Skip to main content
SpringerLink
Log in

Rare sugar d-allose induces programmed cell death in hormone refractory prostate cancer cells

  • Original Paper
  • Published:
Apoptosis Aims and scope Submit manuscript

An Erratum to this article was published on 06 May 2009

Abstract

Development of effective agents for treatment of hormone-refractory prostate cancer (HRPC) has become a national medical priority. d-Allose is a monosaccharide (C-3 epimer of glucose) distributed rarely in nature; because of its scarcity and cost, the biological effect has hardly been studied. In the present study, we demonstrated the inhibitory action of d-allose on proliferation of human HRPC cell lines, DU145 and PC-3 in a dose- and time-dependent manner, while human normal prostate epithelial (NPE) cell line, PrEC showed no remarkable effect. In vitro treatment of d-allose resulted in the alteration of Bcl-2/Bax ratio in favor of apoptosis (programmed cell death, PCD) in both the HRPC cell lines, which was associated with the lowering of mitochondrial transmembrane potential (Δψm) and the release of cytochrome C (cyt C), the cleavage of caspase 3 and poly (ADP-ribose) polymerase (PARP), and the elevation of calcium concentration in cytosol ([Ca2+]c). d-Allose also induced G1 phase arrest of the cell cycle in DU145 cell line. This study for the first time suggested the antiproliferative effect of d-allose through induction of PCD in HRPC cell lines, which could be due to the modulation of mitochondria mediated intrinsic apoptotic pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Penson DF, Albertsen PC, Nelson PS, Barry M, Stanford JL (2001) Determining cause of death in prostate cancer: are death certificates valid? J Natl Cancer Inst 93:1822–1823. doi:10.1093/jnci/93.23.1822

    Article  PubMed  CAS  Google Scholar 

  2. Albertsen P (2000) When is a death from prostate cancer not a death from prostate cancer? J Natl Cancer Inst 92:590–591. doi:10.1093/jnci/92.8.590

    Article  PubMed  CAS  Google Scholar 

  3. Akakura K, Bruchovsky N, Goldenberg SL (1993) Effects of intermittent androgen suppression on androgen-dependent tumors. Cancer 71:2782–2790. doi :10.1002/1097-0142(19930501)71:9<2782::AID-CNCR2820710916>3.0.CO;2-Z

  4. Eastwood GL (1995) A review of gastrointestinal epithelial renewal and its relevance to the development of adenocarcinomas of the gastrointestinal tract. J Clin Gastroenterol 21(Supp):1–11

    Google Scholar 

  5. Abate-Shen C, Shen MM (2000) Molecular genetics of prostate cancer. Genes Dev 14:2410–2434. doi:10.1101/gad.819500

    Article  PubMed  CAS  Google Scholar 

  6. Arunkumar A, Vijayababu MR, Gunadharini N, Krishnamoorthy G, Arunakaran J (2007) Induction of apoptosis and histone hyperacetylation by diallyl disulfide in prostate cancer cell line PC-3. Cancer Lett 251:59–67. doi:10.1016/j.canlet.2006.11.001

    Article  PubMed  CAS  Google Scholar 

  7. Shen JC, Wang TTY, Chang S, Hursting SD (1999) Mechanistic studies of the effects of the retinoid N-(4-hydroxyphenyl) retinamide on prostate cancer cell growth and apoptosis. Mol Carcinog 24:160–168. doi :10.1002/(SICI)1098-2744(199903)24:3<160::AID-MC2>3.0.CO;2-M

  8. Tang DG, Porter AT (1997) Target to apoptosis: a hopeful weapon for prostate cancer. Prostate 32:284–293. doi :10.1002/(SICI)1097-0045(19970901)32:4<284::AID-PROS9>3.0.CO;2-J

  9. Knudson CM, Korsmeyer SJ (1997) Bcl-2 and bax function independently to regulate cell death. Nat Genet 16:358–363. doi:10.1038/ng0897-358

    Article  PubMed  CAS  Google Scholar 

  10. Chao DT, Korsmeyer SJ (1998) Bcl-2 family: regulators of cell death. Annu Rev Immunol 16:395–419. doi:10.1146/annurev.immunol.16.1.395

    Article  PubMed  CAS  Google Scholar 

  11. Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322–1326. doi:10.1126/science.281.5381.1322

    Article  PubMed  CAS  Google Scholar 

  12. Reed JC (1997) Promise and problems of Bcl-2 antisense therapy. J Natl Cancer Inst 89:988–990. doi:10.1093/jnci/89.14.988

    Article  PubMed  CAS  Google Scholar 

  13. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132–1136. doi:10.1126/science.275.5303.1132

    Article  PubMed  CAS  Google Scholar 

  14. Yang J, Liu X, Bhalla K et al (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132. doi:10.1126/science.275.5303.1129

    Article  PubMed  CAS  Google Scholar 

  15. Harris MH, Thompson CB (2000) The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ 7:1182–1191. doi:10.1038/sj.cdd.4400781

    Article  PubMed  CAS  Google Scholar 

  16. Cao G, Luo Y, Nagayama T et al (2002) Cloning and characterization of rat caspase-9: implications for a role in mediating caspase-3 activation and hippocampal cell death after transient cerebral ischemia. J Cereb Blood Flow Metab 22:534–546. doi:10.1097/00004647-200205000-00005

    Article  PubMed  CAS  Google Scholar 

  17. McConkey DJ, Orrenius S (1997) The role of calcium in the regulation of apoptosis. J Leukoc Biol 59:775–783

    Google Scholar 

  18. Lee T, Malathi K, Kohyama S, Silane M, Berenstein A, Jayaraman T (2004) Intracellular calcium release is required for caspase 3 and 9 activation. Cell Biochem Funct 22:35–40. doi:10.1002/cbf.1050

    Article  Google Scholar 

  19. Agus DB, Cordon-Cardo C, Fox W et al (1999) Prostate cancer cell cycle regulators: response to androgen withdrawal and development of androgen independence. J Natl Cancer Inst 91:1869–1876. doi:10.1093/jnci/91.21.1869

    Article  PubMed  CAS  Google Scholar 

  20. Navarro D, Luzardo OP, Fernandez L, Chesa N, Diaz-Chico BN (2002) Transition to androgen-independence in prostate cancer. J Steroid Biochem Mol Biol 81:191–201. doi:10.1016/S0960-0760(02)00064-X

    Article  PubMed  CAS  Google Scholar 

  21. Doner LW (1979) Isomerization of D-fructose by base: liquid chromatographic evaluation and the isolation of D-psicose. Carbohydr Res 70:209–216. doi:10.1016/S0008-6215(00)87101-3

    Article  CAS  Google Scholar 

  22. Livesey G, Brown JC (1996) D-Tagatose is a bulk sweetener with zero energy determined in rats. J Nutr 126:1601–1609

    PubMed  CAS  Google Scholar 

  23. Izumori K (2002) Bioproduction strategies for rare hexose sugars. Naturwissenschaften 89:120–124. doi:10.1007/s00114-002-0297-z

    Article  PubMed  CAS  Google Scholar 

  24. Arnold EC, Silady PJ (1997) Use of (D)-allose as an immunosuppressive agent. US Patent No. 5620960

  25. Hossain MA, Wakabayashi H, Goda F, Kobayashi S, Maeba T, Maeta H (2000) Effect of the immunosuppressants FK506 and D-allose on allogenic orthotopic liver transplantation in rats. Transplant Proc 32:2021–2023. doi:10.1016/S0041-1345(00)01540-2

    Article  PubMed  CAS  Google Scholar 

  26. Murata A, Sekiya K, Watanabe Y (2003) A novel inhibitory effect of D-allose on production of reactive oxygen species from neutrophils. J Biosci Bioeng 96:89–91

    PubMed  CAS  Google Scholar 

  27. Sui L, Dong Y, Watanabe Y et al (2005) The inhibitory effect and possible mechanisms of D-allose on cancer cell proliferation. Int J Oncol 27:907–912

    PubMed  CAS  Google Scholar 

  28. Stone KR, Mickey DD, Wunderli H, Mickey GH, Paulson DF (1978) Isolation of a human prostate carcinoma cell line (DU-145). Int J Cancer 21:274–281. doi:10.1002/ijc.2910210305

    Article  PubMed  CAS  Google Scholar 

  29. Kaighn ME, Narayan S, Ohnuki Y, Lechner JF, Jones LW (1979) Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 17:16–23

    PubMed  CAS  Google Scholar 

  30. Malgaroli A, Milani D, Meldolesi J, Pozzanr T (1987) Fura-2 measurement of cytosolic free calcium in monolayers and suspensions of various types of animal cells. J Cell Biol 105:2145–2155. doi:10.1083/jcb.105.5.2145

    Article  PubMed  CAS  Google Scholar 

  31. Grynkyewicz G, Poenie M, Tsien RY (1985) A new generation of calcium indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

    Google Scholar 

  32. Ruvolo PP, Deng X, May WS (2001) Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 15:515–522. doi:10.1038/sj.leu.2402197

    Article  PubMed  CAS  Google Scholar 

  33. Nelson WG, Wilding G (2001) Prostate cancer prevention agent development: criteria and pipeline for candidate chemoprevention agents. Urology 57:56–63. doi:10.1016/S0090-4295(00)00942-0

    Article  PubMed  CAS  Google Scholar 

  34. Levi MS, Borne RF, Williamson JS (2001) A review of cancer chemopreventive agents. Curr Med Chem 8:1349–1362

    PubMed  CAS  Google Scholar 

  35. Mickey DD, Stone KR, Wunderli H, Mickey GH, Vollmer RT, Paulson DF (1997) Heterotransplantation of a human prostatic adenocarcinoma cell line in nude mice. Cancer Res 37:4049–4058

    Google Scholar 

  36. Borsellino N, Belldegrun A, Bonavida B (1995) Endogenous interleukin 6 is a resistance factor for cis-diamminedichloroplatinum and etoposide-mediated cytotoxicity of human prostate carcinoma cell lines. Cancer Res 55:4633–4639

    PubMed  CAS  Google Scholar 

  37. Marini M, Zunica G, Franceschi C (1985) Inhibition of cell proliferation by D-ribose and deoxy-D-ribose. Proc Soc Exp Biol Med 180:246–257

    PubMed  CAS  Google Scholar 

  38. Colquhoun A, Alaluf S, Bradley A et al (1997) Novel monosaccharides as potent inhibitors of cell proliferation. Cell Biochem Funct 15:243–249. doi :10.1002/(SICI)1099-0844(199712)15:4<243::AID-CBF747>3.0.CO;2-1

  39. Pucci B, Kasten M, Giordano A (2000) Cell cycle and apoptosis. Neoplasia 2:291–299. doi:10.1038/sj.neo.7900101

    Article  PubMed  CAS  Google Scholar 

  40. Gastman BR (2001) Apoptosis and its clinical impact. Head Neck 23:409–425. doi:10.1002/hed.1052

    Article  PubMed  CAS  Google Scholar 

  41. Gupta S, Afaq F, Mukhtar H (2001) Selective growth-inhibitory, cell-cycle deregulatory and apoptotic response of apigenin in normal versus human prostate carcinoma cells. Biochem Biophys Res Commun 287:914–920. doi:10.1006/bbrc.2001.5672

    Article  PubMed  CAS  Google Scholar 

  42. Yamaguchi F, Takata M, Kamitori K et al (2008) Rare sugar D-allose induces specific up-regulation of TXNIP and subsequent G1 cell cycle arrest in hepatocellular carcinoma cells by stabilization of p27kip1. Int J Oncol 32:377–385

    PubMed  CAS  Google Scholar 

  43. Reed JC (1995) Regulation of apoptosis by bcl-2 family proteins and its role in cancer and chemoresistance. Curr Opin Oncol 7:541–546. doi:10.1097/00001622-199511000-00012

    Article  PubMed  CAS  Google Scholar 

  44. Mackey TJ, Borkowski A, Amin P, Jacob SC, Kyprianou N (1998) Bcl-2/bax ratio as a predictive marker for therapeutic response to radiotherapy in patients with prostate cancer. Urology 52:1085–1090. doi:10.1016/S0090-4295(98)00360-4

    Article  PubMed  CAS  Google Scholar 

  45. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312. doi:10.1126/science.281.5381.1309

    Article  PubMed  CAS  Google Scholar 

  46. Marzo I, Brenner C, Zamzami N et al (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027–2031. doi:10.1126/science.281.5385.2027

    Article  PubMed  CAS  Google Scholar 

  47. Narita M, Shimizu S, Ito T et al (1998) Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 95:14681–14686. doi:10.1073/pnas.95.25.14681

    Article  PubMed  CAS  Google Scholar 

  48. McConkey DJ, Nicotera P, Hartzell P, Bellomo G, Wyllie AH, Orrenius S (1989) Glucocorticoids activate a suicide process in thymocytes through an elevation of cytosolic calcium concentration. Arch Biochem Biophys 269:365–370. doi:10.1016/0003-9861(89)90119-7

    Article  PubMed  CAS  Google Scholar 

  49. Lam M, Dubyak G, Chen L, Nunez G, Miesfeld RL, Distelhorst CW (1994) Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated calcium fluxes. Proc Natl Acad Sci USA 91:6569–6573. doi:10.1073/pnas.91.14.6569

    Article  PubMed  CAS  Google Scholar 

  50. He H, Lam M, McCormick TS, Distelhorst CW (1997) Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J Cell Biol 138:1219–1228. doi:10.1083/jcb.138.6.1219

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by KOSEF grant funded by MEST (No. R01-2008-000-11127-0 and 2008-03133), MRC grant from MEST (No. R13-2007-019-00000-0), MOEST grant from EBNCRC (No. 15-2003-012-01001-0) and Brain Korea 21. N. Naha is receiving Post-Doc Fellowship from Brain Korea 21. The authors sincerely thank Dr. Amitabha Das of Synthetic Biology Laboratory, College of Natural Science and Applied Life Science, Gyeongsang National University, for his idea behind this work. We also thank Dr. Shoraf of Biochemistry laboratory, Medicine Dept., Gyeongsang National University, for technical help during FACS.

Author information

Authors and Affiliations

  1. Division of Life Science, Applied Life Science (Brain Korea 21 and EB-NCRC), Gyeongsang National University, Jinju, 660-701, South Korea

    Nibedita Naha, Hae Young Lee, Mi Ja Jo & Myeong Ok Kim

  2. Bioanalysis and Biotransformation Research Centre, Korea Institute of Science and Technology, Cheongryang, Seoul, South Korea

    Bong Chul Chung

  3. Cancer Preventive Material Development Research Centre (CPMDRC) and Institute College of Oriental Medicine, Kyunghee University, Seoul, 130-701, South Korea

    Sung Hoon Kim

Authors
  1. Nibedita Naha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hae Young Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mi Ja Jo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bong Chul Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sung Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Myeong Ok Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Myeong Ok Kim.

Additional information

Author Contributions: N. Naha: Study design, literature survey, experimental work, data interpretation, manuscript preparation; H. Y. Lee and M. J. Jo: Handling secondary culture; B. C. Chung: donated PrEC cell line; S. H. Kim: Fund collection (MRC); M. O. Kim: Corresponding author, manuscript preparation, fund collection (KOSEF, MOEST, BK21).

An erratum to this article can be found at http://dx.doi.org/10.1007/s10495-009-0336-8

Electronic supplementary material

Below are the links to the electronic supplementary material

(JPG 205 kb)

(JPG 335 kb)

(JPG 334 kb)

(JPG 193 kb)

(JPG 176 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naha, N., Lee, H.Y., Jo, M.J. et al. Rare sugar d-allose induces programmed cell death in hormone refractory prostate cancer cells. Apoptosis 13, 1121–1134 (2008). https://doi.org/10.1007/s10495-008-0232-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-008-0232-7

Keywords

Search

Navigation