AMPK Activators Suppress Cervical Cancer Cell Growth through Inhibition of DVL3 Mediated Wnt/β-Catenin Signaling Activity

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Kwan, H T ^a   Chan, David W ^a   Cai, Patty C H ^a   Mak, Celia S L ^a   Yung, Mingo M H ^a   Leung, Thomas H Y ^a   Wong, Oscar G W ^a   Cheung, Annie N Y ^a   Ngan, Hextan Y S ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BETA CATENIN; CYCLIN D1; DISHEVELLED PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; MAMMALIAN TARGET OF RAPAMYCIN; METFORMIN; RAPAMYCIN; UBIQUITIN; WNT PROTEIN;

ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOLECULAR MECHANICS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; UBIQUITINATION; UTERINE CERVIX CANCER; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMP-ACTIVATED PROTEIN KINASES; BETA CATENIN; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FEMALE; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; PHOSPHOPROTEINS; PLASMIDS; SIGNAL TRANSDUCTION; TIME FACTORS; UTERINE CERVICAL NEOPLASMS; WNT PROTEINS;

EID: 84871813739     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053597     Document Type: Article

References (61)

1. Hutchinson DJ, Klein KC, (2008) Human papillomavirus disease and vaccines. American journal of health-system pharmacy: AJHP: official journal of the American Society of Health-System Pharmacists 65: 2105-2112.
2. Szalmas A, Konya J, (2009) Epigenetic alterations in cervical carcinogenesis. Seminars in cancer biology 19: 144-152.
3. Ilyas M, (2005) Wnt signalling and the mechanistic basis of tumour development. J Pathol 205: 130-144.
4. Nusse R, (2005) Wnt signaling in disease and in development. Cell Res 15: 28-32.
5. Herbst A, Kolligs FT, (2007) Wnt signaling as a therapeutic target for cancer. Methods Mol Biol 361: 63-91.
6. Zylberberg B, Dormont D, Ravina JH, Madelenat P, Salat-Baroux J, et al. (1991) [Ovarian carcinomas. Intraperitoneal chemotherapy by needle]. Presse Med 20: 1320-1326.
7. Pereira-Suarez AL, Meraz MA, Lizano M, Estrada-Chavez C, Hernandez F, et al. (2002) Frequent alterations of the beta-catenin protein in cancer of the uterine cervix. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine 23: 45-53.
8. Perez-Plasencia C, Duenas-Gonzalez A, Alatorre-Tavera B, (2008) Second hit in cervical carcinogenesis process: involvement of wnt/beta catenin pathway. Int Arch Med 1: 10.
9. Bulut G, Fallen S, Beauchamp EM, Drebing LE, Sun J, et al. (2011) Beta-catenin accelerates human papilloma virus type-16 mediated cervical carcinogenesis in transgenic mice. PLoS One 6: e27243.
10. Uren A, Fallen S, Yuan H, Usubutun A, Kucukali T, et al. (2005) Activation of the canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Cancer research 65: 6199-6206.
11. Hardie DG, (2003) Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144: 5179-5183.
12. Thomas G, Hall MN, (1997) TOR signalling and control of cell growth. Current opinion in cell biology 9: 782-787.
13. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, et al. (2008) SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell metabolism 8: 224-236.
14. Proud CG, Denton RM, (1997) Molecular mechanisms for the control of translation by insulin. The Biochemical journal 328 (Pt 2): 329-341.
15. Carretero J, Medina PP, Blanco R, Smit L, Tang M, et al. (2007) Dysfunctional AMPK activity, signalling through mTOR and survival in response to energetic stress in LKB1-deficient lung cancer. Oncogene 26: 1616-1625.
16. Vazquez-Martin A, Oliveras-Ferraros C, Lopez-Bonet E, Menendez JA, (2009) AMPK: Evidence for an energy-sensing cytokinetic tumor suppressor. Cell cycle 8: 3679-3683.
17. Cool B, Zinker B, Chiou W, Kifle L, Cao N, et al. (2006) Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell metabolism 3: 403-416.
18. Zhou G, Myers R, Li Y, Chen Y, Shen X, et al. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. The Journal of clinical investigation 108: 1167-1174.
19. Corton JM, Gillespie JG, Hawley SA, Hardie DG, (1995) 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? European journal of biochemistry/FEBS 229: 558-565.
20. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, et al. (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell metabolism 2: 9-19.
21. Yu SY, Chan DW, Liu VW, Ngan HY, (2009) Inhibition of cervical cancer cell growth through activation of upstream kinases of AMP-activated protein kinase. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine 30: 80-85.
22. Alimova IN, Liu B, Fan Z, Edgerton SM, Dillon T, et al. (2009) Metformin inhibits breast cancer cell growth, colony formation and induces cell cycle arrest in vitro. Cell cycle 8: 909-915.
23. Liu B, Fan Z, Edgerton SM, Deng XS, Alimova IN, et al. (2009) Metformin induces unique biological and molecular responses in triple negative breast cancer cells. Cell cycle 8: 2031-2040.
24. Cazzaniga M, Bonanni B, Guerrieri-Gonzaga A, Decensi A, (2009) Is it time to test metformin in breast cancer clinical trials? Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 18: 701-705.
25. Bowker SL, Majumdar SR, Veugelers P, Johnson JA, (2006) Increased cancer-related mortality for patients with type 2 diabetes who use sulfonylureas or insulin. Diabetes care 29: 254-258.
26. Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD, (2005) Metformin and reduced risk of cancer in diabetic patients. BMJ 330: 1304-1305.
27. Jiralerspong S, Palla SL, Giordano SH, Meric-Bernstam F, Liedtke C, et al. (2009) Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 27: 3297-3302.
28. Chan DW, Chan CY, Yam JW, Ching YP, Ng IO, (2006) Prickle-1 negatively regulates Wnt/beta-catenin pathway by promoting Dishevelled ubiquitination/degradation in liver cancer. Gastroenterology 131: 1218-1227.
29. Chan DW, Chan CY, Yam JWP, Ching YP, Ng IO, (2006) Prickle-1 Negatively Regulates Wnt/beta-Catenin Pathway by Promoting Dishevelled Ubiquitination/Degradation in Liver Cancer. Gastroenterology 131: 1218-1227.
30. Metcalfe C, Ibrahim AE, Graeb M, de la Roche M, Schwarz-Romond T, et al. (2010) Dvl2 promotes intestinal length and neoplasia in the ApcMin mouse model for colorectal cancer. Cancer research 70: 6629-6638.
31. Uematsu K, Kanazawa S, You L, He B, Xu Z, et al. (2003) Wnt pathway activation in mesothelioma: evidence of Dishevelled overexpression and transcriptional activity of beta-catenin. Cancer research 63: 4547-4551.
32. Uematsu K, He B, You L, Xu Z, McCormick F, et al. (2003) Activation of the Wnt pathway in non small cell lung cancer: evidence of dishevelled overexpression. Oncogene 22: 7218-7221.
33. Motoshima H, Goldstein BJ, Igata M, Araki E, (2006) AMPK and cell proliferation-AMPK as a therapeutic target for atherosclerosis and cancer. J Physiol 574: 63-71.
34. Ben Sahra I, Le Marchand-Brustel Y, Tanti JF, Bost F, (2010) Metformin in cancer therapy: a new perspective for an old antidiabetic drug? Mol Cancer Ther 9: 1092-1099.
35. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, et al. (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458: 1056-1060.
36. Guigas B, Sakamoto K, Taleux N, Reyna SM, Musi N, et al. (2009) Beyond AICA riboside: in search of new specific AMP-activated protein kinase activators. IUBMB Life 61: 18-26.
37. Dumont FJ, Su Q, (1996) Mechanism of action of the immunosuppressant rapamycin. Life sciences 58: 373-395.
38. Chen H, Liu L, Ma B, Ma TM, Hou JJ, et al. (2011) Protein kinase A-mediated 14-3-3 association impedes human Dapper1 to promote dishevelled degradation. The Journal of biological chemistry 286: 14870-14880.
39. Chung MT, Lai HC, Sytwu HK, Yan MD, Shih YL, et al. (2009) SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signal pathway. Gynecologic oncology 112: 646-653.
40. Zhao Y, Yang ZQ, Wang Y, Miao Y, Liu Y, et al. (2010) Dishevelled-1 and dishevelled-3 affect cell invasion mainly through canonical and noncanonical Wnt pathway, respectively, and associate with poor prognosis in nonsmall cell lung cancer. Molecular carcinogenesis 49: 760-770.
41. Mizutani K, Miyamoto S, Nagahata T, Konishi N, Emi M, et al. (2005) Upregulation and overexpression of DVL1, the human counterpart of the Drosophila dishevelled gene, in prostate cancer. Tumori 91: 546-551.
42. Nagahata T, Shimada T, Harada A, Nagai H, Onda M, et al. (2003) Amplification, up-regulation and over-expression of DVL-1, the human counterpart of the Drosophila disheveled gene, in primary breast cancers. Cancer science 94: 515-518.
43. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
44. Miyoshi Y, Iwao K, Nagasawa Y, Aihara T, Sasaki Y, et al. (1998) Activation of the beta-catenin gene in primary hepatocellular carcinomas by somatic alterations involving exon 3. Cancer research 58: 2524-2527.
45. Sareddy GR, Panigrahi M, Challa S, Mahadevan A, Babu PP, (2009) Activation of Wnt/beta-catenin/Tcf signaling pathway in human astrocytomas. Neurochemistry international 55: 307-317.
46. Uematsu K, Seki N, Seto T, Isoe C, Tsukamoto H, et al. (2007) Targeting the Wnt signaling pathway with dishevelled and cisplatin synergistically suppresses mesothelioma cell growth. Anticancer research 27: 4239-4242.
47. Holloway KR, Calhoun TN, Saxena M, Metoyer CF, Kandler EF, et al. (2010) SIRT1 regulates Dishevelled proteins and promotes transient and constitutive Wnt signaling. Proceedings of the National Academy of Sciences of the United States of America 107: 9216-9221.
48. Zhou J, Huang W, Tao R, Ibaragi S, Lan F, et al. (2009) Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells. Oncogene 28: 1993-2002.
49. Shen Z, Wen XF, Lan F, Shen ZZ, Shao ZM, (2002) The tumor suppressor gene LKB1 is associated with prognosis in human breast carcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research 8: 2085-2090.
50. Zakikhani M, Dowling R, Fantus IG, Sonenberg N, Pollak M, (2006) Metformin is an AMP kinase-dependent growth inhibitor for breast cancer cells. Cancer research 66: 10269-10273.
51. Takatani T, Minagawa M, Takatani R, Kinoshita K, Kohno Y, (2011) AMP-activated protein kinase attenuates Wnt/beta-catenin signaling in human osteoblastic Saos-2 cells. Molecular and cellular endocrinology 339: 114-119.
52. Ben Sahra I, Laurent K, Loubat A, Giorgetti-Peraldi S, Colosetti P, et al. (2008) The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene 27: 3576-3586.
53. Zhuang Y, Miskimins WK, (2008) Cell cycle arrest in Metformin treated breast cancer cells involves activation of AMPK, downregulation of cyclin D1, and requires p27Kip1 or p21Cip1. Journal of molecular signaling 3: 18.
54. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS, (2002) AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. The Journal of biological chemistry 277: 23977-23980.
55. Kimura N, Tokunaga C, Dalal S, Richardson C, Yoshino K, et al. (2003) A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes to cells: devoted to molecular & cellular mechanisms 8: 65-79.
56. Feng Z, Fan X, Jiao Y, Ban K, (2011) Mammalian target of rapamycin regulates expression of beta-catenin in hepatocellular carcinoma. Human pathology 42: 659-668.
57. Ramachandran I, Thavathiru E, Ramalingam S, Natarajan G, Mills WK, et al. (2012) Wnt inhibitory factor 1 induces apoptosis and inhibits cervical cancer growth, invasion and angiogenesis in vivo. Oncogene 31: 2725-2737.
58. Miyazaki K, Fujita T, Ozaki T, Kato C, Kurose Y, et al. (2004) NEDL1, a novel ubiquitin-protein isopeptide ligase for dishevelled-1, targets mutant superoxide dismutase-1. The Journal of biological chemistry 279: 11327-11335.
59. Angers S, Thorpe CJ, Biechele TL, Goldenberg SJ, Zheng N, et al. (2006) The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nature cell biology 8: 348-357.
60. Hu T, Li C, Cao Z, Van Raay TJ, Smith JG, et al. (2010) Myristoylated Naked2 antagonizes Wnt-beta-catenin activity by degrading Dishevelled-1 at the plasma membrane. The Journal of biological chemistry 285: 13561-13568.
61. Shao M, Liu ZZ, Wang CD, Li HY, Carron C, et al. (2009) Down syndrome critical region protein 5 regulates membrane localization of Wnt receptors, Dishevelled stability and convergent extension in vertebrate embryos. Development 136: 2121-2131.