Whole-body imaging of adoptively transferred T cells using magnetic resonance imaging, single photon emission computed tomography and positron emission tomography techniques, with a focus on regulatory T cells

Clinical and Experimental Immunology

Volumn 172, Issue 2, 2013, Pages 169-177

  Leech, J M ^a   Sharif Paghaleh, E ^a,b   Maher, J ^b   Livieratos, L ^c   Lechler, R I ^a   Mullen, G E ^b   Lombardi, G ^a   Smyth, L A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Regulatory T cells; Whole body imaging

Indexed keywords

CARBON 11; COPPER 64; FLUORINE 18; GADOLINIUM; GOLD NANOPARTICLE; INDIUM 111; IODINE 124; IODINE 125; IODINE 131; NITROGEN 13; OXYGEN 15; SODIUM IODIDE SYMPORTER; TECHNETIUM 99M; ZIRCONIUM;

ADOPTIVE TRANSFER; ARTICLE; CELL LABELING; HALF LIFE TIME; HUMAN; IMAGE RECONSTRUCTION; IONIZING RADIATION; ISOTOPE LABELING; MICRO-COMPUTED TOMOGRAPHY; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REPORTER GENE; SENSITIVITY AND SPECIFICITY; SIGNAL NOISE RATIO; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; WHOLE BODY IMAGING;

ADOPTIVE TRANSFER; ANIMALS; CELL LINE; DIAGNOSTIC IMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; POSITRON-EMISSION TOMOGRAPHY; T-LYMPHOCYTES, REGULATORY; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; TRANSPLANTATION;

EID: 84876087398     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12087     Document Type: Article

References (73)

1. Wei S, Kryczek I, Zou W. Regulatory T-cell compartmentalization and trafficking. Blood 2006; 108:426-431.
2. Safinia N, Sagoo P, Lechler R, Lombardi G. Adoptive regulatory T cell therapy: challenges in clinical transplantation. Curr Opin Organ Transplant 2010; 15:427-434.
3. Tang Q, Bluestone JA, Kang SM. CD4(+)Foxp3(+) regulatory T cell therapy in transplantation. J Mol Cell Biol 2012; 4:11-21.
4. Kang SM, Tang Q, Bluestone JA. CD4+CD25+ regulatory T cells in transplantation: progress, challenges and prospects. Am J Transplant 2007; 7:1457-1463.
5. Tang Q, Lee K. Regulatory T-cell therapy for transplantation: how many cells do we need? Curr Opin Organ Transplant 2012; 17:349-354.
6. Tsang JY, Tanriver Y, Jiang S etal. Conferring indirect allospecificity on CD4+CD25+ Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest 2008; 118:3619-3628.
7. Sagoo P, Ali N, Garg G, Nestle FO, Lechler RI, Lombardi G. Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med 2011; 3:83ra42.
8. Li XC, Turka LA. An update on regulatory T cells in transplant tolerance and rejection. Nat Rev Nephrol 2010; 6:577-583.
9. Masteller EL, Tang Q, Bluestone JA. Antigen-specific regulatory T cells - ex vivo expansion and therapeutic potential. Semin Immunol 2006; 18:103-110.
10. Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y. Regulatory T cells and organ transplantation. Semin Immunol 2004; 16:119-126.
11. Xia G, Shah M, Luo X. Prevention of allograft rejection by amplification of Foxp3(+)CD4(+)CD25(+) regulatory T cells. Transl Res 2009; 153:60-70.
12. Wood KJ, Luo S, Akl A. Regulatory T cells: potential in organ transplantation. Transplantation 2004; 77:S6-8.
13. Wood KJ, Bushell A, Hester J. Regulatory immune cells in transplantation. Nat Rev Immunol 2012; 12:417-430.
14. Zhang N, Schroppel B, Lal G etal. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 2009; 30:458-469.
15. Tang Q, Adams JY, Tooley AJ etal. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 2006; 7:83-92.
16. Tang Q, Krummel MF. Imaging the function of regulatory T cells in vivo. Curr Opin Immunol 2006; 18:496-502.
17. de Kemp RA, Epstein FH, Catana C, Tsui BM, Ritman EL. Small-animal molecular imaging methods. J Nucl Med 2010; 51 (Suppl. 1):18S-32S.
18. Gaa J, Rummeny EJ, Seemann MD. Whole-body imaging with PET/MRI. Eur J Med Res 2004; 9:309-312.
19. Pichler BJ, Kolb A, Nagele T, Schlemmer HP. PET/MRI: paving the way for the next generation of clinical multimodality imaging applications. J Nucl Med 2010; 51:333-336.
20. Kircher MF, Gambhir SS, Grimm J. Noninvasive cell-tracking methods. Nat Rev Clin Oncol 2011; 8:677-688.
21. Kircher MF, Allport JR, Graves EE etal. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res 2003; 63:6838-6846.
22. Massoud TF, Gambhir SS. Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 2003; 17:545-580.
23. Kircher MF, Willmann JK. Molecular body imaging: MR imaging, CT, and US. Part I. Principles. Radiology 2012; 263:633-643.
24. Chung JK. Sodium iodide symporter: its role in nuclear medicine. J Nucl Med 2002; 43:1188-1200.
25. Mariani G, Bruselli L, Kuwert T etal. A review on the clinical uses of SPECT/CT. Eur J Nucl Med Mol Imaging 2010; 37:1959-1985.
26. Marsee DK, Shen DH, MacDonald LR etal. Imaging of metastatic pulmonary tumors following NIS gene transfer using single photon emission computed tomography. Cancer Gene Ther 2004; 11:121-127.
27. Hildebrandt IJ, Gambhir SS. Molecular imaging applications for immunology. Clin Immunol 2004; 111:210-224.
28. Khalil MM, Tremoleda JL, Bayomy TB, Gsell W. Molecular SPECT imaging: an overview. Int J Mol Imaging 2011; 2011:796025.
29. Madsen MT. Recent advances in SPECT imaging. J Nucl Med 2007; 48:661-673.
30. Signore A, Mather SJ, Piaggio G, Malviya G, Dierckx RA. Molecular imaging of inflammation/infection: nuclear medicine and optical imaging agents and methods. Chem Rev 2010; 110:3112-3145.
31. Buck AK, Nekolla S, Ziegler S etal. Spect/Ct. J Nucl Med 2008; 49:1305-1319.
32. Lecomte R. Novel detector technology for clinical PET. Eur J Nucl Med Mol Imaging 2009; 36 (Suppl. 1):S69-85.
33. Del Guerra A, Belcari N. State-of-the-art of PET, SPECT and CT for small animal imaging. Nucl Instrum Methods Phys Res A 2007; 583:119-124.
34. Hohn A, Zimmermann K, Schaub E, Hirzel W, Schubiger PA, Schibli R. Production and separation of 'non-standard' PET nuclides at a large cyclotron facility: the experiences at the Paul Scherrer Institute in Switzerland. Q J Nucl Med Mol Imaging 2008; 52:145-150.
35. Rahmim A, Zaidi H. PET versus SPECT: strengths, limitations and challenges. Nucl Med Commun 2008; 29:193-207.
36. Popovtzer R, Agrawal A, Kotov NA etal. Targeted gold nanoparticles enable molecular CT imaging of cancer. Nano Lett 2008; 8:4593-4596.
37. Fushiki H, Kanoh-Azuma T, Katoh M etal. Quantification of mouse pulmonary cancer models by microcomputed tomography imaging. Cancer Sci 2009; 100:1544-1549.
38. Grassi R, Cavaliere C, Cozzolino S etal. Small animal imaging facility: new perspectives for the radiologist. Radiol Med (Torino) 2009; 114:152-167.
39. Patel CM, Sahdev A, Reznek RH. CT, MRI and PET imaging in peritoneal malignancy. Cancer Imaging 2011; 11:123-139.
40. Ottobrini L, Martelli C, Trabattoni DL, Clerici M, Lucignani G. In vivo imaging of immune cell trafficking in cancer. Eur J Nucl Med Mol Imaging 2011; 38:949-968.
41. Tavare R, Sagoo P, Varama G etal. Monitoring of in vivo function of superparamagnetic iron oxide labelled murine dendritic cells during anti-tumour vaccination. PloS ONE 2011; 6:e19662.
42. Yeh TC, Zhang W, Ildstad ST, Ho C. In vivo dynamic MRI tracking of rat T-cells labeled with superparamagnetic iron-oxide particles. Magn Reson Med 1995; 33:200-208.
43. Dodd SJ, Williams M, Suhan JP, Williams DS, Koretsky AP, Ho C. Detection of single mammalian cells by high-resolution magnetic resonance imaging. Biophys J 1999; 76:103-109.
44. Yeh TC, Zhang W, Ildstad ST, Ho C. Intracellular labeling of T-cells with superparamagnetic contrast agents. Magn Reson Med 1993; 30:617-625.
45. Morawski AM, Winter PM, Crowder KC etal. Targeted nanoparticles for quantitative imaging of sparse molecular epitopes with MRI. Magn Reson Med 2004; 51:480-486.
46. Skajaa T, Cormode DP, Falk E, Mulder WJ, Fisher EA, Fayad ZA. High-density lipoprotein-based contrast agents for multimodal imaging of atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30:169-176.
47. Ahrens ET, Flores R, Xu H, Morel PA. In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 2005; 23:983-987.
48. Shapiro EM, Medford-Davis LN, Fahmy TM, Dunbar CE, Koretsky AP. Antibody-mediated cell labeling of peripheral T cells with micron-sized iron oxide particles (MPIOs) allows single cell detection by MRI. Contrast Media Mol Imaging 2007; 2:147-153.
49. Liu L, Ye Q, Wu Y etal. Tracking T-cells in vivo with a new nano-sized MRI contrast agent. Nanomedicine 2012; 8:1345-1354.
50. Roca M, de Vries EF, Jamar F, Israel O, Signore A. Guidelines for the labelling of leucocytes with (111)In-oxine. Inflammation/Infection Taskgroup of the European Association of Nuclear Medicine. Eur J Nucl Med Mol Imaging 2010; 37:835-841.
51. de Vries EF, Roca M, Jamar F, Israel O, Signore A. Guidelines for the labelling of leucocytes with (99m)Tc-HMPAO. Inflammation/ Infection Taskgroup of the European Association of Nuclear Medicine. Eur J Nucl Med Mol Imaging 2010; 37:842-848.
52. Pittet MJ, Grimm J, Berger CR etal. In vivo imaging of T cell delivery to tumors after adoptive transfer therapy. Proc Natl Acad Sci USA 2007; 104:12457-12461.
53. Gambhir SS, Herschman HR, Cherry SR etal. Imaging transgene expression with radionuclide imaging technologies. Neoplasia 2000; 2:118-138.
54. Gravina GL, Festuccia C, Marampon F etal. Biological rationale for the use of DNA methyltransferase inhibitors as new strategy for modulation of tumor response to chemotherapy and radiation. Mol Cancer 2010; 9:305. doi: 10.1186/1476-4598-9-305
55. Lam AP, Dean DA. Progress and prospects: nuclear import of nonviral vectors. Gene Ther 2010; 17:439-447.
56. Serganova I, Ponomarev V, Blasberg R. Human reporter genes: potential use in clinical studies. Nucl Med Biol 2007; 34:791-807.
57. Hooker JM. Modular strategies for PET imaging agents. Curr Opin Chem Biol 2010; 14:105-111.
58. Doubrovin MM, Doubrovina ES, Zanzonico P, Sadelain M, Larson SM, O'Reilly RJ. In vivo imaging and quantitation of adoptively transferred human antigen-specific T cells transduced to express a human norepinephrine transporter gene. Cancer Res 2007; 67:11959-11969.
59. Lee WW, Moon DH, Park SY, Jin J, Kim SJ, Lee H. Imaging of adenovirus-mediated expression of human sodium iodide symporter gene by 99mTcO4 scintigraphy in mice. Nucl Med Biol 2004; 31:31-40.
60. Barton KN, Stricker H, Brown SL etal. Phase I study of noninvasive imaging of adenovirus-mediated gene expression in the human prostate. Mol Ther 2008; 16:1761-1769.
61. Akins EJ, Dubey P. Noninvasive imaging of cell-mediated therapy for treatment of cancer. J Nucl Med 2008; 49 (Suppl. 2):180S-195.
62. Srinivas M, Turner MS, Janjic JM, Morel PA, Laidlaw DH, Ahrens ET. In vivo cytometry of antigen-specific T cells using 19F MRI. Magn Reson Med 2009; 62:747-753.
63. Smirnov P, Poirier-Quinot M, Wilhelm C etal. In vivo single cell detection of tumor-infiltrating lymphocytes with a clinical 1·5 Tesla MRI system. Magn Reson Med 2008; 60:1292-1297.
64. Kanwar B, Gao DW, Hwang AB etal. In vivo imaging of mucosal CD4+ T cells using single photon emission computed tomography in a murine model of colitis. J Immunol Methods 2008; 329:21-30.
65. Parente-Pereira AC, Burnet J, Ellison D etal. Trafficking of CAR-engineered human T cells following regional or systemic adoptive transfer in SCID beige mice. J Clin Immunol 2011; 31:710-718.
66. Koehne G, Doubrovin M, Doubrovina E et al. Serial in vivo imaging of the targeted migration of human HSV-TK-transduced antigen-specific lymphocytes. Nat Biotechnol 2003; 21:405-413.
67. Yaghoubi SS, Jensen MC, Satyamurthy N etal. Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma. Nat Clin Pract Oncol 2009; 6:53-58.
68. Feng NH, Wu HF, Wu J etal. Transplantation tolerance mediated by regulatory T cells in mice. Chin Med J 2004; 117:1184-1189.
69. Sharif-Paghaleh E, Sunassee K, Tavare R etal. In vivo SPECT reporter gene imaging of regulatory T cells. PloS ONE 2011; 6:e25857.
70. Nguyen VH, Zeiser R, Dasilva DL etal. In vivo dynamics of regulatory T-cell trafficking and survival predict effective strategies to control graft-versus-host disease following allogeneic transplantation. Blood 2007; 109:2649-2656.
71. Suffner J, Hochweller K, Kuhnle MC etal. Dendritic cells support homeostatic expansion of Foxp3+ regulatory T cells in Foxp3.LuciDTR mice. J Immunol 2010; 184:1810-1820.
72. Nadig SN, Wieckiewicz J, Wu DC etal. In vivo prevention of transplant arteriosclerosis by ex vivo-expanded human regulatory T cells. Nat Med 2010; 16:809-813.
73. Peterson TE, Shokouhi S. Advances in preclinical SPECT instrumentation. J Nucl Med 2012; 53:841-844.