Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells

Cancer Research

Volumn 67, Issue 6, 2007, Pages 2497-2507

  Saxena, Neeraj K ^a   Sharma, Dipali ^a   Ding, Xiaokun ^a   Lin, Songbai ^a   Marra, Fabio ^b   Merlin, Didier ^a   Anania, Frank A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; JANUS KINASE; LEPTIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECOMBINANT LEPTIN; STAT PROTEIN; STAT3 PROTEIN;

ARTICLE; CANCER GROWTH; CANCER INVASION; CARCINOMA CELL; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN HEPG2; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CARCINOMA, HEPATOCELLULAR; CELL CYCLE; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JANUS KINASES; LEPTIN; LIVER NEOPLASMS; MAP KINASE SIGNALING SYSTEM; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CELL SURFACE; STAT3 TRANSCRIPTION FACTOR;

EID: 34047250349     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3075     Document Type: Article

References (57)

1. Abu-Abid S, Szold A, Klausner J. Obesity and cancer. J Med 2002;33:73-86.
2. Calle EE, Rodriquez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348:1625-38.
3. Matsuzawa Y, Funahashi T, Nakamura T. Molecular mechanism of metabolic syndrome X: contribution of adipocytokines adipocyte-derived bioactive substances. Ann N Y Acad Sci 1999;892:146-54.
4. Rose DP, Komninou D, Stephenson GD. Obesity, adipocytokines, and insulin resistance in breast cancer. Obes Rev 2004;5:153-65.
5. MacDougald OA, Hwang CS, Fan H, Lane MD. Regulated expression of the obese gene product (leptin) in white adipose tissue and 3T3-L1 adipocytes. Proc Natl Acad Sci U S A 1995;92:9034-7.
6. Halaas JL, Gajiwala KS, Maffei M, et al. Weight reducing effects of the plasma protein encoded by the obese gene. Science 1995;269:543-6.
7. Huang L, Li C. Leptin: a multifunctional hormone. Cell Res 2000;10:81-92.
8. Bouloumie A, Drexler HC, Lafontan M, Busse R. Leptin, the product of Ob gene, promotes angiogenesis. Circ Res 1998;83:1059-66.
9. Sierra-Honigmann MR, Nath AK, Murakami C, et al. Biological action of leptin as an angiogenic factor. Science 1998;281:1683-6.
10. Somasunder P, McFadden DW, Hileman SM, Vona-Davis L. Leptin is a growth factor in cancer. J Surg Res 2004;116:337-49.
11. Houseknecht KL, Mantzoros CS, Kuliawat R, Hadro E, Flier JS, Kahn BB. Evidence for leptin binding to proteins in serum of rodents and humans: modulation with obesity. Diabetes 1996;45:1638-43.
12. Sinha MK, Opentanova I, Ohannesian JP, et al. Evidence of free and bound leptin in human circulation. Studies in lean and obese subjects and during short-term fasting. J Clin Invest 1996;98:1277-82.
13. Bjorbaek C, Uotani S, da Silva B, Flier JS. Divergent signaling capacities of the long and short isoforms of the leptin receptor. J Biol Chem 1997;272:32686-95.
14. Tartaglia LA. The leptin receptor. J Biol Chem 1997; 272:6093-6.
15. Ahima RS, Osei SY. Leptin signaling. Physiol Behav 2004;81:223-41.
16. Bahrenberg G, Behrmann I, Barthel A, et al. Identification of the critical sequence elements in the cytoplasmic domain of leptin receptor isoforms required for Janus kinase/signal transducer and activator of transcription activation by receptor heterodimers. Mol Endocrinol 2002;16:859-72.
17. Bjorbaek C, El-Haschimi K, Frantz JD, Flier JS. The role of SOCS-3 in leptin signaling and leptin resistance. J Biol Chem 1999;274:30059-65.
18. Emilsson V, Arch JR, de Groot RP, Lister CA, Cawthorne MA. Leptin treatment increases suppressors of cytokine signaling in central and peripheral tissues. FEBS Lett 1999;455:170-4.
19. Bjorbaek C, Elmquist JK, Frantz JD, Shoelson SE, Flier JS. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol Cell 1998;1:619-25.
20. Kaaks R, Lukanova A, Kurzer MS. Obesity, endogenous hormones and hepatocellular carcinoma risk: a systemic review. Cancer Epidemiol Biomarkers Prev 2002;11:1531-43.
21. Qian Y, Fan JG. Obesity, fatty liver and liver cancer. Hepatobiliary Pancreat Dis Int 2005;4:173-7.
22. Caldwell SH, Crespo DM, Kang HS, Al-Osaimi AM. Obesity and hepatocellular carcinoma. Gastroenterology 2004;127:S97-103.
23. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 2004;127:S27-34.
24. Regimbeau JM, Colombat M, Mognol P, et al. Obesity and diabetes as a risk factor for hepatocellular carcinoma. Liver Transpl 2004;10:S69-73.
25. Moller H, Mellemgaard A, Lindvig K, Olsen J. Obesity and cancer risk: a Danish record-linkage study. Eur J Cancer 1994;30A:344-50.
26. Nair S, Mason A, Eason J, Loss G, Perrillo RP. Is obesity an independent risk factor for hepatocellular carcinoma in cirrhosis? Hepatology 2002;36:150-5.
27. Petridou E, Belechri M, Dessypris N, et al. Leptin and body mass index in relation to hepatocellular carcinoma risk. Ann Nutr Metab 2002;46:147-51.
28. Aden DP, Fogel A, Plotkin S, Damjanov I, Knowles BB. Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 1979;282:615-6.
29. Nakabayashi H, Taketa K, Yamane T, et al. Phenotypical stability of a human hepatoma cell line, Huh7, in long-term culture with chemically defined medium. Jpn J Cancer Res 1984;75:151-8.
30. Sharma D, Saxena NK, Vertino PM, Anania FA. Leptin promotes the proliferative response and invasiveness in human endometrial cancer cells by activating multiple signal-transduction pathways. Endocr Relat Cancer 2006;13:629-40.
31. Saxena NK, Titus MA, Ding X, et al. Leptin as a novel profibrogenic cytokine in hepatic stellate cells: mitogenesis and inhibition of apoptosis mediated by extracellular regulated kinase (Erk) and Akt phosphorylation. FASEB J 2004;18:I612-4.
32. Keese CR, Bhawe K, Wegener J, Giaever I. Real-time impedance assay to follow the invasive activities of metastatic cells in culture. Biotechniques 2002;33: 842-50.
33. McLane MA, Zhang X, Tian J, et al. Scratching below the surface: wound healing and alanine mutagenesis provide unique insights into interactions between eristostatin, platelets and melanoma cells. Pathophysiol Haemost Thromb 2005;34:164-8.
34. Wegener J, Keese CR, Giaever I. Electric cell-substrate impedance sensing (ECIS) as a non invasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res 2000;259:158-66.
35. Driss A, Charrier L, Yan Y, Nduati V, Sitaraman S, Merlin D. Dystroglycan receptor is involved in integrin activation in intestinal epithelia. Am J Physiol Gastrointest Liver Physiol 2006;290:G1228-42.
36. Fu M, Wang C, Li Z, Sakamaki T, Pestell RG. CyclinD1: normal and abnormal functions. Endocrinol 2004;145:5439-47.
37. Ghaleb AM, Nandan MO, Chanchevalap S, Dalton WB, Hisamuddin IM, Yang VW. Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res 2005;15:92-6.
38. Tang ZY, Ye SL, Liu YK, et al. A decade's studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol 2004;130:187-96.
39. Yamaguchi H, Wyckoff J, Condeelis J. Cell migration in tumors. Curr Opin Cell Biol 2005;17:559-64.
40. Pai R, Lin C, Tran T, Tarnawski A. Leptin activates STAT and ERK2 pathways and induces gastric cancer cell proliferation. Biochem Biophys Res Commun 2005; 331:984-92.
41. Choi JH, Park SH, Leung PC, Choi KC. Expression of leptin receptors and potential effects of leptin on the cell growth and activation of mitogen-activated protein kinases in ovarian cancer cells. J Clin Endocrinol Metab 2005;90:207-10.
42. Somasundar P, Frankenberry KA, Skinner H, et al. Prostate cancer cell proliferation is influenced by leptin. J Surg Res 2004;118:71-82.
43. Somasundar P, Yu AK, Vona-Davis L, McFadden DW. Differential effects of leptin on cancer in vitro. J Surg Res 2003;113:50-5.
44. Elinav E, Abd-Elnabi A, Pappo O, et al. Suppression of hepatocellular carcinoma growth in mice via leptin, is associated with inhibition of tumor cell growth and natural killer cell activation. J Hepatol 2006;44:529-36.
45. Wang S-N, Yeh Y-T, Yang S-F, Chai C-Y, Lee K-T. Potential role of leptin expression in hepatocellular carcinoma. J Clin Pathol 2006;59:930-4.
46. Kitade M, Yoshiji H, Kojima H, et al. Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology 2006;44: 983-91.
47. Sebolt-Leopold JS. MEK inhibitors: a therapeutic approach to targeting the Ras-MAP kinase pathway in tumors. Curr Pharm Des 2004;10:1907-14.
48. Panka DJ, Atkins MB, Mier JW. Targeting the mitogen-activated protein kinase pathway in the treatment of malignant melanoma. Clin Cancer Res 2006;12:2371-5.
49. Franke T, Kaplan D, Cantley L. PI3K: downstream AKT blocks apoptosis. Cell 1997;88:435-7.
50. Toker A, Yoeli-Lerner M. Akt signaling and cancer: surviving but not moving on. Cancer Res 2006;66: 3963-6.
51. Su JD, Mayo LD, Donner DB, Durden DL. PTEN and phosphatidylinositol 3′-kinase inhibitors up-regulate p53 and block tumor-induced angiogenesis: evidence for an effect on the tumor and endothelial compartment. Cancer Res 2003;63:3585-92.
52. Hu L, Zaloudek C, Mills GB, Gray J, Jaffe RB. In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3′-kinase inhibitor (LY294002). Clin Cancer Res 2000;6:880-6.
53. Jin X, Gossett DR, Wang S, et al. Inhibition of AKT survival pathway by a small molecule inhibitor in human hepatocellular carcinoma cells. Br J Cancer 2004;91:1808-12.
54. Meydan N, Grunberger T, Dadi H, et al. Inhibition of acute lymphoblastic leukaema by a Jak-2 inhibitor. Nature 1996;379:645-8.
55. Catlett-Falcone R, Landowski TH, Oshiro MM, et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999;10:105-15.
56. Grandis JR, Drenning SD, Chakraborty A, et al. Requirement of Stat3 but not StatI activation for epidermal growth factor receptor-mediated cell growth in vitro. J Clin Invest 1998;102:1385-92.
57. Song H, Wang R, Wang S, Lin J. A low-molecular-weight compound discovered through virtual database screening inhibits Stat3 function in breast cancer cells. Proc Natl Acad Sci U S A 2005;102:4700-5.