10 ns PEFs induce a histological response linked to cell death and cytotoxic T-lymphocytes in an immunocompetent mouse model of peritoneal metastasis.
Animals
Antibiotics, Antineoplastic
/ therapeutic use
Cell Death
Colorectal Neoplasms
/ pathology
Combined Modality Therapy
Disease Models, Animal
Electric Stimulation Therapy
/ methods
Immunocompetence
Mice
Mitomycin
/ therapeutic use
Oxaliplatin
/ therapeutic use
Peritoneal Neoplasms
/ pathology
T-Lymphocytes, Cytotoxic
Time Factors
Treatment Outcome
Histological response
Mice model
Multiphoton imaging
Peritoneal metastasis
nsPEF
Journal
Clinical & translational oncology : official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico
ISSN: 1699-3055
Titre abrégé: Clin Transl Oncol
Pays: Italy
ID NLM: 101247119
Informations de publication
Date de publication:
Jun 2021
Jun 2021
Historique:
received:
30
09
2020
accepted:
10
11
2020
pubmed:
8
3
2021
medline:
15
12
2021
entrez:
7
3
2021
Statut:
ppublish
Résumé
The application of nanosecond pulsed electric fields (nsPEFs) could be an effective therapeutic strategy for peritoneal metastasis (PM) from colorectal cancer (CRC). The aim of this study was to evaluate in vitro the sensitivity of CT-26 CRC cells to nsPEFs in combination with chemotherapeutic agents, and to observe the subsequent in vivo histologic response. In vitro cellular assays were performed to assess the effects of exposure to 1, 10, 100, 500 and 1000 10 ns pulses in a cuvette or bi-electrode system at 10 and 200 Hz. nsPEF treatment was applied alone or in combination with oxaliplatin and mitomycin. Cell death was detected by flow cytometry, and permeabilization and intracellular calcium levels by fluorescent confocal microscopy after treatment. A mouse model of PM was used to investigate the effects of in vivo exposure to pulses delivered using a bi-electrode system; morphological changes in mitochondria were assessed by electron microscopy. Fibrosis was measured by multiphoton microscopy, while the histological response (HR; hematoxylin-eosin-safran stain), proliferation (KI67, DAPI), and expression of immunological factors (CD3, CD4, CD8) were evaluated by classic histology. 10 ns PEFs exerted a dose-dependent effect on CT-26 cells in vitro and in vivo, by inducing cell death and altering mitochondrial morphology after plasma membrane permeabilization. In vivo results indicated a specific CD8+ T cell immune response, together with a strong HR according to the Peritoneal Regression Grading Score (PRGS). The effects of nsPEFs on CT-26 were confirmed in a mouse model of CRC with PM.
Identifiants
pubmed: 33677709
doi: 10.1007/s12094-020-02525-1
pii: 10.1007/s12094-020-02525-1
doi:
Substances chimiques
Antibiotics, Antineoplastic
0
Oxaliplatin
04ZR38536J
Mitomycin
50SG953SK6
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1220-1237Références
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JWW, Comber H, Forman D, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–403. https://doi.org/10.1016/j.ejca.2012.12.027 .
doi: 10.1016/j.ejca.2012.12.027
pubmed: 23485231
Surveillance, Epidemiology, and End Results Program. Cancer stat facts: colon and rectum cancer National Cancer Institute. 2020 http://seer.cancer.gov/statfacts/html/colorect.html .
Franko J, Shi Q, Meyers JP, Maughan TS, Adams RA, Seymour MT, Saltz L, Punt CJA, Koopman M, Tournigand C, Tebbutt NC, Diaz-Rubio E, Souglakos J, et al. Prognosis of patients with peritoneal metastatic colorectal cancer given systemic therapy: an analysis of individual patient data from prospective randomised trials from the Analysis and Research in Cancers of the Digestive System (ARCAD) database. Lancet Oncol. 2016;17:1709–19. https://doi.org/10.1016/S1470-2045(16)30500-9 .
doi: 10.1016/S1470-2045(16)30500-9
pubmed: 27743922
Phelip JM, Tougeron D, Léonard D, Benhaim L, Desolneux G, Dupré A, Michel P, Penna C, Tournigand C, Louvet C, Christou N, Chevallier P, Dohan A, et al. Metastatic colorectal cancer (mCRC): French intergroup clinical practice guidelines for diagnosis, treatments and follow-up (SNFGE, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO, SFR). Dig Liver Dis. 2019;51:1357–63. https://doi.org/10.1016/j.dld.2019.05.035 .
doi: 10.1016/j.dld.2019.05.035
pubmed: 31320305
Pinto A, Pocard M. Hyperthermic intraperitoneal chemotherapy with cisplatin and mitomycin C for colorectal cancer peritoneal metastases: a systematic review of the literature. Pleura Peritoneum. 2019;4:20190006. https://doi.org/10.1515/pp-2019-0006 .
doi: 10.1515/pp-2019-0006
pubmed: 31388562
pmcid: 6668656
Elias D, El Otmany A, Bonnay M, Paci A, Ducreux M, Antoun S, Lasser P, Laurent S, Bourget P. Human pharmacokinetic study of heated intraperitoneal oxaliplatin in increasingly hypotonic solutions after complete resection of peritoneal carcinomatosis. Oncology. 2002;63:346–52. https://doi.org/10.1159/000066229 .
doi: 10.1159/000066229
pubmed: 12417789
Elias D, Pocard M, Sideris L, Edè C, Ducreux M, Boige V, Lasser P. Preliminary results of intraperitoneal chemohyperthermia with oxaliplatin in peritoneal carcinomatosis of colorectal origin. Br J Surg. 2004;91:455–6. https://doi.org/10.1002/bjs.4399 .
doi: 10.1002/bjs.4399
pubmed: 15048746
Elias D, Gilly F, Boutitie F, Quenet F, Bereder J-M, Mansvelt B, Lorimier G, Dubè P, Glehen O. Peritoneal colorectal carcinomatosis treated with surgery and perioperative intraperitoneal chemotherapy: retrospective analysis of 523 patients from a multicentric French study. J Clin Oncol. 2010;28:63–8. https://doi.org/10.1200/JCO.2009.23.9285 .
doi: 10.1200/JCO.2009.23.9285
pubmed: 19917863
Glehen O, Gilly FN, Boutitie F, Bereder JM, Quenet F, Sideris L, Mansvelt B, Lorimier G, Msika S, Elias D, French Surgical Association. Toward curative treatment of peritoneal carcinomatosis from nonovarian origin by cytoreductive surgery combined with perioperative intraperitoneal chemotherapy: a multi-institutional study of 1,290 patients. Cancer. 2010;116:5608–18. https://doi.org/10.1002/cncr.25356 .
doi: 10.1002/cncr.25356
pubmed: 20737573
Goéré D, Malka D, Tzanis D, Gava V, Boige V, Eveno C, Maggiori L, Dumont F, Ducreux M, Elias D. Is there a possibility of a cure in patients with colorectal peritoneal carcinomatosis amenable to complete cytoreductive surgery and intraperitoneal chemotherapy? Ann Surg. 2013;257:1065–71. https://doi.org/10.1097/SLA.0b013e31827e9289 .
doi: 10.1097/SLA.0b013e31827e9289
pubmed: 23299520
Miklavčič D, Mir LM, Thomas VP. Electroporation-based technologies and treatments. J Membrane Biol. 2010;236:1–2. https://doi.org/10.1007/s00232-010-9287-9 .
doi: 10.1007/s00232-010-9287-9
Mir LM. Electroporation-based gene therapy: recent evolution in the mechanism description and technology developments. Methods Mol Biol. 2014;1121:3–23. https://doi.org/10.1007/978-1-4614-9632-8_1 .
doi: 10.1007/978-1-4614-9632-8_1
pubmed: 24510808
Davalos RV, Mir ILM, Rubinsky B. Tissue ablation with irreversible electroporation. Ann Biomed Eng. 2005;33:223–31. https://doi.org/10.1007/s10439-005-8981-8 .
doi: 10.1007/s10439-005-8981-8
pubmed: 15771276
Bardet SM, Carr L, Soueid M, Arnaud-Cormos D, Leveque P, O’Connor RP. Multiphoton imaging reveals that nanosecond pulsed electric fields collapse tumor and normal vascular perfusion in human glioblastoma xenografts. Sci Rep. 2016;6:34443. https://doi.org/10.1038/srep34443 .
doi: 10.1038/srep34443
pubmed: 27698479
pmcid: 5048165
Miao X, Yin S, Shao Z, Zhang Y, Chen X. Nanosecond pulsed electric field inhibits proliferation and induces apoptosis in human osteosarcoma. J Orthop Surg Res. 2015;10:104. https://doi.org/10.1186/s13018-015-0247-z .
doi: 10.1186/s13018-015-0247-z
pubmed: 26148858
pmcid: 4496869
Cui G, Diao H. Research advances of anti-tumor immune response induced by pulse electric field ablation. Zhejiang Da Xue Xue Bao Yi Xue Ban. 2015;44:672–7.
pubmed: 26822051
Rossi A, Pakhomova ON, Mollica PA, Casciola M, Mangalanathan U, Pakhomov AG, Muratori C. Nanosecond pulsed electric fields induce endoplasmic reticulum stress accompanied by immunogenic cell death in murine models of lymphoma and colorectal cancer. Cancers. 2019. https://doi.org/10.3390/cancers11122034 .
doi: 10.3390/cancers11122034
pubmed: 31861557
pmcid: 7017364
Chen X, James Swanson R, Kolb JF, Nuccitelli R, Schoenbach KH. Histopathology of normal skin and melanomas after nanosecond pulsed electric field treatment. Melanoma Res. 2009;19:361–71. https://doi.org/10.1097/CMR.0b013e32832f1558 .
doi: 10.1097/CMR.0b013e32832f1558
pubmed: 19730404
pmcid: 3137734
Chen X, Kolb JF, Swanson RJ, Schoenbach KH, Beebe SJ. Apoptosis initiation and angiogenesis inhibition: melanoma targets for nanosecond pulsed electric fields. Pigment Cell Melanoma Res. 2010;23:554–63. https://doi.org/10.1111/j.1755-148X.2010.00704.x .
doi: 10.1111/j.1755-148X.2010.00704.x
pubmed: 20370854
Neumann E, Sowers AE, Jordan CA. Electroporation and electrofusion in cell biology. New York: Plenum Press; 1989.
doi: 10.1007/978-1-4899-2528-2
Teissié A, Eynard A, Gabriel A, Rols A. Electropermeabilization of cell membranes. Adv Drug Deliv Rev. 1999;35:3–19. https://doi.org/10.1016/s0169-409x(98)00060-x .
doi: 10.1016/s0169-409x(98)00060-x
pubmed: 10837686
Breton M, Mir LM. Microsecond and nanosecond electric pulses in cancer treatments. Bioelectromagnetics. 2012;33:106–23. https://doi.org/10.1002/bem.20692 .
doi: 10.1002/bem.20692
pubmed: 21812011
Pakhomov AG, Miklavcic D, Markov MS, editors. Advanced electroporation techniques in biology in medicine. Boca Raton: CRC Press; 2010.
Zimmermann U, Friedrich U, Mussauer H, Gessner P, Hämel K, Sukhorukov V. Electromanipulation of mammalian cells: fundamentals and application. IEEE Trans Plasma Sci. 2000;28(1):72–822000.
doi: 10.1109/27.842868
Tarek M. Membrane electroporation: a molecular dynamics simulation. Biophys J. 2005;88:4045–53. https://doi.org/10.1529/biophysj.104.050617 .
doi: 10.1529/biophysj.104.050617
pubmed: 15764667
pmcid: 1305635
Gowrishankar TR, Esser AT, Vasilkoski Z, Smith KC, Weaver JC. Microdosimetry for conventional and supra-electroporation in cells with organelles. Biochem Biophys Res Commun. 2006;341:1266–76. https://doi.org/10.1016/j.bbrc.2006.01.094 .
doi: 10.1016/j.bbrc.2006.01.094
pubmed: 16469297
Delemotte L, Tarek M. Molecular dynamics simulations of lipid membrane electroporation. J Membr Biol. 2012;245:531–43. https://doi.org/10.1007/s00232-012-9434-6 .
doi: 10.1007/s00232-012-9434-6
pubmed: 22644388
Kotnik T, Rems L, Tarek M, Miklavčič D. Membrane electroporation and electropermeabilization: mechanisms and models. Annu Rev Biophys. 2019;48:63–91. https://doi.org/10.1146/annurev-biophys-052118-115451 .
doi: 10.1146/annurev-biophys-052118-115451
pubmed: 30786231
Cui C, Merritt R, Fu L, Pan Z. Targeting calcium signaling in cancer therapy. Acta Pharm Sin B. 2017;7:3–17. https://doi.org/10.1016/j.apsb.2016.11.001 .
doi: 10.1016/j.apsb.2016.11.001
pubmed: 28119804
Carr L, Bardet SM, Arnaud-Cormos D, Leveque P, O’Connor RP. Visualisation of an nsPEF induced calcium wave using the genetically encoded calcium indicator GCaMP in U87 human glioblastoma cells. Bioelectrochemistry. 2018;119:68–75. https://doi.org/10.1016/j.bioelechem.2017.09.003 .
doi: 10.1016/j.bioelechem.2017.09.003
pubmed: 28917183
White JA, Blackmore PF, Schoenbach KH, Beebe SJ. Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J Biol Chem. 2004;279:22964–72. https://doi.org/10.1074/jbc.M311135200 .
doi: 10.1074/jbc.M311135200
pubmed: 15026420
Vernier PT, Sun Y, Marcu L, Salemi S, Craft CM, Gundersen MA. Calcium bursts induced by nanosecond electric pulses. Biochem Biophys Res Commun. 2003;310:286–95. https://doi.org/10.1016/j.bbrc.2003.08.140 .
doi: 10.1016/j.bbrc.2003.08.140
pubmed: 14521908
Semenov I, Xiao S, Pakhomov AG. Primary pathways of intracellular Ca(2+) mobilization by nanosecond pulsed electric field. Biochim Biophys Acta. 2013;1828:981–9. https://doi.org/10.1016/j.bbamem.2012.11.032 .
doi: 10.1016/j.bbamem.2012.11.032
pubmed: 23220180
Beebe SJ, Sain NM, Ren W. Induction of cell death mechanisms and apoptosis by nanosecond pulsed electric fields (nsPEFs). Cells. 2013;2:136–62. https://doi.org/10.3390/cells2010136 .
doi: 10.3390/cells2010136
pubmed: 24709649
pmcid: 3972658
Nuccitelli R, McDaniel A, Connolly R, Zelickson B, Hartman H. Nano-pulse stimulation induces changes in the intracellular organelles in rat liver tumors treated in situ. Lasers Surg Med. 2020;52(9):882–9. https://doi.org/10.1002/lsm.23239 .
doi: 10.1002/lsm.23239
pubmed: 32220023
pmcid: 7586959
Ren Z, Chen X, Cui G, Yin S, Chen L, Jiang J, Hu Z, Xie H, Zheng S, Zhou L. Nanosecond pulsed electric field inhibits cancer growth followed by alteration in expressions of NF-κB and Wnt/β-catenin signaling molecules. PLoS ONE. 2013;8:e74322. https://doi.org/10.1371/journal.pone.0074322 .
doi: 10.1371/journal.pone.0074322
pubmed: 24069295
pmcid: 3775773
Rossi A, Pakhomova ON, Pakhomov AG, Weygandt S, Bulysheva AA, Murray LE, Mollica PA, Muratori C. Mechanisms and immunogenicity of nsPEF-induced cell death in B16F10 melanoma tumors. Sci Rep. 2019;9:431. https://doi.org/10.1038/s41598-018-36527-5 .
doi: 10.1038/s41598-018-36527-5
pubmed: 30674926
pmcid: 6344591
Xu X, Chen Y, Zhang R, Miao X, Chen X. Activation of anti-tumor Immune response by ablation of HCC with nanosecond pulsed electric field. J Clin Transl Hepatol. 2018;6:85–8. https://doi.org/10.14218/JCTH.2017.00042 .
doi: 10.14218/JCTH.2017.00042
pubmed: 29577034
Chen R, Sain NM, Harlow KT, Chen Y-J, Shires PK, Heller R, Beebe SJ. A protective effect after clearance of orthotopic rat hepatocellular carcinoma by nanosecond pulsed electric fields. Eur J Cancer. 2014;50:2705–13. https://doi.org/10.1016/j.ejca.2014.07.006 .
doi: 10.1016/j.ejca.2014.07.006
pubmed: 25081978
Nuccitelli R, Berridge JC, Mallon Z, Kreis M, Athos B, Nuccitelli P. Nanoelectroablation of murine tumors triggers a CD8-dependent inhibition of secondary tumor growth. PLoS ONE. 2015;10:e0134364. https://doi.org/10.1371/journal.pone.0134364 .
doi: 10.1371/journal.pone.0134364
pubmed: 26231031
pmcid: 4521782
Nuccitelli R, Tran K, Lui K, Huynh J, Athos B, Kreis M, Nuccitelli P, De Fabo EC. Non-thermal nanoelectroablation of UV-induced murine melanomas stimulates an immune response. Pigment Cell Melanoma Res. 2012;25:618–29. https://doi.org/10.1111/j.1755-148X.2012.01027.x .
doi: 10.1111/j.1755-148X.2012.01027.x
pubmed: 22686288
pmcid: 3760242
Soueid M, Kohler S, Carr L, Bardet SM, O’Connor RP, Leveque P, Arnaud-Cormos P. Electromagnetic analysis of an aperture modified TEM cell including an ITO layer for real-time observation of biological cells exposed to microwaves. Progr Electromagn Res. 2014;149:193–204.
doi: 10.2528/PIER14053108
Kenaan M, El Amari S, Silve A, Merla C, Mir LM, Couderc V, Arnaud-Cormos D, Leveque P. Characterization of a 50- Ω exposure setup for high-voltage nanosecond pulsed electric field bioexperiments. IEEE Trans Biomed Eng. 2011;58:207–14. https://doi.org/10.1109/TBME.2010.2081670 .
doi: 10.1109/TBME.2010.2081670
pubmed: 20876001
Wu Y-H, Arnaud-Cormos D, Casciola M, Sanders JM, Leveque P, Vernier PT. Moveable wire electrode microchamber for nanosecond pulsed electric-field delivery. IEEE Trans Biomed Eng. 2013;60:489–96. https://doi.org/10.1109/TBME.2012.2228650 .
doi: 10.1109/TBME.2012.2228650
pubmed: 23192479
Taibi A, Albouys J, Jacques J, Perrin M-L, Yardin C, Durand Fontanier S, Bardet SM. Comparison of implantation sites for the development of peritoneal metastasis in a colorectal cancer mouse model using non-invasive bioluminescence imaging. PLoS ONE. 2019;14:e0220360. https://doi.org/10.1371/journal.pone.0220360 .
doi: 10.1371/journal.pone.0220360
pubmed: 31365553
pmcid: 6668798
Solass W, Sempoux C, Detlefsen S, Carr NJ, Bibeau F. Peritoneal sampling and histological assessment of therapeutic response in peritoneal metastasis: proposal of the Peritoneal Regression Grading Score (PRGS). Pleura and Peritoneum. 2016;1(2):99–107. https://doi.org/10.1515/pp-2016-0011 .
doi: 10.1515/pp-2016-0011
pubmed: 30911613
pmcid: 6328069
Yin S, Chen X, Hu C, Zhang X, Hu Z, Yu J, Feng X, Jiang K, Ye S, Shen K, Xie H, Zhou L, James Swanson R, et al. Nanosecond pulsed electric field (nsPEF) treatment for hepatocellular carcinoma: a novel locoregional ablation decreasing lung metastasis. Cancer Lett. 2014;346:285–91. https://doi.org/10.1016/j.canlet.2014.01.009 .
doi: 10.1016/j.canlet.2014.01.009
pubmed: 24462824
Chen X, Yin S, Hu C, Chen X, Jiang K, Ye S, Feng X, Fan S, Xie H, Zhou L, Zheng S. Comparative study of nanosecond electric fields in vitro and in vivo on hepatocellular carcinoma indicate macrophage infiltration contribute to tumor ablation in vivo. PLoS ONE. 2014;9:e86421. https://doi.org/10.1371/journal.pone.0086421 .
doi: 10.1371/journal.pone.0086421
pubmed: 24475118
pmcid: 3903538
Takeshima T, Chamoto K, Wakita D, Ohkuri T, Togashi Y, Shirato H, Kitamura H, Nishimura T. Local radiation therapy inhibits tumor growth through the generation of tumor-specific CTL: its potentiation by combination with Th1 cell therapy. Cancer Res. 2010;70:2697–706. https://doi.org/10.1158/0008-5472.CAN-09-2982 .
doi: 10.1158/0008-5472.CAN-09-2982
pubmed: 20215523
Abboud K, André T, Brunel M, Ducreux M, Eveno C, Glehen O, Goéré D, Gornet J-M, Lefevre JH, Mariani P, Pinto A, Quenet F, Sgarbura O, et al. Management of colorectal peritoneal metastases: expert opinion. J Visc Surg. 2019;156:377–9. https://doi.org/10.1016/j.jviscsurg.2019.08.002 .
doi: 10.1016/j.jviscsurg.2019.08.002
pubmed: 31466831
Alyami M, Hübner M, Grass F, Bakrin N, Villeneuve L, Laplace N, Passot G, Glehen O, Kepenekian V. Pressurised intraperitoneal aerosol chemotherapy: rationale, evidence, and potential indications. Lancet Oncol. 2019;20:e368–77. https://doi.org/10.1016/S1470-2045(19)30318-3 .
doi: 10.1016/S1470-2045(19)30318-3
pubmed: 31267971
Hristov K, Mangalanathan U, Casciola M, Pakhomova ON, Pakhomov AG. Expression of voltage-gated calcium channels augments cell susceptibility to membrane disruption by nanosecond pulsed electric field. Biochim Biophys Acta Biomembr. 2018;1860:2175–83. https://doi.org/10.1016/j.bbamem.2018.08.017 .
doi: 10.1016/j.bbamem.2018.08.017
pubmed: 30409513
Nesin OM, Pakhomova ON, Xiao S, Pakhomov AG. Manipulation of cell volume and membrane pore comparison following single cell permeabilization with 60- and 600-ns electric pulses. Biochim Biophys Acta. 2011;1808:792–801. https://doi.org/10.1016/j.bbamem.2010.12.012 .
doi: 10.1016/j.bbamem.2010.12.012
pubmed: 21182825
Pakhomov AG, Kolb JF, White JA, Joshi RP, Xiao S, Schoenbach KH. Long-lasting plasma membrane permeabilization in mammalian cells by nanosecond pulsed electric field (nsPEF). Bioelectromagnetics. 2007;28:655–63. https://doi.org/10.1002/bem.20354 .
doi: 10.1002/bem.20354
pubmed: 17654532
Bowman AM, Nesin OM, Pakhomova ON, Pakhomov AG. Analysis of plasma membrane integrity by fluorescent detection of Tl(+) uptake. J Membr Biol. 2010;236:15–26. https://doi.org/10.1007/s00232-010-9269-y .
doi: 10.1007/s00232-010-9269-y
pubmed: 20623351
pmcid: 2922847
Creighton TE. Proteins: structures and molecular properties. New York: W.H. Freeman; 1993.
Nuccitelli R, Chen X, Pakhomov AG, Baldwin WH, Sheikh S, Pomicter JL, Ren W, Osgood C, Swanson RJ, Kolb JF, Beebe SJ, Schoenbach KH. A new pulsed electric field therapy for melanoma disrupts the tumor’s blood supply and causes complete remission without recurrence. Int J Cancer. 2009;125:438–45. https://doi.org/10.1002/ijc.24345 .
doi: 10.1002/ijc.24345
pubmed: 19408306
pmcid: 2731679
Beebe SJ, White J, Blackmore PF, Deng Y, Somers K, Schoenbach KH. Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol. 2003;22:785–96. https://doi.org/10.1089/104454903322624993 .
doi: 10.1089/104454903322624993
pubmed: 14683589
Beebe SJ, Fox PM, Rec LJ, Willis ELK, Schoenbach KH. Nanosecond, high-intensity pulsed electric fields induce apoptosis in human cells. FASEB J. 2003;17:1493–5. https://doi.org/10.1096/fj.02-0859fje .
doi: 10.1096/fj.02-0859fje
pubmed: 12824299
Ford WE, Ren W, Blackmore PF, Schoenbach KH, Beebe SJ. Nanosecond pulsed electric fields stimulate apoptosis without release of pro-apoptotic factors from mitochondria in B16f10 melanoma. Arch Biochem Biophys. 2010;497:82–9. https://doi.org/10.1016/j.abb.2010.03.008 .
doi: 10.1016/j.abb.2010.03.008
pubmed: 20346344
Hall EH, Schoenbach KH, Beebe SJ. Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells. Apoptosis. 2007;12:1721–31. https://doi.org/10.1007/s10495-007-0083-7 .
doi: 10.1007/s10495-007-0083-7
pubmed: 17520193
Vincelette RL, Roth CC, McConnell MP, Payne JA, Beier HT, Ibey BL. Thresholds for phosphatidylserine externalization in Chinese hamster ovarian cells following exposure to nanosecond pulsed electrical fields (nsPEF). PLoS ONE. 2013;8:e63122. https://doi.org/10.1371/journal.pone.0063122 .
doi: 10.1371/journal.pone.0063122
pubmed: 23658665
pmcid: 3639203
Muratori C, Pakhomov AG, Gianulis E, Meads J, Casciola M, Mollica PA, Pakhomova ON. Activation of the phospholipid scramblase TMEM16F by nanosecond pulsed electric fields (nsPEF) facilitates its diverse cytophysiological effects. J Biol Chem. 2017;292:19381–91. https://doi.org/10.1074/jbc.M117.803049 .
doi: 10.1074/jbc.M117.803049
pubmed: 28982976
pmcid: 5702676
Pakhomova ON, Gregory BW, Semenov I, Pakhomov AG. Two modes of cell death caused by exposure to nanosecond pulsed electric field. PLoS ONE. 2013;8:e70278. https://doi.org/10.1371/journal.pone.0070278 .
doi: 10.1371/journal.pone.0070278
pubmed: 23894630
pmcid: 3720895
Mir LM, Orlowski S, Belehradek J, Paoletti C. Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. Eur J Cancer. 1991;27:68–72.
doi: 10.1016/0277-5379(91)90064-K
García-Sánchez T, Leray I, Ronchetti M, Cadossi R, Mir LM. Impact of the number of electric pulses on cell electrochemotherapy in vitro: limits of linearity and saturation. Bioelectrochemistry. 2019;129:218–27. https://doi.org/10.1016/j.bioelechem.2019.05.021 .
doi: 10.1016/j.bioelechem.2019.05.021
pubmed: 31200252
Wu S, Guo J, Wei W, Zhang J, Fang J, Beebe SJ. Enhanced breast cancer therapy with nsPEFs and low concentrations of gemcitabine. Cancer Cell Int. 2014;14:98. https://doi.org/10.1186/s12935-014-0098-4 .
doi: 10.1186/s12935-014-0098-4
pubmed: 25379013
pmcid: 4209047
Morotomi-Yano K, Akiyama H, Yano K. Nanosecond pulsed electric fields activate MAPK pathways in human cells. Arch Biochem Biophys. 2011;515:99–106. https://doi.org/10.1016/j.abb.2011.09.002 .
doi: 10.1016/j.abb.2011.09.002
pubmed: 21933660
Morotomi-Yano K, Oyadomari S, Akiyama H, Yano K. Nanosecond pulsed electric fields act as a novel cellular stress that induces translational suppression accompanied by eIF2α phosphorylation and 4E-BP1 dephosphorylation. Exp Cell Res. 2012;318:1733–44. https://doi.org/10.1016/j.yexcr.2012.04.016 .
doi: 10.1016/j.yexcr.2012.04.016
pubmed: 22652449
Morotomi-Yano K, Akiyama H, Yano K. Nanosecond pulsed electric fields activate AMP-activated protein kinase: implications for calcium-mediated activation of cellular signaling. Biochem Biophys Res Commun. 2012;428:371–5. https://doi.org/10.1016/j.bbrc.2012.10.061 .
doi: 10.1016/j.bbrc.2012.10.061
pubmed: 23103546
Gao C, Zhang X, Chen J, Zhao J, Liu Y, Zhang J, Wang J. Utilizing the nanosecond pulse technique to improve antigen intracellular delivery and presentation to treat tongue squamous cell carcinoma. Med Oral Patol Oral Cir Bucal. 2018;23:e344–50. https://doi.org/10.4317/medoral.22227 .
doi: 10.4317/medoral.22227
pubmed: 29680844
pmcid: 5945238
Kaufman D, Martinez M, Jauregui L, Ebbers E, Nuccitelli R, Knape WA, Uecker D, Mehregan D. A dose-response study of a novel method of selective tissue modification of cellular structures in the skin with nanosecond pulsed electric fields. Lasers Surg Med. 2020;52:315–22. https://doi.org/10.1002/lsm.23145 .
doi: 10.1002/lsm.23145
pubmed: 31376199
Nuccitelli R, Wood R, Kreis M, Athos B, Huynh J, Lui K, Nuccitelli P, Epstein EH. First-in-human trial of nanoelectroablation therapy for basal cell carcinoma: proof of method. Exp Dermatol. 2014;23:135–7. https://doi.org/10.1111/exd.12303 .
doi: 10.1111/exd.12303
pubmed: 24330263
pmcid: 3946678
Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol. 2002;2:965–75. https://doi.org/10.1038/nri957 .
doi: 10.1038/nri957
pubmed: 12461569
Tougeron D, Fauquembergue E, Latouche J-B. Immune response and colorectal cancer. Bull Cancer. 2013;100:283–94. https://doi.org/10.1684/bdc.2013.1716 .
doi: 10.1684/bdc.2013.1716
pubmed: 23501583
Atreya I, Neurath MF. Immune cells in colorectal cancer: prognostic relevance and therapeutic strategies. Exp Rev Anticancer Ther. 2008;8:561–72. https://doi.org/10.1586/14737140.8.4.561 .
doi: 10.1586/14737140.8.4.561
Rubbia-Brandt L, Giostra E, Brezault C, Roth AD, Andres A, Audard V, Sartoretti P, Dousset B, Majno PE, Soubrane O, Chaussade S, Mentha G, Terris B. Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery. Ann Oncol. 2007;18:299–304. https://doi.org/10.1093/annonc/mdl386 .
doi: 10.1093/annonc/mdl386
pubmed: 17060484
Passot G, You B, Boschetti G, Fontaine J, Isaac S, Decullier E, Maurice C, Vaudoyer D, Gilly F-N, Cotte E, Glehen O. Pathological response to neoadjuvant chemotherapy: a new prognosis tool for the curative management of peritoneal colorectal carcinomatosis. Ann Surg Oncol. 2014;21:2608–14. https://doi.org/10.1245/s10434-014-3647-0 .
doi: 10.1245/s10434-014-3647-0
pubmed: 24668148
Bardet SM, Cortese J, Blanc R, Mounayer C, Rouchaud A. Multiphoton microscopy for pre-clinical evaluation of flow-diverter stents for treating aneurysms. J Neuroradiol. 2020. https://doi.org/10.1016/j.neurad.2020.03.005 .
doi: 10.1016/j.neurad.2020.03.005
pubmed: 32205257
Taibi A, Lo Dico R, Kaci R, Naneix AL, Malgras B, Mathonnet M, Pocard M. Evaluation of a new histological grading system for assessing the response to chemotherapy of peritoneal metastases from colorectal cancer: a mouse model study. Eur J Surg Oncol. 2020;46:160–5. https://doi.org/10.1016/j.ejso.2019.09.008 .
doi: 10.1016/j.ejso.2019.09.008
pubmed: 31540756
Benzerdjeb N, Durieux E, Tantot J, Isaac S, Fontaine J, Harou O, Glehen O, Kepenekian V, Alyami M, Villeneuve L, Laplace N, Traverse-Glehen A, Shisheboran-Devouassoux M, et al. Prognostic impact of combined progression index based on peritoneal grading regression score and peritoneal cytology in peritoneal metastasis. Histopathology. 2020;77(4):548–59. https://doi.org/10.1111/his.14092 .
doi: 10.1111/his.14092
pubmed: 32060943
Taibi A, Dico R, Kaci R, Naneix AL, Mathonnet M, Pocard M. Impact of preoperative chemotherapy on the histological response of patients with peritoneal metastases from colorectal cancer according to peritoneal regression grading score (PRGS) and TRG. Surg Oncol. 2020;33:158–63. https://doi.org/10.1016/j.suronc.2020.02.014 .
doi: 10.1016/j.suronc.2020.02.014
pubmed: 32561082
Lee ZJ, Chia SL, Tan G, Soo KC, Teo CCM. Cost effectiveness of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for management of colorectal peritoneal carcinomatosis. Ann Surg Oncol. 2018;25:2340–6. https://doi.org/10.1245/s10434-018-6508-4 .
doi: 10.1245/s10434-018-6508-4
pubmed: 29948417