Circulating galectins-2,-4 and-8 in cancer patients make important contributions to the increased circulation of several cytokines and chemokines that promote angiogenesis and metastasis

British Journal of Cancer

Volumn 110, Issue 3, 2014, Pages 741-752

  Chen, C ^a   Duckworth, C A ^a   Fu, B ^b   Pritchard, D M ^b   Rhodes, J M ^b   Yu, L G ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

angiogenesis; chemokines; galectins; metastasis

Indexed keywords

ANIMALS; CHEMOKINE CCL2; CHEMOKINE CXCL1; GALECTIN 2; GALECTIN 4; GALECTINS; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-6; MICE; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84893747550     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.793     Document Type: Article

References (56)

1. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, Manova-Todorova K, Leversha M, Hogg N, Seshan VE, Norton L, Brogi E, Massague J (2012) A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150(1): 165-178.
2. Ara T, Declerck YA (2010) Interleukin-6 in bone metastasis and cancer progression. Eur J Cancer 46(7): 1223-1231.
3. Ara T, Song L, Shimada H, Keshelava N, Russell HV, Metelitsa LS, Groshen SG, Seeger RC, DeClerck YA (2009) Interleukin-6 in the bone marrow microenvironment promotes the growth and survival of neuroblastoma cells. Cancer Res 69(1): 329-337.
4. Bandapalli OR, Ehrmann F, Ehemann V, Gaida M, Macher-Goeppinger S, Wente M, Schirmacher P, Brand K (2012) Down-regulation of CXCL1 inhibits tumor growth in colorectal liver metastasis. Cytokine 57(1): 46-53.
5. Barrow H, Guo X, Wandall HH, Pedersen JW, Fu B, Zhao Q, Chen C, Rhodes JM, Yu LG (2011a) Serum galectin-2,-4, and-8 are greatly increased in colon and breast cancer patients and promote cancer cell adhesion to blood vascular endothelium. Clin Cancer Res 17(22): 7035-7046.
6. Barrow H, Rhodes JM, Yu L-G (2011b) The role of galectins in colorectal cancer progression. Int J Cancer 129: 1-8.
7. Barrow H, Rhodes JM, Yu LG (2013) Simultaneous determination of serum galectin-3 and-4 levels detects metastases in colorectal cancer patients. Cell Oncol 36(1): 9-13.
8. Bresalier RS, Byrd JC, Tessler D, Lebel J, Koomen J, Hawke D, Half E, Liu KF, Mazurek N. Great Lakes-New England C, Epidemiology Center of the Early Detection Research N (2004) A circulating ligand for galectin-3 is a haptoglobin-related glycoprotein elevated in individuals with colon cancer. Gastroenterology 127(3): 741-748.
9. Cederfur C, Salomonsson E, Nilsson J, Halim A, Oberg CT, Larson G, Nilsson UJ, Leffler H (2008) Different affinity of galectins for human serum glycoproteins: galectin-3 binds many protease inhibitors and acute phase proteins. Glycobiology 18(5): 384-394.
10. Chen C, Duckworth CA, Zhao Q, Pritchard DM, Rhodes JM, Yu LG (2013) Increased circulation of galectin-3 in cancer induces secretion of metastasis-promoting cytokines from blood vascular endothelium. Clin Cancer Res 19(7): 1693-1704.
11. Chin AR, Wang SE (2013) Cytokines driving breast cancer stemness. Mol Cell Endocri 382(1): 598-602.
12. Chiu HY, Sun KH, Chen SY, Wang HH, Lee MY, Tsou YC, Jwo SC, Sun GH, Tang SJ (2012) Autocrine CCL2 promotes cell migration and invasion via PKC activation and tyrosine phosphorylation of paxillin in bladder cancer cells. Cytokine 59(2): 423-432.
13. Iacovazzi PA, Notarnicola M, Caruso MG, Guerra V, Frisullo S, Altomare DF (2010) Serum levels of galectin-3 and its ligand 90k/mac-2bp in colorectal cancer patients. Immunopharmacol Immunotoxicol 32(1): 160-164.
14. Ikeguchi M, Hatada T, Yamamoto M, Miyake T, Matsunaga T, Fukumoto Y, Yamada Y, Fukuda K, Saito H, Tatebe S (2009) Serum interleukin-6 and-10 levels in patients with gastric cancer. Gastric Cancer 12(2): 95-100.
15. Iurisci I, Tinari N, Natoli C, Angelucci D, Cianchetti E, Iacobelli S (2000) Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin Cancer Res 6(4): 1389-1393.
16. John CM, Leffler H, Kahl-Knutsson B, Svensson I, Jarvis GA (2003) Truncated galectin-3 inhibits tumor growth and metastasis in orthotopic nude mouse model of human breast cancer. Clin Cancer Res 9(6): 2374-2383.
17. Kim M-Y, Oskarsson T, Acharyya S, Nguyen DX, Zhang XHF, Norton L, Massague J (2009a) Tumor self-seeding by circulating cancer cells. Cell 139(7): 1315-1326.
18. Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J (2009b) Tumor self-seeding by circulating cancer cells. Cell 139(7): 1315-1326.
19. Knupfer H, Preiss R (2010) Serum interleukin-6 levels in colorectal cancer patients-a summary of published results. Int J Colorectal Dis 25(2): 135-140.
20. Kogan-Sakin I, Cohen M, Paland N, Madar S, Solomon H, Molchadsky A, Brosh R, Buganim Y, Goldfinger N, Klocker H, Schalken JA, Rotter V (2009) Prostate stromal cells produce CXCL-1, CXCL-2, CXCL-3 and IL-8 in response to epithelia-secreted IL-1. Carcinogenesis 30(4): 698-705.
21. Kowanetz M, Wu XM, Lee J, Tan M, Hagenbeek T, Qu XP, Yu LL, Ross J, Korsisaari N, Cao T, Bou-Reslan H, Kallop D, Weimer R, Ludlam MJC, Kaminker JS, Modrusan Z, van Bruggen N, Peale FV, Carano R, Meng YG, Ferrara N (2010) Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G\+Ly6C\+ granulocytes. Proc Natl Acad Sci USA 107(50): 21248-21255.
22. Kuo PL, Shen KH, Hung SH, Hsu YL (2012) CXCL1/GROalpha increases cell migration and invasion of prostate cancer by decreasing fibulin-1 expression through NF-kappaB/HDAC1 epigenetic regulation. Carcinogenesis 33(12): 2477-2487.
23. Lederle W, Depner S, Schnur S, Obermueller E, Catone N, Just A, Fusenig NE, Mueller MM (2011) IL-6 promotes malignant growth of skin SCCs by regulating a network of autocrine and paracrine cytokines. Int J Cancer 128(12): 2803-2814.
24. Liu FT, Rabinovich GA (2005) Galectins as modulators of tumour progression. Nat Rev Cancer 5(1): 29-41.
25. Luan J, Shattuck-Brandt R, Haghnegahdar H, Owen JD, Strieter R, Burdick M, Nirodi C, Beauchamp D, Johnson KN, Richmond A (1997) Mechanism and biological significance of constitutive expression of MGSA/GRO chemokines in malignant melanoma tumor progression. J Leukoc Biol 62(5): 588-597.
26. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454(7203): 436-444.
27. Michalaki V, Odontiadis M, Syrigos K, Charles P, Waxman J (2004) Serum levels of IL-6 and TNF-alpha correlate with clinicopathological features and patient survival in patients with prostate cancer. Br J Cancer 91(6): 1227-1227.
28. Mizutani Y, Okada Y, Terachi T, Kakehi Y, Yoshida O (1995) Serum granulocyte-stimulating factor levels in patients with urinary-bladder tumor and various urological malignancies. Br J Urol 76(5): 580-586.
29. Monti P, Leone BE, Marchesi F, Balzano G, Zerbi A, Scaltrini F, Pasquali C, Calori G, Pessi F, Sperti C, Di Carlo V, Allavena P, Piemonti L (2003) The CC chemokine MCP-1/CCL2 in pancreatic cancer progression: regulation of expression and potential mechanisms of antimalignant activity. Cancer Res 63(21): 7451-7461.
30. Nagy N, Bronckart Y, Camby I, Legendre H, Lahm H, Kaltner H, Hadari Y, Van Ham P, Yeaton P, Pector JC, Zick Y, Salmon I, Danguy A, Kiss R, Gabius HJ (2002) Galectin-8 expression decreases in cancer compared with normal and dysplastic human colon tissue and acts significantly on human colon cancer cell migration as a suppressor. Gut 50(3): 392-401.
31. Nangia-Makker P, Ochieng J, Christman JK, Raz A (1993) Regulation of the expression of galactoside-binding lectin during human monocytic differentiation. Cancer Res 53(20): 5033-5037.
32. Newlaczyl AU, Yu LG (2011) Galectin-3-a jack-of-all-trades in cancer. Cancer Lett 313(2): 123-128.
33. Payne AS, Cornelius LA (2002) The role of chemokines in melanoma tumor growth and metastasis. J Invest Dermatol 118(6): 915-922.
34. Rechreche H, Mallo GV, Montalto G, Dagorn JC, Iovanna JL (1997) Cloning and expression of the mRNA of human galectin-4, an S-type lectin down-regulated in colorectal cancer. Eur J Biochem 248(1): 225-230.
35. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D (2004) Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 5(2): 163-175.
36. Sakaki M, Oka N, Nakanishi R, Yamaguchi K, Fukumori T, Kanayama HO (2008) Serum level of galectin-3 in human bladder cancer. J Med Invest 55(1-2): 127-132.
37. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, Huget P, Dirix LY (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 103(5): 642-646.
38. Sangeetha SR, Appukuttan PS (2005) IgA1 is the premier serum glycoprotein recognized by human galectin-1 since T antigen (Galbeta1-43GalNAc-) is far superior to non-repeating N-acetyl lactosamine as ligand. Int J Biol Macromol 35(5): 269-276.
39. Sanjuan X, Fernandez PL, Castells A, Castronovo V, van den Brule F, Liu FT, Cardesa A, Campo E (1997) Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 113(6): 1906-1915.
40. Saussez S, Lorfevre F, Lequeux T, Laurent G, Chantrain G, Vertongen F, Toubeau G, Decaestecker C, Kiss R (2008) The determination of the levels of circulating galectin-1 and-3 in HNSCC patients could be used to monitor tumor progression and/or responses to therapy. Oral Oncol 44(1): 86-93.
41. Senapati S, Chaturvedi P, Chaney WG, Chakraborty S, Gnanapragassam VS, Sasson AR, Batra SK (2011) Novel interaction of MUC4 and galectin: potential pathobiological implications for metastasis in lethal pancreatic cancer. Clin Cancer Res 17(2): 267-274.
42. Son DS, Parl AK, Rice VM, Khabele D (2007) Keratinocyte chemoattractant (KC)/human growth-regulated oncogene (GRO) chemokines and pro-inflammatory chemokine networks in mouse and human ovarian epithelial cancer cells. Cancer Biol Ther 6(8): 1302-1312.
43. Tsujimoto H, Ono S, Ichikura T, Matsumoto Y, Yamamoto J, Hase K (2010) Roles of inflammatory cytokines in the progression of gastric cancer: friends or foes? Gastric Cancer 13(4): 212-221.
44. Verbeke H, Struyf S, Laureys G, Van Damme J (2011) The expression and role of CXC chemokines in colorectal cancer. Cytokine Growth Factor Rev 22(5-6): 345-358.
45. Vereecken P, Awada A, Suciu S, Castro G, Morandini R, Litynska A, Lienard D, Ezzedine K, Ghanem G, Heenen M (2009) Evaluation of the prognostic significance of serum galectin-3 in American Joint Committee on Cancer stage III and stage IV melanoma patients. Melanoma Res 19(5): 316-320.
46. Viola A, Sarukhan A, Bronte V, Molon B (2012) The pros and cons of chemokines in tumor immunology. Trend Immunol 33(10): 496-504.
47. Wang J, Yao L, Zhao S, Zhang X, Yin J, Zhang Y, Chen X, Gao M, Ling EA, Hao A, Li G (2012) Granulocyte-colony stimulating factor promotes proliferation, migration and invasion in glioma cells. Cancer Biol Ther 13(6): 389-400.
48. Watanabe M, Takemasa I, Kaneko N, Yokoyama Y, Matsuo E, Iwasa S, Mori M, Matsuura N, Monden M, Nishimura O (2011) Clinical significance of circulating galectins as colorectal cancer markers. Oncol Rep 25(5): 1217-1226.
49. Wei LH, Kuo ML, Chen CA, Chou CH, Lai KB, Lee CN, Hsieh CY (2003) Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene 22(10): 1517-1527.
50. Wesseling J, van der Valk SW, Hilkens J (1996) A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol Biol Cell 7(4): 565-577.
51. Xie L, Ni WK, Chen XD, Xiao MB, Chen BY, He S, Lu CH, Li XY, Jiang F, Ni RZ (2012) The expressions and clinical significances of tissue and serum galectin-3 in pancreatic carcinoma. J Cancer Res Clin Oncol 138(6): 1035-1043.
52. Yoshimura T, Howard OM, Ito T, Kuwabara M, Matsukawa A, Chen K, Liu Y, Liu M, Oppenheim JJ, Wang JM (2013) Monocyte chemoattractant protein-1/ccl2 produced by stromal cells promotes lung metastasis of 4T1 murine breast cancer cells. PloS One 8(3): e58791.
53. Yu LG, Andrews N, Zhao Q, McKean D, Williams JF, Connor LJ, Gerasimenko OV, Hilkens J, Hirabayashi J, Kasai K, Rhodes JM (2007) Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 282(1): 773-781.
54. Zhao Q, Barclay M, Hilkens J, Guo X, Barrow H, Rhodes JM, Yu LG (2010) Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Mol Cancer 9: 154.
55. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, Rhodes JM, Yu LG (2009) Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69(17): 6799-6806.
56. Zollo M, Di Dato V, Spano D, De Martino D, Liguori L, Marino N, Vastolo V, Navas L, Garrone B, Mangano G, Biondi G, Guglielmotti A (2012) Targeting monocyte chemotactic protein-1 synthesis with bindarit induces tumor regression in prostate and breast cancer animal models. Clin Exp Metastasis 29(6): 585-601.