Regulation of endothelial MAPK/ERK signalling and capillary morphogenesis by low-amplitude electric field

Journal of the Royal Society Interface

Volumn 10, Issue 78, 2013, Pages

  Sheikh, Abdul Q ^a   Taghian, Toloo ^b   Hemingway, Bryan ^b   Cho, Hongkwan ^a   Kogan, Andrei B ^b   Narmoneva, Daria A ^a  

^a University of Cincinnati   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Angiogenesis; Electric field; Endothelial cells; ERK; MAPK

Indexed keywords

CELL DEATH; ELECTRIC FIELDS; ENDOTHELIAL CELLS; MORPHOLOGY; NITRIC OXIDE; PHOSPHORYLATION; PHYSIOLOGICAL MODELS; TISSUE;

ANGIOGENESIS; CAPILLARY MORPHOGENESIS; CELL RESPONSE; COMPLEX FORMATIONS; DB/DB MOUSE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ERK; FREQUENCY-SENSITIVE; HIGH FREQUENCY HF; IN-VIVO; LOW-AMPLITUDE; MAPK; MICROVASCULAR ENDOTHELIAL CELLS; MITOGEN ACTIVATED PROTEIN KINASE; NONTHERMAL; PROLIFERATION AND APOPTOSIS; SIGNAL-REGULATED KINASE; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR TISSUE; VEGF RELEASE; VEGFR-2; WOUND HEALING;

ELECTRIC FIELD EFFECTS;

CALCIUM CHANNEL BLOCKING AGENT; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; VASCULOTROPIN; CALCIUM; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; RAF PROTEIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ELECTRIC FIELD; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; MICROVASCULAR ENDOTHELIAL CELL; MORPHOGENESIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TISSUE REGENERATION; WOUND HEALING; ANIMAL; BIOSYNTHESIS; CAPILLARY; CELL CULTURE; CYTOLOGY; ELECTROMAGNETIC FIELD; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PHOSPHORYLATION; TIME;

ANIMALS; APOPTOSIS; CALCIUM; CAPILLARIES; CELL PROLIFERATION; CELLS, CULTURED; ELECTROMAGNETIC FIELDS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; MAP KINASE KINASE 4; MAP KINASE SIGNALING SYSTEM; MICE; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-RAF; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84871343104     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0548     Document Type: Article

References (73)

1. Barker AT, Jaffe LF, Vanable Jr JW. 1982 The glabrous epidermis of cavies contains a powerful battery. Am. J. Physiol. 242, R358-R366.
2. Funk RHW, Monsees TK. 2006 Effects of electromagnetic fields on cells: physiological and therapeutical approaches and molecular mechanisms of interaction. Cells Tissues Organs 182, 59-78. (doi:10.1159/000093061)
3. Ieran M, Zaffuto S, Bagnacani M, Annovi M, Moratti A, Cadossi R. 1990 Effect of low frequency pulsing electromagnetic fields on skin ulcers of venous origin in humans: a double-blind study. J. Orthop. Res. 8, 276-282. (doi:10.1002/jor.1100080217)
4. Salzberg CA, Cooper-Vastola SA, Perez F, Viehbeck MG, Byrne DW. 1995 The effects of non-thermal pulsed electromagnetic energy on wound healing of pressure ulcers in spinal cord-injured patients: a randomized, double-blind study. Ostomy Wound Manage. 41, 42-44.
5. Kanno S, Nobuyuki O, Mayumi A, Saito S, Hori K, Handa Y, Tabayashi K, Sato Y. 1999 Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 99, 2682-2687. (doi:10.1161/01.CIR.99.20. 2682)
6. Akai M, Hayashi K. 2002 Effect of electrical stimulation on musculoskeletal systems; a meta-analysis of controlled clinical trials. Bioelectromagnetics 23, 132-143. (doi:10.1002/bem.106)
7. Larsen JA, Overstreet J. 2008 Pulsed radio frequency energy in the treatment of complex diabetic foot wounds: two cases. J. Wound Ostomy Continence Nurs. 35, 523-527. (doi:10.1097/01.WON.0000335966.98607.1c)
8. Ojingwa JC, Isseroff RR. 2003 Electrical stimulation of wound healing. J. Invest. Dermatol. 121, 1-12. (doi:10.1046/j.1523-1747.2003.12454.x)
9. Markov MS. 2007 Pulsed electromagnetic field therapy history, state of the art and future. Environmentalist 27, 465-475. (doi:10.1007/s10669-007-9128- 2)
10. Zhao M, Bai H, Wang E, Forrester JV, McCaig C. D. 2004 Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J. Cell Sci. 117, 397-405. (doi:10.1242/jcs.00868)
11. Ferrara N, Kerbel RS. 2005 Angiogenesis as a therapeutic target. Nature 438, 967-974. (doi:10.1038/nature04483)
12. Linderman JR, Kloehn MR, Greene AS. 2000 Development of an implantable muscle stimulator: measurement of stimulated angiogenesis and poststimulus vessel regression. Microcirculation 7, 119-128. (doi:10.1038/sj.mn.7300100)
13. Roland D, Ferder M, Kothuru R, Faierman T, Strauch B. 2000 Effects of pulsed magnetic energy on a microsurgically transferred vessel. Plast. Reconstr. Surg. 105, 1371-1374. (doi:10.1097/00006534-200004040-00016)
14. Callaghan MJ, Chang EI, Seiser N, Aarabi S, Ghali S, Kinnucan ER, Simon ER, Gurtner GC. 2008 Pulsed electromagnetic fields accelerate normal and diabetic wound healing by increasing endogenous FGF-2 release. Plast. Reconstr. Surg. 121, 130-141. (doi:10.1097/01.prs.0000293761.27219.84)
15. Bai H, Forrester JV, Zhao M. 2011 DC electric stimulation upregulates angiogenic factors in endothelial cells through activation of VEGF receptors. Cytokine 55, 110-115. (doi:10.1016/j.cyto.2011.03.003)
16. Tepper OM et al. 2004 Electromagnetic fields increase in vitro and in vivo angiogenesis through endothelial release of FGF-2. FASEB J. 18, 1231-1233. (doi:10.1096/fj.03-0847fje)
17. Hopper RA, Verhalen JP, Tepper OT, Mehrara BJ, Detch R, Chang EI, Baharestani S, Simon BJ, Gurtner GC. 2009 Osteoblasts stimulated with pulsed electromagnetic fields increase HUVEC proliferation via a VEGF-A independent mechanism. Bioelectromagnetics 30, 189-97. (doi:10.1002/bem.20459)
18. Li X, Kolega J. 2002 Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells. J. Vasc. Res. 39, 391-404. (doi:10.1159/000064517)
19. Finkelstein E, Chang W, Chao PH, Gruber D, Minden A, Hung CT, Finkelstein E. 2004 Roles of microtubules, cell polarity and adhesion in electricfield-mediated motility of 3T3 fibroblasts. J. Cell Sci. 117, 1533-1545. (doi:10.1242/jcs.00986)
20. Rawe IM, Vlahovic TC. 2011 The use of a portable, wearable form of pulsed radio frequency electromagnetic energy device for the healing of recalcitrant ulcers: a case report. Int. Wound J. 9, 253-258. (doi:10.1111/j.1742-481X.2011. 00853.x)
21. Lappin MS, Lawrie LF, Richards TL, Kramer ED. 2003 Effects of a pulsed electromagnetic therapy on multiple sclerosis fatigue and quality of life: a double-blind, placebo controlled trial. Altern. Ther. Health Med. 9, 38.
22. Guo L, Kubat NJ, Isenberg RA. 2011 Pulsed radio frequency energy (PRFE) use in human medical applications. Electromagn. Biol. Med. 30, 21-45. (doi:10.3109/15368378.2011.566775)
23. Seger R, Krebs EG. 1995 The MAPK signaling cascade. FASEB J. 9, 726-735.
24. Rousseau S, Houle F, Landry J, Huot J. 1997 p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15, 2169-2177. (doi:10.1038/sj.onc.1201380)
25. Gupta K, Kshirsagar S, Li W, Gui L, Ramakrishnan S, Gupta P, Gupta K. 1999 VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp. Cell Res. 247, 495-504. (doi:10.1006/excr.1998.4359)
26. Matsumoto T, Yokote K, Tamura K, Takemoto M, Ueno H, Saito Y, Matsumoto T. 1999 Platelet-derived growth factor activates p38 mitogen-activated protein kinase through a Ras-dependent pathway that is important for actin reorganization and cell migration. J. Biol. Chem. 274, 13 954-13 960. (doi:10.1074/jbc.274.20.13954)
27. Hu YL, Li S, Shyy JY, Chien S. 1999 Sustained JNK activation induces endothelial apoptosis: studies with colchicine and shear stress. Am. J. Physiol. 277, H1593-H1599.
28. Deschesnes RG, Huot J, Valerie K, Landry J. 2001 Involvement of p38 in apoptosis-associated membrane blebbing and nuclear condensation. Mol. Biol. Cell. 12, 1569-1582.
29. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, Marais R, Bird D, Marshall CJ. 2006 ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell. 9, 33-44. (doi:10.1016/j.ccr.2005.12.021)
30. Medhora M, Dhanasekaran A, Pratt Jr PF, Cook CR, Dunn LK, Gruenloh SK, Jacobs ER. 2008 Role of JNK in network formation of human lung microvascular endothelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L676-L785. (doi:10.1152/ajplung.00496.2007)
31. Leszczynski D, Joenvaara S, Reivinen J, Kuokka R. 2002 Non-thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: molecular mechanism for cancer- and blood-brain barrier-related effects. Differentiation 70, 120-129. (doi:10.1046/j.1432-0436. 2002.700207.x)
32. Bernardini C, Zannoni A, Turba ME, Bacci ML, Forni M, Mesirca P, Remondini D, Castellani G, Bersani F. 2007 Effects of 50 Hz sinusoidal magnetic fields on Hsp27, Hsp70, Hsp90 expression in porcine aortic endothelial cells (PAEC). Bioelectromagnetics 28, 231-237. (doi:10.1002/bem.20299)
33. Sauer H, Bekhite MM, Hescheler J, Wartenberg M. 2005 Redox control of angiogenic factors and CD31-positive vessel-like structures in mouse embryonic stem cells after direct current electrical field stimulation. Exp. Cell Res. 304, 380-390. (doi:10.1016/j.yexcr.2004.11.026)
34. Nie K, Henderson A. 2003 MAP kinase activation in cells exposed to a 60 Hz electromagnetic field. J. Cell. Biochem. 90, 1197-1206. (doi:10.1002/jcb. 10704)
35. Friedman J, Kraus S, Hauptman Y, Schiff Y, Seger R. 2007 Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem. J. 405, 559-568. (doi:10.1042/BJ20061653)
36. Zhao M et al. 2006 Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN. Nature 442, 457-460. (doi:10.1038/nature04925)
37. Cho MR, Thatte HS, Lee RC, Golan DE. 1996 Reorganization of microfilament structure induced by ac electric fields. FASEB J. 10, 1552-1558.
38. Foster KR. 2000 Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems. IEEE Trans. Plasma Sci. 28, 15-23. (doi:10.1109/27.842819)
39. Lim YC, Garcia-Cardena G, Allport JR, Zervoglos M, Connolly AJ, Gimbrone Jr MA, Luscinskas FW. 2003 Heterogeneity of endothelial cells from different organ sites in T-cell subset recruitment. Am. J. Pathol. 162, 1591. (doi:10.1016/S0002-9440(10)64293-9)
40. Bahr A, Dorn H, Bolz T. 2006 Dosimetric assessment of an exposure system for simulating GSM and WCDMA mobile phone usage. Bioelectromagnetics 27, 320-327. (doi:10.1002/bem.20218)
41. Cho H, Balaji S, Sheikh AQ, Hurley JR, Tian YF, Collier JH, Crombleholme TM, Narmoneva DA. 2011 Regulation of endothelial cell activation and angiogenesis by injectable peptide nanofibers. Acta Biomater. 8, 154-164. (doi:10.1016/j.actbio.2011.08.029)
42. Hurley JR, Balaji S, Narmoneva DA. 2010 Complex temporal regulation of capillary morphogenesis by fibroblasts. Am. J. Physiol. Cell Physiol. 299, C444-C453. (doi:10.1152/ajpcell.00572.2009)
43. Narmoneva DA, Oni O, Sieminski AL, Zhang S, Gertler JP, Kamm RD, Lee RT. 2005 Self-assembling short oligopeptides and the promotion of angiogenesis. Biomaterials 26, 4837. (doi:10.1016/j.biomaterials.2005.01.005)
44. Autiero M, Luttun A, Tjwa M, Carmeliet P. 2003 Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J. Thromb. Haemost. 1, 1356-1370. (doi:10.1046/j.1538-7836.2003.00263.x)
45. Shibuya M. 2006 Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J. Biochem. Mol. Biol. 39, 469-748. (doi:10.5483/BMBRep.2006.39.5.469)
46. Craig TJ, Ciufo LF, Morgan A. 2004 A protein-protein binding assay using coated microtitre plates: increased throughput, reproducibility and speed compared to bead-based assays. J. Biochem. Biophys. Methods 60, 49-60. (doi:10.1016/j.jbbm.2004.04.015)
47. Adler V et al. 2005 Functional interactions of raf and MEK with Jun-N-terminal kinase (JNK) result in a positive feedback loop on the oncogenic ras signaling pathway. Biochemistry 44, 10 784-10 795. (doi:10.1021/bi050619j)
48. Cheng C et al. 2009 Trihydrophobin 1 interacts with PAK1 and regulates ERK/MAPK activation and cell migration. J. Biol. Chem. 284, 8786-8796. (doi:10.1074/jbc.M806144200)
49. Cai J, Hong Y, Weng C, Tan C, Imperato-McGinley J, Zhu YS. 2011 Androgen stimulates endothelial cell proliferation via an androgen receptor/VEGF/cyclin A-mediated mechanism. Am. J. Physiol. Heart Circ. Physiol. 300, H1210-H1221. (doi:10.1152/ajpheart.01210.2010)
50. Fang KS, Ionides E, Oster G, Nuccitelli R, Isseroff RR. 1999 Epidermal growth factor receptor relocalization and kinase activity are necessary for directional migration of keratinocytes in DC electric fields. J. Cell Sci. 112, 1967-1978.
51. 2+. Biochem. J. 353, 503-512. (doi:10.1042/0264-6021:3530503)
52. Vlahos CJ, Matter WF, Hui KY, Brown RF. 1994 A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
53. 2+-PKCα-MAP kinase pathway contributes to stretch-induced hyaluronan synthesis in vitro. Matrix Biol. 25, 306-316. (doi:10.1016/j.matbio. 2006.01.008)
54. Breslin JW, Pappas PJ, Cerveira JJ, Hobson Ii RW, Duran WN. 2003 VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am. J. Physiol. Heart Circ. Physiol. 284, H92-H100.
55. Keswani SG, Katz AB, Lim FY, Zoltick P, Radu A, Alaee D, Herlyn M, Crombleholme TM. 2004 Adenoviral mediated gene transfer of PDGF-B enhances wound healing in type I and type II diabetic wounds. Wound Repair Regen. 12, 497-504. (doi:10.1111/j.1067-1927.2004.12501.x)
56. Roux PP, Blenis J. 2004 ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344. (doi:10.1128/MMBR.68.2.320-344.2004)
57. Bancroft CC, Chen Z, Yeh J, Sunwoo JB, Yeh NT, Jackson S, Jackson C, Van Waes C. 2002 Effects of pharmacologic antagonists of epidermal growth factor receptor, PI3K and MEK signal kinases on NF-κB and AP-1 activation and IL-8 and VEGF expression in human head and neck squamous cell carcinoma lines. Int. J. Cancer 99, 538-548. (doi:10.1002/ijc.10398)
58. Fong TAT et al. 1999 SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types. Cancer Res. 59, 99-106.
59. Galiano RD, Tepper OM, Pelo CR, Bhatt KA, Callaghan M, Bastidas N, Bunting S, Steinmetz HG, Gurtner GC. 2004 Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am. J. Pathol. 164, 1935-1947. (doi:10.1016/S0002-9440(10)63754-6)
60. Monache DS, Alessandro R, Iorio R, Gualtieri G, Colonna R. 2008 Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 29, 640-648. (doi:10.1002/bem.20430)
61. Rubinfeld H, Seger R. 2005 The ERK cascade: a prototype of MAPK signaling. Mol. Biotechnol. 31, 151-174. (doi:10.1385/MB:31:2:151)
62. Bernier SG, Haldar S, Michel T. 2000 Bradykinin-regulated interactions of the mitogen-activated protein kinase pathway with the endothelial nitricoxide synthase. J. Biol. Chem. 275, 30 707-30 715. (doi:10.1074/jbc.M005116200)
63. Chen Y, Medhora M, Falck JR, Pritchard Jr KA, Jacobs ER. 2006 Mechanisms of activation of eNOS by 20-HETE and VEGF in bovine pulmonary artery endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L378-L385. (doi:10.1152/ajplung.00424.2005)
64. Chuderland D, Marmor G, Shainskaya A, Seger R. 2008 Calcium-mediated interactions regulate the subcellular localization of extracellular signal-regulated kinases. J. Biol. Chem. 283, 11 176-11 188. (doi:10.1074/jbc.M709030200)
65. McCubrey JA et al. 2006 Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv. Enzyme Regul. 283, 249-279. (doi:10.1016/j.advenzreg.2006.01.004)
66. Steelman LS, Pohnert SC, Shelton JG, Franklin RA, Bertrand FE, McCubrey JA. 2004 JAK/STAT, Raf/MEK/ERK, PI3K/Akt and BCR-ABL in cell cycle progression and leukemogenesis. Leukemia 18, 189-218. (doi:10.1038/sj.leu.2403241)
67. Alessi DR, Saito Y, Campbell DG, Cohen P, Sithanandam G, Rapp U, Ashworth A, Marhsall CJ, Cowley S. 1994 Identification of the sites in MAP kinase kinase-1 phosphorylated by p74(raf-1). EMBO J. 13, 1610-1619.
68. Vernier PT, Sun Y, Marcu L, Salemi S, Craft CM, Gundersen MA. 2003 Calcium bursts induced by nanosecond electric pulses. Biochem. Biophys. Res. Commun. 310, 286-295. (doi:10.1016/j.bbrc.2003.08.140)
69. Beebe SJ, Blackmore PF, White J, Joshi RP, Schoenbach KH. 2004 Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. Physiol. Meas. 25, 1077-1093. (doi:10.1088/0967-3334/ 25/4/023)
70. Clapham DE. 2007 Calcium signaling. Cell 131, 1047-1058. (doi:10.1016/j.cell.2007.11.028)
71. Nelson TJ, Sun MK, Hongpaisan J, Alkon DL. 2008 Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur. J. Pharmacol. 585, 76-87. (doi:10.1016/j.ejphar.2008.01.051)
72. Ay S, Evcik D. 2009 The effects of pulsed electromagnetic fields in the treatment of knee osteoarthritis: a randomized, placebo-controlled trial. Rheumatol. Int. 29, 663-666. (doi:10.1007/s00296-008-0754-x)
73. Patterson C, Runge MS. 1999 Therapeutic angiogenesis the new electrophysiology. Circulation 99, 2614-2616. (doi:10.1161/01.CIR.99.20.2614)