전체메뉴
검색
Article Search

JMB Journal of Microbiolog and Biotechnology

QR Code QR Code

Research article

References

  1. Avgeropoulos NG, Batchelor TT. 1999. New treatment strategies for malignant gliomas. Oncologist 4: 209-224.
  2. Babilas P, Schreml S, Landthaler M, Szeimies RM. 2010. Photodynamic therapy in dermatology: state of the art. Photodermatol. Photoimmunol. Photomed. 26: 118-132.
    CrossRef
  3. Bui-Xuan NH, Tang PM, Wong CK, Fung KP. 2010. Photoactivated pheophorbide-a, an active component of Scutellaria barbata, enhances apoptosis via the suppression of ERKmediated autophagy in the estrogen receptor-negative human breast adenocarcinoma cells MDA-MB-231. J. Ethnopharmacol. 131: 95-103.
    CrossRef
  4. Busch TM, Cengel KA, Finlay JC. 2009. Pheophorbide a as a photosensitizer in photodynamic therapy: in vivo considerations. Cancer Biol. Ther. 8: 540-542.
    CrossRef
  5. Cieckiewicz E, Angenot L, Gras T, Kiss R, Frederich M. 2012. Potential anticancer activity of young Carpinus betulus leaves. Phytomedicine 19: 278-283.
    CrossRef
  6. Chan JY, Tang PM, Hon P, Au SW, Tsui SK, Waye MM, et al. 2006. Pheophorbide a, a major antitumor component purified from Scutellaria barbata, induces apoptosis in human hepatocellular carcinoma cells. Planta Med. 72: 28-33.
    CrossRef
  7. Chen K, Preub A, Hackbarth S, Wacker M, Langer K, Roder B. 2009. Novel photosensitizer-protein nanoparticles for photodynamic therapy: photophysical characterization and in vitro investigations. J. Photochem. Photobiol. B Biol. 96: 6674.
  8. Cheng HH, Wang HK, Ito J, Bastow KF, Tachibana Y, Nakanishi Y, et al. 2001. Cytotoxic pheophorbide-related compounds from Clerodendrum calamitosum and C. cyrtophyllum. J. Nat. Prod. 64: 915-919.
    CrossRef
  9. Cho ML, Lee HS, Kang IJ, Won MH, You SG. 2011. Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem. 127: 999-1006.
    CrossRef
  10. Compos A, Souza CB, Lhullier C, Falkenberg M, Schenkel EP, Ribeiro-do-Valle RM, Siqueira JM. 2012. Anti-tumour effects of elatol, a marine derivative compound obtained from red algae Laurencia microcladia. J. Pharm. Pharmacol. 64:1146-1154.
    CrossRef
  11. Cui Y, Wang Q, Wang JY, Dong Y, Luo C, Hu G, Lu Y. 2012. Knowkdown of AKT2 expression by RNA interference inhibits proliferation, enhances apoptosis, and increases chemosensitivity to the anticancer drug VM-26 in U87 glioma cells. Brain Res. 1469: 1-9.
    CrossRef
  12. Derradji H, Baatout S. 2003. Apoptosis: a mechanism of cell suicide. In Vivo 17: 185-192.
  13. Hajri A, Wack S, Meyer C, Smith MK, Leberquier C, Kedinger M. 2002. In vitro and in vivo efficacy of photofrin and pheophorbide a, a bacteriochlorin, in photodynamic therapy of colonic cancer cells. Photochem. Photobiol. 75: 140148.
    CrossRef
  14. Harada H, Kamei Y. 1997. Selective cytotoxicity of marine algae extracts to several human leukemic cell lines. Cytotechnology 25: 213-219.
    CrossRef
  15. Hoi SW, Wong HM, Chan JY, Yue GG, Tse GM, Law BK, et al. 2012. Photodynamic therapy of pheophorbide a inhibits the proliferation of human breast tumour via both caspasedependent and -independent apoptotic pathways in vitro and in vivo models. Phytother. Res. 26: 734-742.
    CrossRef
  16. Hyun KH, Yoon CH, Kim RK, Lim EJ, An S, Park MJ, et al. 2011. Eckol suppresses maintenance of stemness and malignancies in glioma stem-like cells. Toxicol. Appl. Pharm. 254: 32-40.
    CrossRef
  17. Islam MN, Ishita IJ, Jin SE, Choi RJ, Lee CM, Kim YS, et al. 2013. Anti-inflammatory activity of edible brown alga Saccharina japonica and its constituents pheophorbide a and pheophytin in LPS-stimulated Raw 264.7 macrophage cells. Food Chem. Toxicol. 55: 541-548.
    CrossRef
  18. Jaffe EA, Nacheman RL, Becker CG, Minick CR. 1973. Culture of human endothelial cells derived from umbilical veins; identification by morphologic and immunologic criteria. J. Clin. Invest. 52: 2745-2756.
    CrossRef
  19. Kato H. 1998. Photodynamic therapy for lung cancer, a review of 19 years’ experience. J. Photochem. Photobiol. B Biol. 42: 96-99.
  20. Kim KN, Ahn G, Heo SJ, Kang SM, Kang MC, Yang HM, et al. 2013. Inhibition of tumor growth in vitro and in vivo by fucoxanthin against melanoma B16F10 cells. Environ. Toxicol. Pharmacol. 35: 39-46.
    CrossRef
  21. Kim KY, Nam KA, Kurihara H, Kim SM. 2008. Potent αglucosidase inhibitors purified from the red alga Greteloupia elliptica. Phytochemistry 69: 2820-2825.
    CrossRef
  22. Lefranc F, Facchini V, Kiss R. 2007. Proautophagic drugs: a novel means to combat apoptosis-resistant cancers, with a special emphasis on glioblastomas. Oncologist 12: 1395-1403.
    CrossRef
  23. Maeda H. 2001. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumorselective macromolecular drug targeting. Adv. Enzyme Regul. 41: 189-207.
    CrossRef
  24. Mang TS. 2004. Laser and light sources for PDT: past, present and future. Photodiagn. Photodyn. Ther. 1: 43-48.
    CrossRef
  25. Nakamura Y, Murakami A, Koshimizu K, Ohigashi H. 1996. Identification of pheophorbide a and its related compounds as possible anti-tumor promoters in the leaves of Neptunia oleracea. Biosci. Biotechnol. Biochem. 60: 1028-1030.
    CrossRef
  26. Nathan TR, Whitelaw DE, Chang SC, Lees WR, Ripley PM, Payne H, et al. 2002. Photodynamic therapy for prostate cancer recurrence after radiotherapy: a phase I study. J. Urol. 168: 1427-1432.
    CrossRef
  27. Park KK, Surh YJ. 1996. Chemopreventive activity of chlorophyllin against mouse skin carcinogenesis by benzo[α]pyrene and benze[α]pyrene-7,8-dihydrodiol-9,10-epoxide. Cancer Lett. 102:143-149.
    CrossRef
  28. Rocha ABD, Lopes RM, Schwartsmann G. 2001. Natural products in anticancer therapy. Curr. Opin. Pharmacol. 1:364-369.
    CrossRef
  29. Sathornsumetee S, Reardon DA, Desjardins A, Quinn JA, Vredenburgh JJ, Rich JN. 2007. Molecularly targeted therapy for malignant glioma. Cancer 110: 13-24.
    CrossRef
  30. Schwartsmann G. 2000. Marine organisms and other novel natural source of new anticancer agents. Ann. Oncol. 11:235-243.
    CrossRef
  31. Shrestha-Bhattarai T, Rangnekar VM. 2010. Cancer-selective apoptotic effects of extracellular and intracellular Par-4. Oncogene 29: 3873-3880.
    CrossRef
  32. Tang PM, Bui-Xuan NH, Wong CK, Fong WP, Fung KP. 2010. Pheophorbide a-mediated photodynamic therapy triggers HLA class I-restricted antigen presentation in human hepatocellular carcinoma. Transl. Oncol. 3: 114-122.
  33. Tang PM, Liu XZ, Zhang DM, Fong WP, Fung KP. 2009. Pheophorbide a based photodynamic therapy induces apoptosis via mitochondrial-mediated pathway in human uterine carcinosarcoma. Cancer Biol. Ther. 8: 533-539.
    CrossRef
  34. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY. 2010. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J. Clin. 60:166-193.
    CrossRef
  35. Vianna DR, Hamerski L, Figueire F, Bernardi A, Visentin LC, Pires ENS, et al. 2012. Selective cytotoxicity and apoptosis induction in glioma cell lines by 5-oxygenated6,7-methylenedioxycoumarins from Pterocaulon species. Eur. J. Med. Chem. 57: 268-274.
    CrossRef
  36. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, et al. 2010. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468: 829-833.
    CrossRef
  37. Wolfsen HC, Hemminger LL. 2006. Salvage photodynamic therapy by using porfimer sodium after chemoradiation therapy: a Western viewpoint. Gastrointest. Endosc. 63: 195-196.
    CrossRef

Related articles in JMB

More Related Articles

Article

Research article

J. Microbiol. Biotechnol. 2014; 24(3): 346-353

Published online March 28, 2014 https://doi.org/10.4014/jmb.1308.08090

Copyright © The Korean Society for Microbiology and Biotechnology.

Glioblastoma-Specific Anticancer Activity of Pheophorbide a from the Edible Red Seaweed Grateloupia elliptica

MyoungLae Cho 1, Gab-Man Park 2, Su-Nam Kim 3, Touseef Amna 4, Seokjoon Lee 5 and Woon-Seob Shin 4*

1East Sea Research Institute, Korea Institute of Ocean Science and Technology, Gyeongbuk, 767-813, Republic of Korea, 2Department of Parasitology, Kwandong University College of Medicine, Gangneung 210-701, Republic of Korea, 3KIST Gangneung Institute, Gangneung 210-340, Republic of Korea, 4Department of Microbiology, Kwandong University College of Medicine, 210-701, Republic of Korea, 4Department of Pharmacology, Kwandong University, College of Medicine, 210-701, Republic of Korea

Received: August 30, 2013; Accepted: November 28, 2013

Abstract

The chlorophyll-related compound pheophorbide a (Pa) was successively purified from an
edible red seaweed, Grateloupia elliptica, using silica, octadecyl silica column chromatography
and reversed phase-high-performance liquid chromatography, as well as the cell cycle
inhibitory and apoptotic effects of Pa being investigated in U87MG glioblastoma cells. The Pa
exhibited strong anticancer effects in the absence of direct photo-irradiation against various
cancer cell lines, including U87MG, SK-OV-3, and HeLa cells. Among the cancer cells, the
strongest anticancer activity of Pa exhibited on U87MG cells with IC50 values of 2.8 μg/ml. In
addition, Pa specifically had cytostatic activity on glioblastoma cells rather than human
umbilical vein endothelial cells. Analysis of the cell cycle distribution showed that Pa induced
G0/G1 arrest of U87 MG cells. In addition, arrested cells induced late apoptosis and DNA
degradation under dark condition. These results suggest that Pa isolated from G. elliptica is a
potential glioblastoma-specific anticancer agent without side effects on normal cells.

Keywords: glioblastoma, selective toxicity, pheophorbide a, anticancer, Grateloupia elliptica, cytostatic

References

  1. Avgeropoulos NG, Batchelor TT. 1999. New treatment strategies for malignant gliomas. Oncologist 4: 209-224.
  2. Babilas P, Schreml S, Landthaler M, Szeimies RM. 2010. Photodynamic therapy in dermatology: state of the art. Photodermatol. Photoimmunol. Photomed. 26: 118-132.
    CrossRef
  3. Bui-Xuan NH, Tang PM, Wong CK, Fung KP. 2010. Photoactivated pheophorbide-a, an active component of Scutellaria barbata, enhances apoptosis via the suppression of ERKmediated autophagy in the estrogen receptor-negative human breast adenocarcinoma cells MDA-MB-231. J. Ethnopharmacol. 131: 95-103.
    CrossRef
  4. Busch TM, Cengel KA, Finlay JC. 2009. Pheophorbide a as a photosensitizer in photodynamic therapy: in vivo considerations. Cancer Biol. Ther. 8: 540-542.
    CrossRef
  5. Cieckiewicz E, Angenot L, Gras T, Kiss R, Frederich M. 2012. Potential anticancer activity of young Carpinus betulus leaves. Phytomedicine 19: 278-283.
    CrossRef
  6. Chan JY, Tang PM, Hon P, Au SW, Tsui SK, Waye MM, et al. 2006. Pheophorbide a, a major antitumor component purified from Scutellaria barbata, induces apoptosis in human hepatocellular carcinoma cells. Planta Med. 72: 28-33.
    CrossRef
  7. Chen K, Preub A, Hackbarth S, Wacker M, Langer K, Roder B. 2009. Novel photosensitizer-protein nanoparticles for photodynamic therapy: photophysical characterization and in vitro investigations. J. Photochem. Photobiol. B Biol. 96: 6674.
  8. Cheng HH, Wang HK, Ito J, Bastow KF, Tachibana Y, Nakanishi Y, et al. 2001. Cytotoxic pheophorbide-related compounds from Clerodendrum calamitosum and C. cyrtophyllum. J. Nat. Prod. 64: 915-919.
    CrossRef
  9. Cho ML, Lee HS, Kang IJ, Won MH, You SG. 2011. Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem. 127: 999-1006.
    CrossRef
  10. Compos A, Souza CB, Lhullier C, Falkenberg M, Schenkel EP, Ribeiro-do-Valle RM, Siqueira JM. 2012. Anti-tumour effects of elatol, a marine derivative compound obtained from red algae Laurencia microcladia. J. Pharm. Pharmacol. 64:1146-1154.
    CrossRef
  11. Cui Y, Wang Q, Wang JY, Dong Y, Luo C, Hu G, Lu Y. 2012. Knowkdown of AKT2 expression by RNA interference inhibits proliferation, enhances apoptosis, and increases chemosensitivity to the anticancer drug VM-26 in U87 glioma cells. Brain Res. 1469: 1-9.
    CrossRef
  12. Derradji H, Baatout S. 2003. Apoptosis: a mechanism of cell suicide. In Vivo 17: 185-192.
  13. Hajri A, Wack S, Meyer C, Smith MK, Leberquier C, Kedinger M. 2002. In vitro and in vivo efficacy of photofrin and pheophorbide a, a bacteriochlorin, in photodynamic therapy of colonic cancer cells. Photochem. Photobiol. 75: 140148.
    CrossRef
  14. Harada H, Kamei Y. 1997. Selective cytotoxicity of marine algae extracts to several human leukemic cell lines. Cytotechnology 25: 213-219.
    CrossRef
  15. Hoi SW, Wong HM, Chan JY, Yue GG, Tse GM, Law BK, et al. 2012. Photodynamic therapy of pheophorbide a inhibits the proliferation of human breast tumour via both caspasedependent and -independent apoptotic pathways in vitro and in vivo models. Phytother. Res. 26: 734-742.
    CrossRef
  16. Hyun KH, Yoon CH, Kim RK, Lim EJ, An S, Park MJ, et al. 2011. Eckol suppresses maintenance of stemness and malignancies in glioma stem-like cells. Toxicol. Appl. Pharm. 254: 32-40.
    CrossRef
  17. Islam MN, Ishita IJ, Jin SE, Choi RJ, Lee CM, Kim YS, et al. 2013. Anti-inflammatory activity of edible brown alga Saccharina japonica and its constituents pheophorbide a and pheophytin in LPS-stimulated Raw 264.7 macrophage cells. Food Chem. Toxicol. 55: 541-548.
    CrossRef
  18. Jaffe EA, Nacheman RL, Becker CG, Minick CR. 1973. Culture of human endothelial cells derived from umbilical veins; identification by morphologic and immunologic criteria. J. Clin. Invest. 52: 2745-2756.
    CrossRef
  19. Kato H. 1998. Photodynamic therapy for lung cancer, a review of 19 years’ experience. J. Photochem. Photobiol. B Biol. 42: 96-99.
  20. Kim KN, Ahn G, Heo SJ, Kang SM, Kang MC, Yang HM, et al. 2013. Inhibition of tumor growth in vitro and in vivo by fucoxanthin against melanoma B16F10 cells. Environ. Toxicol. Pharmacol. 35: 39-46.
    CrossRef
  21. Kim KY, Nam KA, Kurihara H, Kim SM. 2008. Potent αglucosidase inhibitors purified from the red alga Greteloupia elliptica. Phytochemistry 69: 2820-2825.
    CrossRef
  22. Lefranc F, Facchini V, Kiss R. 2007. Proautophagic drugs: a novel means to combat apoptosis-resistant cancers, with a special emphasis on glioblastomas. Oncologist 12: 1395-1403.
    CrossRef
  23. Maeda H. 2001. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumorselective macromolecular drug targeting. Adv. Enzyme Regul. 41: 189-207.
    CrossRef
  24. Mang TS. 2004. Laser and light sources for PDT: past, present and future. Photodiagn. Photodyn. Ther. 1: 43-48.
    CrossRef
  25. Nakamura Y, Murakami A, Koshimizu K, Ohigashi H. 1996. Identification of pheophorbide a and its related compounds as possible anti-tumor promoters in the leaves of Neptunia oleracea. Biosci. Biotechnol. Biochem. 60: 1028-1030.
    CrossRef
  26. Nathan TR, Whitelaw DE, Chang SC, Lees WR, Ripley PM, Payne H, et al. 2002. Photodynamic therapy for prostate cancer recurrence after radiotherapy: a phase I study. J. Urol. 168: 1427-1432.
    CrossRef
  27. Park KK, Surh YJ. 1996. Chemopreventive activity of chlorophyllin against mouse skin carcinogenesis by benzo[α]pyrene and benze[α]pyrene-7,8-dihydrodiol-9,10-epoxide. Cancer Lett. 102:143-149.
    CrossRef
  28. Rocha ABD, Lopes RM, Schwartsmann G. 2001. Natural products in anticancer therapy. Curr. Opin. Pharmacol. 1:364-369.
    CrossRef
  29. Sathornsumetee S, Reardon DA, Desjardins A, Quinn JA, Vredenburgh JJ, Rich JN. 2007. Molecularly targeted therapy for malignant glioma. Cancer 110: 13-24.
    CrossRef
  30. Schwartsmann G. 2000. Marine organisms and other novel natural source of new anticancer agents. Ann. Oncol. 11:235-243.
    CrossRef
  31. Shrestha-Bhattarai T, Rangnekar VM. 2010. Cancer-selective apoptotic effects of extracellular and intracellular Par-4. Oncogene 29: 3873-3880.
    CrossRef
  32. Tang PM, Bui-Xuan NH, Wong CK, Fong WP, Fung KP. 2010. Pheophorbide a-mediated photodynamic therapy triggers HLA class I-restricted antigen presentation in human hepatocellular carcinoma. Transl. Oncol. 3: 114-122.
  33. Tang PM, Liu XZ, Zhang DM, Fong WP, Fung KP. 2009. Pheophorbide a based photodynamic therapy induces apoptosis via mitochondrial-mediated pathway in human uterine carcinosarcoma. Cancer Biol. Ther. 8: 533-539.
    CrossRef
  34. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY. 2010. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J. Clin. 60:166-193.
    CrossRef
  35. Vianna DR, Hamerski L, Figueire F, Bernardi A, Visentin LC, Pires ENS, et al. 2012. Selective cytotoxicity and apoptosis induction in glioma cell lines by 5-oxygenated6,7-methylenedioxycoumarins from Pterocaulon species. Eur. J. Med. Chem. 57: 268-274.
    CrossRef
  36. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, et al. 2010. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468: 829-833.
    CrossRef
  37. Wolfsen HC, Hemminger LL. 2006. Salvage photodynamic therapy by using porfimer sodium after chemoradiation therapy: a Western viewpoint. Gastrointest. Endosc. 63: 195-196.
    CrossRef