Molecular Pathways: Adiponectin and Leptin Signaling in Cancer

Clinical Cancer Research - Tập 19 Số 8 - Trang 1926-1932 - 2013
Michael N. VanSaun1
1Author's Affiliation: Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee

Tóm tắt

Abstract

The increasing percentage of obese individuals in the population and its independent association of increased risk for the development of cancer have heightened the necessity to understand the molecular mechanisms that underlie this connection. The deregulation of adipokines in the setting of obesity and their impact on cancer progression and metastasis is one such area of research. Adipokines are bioactive proteins that mediate metabolism, inflammation, angiogenesis, and proliferation. Altered levels of adipokines or their cognate receptors in cancers can ultimately lead to an imbalance in downstream molecular pathways. Discovery of adipokine receptors in various cancers has highlighted the potential for novel therapeutic targets. Leptin and adiponectin represent two adipokines that elicit generally opposing molecular effects. Epidemiologic studies have highlighted associations between increased serum leptin levels and increased tumor growth, whereas adiponectin exhibits an inverse correlation with cancer development. This review addresses the current level of understanding of molecular pathways activated by adiponectin and leptin to identify the areas of intervention and facilitate advancement in the field. Clin Cancer Res; 19(8); 1926–32. ©2013 AACR.

Từ khóa


Tài liệu tham khảo

Bjorbaek, 2004, Leptin signaling in the central nervous system and the periphery, Recent Prog Horm Res, 59, 305, 10.1210/rp.59.1.305

Considine, 1996, Serum immunoreactive-leptin concentrations in normal-weight and obese humans, N Engl J Med, 334, 292, 10.1056/NEJM199602013340503

Ceddia, 2005, Direct metabolic regulation in skeletal muscle and fat tissue by leptin: implications for glucose and fatty acids homeostasis, Int J Obes (Lond), 29, 1175, 10.1038/sj.ijo.0803025

Martin, 2008, Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease, J Am Coll Cardiol, 52, 1201, 10.1016/j.jacc.2008.05.060

St-Pierre, 2012, Modulation of leptin resistance by protein tyrosine phosphatases, Cell Metab, 15, 292, 10.1016/j.cmet.2012.02.004

Kadowaki, 2005, Adiponectin and adiponectin receptors, Endocr Rev, 26, 439, 10.1210/er.2005-0005

Waki, 2005, Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1, Endocrinology, 146, 790, 10.1210/en.2004-1096

Arita, 1999, Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity, Biochem Biophys Res Commun, 257, 79, 10.1006/bbrc.1999.0255

Weyer, 2001, Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia, J Clin Endocrinol Metab, 86, 1930, 10.1210/jcem.86.5.7463

Yamauchi, 2003, Cloning of adiponectin receptors that mediate antidiabetic metabolic effects, Nature, 423, 762, 10.1038/nature01705

Bjursell, 2007, Opposing effects of adiponectin receptors 1 and 2 on energy metabolism, Diabetes, 56, 583, 10.2337/db06-1432

Yamauchi, 2007, Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions, Nat Med, 13, 332, 10.1038/nm1557

Kim, 2010, Adiponectin represses colon cancer cell proliferation via AdipoR1- and -R2-mediated AMPK activation, Mol Endocrinol, 24, 1441, 10.1210/me.2009-0498

Man, 2010, Suppression of liver tumor growth and metastasis by adiponectin in nude mice through inhibition of tumor angiogenesis and downregulation of Rho kinase/IFN-inducible protein 10/matrix metalloproteinase 9 signaling, Clin Cancer Res, 16, 967, 10.1158/1078-0432.CCR-09-1487

Wang, 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, 10.1158/0008-5472.CAN-06-1969

Ishikawa, 2007, Adiponectin inhibits the growth and peritoneal metastasis of gastric cancer through its specific membrane receptors AdipoR1 and AdipoR2, Cancer Sci, 98, 1120, 10.1111/j.1349-7006.2007.00486.x

Chiu, 2009, Involvement of AdipoR receptor in adiponectin-induced motility and alpha2beta1 integrin upregulation in human chondrosarcoma cells, Carcinogenesis, 30, 1651, 10.1093/carcin/bgp156

Han, 2012, Leptin promotes human glioblastoma growth through activating Signal Transducers and Activators of Transcription 3 signaling, Brain Res Bull, 87, 274, 10.1016/j.brainresbull.2011.11.007

Liu, 2011, Leptin activates STAT3 and ERK1/2 pathways and induces endometrial cancer cell proliferation, J Huazhong Univ Sci Technolog Med Sci, 31, 365, 10.1007/s11596-011-0382-7

Endo, 2011, Leptin acts as a growth factor for colorectal tumours at stages subsequent to tumour initiation in murine colon carcinogenesis, Gut, 60, 1363, 10.1136/gut.2010.235754

Saxena, 2007, Leptin-induced growth stimulation of breast cancer cells involves recruitment of histone acetyltransferases and mediator complex to CYCLIN D1 promoter via activation of Stat3, J Biol Chem, 282, 13316, 10.1074/jbc.M609798200

Knight, 2011, Survivin upregulation, dependent on leptin-EGFR-Notch1 axis, is essential for leptin-induced migration of breast carcinoma cells, Endocr Relat Cancer, 18, 413, 10.1530/ERC-11-0075

Yeh, 2009, Leptin induces migration and invasion of glioma cells through MMP-13 production, Glia, 57, 454, 10.1002/glia.20773

Fava, 2008, Leptin enhances cholangiocarcinoma cell growth, Cancer Res, 68, 6752, 10.1158/0008-5472.CAN-07-6682

Saxena, 2007, 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 Res, 67, 2497, 10.1158/0008-5472.CAN-06-3075

Birmingham, 2009, Novel mechanism for obesity-induced colon cancer progression, Carcinogenesis, 30, 690, 10.1093/carcin/bgp041

Cleary, 2009, Targeting the adiponectin:leptin ratio for postmenopausal breast cancer prevention, Front Biosci (Schol Ed), 1, 329, 10.2741/s30

Bjorbaek, 1997, Divergent signaling capacities of the long and short isoforms of the leptin receptor, J Biol Chem, 272, 32686, 10.1074/jbc.272.51.32686

Hekerman, 2005, Pleiotropy of leptin receptor signalling is defined by distinct roles of the intracellular tyrosines, FEBS J, 272, 109, 10.1111/j.1432-1033.2004.04391.x

Murakami, 1997, A short form of leptin receptor performs signal transduction, Biochem Biophys Res Commun, 231, 26, 10.1006/bbrc.1996.6030

Zhang, 2009, The soluble leptin receptor neutralizes leptin-mediated STAT3 signalling and anorexic responses in vivo, Br J Pharmacol, 158, 475, 10.1111/j.1476-5381.2009.00246.x

Montoye, 2006, Analysis of leptin signalling in hematopoietic cells using an adapted MAPPIT strategy, FEBS Lett, 580, 3301, 10.1016/j.febslet.2006.04.094

Shi, 2000, Molecular mechanism for the Shp-2 tyrosine phosphatase function in promoting growth factor stimulation of Erk activity, Mol Cell Biol, 20, 1526, 10.1128/MCB.20.5.1526-1536.2000

Bjorbaek, 2001, Divergent roles of SHP-2 in ERK activation by leptin receptors, J Biol Chem, 276, 4747, 10.1074/jbc.M007439200

Ling, 2005, DOK1 mediates SHP-2 binding to the alphaVbeta3 integrin and thereby regulates insulin-like growth factor I signaling in cultured vascular smooth muscle cells, J Biol Chem, 280, 3151, 10.1074/jbc.M411035200

Knobelspies, 2010, Mechanism of attenuation of leptin signaling under chronic ligand stimulation, BMC Biochem, 11, 2, 10.1186/1471-2091-11-2

Dunn, 2005, Feedback inhibition of leptin receptor/Jak2 signaling via Tyr1138 of the leptin receptor and suppressor of cytokine signaling 3, Mol Endocrinol, 19, 925, 10.1210/me.2004-0353

Handy, 2011, Adiponectin inhibits leptin signalling via multiple mechanisms to exert protective effects against hepatic fibrosis, Biochem J, 440, 385, 10.1042/BJ20102148

Mao, 2006, APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function, Nat Cell Biol, 8, 516, 10.1038/ncb1404

Gwinn, 2008, AMPK phosphorylation of raptor mediates a metabolic checkpoint, Mol Cell, 30, 214, 10.1016/j.molcel.2008.03.003

Lee, 2012, AMPK promotes p53 acetylation via phosphorylation and inactivation of SIRT1 in liver cancer cells, Cancer Res, 72, 4394, 10.1158/0008-5472.CAN-12-0429

Kim, 2009, Adiponectin-activated AMPK stimulates dephosphorylation of AKT through protein phosphatase 2A activation, Cancer Res, 69, 4018, 10.1158/0008-5472.CAN-08-2641

Barb, 2007, Adiponectin signals in prostate cancer cells through Akt to activate the mammalian target of rapamycin pathway, Endocr Relat Cancer, 14, 995, 10.1677/ERC-06-0091

Uddin, 2009, Overexpression of leptin receptor predicts an unfavorable outcome in Middle Eastern ovarian cancer, Mol Cancer, 8, 74, 10.1186/1476-4598-8-74

Ishikawa, 2004, Enhanced expression of leptin and leptin receptor (OB-R) in human breast cancer, Clin Cancer Res, 10, 4325, 10.1158/1078-0432.CCR-03-0749

Cleary, 2004, Leptin receptor-deficient MMTV-TGF-alpha/Lepr(db)Lepr(db) female mice do not develop oncogene-induced mammary tumors, Exp Biol Med (Maywood), 229, 182, 10.1177/153537020422900207

Xue, 2012, Lentivirus-mediated RNA interference targeting the ObR gene in human breast cancer MCF-7 cells in a nude mouse xenograft model, Chin Med J (Engl), 125, 1563

Yang, 2009, Leptin enhances cell migration in human chondrosarcoma cells through OBRl leptin receptor, Carcinogenesis, 30, 566, 10.1093/carcin/bgp023

Zyromski, 2009, Obesity potentiates the growth and dissemination of pancreatic cancer, Surgery, 146, 258, 10.1016/j.surg.2009.02.024

Nyante, 2011, Common genetic variation in adiponectin, leptin, and leptin receptor and association with breast cancer subtypes, Breast Cancer Res Treat, 129, 593, 10.1007/s10549-011-1517-z

Sadik, 2012, The significance of serum levels of adiponectin, leptin, and hyaluronic acid in hepatocellular carcinoma of cirrhotic and noncirrhotic patients, Hum Exp Toxicol, 31, 311, 10.1177/0960327111431091

Arisan, 2009, Serum adipocytokine levels in prostate cancer patients, Urol Int, 82, 203, 10.1159/000200801

Aliustaoglu, 2010, Preoperative serum leptin levels in patients with breast cancer, Med Oncol, 27, 388, 10.1007/s12032-009-9222-z

Mantovani, 2000, Serum levels of leptin and proinflammatory cytokines in patients with advanced-stage cancer at different sites, J Mol Med (Berl), 78, 554, 10.1007/s001090000137

Miyoshi, 2006, High expression of leptin receptor mRNA in breast cancer tissue predicts poor prognosis for patients with high, but not low, serum leptin levels, Int J Cancer, 118, 1414, 10.1002/ijc.21543

Dalamaga, 2009, Pancreatic cancer expresses adiponectin receptors and is associated with hypoleptinemia and hyperadiponectinemia: a case-control study, Cancer Causes Control, 20, 625, 10.1007/s10552-008-9273-z

Dalbec, 2010, Adipokines and cytokines in human pancreatic juice: unraveling the local pancreatic inflammatory milieu, Dig Dis Sci, 55, 2108, 10.1007/s10620-009-0977-z

Salageanu, 2010, Serum levels of adipokines resistin and leptin in patients with colon cancer, J Med Life, 3, 416

Bolukbas, 2004, Serum leptin concentration and advanced gastrointestinal cancers: a case controlled study, BMC Cancer, 4, 29, 10.1186/1471-2407-4-29

Vona-Davis, 2007, Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression, Endocr Relat Cancer, 14, 189, 10.1677/ERC-06-0068

Mathur, 2009, Pancreatic steatosis promotes dissemination and lethality of pancreatic cancer, J Am Coll Surg, 208, 989, 10.1016/j.jamcollsurg.2008.12.026

White, 2010, Insulin, leptin, and tumoral adipocytes promote murine pancreatic cancer growth, J Gastrointest Surg, 14, 1888, 10.1007/s11605-010-1349-x

Ferla, 2011, Glioblastoma-derived leptin induces tube formation and growth of endothelial cells: comparison with VEGF effects, BMC Cancer, 11, 303, 10.1186/1471-2407-11-303

Nejati-Koshki, 2012, Inhibition of leptin gene expression and secretion by silibinin: possible role of estrogen receptors, Cytotechnology, 64, 719, 10.1007/s10616-012-9452-3

Barb, 2007, Adiponectin in relation to malignancies: a review of existing basic research and clinical evidence, Am J Clin Nutr, 86, s858, 10.1093/ajcn/86.3.858S

Kaklamani, 2008, Variants of the adiponectin (ADIPOQ) and adiponectin receptor 1 (ADIPOR1) genes and colorectal cancer risk, JAMA, 300, 1523, 10.1001/jama.300.13.1523

Kaklamani, 2008, Variants of the adiponectin and adiponectin receptor 1 genes and breast cancer risk, Cancer Res, 68, 3178, 10.1158/0008-5472.CAN-08-0533

Kaklamani, 2011, Polymorphisms of ADIPOQ and ADIPOR1 and prostate cancer risk, Metabolism, 60, 1234, 10.1016/j.metabol.2011.01.005

Kamada, 2007, Hypoadiponectinemia accelerates hepatic tumor formation in a nonalcoholic steatohepatitis mouse model, J Hepatol, 47, 556, 10.1016/j.jhep.2007.03.020

Fujisawa, 2008, Adiponectin suppresses colorectal carcinogenesis under the high-fat diet condition, Gut, 57, 1531, 10.1136/gut.2008.159293

Landskroner-Eiger, 2009, Proangiogenic contribution of adiponectin toward mammary tumor growth in vivo, Clin Cancer Res, 15, 3265, 10.1158/1078-0432.CCR-08-2649

Denzel, 2009, Adiponectin deficiency limits tumor vascularization in the MMTV-PyV-mT mouse model of mammary cancer, Clin Cancer Res, 15, 3256, 10.1158/1078-0432.CCR-08-2661

Drew, 2007, Insulin, leptin, and adiponectin receptors in colon: regulation relative to differing body adiposity independent of diet and in response to dimethylhydrazine, Am J Physiol Gastrointest Liver Physiol, 293, G682, 10.1152/ajpgi.00231.2007

Mistry, 2006, The regulation of adiponectin receptors in human prostate cancer cell lines, Biochem Biophys Res Commun, 348, 832, 10.1016/j.bbrc.2006.07.139

Takahata, 2007, Demonstration of adiponectin receptors 1 and 2 mRNA expression in human breast cancer cells, Cancer Lett, 250, 229, 10.1016/j.canlet.2006.10.006

Barresi, 2009, The expression of adiponectin receptors Adipo-R1 and Adipo-R2 is associated with an intestinal histotype and longer survival in gastric carcinoma, J Clin Pathol, 62, 705, 10.1136/jcp.2009.066175

Crimmins, 2007, Polymorphisms in adiponectin receptor genes ADIPOR1 and ADIPOR2 and insulin resistance, Obes Rev, 8, 419, 10.1111/j.1467-789X.2007.00348.x

Amjadi, 2011, Leptin promotes melanoma tumor growth in mice related to increasing circulating endothelial progenitor cells numbers and plasma NO production, J Exp Clin Cancer Res, 30, 21, 10.1186/1756-9966-30-21

Otvos, 2011, Efficacy of a leptin receptor antagonist peptide in a mouse model of triple-negative breast cancer, Eur J Cancer, 47, 1578, 10.1016/j.ejca.2011.01.018

Gonzalez, 2006, Leptin signaling promotes the growth of mammary tumors and increases the expression of vascular endothelial growth factor (VEGF) and its receptor type two (VEGF-R2), J Biol Chem, 281, 26320, 10.1074/jbc.M601991200

Zastrow, 2003, The soluble leptin receptor is crucial for leptin action: evidence from clinical and experimental data, Int J Obes Relat Metab Disord, 27, 1472, 10.1038/sj.ijo.0802432

Chen, 2006, Induction of leptin resistance through direct interaction of C-reactive protein with leptin, Nat Med, 12, 425, 10.1038/nm1372

Otani, 2010, Adiponectin suppresses tumorigenesis in Apc(Min)(/+) mice, Cancer Lett, 288, 177, 10.1016/j.canlet.2009.06.037

Choi, 2005, Effect of PPAR-alpha and -gamma agonist on the expression of visfatin, adiponectin, and TNF-alpha in visceral fat of OLETF rats, Biochem Biophys Res Commun, 336, 747, 10.1016/j.bbrc.2005.08.203

Chinetti, 2004, Expression of adiponectin receptors in human macrophages and regulation by agonists of the nuclear receptors PPARalpha, PPARgamma, and LXR, Biochem Biophys Res Commun, 314, 151, 10.1016/j.bbrc.2003.12.058

O'Leary, 2007, Enhanced adiponectin multimer ratio and skeletal muscle adiponectin receptor expression following exercise training and diet in older insulin-resistant adults, Am J Physiol Endocrinol Metab, 293, E421, 10.1152/ajpendo.00123.2007

Mittendorfer, 2011, Recombinant human leptin treatment does not improve insulin action in obese subjects with type 2 diabetes, Diabetes, 60, 1474, 10.2337/db10-1302

Aljada, 2012, Metformin and neoplasia: implications and indications, Pharmacol Ther, 133, 108, 10.1016/j.pharmthera.2011.09.004

Currie, 2012, Mortality after incident cancer in people with and without type 2 diabetes: impact of metformin on survival, Diabetes Care, 35, 299, 10.2337/dc11-1313

He, 2012, Metformin and thiazolidinediones are associated with improved breast cancer-specific survival of diabetic women with HER2+ breast cancer, Ann Oncol, 23, 1771, 10.1093/annonc/mdr534

He, 2011, Thiazolidinediones and metformin associated with improved survival of diabetic prostate cancer patients, Ann Oncol, 22, 2640, 10.1093/annonc/mdr020

Bodles, 2006, Pioglitazone increases secretion of high-molecular-weight adiponectin from adipocytes, Am J Physiol Endocrinol Metab, 291, E1100, 10.1152/ajpendo.00187.2006

Colmers, 2012, Thiazolidinedione use and cancer incidence in type 2 diabetes: a systematic review and meta-analysis, Diabetes Metab, 38, 475, 10.1016/j.diabet.2012.06.003

Koh, 2005, Beneficial effects of fenofibrate to improve endothelial dysfunction and raise adiponectin levels in patients with primary hypertriglyceridemia, Diabetes Care, 28, 1419, 10.2337/diacare.28.6.1419

Jing, 2005, Targeting Stat3 in cancer therapy, Anticancer Drugs, 16, 601, 10.1097/00001813-200507000-00002

Yap, 2008, Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises, Curr Opin Pharmacol, 8, 393, 10.1016/j.coph.2008.08.004

Kim, 2012, Novel small molecule Raf kinase inhibitors for targeted cancer therapeutics, Arch Pharm Res, 35, 605, 10.1007/s12272-012-0403-5

Pischon, 2008, Obesity and cancer, Proc Nutr Soc, 67, 128, 10.1017/S0029665108006976