Pyrroloquinoline quinone induces cancer cell apoptosis via mitochondrial-dependent pathway and down-regulating cellular Bcl-2 protein expression

Journal of Cancer

Volumn 5, Issue 7, 2014, Pages 609-624

  Min, Zhihui ^a,b,c   Wang, Lingyan ^a   Jin, Jianjun ^a,b   Wang, Xiangdong ^a,b,c   Zhu, Bijun ^a   Chen, Hao ^d   Cheng, Yunfeng ^a,b,c  

^a FUDAN UNIVERSITY   (China)

^b ZHONGSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

^c Shanghai Key Laboratory of Organ Transplantation   (China)

^d TONGJI UNIVERSITY   (China)

Author keywords

Apoptosis; Bcl 2; MAPK; Mitochondrial membrane potential; Pyrroloquinoline quinone (PQQ)

Indexed keywords

EID: 84905509457     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.9002     Document Type: Article

References (46)

1. Salisbury SA, Forrest HS, Cruse WB, Kennard O. A novel coenzyme from bacterial primary alcohol dehydrogenases. Nature. 1979; 280: 843-4.
2. Kasahara T, Kato T. Nutritional biochemistry: A new redox-cofactor vitamin for mammals. Nature. 2003; 422: 832. doi:10.1038/422832a.
3. Kumazawa T, Sato K, Seno H, Ishii A, Suzuki O. Levels of pyrroloquinoline quinone in various foods. The Biochemical journal. 1995; 307 (Pt 2): 331-3.
4. Noji N, Nakamura T, Kitahata N, Taguchi K, Kudo T, Yoshida S, et al. Simple and sensitive method for pyrroloquinoline quinone (PQQ) analysis in various foods using liquid chromatography/electrospray-ionization tandem mass spectrometry. Journal of agricultural and food chemistry. 2007; 55: 7258-63. doi:10.1021/jf070483r.
5. He K, Nukada H, Urakami T, Murphy MP. Antioxidant and pro-oxidant properties of pyrroloquinoline quinone (PQQ): implications for its function in biological systems. Biochemical pharmacology. 2003; 65: 67-74.
6. Tao R, Karliner JS, Simonis U, Zheng J, Zhang J, Honbo N, et al. Pyrroloquinoline quinone preserves mitochondrial function and prevents oxidative injury in adult rat cardiac myocytes. Biochemical and biophysical research communications. 2007; 363: 257-62. doi:10.1016/j.bbrc.2007.08.041.
7. Hara H, Hiramatsu H, Adachi T. Pyrroloquinoline quinone is a potent neuroprotective nutrient against 6-hydroxydopamine-induced neurotoxicity. Neurochemical research. 2007; 32: 489-95. doi:10.1007/s11064-006-9257-x.
8. Xiong XH, Zhao Y, Ge X, Yuan SJ, Wang JH, Zhi JJ, et al. Production and radioprotective effects of pyrroloquinoline quinone. International journal of molecular sciences. 2011; 12: 8913-23. doi:10.3390/ijms12128913.
9. Shankar BS, Pandey R, Amin P, Misra HS, Sainis KB. Role of glutathione in augmenting the anticancer activity of pyrroloquinoline quinone (PQQ). Redox report: communications in free radical research. 2010; 15: 146-54. doi:10.1179/174329210X12650506623762.
10. Tchaparian E, Marshal L, Cutler G, Bauerly K, Chowanadisai W, Satre M, et al. Identification of transcriptional networks responding to pyrroloquinoline quinone dietary supplementation and their influence on thioredoxin expression, and the JAK/STAT and MAPK pathways. The Biochemical journal. 2010; 429: 515-26. doi:10.1042/BJ20091649.
11. Zhang Q, Shen M, Ding M, Shen D, Ding F. The neuroprotective action of pyrroloquinoline quinone against glutamate-induced apoptosis in hippocampal neurons is mediated through the activation of PI3K/Akt pathway. Toxicology and applied pharmacology. 2011; 252: 62-72. doi:10.1016/j.taap.2011.02.006.
12. Toimela T, Tahti H, Ylikomi T. Comparison of an automated pattern analysis machine vision time-lapse system with traditional endpoint measurements in the analysis of cell growth and cytotoxicity. Alternatives to laboratory animals : ATLA. 2008; 36: 313-25.
13. Zhang P, Xu Y, Sun J, Li X, Wang L, Jin L. Protection of pyrroloquinoline quinone against methylmercury-induced neurotoxicity via reducing oxidative stress. Free radical research. 2009; 43: 224-33. doi:10.1080/10715760802677348.
14. Kumazawa T, Hiwasa T, Takiguchi M, Suzuki O, Sato K. Activation of Ras signaling pathways by pyrroloquinoline quinone in NIH3T3 mouse fibroblasts. International journal of molecular medicine. 2007; 19: 765-70.
15. Kimura K, Takada M, Ishii T, Tsuji-Naito K, Akagawa M. Pyrroloquinoline quinone stimulates epithelial cell proliferation by activating epidermal growth factor receptor through redox cycling. Free radical biology & medicine. 2012; 53: 1239-51. doi:10.1016/j.freeradbiomed.2012.07.015.
16. Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis: an international journal on programmed cell death. 2000; 5: 415-8.
17. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W, et al. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. The Journal of biological chemistry. 2003; 278: 37832-9. doi:10.1074/jbc.M301546200.
18. Bras M, Queenan B, Susin SA. Programmed cell death via mitochondria: different modes of dying. Biochemistry Biokhimiia. 2005; 70: 231-9.
19. Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Molecular cell. 1999; 3: 159-67.
20. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature. 2004; 432: 307-15. doi:10.1038/nature03098.
21. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. The Journal of experimental medicine. 1996; 184: 1155-60.
22. Singh N, Nambiar D, Kale RK, Singh RP. Usnic Acid inhibits growth and induces cell cycle arrest and apoptosis in human lung carcinoma a549 cells. Nutrition and cancer. 2013; 65 Suppl 1: 36-43. doi:10.1080/01635581.2013.785007.
23. Tung YT, Chen HL, Lee CY, Chou YC, Lee PY, Tsai HC, et al. Active Component of Danshen (Salvia miltiorrhiza Bunge), Tanshinone I, Attenuates Lung Tumorigenesis via Inhibitions of VEGF, Cyclin A, and Cyclin B Expressions. Evidence-based complementary and alternative medicine: eCAM. 2013; 2013: 319247. doi:10.1155/2013/319247.
24. Antonoff MB, Chugh R, Borja-Cacho D, Dudeja V, Clawson KA, Skube SJ, et al. Triptolide therapy for neuroblastoma decreases cell viability in vitro and inhibits tumor growth in vivo. Surgery. 2009; 146: 282-90. doi:10.1016/j.surg.2009.04.023.
25. Chen YH, Yeh CW, Lo HC, Su SL, Hseu YC, Hsu LS. Generation of reactive oxygen species mediates butein-induced apoptosis in neuroblastoma cells. Oncology reports. 2012; 27: 1233-7. doi:10.3892/or.2012.1632.
26. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer research. 1999; 59: 1693s-700s.
27. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 1998; 94: 481-90.
28. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Molecular cell. 2010; 37: 299-310. doi:10.1016/j.molcel.2010.01.025.
29. Rolland SG, Conradt B. New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Current opinion in cell biology. 2010; 22: 852-8. doi:10.1016/j.ceb.2010.07.014.
30. Janicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. The Journal of biological chemistry. 1998; 273: 9357-60.
31. Singh T, Sharma SD, Katiyar SK. Grape proanthocyanidins induce apoptosis by loss of mitochondrial membrane potential of human non-small cell lung cancer cells in vitro and in vivo. PloS one. 2011; 6: e27444. doi:10.1371/journal.pone.0027444.
32. Jung KH, Noh JH, Kim JK, Eun JW, Bae HJ, Xie HJ, et al. HDAC2 overexpression confers oncogenic potential to human lung cancer cells by deregulating expression of apoptosis and cell cycle proteins. Journal of cellular biochemistry. 2012; 113: 2167-77. doi:10.1002/jcb.24090.
33. Dhanasekaran DN, Johnson GL. MAPKs: function, regulation, role in cancer and therapeutic targeting. Oncogene. 2007; 26: 3097-9. doi:10.1038/sj.onc.1210395.
34. Hu M, Du Q, Vancurova I, Lin X, Miller EJ, Simms HH, et al. Proapoptotic effect of curcumin on human neutrophils: activation of the p38 mitogen-activated protein kinase pathway. Critical care medicine. 2005; 33: 2571-8.
35. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell research. 2005; 15: 11-8. doi:10.1038/sj.cr.7290257.
36. Owens TW, Valentijn AJ, Upton JP, Keeble J, Zhang L, Lindsay J, et al. Apoptosis commitment and activation of mitochondrial Bax during anoikis is regulated by p38MAPK. Cell death and differentiation. 2009; 16: 1551-62. doi:10.1038/cdd.2009.102.
37. Van Laethem A, Van Kelst S, Lippens S, Declercq W, Vandenabeele P, Janssens S, et al. Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apoptosis induced by UVB irradiation in human keratinocytes. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2004; 18: 1946-8. doi:10.1096/fj.04-2285fje.
38. Vermeulen L, Vanden Berghe W, Beck IM, De Bosscher K, Haegeman G. The versatile role of MSKs in transcriptional regulation. Trends in biochemical sciences. 2009; 34: 311-8. doi:10.1016/j.tibs.2009.02.007.
39. Kim BJ, Ryu SW, Song BJ. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. The Journal of biological chemistry. 2006; 281: 21256-65. doi:10.1074/jbc.M510644200.
40. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 2002; 298: 1911-2. doi:10.1126/science.1072682.
41. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochimica et biophysica acta. 2007; 1773: 1263-84. doi:10.1016/j.bbamcr.2006.10.001.
42. Meloche S, Pouyssegur J. The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene. 2007; 26: 3227-39. doi:10.1038/sj.onc.1210414.
43. He B, Liu SQ, Li HH. [The extracellular signal-regulated kinase was promoted by pyrroloquinoline quinine in cultured Schwann cells]. Zhonghua zheng xing wai ke za zhi = Zhonghua zhengxing waike zazhi = Chinese journal of plastic surgery. 2010; 26: 444-7.
44. Gotfryd K, Skladchikova G, Lepekhin EA, Berezin V, Bock E, Walmod PS. Cell type-specific anti-cancer properties of valproic acid: independent effects on HDAC activity and Erk1/2 phosphorylation. BMC cancer. 2010; 10: 383. doi:10.1186/1471-2407-10-383.
45. Kim JK, Choi JW, Lim S, Kwon O, Seo JK, Ryu SH, et al. Phospholipase C-eta1 is activated by intracellular Ca(2+) mobilization and enhances GPCRs/PLC/Ca(2+) signaling. Cellular signalling. 2011; 23: 1022-9. doi:10.1016/j.cellsig.2011.01.017.
46. Sidiropoulou E, Sachana M, Flaskos J, Harris W, Hargreaves AJ, Woldehiwet Z. Fipronil interferes with the differentiation of mouse N2a neuroblastoma cells. Toxicology letters. 2011; 201: 86-91. doi:10.1016/j.toxlet.2010.12.009.