Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 6/2017

Open Access 01-06-2017 | Review Article

Imaging the DNA damage response with PET and SPECT

Authors: James C. Knight, Sofia Koustoulidou, Bart Cornelissen

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 6/2017

Login to get access

Abstract

DNA integrity is constantly challenged by endogenous and exogenous factors that can alter the DNA sequence, leading to mutagenesis, aberrant transcriptional activity, and cytotoxicity. Left unrepaired, damaged DNA can ultimately lead to the development of cancer. To overcome this threat, a series of complex mechanisms collectively known as the DNA damage response (DDR) are able to detect the various types of DNA damage that can occur and stimulate the appropriate repair process. Each DNA damage repair pathway leads to the recruitment, upregulation, or activation of specific proteins within the nucleus, which, in some cases, can represent attractive targets for molecular imaging. Given the well-established involvement of DDR during tumorigenesis and cancer therapy, the ability to monitor these repair processes non-invasively using nuclear imaging techniques may facilitate the earlier detection of cancer and may also assist in monitoring response to DNA damaging treatment. This review article aims to provide an overview of recent efforts to develop PET and SPECT radiotracers for imaging of DNA damage repair proteins.
Literature
5.
8.
go back to reference Koorstra JBM, Hong SM, Shi C, Meeker AK, Ryu JK, Offerhaus GJA, et al. Widespread activation of the DNA damage response in human pancreatic intraepithelial neoplasia. Modern Pathol. 2009;22(11):1439–45. doi:10.1038/modpathol.2009.114.CrossRef Koorstra JBM, Hong SM, Shi C, Meeker AK, Ryu JK, Offerhaus GJA, et al. Widespread activation of the DNA damage response in human pancreatic intraepithelial neoplasia. Modern Pathol. 2009;22(11):1439–45. doi:10.​1038/​modpathol.​2009.​114.CrossRef
9.
go back to reference Kshirsagar M, Jiang W, Shih IM. DNA damage response is prominent in ovarian high-grade serous carcinomas, especially those with Rsf-1 (HBXAP) overexpression. J Oncol. 2012. doi:10.1155/2012/621685.PubMed Kshirsagar M, Jiang W, Shih IM. DNA damage response is prominent in ovarian high-grade serous carcinomas, especially those with Rsf-1 (HBXAP) overexpression. J Oncol. 2012. doi:10.​1155/​2012/​621685.PubMed
10.
go back to reference Matsuda Y, Wakai T, Kubota M, Osawa M, Takamura M, Yamagiwa S et al. DNA damage sensor γ-H2AX is increased in preneoplastic lesions of hepatocellular carcinoma. Scientific World J. 2013;2013. doi:10.1155/2013/597095. Matsuda Y, Wakai T, Kubota M, Osawa M, Takamura M, Yamagiwa S et al. DNA damage sensor γ-H2AX is increased in preneoplastic lesions of hepatocellular carcinoma. Scientific World J. 2013;2013. doi:10.​1155/​2013/​597095.
11.
go back to reference Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JHJ. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15(7):465–81. doi:10.1038/nrm3822.PubMedCrossRef Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JHJ. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15(7):465–81. doi:10.​1038/​nrm3822.PubMedCrossRef
12.
go back to reference Gorgoulis VG, Vassiliou LVF, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature. 2005;434(7035):907–13. doi:10.1038/nature03485.PubMedCrossRef Gorgoulis VG, Vassiliou LVF, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature. 2005;434(7035):907–13. doi:10.​1038/​nature03485.PubMedCrossRef
13.
go back to reference Sedelnikova OA, Bonner WM. γH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle. 2006;5(24):2909–13.PubMedCrossRef Sedelnikova OA, Bonner WM. γH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle. 2006;5(24):2909–13.PubMedCrossRef
16.
go back to reference Dexheimer ST. DNA repair pathways and mechanisms. In: Mathews AL, Cabarcas MS, Hurt ME, editors. DNA Repair of Cancer Stem Cells. Dordrecht: Springer Netherlands; 2013. p. 19–32.CrossRef Dexheimer ST. DNA repair pathways and mechanisms. In: Mathews AL, Cabarcas MS, Hurt ME, editors. DNA Repair of Cancer Stem Cells. Dordrecht: Springer Netherlands; 2013. p. 19–32.CrossRef
23.
26.
go back to reference Virág L, Szabó C. The therapeutic potential of poly(ADP-Ribose) polymerase inhibitors. Pharmacol Rev. 2002;54(3):375–429.PubMedCrossRef Virág L, Szabó C. The therapeutic potential of poly(ADP-Ribose) polymerase inhibitors. Pharmacol Rev. 2002;54(3):375–429.PubMedCrossRef
37.
go back to reference Bièche I, De Murcia G, Lidereau R. Poly(ADP-ribose) polymerase gene expression status and genomic instability in human breast cancer. Clin Cancer Res. 1996;2(7):1163–7.PubMed Bièche I, De Murcia G, Lidereau R. Poly(ADP-ribose) polymerase gene expression status and genomic instability in human breast cancer. Clin Cancer Res. 1996;2(7):1163–7.PubMed
38.
go back to reference Rojo F, García-Parra J, Zazo S, Tusquets I, Ferrer-Lozano J, Menendez S, et al. Nuclear PARP-1 protein overexpression is associated with poor overall survival in early breast cancer. Ann Oncol. 2012;23(5):1156–64. doi:10.1093/annonc/mdr361.PubMedCrossRef Rojo F, García-Parra J, Zazo S, Tusquets I, Ferrer-Lozano J, Menendez S, et al. Nuclear PARP-1 protein overexpression is associated with poor overall survival in early breast cancer. Ann Oncol. 2012;23(5):1156–64. doi:10.​1093/​annonc/​mdr361.PubMedCrossRef
39.
go back to reference Alanazi M, Pathan AAK, Abduljaleel Z. Association between PARP-1 V762A polymorphism and breast cancer susceptibility in Saudi population. PLoS One. 2013;3:92360. Alanazi M, Pathan AAK, Abduljaleel Z. Association between PARP-1 V762A polymorphism and breast cancer susceptibility in Saudi population. PLoS One. 2013;3:92360.
40.
go back to reference Galia A, Calogero AE, Condorelli R, Fraggetta F, La Corte A, Ridolfo F et al. PARP-1 protein expression in glioblastoma multiforme. Eur J Histochem. 2012;56(1). Galia A, Calogero AE, Condorelli R, Fraggetta F, La Corte A, Ridolfo F et al. PARP-1 protein expression in glioblastoma multiforme. Eur J Histochem. 2012;56(1).
41.
go back to reference Barton VN, Donson AM, Kleinschmidt-DeMasters BK, Gore L, Liu AK, Foreman NK. PARP1 expression in pediatric central nervous system tumors. Pediatr Blood Cancer. 2009;53(7):1227–30. doi:10.1002/pbc.22141.PubMedCrossRef Barton VN, Donson AM, Kleinschmidt-DeMasters BK, Gore L, Liu AK, Foreman NK. PARP1 expression in pediatric central nervous system tumors. Pediatr Blood Cancer. 2009;53(7):1227–30. doi:10.​1002/​pbc.​22141.PubMedCrossRef
42.
43.
go back to reference Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27(3):247–54.PubMedCrossRef Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27(3):247–54.PubMedCrossRef
44.
go back to reference McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet. 2007;8:37–55.PubMedCrossRef McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet. 2007;8:37–55.PubMedCrossRef
45.
go back to reference Cerbinskaite A, Mukhopadhyay A, Plummer ER, Curtin NJ, Edmondson RJ. Defective homologous recombination in human cancers. Cancer Treat Rev. 2012;38(2):89–100.PubMedCrossRef Cerbinskaite A, Mukhopadhyay A, Plummer ER, Curtin NJ, Edmondson RJ. Defective homologous recombination in human cancers. Cancer Treat Rev. 2012;38(2):89–100.PubMedCrossRef
46.
go back to reference Krajewska M, Fehrmann RSN, De Vries EGE, van Vugt MATM. Regulators of homologous recombination repair as novel targets for cancer treatment. Front Genet. 2015;6:1–15.CrossRef Krajewska M, Fehrmann RSN, De Vries EGE, van Vugt MATM. Regulators of homologous recombination repair as novel targets for cancer treatment. Front Genet. 2015;6:1–15.CrossRef
47.
go back to reference Helleday T. Homologous recombination in cancer development, treatment and development of drug resistance. Carcinogenesis. 2010;31(6):955–60.PubMedCrossRef Helleday T. Homologous recombination in cancer development, treatment and development of drug resistance. Carcinogenesis. 2010;31(6):955–60.PubMedCrossRef
48.
go back to reference Renkawitz J, Lademann CA, Jentsch S. Mechanisms and principles of homology search during recombination. Nat Rev Mol Cell Biol. 2014;15(6):369–83.PubMedCrossRef Renkawitz J, Lademann CA, Jentsch S. Mechanisms and principles of homology search during recombination. Nat Rev Mol Cell Biol. 2014;15(6):369–83.PubMedCrossRef
50.
51.
go back to reference Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature. 2007;449(7161):478–82.PubMedCrossRef Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature. 2007;449(7161):478–82.PubMedCrossRef
52.
go back to reference Kuo LJ, Yang L-X. γ-H2AX - A novel biomarker for DNA double-strand breaks. In Vivo. 2008;22(3):305–9.PubMed Kuo LJ, Yang L-X. γ-H2AX - A novel biomarker for DNA double-strand breaks. In Vivo. 2008;22(3):305–9.PubMed
53.
go back to reference Sharma A, Singh K, Almasan A. Histone H2AX phosphorylation: a marker for DNA damage. In: Bjergbæk L, editor. DNA Repair Protocols. Totowa: Humana Press; 2012. p. 613–26.CrossRef Sharma A, Singh K, Almasan A. Histone H2AX phosphorylation: a marker for DNA damage. In: Bjergbæk L, editor. DNA Repair Protocols. Totowa: Humana Press; 2012. p. 613–26.CrossRef
54.
go back to reference Shah K, Boghozian RA, Kartsonaki C, Shah KA, Vallis KA. γH2AX expression in cytological specimens as a biomarker of response to radiotherapy in solid malignancies. Diagn Cytopathol. 2016;44(2):141–6. doi:10.1002/dc.23396.PubMedCrossRef Shah K, Boghozian RA, Kartsonaki C, Shah KA, Vallis KA. γH2AX expression in cytological specimens as a biomarker of response to radiotherapy in solid malignancies. Diagn Cytopathol. 2016;44(2):141–6. doi:10.​1002/​dc.​23396.PubMedCrossRef
55.
go back to reference Banáth JP, Olive PL. Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res. 2003;63(15):4347–50.PubMed Banáth JP, Olive PL. Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res. 2003;63(15):4347–50.PubMed
58.
go back to reference Mah LJ, El-Osta A, Karagiannis TC. [gamma]H2AX: a sensitive molecular marker of DNA damage and repair. Leukemia. 2010;24(4):679–86.PubMedCrossRef Mah LJ, El-Osta A, Karagiannis TC. [gamma]H2AX: a sensitive molecular marker of DNA damage and repair. Leukemia. 2010;24(4):679–86.PubMedCrossRef
59.
go back to reference Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates 3rd JR, et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science. 2004;306(5704):2084–7.PubMedCrossRef Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates 3rd JR, et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science. 2004;306(5704):2084–7.PubMedCrossRef
62.
go back to reference Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene. 2007;26(56):7773–9.PubMedCrossRef Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene. 2007;26(56):7773–9.PubMedCrossRef
64.
go back to reference Cedervall B, Wong R, Albright N, Dynlacht J, Lambin P, Dewey WC. Methods for the quantification of DNA double-strand breaks determined from the distribution of DNA fragment sizes measured by pulsed-field gel electrophoresis. Radiat Res. 1995;143(1):8–16. doi:10.2307/3578920.PubMedCrossRef Cedervall B, Wong R, Albright N, Dynlacht J, Lambin P, Dewey WC. Methods for the quantification of DNA double-strand breaks determined from the distribution of DNA fragment sizes measured by pulsed-field gel electrophoresis. Radiat Res. 1995;143(1):8–16. doi:10.​2307/​3578920.PubMedCrossRef
66.
go back to reference Collins AR. The comet assay for DNA damage and repair: Principles, applications, and limitations. Appl Biochem Biotech - Part B Mol Biotech. 2004;26(3):249–61. doi:10.1385/MB:26:3:249. Collins AR. The comet assay for DNA damage and repair: Principles, applications, and limitations. Appl Biochem Biotech - Part B Mol Biotech. 2004;26(3):249–61. doi:10.​1385/​MB:​26:​3:​249.
68.
go back to reference Löbrich M, Shibata A, Beucher A, Fisher A, Ensminger M, Goodarzi AA, et al. γH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle. 2010;9(4):662–9.PubMedCrossRef Löbrich M, Shibata A, Beucher A, Fisher A, Ensminger M, Goodarzi AA, et al. γH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle. 2010;9(4):662–9.PubMedCrossRef
70.
go back to reference Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol. 1995;5(6):635–42.PubMedCrossRef Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol. 1995;5(6):635–42.PubMedCrossRef
79.
go back to reference Edmonds CE, Makvandi M, Lieberman BP, Xu K, Zeng C, Li S, et al. [18F]FluorThanatrace uptake as a marker of PARP1 expression and activity in breast cancer. Am J Nucl Med Mol Imaging. 2016;6(1):94–101.PubMedPubMedCentral Edmonds CE, Makvandi M, Lieberman BP, Xu K, Zeng C, Li S, et al. [18F]FluorThanatrace uptake as a marker of PARP1 expression and activity in breast cancer. Am J Nucl Med Mol Imaging. 2016;6(1):94–101.PubMedPubMedCentral
82.
go back to reference Reiner T, Keliher EJ, Earley S, Marinelli B, Weissleder R. Synthesis and in vivo imaging of a 18F-labeled PARP1 inhibitor using a chemically orthogonal scavenger-assisted high-performance method. Angew Chem Int Ed. 2011;50(8):1922–5. doi:10.1002/anie.201006579.CrossRef Reiner T, Keliher EJ, Earley S, Marinelli B, Weissleder R. Synthesis and in vivo imaging of a 18F-labeled PARP1 inhibitor using a chemically orthogonal scavenger-assisted high-performance method. Angew Chem Int Ed. 2011;50(8):1922–5. doi:10.​1002/​anie.​201006579.CrossRef
83.
go back to reference Reiner T, Lacy J, Keliher EJ, Yang KS, Ullal A, Kohler RH, et al. Imaging therapeutic PARP inhibition in vivo through bioorthogonally developed companion imaging agents. Neoplasia. 2012;14:169–77.PubMedPubMedCentralCrossRef Reiner T, Lacy J, Keliher EJ, Yang KS, Ullal A, Kohler RH, et al. Imaging therapeutic PARP inhibition in vivo through bioorthogonally developed companion imaging agents. Neoplasia. 2012;14:169–77.PubMedPubMedCentralCrossRef
84.
go back to reference Riss PJ, Soskic V, Schrattenholz A, Roescha F. Synthesis and radiosynthesis of N5-[18F]fluoroethyl- Pirenzepine and its metabolite N5-[18F]fluoroethyl-LS 75. J Labelled Comp Radiopharm. 2009;52(14):576–9. doi:10.1002/jlcr.1687. Riss PJ, Soskic V, Schrattenholz A, Roescha F. Synthesis and radiosynthesis of N5-[18F]fluoroethyl- Pirenzepine and its metabolite N5-[18F]fluoroethyl-LS 75. J Labelled Comp Radiopharm. 2009;52(14):576–9. doi:10.​1002/​jlcr.​1687.
85.
86.
go back to reference Salinas B, Irwin CP, Kossatz S, Bolaender A, Chiosis G, Pillarsetty N et al. Radioiodinated PARP1 tracers for glioblastoma imaging. Eur J Nucl Med Mol Imaging Res. 2015;5(1). doi:10.1186/s13550-015-0123-1. Salinas B, Irwin CP, Kossatz S, Bolaender A, Chiosis G, Pillarsetty N et al. Radioiodinated PARP1 tracers for glioblastoma imaging. Eur J Nucl Med Mol Imaging Res. 2015;5(1). doi:10.​1186/​s13550-015-0123-1.
87.
go back to reference Menear KA, Adcock C, Boulter R, Cockcroft X-L, Copsey L, Cranston A, et al. 4-[3-(4-Cyclopropanecarbonylpiperazine-1-carbonyl)-4-fluorobenzyl]-2H-phthalazin-1-one: a novel bioavailable inhibitor of poly(ADP-ribose) polymerase-1. J Med Chem. 2008;51(20):6581–91. doi:10.1021/jm8001263.PubMedCrossRef Menear KA, Adcock C, Boulter R, Cockcroft X-L, Copsey L, Cranston A, et al. 4-[3-(4-Cyclopropanecarbonylpiperazine-1-carbonyl)-4-fluorobenzyl]-2H-phthalazin-1-one: a novel bioavailable inhibitor of poly(ADP-ribose) polymerase-1. J Med Chem. 2008;51(20):6581–91. doi:10.​1021/​jm8001263.PubMedCrossRef
88.
go back to reference Makvandi M, Xu K, Lieberman BP, Anderson R-C, Effron SS, Winters HD, et al. A radiotracer strategy to quantify PARP-1 expression in vivo provides a biomarker that can enable patient selection for PARP inhibitor therapy. Cancer Res. 2016;76(15):4516.PubMedCrossRef Makvandi M, Xu K, Lieberman BP, Anderson R-C, Effron SS, Winters HD, et al. A radiotracer strategy to quantify PARP-1 expression in vivo provides a biomarker that can enable patient selection for PARP inhibitor therapy. Cancer Res. 2016;76(15):4516.PubMedCrossRef
89.
91.
go back to reference Nelson G, Buhmann M, Von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle. 2009;8(20):3379–83.PubMedCrossRef Nelson G, Buhmann M, Von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle. 2009;8(20):3379–83.PubMedCrossRef
97.
go back to reference Ziegler A, Nervi P, Dürrenberger M, Seelig J. The cationic cell-penetrating peptide CPPTAT derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: optical, biophysical, and metabolic evidence. Biochemistry. 2005;44(1):138–48. doi:10.1021/bi0491604.PubMedCrossRef Ziegler A, Nervi P, Dürrenberger M, Seelig J. The cationic cell-penetrating peptide CPPTAT derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: optical, biophysical, and metabolic evidence. Biochemistry. 2005;44(1):138–48. doi:10.​1021/​bi0491604.PubMedCrossRef
100.
go back to reference Pan L, He Q, Liu J, Chen Y, Ma M, Zhang L, et al. Nuclear-targeted drug delivery of TAT peptide-conjugated monodisperse mesoporous silica nanoparticles. J Am Chem Soc. 2012;134(13):5722–5. doi:10.1021/ja211035w.PubMedCrossRef Pan L, He Q, Liu J, Chen Y, Ma M, Zhang L, et al. Nuclear-targeted drug delivery of TAT peptide-conjugated monodisperse mesoporous silica nanoparticles. J Am Chem Soc. 2012;134(13):5722–5. doi:10.​1021/​ja211035w.PubMedCrossRef
101.
go back to reference Torchilin VP, Rammohan R, Weissig V, Levchenko TS. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc Natl Acad Sci U S A. 2001;98(15):8786–91. doi:10.1073/pnas.151247498.PubMedPubMedCentralCrossRef Torchilin VP, Rammohan R, Weissig V, Levchenko TS. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc Natl Acad Sci U S A. 2001;98(15):8786–91. doi:10.​1073/​pnas.​151247498.PubMedPubMedCentralCrossRef
102.
go back to reference Pang H-B, Braun GB, Ruoslahti E. Neuropilin-1 and heparan sulfate proteoglycans cooperate in cellular uptake of nanoparticles functionalized by cationic cell-penetrating peptides. Sci Adv. 2015;1(10). doi:10.1126/sciadv.1500821. Pang H-B, Braun GB, Ruoslahti E. Neuropilin-1 and heparan sulfate proteoglycans cooperate in cellular uptake of nanoparticles functionalized by cationic cell-penetrating peptides. Sci Adv. 2015;1(10). doi:10.​1126/​sciadv.​1500821.
103.
go back to reference Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. (0021–9258 (Print)). Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. (0021–9258 (Print)).
105.
106.
go back to reference Ferrari A, Pellegrini V, Arcangeli C, Fittipaldi A, Giacca M, Beltram F. Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol Ther. 2003;8(2):284–94.PubMedCrossRef Ferrari A, Pellegrini V, Arcangeli C, Fittipaldi A, Giacca M, Beltram F. Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol Ther. 2003;8(2):284–94.PubMedCrossRef
109.
111.
112.
go back to reference Knight JC, Topping C, Mosley M, Kersemans V, Falzone N, Fernández-Varea JM, et al. PET imaging of DNA damage using 89Zr-labelled anti-γH2AX-TAT immunoconjugates. Eur J Nucl Med Mol Imaging. 2015;42(11):1707–17. doi:10.1007/s00259-015-3092-8.PubMedCrossRef Knight JC, Topping C, Mosley M, Kersemans V, Falzone N, Fernández-Varea JM, et al. PET imaging of DNA damage using 89Zr-labelled anti-γH2AX-TAT immunoconjugates. Eur J Nucl Med Mol Imaging. 2015;42(11):1707–17. doi:10.​1007/​s00259-015-3092-8.PubMedCrossRef
113.
114.
go back to reference Cornelissen B, Waller A, Able S, Vallis KA. Molecular radiotherapy using cleavable radioimmunoconjugates that target eGFR and γH2AX. Mol Cancer Ther. 2013;12(11):2472–82. doi:10.1158/1535-7163.PubMedCrossRef Cornelissen B, Waller A, Able S, Vallis KA. Molecular radiotherapy using cleavable radioimmunoconjugates that target eGFR and γH2AX. Mol Cancer Ther. 2013;12(11):2472–82. doi:10.​1158/​1535-7163.PubMedCrossRef
116.
go back to reference Knight JC, Cornelissen B. Bioorthogonal chemistry: implications for pretargeted nuclear (PET/SPECT) imaging and therapy. Am J Nucl Med Mol Imaging. 2014;4(2):96–113.PubMedPubMedCentral Knight JC, Cornelissen B. Bioorthogonal chemistry: implications for pretargeted nuclear (PET/SPECT) imaging and therapy. Am J Nucl Med Mol Imaging. 2014;4(2):96–113.PubMedPubMedCentral
Metadata
Title
Imaging the DNA damage response with PET and SPECT
Authors
James C. Knight
Sofia Koustoulidou
Bart Cornelissen
Publication date
01-06-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 6/2017
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-016-3604-1

Other articles of this Issue 6/2017

European Journal of Nuclear Medicine and Molecular Imaging 6/2017 Go to the issue