E2F4 and ribonucleotide reductase mediate S-phase arrest in colon cancer cells treated with chlorophyllin

International Journal of Cancer

Volumn 125, Issue 9, 2009, Pages 2086-2094

  Chimploy, Korakod ^a,b   Díaz, G Dario ^a   Li, Qingjie ^a   Carter, Orianna ^a   Dashwood, Wan Mohaiza ^a   Mathews, Christopher K ^b   Williams, David E ^a,b   Bailey, George S ^a,b   Dashwood, Roderick H ^a,b  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Chlorophyllin; Colorectal cancer; Rb E2F pathway; Ribonucleotide reductase

Indexed keywords

BROXURIDINE; CHLOROPHYLL; P21 ACTIVATED KINASE; PROTEIN P53; RIBONUCLEOTIDE REDUCTASE; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F4; ANTINEOPLASTIC AGENT; CHLOROPHYLLIDE; DNA; E2F1 PROTEIN, HUMAN; E2F4 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; COLON CANCER; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; COLON TUMOR; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTICARCINOGENIC AGENTS; CELL LINE, TUMOR; CHLOROPHYLLIDES; COLONIC NEOPLASMS; DNA; E2F1 TRANSCRIPTION FACTOR; E2F4 TRANSCRIPTION FACTOR; HUMANS; RIBONUCLEOTIDE REDUCTASES; S PHASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 70249142203     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24559     Document Type: Article

References (69)

1. Nordlund P, Reichard P. Ribonucleotide reductases. Annu Rev Biochem 2006;75:681-706.
2. Larsson KM, Jordan A, Eliasson R, Reichard P, Logan DT, Nordlund P. Structural mechanism of allosteric substrate specificity regulation in a ribonucleotide reductase. Nat Struct Mol Biol 2004;11:1142-1149 (Pubitemid 39453345)
3. Hendricks SP, Mathews CK. Allosteric regulation of vaccinia virus ribonucleotide reductase, analyzed by simultaneous monitoring of its four activities. J Biol Chem 1998;273:29512-29518
4. Chimploy K, Mathews CK. Mouse ribonucleotide reductase control: influence of substrate binding upon interactions with allosteric effectors. J Biol Chem 2001;276:7093-7100 (Pubitemid 37392008)
5. Chimploy K, Tassotto ML, Mathews CK. Ribonucleotide reductase, a possible agent in deoxyribonucleotide pool asymmetries induced by hypoxia. J Biol Chem 2000;275:39267-39271 (Pubitemid 32058946)
6. Björklund S, Skog S, Tribukait B, Thelander L. S-phase-specific expression of mammalian ribonucleotide reductase R1 and R2 subunit mRNAs. Biochemistry 1990;29:5452-5458 (Pubitemid 20202268)
7. Engström Y, Eriksson S, Jildevik I, Skog S, Thelander L, Tribukait B. Cell cycle-dependent expression of mammalian ribonucleotide reductase. Differential regulation of the two subunits. J Biol Chem 1985;260:9114-9116
8. Chabes AL, Björklund S, Thelander L. S phase-specific transcription of the mouse ribonucleotide reductase R2 gene requires both a proximal repressive E2F-binding site and an upstream promoter activating region. J Biol Chem 2004;279:10796-10807 (Pubitemid 38372692)
9. Chabes AL, Pfleger CM, Kirschner MW, Thelander L. Mouse ribonucleotide reductase R2 protein: a new target for anaphase-promoting complex-Cdh1-mediated proteolysis. Proc Natl Acad Sci USA 2003;100:3925-3929 (Pubitemid 36418133)
10. Chabes AL, Thelander L. Controlled protein degradation regulates ribonucleotide reductase activity in proliferating mammalian cells during the normal cell cycle and in response to DNA damage and replication blocks. J Biol Chem 2000;275:17747-17753 (Pubitemid 30430824)
11. Tanaka H, Arakawa H, Yamaguchi T, Shiraishi K, Fukuda S, Matsui K, Takei Y, Nakamura Y. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 2000;404:42-49 (Pubitemid 30143125)
12. Nakano K, Bálint E, Ashcroft M, Vousden KH. Ribonucleotide reductase gene is a transcriptional target of p53 and p73. Oncogene 2000;19:4283-4289 (Pubitemid 30750926)
13. Bourdon A, Minai L, Serre V, Jais JP, Sarzi E, Aubert S, Chrétien D, de Lonlay P, Paquis-Flucklinger V, Arakawa H, Nakamura Y, Munnich A, et al. Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat Genet 2007;39:776-780 (Pubitemid 46848590)
14. Thelander L. Ribonucleotide reductase and mitochondrial DNA synthesis. Nat Genet 2007;39:703-704 (Pubitemid 46848577)
15. Filatov D, Thelander L. Role of a proximal NF-Y binding promoter element in S phase-specific expression of mouse ribonucleotide reductase R2 gene. J Biol Chem 1995;270:25239-25243
16. Liu X, Zhou B, Xue L, Qiu W, Shih J, Zheng S, Yen Y. Nuclear factor Y regulation and promoter transactivation of human ribonucleotide reductase subunit M2 gene in a Gemcitabine resistant KB clone. Biochem Pharmacol 2004;67:1499-1511 (Pubitemid 38388212)
17. Fan H, Villegas C, Wright JA. Ribonucleotide reductase R2 component is a novel malignancy determinant that cooperates with activated oncogenes to determine transformation and malignant potential. Proc Natl Acad Sci USA 1996;93:14036-14040 (Pubitemid 26424241)
18. Zhou BS, Tsai P, Ker R, Tsai J, Ho R, Yu J, Shih J, Yen Y. Overexpression of transfected human ribonucleotide reductase M2 subunit in human cancer cells enhances their invasive potential. Clin Exp Metastasis 1998;16:43-49 (Pubitemid 28122554)
19. Liu X, Zhou B, Xue L, Shih J, Tye K, Lin W, Qi C, Chu P, Un F, Wen W, Yen Y. Metastasis-suppressing potential of ribonucleotide reductase small subunit p53R2 in human cancer cells. Clin Cancer Res 2006;12:6337-6344 (Pubitemid 44799702)
20. Heidel JD, Yu Z, Liu JY, Rele SM, Liang Y, Zeidan RK, Kornbrust DJ, Davis ME. Administration in non-human primates of escalating intravenous doses of targeted nanoparticles containing ribonucleotide reductase subunit M2 siRNA. Proc Natl Acad Sci USA 2007;104:5715-5721 (Pubitemid 47175600)
21. Shao J, Zhou B, Chu B, Yen Y. Ribonucleotide reductase inhibitors and future drug design. Curr Cancer Drug Targets 2006;6: 409-431 (Pubitemid 44033390)
22. Wang X, Zhenchuk A, Wiman KG, Albertioni F. Regulation of p53R2 and its role as potential target for cancer therapy. Cancer Lett 2009;276:1-7.
23. Johnson DG, Walker CL. Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol 1999;39:295-312.
24. Nevins JR. The Rb/E2F pathway and cancer. Hum Mol Genet 2001;10:699-703.
25. Genovese C, Trani D, Caputi M, Claudio PP. Cell cycle control and beyond: emerging roles for the retinoblastoma gene family. Oncogene 2006;25:5201-5209 (Pubitemid 44299078)
26. Johnson DG, Schneider-Broussard R. Role of E2F in cell cycle control and cancer. Front Biosci 1998;3:d447-58.
27. Martin K, Trouche D, Hagemeier C, Sørensen TS, La Thangue NB, Kouzarides T. Stimulation of E2F1/DP1 transcriptional activity by MDM2 oncoprotein. Nature 1995;375:691-694
28. O'Connor DJ, Lam EW, Griffin S, Zhong S, Leighton LC, Burbidge SA, Lu X. Physical and functional interactions between p53 and cell cycle co-operating transcription factors, E2F1 and DP1. EMBO J 1995;14:6184-6192 (Pubitemid 26007305)
29. Sørensen TS, Girling R, Lee CW, Gannon J, Bandara LR, La Thangue NB. Functional interaction between DP-1 and p53. Mol Cell Biol 1996;16:5888-5895
30. Mayhew CN, Carter SL, Fox SR, Sexton CR, Reed CA, Srinivasan SV, Liu X, Wikenheiser-Brokamp K, Boivin GP, Lee JS, Aronow BJ, Thorgeirsson SS, et al. RB loss abrogates cell cycle control and genome integrity to promote liver tumorigenesis. Gastroenterology 2007;133:976-984 (Pubitemid 47374137)
31. Nacusi LP, Sheaff RJ. Deregulation of cell cycle machinery in pancreatic cancer. Pancreatology 2007;7:373-377 (Pubitemid 47482100)
32. Xing J, Spitz MR, Lu C, Zhao H, Yang H, Wang W, Stewart DJ, Wu X. Deficient G2-M and S checkpoints are associated with increased lung cancer risk: a case-control analysis. Cancer Epidemiol Biomarkers Prev 2007;16:1517-1522
33. Wiman KG. The retinoblastoma gene: role in cell cycle control and cell differentiation. FASEB J 1993;7:841-845 (Pubitemid 23225539)
34. Wang HL, Wang J, Xiao SY, Haydon R, Stoiber D, He TC, Bissonnette M, Hart J. Elevated protein expression of cyclin D1 and Fra-1 but decreased expression of c-Myc in human colorectal adenocarcinomas overexpressing beta-catenin. Int J Cancer 2002; 101:301-310 (Pubitemid 34983184)
35. Kaiser S, Park YK, Franklin JL, Halberg RB, Yu M, Jessen WJ, Freudenberg J, Chen X, Haigis K, Jegga AG, Kong S, Sakthivel B, et al. Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol 2007;8:R131. (Pubitemid 351916552)
36. Díaz GD, Li Q, Dashwood RH. Caspase-8 and apoptosis-inducing factor mediate a cytochrome c-independent pathway of apoptosis in human colon cancer cells induced by the dietary phytochemical chlorophyllin. Cancer Res 2003;63:1254-1261 (Pubitemid 36348703)
37. Arimoto S, Fukuoka S, Itome C, Nakano H, Rai H, Hayatsu H. Binding of polycyclic planar mutagens to chlorophyllin resulting in inhibition of the mutagenic activity. Mutat Res 1993;287:293-305. (Pubitemid 23174197)
38. Breinholt V, Schimerlik M, Dashwood R, Bailey G. Mechanisms of chlorophyllin anticarcinogenesis against aflatoxin B1: complex formation with the carcinogen. Chem Res Toxicol 1995;8:506-514
39. Dashwood RH. Protection by chlorophyllin against the covalent binding of 2-amino-3-methylimidazo[4,5-f]quinoline (IQ) to rat liver DNA. Carcinogenesis 1992;13:113-118
40. Dashwood RH, Breinholt V, Bailey GS. Chemopreventive properties of chlorophyllin: inhibition of aflatoxin B1 (AFB1)-DNA binding in vivo and anti-mutagenic activity against AFB1 and two heterocyclic amines in the Salmonella mutagenicity assay. Carcinogenesis 1991;12:939-942
41. Egner PA, Wang JB, Zhu YR, Zhang BC, Wu Y, Zhang QN, Qian GS, Kuang SY, Gange SJ, Jacobson LP, Helzlsouer KJ, Bailey GS, et al. Chlorophyllin intervention reduces aflatoxin-DNA adducts in individuals at high risk for liver cancer. Proc Natl Acad Sci USA 2001; 98:14601-14606 (Pubitemid 33121438)
42. Guo D, Horio DT, Grove JS, Dashwood RH. Inhibition by chlorophyllin of 2-amino-3-methylimidazo[4,5-f]quinoline-induced tumorigenesis in the male F344 rat. Cancer Lett 1995;95:161-165
43. Guo D, Schut HA, Davis CD, Snyderwine EG, Bailey GS, Dashwood RH. Protection by chlorophyllin and indole-3-carbinol against 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine (PhIP)-induced DNA adducts and colonic aberrant crypts in the F344 rat. Carcinogenesis 1995;16:2931-2937
44. Reddy AP, Harttig U, Barth MC, Baird WM, Schimerlik M, Hendricks JD, Bailey GS. Inhibition of dibenzo[a,l]pyrene-induced multi-organ carcinogenesis by dietary chlorophyllin in rainbow trout. Carcinogenesis 1999;20:1919-1926.
45. Tachino N, Guo D, Dashwood WM, Yamane S, Larsen R, Dashwood R. Mechanisms of the in vitro antimutagenic action of chlorophyllin against benzo[a]pyrene: studies of enzyme inhibition, molecular complex formation and degradation of the ultimate carcinogen. Mutat Res 1994;308:191-203. (Pubitemid 24238949)
46. Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 2004;101:18030-18035 (Pubitemid 40054069)
47. Chung YM, Bae YS, Lee SY. Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylate-induced apoptosis. Free Radic Biol Med 2003;34:434-442
48. Narvaez CJ, Welsh J. Role of mitochondria and caspases in vitamin D-mediated apoptosis of MCF-7 breast cancer cells. J Biol Chem 2001;276:9101-9107 (Pubitemid 37385490)
49. Shankar S, Srivastava RK. Involvement of Bcl-2 family members, phosphatidylinositol 3′-kinase/AKT and mitochondrial p53 in curcumin (diferulolylmethane)-induced apoptosis in prostate cancer. Int J Oncol 2007;30:905-918
50. Rancourt RC, Keng PC, Helt CE, O'Reilly MA. The role of p21CIP1/ WAF1 in growth of epithelial cells exposed to hyperoxia. Am J Lung Cell Mol Physiol 2001;280:L617-26.
51. Ababou M, Dumaire V, Lécluse Y, Amor-Guéret M. Bloom's syndrome protein response to ultraviolet-c radiation and hydroxyureamediated DNA synthesis inhibition. Oncogene 2002;21:2079-2088 (Pubitemid 34270896)
52. Joerges C, Kuntze, I, Herzinger T. Induction of a caffeine-sensitive S-phase cell cycle checkpoint by psoralen plus ultraviolet A radiation. Oncogene 2003;22:6119-6128 (Pubitemid 37281641)
53. Li Q, Dashwood WM, Zhong X, Nakagama H, Dashwood RH. Bcl-2 overexpression in PhIP-induced colon tumors: cloning of the rat Bcl-2 promoter and characterization of a pathway involving beta-catenin, c-Myc and E2F1. Oncogene 2007;26:6194-6202 (Pubitemid 47414373)
54. Li Q, Dashwood WM, Zhong X, Al-Fageeh M, Dashwood RH. Cloning of the rat (-catenin (Ctnnb1) gene promoter and its functional analysis compared with the Catnb and CTNNB1 promoters. Genomics 2004;83:231-242 (Pubitemid 38050112)
55. Moberg K, Starz MA, Lees JA. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol Cell Biol 1996; 16: 1436-1449 (Pubitemid 26095614)
56. Slabaugh MB, Johnson TL, Mathews CK. Vaccinia virus induces ribonucleotide reductase in primate cells. J Virol 1984;52:507-514
57. Tsimberidou AM, Alvarado Y, Giles FJ. Evolving role of ribonucleotide reductase inhibitors in hematologic malignancies. Expert Rev Anticancer Ther 2002;2:437-448 (Pubitemid 34947120)
58. Yarbro JW. Mechanism of action of hydroxyurea. Semin Oncol 1992;19:1-10.
59. van Oijen MG, Slootweg PJ. Gain-of-function mutations in the tumor suppressor gene p53. Clin Cancer Res 2000;6:2138-2145 (Pubitemid 30399178)
60. Chiu LC, Kong CK, Ooi VE. The chlorophyllin-induced cell cycle arrest and apoptosis in human breast cancer MCF-7 cells is associated with ERK deactivation and Cyclin D1 depletion. Int J Mol Med 2005;16:735-740
61. Yamazaki L. Role of the RB tumor suppressor in cancer. Cancer Treat Res 2003;115:209-230
62. Woo MS, Sáanchez I, Dynlacht BD. p130 and p107 use a conserved domain to inhibit cellular cyclin-dependent kinase activity. Mol Cell Biol 1997;17:3566-3579
63. Lin ZP, Belcourt MF, Cory JG, Sartorelli AC. Stable suppression of the R2 subunit of ribonucleotide reductase by R2-targeted short interference RNA sensitizes p53(-/-) HCT-116 colon cancer cells to DNA-damaging agents and ribonucleotide reductase inhibitors. J Biol Chem 2004;279:27030-27038
64. Yoshida T, Haga S, Numata Y, Yamashita K, Mikami T, Ogawa T, Ohkusa T, Okayasu I. Disruption of the p53-p53R2 DNA repair system in ulcerative colitis contributes to colon tumorigenesis. Int J Cancer 2006;118:1395-1403 (Pubitemid 43306525)
65. Kumar SS, Chaubey RC, Devasagayam TP, Priyadarsini KI, Chauhan PS. Inhibition of radiation-induced DNA damage in plasmid pBR322 by chlorophyllin and possible mechanism(s) of action. Mutat Res 1999;425:71-79
66. Kumar SS, Devasagayam TP, Bhushan B, Verma NC. Scavenging of reactive oxygen species by chlorophyllin: an ESR study. Free Radic Res 2001;35:563-574 (Pubitemid 33133592)
67. Kapiotis S, Hermann M, Exner M, Laggner H, Gmeiner BM. Copper- and magnesium protoporphyrin complexes inhibit oxidative modification of LDL induced by hemin, transition metal ions and tyrosyl radicals. Free Radic Res 2005;39:1193-1202 (Pubitemid 41601421)
68. Ouameur AA, Marty R, Tajmir-Riahi HA. Human serum albumin complexes with chlorophyll and chlorophyllin. Biopolymers 2005;77: 129-136 (Pubitemid 40278854)
69. Te C, Gentile JM, Baguley BC, Pearson AE, Gregory T, Ferguson LR. In vivo effects of chlorophyllin on the antitumor agent cyclophosphamide. Int J Cancer 1997;70:84-89