Halaban, and S. M. Weissman Genome-wide screen of promoter methylation identifies novel markers in melanoma Genome Res., August 1, 2009; 19(8): 1462 - 1470. [Abstract] [Full Text] [PDF] |
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B. Birkaya, A. Maddi, J. Joshi, S. J. Free, and P. J. Cullen Role of the Cell Wall Integrity and Filamentous Growth Mitogen-Activated Protein Kinase Pathways in Cell Wall Remodeling during Filamentous Growth Eukaryot. Cell, August 1, 2009; 8(8): 1118 - 1133. [Abstract] [Full Text] [PDF] |
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R. Comitato, K. Nesaretnam, G. Leoni, R. Ambra, R. Canali, A. Bolli, M. Marino, and F. Virgili A novel mechanism of natural vitamin E tocotrienol activity: involvement of ER{beta} signal transduction Am J Physiol Endocrinol Metab, August 1, 2009; 297(2): E427 - E437. [Abstract] [Full Text] [PDF] |
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S. L. Steele, K. H. A. Lo, V. W. T. Li, S. H. Cheng, M. Ekker, and S. F. Perry Loss of M2 muscarinic receptor function inhibits development of hypoxic bradycardia and alters cardiac {beta}-adrenergic sensitivity in larval zebrafish (Danio rerio) Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2009; 297(2): R412 - R420. [Abstract] [Full Text] [PDF] |
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A. Giros, M. Grzybowski, V. R. Sohn, E. Pons, J. Fernandez-Morales, R. M. Xicola, P. Sethi, J. Grzybowski, A. Goel, C. R. Boland, et al. Regulation of Colorectal Cancer Cell Apoptosis by the n-3 Polyunsaturated Fatty Acids Docosahexaenoic and Eicosapentaenoic Cancer Prevention Research, August 1, 2009; 2(8): 732 - 742. [Abstract] [Full Text] [PDF] |
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D. E. Davis, H. C. Roh, K. Deshmukh, J. J. Bruinsma, D. L. Schneider, J. Guthrie, J. D. Robertson, and K. Kornfeld The Cation Diffusion Facilitator Gene cdf-2 Mediates Zinc Metabolism in Caenorhabditis elegans Genetics, August 1, 2009; 182(4): 1015 - 1033. [Abstract] [Full Text] [PDF] |
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J. Zhao and R. A. Dixon MATE Transporters Facilitate Vacuolar Uptake of Epicatechin 3'-O-Glucoside for Proanthocyanidin Biosynthesis in Medicago truncatula and Arabidopsis PLANT CELL, August 1, 2009; 21(8): 2323 - 2340. [Abstract] [Full Text] [PDF] |
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P. Pesaresi, A. Hertle, M. Pribil, T. Kleine, R. Wagner, H. Strissel, A. Ihnatowicz, V. Bonardi, M. Scharfenberg, A. Schneider, et al. Arabidopsis STN7 Kinase Provides a Link between Short- and Long-Term Photosynthetic Acclimation PLANT CELL, August 1, 2009; 21(8): 2402 - 2423. [Abstract] [Full Text] [PDF] |
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M. Remke, S. Pfister, C. Kox, G. Toedt, N. Becker, A. Benner, W. Werft, S. Breit, S. Liu, F. Engel, et al. High-resolution genomic profiling of childhood T-ALL reveals frequent copy-number alterations affecting the TGF-{beta} and PI3K-AKT pathways and deletions at 6q15-16.1 as a genomic marker for unfavorable early treatment response Blood, July 30, 2009; 114(5): 1053 - 1062. [Abstract] [Full Text] [PDF] |
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V. T. Samuel, S. A. Beddow, T. Iwasaki, X.-M. Zhang, X. Chu, C. D. Still, G. S. Gerhard, and G. I. Shulman Fasting hyperglycemia is not associated with increased expression of PEPCK or G6Pc in patients with Type 2 Diabetes PNAS, July 21, 2009; 106(29): 12121 - 12126. [Abstract] [Full Text] [PDF] |
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L. P. Cacheaux, S. Ivens, Y. David, A. J. Lakhter, G. Bar-Klein, M. Shapira, U. Heinemann, A. Friedman, and D. Kaufer Transcriptome Profiling Reveals TGF-{beta} Signaling Involvement in Epileptogenesis J. Neurosci., July 15, 2009; 29(28): 8927 - 8935. [Abstract] [Full Text] [PDF] |
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J. W. Leavenworth, X. Ma, Y.-y. Mo, and M. E. Pauza SUMO Conjugation Contributes to Immune Deviation in Nonobese Diabetic Mice by Suppressing c-Maf Transactivation of IL-4 J. Immunol., July 15, 2009; 183(2): 1110 - 1119. [Abstract] [Full Text] [PDF] |
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N. L. Quach, S. Biressi, L. F. Reichardt, C. Keller, and T. A. Rando Focal Adhesion Kinase Signaling Regulates the Expression of Caveolin 3 and {beta}1 Integrin, Genes Essential for Normal Myoblast Fusion Mol. Biol. Cell, July 15, 2009; 20(14): 3422 - 3435. [Abstract] [Full Text] [PDF] |
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S. Helmig, B. Hadzaad, J. Dohrel, and J. Schneider Influence of the Cyp1B1 L432V Gene Polymorphism and Exposure to Tobacco Smoke on Cyp1B1 mRNA Expression in Human Leukocytes Drug Metab. Dispos., July 1, 2009; 37(7): 1490 - 1495. [Abstract] [Full Text] [PDF] |
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L. Lin, S. Liu, H. Brockway, J. Seok, P. Jiang, W. H. Wong, and Y. Xing Using high-density exon arrays to profile gene expression in closely related species Nucleic Acids Res., July 1, 2009; 37(12): e90 - e90. [Abstract] [Full Text] [PDF] |
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S. Donat, K. Streker, T. Schirmeister, S. Rakette, T. Stehle, M. Liebeke, M. Lalk, and K. Ohlsen Transcriptome and Functional Analysis of the Eukaryotic-Type Serine/Threonine Kinase PknB in Staphylococcus aureus J. Bacteriol., July 1, 2009; 191(13): 4056 - 4069. [Abstract] [Full Text] [PDF] |
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S. Metz, A. Jager, and G. Klug In Vivo Sensitivity of Blue-Light-Dependent Signaling Mediated by AppA/PpsR or PrrB/PrrA in Rhodobacter sphaeroides J. Bacteriol., July 1, 2009; 191(13): 4473 - 4477. [Abstract] [Full Text] [PDF] |
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S. Nouaille, S. Even, C. Charlier, Y. Le Loir, M. Cocaign-Bousquet, and P. Loubiere Transcriptomic Response of Lactococcus lactis in Mixed Culture with Staphylococcus aureus Appl. Envir. Microbiol., July 1, 2009; 75(13): 4473 - 4482. [Abstract] [Full Text] [PDF] |
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J.-R. Wang, H. Hu, G.-H. Wang, J. Li, J.-Y. Chen, and P. Wu Expression of PIN Genes in Rice (Oryza sativa L.): Tissue Specificity and Regulation by Hormones Mol Plant, July 1, 2009; 2(4): 823 - 831. [Abstract] [Full Text] [PDF] |
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G. Curia, T. Papouin, P. Seguela, and M. Avoli Downregulation of Tonic GABAergic Inhibition in a Mouse Model of Fragile X Syndrome Cereb Cortex, July 1, 2009; 19(7): 1515 - 1520. [Abstract] [Full Text] [PDF] |
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K.-D. Yu, G.-H. Di, L. Fan, J. Wu, Z. Hu, Z.-Z. Shen, W. Huang, and Z.-M. Shao A functional polymorphism in the promoter region of GSTM1 implies a complex role for GSTM1 in breast cancer FASEB J, July 1, 2009; 23(7): 2274 - 2287. [Abstract] [Full Text] [PDF] |
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D. Urich, S. Soberanes, Z. Burgess, S. E. Chiarella, A. J. Ghio, K. M. Ridge, D. W. Kamp, N. S. Chandel, G. M. Mutlu, and G. R. S. Budinger Proapoptotic Noxa is required for particulate matter-induced cell death and lung inflammation FASEB J, July 1, 2009; 23(7): 2055 - 2064. [Abstract] [Full Text] [PDF] |
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C. A. Durkin, T. Mock, and E. V. Armbrust Chitin in Diatoms and Its Association with the Cell Wall Eukaryot. Cell, July 1, 2009; 8(7): 1038 - 1050. [Abstract] [Full Text] [PDF] |
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S. Kempe, P. Heinz, E. Kokai, O. Devergne, N. Marx, and T. Wirth Epstein-Barr Virus-Induced Gene-3 Is Expressed in Human Atheroma Plaques Am. J. Pathol., July 1, 2009; 175(1): 440 - 447. [Abstract] [Full Text] [PDF] |
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J. Loeffler-Ragg, D. Mueller, G. Gamerith, T. Auer, S. Skvortsov, B. Sarg, I. Skvortsova, K. J. Schmitz, H.-J. Martin, J. Krugmann, et al. Proteomic identification of aldo-keto reductase AKR1B10 induction after treatment of colorectal cancer cells with the proteasome inhibitor bortezomib Mol. Cancer Ther., July 1, 2009; 8(7): 1995 - 2006. [Abstract] [Full Text] [PDF] |
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F. Rahmani, M. Hummel, J. Schuurmans, A. Wiese-Klinkenberg, S. Smeekens, and J. Hanson Sucrose Control of Translation Mediated by an Upstream Open Reading Frame-Encoded Peptide Plant Physiology, July 1, 2009; 150(3): 1356 - 1367. [Abstract] [Full Text] [PDF] |
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T. Rose, O. Lambotte, C. Pallier, J.-F. Delfraissy, and J.-H. Colle Identification and Biochemical Characterization of Human Plasma Soluble IL-7R: Lower Concentrations in HIV-1-Infected Patients J. Immunol., June 15, 2009; 182(12): 7389 - 7397. [Abstract] [Full Text] [PDF] |
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C. van der Putten, E. A. Zuiderwijk-Sick, L. van Straalen, E. D. de Geus, L. A. Boven, I. Kondova, A. P. IJzerman, and J. J. Bajramovic Differential Expression of Adenosine A3 Receptors Controls Adenosine A2A Receptor-Mediated Inhibition of TLR Responses in Microglia J. Immunol., June 15, 2009; 182(12): 7603 - 7612. [Abstract] [Full Text] [PDF] |
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