AZGP1 is a tumor suppressor in pancreatic cancer inducing mesenchymal-to-epithelial transdifferentiation by inhibiting TGF-Β-mediated ERK signaling

Oncogene

Volumn 29, Issue 37, 2010, Pages 5146-5158

  Kong, B ^a   Michalski, C W ^a   Hong, X ^a   Valkovskaya, N ^a   Rieder, S ^a   Abiatari, I ^a   Streit, S ^a   Erkan, M ^a   Esposito, I ^a   Friess, H ^a   Kleeff, J ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

AZGP1; EMT; MET; pancreatic cancer; transdifferentiation; transforming growth factor

Indexed keywords

ALPHA5 INTEGRIN; CADHERIN; CYTOKERATIN 19; DESMOPLAKIN; HISTONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VIMENTIN; ZINC ALPHA2 GLYCOPROTEIN; AZGP1 PROTEIN, HUMAN; CARRIER PROTEIN; GLYCOPROTEIN; HISTONE DEACETYLASE INHIBITOR;

ARTICLE; CANCER CELL; CELL INVASION; CELL SURVIVAL; CONTROLLED STUDY; DEACETYLATION; DOWN REGULATION; ENERGY METABOLISM; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MESENCHYME; MORPHOLOGY; PANCREAS ADENOCARCINOMA; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CELL DIFFERENTIATION; CELL TRANSDIFFERENTIATION; EPITHELIUM CELL; GENETICS; MESODERM; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TUMOR INVASION; TUMOR SUPPRESSOR GENE;

CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, TUMOR SUPPRESSOR; GLYCOPROTEINS; HISTONE DEACETYLASE INHIBITORS; HUMANS; MESODERM; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; CELL TRANSDIFFERENTIATION;

EID: 77956928318     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.258     Document Type: Article

References (55)

1. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF et al. (2009). Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462: 108-112.
2. Benfield AP, Whiddon BB, Clements JH, Martin SF. (2007). Structural and energetic aspects of Grb2-SH2 domain-swapping. Arch Biochem Biophys 462: 47-53.
3. Biliran Jr H, Wang Y, Banerjee S, Xu H, Heng H, Thakur A et al. (2005). Overexpression of cyclin D1 promotes tumor cell growth and confers resistance to cisplatin-mediated apoptosis in an elastase-myc transgene-expressing pancreatic tumor cell line. Clin Cancer Res 11: 6075-6086.
4. Bing C, Bao Y, Jenkins J, Sanders P, Manieri M, Cinti S et al. (2004). Zinc-alpha2-glycoprotein, a lipid mobilizing factor, is expressed in adipocytes and is up-regulated in mice with cancer cachexia. Proc Natl Acad Sci USA 101: 2500-2505.
5. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. (2005). Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749.
6. Burgi W, Schmid K. (1961). Preparation and properties of Zn-alpha 2-glycoprotein of normal human plasma. J Biol Chem 236: 1066-1074.
7. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. (2003). Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348: 1625-1638.
8. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R et al. (2008). The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233.
9. De Caestecker MP, Parks WT, Frank CJ, Castagnino P, Bottaro DP, Roberts AB et al. (1998). Smad2 transduces common signals from receptor serine-threonine and tyrosine kinases. Genes Dev 12: 1587-1592.
10. Dembinski JL, Krauss S. (2009). Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin Exp Metastasis 26: 611-623.
11. Diez-Itza I, Sanchez LM, Allende MT, Vizoso F, Ruibal A, Lopez-Otin C. (1993). Zn-alpha 2-glycoprotein levels in breast cancer cytosols and correlation with clinical, histological and biochemical parameters. Eur J Cancer 29A: 1256-1260.
12. Dumont N, Wilson MB, Crawford YG, Reynolds PA, Sigaroudinia M, Tlsty TD. (2008). Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers. Proc Natl Acad Sci USA 105: 14867-14872.
13. Ellenrieder V, Hendler SF, Boeck W, Seufferlein T, Menke A, Ruhland C et al. (2001). Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signal-regulated kinase 2 activation. Cancer Res 61: 4222-4228.
14. Esposito I, Kleeff J, Abiatari I, Shi X, Giese N, Bergmann F et al. (2007). Overexpression of cellular inhibitor of apoptosis protein 2 is an early event in the progression of pancreatic cancer. J Clin Pathol 60: 885-895.
15. Evdokimova V, Tognon C, Ng T, Sorensen PH. (2009). Reduced proliferation and enhanced migration: two sides of the same coin? Molecular mechanisms of metastatic progression by YB-1. Cell Cycle 8: 2901-2906.
16. Finkel E. (1996). High hopes for p21 in cancer treatment. Lancet 347: 1034.
17. Freemantle SJ, Liu X, Feng Q, Galimberti F, Blumen S, Sekula D et al. (2007). Cyclin degradation for cancer therapy and chemopre-vention. J Cell Biochem 102: 869-877.
18. Frenette G, Dube JY, Lazure C, Paradis G, Chretien M, Tremblay RR. (1987). The major 40-kDa glycoprotein in human prostatic fluid is identical to Zn-alpha 2-glycoprotein. Prostate 11: 257-270.
19. Friess H, Yamanaka Y, Buchler M, Ebert M, Beger HG, Gold LI et al. (1993). Enhanced expression of transforming growth factor beta isoforms in pancreatic cancer correlates with decreased survival. Gastroenterology 105: 1846-1856.
20. Fritsche P, Seidler B, Schuler S, Schnieke A, Gottlicher M, Schmid RM et al. (2009). HDAC2 mediates therapeutic resistance of pancreatic cancer cells via the BH3-only protein NOXA. Gut 58: 1399-1409.
21. Giehl K, Skripczynski B, Mansard A, Menke A, Gierschik P. (2000). Growth factor-dependent activation of the Ras-Raf-MEK-MAPK pathway in the human pancreatic carcinoma cell line PANC-1 carrying activated K-ras: implications for cell proliferation and cell migration. Oncogene 19: 2930-2942.
22. Glozak MA, Seto E. (2007). Histone deacetylases and cancer. Oncogene 26: 5420-5432.
23. Haigis KM, Kendall KR, Wang Y, Cheung A, Haigis MC, Glickman JN et al. (2008). Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation and tumor progression in the colon. Nat Genet 40: 600-608.
24. Hale LP, Price DT, Sanchez LM, Demark-Wahnefried W, Madden JF. (2001). Zinc alpha-2-glycoprotein is expressed by malignant prostatic epithelium and may serve as a potential serum marker for prostate cancer. Clin Cancer Res 7: 846-853.
25. Hamada S, Satoh K, Hirota M, Kimura K, Kanno A, Masamune A et al. (2007). Bone morphogenetic protein 4 induces epithelial-mesenchymal transition through MSX2 induction on pancreatic cancer cell line. J Cell Physiol 213: 768-774.
26. Horiguchi K, Shirakihara T, Nakano A, Imamura T, Miyazono K, Saitoh M. (2009). Role of Ras signaling in the induction of snail by transforming growth factor-beta. J Biol Chem 284: 245-253.
27. Jaenisch R, Bird A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl): 245-254.
28. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P et al. (2008). Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321: 1801-1806.
29. Ketterer K, Kong B, Frank D, Giese NA, Bauer A, Hoheisel J et al. (2009). Neuromedin U is overexpressed in pancreatic cancer and increases invasiveness via the hepatocyte growth factor c-Met pathway. Cancer Lett 277: 72-81.
30. Khasawneh J, Schulz MD, Walch A, Rozman J, Hrabe de Angelis M, Klingenspor M et al. (2009). Inflammation and mitochondrial fatty acid beta-oxidation link obesity to early tumor promotion. Proc Natl Acad Sci USA 106: 3354-3359.
31. Kretzschmar M, Doody J, Timokhina I, Massague J. (1999). A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev 13: 804-816.
32. Lecanda J, Ganapathy V, DAquino-Ardalan C, Evans B, Cadacio C, Ayala A et al. (2009). TGFbeta prevents proteasomal degradation of the cyclin-dependent kinase inhibitor p27kip1 for cell cycle arrest. Cell Cycle 8: 742-756.
33. Lemoine NR, Jain S, Hughes CM, Staddon SL, Maillet B, Hall PA et al. (1992). Ki-ras oncogene activation in preinvasive pancreatic cancer. Gastroenterology 102: 230-236.
34. Lim JH, Jung CR, Lee CH, Im DS. (2008). Egr-1 and serum response factor are involved in growth factors- and serum-mediated induction of E2-EPF UCP expression that regulates the VHL-HIF pathway. J Cell Biochem 105: 1117-1127.
35. Longnecker DS, Terhune PG. (1998). What is the true rate of K-ras mutation in carcinoma of the pancreas? Pancreas 17: 323-324.
36. Lung FD, Tsai JY. (2003). Grb2 SH2 domain-binding peptide analogs as potential anticancer agents. Biopolymers 71: 132-140.
37. Marrades MP, Martinez JA, Moreno-Aliaga MJ. (2008). ZAG, a lipid mobilizing adipokine, is downregulated in human obesity. J Physiol Biochem 64: 61-66.
38. Mathupala SP, Ko YH, Pedersen PL. (2006). Hexokinase II: cancers double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 25: 4777-4786.
39. Michalski CW, Laukert T, Sauliunaite D, Pacher P, Bergmann F, Agarwal N et al. (2007a). Cannabinoids ameliorate pain and reduce disease pathology in cerulein-induced acute pancreatitis. Gastro-enterology 132: 1968-1978.
40. Michalski CW, Maier M, Erkan M, Sauliunaite D, Bergmann F, Pacher P et al. (2008). Cannabinoids reduce markers of inflammation and fibrosis in pancreatic stellate cells. PLoS One 3: e1701.
41. Michalski CW, Shi X, Reiser C, Fachinger P, Zimmermann A, Buchler MW et al. (2007b). Neurokinin-2 receptor levels correlate with intensity, frequency, and duration of pain in chronic pancreatitis. Ann Surg 246: 786-793.
42. Michaud DS, Giovannucci E, Willett WC, Colditz GA, Stampfer MJ, Fuchs CS. (2001). Physical activity, obesity, height, and the risk of pancreatic cancer. JAMA 286: 921-929.
43. Ohkubo I, Niwa M, Takashima A, Nishikimi N, Gasa S, Sasaki M. (1990). Human seminal plasma Zn-alpha 2-glycoprotein: its purification and properties as compared with human plasma Zn-alpha 2-glycoprotein. Biochim Biophys Acta 1034: 152-156.
44. Roberts AB, Wakefield LM. (2003). The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci USA 100: 8621-8623.
45. Robson EJ, Khaled WT, Abell K, Watson CJ. (2006). Epithelial-to- mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines. Differentiation 74: 254-264.
46. Rolli V, Radosavljevic M, Astier V, Macquin C, Castan-Laurell I, Visentin V et al. (2007). Lipolysis is altered in MHC class I zinc-alpha(2)-glycoprotein deficient mice. FEBS Lett 581: 394-400.
47. Russell ST, Tisdale MJ. (2010). Antidiabetic properties of zinc-alpha2-glycoprotein in ob/ob mice. Endocrinology 151: 948-957.
48. Russell ST, Zimmerman TP, Domin BA, Tisdale MJ. (2004). Induction of lipolysis in vitro and loss of body fat in vivo by zinc-alpha2-glycoprotein. Biochim Biophys Acta 1636: 59-68.
49. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N et al. (2009). A gene expression signature associated with K-Ras addiction reveals regulators of EMT and tumor cell survival. Cancer Cell 15: 489-500.
50. Subramanian G, Schwarz RE, Higgins L, McEnroe G, Chakravarty S, Dugar S et al. (2004). Targeting endogenous transforming growth factor beta receptor signaling in SMAD4-deficient human pancreatic carcinoma cells inhibits their invasive phenotype1. Cancer Res 64: 5200-5211.
51. Tada T, Ohkubo I, Niwa M, Sasaki M, Tateyama H, Eimoto T. (1991). Immunohistochemical localization of Zn-alpha 2-glycopro-tein in normal human tissues. J Histochem Cytochem 39: 1221-1226.
52. Von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, Messer M et al. (2009). E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology 137: 361-371.
53. Wan M, Huang J, Jhala NC, Tytler EM, Yang L, Vickers SM et al. (2005). SCF(beta-TrCP1) controls Smad4 protein stability in pancreatic cancer cells. Am J Pathol 166: 1379-1392.
54. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS et al. (2009). Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 69: 2400-2407.
55. Zhang W, Erkan M, Abiatari I, Giese NA, Felix K, Kayed H et al. (2007). Expression of extracellular matrix metalloproteinase inducer (EMMPRIN/CD147) in pancreatic neoplasm and pancreatic stellate cells. Cancer Biol Ther 6: 218-227.