Evaluation of YO-PRO-1 as an early marker of apoptosis following radiofrequency ablation of colon cancer liver metastases

Cytotechnology

Volumn 66, Issue 2, 2014, Pages 259-273

  Fujisawa, Sho ^a   Romin, Yevgeniy ^a   Barlas, Afsar ^a   Petrovic, Lydia M ^b   Turkekul, Mesruh ^a   Fan, Ning ^a   Xu, Ke ^a   Garcia, Alessandra R ^a   Monette, Sebastien ^a   Klimstra, David S ^a   Erinjeri, Joseph P ^a   Solomon, Stephen B ^a   Manova Todorova, Katia ^a   Sofocleous, Constantinos T ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Apoptosis; Cell necrosis; Cell viability; Colon cancer; Liver tumor ablation; P2X7 receptor; Propidium iodide (PI); TUNEL; YoPro 1 (YP1)

Indexed keywords

EID: 84894368834     PISSN: 09209069     EISSN: 15730778     Source Type: Journal    
DOI: 10.1007/s10616-013-9565-3     Document Type: Article

References (58)

1. Abitabile P, Hartl U, Lange J, Maurer CA (2007) Radiofrequency ablation permits an effective treatment for colorectal liver metastasis. Eur J Surg Oncol 33:67-71. doi: 10.1016/j.ejso.2006.10.040
2. Amersi FF, McElrath-Garza A, Ahmad A, Zogakis T, Allegra DP, Krasne R, Bilchik AJ (2006) Long-term survival after radiofrequency ablation of complex unresectable liver tumors. Arch Surg 141:581-587. doi: 10.1001/archsurg.141.6. 581
3. Boffa DJ, Waka J, Thomas D, Suh S, Curran K, Sharma VK, Besada M, Muthukumar T, Yang H, Suthanthiran M, Manova K (2005) Measurement of apoptosis of intact human islets by confocal optical sectioning and stereologic analysis of YO-PRO-1-stained islets. Transplantation 79:842-845. doi: 10.1097/01.TP.0000155175.24802.73
4. Castañeda F, Kinne RKH (2000) Cytotoxicity of millimolar concentrations of ethanol on HepG2 human tumor cell line compared to normal rat hepatocytes in vitro. J Cancer Res Clin Oncol 126:503-510
5. Chagnon F, Fournier C, Charette PG, Moleski L, Payet MD, Dobbs LG, Lesur O (2010) In vivo intravital endoscopic confocal fluorescence microscopy of normal and acutely injured rat lungs. Lab Invest J Tech Methods Pathol 90:824-834. doi: 10.1038/labinvest.2010.76
6. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, Isakson BE, Bayliss DA, Ravichandran KS (2010) Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467:863-867. doi: 10.1038/nature09413
7. Chiappa A, Makuuchi M, Lygidakis NJ, Zbar AP, Chong G, Bertani E, Sitzler PJ, Biffi R, Pace U, Bianchi PP, Contino G, Misitano P, Orsi F, Travaini L, Trifirò G, Zampino MG, Fazio N, Goldhirsch A, Andreoni B (2009) The management of colorectal liver metastases: expanding the role of hepatic resection in the age of multimodal therapy. Crit Rev Oncol Hematol 72:65-75. doi: 10.1016/j.critrevonc.2008.11.003
8. Chow SC, Kass GEN, Orrenius S (1997) Purines and their roles in apoptosis. Neuropharmacology 36:1149-1156. doi: 10.1016/S0028-3908(97)00123-8
9. Emmett DS, Feranchak A, Kilic G, Puljak L, Miller B, Dolovcak S, McWilliams R, Doctor RB, Fitz JG (2008) Characterization of ionotrophic purinergic receptors in hepatocytes. Hepatology 47:698-705. doi: 10.1002/hep.22035
10. Gawlitta D, Oomens CW, Baaijens FP, Bouten CV (2004) Evaluation of a continuous quantification method of apoptosis and necrosis in tissue cultures. Cytotechnology 46:139-150. doi: 10.1007/s10616-005-2551-7
11. Gillams AR (2005) The use of radiofrequency in cancer. Br J Cancer 92:1825-1829. doi: 10.1038/sj.bjc.6602582
12. Gohla A, Eckert K, Maurer HR (1996) A rapid and sensitive fluorometric screening assay using YO-PRO-1 to quantify tumour cell invasion through Matrigel. Clin Exp Metastasis 14:451-458. doi: 10.1007/BF00128961
13. Goldberg SN, Gazelle GS, Compton CC, Mueller PR, Tanabe KK (2000) Treatment of intrahepatic malignancy with radiofrequency ablation: radiologic-pathologic correlation. Cancer 88:2452-2463. doi: 10.1002/1097-0142(20000601)88:11<2452:AID-CNCR5>3.0.CO;2-3
14. Gorodeski GI (2009) P2X7-mediated chemoprevention of epithelial cancers. Expert Opin Ther Targets 13:1313-1332. doi: 10.1517/14728220903277249
15. Gwak JH, Oh BY, Lee RA, Chung SS, Kim KH (2011) Clinical applications of radio-frequency ablation in liver metastasis of colorectal cancer. J Korean Soc Coloproctol 27:202-210. doi: 10.3393/jksc.2011.27.4.202
16. Hanley PJ, Kronlage M, Kirschning C, del Rey A, Di Virgilio F, Leipziger J, Chessell IP, Sargin S, Filippov MA, Lindemann O, Mohr S, Konigs V, Schillers H, Bahler M, Schwab A (2012) Transient P2X7 receptor activation triggers macrophage death independent of Toll-like receptors 2 and 4, caspase-1, and pannexin-1 proteins. J Biol Chem 287:10650-10663. doi: 10.1074/jbc.M111.332676
17. Hanna NN (2004) Radiofrequency ablation of primary and metastatic hepatic malignancies. Clin Colorectal Cancer 4:92-100
18. Higashiyama S, Noda M, Kawase M, Yagi K (2003) Mixed-ligand modification of polyamidoamine dendrimers to develop an effective scaffold for maintenance of hepatocyte spheroids. J Biomed Mater Res Part A 64:475-482
19. Horbinski C, Mojesky C, Kyprianou N (2010) Live free or die: tales of homeless (cells) in cancer. Am J Pathol 177:1044-1052. doi: 10.1111/j.1582-4934. 2009.00832.x
20. Hur H, Ko YT, Min BS, Kim KS, Choi JS, Sohn SK, Cho CH, Ko HK, Lee JT, Kim NK (2009) Comparative study of resection and radiofrequency ablation in the treatment of solitary colorectal liver metastases. Am J Surg 197:728-736. doi: 10.1016/j.amjsurg.2008.04.013
21. Idziorek T, Estaquier J, De Bels F, Ameisen JC (1995) YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J Immunol Methods 185:249-258. doi: 10.1016/0022-1759(95)00172-7
22. Iglesias R, Locovei S, Roque A, Alberto AP, Dahl G, Spray DC, Scemes E (2008) P2X7 receptor-Pannexin1 complex: pharmacology and signaling. Am J Physiol Cell Physiol 295:C752-C760. doi: 10.1152/ajpcell.00228.2008
23. Ito S, Itoga K, Yamato M, Akamatsu H, Okano T (2010) The co-application effects of fullerene and ascorbic acid on UV-B irradiated mouse skin. Toxicology 267:27-38. doi: 10.1016/j.tox.2009.09.015
24. Jalilian I, Peranec M, Curtis BL, Seavers A, Spildrejorde M, Sluyter V, Sluyter R (2012) Activation of the damage-associated molecular pattern receptor P2X7 induces interleukin-1beta release from canine monocytes. Vet Immunol Immunopathol 149:86-91. doi: 10.1016/j.vetimm.2012.05.004
25. Kim KH, Yoon YS, Yu CS, Kim TW, Kim HJ, Kim PN, Ha HK, Kim JC (2011) Comparative analysis of radiofrequency ablation and surgical resection for colorectal liver metastases. J Korean Surg Soc 81:25-34. doi: 10.4174/jkss.2011.81.1.25
26. Kingham TP, Tanoue M, Eaton A, Rocha FG, Do R, Allen P, De Matteo RP, D'Angelica M, Fong Y, Jarnagin WR (2012) Patterns of recurrence after ablation of colorectal cancer liver metastases. Ann Surg Oncol 19:834-841. doi: 10.1245/s10434-011-2048-x
27. Kohler JE, Dubach JM, Naik HB, Tai K, Blass AL, Soybel DI (2010) Monochloramine-induced toxicity and dysregulation of intracellular Zn 2+ in parietal cells of rabbit gastric glands. Am J Physiol Gastrointest Liver Physiol 299:G170-G178. doi: 10.1152/ajpgi.00355.2009
28. Kuvshinoff BW, Ota DM (2002) Radiofrequency ablation of liver tumors: influence of technique and tumor size. Surgery 132:605-612. doi: 10.1067/msy.2002.127545
29. Lee HY, Bardini M, Burnstock G (2000) P2X receptor immunoreactivity in the male genital organs of the rat. Cell Tissue Res 300:321-330
30. Liao SD, Puro DG (2006) NAD+-induced vasotoxicity in the pericyte-containing microvasculature of the rat retina: effect of diabetes. Invest Ophthalmol Vis Sci 47:5032-5038. doi: 10.1167/iovs.06-0422
31. Liu SYW, Lee KF, Lai PBS (2009) Needle track seeding: a real hazard after percutaneous radiofrequency ablation for colorectal liver metastasis. World J Gastroenterol 15:1653-1655. doi: 10.3748/wjg.15.1653
32. Livraghi T, Solbiati L, Meloni F, Ierace T, Goldberg SN, Gazelle GS (2003) Percutaneous radiofrequency ablation of liver metastases in potential candidates for resection: the "test-of-time" approach. Cancer 97:3027-3035. doi: 10.1002/cncr.11426
33. Lupinacci R, Penna C, Nordlinger B (2007) Hepatectomy for resectable colorectal cancer metastases-indicators of prognosis, definition of resectability, techniques and outcomes. Surg Oncol Clin N Am 16:493-506. doi: 10.1016/j.soc.2007.04.014
34. Manova K, Tomihara-Newberger C, Wang S, Godelman A, Kalantry S, Witty-Blease K, De Leon V, Chen WS, Lacy E, Bachvarova RF (1998) Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice. Dev Dyn 213:293-308. doi: 10.1002/(SICI)1097-0177(199811)213:3<293:AID-AJA6>3.0.CO;2-D
35. McArdle A, Maglara A, Appleton P, Watson AJ, Grierson I, Jackson MJ (1999) Apoptosis in multinucleated skeletal muscle myotubes. Lab Invest 79:1069-1076
36. Michel AD, Kaur R, Chessell IP, Humphrey PPA (2000) Antagonist effects on human P2X 7 receptor-mediated cellular accumulation of YO-PRO-1. Br J Pharmacol 130:513-520
37. Mishra A, Chintagari NR, Guo Y, Weng T, Su L, Liu L (2011) Purinergic P2X 7 receptor regulates lung surfactant secretion in a paracrine manner. J Cell Sci 124:657-668. doi: 10.1242/jcs.066977
38. Misiakos EP, Karidis NP, Kouraklis G (2011) Current treatment for colorectal liver metastases. World J Gastroenterol 17:4067-4075. doi: 10.3748/wjg.v17.i36.4067
39. Morimoto M, Sugimori K, Shirato K, Kokawa A, Tomita N, Saito T, Tanaka N, Nozawa A, Hara M, Sekihara H, Shimada H, Imada T, Tanaka K (2002) Treatment of hepatocellular carcinoma with radiofrequency ablation: radiologic-histologic correlation during follow-up periods. Hepatology 35:1467-1475. doi: 10.1053/jhep.2002.33635
40. Mulier S, Ruers T, Jamart J, Michel L, Marchal G, Ni Y (2008) Radiofrequency ablation versus resection for resectable colorectal liver metastases: time for a randomized trial? An update. Dig Surg 25:445-460. doi: 10.1159/000184736
41. Nishida K, Nakatani T, Ohishi A, Okuda H, Higashi Y, Matsuo T, Fujimoto S, Nagasawa K (2012) Mitochondrial dysfunction is involved in P2X7 receptor-mediated neuronal cell death. J Neurochem 122:1118-1128. doi: 10.1111/j.1471-4159.2012.07868.x
42. Pulvirenti A, Garbagnati F, Regalia E, Coppa J, Marchiano A, Romito R, Schiavo M, Fabbri A, Burgoa L, Mazzaferro V (2001) Experience with radiofrequency ablation of small hepatocellular carcinomas before liver transplantation. Transplant Proc 33:1516-1517. doi: 10.1016/S0041-1345(00)02577- X
43. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM (2011) Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186:6553-6561. doi: 10.4049/jimmunol.1100478
44. Rai R, Richardson C, Flecknell P, Robertson H, Burt A, Manas DM (2005) Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA). J Surg Res 129:147-151. doi: 10.1016/j.jss.2005.03.020
45. Santos F, MacDonald G, Rubel EW, Raible DW (2006) Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear Res 213:25-33. doi: 10.1016/j.heares.2005.12.009
46. Siperstein AE, Berber E, Ballem N, Parikh RT (2007) Survival after radiofrequency ablation of colorectal liver metastases: 10-Year experience. Ann Surg 246:559-565. doi: 10.1097/SLA.0b013e318155a7b6
47. Snoeren N, Jansen MC, Rijken AM, van Hillegersberg R, Slooter G, Klaase J, van den Tol PM, van der Linden E, Ten Kate FJW, van Gulik TM (2009) Assessment of viable tumour tissue attached to needle applicators after local ablation of liver tumours. Dig Surg 26:56-62. doi: 10.1159/000194946
48. Snoeren N, Huiskens J, Rijken AM, Van Hillegersberg R, Van Erkel AR, Slooter GD, Klaase JM, Van Den Tol PM, Ten Kate FJW, Jansen MC, Van Gulik TM (2011) Viable tumor tissue adherent to needle applicators after local ablation: a risk factor for local tumor progression. Ann Surg Oncol 18:3702-3710. doi: 10.1245/s10434-011-1762-8
49. Sofocleous CT, Klein KM, Hubbi B, Brown KT, Weiss SH, Kannarkat G, Hinrichs CR, Contractor D, Bahramipour P, Barone A, Baker SR (2004) Histopathologic evaluation of tissue extracted on the radiofrequency probe after ablation of liver tumors: preliminary findings. Am J Roentgenol 183:209-213
50. Sofocleous CT, Nascimento RG, Petrovic LM, Klimstra DS, Gonen M, Brown KT, Brody LA, Covey AM, Thornton RH, Fong Y, Solomon SB, Schwartz LH, Dematteo RP, Getrajdman GI (2008) Histopathologic and immunohistochemical features of tissue adherent to multitined electrodes after RF ablation of liver malignancies can help predict local tumor progression: initial results 1. Radiology 249:364-374. doi: 10.1148/radiol.2491071752
51. Sofocleous CT, Petre EN, Gonen M, Brown KT, Solomon SB, Covey AM, Alago W, Brody LA, Thornton RH, D'Angelica M, Fong Y, Kemeny NE (2011) CT-guided radiofrequency ablation as a salvage treatment of colorectal cancer hepatic metastases developing after hepatectomy. J Vasc Interv Radiol 22:755-761. doi: 10.1016/j.jvir.2011.01.451
52. Sofocleous CT, Garg S, Petrovic LM, Gonen M, Petre EN, Klimstra DS, Solomon SB, Brown KT, Brody LA, Covey AM, DeMatteo RP, Schwartz L, Kemeny NE (2012) Ki-67 is a prognostic biomarker of survival after radiofrequency ablation of liver malignancies. Ann Surg Oncol 19:4264-4269. doi: 10.1245/s10434-012- 2461-9
53. Solbiati L, Livraghi T, Goldberg SN, Ierace T, Meloni F, Dellanoce M, Cova L, Halpern EF, Gazelle GS (2001) Percutaneous radio-frequency ablation of hepatic metastases from colorectal cancer: long-term results in 117 patients. Radiology 221:159-166
54. Sutherland LM, Williams JAR, Padbury RTA, Gotley DC, Stokes B, Maddern GJ (2006) Radiofrequency ablation of liver tumors: a systematic review. Arch Surg 141:181-190. doi: 10.1001/archsurg.141.2.181
55. Taylor JM, Han Z (2010) Purinergic receptor functionality is necessary for infection of human hepatocytes by hepatitis delta virus and hepatitis b virus. PLoS One 5:e15784. doi: 10.1371/journal.pone.0015784
56. Virginio C, Mackenzie A, North RA, Surprenant A (1999) Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J Physiol 519:335-346. doi: 10.1111/j.1469-7793.1999.0335m.x
57. Wang X, Sofocleous CT, Erinjeri JP, Petre EN, Gonen M, Do KG, Brown KT, Covey AM, Brody LA, Alago W, Thornton RH, Kemeny NE, Solomon SB (2013) Margin size is an independent predictor of local tumor progression after ablation of colon cancer liver metastases. Cardiovasc Intervent Radiol 36:166-175. doi: 10.1007/s00270-012-0377-1
58. Xiao F, Waldrop SL, Khimji AK, Kilic G (2012) Pannexin1 contributes to pathophysiological ATP release in lipoapoptosis induced by saturated free fatty acids in liver cells. Am J Physiol Cell Physiol 303:C1034-C1044. doi: 10.1152/ajpcell.00175.2012