Involvement of intrinsic mitochondrial pathway in neosergeolide-induced apoptosis of human HL-60 leukemia cells: The role of mitochondrial permeability transition pore and DNA damage

References

• Anazetti MC, Melo PS, Durán N, Haun M. (2003). Comparative cytotoxicity of dimethylamide-crotonin in the promyelocytic leukemia cell line (HL60) and human peripheral blood mononuclear cells. Toxicology, 188, 261–274.
   PubMed Web of Science ®Google Scholar
• de Andrade-Neto VF, Pohlit AM, Pinto AC, Silva EC, Nogueira KL, Melo MR, Henrique MC, Amorim RC, Silva LF, Costa MR, Nunomura RC, Nunomura SM, Alecrim WD, Alecrim MG, Chaves FC, Vieira PP. (2007). In vitro inhibition of Plasmodium falciparum by substances isolated from Amazonian antimalarial plants. Mem Inst Oswaldo Cruz, 102, 359–365.
   Google Scholar
• Armstrong JS. (2006). The role of the mitochondrial permeability transition in cell death. Mitochondrion, 6, 225–234.
   PubMed Web of Science ®Google Scholar
• Arseneau JC, Wolter JM, Kuperminc M, Ruckdeschel JC. (1983). A Phase II study of bruceantin (NSC-165, 563) in advanced malignant melanoma. Invest New Drugs, 1, 239–242.
   PubMedGoogle Scholar
• Bertani S, Houël E, Stien D, Chevolot L, Jullian V, Garavito G, Bourdy G, Deharo E. (2006). Simalikalactone D is responsible for the antimalarial properties of an Amazonian traditional remedy made with Quassia amara L. (Simaroubaceae). J Ethnopharmacol, 108, 155–157.
   PubMed Web of Science ®Google Scholar
• Brustovetsky N, Brustovetsky T, Jemmerson R, Dubinsky JM. (2002). Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J Neurochem, 80, 207–218.
   PubMed Web of Science ®Google Scholar
• Collins AR, Ma AG, Duthie SJ. (1995). The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutat Res, 336, 69–77.
   PubMed Web of Science ®Google Scholar
• Collins SJ. (1987). The HL-60 promyelocytic leukemia cell line: proliferation, differentiation, and cellular oncogene expression. Blood, 70, 1233–1244.
   PubMed Web of Science ®Google Scholar
• Crow JP. (1997). Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide, 1, 145–157.
   PubMed Web of Science ®Google Scholar
• Cuendet M, Christov K, Lantvit DD, Deng Y, Hedayat S, Helson L, McChesney JD, Pezzuto JM. (2004). Multiple myeloma regression mediated by bruceantin. Clin Cancer Res, 10, 1170–1179.
   PubMed Web of Science ®Google Scholar
• Cuendet M, Pezzuto JM. (2004). Antitumor activity of bruceantin: An old drug with new promise. J Nat Prod, 67, 269–272.
   PubMed Web of Science ®Google Scholar
• Cury-Boaventura MF, Pompéia C, Curi R. (2004). Comparative toxicity of oleic acid and linoleic acid on Jurkat cells. Clin Nutr, 23, 721–732.
   PubMed Web of Science ®Google Scholar
• del Castillo-Olivares A, Yantiri F, Chueh PJ, Wang S, Sweeting M, Sedlak D, Morré DM, Burgess J, Morré DJ. (1998). A drug-responsive and protease-resistant peripheral NADH oxidase complex from the surface of HeLa S cells. Arch Biochem Biophys, 358, 125–140.
   PubMed Web of Science ®Google Scholar
• Eckhardt SG, Dai A, Davidson KK, Forseth BJ, Wahl GM, Von Hoff DD. (1994). Induction of differentiation in HL60 cells by the reduction of extrachromosomally amplified c-myc. Proc Natl Acad Sci USA, 91, 6674–6678.
   PubMedGoogle Scholar
• Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol, 148, 2207–2216.
   PubMed Web of Science ®Google Scholar
• Gao SY, Wang QJ, Ji YB. (2006). Effect of solanine on the membrane potential of mitochondria in HepG2 cells and [Ca2+]i in the cells. World J Gastroenterol, 12, 3359–3367.
   Google Scholar
• Green DR. (1998). Apoptotic pathways: The roads to ruin. Cell, 94, 695–698.
   PubMed Web of Science ®Google Scholar
• Guo Z, Vangapandu S, Sindelar RW, Walker LA, Sindelar RD. (2005a). Biologically active quassinoids and their chemistry: Potential leads for drug design. Curr Med Chem, 12, 173–190.
   PubMed Web of Science ®Google Scholar
• Guo Z, Vangapandu S, Nimrod A, Walker LA, Sindelar RD. (2005b). Synthesis of A/B-ring partial analogs of bruceantin as potential antimalarial agents. Med Chem, 1, 3–11.
   Google Scholar
• Hartmann A, Speit G. (1997). The contribution of cytotoxicity to DNA-effects in the single cell gel test (comet assay). Toxicol Lett, 90, 183–188.
   PubMed Web of Science ®Google Scholar
• Hempel SL, Buettner GR, O’Malley YQ, Wessels DA, Flaherty DM. (1999). Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: Comparison with 2′,7′-dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2′,7′-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radic Biol Med, 27, 146–159.
   PubMed Web of Science ®Google Scholar
• Holm M, Thomsen M, Høyer M, Hokland P. (1998). Optimization of a flow cytometric method for the simultaneous measurement of cell surface antigen, DNA content, and in vitro BrdUrd incorporation into normal and malignant hematopoietic cells. Cytometry, 32, 28–36.
   Google Scholar
• Hsu CL, Yen GC. (2007). Effects of capsaicin on induction of apoptosis and inhibition of adipogenesis in 3T3-L1 cells. J Agric Food Chem, 55, 1730–1736.
   PubMed Web of Science ®Google Scholar
• Imamura K, Fukamiya N, Okano M, Tagahara K, Lee KH. (1993). Bruceanols D, E, and F three new cytotoxic quassinoids from Brucea antidysenterica. J Nat Prod, 56, 2091–2097.
   PubMed Web of Science ®Google Scholar
• Itokawa H, Ibraheim ZZ, Qiao YF, Takeya K. (1993). Anthraquinones, naphthohydroquinones and naphthohydroquinone dimers from Rubia cordifolia and their cytotoxic activity. Chem Pharm Bull, 41, 1869–1872.
   PubMed Web of Science ®Google Scholar
• Jiang D, Sullivan PG, Sensi SL, Steward O, Weiss JH. (2001). Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J Biol Chem, 276, 47524–47529.
   PubMed Web of Science ®Google Scholar
• Jiang G, Albihn A, Tang T, Tian Z, Henriksson M. (2008). Role of Myc in differentiation and apoptosis in HL60 cells after exposure to arsenic trioxide or all-trans retinoic acid. Leuk Res, 32, 297–307.
   PubMed Web of Science ®Google Scholar
• Jiwajinda S, Santisopasri V, Murakami A, Sugiyama H, Gasquet M, Riad E, Balansard G, Ohigashi H. (2002). In vitro anti-tumor promoting and anti-parasitic activities of the quassinoids from Eurycoma longifolia, a medicinal plant in Southeast Asia. J Ethnopharmacol, 82, 55–58.
   PubMed Web of Science ®Google Scholar
• Kaina B. (2003). DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol, 66, 1547–1554.
   PubMed Web of Science ®Google Scholar
• Karran P, Stephenson C. (1990). Mismatch binding proteins and tolerance to alkylating agents in human cells. Mutat Res, 236, 269–275.
   Google Scholar
• Kerr JF, Winterford CM, Harmon BV. (1994). Apoptosis. Its significance in cancer and cancer therapy. Cancer, 73, 2013–2026.
   PubMed Web of Science ®Google Scholar
• Klaude M, Eriksson S, Nygren J, Ahnström G. (1996). The comet assay: Mechanisms and technical considerations. Mutat Res, 363, 89–96.
   PubMed Web of Science ®Google Scholar
• Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. (1994). Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood, 84, 1415–1420.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Dallaporta B, Resche-Rigon M. (1998). The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol, 60, 619–642.
   PubMed Web of Science ®Google Scholar
• Krysko DV, Vanden Berghe T, D’Herde K, Vandenabeele P. (2008). Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods, 44, 205–221.
   PubMed Web of Science ®Google Scholar
• Kupchan SM, Britton RW, Ziegler MF, Sigel CW. (1973). Bruceantin, a new potent antileukemic simaroubolide from Brucea antidysenterica. J Org Chem, 38, 178–179.
   PubMed Web of Science ®Google Scholar
• Kupchan SM, Lacadie JA, Howie GA, Sickles BR. (1976). Structural requirements for biological activity among antileukemic glaucarubolone ester quassinoids. J Med Chem, 19, 1130–1133.
   Google Scholar
• Lackinger D, Kaina B. (2000). Primary mouse fibroblasts deficient for c-Fos, p53 or for both proteins are hypersensitive to UV light and alkylating agent-induced chromosomal breakage and apoptosis. Mutat Res, 457, 113–123.
   PubMed Web of Science ®Google Scholar
• Lackinger D, Eichhorn U, Kaina B. (2001). Effect of ultraviolet light, methyl methanesulfonate and ionizing radiation on the genotoxic response and apoptosis of mouse fibroblasts lacking c-Fos, p53 or both. Mutagenesis, 16, 233–241.
   PubMed Web of Science ®Google Scholar
• Lau ST, Lin ZX, Liao Y, Zhao M, Cheng CH, Leung PS. (2009). Bruceine D induces apoptosis in pancreatic adenocarcinoma cell line PANC-1 through the activation of p38-mitogen activated protein kinase. Cancer Lett, 281, 42–52.
   Google Scholar
• LeBel CP, Ischiropoulos H, Bondy SC. (1992). Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol, 5, 227–231.
   PubMed Web of Science ®Google Scholar
• Lee KH, Okano M, Hall IH, Brent DA, Soltmann B. (1982). Antitumor agents XLV: Bisbrusatolyl and brusatolyl esters and related compounds as novel potent antileukemic agents. J Pharm Sci, 71, 338–345.
   Google Scholar
• Lemasters JJ. (1999). V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol, 276, G1–G6.
   PubMed Web of Science ®Google Scholar
• Lumonadio L, Atassi G, Vanhaelen M, Vanhaelen-Fastre R. (1991). Antitumor activity of quassinoids from Hannoa klaineana. J Ethnopharmacol, 31, 59–65.
   Google Scholar
• Marcelli M, Cunningham GR, Walkup M, He Z, Sturgis L, Kagan C, Mannucci R, Nicoletti I, Teng B, Denner L. (1999). Signaling pathway activated during apoptosis of the prostate cancer cell line LNCaP: overexpression of caspase-7 as a new gene therapy strategy for prostate cancer. Cancer Res, 59, 382–390.
   PubMed Web of Science ®Google Scholar
• Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med, 182, 1545–1556.
   PubMed Web of Science ®Google Scholar
• Mata-Greenwood E, Daeuble JF, Grieco PA, Dou J, McChesney JD, Mehta RG, Kinghorn AD, Pezzuto JM. (2001). Novel esters of glaucarubolone as inducers of terminal differentiation of promyelocytic HL-60 cells and inhibitors of 7,12-dimethylbenz[a]anthracene-induced preneoplastic lesion formation in mouse mammary organ culture. J Nat Prod, 64, 1509–1513.
   Google Scholar
• Mata-Greenwood E, Cuendet M, Sher D, Gustin D, Stock W, Pezzuto JM. (2002). Brusatol-mediated induction of leukemic cell differentiation and G(1) arrest is associated with down-regulation of c-myc. Leukemia, 16, 2275–2284.
   PubMed Web of Science ®Google Scholar
• Militão GC, Dantas IN, Pessoa C, Falcão MJ, Silveira ER, Lima MA, Curi R, Lima T, Moraes MO, Costa-Lotufo LV. (2006). Induction of apoptosis by pterocarpans from Platymiscium floribundum in HL-60 human leukemia cells. Life Sci, 78, 2409–2417.
   PubMedGoogle Scholar
• Miyamae Y, Yamamoto M, Sasaki YF, Kobayashi H, Igarashi-Soga M, Shimoi K, Hayashi M. (1998). Evaluation of a tissue homogenization technique that isolates nuclei for the in vivo single cell gel electrophoresis (comet) assay: A collaborative study by five laboratories. Mutat Res, 418, 131–140.
   PubMed Web of Science ®Google Scholar
• Morré DJ, Grieco PA, Morré DM. (1998). Mode of action of the anticancer quassinoids–inhibition of the plasma membrane NADH oxidase. Life Sci, 63, 595–604.
   Google Scholar
• Mosmann T. (1983). Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods, 65, 55–63.
   PubMed Web of Science ®Google Scholar
• Murakami C, Fukamiya N, Tamura S, Okano M, Bastow KF, Tokuda H, Mukainaka T, Nishino H, Lee KH. (2004). Multidrug-resistant cancer cell susceptibility to cytotoxic quassinoids, and cancer chemopreventive effects of quassinoids and canthin alkaloids. Bioorg Med Chem, 12, 4963–4968.
   PubMed Web of Science ®Google Scholar
• Nicholson DW. (1999). Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ, 6, 1028–1042.
   PubMed Web of Science ®Google Scholar
• Nicotera P, Leist M, Ferrando-May E. (1999). Apoptosis and necrosis: different execution of the same death. Biochem Soc Symp, 66, 69–73.
   PubMedGoogle Scholar
• Okano M, Fukamiya N, Aratani T, Juichi M, Lee KH. (1985). Antitumor agents, 74. Bruceanol-A and -B, two new antileukemic quassinoids from Brucea antidysenterica. J Nat Prod, 48, 972–975.
   Google Scholar
• Okano M, Fukamiya N, Lee KH. (1990). Biologically active compounds from simaroubaceous plants. In: Atta-ur-Rahman, ed. Studies in Natural Products Chemistry. Amsterdam: Elsevier, 369–404.
   Google Scholar
• Okano M, Fukamiya N, Tagahara K, Cosentino M, Lee T, Morris-Natschke S, Lee KH. (1996). Anti-HIV activity of quassionoids. Bioorg Med Lett, 6, 701–706.
   Web of Science ®Google Scholar
• Pera F, Mattias P, Detzer K. (1977). Methods for determining the proliferation kinetics of cells by means of 5-bromodeoxyuridine. Cell Tissue Kinet, 10, 255–264.
   Google Scholar
• Pérez-Ortiz JM, Tranque P, Burgos M, Vaquero CF, Llopis J. (2007). Glitazones induce astroglioma cell death by releasing reactive oxygen species from mitochondria: Modulation of cytotoxicity by nitric oxide. Mol Pharmacol, 72, 407–417.
   Google Scholar
• Piacentini M, Fesus L, Farrace MG, Ghibelli L, Piredda L, Melino G. (1991). The expression of “tissue” transglutaminase in two human cancer cell lines is related with the programmed cell death (apoptosis). Eur J Cell Biol, 54, 246–254.
   PubMed Web of Science ®Google Scholar
• Polonsky J, Varon Z, Moretti C, Pettit GR, Herald CL, Rideout JA, Saha SB, Khastgir HN. (1980). The antineoplastic quassinoids of Simaba cuspidata spruce and Ailanthus grandis Prain. J Nat Prod, 43, 503–509.
   PubMed Web of Science ®Google Scholar
• Reed JC, Jurgensmeier JM, Matsuyama S. (1998). Bcl-2 family proteins and mitochondria. Biochim Biophys Acta, 1366, 127–137.
   PubMed Web of Science ®Google Scholar
• Roos WP, Kaina B. (2006). DNA damage-induced cell death by apoptosis. Trends Mol Med, 12, 440–450.
   PubMed Web of Science ®Google Scholar
• Rosati A, Quaranta E, Ammirante M, Turco MC, Leone A, De Feo V. (2004). Quassinoids can induce mitochondrial membrane depolarisation and caspase 3 activation in human cells. Cell Death Differ, 11 Suppl 2, S216–S218.
   Google Scholar
• Shimizu T, Pommier Y. (1997). Camptothecin-induced apoptosis in p53-null human leukemia HL60 cells and their isolated nuclei: Effects of the protease inhibitors Z-VAD-fmk and dichloroisocoumarin suggest an involvement of both caspases and serine proteases. Leukemia, 11, 1238–1244.
   Google Scholar
• Silva J, Freitas TRO, Heuser V, Marinho JR, Erdtmann B. (2000). Genotoxicity biomonitoring in coal regions using wild rodent Ctenomys torquatus by comet assay and micronucleus test. Environ Mol Mutagen, 35, 270–278.
   Google Scholar
• Silva EC, Cavalcanti BC, Amorim RC, Lucena JF, Quadros DS, Tadei WP, Montenegro RC, Costa-Lotufo LV, Pessoa C, Moraes MO, Nunomura RC, Nunomura SM, Melo MR, Andrade-Neto VF, Silva LF, Vieira PP, Pohlit AM. (2009). Biological activity of neosergeolide and isobrucein B (and two semi-synthetic derivatives) isolated from the Amazonian medicinal plant Picrolemma sprucei (Simaroubaceae). Mem Inst Oswaldo Cruz, 104, 48–56.
   Google Scholar
• Singh NP, McCoy MT, Tice RR, Schneider EL. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res, 175, 184–191.
   PubMed Web of Science ®Google Scholar
• Smaili SS, Hsu YT, Carvalho AC, Rosenstock TR, Sharpe JC, Youle RJ. (2003). Mitochondria, calcium and pro-apoptotic proteins as mediators in cell death signaling. Braz J Med Biol Res, 36, 183–190.
   Google Scholar
• Strasser A, O’Connor L, Dixit VM. (2000). Apoptosis signaling. Annu Rev Biochem, 69, 217–245.
   PubMed Web of Science ®Google Scholar
• Sultan A, Sokolove PM. (2001). Palmitic acid opens a novel cyclosporin A-insensitive pore in the inner mitochondrial membrane. Arch Biochem Biophys, 386, 37–51.
   PubMed Web of Science ®Google Scholar
• Surrallés J, Xamena N, Creus A, Catalán J, Norppa H, Marcos R. (1995). Induction of micronuclei by five pyrethroid insecticides in whole-blood and isolated human lymphocyte cultures. Mutat Res, 341, 169–184.
   PubMed Web of Science ®Google Scholar
• Thornberry NA, Lazebnik Y. (1998). Caspases: Enemies within. Science, 281, 1312–1316.
   PubMed Web of Science ®Google Scholar
• Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF. (2000). Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen, 35, 206–221.
   PubMed Web of Science ®Google Scholar
• Tischler M, Cardellina JH 2nd, Boyd MR, Cragg GM. (1992). Cytotoxic quassinoids from Cedronia granatensis. J Nat Prod, 55, 667–671.
   Google Scholar
• Van Cruchten S, Van Den Broeck W. (2002). Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol, 31, 214–223.
   PubMed Web of Science ®Google Scholar
• van Loo G, Saelens X, van Gurp M, MacFarlane M, Martin SJ, Vandenabeele P. (2002). The role of mitochondrial factors in apoptosis: A Russian roulette with more than one bullet. Cell Death Differ, 9, 1031–1042.
   PubMed Web of Science ®Google Scholar
• von Bueren AO, Shalaby T, Rajtarova J, Stearns D, Eberhart CG, Helson L, Arcaro A, Grotzer MA. (2007). Anti-proliferative activity of the quassinoid NBT-272 in childhood medulloblastoma cells. BMC Cancer, 7, 19.
   Google Scholar
• Wiseman CL, Yap HY, Bedikian AY, Bodey GP, Blumenschein GR. (1982). Phase II trial of bruceantin in metastatic breast carcinoma. Am J Clin Oncol, 5, 389–391.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Liu J, McMartin KE. (2008). Inhibition of NADPH oxidase activity promotes differentiation of B16 melanoma cells. Oncol Rep, 19, 1225–1230.
   Google Scholar
• Zoratti M, Szabò I. (1995). The mitochondrial permeability transition. Biochim Biophys Acta, 1241, 139–176.
   PubMed Web of Science ®Google Scholar
• Zuco V, Supino R, Righetti SC, Cleris L, Marchesi E, Gambacorti-Passerini C, Formelli F. (2002). Selective cytotoxicity of betulinic acid on tumor cell lines, but not on normal cells. Cancer Lett, 175, 17–25.
   PubMed Web of Science ®Google Scholar