Detection of migration of locally implanted AC133+ stem cells by cellular magnetic resonance imaging with histological findings

FASEB Journal

Volumn 22, Issue 9, 2008, Pages 3234-3246

  Arbab, Ali S ^a,d   Janic, Branislava ^a   Knight, Robert A ^a   Anderson, Stasia A ^b   Pawelczyk, Edyta ^c   Rad, Ali M ^a   Read, Elizabeth J ^c   Pandit, Sunil D ^c   Frank, Joseph A ^c  

^a HENRY FORD HOSPITAL   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d HENRY FORD HEALTH SYSTEM   (United States)

Author keywords

Angiogenesis; Magnetically labeled AC133+ cells; MRI; Tumors

Indexed keywords

CD133 ANTIGEN; FERRIC FERROCYANIDE; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PLATELET DERIVED GROWTH FACTOR; PROTAMINE SULFATE; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GLIOMA; HISTOLOGY; HUMAN; HUMAN CELL; LABELING INDEX; MELANOMA CELL; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TISSUE SECTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; FEMALE; GLIOMA; GLYCOPROTEINS; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IRON; MAGNETIC RESONANCE IMAGING; MATRIX METALLOPROTEINASE 2; MELANOMA, AMELANOTIC; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; OXIDES; PEPTIDES; PLATELET-DERIVED GROWTH FACTOR; PROTAMINES; RATS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS MUSCULUS; RATTUS;

EID: 51349095580     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-105676     Document Type: Article

References (54)

1. Folkman, J. (2007) Angiogenesis: an organizing principle for drug discovery? Nat. Rev. Drug Discov. 6, 273-286
2. Shi, Q., Rafii, S., Wu, M. H., Wijelath, E. S., Yu, C., Ishida, A., Fujita, Y., Kothari, S., Mohle, R., Sauvage, L. R., Moore, M. A., Storb, R. F., and Hammond, W. P. (1998) Evidence for circulating bone marrow-derived endothelial cells. Blood 92, 362-367
3. Samejima, N., and Yamazaki, K. (1988) A study on the vascular proliferation in tissues around the tumor in breast cancer. Jpn. J. Surg. 18, 235-242
4. Ellis, L. M., Liu, W., Ahmad, S. A., Fan, F., Jung, Y. D., Shaheen, R. M., and Reinmuth, N. (2001) Overview of angiogenesis: Biologic implications for antiangiogenic therapy. Semin. Oncol. 28, 94-104
5. Liekens, S., De Clercq, E., and Neyts, J. (2001) Angiogenesis: regulators and clinical applications. Biochem. Pharmacol. 61, 253-270
6. Zhang, Z. G., Zhang, L., Jiang, Q., and Chopp, M. (2002) Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ. Res. 90, 284-288
7. Tomanek, R. J., and Schatteman, G. C. (2000) Angiogenesis: new insights and therapeutic potential. Anat. Rec. 261, 126-135
8. Hotfilder, M., Nowak-Gottl, U., and Wolff, J. E. (1997) Tumor-angiogenesis: a network of cytokines. Klin. Padiatr. 209, 265-270
9. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., and Isner, J. M. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967
10. Reyes, M., Dudek, A., Jahagirdar, B., Koodie, L., Marker, P. H., and Verfaillie, C. M. (2002) Origin of endothelial progenitors in human postnatal bone marrow. J. Clin. Invest. 109, 337-346
11. Rafii, S., Lyden, D., Benezra, R., Hattori, K., and Heissig, B. (2002) Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat. Rev. Cancer 2, 826-835
12. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., Chadburn, A., Heissig, B., Marks, W., Witte, L., Wu, Y., Hicklin, D., Zhu, Z., Hackett, N. R., Crystal, R. G., Moore, M. A., Hajjar, K. A., Manova, K., Benezra, R., and Rafii, S. (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7, 1194-1201
13. Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., Low, W. C., Largaespada, D. A., and Verfaillie, C. M. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49
14. Gill, M., Dias, S., Hattori, K., Rivera, M. L., Hicklin, D., Witte, L., Girardi, L., Yurt, R., Himel, H., and Rafii, S. (2001) Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ. Res. 88, 167-174
15. Gehling, U. M., Ergun, S., Schumacher, U., Wagener, C., Pantel, K., Otte, M., Schuch, G., Schafhausen, P., Mende, T., Kilic, N., Kluge, K., Schafer, B., Hossfeld, D. K., and Fiedler, W. (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95, 3106-3112
16. + cells in vitro. Acta Pharmacol. Sin. 24, 212-218
17. + lymphatic/vascular endothelial precursor cells. Blood 101, 168-172
18. + cells. Eur. J. Haematol. 70, 143-150
19. Arbab, A. S., Pandit, S. D., Anderson, S. A., Yocum, G. T., Bur, M., Frenkel, V., Khuu, H. M., Read, E. J., and Frank, J. A. (2006) Magnetic resonance imaging and confocal microscopy studies of magnetically labeled endothelial progenitor cells trafficking to sites of tumor angiogenesis. Stem Cells 24, 671-678
20. Murohara, T. (2001) Therapeutic vasculogenesis using human cord blood-derived endothelial progenitors. Trends Cardiovas. Med. 11, 303-307
21. Murohara, T., Ikeda, H., Duan, J., Shintani, S., Sasaki, K., Eguchi, H., Onitsuka, I., Matsui, K., and Imaizumi, T. (2000) Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J. Clin. Invest. 105, 1527-1536
22. Shintani, S., Murohara, T., Ikeda, H., Ueno, T., Sasaki, K., Duan, J., and Imaizumi, T. (2001) Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103, 897-903
23. Asahara, T., and Kawamoto, A. (2004) Endothelial progenitor cells for postnatal vasculogenesis. Am. J. Physiol. Cell Physiol. 287, C572-C579
24. Hilbe, W., Dirnhofer, S., Oberwasserlechner, F., Schmid, T., Gunsilius, E., Hilbe, G., Woll, E., and Kahler, C. M. (2004) CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J. Clin. Path. 57, 965-969
25. Peterson, D. A. (2004) Umbilical cord blood cells and brain stroke injury: bringing in fresh blood to address an old problem. J. Clin. Invest. 114, 312-314
26. Yoshimura, H., Dhar, D. K., Kohno, H., Kubota, H., Fujii, T., Ueda, S., Kinugasa, S., Tachibana, M., and Nagasue, N. (2004) Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clin. Cancer Res. 10, 8554-8560
27. Detwiller, K. Y., Fernando, N. T., Segal, N. H., Ryeom, S. W., D'Amore, P. A., and Yoon, S. S. (2005) Analysis of hypoxia-related gene expression in sarcomas and effect of hypoxia on RNA interference of vascular endothelial cell growth factor A. Cancer Res. 65, 5881-5889
28. Vaupel, P., and Mayer, A. (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 26, 225-239
29. Vaupel, P., Mayer, A., and Hockel, M. (2004) Tumor hypoxia and malignant progression. Meth. Enzymol. 381, 335-354
30. Ferrari, N., Glod, J., Lee, J., Kobiler, D., and Fine, H. A. (2003) Bone marrow-derived, endothelial progenitor-like cells as angiogenesis-selective gene-targeting vectors. Gene Ther. 10, 647-656
31. + progenitors for the repair of infarcted myocardium. J. Am. Coll. Cardiol. 44, 458-463
32. Moore, X. L., Lu, J., Sun, L., Zhu, C. J., Tan, P., and Wong, M. C. (2004) Endothelial progenitor cells' "homing" specificity to brain tumors. Gene Ther. 11, 811-818
33. Takahashi, T., Kalka, C., Masuda, H., Chen, D., Silver, M., Kearney, M., Magner, M., Isner, J. M., and Asahara, T. (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 5, 434-438
34. Arbab, A. S., Jordan, E. K., Wilson, L. B., Yocum, G. T., Lewis, B. K., and Frank, J. A. (2004) In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum. Gene Ther. 15, 351-360
35. Anderson, S. A., Shukaliak-Quandt, J., Jordan, E. K., Arbab, A. S., Martin, R., McFarland, H., and Frank, J. A. (2004) Magnetic resonance imaging of labeled T-cells in a mouse model of multiple sclerosis. Ann. Neurol. 55, 654-659
36. Anderson, S. A., Glod, J., Arbab, A. S., Noel, M., Ashari, P., Fine, H. A., and Frank, J. A. (2005) Noninvasive MR imaging of magnetically labeled stem cells to directly identify neovasculature in a glioma model. Blood 105, 420-425
37. Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J., and Frank, J. A. (2004) Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 104, 1217-1223
38. Yoshida, D., Kim, K., Noha, M., and Teramoto, A. (2006) Hypoxia inducible factor 1-alpha regulates of platelet derived growth factor-B in human glioblastoma cells. J. Neurooncol. 76, 13-21
39. Carmeliet, P. (2000) Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395
40. Carmeliet, P. (2005) VEGF as a key mediator of angiogenesis in cancer. Oncology 69, 4-10
41. Carmeliet, P. (2003) Angiogenesis in health and disease. Nat. Med. 9, 653-660
42. Fomchenko, E. I., and Holland, E. C. (2007) Platelet-derived growth factor-mediated gliomagenesis and brain tumor recruitment. Neurosurg. Clin. N. Am. 18, 39-58
43. Westermark, B., Heldin, C. H., and Nister, M. (1995) Platelet-derived growth factor in human glioma. Glia 15, 257-263
44. Rigolin, G. M., Mauro, E., Ciccone, M., Fraulini, C., Sofritti, O., Castoldi, G., and Cuneo, A. (2007) Neoplastic circulating endothelial-like cells in patients with acute myeloid leukaemia. Eur. J. Haematol. 78, 365-373
45. + endothelial progenitor cells from peripheral blood. J. Immunoassay Immunochem. 28, 13-23
46. Allanore, Y., Batteux, F., Avouac, J., Assous, N., Weill, B., and Kahan, A. (2007) Levels of circulating endothelial progenitor cells in systemic sclerosis. Clin. Exp. Rheumatol. 25, 60-66
47. + hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 91, 4523-4530
48. Jo, D. Y., Rafii, S., Hamada, T., and Moore, M. A. (2000) Chemotaxis of primitive hematopoietic cells in response to stromal cell-derived factor-1. J. Clin. Invest. 105, 101-111
49. Arbab, A. S., Yocum, G. T., Rad, A. M., Khakoo, A. Y., Fellowes, V., Read, E. J., and Frank, J. A. (2005) Labeling of cells with ferumoxides- protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR Biomed. 18, 553-559
50. +) hemangiocytes. Nat. Med. 12, 557-567
51. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., and Gurtner, G. C. (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-864
52. Arbab, A. S., Iskander, A. S. M., Rad, A. M., Anderson, S. A., Pandit, S. D., Read, E. J., and Frank, J. A. (2006) Migration of endothelial progenitor cells is related to HIF-1a induced SDF-1 expression. Mol. Imaging 5, 233
53. Rad, A. M., Arbab, A. S., Iskander, A. S., Jiang, Q., and Soltanian-Zadeh, H. (2007) Quantification of superparamagnetic iron oxide (SPIO)-labeled cells using MRI. J. Magn. Reson. Imaging 26, 366-374
54. Pawelczyk, E., Arbab, A. S., Chaudhry, A., Balakumaran, A., Robey, P. G., and Frank, J. A. (2008) In vitro model of brdu or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: implications for cellular therapy. Stem Cells 26, 1366-1375