Directing migration of endothelial progenitor cells with applied DC electric fields

Stem Cell Research

Volumn 8, Issue 1, 2012, Pages 38-48

  Zhao, Zhiqiang ^a   Qin, Lu ^a,b   Reid, Brian ^c   Pu, Jin ^a   Hara, Takahiko ^d   Zhao, Min ^c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MIGRATION; DIRECT CURRENT; ELECTROSTIMULATION; ENDOTHELIAL PROGENITOR CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE ENGINEERING;

ANIMALS; BIOLOGICAL MARKERS; CELL LINE; CELL MOVEMENT; ELECTRICITY; ENDOTHELIAL CELLS; MICE; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 80052735461     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2011.08.001     Document Type: Article

References (44)

1. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., Witzenbichler B., Schatteman G., Isner J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997, 275:964-967.
2. Akeson A.L., Wetzel B., Thompson F.Y., Brooks S.K., Paradis H., Gendron R.L., Greenberg J.M. Embryonic vasculogenesis by endothelial precursor cells derived from lung mesenchyme. Dev. Dyn. 2000, 217:11-23.
3. Iwatsuki K., Tanaka K., Kaneko T., Kazama R., Okamoto S., Nakayama Y., Ito Y., Satake M., Takahashi S., Miyajima A., Watanabe T., Hara T. Runx1 promotes angiogenesis by downregulation of insulin-like growth factor-binding protein-3. Oncogene 2005, 24:1129-1137.
4. Shi Q., Rafii S., Wu M.H., Wijelath E.S., Yu C., Ishida A., Fujita Y., Kothari S., Mohle R., Sauvage L.R., Moore M.A., Storb R.F., Hammond W.P. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998, 92:362-367.
5. Zhao Z., Walczysko P., Zhao M. Intracellular Ca2+ stores are essential for injury induced Ca2+ signaling and re-endothelialization. J. Cell. Physiol. 2008, 214:595-603.
6. Yamashita J., Itoh H., Hirashima M., Ogawa M., Nishikawa S., Yurugi T., Naito M., Nakao K., Nishikawa S. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000, 408:92-96.
7. Hristov M., Weber C. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J. Cell. Mol. Med. 2004, 8:498-508.
8. Akeson A.L., Brooks S.K., Thompson F.Y., Greenberg J.M. In vitro model for developmental progression from vasculogenesis to angiogenesis with a murine endothelial precursor cell line, MFLM-4. Microvasc. Res. 2001, 61:75-86.
9. Akeson A., Herman A., Wiginton D., Greenberg J. Endothelial cell activation in a VEGF-A gradient: relevance to cell fate decisions. Microvasc. Res. 2010, 80:65-74.
10. Hristov M., Weber C. Endothelial progenitor cells in vascular repair and remodeling. Pharmacol. Res. 2008, 58:148-151.
11. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000, 407:242-248.
12. McCaig C.D., Rajnicek A.M., Song B., Zhao M. Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 2005, 85:943-978.
13. Zhao M., Song B., Pu J., Wada T., Reid B., Tai G., Wang F., Guo A., Walczysko P., Gu Y., Sasaki T., Suzuki A., Forrester J.V., Bourne H.R., Devreotes P.N., McCaig C.D., Penninger J.M. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 2006, 442:457-460.
14. Nuccitelli R. A role for endogenous electric fields in wound healing. Curr. Top. Dev. Biol. 2003, 58:1-26.
15. Barker A.T., Jaffe L.F., Vanable J.W. The glabrous epidermis of cavies contains a powerful battery. Am. J. Physiol. 1982, 242:R358-R366.
16. Li X., Kolega J. Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells. J. Vasc. Res. 2002, 39:391-404.
17. Bai H., McCaig C.D., Forrester J.V., Zhao M. DC electric fields induce distinct preangiogenic responses in microvascular and macrovascular cells. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1234-1239.
18. Zhao M., Bai H., Wang E., Forrester J.V., McCaig C.D. Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J. Cell. Sci. 2004, 117:397-405.
19. Patterson C., Runge M.S. Therapeutic angiogenesis: the new electrophysiology?. Circulation 1999, 99:2614-2616.
20. Kanno S., Oda N., Abe M., Saito S., Hori K., Handa Y., Tabayashi K., Sato Y. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 1999, 99:2682-2687.
21. Linderman J.R., Kloehn M.R., Greene A.S. Development of an implantable muscle stimulator: measurement of stimulated angiogenesis and poststimulus vessel regression. Microcirculation 2000, 7:119-128.
22. Sheikh I., Tchekanov G., Krum D., Hare J., Djelmami-Hani M., Maddikunta R., Mortada M.E., Karakozov P., Baibekov I., Hauck J., Bajwa T., Akhtar M., Chekanov V. Effect of electrical stimulation on arteriogenesis and angiogenesis after bilateral femoral artery excision in the rabbit hind-limb ischemia model. Vasc. Endovascular. Surg. 2005, 39:257-265.
23. Kloth L.C. Electrical stimulation for wound healing: a review of evidence from in vitro studies, animal experiments, and clinical trials. Int. J. Low Extrem. Wounds. 2005, 4:23-44.
24. Nagasaka M., Kohzuki M., Fujii T., Kanno S., Kawamura T., Onodera H., Itoyama Y., Ichie M., Sato Y. Effect of low-voltage electrical stimulation on angiogenic growth factors in ischaemic rat skeletal muscle. Clin. Exp. Pharmacol. Physiol. 2006, 33:623-627.
25. Hang J., Kong L., Gu J.W., Adair T.H. VEGF gene expression is upregulated in electrically stimulated rat skeletal muscle. Am. J. Physiol. 1995, 269:H1827-H1831.
26. Pu J., Zhao M. Golgi polarization in a strong electric field. J. Cell. Sci. 2005, 118:1117-1128.
27. Hristov M., Zernecke A., Bidzhekov K., Liehn E.A., Shagdarsuren E., Ludwig A., Weber C. Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury. Circ. Res. 2007, 100:590-597.
28. Takahashi T., Kalka C., Masuda H., Chen D., Silver M., Kearney M., Magner M., Isner J.M., Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 1999, 5:434-438.
29. Gurtner G.C., Chang E. "Priming" endothelial progenitor cells: a new strategy to improve cell based therapeutics. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1034-1035.
30. Peichev M., Naiyer A.J., Pereira D., Zhu Z., Lane W.J., Williams M., Oz M.C., Hicklin D.J., Witte L., Moore M.A., Rafii S. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000, 95:952-958.
31. Zemani F., Silvestre J.S., Fauvel-Lafeve F., Bruel A., Vilar J., Bieche I., Laurendeau I., Galy-Fauroux I., Fischer A.M., Boisson-Vidal C. Ex vivo priming of endothelial progenitor cells with SDF-1 before transplantation could increase their proangiogenic potential. Arterioscler. Thromb. Vasc. Biol. 2008, 28:644-650.
32. Nuccitelli R. Endogenous ionic currents and DC electric fields in multicellular animal tissues. Bioelectromagnetics 1992, (Suppl. 1):147-157.
33. Hotary K.B., Robinson K.R. Evidence of a role for endogenous electrical fields in chick embryo development. Development 1992, 114:985-996.
34. McCaig C.D., Zhao M. Physiological electrical fields modify cell behaviour. Bioessays 1997, 19:819-826.
35. Sawyer P.N., Pate J.W. Bio-electric phenomena as an etiologic factor in intravascular thrombosis. Am. J. Physiol. 1953, 175:103-107.
36. Sawyer P.N., Himmelfarb E., Lustrin I., Ziskind H. Measurement of streaming potentials of mammalian blood vessels, aorta and vena cava, in vivo. Biophys. J. 1966, 6:641-651.
37. Coronel R., Wilms-Schopman F.J., Opthof T., van Capelle F.J., Janse M.J. Injury current and gradients of diastolic stimulation threshold, TQ potential, and extracellular potassium concentration during acute regional ischemia in the isolated perfused pig heart. Circ. Res. 1991, 68:1241-1249.
38. Hammerick K.E., James A.W., Huang Z., Prinz F.B., Longaker M.T. Pulsed direct current electric fields enhance osteogenesis in adipose-derived stromal cells. Tissue Eng. Part A. 2010, 16:917-931.
39. Zhang, J., Calafiore, M., Zeng, Q., Zhang, X., Huang, Y., Li, R.A., Deng, W., Zhao, M., in press. Electrically guiding migration of human induced pluripotent stem cells. Stem Cell. Rev. doi:. doi:10.1007/s12015-011-9247-5.
40. Sun L., Tran N., Liang C., Hubbard S., Tang F., Lipson K., Schreck R., Zhou Y., McMahon G., Tang C. Identification of substituted 3-[(4,5,6, 7-tetrahydro-1H-indol-2-yl)methylene]-1,3-dihydroindol-2-ones as growth factor receptor inhibitors for VEGF-R2 (Flk-1/KDR), FGF-R1, and PDGF-Rbeta tyrosine kinases. J. Med. Chem. 2000, 43:2655-2663.
41. Chavakis E., Carmona G., Urbich C., Gottig S., Henschler R., Penninger J.M., Zeiher A.M., Chavakis T., Dimmeler S. Phosphatidylinositol-3-kinase-gamma is integral to homing functions of progenitor cells. Circ. Res. 2008, 102:942-949.
42. Kawasaki K., Watabe T., Sase H., Hirashima M., Koide H., Morishita Y., Yuki K., Sasaoka T., Suda T., Katsuki M., Miyazono K., Miyazawa K. Ras signaling directs endothelial specification of VEGFR2+ vascular progenitor cells. J. Cell. Biol. 2008, 181:131-141.
43. Chiang M., Robinson K.R., Vanable J.W. Electrical fields in the vicinity of epithelial wounds in the isolated bovine eye. Exp. Eye Res. 1992, 54:999-1003.
44. Erickson C.A., Nuccitelli R. Embryonic fibroblast motility and orientation can be influenced by physiological electric fields. J. Cell. Biol. 1984, 98:296-307.