CCR9-mediated signaling through β-catenin and identification of a novel CCR9 antagonist

Molecular Oncology

Volumn 9, Issue 8, 2015, Pages 1599-1611

  Lee, Sangjun ^a   Heinrich, Eileen L ^a   Li, Lily ^a   Lu, Jianming ^a   Choi, Audrey H ^a   Levy, Rachel A ^a   Wagner, Jeffrey E ^a   Yip, M L Richard ^b   Vaidehi, Nagarajan ^a   Kim, Joseph ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

CCL25; CCR9; Drug resistance; Pancreatic cancer; catenin

Indexed keywords

BETA CATENIN; CHEMOKINE RECEPTOR CCR ANTAGONIST; CHEMOKINE RECEPTOR CCR9; CYCLIN D1; CYCLIN E; GEMCITABINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UVOMORULIN; VERCIRNON; WNT PROTEIN; ANTINEOPLASTIC AGENT; BETA CHEMOKINE; CC CHEMOKINE RECEPTOR 9; CCL25 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR;

ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER RESISTANCE; CELL PROLIFERATION; COMPUTER MODEL; CONTROLLED STUDY; DRUG BINDING SITE; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; HUMAN; HUMAN CELL; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR INVASION; ANTAGONISTS AND INHIBITORS; BIOLOGY; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECTS; DRUG SCREENING; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR DOCKING; MOLECULARLY TARGETED THERAPY; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; WNT SIGNALING PATHWAY;

ANTINEOPLASTIC AGENTS; BETA CATENIN; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINES, CC; COMPUTATIONAL BIOLOGY; DRUG DISCOVERY; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; HUMANS; MOLECULAR DOCKING SIMULATION; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; RECEPTORS, CCR; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84942192022     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2015.04.012     Document Type: Article

References (39)

1. 2012. CCR9 Program - Overview. http://www.chemocentryx.com/about/overview.html.
2. Al-Aynati M.M., Radulovich N., Riddell R.H., Tsao M.S. Epithelial-cadherin and beta-catenin expression changes in pancreatic intraepithelial neoplasia. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2004, 10:1235-1240.
3. Amersi F.F., Terando A.M., Goto Y., Scolyer R.A., Thompson J.F., Tran A.N., Faries M.B., Morton D.L., Hoon D.S. Activation of CCR9/CCL25 in cutaneous melanoma mediates preferential metastasis to the small intestine. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2008, 14:638-645.
4. Ballesteros J.A., Weinstein H., Stuart C.S. [19] Integrated Methods for the Construction of Three-dimensional Models and Computational Probing of Structure-function Relations in G Protein-coupled Receptors, Methods in Neurosciences 1995, 366-428. Academic Press.
5. Berendsen H.J.C., van der Spoel D., van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Computer Phys. Commun. 1995, 91:43-56.
6. Botrugno O.A., Fayard E., Annicotte J.S., Haby C., Brennan T., Wendling O., Tanaka T., Kodama T., Thomas W., Auwerx J., Schoonjans K. Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation. Mol. Cel. 2004, 15:499-509.
7. Chen H.J., Edwards R., Tucci S., Bu P., Milsom J., Lee S., Edelmann W., Gumus Z.H., Shen X., Lipkin S. Chemokine 25-induced signaling suppresses colon cancer invasion and metastasis. J. Clin. Invest. 2012, 122:3184-3196.
8. Davidson G., Niehrs C. Emerging links between CDK cell cycle regulators and Wnt signaling. Trends Cell Biol. 2010, 20:453-460.
9. Froeling F.E., Feig C., Chelala C., Dobson R., Mein C.E., Tuveson D.A., Clevers H., Hart I.R., Kocher H.M. Retinoic acid-induced pancreatic stellate cell quiescence reduces paracrine Wnt-beta-catenin signaling to slow tumor progression. Gastroenterology 2011, 141:1486-1497.
10. Hall S.E., Mao A., Nicolaidou V., Finelli M., Wise E.L., Nedjai B., Kanjanapangka J., Harirchian P., Chen D., Selchau V., Ribeiro S., Schyler S., Pease J.E., Horuk R., Vaidehi N. Elucidation of binding sites of dual antagonists in the human chemokine receptors CCR2 and CCR5. Mol. Pharmacol. 2009, 75:1325-1336.
11. Heinrich E.L., Arrington A.K., Ko M.E., Luu C., Lee W., Lu J., Kim J. Paracrine activation of chemokine receptor CCR9 enhances the invasiveness of pancreatic Cancer cells. Cancer Microenviron. 2013, 6:241-245.
12. Johnson-Holiday C., Singh R., Johnson E., Singh S., Stockard C.R., Grizzle W.E., Lillard J.W. CCL25 mediates migration, invasion and matrix metalloproteinase expression by breast cancer cells in a CCR9-dependent fashion. Int. J. Oncol. 2011, 38:1279-1285.
13. Kikuta K., Masamune A., Watanabe T., Ariga H., Itoh H., Hamada S., Satoh K., Egawa S., Unno M., Shimosegawa T. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem. Biophys. Res. Commun. 2010, 403:380-384.
14. Kim J., Yip M.L., Shen X., Li H., Hsin L.Y., Labarge S., Heinrich E.L., Lee W., Lu J., Vaidehi N. Identification of anti-malarial compounds as novel antagonists to chemokine receptor CXCR4 in pancreatic cancer cells. PLoS One 2012, 7:e31004.
15. Kwon C., Cheng P., King I.N., Andersen P., Shenje L., Nigam V., Srivastava D. Notch post-translationally regulates beta-catenin protein in stem and progenitor cells. Nat. Cel. Biol. 2011, 13:1244-1251.
16. Lam A.R., Bhattacharya S., Patel K., Hall S.E., Mao A., Vaidehi N. Importance of receptor flexibility in binding of cyclam compounds to the chemokine receptor CXCR4. J. Chem. Inf. Model. 2011, 51:139-147.
17. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 2007, 23:2947-2948.
18. Le Maithao N., S.X., Lee Wendy, Duldulao Marjun Philip, Garcia-Aguilar Julio, Kim Joseph Paradoxical cross-talk between the Stat3 and MAPK pathways in CCL25-CCR9 mediated pancreatic cancer growth and proliferation. J. Clin. Oncol. 2012, 30(Suppl. 4). (abstr 231).
19. Li J., Zhou B.P. Activation of beta-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011, 11:49.
20. Li Y.J., Wei Z.M., Meng Y.X., Ji X.R. Beta-catenin up-regulates the expression of cyclinD1, c-myc and MMP-7 in human pancreatic cancer: relationships with carcinogenesis and metastasis. World J. Gastroenterol. 2005, 11:2117-2123.
21. Louvet C., Labianca R., Hammel P., Lledo G., Zampino M.G., Andre T., Zaniboni A., Ducreux M., Aitini E., Taieb J., Faroux R., Lepere C., de Gramont A. Gemcitabine in combination with oxaliplatin compared with gemcitabine alone in locally advanced or metastatic pancreatic cancer: results of a GERCOR and GISCAD phase III trial. J. Clin. Oncol. 2005, 23:3509-3516.
22. Masyuk M., Brand-Saberi B. Recruitment of skeletal muscle progenitors to secondary sites: a role for CXCR4/SDF-1 signalling in skeletal muscle development. Results Probl. Cel. Differ. 2015, 56:1-23.
23. Morris J.P.t., Wang S.C., Hebrok M. KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat. Rev. Cancer 2010, 10:683-695.
24. Oettle H., Post S., Neuhaus P., Gellert K., Langrehr J., Ridwelski K., Schramm H., Fahlke J., Zuelke C., Burkart C., Gutberlet K., Kettner E., Schmalenberg H., Weigang-Koehler K., Bechstein W.O., Niedergethmann M., Schmidt-Wolf I., Roll L., Doerken B., Riess H. Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA 2007, 297:267-277.
25. Rogers H.A., Sousa S., Salto C., Arenas E., Coyle B., Grundy R.G. WNT/beta-catenin pathway activation in Myc immortalised cerebellar progenitor cells inhibits neuronal differentiation and generates tumours resembling medulloblastoma. Br. J. Cancer 2012, 107:1144-1152.
26. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234:779-815.
27. Shah A.N., Summy J.M., Zhang J., Park S.I., Parikh N.U., Gallick G.E. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann. Surg. Oncol. 2007, 14:3629-3637.
28. Shen X., Mailey B., Ellenhorn J.D., Chu P.G., Lowy A.M., Kim J. CC chemokine receptor 9 enhances proliferation in pancreatic intraepithelial neoplasia and pancreatic cancer cells. J. Gastrointest. Surg. 2009, 13:1955-1962.
29. Singh R., Stockard C.R., Grizzle W.E., Lillard J.W., Singh S. Expression and histopathological correlation of CCR9 and CCL25 in ovarian cancer. Int. J. Oncol. 2011, 39:373-381.
30. Vaidehi N., Pease J.E., Horuk R. Modeling small molecule-compound binding to G-protein-coupled receptors. Methods Enzymol. 2009, 460:263-288.
31. Valenta T., Hausmann G., Basler K. The many faces and functions of beta-catenin. EMBO J. 2012, 31:2714-2736.
32. Vermeulen L., De Sousa E.M.F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., Sprick M.R., Kemper K., Richel D.J., Stassi G., Medema J.P. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cel. Biol. 2010, 12:468-476.
33. Vicari A.P., Figueroa D.J., Hedrick J.A., Foster J.S., Singh K.P., Menon S., Copeland N.G., Gilbert D.J., Jenkins N.A., Bacon K.B., Zlotnik A. TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development. Immunity 1997, 7:291-301.
34. Vlad A., Rohrs S., Klein-Hitpass L., Muller O. The first five years of the Wnt targetome. Cell Signal. 2008, 20:795-802.
35. Wu B., Chien E.Y., Mol C.D., Fenalti G., Liu W., Katritch V., Abagyan R., Brooun A., Wells P., Bi F.C., Hamel D.J., Kuhn P., Handel T.M., Cherezov V., Stevens R.C. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science (New York, N.Y.) 2010, 330:1066-1071.
36. Youn B.S., Kim Y.J., Mantel C., Yu K.Y., Broxmeyer H.E. Blocking of c-FLIP(L)-independent cycloheximide-induced apoptosis or Fas-mediated apoptosis by the CC chemokine receptor 9/TECK interaction. Blood 2001, 98:925-933.
37. Zaballos A., Gutierrez J., Varona R., Ardavin C., Marquez G. Cutting edge: identification of the orphan chemokine receptor GPR-9-6 as CCR9, the receptor for the chemokine TECK. J. Immunol. 1999, 162:5671-5675.
38. Zeng G., Germinaro M., Micsenyi A., Monga N.K., Bell A., Sood A., Malhotra V., Sood N., Midda V., Monga D.K., Kokkinakis D.M., Monga S.P. Aberrant Wnt/beta-catenin signaling in pancreatic adenocarcinoma. Neoplasia (New York, N.Y.) 2006, 8:279-289.
39. Zlotnik A., Burkhardt A.M., Homey B. Homeostatic chemokine receptors and organ-specific metastasis. Nat. Rev. Immunol. 2011, 11:597-606.