Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Autophagy-associated Targeting Pathways of Natural Products during Cancer Treatment

  • Zhang, Shu-Fang (Graduate School, Wuhan Sports University) ;
  • Wang, Xiao-Lu (College of Sports Science and Technology, Wuhan Sports University) ;
  • Yang, Xiao-Qi (Graduate School, Wuhan Sports University) ;
  • Chen, Ning (College of Health Science, Hubei Provincial Collaborative Innovation Center for Exercise, Intervention and Health Promotion, Wuhan Sports University)
  • Published : 2015.01.22
Download PDF
⟨ Previous Next ⟩

Abstract

It is well known that conventional chemotherapy and radiation therapy can result in toxicity to both normal cells and tumor cells, which causes limitations in the application of these therapeutic strategies for cancer control. Novel and effective therapeutic strategies for cancers with no or low toxicity for normal cells are a high priority. Therefore, natural products with anticancer activity have gained more and more attention due to their favorable safety and efficacy profiles. Pre-clinical and clinical studies have demonstrated that several representative natural compounds such as resveratrol, epigallocatechin-3-gallate, curcumin, allicin and ginsenosides have obvious anticancer potential. In this article, we summarize autophagy-associated targeting pathways of such natural products for inducing the death of cancer cells, and discuss the core autophagic pathways involved in cancer treatments. Recent advances in the discovery, evaluation and exploitation of natural compounds as therapeutic agents for cancers will provide references and support in pre-clinical and clinical application of novel natural drugs for the treatment of primary and metastatic tumors in the future.

Keywords

References

  1. Aggarwal BB, Shishodia S, Takada Y, et al (2005). Curcumin suppresses the paclitaxel-induced nuclear factor-kappaB pathway in breast cancer cells and inhibits lung metastasis of human breast cancer in nude mice. Clin Cancer Res, 11, 7490-8. https://doi.org/10.1158/1078-0432.CCR-05-1192
  2. Ahmad N, Feyes DK, Nieminen AL, et al (1997). Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. J Natl Cancer Inst, 89, 1881-6. https://doi.org/10.1093/jnci/89.24.1881
  3. Ajabnoor GM, Crook T, Coley HM (2012). Paclitaxel resistance is associated with switch from apoptotic to autophagic cell death in MCF-7 breast cancer cells. Cell Death Dis, 3, 260. https://doi.org/10.1038/cddis.2011.139
  4. Alkhalaf M (2007). Resveratrol-induced apoptosis is associated with activation of p53 and inhibition of protein translation in T47D human breast cancer cells. Pharmacol, 80, 134-43. https://doi.org/10.1159/000103253
  5. Altonsy MO, Andrews SC (2011). Diallyl disulphide, a beneficial component of garlic oil, causes a redistribution of cell-cycle growth phases, induces apoptosis, and enhances butyrate-induced apoptosis in colorectal adenocarcinoma cells (HT-29). Nutr Cancer, 63, 1104-13. https://doi.org/10.1080/01635581.2011.601846
  6. Amagase H (2006). Clarifying the real bioactive constituents of garlic. J Nutr, 136, 716-25.
  7. Aoki H, Takada Y, Kondo S, et al (2007). Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol, 72, 29-39. https://doi.org/10.1124/mol.106.033167
  8. Aras A, Khokhar AR, Qureshi MZ, et al (2014). Targeting cancer with nano-bullets: curcumin, EGCG, resveratrol and quercetin on flying carpets. Asian Pac J Cancer Prev, 15, 3865-71. https://doi.org/10.7314/APJCP.2014.15.9.3865
  9. Aziz MH, Kumar R, Ahmad N (2003). Cancer chemoprevention by resveratrol: in vitro and in vivo studies and the underlying mechanisms (review). Int J Oncol, 23, 17-28.
  10. Baena R, Salinas P (2014). Diet and cancer: risk factors and epidemiological evidence. Maturitas, 77, 202-8. https://doi.org/10.1016/j.maturitas.2013.11.010
  11. Balunas MJ, Kinghorn AD (2005). Drug discovery from medicinal plants. Life Sci, 78, 431-41. https://doi.org/10.1016/j.lfs.2005.09.012
  12. Banjerdpongchai R, Khaw-On P (2013). Terpinen-4-ol induces autophagic and apoptotic cell death in human leukemic HL-60 cells. Asian Pac J Cancer Prev, 14, 7537-42. https://doi.org/10.7314/APJCP.2013.14.12.7537
  13. Bansal SS, Goel M, Aqil F, et al (2011). Advanced drug delivery systems of curcumin for cancer chemoprevention. Cancer Prev Res (Phila), 4, 1158-71. https://doi.org/10.1158/1940-6207.CAPR-10-0006
  14. Bertelli AA, Das DK (2009). Grapes, wines, resveratrol, and heart health. J Cardiovasc Pharmacol, 54, 468-76. https://doi.org/10.1097/FJC.0b013e3181bfaff3
  15. Boya P, Gonzalez-Polo RA, Casares N, et al (2005). Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol, 25, 1025-40. https://doi.org/10.1128/MCB.25.3.1025-1040.2005
  16. Chen N, Karantza-Wadsworth V (2009). Role and regulation of autophagy in cancer. Biochim Biophys Acta, 1793, 1516-23. https://doi.org/10.1016/j.bbamcr.2008.12.013
  17. Chen N, Karantza V (2011). Autophagy as a therapeutic target in cancer. Cancer Biol Ther, 11, 157-68. https://doi.org/10.4161/cbt.11.2.14622
  18. Cheng Y, Qiu F, Huang J, et al (2008). Apoptosis-suppressing and autophagy-promoting effects of calpain on oridonin-induced L929 cell death. Arch Biochem Biophys, 475, 148-55. https://doi.org/10.1016/j.abb.2008.04.027
  19. Chu YL, Ho CT, Chung JG, et al (2012). Allicin induces p53-mediated autophagy in Hep G2 human liver cancer cells. J Agric Food Chem, 60, 8363-71. https://doi.org/10.1021/jf301298y
  20. Clarke PG (1990). Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl), 181, 195-213.
  21. Clement MV, Hirpara JL, Chawdhury SH, et al (1998). Chemopreventive agent resveratrol, a natural product derived from grapes, triggers CD95 signaling-dependent apoptosis in human tumor cells. Blood, 92, 996-1002.
  22. Cui Q, Tashiro S, Onodera S, et al (2006). Augmentation of oridonin-induced apoptosis observed with reduced autophagy. J Pharmacol Sci, 101, 230-9. https://doi.org/10.1254/jphs.FPJ06003X
  23. Degenhardt K, Mathew R, Beaudoin B, et al (2006). Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell, 10, 51-64. https://doi.org/10.1016/j.ccr.2006.06.001
  24. Eccles DM, Cranston G, Steel CM, et al (1990). Allele losses on chromosome 17 in human epithelial ovarian carcinoma. Oncogene, 5, 1599-601.
  25. Futreal PA, Soderkvist P, Marks JR, et al (1992). Detection of frequent allelic loss on proximal chromosome 17q in sporadic breast carcinoma using microsatellite length polymorphisms. Cancer Res, 52, 2624-7.
  26. Gao SM, Yang JJ, Chen CQ, et al (2012). Pure curcumin decreases the expression of WT1 by upregulation of miR-15a and miR-16-1 in leukemic cells. J Exp Clin Cancer Res, 31, 27. https://doi.org/10.1186/1756-9966-31-27
  27. Gao X, Zacharek A, Salkowski A, et al (1995). Loss of heterozygosity of the BRCA1 and other loci on chromosome 17q in human prostate cancer. Cancer Res, 55, 1002-5.
  28. Gossner G, Choi M, Tan L, et al (2007). Genistein-induced apoptosis and autophagocytosis in ovarian cancer cells. Gynecol Oncol, 105, 23-30. https://doi.org/10.1016/j.ygyno.2006.11.009
  29. Jang M, Cai L, Udeani GO, et al (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science, 275, 218-20. https://doi.org/10.1126/science.275.5297.218
  30. Jia YL, Li J, Qin ZH, et al (2009). Autophagic and apoptotic mechanisms of curcumin-induced death in K562 cells. J Asian Nat Prod Res, 11, 918-28. https://doi.org/10.1080/10286020903264077
  31. Juhasz G, Hill JH, Yan Y, et al (2008). The class III PI (3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol, 181, 655-66. https://doi.org/10.1083/jcb.200712051
  32. Kallifatidis G, Hoepfner D, Jaeg T, et al (2013). The marine natural product manzamine A targets vacuolar ATPases and inhibits autophagy in pancreatic cancer cells. Mar Drugs, 11, 3500-16. https://doi.org/10.3390/md11093500
  33. Kang HJ, Lee SH, Price JE, et al (2009). Curcumin suppresses the paclitaxel-induced nuclear factor-kappaB in breast cancer cells and potentiates the growth inhibitory effect of paclitaxel in a breast cancer nude mice model. Breast J, 15, 223-9. https://doi.org/10.1111/j.1524-4741.2009.00709.x
  34. Kim J, Park EJ (2002). Cytotoxic anticancer candidates from natural resources. Curr Med Chem Anticancer Agents, 2, 485-537. https://doi.org/10.2174/1568011023353949
  35. Kim SM, Lee SY, Cho JS, et al (2010). Combination of ginsenoside Rg3 with docetaxel enhances the susceptibility of prostate cancer cells via inhibition of NF-kappaB. Eur J Pharmacol, 631, 1-9. https://doi.org/10.1016/j.ejphar.2009.12.018
  36. Kinghorn AD, Chin YW, Swanson SM (2009). Discovery of natural product anticancer agents from biodiverse organisms. Curr Opin Drug Discov Devel, 12, 189-96.
  37. Kiraly-Veghely Z, Tyihak E, Albert L, et al (1998). Identification and measurement of resveratrol and formaldehyde in parts of white and blue grape berries. Acta Biol Hung, 49, 281-9.
  38. Klinge CM, Risinger KE, Watts MB, et al (2003). Estrogenic activity in white and red wine extracts. J Agric Food Chem, 51, 1850-7. https://doi.org/10.1021/jf0259821
  39. Kma L (2013). Roles of plant extracts and constituents in cervical cancer therapy. Asian Pac J Cancer Prev, 14, 3429-36. https://doi.org/10.7314/APJCP.2013.14.6.3429
  40. Lachumy SJ, Oon CE, Deivanai S, et al (2013). Herbal remedies for combating irradiation: a green anti-irradiation approach. Asian Pac J Cancer Prev, 14, 5553-65. https://doi.org/10.7314/APJCP.2013.14.10.5553
  41. Lao F, Shang Y, Liu D (2009). Autophagy pathway of raji cell death induced by resveratrol. Chinese J Biologicals, 22, 654-8.
  42. Lao Y, Wan G, Liu Z, et al (2014). The natural compound oblongifolin C inhibits autophagic flux and enhances antitumor efficacy of nutrient deprivation. Autophagy, 10, 736-49. https://doi.org/10.4161/auto.28034
  43. Larocque K, Ovadje P, Djurdjevic S, et al (2014). Novel analogue of colchicine induces selective pro-death autophagy and necrosis in human cancer cells. PLoS One, 9, 87064. https://doi.org/10.1371/journal.pone.0087064
  44. Lee YJ, Kim NY, Suh YA, et al (2011). Involvement of ROS in curcumin-induced autophagic cell death. Korean J Physiol Pharmacol, 15, 1-7. https://doi.org/10.4196/kjpp.2011.15.1.1
  45. Levine B, Kroemer G (2008). Autophagy in the pathogenesis of disease. Cell, 132, 27-42. https://doi.org/10.1016/j.cell.2007.12.018
  46. Liang XH, Jackson S, Seaman M, et al (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature, 402, 672-6. https://doi.org/10.1038/45257
  47. Lum JJ, DeBerardinis RJ, Thompson CB (2005). Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol, 6, 439-48. https://doi.org/10.1038/nrm1660
  48. Mai TT, Moon J, Song Y, et al (2012). Ginsenoside F2 induces apoptosis accompanied by protective autophagy in breast cancer stem cells. Cancer Lett, 321, 144-53. https://doi.org/10.1016/j.canlet.2012.01.045
  49. Mathew R, Karp CM, Beaudoin B, et al (2009). Autophagy suppresses tumorigenesis through elimination of p62. Cell, 137, 1062-75. https://doi.org/10.1016/j.cell.2009.03.048
  50. Meiyanto E, Hermawan A, Anindyajati (2012). Natural products for cancer-targeted therapy: citrus flavonoids as potent chemopreventive agents. Asian Pac J Cancer Prev, 13, 427-36. https://doi.org/10.7314/APJCP.2012.13.2.427
  51. Mizushima N (2010). The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol, 22, 132-9. https://doi.org/10.1016/j.ceb.2009.12.004
  52. Mizushima N, Yoshimori T, Ohsumi Y (2011). The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol, 27, 107-32. https://doi.org/10.1146/annurev-cellbio-092910-154005
  53. Odot J, Albert P, Carlier A, et al (2004). In vitro and in vivo anti-tumoral effect of curcumin against melanoma cells. Int J Cancer, 111, 381-7. https://doi.org/10.1002/ijc.20160
  54. Opipari AW, Jr., Tan L, Boitano AE, et al (2004). Resveratrol-induced autophagocytosis in ovarian cancer cells. Cancer Res, 64, 696-703. https://doi.org/10.1158/0008-5472.CAN-03-2404
  55. Pandey S, Chandravati (2012). Autophagy in cervical cancer: an emerging therapeutic target. Asian Pac J Cancer Prev, 13, 4867-71. https://doi.org/10.7314/APJCP.2012.13.10.4867
  56. Park HW, In G, Han ST, et al (2013). Simultaneous determination of 30 ginsenosides in Panax ginseng preparations using ultra performance liquid chromatography. J Ginseng Res, 37, 457-67. https://doi.org/10.5142/jgr.2013.37.457
  57. Plengsuriyakarn T, Viyanant V, Eursitthichai V, et al (2012). Anticancer activities against cholangiocarcinoma, toxicity and pharmacological activities of Thai medicinal plants in animal models. BMC Complement Altern Med, 12, 23. https://doi.org/10.1186/1472-6882-12-23
  58. Qanungo S, Das M, Haldar S, et al (2005). Epigallocatechin-3-gallate induces mitochondrial membrane depolarization and caspase-dependent apoptosis in pancreatic cancer cells. Carcinogenesis, 26, 958-67.
  59. Qian H, Yang Y, Wang X (2011). Curcumin enhanced adriamycin-induced human liver-derived Hepatoma G2 cell death through activation of mitochondria-mediated apoptosis and autophagy. Eur J Pharm Sci, 43, 125-31. https://doi.org/10.1016/j.ejps.2011.04.002
  60. Qu X, Yu J, Bhagat G, et al (2003). Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest, 112, 1809-20. https://doi.org/10.1172/JCI20039
  61. Rocque GB, Cleary JF (2013). Palliative care reduces morbidity and mortality in cancer. Nat Rev Clin Oncol, 10, 80-9.
  62. Romanov J, Walczak M, Ibiricu I, et al (2012). Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J, 31, 4304-17. https://doi.org/10.1038/emboj.2012.278
  63. Russell SE, Hickey GI, Lowry WS, et al (1990). Allele loss from chromosome 17 in ovarian cancer. Oncogene, 5, 1581-3.
  64. Sabolovic N, Heurtaux T, Humbert AC, et al (2007). cis- and trans-Resveratrol are glucuronidated in rat brain, olfactory mucosa and cultured astrocytes. Pharmacol, 80, 185-92. https://doi.org/10.1159/000104149
  65. Saito H, Inazawa J, Saito S, et al (1993). Detailed deletion mapping of chromosome 17q in ovarian and breast cancers: 2-cM region on 17q21.3 often and commonly deleted in tumors. Cancer Res, 53, 3382-5.
  66. Satoo K, Noda NN, Kumeta H, et al (2009). The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J, 28, 1341-50. https://doi.org/10.1038/emboj.2009.80
  67. Scarlatti F, Bauvy C, Ventruti A, et al (2004). Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1. J Biol Chem, 279, 18384-91. https://doi.org/10.1074/jbc.M313561200
  68. Scarlatti F, Maffei R, Beau I, et al (2008). Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ, 15, 1318-29. https://doi.org/10.1038/cdd.2008.51
  69. Shammas MA, Neri P, Koley H, et al (2006). Specific killing of multiple myeloma cells by (-)-epigallocatechin-3-gallate extracted from green tea: biologic activity and therapeutic implications. Blood, 108, 2804-10. https://doi.org/10.1182/blood-2006-05-022814
  70. Shimizu M, Shirakami Y, Moriwaki H (2008). Targeting receptor tyrosine kinases for chemoprevention by green tea catechin, EGCG. Int J Mol Sci, 9, 1034-49. https://doi.org/10.3390/ijms9061034
  71. Shinojima N, Yokoyama T, Kondo Y, et al (2007). Roles of the Akt/mTOR/p70S6K and ERK1/2 signaling pathways in curcumin-induced autophagy. Autophagy, 3, 635-7. https://doi.org/10.4161/auto.4916
  72. Siddiqui IA, Malik A, Adhami VM, et al (2008). Green tea polyphenol EGCG sensitizes human prostate carcinoma LNCaP cells to TRAIL-mediated apoptosis and synergistically inhibits biomarkers associated with angiogenesis and metastasis. Oncogene, 27, 2055-63. https://doi.org/10.1038/sj.onc.1210840
  73. Tang SN, Singh C, Nall D, et al (2010). The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J Mol Signal, 5, 14. https://doi.org/10.1186/1750-2187-5-14
  74. Thakur VS, Gupta K, Gupta S (2012). Green tea polyphenols increase p53 transcriptional activity and acetylation by suppressing class I histone deacetylases. Int J Oncol, 41, 353-61.
  75. Vidanarachchi JK, Kurukulasuriya MS, Malshani Samaraweera A, et al (2012). Applications of marine nutraceuticals in dairy products. Adv Food Nutr Res, 65, 457-78. https://doi.org/10.1016/B978-0-12-416003-3.00030-5
  76. Weber WA (2009). Assessing tumor response to therapy. J Nucl Med, 50, 1-10. https://doi.org/10.2967/jnumed.108.057174
  77. Weisberger AS, Pensky J (1958). Tumor inhibition by a sulfhydryl-blocking agent related to an active principle of garlic (Allium sativum). Cancer Res, 18, 1301-8.
  78. Wessely R, Schomig A, Kastrati A (2006). Sirolimus and Paclitaxel on polymer-based drug-eluting stents: similar but different. J Am Coll Cardiol, 47, 708-14. https://doi.org/10.1016/j.jacc.2005.09.047
  79. White E, DiPaola RS (2009). The double-edged sword of autophagy modulation in cancer. Clin Cancer Res, 15, 5308-16. https://doi.org/10.1158/1078-0432.CCR-07-5023
  80. Wu SL, Sun ZJ, Yu L, et al (2004). Effect of resveratrol and in combination with 5-FU on murine liver cancer. World J Gastroenterol, 10, 3048-52. https://doi.org/10.3748/wjg.v10.i20.3048
  81. Yang S, Wang X, Contino G, et al (2011). Pancreatic cancers require autophagy for tumor growth. Genes Dev, 25, 717-29. https://doi.org/10.1101/gad.2016111
  82. Yang Z, Klionsky DJ (2010). Eaten alive: a history of macroautophagy. Nat Cell Biol, 12, 814-22. https://doi.org/10.1038/ncb0910-814
  83. Yue Z, Jin S, Yang C, et al (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA, 100, 15077-82. https://doi.org/10.1073/pnas.2436255100
  84. Zhang C, An L, Fengye J (2002). The research progress of ginseng saponin physiological activity. Food Fermentation Industries, 28, 70-4.
  85. Zhang Q, Kang X, Zhao W (2006). Antiangiogenic effect of low-dose cyclophosphamide combined with ginsenoside Rg3 on Lewis lung carcinoma. Biochem Biophys Res Commun, 342, 824-8. https://doi.org/10.1016/j.bbrc.2006.02.044
  86. Zhong LR, Chen X, Wei KM (2013). Radix tetrastigma hemsleyani flavone induces apoptosis in human lung carcinoma a549 cells by modulating the MAPK pathway. Asian Pac J Cancer Prev, 14, 5983-7. https://doi.org/10.7314/APJCP.2013.14.10.5983
  87. Zhou DY, Ding N, Du ZY, et al (2014). Curcumin analogues with high activity for inhibiting human prostate cancer cell growth and androgen receptor activation. Mol Med Rep, 10, 1315-22.

Cited by

  1. Plant phenols and autophagy vol.81, pp.4, 2016, https://doi.org/10.1134/S0006297916040015
  2. Root Extract against Hepatocellular Carcinoma Cells vol.2017, pp.1741-4288, 2017, https://doi.org/10.1155/2017/7218562
  3. Natural products as modulator of autophagy with potential clinical prospects vol.22, pp.3, 2017, https://doi.org/10.1007/s10495-016-1335-1
  4. Curcumin induces apoptotic cell death and protective autophagy in human gastric cancer cells vol.37, pp.6, 2017, https://doi.org/10.3892/or.2017.5637
  5. A Comprehensive Review on Pharmacotherapeutics of Three Phytochemicals, Curcumin, Quercetin, and Allicin, in the Treatment of Gastric Cancer vol.48, pp.4, 2017, https://doi.org/10.1007/s12029-017-9997-7
  6. Tumor Protein (TP)-p53 Members as Regulators of Autophagy in Tumor Cells upon Marine Drug Exposure vol.14, pp.8, 2016, https://doi.org/10.3390/md14080154
  7. Role of caspase-10 in the death of acute leukemia cells vol.12, pp.2, 2016, https://doi.org/10.3892/ol.2016.4785
  8. Lunasin: A promising polypeptide for the prevention and treatment of cancer vol.13, pp.6, 2017, https://doi.org/10.3892/ol.2017.6017
  9. Nutraceutical or Pharmacological Potential of Moringa oleifera Lam. vol.10, pp.3, 2018, https://doi.org/10.3390/nu10030343
  10. Targeting autophagy using natural compounds for cancer prevention and therapy pp.0008543X, 2019, https://doi.org/10.1002/cncr.31978