Skip to main content
Top
Published in: Journal of Natural Medicines 3-4/2011

01-07-2011 | Original Paper

Ferrearin C induces apoptosis via heme oxygenase-1 (HO-1) induction in neuroblastoma

Authors: Tatsuya Hayama, Keiichi Tabata, Taketo Uchiyama, Yasuo Fujimoto, Takashi Suzuki

Published in: Journal of Natural Medicines | Issue 3-4/2011

Login to get access

Abstract

We investigated the cytotoxicity of six neolignans (16), which are similar in structure to furanocyclohexenone with an angular allyl group, in human neuroblastoma cell lines (IMR-32, LA-N-1, NB-39, SK-N-SH) and normal cells [human umbilical vein endothelial cells (HUVEC) and human dermal fibroblasts (HDF)] using a 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. Two neolignans, ferrearin C (1) and 2, showed significant cytotoxicity in neuroblastoma cells. Typical morphologic features of apoptosis were observed for the ferrearin-type neolignans using Hoechst 33342, and apoptotic cytoplasmic membrane inversion was also induced by ferrearin-type neolignans in IMR-32. Furthermore, a Proteome Profiler Array showed that the ferrearin-type neolignans induced the marked expression of heme oxygenase-1 (HO-1). In a western blot analysis, ferrearin C (1) increased the level of Bax and reduced the level of survivin, indicating the activation of the mitochondrial pathway of apoptosis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3:203–216PubMedCrossRef Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3:203–216PubMedCrossRef
2.
go back to reference Maris JM, Matthay KK (1999) Molecular biology of neuroblastoma. J Clin Oncol 17:2264–2279PubMed Maris JM, Matthay KK (1999) Molecular biology of neuroblastoma. J Clin Oncol 17:2264–2279PubMed
3.
go back to reference Tonini GP, Pistoia V (2006) Molecularly guided therapy of neuroblastoma: a review of different approaches. Curr Pharm Design 12:2303–2317CrossRef Tonini GP, Pistoia V (2006) Molecularly guided therapy of neuroblastoma: a review of different approaches. Curr Pharm Design 12:2303–2317CrossRef
4.
go back to reference Evans AE, D’Angio GJ, Randolph J (1971) A proposed staging for children with neuroblastoma. Cancer 27:374–378PubMedCrossRef Evans AE, D’Angio GJ, Randolph J (1971) A proposed staging for children with neuroblastoma. Cancer 27:374–378PubMedCrossRef
5.
go back to reference Pritchard J, Hickman JA (1994) Why does stage 4s neuroblastoma regress spontaneously? Lancet 344:869–870PubMedCrossRef Pritchard J, Hickman JA (1994) Why does stage 4s neuroblastoma regress spontaneously? Lancet 344:869–870PubMedCrossRef
6.
go back to reference Kitanaka C, Kato K, Ijiri R, Sakurada K, Tomiyama A, Noguchi K, Nagashima Y, Nakagawara A, Momoi T, Toyoda Y, Kigasawa H, Nishi T, Shirouzu M, Yokoyama S, Tanaka Y, Kuchino Y (2002) Increased Ras expression and caspase-independent neuroblastoma cell death: possible mechanism of spontaneous neuroblastoma regression. J Natl Cancer Inst 94:358–368PubMed Kitanaka C, Kato K, Ijiri R, Sakurada K, Tomiyama A, Noguchi K, Nagashima Y, Nakagawara A, Momoi T, Toyoda Y, Kigasawa H, Nishi T, Shirouzu M, Yokoyama S, Tanaka Y, Kuchino Y (2002) Increased Ras expression and caspase-independent neuroblastoma cell death: possible mechanism of spontaneous neuroblastoma regression. J Natl Cancer Inst 94:358–368PubMed
8.
go back to reference Uchiyama T, Tabata K, Nomura S, Kaneko Y, Fujimoto Y, Suzuki T (2009) Induction of apoptosis in human leukemia cell (Jurkat) by neolignans isolated from seeds of L. puchury-major. Biol Pharm Bull 32:1749–1753PubMedCrossRef Uchiyama T, Tabata K, Nomura S, Kaneko Y, Fujimoto Y, Suzuki T (2009) Induction of apoptosis in human leukemia cell (Jurkat) by neolignans isolated from seeds of L. puchury-major. Biol Pharm Bull 32:1749–1753PubMedCrossRef
9.
go back to reference Fujimoto Y, Suzuki Y, Uchiyama T (2003) Patent WO 2003/073870 Fujimoto Y, Suzuki Y, Uchiyama T (2003) Patent WO 2003/073870
10.
go back to reference Carlini EA, de Oliveira AB, de Oliveira GG (1983) Psychopharmacological effects of the essential oil fraction and of the hydrolate obtained from the seeds of L. puchury-major. J Ethnopharmacol 8:225–236PubMedCrossRef Carlini EA, de Oliveira AB, de Oliveira GG (1983) Psychopharmacological effects of the essential oil fraction and of the hydrolate obtained from the seeds of L. puchury-major. J Ethnopharmacol 8:225–236PubMedCrossRef
12.
go back to reference Jozkowicz A, Was H, Dulak J (2007) Heme oxygenase-1 in tumors: is it a false friend? Antioxid Redox Signal 12:2099–2118CrossRef Jozkowicz A, Was H, Dulak J (2007) Heme oxygenase-1 in tumors: is it a false friend? Antioxid Redox Signal 12:2099–2118CrossRef
13.
go back to reference Imai M, Kikuchi H, Denda T, Ohyama K, Hirobe C, Toyoda H (2009) Cytotoxic effects of flavonoids against a human colon cancer derived cell line, COLO 201: a potential natural anti-cancer substance. Cancer Lett 276:74–80PubMedCrossRef Imai M, Kikuchi H, Denda T, Ohyama K, Hirobe C, Toyoda H (2009) Cytotoxic effects of flavonoids against a human colon cancer derived cell line, COLO 201: a potential natural anti-cancer substance. Cancer Lett 276:74–80PubMedCrossRef
14.
go back to reference Lee H-Z, Liu W-Z, Hsieh W-T, Tang F-Y, Chung J-G, Leung HW-C (2009) Oxidative stress involvement in Physalis angulata-induced apoptosis in human oral cancer cells. Food Chem Toxicol 47:561–570PubMedCrossRef Lee H-Z, Liu W-Z, Hsieh W-T, Tang F-Y, Chung J-G, Leung HW-C (2009) Oxidative stress involvement in Physalis angulata-induced apoptosis in human oral cancer cells. Food Chem Toxicol 47:561–570PubMedCrossRef
15.
go back to reference Hill M, Pereira V, Chauveau C, Zagani R, Remy S, Tesson L, Mazal D, Ubillos L, Brion R, Asghar K, Mashreghi MF, Kotsch K, Moffett J, Doebis C, Seifert M, Boczkowski J, Osinaga E, Anegon I (2005) Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J 19:1957–1968PubMedCrossRef Hill M, Pereira V, Chauveau C, Zagani R, Remy S, Tesson L, Mazal D, Ubillos L, Brion R, Asghar K, Mashreghi MF, Kotsch K, Moffett J, Doebis C, Seifert M, Boczkowski J, Osinaga E, Anegon I (2005) Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J 19:1957–1968PubMedCrossRef
16.
go back to reference Song W, Su H, Song S, Paudel HK, Schipper HM (2006) Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J Cell Physiol 206:655–663PubMedCrossRef Song W, Su H, Song S, Paudel HK, Schipper HM (2006) Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J Cell Physiol 206:655–663PubMedCrossRef
17.
go back to reference Chen GG, Liu ZM, Vlantis AC, Tse GMK, Leung BCH, van Hasselt CA (2004) Heme oxygenase-1 protects against apoptosis induced by tumor necrosis factor-α and cycloheximide in papillary thyroid carcinoma cells. J Cell Biochem 92:1246–1256PubMedCrossRef Chen GG, Liu ZM, Vlantis AC, Tse GMK, Leung BCH, van Hasselt CA (2004) Heme oxygenase-1 protects against apoptosis induced by tumor necrosis factor-α and cycloheximide in papillary thyroid carcinoma cells. J Cell Biochem 92:1246–1256PubMedCrossRef
18.
go back to reference Busserolles J, Megías J, Terencio MC, Alcaraz MJ (2006) Heme oxygenase-1 inhibits apoptosis in Caco-2 cells via activation of Akt pathway. Int J Biochem Cell Biol 38:1510–1517PubMedCrossRef Busserolles J, Megías J, Terencio MC, Alcaraz MJ (2006) Heme oxygenase-1 inhibits apoptosis in Caco-2 cells via activation of Akt pathway. Int J Biochem Cell Biol 38:1510–1517PubMedCrossRef
19.
go back to reference Liu ZM, Chen GG, Ng EKW, Leung W-K, Sung JJ-Y, Chung SCS (2004) Upregulation of heme oxygenase-1 and p21 confers resistance to apoptosis in human gastric cancer cells. Oncogene 23:503–513PubMedCrossRef Liu ZM, Chen GG, Ng EKW, Leung W-K, Sung JJ-Y, Chung SCS (2004) Upregulation of heme oxygenase-1 and p21 confers resistance to apoptosis in human gastric cancer cells. Oncogene 23:503–513PubMedCrossRef
20.
go back to reference Mayerhofer M, Florian S, Krauth M-T, Aichberger KJ, Bilban M, Marculescu R, Printz D, Fritsch G, Wagner O, Selzer E, Sperr WR, Valent P, Sillaber C (2004) Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 64:3148–3154PubMedCrossRef Mayerhofer M, Florian S, Krauth M-T, Aichberger KJ, Bilban M, Marculescu R, Printz D, Fritsch G, Wagner O, Selzer E, Sperr WR, Valent P, Sillaber C (2004) Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 64:3148–3154PubMedCrossRef
21.
go back to reference Kim B-J, Ryu S-W, Song B-J (2006) JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 281:21256–21265PubMedCrossRef Kim B-J, Ryu S-W, Song B-J (2006) JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 281:21256–21265PubMedCrossRef
22.
go back to reference Zhang H, Kim JK, Edwards CA, Xu Z, Taichman R, Wang C-Y (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7:909–915PubMedCrossRef Zhang H, Kim JK, Edwards CA, Xu Z, Taichman R, Wang C-Y (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7:909–915PubMedCrossRef
23.
go back to reference Chandele A, Prasad V, Jagtap JC, Shukla R, Shastry PR (2004) Upregulation of survivin in G2/M cells and inhibition of caspase 9 activity enhances resistance in staurosporine-induced apoptosis. Neoplasia 6:29–40PubMed Chandele A, Prasad V, Jagtap JC, Shukla R, Shastry PR (2004) Upregulation of survivin in G2/M cells and inhibition of caspase 9 activity enhances resistance in staurosporine-induced apoptosis. Neoplasia 6:29–40PubMed
24.
go back to reference Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, Hwang JI, Chung CW, Jung YK, Oh BH (2001) An anti-apoptosis protein human survivin is a direct inhibitor of caspase-3 and -7. Biochem 40:1117–1123CrossRef Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, Hwang JI, Chung CW, Jung YK, Oh BH (2001) An anti-apoptosis protein human survivin is a direct inhibitor of caspase-3 and -7. Biochem 40:1117–1123CrossRef
25.
go back to reference Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S (1999) Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO J 18:2040–2048PubMedCrossRef Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S (1999) Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO J 18:2040–2048PubMedCrossRef
26.
go back to reference Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson DW (1999) Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J 18:2049–2056PubMedCrossRef Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson DW (1999) Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J 18:2049–2056PubMedCrossRef
27.
go back to reference Kim HP, Wang X, Nakao A, Kim SI, Murase N, Choi ME, Ryter SW, Choi AMK (2005) Caveolin-1 expression by means of p38β mitogen-activated protein kinase mediates the antiproliferative effect of carbon monoxide. Proc Natl Acad Sci U S A 102:11319–11324PubMedCrossRef Kim HP, Wang X, Nakao A, Kim SI, Murase N, Choi ME, Ryter SW, Choi AMK (2005) Caveolin-1 expression by means of p38β mitogen-activated protein kinase mediates the antiproliferative effect of carbon monoxide. Proc Natl Acad Sci U S A 102:11319–11324PubMedCrossRef
28.
go back to reference Gonzalez-Michaca L, Farrugia G, Croatt AJ, Alam J, Nath KA (2004) Heme: a determinant of life and death in renal tubular epithelial cells. Am J Physiol Renal Physiol 286:F370–F377PubMedCrossRef Gonzalez-Michaca L, Farrugia G, Croatt AJ, Alam J, Nath KA (2004) Heme: a determinant of life and death in renal tubular epithelial cells. Am J Physiol Renal Physiol 286:F370–F377PubMedCrossRef
29.
go back to reference Duckers HJ, Boehm M, True AL, Yet S-F, San H, Park JL, Clinton Webb R, Lee M-E, Nabel GJ, Nabel EG (2001) Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med 7:693–698PubMedCrossRef Duckers HJ, Boehm M, True AL, Yet S-F, San H, Park JL, Clinton Webb R, Lee M-E, Nabel GJ, Nabel EG (2001) Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med 7:693–698PubMedCrossRef
Metadata
Title
Ferrearin C induces apoptosis via heme oxygenase-1 (HO-1) induction in neuroblastoma
Authors
Tatsuya Hayama
Keiichi Tabata
Taketo Uchiyama
Yasuo Fujimoto
Takashi Suzuki
Publication date
01-07-2011
Publisher
Springer Japan
Published in
Journal of Natural Medicines / Issue 3-4/2011
Print ISSN: 1340-3443
Electronic ISSN: 1861-0293
DOI
https://doi.org/10.1007/s11418-011-0514-1

Other articles of this Issue 3-4/2011

Journal of Natural Medicines 3-4/2011 Go to the issue