Nuclear Medicine and Biology
Volume 37, Issue 4 , Pages 395-404 , May 2010

Copper-64-diacetyl-bis (N4-methylthiosemicarbazone) accumulates in rich regions of CD133+ highly tumorigenic cells in mouse colon carcinoma

  • Yukie Yoshii

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Takako Furukawa

      Affiliations

    • Molecular Imaging Center, National Institute of Radiological Sciences, Inage, Chiba 263-8555, Japan
    • ,
  • Yasushi Kiyono

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Ryo Watanabe

      Affiliations

    • Faculty of Engineering, University of Fukui, Eiheiji, Fukui 910-8507, Japan
    • ,
  • Atsuo Waki

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Tetsuya Mori

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, Missouri 63110, USA
    • ,
  • Hiroshi Yoshii

      Affiliations

    • Faculty of Medical Sciences, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Myungmi Oh

      Affiliations

    • Faculty of Medical Sciences, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Tatsuya Asai

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • Faculty of Engineering, University of Fukui, Eiheiji, Fukui 910-8507, Japan
    • ,
  • Hidehiko Okazawa

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • ,
  • Michael J. Welch

      Affiliations

    • Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, Missouri 63110, USA
    • ,
  • Yasuhisa Fujibayashi

      Affiliations

    • Biomedical Imaging Research Center, University of Fukui, Eiheiji, Fukui 910-1193, Japan
    • Molecular Imaging Center, National Institute of Radiological Sciences, Inage, Chiba 263-8555, Japan
    • Corresponding Author InformationCorresponding author. Biomedical Imaging Research Center, University of Fukui, Shimoaizuki, Eiheiji, Fukui 910-1193, Japan. Tel.: +81 776 61 8491; fax: +81 776 61 8170.

Received 13 November 2009 ,Revised 23 December 2009 ,Accepted 29 December 2009.

References 

  1. Brown JM. The hypoxic cell: a target for selective cancer therapy—eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res. 1999;59:5863–5870
  2. Padhani AR, Krohn KA, Lewis JS, Alber M. Imaging oxygenation of human tumours. Eur Radiol. 2007;17:861–872
  3. Dehdashti F, Grigsby PW, Mintun MA, Lewis JS, Siegel BA, Welch MJ. Assessing tumor hypoxia in cervical cancer by positron emission tomography with 60Cu-ATSM: relationship to therapeutic response-a preliminary report. Int J Radiat Oncol Biol Phys. 2003;55:1233–1238
  4. Dehdashti F, Mintun MA, Lewis JS, Bradley J, Govindan R, Laforest R. In vivo assessment of tumor hypoxia in lung cancer with 60Cu-ATSM. Eur J Nucl Med Mol Imaging. 2003;30:844–850
  5. Fujibayashi Y, Taniuchi H, Yonekura Y, Ohtani H, Konishi J, Yokoyama A. Copper-62-ATSM: a new hypoxia imaging agent with high membrane permeability and low redox potential. J Nucl Med. 1997;38:1155–1160
  6. Lewis JS, McCarthy DW, McCarthy TJ, Fujibayashi Y, Welch MJ. Evaluation of 64Cu-ATSM in vitro and in vivo in a hypoxic tumor model. J Nucl Med. 1999;40:177–183
  7. Lewis JS, Sharp TL, Laforest R, Fujibayashi Y, Welch MJ. Tumor uptake of copper-diacetyl-bis(N4-methylthiosemicarbazone): effect of changes in tissue oxygenation. J Nucl Med. 2001;42:655–661
  8. Takahashi N, Fujibayashi Y, Yonekura Y, Welch MJ, Waki A, Tsuchida T, et al. Evaluation of 62Cu labeled diacetyl-bis(N4-methylthiosemicarbazone) as a hypoxic tissue tracer in patients with lung cancer. Ann Nucl Med. 2000;14:323–328
  9. Tanaka T, Furukawa T, Fujieda S, Kasamatsu S, Yonekura Y, Fujibayashi Y. Double-tracer autoradiography with Cu-ATSM/FDG and immunohistochemical interpretation in four different mouse implanted tumor models. Nucl Med Biol. 2006;33:743–750
  10. Obata A, Kasamatsu S, McCarthy DW, Welch MJ, Saji H, Yonekura Y, et al. Production of therapeutic quantities of 64Cu using a 12 MeV cyclotron. Nucl Med Biol. 2003;30:535–539
  11. Burgman P, O'Donoghue JA, Lewis JS, Welch MJ, Humm JL, Ling CC. Cell line-dependent differences in uptake and retention of the hypoxia-selective nuclear imaging agent Cu-ATSM. Nucl Med Biol. 2005;32:623–630
  12. Obata A, Kasamatsu S, Lewis JS, Furukawa T, Takamatsu S, Toyohara J, et al. Basic characterization of 64Cu-ATSM as a radiotherapy agent. Nucl Med Biol. 2005;32:21–28
  13. Dehdashti F, Grigsby PW, Lewis JS, Laforest R, Siegel BA, Welch MJ. Assessing tumor hypoxia in cervical cancer by PET with 60Cu-labeled diacetyl-bis(N4-methylthiosemicarbazone). J Nucl Med. 2008;49:201–205
  14. Grigsby PW, Malyapa RS, Higashikubo R, Schwarz JK, Welch MJ, Huettner PC. Comparison of molecular markers of hypoxia and imaging with 60Cu-ATSM in cancer of the uterine cervix. Mol Imaging Biol. 2007;9:278–283
  15. Dietz DW, Dehdashti F, Grigsby PW, Malyapa RS, Myerson RJ, Picus J, et al. Tumor hypoxia detected by positron emission tomography with 60Cu-ATSM as a predictor of response and survival in patients undergoing neoadjuvant chemoradiotherapy for rectal carcinoma: a pilot study. Dis Colon Rectum. 2008;51:1641–1648
  16. Obata A, Yoshimi E, Waki A, Lewis JS, Oyama N, Welch MJ, et al. Retention mechanism of hypoxia selective nuclear imaging/radiotherapeutic agent Cu-diacetyl-bis(N4-methylthiosemicarbazone) (Cu-ATSM) in tumor cells. Ann Nucl Med. 2001;15:499–504
  17. Dearling JL, Lewis JS, Mullen GE, Welch MJ, Blower PJ. Copper bis(thiosemicarbazone) complexes as hypoxia imaging agents: structure–activity relationships. J Biol Inorg Chem. 2002;7:249–259
  18. Holland JP, Giansiracusa JH, Bell SG, Wong LL, Dilworth JR. In vitro kinetic studies on the mechanism of oxygen-dependent cellular uptake of copper radiopharmaceuticals. Phys Med Biol. 2009;54:2103–2119
  19. Obata A, Yoshimoto M, Kasamatsu S, Naiki H, Takamatsu S, Kashikura K, et al. Intra-tumoral distribution of 64Cu-ATSM: a comparison study with FDG. Nucl Med Biol. 2003;30:529–534
  20. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med. 2006;355:1253–1261
  21. Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea—a paradigm shift. Cancer Res. 2006;66:1883–1890discussion 95-6
  22. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760
  23. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67
  24. Blazek ER, Foutch JL, Maki G. Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133− cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys. 2007;67:1–5
  25. Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR, et al. CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE. 2008;e3655:3
  26. Tavaluc RT, Hart LS, Dicker DT, El-Deiry WS. Effects of low confluency, serum starvation and hypoxia on the side population of cancer cell lines. Cell Cycle. 2007;6:2554–2562
  27. Zhou J, Zhang Y. Cancer stem cells: models, mechanisms and implications for improved treatment. Cell Cycle. 2008;7:1360–1370
  28. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–10951
  29. Ieta K, Tanaka F, Haraguchi N, Kita Y, Sakashita H, Mimori K, et al. Biological and genetic characteristics of tumor-initiating cells in colon cancer. Ann Surg Oncol. 2008;15:638–648
  30. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–110
  31. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–115
  32. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–5828
  33. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401
  34. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–824
  35. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24− and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res. 2008;10:R10
  36. Dallas NA, Xia L, Fan F, Gray MJ, Gaur P, van Buren G, et al. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res. 2009;69:1951–1957
  37. Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, et al. CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer. 2008;98:1389–1397
  38. Mehra N, Penning M, Maas J, Beerepoot LV, van Daal N, van Gils CH, et al. Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases. Clin Cancer Res. 2006;12:4859–4866
  39. McCarthy DW, Shefer RE, Klinkowstein RE, Bass LA, Margeneau WH, Cutler CS, et al. Efficient production of high specific activity 64Cu using a biomedical cyclotron. Nucl Med Biol. 1997;24:35–43
  40. Hamacher K, Coenen HH, Stocklin G. Efficient stereospecific synthesis of no-carrier-added 2-[18F]-fluoro-2-deoxy-d-glucose using aminopolyether supported nucleophilic substitution. J Nucl Med. 1986;27:235–238
  41. Oh M, Tanaka T, Kobayashi M, Furukawa T, Mori T, Kudo T, et al. Radio-copper-labeled Cu-ATSM: an indicator of quiescent but clonogenic cells under mild hypoxia in a Lewis lung carcinoma model. Nucl Med Biol. 2009;36:419–426
  42. Fujibayashi Y, Cutler CS, Anderson CJ, McCarthy DW, Jones LA, Sharp T, et al. Comparative studies of Cu-64-ATSM and C-11-acetate in an acute myocardial infarction model: ex vivo imaging of hypoxia in rats. Nucl Med Biol. 1999;26:117–121
  43. Park CH, Bergsagel DE, McCulloch EA. Mouse myeloma tumor stem cells: a primary cell culture assay. J Natl Cancer Inst. 1971;46:411–422
  44. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–111
  45. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov. 2009;8:806–823
  46. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science. 2007;317:337
  47. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells. 2008;26:1818–1830
  48. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133− metastatic colon cancer cells initiate tumors. J Clin Invest. 2008;118:2111–2120

☆ This work was supported in part by the Grants-in-Aid for Young Scientists (B) from the Japan Society for the Promotion of Science, Japan (JSPS) (to Y.Y.); the Joint Research Grant from the Wakasa Wan Energy Research Center, Japan (to Y.F. and Y.Y.); the Research for Promoting Technological Seeds from Japan Science and Technology Agency, Japan (to Y.Y.); the 21st Century Centers of Excellence (COE) program from the JSPS (to Y.F.); and the Grant-in-Aid for Tumor Research from the Ministry of Health, Labor and Welfare, Japan 15-2 (to Y.F.).

PII: S0969-8051(09)00301-1

doi: 10.1016/j.nucmedbio.2009.12.011

Nuclear Medicine and Biology
Volume 37, Issue 4 , Pages 395-404 , May 2010

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