Aptamer technology for tracking cells’ status & function

  • Christian Wiraja 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • David Yeo 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • Daniel Lio 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • Louai Labanieh 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • Mengrou Lu 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • Weian Zhao 1Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
  • Chenjie Xu Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, 70 Nanyang Drive, Singapore 637457, Singapore
Keywords: Aptamer, Biosensor, Contrast agent, Cell tracking, Stem cells, Immune cells, Cancer cells

Abstract

In fields such as cancer biology and regenerative medicine, obtaining information regarding cell bio-distribution, tropism, status, and other cellular functions are highly desired. Understanding cancer behaviors including metastasis is important for developing effective cancer treatments, while assessing the fate of therapeutic cells following implantation is critical to validate the efficacy and efficiency of the therapy. For visualization purposes with medical imaging modalities (e.g. magnetic resonance imaging), cells can be labeled with contrast agents (e.g. iron-oxide nanoparticles), which allows their identification from the surrounding environment. Despite the success of revealing cell biodistribution in vivo, most of the existing agents do not provide information about the status and functions of cells following transplantation. The emergence of aptamers, single-stranded RNA or DNA oligonucleotides of 15 to 60 bases in length, is a promising solution to address this need. When aptamers bind specifically to their cognate molecules, they undergo conformational changes which can be transduced into a change of imaging contrast (e.g. optical, magnetic resonance). Thus by monitoring this signal change, researchers can obtain information about the expression of the target molecules (e.g. mRNA, surface markers, cell metabolites), which offer clues regarding cell status/function in a non-invasive manner. In this review, we summarize recent efforts to utilize aptamers as biosensors for monitoring the status and function of transplanted cells. We focus on cancer cell tracking for cancer study, stem cell tracking for regenerative medicine, and immune cell (e.g. dendritic cells) tracking for immune therapy.

Downloads

Download data is not yet available.

References

Daley GQ: The promise and perils of stem cell therapeutics. Cell Stem Cell. 2012, 10: 740-749.

PubMedCentralPubMedGoogle Scholar

Lindvall O, Kokaia Z: Stem cells in human neurodegenerative disorders—time for clinical translation?. J Clin Invest. 2010, 120: 29-40.

PubMedCentralPubMedGoogle Scholar

Reya T, Morrison SJ, Clarke MF, Weissman IL: Stem cells, cancer, and cancer stem cells. Nature. 2001, 414: 105-111.

PubMedGoogle Scholar

Wheeler DL, Dunn EF, Harari PM: Understanding resistance to EGFR inhibitors—impact on future treatment strategies. Nat Rev Clin Oncol. 2010, 7: 493-507.

PubMedCentralPubMedGoogle Scholar

Mundy GR: Metastasis: Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer. 2002, 2: 584-593.

PubMedGoogle Scholar

Ahrens ET, Bulte JW: Tracking immune cells in vivo using magnetic resonance imaging. Nat Rev Immunol. 2013, 13: 755-763.

PubMedGoogle Scholar

Bremer C, Ntziachristos V, Weissleder R: Optical-based molecular imaging: contrast agents and potential medical applications. Eur Radiol. 2003, 13: 231-243.

PubMedGoogle Scholar

Sevick-Muraca EM, Houston JP, Gurfinkel M: Fluorescence-enhanced, near infrared diagnostic imaging with contrast agents. Curr Opin Chem Biol. 2002, 6: 642-650.

PubMedGoogle Scholar

Antoch G, Freudenberg LS, Beyer T, Bockisch A, Debatin JF: To enhance or not to enhance? 18F-FDG and CT contrast agents in dual-modality 18F-FDG PET/CT. J Nucl Med. 2004, 45: 56S-65S.

PubMedGoogle Scholar

Delbeke D, Coleman RE, Guiberteau MJ, Brown ML, Royal HD, Siegel BA, Townsend DW, Berland LL, Parker JA, Hubner K: Procedure guideline for tumor imaging with 18F-FDG PET/CT 1.0. J Nucl Med. 2006, 47: 885-895.

PubMedGoogle Scholar

Xu C, Tung GA, Sun S: Size and concentration effect of gold nanoparticles on X-ray attenuation as measured on computed tomography. Chem Mater. 2008, 20: 4167-4169.

PubMedCentralPubMedGoogle Scholar

Caravan P, Ellison JJ, McMurry TJ, Lauffer RB: Gadolinium (III) chelates as MRI contrast agents: structure, dynamics, and applications. Chem Rev. 1999, 99: 2293-2352.

PubMedGoogle Scholar

Babes L, Denizot B, Tanguy G, Le Jeune JJ, Jallet P: Synthesis of iron oxide nanoparticles used as MRI contrast agents: a parametric study. J Colloid Interface Sci. 1999, 212: 474-482.

PubMedGoogle Scholar

Gao X, Yang L, Petros JA, Marshall FF: In vivo molecular and cellular imaging with quantum dots. Curr Opin Biotechnol. 2005, 16: 63-72.

PubMedGoogle Scholar

Pi QM, Zhang WJ, Zhou GD, Liu W, Cao Y: Degradation or excretion of quantum dots in mouse embryonic stem cells. BMC Biotechnol. 2010, 10: 36-

PubMedCentralPubMedGoogle Scholar

Gao Y, Cui Y, Chan JK, Xu C: Stem cell tracking with optically active nanoparticles. Am J Nucl Med Mol Imaging. 2013, 3: 232-

PubMedCentralPubMedGoogle Scholar

Tuerk C, Gold L: Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science. 1990, 249: 505-510.

PubMedGoogle Scholar

Ellington AD, Szostak JW: In vitro selection of RNA molecules that bind specific ligands. Nature. 1990, 346: 818-822.

PubMedGoogle Scholar

Huizenga DE, Szostak JW: A DNA aptamer that binds adenosine and ATP. Biochemistry. 1995, 34: 656-665.

PubMedGoogle Scholar

Radi A-E, O'Sullivan CK: Aptamer conformational switch as sensitive electrochemical biosensor for potassium ion recognition. Chem Commun. 2006, 32: 3432-3434.

Google Scholar

Liu J, Lu Y: Fast colorimetric sensing of adenosine and cocaine based on a general sensor design involving aptamers and nanoparticles. Angew Chem Int Ed Engl. 2006, 118: 96-100.

Google Scholar

Wei H, Li B, Li J, Wang E, Dong S: Simple and sensitive aptamer-based colorimetric sensing of protein using unmodified gold nanoparticle probes. Chem Commun. 2007, 36: 3735-3737.

Google Scholar

Huang C-C, Huang Y-F, Cao Z, Tan W, Chang H-T: Aptamer-modified gold nanoparticles for colorimetric determination of platelet-derived growth factors and their receptors. Anal Chem. 2005, 77: 5735-5741.

PubMedGoogle Scholar

Famulok M, Hartig JS, Mayer G: Functional aptamers and aptazymes in biotechnology, diagnostics, and therapy. Chem Rev. 2007, 107: 3715-3743.

PubMedGoogle Scholar

Stojanovic MN, De Prada P, Landry DW: Aptamer-based folding fluorescent sensor for cocaine. J Am Chem Soc. 2001, 123: 4928-4931.

PubMedGoogle Scholar

Liss M, Petersen B, Wolf H, Prohaska E: An aptamer-based quartz crystal protein biosensor. Anal Chem. 2002, 74: 4488-4495.

PubMedGoogle Scholar

McNamara JO, Andrechek ER, Wang Y, Viles KD, Rempel RE, Gilboa E, Sullenger BA, Giangrande PH: Cell type–specific delivery of siRNAs with aptamer-siRNA chimeras. Nat Biotechnol. 2006, 24: 1005-1015.

PubMedGoogle Scholar

Bagalkot V, Zhang L, Levy-Nissenbaum E, Jon S, Kantoff PW, Langer R, Farokhzad OC: Quantum dot-aptamer conjugates for synchronous cancer imaging, therapy, and sensing of drug delivery based on bi-fluorescence resonance energy transfer. Nano Lett. 2007, 7: 3065-3070.

PubMedGoogle Scholar

Wilson C, Szostak JW: Isolation of a fluorophore-specific DNA aptamer with weak redox activity. Chem Biol. 1998, 5: 609-617.

PubMedGoogle Scholar

Burmeister PE, Lewis SD, Silva RF, Preiss JR, Horwitz LR, Pendergrast PS, McCauley TG, Kurz JC, Epstein DM, Wilson C: Direct in vitro selection of a 2'-O-Methyl aptamer to VEGF. Chem Biol. 2005, 12: 25-33.

PubMedGoogle Scholar

Harding FA, Stickler MM, Razo J, DuBridge RB: The immunogenicity of humanized and fully human antibodies. Residual immunogenicity resides in the CDR regions. MAbs. 2010, 2: 256-265.

PubMedCentralPubMedGoogle Scholar

Shigdar S, Lin J, Yu Y, Pastuovic M, Wei M, Duan W: RNA aptamer against a cancer stem cell marker epithelial cell adhesion molecule. Cancer Sci. 2011, 102: 991-998.

PubMedGoogle Scholar

Ko HY, Lee JH, Kang H, Ryu SH, Song IC, Lee DS, Kim S: A nucleolin-targeted multimodal nanoparticle imaging probe for tracking cancer cells using an aptamer. J Nucl Med. 2010, 51: 98-105.

PubMedGoogle Scholar

Tang Z, Shangguan D, Wang K, Shi H, Sefah K, Mallikratchy P, Chen HW, Li Y, Tan W: Selection of aptamers for molecular recognition and characterization of cancer cells. Anal Chem. 2007, 79: 4900-4907.

PubMedGoogle Scholar

Iwagawa T, Ohuchi SP, Watanabe S, Nakamura Y: Selection of RNA aptamers against mouse embryonic stem cells. Biochimie. 2012, 94: 250-257.

PubMedGoogle Scholar

Meng L, Sefah K, Colon DL, Chen H, O’Donoghue M, Xiong X, Tan W: Using live cells to generate aptamers for cancer study. RNA Therapeutics. Volume 629. Edited by: Sioud M. 2010, Humana Press, 353-365. Methods in Molecular Biology

Google Scholar

Fang X, Tan W: Aptamers generated from cell-SELEX for molecular medicine: a chemical biology approach. Acc Chem Res. 2009, 43: 48-57.

Google Scholar

Sefah K, Shangguan D, Xiong X, O'Donoghue MB, Tan W: Development of DNA aptamers using Cell-SELEX. Nat Protoc. 2010, 5: 1169-1185.

PubMedGoogle Scholar

Meyer S, Maufort JP, Nie J, Stewart R, McIntosh BE, Conti LR, Ahmad KM, Soh HT, Thomson JA: Development of an efficient targeted Cell-SELEX procedure for DNA aptamer reagents. PLoS One. 2013, 8: e71798-

PubMedCentralPubMedGoogle Scholar

Shangguan D, Li Y, Tang Z, Cao ZC, Chen HW, Mallikaratchy P, Sefah K, Yang CJ, Tan W: Aptamers evolved from live cells as effective molecular probes for cancer study. Proc Natl Acad Sci. 2006, 103: 11838-11843.

PubMedCentralPubMedGoogle Scholar

Sefah K, Meng L, Lopez-Colon D, Jimenez E, Liu C, Tan W: DNA aptamers as molecular probes for colorectal cancer study. PLoS One. 2010, 5: e14269-

PubMedCentralPubMedGoogle Scholar

Wang AZ, Bagalkot V, Vasilliou CC, Gu F, Alexis F, Zhang L, Shaikh M, Yuet K, Cima MJ, Langer R: Superparamagnetic iron oxide nanoparticle–aptamer bioconjugates for combined prostate cancer imaging and therapy. ChemMedChem. 2008, 3: 1311-1315.

PubMedCentralPubMedGoogle Scholar

Estévez MC, Huang Y-F, Kang H, O’Donoghue MB, Bamrungsap S, Yan J, Chen X, Tan W: Nanoparticle–aptamer conjugates for cancer cell targeting and detection. Cancer Nanotechnology.Volume 624. Edited by: Grobmyer SR, Moudgil BM. 2010, Humana Press, 235-248. Methods in Molecular Biology

Google Scholar

Cerchia L, de Franciscis V: Targeting cancer cells with nucleic acid aptamers. Trends Biotechnol. 2010, 28: 517-525.

PubMedGoogle Scholar

Zueva E, Rubio LI, Ducongé F, Tavitian B: Metastasis-focused cell-based SELEX generates aptamers inhibiting cell migration and invasion. Int J Cancer. 2011, 128: 797-804.

PubMedGoogle Scholar

Coussens LM, Tinkle CL, Hanahan D, Werb Z: MMP-9 supplied by bone marrow–derived cells contributes to skin carcinogenesis. Cell. 2000, 103: 481-490.

PubMedCentralPubMedGoogle Scholar

Lee FY, Borzilleri R, Fairchild CR, Kim S-H, Long BH, Reventos-Suarez C, Vite GD, Rose WC, Kramer RA: BMS-247550 a novel epothilone analog with a mode of action similar to paclitaxel but possessing superior antitumor efficacy. Clin Cancer Res. 2001, 7: 1429-1437.

PubMedGoogle Scholar

PLAXCO KW, Tom Soh H: Switch-based biosensors: a new approach towards real-time, in vivo molecular detection. Trends Biotechnol. 2011, 29: 1-5.

PubMedCentralPubMedGoogle Scholar

Shi H, Tang Z, Kim Y, Nie H, Huang YF, He X, Deng K, Wang K, Tan W: In vivo fluorescence imaging of tumors using molecular aptamers generated by cell-SELEX. Cancer. 2010, 23: 24-

Google Scholar

Zhao W, Schafer S, Choi J, Yamanaka YJ, Lombardi ML, Bose S, Carlson AL, Phillips JA, Teo W, Droujinine IA: Cell-surface sensors for real-time probing of cellular environments. Nat Nanotechnol. 2011, 6: 524-531.

PubMedCentralPubMedGoogle Scholar

Ntziachristos V, Ripoll J, Wang LV, Weissleder R: Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol. 2005, 23: 313-320.

PubMedGoogle Scholar

Kedrin D, Gligorijevic B, Wyckoff J, Verkhusha VV, Condeelis J, Segall JE, van Rheenen J: Intravital imaging of metastatic behavior through a mammary imaging window. Nat Methods. 2008, 5: 1019-

PubMedCentralPubMedGoogle Scholar

Alexander S, Koehl GE, Hirschberg M, Geissler EK, Friedl P: Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem Cell Biol. 2008, 130: 1147-1154.

PubMedGoogle Scholar

Savla R, Taratula O, Garbuzenko O, Minko T: Tumor targeted quantum dot-mucin 1 aptamer-doxorubicin conjugate for imaging and treatment of cancer. J Control Release. 2011, 153: 16-22.

PubMedGoogle Scholar

Shi H, He X, Wang K, Wu X, Ye X, Guo Q, Tan W, Qing Z, Yang X, Zhou B: Activatable aptamer probe for contrast-enhanced in vivo cancer imaging based on cell membrane protein-triggered conformation alteration. Proc Natl Acad Sci. 2011, 108: 3900-3905.

PubMedCentralPubMedGoogle Scholar

Kang WJ, Chae JR, Cho YL, Lee JD, Kim S: Multiplex imaging of single tumor cells using quantum-dot-conjugated aptamers. Small. 2009, 5: 2519-2522.

PubMedGoogle Scholar

Chen X, Estévez M-C, Zhu Z, Huang Y-F, Chen Y, Wang L, Tan W: Using aptamer-conjugated fluorescence resonance energy transfer nanoparticles for multiplexed cancer cell monitoring. Anal Chem. 2009, 81: 7009-7014.

PubMedGoogle Scholar

Charlton J, Sennello J, Smith D: In vivo imaging of inflammation using an aptamer inhibitor of human neutrophil elastase. Chem Biol. 1997, 4: 809-

PubMedGoogle Scholar

Hicke BJ, Stephens AW, Gould T, Chang Y-F, Lynott CK, Heil J, Borkowski S, Hilger C-S, Cook G, Warren S: Tumor targeting by an aptamer. J Nucl Med. 2006, 47: 668-678.

PubMedGoogle Scholar

Pieve C, Perkins A, Missailidis S: Anti-MUC1 aptamers: radiolabelling with (99m) Tc and biodistribution in MCF-7 tumour-bearing mice. Nucl Med Biol. 2009, 36: 703-710.

PubMedGoogle Scholar

Rockey WM, Huang L, Kloepping KC, Baumhover NJ, Giangrande PH, Schultz MK: Synthesis and radiolabeling of chelator–RNA aptamer bioconjugates with copper-64 for targeted molecular imaging. Bioorg Med Chem. 2011, 19: 4080-4090.

PubMedCentralPubMedGoogle Scholar

Hainfeld J, Slatkin D, Focella T, Smilowitz H: Gold nanoparticles: a new X-ray contrast agent. 2014

Google Scholar

Kim D, Park S, Lee JH, Jeong YY, Jon S: Antibiofouling polymer-coated gold nanoparticles as a contrast agent for in vivo X-ray computed tomography imaging. J Am Chem Soc. 2007, 129: 7661-7665.

PubMedGoogle Scholar

Kim D, Jeong YY, Jon S: A drug-loaded aptamer- gold nanoparticle bioconjugate for combined CT imaging and therapy of prostate cancer. ACS Nano. 2010, 4: 3689-3696.

PubMedGoogle Scholar

Jalalian SH, Taghdisi SM, Shahidi Hamedani N, Kalat SAM, Lavaee P, ZandKarimi M, Ghows N, Jaafari MR, Naghibi S, Danesh NM: Epirubicin loaded super paramagnetic iron oxide nanoparticle-aptamer bioconjugate for combined colon cancer therapy and imaging in vivo. Eur J Pharm Sci. 2013, 50: 191-197.

PubMedGoogle Scholar

Chi-hong BC, Dellamaggiore KR, Ouellette CP, Sedano CD, Lizadjohry M, Chernis GA, Gonzales M, Baltasar FE, Fan AL, Myerowitz R: Aptamer-based endocytosis of a lysosomal enzyme. Proc Natl Acad Sci. 2008, 105: 15908-15913.

Google Scholar

Li N, Larson T, Nguyen HH, Sokolov KV, Ellington AD: Directed evolution of gold nanoparticle delivery to cells. Chem Commun. 2010, 46: 392-394.

Google Scholar

Meyer C, Eydeler K, Magbanua E, Zivkovic T, Piganeau N, Lorenzen I, Grötzinger J, Mayer G, Rose-John S, Hahn U: Interleukin-6 receptor specific RNA aptamers for cargo delivery into target cells. RNA Biol. 2012, 9: 67-80.

PubMedCentralPubMedGoogle Scholar

Xiao Z, Shangguan D, Cao Z, Fang X, Tan W: Cell-specific internalization study of an aptamer from whole cell selection. Chem-A Eur J. 2008, 14: 1769-1775.

Google Scholar

Nicholson R, Gee J, Harper M: EGFR and cancer prognosis. Eur J Cancer. 2001, 37: 9-15.

Google Scholar

Kruspe S, Meyer C, Hahn U: Chlorin e6 conjugated interleukin-6 receptor aptamers selectively kill target cells upon irradiation. Mol Ther Nucleic Acids. 2014, 3: e143-

PubMedCentralPubMedGoogle Scholar

Huang YF, Shangguan D, Liu H, Phillips JA, Zhang X, Chen Y, Tan W: Molecular assembly of an aptamer–drug conjugate for targeted drug delivery to tumor cells. ChemBioChem. 2009, 10: 862-868.

PubMedCentralPubMedGoogle Scholar

Caplan AI: Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007, 213: 341-347.

PubMedGoogle Scholar

Griffith LG, Naughton G: Tissue engineering–current challenges and expanding opportunities. Science. 2002, 295: 1009-1014.

PubMedGoogle Scholar

Bianco P, Robey PG: Stem cells in tissue engineering. Nature. 2001, 414: 118-121.

PubMedGoogle Scholar

Phinney DG, Prockop DJ: Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views. Stem Cells. 2007, 25: 2896-2902.

PubMedGoogle Scholar

Aggarwal S, Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005, 105: 1815-1822.

PubMedGoogle Scholar

Ringdén O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lönnies H, Marschall H-U, Dlugosz A, Szakos A, Hassan Z: Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006, 81: 1390-1397.

PubMedGoogle Scholar

Ryan JM, Barry FP, Murphy JM, Mahon BP: Mesenchymal stem cells avoid allogeneic rejection. J Inflamm. 2005, 2: 8-

Google Scholar

Zhu Y, Sun Z, Han Q, Liao L, Wang J, Bian C, Li J, Yan X, Liu Y, Shao C: Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia. 2009, 23: 925-933.

PubMedGoogle Scholar

Ramasamy R, Lam EW, Soeiro I, Tisato V, Bonnet D, Dazzi F: Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia. 2006, 21: 304-310.

PubMedGoogle Scholar

Guo KT, SchÄfer R, Paul A, Gerber A, Ziemer G, Wendel HP: A new technique for the isolation and surface immobilization of mesenchymal stem cells from whole bone marrow using high-specific DNA aptamers. Stem Cells. 2006, 24: 2220-2231.

PubMedGoogle Scholar

Schäfer R, Wiskirchen J, Guo K, Neumann B, Kehlbach R, Pintaske J, Voth V, Walker T, Scheule A, Greiner T: Aptamer-based isolation and subsequent imaging of mesenchymal stem cells in ischemic myocard by magnetic resonance imaging. RöFo-Fortschritte auf dem Gebiet der Röntgenstrahlen und der bildgebenden Verfahren. 2007, New York: © Georg Thieme Verlag KG Stuttgart, 1009-1015.

Google Scholar

Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, Herault O, Charbord P, Domenech J: The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells. 2007, 25: 1737-1745.

PubMedGoogle Scholar

Ball SG, Shuttleworth CA, Kielty CM: Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med. 2007, 11: 1012-1030.

PubMedCentralPubMedGoogle Scholar

Vicens MC, Sen A, Vanderlaan A, Drake TJ, Tan W: Investigation of molecular beacon aptamer-based bioassay for platelet-derived growth factor detection. ChemBioChem. 2005, 6: 900-907.

PubMedGoogle Scholar

Fang X, Sen A, Vicens M, Tan W: Synthetic DNA aptamers to detect protein molecular variants in a high-throughput fluorescence quenching assay. ChemBioChem. 2003, 4: 829-834.

PubMedGoogle Scholar

Mellman I, Steinman RM: Dendritic cells-specialized and regulated antigen processing machines. Cell. 2001, 106: 255-258.

PubMedGoogle Scholar

Cella M, Sallusto F, Lanzavecchia A: Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol. 1997, 9: 10-16.

PubMedGoogle Scholar

Banchereau J, Steinman RM: Dendritic cells and the control of immunity. Nature. 1998, 392: 245-252.

PubMedGoogle Scholar

Fong L, Engleman EG: Dendritic cells in cancer immunotherapy. Annu Rev Immunol. 2000, 18: 245-273.

PubMedGoogle Scholar

Figdor CG, de Vries IJM, Lesterhuis WJ, Melief CJ: Dendritic cell immunotherapy: mapping the way. Nat Med. 2004, 10: 475-480.

PubMedGoogle Scholar

Lutz MB, Schuler G: Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity?. Trends Immunol. 2002, 23: 445-449.

PubMedGoogle Scholar

Horan PK, Melnicoff MJ, Jensen BD, Slezak SE: Fluorescent cell labeling for in vivo and in vitro cell tracking. Methods Cell Biol. 1990, 33: 469-490.

PubMedGoogle Scholar

Edinger M, Cao Y-A, Verneris MR, Bachmann MH, Contag CH, Negrin RS: Revealing lymphoma growth and the efficacy of immune cell therapies using in vivo bioluminescence imaging. Blood. 2003, 101: 640-648.

PubMedGoogle Scholar

Berezovski MV, Lechmann M, Musheev MU, Mak TW, Krylov SN: Aptamer-facilitated biomarker discovery (AptaBiD). J Am Chem Soc. 2008, 130: 9137-9143.

PubMedGoogle Scholar

Hui Y, Shan L, Lin-fu Z, Jian-hua Z: Selection of DNA aptamers against DC-SIGN protein. Mol Cell Biochem. 2007, 306: 71-77.

PubMedGoogle Scholar

van Kooyk Y, Geijtenbeek TB: DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol. 2003, 3: 697-709.

PubMedGoogle Scholar

Wengerter BC, Katakowski JA, Rosenberg JM, Park CG, Almo SC, Palliser D, Levy M: Aptamer-targeted antigen delivery. Mol Ther. 2014, 22 (7): 1375-1387.

PubMedCentralPubMedGoogle Scholar

McNamara JO, Kolonias D, Pastor F, Mittler RS, Chen L, Giangrande PH, Sullenger B, Gilboa E: Multivalent 4-1BB binding aptamers costimulate CD8+ T cells and inhibit tumor growth in mice. J Clin Invest. 2008, 118: 376-

PubMedCentralPubMedGoogle Scholar

Dollins CM, Nair S, Boczkowski D, Lee J, Layzer JM, Gilboa E, Sullenger BA: Assembling OX40 aptamers on a molecular scaffold to create a receptor-activating aptamer. Chem Biol. 2008, 15: 675-682.

PubMedCentralPubMedGoogle Scholar

Santulli-Marotto S, Nair SK, Rusconi C, Sullenger B, Gilboa E: Multivalent RNA aptamers that inhibit CTLA-4 and enhance tumor immunity. Cancer Res. 2003, 63: 7483-7489.

PubMedGoogle Scholar

Syed MA, Pervaiz S: Advances in aptamers. Oligonucleotides. 2010, 20: 215-224.

PubMedGoogle Scholar

Keefe AD, Pai S, Ellington A: Aptamers as therapeutics. Nat Rev Drug Discov. 2010, 9: 537-550.

PubMedGoogle Scholar

Pestourie C, Tavitian B, Duconge F: Aptamers against extracellular targets for in vivo applications. Biochimie. 2005, 87: 921-930.

PubMedGoogle Scholar

Younes C, Boisgard R, Tavitian B: Labelled oligonucleotides as radiopharmaceuticals: pitfalls, problems and perspectives. Curr Pharm Des. 2002, 8: 1451-1466.

PubMedGoogle Scholar

Nam SY, Ricles LM, Suggs LJ, Emelianov SY: In vivo ultrasound and photoacoustic monitoring of mesenchymal stem cells labeled with gold nanotracers. PLoS One. 2012, 7: e37267-

PubMedCentralPubMedGoogle Scholar

Wang H, Cao F, De A, Cao Y, Contag C, Gambhir SS, Wu JC, Chen X: Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells. 2009, 27: 1548-1558.

PubMedCentralPubMedGoogle Scholar

Wullner U, Neef I, Eller A, Kleines M, Tur MK, Barth S: Cell-specific induction of apoptosis by rationally designed bivalent aptamer-siRNA transcripts silencing eukaryotic elongation factor 2. Curr Cancer Drug Targets. 2008, 8: 554-565.

PubMedGoogle Scholar

Chu TC, Twu KY, Ellington AD, Levy M: Aptamer mediated siRNA delivery. Nucleic Acids Res. 2006, 34: e73-

PubMedCentralPubMedGoogle Scholar

Tucker CE, Chen L-S, Judkins MB, Farmer JA, Gill SC, Drolet DW: Detection and plasma pharmacokinetics of an anti-vascular endothelial growth factor oligonucleotide-aptamer (NX1838) in rhesus monkeys. J Chromatogr B Biomed Sci Appl. 1999, 732: 203-212.

PubMedGoogle Scholar

Keefe AD, Cload ST: SELEX with modified nucleotides. Curr Opin Chem Biol. 2008, 12: 448-456.

PubMedGoogle Scholar

Famulok M, Mayer G, Blind M: Nucleic acid aptamers from selection in vitro to applications in vivo. Acc Chem Res. 2000, 33: 591-599.

PubMedGoogle Scholar

Shangguan D, Cao ZC, Li Y, Tan W: Aptamers evolved from cultured cancer cells reveal molecular differences of cancer cells in patient samples. Clin Chem. 2007, 53: 1153-1155.

PubMedGoogle Scholar

Xiao Z, Farokhzad OC: Aptamer-functionalized nanoparticles for medical applications: challenges and opportunities. ACS Nano. 2012, 6: 3670-3676.

PubMedCentralPubMedGoogle Scholar

Schmidt KS, Borkowski S, Kurreck J, Stephens AW, Bald R, Hecht M, Friebe M, Dinkelborg L, Erdmann VA: Application of locked nucleic acids to improve aptamer in vivo stability and targeting function. Nucleic Acids Res. 2004, 32: 5757-5765.

PubMedCentralPubMedGoogle Scholar

Mi J, Liu Y, Rabbani ZN, Yang Z, Urban JH, Sullenger BA, Clary BM: In vivo selection of tumor-targeting RNA motifs. Nat Chem Biol. 2010, 6: 22-24.

PubMedCentralPubMedGoogle Scholar

Cheng C, Chen YH, Lennox KA, Behlke MA, Davidson BL: In vivo SELEX for Identification of Brain-penetrating Aptamers. Mol Ther Nucleic Acids. 2013, 2: e67-

PubMedCentralPubMedGoogle Scholar

Cerchia L, Ducongé F, Pestourie C, Boulay J, Aissouni Y, Gombert K, Tavitian B, de Franciscis V, Libri D: Neutralizing aptamers from whole-cell SELEX inhibit the RET receptor tyrosine kinase. PLoS Biol. 2005, 3: e123-

PubMedCentralPubMedGoogle Scholar

Yoo H, Jung H, Kim SA, Mok H: Multivalent comb-type aptamer–siRNA conjugates for efficient and selective intracellular delivery. Chem Commun. 2014, 50: 6765-6767.

Google Scholar

Li W-M, Bing T, Wei J-Y, Chen Z-Z, Shangguan D-H, Fang J: Cell-SELEX-based selection of aptamers that recognize distinct targets on metastatic colorectal cancer cells. Biomaterials. 2014, 35: 6998-7007.

PubMedGoogle Scholar

O'Sullivan CK: Aptasensors–the future of biosensing?. Anal Bioanal Chem. 2002, 372: 44-48.

PubMedGoogle Scholar

El-Sagheer AH, Brown T: New strategy for the synthesis of chemically modified RNA constructs exemplified by hairpin and hammerhead ribozymes. Proc Natl Acad Sci. 2010, 107: 15329-15334.

PubMedCentralPubMedGoogle Scholar

Brody EN, Gold L: Aptamers as therapeutic and diagnostic agents. Rev Mol Biotechnol. 2000, 74: 5-13.

Google Scholar

Vater A, Jarosch F, Buchner K, Klussmann S: Short bioactive Spiegelmers to migraine-associated calcitonin gene-related peptide rapidly identified by a novel approach: Tailored-SELEX. Nucleic Acids Res. 2003, 31: e130-

PubMedCentralPubMedGoogle Scholar

Porciani D, Signore G, Marchetti L, Mereghetti P, Nifosì R, Beltram F: Two interconvertible folds modulate the activity of a DNA aptamer against transferrin receptor. Mol Ther Nucleic Acids. 2014, 3: e144-

PubMedCentralPubMedGoogle Scholar

White RR, Sullenger BA, Rusconi CP: Developing aptamers into therapeutics. J Clin Investig. 2000, 106: 929-934.

PubMedCentralPubMedGoogle Scholar

Zhou J, Rossi JJ: Aptamer-targeted cell-specific RNA interference. Silence. 2010, 1: 4-

PubMedCentralPubMedGoogle Scholar

Bouchard P, Hutabarat R, Thompson K: Discovery and development of therapeutic aptamers. Annu Rev Pharmacol Toxicol. 2010, 50: 237-257.

PubMedGoogle Scholar

Zhou J, Rossi JJ: Cell-type-specific, aptamer-functionalized agents for targeted disease therapy. Mol Ther Nucleic Acids. 2014, 3: e169-

PubMedCentralPubMedGoogle Scholar

White RR, Shan S, Rusconi CP, Shetty G, Dewhirst MW, Kontos CD, Sullenger BA: Inhibition of rat corneal angiogenesis by a nuclease-resistant RNA aptamer specific for angiopoietin-2. Proc Natl Acad Sci. 2003, 100: 5028-5033.

PubMedCentralPubMedGoogle Scholar

Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae S-K, Kittappa R, McKay RD: Notch signalling regulates stem cell numbers in vitro and in vivo. Nature. 2006, 442: 823-826.

PubMedGoogle Scholar

Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA: Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002, 109: 625-637.

PubMedCentralPubMedGoogle Scholar

Gnecchi M, Zhang Z, Ni A, Dzau VJ: Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008, 103: 1204-1219.

PubMedCentralPubMedGoogle Scholar

Crisostomo PR, Wang Y, Markel TA, Wang M, Lahm T, Meldrum DR: Human mesenchymal stem cells stimulated by TNF-α, LPS, or hypoxia produce growth factors by an NFκB-but not JNK-dependent mechanism. Am J Physiol Regul Integr Comp Physiol. 2008, 294: C675-C682.

Google Scholar

Gabrilovich DI, Chen HL, Girgis KR, Cunningham HT, Meny GM, Nadaf S, Kavanaugh D, Carbone DP: Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med. 1996, 2: 1096-1103.

PubMedGoogle Scholar

Lee AS, Tang C, Rao MS, Weissman IL, Wu JC: Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med. 2013, 19: 998-1004.

PubMedCentralPubMedGoogle Scholar

Phinney DG: Functional heterogeneity of mesenchymal stem cells: implications for cell therapy. J Cell Biochem. 2012, 113: 2806-2812.

PubMedGoogle Scholar

Published
2014-10-27
Section
Review