CCR9/CCL25 expression in non-small cell lung cancer correlates with aggressive disease and mediates key steps of metastasis

Oncotarget

Volumn 5, Issue 20, 2014, Pages 10170-10179

  Gupta, Pranav ^a   Sharma, Praveen K ^b   Mir, Hina ^a   Singh, Rajesh ^a   Singh, Nalinaksha ^a   Kloecker, Goetz H ^c   Lillard, James W ^a   Singh, Shailesh ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b CENTRAL UNIVERSITY OF JHARKHAND   (India)

^c University of Louisville School of Medicine   (United States)

Author keywords

Ccl25; Ccr9; Chemokine receptor; Non small cell lung cancer

Indexed keywords

CHEMOKINE RECEPTOR CCR; CHEMOKINE RECEPTOR CCR9; MATRIX METALLOPROTEINASE; PROTEIN CCL25; TISSUE INHIBITOR OF METALLOPROTEINASE; UNCLASSIFIED DRUG; BETA CHEMOKINE; CC CHEMOKINE RECEPTOR 9; CCL25 PROTEIN, HUMAN;

ARTICLE; CANCER CELL LINE; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; METASTASIS; NON SMALL CELL LUNG CANCER; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SQUAMOUS CELL LUNG CARCINOMA; TISSUE LEVEL; ADENOCARCINOMA; BIOSYNTHESIS; BLOOD; CASE CONTROL STUDY; DISEASE COURSE; LUNG TUMOR; METABOLISM; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE;

ADENOCARCINOMA; CARCINOMA, NON-SMALL-CELL LUNG; CASE-CONTROL STUDIES; CELL LINE, TUMOR; CHEMOKINES, CC; DISEASE PROGRESSION; HUMANS; LUNG NEOPLASMS; NEOPLASM METASTASIS; PROGNOSIS; RECEPTORS, CCR;

EID: 84923376873     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2526     Document Type: Article

References (49)

1. Yang P, Allen MS, Aubry MC, Wampfler JA, Marks RS, Edell ES, Thibodeau S, Adjei AA, Jett J, Deschamps C. Clinical features of 5,628 primary lung cancer patients: experience at Mayo Clinic from 1997 to 2003. Chest 2005; 128:452-62.
2. Montazeri A, Milroy R, Hole D, McEwen J, Gillis CR. Quality of life in lung cancer patients: as an important prognostic factor. Lung Cancer 2001; 31:233-40.
3. Potti A, Abdel-Raheem M, Levitt R, Schell DA, Mehdi SA. Intramedullary spinal cord metastases (ISCM) and non-small cell lung carcinoma (NSCLC): clinical patterns, diagnosis and therapeutic considerations. Lung Cancer 2001; 31:319-23.
4. Spano J-P, Andre F, Morat L, Sabatier L, Besse B, Combadiere C, Deterre P, Martin A, Azorin J, Valeyre D, et al. Chemokine receptor CXCR4 and early-stage non-small cell lung cancer: pattern of expression and correlation with outcome. Ann Oncol 2004; 15:613-7.
5. Svensson M, Agace WW. Role of CCL25/CCR9 in immune homeostasis and disease. Expert Rev Clin Immunol 2006; 2:759-73.
6. Mukaida N, Sasaki S-I, Baba T. Chemokines in cancer development and progression and their potential as targeting molecules for cancer treatment. Mediators Inflamm 2014; 2014:170381.
7. Chen HJ, Edwards R, Tucci S, Bu P, Milsom J, Lee S, Edelmann W, Gümüs ZH, Shen X, Lipkin S. Chemokine 25-induced signaling suppresses colon cancer invasion and metastasis. J Clin Invest 2012; 122:3184-96.
8. Singh S, Singh UP, Stiles JK, Grizzle WE, Lillard JW. Expression and functional role of CCR9 in prostate cancer cell migration and invasion. Clin Cancer Res 2004; 10:8743-50.
9. Singh R, Stockard CR, Grizzle WE, Lillard JW, Singh S. Expression and histopathological correlation of CCR9 and CCL25 in ovarian cancer. Int J Oncol 2011; 39:373-81.
10. Johnson-Holiday C, Singh R, Johnson E, Singh S, Stockard CR, Grizzle WE, Lillard JW. CCL25 mediates migration, invasion and matrix metalloproteinase expression by breast cancer cells in a CCR9-dependent fashion. Int J Oncol 2011; 38:1279-85.
11. Johnson EL, Singh R, Singh S, Johnson-Holiday CM, Grizzle WE, Partridge EE, Lillard JW. CCL25-CCR9 interaction modulates ovarian cancer cell migration, metalloproteinase expression, and invasion. World J Surg Oncol 2010; 8:62.
12. Johnson EL, Singh R, Johnson-Holiday CM, Grizzle WE, Partridge EE, Lillard JW, Singh S. CCR9 interactions support ovarian cancer cell survival and resistance to cisplatin-induced apoptosis in a PI3K-dependent and FAK-independent fashion. J Ovarian Res 2010; 3:15.
13. Su L, Zhang J, Xu H, Wang Y, Chu Y, Liu R, Xiong S. Differential expression of CXCR4 is associated with the metastatic potential of human non-small cell lung cancer cells. Clin Cancer Res 2005; 11:8273-80.
14. Zhu YM, Webster SJ, Flower D, Woll PJ. Interleukin-8/CXCL8 is a growth factor for human lung cancer cells. Br J Cancer 2004; 91:1970-6.
15. Phillips RJ, Burdick MD, Lutz M, Belperio JA, Keane MP, Strieter RM. The stromal derived factor-1/CXCL12-CXC chemokine receptor 4 biological axis in non-small cell lung cancer metastases. Am J Respir Crit Care Med 2003; 167:1676-86.
16. Saintigny P, Massarelli E, Lin S, Ahn Y-H, Chen Y, Goswami S, Erez B, O'Reilly MS, Liu D, Lee JJ, et al. CXCR2 expression in tumor cells is a poor prognostic factor and promotes invasion and metastasis in lung adenocarcinoma. Cancer Res 2013; 73:571-82.
17. Chen JJW, Yao P-L, Yuan A, Hong T-M, Shun C-T, Kuo M-L, Lee Y-C, Yang P-C. Up-regulation of tumor interleukin-8 expression by infiltrating macrophages: its correlation with tumor angiogenesis and patient survival in non-small cell lung cancer. Clin Cancer Res 2003; 9:729-37.
18. Wang JM, Deng X, Gong W, Su S. Chemokines and their role in tumor growth and metastasis. J Immunol Methods 1998; 220:1-17.
19. Zlotnik A. Chemokines in neoplastic progression. Semin Cancer Biol 2004; 14:181-5.
20. Sivrikoz ON, Doganay L, Sivrikoz UK, Karaarslan S, Sanal SM. Distribution of CXCR4 and γ-catenin expression pattern in breast cancer subtypes and their relationship to axillary nodal involvement. Pol J Pathol 2013; 64:253-9.
21. Wang W-N, Chen Y, Zhang Y-D, Hu T-H. The regulatory mechanism of CCR7 gene expression and its involvement in the metastasis and progression of gastric cancer. Tumour Biol 2013; 34:1865-71.
22. Wald O, Shapira OM, Izhar U. CXCR4/CXCL12 axis in non small cell lung cancer (NSCLC) pathologic roles and therapeutic potential. Theranostics 2013; 3:26-33.
23. Rhee Y-H, Chung P-S, Kim S-H, Ahn JC. CXCR4 and PTEN are involved in the anti-metastatic regulation of anethole in DU145 prostate cancer cells. Biochem Biophys Res Commun 2014; 447:557-62.
24. Sekiya R, Kajiyama H, Sakai K, Umezu T, Mizuno M, Shibata K, Yamamoto E, Fujiwara S, Nagasaka T, Kikkawa F. Expression of CXCR4 indicates poor prognosis in patients with clear cell carcinoma of the ovary. Hum Pathol 2012; 43:904-10.
25. Wang L, Wang Z, Liu X, Liu F. High-level C-X-C chemokine receptor type 4 expression correlates with brain-specific metastasis following complete resection of non-small cell lung cancer. Oncol Lett 2014; 7:1871-6.
26. Haibi El CP, Sharma PK, Singh R, Johnson PR, Suttles J, Singh S, Lillard JW. PI3Kp110-, Src-, FAK-dependent and DOCK2-independent migration and invasion of CXCL13-stimulated prostate cancer cells. Mol Cancer 2010; 9:85.
27. Biswas S, Sengupta S, Roy Chowdhury S, Jana S, Mandal G, Mandal PK, Saha N, Malhotra V, Gupta A, Kuprash DV, et al. CXCL13-CXCR5 co-expression regulates epithelial to mesenchymal transition of breast cancer cells during lymph node metastasis. Breast Cancer Res Treat 2014; 143:265-76.
28. 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. Int J Cancer 2010; 127:2020-30.
29. Ichinose Y, Yano T, Asoh H, Yokoyama H. Prognostic factors obtained by a pathologic examination in completely resected non-small-cell lung cancer. An analysis in each pathologic stage. J Thorac Cardiovasc Surg 1995; 110: 601-5.
30. Suzuki K, Nagai K, Yoshida J, Nishimura M, Takahashi K, Yokose T, Nishiwaki Y. Conventional clinicopathologic prognostic factors in surgically resected nonsmall cell lung carcinoma. A comparison of prognostic factors for each pathologic TNM stage based on multivariate analyses. Cancer 1999; 86:1976-84.
31. Mirsadraee S, Oswal D, Alizadeh Y, Caulo A, van Beek E. The 7th lung cancer TNM classification and staging system: Review of the changes and implications. World J Radiol 2012; 4:128-34.
32. Saintigny P, Burger JA. Recent advances in non-small cell lung cancer biology and clinical management. Discov Med 2012; 13:287-97.
33. Panse J, Friedrichs K, Marx A, Hildebrandt Y, Luetkens T, Barrels K, Horn C, Stahl T, Cao Y, Milde-Langosch K, et al. Chemokine CXCL13 is overexpressed in the tumour tissue and in the peripheral blood of breast cancer patients. Br J Cancer 2008; 99:930-8.
34. Del Grosso F, Coco S, Scaruffi P, Stigliani S, Valdora F, Benelli R, Salvi S, Boccardo S, Truini M, Croce M, et al. Role of CXCL13-CXCR5 crosstalk between malignant neuroblastoma cells and Schwannian stromal cells in neuroblastic tumors. Mol Cancer Res 2011; 9:815-23.
35. Signoret N, Hewlett L, Wavre S, Pelchen-Matthews A, Oppermann M, Marsh M. Agonist-induced endocytosis of CC chemokine receptor 5 is clathrin dependent. Mol Biol Cell 2005; 16:902-17.
36. Schmalfeldt B, Prechtel D, Härting K, Späthe K, Rutke S, Konik E, Fridman R, Berger U, Schmitt M, Kuhn W, et al. Increased expression of matrix metalloproteinases (MMP)- 2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer. Clin Cancer Res 2001; 7:2396-404.
37. Singh S, Singh R, Singh UP, Rai SN, Novakovic KR, Chung LWK, Didier PJ, Grizzle WE, Lillard JW. Clinical and biological significance of CXCR5 expressed by prostate cancer specimens and cell lines. Int J Cancer 2009; 125:2288-95.
38. DI Carlo A. Matrix metalloproteinase-2 and -9 and tissue inhibitor of metalloproteinase-1 and -2 in sera and urine of patients with renal carcinoma. Oncol Lett 2014; 7:621-6.
39. Radenkovic S, Konjevic G, Jurisic V, Karadzic K, Nikitovic M, Gopcevic K. Values of MMP-2 and MMP-9 in tumor tissue of basal-like breast cancer patients. Cell Biochem Biophys 2014; 68:143-52.
40. Bourboulia D, Stetler-Stevenson WG. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): Positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 2010; 20:161-8.
41. Schelter F, Grandl M, Seubert B, Schaten S, Hauser S, Gerg M, Boccaccio C, Comoglio P, Krüger A. Tumor cell-derived Timp-1 is necessary for maintaining metastasis-promoting Met-signaling via inhibition of Adam-10. Clin Exp Metastasis 2011; 28:793-802.
42. Fu ZY, Lv JH, Ma CY, Yang DP, Wang T. Tissue inhibitor of metalloproteinase-1 decreased chemosensitivity of MDA-435 breast cancer cells to chemotherapeutic drugs through the PI3K/AKT/NF-k{cyrillic}B pathway. Biomed Pharmacother 2011; 65:163-7.
43. Sun J, Stetler-Stevenson WG. Overexpression of tissue inhibitors of metalloproteinase 2 up-regulates NF-kappaB activity in melanoma cells. J Mol Signal 2009; 4:4.
44. Gong Y, Scott E, Lu R, Xu Y, Oh WK, Yu Q. TIMP-1 promotes accumulation of cancer associated fibroblasts and cancer progression. PLoS ONE 2013; 8:e77366.
45. Yamashita K, Suzuki M, Iwata H, Koike T, Hamaguchi M, Shinagawa A, Noguchi T, Hayakawa T. Tyrosine phosphorylation is crucial for growth signaling by tissue inhibitors of metalloproteinases (TIMP-1 and TIMP-2). FEBS Lett 1996; 396:103-7.
46. Nemeth JA, Rafe A, Steiner M, Goolsby CL. TIMP-2 growth-stimulatory activity: a concentration- and cell type-specific response in the presence of insulin. Exp Cell Res 1996; 224:110-5.
47. Lizárraga F, Maldonado V, Meléndez-Zajgla J. Tissue inhibitor of metalloproteinases-2 growth-stimulatory activity is mediated by nuclear factor-kappa B in A549 lung epithelial cells. Int J Biochem Cell Biol 2004; 36:1655-63.
48. Stetler-Stevenson WG. The tumor microenvironment: regulation by MMP-independent effects of tissue inhibitor of metalloproteinases-2. Cancer Metastasis Rev 2008; 27:57-66.
49. Hoegy SE, Oh HR, Corcoran ML, Stetler-Stevenson WG. Tissue inhibitor of metalloproteinases-2 (TIMP-2) suppresses TKR-growth factor signaling independent of metalloproteinase inhibition. J Biol Chem 2001; 276:3203-14.