Role of dysregulated expression of leptin and leptin receptors in colorectal carcinogenesis

Tumor Biology

Volumn 35, Issue 2, 2014, Pages 871-879

  Uddin, Shahab ^a   Hussain, Azhar R ^a   Khan, Omar S ^b   Al Kuraya, Khawla S ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b BENEDICTINE UNIVERSITY   (United States)

Author keywords

Colorectal cancer; Leptin; Ob R; PI3 kinase AKT pathway

Indexed keywords

CYCLOOXYGENASE 2; JANUS KINASE; LEPTIN; LEPTIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STAT PROTEIN;

APOPTOSIS; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL MIGRATION; CELL SURVIVAL; COLORECTAL CANCER; COLORECTAL CARCINOGENESIS; HUMAN; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ADIPOSE TISSUE; CARCINOGENESIS; COLORECTAL NEOPLASMS; ENERGY METABOLISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEOSTASIS; HUMANS; LEPTIN; RECEPTORS, LEPTIN; SIGNAL TRANSDUCTION;

EID: 84898400396     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-013-1166-4     Document Type: Review

References (90)

1. Tartaglia LA, Dembski M, Weng X, Deng N, Culpepper J, Devos R, et al. Identification and expression cloning of a leptin receptor, Ob-R. Cell. 1995;83:1263-71.
2. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372:425-32.
3. Gorska E, Popko K, Stelmaszczyk-Emmel A, Ciepiela O, Kucharska A, Wasik M. Leptin receptors. Eur JMed Res. 2010;15 Suppl 2:50-4.
4. Jung CH, Kim MS. Molecular mechanisms of central leptin resistance in obesity. Arch Pharm Res. 2013;36:201-7.
5. Tong Q, Xu Y. Central leptin regulation of obesity and fertility. Curr Obes Rep. 2012;1:236-44.
6. Guffey CR, Fan D, Singh UP, Murphy EA. Linking obesity to colorectal cancer: recent insights into plausible biological mechanisms. Curr Opin Clin Nutr Metab Care. 2013;16:595-600.
7. Ogden CL, Carroll MD, Kit BK, Flegal KM. prevalence of obesity and trends in body mass index among us children and adolescents, 1999-2010. JAMA, J Am Med Assoc. 2012;307:483-90.
8. Sun Z, Dragon S, Becker A, Gounni AS. Leptin inhibits neutrophil apoptosis in children via erk/nf-kappab-dependent pathways. PloS one. 2013;8:e55249.
9. Sheffield L. Malignant transformation of mammary epithelial cells increases expression of leptin and leptin receptor. Endocr Res. 2008;33:111-8.
10. Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E, et al. American Cancer S: cancer statistics, 2004. CA Cancer J Clin. 2004;54:8-29.
11. Golan T, Urban D, Berger R, Lawrence YR. Changing prognosis of metastatic colorectal adenocarcinoma: differential improvement by age and tumor location. Cancer. 2013;119:3084-91.
12. Boeing H. Obesity and cancer-the update 2013. Best Pract Res Clin Endocrinol Metab. 2013;27:219-27.
13. Bardou M, Barkun AN, Martel M. Obesity and colorectal cancer. Gut. 2013;62:933-47.
14. Terry PD, Miller AB, Rohan TE. Obesity and colorectal cancer risk in women. Gut. 2002;51:191-4.
15. Stattin P, Lukanova A, Biessy C, Soderberg S, Palmqvist R, Kaaks R, et al. Obesity and colon cancer: does leptin provide a link? Int J Cancer. 2004;109:149-52.
16. Sinicrope FA, Foster NR, Sargent DJ, O'Connell MJ, Rankin C. Obesity is an independent prognostic variable in colon cancer survivors. Clin Cancer Res. 2010;16:1884-93.
17. Bray GA. Medical consequences of obesity. J Clin Cancer Endocrinol Metab. 2004;89:2583-9.
18. Liefers SC, te Pas MF, Veerkamp RF, van der Lende T. Associations between leptin gene polymorphisms and production, live weight, energy balance, feed intake, and fertility in holstein heifers. J Dairy Sci. 2002;85:1633-8.
19. Gribovskaja-Rupp I, Kosinski L, Ludwig KA. Obesity and colorectal cancer. Clin Colon Rectal Surg. 2011;24:229-43.
20. Gonullu G, Kahraman H, Bedir A, Bektas A, Yucel I. Association between adiponectin, resistin, insulin resistance, and colorectal tumors. Int J Colorectal Dis. 2010;25:205-12.
21. Erkasap N, Ozkurt M, Erkasap S, Yasar F, Uzuner K, Ihtiyar E, et al. Leptin receptor (Ob-R) mRNA expression and serum leptin concentration in patients with colorectal and metastatic colorectal cancer. Braz J Med Biol Res. 2013;46:306-10.
22. Tutino V, Notarnicola M, Guerra V, Lorusso D, Caruso MG. Increased soluble leptin receptor levels are associated with advanced tumor stage in colorectal cancer patients. Anticancer Res. 2011;31:3381-3.
23. Song M, Zhang X, Wu K, Ogino S, Fuchs CS, Giovannucci EL, Chan AT. Plasma adiponectin and soluble leptin receptor and risk of colorectal cancer: a prospective study. Cancer Prev Res 2013
24. Paik SS, Jang SM, Jang KS, Lee KH, Choi D, Jang SJ. Leptin expression correlates with favorable clinicopathologic phenotype and better prognosis in colorectal adenocarcinoma. Ann Surg Oncol. 2009;16:297-303.
25. Abolhassani M, Aloulou N, Chaumette MT, Aparicio T, Martin-Garcia N, Mansour H, et al. Leptin receptor-related immune response in colorectal tumors: the role of colonocytes and interleukin-8. Cancer Res. 2008;68:9423-32.
26. Aloulou N, Bastuji-Garin S, Le Gouvello S, Abolhassani M, Chaumette MT, Charachon A, et al. Involvement of the leptin receptor in the immune response in intestinal cancer. Cancer Res. 2008;68:9413-22.
27. Koda M, Sulkowska M, Kanczuga-Koda L, Surmacz E, Sulkowski S. Overexpression of the obesity hormone leptin in human colorectal cancer. J Clin Pathol. 2007;60:902-6.
28. Fenton JI, Lavigne JA, Perkins SN, Liu H, Chandramouli GV, Shih JH, et al.Microarray analysis reveals that leptin induces autocrine/paracrine cascades to promote survival and proliferation of colon epithelial cells in an apc genotype-dependent fashion. Mol Carcinog. 2008;47:9-21.
29. Fenton JI, Hursting SD, Perkins SN, Hord NG. Interleukin-6 production induced by leptin treatment promotes cell proliferation in an apc (min/+) colon epithelial cell line. Carcinogenesis. 2006;27:1507-15.
30. FitzGerald AJ, Mandir N, Goodlad RA. Leptin, cell proliferation and crypt fission in the gastrointestinal tract of intravenously fed rats. Cell Prolif. 2005;38:25-33.
31. Uddin S, Bavi PP, Hussain AR, Alsbeih G, Al-Sanea N, Abduljabbar A, et al. Leptin receptor expression in middle eastern colorectal cancer and its potential clinical implication. Carcinogenesis. 2009;30:1832-40.
32. Janeckova R. The role of leptin in human physiology and pathophysiology. Physiol Res Acad Sci Bohemoslov. 2001;50:443-59.
33. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. New Engl J Med. 1996;334:292-5.
34. Liu L, Zhong R, Wei S, Xiang H, Chen J, Xie D, et al. The leptin gene family and colorectal cancer: interaction with smoking behavior and family history of cancer. PLoS ONE. 2013;8:e60777.
35. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E, et al. Role of leptin in the neuroendocrine response to fasting. Nature. 1996;382:250-2.
36. Chua Jr SC, Chung WK, Wu-Peng XS, Zhang Y, Liu SM, Tartaglia L, et al. Phenotypes of mouse diabetes and rat fatty due to mutations in the ob (leptin) receptor. Science. 1996;271:994-6.
37. Ahima RS, Flier JS. Leptin. Ann Rev Physiol. 2000;62:413-37.
38. Lin J, Barb CR, Matteri RL, Kraeling RR, Chen X, Meinersmann RJ, et al. Long form leptin receptor mRNA expression in the brain, pituitary, and other tissues in the pig. Dom Animal Endocrinol. 2000;19:53-61.
39. Caprio M, Fabbrini E, Isidori AM, Aversa A, Fabbri A. Leptin in reproduction. Trends Endocrinol Metabol TEM. 2001;12:65-72.
40. Bartucci M, Svensson S, Ricci-Vitiani L, Dattilo R, Biffoni M, Signore M, et al. Obesity hormone leptin induces growth and interferes with the cytotoxic effects of 5-fluorouracil in colorectal tumor stem cells. Endocrine Rel Cancer. 2010;17:823-33.
41. Birmingham JM, Busik JV, Hansen-Smith FM, Fenton JI. Novel mechanism for obesity-induced colon cancer progression. Carcinogenesis. 2009;30:690-7.
42. Amemori S, Ootani A, Aoki S, Fujise T, Shimoda R, Kakimoto T, et al. Adipocytes and preadipocytes promote the proliferation of colon cancer cells in vitro. Am J Physiol Gastrointest Liver Physiol. 2007;292:G923-9.
43. Saxena NK, Sharma D, Ding X, Lin S, Marra F, Merlin D, et al. 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. 2007;67:2497-507.
44. Huang XF, Chen JZ. Obesity, the PI3K/AKT signal pathway and colon cancer. Obes Rev. 2009;10:610-16.
45. Ogunwobi OO, Beales IL. Cyclo-oxygenase-independent inhibition of apoptosis and stimulation of proliferation by leptin in human colon cancer cells. Dig Dis Sci. 2007;52:1934-45.
46. 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.
47. 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. Endocrine Rel Cancer. 2006;13:629-40.
48. Deo DD, Rao AP, Bose SS, Ouhtit A, Baliga SB, Rao SA, et al. Differential effects of leptin on the invasive potential of androgen-dependent and -independent prostate carcinoma cells. J Biomed Biotechnol. 2008;2008:163902.
49. Gao J, Tian J, Lv Y, Shi F, Kong F, Shi H, et al. Leptin induces functional activation of cyclooxygenase-2 through JAK2/STAT3, MAPK/ERK, and PI3K/AKT pathways in human endometrial cancer cells. Cancer Sci. 2009;100:389-95.
50. Beales IL, Ogunwobi OO. Leptin synergistically enhances the antiapoptotic and growth-promoting effects of acid in oe33 oesophageal adenocarcinoma cells in culture. Mol Cell Endocrinol. 2007;274:60-8.
51. Quintas-Cardama A, Verstovsek S. Molecular pathways: JAK/STAT pathway: mutations, inhibitors, and resistance. Clin Cancer Res. 2013;19:1933-40.
52. Yu JH, Kim H. Role of Janus kinase/signal transducers and activators of transcription in the pathogenesis of pancreatitis and pancreatic cancer. Gut Liver. 2012;6:417-22.
53. Singh N, Hussain S, Bharadwaj M, Kakkar N, Singh SK, Sobti RC. Overexpression of signal transducer and activator of transcription (stat-3 and stat-5) transcription factors and alteration of suppressor of cytokine signaling (socs-1) protein in prostate cancer. J Recept Signal Transduct Res. 2012;32:321-27.
54. Ma XT, Wang S, Ye YJ, Du RY, Cui ZR, Somsouk M. Constitutive activation of STAT3 signaling pathway in human colorectal carcinoma. World J Gastroentorol WJG. 2004;10:1569-73.
55. Osaki LH, Gama P. Mapks and signal transduction in the control of gastrointestinal epithelial cell proliferation and differentiation. Int J Mol Sci. 2013;14:10143-61.
56. Taylor CA, Zheng Q, Liu Z, Thompson JE. Role of p38 and jnk mapk signaling pathways and tumor suppressor p53 on induction of apoptosis in response to ad-eif5a1 in a549 lung cancer cells. Mol Cancer. 2013;12:35.
57. Weston CR, Lambright DG, Davis RJ. Signal transduction. MAP kinase signaling specificity. Science. 2002;296:2345-7.
58. Hegyi K, Fulop K, Kovacs K, Toth S, Falus A. Leptin-induced signal transduction pathways. Cell Biol Int. 2004;28:159-69.
59. van den Brink GR, O'Toole T, Hardwick JC, van den Boogaardt DE, Versteeg HH, van Deventer SJ, et al. Leptin signaling in human peripheral blood mononuclear cells, activation of p38 and p42/44 mitogen-activated protein (map) kinase and p70 s6 kinase. Mol Cell Biol Res Comm MCBRC. 2000;4:144-50.
60. Dreyer MG, Juge-Aubry CE, Gabay C, Lang U, Rohner-Jeanrenaud F, Dayer JM, et al. Leptin activates the promoter of the interleukin-1 receptor antagonist through p42/44 mitogen-activated protein kinase and a composite nuclear factor kappa b/pu.1 binding site. Biochem J. 2003;370:591-9.
61. Ogunwobi O, Mutungi G, Beales IL. Leptin stimulates proliferation and inhibits apoptosis in barrett's esophageal adenocarcinoma cells by cyclooxygenase-2-dependent, prostaglandin-e2-mediated transactivation of the epidermal growth factor receptor and c-jun nh2-terminal kinase activation. Endocrinology. 2006; 147:4505-16.
62. Sun Y, Sinicrope FA. Selective inhibitors of mek1/erk44/42 and p38 mitogen-activated protein kinases potentiate apoptosis induction by sulindac sulfide in human colon carcinoma cells. Mol Cancer Ther. 2005;4:51-9.
63. Nishihara H, Hwang M, Kizaka-Kondoh S, Eckmann L, Insel PA. Cyclic amp promotes camp-responsive element-binding prote-independent induction of cellular inhibitor of apoptosis protein-2 and suppresses apoptosis of colon cancer cells through erk1/2 and p38 mapk. J Biol Chem. 2004;279:26176-83.
64. Chan UP, Lee JF, Wang SH, Leung KL, Chen GG. Induction of colon cancer cell death by 7-hydroxystaurosporine (ucn-01) is associated with increased p38 mapk and decreased bcl-xl. Anti Canc Drugs. 2003;14:761-6.
65. Lee EJ, Park HG, Kang HS. Sodium salicylate induces apoptosis in hct116 colorectal cancer cells through activation of p38mapk. Int J Oncol. 2003;23:503-8.
66. Hussain AR, Ahmed SO, Ahmed M, Khan OS, Al Abdulmohsen S, Platanias LC, et al. Cross-talk between nfkb and the PI3-kinase/AKT pathway can be targeted in primary effusion lymphoma (pel) cell lines for efficient apoptosis. PLoS ONE. 2012;7:e39945.
67. Li W, Wang H, Kuang CY, Zhu JK, Yu Y, Qin ZX, et al. An essential role for the id1/pi3k/akt/nfkb/survivin signalling pathway in promoting the proliferation of endothelial progenitor cells in vitro. Mol Cell Biochem. 2012;363:135-45.
68. Rayet B, Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene. 1999;18:6938-47.
69. Carpenter CL, Duckworth BC, Auger KR, Cohen B, Schaffhausen BS, Cantley LC. Purification and characterization of phosphoinositide 3-kinase from rat liver. J Biol Chem. 1990;265:19704-11.
70. Chen HC, Guan JL. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A. 1994;91:10148-52.
71. Cantley LC. The phosphoinositide 3-kinase pathway. Science. 2002;296:1655-57.
72. Jiang BH, Aoki M, Zheng JZ, Li J, Vogt PK. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase akt/protein kinase b. Proc Natl Acad Sci U S A. 1999;96:2077-81.
73. Uddin S, Bu R, Ahmed M, Abubaker J, Al-Dayel F, Bavi P, et al. Overexpression of leptin receptor predicts an unfavorable outcome in middle eastern ovarian cancer. Mol Cancer. 2009;8:74.
74. Uddin S, Bavi P, Siraj AK, Ahmed M, Al-Rasheed M, Hussain AR, et al. Leptin-r and its association with PI3K/AKT signaling pathway in papillary thyroid carcinoma. Endocrine Rel Cancer. 2010;17:191-202.
75. Wang D, Chen J, Chen H, Duan Z, Xu Q, Wei M, et al. Leptin regulates proliferation and apoptosis of colorectal carcinoma through PI3K/AKT/mTOR signalling pathway. J Biosci. 2012;37:91-101.
76. Rao CV, Janakiram NB, Mohammed A. Lipoxygenase and cyclooxygenase pathways and colorectal cancer prevention. Curr Colorectal Cancer Rep. 2012;8:316-24.
77. Muller-Decker K. Cyclooxygenase-dependent signaling is causally linked to non-melanoma skin carcinogenesis: pharmacological, genetic, and clinical evidence. Canc Metastasis Rev. 2011;30:343-61.
78. Liu CH, Chang SH, Narko K, Trifan OC, Wu MT, Smith E, et al. Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J Biol Chem. 2001;276:18563-69.
79. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell. 1998;93:705-16.
80. Perlikos F, Harrington KJ, Syrigos KN. Key molecular mechanisms in lung cancer invasion and metastasis: a comprehensive review. Crit Rev Oncol Hematol. 2013;87:1-11.
81. Bhave SL, Teknos TN, Pan Q. Molecular parameters of head and neck cancer metastasis. Crit Rev Eukaryot Gen Expr. 21:143-53.
82. Salzmann S, Seher A, Trebing J, Weisenberger D, Rosenthal A, Siegmund D, et al. Fibroblast growth factor inducible (fn14)-specific antibodies concomitantly display signaling pathway-specific agonistic and antagonistic activity. J Biol Chem. 2013;288:13455-66.
83. Sarfstein R, Werner H. Minireview: nuclear insulin and insulin-like growth factor-1 receptors: a novel paradigm in signal transduction. Endocrinology. 2013;154:1672-79.
84. Chan CM, Chang HH, Wang VC, Huang CL, Hung CF. Inhibitory effects of resveratrol on pdgf-bb-induced retinal pigment epithelial cell migration via pdgfrbeta, pi3k/akt and mapk pathways. PloS ONE. 2013;8:e56819.
85. Stattin P, Palmqvist R, Soderberg S, Biessy C, Ardnor B, Hallmans G, et al. Plasma leptin and colorectal cancer risk: a prospective study in northern sweden. Oncol Rep. 2003;10:2015-21.
86. Sierra-Honigmann MR, Nath AK, Murakami C, Garcia-Cardena G, Papapetropoulos A, Sessa WC, et al. Biological action of leptin as an angiogenic factor. Science. 1998;281:1683-6.
87. Hardwick JC, Van Den Brink GR, Offerhaus GJ, Van Deventer SJ, Peppelenbosch MP. Leptin is a growth factor for colonic epithelial cells. Gastroenterology. 2001;121:79-90.
88. Attoub S, Noe V, Pirola L, Bruyneel E, Chastre E, Mareel M, et al. Leptin promotes invasiveness of kidney and colonic epithelial cells via phosphoinositide 3-kinase-, rho-, and rac-dependent signaling pathways. FASEB J. 2000;14:2329-38.
89. Liu Z, Uesaka T, Watanabe H, Kato N. High fat diet enhances colonic cell proliferation and carcinogenesis in rats by elevating serum leptin. Int J Oncol. 2001;19:1009-14.
90. Fox SB, Gasparini G, Harris AL. Angiogenesis: pathological, prognostic, and growth-factor pathways and their link to trial design and anticancer drugs. Lancet Oncol. 2001;2:278-89.