The SEA complex – the beginning

Наличие разнообразных внутриклеточных мембранных органелл, динамически связанных посредством селективного транспорта, является отличительной особенностью эукариотической клетки. Множество белков, необходимых для образования и существования этих органелл, имеют сходную эволюционную историю. Недавно м...

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Hauptverfasser: Algret R., Dokudovskaya, S.S.
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Zitieren:The SEA complex – the beginning / R.Algret, S.S. Dokudovskaya // Вiopolymers and Cell. — 2012. — Т. 28, № 4. — С. 281–284. — Бібліогр.: 20 назв. — англ.

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Digital Library of Periodicals of National Academy of Sciences of Ukraine
id nasplib_isofts_kiev_ua-123456789-156925
record_format dspace
spelling Algret R.
Dokudovskaya, S.S.
2019-06-19T10:54:08Z
2019-06-19T10:54:08Z
2012
The SEA complex – the beginning / R.Algret, S.S. Dokudovskaya // Вiopolymers and Cell. — 2012. — Т. 28, № 4. — С. 281–284. — Бібліогр.: 20 назв. — англ.
0233-7657
DOI: http://dx.doi.org/10.7124/bc.00005A
https://nasplib.isofts.kiev.ua/handle/123456789/156925
577.22
Наличие разнообразных внутриклеточных мембранных органелл, динамически связанных посредством селективного транспорта, является отличительной особенностью эукариотической клетки. Множество белков, необходимых для образования и существования этих органелл, имеют сходную эволюционную историю. Недавно мы открыли новый консервативный белковый комплекс – SEA-комплекс, обладающий структурными характеристиками, схожими с таковыми мембран транспортных везикул (COPII), а также их вспомогательных партнеров (HOPS/CORVET) и ядерной поры (NPC). Дрожжевой SEA-комплекс динамически взаимодействует с вакуолями. Данные о функции SEA-комплекса очень малочисленны. В представленном миниобзоре обсуждается возможная функция SEA-комплекса, основываясь на результатах генетических и функциональных исследований, проведенных на дрожжах и других эукариотах. Ключевые слова: дрожжи Saccharomyces cerevisiae, SEA-комплекс, вакуоли.
Наявність різноманітних внутрішньоклітинних мембранних органел, динамічно пов’язаних за посередництвом селективного транспорту, є відмінною особливістю еукаріотичної клитини. Багато білків, необхідних для утворення та існування цих органел, мають подібну еволюційну історію. Недавно ми відкрили новий консервативний білковый комплекс – SEA-комплекс, якому притаманні структурні характеристики, схожі з такими мембран транспортных везикул (COPII) та їхніх допоміжних партнерів (HOPS/ CORVET) і ядерної пори (NPC). Дріжджовий SEA-комплекс динамічно взаємодіє з вакуолями. Дані щодо функції SEA-комплексу є доволі малочисельними. В представленому мініогляді обговорюється можлива функція SEA-комплексу з урахуванням результатів генетичних і функціональних досліджень, проведених на дріжджах та інших еукаріотах. Ключові слова: дріжджі Saccharomyces cerevisiae, SEA-комплекс, вакуолі.
The presence of distinctive internal membrane compartments, dynamically connected via selective transport pathways, is a hallmark of eukaryotic cells. Many of the proteins required for formation and maintenance of these compartments share an evolutionary history. We have recently identified a new conserved protein complex – the SEA complex – that possesses proteins with structural characteristics similar to the membrane coating complexes such as the nuclear pore complex (NPC), the COPII vesicle coating complex and HOPS/CORVET tethering complexes. The SEA complex in yeast is dynamically associated to the vacuole. The data on the function of the SEA complex remain extremely limited. Here we will discuss a possible role of the SEA complex based on the data from genetic assays and a number of functional studies in both yeast and other eukaryotes. Keywords: Saccharomyces cerevisiae, the SEA complex, vacuoles.
en
Інститут молекулярної біології і генетики НАН України
Вiopolymers and Cell
Minireviews
The SEA complex – the beginning
SEA-комплекс – початок
SEA-комплекс – начало
Article
published earlier
institution Digital Library of Periodicals of National Academy of Sciences of Ukraine
collection DSpace DC
title The SEA complex – the beginning
spellingShingle The SEA complex – the beginning
Algret R.
Dokudovskaya, S.S.
Minireviews
title_short The SEA complex – the beginning
title_full The SEA complex – the beginning
title_fullStr The SEA complex – the beginning
title_full_unstemmed The SEA complex – the beginning
title_sort sea complex – the beginning
author Algret R.
Dokudovskaya, S.S.
author_facet Algret R.
Dokudovskaya, S.S.
topic Minireviews
topic_facet Minireviews
publishDate 2012
language English
container_title Вiopolymers and Cell
publisher Інститут молекулярної біології і генетики НАН України
format Article
title_alt SEA-комплекс – початок
SEA-комплекс – начало
description Наличие разнообразных внутриклеточных мембранных органелл, динамически связанных посредством селективного транспорта, является отличительной особенностью эукариотической клетки. Множество белков, необходимых для образования и существования этих органелл, имеют сходную эволюционную историю. Недавно мы открыли новый консервативный белковый комплекс – SEA-комплекс, обладающий структурными характеристиками, схожими с таковыми мембран транспортных везикул (COPII), а также их вспомогательных партнеров (HOPS/CORVET) и ядерной поры (NPC). Дрожжевой SEA-комплекс динамически взаимодействует с вакуолями. Данные о функции SEA-комплекса очень малочисленны. В представленном миниобзоре обсуждается возможная функция SEA-комплекса, основываясь на результатах генетических и функциональных исследований, проведенных на дрожжах и других эукариотах. Ключевые слова: дрожжи Saccharomyces cerevisiae, SEA-комплекс, вакуоли. Наявність різноманітних внутрішньоклітинних мембранних органел, динамічно пов’язаних за посередництвом селективного транспорту, є відмінною особливістю еукаріотичної клитини. Багато білків, необхідних для утворення та існування цих органел, мають подібну еволюційну історію. Недавно ми відкрили новий консервативний білковый комплекс – SEA-комплекс, якому притаманні структурні характеристики, схожі з такими мембран транспортных везикул (COPII) та їхніх допоміжних партнерів (HOPS/ CORVET) і ядерної пори (NPC). Дріжджовий SEA-комплекс динамічно взаємодіє з вакуолями. Дані щодо функції SEA-комплексу є доволі малочисельними. В представленому мініогляді обговорюється можлива функція SEA-комплексу з урахуванням результатів генетичних і функціональних досліджень, проведених на дріжджах та інших еукаріотах. Ключові слова: дріжджі Saccharomyces cerevisiae, SEA-комплекс, вакуолі. The presence of distinctive internal membrane compartments, dynamically connected via selective transport pathways, is a hallmark of eukaryotic cells. Many of the proteins required for formation and maintenance of these compartments share an evolutionary history. We have recently identified a new conserved protein complex – the SEA complex – that possesses proteins with structural characteristics similar to the membrane coating complexes such as the nuclear pore complex (NPC), the COPII vesicle coating complex and HOPS/CORVET tethering complexes. The SEA complex in yeast is dynamically associated to the vacuole. The data on the function of the SEA complex remain extremely limited. Here we will discuss a possible role of the SEA complex based on the data from genetic assays and a number of functional studies in both yeast and other eukaryotes. Keywords: Saccharomyces cerevisiae, the SEA complex, vacuoles.
issn 0233-7657
url https://nasplib.isofts.kiev.ua/handle/123456789/156925
citation_txt The SEA complex – the beginning / R.Algret, S.S. Dokudovskaya // Вiopolymers and Cell. — 2012. — Т. 28, № 4. — С. 281–284. — Бібліогр.: 20 назв. — англ.
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fulltext 281 MINIREVIEWS UDC 577.22 The SEA complex – the beginning R. Algret, S. S. Dokudovskaya CNRS UMR 8126, UniversitJ Paris-Sud 11, Institut Gustave Roussy 114, rue Edouard Vaillant, Villejuif, France, 94805 s.dokud@gmail.com The presence of distinctive internal membrane compartments, dynamically connected via selective transport pathways, is a hallmark of eukaryotic cells. Many of the proteins required for formation and maintenance of these compartments share an evolutionary history. We have recently identified a new conserved protein complex – the SEA complex – that possesses proteins with structural characteristics similar to the membrane coating comp- lexes such as the nuclear pore complex (NPC), the COPII vesicle coating complex and HOPS/CORVET tethe- ring complexes. The SEA complex in yeast is dynamically associated to the vacuole. The data on the function of the SEA complex remain extremely limited. Here we will discuss a possible role of the SEA complex based on the data from genetic assays and a number of functional studies in both yeast and other eukaryotes. Keywords: Saccharomyces cerevisiae, the SEA complex, vacuoles. What is the SEA complex? The SEA complex is a ~1 MDa protein complex that was discovered in yeast Saccharo- my ces cerevisiae during immunopurification of genomi- cally tagged version of one of the components of the NPC, the nucleoporin Seh1 [1]. As a bone fide nucleoporin, Seh1 co-purifies with the Nup84 subcomplex, a key com- ponent of the NPC’s membrane-coating scaffold. How- ever, Seh1 also co-purifies with Npr2, Npr3, Sec13 and four high-molecular-weight proteins (Yjr138p (Iml1), Yol138p (Rtc1), Ydr128p (Mtc5), and Ybl104p). To ref- lect their association with Seh1, these proteins were gi- ven a common name, Sea (for Seh1-associated), and were renamed Sea1 through Sea4, respectively. Tagged ver- sions of each of Sea1–Sea4 copurified with each other, and with Seh1, Sec13, Npr2, and Npr3. Sec13 is also a member of the NPC’s Nup84 subcomplex. In addition, Sec13 interacts with Sec31 in ER-trafficking COPII vesicles; however, other NPC proteins or members of COPII vesicles were not found to be associated with the Sea proteins, and the Sea proteins did not localize to the NPC or ER, confirming that this group of proteins forms a novel and distinct complex, the SEA complex, entire- ly separate from the NPC or COPII. How conserved is the SEA complex? The full SEA complex is specific to animals and fungi [1]. There is no evidence for any SEA complex gene in plants (with the exception of Seh1 and Sec13, which certainly fulfill other functions in this lineage). In other eukaryotic su- pergroups the SEA complex members are not always re- tained. The evolutionary profile of the SEA complex suggests that it might be dispensable in many biolo- gical contexts, having a specialized life-style specific role rather than a function central to eukaryotic fitness. Where is the SEA complex localized? The expres- sion level of the SEA complexes members is very low both in yeast and in human cells, which make the task of their localization challenging. Nevertheless the com- bination of subcellular fractionation and fluorescent microscopy detected yeast SEA complex as dynamical- ly associated to the vacuole membrane [1]. The proteo- mic study of human placenta lysosomes also found ho- mologues of Sea1, Sea2, Sea4, Seh1, and Sec13 to be as- sociated to the lysosomal membrane [2]. However, be- cause of the low level of expression of the SEA comp- lex components it is possible that they can be found el- sewhere in the cell. What is the structural specificity of the SEA comp- lex members? Sea proteins contain structural elements ISSN 0233–7657. Biopolymers and Cell. 2012. Vol. 28. N 4. P. 281–284 Ó Institute of Molecular Biology and Genetics, NAS of Ukraine, 2012 present in intracellular structural trafficking complexes [1]. For example, the Sea2-Sea4 proteins are predicted to possess a b-propeller/a-solenoid architecture charac- teristic of proteins that form coats around membranes and participate in membrane tethering. Notably, SEA complex contains five proteins with b-propellers, a do- main common in coating assemblies. Among those pro- teins with b-propellers are Seh1 and Sec13 – two evolu- tionary conserved paraloges that are known members of other coating assemblies – NPC (both proteins) and COPII (Sec13 only). Seh1 forms a dimer with Sea4, which besides b-propeller and a-solenoid, contains a C-terminal RING domain. The structural organization of the Sea4 is identical to a number of proteins in HOPS and CORVET complexes, which have been implicated in tethering membranes together prior to their fusion. Similar to several proteins of HOPS/CORVET Sea2– Sea4 have a C-terminal RING domain. The high fre- quency of RING domains in the SEA complex suggests that the complex may act as an E3 ubiquitin ligase. What did we learn about SEA complex function from yeast studies? Not too much so far. The majority of the data concerns Npr2 and Npr3. These two proteins in yeast act as upstream regulators of TORC1 kinase in response to nitrogen starvation [3]. Accordingly, the process of autophagy, which is induced in the response to nitrogen starvation, is impaired in the absence of Npr2 and to some extent of Npr3 [1, 4]. Interestingly, Npr2, Npr3 and Sea1 also required for a specific varia- tion of autophagy, which can be induced in the absence of nitrogen starvation, but simply upon the change from rich to a minimal medium [5]. Otherwise SEA complex deletion strains exhibited relatively robust growth under a broad range of tests [1] (http://www.yeastgenome.org/). This presumes that the SEA complex functions alongside other related comp- lexes and may be redundant under numerous growth conditions. However, complete redundancy is unlike- ly given evolutionary conservation of SEA complex subunits, especially in the animals and fungi. Recent papers on yeast synthetic genetic interactions [6] and chemical genetic profiles [7] shed a bit of a light on a possible role of the SEA complex. Analysis of these data suggests that SEA complex members are impli- cated in multiple genetic interactions with genes res- ponsible for cell wall biogenesis and integrity, amino acid biogenesis and sorting, membrane trafficking, ubiquitination and autophagy. One of the strongest genetic interactions that invol- ve SEA complex members is the cooperation with the genes responsible for cell wall biogenesis and integri- ty. Thus, all five SEA complex genes appeared in Cos- tanzo et al. [6] survey exhibit genetic interaction with MAP kinase Bck1; four SEA complex genes involved in genetic interaction with another MAP kinase – Slt2. In addition, Sea4 is synthetically lethal with Las21 – an integral plasma membrane protein involved in the syn- thesis of the glycosylphosphatidylinositol (GPI) core structure [8]. Similar to SEA complex genes Las21 is involved in negative genetic interactions with Pkc1 and Slt2 [6] and synthetically lethal with Bck1 [8]. A gene cohort involved in amino acid biosynthesis and sorting exhibits a large number of strong genetic in- teractions with SEA complex subunits. Notably, HOPS/ CORVET belongs to this same interaction cluster [6], further underscoring the similarity between these comp- lexes and the SEA complex. One module in the cluster is responsible for sorting of a general amino acid per- mease Gap1. Gap1 is a general amino acid permease that can transport all amino acids. GAP1 is transcriptio- nally regulated by the available nitrogen source via nit- rogen catabolite repression (NCR). Interestingly, both Npr2 and Npr3 are probably involved in the NCR cont- rol [9]. Gap1 sorting is mediated by number of proteins and complexes, including EGO complex, Lst proteins and Rsp5-Bul1-Bul2 trimer, which ubiquitinate Gap1 itself. All of these genes display genetic interactions with the SEA complex members. In addition chemical genomic survey reports that Sea2, Sea4 and Sec13 show similar homozygous co-fitness with a number of genes involved in Gap1 sorting [7]. The most striking examples of SEA components ge- netic interaction is connection with genes involved in the biosynthesis of homoserine with almost entire set of the genes responsible for this pathway exhibiting very strong genetic interactions with 4 or 5 SEA complex members [6]. The majority of amino acids biosynthesis pathway genes, including those, involved in the genetic interac- tions with SEA complex genes are regulated by Gcn4 transcriptional activator [10]. Strikingly, Sea4 has mul- tiple Gcn4 binding sites in its promoter [11], and there- fore can be implicated in the control of amino acid biosyn- 282 ALGRET R., DOKUDOVSKAYA S. S. thesis. Interestingly, a chemical genomic survey identi- fied a small group of genes, required for resistance to di- verse perturbations [7]. These genes referred to as multi- drug resistance (MDR). Genes that involved in aromatic amino acid biosynthesis (and synthetic genetic interac- tions with SEA components), GCN4 and NPR2 together with NPR3 are all belong to the MDR group. By the way, NPR2 and NPR3 exhibit absolutely identical co-fitness of respective homozygous deletion strains in chemical genomic survey, which is a strong indication for these two proteins share similar biological process and mo- lecular function [7]. All the observations described here suggest that the SEA complex plays a role in the regu- lation of amino acid biosynthesis and autophagy. What do we know about SEA complex components in high eukaryotes? The fact that all SEA complex mem- bers were retained in higher eukaryotes underlines func- tional importance of this assembly. Nevertheless, infor- mation about SEA complex components in higher euka- ryotes is even more limited than in yeast. So far no pa- pers were published on Sea1, Sea2, Sea3 homologues. Sea4 homologue in Drosophila (missing oocyte, mio) is localized to the nucleus and required for the mainte- nance of the meiotic cycle and oocyte identity [12]. Im- portantly, Mio forms a complex with Seh1. Both pro- teins are dispensable for somatic development, but re- quired for development of the mature egg. In addition Seh1 is required for Mio protein stability [13]. Human Seh1 also functions in chromosome alignment and se- gregation by regulating the centromeric localization of Aurora B and other chromosome passenger complex proteins [14]. Although Sea1-Sea4 and Npr2, Npr3 seems not to be present in plants, Seh1 in Arabidopsis is found in multiple locations, including nucleus, Golgi and prevacuolar compartment. AtSeh1 is suggested to play a role in membrane association of dynamin-rela- ted protein 2A, which is in turn required for protein traf- ficking from trans-Golgi network to the central vacuole [15]. Npr2 homologue in human – Nprl2 – has been cha- racterized as a novel tumor suppressor [16]. Low ex- pression of Nprl2 in different types of lung cancers and other tumors was correlated with resistance to cisplatin, one of the mainstays of chemotherapy for lung cancer [17]. Remarkably, the first information about cisplatin resistance of Npr2 deletion strains came from the stu- dies in yeast [18]. Nprl2 interacts with Pdk1 kinase, a key regulator of cell proliferation and survival [19]. Interestingly, Pdk1, which plays a role in cellular trans- formation and tumor growth, is one of the well-defined upstream regulators of TORC1 pathway in mammalian cells. In addition Nprl2 forms a complex with Npr3 homologue Nprl3 [3], which suggests that Nprl2/Nprl3 might also signal to TORC1, similar to their yeast coun- terparts. Finally a recent study has demonstrated that Nprl3 (C16orf35) is a nucleocytoplasmic protein that interacts with transcriptional factor p73, a member of p53 family proteins involved in tumor suppression and embryonic development [20]. What are the future directions in the SEA complex study? The study of the SEA complex is in its primary steps and all directions are open and have to be explo- red. The importance of the SEA complex is underlined by the fact that all of its components have been retained in animals and fungi. The integrative approaches which can combine data on structure, function, regulation and coming from different model organisms should be the most informative. The results of these studies might be of a broad interest given that the Nprl2 in human has been characterized as a novel tumor suppressor [16] and the Nprl3 interacts with p73 [20] – a member of p53 family of transcription factors involved in tumor suppression. Acknowledgements. We are grateful to the support from Fondation de France, Fondation pour la Recher- che Medicale and Fondation Gustave Roussy. Ð. Àëãðå, Ñ. Ñ. Äî êó äî âñüêà SEA-êîì ïëåêñ – ïî ÷à òîê Ðå çþ ìå Íà ÿâí³ñòü ð³çíî ìàí³òíèõ âíóòð³øíüîêë³òèí íèõ ìåì áðàí íèõ îðãà- íåë, äè íàì³÷íî ïî â’ÿ çà íèõ çà ïî ñå ðåä íèö òâîì ñå ëåê òèâ íî ãî òðàíñ- ïîðòó, º â³äì³ííîþ îñîá ëèâ³ñòþ åó êàð³îò è÷ íî¿ êëè òè íè. Áà ãà òî á³ëê³â, íå îáõ³äíèõ äëÿ óòâî ðåí íÿ òà ³ñíó âàí íÿ öèõ îðãà íåë, ìà þòü ïîä³áíó åâî ëþö³éíó ³ñòîð³þ. Íå äàâ íî ìè â³äêðè ëè íî âèé êîí ñåð âà - òèâ íèé á³ëêî âûé êîì ïëåêñ – SEA-êîì ïëåêñ, ÿêî ìó ïðè òà ìàíí³ ñòðóê òóðí³ õà ðàê òå ðèñ òè êè, ñõîæ³ ç òà êè ìè ìåì áðàí òðàíñ - ïîð òíûõ âå çè êóë (COPII) òà ¿õí³õ äî ïîì³æíèõ ïàð òíåð³â (HOPS/ CORVET) ³ ÿäåð íî¿ ïîðè (NPC). Äð³æäæî âèé SEA-êîì ïëåêñ äè - íàì³÷íî âçàºìî䳺 ç âà êó î ëÿ ìè. Äàí³ ùîäî ôóíêö³¿ SEA-êîì ïëåê ñó º äî âîë³ ìà ëî ÷è ñåëü íè ìè.  ïðåä ñòàâ ëå íî ìó ì³í³îãëÿä³ îá ãî âî ðþ- ºòüñÿ ìîæ ëè âà ôóíêö³ÿ SEA-êîì ïëåê ñó ç óðà õó âàí íÿì ðå çóëü òà- ò³â ãå íå òè÷ íèõ ³ ôóíêö³îíàëü íèõ äîñë³äæåíü, ïðî âå äå íèõ íà äð³æä- æàõ òà ³íøèõ åó êàð³îòàõ. Êëþ ÷îâ³ ñëî âà: äð³æäæ³ Saccharomyces cerevisiae, SEA-êîìï- ëåêñ, âà êó îë³. 283 THE SEA COMPLEX – THE BEGINNING ALGRET R., DOKUDOVSKAYA S. S. Ð. Àëãðå, Ñ. Ñ. Äî êó äîâ ñêàÿ SEA-êîì ïëåêñ – íà ÷à ëî Ðå çþ ìå Íà ëè ÷èå ðàç íî îá ðàç íûõ âíóò ðèê ëå òî÷ íûõ ìåì áðàí íûõ îðãà íåëë, äè íà ìè ÷åñ êè ñâÿ çàí íûõ ïî ñðå äñòâîì ñå ëåê òèâ íî ãî òðàíñ ïîð òà, ÿâ ëÿ åò ñÿ îò ëè ÷è òåëü íîé îñî áåí íîñ òüþ ýó êà ðè î òè ÷åñ êîé êëåò - êè. Ìíî æåñ òâî áåë êîâ, íå îá õî äè ìûõ äëÿ îá ðà çî âà íèÿ è ñó ùåñò- âî âà íèÿ ýòèõ îðãà íåëë, èìå þò ñõîä íóþ ýâî ëþ öè îí íóþ èñ òî ðèþ. Íå äàâ íî ìû îò êðû ëè íî âûé êîí ñåð âà òèâ íûé áåë êî âûé êîì ïëåêñ – SEA-êîì ïëåêñ, îá ëà äà þ ùèé ñòðóê òóð íû ìè õà ðàê òå ðèñ òè êà ìè, ñõî æè ìè ñ òà êîâû ìè ìåì áðàí òðàíñ ïîð òíûõ âå çè êóë (COPII), à òàê æå èõ âñïî ìî ãà òåëü íûõ ïàð òíå ðîâ (HOPS/CORVET) è ÿäåð - íîé ïîðû (NPC). Äðîæ æå âîé SEA-êîì ïëåêñ äè íà ìè ÷åñ êè âçà è ìî - äå éñòâó åò ñ âà êó î ëÿ ìè. Äàí íûå î ôóíê öèè SEA-êîì ïëåê ñà î÷åíü ìà ëî ÷èñ ëåí íû.  ïðåä ñòàâ ëåí íîì ìè íè îá çî ðå îá ñóæ äà åò ñÿ âîç - ìîæíàÿ ôóíê öèÿ SEA-êîì ïëåê ñà, îñíî âû âà ÿñü íà ðå çóëü òà òàõ ãå- íåòè ÷åñ êèõ è ôóíê öè î íàëü íûõ èñ ñëå äî âà íèé, ïðî âå äåí íûõ íà äðîæ- æàõ è äðó ãèõ ýó êà ðè î òàõ. Êëþ ÷å âûå ñëî âà: äðîæ æè Saccharomyces cerevisiae, SEA-êîìï- ëåêñ, âà êó î ëè. REFERENCES 1. Dokudovskaya S., Waharte F., Schlessinger A., Pieper U., De- vos D. P., Cristea I. M., Williams R., Salamero J., Chait B. T., Sa- li A., Field M. C., Rout M. P., Dargemont C. 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