Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression

Human interferon α2b gene was transiently expressed in Nicotiana excelsior plants. Fusion with N. plumbaginifolia calreticulin signal peptide for improved apoplast targeting and carrying out the expression under optimized conditions resulted in maximal interferon activity of 3.2 • 10³ IU/g fresh wei...

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Datum:2010
Hauptverfasser: Sindarovska, Y.R., Gerasymenko, I.M., Sheludko, Y.V., Olevinskaya, Z.M., Spivak, N.Y., Kuchuk, N.V.
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Veröffentlicht: Інститут клітинної біології та генетичної інженерії НАН України 2010
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spelling nasplib_isofts_kiev_ua-123456789-667972025-02-23T17:52:51Z Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression Получение интерферона альфа-2b человека методом Agrobacterium-опосредованной транзиентной экспрессии в Nicotiana excelsior Отримання інтерферону альфа-2b людини методом Agrobacterіum-опосередкованої транзієнтної експресії в Nіcotіana excelsіor Sindarovska, Y.R. Gerasymenko, I.M. Sheludko, Y.V. Olevinskaya, Z.M. Spivak, N.Y. Kuchuk, N.V. Оригинальные работы Human interferon α2b gene was transiently expressed in Nicotiana excelsior plants. Fusion with N. plumbaginifolia calreticulin signal peptide for improved apoplast targeting and carrying out the expression under optimized conditions resulted in maximal interferon activity of 3.2 • 10³ IU/g fresh weight (FW) with an average of 2.1 ± 0.8 • 10³ IU/g FW. It proves that N. excelsior is a suitable host for Agrobacterium-mediated transient expression of genes encoding physiologically active human proteins. The transient expression conditions optimized for GFP marker protein were confirmed to be preferable for hIFN α2b. Ген интерферона α2b был транзиентно экспрессирован в растениях Nicotiana excelsior. Слияние целевого гена с последовательностью калретикулинового сигнального пептида из N. plumbaginifolia для улучшения транспорта продукта в апопласт и проведения транзиентной экспрессии в оптимальных условиях позволило добиться максимальной активности интерферона в листьях 3.2 • 10³ МЕ/г сырой массы при среднем значении 2.1 ± 0.8 • 10³ МЕ/г. Полученные результаты свидетельствуют о возможности использования N. excelsior для Agrobacterium-опосредованной транзиентной экспрессии фармацевтически активных белков человека. Показано, что условия транзиентной экспрессии, оптимизированные для получения репортерного белка GFP, подходят также для экспрессии гена интерферона α2b человека. Ген інтерферону α2b було транзієнтно експресовано у рослинах Nіcotіana excelsіor. Злиття цільового гена з послідовністю калретикулинового сигнального пептиду з N. plumbagіnіfolіa для поліпшення транспорту продукту в апопласт і проведення транзієнтної експресії в оптимальних умовах дозволило добитися максимальної активності інтерферону в листях 3.2 • 10³ МО/г сирої маси при середньому значенні 2.1 ± 0.8 • 10³ МО/г с.в. Отримані результати свідчать про можливість використання N. excelsіor для Agrobacterіum-опосередкованої транзієнтної експресії фармацевтично активних білків людини. Було показано, що умови транзієнтної експресії, оптимізовані для отримання репортерного білка GFP, підходять також для експресії гена інтерферону α2b людини. 2010 Article Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression / Y.R. Sindarovska, I.M. Gerasymenko, Y.V. Sheludko, Z.M. Olevinskaya, N.Y. Spivak, N.V. Kuchuk // Цитология и генетика. — 2010. — Т. 44, № 5. — С. 60-64. — Бібліогр.: 32 назв. — англ. 0564-3783 https://nasplib.isofts.kiev.ua/handle/123456789/66797 57.084.1+582.926.2+577.21 en Цитология и генетика application/pdf Інститут клітинної біології та генетичної інженерії НАН України
institution Digital Library of Periodicals of National Academy of Sciences of Ukraine
collection DSpace DC
language English
topic Оригинальные работы
Оригинальные работы
spellingShingle Оригинальные работы
Оригинальные работы
Sindarovska, Y.R.
Gerasymenko, I.M.
Sheludko, Y.V.
Olevinskaya, Z.M.
Spivak, N.Y.
Kuchuk, N.V.
Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
Цитология и генетика
description Human interferon α2b gene was transiently expressed in Nicotiana excelsior plants. Fusion with N. plumbaginifolia calreticulin signal peptide for improved apoplast targeting and carrying out the expression under optimized conditions resulted in maximal interferon activity of 3.2 • 10³ IU/g fresh weight (FW) with an average of 2.1 ± 0.8 • 10³ IU/g FW. It proves that N. excelsior is a suitable host for Agrobacterium-mediated transient expression of genes encoding physiologically active human proteins. The transient expression conditions optimized for GFP marker protein were confirmed to be preferable for hIFN α2b.
format Article
author Sindarovska, Y.R.
Gerasymenko, I.M.
Sheludko, Y.V.
Olevinskaya, Z.M.
Spivak, N.Y.
Kuchuk, N.V.
author_facet Sindarovska, Y.R.
Gerasymenko, I.M.
Sheludko, Y.V.
Olevinskaya, Z.M.
Spivak, N.Y.
Kuchuk, N.V.
author_sort Sindarovska, Y.R.
title Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
title_short Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
title_full Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
title_fullStr Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
title_full_unstemmed Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression
title_sort production of human interferon alfa 2b in plants of nicotiana excelsior by agrobacterium-mediated transient expression
publisher Інститут клітинної біології та генетичної інженерії НАН України
publishDate 2010
topic_facet Оригинальные работы
url https://nasplib.isofts.kiev.ua/handle/123456789/66797
citation_txt Production of human interferon alfa 2b in plants of Nicotiana excelsior by Agrobacterium-mediated transient expression / Y.R. Sindarovska, I.M. Gerasymenko, Y.V. Sheludko, Z.M. Olevinskaya, N.Y. Spivak, N.V. Kuchuk // Цитология и генетика. — 2010. — Т. 44, № 5. — С. 60-64. — Бібліогр.: 32 назв. — англ.
series Цитология и генетика
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fulltext УДК 57.084.1+582.926.2+577.21 Y.R. SINDAROVSKA 1, I.M. GERASYMENKO 1, Y.V. SHELUDKO 1, Z.M. OLEVINSKAYA 2, N.Y. SPIVAK 2, N.V. KUCHUK 1 1 Institute of Cell Biology and Genetic Engineering NAS of Ukraine, Kiev 03680, Ukraine, E�mail: ysheludko@ukr.net 2 Institute of Microbiology and Virology NAS of Ukraine, Kiev PRODUCTION OF HUMAN INTERFERON ALFA 2b IN PLANTS OF NICOTIANA EXCELSIOR BY AGROBACTERIUM� MEDIATED TRANSIENT EXPRESSION Human interferon α2b gene was transiently expressed in Nicotiana excelsior plants. Fusion with N. plumbaginifolia calreticulin signal peptide for improved apoplast targeting and carrying out the expression under optimized conditions result� ed in maximal interferon activity of 3.2 · 103 IU/g fresh weight (FW) with an average of 2.1 ± 0.8 · 103 IU/g FW. It proves that N. excelsior is a suitable host for Agrobacterium�mediat� ed transient expression of genes encoding physiologically active human proteins. The transient expression conditions optimized for GFP marker protein were confirmed to be preferable for hIFN α2b. Introduction. Interferons are a large family of multifunctional secreted proteins involved in ani� mal antiviral defence, cell growth regulation and immune system activation [1]. Interferons are used to treat several diseases including some types of cancer and hepatitis C [1]. Recombinant human interferons have been produced in bacteria, yeast, insect and mammalian cells, and several plant species [2–11]. Plants as a source of foreign pro� teins have a number of advantages over microbial or animal cell systems. In contrast to bacteria cor� rect posttranslational modifications of recombi� nant proteins take place in plant cells as well as folding and assembling of multimeric proteins, e.g. antibodies [12–14]. Plants do not contain bacteri� al toxins and human pathogens like viruses and prions, that makes the recombinant proteins of plant origin safer [15]. In some cases they can be used without prior purification as edible vaccines that lowers production costs considerably [15]. The main drawback of plants with stably trans� formed nuclear genome is the moderate level of target protein accumulation. The recombinant protein production usually does not exceed of 1 % of total soluble proteins (TSP) [16] due to the low transgene expression level and/or the protein product instability (for strategies to enhance stable transgene expression and product accumulation in plants, see [17]). Plastid transformation often allows selecting of transplastomic plants with high level of recombinant protein accumulation [18]. However, it is a time�consuming task, up to date feasible for a restricted number of plant species. Modern approaches to transient gene expression in plants lead to accumulation of large amount of recombinant proteins within a very short time [19]. This method was successfully applied for produc� tion of a number of recombinant proteins, e.g. tumor�specific antibodies [20] and vaccines [21] and human growth hormone [22]. The efficiency of the transient expression may be increased by vector system modification [23, 24] and/or by opti� mization of the expression conditions and choosing of an appropriate plant host species [25]. Here we report the production of active human interferon alfa 2b in plants of Nicotiana excelsior, previously selected as a promising host species for Agrobacterium�mediated transient expression using GFP marker protein [25]. Materials and methods. Plant material. Seeds of N. benthamiana and N. excelsior were obtained from the National Germplasm Bank of World Flora of ISSN 0564–3783. Цитология и генетика. 2010. № 560 © Y.R. SINDAROVSKA, I.M. GERASYMENKO, Y.V. SHELUDKO, Z.M. OLEVINSKAJA, N.Y. SPIVAK, N.V. KUCHUK, 2010 the Institute of Cell Biology and Genetic Enginee� ring (Kiev, Ukraine). In greenhouse plants were grown at 20–25 °С and 14 h light period (3000– 4000 lux). Bacterial strains and genetic constructs. Genetic constructs pICH10881, pICH10570, pICH13301 (with the native hIFN�α2b gene), pICH17311 (with the recombinant hIFN�α2b gene) and pICH7410 (with reporter GFP gene) represent a viral�based module vector system described in details in [23]. The plasmid pICH6692 contained the gene of the p19 protein of tomato bushy stunt virus, a suppres� sor of post�transcriptional gene silencing [26] driven by 35S CaMV promoter. All the mentioned plas� mids were obtained for scientific purposes from Icon Genetics GmbH (Halle/Saale, Germany). Agrobacterium tumefaciens strain GV3101 trans� formed with individual constructs was grown overnight in LB medium supplemented with 50 mg/l of rifampicin and 50 mg/l of carbenicillin or kanamycin, and 100 μM of acetosyringone. Transient expression assay. Plant infiltration was performed as described in [27] with several modi� fications [23]: A. tumefaciens cells of overnight cul� ture were centrifuged and resuspended with the infiltration buffer (10 mM MES, pH 5.5; 10 mM MgSO4; 100 μM acetosyringone). The Agrobacte� rium suspensions harboring different plasmid vec� tors were mixed in the equal volumes so that the final optical density (OD 600) of each suspension in the infiltration buffer amounted 0.5. The leaves of greenhouse grown plants were infiltrated with Agrobacterium mixture (50 mkl/leaf) by using a syringe without a needle. The Agrobacterium mix� ture was injected into mesophile tissue of the 2nd – 4th upper leaves. After infiltration, the plants were further grown under greenhouse conditions and harvested at 14–18 days post infiltration. All exper� iments were carried out in 4–6 replications. Interferon activity assay. Extracts from plant leaves were prepared in equal volume of 100 mM Tris/HCl buffer, pH 8.0, containing 5 mM Na2EDTA, 100 mM NaCl, 10 mM β�mercap� toethanol, and 2.5 % PVP. The total protein con� tent was measured by the method of Bradford [28]. The assays were performed in sterile 96�well microtiter plates. Each well was filled with 100 μl of transmissible neonatal pig testis cell suspension (105 cell/ml) in RPMI�1640 medium [31]. The cells were cultivated for 18 hours at 37 °С. Samples to be titrated for interferon activity were diluted 20�fold with RPMI�1640 medium and placed in the first row of wells of an empty plate. Two�fold dilu� tions of the samples with RPMI�1640 medium were made serially to the end of the well columns. The RPMI�1640 medium in the wells with the cells was replaced with sample dilution rows and the cells were further incubated for 18 hours at 37 °С. The� reafter 100 μl of vesicular stomatitis virus (100 CPE50/0.1 ml) was added to each well (except of cell control wells, where 100 μl of RPMI�1640 medium were applied). The cells were cultivated at 37 °С for 24 hours (until the cytopathic effect was fully developed in the virus control wells). The medium from the wells was evaporated and the cells were stained with crystal violet. The wells where 50 % of the cells were protected from the virus cytopathic effect were detected by microscop� ic examination. Standard interferon solution was included in all assays to determine the absolute titer. Results and discussion. Transient expression is often carried out in N. benthamiana [e.g., 14, 22], but this plant species has a rather small biomass yield that hinders its application for large�scale production of recombinant proteins. In our previ� ous studies we have selected N. excelsior as a better host for transient expression. This species dis� played the best characteristics in regard to biomass yield as well as GFP accumulation level [25]. The target hIFN�α2b gene was introduced into N. excelsior plants as a part of a viral�based module vector system. This system consists of three ele� ments delivered in plant by simultaneous infiltra� tion of Agrobacterium strains carrying correspon� ding plasmids. Two modules containing viral genes and regulatory elements and the target gene are combined inside of the plant cell by the Streptomyces phage PhiC31 site�specific recombinase encoded in the third plasmid. The resulting DNA molecule contains the viral genes of the RNA�dependent RNA polymerase, movement protein and the tar� get gene driven by the subgenomic promoter of a viral coat protein. DNA is able to move from cell to cell due to the movement protein [23]. In our experiments the greenhouse grown N. excelsior plants were infiltrated with a mixture of four Agrobacterium strains carrying the three mod� ules of the viral�based expression system and a vec� tor with the gene encoding p19 protein of tomato bushy stunt virus, a suppressor of gene silencing ІSSN 0564–3783. Цитология и генетика. 2010. № 5 61 Production of human interferon alfa 2b in plants of Nicotiana excelsior [26]. For monitoring of the transient expression process, one of the leaves on each plant was infiltrat� ed with an analogous Agrobacterium mixture but carrying the marker GFP gene instead of hIFN� α2b. The activity of interferon in the leaf extracts was measured by its ability to protect animal cells in vitro against viral replication [29, 30]. For the construct with native hIFN�α2b gene we deter� mined interferon activity in the extracts and found that it reached the maximum level of 8 · 102 IU/g FW with an average of 1.3 ± 0.59 · 102 IU/g FW. This value corresponds to 1.3–2 ng/g of leaf fresh weight. We checked several parameters which were shown to influence on recombinant protein produc� tion via transient expression using GFP as a reporter [25]. It was found that the activity of interferon was approximately 3–4 times higher in the upper leaves of the plant than in lower ones (2.5 · 102 IU/g and 0.65 · 102 IU/g, respectively). Co�expression of the p19 protein, a suppressor of gene silencing [17], improved the interferon yield at least 15�fold (8 · 102 IU/g compared with 0.5 · 102 IU/g in the experiments without the p19 suppressor of silenc� ing). These data corresponds well to the results obtained for GFP reporter protein [25]. The accumulation level of interferon was consid� erably lower than that of GFP obtained under the same conditions [25]. These results can be explained by lower stability of interferon in the plant cells as compared with GFP. The action of cell proteases is known to be a limiting factor for recombinant pro� tein accumulation in plants [32]. One of possible ways to overcome this problem is subcellular pro� tein targeting to organelles (e.g. chloroplasts or endoplasmic reticulum (ER)) or into apoplast [17, 22]. It is accomplished by fusion of the protein of interest with specific aminoacid sequences that direct it to the corresponding cell compartment. To be excreted into apoplast, a protein should con� tain on its N�terminus a signal sequence that is usually cleaved during protein translocation through the ER membrane. Native hIFN�α2b gene encodes signal sequence that ensures its secretion from leukocytes. This sequence supports analogous tar� geting in plant cells, but possibly at lower rate. To amend the process of interferon excretion into apoplast, we have used a recombinant hIFN� α2b gene attached to N. plumbaginifolia calretic� ulin signal peptide. It was reported previously that fusion with N. plumbaginifolia calreticulin signal peptide led to high level of transient expression of hIFN�α2b gene in N. benthamiana [22]. In our experiments the transient expression of the recom� binant hIFN�α2b gene resulted in approximately 15�fold higher interferon activity than in case of using the native gene (2.06 ± 7.8 · 103 IU/g of leaf extract corresponding to 20–30 ng/g FW) (Figure). The maximum activity amounted to 3,2 · 103 IU/g of leaf extract (30–50 ng/g FW). Physiologically active human interferons have been produced earlier in several plant species by stable nuclear transformation [2–7], chloroplast transformation [8] and transient expression [9– 11]. The highest level of hIFN�α2b (up to 20 % TSP, or 3 mg/g FW) was reported for tobacco transplastomic plants [8]. The interferon activity in stable nuclear transformants reached approximate� ly 5 · 102 IU/g FW [5, 11]. Transient expression resulted in approximately 10�fold higher activities (3.1 · 104 IU/ml for interferon β in lettuce [10] and 2.1 · 104 IU/g FW for interferon α2a in cucurbits [9]), although in some cases the interferon con� tent was lower (0.3 ng/g FW for chicken interferon α in lettuce [11]). Our results with 2.1 ± 0.8 · 103 IU/g FW of human interferon α2b in N. excelsior prove the effectiveness of the transient expression method. We can conclude that N. excelsior is a suitable host for transient expression of genes encoding physiologically active human proteins, e.g. inter� feron α2b. The transient expression conditions optimized for GFP marker protein were con� firmed to be preferable for hIFN α2b. ISSN 0564–3783. Цитология и генетика. 2010. № 562 Y.R. Sindarovska, I.M. Gerasymenko, Y.V. Sheludko et al. Activity of interferon in leaf extracts of N. excelsior transient� ly expressing native or recombinant (fused to N. plumbagini� folia calreticulin signal peptide) human interferon α2b gene Я.Р. Синдаровская, И.М. Герасименко, Ю.В. Шелудько, З.M. Олевинская, Н.Я. Спивак, Н.В. Кучук ПОЛУЧЕНИЕ ИНТЕРФЕРОНА АЛЬФА�2b ЧЕЛОВЕКА МЕТОДОМ AGROBACTERIUM� ОПОСРЕДОВАННОЙ ТРАНЗИЕНТНОЙ ЭКСПРЕССИИ В NICOTIANA EXCELSIOR Ген интерферона α2b был транзиентно экспресси� рован в растениях Nicotiana excelsior. Слияние целевого гена с последовательностью калретикулинового сиг� нального пептида из N. plumbaginifolia для улучшения транспорта продукта в апопласт и проведения транзи� ентной экспрессии в оптимальных условиях позволило добиться максимальной активности интерферона в листьях 3.2 · 10 3 МЕ/г сырой массы при среднем зна� чении 2.1 ± 0.8 · 10 3 МЕ/г. Полученные результаты свидетельствуют о возможности использования N. excel� sior для Agrobacterium�опосредованной транзиентной экспрессии фармацевтически активных белков чело� века. Показано, что условия транзиентной экспрессии, оптимизированные для получения репортерного белка GFP, подходят также для экспрессии гена интерферона α2b человека. Я.Р. Сіндаровська, І.М. Герасименко, Ю.В. Шелудько, З. M. Олевинська, М.Я. Співак, М.В. Кучук ОТРИМАННЯ ІНТЕРФЕРОНУ АЛЬФА�2b ЛЮДИНИ МЕТОДОМ AGROBACTERІUM� ОПОСЕРЕДКОВАНОЇ ТРАНЗІЄНТНОЇ ЕКСПРЕСІЇ В NІCOTІANA EXCELSІOR Ген інтерферону α2b було транзієнтно експресовано у рослинах Nіcotіana excelsіor. Злиття цільового гена з послідовністю калретикулинового сигнального пепти� ду з N. plumbagіnіfolіa для поліпшення транспорту про� дукту в апопласт і проведення транзієнтної експресії в оптимальних умовах дозволило добитися максимальної активності інтерферону в листях 3.2 · 10 3 МО/г сирої маси при середньому значенні 2.1 ± 0.8 · 10 3 МО/г с.в. 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Received 16.03.10 ISSN 0564–3783. Цитология и генетика. 2010. № 564 Y.R. Sindarovska, I.M. Gerasymenko, Y.V. Sheludko et al.