C2
Function and Life History

Memory mechanisms of undernutrition in the gut ecosystem

Protein-energy malnutrition (PEM) is a serious global health problem that leads to high mortality rates due to concomitant morbidities such as infections and multiple organ failure. Although we know that the gut microbiome plays an important role in the etiology of PEM, little is known about its role in long-term consequences. To close this significant knowledge gap, we aim to use the strengths of two experimental systems, mouse (C2.2, PI Rosenstiel) and fly (C2.1, PI Roeder), in a complementary manner to obtain a mechanistic understanding of the processes underlying the long-lasting consequences of PEM on different body functions.

To achieve this, we will exploit the experimental advantages of the mouse model to construct an epigenetic/transcriptomic cell atlas of molecular sequelae of malnutrition, comprising all organs of interest. This atlas will generate hypotheses for functional experiments on the role of long-term epigenetic imprints and serve as a valuable resource to the scientific community, extending beyond this project.

In parallel, we will use the Drosophila model to elucidate the role of G protein-coupled receptors (GPCRs) as sensors of nutrients and microbial products, using comprehensive screening approaches, including in vivo Tango-Trace assays. Additionally, the role of the gut as a central hub for communication between the intestinal ecosystem and the host will be examined. To decipher this crucial step of the systemic PEM effect, we will identify the proteins secreted by the intestines in response to PEM.

In both model systems, we aim to understand the molecular basis of sustained infection susceptibility following PEM episodes, including the contribution of the microbiota. Finally, microbiota-directed interventional strategies that may counteract the long-term effects of a PEM episode on infection susceptibility will be developed and tested.

The C2 project will centrally contribute to an improved understanding of the long-lasting and adverse health effects of PEM, while also opening new avenues for targeting these pathological conditions.

C2
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C2
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2023
A2
C2
Z3

A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression

Knop M, Treitz C, Bettendorf S, Bossen J, von Frieling J, Doms S, Bruchhaus I, Kuehnlein RP, Baines JF, Tholey A, Roeder T (2023) A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression. bioRxiv, doi: https://doi.org/10.1101/2023.06.02.543385

2023
C2

Hemocytes and fat body cells, the only professional immune cell types in Drosophila, show strikingly different responses to systemic infections.

 Vaibhvi V, Kuenzel S, Roeder T (2022) Hemocytes and fat body cells, the only professional immune cell types in Drosophila, show strikingly different responses to systemic infections. Frontiers Immunology 13, 1040510, doi: 10.3389/fimmu.2022.1040510.

 

2023
A1
C2

Recurrent phases of strict protein limitation inhibit tumor growth and restore lifespan in a Drosophila intestinal cancer model.

Pfefferkorn RM, Mortzfeld BM, Fink C, von Frieling JBossen J, Esser D, Kaleta CRosenstiel P, Heine H, Roeder T (2023) Recurrent phases of strict protein limitation inhibit tumor growth and restore lifespan in a Drosophila intestinal cancer model. Aging&Disease in press.

2023
C2

The tracheal immune system of insects – a blueprint for understanding epithelial immunity.

Bossen J, Kühle, J-P, Roeder T (2023) The tracheal immune system of insects – a blueprint for understanding epithelial immunity. Insect Biochem Mol Biol 157, 103960. https://doi.org/10.1016/j.ibmb.2023.103960

2023
A2
A4
C1
C2

The microbiome of the marine flatworm Macrostomum lignano provides fitness advantages and exhibits circadian rhythmicity

Ma YHe JSieber Mvon Frieling J, Bruchhaus I, Baines JF, Bickmeyer U, Roeder T (2023) The microbiome of the marine flatworm Macrostomum lignano provides fitness advantages and exhibits circadian rhythmicity. Communications Biology 6: 289. https://doi.org/10.1038/s42003-023-04671-y.

2023
A2
C2
Z3

A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression

Knop M, Treitz C, Bettendorf S, Bossen J, von Frieling J, Doms S, Bruchhaus I, Kuehnlein RP, Baines JF, Tholey ARoeder T (2023) A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression. bioRxiv, doi: https://doi.org/10.1101/2023.06.02.543385

2022
C2

An aqueous extract of the brown alga Eisenia bicyclis extends lifespan in a sex-specific manner by interfering with the Tor-FoxO axis.

Tahanzadeh NKnop M, Seidler Y, Dirndorfer S, Lürsen K, Bruchhaus I, Lang R, Rimbach G, Roeder T (2022) An aqueous extract of the brown alga Eisenia bicyclis extends lifespan in a sex-specific manner by interfering with the Tor-FoxO axis. Aging 14, doi.org/10.18632/aging.204218.

 

2022
A2
C2

DNA methyltransferase 3A controls intestinal epithelial barrier function and regeneration in the colon

Fazio A, Bordoni D, Kuiper JWP, Franke A, Rosenstiel P. et al. DNA methyltransferase 3A controls intestinal epithelial barrier function and regeneration in the colon. Nat Commun 13, 6266 (2022). https://doi.org/10.1038/s41467-022-33844-2

 

2021
A1
C2
Z2

Microbial regulation of hexokinase 2 links mitochondrial metabolism and cell death in colitis.

Hinrichsen F, Hamm J, Westermann M, Schröder L, Shima K, Mishra N, Walker A, Sommer N, Klischies K, Prasse D, Zimmermann J, Kaiser S, Bordoni D, Fazio A, Marinos G, Laue G, Imm S, Tremaroli V, Basic M, Häsler R, Schmitz RA, Krautwald S, Wolf A, Stecher B, Schmitt-Kopplin P, Kaleta C, Rupp J, Bäckhed F, Rosenstiel P, Sommer F (2021) Cell Metab 33(12):2355-2366.e8. doi: 1016/j.cmet.2021.11.004

2021
C2

Low-protein diet applied as part of combination therapy or standalone normalizes lifespan and tumor proliferation in a model of intestinal cancer

Proske A, Bossen J,  von Frieling J, Roeder T (2021) Aging (Albany NY). 13(21):24017-24036. doi: 10.18632/aging.203692.

2021
C2

Constitutive immune activity promotes JNK- and FoxO-dependent remodeling of Drosophila airways.

Wagner C, Uliczka K, Bossen J, Niu X, Fink C, Thiedmann M, Knop M, Vock C, Abdelsadik A, Zissler UM, Isermann K, Garn H, Pieper M, Wegmann M, Koczulla AR, Vogelmeier CF, Schmidt-Weber CB, Fehrenbach H, König P, Silverman N, Renz H, Pfefferle P, Heine H, Roeder T (2021) Cell Reports 35(1): 108956, doi: 10.1016/j.celrep.2021.108956.

2020
C2

Nutritional targeting of the microbiome as potential 3 therapy for malnutrition and chronic inflammation

Schröder L , Kaiser S , Flemer B , Hamm J , Hinrichsen F , Bordoni D , Rosenstiel P , Sommer F (2020) Nutrients. 12(10):E3032. doi: 10.3390/nu12103032.

2020
C2

A high-fat diet induces a microbiota-dependent increase in stem cell activity in the Drosophila intestine.

von Frieling J, Faisal MN, Sporn F, Pfefferkorn R, Nolte SS, Sommer F, Rosenstiel P, Roeder T (2020) PLoS Genet. 16(5):e1008789. doi: 10.1371/journal.pgen.1008789

2020
C2

Furbellow (brown algae) extract increases lifespan Drosophila by interfering with TOR-signalling.

Li Y, Romey-Glüsing R, Tahan Zadeh T, von Frieling J, Hoffmann J, Huebbe P, Bruchhaus I, Rimbach G, Fink C, Roeder T (2020) Nutrients. 12:1172, doi:10.3390/nu12041172

2020
A2
C2
Z3

NOD2 influences trajectories of intestinal microbiota recovery after antibiotic perturbation

Moltzau Anderson J, Lipinski S, Sommer F, Pan W-H, Boulard O, Rehman A, Falk-Paulsen M, Stengel ST, Aden K, Häsler R, Bharti R, Künzel S, Baines JF, Chamaillard M, Rosenstiel P (2020) Cell Mol Gastroenterol Hepatol. 10(2): 365-389. doi: 10.1016/j.jcmgh.2020.03.008

2020
C2

FAMIN Is a Multifunctional Purine Enzyme Enabling the Purine Nucleotide Cycle.

Cader MZ, de Almeida Rodrigues RP, West JA, Sewell GW, Md-Ibrahim MN, Reikine S, Sirago G, Unger LW, Iglesias-Romero AB, Ramshorn K, Haag LM, Saveljeva S, Ebel JF, Rosenstiel P, Kaneider NC, Lee JC, Lawley TD, Bradley A, Dougan G, Modis Y, Griffin JL, Kaser A (2020) Cell. 180(2):278-295.e23. doi:10.1016/j.cell.2019.12.017

2020
C2

Adrenergic signaling in muscularis macrophages limits infection-induced neuronal loss.

Matheis F, Muller PA, Graves CL, Gabanyi I, Kerner ZJ, Costa-Borges D, Ahrends T, Rosenstiel P, Mucida D (2020) Cell. 180(1): 64-78.e16. doi:10.1016/j.cell.2019.12.002

2020
C2

Autophagy of intestinal epithelial cells inhibits colorectal carcinogenesis induced by colibactin-producing Escherichia coli in Apc(Min/+) mice.

Lucas C, Salesse L, Thi Hoang MH, Bonnet M, Sauvanet P, Larabi A, Godfraind C, Gagnière J, Pezet D, Rosenstiel P, Barnich N, Bonnet R, Dalmasso G, Nguyen HTT (2020) Gastroenterology. 158(5): 1373-1388. doi:10.1053/j.gastro.2019.12.026

2020
C2

Factors that affect the translation of dietary restriction into a longer life

von Frieling J, Roeder T (2020) IUBMB Life. 72: 814–824. doi: 10.1002/iub.2224

2019
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B2
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INF

Advancing our functional understanding of host–microbiota interactions: a need for new types of studies

He J, Lange J, Marinos G, Bathia J, Harris D, Soluch R, Vaibhvi V, Deines P, Hassani MA, Wagner K-S, Zapien‐Campos R, Jaspers C, Sommer F (2019) BioEssays, 1900211 (1-5). doi: 10.1002/bies.201900211

 

2019
C2

Dietary tryptophan links encephalogenicity of autoreactive T cells with gut microbial ecology

Sonner JK*, Keil M*, Falk-Paulsen M*, Mishra N, Rehman A, Kramer M, Deumelandt K, Röwe J, Sanghvi K, Wolf L, von Landenberg A, Wolff H, Bharti R, Oezen I, Lanz TV, Wanke F, Tang Y, Brandao I, Mohapatra SR, Epping L, Grill A, Röth R, Niesler B, Meuth SG, Opitz CA, Okun JG, Reinhardt C, Kurschus FC, Wick W, Bode HB, Rosenstiel P*, Platten M* (2019) Nat Commun. 10(1):4877. doi: 10.1038/s41467-019-12776-4. *shared first or last authorship

2019
C2

The microbiota promotes arterial thrombosis in low-density lipoprotein receptor-deficient mice

Kiouptsi K#, Jäckel S#, Pontarollo G#, Grill A, Kuijpers MJE, Wilms E, Weber C, Sommer F, Nagy M, Neideck C, Jansen Y, Ascher S, Formes H, Karwot C, Bayer F, Kollar B, Subramaniam S, Molitor M, Wenzel P, Rosenstiel P, Todorov H, Gerber S, Walter U, Jurk K, Heemskerk JWM, van der Vorst EPC#, Döring Y#, Reinhardt C (2019) mBio. 10(5). doi: 10.1128/mBio.02298-19. # Contributed equally

2019
A1
C2

Prdx4 limits caspase-1 activation and restricts inflammasome-mediated signaling by extracellular vesicles

Lipinski S, Pfeuffer S, Arnold P, Treitz C, Aden K, Ebsen H, Falk-Paulsen M, Gisch N, Fazio A, Kuiper J, Luzius A, Billmann-Born S, Schreiber S, Nuñez G, Beer HD, Strowig T, Lamkanfi M, Tholey A, Rosenstiel P (2019) EMBO J. 38(20) doi: 10.15252/embj.2018101266.

2019
A4
B1
C2

A phage protein aids bacterial symbionts in eukaryote immune evasion

Jahn MT, Arkhipova K, Markert SM, Stigloher C, Lachnit T, Pita L, Kupczok A, Ribes M, Stengel ST, Rosenstiel P, Dutilh BE, Hentschel U (2019) Cell Host & Microbe, doi: 10.1016/j.chom.2019.08.019

2019
A1
A2
A3
B1
B2
C1
C2
INF
Z3

Comparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms

Rausch P, Rühlemann M, Hermes BM, Doms S, Dagan T, Dierking K, Domin H, Fraune S, von Frieling J, Hentschel U, Heinsen F-A, Höppner M, Jahn MT, Jaspers C, Kissoyan KAB, Langfeldt D, Rehman A, Reusch TBH, Roeder T, Schmitz RA, Schulenburg H, Soluch R, Sommer F, Stukenbrock E, Weiland-Bräuer N, Rosenstiel P, Franke A, Bosch T, Baines JF (2019) Microbiome, doi: 10.1186/s40168-019-0743-1

2019
A4
B1
C1
C2

Temperature and insulin signaling regulate body size in Hydra by the Wnt and TGF-beta pathways

Mortzfeld BM*, Taubenheim J*, Klimovich AV, Fraune S, Rosenstiel P, Bosch TCG (2019) Nature Communications 10, 3257. doi: 10.1038/s41467-019-11136-6

2019
C2

Drosophila melanogaster in nutrition research—the importance of standardizing experimental diets

Lüersen K, Roeder T, Rimbach G (2019) Genes Nutr. 14: 3. doi: 10.1186/s12263-019-0627-9

2019
C2

Epithelial endoplasmic reticulum stress orchestrates a protective IgA response

Grootjans J*, Krupka N*, Hosomi S*, Matute JD, Hanley T, Saveljeva S, Gensollen T, Heijmans J, Li H, Limenitakis JP, Ganal-Vonarburg SC, Suo S, Luoma AM, Shimodaira Y, Duan J, Shih DQ, Conner ME, Glickman JN, Fuhler GM, Palm NW, de Zoete MR, van der Woude CJ, Yuan G-C, Wucherpfennig KW, Targan SR, Rosenstiel P, Flavell RA, McCoy KD, Macpherson AJ, Kaser A, Blumberg, RS (2019) Science. 363(6430): 993–998. doi: 10.1126/science.aat7186

2018
A2
B2
C1
C2
INF
Z2

Functions of the Microbiota for the Physiology of Animal Metaorganisms

Esser D, · Lange J, · Marinos G, · Sieber M, Best L, Prasse D, Bathia J, Rühlemann MC, Boersch K, Jaspers C, Sommer F (2018) J Innate Immun DOI: 10.1159/000495115

2018
C2
Z3

ATG16L1 orchestrates interleukin-22 signaling in the intestinal epithelium via cGAS-STING.

Aden K, Tran F, Ito G, Sheibani-Tezerji R, Lipinski S, Kuiper JW, Tschurtschenthaler M, Saveljeva S, Bhattacharyya J, Häsler R, Bartsch K, Luzius A, Jentzsch M, Falk-Paulsen M, Stengel ST, Welz L, Schwarzer R, Rabe B, Barchet W, Krautwald S, Hartmann G, Pasparakis M, Blumberg RS, Schreiber S, Kaser A, Rosenstiel P (2018); Gastroenterology. pii: jem.20171029. doi: 10.1084/jem.20171029

2018
A2
C2

Exposure to the gut microbiota drives distinct methylome and transcriptome changes in intestinal epithelial cells during postnatal development

Franke A, Schultze JL, Bäckhed F, Rosenstiel P (2018) Genome Med. 10(1):27. doi: 10.1186/s13073-018-0534-5.
2018
C2

Impaired Wnt signaling in dopamine containing neurons is associated with pathogenesis in a rotenone triggered Drosophila Parkinson’s disease model.

Stephano F, Nolte S, Hoffmann J, El-Kholy S, von Frieling J, Bruchhaus I, Fink C, Roeder T (2018); Sci Rep. 8(1):2372. doi: 10.1038/s41598-018-20836-w

2018
C2
Z3

A Drosophila model of cigarette smoke induced COPD identifies Nrf2 signaling as an expedient target for intervention.

Prange R, Thiedmann M, Bhandari A, Mishra N, Sinha A, Häsler R, Rosenstiel P, Uliczka K, Wagner C, Yildirim AÖ, Fink C, Roeder T (2018); Aging (Albany NY). 10(8):2122-2135. doi: 10.18632/aging.101536

2018
A4
C1
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Z1
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Grow With the Challenge – Microbial Effects on Epithelial Proliferation, Carcinogenesis, and Cancer Therapy

Von Frieling J, Fink C, Hamm J, Klischies K, Forster M, Thomas C. G. Bosch TCG, Roeder T, P Rosenstiel P, Sommer F (2018); Front. Microbiol. doi: 10.3389/fmicb.2018.02020

2018
C2
Z3

Neonatal selection by Toll-like receptor 5 influences long-term gut microbiota composition.

Fulde M, Sommer F, Chassaing B, van Vorst K, Dupont A, Hensel M, Basic M, Klopfleisch R, Rosenstiel P, Bleich A, Bäckhed F, Gewirtz AT, Hornef MW (2018); Nature 560(7719):489-493. doi: 10.1038/s41586-018-0507-2

2018
A2
C2
INF
Z3

Exposure to the gut microbiota drives distinct methylome and transcriptome changes in intestinal epithelial cells during postnatal development.

Pan WH, Sommer F, Falk-Paulsen M, Ulas T, Best P, Fazio A, Kachroo P, Luzius A, Jentzsch M, Rehman A, Müller F, Lengauer T, Walter J, Künzel S, Baines JF, Schreiber S, Franke A, Schultze JL, Bäckhed F, Rosenstiel P (2018); Genome Med. 10(1):27. doi: 10.1186/s13073-018-0534-5

2018
A2
C2
INF
Z3

The antibiotic resistome and microbiota landscape of refugees from Syria, Iraq and Afghanistan in Germany.

Häsler R, Kautz C, Rehman A, Podschun R, Gassling V, Brzoska P, Sherlock J, Gräsner J T, Hoppenstedt G, Schubert S, Ferlinz A, Lieb W, Laudes M, Heinsen F A, Scholz J, Harmsen D, Franke A, Eisend S, Kunze T, Fickenscher H, Ott S, Rosenstiel P, Schreiber S (2018); Microbiome., 6(1):37. doi: 10.1186/s40168-018-0414-7

2018
C2

Nutritional regimens with periodically recurring phases of dietary restriction extend lifespan in Drosophila.

Romey-Glüsing R, Li Y, Hoffmann J, von Frieling J, Knop M, Pfefferkorn R, Bruchhaus I, Fink C, Roeder T (2018); FASEB J., 5:fj201700934R. doi: 10.1096/fj.201700934R

2017
C2

Drosophila Fecal Sampling.

Christine Fink, Jakob von Frieling, Mirjam Knop, Thomas Roeder (2017); Bio-protocols, 7(18):e2547. doi: 10.21769/BioProtoc.2547

2017
C2

The Role of Monoaminergic Neurotransmission for Metabolic Control in the Fruit Fly Drosophila Melanogaster.

Li Y, Tiedemann L, von Frieling J, Nolte S, El-Kholy S, Stephano F, Gelhaus C, Bruchhaus I, Fink C, Roeder T (2017); Front. Syst. Neurosci., 11:60. doi: 10.3389/fnsys.2017.00060

2017
C2
Z3

The resilience of the intestinal microbiota influences health and disease.

Sommer F, Anderson J M, Bharti R, Raes J, Rosenstiel P (2017); Nat Rev Microbiol., doi: 10.1038/nrmicro.2017.58

2017
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Efficacy of Sterile Fecal Filtrate Transfer for Treating Patients With Clostridium difficile Infection. Gastroenterology.

Ott S J, Waetzig G H, Rehman A, Moltzau-Anderson J, Bharti R, Grasis J A, Cassidy L, Tholey A, Fickenscher H, Seegert D, Rosenstiel P, Schreiber S (2017); Gastroenterology, 152(4):799-811.e7. doi: 10.1053/j.gastro.2016.11.010

2016
C2

Octopamine controls starvation resistance, life span and metabolic traits in Drosophila.

Li Y, Hoffmann J, Li Y, Stephano F, Bruchhaus I, Fink C, Roeder T (2016); Sci Rep., 6:35359. doi: 10.1038/srep35359

2016
C2
Z3

Enterococcus hirae and Barnesiella intestinihominis Facilitate Cyclophosphamide-Induced Therapeutic Immunomodulatory Effects.

Daillère R, Vétizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, Duong C P, Flament C, Lepage P, Roberti M P, Routy B, Jacquelot N, Apetoh L, Becharef S, Rusakiewicz S, Langella P, Sokol H, Kroemer G, Enot D10, Roux A, Eggermont A, Tartour E, Johannes L, Woerther P L, Chachaty E, Soria J C, Golden E, Formenti S, Plebanski M, Madondo M, Rosenstiel P, Raoult D, Cattoir V, Boneca I G, Chamaillard M, Zitvogel L (2016); Immunity., 45(4):931-943. doi: 10.1016/j.immuni.2016.09.009

2016
A2
C2
INF
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Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota.

Wang J, Thingholm L B, Skiecevičienė J, Rausch P, Kummen M, Hov J R, Degenhardt F, Heinsen F A, Rühlemann M C, Szymczak S, Holm K, Esko T, Sun J, Pricop-Jeckstadt M, Al-Dury S, Bohov P, Bethune J, Sommer F, Ellinghaus D, Berge R K, Hübenthal M, Koch M, Schwarz K, Rimbach G, Hübbe P, Pan W H, Sheibani-Tezerji R, Häsler R, Rosenstiel P, D’Amato M, Cloppenborg-Schmidt K, Künzel S, Laudes M, Marschall H U, Lieb W, Nöthlings U, Karlsen T H, Baines J F, Franke A (2016); Nat Genet., 48(11):1396-1406. doi: 10.1038/ng.3695

2016
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Epithelial IL-23R Signaling Licenses Protective IL-22 Responses in Intestinal Inflammation.

Aden K, Rehman A, Falk-Paulsen M, Secher T, Kuiper J, Tran F, Pfeuffer S, Sheibani-Tezerji R, Breuer A, Luzius A, Jentzsch M, Häsler R, Billmann-Born S, Will O, Lipinski S, Bharti R, Adolph T, Iovanna J L, Kempster S L, Blumberg R S, Schreiber S, Becher B, Chamaillard M, Kaser A, Rosenstiel P (2016); Cell Rep., 16(8):2208-18. doi: 10.1016/j.celrep.2016.07.054

2016
C2

Intestinal FoxO signaling is required to survive oral infection in Drosophila.

Fink C, Hoffmann J, Knop M, Li Y, Isermann K, Roeder T (2016); Mucosal Immunol., 9:927-936. doi: 10.1038/mi.2015.112

2016
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The native microbiome of the nematode Caenorhabditis elegans: Gateway to a new host-microbiome model.

Dirksen P, Marsh SA, Braker I, Heitland N, Wagner S, Nakad R, Mader S, Petersen C, Kowallik V, Rosenstiel P C, Felix M A, Schulenburg H (2016); BMC Biology, 14:38. doi:10.1186/s12915-016-0258-1

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