Labeling human mesenchymal stem cells with gold nanocages for in vitro and in vivo tracking by two-photon microscopy and photoacoustic microscopy

Theranostics

Volumn 3, Issue 8, 2013, Pages 532-543

  Zhang, Yu Shrike ^a   Wang, Yu ^b   Wang, Lidai ^b   Wang, Yucai ^a   Cai, Xin ^b   Zhang, Chi ^b   Wang, Lihong V ^b   Xia, Younan ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Blood vessels; Gold nanocages; Human mesenchymal stem cells; Nanoparticles; Stem cell therapy; U87 glioblastoma

Indexed keywords

GOLD NANOCAGE; HEMOGLOBIN; NANOCAGE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL; CELL COUNT; CELL DIFFERENTIATION; CELL HOMING; CELL LABELING; CELL LINEAGE; CELL MIGRATION; CELL TRACKING; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE MICROSCOPY; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHOTOACOUSTIC MICROSCOPY;

EID: 84883177523     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.5369     Document Type: Article

References (57)

1. Koike N, Fukumura D, Gralla O, Au P, Schechner JS, Jain RK. Tissue engineering: creation of long-lasting blood vessels. Nature. 2004; 428: 138-9.
2. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007; 110: 3499-506.
3. Humphreys BD, Bonventre JV. Mesenchymal stem cells in acute kidney injury. Annu Rev Med. 2008; 59: 311-25.
4. Stappenbeck TS, Miyoshi H. The role of stromal stem cells in tissue regeneration and wound repair. Science. 2009; 324: 1666-9.
5. Bexell D, Scheding S, Bengzon J. Toward brain tumor gene therapy using multipotent mesenchymal stromal cell vectors. Mol Ther. 2010; 18: 1067-75.
6. Borthwick L. The dark side of mesenchymal stem cells. Nat Rep Stem Cells. 2007. DOI:10.1038/stemcells.2007.107.
7. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res. , 2004, 95,9-20
8. Lu D, Mahmood A, Wang L, Li Y, Lu M, Chopp M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport. 2001; 12: 559-63.
9. Guo J, Lin G-s, Bao C-y, Hu Z-m, Hu M-y. Anti-inflammation role for mesenchymal stem cells transplantation in myocardial infarction. Inflammation. 2007; 30: 97-104.
10. Chen X, Lin X, Zhao J, Shi W, Zhang H, Wang Y, et al. A tumor-selective biotherapy with prolonged impact on established metastases nased on cytokine gene-engineered MSCs. Mol Ther. 2008; 16: 749-56.
11. Hu Y-L, Fu Y-H, Tabata Y, Gao J-Q. Mesenchymal stem cells: a promising targeted-delivery vehicle in cancer gene therapy. J Control Release. 2010; 147: 154-62.
12. Hung S-C, Deng W-P, Yang WK, Liu R-S, Lee C-C, Su T-C, et al. Mesenchymal stem cell targeting of microscopic tumors and tumorstroma development monitored by noninvasive in vivo positron emission tomography imaging. Clinical Cancer Res. 2005; 11: 7749-56.
13. Rodriguez-Porcel M. In vivo imaging and monitoring of transplanted stem cells: clinical applications. Curr Cardiol Rep. 2010; 12: 51-8.
14. Chin BB, Nakamoto Y, Bulte JW, Pittenger MF, Wahl R, Kraitchman DL. 111In oxine labelled mesenchymal stem cell SPECT after intravenous administration in myocardial infarction. Nucl Med Commun. 2003; 24: 1149-54.
15. Reagan MR, Kaplan DL. Concise review: mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem Cells. 2011; 29: 920-7.
16. Andreas K, Georgieva R, Ladwig M, Mueller S, Notter M, Sittinger M, et al. Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. Biomaterials. 2012; 33: 4515-25.
17. Tran LA, Krishnamurthy R, Muthupillai R, da Graça Cabreira-Hansen M, Willerson JT, Perin EC, et al. Gadonanotubes as magnetic nanolabels for stem cell detection. Biomaterials. 2010; 31: 9482-91.
18. Torrente Y, Gavina M, Belicchi M, Fiori F, Komlev V, Bresolin N, et al. High-resolution X-ray microtomography for three-dimensional visualization of human stem cell muscle homing. FEBS Lett. 2006; 580: 5759-64.
19. Giuliani A, Frati C, Rossini A, Komlev VS, Lagrasta C, Savi M, et al. High-resolution X-ray microtomography for three-dimensional imaging of cardiac progenitor cell homing in infarcted rat hearts. J Tissue Eng Regen Med. 2011; 5: e168-e78.
20. Chakraborty SK, Fitzpatrick JAJ, Phillippi JA, Andreko S, Waggoner AS, Bruchez MP, et al. Cholera toxin B conjugated quantum dots for live cell labeling. Nano Lett. 2007; 7: 2618-26.
21. Ranjbarvaziri S, Kiani S, Akhlaghi A, Vosough A, Baharvand H, Aghdami N. Quantum dot labeling using positive charged peptides in human hematopoetic and mesenchymal stem cells. Biomaterials. 2011; 32: 5195-205.
22. Yu X, Song S-K, Chen J, Scott MJ, Fuhrhop RJ, Hall CS, et al. High-resolution MRI characterization of human thrombus using a novel fibrin-targeted paramagnetic nanoparticle contrast agent. Magnet Reson Med. 2000; 44: 867-72.
23. Lee J-H, Jun Y-w, Yeon S-I, Shin J-S, Cheon J. Dual-mode nanoparticle probes for high-performance magnetic resonance and fluorescence imaging of neuroblastoma. Angew Chem Int Ed. 2006; 118: 8340-2.
24. Rogers WJ, Meyer CH, Kramer CM. Technology insight: in vivo cell tracking by use of MRI. Nat Clin Pract Cardiovasc Med. 2006; 3: 554-62.
25. Derfus AM, Chan WCW, Bhatia SN. Probing the cytotoxicity of semiconductor quantum dots. Nano Lett. 2003; 4: 11-8.
26. Hardman R. A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect. 2006; 114: 165-72.
27. Klinck RJ, Campbell GM, Boyd SK. Radiation effects on bone architecture in mice and rats resulting from in vivo micro-computed tomography scanning. Med Eng Phys. 2008; 30: 888-95.
28. Ritman EL. Molecular imaging in small animals-roles for micro-CT. J Cell Biochem. 2002; 87: 116-24.
29. Skrabalak SE, Au L, Li X, Xia Y. Facile synthesis of Ag nanocubes and Au nanocages. Nat Protoc. 2007; 2: 2182-90.
30. Wang Y, Hu S, Maslov K, Zhang Y, Xia Y, Wang LV. In vivo integrated photoacoustic and confocal microscopy of hemoglobin oxygen saturation and oxygen partial pressure. Opt Lett. 2011; 36: 1029-31.
31. Zhang C, Maslov K, Wang LV. Subwavelength-resolution label-free photoacoustic microscopy of optical absorption in vivo. Opt Lett. 2010; 35: 3195-7.
32. Song KH, Wang LV. Deep reflection-mode photoacoustic imaging of biological tissue. J Biomed Opt. 2007; 12: 060503-3.
33. Wang L, Maslov K, Yao J, Rao B, Wang LV. Fast voice-coil scanning optical-resolution photoacoustic microscopy. Opt Lett. 2011; 36: 139-41.
34. Au L, Zhang Q, Cobley CM, Gidding M, Schwartz AG, Chen J, et al. Quantifying the cellular uptake of antibody-conjugated Au nanocages by two-photon microscopy and inductively coupled plasma mass spectrometry. ACS Nano. 2010; 4: 35-42.
35. Yavuz MS, Cheng Y, Chen J, Cobley CM, Zhang Q, Rycenga M, et al. Gold nanocages covered by smart polymers for controlled release with near-infrared light. Nat Mater. 2009; 8: 935-9.
36. Li W, Cai X, Kim C, Sun G, Zhang Y, Deng R, et al. Gold nanocages covered with thermally-responsive polymers for controlled release by high-intensity focused ultrasound. Nanoscale. 2011; 3: 1724-30.
37. Cho EC, Xie J, Wurm PA, Xia Y. Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant. Nano Lett. 2009; 9: 1080-4.
38. Cho EC, Zhang Q, Xia Y. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotechnol. 2011; 6: 385-91.
39. Cang H, Sun T, Li ZY, Chen J, Wiley BJ, Xia Y, et al. Gold nanocages as contrast agents for spectroscopic optical coherence tomography. Opt Lett. 2005; 30: 3048-50.
40. Tong L, Cobley CM, Chen J, Xia Y, Cheng J-X. Bright three-photon luminescence from gold/silver alloyed nanostructures for nioimaging with negligible photothermal toxicity. Angew Chem Int Ed. 2010; 49: 3485-8.
41. Song KH, Kim C, Cobley CM, Xia Y, Wang LV. Near-infrared gold nanocages as a new class of tracers for photoacoustic sentinel lymph node mapping on a rat model. Nano Lett. 2009; 9: 183-8.
42. Kim C, Cho EC, Chen J, Song KH, Au L, Favazza C, et al. In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. ACS Nano. 2010; 4: 4559-64.
43. Rycenga M, Hou KK, Cobley CM, Schwartz AG, Camargo PHC, Xia Y. Probing the surface-enhanced Raman scattering properties of Au-Ag nanocages at two different excitation wavelengths. Phys Chem Chem Phys. 2009; 11: 5903-8.
44. Bulte JWM, Kraitchman DL, Mackay AM, Pittenger MF. Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood. 2004; 104: 3410-3.
45. Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T. Quantum dots versus organic dyes as fluorescent labels. Nat Methods. 2008; 5: 763-75.
46. Zipfel WR, Williams RM, Webb WW. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol. 2003; 21: 1369-77.
47. Wang LV. Multiscale photoacoustic microscopy and computed tomography. Nat Photon. 2009; 3: 503-9.
48. Cho EC, Kim C, Zhou F, Cobley CM, Song KH, Chen J, et al. Measuring the optical absorption cross sections of Au-Ag nanocages and Au nanorods by photoacoustic imaging. J Phys Chem C. 2009; 113: 9023-8.
49. Cho EC, Zhang Y, Cai X, Moran CH, Wang LV, Xia Y. A quantitative analysis of the fate of Au nanocages after uptake by U87-MG tumor cells under both in vitro and in vivo conditions. Angew Chem Int Ed; in press. DOI: 10.1002/anie.201208096.
50. Ku G, Wang LV. Deeply penetrating photoacoustic tomography in biological tissues enhancedwith an optical contrast agent. Opt Lett. 2005; 30: 507-9.
51. Kim C, Erpelding TN, Jankovic L, Pashley MD, Wang LV. Deeply penetrating in vivo photoacoustic imaging using a clinical ultrasound array system. Biomed Opt Express. 2010; 1: 278-84.
52. Zhang HF, Maslov K, Stoica G, Wang LV. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol. 2006; 24: 848-51.
53. Cai X, Zhang Y, Li L, Choi S-W, MacEwan MR, Yao J, et al. Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography. Tissue Eng C. 2013; 19: 196.
54. Yao J, Wang LV. Transverse flow imaging based on photoacoustic Doppler bandwidth broadening. J Biomed Opt. 2010; 15: 021304-5.
55. Zhang HF, Maslov K, Sivaramakrishnan M, Stoica G, Wang LV. Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy. Appl Phys Lett. 2007; 90: 053901.
56. Yao J, Maslov K, Zhang Y, Xia Y, Wang LV. Label-free oxygen-metabolic photoacoustic microscopy in vivo. J Biomed Opt. 2011; 16: 076003-11.
57. Zhang Y, Cai X, Wang Y, Zhang C, Li L, Choi S-W, et al. Noninvasive photoacoustic microscopy of living cells in two and three dimensions through enhancement by a metabolite dye. Angew Chem Int Ed. 2011; 50: 7359-63.