Moderate strength (0.23-0.28 T) static magnetic fields (SMF) modulate signaling and differentiation in human embryonic cells

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Wang, Zhiyun ^a   Sarje, Anshu ^b   Che, Pao Lin ^a   Yarema, Kevin J ^a  

^a Johns Hopkins University   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDE ALPHA 2,3 SIALYLTRANSFERASE; GANGLIOSIDE GM3; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; NEURAMINIDASE 3; SIALIDASE; SIALYLTRANSFERASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; GANGLIOSIDE; MESSENGER RNA; TLR4 PROTEIN, MOUSE;

ARTICLE; BIOSENSOR; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ELECTROMAGNETIC FIELD; EMBRYO CELL; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LIPID BIOSENSOR; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; SIGNAL TRANSDUCTION; STATIC MAGNETIC FIELD; UPREGULATION; ANIMAL EMBRYO; CELL LINE; COMPUTER PROGRAM; CYTOLOGY; GENE EXPRESSION; GENETICS; MAGNETISM; METABOLISM; SECRETION;

ANIMALIA;

BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; EMBRYO, MAMMALIAN; GANGLIOSIDES; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; INTERLEUKIN-6; MAGNETICS; MAP KINASE SIGNALING SYSTEM; RNA, MESSENGER; SOFTWARE; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION, GENETIC;

EID: 69049096109     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-356     Document Type: Article

References (86)

1. Wiltschko W Wiltschko R Magnetic orientation in birds J Exp Biol 1996, 199:29-38. 10.1016/0022-0981(95)00166-2 9317275
2. Wiltschko W Wiltschko R Light-dependent magnetoreception in birds: The behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities J Exp Biol 2001, 214:3295-3302.
3. Mora CV Davison M Wild JM Walker MM Magnetoreception and its trigeminal mediation in the homing pigeon Nature 2004, 432:508-511. 10.1038/ nature03077 15565156
4. Presti D Pettigrew JD Ferromagnetic coupling to muscle receptors as a basis for geomagnetic field sensitivity in animals Nature 1980, 285:99-101. 10.1038/285099a0 7374763
5. Maeda K Henbest KB Cintolesi F Kuprov I Rodgers CT Liddell PA Gust D Timmel CR Hore PJ Chemical compass model of avian magnetoreception Nature 2008, 453:387-390. 10.1038/nature06834 18449197
6. Cromie WJ Depressed get a lift from MRI Harvard University Gazette 2004 http://www.hno.harvard.edu/gazette/2004/01.22/01-depression.html
7. Weintraub MI Cole SP A randomized controlled trial of the effects of a combination of static and dynamic magnetic fields on carpal tunnel syndrome Pain Med 2008, 9:493-504. 10.1111/j.1526-4637.2007.00324.x 18777606
8. Weintraub MI Wolfe GI Barohn RA Cole SP Parry GJ Hayat G Cohen JA Page JC Bromberg MB Schwartz SL Static magnetic field therapy for symptomatic diabetic neuropathy: A randomized, double-blind, placebo-controlled trial Arch Phys Med Rehabil 2003, 84:736-746. 10.1016/ S0003-9993(03)00106-0 12736891
9. László J Gyires K 3 T homogeneous static magnetic field of a clinical MR significantly inhibits pain in mice Life Sci 2009, 84:12-17. 10.1016/j.lfs.2008.10.009 19000698
10. Okano H Ohkubo C Modulatory effects of static magnetic fields on blood pressure in rabbits Bioelectromagnetics 2001, 22:408-418. 10.1002/bem.68 11536282
11. Man D Man B Plosker H The influence of permanent magnetic field therapy on wound healing in suction lipectomy patients: A double-blind study Plast Reconstr Surg 1999, 104:2261-2266. 10.1097/ 00006534-199912000-00051 11149796
12. Weinberger A Nyska A Giler S Treatment of experimental inflammatory synovitis with continuous magnetic field Is J Med Sci 1996, 32:1197-1201.
13. Morris CE Skalak TC Chronic static magnetic field exposure alters microvessel enlargement resulting from surgical intervention J Appl Physiol 2007, 103:629-636. 10.1152/japplphysiol.01133.2006 17478604
14. Nuccitelli S Cerella C Cordisco S Albertini MC Accorsi A De Nicola M D'Alessio M Radogna F Magrini A Bergamaschi A Ghibelli L Hyperpolarization of plasma membrane of tumor cells sensitive to antiapoptotic effects of magnetic fields Ann NY Acad Sci 2006, 1090:217-225. 10.1196/annals.1378.024 17384265
15. De Nicola M Cordisco S Cerella C Albertini MC D'Alessio M Accorsi A Bergamaschi A Magrini A Ghibelli L Magnetic fields protect from apoptosis via redox alteration Ann NY Acad Sci 2006, 1090:59-68. 10.1196/ annals.1378.006 17384247
16. Rosen AD Mechanism of action of moderate-intensity static magnetic fields on biological systems Cell Biochem Biophys 2003, 39:163-173. 10.1385/CBB:39:2:163 14515021
17. Rosen AD Effect of 125 mT static magnetic field on the kinetics of voltage activated Na+ channels in GH3 cells Bioelectromagnetics 2003, 24:517-523. 10.1002/bem.10124 12955757
18. Tenuzzo B Chionna A Panzarini E Lanubile R Tarantino P Di Jeso B Dwikat M Dini L Biological effects of 6 mT static magnetic fields: A comparative study in different cell types Bioelectromagnetics 2006, 27:560-577. 10.1002/bem.20252 16724329
19. Szabo G Dolganiuc A Dai Q Pruett SB TLR4, ethanol, and lipid rafts: A new mechanism of ethanol action with implications for other receptor-mediated effects J Immunol 2007, 178:1243-1249. 17237368
20. Chiu KH Ou KL Lee SY Lin CT Chang WJ Chen CC Huang HM Static magnetic fields promote osteoblast-like cells differentiation via increasing the membrane rigidity Ann Biomed Eng 2007, 35:1932-1939. 10.1007/ s10439-007-9370-2 17721730
21. Mayburd AL Martlínez A Sackett D Liu H Shih J Tauler J Avis I Mulshine JL Ingenuity network-assisted transcription profiling: Identification of a new pharmacologic mechanism for MK886 Clin Cancer Res 2006, 12:1820-1827. 10.1158/1078-0432.CCR-05-2149 16551867
22. Ganter B Giroux CN Emerging applications of network and pathway analysis in drug discovery and development Curr Opin Drug Discov Devel 2008, 11:86-94. 18175271
23. Gusev Y Computational methods for analysis of cellular functions and pathways collectively targeted by differentially expressed microRNA Methods 2008, 44:61-72. 10.1016/j.ymeth.2007.10.005 18158134
24. Shamblott MJ Axelman J Littlefield JW Blumenthal PD Huggins GR Cui Y Cheng L Gearhart JD Human embryonic germ cell derivatives express a broad range of developmentally distinct markers and proliferate extensively in vitro Proc Natl Acad Sci USA 2001, 98:113-118. 10.1073/ pnas.021537998 14553 11134532
25. Hirai T Nakamichi N Yoneda Y Activator protein-1 complex expressed by magnetism in cultured rat hippocampal neurons Biochem Biophys Res Commun 2002, 292:200-207. 10.1006/bbrc.2002.6618 11890693
26. Huang Y Yan J Lubet R Kensler TW Sutter TR Identification of novel transcriptional networks in response to treatment with the anticarcinogen 3H-1,2-dithiole-3-thione Physiol Genomics 2006, 24:144-153. 16317079
27. Petrov E Martinac B Modulation of channel activity and gadolinium block of MscL by static magnetic fields Eur Biophys J 2007, 36:95-105. 10.1007/ s00249-006-0109-z 17089151
28. Jüttler E Tarabin V Schwaninger M Interleukin-6 (IL-6): A possible neuromodulator induced by neuronal activity Neuroscientist 2002, 8:268-275. 12061506
29. Kühl M Sheldahl LC Park M Miller JR Moon RT The Wnt/Ca2+ pathway: A new vertebrate Wnt signaling pathway takes shape Trends Genet 2000, 16:279-283. 10.1016/S0168-9525(00)02028-X 10858654
30. Strieth S Strelczyk D Eichhorn ME Dellian M Luedemann S Griebel J Bellemann M Berghaus A Brix G Static magnetic fields induce blood flow decrease and platelet adherence in tumor microvessels Cancer Biol Ther 2008, 7:814-819. 18340115
31. Okano H Onmori R Tomita N Ikada Y Effects of a moderate-intensity static magnetic field on VEGF-A stimulated endothelial capillary tubule formation in vitro Bioelectromagnetics 2006, 27:628-640. 10.1002/ bem.20246 16838273
32. Okano H Tomita N Ikada Y Effects of 120 mT static magnetic field on TGF-β1-inhibited endothelial tubular formation in vitro Bioelectromagnetics 2007, 28:497-499. 10.1002/bem.20330 17516506
33. Okano H Tomita N Ikada Y Spatial gradient effects of 120 mT static magnetic field on endothelial tubular formation in vitro Bioelectromagnetics 2008, 29:233-236. 10.1002/bem.20376 18041023
34. Lin CT Lee SY Chen CY Chen CA Lin CP Huang HM Long-term continuous exposure to static magnetic field reduces popolysaccharide-induced cytotoxicity of fibroblasts Int J Radiat Biol 2008, 84:219-226. 10.1080/ 09553000801902158 18300022
35. Taga T Fukuda S Role of IL-6 in the neural stem cell differentiation Clin Rev Allergy Immunol 2006, 28:249-256. 10.1385/CRIAI:28:3:249
36. Dai JC He P Chen X Greenfield EM TNFα and PTH utilize distinct mechanisms to induce IL-6 and RANKL expression with markedly different kinetics Bone 2006, 38:509-520. 10.1016/j.bone.2005.10.007 16316790
37. Inoue KI Takano H Yanagisawa R Sakurai M Shimada A Morita T Sato M Yoshino S Yoshikawa T Role of interleukin-6 in toll-like receptor 4 and 2 expressions induced by lipopolysaccharide in the lung Immunopharmacol Immunotoxicol 2007, 29:63-68. 10.1080/08923970701282478 17464767
38. Jou I Lee JH Park SY Yoon HJ Joe E-H Park EJ Gangliosides trigger inflammatory responses via TLR4 in brain glia Am J Pathol 2006, 168:1619-1630. 10.2353/ajpath.2006.050924 1606595 16651628
39. Song J Duncan MJ Li G Chan C Grady R Stapleton A Abraham SN A novel TLR4-mediated signaling pathway leading to IL-6 responses in human bladder epithelial cells PLoS Pathogens 2007, 3:e60. 10.1371/ journal.ppat.0030060 1857715 17465679
40. Triantafilou M Morath S Mackie A Hartung T Triantafilou K Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane J Cell Sci 2004, 17:4007-4014. 10.1242/jcs.01270
41. Rehli M Of mice and men: Species variations of Toll-like receptor expression Trends Immunol 2002, 23:375-378. 10.1016/ S1471-4906(02)02259-7 12133792
42. Weiss DS Raupach B Takeda K Akira S Zychlinsky A Toll-like receptors are temporally involved in host defense J Immunol 2004, 172:4463-4469. 15034062
43. Muzio M Bosisio D Polentarutti N D'amico G Stoppacciaro A Mancinelli R van't Veer C Penton-Rol G Ruco LP Allavena P Mantovani A Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: Selective expression of TLR3 in dendritic cells J Immunol 2000, 164:5998-6004. 10820283
44. Rosen AD Chastney EE Effect of long term exposure to 0.5 T static magnetic fields on growth and size of GH3 cells Bioelectromagnetics 2009, 30:114-119. 10.1002/bem.20452 18839411
45. Tenuzzo B Vergallo C Dini L Effect of 6 mT static magnetic field on the bcl-2, bax, p53 and hsp70 expression in freshly isolated and in vitro aged human lymphocytes Tissue Cell 2009, 41:169-179. 10.1016/ j.tice.2008.09.004 19054536
46. Fedrowitz M Kamino K Löscher W Significant differences in the effects of magnetic field exposure on 7,12- dimethylbenz(α)anthracene-induced mammary carcinogenesis in two substrains of Sprague-Dawley rats Cancer Res 2004, 64:243-251. 10.1158/ 0008-5472.CAN-03-2808 14729631
47. Ueno S Saito S Wada T Yamaguchi K Satoh M Arai Y Miyagi T Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility J Biol Chem 2006, 281:7756-7764. 10.1074/jbc.M509668200 16428383
48. Hakomori S-I The glycosynapse Proc Natl Acad Sci USA 2002, 99:225-232. 10.1073/pnas.012540899 117543 11773621
49. Allende ML Proia RL Lubricating cell signaling pathways with gangliosides Curr Opin Struct Biol 2002, 12:587-592. 10.1016/ S0959-440X(02)00376-7 12464309
50. Van Wagoner NJ Benveniste EN Interleukin-6 expression and regulation in astrocytes J Neuroimmunol 1999, 100:124-139. 10.1016/ S0165-5728(99)00187-3 10695723
51. Chung T-W Choi H-J Lee Y-C Kim C-H Molecular mechanism for transcriptional activation of ganglioside GM3 synthase and its function in differentiation of HL-60 cells Glycobiology 2005, 15:233-244. 10.1093/ glycob/cwh156 15385432
52. Kamimura D Ishihara K Hirano T IL-6 signal transduction and its physiological roles: The signal orchestration model Rev Physiol Biochem Pharmacol 2003, 149:1-38. full_text 12687404
53. Odintsova E Butters TD Monti E Sprong H van Meer G Berditchevski F Gangliosides play an important role in the organization of CD82-enriched microdomains Biochem J 2006, 400:315-325. 10.1042/BJ20060259 1652826 16859490
54. Müthing J Maurer U Weber-Schürholz S Glycosphingolipids of skeletal muscle: II. Modulation of Ca2+-flux in triad membranes by gangliosides Carbohydr Res 1998, 307:147-157. 10.1016/ S0008-6215(98)00028-7 9658570
55. Zhang X Min X Yang F Conformational basis of the phospholipid requirement for the activity of SR Ca2+-ATPase Chem Phys Lipids 1998, 97:55-64. 10.1016/S0009-3084(98)00092-9 10081149
56. Wang Y Tsui Z Yang F Mechanistic study of modulation of SR Ca2+-ATPase activity by gangliosides GM1 and GM3 through some biophysical measurements Glycoconjug J 1999, 16:781-786. 10.1023/A:1007123714104
57. Wang LH Tu YP Yang XY Tsui ZC Yang FY Effect of ganglioside GM3 on the activity and conformation of reconstituted Ca2+-ATPase FEBS Lett 1996, 388:128-130. 10.1016/0014-5793(96)00534-0 8690070
58. Wang Y Tsui Z Yang F Antagonistic effect of ganglioside GM1 and GM3 on the activity and conformation of sarcoplasmic reticulum Ca2+-ATPase FEBS Lett 1999, 457:144-148. 10.1016/S0014-5793(99)01024-8 10486582
59. Nakashima K Takizawa T Ochiai W Yanagisawa M Hisatsune T Nakafuku M Miyazono K Kishimoto T Kageyama R Taga T BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis Proc Natl Acad Sci USA 2001, 98:5868-5873. 10.1073/ pnas.101109698 33305 11331769
60. See J Zhang X Eraydin N Mun S-B Mamontov P Golden JA Grinspan JB Oligodendrocyte maturation is inhibited by bone morphogenetic protein Mol Cell Neurosci 2004, 26:481-492. 10.1016/j.mcn.2004.04.004 15276151
61. Zhang P-L Izrael M Ainbinder E Ben-Simchon L Chebath J Revel M Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein Mol Cell Neurosci 2006, 31:387-398. 10.1016/ j.mcn.2005.10.014 16325417
62. Henderson B Kind M Boeck G Helmberg A Wick G Gene expression profiling of human endothelial cells exposed to 50-Hz magnetic fields fails to produce regulated candidate genes Cell Stress Chaperones 2006, 11:227-232. 10.1379/CSC-196.1 1576470 17009595
63. Blank M Goodman R Electromagnetic initiation of transcription at specific DNA sites J Cell Biochem 2001, 81:689-692. 10.1002/jcb.1102 11329623
64. Lin H Han L Blank M Head M Goodman R Magnetic field activation of protein-DNA binding J Cell Biochem 1998, 70:297-303. 10.1002/ (SICI)1097-4644(19980901)70:3<297::AID-JCB2>3.0.CO;2-I 9706866
65. Lin H Blank M Goodman R A magnetic field-responsive domain in the human HSP70 promoter J Cell Biochem 1999, 75:170-176. 10.1002/ (SICI)1097-4644(19991001)75:1<170::AID-JCB17>3.0.CO;2-5 10462715
66. Lin H Blank M Rossol-Haseroth K Goodman R Regulating genes with electromagnetic response elements J Cell Biochem 2001, 81:143-148. 10.1002/1097-4644(20010401)81:1<143::AID-JCB1030>3.0.CO;2-4 11180404
67. Eichwald C Walleczek J Magnetic field perturbations as a tool for controlling enzyme-regulated and oscillatory biochemical reactions Biophys Chem 1998, 74:209-224. 10.1016/S0301-4622(98)00180-X 17029747
68. Henbest KB Maeda K Hore PJ Joshi M Bacher A Bittl R Weber S Timmel CR Schleicher E Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase Proc Natl Acad Sci USA 2008, 105:14395-14399. 10.1073/pnas.0803620105 2567148 18799743
69. Rodgers CT Hore PJ Chemical magnetoreception in birds: The radical pair mechanism Proc Natl Acad Sci USA 2009, 106:353-360. 10.1073/ pnas.0711968106 2626707 19129499
70. Gray JR Frith CH Parker D In vivo enhancement of chemotherapy with static electric or magnetic fields Bioelectromagnetics 2000, 21:575-583. 10.1002/1521-186X(200012)21:8<575::AID-BEM3>3.0.CO;2-F 11102947
71. Tofani S Barone D Cintorino M de Santi MM Ferrara A Orlassino R Ossola P Peroglio F Rolfo K Ronchetto F Static and ELF magnetic fields induce tumor growth inhibition and apoptosis Bioelectromagnetics 2001, 22:419-428. 10.1002/bem.69 11536283
72. Campbell CT Aich U Weier CA Wang JJ Choi SS Wen MM Maisel K Sampathkumar S-G Yarema KJ Targeting pro-invasive oncogenes with short chain fatty acid-hexosamine analogs inhibits the mobility of metastatic MDA-MB-231 breast cancer cell J Med Chem 2008, 51:8135-8147. 10.1021/jm800873k 19053749
73. Bonlie DR Treatment using oriented unidirectional DC magnetic field United States Patent 2001.
74. Engström S Markov MS McLean MJ Holcomb RR Markov JM Effects of non-uniform static magnetic fields on the rate of myosin phosphorylation Bioelectromagnetics 2002, 23:475-479. 10.1002/bem.10035 12210566
75. Edgar R Domrachev M Lasha AE Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207 99122 11752295
76. Kirschbaum B Effect of high bicarbonate hemodialysis on ionized calcium and risk of metastatic calcification Clin Chim Acta 2004, 343:231-236. 10.1016/j.cccn.2004.02.003 15115701
77. Wang Z Sun Z Li AV Yarema KJ Roles for GNE outside of sialic acid biosynthesis: Modulation of sialyltransferase and BiP expression, GM3 and GD3 biosynthesis, proliferation and apoptosis, and ERK1/2 phosphorylation J Biol Chem 2006, 281:27016-27028. 10.1074/ jbc.M604903200 16847058
78. Elmouelhi N Aich U Paruchuri VD Meledeo MA Campbell CT Wang JJ Srinivas R Khanna HS Yarema KJ Hexosamine template. A platform for modulating gene expression and for sugar-based drug discovery J Med Chem 2009, 52:2515-2530. 10.1021/jm801661m 19326913
79. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method Methods 2001, 25:402-408. 10.1006/meth.2001.1262 11846609
80. Lovat PE Di Sano F Corazzari M Fazi B Donnorso RP Pearson AD Hall AG Redfern CP Piacentini M Gangliosides link the acidic sphingomyelinase-mediated induction of ceramide to 12-lipoxygenase-dependent apoptosis of neuroblastoma in response to fenretinide J Natl Cancer Inst 2004, 96:1288-1299. 15339967
81. Siddiqui RA Jenski LJ Harvey KA Wiesehan JD Stillwell W Zaloga GP Cell-cycle arrest in Jurkat leukaemic cells: A possible role for docosahexaenoic acid Biochem J 2003, 371:621-629. 10.1042/BJ20021667 1223278 12492401
82. Cen S Guo F Niu M Saadatmand J Deflassieux J Kleiman L The interaction between HIV-1 Gag and APOBEC3G J Biol Chem 2004, 279:33177-33184. 10.1074/jbc.M402062200 15159405
83. Sampathkumar S-G Jones MB Meledeo MA Campbell CT Choi SS Hida K Gomutputra P Sheh A Gilmartin T Head SR Yarema KJ Targeting glycosylation pathways and the cell cycle: Sugar- dependent activity of butyrate-carbohydrate cancer prodrugs Chem Biol 2006, 13:1265-1275. 10.1016/j.chembiol.2006.09.016 17185222
84. Jones MB Teng H Rhee JK Baskaran G Lahar N Yarema KJ Characterization of the cellular uptake and metabolic conversion of acetylated N-acetylmannosamine (ManNAc) analogues to sialic acids Biotechnol Bioeng 2004, 85:394-405. 10.1002/bit.10901 14755557
85. Kim EJ Jones MB Rhee JK Sampathkumar SG Yarema KJ Establishment of N-acetylmannosamine (ManNAc) analogue-resistant cell lines as improved hosts for sialic acid engineering applications Biotechnol Prog 2004, 20:1674-1682. 10.1021/bp049841q 15575698
86. Kim EJ Sampathkumar SG Jones MB Rhee JK Baskaran G Yarema KJ Characterization of the metabolic flux and apoptotic effects of O-hydroxyl- and N-acetylmannosamine (ManNAc) analogs in Jurkat (human T-lymphoma-derived) cells J Biol Chem 2004, 279: 8342-18352. 10.1074/ jbc.M400205200 14966124