Iranian Journal of Radiology

Published by: Kowsar

In Vivo Tracking of Mesenchymal Stem Cell in Rat Genitalia with Erectile Dysfunction Labeled by Superparamagnetic Iron Oxide Using Magnetic Resonance Imaging and Its Therapeutic Effect

Kyung Taek Oh 1 , Ngoc Ha Hoang 2 , So-Young Park 3 , Eun Seong Lee 4 , Jang Hwan Kim 5 and Young Taik Oh 6 , *
Authors Information
1 College of Pharmacy, Chung-Ang University, Dongjak-Gu, Seoul, Republic of Korea
2 Department of Pharmaceutics, Hanoi University of Pharmacy, Hanoi, Vietnam
3 Laboratory of Pharmacognosy, College of Pharmacy, Dankook University, Dongnam-Gu, Cheonan, Republic of Korea
4 Division of Biotechnology, The Catholic University of Korea, Wonmi-gu, Bucheon-si, Republic of Korea
5 Department of Urology, College of Medicine, Yonsei University, Seoul, Republic of Korea
6 Department of Radiology and Research Institute of Radiological Science, College of Medicine, Yonsei University, Seodaemun-gu, Seoul, Republic of Korea
Article information
  • Iranian Journal of Radiology: July 2018, 15 (3); e56003
  • Published Online: May 20, 2018
  • Article Type: Research Article
  • Received: June 23, 2017
  • Revised: December 27, 2017
  • Accepted: January 2, 2018
  • DOI: 10.5812/iranjradiol.56003

To Cite: Taek Oh K, Ha Hoang N, Park S, Seong Lee E, Hwan Kim J, et al. In Vivo Tracking of Mesenchymal Stem Cell in Rat Genitalia with Erectile Dysfunction Labeled by Superparamagnetic Iron Oxide Using Magnetic Resonance Imaging and Its Therapeutic Effect, Iran J Radiol. 2018 ; 15(3):e56003. doi: 10.5812/iranjradiol.56003.

Copyright © 2018, Iranian Journal of Radiology. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited
1. Background
2. Objectives
3. Materials and Methods
4. Results
5. Discussion
  • 1. Kircher MF, Gambhir SS, Grimm J. Noninvasive cell-tracking methods. Nat Rev Clin Oncol. 2011;8(11):677-88. doi: 10.1038/nrclinonc.2011.141. [PubMed: 21946842].
  • 2. Reagan MR, Kaplan DL. Concise review: Mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem Cells. 2011;29(6):920-7. doi: 10.1002/stem.645. [PubMed: 21557390]. [PubMed Central: PMC4581846].
  • 3. 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(5). e37267. doi: 10.1371/journal.pone.0037267. [PubMed: 22615959]. [PubMed Central: PMC3353925].
  • 4. Tornblom M, Eriksson H, Franzen S, Gustafsson O, Lilja H, Norming U, et al. Lead time associated with screening for prostate cancer. Int J Cancer. 2004;108(1):122-9. doi: 10.1002/ijc.11554. [PubMed: 14618626].
  • 5. Terreno E, Castelli DD, Viale A, Aime S. Challenges for molecular magnetic resonance imaging. Chem Rev. 2010;110(5):3019-42. doi: 10.1021/cr100025t. [PubMed: 20415475].
  • 6. Pysz MA, Gambhir SS, Willmann JK. Molecular imaging: current status and emerging strategies. Clin Radiol. 2010;65(7):500-16. doi: 10.1016/j.crad.2010.03.011. [PubMed: 20541650]. [PubMed Central: PMC3150531].
  • 7. 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(5):3112-45. doi: 10.1021/cr900351r. [PubMed: 20415479].
  • 8. Kircher MF, de la Zerda A, Jokerst JV, Zavaleta CL, Kempen PJ, Mittra E, et al. A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle. Nat Med. 2012;18(5):829-34. doi: 10.1038/nm.2721. [PubMed: 22504484]. [PubMed Central: PMC3422133].
  • 9. Tassa C, Shaw SY, Weissleder R. Dextran-coated iron oxide nanoparticles: a versatile platform for targeted molecular imaging, molecular diagnostics, and therapy. Acc Chem Res. 2011;44(10):842-52. doi: 10.1021/ar200084x. [PubMed: 21661727]. [PubMed Central: PMC3182289].
  • 10. Jokerst JV, Gambhir SS. Molecular imaging with theranostic nanoparticles. Acc Chem Res. 2011;44(10):1050-60. doi: 10.1021/ar200106e. [PubMed: 21919457]. [PubMed Central: PMC3196845].
  • 11. Cho EC, Glaus C, Chen J, Welch MJ, Xia Y. Inorganic nanoparticle-based contrast agents for molecular imaging. Trends Mol Med. 2010;16(12):561-73. doi: 10.1016/j.molmed.2010.09.004. [PubMed: 21074494]. [PubMed Central: PMC3052982].
  • 12. Arifin DR, Long CM, Gilad AA, Alric C, Roux S, Tillement O, et al. Trimodal gadolinium-gold microcapsules containing pancreatic islet cells restore normoglycemia in diabetic mice and can be tracked by using US, CT, and positive-contrast MR imaging. Radiology. 2011;260(3):790-8. doi: 10.1148/radiol.11101608. [PubMed: 21734156]. [PubMed Central: PMC3157003].
  • 13. Kim T, Momin E, Choi J, Yuan K, Zaidi H, Kim J, et al. Mesoporous silica-coated hollow manganese oxide nanoparticles as positive T1 contrast agents for labeling and MRI tracking of adipose-derived mesenchymal stem cells. J Am Chem Soc. 2011;133(9):2955-61. doi: 10.1021/ja1084095. [PubMed: 21314118]. [PubMed Central: PMC3048840].
  • 14. Yang J, Lim EK, Lee ES, Suh JS, Haam S, Huh YM. Magnetoplex based on MnFe2O4 nanocrystals for magnetic labeling and MR imaging of human mesenchymal stem cells. J Nanoparticle Res. 2010;12(4):1275-83. doi: 10.1007/s11051-009-9837-1.
  • 15. Cromer Berman SM, Walczak P, Bulte JW. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011;3(4):343-55. doi: 10.1002/wnan.140. [PubMed: 21472999]. [PubMed Central: PMC3193153].
  • 16. Ahrens ET, Bulte JW. Tracking immune cells in vivo using magnetic resonance imaging. Nat Rev Immunol. 2013;13(10):755-63. doi: 10.1038/nri3531. [PubMed: 24013185]. [PubMed Central: PMC3886235].
  • 17. Liu G, Wang Z, Lu J, Xia C, Gao F, Gong Q, et al. Low molecular weight alkyl-polycation wrapped magnetite nanoparticle clusters as MRI probes for stem cell labeling and in vivo imaging. Biomaterials. 2011;32(2):528-37. doi: 10.1016/j.biomaterials.2010.08.099. [PubMed: 20869767].
  • 18. Engel J, Bastian PJ, Baur H, Beer V, Chaussy C, Gschwend JE, et al. Survival benefit of radical prostatectomy in lymph node-positive patients with prostate cancer. Eur Urol. 2010;57(5):754-61. doi: 10.1016/j.eururo.2009.12.034. [PubMed: 20106588].
  • 19. Ward JF, Slezak JM, Blute ML, Bergstralh EJ, Zincke H. Radical prostatectomy for clinically advanced (cT3) prostate cancer since the advent of prostate-specific antigen testing: 15-year outcome. BJU Int. 2005;95(6):751-6. doi: 10.1111/j.1464-410X.2005.05394.x. [PubMed: 15794776].
  • 20. Walsh PC, Lepor H, Eggleston JC. Radical prostatectomy with preservation of sexual function: anatomical and pathological considerations. Prostate. 1983;4(5):473-85. [PubMed: 6889192].
  • 21. Quinlan DM, Epstein JI, Carter BS, Walsh PC. Sexual function following radical prostatectomy: influence of preservation of neurovascular bundles. J Urol. 1991;145(5):998-1002. [PubMed: 2016818].
  • 22. Bochinski D, Lin GT, Nunes L, Carrion R, Rahman N, Lin CS, et al. The effect of neural embryonic stem cell therapy in a rat model of cavernosal nerve injury. BJU Int. 2004;94(6):904-9. doi: 10.1111/j.1464-410X.2003.05057.x. [PubMed: 15476533].
  • 23. Arbab AS, Yocum GT, Kalish H, Jordan EK, Anderson SA, Khakoo AY, et al. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood. 2004;104(4):1217-23. doi: 10.1182/blood-2004-02-0655. [PubMed: 15100158].
  • 24. Arbab AS, Yocum GT, Wilson LB, Parwana A, Jordan EK, Kalish H, et al. Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability. Mol Imaging. 2004;3(1):24-32. doi: 10.1162/153535004773861697. [PubMed: 15142409].
  • 25. Caplan AI. Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng. 2005;11(7-8):1198-211. doi: 10.1089/ten.2005.11.1198. [PubMed: 16144456].
  • 26. Sheikh AY, Wu JC. Molecular imaging of cardiac stem cell transplantation. Curr Cardiol Rep. 2006;8(2):147-54. [PubMed: 16524542].
  • 27. Zhang T, Stilwell JL, Gerion D, Ding L, Elboudwarej O, Cooke PA, et al. Cellular effect of high doses of silica-coated quantum dot profiled with high throughput gene expression analysis and high content cellomics measurements. Nano Lett. 2006;6(4):800-8. doi: 10.1021/nl0603350. [PubMed: 16608287]. [PubMed Central: PMC2730586].
  • 28. Sun C, Lee JS, Zhang M. Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev. 2008;60(11):1252-65. doi: 10.1016/j.addr.2008.03.018. [PubMed: 18558452]. [PubMed Central: PMC2702670].
  • 29. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JW, Frank JA. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation. 2003;76(7):1123-30. doi: 10.1097/01.TP.0000089237.39220.83. [PubMed: 14557764].
  • 30. 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(18):4515-25. doi: 10.1016/j.biomaterials.2012.02.064. [PubMed: 22445482].
  • 31. Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, Lewis BK, et al. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology. 2003;228(2):480-7. doi: 10.1148/radiol.2281020638. [PubMed: 12819345].
  • 32. Arbab AS, Liu W, Frank JA. Cellular magnetic resonance imaging: current status and future prospects. Expert Rev Med Devices. 2006;3(4):427-39. doi: 10.1586/17434440.3.4.427. [PubMed: 16866640].
  • 33. Miralles-Garcia JM, Garcia-Diez LC. Specific aspects of erectile dysfunction in endocrinology. Int J Impot Res. 2004;16 Suppl 2:S10-2. doi: 10.1038/sj.ijir.3901237. [PubMed: 15496851].
  • 34. Sainz I, Amaya J, Garcia M. Erectile dysfunction in heart disease patients. Int J Impot Res. 2004;16 Suppl 2:S13-7. doi: 10.1038/sj.ijir.3901238. [PubMed: 15496852].
  • 35. Iacono F, Giannella R, Somma P, Manno G, Fusco F, Mirone V. Histological alterations in cavernous tissue after radical prostatectomy. J Urol. 2005;173(5):1673-6. doi: 10.1097/01.ju.0000154356.76027.4f. [PubMed: 15821546].
  • 36. Walsh PC, Donker PJ. Impotence following radical prostatectomy: insight into etiology and prevention. 1982. J Urol. 2002;167(2 Pt 2):1005-10. [PubMed: 11905870].
  • 37. Carson CC, Lue TF. Phosphodiesterase type 5 inhibitors for erectile dysfunction. BJU Int. 2005;96(3):257-80. doi: 10.1111/j.1464-410X.2005.05614.x. [PubMed: 16042713].
  • 38. Manecke RG, Mulhall JP. Medical treatment of erectile dysfunction. Ann Med. 1999;31(6):388-98. [PubMed: 10680853].
  • 39. Song YS, Lee HJ, Park IH, Kim WK, Ku JH, Kim SU. Potential differentiation of human mesenchymal stem cell transplanted in rat corpus cavernosum toward endothelial or smooth muscle cells. Int J Impot Res. 2007;19(4):378-85. doi: 10.1038/sj.ijir.3901539. [PubMed: 17460699].
  • 40. Song H, Chang W, Lim S, Seo HS, Shim CY, Park S, et al. Tissue transglutaminase is essential for integrin-mediated survival of bone marrow-derived mesenchymal stem cells. Stem Cells. 2007;25(6):1431-8. doi: 10.1634/stemcells.2006-0467. [PubMed: 17347495].
  • 41. Wang YX, Hussain SM, Krestin GP. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur Radiol. 2001;11(11):2319-31. doi: 10.1007/s003300100908. [PubMed: 11702180].
  • 42. Bivalacqua TJ, Deng W, Kendirci M, Usta MF, Robinson C, Taylor BK, et al. Mesenchymal stem cells alone or ex vivo gene modified with endothelial nitric oxide synthase reverse age-associated erectile dysfunction. Am J Physiol Heart Circ Physiol. 2007;292(3):H1278-90. doi: 10.1152/ajpheart.00685.2006. [PubMed: 17071732].
  • 43. Postlethwaite AE, Keski-Oja J, Moses HL, Kang AH. Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J Exp Med. 1987;165(1):251-6. [PubMed: 3491869]. [PubMed Central: PMC2188256].
  • 44. Laping NJ, Grygielko E, Mathur A, Butter S, Bomberger J, Tweed C, et al. Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol. 2002;62(1):58-64. [PubMed: 12065755].
  • 45. Moreland RB, Traish A, McMillin MA, Smith B, Goldstein I, Saenz de Tejada I. PGE1 suppresses the induction of collagen synthesis by transforming growth factor-beta 1 in human corpus cavernosum smooth muscle. J Urol. 1995;153(3 Pt 1):826-34. [PubMed: 7861547].
  • 46. Moreland RB. Is there a role of hypoxemia in penile fibrosis: a viewpoint presented to the Society for the Study of Impotence. Int J Impot Res. 1998;10(2):113-20. [PubMed: 9647948].
  • 47. Ryu JK, Song SU, Choi HK, Seong DH, Yoon SM, Kim SJ, et al. Plasma transforming growth factor-beta1 levels in patients with erectile dysfunction. Asian J Androl. 2004;6(4):349-53. [PubMed: 15546028].
  • 48. Leungwattanakij S, Bivalacqua TJ, Usta MF, Yang DY, Hyun JS, Champion HC, et al. Cavernous neurotomy causes hypoxia and fibrosis in rat corpus cavernosum. J Androl. 2003;24(2):239-45. [PubMed: 12634311].

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