Adiponectin represses colon cancer cell proliferation via AdipoR1- and -R2-mediated AMPK activation

Molecular Endocrinology

Volumn 24, Issue 7, 2010, Pages 1441-1452

  Kim, A Young ^a   Lee, Yun Sok ^a   Kim, Kang Ho ^a   Lee, Jae Ho ^a   Lee, Hee Kyu ^b   Jang, Su Hwa ^c   Kim, Seong Eun ^d   Lee, Gha Young ^a   Lee, Joo Won ^a   Jung, Sung Ae ^d   Chung, Hee Yong ^c   Jeong, Sunjoo ^b   Kim, Jae Bum ^a  

^a Seoul National University   (South Korea)

^b Dankook University   (South Korea)

^c Hanyang University College of Medicine   (South Korea)

^d Ewha Womans University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ADIPOCYTOKINE; ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; PROTEIN P21; PROTEIN P27; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; ADIPONECTIN RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ARTICLE; CANCER INHIBITION; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; APOPTOSIS; CELL CYCLE; CHO CELL LINE; COLONIC NEOPLASMS; CRICETULUS; DRUG EFFECTS; GENETICS; HAMSTER; HCT116 CELL LINE; HT 29 CELL LINE; METABOLISM; POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CHO CELLS; COLONIC NEOPLASMS; CRICETINAE; CRICETULUS; HCT116 CELLS; HT29 CELLS; HUMANS; POLYMERASE CHAIN REACTION; RECEPTORS, ADIPONECTIN;

EID: 77954828973     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2009-0498     Document Type: Article

References (62)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ 2008 Cancer statistics, 2008. CA Cancer J Clin 58:71-96
2. Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, Flanders WD, Rodriguez C, Sinha R, Calle EE 2005 Meat consumption and risk of colorectal cancer. JAMA 293:172-182 (Pubitemid 40095868)
3. Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P 1995 Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269:546-549
4. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE 2001 The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 7:947-953
5. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF 2001 Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98:2005-2010
6. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF 1995 A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270:26746-26749
7. Hu E, Liang P, Spiegelman BM 1996 AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 271:10697-10703
8. 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
9. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T 2003 Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423:762-769
10. 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
11. Kubota N, Yano W, Kubota T, Yamauchi T, Itoh S, Kumagai H, Kozono H, Takamoto I, Okamoto S, Shiuchi T, Suzuki R, Satoh H, Tsuchida A, Moroi M, Sugi K, Noda T, Ebinuma H, Ueta Y, Kondo T, Araki E, Ezaki O, Nagai R, Tobe K, Terauchi Y, Ueki K, Minokoshi Y, Kadowaki T 2007 Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab 6:55-68
12. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, Tsuchida A, Kumagai K, Kozono H, Hada Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Awazawa M, Takamoto I, Froguel P, Hara K, Tobe K, Nagai R, Ueki K, Kadowaki T 2007 Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 13:332-339
13. Chen DC, Chung YF, Yeh YT, Chaung HC, Kuo FC, Fu OY, Chen HY, Hou MF, Yuan SS 2006 Serum adiponectin and leptin levels in Taiwanese breast cancer patients. Cancer Lett 237:109-114
14. Goktas S, Yilmaz MI, Caglar K, Sonmez A, Kilic S, Bedir S 2005 Prostate cancer and adiponectin. Urology 65:1168-1172
15. Petridou E, Mantzoros C, Dessypris N, Koukoulomatis P, Addy C, Voulgaris Z, Chrousos G, Trichopoulos D 2003 Plasma adiponectin concentrations in relation to endometrial cancer: a case-control study in Greece. J Clin Endocrinol Metab 88:993-997
16. Ishikawa M, Kitayama J, Kazama S, Hiramatsu T, Hatano K, Nagawa H 2005 Plasma adiponectin and gastric cancer. Clin Cancer Res 11:466-472
17. Kaklamani VG, Sadim M, Hsi A, Offit K, Oddoux C, Ostrer H, Ahsan H, Pasche B, Mantzoros C 2008 Variants of the adiponectin and adiponectin receptor 1 genes and breast cancer risk. Cancer Res 68:3178-3184
18. 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
19. 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-3β/β-catenin signaling pathway and attenuates mammary tumorigenesis of MDA-MB-231 cells in nude mice. Cancer Res 66:11462-11470 (Pubitemid 46009979)
20. 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
21. Bub JD, Miyazaki T, Iwamoto Y 2006 Adiponectin as a growth inhibitor in prostate cancer cells. Biochem Biophys Res Commun 340:1158-1166
22. 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 (Pubitemid 350074060)
23. Ishikawa M, Kitayama J, Yamauchi T, Kadowaki T, Maki T, Miyato H, Yamashita H, Nagawa H 2007 Adiponectin inhibits the growth and peritoneal metastasis of gastric cancer through its specific membrane receptors AdipoR1 and AdipoR2. Cancer Sci 98: 1120-1127
24. Wei EK, Giovannucci E, Fuchs CS, Willett WC, Mantzoros CS 2005 Low plasma adiponectin levels and risk of colorectal cancer in men: a prospective study. J Natl Cancer Inst 97:1688-1694
25. Fukumoto J, Otake T, Tajima O, Tabata S, Abe H, Mizoue T, Ohnaka K, Kono S 2008 Adiponectin and colorectal adenomas: Self Defense Forces Health Study. Cancer Sci 99:781-786 (Pubitemid 351448083)
26. Otake S, Takeda H, Suzuki Y, Fukui T, Watanabe S, Ishihama K, Saito T, Togashi H, Nakamura T, Matsuzawa Y, Kawata S 2005 Association of visceral fat accumulation and plasma adiponectin with colorectal adenoma: evidence for participation of insulin resistance. Clin Cancer Res 11:3642-3646
27. Erarslan E, Turkay C, Koktener A, Koca C, Uz B, Bavbek N 2009 Association of visceral fat accumulation and adiponectin levels with colorectal neoplasia. Dig Dis Sci 54:862-868
28. Kaklamani VG, Wisinski KB, Sadim M, Gulden C, Do A, Offit K, Baron JA, Ahsan H, Mantzoros C, Pasche B 2008 Variants of the adiponectin (ADIPOQ) and adiponectin receptor 1 (ADIPOR1) genes and colorectal cancer risk. JAMA 300:1523-1531
29. Fujisawa T, Endo H, Tomimoto A, Sugiyama M, Takahashi H, Saito S, Inamori M, Nakajima N, Watanabe M, Kubota N, Yamauchi T, Kadowaki T, Wada K, Nakagama H, Nakajima A 2008 Adiponectin suppresses colorectal carcinogenesis under the high-fat diet condition. Gut 57:1531-1538
30. Nishihara T, Baba M, Matsuda M, Inoue M, Nishizawa Y, Fukuhara A, Araki H, Kihara S, Funahashi T, Tamura S, Hayashi N, Iishi H, Shimomura I 2008 Adiponectin deficiency enhances colorectal carcinogenesis and liver tumor formation induced by azoxymethane in mice. World J Gastroenterol 14:6473-6480
31. Yang YA, Morin PJ, Han WF, Chen T, Bornman DM, Gabrielson EW, Pizer ES 2003 Regulation of fatty acid synthase expression in breast cancer by sterol regulatory element binding protein-1c. Exp Cell Res 282:132-137
32. Chuu CP, Hiipakka RA, Kokontis JM, Fukuchi J, Chen RY, Liao S 2006 Inhibition of tumor growth and progression of LNCaP prostate cancer cells in athymic mice by androgen and liver X receptor agonist. Cancer Res 66:6482-6486
33. Li JN, Mahmoud MA, Han WF, Ripple M, Pizer ES 2000 Sterol regulatory element-binding protein-1 participates in the regulation of fatty acid synthase expression in colorectal neoplasia. Exp Cell Res 261:159-165
34. Alo' PL, Visca P, Marci A, Mangoni A, Botti C, Di Tondo U 1996 Expression of fatty acid synthase (FAS) as a predictor of recurrence in stage I breast carcinoma patients. Cancer 77:474-482
35. Epstein JI, Carmichael M, Partin AW 1995 OA-519 (fatty acid synthase) as an independent predictor of pathologic state in adenocarcinoma of the prostate. Urology 45:81-86
36. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE 2001 Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108:1167-1174
37. Salt IP, Johnson G, Ashcroft SJ, Hardie DG 1998 AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic β cells, and may regulate insulin release. Biochem J 335 (Pt 3):533-539 (Pubitemid 28515405)
38. Carlson CL, Winder WW 1999 Liver AMP-activated protein kinase and acetyl-CoA carboxylase during and after exercise. J Appl Physiol 86:669-674
39. Rattan R, Giri S, Singh AK, Singh I 2005 5-Aminoimidazole-4-carboxamide- 1-β-D-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase. J Biol Chem 280:39582-39593
40. Xiang X, Saha AK, Wen R, Ruderman NB, Luo Z 2004 AMP-activated protein kinase activators can inhibit the growth of prostate cancer cells by multiple mechanisms. Biochem Biophys Res Commun 321:161-167 (Pubitemid 39055618)
41. 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-β-D-ribofuranoside, in a human hepatocellular carcinoma cell line. Biochem Biophys Res Commun 287:562-567
42. Sugiyama M, Takahashi H, Hosono K, Endo H, Kato S, Yoneda K, Nozaki Y, Fujita K, Yoneda M, Wada K, Nakagama H, Nakajima A 2009 Adiponectin inhibits colorectal cancer cell growth through the AMPK/mTOR pathway. Int J Oncol 34:339-344
43. Jackowski S, Wang J, Baburina I 2000 Activity of the phosphatidylcholine biosynthetic pathway modulates the distribution of fatty acids into glycerolipids in proliferating cells. Biochim Biophys Acta 1483:301-315
44. Pizer ES, Lax SF, Kuhajda FP, Pasternack GR, Kurman RJ 1998 Fatty acid synthase expression in endometrial carcinoma: correlation with cell proliferation and hormone receptors. Cancer 83:528-537
45. Rashid A, Pizer ES, Moga M, Milgraum LZ, Zahurak M, Pasternack GR, Kuhajda FP, Hamilton SR 1997 Elevated expression of fatty acid synthase and fatty acid synthetic activity in colorectal neoplasia. Am J Pathol 150:201-208
46. Pizer ES, Wood FD, Heine HS, Romantsev FE, Pasternack GR, Kuhajda FP 1996 Inhibition of fatty acid synthesis delays disease progression in a xenograft model of ovarian cancer. Cancer Res 56:1189-1193
47. Pizer ES, Wood FD, Pasternack GR, Kuhajda FP 1996 Fatty acid synthase (FAS): a target for cytotoxic antimetabolites in HL60 promyelocytic leukemia cells. Cancer Res 56:745-751
48. Furuya Y, Akimoto S, Yasuda K, Ito H 1997 Apoptosis of androgen-independent prostate cell line induced by inhibition of fatty acid synthesis. Anticancer Res 17:4589-4593 (Pubitemid 28081749)
49. Kim JB, Sarraf P, Wright M, Yao KM, Mueller E, Solanes G, Lowell BB, Spiegelman BM 1998 Nutritional and insulin regulation of fatty acid synthetase and leptin gene expression through ADD1/SREBP1. J Clin Invest 101:1-9
50. Lopez JM, Bennett MK, Sanchez HB, Rosenfeld JM, Osborne TF 1996 Sterol regulation of acetyl coenzyme A carboxylase: a mechanism for coordinate control of cellular lipid. Proc Natl Acad Sci USA 93:1049-1053
51. Tabor DE, Kim JB, Spiegelman BM, Edwards PA 1998 Transcriptional activation of the stearoyl-CoA desaturase 2 gene by sterol regulatory element-binding protein/adipocyte determination and differentiation factor 1. J Biol Chem 273:22052-22058
52. Shklyaev S, Aslanidi G, Tennant M, Prima V, Kohlbrenner E, Kroutov V, Campbell-Thompson M, Crawford J, Shek EW, Scarpace PJ, Zolotukhin S 2003 Sustained peripheral expression of transgene adiponectin offsets the development of diet-induced obesity in rats. Proc Natl Acad Sci USA 100:14217-14222
53. Viollet B, Guigas B, Leclerc J, Hebrard S, Lantier L, Mounier R, Andreelli F, Foretz M 2009 AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives. Acta Physiol (Oxf) 196:81-98
54. Williams CJ, Mitsiades N, Sozopoulos E, Hsi A, Wolk A, Nifli AP, Tseleni-Balafouta S, Mantzoros CS 2008 Adiponectin receptor expression is elevated in colorectal carcinomas but not in gastrointestinal stromal tumors. Endocr Relat Cancer 15:289-299
55. Lukanova A, Söderberg S, Kaaks R, Jellum E, Stattin P 2006 Serum adiponectin is not associated with risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 15:401-402
56. Ealey KN, Archer MC 2009 Elevated circulating adiponectin and elevated insulin sensitivity in adiponectin transgenic mice are not associated with reduced susceptibility to colon carcinogenesis. Int J Cancer 124:2226-2230
57. Kumor A, Daniel P, Pietruczuk M, Malecka-Panas E 2009 Serum leptin, adiponectin, and resistin concentration in colorectal adenoma and carcinoma (CC) patients. Int J Colorectal Dis 24:275-281
58. Pechlivanis S, Bermejo JL, Pardini B, Naccarati A, Vodickova L, Novotny J, Hemminki K, Vodicka P, Försti A 2009 Genetic variation in adipokine genes and risk of colorectal cancer. Eur J Endocrinol 160:933-940
59. Zakikhani M, Dowling RJ, Sonenberg N, Pollak MN 2008 The effects of adiponectin and metformin on prostate and colon neoplasia involve activation of AMP-activated protein kinase. Cancer Prev Res (Phila Pa) 1:369-375
60. Yoon MJ, Lee GY, Chung JJ, Ahn YH, Hong SH, Kim JB 2006 Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor α. Diabetes 55:2562-2570
61. Cifone MA, Fidler IJ 1980 Correlation of patterns of anchorage- independent growth with in vivo behavior of cells from a murine fibrosarcoma. Proc Natl Acad Sci USA 77:1039-1043
62. Lewis JD, Payton LA, Whitford JG, Byrne JA, Smith DI, Yang L, Bright RK 2007 Induction of tumorigenesis and metastasis by the murine orthologue of tumor protein D52. Mol Cancer Res 5:133-144 (Pubitemid 46423994)