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Journal of Molecular Evolution

, Volume 86, Issue 3–4, pp 240–253 | Cite as

Evolution of Melanoma Antigen-A11 (MAGEA11) During Primate Phylogeny

  • Christopher S. Willett
  • Elizabeth M. Wilson
Original Article
  • 149 Downloads

Abstract

Melanoma antigen-A11 (MAGE-A11) is an X-linked and primate-specific steroid hormone receptor transcriptional coregulator and proto-oncogenic protein whose increased expression promotes the growth of prostate cancer. The MAGEA11 gene is expressed at low levels in normal human testis, ovary, and endometrium, and at highest levels in castration-resistant prostate cancer. Annotated genome predictions throughout the surviving primate lineage show that MAGEA11 acquired three 5′ coding exons unique within the MAGEA subfamily during the evolution of New World monkeys (NWM), Old World monkeys (OWM), and apes. MAGE-A11 in all primates has a conserved FXXIF coactivator-binding motif that suggests interaction with p160 coactivators contributed to its early evolution as a transcriptional coregulator. An ancestral form of MAGE-A11 in the more distantly related lemur has significant amino acid sequence identity with human MAGE-A11, but lacks coregulator activity based on the absence of the three 5′ coding exons that include a nuclear localization signal (NLS). NWM MAGE-A11 has greater amino acid sequence identity than lemur to human MAGE-A11, but inframe premature stop codons suggest that MAGEA11 is a pseudogene in NWM. MAGE-A11 in OWM and apes has nearly identical 5′ coding exon amino acid sequence and conserved interaction sites for p300 acetyltransferase and cyclin A. We conclude that the evolution of MAGEA11 within the lineage leading to OWM and apes resulted in steroid hormone receptor transcriptional coregulator activity through the acquisition of three 5′ coding exons that include a NLS sequence and nonsynonymous substitutions required to interact with cell cycle regulatory proteins and transcription factors.

Keywords

Melanoma antigen-A11 MAGEA11 MAGE-A11 Androgen receptor Primate Evolution New World monkey Old World monkey Ape Lemur 

Abbreviations

AF2

Activation function 2

AR

Androgen receptor

MHD

MAGE homology domain

MAGEA11

Melanoma antigen-A11 gene

MAGE-A11

Melanoma antigen-A11 protein

MYA

Million years ago

NCBI

National Center for Biotechnology Information

NWM

New World monkeys

NLS

Nuclear localization signal

OWM

Old World monkeys

TIF2

Transcriptional intermediary factor 2

Notes

Acknowledgements

The work was supported by United States Public Health Service National Cancer Institute, National Institutes of Health (Grant No. P01-CA77739). We thank Frank S. French for reviewing the manuscript.

Author Contributions

CSW and EMW contributed to data analysis and preparation of the manuscript.

References

  1. Artamonova II, Gelfand MS (2004) Evolution of the exon-intron structure and alternative splicing of the MAGE-A family of cancer/testis antigens. J Mol Evol 59:620–631CrossRefPubMedGoogle Scholar
  2. Askew EB, Bai S, Hnat AT, Minges JT, Wilson EM (2009) Melanoma antigen gene protein-A11 (MAGE-11) F-box links the androgen receptor NH2-terminal transactivation domain to p160 coactivators. J Biol Chem 284:34793–34808CrossRefPubMedPubMedCentralGoogle Scholar
  3. Askew EB, Bai S, Blackwelder AJ, Wilson EM (2010) Transcriptional synergy between melanoma antigen gene protein-A11 (MAGE-11) and p300 in androgen receptor signaling. J Biol Chem 285:21824–21836CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baertsch R, Diekhans M, Kent WJ, Haussler D, Brosius J (2008) Retrocopy contributions to the evolution of the human genome. BMC Genom 9:466CrossRefGoogle Scholar
  5. Bai S, Wilson EM (2008) Epidermal growth factor-dependent phosphorylation and ubiquitinylation of MAGE-11 regulates its interaction with the androgen receptor. Mol Cell Biol 28:1947–1963CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bai S, He B, Wilson EM (2005) Melanoma antigen gene protein MAGE-11 regulates androgen receptor function by modulating the interdomain interaction. Mol Cell Biol 25:1238–1257CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bai S, Grossman G, Yuan L, Lessey BA, French FS, Young SL, Wilson EM (2008) Hormone control and expression of androgen receptor coregulator MAGE-11 in human endometrium during the window of receptivity to embryo implantation. Mol Hum Reprod 14:107–116CrossRefPubMedGoogle Scholar
  8. Barker PA, Salehi A (2002) The MAGE proteins: emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res 67:705–712CrossRefPubMedGoogle Scholar
  9. Brosius J (1991) Retroposons–seeds of evolution. Science 251:753CrossRefPubMedGoogle Scholar
  10. Brosius J (2003) Gene duplication and other evolutionary strategies: from the RNA world to the future. J Struct Funct Genom 3:1–17CrossRefGoogle Scholar
  11. Brown CJ, Goss SJ, Lubahn DB, Joseph DR, Wilson EM, French FS, Willard HF (1989) Androgen receptor locus on the human X chromosome: regional localization to Xq11-12 and description of a DNA polymorphism. Am J Hum Genet 44:264–269PubMedPubMedCentralGoogle Scholar
  12. Burchardt T, Burchardt M, Chen MW, Cao Y, de la Taille A, Shabsigh A, Hayek O, Dorai T, Buttyan R (1999) Transdifferentiation of prostate cancer cells to a neuroendocrine cell phenotype in vitro and in vivo. J Urol 162:1800–1805CrossRefPubMedGoogle Scholar
  13. Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S (2001) An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 61:5544–5551PubMedGoogle Scholar
  14. Choong CS, Kemppainen JA, Wilson EM (1998) Evolution of the primate androgen receptor: a structural basis for disease. J Mol Evol 47:334–342CrossRefPubMedGoogle Scholar
  15. Choudhary M, Singh A, Kaur S, Arora K (2014) Enhancing lung cancer diagnosis: electrochemical simultaneous bianalyte immunosensing using carbon nanotubes-chitosan nanocomposite. Appl Biochem Biotechnol 174:1188–1200CrossRefPubMedGoogle Scholar
  16. De Plaen E, Arden K, Traversari C, Gaforio JJ, Szikora JP, De Smet C, Brasseur F, van der Bruggen P, Lethé B, Lurquin C, Brasseur R, Chomez P, De Backer O, Cawenee W, Boon T (1994) Structure, chromosomal localization, and expression of 12 genes of the MAGE family. Immunogenetics 40:360–369CrossRefPubMedGoogle Scholar
  17. Delbridge ML, Graves JA (2007) Origin and evolution of spermatogenesis genes on the human sex chromosomes. Soc Reprod Fertil Suppl 65:1–17PubMedGoogle Scholar
  18. Doyle JM, Gao J, Wang J, Yang M, Potts PR (2010) MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol Cell 39:963–974CrossRefPubMedPubMedCentralGoogle Scholar
  19. Emerson JJ, Kaessmann H, Betrán E, Long M (2004) Extensive gene traffic on the mammalian X chromosome. Science 303:537–540CrossRefPubMedGoogle Scholar
  20. Finta C, Zaphiropoulos PG (2000) The human cytochrome P450 3A locus. Gene evolution by capture of downstream exons. Gene 260:13–23CrossRefPubMedGoogle Scholar
  21. Ge L, Liu S, Xie L, Sang L, Ma C, Li H (2015) Differential mRNA expression profiling of oral squamous cell carcinoma by high-throughput RNA sequencing. J Biomed Res 29:397–404PubMedCentralGoogle Scholar
  22. Gogarten JP, Olendzenski L (1999) Orthologs, paralogs and genome comparisons. Curr Opin Genet Dev 9:630–636CrossRefPubMedGoogle Scholar
  23. Gómez JM, Verdú M, González-Megías A, Méndez M (2016) The phylogenetic roots of human lethal violence. Nature 538:233–237CrossRefPubMedGoogle Scholar
  24. Guo L, Sang M, Liu Q, Fan X, Zhang X, Shan B (2013) The expression and clinical significance of melanoma-associated antigen-A1, -A3 and -A11 in glioma. Oncol Lett 6:55–62CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hartmann S, Kriegebaum U, Küchler N, Brands RC, Linz C, Kübler AC, Müller-Richter UD (2014) Correlation of MAGE-A tumor antigens and the efficacy of various chemotherapeutic agents in head and neck carcinoma cells. Clin Oral Investig 18:189–197CrossRefPubMedGoogle Scholar
  26. Hartmann S, Brisam M, Rauthe S, Driemel O, Brands RC, Rosenwald A, Kübler AC, Müller-Richter UD (2016) Contrary melanoma-associated antigen-A expression at the tumor front and center: a comparative analysis of stage I and IV head and neck squamous cell carcinoma. Oncol Lett 12:2942–2947CrossRefPubMedPubMedCentralGoogle Scholar
  27. He B, Kemppainen JA, Voegel JJ, Gronemeyer H, Wilson EM (1999) Activation function 2 in the human androgen receptor ligand binding domain mediates interdomain communication with the NH2-terminal domain. J Biol Chem 274:37219–37225CrossRefPubMedGoogle Scholar
  28. He B, Kemppainen JA, Wilson EM (2000) FXXLF and WXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J Biol Chem 275:22986–22994CrossRefPubMedGoogle Scholar
  29. He B, Bowen NT, Minges JT, Wilson EM (2001) Androgen-induced NH2- and COOH-terminal interaction inhibits p160 coactivator recruitment by activation function 2. J Biol Chem 276:42293–42301CrossRefPubMedGoogle Scholar
  30. He B, Minges JT, Lee LW, Wilson EM (2002) The FXXLF motif mediates androgen receptor-specific interactions with coregulators. J Biol Chem 277:10226–10235CrossRefPubMedGoogle Scholar
  31. He B, Gampe RT Jr, Kole AJ, Hnat AT, Stanley TB, An G, Stewart EL, Kalman RI, Minges JT, Wilson EM (2004) Structural basis for androgen receptor interdomain and coactivator interactions suggests a transition in nuclear receptor activation function dominance. Mol Cell 16:425–438CrossRefPubMedGoogle Scholar
  32. Henderson DJ, Byrne A, Dulla K, Jenster G, Hoffmann R, Baillie GS, Houslay MD (2014) The cAMP phosphodiesterase-4D7 (PDE4D7) is downregulated in androgen-independent prostate cancer cells and mediates proliferation by compartmentalising cAMP at the plasma membrane of VCaP prostate cancer cells. Br J Cancer 110:1278–1287CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hou SY, Sang MX, Geng CZ, Liu WH, Lü WH, Xu YY, Shan BE (2014) Expressions of MAGE-A9 and MAGE-A11 in breast cancer and their expression mechanism. Arch Med Res 45:44–51CrossRefPubMedGoogle Scholar
  34. Hsu CL, Chen YL, Yeh S, Ting HJ, Hu YC, Lin H, Wang X, Chang C (2003) The use of phage display technique for the isolation of androgen receptor interacting peptides with (F/W)XXL(F/W) and FXXLY new signature motifs. J Biol Chem 278:23691–23698CrossRefPubMedGoogle Scholar
  35. Irvine RA, Coetzee GA (1999) Additional upstream coding sequences of MAGE-11. Immunogenetics 49:585CrossRefPubMedGoogle Scholar
  36. Karpf AR, Bai S, James SR, Mohler JL, Wilson EM (2009) Increased expression of androgen receptor coregulator MAGE-11 in prostate cancer by DNA hypomethylation and cyclic AMP. Mol Cancer Res 7:523–535CrossRefPubMedPubMedCentralGoogle Scholar
  37. Katsura Y, Satta Y (2011) Evolutionary history of the cancer immunity antigen MAGE gene family. PLoS ONE 6:e20365CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, Siepel A (2008) Patterns of positive selection in six mammalian genomes. PLoS Genet 4:e1000144CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lagarde WH, Blackwelder AJ, Minges JT, Hnat AT, French FS, Wilson EM (2012) Androgen receptor exon 1 mutation causes androgen insensitivity by creating phosphorylation site and inhibiting melanoma antigen-A11 activation of NH2- and carboxyl-terminal interaction-dependent transactivation. J Biol Chem 287:10905–10915CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH (2007) Classical nuclear localization signals: definition, function, and interaction with importin alpha. J Biol Chem 282:5101–5105CrossRefPubMedGoogle Scholar
  41. Lange A, McLane LM, Mills RE, Devine SE, Corbett AH (2010) Expanding the definition of the classical bipartite nuclear localization signal. Traffic 11:311–323CrossRefPubMedGoogle Scholar
  42. Lee AK, Potts PR (2017) A comprehensive guide to the MAGE family of ubiquitin ligases. J Mol Biol 429:1114–1142CrossRefPubMedGoogle Scholar
  43. Lian Y, Sang M, Ding C, Zhou X, Fan X, Xu Y, Lü W, Shan B (2012) Expressions of MAGE-A10 and MAGE-A11 in breast cancers and their prognostic significance: a retrospective clinical study. J Cancer Res Clin Oncol 138:519–527CrossRefPubMedGoogle Scholar
  44. Liu Q, Su S, Blackwelder AJ, Minges JT, Wilson EM (2011) Gain in transcriptional activity by primate-specific coevolution of melanoma antigen-A11 and its interaction site in androgen receptor. J Biol Chem 286:29951–29963CrossRefPubMedPubMedCentralGoogle Scholar
  45. Liu S, Sang M, Xu Y, Gu L, Liu F, Shan B (2016) Expression of MAGE-A1, -A9, -A11 in laryngeal squamous cell carcinoma and their prognostic significance: a retrospective clinical study. Acta Otolaryngol 136:506–513CrossRefPubMedGoogle Scholar
  46. Martin RD (2007) The evolution of human reproduction: a primatological perspective. Am J Phys Anthropol Suppl 45:59–84CrossRefGoogle Scholar
  47. Merkle D, Hoffmann R (2011) Roles of cAMP and cAMP-dependent protein kinase in the progression of prostate cancer: cross-talk with the androgen receptor. Cell Signal 23:507–515CrossRefPubMedGoogle Scholar
  48. Minges JT, Su S, Grossman G, Blackwelder AJ, Pop EA, Mohler JL, Wilson EM (2013) Melanoma antigen-A11 (MAGE-A11) enhances transcriptional activity by linking androgen receptor dimers. J Biol Chem 288:1939–1952CrossRefPubMedGoogle Scholar
  49. Minges JT, Grossman G, Zhang P, Kafri T, Wilson EM (2015) Post-translational down-regulation of melanoma antigen-A11 (MAGE-A11) by human p14-ARF tumor suppressor. J Biol Chem 290:25174–25187CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, Sninsky J, Adams MD, Cargill M (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3:e170CrossRefPubMedPubMedCentralGoogle Scholar
  51. Quigley CA, De Bellis A, Marschke KB, El Awady MK, Wilson EM, French FS (1995) Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 16:271–321PubMedGoogle Scholar
  52. Rasweiler JJ, de Bonilla H (1992) Menstruation in short-tailed fruit bats (Carollia spp.). J Reprod Fertil 95:231–248CrossRefPubMedGoogle Scholar
  53. Rogers J, Gibbs RA (2014) Comparative primate genomics: emerging patterns of genome content and dynamics. Nat Rev Genet 15:347–359CrossRefPubMedPubMedCentralGoogle Scholar
  54. Rogner UC, Wilke K, Steck E, Korn B, Poustka A (1995) The melanoma antigen gene (MAGE) family is clustered in the chromosomal band Xq28. Genomics 29:725–731CrossRefPubMedGoogle Scholar
  55. Sang M, Lian Y, Zhou X, Shan B (2011) MAGE-A family: attractive targets for cancer immunotherapy. Vaccine 29:8496–8500CrossRefPubMedGoogle Scholar
  56. Sang M, Gu L, Liu F, Lian Y, Yin D, Fan X, Ding C, Huang W, Liu S, Shan B (2016) Prognostic significance of MAGE-A11 in esophageal squamous cell carcinoma and identification of related genes based on DNA microarray. Arch Med Res 47:151–161CrossRefPubMedGoogle Scholar
  57. Sang M, Gu L, Yin D, Liu F, Lian Y, Zhang X, Liu S, Huang W, Wu Y, Shan B (2017) MAGE-A family expression is correlated with poor survival of patients with lung adenocarcinoma: a retrospective clinical study based on tissue microarray. J Clin Pathol 70:533–540CrossRefPubMedGoogle Scholar
  58. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Federhen S, Feolo M, Fingerman IM, Geer LY, Helmberg W, Kapustin Y, Krasnov S, Landsman D, Lipman DJ, Lu Z, Madden TL, Madej T, Maglott DR, Marchler-Bauer A, Miller V, Karsch-Mizrachi I, Ostell J, Panchenko A, Phan L, Pruitt KD, Schuler GD, Sequeira E, Sherry ST, Shumway M, Sirotkin K, Slotta D, Souvorov A, Starchenko G, Tatusova TA, Wagner L, Wang Y, Wilbur WJ, Yaschenko E, Ye J (2012) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 40:D13-25CrossRefPubMedGoogle Scholar
  59. Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen YT (2002) Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol Rev 188:22–32CrossRefPubMedGoogle Scholar
  60. Souvorov A, Kapustin Y, Kiryutin B, Chetvernin V, Tatusova T, Lipman D (2010) Gnomon–NCBI eukaryotic gene prediction tool. http://scholar.google.com/scholar_url?url=https://pdfs.semanticscholar.org/c47c/93d21f08052d6b2d9d115b8c4c210f82f197.pdf&hl=en&sa=X&scisig=AAGBfm2d9YAZIEDDIJs3T5h560pO1Ok6yQ&nossl=1&oi=scholarrGoogle Scholar
  61. Stevenson BJ, Iseli C, Panji S, Zahn-Zabal M, Hide W, Old LJ, Simpson AJ, Jongeneel CV (2007) Rapid evolution of cancer/testis genes on the X chromosome. BMC Genom 8:129CrossRefGoogle Scholar
  62. Su S, Blackwelder AJ, Grossman G, Minges JT, Yuan L, Young SL, Wilson EM (2012) Primate-specific melanoma antigen-A11 regulates isoform-specific human progesterone receptor-B transactivation. J Biol Chem 287:34809–34824CrossRefPubMedPubMedCentralGoogle Scholar
  63. Su S, Minges JT, Grossman G, Blackwelder AJ, Mohler JL, Wilson EM (2013) Proto-oncogene activity of melanoma antigen-A11 (MAGE-A11) regulates retinoblastoma-related p107 and E2F1 proteins. J Biol Chem 288:24809–24824CrossRefPubMedPubMedCentralGoogle Scholar
  64. Su S, Chen X, Geng J, Minges JT, Grossman G, Wilson EM (2017) Melanoma antigen-A11 regulates substrate-specificity of Skp2-mediated protein degradation. Mol Cell Endocrinol 439:1–9CrossRefPubMedGoogle Scholar
  65. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144CrossRefPubMedGoogle Scholar
  66. Taniura H, Kobayashi M, Yoshikawa K (2005) Functional domains of necdin for protein-protein interaction, nuclear matrix targeting, and cell growth suppression. J Cell Biochem 94:804–815CrossRefPubMedGoogle Scholar
  67. Turner LM, Hoekstra HE (2008) Causes and consequences of the evolution of reproductive proteins. Int J Dev Biol 52:769–780CrossRefPubMedGoogle Scholar
  68. Vinckenbosch N, Dupanloup I, Kaessmann H (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA 103:3220–3225CrossRefPubMedPubMedCentralGoogle Scholar
  69. Voegel JJ, Heine MJ, Tini M, Vivat V, Chambon P, Gronemeyer H (1998) The coactivator TIF2 contains three nuclear receptor-binding motifs and mediates transactivation through CBP binding-dependent and -independent pathways. EMBO J 17:507–519CrossRefPubMedPubMedCentralGoogle Scholar
  70. Weon JL, Potts PR (2015) The MAGE protein family and cancer. Curr Opin Cell Biol 37:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wilson EM (2010) Androgen receptor molecular biology and potential targets in prostate cancer. Ther Adv Urol 2:105–117CrossRefPubMedPubMedCentralGoogle Scholar
  72. Xia LP, Xu M, Chen Y, Shao WW (2013) Expression of MAGE-A11 in breast cancer tissues and its effects on the proliferation of breast cancer cells. Mol Med Rep 7:254–258CrossRefPubMedGoogle Scholar
  73. Yan G, Zhang G, Fang X, Zhang Y, Li C, Ling F, Cooper DN, Li Q, Li Y, van Gool AJ, Du H, Chen J, Chen R, Zhang P, Huang Z, Thompson JR, Meng Y, Bai Y, Wang J, Zhuo M, Wang T, Huang Y, Wei L, Li J, Wang Z, Hu H, Yang P, Le L, Stenson PD, Li B, Liu X, Ball EV, An N, Huang Q, Zhang Y, Fan W, Zhang X, Li Y, Wang W, Katze MG, Su B, Nielsen R, Yang H, Wang J, Wang X, Wang J (2011) Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nat Biotechnol 29:1019–1023CrossRefPubMedGoogle Scholar
  74. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefPubMedGoogle Scholar
  75. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedPubMedCentralGoogle Scholar
  76. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118CrossRefPubMedGoogle Scholar
  77. Zhang YE, Long M (2014) New genes contribute to genetic and phenotypic novelties in human evolution. Curr Opin Genet Dev 29:90–96CrossRefPubMedPubMedCentralGoogle Scholar
  78. Zhao Q, Caballero OL, Simpson AJ, Strausberg RL (2012) Differential evolution of MAGE genes based on expression pattern and selection pressure. PLoS ONE 7:e48240CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyUniversity of North CarolinaChapel HillUSA
  2. 2.Laboratories for Reproductive Biology, Department of Pediatrics, Lineberger Comprehensive Cancer Center, and Department of Biochemistry and BiophysicsUniversity of North CarolinaChapel HillUSA

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