Epidermal growth factor down-regulates the expression of neutrophil gelatinase-associated lipocalin (NGAL) through E-cadherin in pancreatic cancer cells

Cancer

Volumn 117, Issue 11, 2011, Pages 2408-2418

  Tong, Zhimin ^a   Chakraborty, Subhankar ^b   Sung, Bokyung ^a   Koolwal, Pooja ^a   Kaur, Sukhwinder ^b   Aggarwal, Bharat B ^a   Mani, Sendurai A ^a   Bresalier, Robert S ^a   Batra, Surinder K ^b   Guha, Sushovan ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

E cadherin; Epidermal growth factor; Neutrophil gelatinase associated lipocalin; Nuclear factor jB; Pancreatic cancer

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; UVOMORULIN;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

E-CADHERIN; EPIDERMAL GROWTH FACTOR; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; NUCLEAR FACTOR ΚB; PANCREATIC CANCER;

ACUTE-PHASE PROTEINS; CADHERINS; CELL LINE, TUMOR; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIPOCALINS; NEOPLASM GRADING; NEOPLASM STAGING; NF-KAPPA B; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

EID: 79958741772     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.25803     Document Type: Article

References (48)

1. Flower DR. The lipocalin protein family: structure and function. Biochem J. 1996;318(pt 1):1-14. (Pubitemid 26283618)
2. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell. 2002;10:1033-1043. (Pubitemid 36001971)
3. Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M, Kjeldsen L. Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut. 1996;38:414-420.
4. Saiga H, Nishimura J, Kuwata H, et al. Lipocalin 2-dependent inhibition of mycobacterial growth in alveolar epithelium. J Immunol. 2008;181:8521-8527.
5. Mishra J, Mori K, Ma Q, et al. Amelioration of ischemic acute renal injury by neutrophil gelatinase-associated lipocalin. J Am Soc Nephrol. 2004;15:3073-3082. (Pubitemid 39578839)
6. Stoesz SP, Friedl A, Haag JD, Lindstrom MJ, Clark GM, Gould MN. Heterogeneous expression of the lipocalin NGAL in primary breast cancers. Int J Cancer. 1998;79: 565-572. (Pubitemid 28549466)
7. Bartsch S, Tschesche H. Cloning and expression of human neutrophil lipocalin cDNA derived from bone marrow and ovarian cancer cells. FEBS Lett. 1995;357:255-259.
8. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat. 2008;108:389-397. (Pubitemid 351431077)
9. Zhang H, Xu L, Xiao D, et al. Upregulation of neutrophil gelatinase-associated lipocalin in oesophageal squamous cell carcinoma: significant correlation with cell differentiation and tumour invasion. J Clin Pathol. 2007;60:555-561. (Pubitemid 46867169)
10. Lim R, Ahmed N, Borregaard N, et al. Neutrophil gelatinase-associated lipocalin (NGAL) an early screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition. Int J Cancer. 2007;120:2426-2434. (Pubitemid 46642130)
11. Lee H-J, Lee E-K, Lee K-J, Hong S-W, Yoon Y, Kim J-S. Ectopic expression of neutrophil gelatinase-associated lipocalin suppresses the invasion and liver metastasis of colon cancer cells. Int J Cancer. 2006;118:2490-2497.
12. Tong Z, Kunnumakkara AB, Wang H, et al. Neutrophil gelatinase-associated lipocalin: a novel suppressor of invasion and angiogenesis in pancreatic cancer. Cancer Res. 2008;68: 6100-6108.
13. Moniaux N, Chakraborty S, Yalniz M, et al. Early diagnosis of pancreatic cancer: neutrophil gelatinase-associated lipocalin as a marker of pancreatic intraepithelial neoplasia. Br J Cancer. 2008;98:1540-1547. (Pubitemid 351652327)
14. Normanno N, De Luca A, Bianco C, et al. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene. 2006;366:2-16. (Pubitemid 43199589)
15. Salomon DS, Brandt R, Ciardiello F, Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol. 1995;19:183-232.
16. Korc M, Chandrasekar B, Yamanaka Y, Friess H, Buchier M, Beger HG. Overexpression of the epidermal growth factor receptor in human pancreatic cancer is associated with concomitant increases in the levels of epidermal growth factor and transforming growth factor alpha. J Clin Invest. 1992;90:1352-1360.
17. Poon SL, Hammond GT, Leung PCK. Epidermal growth factor-induced GnRH-II synthesis contributes to ovarian cancer cell invasion. Mol Endocrinol. 2009;23:1646-1656.
18. Lee M-Y, Chou C-Y, Tang M-J, Shen M-R. Epithelial-mesenchymal transition in cervical cancer: correlation with tumor progression, epidermal growth factor receptor overexpression, and snail up-regulation. Clin Cancer Res. 2008;14:4743-4750.
19. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell. 2003;4:499-515. (Pubitemid 38050046)
20. Kimura F Iwaya K, Kawaguchi T, et al. Epidermal growth factor-dependent enhancement of invasiveness of squamous cell carcinoma of the breast. Cancer Sci. 2010;101:1133-1140.
21. Yamanaka Y, Friess H, Kobrin MS, Buchler M, Beger HG, Korc M. Coexpression of epidermal growth factor receptor and ligands in human pancreatic cancer is associated with enhanced tumor aggressiveness. Anticancer Res. 1993;13:565-569.
22. Pryczynicz A, Guzinska-Ustymowicz K, Kemona A, Czyzewska J. Expression of EGF and EGFR strongly correlates with metastasis of pancreatic ductal carcinoma. Anticancer Res. 2008;28:1399-1404. (Pubitemid 351578886)
23. Binker MG, Binker-Cosen AA, Richards D, Oliver B, Cosen-Binker LI. EGF promotes invasion by PANC-1 cells through Rac1/ROS-dependent secretion and activation of MMP-2. Biochem Biophys Res Commun. 2009;379:445-450.
24. Zhang H, Ma G, Dong M, et al. Epidermal growth factor promotes invasiveness of pancreatic cancer cells through NF-kappaB-mediated proteinase productions. Pancreas. 2006;32:101-109. (Pubitemid 41803654)
25. Hu L, Hittelman W, Lu T, et al. NGAL decreases E-cad-herin-mediated cell-cell adhesion and increases cell motility and invasion through Rac1 in colon carcinoma cells. Lab Invest. 2009;89:531-548.
26. Chaturvedi MM, Mukhopadhyay A, Aggarwal BB. Assay for redox-sensitive transcription factor. Methods Enzymol. 2000; 319:585-602. (Pubitemid 30448077)
27. Ueda S, Ogata S, Tsuda H, et al. The correlation between cytoplasmic overexpression of epidermal growth factor receptor and tumor aggressiveness: poor prognosis in patients with pancreatic ductal adenocarcinoma [serial online]. Pancreas. 2004;29:e1-e8.
28. Tobita K, Kijima H, Dowaki S, et al. Epidermal growth factor receptor expression in human pancreatic cancer: significance for liver metastasis. Int J Mol Med. 2003;11:305-309.
29. Kumei S, Motomura W, Yoshizaki T, Takakusaki K, Okumura T. Troglitazone increases expression of E-cadherin and claudin 4 in human pancreatic cancer cells. Biochem Biophys Res Commun. 2009;380:614-619.
30. Honma N, Genda T, Matsuda Y, et al. MEK/ERK signaling is a critical mediator for integrin-induced cell scattering in highly metastatic hepatocellular carcinoma cells. Lab Invest. 2006;86:687-696. (Pubitemid 43901666)
31. Furuse J. Growth factors as therapeutic targets in HCC. Crit Rev Oncol Hematol. 2008;67:8-15.
32. Gibbs JB. Anticancer drug targets: growth factors and growth factor signaling. J Clin Invest. 2000;105:9-13. (Pubitemid 30036381)
33. Li S-H, Hawthorne VS, Neal CL, et al. Upregulation of neutrophil gelatinase-associated lipocalin by ErbB2 through nuclear factor-kappaB activation. Cancer Res. 2009;69:9163-9168.
34. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009;28:15-33.
35. von Burstin J, Eser S, Paul MC, et al. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex [serial online]. Gastroenterology. 2009;137:361-371.
36. Joo Y-E, Rew J-S, Park C-S, Kim S-J. Expression of E-cadherin, alpha- and beta-catenins in patients with pancreatic adenocarcinoma. Pancreatology. 2002;2:129-137. (Pubitemid 34639088)
37. Lo H-W, Hsu S-C, Xia W, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res. 2007;67:9066-9076. (Pubitemid 47535891)
38. Wang F, Sloss C, Zhang X, Lee SW, Cusack JC. Membrane-bound heparin-binding epidermal growth factor like growth factor regulates E-cadherin expression in pancreatic carcinoma cells. Cancer Res. 2007;67:8486-8493. (Pubitemid 47437422)
39. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008;68: 3645-3654.
40. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mammary Gland Biol Neoplasia. 2009;14:29-43.
41. Arumugam T, Ramachandran V, Fournier KF, et al. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009;69:5820-5828.
42. Frolov A, Schuller K, Tzeng C-WD, et al. ErbB3 expression and dimerization with EGFR influence pancreatic cancer cell sensitivity to erlotinib. Cancer Biol Ther. 2007;6:548-554. (Pubitemid 47328329)
43. Yang L, Amann JM, Kikuchi T, et al. Inhibition of epidermal growth factor receptor signaling elevates 15-hydroxy-prostaglandin dehydrogenase in non-small-cell lung cancer. Cancer Res. 2007;67:5587-5593. (Pubitemid 46984987)
44. Iannetti A, Pacifico F, Acquaviva R, et al. The neutrophil gelatinase-associated lipocalin (NGAL), a NF-kappaB-regulated gene, is a survival factor for thyroid neoplastic cells. Proc Natl Acad Sci U S A. 2008;105:14058-14063.
45. Bolignano D, Donato V, Lacquaniti A, et al. Neutrophil gelatinase-associated lipocalin (NGAL) in human neoplasias: a new protein enters the scene. Cancer Lett. 2010;288:10-16.
46. Banan A, Zhang LJ, Farhadi A, Fields JZ, Shaikh M, Keshavarzian A. PKC-beta1 isoform activation is required for EGF-induced NF-kappaB inactivation and IkappaBalpha stabilization and protection of F-actin assembly and barrier function in enterocyte monolayers. Am J Physiol Cell Physiol. 2004;286:C723-38. (Pubitemid 38292679)
47. Biswas DK, Cruz AP, Gansberger E, Pardee AB. Epidermal growth factor-induced nuclear factor kappa B activation: a major pathway of cell-cycle progression in estrogen-receptor negative breast cancer cells. Proc Natl Acad Sci U S A. 2000;97:8542-8547. (Pubitemid 30639709)
48. Husvik C, Bryne M, Halstensen TS. Epidermal growth factor-induced cyclooxygenase-2 expression in oral squamous cell carcinoma cell lines is mediated through extracellular signalregulated kinase 1/2 and p38 but is Src and nuclear factorkappa B independent. Eur J Oral Sci. 2009;117:528-535.