Christopher A. Makaroff, Jr.


Full Professor and Chair,
 Dept. of Chemistry and Biochemistry

RESEARCH AND PROFESSIONAL EXPERIENCE:  

Other Professional Services:

Editorial Board: Plant Signaling and Behavior, 2005-

Ad hoc manuscript reviewer:
Current Genetics, Development, FEBS Lett., Genetics, HortScience, Nucleic Acids Res., New Biologist, Plant Science, The Plant Cell, Plant Journal, PNAS, Theoretical and Applied Genetics, Plant Mol. Biol., Protoplasma, J. Cell Biol, J. Amer. Chem Soc., Plant Physiol. Sexual Plant Reprod.

 Program Review
2002 Department of Chemistry, Edinboro University
2003 Department of Chemistry, Slippery Rock University

 Ad hoc grant proposal reviewer:
DOE, NSF, USDA, Basic Research Foundation, Sci. & Engineering Council of Canada

 Grant Panel member
1998    USDA Genetic Mechanisms Grant Review Panel
1998    NSF Biochemistry of Gene Expression Grant Review Panel
1999    USDA Genetic Mechanisms Grant Review Panel
2001    NIH BIOL Study Section
2000        NIH ZRG1 Study Section (3 panels)
2001        NIH ZRG1 Study Section (3 panels)
2002        NIH ZRG1 Study Section (3 panels)
2003        NIH ZRG1 Study Section (3 panels)
2004        NIH ZRG1 Study Section (3 panels)
2005    NIH NDT Study Section (1 panel)
2005        NIH ZRG1 Study Section

 
Externally Funded Research

      

                                                     Educational Funding

Institutional Funding

Ohio Eminent Scholar in Structural Biology, M. Novak (co-PI), Ohio Board of Regents $1,250,000 2003

 Graduate Students Mentored

 Kevin Geiss, Intron Loss from the Mitochondrial nad4 gene of Lactuca sativa:  Evidence for Homologous Recombination of a cDNA Intermediate and A Comparative Light Microscopy Study of Microsporogenesis in Normal, Ogura Male-Fertile and Ogura Male-Sterile Radish (Raphanus sativus) (M.S., August 1993).

 Brenda Peirson, Molecular and Cytochemical Characterization of A. thaliana  Meiotic Mutant (Ph.D., December 1996).

 Xuefang Bai, M.S., Identification and Molecular Characterization of the SYN1 Gene in A. thaliana (M.S., August 1998).

 Dawn Paxson-Sowders, The Isolation and Characterization of dex1, a Pollen Wall Mutant of Arabidopsis thaliana (Ph.D., May 2000).

 Trinity Zang, Overexpression and Characterization of Glyoxalase II Isozymes from Arabidopsis thaliana (M.S., August 2000).

 Sarah Rhee, Characterization of Glyoxalase II Isozymes in Arabidopsis thaliana (M.S., August 2001).

 Beth Kostic, Localization and Calcium Binding Studies of DEX1 from Arabidopsis thaliana (M.S., August 2002).

 George Nimako, Determination of the Amino Terminus of the Mitochondrial Glyoxalase II Isozymes Using a Proteomic Approach (M.S., December 2003).

 Wing See Lam, The Isolation and Characterization of Arabidopsis AtSMCl and AtSMC3 (Ph.D., August 2004).

 Gishanthi Marasinghe, Over-expression and Characterization of a Mitochondrial Glyoxalase II from Arabidopsis thaliana (M.S., December 2004).

 Zhe Liu.  Cohesins and the Role of ESP1 in Regulating Chromatid Cohesion in Mitosis and Meiosis (Ph.D., December  2005).

 Kingsley Boateng.  The Role of SWI1 Protein in Sister Chromatid Cohesion During Meiosis in Arabidopsis (current).

 Meghan Holdorf.  Structure Function Studies on Glyoxalase 2-3 (current).

 Sriram Devanathan.  Functional Studies on Mitochondrial Glyoxalases 2-1,and 2-5 (current)

 Pattrananee Limphong. Structural Studies on Mitochondrial Glyoxalases, 2-1 and 2-5 (current)

 Postdoctoral Researchers Mentored

 Heather Owen (1991-94).  Isolation and Characterization of Meiotic Genes.  Current Position:  Director of Microscope Facility, University of Wisconsin, Milwaukee, WI.

 Subbah Krishnasamy (1991-94).  The Ogura Cytoplasm of Radish.  Current Position:  Research Associate Professor, University of Illinois, Chicago, IL.

 Mrinal Maiti (1995-96).  Mitochondrial Rearrangements in the Og Cytoplasm of Radish.  Current Position:  Research Scientist, Bose Institute.

 Fugui Dong (1997-00).  Isolation and Characterization of Arabidopsis Meiotic Genes.  Current Position:  Research Scientist, Merck.

 Cai Xue (1998-02).  Chromosome Cohesion in Arabidopsis Meiosis.  Current Position:  Research Associate, University of Oklahoma,

 Xiaohui Yang (2000-).  Identification and Characterization of Meiotic Cell Cycle Proteins, Current.

 Varsha Raja (2002).  Chromosome Cohesion in Arabidopsis.

 Ming Xia (2001-03).  Chromosome Cohesion in Arabidopsis.  Current Position:  Research Scientist, Children’s Hospital.

 Ling Jiang (2004-).  Chromosome Cohesion in Arabidopsis. Current.

 Laura Stritmatter (2006-2007) Cytological Characterization of female Gametophytic and Embryo defective Mutants of Arabidopsis, Current

Cheng Bai (2007-)

PUBLICATIONS:
  (*Graduate Student  and **Undergraduate Student Co-authors)

1.  Chetsanga C. J., Lozon, M., Makaroff, C. A. and Savage, L. 1981  Purification and Characterization of Escherichia coli Formamidopyrimidine-DNA Glycosylase that Excises Damaged 7-Methylguanosine from Deoxyribonucleic Acid. Biochemistry 20: 5201-5207.
2.  Chetsanga, C. J. and Makaroff, C. A. 1982  Alkaline Opening of the Imidazole Ring of 7-Methyl-guanosine.  1. Analysis of the Resulting Pyrimidine Derivatives. Chem. Biol. Interact. 41: 227-233.
3.  Chetsanga, C. J., Bearie, B. and Makaroff, C. A. 1982  Alkaline Opening of the Imidazole Ring  of 7-Methylguanosine.  2. Further Studies on Reaction Mechanisms and Products. Chem. Biol. Interact. 41: 235-249.
4.  Makaroff, C. A., Zalkin, H., Switzer, R. L. and Vollmer, S. J. 1983  Cloning of the Bacillus subtilis Glutamine Phosphoribosylpyrophosphate Amidotransferase Gene in Escherichia coli.  Nucleotide Sequence Determination and Properties of the Plasmid Encoded Enzyme.  J. Biol. Chem. 258: 10586-10593.
5.  Makaroff, C. A. and Zalkin, H. 1985  Regulation of Escherichia coli purF.  Analysis of the Control Region of a pur Regulon Gene. J. Biol. Chem. 260: 10378-10387.
6.  Makaroff, C.A., Paluh, J. L. and Zalkin, H. 1986  Mutagenesis of Ligands to the 4Fe-4S  Center of Bacillus subtilis  Glutamine Phosphoribosylpyrophosphate Amidotransferase. J. Biol. Chem. 261: 11416-11423.
7.  Weng, M., Makaroff, C. A. and Zalkin, H. 1986  Nucleotide Sequence of Escherichia coli  pyrG Encoding CTP Synthetase. J. Biol. Chem. 261: 5568-5574.
8.  Makaroff, C. A. and Palmer, J. D. 1987  Extensive, Mitochondrial Specific Transcription of the Brassica campestris Mitochondrial Genome.  Nucleic Acids Res. 15: 5141-5156.
9.  Makaroff, C. A. and Palmer, J. D. 1988  Mitochondrial DNA Rearrangements and Transcriptional Alterations in the Ogura Male-Sterile Cytoplasm of Radish. Mol. Cell. Biol. 8: 1474-1480.
10.  Makaroff, C. A., Apel, I. J. and Palmer J. D.  1989 The atp6 Coding Region has been Disrupted and a Novel Reading Frame Generated in the Ogura Radish Mitochondrial Genome, J. Biol. Chem. 264:11706-11713.
11.  Grandoni, J. A., Switzer, R. R., Makaroff, C. A., and Zalkin, H.  1989 Evidence that the Iron-Sulfur Cluster of Bacillus subtilis Glutamine Phosphoribosylpyrophosphate Amidotransferase Determines Stability of the Enzyme to Degradation In vivo, J. Biol. Chem., 264: 6058-6064.
12.  Makaroff, C. A., Apel, I. J. and Palmer, J. D.  1990 Characterization of Radish Mitochondrial atpA: Influence of Nuclear Background on Transcription of atpA-Associated Sequences and Relationship with Male Sterility.  Plant Mol. Biol. 15:735-746
13.  Makaroff, C. A., Apel, I. J., and Palmer, J. D.  1991 The Role of cox-I Associated Repeated Sequences in Plant Mitochondrial DNA Rearrangements and Radish Cytoplasmic Male Sterility.  Current Genetics 19:183-190.
14.  Christy, M. C., Makaroff, C. A., and Earle, E. D.  1991  Atrazine-resistant Cytoplasmic Male-Sterile-nigra Broccoli Obtained by Protoplast Fusion Between Cytoplasmic Male-Sterile Brassica oleracea and Atrazine-Resistant Brassica campestris.  Theor. Appl. Genetics 83:201-208.
15.  Temple, M., Makaroff, C. A., Earle, E. D., and Mutschler, M. A. 1992 Mitochondrial Recombination in Protoplast Fusion-Derived Brassica napus Plants.  Current Genetics, 22: 243-249.
16.  **Gass, D. G., Makaroff, C. A., and Palmer, J. D. 1992 Variable Intron Content of the NADH Dehydrogenase Subunit Four Gene of Plant Mitochondria.  Current Genetics, 21: 423-430.
17.  Krishnasamy, S., and Makaroff, C. A. 1993 Characterization of the Radish Mitochondrial orfB Locus: Possible Relationship with Male Sterility in Ogura Radish.  Current Genetics, 24:156-163
18.  Krishnasamy, S., Grant, R., and Makaroff, C. A.  1994 Subunit 6 of the Fo ATP Synthase Complex From Cytoplasmic Male Sterile Radish: RNA Editing and NH2-Terminal Protein Sequencing. Plant Mol. Biol., 24:129-141
19.  *Geiss, K. T. **Abbas, G., and Makaroff, C. A. 1994 Intron Loss in the nad4 Gene of Lettuce: Homologous Recombination of a Reverse-Transcribed RNA Intermediate.  Mol. and Gen. Genetics, 243:97-105
20.  Krishnasamy, S., and Makaroff, C. A.  1994 Organ-Specific Reduction of a Mitochondrial Protein Accompanies Nuclear Restoration in Cytoplasmic Male-Sterile Radish.  Plant Mol. Biol., 26:935-946
21.  Owen, H., Makaroff, C. A. 1995 Ultrastructure of Microsporogenesis and Microgametogenesis in Arabidopsis thaliana (L. Heynh.) ecotype Wassilewskija.  Protoplasma, 185:7-21
22.  *Peirson, B. N., Owen, H. A., Feldmann, K. A. and Makaroff, C. A. 1996  Characterization of Three Male-Sterile Mutants of Arabidopsis thaliana Exhibiting Alterations In Meiosis.  Sex. Plant Reproduction, 9:1-16
23.  **Rankin, C. T. , **Cutright, M. T., Makaroff, C. A. 1996  Characterization of the Radish Mitochondrial nad3/rps12 Locus: Analysis of Recombination Repeats and RNA Editing.  Current Genetics, 29:564-571
24.  Katembe, W. J., Swatzell, L. J., Makaroff, C. A., Kiss, J. Z. 1997  Immunolocalization of Integrin-like Proteins in Arabidopsis and Chara.  Physiologia Plantarum 99:7-14
25.  *Peirson, B. N., **Bowling, S. E., Makaroff, C. A.  1997 A Defect in Synapsis Causes Sterility in a T-DNA-Tagged Mutant Of Arabidopsis  Plant Journal, 11:659-669
26.  *Paxson-Sowders, D. M., Owen, H. A., Makaroff, C. A.  1997 A Comparative Ultrastructural Analysis of Exine Pattern Development in Wild-Type Arabidopsis and a Mutant Defective in Pattern Formation  Protoplasma, 198:53-65
27.  Maiti, M. K., Krishnasamy, S., Owen, H. A. and Makaroff, C. A.  1997 Molecular Characterization of Glyoxalase II from Arabidopsis thaliana.  Plant Mol. Biol.,35:471-481
28.  Crowder, M. W., Maiti, M. K., **Banovic, L., Makaroff, C. A. 1997 Glyoxalase II from A. thaliana Requires Zn(II) for Catalytic Activity FEBS Lett., 418:351-354
29.  Dong, F. G., Wilson, K. G., Makaroff, C. A. 1998 Analysis of the Four cox2 Genes Found in Turnip (Brassica campestris, Brassicacea) Mitochondria.  Amer. J. Bot., 85:153-161
30.  Dong, F. G., Wilson K. G., Makaroff, C. A.  1998 The Radish (Raphanus sativus L.) Mitochondrial cox2 Gene Contains an ACG at the Predicted Translation Initiation Site.  Current Genetics, 34:79-87
31. *Bai, X., *Peirsion, B. N., Dong, F., Cai, X., Makaroff, C. A. 1999 Isolation and Characterization of SYN1, a RAD21-like Gene Essential for Meiosis in Arabidopsis, The Plant Cell, 11:417-430
32. Swatzell, L.J., Edelmann, R.E., Makaroff, C.A., Kiss, J.Z. 1999  Integrin-Like Proteins Are Localized to Membrane Fractions, Not Plastids, in Arabidopsis.  Plant Cell Physiol. 40, 173-183.
33. *Zang, T.M., **Hollman, D.A., Crawford, P., Crowder, M.W., Makaroff, C.A. 2001 Arabidopsis Glyoxalase II Contains A Zinc/Iron Binuclear Metal Center That is Essential for Substrate Binding And Catalysis.  J. Biol. Chem., 267:4788-4795
34. Dong, F., Xue, C., Makaroff, C.A. 2001 Cloning and Characterization of Two Arabidopsis Genes That Belong to the RAD21/REC8 Family of Chromosome Cohesin Proteins. Gene, 271:91-108
35. Xue, C., Makaroff, C.A. 2001 The dsy10 Mutation of Arabidopsis Results Desynapsis and a General Breakdown in Meiosis. Sex. Plant Repro., 14: 63-67
36. *Paxson-Sowders, D. M., **Dodrill, C., Owen, H.A., Makaroff, C. A.  2001 Isolation and Characterization of dex1, a Gene Essential for Exine Pattern Formation in Arabidopsis. Plant Physiol. 127:1739-1749
37. Yang, X., Makaroff, C.A., Ma, H.  2003  The Arabidopsis Male Meiocyte Death1 Gene Is Required For Male Meiosis And Encodes a Novel Putative Chromatin Remodeling Factor. Plant Cell, 15, 1281-1295
38. Yang, K.-W., **Sobieski, D.N., Carenbauer, A.L., Crawford, P.A., Makaroff, C.A., Crowder, M.W. 2003 Explaining the Inhibition of Glyoxalase II by 9-Fluorenylmethoxycarbonyl-protected Glutathione Derivatives.  Archives Biochem. Biophys., 414, 271-278
39. Xue, C., Dong, F., Edelman, R., Makaroff, C.A. 2003 The Arabidopsis SYN1 Cohesin Protein is Required For Sister Chromatid Arm Cohesion and Homologous Chromosome Pairing. J Cell Science, 116: 2999-3007
40. Mercier, R., Armstrong, S.J., Horlow, C., Jackson, N.P., Makaroff, C.A., Vezon, D., Pelletier, G., Jones, G.H., Franklin, F.C.  2003 The Meiotic Protein SWI1 is Required For Axial Element Formation and Recombination Initiation in Arabidopsis.  Development 130: 3309-3318
41. Schilling, O., *Wenzel, N., **Naylor, M., Vogel, A., Crowder^, M., Makaroff, C., and Meyer–Klaucke, W. 2003  Flexible Metal Binding of the Metallo–b–Lactamase Domain: Glyoxalase II Incorporates Iron, Manganese, and Zinc in vivo. Biochem., 42:11777-11786
42. *Wenzel N.F., Carenbauer A.L., **Pfiester M.P., Schilling O., Meyer-Klaucke W., Makaroff C.A., Crowder M.W.  2004 The Binding of Iron and Zinc to Glyoxalase II Occurs Exclusively as Di-metal Centers and is Unique Within the Metallo-beta-lactamase Family. J Bio. Inorg Chem.  9:429-438
43. Yang, X., Makaroff, C.A., Ma, H.  2004  Characterization of an Unusual Ds Element: Evidence for Insertion by a Circular Intermediate. Plant Mol. Biol. 55:751-763
44. *Lam, W. S., Yang, X., Makaroff, C.A. 2005 Characterization of Arabidopsis thaliana SMC: Evidence That AtSMC3 May Have Additional Roles Beyond Chromosome Cohesion. J. Cell Science, 118:3037-3048.
45. Li, W., Yang,  X.,  Lin,  Z.,  Timofejeva  L.,  Xiao, R., Makaroff, C.A.,  Ma, H. 2005 Normal Meiotic Chromosome Pairing,  double Strand DNA Break Repair, and Synapsis Requires the AtRAD51C gene in Arabidopsis.  Plant Physiology, 138:965-976.
46. *Marasinghe, G. P. K., **Sander,^, I.M., Bennett, B., Periyannan, G., Yang, K.-W.,  Makaroff, C.A., Crowder, M.W. 2005 Structural Studies On A Mitochondrial Glyoxlase II, J. Biol. Chem., 280: 40668-40675
47. *Zhe, L., Makaroff, C. A. 2006 Arabidopsis AtESP1 is an Essential Gene Required for the Release of Sister Chromatid Cohesion. Plant Cell, 18: 1213-1225
48. Zou, D., Yang, X., Li Quan, L.,Timofejeva, L., Rigel. N.W., Ma, H., Makaroff, C.A.,  2006 ASK1, a SKP1-like Gene, is Required for Chromosome Pairing Condensation and Separation and involved in SYN1 Cohesin Degradation During Meiosis. Plant Mol. Biol.,  63: 99-110
49. McCoy, J.G., Bingman, C.A., Eduard, B., *Holdorf, M.M., Makaroff, C.A., Phillips, G. N. 2006 Structure of an ETHE1-like Protein from Arabidopsis thaliana.  Acta Crystallographica, Sec. D,  964-970.
50. Zou, D., Yang, X., Timofejeva, L. Ma, H., Makaroff, C.A.,  2006 The Arabidopsis SKP1 homologue ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus, J. Cell Sci,  19: 4025-4032
51. Pereira, LAR, Bratanova, M, Xue, C, Makaroff, CA, Emery, RJN, Moffatt, BA  2006 Methyl Recycling activities are Co-ordinately regulated During Plant Development.  J Exp. Botany, submitted

Book Chapters

1.  Palmer J. D., Makaroff, C. A., Apel, I. J. and Shirzadigan, M. 1990 Fluid Structure of Plant Mitochondrial Genomes: Evolutionary and Functional Implications, UCLA Symposia on Molecular and Cellular Biology, New Series, Vol. 122, Editors M. Clegg and G. S. O Brian, Alan Liss Inc., New York, NY, 85-96.
2.  Makaroff, C. A. 1995 CMS of Brassica , In Advances in Cellular and Molecular Biology of Plants volume 2: Molecular Biology of the Mitochondria.  Editors C. S. Levings III and I. K. Vasil Eds., 515-555
3.  Makaroff, C. A. 1997 Cytoplasmic Male Sterility: Molecular Studies, In Recent Advances in Oilseed Brassicas.  Editors H. R. Kalia, and S. K. Gupta, Kalyani Publishers, Ludhiana, pp.92-111

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 INVITED PRESENTATIONS AT NATIONAL/INTERNATIONAL MEETINGS:  

1987    Brassica Mitochondrial DNAs: Structure, Function and Expression.  Crucifer Genetics Workshop #4,
            University of Wisconsin-Madison, Molecular Biology Group. Chairman and Speaker
1987    Brassica Mitochondrial DNAs: Structure, Function and Expression.  ASBMB Meeting,
            Philadelphia, PA, Plant Molecular Biology Section. Invited Speaker.
1988    Alterations Associated with the Male Sterile Cytoplasm of Radish. Third Int. Workshop on the
            Mitochondrial Genome of Higher Plants. Roscoff, France. Invited Speaker
1990    Mitochondrial Alterations Associated with Male Sterility in Ogura Radish.  Crucifer Genetics
            Workshop #5, University of California , Davis. Invited Speaker
1990    Mitochondrial Alterations Associated with Male Sterility in Ogura Radish.  Fourth Int. Conference
            on Plant Mitochondria.  Cornell University. Invited Speaker.
1990    Mitochondrial Alterations Associated with Male Sterility in Ogura Radish.  Crucifer Genetics
            Workshop #6, Cornell University. Invited Speaker
1992    Mitochondrial Alterations Associated with CMS in Ogura Radish.  Fourth International Congress
            of Plant Mitochondria, Berlin, Germany.  Invited Speaker, declined offer because of teaching conflicts.
1993    Cytoplasmic Male Sterility in Ogura Radish: Effect of Nuclear Background on Mitochondrial
            Function.  XV International Botanical Congress, Yokohama Japan. Invited Speaker
1996    Molecular Analysis of the Brassica CMS.  International Symposium on Plant Molecular Biology,
            Lucknow India. Invited Speaker, declined invitation
1997    Molecular and cytochemical characterization of syn1, a synaptic mutant of Arabidopsis.
            8th Int. Conf. on  Arabidopsis  Research, Madison, WI. Invited speaker
1997    International Meeting of Plant Physiologists, Vancouver, BC.  Session Chair for Reproductive Biology session
1997    Characterization of Arabidopsis Mutants Exhibiting Defects in Microsporogenesis. International Meeting of Plant
            Physiologists, Vancouver, BC. Invited speaker
1998    Characterization of Arabidopsis Mutants Exhibiting Defects In Meiosis.  Meiosis Gordon Conference.
            Invited speaker
1999    Isolation And Characterization Of RAD21-Like Genes Essential For Meiosis And Mitosis In Arabidopsis.
            American Society of Plant Physiology and Molecular Biology, Baltimore, MD. Invited speaker
1999    Isolation And Characterization Of RAD21-Like Genes Essential For Meiosis In Arabidopsis.  International
            Botanical Congress, St. Louis MO. Invited speaker
2000        Isolation and Characterization of Proteins Required For Chromosome Condensation And Sister Chromatid
            Cohesion During Meiosis And Mitosis.  Frontiers in Sexual Plant Reproduction, Albany, NY.  Invited speaker
2001    Investigating Early Meiotic Events in Arabidopsis Plant Reproduction 2002. State College, PA Invited speaker
2002    The Arabidopsis SYN1 Cohesin Protein Is Required For Meiotic Chromosome Arm Cohesion From Early
            Prophase To Anaphase, Meiosis Gordon Conference, Invited speaker
2004    DEX1, a protein required for exine pattern development in Arabidopsis thaliana XI International
            Palynologycal Congress. Granada, Spain, invited speaker

INVITED SEMINARS:

1988    Dept. of Plant Sciences, Institute de Biologie Moleculaire et Cellulaire, Strasbourg, France
1989    Central research and Development, DuPont
            Chemistry, Notre Dame
            Chemistry, Miami University
            Plant Breeding, Cornell University
            Microbiology, Miami University
1990    Plant Biology, Purdue University
            Biochemistry Seminar Series, Northern Illinois University
            Plant Biology, Ohio State University
            Biology Seminar Series, Bowling Green University
1991    Botany, Miami  University
1992    Biology, University of Michigan
1993    Dept. of Agriculture, Kobe University, Kobe Japan
            Research Institute of Agricultural Resources, Ishikawa, Japan
            Sakata Seed Co. Chiba, Japan
1994    Environmental and Plant Biology, Ohio University
            Biology, McGill University
            Biology, University of Toledo
            Sigma Xi Seminar Speaker, Eastern Kentucky University
1995    Biology, Western Kentucky University
            Botany, Miami University
1996    Biology, Indiana Purdue Fort Wayne
1997    Biology, Eastern Kentucky University
1998    Plant Biology, Ohio State University
1999    Biotech Center, Rutgers University
2001    Chemistry, Western Kentucky University
            Plant Biology, Purdue University
2002    Biology, Penn State University
2003    Genetics Program, University of Arizona
2004    Donald Danforth Plant Biology Center

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