Carboxypeptidase E promotes cancer cell survival, but inhibits migration and invasion

Cancer Letters

Volumn 341, Issue 2, 2013, Pages 204-213

  Murthy, Saravana R K ^a   Dupart, Evan ^a   Al Sweel, Najla ^a   Chen, Alexander ^a   Cawley, Niamh X ^a   Loh, Y Peng ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Cell invasion; Cell survival; Fibrosarcoma; Hepatocellular carcinoma; Pheochromocytoma

Indexed keywords

BETA CATENIN; CARBOXYPEPTIDASE H; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2; MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL HYPOXIA; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG CYTOTOXICITY; FIBROSARCOMA; GENE EXPRESSION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; METABOLIC STRESS; MIGRATION INHIBITION; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL MOTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; METABOLISM; NEOPLASM; PATHOLOGY; PC12 CELL LINE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANTIBODIES, MONOCLONAL; CARBOXYPEPTIDASE H; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM INVASIVENESS; NEOPLASMS; PC12 CELLS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 84887149104     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.08.011     Document Type: Article

References (44)

1. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nature reviews. Cancer 2002, 2:563-572.
2. Neumann H.P., Bausch B., McWhinney S.R., Bender B.U., Gimm O., Franke G., Schipper J., Klisch J., Altehoefer C., Zerres K., Januszewicz A., Eng C., Smith W.M., Munk R., Manz T., Glaesker S., Apel T.W., Treier M., Reineke M., Walz M.K., Hoang-Vu C., Brauckhoff M., Klein-Franke A., Klose P., Schmidt H., Maier-Woelfle M., Peczkowska M., Szmigielski C. Germ-line mutations in nonsyndromic pheochromocytoma. The New England Journal of Medicine 2002, 346:1459-1466.
3. North W.G., Du J. Key peptide processing enzymes are expressed by a variant form of small-cell carcinoma of the lung. Peptides 1998, 19:1743-1747.
4. Azzoni C., D'Adda T., Tamburrano G., Coscelli C., Madsen O.D., Scopsi L., Bordi C. Functioning human insulinomas. An immunohistochemical analysis of intracellular insulin processing. Virchows Archiv: An International Journal of Pathology 1998, 433:495-504.
5. Zhang J.H., Zhou D., You J., Tang B.S., Li P.Y., Tang S.S. Differential processing of neuropeptide proprotein in human breast adenocarcinoma. Journal of Endocrinological Investigation 2013.
6. Horing E., Harter P.N., Seznec J., Schittenhelm J., Buhring H.J., Bhattacharyya S., von Hattingen E., Zachskorn C., Mittelbronn M., Naumann U. The "go or grow" potential of gliomas is linked to the neuropeptide processing enzyme carboxypeptidase E and mediated by metabolic stress. Acta Neuropathologica 2012, 124:83-97.
7. He P., Varticovski L., Bowman E.D., Fukuoka J., Welsh J.A., Miura K., Jen J., Gabrielson E., Brambilla E., Travis W.D., Harris C.C. Identification of carboxypeptidase E and gamma-glutamyl hydrolase as biomarkers for pulmonary neuroendocrine tumors by cDNA microarray. Human Pathology 2004, 35:1196-1209.
8. Cawley N.X., Wetsel W.C., Murthy S.R., Park J.J., Pacak K., Loh Y.P. New roles of carboxypeptidase E in endocrine and neural function and cancer. Endocrine Reviews 2012, 33:216-253.
9. Y. Cheng, N.X. Cawley, Y.P. Loh, Carboxypeptidase E/NFa1: A new neurotrophic factor against oxidative stress-induced apoptotic cell death mediated by ERK and PI3-K/AKT pathways, PloS one (2013).
10. Murthy S.R., Pacak K., Loh Y.P. Carboxypeptidase E: elevated expression correlated with tumor growth and metastasis in pheochromocytomas and other cancers. Cellular and Molecular Neurobiology 2010, 30:1377-1381.
11. Lee T.K., Murthy S.R., Cawley N.X., Dhanvantari S., Hewitt S.M., Lou H., Lau T., Ma S., Huynh T., Wesley R.A., Ng I.O., Pacak K., Poon R.T., Loh Y.P. An N-terminal truncated carboxypeptidase E splice isoform induces tumor growth and is a biomarker for predicting future metastasis in human cancers. The Journal of Clinical Investigation 2011, 121:880-892.
12. K. Zhou, H. Liang, Y. Liu, C. Yang, P. Liu, X. Jiang, Overexpression of CPE-DeltaN predicts poor prognosis in colorectal cancer patients. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine (2013).
13. Skalka N., Caspi M., Caspi E., Loh Y.P., Rosin-Arbesfeld R. Carboxypeptidase E: a negative regulator of the canonical Wnt signaling pathway. Oncogene 2012.
14. Murthy S.R., Thouennon E., Li W.S., Cheng Y., Bhupatkar J., Cawley N.X., Lane M., Merchenthaler I., Loh Y.P. Carboxypeptidase E protects hippocampal neurons during Stress in male mice by up-regulating pro-survival BCL2 protein expression. Endocrinology 2013, 10.
15. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proceedings of the National Academy of Sciences of the United States of America 1976, 73:2424-2428.
16. Korzeniewski C., Callewaert D.M. An enzyme-release assay for natural cytotoxicity. Journal of Immunological Methods 1983, 64:313-320.
17. Fricker L.D., Plummer T.H., Snyder S.H. Enkephalin convertase: potent, selective, and irreversible inhibitors. Biochemical and Biophysical Research Communications 1983, 111:994-1000.
18. Jacobson M.D., Raff M.C. Programmed cell death and Bcl-2 protection in very low oxygen. Nature 1995, 374:814-816.
19. Balmanno K., Cook S.J. Tumour cell survival signalling by the ERK1/2 pathway. Cell Death and Differentiation 2009, 16:368-377.
20. Ballif B.A., Blenis J. Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth & Differentiation: the Molecular Biology Journal of the American Association for Cancer Research 2001, 12:397-408.
21. Marshall C.J., Hall A., Weiss R.A. A transforming gene present in human sarcoma cell lines. Nature 1982, 299:171-173.
22. Fan X., Olson S.J., Blevins L.S., Allen G.S., Johnson M.D. Immunohistochemical localization of carboxypeptidases D, E, and Z in pituitary adenomas and normal human pituitary. Journal of Histochemistry and Cytochemistry 2002, 50:1509-1516.
23. He P., Varticovski L., Bowman E.D., Fukuoka J., Welsh J.A., Miura K., Jen J., Gabrielson E., Brambilla E., Travis W.D., Harris C.C. Identification of carboxypeptidase E and gamma-glutamyl hydrolase as biomarkers for pulmonary neuroendocrine tumors by cDNA microarray. Human Pathology 2004, 35:1196-1209.
24. Tang S.S., Zhang J.H., Liu H.X., Li H.Z. PC2/CPE-mediated pro-protein processing in tumor cells and its differentiated cells or tissues. Molecular and Cellular Endocrinology 2009, 303:43-49.
25. Greene D., Das B., Fricker L.D. Regulation of carboxypeptidase E. Effect of pH, temperature and Co2+ on kinetic parameters of substrate hydrolysis. The Biochemical Journal 1992, 285(Pt 2):613-618.
26. Boucher M.J., Morisset J., Vachon P.H., Reed J.C., Laine J., Rivard N. MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-X(L), and Mcl-1 and promotes survival of human pancreatic cancer cells. Journal of Cellular Biochemistry 2000, 79:355-369.
27. Kolch W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. The Biochemical Journal 2000, 351(Pt 2):289-305.
28. Schulze A., Lehmann K., Jefferies H.B., McMahon M., Downward J. Analysis of the transcriptional program induced by Raf in epithelial cells. Genes & Development 2001, 15:981-994.
29. Xaus J., Comalada M., Valledor A.F., Cardo M., Herrero C., Soler C., Lloberas J., Celada A. Molecular mechanisms involved in macrophage survival, proliferation, activation or apoptosis. Immunobiology 2001, 204:543-550.
30. Cakir M., Grossman A.B. Targeting MAPK (Ras/ERK) and PI3K/Akt pathways in pituitary tumorigenesis. Expert Opinion on Therapeutic Targets 2009, 13:1121-1134.
31. Naor Z. Signaling by G-protein-coupled receptor (GPCR): studies on the GnRH receptor. Frontiers in Neuroendocrinology 2009, 30:10-29.
32. Pugazhenthi S., Nesterova A., Sable C., Heidenreich K.A., Boxer L.M., Heasley L.E., Reusch J.E. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. The Journal of Biological Chemistry 2000, 275:10761-10766.
33. de La Coste A., Romagnolo B., Billuart P., Renard C.A., Buendia M.A., Soubrane O., Fabre M., Chelly J., Beldjord C., Kahn A., Perret C. Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:8847-8851.
34. Billadeau D.D. Primers on molecular pathways. The glycogen synthase kinase-3beta. Pancreatology 2007, 7:398-402.
35. Chung E.J., Hwang S.G., Nguyen P., Lee S., Kim J.S., Kim J.W., Henkart P.A., Bottaro D.P., Soon L., Bonvini P., Lee S.J., Karp J.E., Oh H.J., Rubin J.S., Trepel J.B. Regulation of leukemic cell adhesion, proliferation, and survival by beta-catenin. Blood 2002, 100:982-990.
36. Perkins N.D. NF-kappaB: tumor promoter or suppressor?. Trends in Cell Biology 2004, 14:64-69.
37. Ghosh S., Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002, 109(Suppl.):S81-96.
38. Silverman N., Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes & Development 2001, 15:2321-2342.
39. Grimes C.A., Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Progress in Neurobiology 2001, 65:391-426.
40. Meliopoulos V.A., Andersen L.E., Brooks P., Yan X., Bakre A., Coleman J.K., Tompkins S.M., Tripp R.A. MicroRNA regulation of human protease genes essential for influenza virus replication. PLoS ONE 2012, 7:e37169.
41. Persad R., Huynh H.Q., Hao L., Ha J.R., Sergi C., Srivastava R., Persad S. Angiogenic remodeling in pediatric EoE is associated with increased levels of VEGF-A, angiogenin, IL-8, and activation of the TNF-alpha-NFkappaB pathway. Journal of Pediatric Gastroenterology and Nutrition 2012, 55:251-260.
42. Lee C., Hu J., Ralls S., Kitamura T., Loh Y.P., Yang Y., Mukouyama Y.S., Ahn S. The molecular profiles of neural stem cell niche in the adult subventricular zone. PLoS ONE 2012, 7:e50501.
43. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
44. Nguyen A., Rosner A., Milovanovic T., Hope C., Planutis K., Saha B., Chaiwun B., Lin F., Imam S.A., Marsh J.L., Holcombe R.F. Wnt pathway component LEF1 mediates tumor cell invasion and is expressed in human and murine breast cancers lacking ErbB2 (her-2/neu) overexpression. International Journal of Oncology 2005, 27:949-956.