Synergistic effect of EMFBEMER-type pulsed weak electromagnetic field and HPMA-bound doxorubicin on mouse EL4 T-cell lymphoma

Journal of Drug Targeting

Volumn 19, Issue 10, 2011, Pages 890-899

  Řhov, Blanka ^a   Etrych, Tom ^b   Rov, Milada ^a   Tomala, Jakub ^a   Ulbrich, Karel ^b   Kov, Marek ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b INSTITUTE OF MACROMOLECULAR CHEMISTRY   (Czech Republic)

Author keywords

Anticancer resistance; Athymic mice; DOXHYD HPMA; EL4 T cell lymphoma; EMF; Stimulation of the immune system

Indexed keywords

CANCER ANTIBODY; DOXORUBICIN; EL4 ANTIBODY; HEAT SHOCK PROTEIN 70; N (2 HYDROXYPROPYL)METHACRYLAMIDE COPOLYMER; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN N (2 HYDROXYPROPYL)METHACRYLAMIDE COPOLYMER CONJUGATE; DOXORUBICIN-N-(2-HYDROXYPROPYL)METHACRYLAMIDE COPOLYMER CONJUGATE; DRUG DERIVATIVE; POLYMETHACRYLIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST ADENOCARCINOMA; CANCER SURVIVAL; CONTROLLED STUDY; DRUG FORMULATION; DRUG POTENTIATION; ELECTROMAGNETIC FIELD; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL LYMPHOMA; TUMOR GROWTH; ANIMAL; C57BL MOUSE; DOSE RESPONSE; IMMUNOCOMPROMISED PATIENT; METABOLISM; MULTIMODALITY CANCER THERAPY; NUDE MOUSE; PATHOLOGY; SURVIVAL RATE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; COMBINED MODALITY THERAPY; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; ELECTROMAGNETIC FIELDS; FEMALE; HSP70 HEAT-SHOCK PROTEINS; IMMUNOCOMPROMISED HOST; LYMPHOMA, T-CELL; MICE; MICE, INBRED C57BL; MICE, NUDE; POLYMETHACRYLIC ACIDS; SURVIVAL RATE;

EID: 81255143443     PISSN: 1061186X     EISSN: 10292330     Source Type: Journal    
DOI: 10.3109/1061186X.2011.622403     Document Type: Article

References (68)

1. Akan Z, Aksu B, Tulunay A, Bilsel S, Inhan-Garip A. (2010). Extremely low-frequency electromagnetic fields affect the immune response of monocyte-derived macrophages to pathogens. Bioelectromagnetics, 31, 603-612.
2. Arafa HM, Abd-Allah AR, El-Mahdy MA, Ramadan LA, Hamada FM. (2003). Immunomodulatory effects of L-carnitine and q10 in mouse spleen exposed to low-frequency high-intensity magnetic field. Toxicology, 187, 171-181. (Pubitemid 36426928)
3. Barbault A, Costa FP, Bottger B, Munden RF, Bomholt F, Kuster N, Pasche B. (2009). Amplitude-modulated electromagnetic fields for the treatment of cancer: Discovery of tumor-specific frequencies and assessment of a novel therapeutic approach. J Exp Clin Cancer Res, 28, 51.
4. Beneduci A, Chidichimo G, De Rose R, Filippelli L, Straface SV, Venuta S. (2005). Frequency and irradiation time-dependant antiproliferative effect of low-power millimeter waves on RPMI 7932 human melanoma cell line. Anticancer Res, 25, 1023-1028. (Pubitemid 40546877)
5. Beniashvili D, Avinoach'm I, Baasov D, Zusman I. (2005). The role of household electromagnetic fields in the development of mammary tumors in women: Clinical case-record observations. Med Sci Monit, 11, CR10-CR13. (Pubitemid 40116394)
6. Blank M, Goodman R. (1999). Electromagnetic fields may act directly on DNA. J Cell Biochem, 75, 369-374. (Pubitemid 29521645)
7. Boscolo P, Di Gioacchino M, Di Giampaolo L, Antonucci A, Di Luzio S. (2007). Combined effects of electromagnetic fields on immune and nervous responses. Int J Immunopathol Pharmacol, 20, 59-63.
8. Busljeta I, Trosic I, Milkovic-Kraus S. (2004). Erythropoietic changes in rats after 2.45 GJz nonthermal irradiation. Int J Hyg Environ Health, 207, 549-554. (Pubitemid 40824331)
9. Cameron IL, Sun LZ, Short N, Hardman WE, Williams CD. (2005). Therapeutic Electromagnetic Field (TEMF) and gamma irradiation on human breast cancer xenograft growth, angiogenesis and metastasis. Cancer Cell Int, 5, 23.
10. de Vocht F. (2010). Dirty electricity: What, where, and should we care?. J Expo Sci Environ Epidemiol, 20, 399-405.
11. Dressel R, Günther E. (1999). Heat-induced expression of MHC-linked HSP70 genes in lymphocytes varies at the single-cell level. J Cell Biochem, 72, 558-569. (Pubitemid 29088307)
12. Di Giampaolo L, Di Donato A, Antonucci A, Paiardini G, Travaglini P, Spagnoli G, Magrini A, Reale M, Dadorante V, Iannaccone U, Di Sciascio MB, Di Gioacchino M, Boscolo P. (2006). Follow up study on the immune response to low frequency electromagnetic fields in men and women working in a museum. Int J Immunopathol Pharmacol, 19, 37-42.
13. Dunn GP, Old LJ, Schreiber RD. (2004). The immunobiology of cancer immunosurveillance and immunoediting. Immunity, 21, 137-148. (Pubitemid 39094044)
14. Erren TC. (2001). A meta-analysis of epidemiologic studies of electric and magnetic fields and breast cancer in women and men. Bioelectromagnetics, Suppl 5, S105-S119.
15. Etrych T, Mrkvan T, Chytil P, Koňák ?, Ří hová B, Ulbrich K. (2008). N-(2-hydroxypropyl)methacrylamide-based polymer conjugates with pH-controlled activation of doxorubicin. I. New synthesis, physicochemical characterization and preliminary biological evaluation. J Appl Polym Sci, 109, 3050-3061.
16. Forssén UM, Rutqvist LE, Ahlbom A, Feychting M. (2005). Occupational magnetic fields and female breast cancer: A case-control study using Swedish population registers and new exposure data. Am J Epidemiol, 161, 250-259. (Pubitemid 40223513)
17. Gabrys M. (2004). Pulsierende Magnetfeldtherapie bei zytostatisch bedingter Polyneuropathie. Deutsche Zeitschrift für Onkologie 3, 154-156. (Pubitemid 40012983)
18. Gapeyev AB, Kulagina TP, Aripovsky AV, Chemeris NK. (2011). The role of fatty acids in anti-inflammatory effects of low-intensity extremely high-frequency electromagnetic radiation. Bioelectromagnetics, 32, 388-395.
19. Girgert R, Schimming H, Krner W, Gründker C, Hanf V. (2005). Induction of tamoxifen resistance in breast cancer cells by ELF electromagnetic fields. Biochem Biophys Res Commun, 336, 1144-1149. (Pubitemid 41383441)
20. Gobba F, Bargellini A, Bravo G, Scaringi M, Cauteruccio L, Borella P. (2009a). Natural killer cell activity decreases in workers occupationally exposed to extremely low frequency magnetic fields exceeding 1 microT. Int J Immunopathol Pharmacol, 22, 1059-1066.
21. Gobba F, Bargellini A, Scaringi M, Bravo G, Borella P. (2009b). Extremely low frequency-magnetic fields (ELF-EMF) occupational exposure and natural killer activity in peripheral blood lymphocytes. Sci Total Environ, 407, 1218-1223.
22. Grassi C, D'Ascenzo M, Torsello A, Martinotti G, Wolf F, Cittadini A, Azzena GB. (2004). Effects of 50 Hz electromagnetic fields on voltage-gated Ca2+ channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium, 35, 307-315. (Pubitemid 38351200)
23. Greco F, Vicent MJ. (2009). Combination therapy: Opportunities and challenges for polymer-drug conjugates as anticancer nanomedicines. Adv Drug Deliv Rev, 61, 1203-1213.
24. Chen C, Ma X, Zhong M, Yu Z. (2010). Extremely low-frequency electromagnetic fields exposure and female breast cancer risk: A meta-analysis based on 24,338 cases and 60,628 controls. Breast Cancer Res Treat, 123, 569-576.
25. Jian W, Wei Z, Zhiqiang C, Zheng F. (2009). X-ray-induced apoptosis of BEL-7402 cell line enhanced by extremely low frequency electromagnetic field in vitro. Bioelectromagnetics, 30, 163-165.
26. Jiménez-García MN, Arellanes-Robledo J, Aparicio-Bautista DI, Rodríguez-Segura MA, Villa-TreviÃo S, Godina-Nava JJ. (2010). Anti-proliferative effect of extremely low frequency electromagnetic field on preneoplastic lesions formation in the rat liver. BMC Cancer, 10, 159.
27. Jin M, Blank M, Goodman R. (2000). ERK1/2 phosphorylation, induced by electromagnetic fields, diminishes during neoplastic transformation. J Cell Biochem, 78, 371-379. (Pubitemid 30491066)
28. Kafka WA. (1998). Vorrichtung und elektrisches oder elektromagnetisches Signal zur Beeinflussung biologischer Systeme. Europäische Patentanmeldung 98119944.1 v 21.10.98.
29. Kafka WA, Spodaryk K. (2003). Effects of extremely weak BEMER 3000 type pulsed electromagnetic fields on red blood cell metabolism and hemoglobin oxygen affinity, Fizoterapia, 11, 24-31.
30. Kafka WA, Schütze N, Walther M. (2005). Einsatz extrem niederfrequent (BEMER typisch) gepulster schwacher elektromagnetischer Felder im Bereich der Orthopädie (Application of extreme low frequent (BEMER type) pulsed electromagnetic fields in orthopedics). Orthopädische Praxis, 41, 1, 22-24.
31. de Kleijn S, Bouwens M, Verburg-van Kemenade BM, Cuppen JJ, Ferwerda G, Hermans PW. (2011). Extremely low frequency electromagnetic field exposure does not modulate toll-like receptor signaling in human peripheral blood mononuclear cells. Cytokine, 54, 43-50.
32. Kopecek J, Kopecková P. (2010). HPMA copolymers: Origins, early developments, present, and future. Adv Drug Deliv Rev, 62, 122-149.
33. Kopecek J. (2010). Biomaterials and drug delivery: Past, present, and future. Mol Pharm, 7, 922-925.
34. Krinick NL, Sun Y, Joyner D, Spikes JD, Straight RC, Kopecek J. (1994). A polymeric drug delivery system for the simultaneous delivery of drugs activatable by enzymes and/or light. J Biomater Sci Polym Ed, 5, 303-324.
35. Lammers T, Ulbrich K. (2010). HPMA copolymers: 30 years of advances. Adv Drug Deliv Rev, 62, 119-121.
36. Lacy-Hulbert A, Metcalfe JC, Hesketh R. (1998). Biological responses to electromagnetic fields. FASEB J, 12, 395-420. (Pubitemid 28146520)
37. Lange S, Viergutz T, Simkó M. (2004). Modifications in cell cycle kinetics and in expression of G1 phase-regulating proteins in human amniotic cells after exposure to electromagnetic fields and ionizing radiation. Cell Prolif, 37, 337-349. (Pubitemid 39281184)
38. Lin H, Blank M, Goodman R. (1999). A magnetic field-responsive domain in the human HSP70 promoter. J Cell Biochem, 75, 170-176. (Pubitemid 29402555)
39. Liang Y, Hannan CJJr, Chang BK, Schoenlein PV. (1997). Enhanced potency of daunorubicin against multidrug resistant subline KB-ChR-8-5-11 by a pulsed magnetic field. Anticancer Res, 17, 2083-2088. (Pubitemid 27320949)
40. Laqué-Rupérez E, Ruiz-Gómez MJ, de la PeÃa L, Gil L, Martínez-Morillo M. (2003). Methotrexate cytotoxicity on MCF-7 breast cancer cells is not altered by exposure to 25 Hz, 1.5 mT magnetic field and iron (III) chloride hexahydrate. Bioelectrochemistry, 60, 81-86. (Pubitemid 36945009)
41. Lammers T. (2010). Improving the efficacy of combined modality anticancer therapy using HPMA copolymer-based nanomedicine formulations. Adv Drug Deliv Rev, 62, 203-230.
42. Murthy SN. (1999). Magnetophoresis: An approach to enhance transdermal drug diffusion. Pharmazie, 54, 377-379. (Pubitemid 29237191)
43. Orel VE, Kudryavets YI, Satz S, Bezdenezhnih NA, Danko ML, Khranovskaya NN, Romanov AV, Dzyatkovskaya NN, Burlaka AP. (2005). Mechanochemically activated doxorubicin nanoparticles in combination with 40 MHz frequency irradiation on A-549 lung carcinoma cells. Drug Deliv, 12, 171-178. (Pubitemid 40604997)
44. Phillips JL, Singh NP, Lai H. (2009). Electromagnetic fields and DNA damage. Pathophysiology, 16, 79-88.
45. Plotnikov A, Fishman D, Tichler T, Korenstein R, Keisari Y. (2004). Low electric field enhanced chemotherapy can cure mice with CT-26 colon carcinoma and induce anti-tumour immunity. Clin Exp Immunol, 138, 410-416. (Pubitemid 39573619)
46. Pollán M, Gustavsson P, Floderus B. (2001). Breast cancer, occupation, and exposure to electromagnetic fields among Swedish men. Am J Ind Med, 39, 276-285. (Pubitemid 32176366)
47. Porock D, Gentry J. (2002). Re: Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst, 94, 530-1; author reply 533.
48. Prestwich RJ, Errington F, Hatfield P, Merrick AE, Ilett EJ, Selby PJ, Melcher AA. (2008). The immune system-Is it relevant to cancer development, progression and treatment?. Clin Oncol, 20, 101-112. (Pubitemid 351194288)
49. Rannug A, Holmberg B, Ekstrm T, Mild KH. (1993). Rat liver foci study on coexposure with 50 Hz magnetic fields and known carcinogens. Bioelectromagnetics, 14, 17-27.
50. Rossi E, Corsetti MT, Sukkar S, Poggi C. (2007). Extremely low frequency electromagnetic fields prevent chemotherapy induced myelotoxicity. Electromagn Biol Med, 26, 277-281.
51. Richard D, Lange S, Viergutz T, Kriehuber R, Weiss DG, Myrtill S. (2002). Influence of 50 Hz electromagnetic fields in combination with a tumour promoting phorbol ester on protein kinase C and cell cycle in human cells. Mol Cell Biochem, 232, 133-141. (Pubitemid 34413890)
52. Ronchetto F, Barone D, Cintorino M, Berardelli M, Lissolo S, Orlassino R, Ossola P, Tofani S. (2004). Extremely low frequency-modulated static magnetic fields to treat cancer: A pilot study on patients with advanced neoplasm to assess safety and acute toxicity. Bioelectromagnetics, 25, 563-571. (Pubitemid 39552043)
53. Ruiz-Gómez MJ, Martínez-Morillo M. (2009). Electromagnetic fields and the induction of DNA strand breaks. Electromagn Biol Med, 28, 201-214.
54. Ríhová B, Strohalm J, Kubácková K, Jelínková M, Hovorka O, Kovár M, Plocová D, Sírová M, St'astný M, Rozprimová L, Ulbrich K. (2002). Acquired and specific immunological mechanisms co-responsible for efficacy of polymer-bound drugs. J Control Release, 78, 97-114. (Pubitemid 34081856)
55. Ríhová B, Kovár M. (2010). Immunogenicity and immunomodulatory properties of HPMA-based polymers. Adv Drug Deliv Rev, 62, 184-191.
56. Scarfí MR, Sannino A, Perrotta A, Sarti M, Mesirca P, Bersani F. (2005). Evaluation of genotoxic effects in human fibroblasts after intermittent exposure to 50 Hz electromagnetic fields: A confirmatory study. Radiat Res, 164, 270-276. (Pubitemid 41233780)
57. Scott A, Dana KM, Stewens RY. (2002). Residential magnetic fields and risk of breast cancer. Am J Epidemiol, 155, 446-454.
58. Sommer AM, Streckert J, Bitz AK, Hansen VW, Lerchl A. (2004). No effects of GSM-modulated 900 MHz electromagnetic fields on survival rate and spontaneous development of lymphoma in female AKR/J mice. BMC Cancer, 4, 77.
59. Sommer AM, Bitz AK, Streckert J, Hansen VW, Lerchl A. (2007). Lymphoma development in mice chronically exposed to UMTSmodulated radiofrequency electromagnetic fields. Radiat Res, 168, 72-80. (Pubitemid 351292927)
60. Sirova M, Mrkvan T, Etrych T, Chytil P, Rossmann P, Ibrahimova M, Kovar L, Ulbrich K, Rihova B. (2010). Preclinical evaluation of linear HPMA-doxorubicin conjugates with pH-sensitive drug release: Efficacy, safety, and immunomodulating activity in murine model. Pharm Res, 27, 200-208.
61. Tofani S, Cintorino M, Barone D, Berardelli M, De Santi MM, Ferrara A, Orlassino R, Ossola P, Rolfo K, Ronchetto F, Tripodi SA, Tosi P. (2002). Increased mouse survival, tumor growth inhibition and decreased immunoreactive p53 after exposure to magnetic fields. Bioelectromagnetics, 23, 230-238. (Pubitemid 38622900)
62. Tokalov SV, Gutzeit HO. (2004). Weak electromagnetic fields (50 Hz) elicit a stress response in human cells. Environ Res, 94, 145-151. (Pubitemid 38156095)
63. Trosic I, Busljeta I, Pavicic I. (2004). Blood-forming system in rats after whole-body microwave exposure; reference to the lymphocytes. Toxicol Lett, 154, 125-132. (Pubitemid 39314596)
64. Tuschl H, Novak W, Molla-Djafari H. (2006). In vitro effects of GSM modulated radiofrequency fields on human immune cells. Bioelectromagnetics, 27, 188-196.
65. Vijayalaxmi J, Prihoda TJ. (2009). Genetic damage in mammalian somatic cells exposed to extremely low frequency electro-magnetic fields: A meta-analysis of data from 87 publications (1990-2007). Int J Radiat Biol, 85, 196-213.
66. Weiderpass E, Vainio H, Kauppinen T, Vasama-Neuvonen K, Partanen T, Pukkala E. (2003). Occupational exposures and gastrointestinal cancers among Finnish women. J Occup Environ Med, 45, 305-310.
67. Williams CD, Markov MS, Hardman WE, Cameron, I.L. (2001). Therapeutic electromagnetic field effects on angiogenesis and tumor growth. Anticancer Res, 21, 3887-3891. (Pubitemid 34229258)
68. Zheng T, Holford T, Mayne S. (2000). Exposure to electromagnetic fields from use of electric blankets and other in-home electrical appliances and breast cancer risk. Am J Epidemiol, 151, 1103-1111. (Pubitemid 30489206)