Cytotoxicity of unsaturated fatty acids in fresh human tumor explants: Concentration thresholds and implications for clinical efficacy

Lipids in Health and Disease

Volumn 8, Issue , 2009, Pages

  Scheim, David E ^a  

^a NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA LINOLENIC ACID; LINOLENIC ACID;

ARTICLE; BREAST CARCINOMA; CHEMOSENSITIVITY; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; EXPLANT; FEMALE; GLIOBLASTOMA; HUMAN; MALE; MELANOMA; ORGAN CULTURE; OVARY ADENOCARCINOMA; PANCREAS CARCINOMA; CELL DEATH; DOSE RESPONSE; DRUG EFFECT; DRUG SCREENING; NEOPLASM; PATHOLOGY; SERUM; TREATMENT OUTCOME;

ANIMALIA;

ALPHA-LINOLENIC ACID; CELL DEATH; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; GAMMA-LINOLENIC ACID; HUMANS; NEOPLASMS; SERUM; TREATMENT OUTCOME;

EID: 75149133670     PISSN: None     EISSN: 1476511X     Source Type: Journal    
DOI: 10.1186/1476-511X-8-54     Document Type: Article

References (100)

1. Differential sensitivity of tumorigenic and genetically related non-tumorigenic cells to cytotoxic polyunsaturated fatty acids. ME Begin S Sircar JM Weber, Anticancer Res 1989 9 1049 1052 2554786
2. Cytotoxic effect of cis-parinaric acid in cultured malignant cells. AS Cornelius NR Yerram DA Kratz AA Spector, Cancer Res 1991 51 6025 6030 1933865
3. Tumoricidal action of cis-unsaturated fatty acids and their relationship to free radicals and lipid peroxidation. UN Das, Cancer Lett 1991 56 235 243 10.1016/0304-3835(91)90008-6 1850658
4. Mechanism of lipid peroxidation in cancer cells in response to gamma-linolenic acid (GLA) analyzed by GC-MS(I): Conjugated dienes with peroxyl (or hydroperoxyl) groups and cell-killing effects. S Takeda PG Sim DF Horrobin T Sanford KA Chisholm V Simmons, Anticancer Res 1993 13 193 199 8386494
5. Cytotoxicity of cis-parinaric acid in cultured malignant gliomas. VC Traynelis TC Ryken AS Cornelius, Neurosurgery 1995 37 484 489 10.1097/00006123-199509000-00017 7501114
6. Arachidonic and docosahexaenoic acids reduce the growth of A549 human lung-tumor cells increasing lipid peroxidation and PPARs. A Trombetta M Maggiora G Martinasso P Cotogni RA Canuto G Muzio, Chem Biol Interact 2007 165 239 250 10.1016/j.cbi.2006.12.014 17275799
7. Is gamma-linolenic acid an effective intravesical agent for superficial bladder cancer? In vitro cytotoxicity and in vivo tolerance studies. LZ Solomon AM Jennings MC Hayes PS Bass BR Birch AJ Cooper, Urol Res 1998 26 11 15 10.1007/s002400050016 9537690
8. Intravesical chemotherapy with gamma linolenic acid becomes a realistic prospect in serum-free applications: in vitro cytotoxicity and systemic absorption studies. LZ Solomon AM Jennings P Sharpe AJ Cooper BR Birch, J Urol 1998 160 2280 2283 10.1016/S0022-5347(01)62310-3 9817384
9. Mechanism of apoptosis in HL-60 cells induced by n-3 and n-6 polyunsaturated fatty acids. K Arita H Kobuchi T Utsumi Y Takehara J Akiyama AA Horton K Utsumi, Biochem Pharmacol 2001 62 821 828 10.1016/S0006-2952(01)00723-7 11543718
10. Influence of n-3 fatty acids on the growth of human breast cancer cells in vitro: relationship to peroxides and vitamin-E. V Chajes W Sattler A Stranzl GM Kostner, Breast Cancer Res Treat 1995 34 199 212 10.1007/BF00689711 7579484
11. Effect of eicosapentaenoic acid and other fatty acids on the growth in vitro of human pancreatic cancer cell lines. JS Falconer JA Ross KC Fearon RA Hawkins MG O'Riordain DC Carter, Br J Cancer 1994 69 826 832 8180010
12. n-3 and n-6 fatty acid processing and growth effects in neoplastic and non-cancerous human mammary epithelial cell lines. SI Grammatikos PV Subbaiah TA Victor WM Miller, Br J Cancer 1994 70 219 227 8054269
13. Arachidonic acid suppresses growth of human lung tumor A549 cells through down-regulation of ALDH3A1 expression. G Muzio A Trombetta M Maggiora G Martinasso V Vasiliou N Lassen RA Canuto, Free Radic Biol Med 2006 40 1929 1938 10.1016/j.freeradbiomed.2006.01.020 16716894
14. Induction of apoptosis in K562/ADM cells by gamma-linolenic acid involves lipid peroxidation and activation of caspase-3. X Kong H Ge L Hou L Shi Z Liu, Chem Biol Interact 2006 162 140 148 10.1016/j.cbi.2006.05.019 16857180
15. Opposing effects of n-6 and n-3 polyunsaturated fatty acids on pancreatic cancer growth. H Funahashi M Satake S Hasan H Sawai RA Newman HA Reber OJ Hines G Eibl, Pancreas 2008 36 353 362 10.1097/MPA.0b013e31815ccc44 18437081
16. Gamma-linolenic acid (GLA) is cytotoxic to 36B10 malignant rat astrocytoma cells but not to 'normal' rat astrocytes. S Vartak R McCaw CS Davis ME Robbins AA Spector, Br J Cancer 1998 77 1612 1620 9635836
17. Effects of n-3 fatty acids during neoplastic progression and comparison of in vitro and in vivo sensitivity of two human tumour cell lines. L Maehle E Eilertsen S Mollerup S Schonberg HE Krokan A Haugen, Br J Cancer 1995 71 691 696 7710930
18. Transformation renders MDR cells more sensitive to polyunsaturated fatty acids. S Sircar F Cai ME Begin JM Weber, Anticancer Res 1990 10 1783 1786 2178327
19. Vitamin E blocks the cytotoxic effect of gamma-linolenic acid when administered as late as the time of onset of cell death-insight into the mechanism of fatty acid induced cytotoxicity. GW Ells KA Chisholm VA Simmons DF Horrobin, Cancer Lett 1996 98 207 211 8556710
20. Effects of N-6 essential fatty acids on glioma invasion and growth: experimental studies with glioma spheroids in collagen gels. HS Bell SB Wharton HA Leaver IR Whittle, J Neurosurg 1999 91 989 996 10.3171/jns.1999.91.6.0989 10584845
21. Physiochemical perturbation of alpha-linolenic acid related to cell proliferation. H Fukui T Sato J Sunamoto, Bulletin of the Chemical Society of Japan 1994 67 2213 2218 10.1246/bcsj.67.2213 (Pubitemid 24315405)
22. Highly unsaturated fatty acid induced tumour regression in glioma pharmacodynamics and bioavailability of gamma linolenic acid in an implantation glioma model: effects on tumour biomass, apoptosis and neuronal tissue histology. HA Leaver SB Wharton HS Bell IM Leaver-Yap IR Whittle, Prostaglandins Leukot Essent Fatty Acids 2002 67 283 292 10.1054/plef.2002.0431 12445487
23. Dependence of photocarcinogenesis and photoimmunosuppression in the hairless mouse on dietary polyunsaturated fat. VE Reeve M Bosnic C Boehm-Wilcox, Cancer Lett 1996 108 271 279 10.1016/S0304-3835(96)04460-6 8973605
24. N-3 and N-6 fatty acids in breast adipose tissue and relative risk of breast cancer in a case-control study in Tours, France. V Maillard P Bougnoux P Ferrari ML Jourdan M Pinault F Lavillonniere G Body O Le Floch V Chajes, Int J Cancer 2002 98 78 83 10.1002/ijc.10130 11857389
25. Fat intake and risk of squamous cell carcinoma of the skin. IA Hakim RB Harris C Ritenbaugh, Nutr Cancer 2000 36 155 162 10.1207/S15327914NC3602-3 10890025
26. n-3 fatty acids decrease colonic epithelial cell proliferation in high-risk bowel mucosa. YC Huang JM Jessup RA Forse S Flickner D Pleskow HT Anastopoulos V Ritter GL Blackburn, Lipids 1996 31 Suppl 313 317 10.1007/BF02637099 8729142
27. Effect of lithium gamma-linolenate on the growth of experimental human pancreatic carcinoma. D Ravichandran A Cooper CD Johnson, Br J Surg 1998 85 1201 1205 10.1046/j.1365-2168.1998.00838.x 9752859
28. Gamma-linolenic acid inhibits both tumour cell cycle progression and angiogenesis in the orthotopic C6 glioma model through changes in VEGF, Flt1, ERK1/2, MMP2, cyclin D1, pRb, p53 and p27 protein expression. JA Miyake M Benadiba A Colquhoun, Lipids Health Dis 2009 8 8 10.1186/1476-511X-8-8 19292920
29. Local application of gamma-linolenic acid in the treatment of human gliomas. UN Das VV Prasad DR Reddy, Cancer Lett 1995 94 147 155 10.1016/0304-3835(95)03844-M 7634242
30. Intratumoral gamma-linoleic acid therapy of human gliomas. MR Naidu UN Das A Kishan, Prostaglandins Leukot Essent Fatty Acids 1992 45 181 184 10.1016/0952-3278(92)90110-5 1589443
31. Gamma-linolenic acid therapy of human gliomas. A Bakshi D Mukherjee AK Banerji UN Das, Nutrition 2003 19 305 309 10.1016/S0899-9007(02)00862-6 12679162
32. Gamma-linolenic acid therapy of human glioma-a review of in vitro, in vivo, and clinical studies. UN Das, Med Sci Monit 2007 13 A119 131 17599036
33. Intravesical meglumine gamma-linolenic acid in superficial bladder cancer: an efficacy study. NM Harris TJ Crook JP Dyer LZ Solomon P Bass AJ Cooper BR Birch, Eur Urol 2002 42 39 42 10.1016/S0302-2838(02)00208-7 12121728
34. Randomized, dose-finding phase III study of lithium gamolenate in patients with advanced pancreatic adenocarcinoma. CD Johnson M Puntis N Davidson S Todd R Bryce, Br J Surg 2001 88 662 668 10.1046/j.0007-1323.2001.01770.x 11350436
35. Controlled trial of gamma linolenic acid in Duke's C colorectal cancer. MB McIllmurray W Turkie, Br Med J (Clin Res Ed) 1987 294 1260 10.1136/bmj.294.6582.1260 3036291
36. The effect of gamma-linolenic acid, an in vitro cytostatic substance contained in evening primrose oil, on primary liver cancer. A double-blind placebo controlled trial. CF van der Merwe J Booyens HF Joubert CA van der Merwe, Prostaglandins Leukot Essent Fatty Acids 1990 40 199 202 10.1016/0952-3278(90)90098-6 2169638
37. Cytotoxic effects of two gamma linoleic salts (lithium gammalinolenate or meglumine gammalinolenate) alone or associated with a nitrosourea: an experimental study on human glioblastoma cell lines. K Ilc JM Ferrero JL Fischel P Formento R Bryce MC Etienne G Milano, Anticancer Drugs 1999 10 413 417 10.1097/00001813-199904000-00010 10378677
38. Dietary fish oil inhibits human breast carcinoma growth: a function of increased lipid peroxidation. MJ Gonzalez RA Schemmel L Dugan Jr JI Gray CW Welsch, Lipids 1993 28 827 832 10.1007/BF02536237 8231658
39. Individual human tumors in short-term micro-organ cultures: chemosensitivity testing by fluorescent cytoprinting. B Rotman C Teplitz K Dickinson JP Cozzolino, In Vitro Cell Dev Biol 1988 24 1137 1146 10.1007/BF02620817 3192508
40. Tumor Micro-organ cultures. B Rotman, Cell and Tissue Culture: Laboratory Procedures Chichester: John Wiley & Sons, Griffiths JDA, Newell DG, 1994 20.29.22-20.29.25
41. Prediction of response to drug therapy of cancer. A review of in vitro assays. WT Bellamy, Drugs 1992 44 690 708 10.2165/00003495-199244050-00002 1280562
42. Predictive value of the fluorescent cytoprint assay (FCA): a retrospective correlation study of in vitro chemosensitivity and individual responses to chemotherapy. LA Leone PA Meitner TJ Myers WR Grace WH Gajewski HJ Fingert B Rotman, Cancer Invest 1991 9 491 503 10.3109/07357909109018947 1933482
43. Prediction of drug resistance in cancer chemotherapy: the Kern and DiSC assays. LM Weisenthal DH Kern, Oncology (Williston Park) 1991 5 93 103 disc 104, 111-104, 117-108. 1835882
44. An overview of chemosensitivity testing. RD Blumenthal, Methods Mol Med 2005 110 3 18 15901922
45. Modeling of in vitro drug activity and prediction of clinical outcome in acute myeloid leukemia. A Quartino MO Karlsson A Freijs N Jonsson P Nygren J Kristensen E Lindhagen R Larsson, J Clin Pharmacol 2007 47 1014 1021 10.1177/0091270007302563 17660484
46. Cytotoxic action of cis-unsaturated fatty acids on human cervical carcinoma (HeLa) cells in vitro. PS Sagar UN Das, Prostaglandins Leukot Essent Fatty Acids 1995 53 287 299 10.1016/0952-3278(95)90129-9 8577783
47. Hepatocyte proliferation in vitro: its dependence on the use of serum-free hormonally defined medium and substrata of extracellular matrix. R Enat DM Jefferson N Ruiz-Opazo Z Gatmaitan LA Leinwand LM Reid, Proc Natl Acad Sci USA 1984 81 1411 1415 10.1073/pnas.81.5.1411 6584889
48. Incorporation of fatty acids by concanavalin A-stimulated lymphocytes and the effect on fatty acid composition and membrane fluidity. PC Calder P Yaqoob DJ Harvey A Watts EA Newsholme, Biochem J 1994 300 Pt 2 509 518 8002957
49. The decreased transfer of arachidonic acid from triglycerides to phospholipids during proliferation of a human gastric tumor (HGT) cell line is not linked to modification of membrane fluidity. A Najid D Es-Saady Y Denizot, Cancer Lett 1994 79 189 192 10.1016/0304-3835(94)90259-3 8019978
50. Mechanisms of the selective cytotoxic actions of certain essential fatty acids. RC Cantrill GW Ells AC DeMarco DF Horrobin, Adv Exp Med Biol 1997 400A 539 544 9547602
51. Cytostatic sensitivity and MDR in bladder carcinoma cells: implications for tumor therapy. H Schuldes JH Dolderer C Schoch R Bickeboller BG Woodcock, Int J Clin Pharmacol Ther 2000 38 204 208 10783830
52. Protein and lipid lateral diffusion in normal and Rous sarcoma virus transformed chick embryo fibroblasts. JA Boullier JS Peacock DA Roess BG Barisas, Biochim Biophys Acta 1992 1107 193 199 10.1016/0005-2736(92)90347-O 1319742
53. Local degradation of fibronectin at sites of expression of the transforming gene product pp60src. WT Chen JM Chen SJ Parsons JT Parsons, Nature 1985 316 156 158 10.1038/316156a0 2989711
54. Structure and properties of an under-sulfated heparan sulfate proteoglycan synthesized by a rat hepatoma cell line. J Robinson M Viti M Hook, J Cell Biol 1984 98 946 953 10.1083/jcb.98.3.946 6230367
55. High molecular weight, cell surface-associated glycoprotein (fibronectin) lost in malignant transformation. A Vaheri DF Mosher, Biochim Biophys Acta 1978 516 1 25 361081
56. Changes in microfilament organization and surface topogrophy upon transformation of chick embryo fibroblasts with Rous sarcoma virus. E Wang AR Goldberg, Proc Natl Acad Sci USA 1976 73 4065 4069 10.1073/pnas.73.11.4065 186784
57. Early changes in the distribution and organization of microfilament proteins during cell transformation. CB Boschek BM Jockusch RR Friis R Back E Grundmann H Bauer, Cell 1981 24 175 184 10.1016/0092-8674(81)90513-4 6263486
58. Temperature-sensitive changes in surface modulating assemblies of fibroblasts transformed by mutants of Rous sarcoma virus. GM Edelman I Yahara, Proc Natl Acad Sci USA 1976 73 2047 2051 10.1073/pnas.73.6.2047 180536
59. Actin cytoskeletal organization loss in the benign-to-malignant tumor transition in cultured human colonic epithelial cells. E Friedman M Verderame S Winawer R Pollack, Cancer Res 1984 44 3040 3050 6722823
60. Sensitivity of tumour cells to heat and ways of modifying the response. MB Yatvin WH Dennis JA Elegbede CE Elson, Symp Soc Exp Biol 1987 41 235 267 3332486
61. Metabolism of fatty acids by cultured tumor cells and their diploid precursor fibroblasts. LW Daniel LS Kucera M Waite, J Biol Chem 1980 255 5697 5702 6247342
62. Modification of the lipid composition of normal and Rous sarcoma virus-infected cells. Effects on transformation-associated membrane properties. AH Hale JE Pessin F Palmer MJ Weber M Glaser, J Biol Chem 1977 252 6190 6200 197083
63. Exposure to free fatty acid increases the transfer of albumin across cultured endothelial monolayers. B Hennig DM Shasby AB Fulton AA Spector, Arteriosclerosis 1984 4 489 497 6477300
64. Retention of human skin fibroblast fatty acid modifications during maintenance culture. AA Spector GM Denning LL Stoll, In Vitro 1980 16 932 940 10.1007/BF02619331 7450783
65. The influence of fatty acids on model cholesterol/phospholipid membranes. K Hac-Wydro P Wydro, Chem Phys Lipids 2007 150 66 81 10.1016/j.chemphyslip. 2007.06.213 17651712
66. Antitumour and pro-apoptotic actions of highly unsaturated fatty acids in glioma. HA Leaver HS Bell MT Rizzo JW Ironside A Gregor SB Wharton IR Whittle, Prostaglandins Leukot Essent Fatty Acids 2002 66 19 29 10.1054/plef.2001.0336 12051954
67. Growth inhibitory effect of lithium gammalinolenate on pancreatic cancer cell lines: the influence of albumin and iron. D Ravichandran A Cooper CD Johnson, Eur J Cancer 1998 34 188 192 10.1016/S0959-8049(97)00369-9 9624256
68. Anticancer activity of free gamma-linolenic acid on AH-109A rat hepatoma cells and the effect of serum albumin on anticancer activity of gamma-linolenic acid in vitro. Y Hayashi S Fukushima T Hirata S Kishimoto T Katsuki M Nakano, J Pharmacobiodyn 1990 13 705 711 1965510
69. Circulating nonesterified fatty acid level as a predictive risk factor for sudden death in the population. X Jouven MA Charles M Desnos P Ducimetiere, Circulation 2001 104 756 761 10.1161/hc3201.094151 11502698
70. Effects of caffeine on plasma free fatty acids, urinary catecholamines, and drug binding. RV Patwardhan PV Desmond RF Johnson GD Dunn DH Robertson AM Hoyumpa Jr S Schenker, Clin Pharmacol Ther 1980 28 398 403 7408399
71. Unesterified fatty acid in human blood plasma. RS Gordon Jr A Cherkes, J Clin Invest 1956 35 206 212 10.1172/JCI103265 13286339
72. Effect of 24-hour food-and-water deprivation on biochemical variables in blood. T Horne A Gutman SH Blondheim HB Aronson, Isr J Med Sci 1982 18 591 595 7096042
73. The effects of two levels of caffeine ingestion on excess postexercise oxygen consumption in untrained women. K Donelly L McNaughton, Eur J Appl Physiol Occup Physiol 1992 65 459 463 10.1007/BF00243514 1425653
74. Effects of caffeine ingestion on metabolic responses to prolonged walking in sedentary males. HJ Engels EM Haymes, Int J Sport Nutr 1992 2 386 396 1299508
75. Duration of coffee-and exercise-induced changes in the fatty acid profile of human serum. V Mougios S Ring A Petridou MG Nikolaidis, J Appl Physiol 2003 94 476 484 12391036
76. Plasma Free Fatty Acids in Exercise. K Rodahl HI Miller B Issekutz Jr, J Appl Physiol 1964 19 489 492 14173547
77. Plasma-triglycerides and exercise: a delicate balance. G Schlierf A Dinsenbacher U Voggenreiter B Drews H Kather M Kohlmeier, Klin Wochenschr 1988 66 129 133 10.1007/BF01774227 3352193
78. Effect of elevated blood FFA levels on endurance performance after a single fat meal ingestion. G Okano Y Sato Y Murata, Med Sci Sports Exerc 1998 30 763 768 10.1097/00005768-199805000-00019 9588621
79. Absorption of the n-3 eicosapentaenoic and docosahexaenoic acids as ethyl esters and triglycerides by humans. A Nordoy L Barstad WE Connor L Hatcher, Am J Clin Nutr 1991 53 1185 1190 1826985
80. Effects of polyunsaturated fatty acids and of their oxidation products on cell survival. ME Begin, Chem Phys Lipids 1987 45 269 313 10.1016/0009-3084(87) 90069-7 3319230
81. Concentration-dependent effect of iron on gamma-linolenic acid toxicity in ZR-75-1 human breast tumor cells in culture. RC Cantrill G Ells K Chisholm DF Horrobin, Cancer Lett 1993 72 99 102 10.1016/0304-3835(93)90017-4 8402582
82. Intracellular oxidation by human glioma cell populations: effect of arachidonic acid. HA Leaver JR Williams C Smith IR Whittle, Prostaglandins Leukot Essent Fatty Acids 2004 70 449 453 10.1016/j.plefa.2003.09.005 15062847
83. Changes in mechanisms of monocyte/macrophage-mediated cytotoxicity during culture. Reactive oxygen intermediates are involved in monocyte-mediated cytotoxicity, whereas reactive nitrogen intermediates are employed by macrophages in tumor cell killing. JH Martin SW Edwards, J Immunol 1993 150 3478 3486 8385686
84. Lipoprotein lipase activity and gene expression in lung cancer and in adjacent noncancer lung tissue. D Cerne E Melkic Z Trost M Sok J Marc, Exp Lung Res 2007 33 217 225 10.1080/01902140701481054 17620184
85. Metabolic effects of caffeine in humans: lipid oxidation or futile cycling? KJ Acheson G Gremaud I Meirim F Montigon Y Krebs LB Fay LJ Gay P Schneiter C Schindler L Tappy, Am J Clin Nutr 2004 79 40 46 14684395
86. Stimulation of fatty acid release in glioblastoma cells by caffeine. I Jeng N Klemm, Biochem Int 1984 9 631 635 6441576
87. Effect of polyunsaturated fatty acids on the drug sensitivity of human tumour cell lines resistant to either cisplatin or doxorubicin. JA Plumb W Luo DJ Kerr, Br J Cancer 1993 67 728 733 8385976
88. Greater sensitivity of human multidrug-resistant (mdr) cancer cells to polyunsaturated fatty acids than their non-mdr counterparts. JM Weber S Sircar ME Begin, J Natl Cancer Inst 1994 86 638 639 10.1093/jnci/86.8.638 8145280
89. Effects of polyunsaturated fatty acids on vincristine-resistance in human neuroblastoma cells. S Ikushima F Fujiwara S Todo S Imashuku, Anticancer Res 1991 11 1215 1220 1888152
90. Influence of docosahexaenoic acid on cisplatin resistance in a human small cell lung carcinoma cell line. H Timmer-Bosscha GA Hospers C Meijer NH Mulder FA Muskiet IA Martini DR Uges EG de Vries, J Natl Cancer Inst 1989 81 1069 1075 10.1093/jnci/81.14.1069 2544740
91. Elevated serum free fatty acid concentrations inhibit T lymphocyte signaling. TM Stulnig M Berger M Roden H Stingl D Raederstorff W Waldhausl, FASEB J 2000 14 939 947 10783148
92. Effect of elevated lipid concentrations on human skeletal muscle gene expression. RJ Tunstall D Cameron-Smith, Metabolism 2005 54 952 959 10.1016/j.metabol.2005.02.012 15988707
93. An evolutionary model of carcinogenesis. RA Gatenby TL Vincent, Cancer Res 2003 63 6212 6220 14559806
94. Ionizing radiation induces heritable disruption of epithelial cell interactions. CC Park RL Henshall-Powell AC Erickson R Talhouk B Parvin MJ Bissell MH Barcellos-Hoff, Proc Natl Acad Sci USA 2003 100 10728 10733 10.1073/pnas.1832185100 12960393
95. The role of the surface electrical transmembrane potential in normal and malignant mitogenesis. CD Cone Jr, Ann N Y Acad Sci 1974 238 420 435 10.1111/j.1749-6632.1974.tb26808.x 4613241
96. Induction of mitosis in mature neurons in central nervous system by sustained depolarization. CD Cone Jr CM Cone, Science 1976 192 155 158 10.1126/science.56781 56781
97. Transplantation of pluripotential nuclei from triploid frog tumors. RG McKinnell BA Deggins DD Labat, Science 1969 165 394 396 10.1126/science.165. 3891.394 5815255
98. Mouse embryos cloned from brain tumors. L Li MC Connelly C Wetmore T Curran JI Morgan, Cancer Res 2003 63 2733 2736 12782575
99. Reprogramming of a melanoma genome by nuclear transplantation. K Hochedlinger R Blelloch C Brennan Y Yamada M Kim L Chin R Jaenisch, Genes Dev 2004 18 1875 1885 10.1101/gad.1213504 15289459
100. AC Braun, The Biology of Cancer Reading, Mass.: Addison-Wesley 1974