CCR9 in cancer: Oncogenic role and therapeutic targeting

Journal of Hematology and Oncology

Volumn 9, Issue 1, 2016, Pages

  Tu, Zhenbo ^a   Xiao, Ruijing ^a   Xiong, Jie ^a   Tembo, Kingsley M ^a   Deng, Xinzhou ^a   Xiong, Meng ^a   Liu, Pan ^a   Wang, Meng ^a   Zhang, Qiuping ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Biomarker; CCL25; CCR9; Chemoresistance; Metastasis; Targeting therapy

Indexed keywords

BETA CATENIN; CHEMOKINE; CHEMOKINE CCL25; CHEMOKINE RECEPTOR CCR9; COLLAGEN TYPE 4; GELATINASE A; GELATINASE B; IMMUNOTOXIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CCR9; MULTIDRUG RESISTANCE PROTEIN; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN ERM; PROTEIN KINASE B; STAT PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BETA CHEMOKINE; CC CHEMOKINE RECEPTOR 9; CCL25 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR;

ABSORPTION; CANCER CELL; CANCER RESISTANCE; CARCINOGENICITY; COLLAGEN DEGRADATION; CONFORMATIONAL TRANSITION; CYTOTOXICITY; DRUG RESISTANCE; DRUG TARGETING; DRUG TRANSPORT; GENE; HUMAN; METASTASIS; MICROVILLUS; MOLECULARLY TARGETED THERAPY; NONHUMAN; PARACRINE SIGNALING; POLARIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PTEN GENE; REVIEW; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; METABOLISM; NEOPLASMS; PATHOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CHEMOKINES, CC; DRUG RESISTANCE, NEOPLASM; HUMANS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; NEOPLASMS; RECEPTORS, CCR; SIGNAL TRANSDUCTION;

EID: 84958154947     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-016-0236-7     Document Type: Review

References (66)

1. Weitzenfeld P, Ben-Baruch A. The chemokine system, and its CCR5 and CXCR4 receptors, as potential targets for personalized therapy in cancer. Cancer Lett. 2014;352(1):36-53.
2. Sharma S, Zhu L, Srivastava MK, Harris-White M, Huang M, Lee JM, et al. CCL21 chemokine therapy for lung cancer. Int Trends Immun. 2013;1(1):10-5.
3. Lazennec G, Richmond A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med. 2010;16(3):133-44.
4. Mukaida N, Baba T. Chemokines in tumor development and progression. Exp Cell Res. 2012;318(2):95-102.
5. Sarvaiya PJ, Guo D, Ulasov I, Gabikian P, Lesniak MS. Chemokines in tumor progression and metastasis. Oncotarget. 2013;4(12):2171-85.
6. Valdivia-Silva JE, Franco-Barraza J, Silva AL, Pont GD, Soldevila G, Meza I, et al. Effect of pro-inflammatory cytokine stimulation on human breast cancer: implications of chemokine receptor expression in cancer metastasis. Cancer Lett. 2009;283(2):176-85.
7. Mirandola L, Chiriva-Internati M, Montagna D, Locatelli F, Zecca M, Ranzani M, et al. Notch1 regulates chemotaxis and proliferation by controlling the CC-chemokine receptors 5 and 9 in T cell acute lymphoblastic leukaemia. J Pathol. 2012;226(5):713-22.
8. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11-30.
9. Zhang Z, Qin C, Wu Y, Su Z, Xian G, Hu B. CCR9 as a prognostic marker and therapeutic target in hepatocellular carcinoma. Oncol Rep. 2014;31(4):1629-36.
10. Koga A, Kajihara I, Yamada S, Makino K, Ichihara A, Aoi J, et al. Enhanced CCR9 expression levels in psoriatic skin are associated with poor clinical outcome to infliximab treatment. J Dermatol. 2015.
11. Singh R, Stockard CR, Grizzle WE, Lillard Jr JW, Singh S. Expression and histopathological correlation of CCR9 and CCL25 in ovarian cancer. Int J Oncol. 2011;39(2):373-81.
12. Li B, Wang Z, Zhong Y, Lan J, Li X, Lin H. CCR9-CCL25 interaction suppresses apoptosis of lung cancer cells by activating the PI3K/Akt pathway. Med Oncol. 2015;32(3):66.
13. Shen X, Mailey B, Ellenhorn JD, Chu PG, Lowy AM, Kim J. CC chemokine receptor 9 enhances proliferation in pancreatic intraepithelial neoplasia and pancreatic cancer cells. Journal of gastrointestinal surgery: official journal of the Society for Surgery of the Alimentary Tract. 2009;13(11):1955-62. discussion 1962.
14. Sharma PK, Singh R, Novakovic KR, Eaton JW, Grizzle WE, Singh S. CCR9 mediates PI3K/AKT-dependent antiapoptotic signals in prostate cancer cells and inhibition of CCR9-CCL25 interaction enhances the cytotoxic effects of etoposide. International journal of cancer Journal international du cancer. 2010;127(9):2020-30.
15. Johnson-Holiday C, Singh R, Johnson EL, Grizzle WE, Lillard Jr JW, Singh S. CCR9-CCL25 interactions promote cisplatin resistance in breast cancer cell through Akt activation in a PI3K-dependent and FAK-independent fashion. World journal of surgical oncology. 2011;9:46.
16. Johnson EL, Singh R, Johnson-Holiday CM, Grizzle WE, Partridge EE, Lillard Jr JW, et al. CCR9 interactions support ovarian cancer cell survival and resistance to cisplatin-induced apoptosis in a PI3K-dependent and FAK-independent fashion. Journal of ovarian research. 2010;3:15.
17. Qiuping Z, Jei X, Youxin J, Wei J, Chun L, Jin W, et al. CC chemokine ligand 25 enhances resistance to apoptosis in CD4+ T cells from patients with T-cell lineage acute and chronic lymphocytic leukemia by means of Livin activation. Cancer Res. 2004;64(20):7579-87.
18. Zhang L, Xiao R, Xiong J, Leng J, Ehtisham A, Hu Y, et al. Activated ERM protein plays a critical role in drug resistance of MOLT4 cells induced by CCL25. PLoS One. 2013;8(1):e52384.
19. Khandelwal N, Breinig M, Speck T, Michels T, Kreutzer C, Sorrentino A, et al. A high-throughput RNAi screen for detection of immune-checkpoint molecules that mediate tumor resistance to cytotoxic T lymphocytes. EMBO Mol Med. 2015;7(4):450-63.
20. Lee S, Heinrich EL, Li L, Lu J, Choi AH, Levy RA, et al. CCR9-mediated signaling through beta-catenin and identification of a novel CCR9 antagonist. Mol Oncol. 2015;9(8):1599-611.
21. Johnson EL, Singh R, Singh S, Johnson-Holiday CM, Grizzle WE, Partridge EE, et al. CCL25-CCR9 interaction modulates ovarian cancer cell migration, metalloproteinase expression, and invasion. World journal of surgical oncology. 2010;8:62.
22. Singh S, Singh UP, Stiles JK, Grizzle WE, Lillard Jr JW. Expression and functional role of CCR9 in prostate cancer cell migration and invasion. Clinical cancer research: an official journal of the American Association for Cancer Research. 2004;10(24):8743-50.
23. Gupta P, Sharma PK, Mir H, Singh R, Singh N, Kloecker GH, et al. CCR9/CCL25 expression in non-small cell lung cancer correlates with aggressive disease and mediates key steps of metastasis. Oncotarget. 2014.
24. Wang Y, Yu J, Luo X, Wang X, Li M, Wang L, et al. Abnormal regulation of chemokine TECK and its receptor CCR9 in the endometriotic milieu is involved in pathogenesis of endometriosis by way of enhancing invasiveness of endometrial stromal cells. Cellular & molecular immunology. 2010;7(1):51-60.
25. Qiuping Z, Qun L, Chunsong H, Xiaolian Z, Baojun H, Mingzhen Y, et al. Selectively increased expression and functions of chemokine receptor CCR9 on CD4+ T cells from patients with T-cell lineage acute lymphocytic leukemia. Cancer Res. 2003;63(19):6469-77.
26. Zhou B, Leng J, Hu M, Zhang L, Wang Z, Liu D, et al. Ezrin is a key molecule in the metastasis of MOLT4 cells induced by CCL25/CCR9. Leuk Res. 2010;34(6):769-76.
27. Zhang L, Yu B, Hu M, Wang Z, Liu D, Tong X, et al. Role of Rho-ROCK signaling in MOLT4 cells metastasis induced by CCL25. Leuk Res. 2011;35(1):103-9.
28. Heinrich EL, Arrington AK, Ko ME, Luu C, Lee W, Lu J, et al. Paracrine activation of chemokine receptor CCR9 enhances the invasiveness of pancreatic cancer cells. Cancer microenvironment: official journal of the International Cancer Microenvironment Society. 2013;6(3):241-5.
29. Seidl H, Richtig E, Tilz H, Stefan M, Schmidbauer U, Asslaber M, et al. Profiles of chemokine receptors in melanocytic lesions: de novo expression of CXCR6 in melanoma. Hum Pathol. 2007;38(5):768-80.
30. Amersi FF, Terando AM, Goto Y, Scolyer RA, Thompson JF, Tran AN, et al. Activation of CCR9/CCL25 in cutaneous melanoma mediates preferential metastasis to the small intestine. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008;14(3):638-45.
31. Letsch A, Keilholz U, Schadendorf D, Assfalg G, Asemissen AM, Thiel E, et al. Functional CCR9 expression is associated with small intestinal metastasis. The Journal of investigative dermatology. 2004;122(3):685-90.
32. Nagakubo D, Jin Z, Hieshima K, Nakayama T, Shirakawa AK, Tanaka Y, et al. Expression of CCR9 in HTLV-1+ T cells and ATL cells expressing Tax. International journal of cancer Journal international du cancer. 2007;120(7):1591-7.
33. Miething C, Scuoppo C, Bosbach B, Appelmann I, Nakitandwe J, Ma J, et al. PTEN action in leukaemia dictated by the tissue microenvironment. Nature. 2014;510(7505):402-6.
34. Breton CS, Nahimana A, Aubry D, Macoin J, Moretti P, Bertschinger M, et al. A novel anti-CD19 monoclonal antibody (GBR 401) with high killing activity against B cell malignancies. J Hematol Oncol. 2014;7:33.
35. Wu J, Fu J, Zhang M, Liu D. Blinatumomab: a bispecific T cell engager (BiTE) antibody against CD19/CD3 for refractory acute lymphoid leukemia. J Hematol Oncol. 2015;8:104.
36. Fan D, Li W, Yang Y, Zhang X, Zhang Q, Yan Y, et al. Redirection of CD4+ and CD8+ T lymphocytes via an anti-CD3 x anti-CD19 bi-specific antibody combined with cytosine arabinoside and the efficient lysis of patient-derived B-ALL cells. J Hematol Oncol. 2015;8(1):108.
37. Ehrlich D, Wang B, Lu W, Dowling P, Yuan R. Intratumoral anti-HuD immunotoxin therapy for small cell lung cancer and neuroblastoma. J Hematol Oncol. 2014;7:91.
38. Kuhne MR, Mulvey T, Belanger B, Chen S, Pan C, Chong C, et al. BMS-936564/MDX-1338: a fully human anti-CXCR4 antibody induces apoptosis in vitro and shows antitumor activity in vivo in hematologic malignancies. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013;19(2):357-66.
39. Panjideh H, Muller G, Koch M, Wilde F, Scheu S, Moldenhauer G, et al. Immunotherapy of B-cell non-Hodgkin lymphoma by targeting the chemokine receptor CXCR5 in a preclinical mouse model. International journal of cancer Journal international du cancer. 2014;135(11):2623-32.
40. Ishii T, Ishida T, Utsunomiya A, Inagaki A, Yano H, Komatsu H, et al. Defucosylated humanized anti-CCR4 monoclonal antibody KW-0761 as a novel immunotherapeutic agent for adult T-cell leukemia/lymphoma. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010;16(5):1520-31.
41. Somovilla-Crespo B, Alfonso-Perez M, Cuesta-Mateos C, Carballo-de Dios C, Beltran AE, Terron F, et al. Anti-CCR7 therapy exerts a potent anti-tumor activity in a xenograft model of human mantle cell lymphoma. J Hematol Oncol. 2013;6:89.
42. Chamorro S, Vela M, Franco-Villanueva A, Carramolino L, Gutierrez J, Gomez L, et al. Antitumor effects of a monoclonal antibody to human CCR9 in leukemia cell xenografts. mAbs. 2014;6(4):1000-12.
43. Antignani A, Fitzgerald D. Immunotoxins: the role of the toxin. Toxins. 2013;5(8):1486-502.
44. Mazor R, Eberle JA, Hu X, Vassall AN, Onda M, Beers R, et al. Recombinant immunotoxin for cancer treatment with low immunogenicity by identification and silencing of human T-cell epitopes. Proc Natl Acad Sci U S A. 2014;111(23):8571-6.
45. Fan G, Wang Z, Hao M, Li J. Bispecific antibodies and their applications. J Hematol Oncol. 2015;8(1):130.
46. Suresh T, Lee LX, Joshi J, Barta SK. New antibody approaches to lymphoma therapy. J Hematol Oncol. 2014;7:58.
47. Fonseca NA, Gregorio AC, Valerio-Fernandes A, Simoes S, Moreira JN. Bridging cancer biology and the patients' needs with nanotechnology-based approaches. Cancer Treat Rev. 2014;40(5):626-35.
48. Unger E, Porter T, Lindner J, Grayburn P. Cardiovascular drug delivery with ultrasound and microbubbles. Adv Drug Deliv Rev. 2014;72:110-26.
49. Yu Y, Zhang M, Zhang X, Cai Q, Hong S, Jiang W, et al. Synergistic effects of combined platelet-activating factor receptor and epidermal growth factor receptor targeting in ovarian cancer cells. J Hematol Oncol. 2014;7:39.
50. Liu W, Onda M, Lee B, Kreitman RJ, Hassan R, Xiang L, et al. Recombinant immunotoxin engineered for low immunogenicity and antigenicity by identifying and silencing human B-cell epitopes. Proc Natl Acad Sci U S A. 2012;109(29):11782-7.
51. Smith AD, Roda D, Yap TA. Strategies for modern biomarker and drug development in oncology. J Hematol Oncol. 2014;7:70.
52. Bera TK, Onda M, Kreitman RJ, Pastan I. An improved recombinant Fab-immunotoxin targeting CD22 expressing malignancies. Leuk Res. 2014;38(10):1224-9.
53. Weldon JE, Xiang L, Zhang J, Beers R, Walker DA, Onda M, et al. A recombinant immunotoxin against the tumor-associated antigen mesothelin reengineered for high activity, low off-target toxicity, and reduced antigenicity. Mol Cancer Ther. 2013;12(1):48-57.
54. Wayne AS, Fitzgerald DJ, Kreitman RJ, Pastan I. Immunotoxins for leukemia. Blood. 2014;123(16):2470-7.
55. Hu Y, Zhang L, Wu R, Han R, Jia Y, Jiang Z, et al. Specific killing of CCR9 high-expressing acute T lymphocytic leukemia cells by CCL25 fused with PE38 toxin. Leuk Res. 2011;35(9):1254-60.
56. Tong X, Zhang L, Zhang L, Hu M, Leng J, Yu B, et al. The mechanism of chemokine receptor 9 internalization triggered by interleukin 2 and interleukin 4. Cellular & molecular immunology. 2009;6(3):181-9.
57. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124-8.
58. Fusi A, Liu Z, Kummerlen V, Nonnemacher A, Jeske J, Keilholz U. Expression of chemokine receptors on circulating tumor cells in patients with solid tumors. J Transl Med. 2012;10:52.
59. Kuhnelt-Leddihn L, Muller H, Eisendle K, Zelger B, Weinlich G. Overexpression of the chemokine receptors CXCR4, CCR7, CCR9, and CCR10 in human primary cutaneous melanoma: a potential prognostic value for CCR7 and CCR10? Arch Dermatol Res. 2012;304(3):185-93.
60. Rehm A, Anagnostopoulos I, Gerlach K, Broemer M, Scheidereit C, Johrens K, et al. Identification of a chemokine receptor profile characteristic for mediastinal large B-cell lymphoma. International journal of cancer Journal international du cancer. 2009;125(10):2367-74.
61. Deutsch AJ, Steinbauer E, Hofmann NA, Strunk D, Gerlza T, Beham-Schmid C, et al. Chemokine receptors in gastric MALT lymphoma: loss of CXCR4 and upregulation of CXCR7 is associated with progression to diffuse large B-cell lymphoma. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2013;26(2):182-94.
62. Wu W, Doan N, Said J, Karunasiri D, Pullarkat ST. Strong expression of chemokine receptor CCR9 in diffuse large B-cell lymphoma and follicular lymphoma strongly correlates with gastrointestinal involvement. Hum Pathol. 2014;45(7):1451-8.
63. Fan J, Zhang L, Wang Q, Lin H. Chemokine receptor 9 high-expression involved in the migration and invasion of the non-small-cell lung cancer cells. Asian Biomedicine. 2011;5(1):7.
64. Johnson-Holiday C, Singh R, Johnson E, Singh S, Stockard CR, Grizzle WE, et al. CCL25 mediates migration, invasion and matrix metalloproteinase expression by breast cancer cells in a CCR9-dependent fashion. Int J Oncol. 2011;38(5):1279-85.
65. Chen HJ, Edwards R, Tucci S, Bu P, Milsom J, Lee S, et al. Chemokine 25-induced signaling suppresses colon cancer invasion and metastasis. J Clin Invest. 2012;122(9):3184-96.
66. Ye LF, Huang J, Zhang LP, Chen Z. Intracellular expression profile and clinical significance of the CCR9-CCL25 chemokine receptor complex in nasopharyngeal carcinoma. J Laryngol Otol. 2015;129(10):1013-9.