Matrix metalloproteinase-1-mediated mesenchymal stem cell tumor tropism is dependent on crosstalk with stromal derived growth factor 1/C-X-C chemokine receptor 4 axis

FASEB Journal

Volumn 28, Issue 10, 2014, Pages 4359-4368

  Ho, Ivy A W ^a   Yulyana, Yulyana ^a   Sia, Kian C ^a   Newman, Jennifer P ^a   Guo, Chang M ^b   Hui, Kam M ^a,c,d,e   Lam, Paula Y P ^a,b,d  

^a DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

CXCR 4; Migration; MMP 1; MSCs; SDF 1

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; INTERSTITIAL COLLAGENASE; PROTEINASE ACTIVATED RECEPTOR 1; CXCR4 PROTEIN, HUMAN; MMP1 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

ADULT; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; MESENCHYMAL STEM CELL; MIDDLE AGED; NEOPLASM; PROTEIN EXPRESSION; RNA INTERFERENCE; TROPISM; TUMOR CELL; CELL CULTURE; CELL MOTION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; FEMALE; HUMANS; MALE; MATRIX METALLOPROTEINASE 1; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; RECEPTOR, PAR-1; RECEPTORS, CXCR4; TUMOR MICROENVIRONMENT;

EID: 84907703211     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-252551     Document Type: Article

References (46)

1. Reagan, M. R., and Kaplan, D. L. (2011) Concise review: mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem Cells 29, 920-927
2. Galipeau, J. (2013) The mesenchymal stromal cells dilemma- does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 15, 2-8
3. Sonabend, A. M., Ulasov, I. V., Tyler, M. A., Rivera, A. A., Mathis, J. M., and Lesniak, M. S. (2008) Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma. Stem Cells 26, 831-841
4. Sasportas, L. S., Kasmieh, R., Wakimoto, H., Hingtgen, S., van de Water, J. A., Mohapatra, G., Figueiredo, J. L., Martuza, R. L., Weissleder, R., and Shah, K. (2009) Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc. Natl. Acad. Sci. U. S. A. 106, 4822-4827
5. Ho, I. A., and Lam, P. Y. (2013) Signaling molecules and pathways involved in MSC tumor tropism. Histol. Histopathol. 28, 1427-1438
6. Li, G., Hattermann, K., Mentlein, R., Mehdorn, H. M., and Held-Feindt, J. (2013) The transmembrane chemokines CXCL16 and CX3CL1 and their receptors are expressed in human meningiomas. Oncol. Rep. 29, 563-570
7. Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., Nagler, A., Ben-Hur, H., Many, A., Shultz, L., Lider, O., Alon, R., Zipori, D., and Lapidot, T. (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283, 845-848
8. Dar, A., Kollet, O., and Lapidot, T. (2006) Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp. Hematol. 34, 967-975
9. Hamm, H. E. (1998) The many faces of G protein signaling. J. Biol. Chem. 273, 669-672
10. Balabanian, K., Lagane, B., Infantino, S., Chow, K. Y., Harriague, J., Moepps, B., Arenzana-Seisdedos, F., Thelen, M., and Bachelerie, F. (2005) The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 280, 35760-35766
11. Cubedo, N., Cerdan, E., Sapede, D., and Rossel, M. (2009) CXCR4 and CXCR7 cooperate during tangential migration of facial motoneurons. Mol. Cell. Neurosci. 40, 474-484
12. Wynn, R. F., Hart, C. A., Corradi-Perini, C., O'Neill, L., Evans, C. A., Wraith, J. E., Fairbairn, L. J., and Bellantuono, I. (2004) A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 104, 2643-2645
13. Ip, J. E., Wu, Y., Huang, J., Zhang, L., Pratt, R. E., and Dzau, V. J. (2007) Mesenchymal stem cells use integrin beta1 not CXC chemokine receptor 4 for myocardial migration and engraftment. Mol. Biol. Cell 18, 2873-2882
14. Huang, W., Wang, T., Zhang, D., Zhao, T., Dai, B., Ashraf, A., Wang, X., Xu, M., Millard, R. W., Fan, G. C., Ashraf, M., Yu, X. Y., and Wang, Y. (2012) Mesenchymal stem cells overexpressing CXCR4 attenuate remodeling of postmyocardial infarction by releasing matrix metalloproteinase-9. Stem Cells Dev. 21, 778-789
15. Park, S. A., Ryu, C. H., Kim, S. M., Lim, J. Y., Park, S. I., Jeong, C. H., Jun, J. A., Oh, J. H., Park, S. H., Oh, W., and Jeun, S. S. (2011) CXCR4-transfected human umbilical cord blood-derived mesenchymal stem cells exhibit enhanced migratory capacity toward gliomas. Int. J. Oncol. 38, 97-103
16. Ryu, C. H., Park, S. A., Kim, S. M., Lim, J. Y., Jeong, C. H., Jun, J. A., Oh, J. H., Park, S. H., Oh, W. I., and Jeun, S. S. (2010) Migration of human umbilical cord blood mesenchymal stem cells mediated by stromal cell-derived factor-1/CXCR4 axis via Akt, ERK, and p38 signal transduction pathways. Biochem. Biophys. Res. Commun. 398, 105-110
17. Song, C. H., Honmou, O., Furuoka, H., and Horiuchi, M. (2011) Identification of chemoattractive factors involved in the migration of bone marrow-derived mesenchymal stem cells to brain lesions caused by prions. J. Virol. 85, 11069-11078
18. Ho, I. A., Chan, K. Y., Ng, W. H., Guo, C. M., Hui, K. M., Cheang, P., and Lam, P. Y. (2009) Matrix metalloproteinase 1 is necessary for the migration of human bone marrow-derived mesenchymal stem cells toward human glioma. Stem Cells 27, 1366-1375
19. Blackburn, J. S., Liu, I., Coon, C. I., and Brinckerhoff, C. E. (2009) A matrix metalloproteinase-1/protease activated receptor-1 signaling axis promotes melanoma invasion and metastasis. Oncogene 28, 4237-4248
20. Trivedi, V., Boire, A., Tchernychev, B., Kaneider, N. C., Leger, A. J., O'Callaghan, K., Covic, L., and Kuliopulos, A. (2009) Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site. Cell 137, 332-343
21. Coughlin, S. R. (2000) Thrombin signalling and proteaseactivated receptors. Nature 407, 258-264
22. Wautier, F., Wislet-Gendebien, S., Chanas, G., Rogister, B., and Leprince, P. (2007) Regulation of nestin expression by thrombin and cell density in cultures of bone mesenchymal stem cells and radial glial cells. BMC Neurosci. 8, 104
23. Coughlin, S. R. (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J. Thromb. Haemost. 3, 1800-1814
24. Bergmann, S., Junker, K., Henklein, P., Hollenberg, M. D., Settmacher, U., and Kaufmann, R. (2006) PAR-type thrombin receptors in renal carcinoma cells: PAR1-mediated EGFR activation promotes cell migration. Oncol. Rep. 15, 889-893
25. Darmoul, D., Gratio, V., Devaud, H., Peiretti, F., and Laburthe, M. (2004) Activation of proteinase-activated receptor 1 promotes human colon cancer cell proliferation through epidermal growth factor receptor transactivation. Mol. Cancer Res. 2, 514-522
26. Kaufmann, R., Rahn, S., Pollrich, K., Hertel, J., Dittmar, Y., Hommann, M., Henklein, P., Biskup, C., Westermann, M., Hollenberg, M. D., and Settmacher, U. (2007) Thrombinmediated hepatocellular carcinoma cell migration: cooperative action via proteinase-activated receptors 1 and 4. J. Cell. Physiol. 211, 699-707
27. Smadja, D. M., Bieche, I., Uzan, G., Bompais, H., Muller, L., Boisson-Vidal, C., Vidaud, M., Aiach, M., and Gaussem, P. (2005) PAR-1 activation on human late endothelial progenitor cells enhances angiogenesis in vitro with upregulation of the SDF-1/CXCR4 system. Arterioscler. Thromb. Vasc. Biol. 25, 2321-2327
28. Ho, I. A., Chan, K. Y., Miao, L., Shim, W. S., Guo, C. M., Cheang, P., Hui, K. M., and Lam, P. Y. (2008) HSV-1 amplicon viral vector-mediated gene transfer to human bone marrow-derived mesenchymal stem cells. Cancer Gene Ther. 15, 553-562
29. Broxmeyer, H. E., Orschell, C. M., Clapp, D. W., Hangoc, G., Cooper, S., Plett, P. A., Liles, W. C., Li, X., Graham-Evans, B., Campbell, T. B., Calandra, G., Bridger, G., Dale, D. C., and Srour, E. F. (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J. Exp. Med. 201, 1307-1318
30. Dillmann, F., Veldwijk, M. R., Laufs, S., Sperandio, M., Calandra, G., Wenz, F., Zeller, J., and Fruehauf, S. (2009) Plerixafor inhibits chemotaxis toward SDF-1 and CXCR4-mediated stroma contact in a dose-dependent manner resulting in increased susceptibility of BCR-ABL+ cell to Imatinib and Nilotinib. Leuk. Lymphoma 50, 1676-1686
31. Ghadge, S. K., Muhlstedt, S., Ozcelik, C., and Bader, M. (2011) SDF-1alpha as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol. Ther. 129, 97-108
32. Wang, Y., Deng, Y., and Zhou, G. Q. (2008) SDF-1alpha/ CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res. 1195, 104-112
33. Kitaori, T., Ito, H., Schwarz, E. M., Tsutsumi, R., Yoshitomi, H., Oishi, S., Nakano, M., Fujii, N., Nagasawa, T., and Nakamura, T. (2009) Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum. 60, 813-823
34. Sun, X., Wei, L., Chen, Q., and Terek, R. M. (2010) CXCR4/ SDF1 mediate hypoxia induced chondrosarcoma cell invasion through ERK signaling and increased MMP1 expression. Mol. Cancer 9, 17
35. Eck, S. M., Cote, A. L., Winkelman, W. D., and Brinckerhoff, C. E. (2009) CXCR4 and matrix metalloproteinase-1 are elevated in breast carcinoma-associated fibroblasts and in normal mammary fibroblasts exposed to factors secreted by breast cancer cells. Mol. Cancer Res. 7, 1033-1044
36. Christopherson, K. W., 2nd, Hangoc, G., Mantel, C. R., and Broxmeyer, H. E. (2004) Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 305, 1000-1003
37. Song, C., and Li, G. (2011) CXCR4 and matrix metalloproteinase- 2 are involved in mesenchymal stromal cell homing and engraftment to tumors. Cytotherapy 13, 549-561
38. Lee, Y., Kim, H., Kim, S., Kim, K. H., and Chung, J. H. (2010) Activation of toll-like receptors 2, 3 or 5 induces matrix metalloproteinase- 1 and -9 expression with the involvement of MAPKs and NF-kappaB in human epidermal keratinocytes. Exp. Dermatol. 19, e44-49
39. Zhan, Y., Abi Saab, W. F., Modi, N., Stewart, A. M., Liu, J., and Chadee, D. N. (2012) Mixed lineage kinase 3 is required for matrix metalloproteinase expression and invasion in ovarian cancer cells. Exp. Cell Res. 318, 1641-1648
40. Jones, S. W., Brockbank, S. M., Mobbs, M. L., Le Good, N. J., Soma-Haddrick, S., Heuze, A. J., Langham, C. J., Timms, D., Newham, P., and Needham, M. R. (2006) The orphan G-protein coupled receptor RDC1: evidence for a role in chondrocyte hypertrophy and articular cartilage matrix turnover. Osteoarthritis Cartilage 14, 597-608
41. Kim, S. J., Shin, J. Y., Lee, K. D., Bae, Y. K., Choi, I. J., Park, S. H., and Chun, K. H. (2011) Galectin-3 facilitates cell motility in gastric cancer by up-regulating protease-activated receptor-1 (PAR-1) and matrix metalloproteinase-1 (MMP-1). PLoS One 6, e25103
42. Decaillot, F. M., Kazmi, M. A., Lin, Y., Ray-Saha, S., Sakmar, T. P., and Sachdev, P. (2011) CXCR7/CXCR4 heterodimer constitutively recruits beta-arrestin to enhance cell migration. J. Biol. Chem. 286, 32188-32197
43. Carbajal, K. S., Schaumburg, C., Strieter, R., Kane, J., and Lane, T. E. (2010) Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 107, 11068-11073
44. Wang, Y. G., Kim, S. J., Baek, J. H., Lee, H. W., Jeong, S. Y., and Chun, K. H. (2012) Galectin-3 increases the motility of mouse melanoma cells by regulating matrix metalloproteinase-1 expression. Exp. Mol. Med. 44, 387-393
45. Janowska-Wieczorek, A., Marquez, L. A., Dobrowsky, A., Ratajczak, M. Z., and Cabuhat, M. L. (2000) Differential MMP and TIMP production by human marrow and peripheral blood CD34(+) cells in response to chemokines. Exp. Hematol. 28, 1274-1285
46. Ponte, A. L., Marais, E., Gallay, N., Langonne, A., Delorme, B., Herault, O., Charbord, P., and Domenech, J. (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25, 1737-1745