Anterior Gradient-3: A novel biomarker for ovarian cancer that mediates cisplatin resistance in xenograft models

Journal of Immunological Methods

Volumn 378, Issue 1-2, 2012, Pages 20-32

  Gray, Terry A ^a   MacLaine, Nicola J ^a   Michie, Caroline O ^a   Bouchalova, Pavla ^b   Murray, Euan ^a   Howie, Jacqueline ^a   Hrstka, Roman ^b   Maslon, Magdalena M ^a   Nenutil, Rudolf ^b   Vojtesek, Borek ^b   Langdon, Simon ^a   Hayward, Larry ^a   Gourley, Charlie ^a   Hupp, Ted R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MASARYK MEMORIAL CANCER INSTITUTE   (Czech Republic)

Author keywords

AGR2; AGR3; Endoplasmic reticulum; Monoclonal antibody; Ovarian cancer; P53

Indexed keywords

ANTERIOR GRADIENT 2 PROTEIN; ANTERIOR GRADIENT 3 PROTEIN; CISPLATIN; ESTROGEN RECEPTOR; MONOCLONAL ANTIBODY; PROTEIN DISULFIDE ISOMERASE; TUMOR MARKER; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER RESISTANCE; CARCINOGENESIS; CHROMOSOME 7P; CONTROLLED STUDY; CYTOSOL; DISEASE ASSOCIATION; DNA DAMAGE; FEMALE; GENE OVEREXPRESSION; GENETIC SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; TUMOR GENE; TUMOR MODEL; TUMOR XENOGRAFT;

AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; CARRIER PROTEINS; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; EPITOPE MAPPING; FEMALE; HUMANS; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PROTEINS; RECEPTORS, ESTROGEN; TRANSFECTION; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84859422674     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2012.01.013     Document Type: Article

References (57)

1. Aberger F., Weidinger G., Grunz H., Richter K. Anterior specification of embryonic ectoderm: the role of the Xenopus cement gland-specific gene XAG-2. Mech. Dev. 1998, 72:115.
2. Adam P.J., Boyd R., Tyson K.L., Fletcher G.C., Stamps A., Hudson L., Poyser H.R., Redpath N., Griffiths M., Steers G., Harris A.L., Patel S., Berry J., Loader J.A., Townsend R.R., Daviet L., Legrain P., Parekh R., Terrett J.A. Comprehensive proteomic analysis of breast cancer cell membranes reveals unique proteins with potential roles in clinical cancer. J. Biol. Chem. 2003, 278:6482.
3. Alanen H.I., Williamson R.A., Howard M.J., Lappi A.K., Jantti H.P., Rautio S.M., Kellokumpu S., Ruddock L.W. Functional characterization of ERp18, a new endoplasmic reticulum-located thioredoxin superfamily member. J. Biol. Chem. 2003, 278:28912.
4. Appenzeller-Herzog C., Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim. Biophys. Acta 2008, 1783:535.
5. Barraclough D.L., Platt-Higgins A., de Silva Rudland S., Barraclough R., Winstanley J., West C.R., Rudland P.S. The metastasis-associated anterior gradient 2 protein is correlated with poor survival of breast cancer patients. Am. J. Pathol. 2009, 175:1848.
6. Bast R.C., Hennessy B., Mills G.B. The biology of ovarian cancer: new opportunities for translation. Nat. Rev. Cancer 2009, 9:415.
7. Di Valentin E., Crahay C., Garbacki N., Hennuy B., Gueders M., Noel A., Foidart J.M., Grooten J., Colige A., Piette J., Cataldo D. New asthma biomarkers: lessons from murine models of acute and chronic asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296:L185.
8. Dong A., Gupta A., Pai R.K., Tun M., Lowe A.W. The human adenocarcinoma-associated gene, AGR2, induces expression of amphiregulin through Hippo pathway co-activator YAP1 activation. J. Biol. Chem. 2011, 286:18301.
9. Fletcher G.C., Patel S., Tyson K., Adam P.J., Schenker M., Loader J.A., Daviet L., Legrain P., Parekh R., Harris A.L., Terrett J.A. hAG-2 and hAG-3, human homologues of genes involved in differentiation, are associated with oestrogen receptor-positive breast tumours and interact with metastasis gene C4.4a and dystroglycan. Br. J. Cancer 2003, 88:579.
10. Fourtouna A., Murray E., Nicholson J., Maslon M.M., Pang L., Dryden D.T.F., Hupp T.R. The Anterior Gradient-2 pathway as a model for developing peptide-aptamer anti-cancer drug leads that stimulate p53 function. Curr. Chem. Biol. 2009, 3:124.
11. Fritzsche F.R., Dahl E., Dankof A., Burkhardt M., Pahl S., Petersen I., Dietel M., Kristiansen G. Expression of AGR2 in non small cell lung cancer. Histol. Histopathol. 2007, 22:703.
12. Groome M., Lindsay J., Ross P.E., Cotton J.P., Hupp T.R., Dillon J.F. Use of oesophageal stress response proteins as potential biomarkers in the screening for Barrett's oesophagus. Eur. J. Gastroenterol. Hepatol. 2008, 20:961.
13. Hao Y., Triadafilopoulos G., Sahbaie P., Young H.S., Omary M.B., Lowe A.W. Gene expression profiling reveals stromal genes expressed in common between Barrett's esophagus and adenocarcinoma. Gastroenterology 2006, 131:925.
14. Harlow E., Lane D. Antibodies, A Laboratory Manual 1988, CSHL, New York.
15. Hatahet F., Ruddock L.W. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 2009, 11:2807.
16. Hengel, S., Murray, E., Langdon, S., Hayward, R., Hupp, T. and Goodlett, D. (accepted for publication) A PACIFIC proteomics screens identifies AGR2 as a dominant Tamoxifen-induced protein in MCF7 cells. J. Proteome Res. 10, 4567-4578.
17. Hess V., A'Hern R., Nasiri N., King D.M., Blake P.R., Barton D.P., Shepherd J.H., Ind T., Bridges J., Harrington K., Kaye S.B., Gore M.E. Mucinous epithelial ovarian cancer: a separate entity requiring specific treatment. J. Clin. Oncol. 2004, 22:1040.
18. Hopwood D., Moitra S., Vojtesek B., Johnston D.A., Dillon J.F., Hupp T.R. Biochemical analysis of the stress protein response in human oesophageal epithelium. Gut 1997, 41:156.
19. Hrstka R., Nenutil R., Fourtouna A., Maslon M.M., Naughton C., Langdon S., Murray E., Larionov A., Petrakova K., Muller P., Dixon M.J., Hupp T.R., Vojtesek B. The pro-metastatic protein anterior gradient-2 predicts poor prognosis in tamoxifen-treated breast cancers. Oncogene 2010, 29:4838.
20. Iacobuzio-Donahue C.A., Maitra A., Olsen M., Lowe A.W., van Heek N.T., Rosty C., Walter K., Sato N., Parker A., Ashfaq R., Jaffee E., Ryu B., Jones J., Eshleman J.R., Yeo C.J., Cameron J.L., Kern S.E., Hruban R.H., Brown P.O., Goggins M. Exploration of global gene expression patterns in pancreatic adenocarcinoma using cDNA microarrays. Am. J. Pathol. 2003, 162:1151.
21. Innes H.E., Liu D., Barraclough R., Davies M.P., O'Neill P.A., Platt-Higgins A., de Silva Rudland S., Sibson D.R., Rudland P.S. Significance of the metastasis-inducing protein AGR2 for outcome in hormonally treated breast cancer patients. Br. J. Cancer 2006, 94:1057.
22. King E.R., Tung C.S., Tsang Y.T., Zu Z., Lok G.T., Deavers M.T., Malpica A., Wolf J.K., Lu K.H., Birrer M.J., Mok S.C., Gershenson D.M., Wong K.K. The anterior gradient homolog 3 (AGR3) gene is associated with differentiation and survival in ovarian cancer. Am. J. Surg. Pathol. 2011, 35:904.
23. Kristiansen G., Pilarsky C., Wissmann C., Kaiser S., Bruemmendorf T., Roepcke S., Dahl E., Hinzmann B., Specht T., Pervan J., Stephan C., Loening S., Dietel M., Rosenthal A. Expression profiling of microdissected matched prostate cancer samples reveals CD166/MEMD and CD24 as new prognostic markers for patient survival. J. Pathol. 2005, 205:359.
24. Kumar A., Godwin J.W., Gates P.B., Garza-Garcia A.A., Brockes J.P. Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 2007, 318:772.
25. Leedham S.J., Preston S.L., McDonald S.A., Elia G., Bhandari P., Poller D., Harrison R., Novelli M.R., Jankowski J.A., Wright N.A. Individual crypt genetic heterogeneity and the origin of metaplastic glandular epithelium in human Barrett's oesophagus. Gut 2008, 57:1041.
26. Lepreux S., Bioulac-Sage P., Chevet E. Differential expression of the anterior gradient protein-2 is a conserved feature during morphogenesis and carcinogenesis of the biliary tree. Liver Int. 2011, 31:322.
27. Liu D., Rudland P.S., Sibson D.R., Platt-Higgins A., Barraclough R. Human homologue of cement gland protein, a novel metastasis inducer associated with breast carcinomas. Cancer Res. 2005, 65:3796.
28. Lowe A.W., Olsen M., Hao Y., Lee S.P., Taek Lee K., Chen X., van de Rijn M., Brown P.O. Gene expression patterns in pancreatic tumors, cells and tissues. PLoS One 2007, 2:e323.
29. Mackay A., Urruticoechea A., Dixon J.M., Dexter T., Fenwick K., Ashworth A., Drury S., Larionov A., Young O., White S., Miller W.R., Evans D.B., Dowsett M. Molecular response to aromatase inhibitor treatment in primary breast cancer. Breast Cancer Res. 2007, 9:R37.
30. Macleod K., Mullen P., Sewell J., Rabiasz G., Lawrie S., Miller E., Smyth J.F., Langdon S.P. Altered ErbB receptor signaling and gene expression in cisplatin-resistant ovarian cancer. Cancer Res. 2005, 65:6789.
31. Maslon M.M., Hrstka R., Vojtesek B., Hupp T.R. A divergent substrate-binding loop within the pro-oncogenic protein anterior gradient-2 forms a docking site for Reptin. J. Mol. Biol. 2010, 404:418.
32. Missiaglia E., Blaveri E., Terris B., Wang Y.H., Costello E., Neoptolemos J.P., Crnogorac-Jurcevic T., Lemoine N.R. Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int. J. Cancer 2004, 112:100.
33. Murray E., McKenna E.O., Burch L.R., Dillon J., Langridge-Smith P., Kolch W., Pitt A., Hupp T.R. Microarray-formatted clinical biomarker assay development using peptide aptamers to anterior gradient-2. Biochemistry 2007, 46:13742.
34. Nenutil R., Smardova J., Pavlova S., Hanzelkova Z., Muller P., Fabian P., Hrstka R., Janotova P., Radina M., Lane D.P., Coates P.J., Vojtesek B. Discriminating functional and non-functional p53 in human tumours by p53 and MDM2 immunohistochemistry. J. Pathol. 2005, 207:251.
35. Pang L.Y., Scott M., Hayward R.L., Mohammed H., Whitelaw C.B., Smith G.C., Hupp T.R. p21(WAF1) is component of a positive feedback loop that maintains the p53 transcriptional program. Cell Cycle 2011, 10:932.
36. Park S.W., Zhen G., Verhaeghe C., Nakagami Y., Nguyenvu L.T., Barczak A.J., Killeen N., Erle D.J. The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6950.
37. Persson S., Rosenquist M., Knoblach B., Khosravi-Far R., Sommarin M., Michalak M. Diversity of the protein disulfide isomerase family: identification of breast tumor induced Hag2 and Hag3 as novel members of the protein family. Mol. Phylogenet. Evol. 2005, 36:734.
38. Pignata S., Ferrandina G., Scarfone G., Scollo P., Odicino F., Cormio G., Katsaros D., Villa A., Mereu L., Ghezzi F., Manzione L., Lauria R., Breda E., Alletti D.G., Ballardini M., Lombardi A.V., Sorio R., Mangili G., Priolo D., Magni G., Morabito A. Activity of chemotherapy in mucinous ovarian cancer with a recurrence free interval of more than 6 months: results from the SOCRATES retrospective study. BMC Cancer 2008, 8:252.
39. Pohler E., Craig A.L., Cotton J., Lawrie L., Dillon J.F., Ross P., Kernohan N., Hupp T.R. The Barrett's antigen anterior gradient-2 silences the p53 transcriptional response to DNA damage. Mol. Cell. Proteomics 2004, 3:534.
40. Ramachandran V., Arumugam T., Wang H., Logsdon C.D. Anterior gradient 2 is expressed and secreted during the development of pancreatic cancer and promotes cancer cell survival. Cancer Res. 2008, 68:7811.
41. Raykhel I., Alanen H., Salo K., Jurvansuu J., Nguyen V.D., Latva-Ranta M., Ruddock L. A molecular specificity code for the three mammalian KDEL receptors. J. Cell Biol. 2007, 179:1193.
42. Raykhel I., Alanen H., Salo K., Jurvansuu J., Nguyen V.D., Latva-Ranta M., Ruddock L. A molecular specificity code for the three mammalian KDEL receptors. J. Cell Biol. 2007, 179:1193.
43. Sato S., Itamochi H., Kigawa J., Oishi T., Shimada M., Naniwa J., Uegaki K., Nonaka M., Terakawa N. Combination chemotherapy of oxaliplatin and 5-fluorouracil may be an effective regimen for mucinous adenocarcinoma of the ovary: a potential treatment strategy. Cancer Sci. 2009, 100:546.
44. Sive H., Bradley L. A sticky problem: the Xenopus cement gland as a paradigm for anteroposterior patterning. Dev. Dyn. 1996, 205:265.
45. Sive H.L., Hattori K., Weintraub H. Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 1989, 58:171.
46. Smirnov D.A., Zweitzig D.R., Foulk B.W., Miller M.C., Doyle G.V., Pienta K.J., Meropol N.J., Weiner L.M., Cohen S.J., Moreno J.G., Connelly M.C., Terstappen L.W., O'Hara S.M. Global gene expression profiling of circulating tumor cells. Cancer Res. 2005, 65:4993.
47. Thompson D.A., Weigel R.J. hAG-2, the human homologue of the Xenopus laevis cement gland gene XAG-2, is coexpressed with estrogen receptor in breast cancer cell lines. Biochem. Biophys. Res. Commun. 1998, 251:111.
48. Umar A., Kang H., Timmermans A.M., Look M.P., Meijer-van Gelder M.E., den Bakker M.A., Jaitly N., Martens J.W., Luider T.M., Foekens J.A., Pasa-Tolic L. Identification of a putative protein profile associated with tamoxifen therapy resistance in breast cancer. Mol. Cell. Proteomics 2009, 8:1278.
49. Wang Z., Hao Y., Lowe A.W. The adenocarcinoma-associated antigen, AGR2, promotes tumor growth, cell migration, and cellular transformation. Cancer Res. 2008, 68:492.
50. Wang X., Ouyang H., Yamamoto Y., Kumar P.A., Wei T.S., Dagher R., Vincent M., Lu X., Bellizzi A.M., Ho K.Y., Crum C.P., Xian W., McKeon F. Residual embryonic cells as precursors of a Barrett's-like metaplasia. Cell 2011, 145:1023.
51. Workman P., Aboagye E.O., Balkwill F., Balmain A., Bruder G., Chaplin D.J., Double J.A., Everitt J., Farningham D.A., Glennie M.J., Kelland L.R., Robinson V., Stratford I.J., Tozer G.M., Watson S., Wedge S.R., Eccles S.A. Guidelines for the welfare and use of animals in cancer research. Br. J. Cancer 2010, 102:1555.
52. Yagui-Beltran A., Craig A.L., Lawrie L., Thompson D., Pospisilova S., Johnston D., Kernohan N., Hopwood D., Dillon J.F., Hupp T.R. The human oesophageal squamous epithelium exhibits a novel type of heat shock protein response. Eur. J. Biochem. 2001, 268:5343.
53. Zhang Z., Henzel W.J. Signal peptide prediction based on analysis of experimentally verified cleavage sites. Protein Sci. 2004, 13:2819.
54. Zhang J.S., Gong A., Cheville J.C., Smith D.I., Young C.Y. AGR2, an androgen-inducible secretory protein overexpressed in prostate cancer. Genes Chromosomes Cancer 2005, 43:249.
55. Zhang Y., Forootan S.S., Liu D., Barraclough R., Foster C.S., Rudland P.S., Ke Y. Increased expression of anterior gradient-2 is significantly associated with poor survival of prostate cancer patients. Prostate Cancer Prostatic Dis. 2007, 10:293.
56. Zheng W., Rosenstiel P., Huse K., Sina C., Valentonyte R., Mah N., Zeitlmann L., Grosse J., Ruf N., Nurnberg P., Costello C.M., Onnie C., Mathew C., Platzer M., Schreiber S., Hampe J. Evaluation of AGR2 and AGR3 as candidate genes for inflammatory bowel disease. Genes Immun. 2006, 7:11.
57. Zhu H., Lam D.C., Han K.C., Tin V.P., Suen W.S., Wang E., Lam W.K., Cai W.W., Chung L.P., Wong M.P. High resolution analysis of genomic aberrations by metaphase and array comparative genomic hybridization identifies candidate tumour genes in lung cancer cell lines. Cancer Lett. 2007, 245:303.