Critical Role of AMPK/FoxO3A Axis in Globular Adiponectin-Induced Cell Cycle Arrest and Apoptosis in Cancer Cells

Journal of Cellular Physiology

Volumn 231, Issue 2, 2016, Pages 357-369

  Shrestha, Anup ^a   Nepal, Saroj ^a   Kim, Mi Jin ^a   Chang, Jae Hoon ^a   Kim, Sang Hyun ^b   Jeong, Gil Saeng ^c   Jeong, Chul Ho ^c   Park, Gyu Hwan ^d   Jung, Sunghee ^e   Lim, Jaecheong ^e   Cho, Eunha ^e   Lee, Soyoung ^e   Park, Pil Hoon ^a  

^a Yeungnam University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c Keimyung University   (South Korea)

^d Kyungpook National University   (South Korea)

^e Korea Atomic Energy Research Institute   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ADIPONECTIN; CASPASE 3; CASPASE 7; CYCLIN D1; FAS LIGAND; PROTEIN KINASE LKB1; PROTEIN P27; TRANSCRIPTION FACTOR FKHRL1; ADIPOQ PROTEIN, HUMAN; CASP3 PROTEIN, HUMAN; CASP7 PROTEIN, HUMAN; FASLG PROTEIN, HUMAN; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA; STK11 PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE SILENCING; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL CYCLE CHECKPOINT; GENE INACTIVATION; GENETICS; HEPG2 CELL LINE; MCF 7 CELL LINE; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; APOPTOSIS; CASPASE 3; CASPASE 7; CELL CYCLE CHECKPOINTS; FAS LIGAND PROTEIN; FORKHEAD TRANSCRIPTION FACTORS; GENE KNOCKOUT TECHNIQUES; HEP G2 CELLS; HUMANS; MCF-7 CELLS; MODELS, BIOLOGICAL; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84944909674     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25080     Document Type: Article

References (67)

1. Adachi M, Brenner DA. 2008. High molecular weight adiponectin inhibits proliferation of hepatic stellate cells via activation of adenosine monophosphate-activated protein kinase. Hepatology (Baltimore, Md) 47:677-685.
2. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y. 1999. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257:79-83.
3. Barb D, Williams CJ, Neuwirth AK, Mantzoros CS. 2007. Adiponectin in relation to malignancies: A review of existing basic research and clinical evidence. Am J Clin Nutr 86:s858-s866.
4. Barreyro FJ, Kobayashi S, Bronk SF, Werneburg NW, Malhi H, Gores GJ. 2007. Transcriptional regulation of Bim by FoxO3A mediates hepatocyte lipoapoptosis. J Biol Chem 282:27141-27154.
5. Biggs WH, III, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. 1999. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 96:7421-7426.
6. Brakenhielm E, Veitonmaki N, Cao R, Kihara S, Matsuzawa Y, Zhivotovsky B, Funahashi T, Cao Y. 2004. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc Natl Acad Sci USA 101:2476-2481.
7. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
8. Bub JD, Miyazaki T, Iwamoto Y. 2006. Adiponectin as a growth inhibitor in prostate cancer cells. Biochem Biophys Res Commun 340:1158-1166.
9. Calnan DR, Brunet A. 2008. The FoxO code. Oncogene 27:2276-2288.
10. Chen MJ, Yeh YT, Lee KT, Tsai CJ, Lee HH, Wang SN. 2012. The promoting effect of adiponectin in hepatocellular carcinoma. J Surg Oncol 106:181-187.
11. Chen Q, Ganapathy S, Singh KP, Shankar S, Srivastava RK. 2010. Resveratrol induces growth arrest and apoptosis through activation of FOXO transcription factors in prostate cancer cells. PLoS ONE 5:e15288.
12. Chiacchiera F, Matrone A, Ferrari E, Ingravallo G, Lo Sasso G, Murzilli S, Petruzzelli M, Salvatore L, Moschetta A, Simone C. 2009. P38alpha blockade inhibits colorectal cancer growth in vivo by inducing a switch from HIF1alpha- to FoxO-dependent transcription. Cell Death Differ 16:1203-1214.
13. Chiacchiera F, Simone C. 2009. Inhibition of p38alpha unveils an AMPK-FoxO3A axis linking autophagy to cancer-specific metabolism. Autophagy 5:1030-1033.
14. Chiacchiera F, Simone C. 2010. The AMPK-FoxO3A axis as a target for cancer treatment. Cell Cycle 9:1091-1096.
15. Cong L, Gasser J, Zhao J, Yang B, Li F, Zhao AZ. 2007. Human adiponectin inhibits cell growth and induces apoptosis in human endometrial carcinoma cells, HEC-1-A and RL95 2. Endocr Relat Cancer 14:713-720.
16. Dalamaga M, Diakopoulos KN, Mantzoros CS. 2012. The role of adiponectin in cancer: A review of current evidence. Endocr Rev 33:547-594.
17. Denzel MS, Hebbard LW, Shostak G, Shapiro L, Cardiff RD, Ranscht B. 2009. Adiponectin deficiency limits tumor vascularization in the MMTV-PyV-mT mouse model of mammary cancer. Clin Cancer Res 15:3256-3264.
18. Diehl JA. 2002. Cycling to cancer with cyclinD1. Cancer Biol Ther 1:226-231.
19. Dieudonne MN, Bussiere M, Dos Santos E, Leneveu MC, Giudicelli Y, Pecquery R. 2006. Adiponectin mediates antiproliferative and apoptotic responses in human MCF7 breast cancer cells. Biochem Biophys Res Commun 345:271-279.
20. Elmore S. 2007. Apoptosis: A review of programmed cell death. Toxicol Pathol 35:495-516.
21. Feng Q, Sekula D, Muller R, Freemantle SJ, Dmitrovsky E. 2007. Uncovering residues that regulate cyclin D1 proteasomal degradation. Oncogene 26:5098-5106.
22. Fernandez de Mattos S, Essafi A, Soeiro I, Pietersen AM, Birkenkamp KU, Edwards CS, Martino A, Nelson BH, Francis JM, Jones MC, Brosens JJ, Coffer PJ, Lam EW. 2004. FoxO3a and BCR-ABL regulate cyclin D2 transcription through a STAT5/BCL6-dependent mechanism. Mol Cell Biol 24:10058-10071.
23. Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, Firpo E, Polyak K, Tsai LH, Broudy V, Perlmutter RM, Kaushansky K, Roberts JM. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85:733-744.
24. Glauser DA, Schlegel W. 2009. The FoxO/Bcl-6/cyclin D2 pathway mediates metabolic and growth factor stimulation of proliferation in Min6 pancreatic beta-cells. J Recept Signal Transduct Res 29:293-298.
25. Golias CH, Charalabopoulos A, Charalabopoulos K. 2004. Cell proliferation and cell cycle control: A mini review. Int J Clin Pract 58:1134-1141.
26. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. 2003. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2:28.
27. Hirai H, Satoh H, Kudoh A, Watanabe T. 2013. Interaction between resistin and adiponectin in the proliferation of rat vascular smooth muscle cells. Mol Cell Endocrinol 366:108-116.
28. Huang H, Tindall DJ. 2007. Dynamic FoxO transcription factors. J Cell Sci 120(Pt 15):2479-2487.
29. Imamura K, Ogura T, Kishimoto A, Kaminishi M, Esumi H. 2001. Cell cycle regulation via p53 phosphorylation by a 5'-AMP activated protein kinase activator, 5-aminoimidazole- 4-carboxamide-1-beta-D-ribofuranoside, in a human hepatocellular carcinoma cell line. Biochem Biophys Res Commun 287:562-567.
30. Kang JH, Lee YY, Yu BY, Yang BS, Cho KH, Yoon DK, Roh YK. 2005. Adiponectin induces growth arrest and apoptosis of MDA-MB-231 breast cancer cell. Arch Pharm Res 28:1263-1269.
31. Kato M, Watabe K, Tsujii M, Funahashi T, Shimomura I, Takehara T. 2014. Adiponectin inhibits murine pancreatic cancer growth. Dig Dis Sci 59:1192-1196.
32. Kelesidis I, Kelesidis T, Mantzoros CS. 2006. Adiponectin and cancer: A systematic review. Br J Cancer 94:1221-1225.
33. Kim AY, Lee YS, Kim KH, Lee JH, Lee HK, Jang SH, Kim SE, Lee GY, Lee JW, Jung SA, Chung HY, Jeong S, Kim JB. 2010. Adiponectin represses colon cancer cell proliferation via AdipoR1- and -R2-mediated AMPK activation. Mol Endocrinol (Baltimore, Md) 24:1441-1452.
34. Krishan S, Richardson DR, Sahni S. 2014. AMP kinase (PRKAA1). J Clin Pathol 67:758-763.
35. Landskroner-Eiger S, Qian B, Muise ES, Nawrocki AR, Berger JP, Fine EJ, Koba W, Deng Y, Pollard JW, Scherer PE. 2009. Proangiogenic contribution of adiponectin toward mammary tumor growth in vivo. Clin Cancer Res 15:3265-3276.
36. Lee MH, Klein RL, El-Shewy HM, Luttrell DK, Luttrell LM. 2008. The adiponectin receptors AdipoR1 and AdipoR2 activate ERK1/2 through a Src/Ras-dependent pathway and stimulate cell growth. Biochemistry 47:11682-11692.
37. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK, Bonni A. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987-1001.
38. Li XN, Song J, Zhang L, LeMaire SA, Hou X, Zhang C, Coselli JS, Chen L, Wang XL, Zhang Y, Shen YH. 2009. Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes 58:2246-2257.
39. Luo Z, Zang M, Guo W. 2010. AMPK as a metabolic tumor suppressor: Control of metabolism and cell growth. Future Oncol 6:457-470.
40. Massague J. 2004. G1 cell-cycle control and cancer. Nature 432:298-306.
41. 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(Pt 1):63-71.
42. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W, Bultsma Y, McBurney M, Guarente L. 2004. Mammalian SIRT1 represses forkhead transcription factors. Cell 116:551-563.
43. Nepal S, Kim MJ, Subedi A, Lee ES, Yong CS, Kim JA, Kang W, Kwak MK, Arya DS, Park PH. 2012. Globular adiponectin inhibits ethanol-induced apoptosis in HepG2 cells through heme oxygenase-1 induction. Biochem Pharmacol 84:974-983.
44. Nepal S, Park PH. 2013. Activation of autophagy by globular adiponectin attenuates ethanol-induced apoptosis in HepG2 cells: involvement of AMPK/FoxO3A axis. Biochim Biophys Acta 1833:2111-2125.
45. Ogunwobi OO, Beales IL. 2006. Adiponectin stimulates proliferation and cytokine secretion in colonic epithelial cells. Regul Pept 134:105-113.
46. Okoshi R, Ozaki T, Yamamoto H, Ando K, Koida N, Ono S, Koda T, Kamijo T, Nakagawara A, Kizaki H. 2008. Activation of AMP-activated protein kinase induces p53-dependent apoptotic cell death in response to energetic stress. J Biol Chem 283:3979-3987.
47. Ouchi N, Walsh K. 2007. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 380:24-30.
48. Pfeiler GH, Buechler C, Neumeier M, Schaffler A, Schmitz G, Ortmann O, Treeck O. 2008. Adiponectin effects on human breast cancer cells are dependent on 17-beta estradiol. Oncol Rep 19:787-793.
49. Queiroz EA, Puukila S, Eichler R, Sampaio SC, Forsyth HL, Lees SJ, Barbosa AM, Dekker RF, Fortes ZB, Khaper N. 2014. Metformin induces apoptosis and cell cycle arrest mediated by oxidative stress, AMPK and FOXO3a in MCF-7 breast cancer cells. PLoS ONE 9:e98207.
50. Salih DA, Brunet A. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20:126-136.
51. Saxena NK, Fu PP, Nagalingam A, Wang J, Handy J, Cohen C, Tighiouart M, Sharma D, Anania FA. 2010. Adiponectin modulates C-jun N-terminal kinase and mammalian target of rapamycin and inhibits hepatocellular carcinoma. Gastroenterology 139:1762-1773, 1773 e1761-1765.
52. Saxena NK, Sharma D. 2010. Metastasis suppression by adiponectin: LKB1 rises up to the challenge. Cell Adh Migr 4:358-362.
53. Schmidt M, Fernandez de Mattos S, van der Horst A, Klompmaker R, Kops GJ, Lam EW, Burgering BM, Medema RH. 2002. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 22:7842-7852.
54. Sherr CJ, Roberts JM. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512.
55. Swarbrick MM, Havel PJ. 2008. Physiological, pharmacological, and nutritional regulation of circulating adiponectin concentrations in humans. Metab Syndr Relat Disord 6:87-102.
56. Ungefroren H, Gieseler F, Fliedner S, Lehnert H. 2015. Obesity and cancer. Horm Mol Biol Clin Investig 21:5-15.
57. Vermeulen K, Van Bockstaele DR, Berneman ZN. 2003. The cell cycle: A review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 36:131-149.
58. Wang K, Li PF. 2010. Foxo3a regulates apoptosis by negatively targeting miR-21. J Biol Chem 285:16958-16966.
59. Wang Y, Lam JB, Lam KS, Liu J, Lam MC, Hoo RL, Wu D, Cooper GJ, Xu A. 2006. Adiponectin modulates the glycogen synthase kinase-3beta/beta-catenin signaling pathway and attenuates mammary tumorigenesis of MDA-MB-231 cells in nude mice. Cancer Res 66:11462-11470.
60. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. 2002. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8:1288-1295.
61. Yang JY, Xia W, Hu MC. 2006. Ionizing radiation activates expression of FOXO3a, Fas ligand, and Bim, and induces cell apoptosis. Int J Oncol 29:643-648.
62. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, Lang JY, Lai CC, Chang CJ, Huang WC, Huang H, Kuo HP, Lee DF, Li LY, Lien HC, Cheng X, Chang KJ, Hsiao CD, Tsai FJ, Tsai CH, Sahin AA, Muller WJ, Mills GB, Yu D, Hortobagyi GN, Hung MC. 2008. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10:138-148.
63. Yokota T, Oritani K, Takahashi I, Ishikawa J, Matsuyama A, Ouchi N, Kihara S, Funahashi T, Tenner AJ, Tomiyama Y, Matsuzawa Y. 2000. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 96:1723-1732.
64. Zhang X, Gan L, Pan H, Guo S, He X, Olson ST, Mesecar A, Adam S, Unterman TG. 2002. Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J Biol Chem 277:45276-45284.
65. Zhang X, Tang N, Hadden TJ, Rishi AK. 2011. Akt, FoxO and regulation of apoptosis. Biochim Biophys Acta 1813:1978-1986.
66. Zhao Y, Wang Y, Zhu WG. 2011. Applications of post-translational modifications of FoxO family proteins in biological functions. J Mol Cell Biol 3:276-282.
67. 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. J Mol Signal 3:18.