Leptin induces matrix metalloproteinase 7 expression to promote ovarian cancer cell invasion by activating ERK and JNK pathways

Journal of Cellular Biochemistry

Volumn 119, Issue 2, 2018, Pages 2333-2344

  Ghasemi, Ahmad ^a   Hashemy, Seyed Isaac ^b   Aghaei, Mahmoud ^a   Panjehpour, Mojtaba ^a  

^a ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

cell invasion; leptin; matrix metalloproteinase 7; ovarian cancer

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; GELATIN; GELATINASE A; GELATINASE B; LEPTIN; MATRILYSIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; 2-(2-AMINO-3-METHOXYPHENYL)-4H-1-BENZOPYRAN-4-ONE; ANTHRACENE DERIVATIVE; FLAVONOID; MMP7 PROTEIN, HUMAN; PYRAZOLANTHRONE;

ARTICLE; CAOV-3 CELL LINE; CELL INVASION ASSAY; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; GENETIC TRANSFECTION; OVARIAN CANCER CELL LINE; OVCAR-3 CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SK-OV-3 CELL LINE; TUMOR INVASION; WESTERN BLOTTING; WOUND HEALING ASSAY; ZYMOGRAPHY; CELL MOTION; FEMALE; GENE KNOCKDOWN; GENETICS; HUMAN; MAPK SIGNALING; METABOLISM; OVARY TUMOR; TUMOR CELL LINE;

ANTHRACENES; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FLAVONOIDS; GENE KNOCKDOWN TECHNIQUES; HUMANS; LEPTIN; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 7; NEOPLASM INVASIVENESS; OVARIAN NEOPLASMS;

EID: 85031688102     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.26396     Document Type: Article

References (50)

1. Louie SM, Roberts LS, Nomura DK. Mechanisms linking obesity and cancer. Biochim Biophys Acta. 2013; 1831:1499–1508.
2. 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; 90:207–210.
3. Choi JH, Lee KT, Leung PC. Estrogen receptor alpha pathway is involved in leptin-induced ovarian cancer cell growth. Carcinogenesis. 2011; 32:589–596.
4. Frühbeck G. Intracellular signalling pathways activated by leptin. Biochem J. 2006; 393:7–20.
5. McMurtry V, Simeone AM, Nieves-Alicea R, Tari AM. Leptin utilizes Jun N-terminal kinases to stimulate the invasion of MCF-7 breast cancer cells. Clin Exp Metastasis. 2009; 26:197–204.
6. Lin MC, Tsai SY, Wang FY, Liu FH, Syu JN, Tang FY. Leptin induces cell invasion and the upregulation of matrilysin in human colon cancer cells. BioMedicine. 2013; 3:174–180.
7. Dong Z, Xu X, Du L, et al. Leptin-mediated regulation of MT1-MMP localization is KIF1B dependent and enhances gastric cancer cell invasion. Carcinogenesis. 2013; 34:974–983.
8. Sharma D, Saxena N, Vertino P, Anania F. Leptin promotes the proliferative response and invasiveness in human endometrial cancer cells by activating multiple signal-transduction pathways. Endocr Relat Cancer. 2006; 13:629–640.
9. Uddin S, Bu R, Ahmed M, et al. Overexpression of leptin receptor predicts an unfavorable outcome in Middle Eastern ovarian cancer. Mol Cancer. 2009; 8:74.
10. Kato S, Abarzúa Catalán L, Delpiano C, et al. Leptin stimulates migration and invasion and maintains cancer stem-like properties in ovarian cancer cells: an explanation for poor outcomes in obese women. Oncotarget. 2015; 6:21100–21119.
11. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69–90.
12. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol. 2010; 177:1053–1064.
13. Romero I, Bast RC, Jr. Minireview: human ovarian cancer: biology, current management, and paths to personalizing therapy. Endocrinology. 2012; 153:1593–1602.
14. Clark AG, Vignjevic DM. Modes of cancer cell invasion and the role of the microenvironment. Curr Opin Cell Biol. 2015; 36:13–22.
15. Diaz ES, Karlan BY, Li AJ. Obesity-associated adipokines correlate with survival in epithelial ovarian cancer. Gynecol Oncol. 2013; 129:353–357.
16. Ghasemi A, Hashemy SI, Aghaei M, Panjehpour M. RhoA/ROCK pathway mediates leptin-induced uPA expression to promote cell invasion in ovarian cancer cells. Cell Signal. 2017; 32:104–114.
17. Wang FQ, So J, Reierstad S, Fishman DA. Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int J Cancer. 2005; 114:19–31.
18. Hadler-Olsen E, Winberg JO, Uhlin-Hansen L. Matrix metalloproteinases in cancer: Their value as diagnostic and prognostic markers and therapeutic targets. Tumor Biol. 2013; 34:2041–2051.
19. Ii M, Yamamoto H, Adachi Y, Maruyama Y, Shinomura Y. Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med. 2006; 231:20–27.
20. Tanimoto H, Underwood LJ, Shigemasa K, et al. The matrix metalloprotease pump-1 (MMP-7, Matrilysin): a candidate marker/target for ovarian cancer detection and treatment. Tumor Biol. 1999; 20:88–98.
21. Yin JG, Liu XY, Wang B, et al. Gene expression profiling analysis of ovarian cancer. Oncol Lett. 2016; 12:405–412.
22. Vihinen P, Kähäri VM. Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer. 2002; 99:157–166.
23. Imai K, Yokohama Y, Nakanishi I, et al. Matrix metalloproteinase 7 (matrilysin) from human rectal carcinoma cells activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties. J Biol Chem. 1995; 270:6691–6697.
24. Yang R, Barouch LA. Leptin signaling and obesity cardiovascular consequences. Circ Res. 2007; 101:545–559.
25. Chang MC, Chen CA, Chen PJ, et al. Mesothelin enhances invasion of ovarian cancer by inducing MMP-7 through MAPK/ERK and JNK pathways. Biochem J. 2012; 442:293–302.
26. Reddy KB, Nabha SM, Atanaskova N. Role of MAP kinase in tumor progression and invasion. Cancer Metastasis Rev. 2003; 22:395–403.
27. Kramer N, Walzl A, Unger C, et al. In vitro cell migration and invasion assays. Mutat Res. 2013; 752:10–24.
28. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011; 29:415–445.
29. Macciò A, Madeddu C. Inflammation and ovarian cancer. Cytokine. 2012; 58:133–147.
30. Krempler F, Hell E, Winkler C, Breban D, Patsch W. Plasma leptin levels. Arterioscler Thromb Vasc Biol. 1998; 18:1686–1690.
31. Nieman KM, Romero IL, Van Houten B, Lengyel E. Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochim Biophys Acta. 2013; 1831:1533–1541.
32. Cox TR, Erler JT. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech. 4:165.
33. Yeh WL, Lu DY, Lee MJ, Fu WM. Leptin induces migration and invasion of glioma cells through MMP-13 production. Glia. 2009; 57:454–464.
34. Wang H, Cheng H, Shao Q, et al. Leptin-promoted human extravillous trophoblast invasion is MMP14 dependent and requires the cross talk between Notch1 and PI3K/Akt signaling. Biol Reprod. 2014; 90:78.
35. Fan Y, Gan Y, Shen Y, et al. Leptin signaling enhances cell invasion and promotes the metastasis of human pancreatic cancer via increasing MMP-13 production. Oncotarget. 2015; 6:16120.
36. Yamashita K, Azumano I, Mai M, Okada Y. Expression and tissue localization of matrix metalloproteinase 7 (matrilysin) in human gastric carcinomas. Implications for vessel invasion and metastasis. Int J Cancer. 1998; 79:187–194.
37. Mori M, Barnard GF, Mimori K, Ueo H, Akiyoshi T, Sugimachi K. Overexpression of matrix metalloproteinase-7 mRNA in human colon carcinomas. Cancer. 1995; 75:1516–1519.
38. Ueno H, Yamashita K, Azumano I, Inoue M, Okada Y. Enhanced production and activation of matrix metalloproteinase-7 (matrilysin) in human endometrial carcinomas. Int J Cancer. 1999; 84:470–477.
39. Zhao H, Yang Z, Wang X, et al. Triptolide inhibits ovarian cancer cell invasion by repression of matrix metalloproteinase 7 and 19 and upregulation of E-cadherin. Exp Mol Med. 2012; 44:633–641.
40. Chen C, Chang YC, Lan MS, Breslin M. Leptin stimulates ovarian cancer cell growth and inhibits apoptosis by increasing cyclin D1 and Mcl-1 expression via the activation of the MEK/ERK1/2 and PI3K/Akt signaling pathways. Int J Oncol. 2013; 42:1113–1119.
41. Miyazaki T, Bub JD, Iwamoto Y. C-Jun NH 2-terminal kinase mediates leptin-stimulated androgen-independent prostate cancer cell proliferation via signal transducer and activator of transcription 3 and Akt. Biochim Biophys Acta. 2008; 1782:593–604.
42. 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; 147:4505–4516.
43. Ogunwobi OO, Beales IL. The anti-apoptotic and growth stimulatory actions of leptin in human colon cancer cells involves activation of JNK mitogen activated protein kinase, JAK2 and PI3 kinase/Akt. Int J Colorectal Dis. 2007; 22:401–409.
44. Gonzalez-Perez RR, Xu Y, Guo S, Watters A, Zhou W, Leibovich SJ. Leptin upregulates VEGF in breast cancer via canonic and non-canonical signalling pathways and NFκB/HIF-1α activation. Cell Signal. 2010; 22:1350–1362.
45. Yoon KW, Park SY, Kim JY, et al. Leptin-induced adhesion and invasion in colorectal cancer cell lines. Oncol Rep. 2014; 31:2493–2498.
46. Yuan HJ, Sun KW, Yu K. Leptin promotes the proliferation and migration of human breast cancer through the extracellular-signal regulated kinase pathway. Mol Med Rep. 2014; 9:350–354.
47. Saxena NK, Sharma D, Ding X, 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; 67:2497–2507.
48. Overall CM, López-Otín C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer. 2002; 2:657–672.
49. Dozier S, Escobar G, Lindsey M. Matrix metalloproteinase (MMP)-7 activates MMP-8 but not MMP-13. Med Chem. 2006; 2:523–526.
50. Hsu T, Lin S, Lu P, Chang WC, Hung C, Yeh Y, Su W, Liao P, Hung J. MMP7-mediated cleavage of nucleolin at Asp255 induces MMP9 expression to promote tumor malignancy. Oncogene. 2015; 34:826–837.