Advances in stem cell research have provided important understanding of the cell biology and offered great promise for developing new strategies for tissue regeneration. The beneficial effects of stem cell therapy depend also by the development of new approachs for the track of stem cells in living subjects over time after transplantation. Recent developments in the use of nanotechnologies have contributed to advance of the high-resolution in vivo imaging methods, including positron emission tomography (PET), single-photon emission tomography (SPECT), magnetic resonance (MR) imaging, and X-Ray computed microtomography (microCT). This review examines the use of nanotechnologies for stem cell tracking.
References
[1]
Bryder, D; Rossi, DJ; Weissman, IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am. J. Pathol？2006, 169, 338–346.
[2]
Asahara, T; Kawamoto, A. Endothelial progenitor cells for postnatal vasculogenesis. Am. J. Physiol. Cell Physiol？2004, 287, C572–C579.
[3]
Lindvall, O; Kokaia, Z; Martinez-Serrano, A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat. Med？2004, 10, S42–S50.
[4]
Bonner-Weir, S; Weir, GC. New sources of pancreatic beta-cells. Nat. Biotechnol？2005, 23, 857–861.
[5]
Mimeault, M; Batra, SK. Concise review: recent advances on the significance of stem cells in tissue regeneration and cancer therapies. Stem Cells？2006, 24, 2319–2345.
[6]
Arbab, AS; Yocum, GT; Kalish, H; Jordan, EK; Anderson, SA; Khakoo, AY; Read, EJ; Frank, JA. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood？2004, 104, 1217–1223.
[7]
Kamaly, N; Kalber, T; Ahmad, A; Oliver, MH; So, PW; Herlihy, AH; Bell, JD; Jorgensen, MR; Miller, AD. Bimodal paramagnetic and fluorescent liposomes for cellular and tumor magnetic resonance imaging. Bioconjug Chem？2008, 19, 118–129.
[8]
Aime, S; Barge, A; Cabella, C; Crich, SG; Gianolio, E. Targeting cells with MR imaging probes based on paramagnetic Gd(III) chelates. Curr. Pharm. Biotechnol？2004, 5, 509–518.
[9]
Anderson, SA; Lee, KK; Frank, JA. Gadolinium-fullerenol as a paramagnetic contrast agent for cellular imaging. Invest. Radiol？2006, 41, 332–338.
[10]
Bogaards, A; Sterenborg, HJ; Trachtenberg, J; Wilson, BC; Lilge, L. In vivo quantification of fluorescent molecular markers in real-time by ratio imaging for diagnostic screening and image-guided surgery. Lasers Surg. Med？2007, 39, 605–613.
[11]
Bhaumik, S; Gambhir, SS. Optical imaging of Renilla luciferase reporter gene expression in living mice. Proc. Natl. Acad. Sci. USA？2002, 99, 377–382.
[12]
Bulte, JW; Arbab, AS; Douglas, T; Frank, JA. Preparation of magnetically labeled cells for cell tracking by magnetic resonance imaging. Methods Enzymol？2004, 386, 275–299.
[13]
Sheikh, AY; Lin, SA; Cao, F; Cao, Y; van der Bogt, KE; Chu, P; Chang, CP; Contag, CH; Robbins, RC; Wu, JC. Molecular imaging of bone marrow mononuclear cell homing and engraftment in ischemic myocardium. Stem Cells？2007, 25, 2677–2684.
[14]
Ferreira, L; Karp, JM; Nobre, L; Langer, R. New opportunities: the use of nanotechnologies to manipulate and track stem cells. Cell Stem Cell？2008, 3, 136–146.
[15]
Bulte, JWM; Douglas, T; Witwer, B; Zhang, SC; Strable, E; Lewis, BK; Zywicke, H; Miller, B; van Gelderen, P; Moskowitz, BM; Duncan, ID; Frank, JA. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat. Biotechnol？2001, 19, 1141–1147.
[16]
Gavina, M; Belicchi, M; Rossi, B; Ottoboni, L; Colombo, F; Meregalli, M; Battistelli, M; Forzenigo, L; Biondetti, P; Pisati, F; Parolini, D; Farini, A; Issekutz, AC; Bresolin, N; Rustichelli, F; Constantin, G; Torrente, Y. VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood？2006, 108, 2857–2866.
[17]
Torrente, Y; Gavina, M; Belicchi, M; Fiori, F; Komlev, V; Bresolin, N; Rustichelli, F. High-resolution X-ray microtomography for three-dimensional visualization of human stem cell muscle homing. FEBS Lett？2006, 580, 5759–5764.
[18]
Walczak, P; Zhang, J; Gilad, AA; Kedziorek, DA; Ruiz-Cabello, J; Young, RG; Pittenger, MF; van Zijl, PC; Huang, J; Bulte, JW. Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke？2008, 39, 1569–1574.
[19]
Heyn, C; Ronald, JA; Mackenzie, LT; MacDonald, IC; Chambers, AF; Rutt, BK; Foster, PJ. In vivo magnetic resonance imaging of single cells in mouse brain with optical validation. Magn. Reson. Med？2006, 55, 23–29.
[20]
Heyn, C; Ronald, JA; Ramadan, SS; Snir, JA; Barry, AM; MacKenzie, LT; Mikulis, DJ; Palmieri, D; Bronder, JL; Steeg, PS; Yoneda, T; MacDonald, IC; Chambers, AF; Rutt, BK; Foster, PJ. In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn. Reson. Med？2006, 56, 1001–1010.
[21]
Himmelreich, U; Hoehn, M. Stem cell labeling for magnetic resonance imaging. Minim. Invasive Ther. Allied Technol？2008, 17, 132–142.
[22]
Bulte, JW; Kraitchman, DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed？2004, 17, 484–499.
[23]
Lewin, M; Carlesso, N; Tung, CH; Tang, XW; Cory, D; Scadden, DT; Weissleder, R. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol？2000, 18, 410–414.
[24]
Modo, M; Cash, D; Mellodew, K; Williams, SC; Fraser, SE; Meade, TJ; Price, J; Hodges, H. Tracking transplanted stem cell migration using bifunctional, contrast agent-enhanced, magnetic resonance imaging. Neuroimage？2002, 17, 803–811.
[25]
Kim, D; Hong, KS; Song, J. The present status of cell tracking methods in animal models using magnetic resonance imaging technology. Mol. Cells？2007, 23, 132–137.
Guzman, R; Uchida, N; Bliss, TM; He, D; Christopherson, KK; Stellwagen, D; Capela, A; Greve, J; Malenka, RC; Moseley, ME; Palmer, TD; Steinberg, GK. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc. Natl. Acad. Sci. USA？2007, 104, 10211–10216.
[28]
Walter, GA; Cahill, KS; Huard, J; Feng, H; Douglas, T; Sweeney, HL; Bulte, JW. Noninvasive monitoring of stem cell transfer for muscle disorders. Magn. Reson. Med？2004, 51, 273–277.
[29]
Arai, T; Kofidis, T; Bulte, JW; de Bruin, J; Venook, RD; Berry, GJ; McConnell, MV; Quertermous, T; Robbins, RC; Yang, PC. Dual in vivo magnetic resonance evaluation of magnetically labeled mouse embryonic stem cells and cardiac function at 1.5 t. Magn. Reson. Med？2006, 55, 203–209.
[30]
Kraitchman, DL; Tatsumi, M; Gilson, WD; Ishimori, T; Kedziorek, D; Walczak, P; Segars, WP; Chen, HH; Fritzges, D; Izbudak, I; Young, RG; Marcelino, M; Pittenger, MF; Solaiyappan, M; Boston, RC; Tsui, BM; Wahl, RL; Bulte, JW. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation？2005, 112, 1451–1461.
[31]
Kustermann, E; Roell, W; Breitbach, M; Wecker, S; Wiedermann, D; Buehrle, C; Welz, A; Hescheler, J; Fleischmann, BK; Hoehn, M. Stem cell implantation in ischemic mouse heart: a high-resolution magnetic resonance imaging investigation. NMR Biomed？2005, 18, 362–370.
[32]
Arbab, AS; Liu, W; Frank, JA. Cellular magnetic resonance imaging: current status and future prospects. Exp. Rev. Med. Dev？2006, 3, 427–439.
[33]
Lewin, JS; Nour, SG; Duerk, JL. Magnetic resonance image-guided biopsy and aspiration. Top Magn. Reson. Imaging？2000, 11, 173–183.
[34]
Zhu, J; Zhou, L; Xing, WF. Tracking neural stem cells in patients with brain trauma. N. Engl. J. Med？2006, 355, 2376–2378.
[35]
de Vries, IJ; Lesterhuis, WJ; Barentsz, JO; Verdijk, P; van Krieken, JH; Boerman, OC; Oyen, WJ; Bonenkamp, JJ; Boezeman, JB; Adema, GJ; Bulte, JW; Scheenen, TW; Punt, CJ; Heerschap, A; Figdor, CG. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol？2005, 23, 1407–1413.
[36]
Becker, W; Meller, J. The role of nuclear medicine in infection and inflammation. Lancet Infect. Dis？2001, 1, 326–333.
[37]
Eggert, AA; Schreurs, MW; Boerman, OC; Oyen, WJ; de Boer, AJ; Punt, CJ; Figdor, CG; Adema, GJ. Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res？1999, 59, 3340–3345.
[38]
Bohnen, NI; Charron, M; Reyes, J; Rubinstein, W; Strom, SC; Swanson, D; Towbin, R. Use of indium-111-labeled hepatocytes to determine the biodistribution of transplanted hepatocytes through portal vein infusion. Clin. Nucl. Med？2000, 25, 447–450.
Slotkin, JR; Chakrabarti, L; Dai, HN; Carney, RS; Hirata, T; Bregman, BS; Gallicano, GI; Corbin, JG; Haydar, TF. In vivo quantum dot labeling of mammalian stem and progenitor cells. Dev. Dyn？2007, 236, 3393–3401.
[44]
Chakraborty, SK; Fitzpatrick, JA; Phillippi, JA; Andreko, S; Waggoner, AS; Bruchez, MP; Ballou, B. Cholera toxin B conjugated quantum dots for live cell labeling. Nano Lett？2007, 7, 2618–2626.
[45]
Chen, H; Titushkin, I; Stroscio, M; Cho, M. Altered membrane dynamics of quantum dot-conjugated integrins during osteogenic differentiation of human bone marrow derived progenitor cells. Biophys. J？2007, 92, 1399–1408.
[46]
Ashbridge, DA; Thorne, MS; Rivers, ML; Muccino, JC; O’Day, PA. Image optimization and analysis of synchrotron X-ray computed microtomography (CmT) data. Comput Geosci？2003, 29, 823–836.
[47]
Kinney, JH; Ryaby, JT; Haupt, DL; Lane, NE. Three-dimensional in vivo morphometry of trabecular bone in the OVX rat model of osteoporosis. Technol. Health Care？1998, 6, 339–350.
[48]
Bayat, SAL; Boller, E; Brochard, T; Peyrin, F. In vivo imaging of bone micro-architecture in mice with 3D synchrotron radiation microtomography. Nucl. Instr. Meth. A？2005, 52, 548–247.
[49]
David, V; Laroche, N; Boudignon, B; Lafage-Proust, MH; Alexandre, C; Ruegsegger, P; Vico, L. Noninvasive in vivo monitoring of bone architecture alterations in hindlimb-unloaded female rats using novel three-dimensional microcomputed tomography. J. Bone Miner. Res？2003, 18, 1622–1631.
[50]
Boyd, SK; Davison, P; Muller, R; Gasser, JA. Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone？2006, 39, 854–862.
[51]
Cancedda, R; Cedola, A; Giuliani, A; Komlev, V; Lagomarsino, S; Mastrogiacomo, M; Peyrin, F; Rustichelli, F. Bulk and interface investigations of scaffolds and tissue-engineered bones by X-ray microtomography and X-ray microdiffraction. Biomaterials？2007, 28, 2505–2524.
[52]
Brunke, OS; Fritsche, C; Hilger, I; Kaiser, WO. Determination of magnetic particle distribution in biomedical applications by X-ray microtomography. J. Mag. Magn. Mat？2005, 289, 428–430.
[53]
Hsieh, SC; Wang, FF; Hung, SC; Chen, YJ; Wang, YJ. The internalized CdSe/ZnS quantum dots impair the chondrogenesis of bone marrow mesenchymal stem cells. J. Biomed. Mater. Res. B Appl. Biomater？2006, 79, 95–101.
[54]
Hsieh, SC; Wang, FF; Lin, CS; Chen, YJ; Hung, SC; Wang, YJ. The inhibition of osteogenesis with human bone marrow mesenchymal stem cells by CdSe/ZnS quantum dot labels. Biomaterials？2006, 27, 1656–1664.
[55]
Dubertret, B; Skourides, P; Norris, DJ; Noireaux, V; Brivanlou, AH; Libchaber, A. In vivo imaging of quantum dots encapsulated in phospholipid micelles. Science？2002, 298, 1759–1762.
[56]
Beckmann, N; Cannet, C; Babin, AL; Ble, FX; Zurbruegg, S; Kneuer, R; Dousset, V. In vivo visualization of macrophage infiltration and activity in inflammation using magnetic resonance imaging. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol？2009, 1, 272–298.
[57]
Tian: Bioluminescent imaging demonstrates that transplanted human embryonic stem cell-derived CD34(+) cells preferentially develop into endothelial cells. Stem Cells？2009, 27, 2675–2685.
[58]
Gainkam, LO; Huang, L; Caveliers, V; Keyaerts, M; Hernot, S; Vaneycken, I; Vanhove, C; Revets, H; De Baetselier, P; Lahoutte, T. Comparison of the biodistribution and tumor targeting of two 99mTc-labeled anti-EGFR nanobodies in mice, using pinhole SPECT/micro-CT. J. Nucl. Med？2008, 49, 788–795.
