Enhanced homing permeability and retention of bone marrow stromal cells by noninvasive pulsed focused ultrasound

Stem Cells

Volumn 30, Issue 6, 2012, Pages 1216-1227

  Ziadloo, Ali ^a   Burks, Scott R ^a   Gold, Eric M ^a   Lewis, Bobbi K ^a   Chaudhry, Aneeka ^a   Merino, Maria J ^b   Frenkel, Victor ^a   Frank, Joseph A ^a,c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NONE   (United States)

Author keywords

Cytokines; Enhanced homing permeability and retention; Ferumoxides; High intensity focused ultrasound; ICAM; Integrins; Mechanotransduction; Mesenchymal stem cells; Protamine; Pulsed focused ultrasound; Stem cell migration; VCAM

Indexed keywords

CYTOKINE; GROWTH FACTOR; INTEGRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; FEMALE; HISTOLOGY; HUMAN; HUMAN CELL; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; STROMA CELL; ULTRASOUND; UPREGULATION;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL CULTURE TECHNIQUES; CYTOKINES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, NUDE; STROMAL CELLS; ULTRASONICS;

MURINAE;

EID: 84861873664     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1099     Document Type: Article

References (52)

1. Uccelli A, Moretta L, Pistoia V.Mesenchymal stem cells in health and disease. Nature reviews. Immunology 2008;8:726-736.
2. Singer NG, Caplan AI.Mesenchymal stem cells: Mechanisms of inflammation. Annu Rev Pathol 2011;6:457-478.
3. Harting MT, Jimenez F, Xue H et al. Intravenous mesenchymal stem cell therapy for traumatic brain injury. J Neurosurg 2009;110: 1189-1197.
4. Schrepfer S, Deuse T, Reichenspurner H et al. Stem cell transplantation: The lung barrier. Transplant Proc 2007;39:573-576. (Pubitemid 46386222)
5. Baer PC, Geiger H.Mesenchymal stem cell interactions with growth factors on kidney repair. Curr Opin Nephrol Hypertens 2010;19:1-6.
6. Karp JM, Leng Teo GS.Mesenchymal stem cell homing: The devil is in the details. Cell Stem Cell 2009;4:206-216.
7. Steingen C, Brenig F, Baumgartner L et al. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol 2008;44:1072-1084.
8. Deak E, Seifried E, Henschler R.Homing pathways of mesenchymal stromal cells (MSCs) and their role in clinical applications. Int Rev Immunol 2010;29:514-529.
9. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myo-cardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54-63.
10. Ley K, Laudanna C, Cybulsky MI et al. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 2007;7:678-689. (Pubitemid 47327397)
11. Sordi V.Mesenchymal stem cell homing capacity. Transplantation 2009;87:S42-S45.
12. Luster AD, Alon R, von Andrian UH.Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol 2005;6:1182-1190. (Pubitemid 43045626)
13. Tempany CM, McDannold NJ, Hynynen K et al. Focused ultrasound surgery in oncology: Overview and principles. Radiology 2011;259:39-56.
14. Frenkel V.Ultrasound mediated delivery of drugs and genes to solid tumors. Adv Drug Deliv Rev 2008;60:1193-1208.
15. Chen CS.Mechanotransduction-A field pulling together? J Cell Sci 2008;121:3285-3292.
16. Schwartz MA, DeSimone DW.Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 2008;20:551-556.
17. Burks SR, Ziadloo A, Hancock HA et al. Investigation of cellular and molecular responses to pulsed focused ultrasound in a mouse model. PLoS One 2011;6:e24730.
18. Dromi S, Frenkel V, Luk A et al. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res 2007;13:2722-2727. (Pubitemid 46788041)
19. Poff JA, Allen CT, Traughber B et al. Pulsed high-intensity focused ultrasound enhances apoptosis and growth inhibition of squamous cell carcinoma xenografts with proteasome inhibitor bortezomib. Radiology 2008;248:485-491.
20. Arbab AS, Yocum GT, Kalish H et al. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 2004;104:1217-1223. (Pubitemid 39038047)
21. Balakumaran A, Pawelczyk E, Ren J et al. Superparamagnetic iron oxide nanoparticles labeling of bone marrow stromal (mesenchymal) cells does not affect their "stemness". PLoS One 2010;5:e11462.
22. Vilalta M, Degano IR, Bago J et al. Biodistribution, long-term survival, and safety of human adipose tissue-derived mesenchymal stem cells transplanted in nude mice by high sensitivity non-invasive bioluminescence imaging. Stem Cells Dev 2008;17:993-1003.
23. Yagi H, Soto-Gutierrez A, Parekkadan B et al. Mesenchymal stem cells: Mechanisms of immunomodulation and homing. Cell Transplantation 2010;19:667-679.
24. Hart AL, Ng SC, Mann E et al. Homing of immune cells: Role in homeostasis and intestinal inflammation. Inflamm Bowel Dis 2010;16: 1969-1977.
25. Gurish MF, Boyce JA.Mast cells: Ontogeny, homing, and recruitment of a unique innate effector cell. J Allergy Clin Immunol 2006;117: 1285-1291. (Pubitemid 43810217)
26. Pelus LM, Fukuda S.Chemokine-mobilized adult stem cells; defining a better hematopoietic graft. Leukemia 2008;22:466-473. (Pubitemid 351386716)
27. Mueller FJ, Serobyan N, Schraufstatter IU et al. Adhesive interactions between human neural stem cells and inflamed human vascular endothelium are mediated by integrins. Stem Cells 2006;24:2367-2372. (Pubitemid 44674295)
28. Pawelczyk E, Jordan EK, Balakumaran A et al. In vivo transfer of intracellular labels from locally implanted bone marrow stromal cells to resident tissue macrophages. PLoS One 2009;4:e6712.
29. Rieck B, Schlaak S.Measurement in vivo of the survival rate in autologous adipocyte transplantation. Plast Reconstr Surg 2003;111: 2315-2323. (Pubitemid 36676810)
30. Kondziolka D, Steinberg GK, Cullen SB et al. Evaluation of surgical techniques for neuronal cell transplantation used in patients with stroke. Cell Transplant 2004;13:749-754. (Pubitemid 40280212)
31. Lee PH, Kim JW, Bang OY et al. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin Pharmacol Ther 2008;83:723-730. (Pubitemid 351556019)
32. Bos C, Delmas Y, Desmouliere A et al. In vivo MR imaging of intravascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver. Radiology 2004;233:781-789.
33. Chanda D, Kumar S, Ponnazhagan S.Therapeutic potential of adult bone marrow-derived mesenchymal stem cells in diseases of the skeleton. J Cell Biochem 2010;111:249-257.
34. Brunner S, Engelmann MG, Franz WM.Stem cell mobilisation for myocardial repair. Expert Opin Biol Ther 2008;8:1675-1690.
35. Capoccia BJ, Robson DL, Levac KD et al. Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity. Blood 2009;113:5340-5351.
36. Mahmood A, Lu D, Chopp M.Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery 2004;55:1185-1193.
37. Francois S, Bensidhoum M, Mouiseddine M et al. Local irradiation not only induces homing of human mesenchymal stem cells at exposed sites but promotes their widespread engraftment to multiple organs: A study of their quantitative distribution after irradiation damage. Stem Cells 2006;24:1020-1029. (Pubitemid 44464735)
38. Klopp AH, Spaeth EL, Dembinski JL et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res 2007;67:11687-11695.
39. Arbab AS, Jordan EK, Wilson LB et al. In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum Gene Ther 2004;15:351-360. (Pubitemid 38469777)
40. Polyak B, Fishbein I, Chorny M et al. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc Natl Acad Sci USA 2008;105:698-703. (Pubitemid 351171771)
41. Kyrtatos PG, Lehtolainen P, Junemann-Ramirez M et al. Magnetic tagging increases delivery of circulating progenitors in vascular injury. JACC Cardiovasc Interv 2009;2:794-802.
42. Paliwal S, Mitragotri S.Therapeutic opportunities in biological responses of ultrasound. Ultrasonics 2008;48:271-278.
43. Barzelai S, Sharabani-Yosef O, Holbova R et al. Low-intensity ultra-sound induces angiogenesis in rat hind-limb ischemia. Ultrasound Med Biol 2006;32:139-145. (Pubitemid 41814869)
44. Mizrahi N, Seliktar D, Kimmel E.Ultrasound-induced angiogenic response in endothelial cells. Ultrasound Med Biol 2007;33:1818-1829. (Pubitemid 47632996)
45. Yu T, Hu D, Xu C.Microbubbles improve the ablation efficiency of extracorporeal high intensity focused ultrasound against kidney tissues. World J Urol 2008;26:631-636.
46. Krasovitski B, Frenkel V, Shoham S et al. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc Natl Acad Sci USA 2011;108:3258-3263.
47. Hancock HA, Smith LH, Cuesta J et al. Investigations into pulsed high-intensity focused ultrasound-enhanced delivery: Preliminary evidence for a novel mechanism. Ultrasound Med Biol 2009;35:1722-1736.
48. Furlani D, Ugurlucan M, Ong L et al. Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc Res 2009;77:370-376.
49. English K, French A, Wood KJ.Mesenchymal stromal cells: Facilitators of successful transplantation? Cell Stem Cell 2010;7:431-442.
50. Pasquier E, Kavallaris M, Andre N.Metronomic chemotherapy: New rationale for new directions. Nat Rev Clin Oncol 2010;7:455-465.
51. Orsi F, Zhang L, Arnone P et al. High-intensity focused ultrasound ablation: Effective and safe therapy for solid tumors in difficult locations. AJR Am J Roentgenol 2010;195:W245-W252.
52. Hwang JH, Zhou Y, Warren C et al. Targeted venous occlusion using pulsed high-intensity focused ultrasound. IEEE Trans Biomed Eng 2010;57:37-40.