Non-invasive imaging of human embryonic stem cells

Current Pharmaceutical Biotechnology

Volumn 11, Issue 6, 2010, Pages 685-692

  Hong, Hao ^a   Yang, Yunan ^a   Zhang, Yin ^a   Cai, Weibo ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Bioluminescence imaging (BLI); Cell tracking; Human embryonic stem cells (hESCs); Magnetic resonance imaging (MRI); Molecular imaging; Positron emission tomography (PET); Regenerative medicine; Single photon emission computed tomography (SPECT)

Indexed keywords

RADIOISOTOPE; DIAGNOSTIC AGENT;

BIOLUMINESCENCE; CELL FUNCTION; CELL LABELING; CELL PROLIFERATION; CELL SURVIVAL; CELL TRACKING; CLINICAL RESEARCH; EMBRYONIC STEM CELL; FLUORESCENCE IMAGING; HUMAN; NEURAL STEM CELL; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TERATOMA; CELL CULTURE; CYTOLOGY; GENETIC PROCEDURES; IMAGE ENHANCEMENT; METHODOLOGY; MOLECULAR PROBE; SCINTISCANNING;

CELL TRACKING; CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; IMAGE ENHANCEMENT; MOLECULAR PROBE TECHNIQUES; MOLECULAR PROBES;

EID: 79951663081     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920110792246500     Document Type: Review

References (62)

1. Thomson, J.A.; Itskovitz-Eldor, J.; Shapiro, S.S.; Waknitz, M.A.; Swiergiel, J.J.; Marshall, V.S.; Jones, J.M. Embryonic stem cell lines derived from human blastocysts. Science. 1998, 282. 1145-1147.
2. Mountford, J.C. Human embryonic stem cells: origins, characteristics and potential for regenerative therapy. Transfus. Med. 2008, 18. 1-12.
3. Sartipy, P.; Bjorquist, P.; Strehl, R.; Hyllner, J. The application of human embryonic stem cell technologies to drug discovery. Drug Discov. Today. 2007, 12. 688-699.
4. Singec, I.; Jandial, R.; Crain, A.; Nikkhah, G.; Snyder, E.Y. The leading edge of stem cell therapeutics. Annu. Rev. Med. 2007, 58. 313-328.
5. Trounson, A. New perspectives in human stem cell therapeutic research. BMC Med. 2009, 7. 29.
6. Guillaume, D.J.; Zhang, S.C. Human embryonic stem cells: a potential source of transplantable neural progenitor cells. Neurosurg. Focus. 2008, 24. E3.
7. Keirstead, H.S.; Nistor, G.; Bernal, G.; Totoiu, M.; Cloutier, F.; Sharp, K.; Steward, O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 2005, 25. 4694-4705.
8. Koelling, S.; Miosge, N. Stem cell therapy for cartilage regeneration in osteoarthritis. Expert Opin. Biol. Ther. 2009, 9. 1399-1405.
9. Xue, T.; Cho, H.C.; Akar, F.G.; Tsang, S.Y.; Jones, S.P.; Marban, E.; Tomaselli, G.F.; Li, R.A. Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation. 2005, 111. 11-20.
10. Swijnenburg, R.J.; van der Bogt, K.E.; Sheikh, A.Y.; Cao, F.; Wu, J.C. Clinical hurdles for the transplantation of cardiomyocytes derived from human embryonic stem cells: role of molecular imaging. Curr. Opin. Biotechnol. 2007, 18. 38-45.
11. Laflamme, M.A.; Chen, K.Y.; Naumova, A.V.; Muskheli, V.; Fugate, J.A.; Dupras, S.K.; Reinecke, H.; Xu, C.; Hassanipour, M.; Police, S.; O'Sullivan, C.; Collins, L.; Chen, Y.; Minami, E.; Gill, E.A.; Ueno, S.; Yuan, C.; Gold, J.; Murry, C.E. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 2007, 25. 1015-1024.
12. van Laake, L.W.; Passier, R.; Doevendans, P.A.; Mummery, C.L. Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ. Res. 2008, 102. 1008-1010.
13. Narsinh, K.H.; Cao, F.; Wu, J.C. Molecular imaging of human embryonic stem cells. Methods Mol. Biol. 2009, 515. 13-32.
14. Mankoff, D.A. A definition of molecular imaging. J. Nucl. Med. 2007, 48. 18N, 21N.
15. Massoud, T.F.; Gambhir, S.S. Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev. 2003, 17. 545-580.
16. Cai, W.; Chen, X. Multimodality imaging of vascular endothelial growth factor and vascular endothelial growth factor receptor expression. Front. Biosci. 2007, 12. 4267-4279.
17. Arbab, A.S.; Liu, W.; Frank, J.A. Cellular magnetic resonance imaging: current status and future prospects. Expert Rev. Med. Devices. 2006, 3. 427-439.
18. Budde, M.D.; Frank, J.A. Magnetic tagging of therapeutic cells for MRI. J. Nucl. Med. 2009, 50. 171-174.
19. Pearl, J.; Wu, J.C. Seeing is believing: tracking cells to determine the effects of cell transplantation. Semin. Thorac. Cardiovasc. Surg. 2008, 20. 102-109.
20. Tallheden, T.; Nannmark, U.; Lorentzon, M.; Rakotonirainy, O.; Soussi, B.; Waagstein, F.; Jeppsson, A.; Sjogren-Jansson, E.; Lindahl, A.; Omerovic, E. In vivo MR imaging of magnetically labeled human embryonic stem cells. Life Sci. 2006, 79. 999-1006.
21. van Laake, L.W.; Passier, R.; Monshouwer-Kloots, J.; Nederhoff, M.G.; Ward-van Oostwaard, D.; Field, L.J.; van Echteld, C.J.; Doevendans, P.A.; Mummery, C.L. Monitoring of cell therapy and assessment of cardiac function using magnetic resonance imaging in a mouse model of myocardial infarction. Nat. Protoc. 2007, 2. 2551-2567.
22. Henning, T.D.; Boddington, S.; Daldrup-Link, H.E. Labeling hESCs and hMSCs with iron oxide nanoparticles for non-invasive in vivo tracking with MR imaging. J. Vis. Exp. 2008, pii: 685.
23. Chung, J.; Yamada, M.; Yang, P.C. Magnetic resonance imaging of human embryonic stem cells. Curr. Protoc. Stem Cell Biol. 2009, Chapter 5. Unit 5A. 3.
24. Sykova, E.; Jendelova, P. Magnetic resonance tracking of transplanted stem cells in rat brain and spinal cord. Neurodegener. Dis. 2006, 3. 62-67.
25. Sykova, E.; Jendelova, P. In vivo tracking of stem cells in brain and spinal cord injury. Prog. Brain Res. 2007, 161. 367-383.
26. Stroh, A.; Boltze, J.; Sieland, K.; Hild, K.; Gutzeit, C.; Jung, T.; Kressel, J.; Hau, S.; Reich, D.; Grune, T.; Zimmer, C. Impact of magnetic labeling on human and mouse stem cells and their longterm magnetic resonance tracking in a rat model of Parkinson disease. Mol. Imaging. 2009, 8. 166-178.
27. Ben-Hur, T.; van Heeswijk, R.B.; Einstein, O.; Aharonowiz, M.; Xue, R.; Frost, E.E.; Mori, S.; Reubinoff, B.E.; Bulte, J.W. Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn. Reson. Med. 2007, 57. 164-171.
28. Yamada, M.; Yang, P. In vitro labeling of human embryonic stem cells for magnetic resonance imaging. J. Vis. Exp. 2008, ID=827.
29. Yamada, M.; Gurney, P.T.; Chung, J.; Kundu, P.; Drukker, M.; Smith, A.K.; Weissman, I.L.; Nishimura, D.; Robbins, R.C.; Yang, P.C. Manganese-guided cellular MRI of human embryonic stem cell and human bone marrow stromal cell viability. Magn. Reson. Med. 2009, 62. 1047-1054.
30. Li, Z.; Suzuki, Y.; Huang, M.; Cao, F.; Xie, X.; Connolly, A.J.; Yang, P.C.; Wu, J.C. Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells. 2008, 26. 864-873.
31. Wilson, K.; Yu, J.; Lee, A.; Wu, J.C. In vitro and in vivo bioluminescence reporter gene imaging of human embryonic stem cells. J. Vis. Exp. 2008, ID=740.
32. Dothager, R.S.; Flentie, K.; Moss, B.; Pan, M.H.; Kesarwala, A.; Piwnica-Worms, D. Advances in bioluminescence imaging of live animal models. Curr. Opin. Biotechnol. 2009, 20. 45-53.
33. Cai, W.; Hsu, A.R.; Li, Z.B.; Chen, X. Are quantum dots ready for in vivo imaging in human subjects? Nanoscale Res. Lett. 2007, 2. 265-281.
34. Cao, F.; Xie, X.; Gollan, T.; Zhao, L.; Narsinh, K.; Lee, R.J.; Wu, J.C. Comparison of gene-transfer efficiency in human embryonic stem cells. Mol. Imaging Biol. 2010, 12. 15-24.
35. Barberi, T.; Bradbury, M.; Dincer, Z.; Panagiotakos, G.; Socci, N.D.; Studer, L. Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat. Med. 2007, 13. 642-648.
36. Bradbury, M.S.; Panagiotakos, G.; Chan, B.K.; Tomishima, M.; Zanzonico, P.; Vider, J.; Ponomarev, V.; Studer, L.; Tabar, V. Optical bioluminescence imaging of human ES cell progeny in the rodent CNS. J. Neurochem. 2007, 102. 2029-2039.
37. Chan, K.M.; Raikwar, S.P.; Zavazava, N. Strategies for differentiating embryonic stem cells (ESC) into insulin-producing cells and development of non-invasive imaging techniques using bioluminescence. Immunol. Res. 2007, 39. 261-270.
38. Duan, Y.; Catana, A.; Meng, Y.; Yamamoto, N.; He, S.; Gupta, S.; Gambhir, S.S.; Zern, M.A. Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells. 2007, 25. 3058-3068.
39. Laurila, J.P.; Laatikainen, L.; Castellone, M.D.; Trivedi, P.; Heikkila, J.; Hinkkanen, A.; Hematti, P.; Laukkanen, M.O. Human embryonic stem cell-derived mesenchymal stromal cell transplantation in a rat hind limb injury model. Cytotherapy. 2009, 1-12.
40. Lee, A.S.; Tang, C.; Cao, F.; Xie, X.; van der Bogt, K.; Hwang, A.; Connolly, A.J.; Robbins, R.C.; Wu, J.C. Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle. 2009, 8. 2608-2612.
41. Swijnenburg, R.J.; Schrepfer, S.; Govaert, J.A.; Cao, F.; Ransohoff, K.; Sheikh, A.Y.; Haddad, M.; Connolly, A.J.; Davis, M.M.; Robbins, R.C.; Wu, J.C. Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc. Natl. Acad. Sci. USA. 2008, 105. 12991-12996.
42. Tian, X.; Hexum, M.K.; Penchev, V.R.; Taylor, R.J.; Shultz, L.D.; Kaufman, D.S. Bioluminescent imaging demonstrates that transplanted human embryonic stem cell-derived CD34(+) cells preferentially develop into endothelial cells. Stem Cells. 2009, 27. 2675-2685.
43. Wilson, K.D.; Huang, M.; Wu, J.C. Bioluminescence reporter gene imaging of human embryonic stem cell survival, proliferation, and fate. Methods Mol. Biol. 2009, 574. 87-103.
44. Tzukerman, M.; Rosenberg, T.; Ravel, Y.; Reiter, I.; Coleman, R.; Skorecki, K. An experimental platform for studying growth and invasiveness of tumor cells within teratomas derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA. 2003, 100. 13507-13512.
45. Tzukerman, M.; Skorecki, K.L. A novel experimental platform for investigating cancer growth and anti-cancer therapy in a human tissue microenvironment derived from human embryonic stem cells. Methods Mol. Biol. 2006, 331. 329-346.
46. Vallier, L.; Rugg-Gunn, P.J.; Bouhon, I.A.; Andersson, F.K.; Sadler, A.J.; Pedersen, R.A. Enhancing and diminishing gene function in human embryonic stem cells. Stem Cells. 2004, 22. 2-11.
47. Kita-Matsuo, H.; Barcova, M.; Prigozhina, N.; Salomonis, N.; Wei, K.; Jacot, J.G.; Nelson, B.; Spiering, S.; Haverslag, R.; Kim, C.; Talantova, M.; Bajpai, R.; Calzolari, D.; Terskikh, A.; McCulloch, A.D.; Price, J.H.; Conklin, B.R.; Chen, H.S.; Mercola, M. Lentiviral vectors and protocols for creation of stable hESC lines for fluorescent tracking and drug resistance selection of cardiomyocytes. PLoS One. 2009, 4. e5046.
48. Irion, S.; Luche, H.; Gadue, P.; Fehling, H.J.; Kennedy, M.; Keller, G. Identification and targeting of the ROSA26 locus in human embryonic stem cells. Nat. Biotechnol. 2007, 25. 1477-1482.
49. Ferreira, L.; Karp, J.M.; Nobre, L.; Langer, R. New opportunities: the use of nanotechnologies to manipulate and track stem cells. Cell Stem Cell. 2008, 3. 136-146.
50. Boddington, S.; Henning, T.D.; Sutton, E.J.; Daldrup-Link, H.E. Labeling stem cells with fluorescent dyes for non-invasive detection with optical imaging. J. Vis. Exp. 2008, ID=686.
51. Boddington, S.E.; Henning, T.D.; Jha, P.; Schlieve, C.R.; Mandrussow, L.; Denardo, D.; Bernstein, H.S.; Ritner, C.; Golovko, D.; Lu, Y.; Zhao, S.; Daldrup-Link, H.E. Labeling human embryonic stem cell derived cardiomyocytes with indocyanine green for noninvasive tracking with optical imaging: an fda compatible alternative to firefly luciferase. Cell Transplant. 2010, 19(1), 55-65.
52. Mueller, D.; Shamblott, M.J.; Fox, H.E.; Gearhart, J.D.; Martin, L.J. Transplanted human embryonic germ cell-derived neural stem cells replace neurons and oligodendrocytes in the forebrain of neonatal mice with excitotoxic brain damage. J. Neurosci. Res. 2005, 82. 592-608.
53. Shanthly, N.; Aruva, M.R.; Zhang, K.; Mathew, B.; Thakur, M.L. Stem cells: a regenerative pharmaceutical. Q. J. Nucl. Med. Mol. Imaging. 2006, 50. 205-216.
54. Lappalainen, R.S.; Narkilahti, S.; Huhtala, T.; Liimatainen, T.; Suuronen, T.; Narvanen, A.; Suuronen, R.; Hovatta, O.; Jolkkonen, J. The SPECT imaging shows the accumulation of neural progenitor cells into internal organs after systemic administration in middle cerebral artery occlusion rats. Neurosci. Lett. 2008, 440. 246-250.
55. Cao, F.; Li, Z.; Lee, A.; Liu, Z.; Chen, K.; Wang, H.; Cai, W.; Chen, X.; Wu, J.C. Noninvasive de novo imaging of human embryonic stem cell-derived teratoma formation. Cancer Res. 2009, 69. 2709-2713.
56. Cai, W.; Chen, X. Multimodality molecular imaging of tumor angiogenesis. J. Nucl. Med. 2008, 49 (Suppl 2), 113S-128S.
57. Cai, W.; Niu, G.; Chen, X. Imaging of integrins as biomarkers for tumor angiogenesis. Curr. Pharm. Des. 2008, 14. 2943-2973.
58. 3antagonism. Anti-Cancer Agents Med. Chem. 2006, 6. 407-428.
59. Cai, W.; Rao, J.; Gambhir, S.S.; Chen, X. How molecular imaging is speeding up anti-angiogenic drug development. Mol. Cancer Ther. 2006, 5. 2624-2633.
60. Daadi, M.M.; Li, Z.; Arac, A.; Grueter, B.A.; Sofilos, M.; Malenka, R.C.; Wu, J.C.; Steinberg, G.K. Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain. Mol. Ther. 2009, 17. 1282-1291.
61. Pomper, M.G.; Hammond, H.; Yu, X.; Ye, Z.; Foss, C.A.; Lin, D.D.; Fox, J.J.; Cheng, L. Serial imaging of human embryonic stem-cell engraftment and teratoma formation in live mouse models. Cell Res. 2009, 19. 370-379.
62. Cao, F.; Drukker, M.; Lin, S.; Sheikh, A.Y.; Xie, X.; Li, Z.; Connolly, A.J.; Weissman, I.L.; Wu, J.C. Molecular imaging of embryonic stem cell misbehavior and suicide gene ablation. Cloning Stem Cells. 2007, 9. 107-117.