Divergent roles of CD44 and carcinoembryonic antigen in colon cancer metastasis

FASEB Journal

Volumn 26, Issue 6, 2012, Pages 2648-2656

  Dallas, Matthew R ^a,b   Liu, Guosheng ^c,d   Chen, Wei Chiang ^a,b   Thomas, Susan N ^e   Wirtz, Denis ^a,b   Huso, David L ^c,d   Konstantopoulos, Konstantinos ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c DEPARTMENT OF PATHOLOGY   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

CEA; Cytoplasmic compliance; Migration

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; HERMES ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOMA CELL; CELL AGGREGATION; CELL MIGRATION; COLON CANCER; COLON CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG PARENCHYMA; MALE; METASTASIS; MOUSE; NONHUMAN; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; WOUND HEALING;

ANIMALS; ANTIGENS, CD44; CARCINOEMBRYONIC ANTIGEN; CELL MOVEMENT; COLONIC NEOPLASMS; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; LIVER NEOPLASMS; LUNG NEOPLASMS; MICE; NEOPLASM METASTASIS; TUMOR CELLS, CULTURED;

EID: 84861786167     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-203786     Document Type: Article

References (51)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
2. Napier, S. L., Healy, Z. R., Schnaar, R. L., and Konstantopoulos, K. (2007) Selectin ligand expression regulates the initial vascular interactions of colon carcinoma cells: the roles of CD44v and alternative sialofucosylated selectin ligands. J. Biol. Chem. 282, 3433-3441 (Pubitemid 47084453)
3. Thomas, S. N., Zhu, F., Schnaar, R. L., Alves, C. S., and Konstantopoulos, K. (2008) Carcinoembryonic antigen and CD44 variant isoforms cooperate to mediate colon carcinoma cell adhesion to E-and L-selectin in shear flow. J. Biol. Chem. 283, 15647
4. Wirtz, D., Konstantopoulos, K., and Searson, P. C. (2011) The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11, 512-522
5. Ponta, H., Sherman, L., and Herrlich, P. a. (2003) CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45 (Pubitemid 36077255)
6. Alves, C. S., Yakovlev, S., Medved, L., and Konstantopoulos, K. (2009) Biomolecular characterization of CD44-fibrin(ogen) binding. J. Biol. Chem. 284, 1177
7. Wielenga, V. J. M., Heider, K. H., Johan, G., Offerhaus, A., Adolf, G. R., van den Berg, F. M., Ponta, H., Herrlich, P., and Pals, S. T. (1993) Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression. Cancer Res. 53, 4754
8. Weg-Remers, S., Anders, M., von Lampe, B., Riecken, E. O., Schuder, G., Feifel, G., Zeitz, M., and Stallmach, A. (1998) Decreased expression of CD44 splicing variants in advanced colorectal carcinomas. Eur. J. Cancer 34, 1607-1611 (Pubitemid 28446346)
9. Kaufmann, M., von Minckwitz, G., Heider, K., Ponta, H., Herrlich, P., and Sinn, H. (1995) CD44 variant exon epitopes in primary breast cancer and length of survival. Lancet 345, 615-619
10. Noordzij, M. A., van Steenbrugge, G. J., Schröder, F. H., and van der Kwast, T. H. (1999) Decreased expression of CD44 in metastatic prostate cancer. Int. J. Cancer 84, 478-483
11. Gao, A. C., Lou, W., Dong, J. T., and Isaacs, J. T. (1997) CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13. Cancer Res. 57, 846-849 (Pubitemid 27098007)
12. Harada, N., Mizoi, T., Kinouchi, M., Hoshi, K., Ishii, S., Shiiba, K., Sasaki, I., and Matsuno, S. (2001) Introduction of antisense CD44s CDNA down-regulates expression of overall CD44 isoforms and inhibits tumor growth and metastasis in highly metastatic colon carcinoma cells. Int. J. Cancer 91, 67-75
13. Jothy, S. (2003) CD44 and its partners in metastasis. Clin. Exp. Metastasis 20, 195-201
14. Louderbough, J. M. V., and Schroeder, J. A. (2011) Understanding the dual nature of CD44 in breast cancer progression. Mol. Cancer Res. 9, 1573-1586
15. Li, Y., Cao, H., Jiao, Z., Pakala, S. B., Sirigiri, D. N. R., Li, W., Kumar, R., and Mishra, L. (2010) Carcinoembryonic antigen interacts with TGF-β receptor and inhibits TGF-β signaling in colorectal cancers. Cancer Res. 70, 8159-8168
16. Kitsuki, H., Katano, M., Morisaki, T., and Torisu, M. (1995) CEA-mediated homotypic aggregation of human colorectal carcinoma cells in a malignant effusion. Cancer Lett. 88, 7-13
17. Wirth, T., Soeth, E., Czubayko, F., and Juhl, H. (2002) Inhibition of endogenous carcinoembryonic antigen (CEA) increases the apoptotic rate of colon cancer cells and inhibits metastatic tumor growth. Clin. Exp. Metastasis 19, 155-160 (Pubitemid 34264085)
18. Jessup, J. M., Laguinge, L., Lin, S., Samara, R., Aufman, K., Battle, P., Frantz, M., Edmiston, K. H., and Thomas, P. (2004) Carcinoembryonic antigen induction of IL-10 and IL-6 inhibits hepatic ischemic/reperfusion injury to colorectal carcinoma cells. Int. J. Cancer 111, 332-337 (Pubitemid 38998812)
19. Hammarström, S. (1999) The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Sem. Cancer Biol. 9, 67-81
20. Shively, J. E., and Beatty, J. D. (1985) CEA-related antigens: molecular biology and clinical significance. Crit. Rev. Oncol. Hematol. 2, 355-399
21. Goldenberg, D., Sharkey, R., and Primus, F. (1976) Carcinoembryonic antigen in histopathology: immunoperoxidase staining of conventional tissue sections. J. Natl. Cancer Inst. 57, 11-22
22. Blumenthal, R. D., Hansen, H. J., and Goldenberg, D. M. (2005) Inhibition of adhesion, invasion, and metastasis by antibodies targeting CEACAM6 (NCA-90) and CEACAM5 (carcinoembryonic antigen). Cancer Res. 65, 8809-8817 (Pubitemid 41377369)
23. Rago, C., Huso, D. L., Diehl, F., Karim, B., Liu, G., Papadopoulos, N., Samuels, Y., Velculescu, V. E., Vogelstein, B., Kinzler, K. W., and Diaz, L. a. (2007) Serial assessment of human tumor burdens in mice by the analysis of circulating DNA. Cancer Res. 67, 9364-9370 (Pubitemid 47535926)
24. McCarty, O. J. T., Mousa, S. A., Bray, P. F., and Konstantopoulos, K. (2000) Immobilized platelets support human colon carcinoma cell tethering, rolling, and firm adhesion under dynamic flow conditions. Blood 96, 1789
25. Jadhav, S., Bochner, B. S., and Konstantopoulos, K. (2001) Hydrodynamic shear regulates the kinetics and receptor specificity of polymorphonuclear leukocyte-colon carcinoma cell adhesive interactions. J. Immunol. 167, 5986-5993 (Pubitemid 33062796)
26. Updyke, T. V., and Nicolson, G. L. (1986) Malignant melanoma cell lines selected in vitro for increased homotypic adhesion properties have increased experimental metastatic potential. Clin. Exp. Metastasis 4, 273-284 (Pubitemid 17216306)
27. Hashino, J., Fukuda, Y., Oikawa, S., Nakazato, H., and Nakanishi, T. (1994) Metastatic potential of human colorectal carcinoma SW1222 cells transfected with cDNA encoding carcinoembryonic antigen. Clin. Exp. Metastasis 12, 324-328 (Pubitemid 24257070)
28. Cross, S. E., Jin, Y.-S., Rao, J., and Gimzewski, J. K. (2007) Nanomechanical analysis of cells from cancer patients. Nat. Nanotech. 2, 780-783 (Pubitemid 350223349)
29. Guck, J., Schinkinger, S., Lincoln, B., Wottawah, F., Ebert, S., Romeyke, M., Lenz, D., Erickson, H. M., Ananthakrishnan, R., Mitchell, D., Käs, J., Ulvick, S., and Bilby, C. (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88, 3689-3698 (Pubitemid 40586616)
30. Swaminathan, V., Mythreye, K., O'Brien, E. T., Berchuck, A., Blobe, G. C., and Superfine, R. (2011) Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines. Cancer Res. 71, 5075-5080
31. Wirtz, D. (2009) Particle-tracking microrheology of living cells: principles and applications. Annu. Rev. Biophys. 38, 301-326
32. Terpe, H. J., Störkel, S., Zimmer, U., Anquez, V., Fischer, C., Pantel, K., and Günthert, U. (1996) Expression of CD44 isoforms in renal cell tumors: Positive correlation to tumor differentiation. Am. J. Pathol. 148, 453-463
33. Yüce, I., Bayram, A., Caǧli, S., Canöz, O., Bayram, S., and Güney, E. (2011) The role of CD44 and matrix metalloproteinase-9 expression in predicting neck metastasis of supraglottic laryngeal carcinoma. Am. J. Otolaryngol. 32, 141-146
34. Lopez, J. I., Camenisch, T. D., Stevens, M. V., Sands, B. J., McDonald, J., and Schroeder, J. A. (2005) CD44 attenuates metastatic invasion during breast cancer progression. Cancer Res. 65, 6755-6763 (Pubitemid 41060713)
35. Choi, S. H., Takahashi, K., Eto, H., Yoon, S. S., and Tanabe, K. K. (2000) CD44s expression in human colon carcinomas influences growth of liver metastases. Int. J. Cancer 85, 523-526 (Pubitemid 30075131)
36. Mulder, J. W. R., Sewnath, M., Offerhaus, G., and Pals, S. (1994) Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 344, 1470-1472 (Pubitemid 24351702)
37. Klingbeil, P., Marhaba, R., Jung, T., Kirmse, R., Ludwig, T., and Zöller, M. (2009) CD44 variant isoforms promote metastasis formation by a tumor cell-matrix cross-talk that supports adhesion and apoptosis resistance. Mol. Cancer Res. 7, 168-179
38. Yang, X.-R., Xu, Y., Yu, B., Zhou, J., Qiu, S.-J., Shi, G.-M., Zhang, B.-H., Wu, W.-Z., Shi, Y.-H., Wu, B., Yang, G.-H., Ji, Y., and Fan, J. (2010) High expression levels of putative hepatic stem/progenitor cell biomarkers related to tumour angiogenesis and poor prognosis of hepatocellular carcinoma. Gut 59, 953-962
39. Morrin, M., and Delaney, P. (2002) CD44v6 is not relevant in colorectal tumour progression. Int. J. Colorectal Dis. 17, 30-36 (Pubitemid 41398988)
40. De Marzo, A. M., Bradshaw, C., Sauvageot, J., Epstein, J. I., and Miller, G. J. (1998) CD44 and CD44v6 downregulation in clinical prostatic carcinoma: relation to Gleason grade and cytoarchitecture. Prostate 34, 162-168 (Pubitemid 28156605)
41. Murray, E. W., and Robbins, S. M. (1998) Antibody cross-linking of the glycosylphosphatidylinositol-linked protein CD59 on hematopoietic cells induces signaling pathways resembling activation by complement. J. Biol. Chem. 273, 25279-25284 (Pubitemid 28443293)
42. Kim, H.-R., Wheeler, M. A., Wilson, C. M., Iida, J., Eng, D., Simpson, M. A., McCarthy, J. B., and Bullard, K. M. (2004) Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Res. 64, 4569-4576 (Pubitemid 38856930)
43. Zeilstra, J., Joosten, S. P. J., Dokter, M., Verwiel, E., Spaargaren, M., and Pals, S. T. (2008) Deletion of the WNT target and cancer stem cell marker CD44 in Apc(Min/+) mice attenuates intestinal tumorigenesis. Cancer Res. 68, 3655-3661
44. Nelson, W. J., and Nusse, R. (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487 (Pubitemid 38314410)
45. Yoshioka, T., Masuko, T., Kotanagi, H., Aizawa, O., Saito, Y., Nakazato, H., Koyama, K., and Hashimoto, Y. (1998) Homotypic adhesion through carcinoembryonic antigen plays a role in hepatic metastasis development. Jpn. J. Cancer Res. 89, 177-185 (Pubitemid 28143445)
46. Gangopadhyay, A., Bajenova, O., Kelly, T. M., and Thomas, P. (1996) Carcinoembryonic antigen induces cytokine expression in Kupffer cells: implications for hepatic metastasis from colorectal cancer. Cancer Res. 56, 4805
47. Edmiston, K. H., Gangopadhyay, A., Shoji, Y., Jessup, J. M., Nachman, A. P., and Thomas, P. (1997) In vivo induction of murine cytokine production by carcinoembryonic antigen. Cancer Res. 4432-4436 (Pubitemid 27413456)
48. Gangopadhyay, A., Lazure, D. A., and Thomas, P. (1998) Adhesion of colorectal carcinoma cells to the endothelium is mediated by cytokines from CEA stimulated Kupffer cells. Clin. Exp. Metastasis 16, 703-712 (Pubitemid 29170480)
49. Jessup, J. M., Samara, R., Battle, P., and Laguinge, L. M. (2005) Carcinoembryonic antigen promotes tumor cell survival in liver through an IL-10-dependent pathway. Clin. Exp. Metastasis 21, 709-717 (Pubitemid 40755011)
50. O'Brien, C. A., Pollett, A., Gallinger, S., and Dick, J. E. (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106-110 (Pubitemid 46067310)
51. Fang, D. D., Kim, Y. J., Lee, C. N., Aggarwal, S., Mckinnon, K., Mesmer, D., Norton, J., Birse, C. E., He, T., Ruben, S. M., and Moore, P. A. (2010) Expansion of CD133+ colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br. J. Cancer 103, 1265-1275