Publications – Michelle Heck

Affinity Purification-Mass Spectrometry Identifies a Novel Interaction between a Polerovirus and a Conserved Innate Immunity Aphid Protein that Regulates Transmission Efficiency
2021.
DeBlasio, S.L., Wilson, J.R., Tamborindeguy, C., Johnson, R.S., Pinheiro, P.V., MacCoss, M.J., Gray, S.M., Heck, Michelle L.
J Proteome Res..
20
:
3365–3387
Proteomic Polyphenism in Color Morphotypes of Diaphorina citri, Insect Vector of Citrus Greening Disease
2021.
Hosseinzadeh, S., Higgins, S.A., Ramsey, J., Howe, K., Griggs, M., Castrillo, L., Heck, Michelle L.
J Proteome Res..
20
:
2851–2866
Bacterial Vector-Borne Plant Diseases: Unanswered Questions and Future Directions
2020.
Huang, W., Reyes-Caldas, P., Mann, M., Seifbarghi, S., Kahn, A., Almeida, R.P.P., Béven, L., Heck, Michelle L., Hogenhout, S.A., Coaker, G.
Mol Plant..
13
:
1379–1393
Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts
2020.
Coates, L.C., Mahoney, J., Ramsey, J.S., Warwick, E., Johnson, R., MacCoss, M.J., Krasnoff, S.B., Howe, K.J., Moulton, K., Saha, S., Mueller, Lukas A., Hall, D.G., Shatters, R.G., Heck, Michelle L., Slupsky, C.M.
PloS One.
15
:
Proteomics in non-model organisms: a new analytical frontier.
2020.
Heck, Michelle L., Neely B.A.
J Proteome Res..
:
RNA aptamer capture of macromolecular complexes for mass spectrometry analysis
2020.
Ray, J., Kruse, A., Ozer, A., Kajitani, T., Johnson, R., MacCoss, M., Heck, Michelle L., Lis, J.T.
Nucleic Acids Res..
:
Longitudinal transcriptomic, proteomic, and metabolomic analysis of Citrus limon response to graft inoculation by ‘Candidatus Liberibacter asiaticus‘.
2020.
Ramsey, J.S., Chin, E.L., Chavez, J.D., Saha, S., Mischuk, D., Mahoney, J., Mohr, J., Robison, F.M., Mitrovic, E., Xu, Y., Strickler, S.R., Fernandez, N., Zhong, X., Polek, M., Godfrey, K.E., Giovannoni, James J., Mueller, Lukas A., Slupsky, C.M., Bruce, J.E., Heck, Michelle L.
J Proteome Res.
:
Peptidomics approaches for the identification of bioactive molecules from Diaphorina citri
2020.
Fleites, L.A., Johnson, R., Kruse, A.R., Nachman, R.J., Hall, D.G., MacCoss, M.J., Heck, Michelle L.
J Proteome Res..
:
Siderophores from the Entomopathogenic Fungus Beauveria bassiana
2020.
Krasnoff, S.B., Howe, K.J., Heck, Michelle L., Donzelli, B.G.G.
J. Nat. Prod..
83
:
296–304
Longitudinal transcriptomic, proteomic, and metabolomic analyses of Citrus sinensis (L.) Osbeck graft-inoculated with ‘Candidatus Liberibacter asiaticus’.
2019.
Chin, E.L., Ramsey, J.S., Mishchuk, D.O., Saha, S., Foster, E., Chavez, J.D., Howe, K., Zhong, X., Polek, M., Godfrey, K.E., Mueller, Lukas A., Bruce, J.E., Heck, Michelle L., Slupsky, C.M.
J Proteome Res..
:
A polerovirus, Potato Leafroll virus, alters plant-vector interactions using three viral proteins
2019.
Patton, M.F., Bak, A., Sayre, J., Heck, Michelle L., Casteel C.L.
Plant Cell Environ..
:
Assessing protein sequence database suitability using de novo sequencing.
2019.
Johnson, R., Searle, B.C., Nunn, B.L., Gilmore, J.M., Phillips, M., Amemiya, C.T., Heck, Michelle L., MacCoss, M.J.
Mol Cell Proteomics..
19
:
198–208
Lessons from One Fastidious Bacterium to Another: What Can We Learn about Liberibacter Species from Xylella fastidiosa
2019.
Kruse, A., Fleites, L.A., Heck, Michelle L.
Insects.
10
:
E300
Distribution and Variation of Bacterial Endosymbiont and “Candidatus Liberibacter asiaticus” Titer in the Huanglongbing Insect Vector, Diaphorina citri Kuwayama.
2019.
Hosseinzadeh, S, Shams-Bakhsh, M, Mann, M, Fattah-Hosseini, S, Bagheri, A, Mehrabadi, M, Heck, Michelle L.
Microb Ecol.
78
:
206
The Identity of a Single Residue of the RNA-Dependent RNA Polymerase of Grapevine Fanleaf Virus Modulates Vein Clearing in Nicotiana benthamiana
2019.
Osterbaan, L.J., Choi, J., Kenney, J., Flasco, M., Vigne, E., Schmitt-Keichinger, C., Rebelo, A.R., Heck, Michelle L., Fuchs, M.
Molecular Plant-Microbe Interactions.
32
:
790–801
Looking Through the Lens of ‘Omics Technologies: Insights Into the Transmission of Insect Vector-borne Plant Viruses
2019.
Wilson, J.R., DeBlasio, S.L., Alexander, M.M., Heck, Michelle L.
Current Issues in Molecular Biology.
34
:
113–144
Plant Viruses Transmitted in Two Different Modes Produce Differing Effects on Small RNA-Mediated Processes in Their Aphid Vector
2019.
Pinheiro, P.V., Wilson, J.R., Xu, Y., Zheng, Y., Rebelo, A.R., Fattah-Hosseini, S., Kruse, A., Santos Dos Silva, R., Xu, Y., Kramer, M., Giovannoni, James, Fei, Zhangjun, Gray, S., Heck, Michelle L.
Phytobiomes.
3
:
71–81
Color morphology of Diaphorina citri influences interactions with its bacterial endosymbionts and ‘Candidatus Liberibacter asiaticus’
2019.
Hosseinzadeh, S, Ramsey, J, Mann, M, Bennett, L, Hunter, WB, Shams-Bakhsh, M, Hall, DG, Heck, Michelle L.
PLOS One.
14
:
e0216599
Candidatus Liberibacter asiaticus Minimally Alters Expression of Immunity and Metabolism Proteins in Hemolymph of Diaphorina citri, the Insect Vector of Huanglongbing
2018.
Kruse, A., Ramsey, J.S., Johnson, R., Hall, D.G., MacCoss, M.J., Heck, Michelle L.
Journal of Proteome Research.
17
:
2995–3011
Targeted disruption of aphid transmission: a vision for the management of crop diseases caused by Luteoviridae members
2018.
Heck, Michelle L., Brault, V.
Current Opinion in Virology.
33
:
24–32
Distribution and Variation of Bacterial Endosymbiont and “Candidatus Liberibacter asiaticus” Titer in the Huanglongbing Insect Vector, Diaphorina citri Kuwayama
2018.
Hosseinzadeh, S, Shams-Bakhsh, M, Mann, M, Fattah-Hosseini, S, Bagheri, A, Mehrabadi, M, Heck, Michelle L.
Microb Ecol.
:
The Interaction Dynamics of Two Potato Leafroll Virus Movement Proteins Affects Their Localization to the Outer Membranes of Mitochondria and Plastids
2018.
DeBlasio, S.G., Xu, Y., Johnson, R.S., Rebelo, A.R., MacCoss, M.J., Gray, S.M., and Heck, Michelle L.
Viruses.
10
:
585
Disruption of chloroplast function through downregulation of phytoene desaturase enhances the systemic accumulation of an aphid-borne, phloem-restricted virus
2018.
DeBlasio, S. L., Rebelo, A. R., Parks, K., Gray, S., Heck, Michelle L.
Molecular Plant-Microbe Interactions.
:
Insect Transmission of Plant Pathogens: a Systems Biology Perspective
2018.
Heck, Michelle L.
mSystems.
3
:
e00168-17–e00168-17
The quest for a non-vector psyllid: Natural variation in acquisition and transmission of the huanglongbing pathogen ‘Candidatus Liberibacter asiaticus’ by Asian citrus psyllid isofemale lines
2018.
Ammar, E. D., Hall, D. G., Hosseinzadeh, S., Heck, Michelle L.
PLOS One.
13
:
e0195804–e0195804
A Stem-Loop Structure in Potato Leafroll Virus Open Reading Frame 5 (ORF5) Is Essential for Readthrough Translation of the Coat Protein ORF Stop Codon 700 Bases Upstream
2018.
Xu, Y., Ju, H. J., DeBlasio, S., Carino, E. J., Johnson, R., MacCoss, M., Heck, Michelle L., Miller, W. A., Gray, Stewart
Journal of Virology.
92
:
Diaphorina citri Nymphs Are Resistant to Morphological Changes Induced by “Candidatus Liberibacter asiaticus” in Midgut Epithelial Cells
2018.
Mann, M., Fattah-Hosseini, S., Ammar, E. D., Stange, R., Warrick, E., Sturgeon, K., Shatters, R., Heck, Michelle L.
Infection and Immunity.
86
:
Potato leafroll virus alters small RNA production in its aphid vector during plant viral infection to promote virus dispersal
2017.
Wilson, J., Pinheiro, P., Xu, Y., Zheng, Y., Rebelo, A. R., Fattahalhosseini, S., Kruse, A., Dos Silva, R. S., Xu, Y., Giovannoni, J., Fei, Zhangjun, Gray, S., Heck, Michelle L.
PHYTOPATHOLOGY.
107
:
206–207
Improved annotation of the insect vector of citrus greening disease: biocuration by a diverse genomics community
2017.
Saha, S., Hosmani, P. S., Villalobos-Ayala, K., Miller, S., Shippy, T., Flores, M., Rosendale, A., Cordola, C., Bell, T., Mann, H., DeAvila, G., DeAvila, D., Moore, Z., Buller, K., Ciolkevich, K., Nandyal, S., Mahoney, R., Van Voorhis, J., Dunlevy, M., Farrow, D., Hunter, D., Morgan, T., Shore, K., Guzman, V., Izsak, A., Dixon, D. E., Cridge, A., Cano, L., Cao, X., Jiang, H., Leng, N., Johnson, S., Cantarel, B. L., Richards, S., English, A., Shatters, R. G., Childers, C., Chen, M. J., Hunter, W., Heck, Michelle L., Mueller, Lukas A., Munoz-Torres, M., Nelson, D., Poelchau, M. F., Benoit, J. B., Wiersma-Koch, H., D'Elia, T., Brown, S. J.
Database : the journal of biological databases and curation.
2017
:
Host protein interaction network associated with the non- incorporated form of the potato leafroll virus RTP identified using mass spectrometry
2017.
Deblasio, S. L., Rebelo, A. R., Johnson, R., Gray, S., MacCoss, M., Heck, Michelle L.
PHYTOPATHOLOGY.
107
:
24–24
Leveraging ‘omics technologies to develop new initiatives for controlling vector-borne plant pathogens
2017.
Deblasio, S., Heck, Michelle L.
PHYTOPATHOLOGY.
107
:
6–6
Comparative proteomics to identify critical proteins for transmission of Candidatus Liberibacter asiacticus by the Asian citrus psyllid
2017.
Kruse, A., Saha, S., Johnson, R., Fattahalhosseini, S., Warwick, E., Sturgeon, K., MacCoss, M., Shatters, R., Heck, Michelle L.
PHYTOPATHOLOGY.
107
:
9–9
Combining ‘omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut
2017.
Kruse, A., Fattah-Hosseini, S., Saha, S., Johnson, R., Warwick, E. R., Sturgeon, K., Mueller, Lukas A., Maccoss, M. J., Shatters, R. G., Heck, Michelle L.
PLOS One.
12
:
e0179531–e0179531
Structural biology of viruses in the luteoviridae
2017.
Alexander, M., Mohr, J., Chavez, J., DeBlasio, S., Ziegler-Graff, V., Brault, V., Bruce, J., Heck, Michelle L.
PHYTOPATHOLOGY.
107
:
5–5
Protein interaction networks at the host–microbe interface in Diaphorina citri , the insect vector of the citrus greening pathogen
2017.
Ramsey, J. S., Chavez, J. D., Johnson, R., Hosseinzadeh, S., Mahoney, J. E., Mohr, J. P., Robison, F., Zhong, X., Hall, D. G., Maccoss, M., Bruce, J., Heck, Michelle L.
Royal Society Open Science.
4
:
160545–160545
Evaluation of a Bead-Free Coimmunoprecipitation Technique for Identification of Virus-Host Protein Interactions Using High-Resolution Mass Spectrometry
2017.
DeBlasio, S. L., Bereman, M. S., Mahoney, J., Thannhauser, T. W., Gray, S. M., MacCoss, M. J., Heck, Michelle L.
Journal of Biomolecular Techniques : JBT.
28
:
111–121
Host Plants Indirectly Influence Plant Virus Transmission by Altering Gut Cysteine Protease Activity of Aphid Vectors
2017.
Pinheiro, P. V., Ghanim, M., Alexander, M., Rebelo, A. R., Santos, R. S., Orsburn, B. C., Gray, S., Heck, Michelle L.
Mol Cell Proteomics.
16
:
S230–S243
Relative susceptibility of Musa genotypes to banana bunchy top disease in Cameroon and implication for disease management
2017.
Ngatat, S., Hanna, R., Kumar, P. L., Gray, S. M., Heck, Michelle L., Ghogomu, R. T., Fontem, D. A.
Crop Protection.
101
:
116–122
Insights in luteovirid structural biology guided by chemical cross-linking and high resolution mass spectrometry
2017.
Alexander, M. M., Mohr, J. P., DeBlasio, S. L., Chavez, J. D., Ziegler-Graff, V., Brault, V., Bruce, J. E., Heck, Michelle L.
Virus Research.
241
:
42–52
A molecular tug-of-war: Global plant proteome changes during viral infection
2016.
Alexander, M. M., Heck, Michelle L.
Current Plant Biology.
5
:
13–24
Morphological abnormalities and cell death in the Asian citrus psyllid (Diaphorina citri) midgut associated with Candidatus Liberibacter asiaticus
2016.
Ghanim, M., Fattah-Hosseini, S., Levy, A., Heck, Michelle L.
Nature Scientific Reports.
6
:
A General Method for Targeted Quantitative Cross-Linking Mass Spectrometry
2016.
Chavez, J. D., Eng, J. K., Schweppe, D. K., Heck, Michelle L., Rivera, K., Zhong, X., Wu, X., Allen, T., Khurgel, M., Kumar, A., Lampropoulos, A., Larsson, M., Maity, S., Morozov, Y., Pathmasiri, W., Perez-Neut, M., Pineyro-Ruiz, C., Polina, E., Post, S., Rider, M., Tokmina-Roszyk, D., Tyson, K., Sant'Ana, D. VP, Bruce, J. E.
PLOS One.
11
:
e0167547–e0167547
Visualization of Host-Polerovirus Interaction Topologies Using Protein Interaction Reporter Technology
2016.
DeBlasio, S. L., Chavez, J. D., Alexander, M. M., Ramsey, J., Eng, J. K., Mahoney, J., Gray, S. M., Bruce, J. E., Heck, Michelle L.
Journal of Virology.
90
:
1973–1987
Model System-Guided Protein Interaction Mapping for Virus Isolated from Phloem Tissue
2016.
Deblasio, S. L., Johnson, R. S., Maccoss, M. J., Gray, S. M., Heck, Michelle L.
Journal of Proteome Research.
15
:
4601–4611
The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host 5 adaptation, and insecticide resistance
2016.
Chen, W., Hasegawa, D. K., Kaur, N., Kliot, A., Pinheiro, P. V., Luan, J., Stensmyr, M. C., Zheng, Y., Liu, W., Sun, H., Xu, Y., Luo, Y., Kruse, A., Yang, X., Kontsedalov, S., Lebedev, G., Fisher, T. W., Nelson, D. R., Hunter, W. B., Brown, J. K., Jander, Georg, Heck, Michelle L., Douglas, Angela E., Ghanim, M., Simmons, A. M., Wintermantel, W. M., Ling, K. S., Fei, Zhangjun
BMC Biology.
14
:
Metabolic Interplay between the Asian Citrus Psyllid and Its Profftella Symbiont: An Achilles’ Heel of the Citrus Greening Insect Vector
2015.
Ramsey, J. S., Johnson, R. S., Hoki, J. S., Kruse, A., Mahoney, J., Hilf, M. E., Hunter, W. B., Hall, D. G., Schroeder, Frank, MacCoss, M. J., Heck, Michelle L.
PLOS One.
10
:
e0140826–e0140826
Comparative proteomics and RNA aptamer technology to identify critical factors for transmission of Candidatus Liberibacter asiacticus by the Asian citrus psyllid
2015.
Kruse, A., Ozer, A., Johnson, R., Ghanim, M., Lis, J., Shatters, R., MacCoss, M., Heck, Michelle L.
MOLECULAR BIOLOGY OF THE CELL.
26
:
Is there a role for symbiotic bacteria in plant virus transmission by insects?
2015.
Pinheiro, P. V., Kliot, A., Ghanim, M., Heck, Michelle L.
Current Opinion in Insect Science.
8
:
69–78
Potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection
2015.
Deblasio, S. L., Johnson, R., Sweeney, M. M., Karasev, A., Gray, S. M., Maccoss, M. J., Heck, Michelle L.
Proteomics.
15
:
2098–2112
Persistent, circulative transmission of begomoviruses by whitefly vectors
2015.
Rosen, R., Kanakala, S., Kliot, A., Cathrin Pakkianathan, B., Farich, B. A., Santana-Magal, N., Elimelech, M., Kontsedalov, S., Lebedev, G., Heck, Michelle L., Ghanim, M.
Current opinion in virology.
15
:
1–8
Insights Into the Polerovirus– Plant Interactome Revealed by Coimmunoprecipitation and Mass Spectrometry
2015.
Deblasio, S. L., Johnson, R., Mahoney, J., Karasev, A., Gray, S. M., MacCoss, M. J., Heck, Michelle L.
Molecular Plant-Microbe Interactions.
28
:
467–481
Implication of the Bacterial Endosymbiont Rickettsia spp. in Interactions of the Whitefly Bemisia tabaci with Tomato Yellow Leaf Curl Virus
2014.
Kliot, A., Heck, Michelle L., Czosnek, H., Ghanim, M.
Journal of Virology.
88
:
5652–5660
Evidence for lysine acetylation in the Coat protein of a polerovirus
2014.
Heck, Michelle L., Johnson, R., Sweeney, M., DeBlasio, S. L., Bruce, J. E., MacCoss, M. J., Gray, S. M.
The Journal of general virology.
95
:
2321–2329
Visualizing molecular signatures of host-virus protein interactions using high resolution mass spectrometry
2014.
Heck, Michelle L., Bruce, J. E., DeBlasio, S. L., Chavez, J. D., Mahoney, J., Eng, J., Gray, S. M.
PHYTOPATHOLOGY.
104
:
141–141
Evidence of the Biochemical Basis of Host Virulence in the Greenbug Aphid, Schizaphis graminum (Homoptera: Aphididae)
2014.
Pinheiro, P., Bereman, M. S., Burd, J., Pals, M., Armstrong, S., Howe, K. J., Thannhauser, T. W., MacCoss, M. J., Gray, S. M., Heck, Michelle L.
Journal of Proteome Research.
13
:
2094–2108
Circulative, “Nonpropagative” Virus Transmission: An Orchestra of Virus-, Insect-, and Plant-Derived Instruments
2014.
Gray, Stewart, Heck, Michelle L., Ghanim, M.
ADVANCES IN VIRUS RESEARCH, VOL 89.
89
:
141–199
Long term evaluation of the susceptibility of 16 Musa genotypes to banana bunchy top disease in Cameroon, Central Africa
2013.
Ngatat, S., Hanna, R., Kumar, L., Gray, S. M., Heck, Michelle L., Fontem, D. A.
PHYTOPATHOLOGY.
103
:
103–103
Genomic and Proteomic Analysis of Schizaphis graminum Reveals Cyclophilin Proteins Are Involved in the Transmission of Cereal Yellow Dwarf Virus
2013.
Tamborindeguy, C., Bereman, M. S., DeBlasio, S., Igwe, D., Smith, D. M., White, F., MacCoss, M. J., Gray, Stewart, Heck, Michelle L.
PLOS One.
8
:
e71620–e71620
Characterization of protein biomarkers linked to transmission competent and transmission refractive aphid and whitefly populations in Nigeria
2013.
Igwe, D., Ngatat, S., Heck, Michelle L., Bereman, M. S., MacCoss, M. J., Gray, S. M., Hanna, R., Kumar, L.
PHYTOPATHOLOGY.
103
:
65–65
Homopteran Vector Biomarkers for Efficient Circulative Plant Virus Transmission are Conserved in Multiple Aphid Species and the Whitefly Bemisia tabaci
2012.
Heck, Michelle L., Bereman, M., Fish, T., MacCoss, M. J., Gray, Stewart
Journal of Integrative Agriculture.
11
:
249–262
Discovery and Targeted LC-MS/MS of Purified Polerovirus Reveals Differences in the Virus-Host Interactome Associated with Altered Aphid Transmission
2012.
Heck, Michelle L., Peter, K. A., Bereman, M. S., Howe, K., Fish, T., Smith, D., Gildow, F., MacCoss, M. J., Thannhauser, T. W., Gray, Stewart
PLOS One.
7
:
e48177–e48177
Cross-linking Measurements of the Potato leafroll virus Reveal Protein Interaction Topologies Required for Virion Stability, Aphid Transmission, and Virus-Plant Interactions
2012.
Chavez, J. D., Heck, Michelle L., Weisbrod, C. R., Ju, H. J., Eng, J. K., Gray, Stewart, Bruce, J. E.
Journal of Proteome Research.
11
:
2968–2981
Using proteomics and mass spectrometry to explore the dynamic virus-vector interface
2012.
Heck, Michelle L.
PHYTOPATHOLOGY.
102
:
164–164
Tangible benefits of the aphid Acyrthosiphon pisum genome sequencing for aphid proteomics: Enhancements in protein identification and data validation for homology-based proteomics
2011.
Heck, Michelle L., Tamborindeguy, C., Rolland, M., Howe, K., Thannhauser, T. W., Gray, Stewart
Journal of Insect Physiology.
57
:
179–190
Exploring the insect vector-virus interactome using co-immunoprecipitation coupled to mass spectrometry
2011.
Gray, S., Heck, Michelle L., Howe, K., Fish, T., Thannhauser, T.
PHYTOPATHOLOGY.
101
:
S63–S63
Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission
2011.
Heck, Michelle L., Tamborindeguy, C., Fish, T., Howe, K., Thannhauser, T. W., Gray, Stewart
Journal of Virology.
85
:
2148–2166
Biomarker discovery from the top down: Protein biomarkers for efficient virus transmission by insects (Homoptera: Aphididae) discovered by coupling genetics and 2-D DIGE
2011.
Heck, Michelle L., Howe, K., Fish, T., Smith, D., Mahoney, J., Tamborindeguy, C., Burd, J., Thannhauser, T. W., Gray, Stewart
Proteomics.
11
:
2440–2458
Host proteins implicated in the aphid transmission of cereal yellow dwarf virus-RPV
2010.
Peter, K., Heck, Michelle L., Gildow, F., Thannhauser, T., Gray, S.
PHYTOPATHOLOGY.
100
:
S100–S100
Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport
2009.
Benitez-Alfonso, Y., Heck, Michelle L., San Roman, A., Thomas, C., Maule, A., Hearn, S., Jackson, D.
Proceedings of the National Academy of Sciences.
106
:
3615–3620
A comparison of protein extraction methods suitable for gel-based proteomic studies of aphid proteins
2009.
Heck, Michelle L., Fish, T., Yang, X., Mclaughlin, M., Thannhauser, T. W., Gray, S.
Journal of Biomolecular Techniques : JBT.
20
:
201–215
Plasmodesmata form and function
2004.
Heck, Michelle L., Jackson, D.
Current Opinion in Cell Biology.
16
:
500–506

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