Skip to main content
SpringerLink
Log in

Apoptosis imaging by radionuclide probes

  • Original Paper
  • Published:
Journal of the Iranian Chemical Society Aims and scope Submit manuscript

Abstract

Apoptosis has attracted more and more research interests due to the critical role it played in the human health. Also, it is often confused with other types of cell death. Thus, methods that enable sensitive detection and noninvasive visualized imaging of apoptosis will be of enormous benefit in the development of new diagnostics, therapies and patient management. During the past decades, with the development of apoptosis understanding and molecular imaging modalities, a large collection of imaging agents based on well-defined molecular markers and/or physiological features have been developed and tested in preclinical and clinical studies. In this review, we mainly discuss radionuclide imaging probes, ranging from simple attachments of reporter moieties to proteins and peptides, to rationally designed probes that allow multimodal imaging. Furthermore, we briefly outline the current status of clinical translation and attempt to give an outlook on the further study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. J. Yin, P. Miao, Chem. Asian J. 11, 632 (2016)

    Article  CAS  Google Scholar 

  2. C.J. Norbury, I.D. Hickson, Annu. Rev. Pharmacol. Toxicol. 41, 367 (2001)

    Article  CAS  Google Scholar 

  3. C.B. Thompson, Science 267, 1456 (1995)

    Article  CAS  Google Scholar 

  4. G.I. Evan, K.H. Vousden, Nature 411, 342 (2001)

    Article  CAS  Google Scholar 

  5. W. Zeng, X. Wang, P. Xu, G. Liu, H.S. Eden, X. Chen, Theranostics 5, 559 (2015)

    Article  CAS  Google Scholar 

  6. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, A.B. Hjelmeland, M.W. Dewhirst, D.D. Bigner, J.N. Rich, Nature 444, 756 (2006)

    Article  CAS  Google Scholar 

  7. J.R. Starkey, A.K. Rebane, M.A. Drobizhev, F. Meng, A. Gong, A. Elliott, K. McInnerney, C.W. Spangler, Clin. Cancer Res. 14, 6564 (2008)

    Article  CAS  Google Scholar 

  8. L. Zhang, X. Ren, E. Alt, X. Bai, S. Huang, Z. Xu, P.M. Lynch, M.P. Moyer, X.F. Wen, X. Wu, Nature 464, 1058 (2010)

    Article  CAS  Google Scholar 

  9. E.E. Creppy, A. Diallo, S. Moukha, C. Eklu-Gadegbeku, D. Cros, Int. J. Environ. Res. Public Health 11, 8069 (2014)

    Article  CAS  Google Scholar 

  10. S. Gannavaram, A. Debrabant, Front. Cell. Infect. Microbiol. 2, 95 (2012)

    Article  Google Scholar 

  11. G.L. Størvold, J. Landskron, M. Strozynski, M.O. Arntzen, C.J. Koehler, M.E. Kalland, K. Tasken, B. Thiede, J. Proteomics 91, 344 (2013)

    Article  Google Scholar 

  12. X. Yu, D. Acehan, J.F. Ménétret, C.R. Booth, S.J. Ludtke, S.J. Riedl, Y. Shi, X. Wang, C.W. Akey, Structure 13, 1725 (2005)

    Article  CAS  Google Scholar 

  13. L. Bouchier-Hayes, C. Munoz-Pinedo, S. Connell, D.R. Green, Methods 44, 222 (2008)

    Article  CAS  Google Scholar 

  14. Y. Min, J. Li, F. Liu, E.K. Yeow, B. Xing, Angew. Chem. Int. Ed. 53, 1012 (2014)

    Article  CAS  Google Scholar 

  15. Y.L. Pan, M.L. Guo, Z. Nie, Y. Huang, Y. Peng, A.F. Liu, M. Qing, S.Z. Yao, Chem. Commun. 48, 997 (2012)

    Article  CAS  Google Scholar 

  16. J.M. Hakumäki, T. Liimatainen, Eur. J. Radiol. 56, 143 (2005)

    Article  Google Scholar 

  17. G. Sugiura, H. Kühn, M. Sauter, U. Haberkorn, W. Mier, Molecules 19, 2135 (2014)

    Article  Google Scholar 

  18. M.B. Tanzola, G.J. Kersh, Mol. Immunol. 43, 754 (2006)

    Article  CAS  Google Scholar 

  19. V. Gerke, S.E. Moss, Physiol. Rev. 82, 331 (2002)

    Article  CAS  Google Scholar 

  20. C.M. Lahorte, J.L. Vanderheyden, N. Steinmetz, C. van de Wiele, R.A. Dierckx, G. Slegers, Eur. J. Nucl. Med. Mol. Imaging 31, 887 (2004)

    Article  CAS  Google Scholar 

  21. G.J. Kemerink, H.H. Boersma, P.W. Thimister, L. Hofstra, I.H. Liem, M.T. Pakbiers, D. Janssen, C.P. Reutelingsperger, G.A. Heidendal, Eur. J. Nucl. Med. 28, 1373 (2001)

    Article  CAS  Google Scholar 

  22. J.L. Vanderheyden, G. Liu, J. He, B. Patel, J.F. Tait, D.J. Hnatowich, Nucl. Med. Biol. 33, 135 (2006)

    Article  CAS  Google Scholar 

  23. M.J. Abrams, M. Juweid, C.I. tenKate, D.A. Schwartz, M.M. Hauser, F.E. Gaul, A.J. Fuccello, R.H. Rubin, H.W. Strauss, A.J. Fischman, J. Nucl. Med. 31, 2022 (1990)

    CAS  Google Scholar 

  24. F.G. Blankenberg, P.D. Katsikis, J.F. Tait, R.E. Davis, L. Naumovski, K. Ohtsuki, S. Kopiwoda, M.J. Abrams, M. Darkes, R.C. Robbins, H.T. Maecker, H.W. Strauss, Proc. Natl. Acad. Sci. U S A 95, 6349 (1998)

    Article  CAS  Google Scholar 

  25. M. Kartachova, N. van Zandwijk, S. Burgers, H. van Tinteren, M. Verheij, R.A. Valdés Olmos, J. Clin. Oncol. 25, 2534 (2007)

    Article  CAS  Google Scholar 

  26. M.S. Kartachova, R.A. Valdés Olmos, R.L. Haas, F.J. Hoebers, M. Herk, M. Verheij, Nucl. Med. Commun. 29, 39 (2008)

    Article  Google Scholar 

  27. H. Fonge, M. de Saint Hubert, K. Vunckx, D. Rattat, J. Nuyts, G. Bormans, Y. Ni, C. Reutelingsperger, A. Verbruggen, Bioorg. Med. Chem. Lett. 18, 3794 (2008)

    Article  CAS  Google Scholar 

  28. C. Lu, Q. Jiang, M. Hu, C. Tan, Y. Ji, H. Yu, Z. Hua, Molecules 18, 6908 (2013)

    Article  CAS  Google Scholar 

  29. X. Wen, Q.P. Wu, S. Ke, S. Wallace, C. Charnsangavej, P. Huang, D. Liang, D. Chow, C. Li, Cancer Biother. Radiopharm. 18, 819 (2003)

    Article  CAS  Google Scholar 

  30. S. Ke, X. Wen, Q.P. Wu, S. Wallace, C. Charnsangavej, A.M. Stachowiak, C.L. Stephens, J.L. Abbruzzese, D.A. Podoloff, C. Li, J. Nucl. Med. 45, 108 (2004)

    CAS  Google Scholar 

  31. J. Toretsky, A. Levensona, I.N. Weinberg, J.F. Tait, A. Urena, R.C. Mease, Nucl. Med. Biol. 31, 747 (2004)

    Article  CAS  Google Scholar 

  32. J. Zhu, F. Wang, W. Fang, Z. Hua, Z. Wang, J. Radioanal. Nucl. Chem. 298, 1733 (2013)

    Article  CAS  Google Scholar 

  33. B. de Bruin, B. Kuhnast, F. Hinnen, L. Yaouancq, M. Amessou, L. Johannes, A. Samson, R. Boisgard, B. Tavitian, F. Dollé, Bioconjug. Chem. 16, 406 (2005)

    Article  Google Scholar 

  34. H. Wang, H. Gao, N. Guo, G. Niu, Y. Ma, D.O. Kiesewetter, X. Chen, Theranostics 2, 607 (2012)

    Article  CAS  Google Scholar 

  35. C. Lu, Q. Jiang, M. Hu, C. Tan, H. Yu, Z. Hua, Molecules 20, 4902 (2015)

    Article  CAS  Google Scholar 

  36. M. Bauwens, De M. Saint-Hubert, E. Devos, N. Deckers, C. Reutelingsperger, L. Mortelmans, U. Himmelreich, F.M. Mottaghy, A. Verbruggen, Nucl. Med. Biol. 38, 381 (2011)

    Article  CAS  Google Scholar 

  37. F. Wang, W. Fang, M.R. Zhang, M. Zhao, B. Liu, Z. Wang, Z. Hua, M. Yang, K. Kumata, A. Hatori, T. Yamasaki, K. Yanamoto, K. Suzuki, J. Nucl. Med. 52, 592 (2011)

    Article  CAS  Google Scholar 

  38. R.H. Poulsen, J.T. Rasmussen, J.A. Ejlersen, C. Flø, L. Falborg, C.W. Heegaard, M. Rehling, Ejnmmi Res. 3, 15 (2013)

    Article  Google Scholar 

  39. C. Xiong, K. Brewer, S. Song, R. Zhang, W. Lu, X. Wen, C. Li, J. Med. Chem. 54, 1825 (2011)

    Article  CAS  Google Scholar 

  40. S. Song, C. Xiong, W. Lu, G. Ku, G. Huang, C. Li, J. Nucl. Med. 54, 104 (2013)

    Article  CAS  Google Scholar 

  41. R. Ghidoni, G. Sala, A. Giuliani, Biochim. Biophys. Acta 1439, 17 (1999)

    Article  CAS  Google Scholar 

  42. K. Emoto, N. Toyama-Sorimachi, H. Karasuyama, K. Inoue, M. Umeda, Exp. Cell Res. 232, 430 (1997)

    Article  CAS  Google Scholar 

  43. F. Hayashi, K. Nagashima, Y. Terui, Y. Kawamura, K. Matsumoto, H. Itazaki, J. Antibiot. (Tokyo) 43, 1421 (1990)

    Article  CAS  Google Scholar 

  44. N. Zimmermann, S. Freund, A. Fredenhagen, G. Jung, Eur. J. Biochem. 216, 419 (1993)

    Article  CAS  Google Scholar 

  45. M. Zhao, Z. Li, S. Bugenhagen, J. Nucl. Med. 49, 1345 (2008)

    Article  CAS  Google Scholar 

  46. J. Li, J. Yuan, Oncogene 27, 6194 (2008)

    Article  CAS  Google Scholar 

  47. D.W. Nicholson, N.A. Thornberry, Trends Biochem. Sci. 22, 299 (1997)

    Article  CAS  Google Scholar 

  48. H. Su, G. Chen, U. Gangadharmath, L.F. Gomez, Q. Liang, F. Mu, V.P. Mocharla, A.K. Szardenings, J.C. Walsh, C.F. Xia, C. Yu, H.C. Kolb, Mol. Imaging Biol. 15, 739 (2013)

    Article  Google Scholar 

  49. H. Su, N. Gorodny, L.F. Gomez, U. Gangadharmath, F. Mu, G. Chen, J.C. Walsh, K. Szardenings, H.C. Kolb, B. Tamarappoo, Circ. Cardiovasc. Imaging 8, e001952 (2015)

    Article  Google Scholar 

  50. R.G. Hanshaw, B.D. Smith, Bioorg. Med. Chem. 13, 5035 (2005)

    Article  CAS  Google Scholar 

  51. B.A. Smith, S. Xiao, W. Wolter, J. Wheeler, M.A. Suckow, B.D. Smith, Apoptosis 16, 722 (2011)

    Article  Google Scholar 

  52. L. Wyffels, B.D. Gray, C. Barber, S.K. Moore, J.M. Woolfenden, K.Y. Pak, Z. Liu, Bioorg. Med. Chem. 19, 3425 (2011)

    Article  CAS  Google Scholar 

  53. A. Reshef, A. Shirvan, R.N. Waterhouse, H. Grimberg, G. Levin, A. Cohen, L.G. Ulysse, G. Friedman, G. Antoni, I. Ziv, J. Nucl. Med. 49, 1520 (2008)

    Article  CAS  Google Scholar 

  54. J. Höglund, A. Shirvan, G. Antoni, S.Å. Gustavsson, B. Långström, A. Ringheim, J. Sörensen, M. Ben-Ami, I. Ziv, J. Nucl. Med. 52, 720 (2011)

    Article  Google Scholar 

  55. M. Bauwens, De M. Saint-Hubert, J. Cleynhens, L. Brams, E. Devos, F.M. Mottaghy, A. Verbruggen, PLoS ONE 7, 38428 (2012)

    Article  Google Scholar 

  56. M. Torkzadeh-Mahani, F. Ataei, M. Nikkhah, S. Hosseinkhani, Biosens. Bioelectron. 38, 362 (2012)

    Article  CAS  Google Scholar 

  57. Y. Wang, J.T. Chen, X.P. Yan, Anal. Chem. 85, 2529 (2013)

    Article  CAS  Google Scholar 

  58. J.K. Willmann, N. van Bruggen, L.M. Dinkelborg, S.S. Gambhir, Nat. Rev. Drug Discov. 7, 591 (2008)

    Article  CAS  Google Scholar 

  59. H. Lee, W.J. Akers, P.P. Cheney, W.B. Edwards, K. Liang, J.P. Culver, S. Achilefu, J. Biomed. Opt. 14, 040507 (2009)

    Article  Google Scholar 

  60. M. De Saint-Hubert, M. Bauwens, N. Deckers, M. Drummen, K. Douma, P. Granton, G. Hendrikx, D. Kusters, J. Bucerius, C.P. Reutelingsperger, F.M. Mottaghy, Mol. Imaging Biol. 16, 246 (2014)

    Article  CAS  Google Scholar 

  61. R. Zhang, W. Lu, X. Wen, M. Huang, M. Zhou, D. Liang, C. Li, J. Nucl. Med. 52, 958 (2011)

    Article  CAS  Google Scholar 

  62. R. Zhang, M. Huang, M. Zhou, X. Wen, Q. Huang, C. Li, Mol. Imaging 12, 182 (2013)

    CAS  Google Scholar 

  63. F.G. Blankenberg, J. Nucl. Med. 49, S81 (2008)

    Article  Google Scholar 

  64. K. Chen, X. Chen, Curr. Top. Med. Chem. 10, 1227 (2010)

    Article  CAS  Google Scholar 

  65. J. Xie, S. Jon, Theranostics 2, 122 (2012)

    Article  Google Scholar 

  66. M.S. Muthu, D.T. Leong, L. Mei, S.S. Feng, Theranostics 4, 660 (2014)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully appreciate the support from the Natural Science Foundation of Heilongjiang Province (No C201459).

Author information

Authors and Affiliations

  1. Basic Medicine Department, Qiqihar Medical University, Qiqihar, 161006, China

    Chunhui Xia, Zhiqiang Lun, Xiuying Lin & Yu Wang

  2. Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjing, 300070, China

    Baiqi Wang

Authors
  1. Chunhui Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhiqiang Lun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiuying Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baiqi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu Wang.

Ethics declarations

Conflict of interest

The author(s) confirm that this article content has no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xia, C., Lun, Z., Lin, X. et al. Apoptosis imaging by radionuclide probes. J IRAN CHEM SOC 14, 2437–2447 (2017). https://doi.org/10.1007/s13738-017-1178-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13738-017-1178-x

Keywords

Search

Navigation