Recent advances into the understanding of mesenchymal stem cell trafficking

British Journal of Haematology

Volumn 137, Issue 6, 2007, Pages 491-502

  Fox, James M ^a,b   Chamberlain, Giselle ^b   Ashton, Brian A ^b   Middleton, Jim ^b  

^a ROBERT JONES AND AGNES HUNT ORTHOPAEDIC HOSPITAL   (United Kingdom)

^b KEELE UNIVERSITY   (United Kingdom)

Author keywords

Cell trafficking; Chemokines; Integrin; Mesenchymal stem cells; Selectin

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; CELL ADHESION MOLECULE; CELL MARKER; CHEMOKINE; ENDOGLIN; HLA ANTIGEN; INTEGRIN; SELECTIN; STAGE SPECIFIC EMBRYO ANTIGEN 4; THY 1 ANTIGEN; VASCULAR CELL ADHESION MOLECULE 1;

BLOOD FLOW; CELL ADHESION; CELL DIFFERENTIATION; CELL HOMING; CELL LINEAGE; CELL MIGRATION; CELL STIMULATION; CELL SURFACE; CELL TRANSPORT; CYTOLOGY; ENDOTHELIUM; FLOW CYTOMETRY; HUMAN; INFLAMMATION; LEUKOCYTE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOLECULAR DYNAMICS; MULTIPOTENT STEM CELL; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TARGET VARIABLE; TISSUE INJURY;

ADULT; ADULT STEM CELLS; CELL ADHESION MOLECULES; CELL MOVEMENT; CHEMOKINES; HUMANS; MESENCHYMAL STEM CELLS; MULTIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; WOUND HEALING;

EID: 34249290744     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2007.06610.x     Document Type: Review

References (105)

1. Abbott, J.D., Huang, Y., Liu, D., Hickey, R., Krause, D.S. Giordano, F.J. (2004) Stromal cell-derived factor-1α plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation, 110, 3300 3305.
2. Arbab, A.S., Jordan, E.K., Wilson, L.B., Yocum, G.T., Lewis, B.K. Frank, J.A. (2004a) In vivo trafficking and targeted delivery of magnetically labeled stem cells. Human Gene Therapy, 15, 351 360.
3. Arbab, A.S., Yocum, G.T., Kalish, H., Jordan, E.K., Anderson, S.A., Khakoo, A.Y., Read, E.J. Frank, J.A. (2004b) Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood, 104, 1217 1223.
4. Arbab, A.S., Yocum, G.T., Rad, A.M., Khakoo, A.Y., Fellowes, V., Read, E.J. 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 in Biomedicine, 18, 553 559.
5. Barbash, I.M., Chouraqui, P., Baron, J., Feinberg, M.S., Etzion, S., Tessone, A., Miller, L., Guetta, E., Zipori, D., Kedes, L.H., Kloner, R.A. Leor, J. (2003) Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation, 108, 863 868.
6. Barry, F.P., Boynton, R.E., Haynesworth, S., Murphy, J.M. Zaia, J. (1999) The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochemical and Biophysical Research Communications, 265, 134 139.
7. Batten, P., Sarathchandra, P., Antoniw, J.W., Tay, S.S., Lowdell, M.W., Taylor, P.M. Yacoub, M.H. (2006) Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: relevance to tissue engineering human heart valves. Tissue Engineering, 12, 2263 2273.
8. Beyer Nardi, N. da Silva Meirelles, L. (2006) Mesenchymal stem cells: isolation, in vitro expansion and characterization. Handbook of Experimental Pharmacology, 174, 249 282.
9. Bos, C., Delmas, Y., Desmouliere, A., Solanilla, A., Hauger, O., Grosset, C., Dubus, I., Ivanovic, Z., Rosenbaum, J., Charbord, P., Combe, C., Bulte, J.W., Moonen, C.T., Ripoche, J. Grenier, N. (2004) In vivo MR imaging of intravascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver. Radiology, 233, 781 789.
10. Bruder, S.P., Horowitz, M.C., Mosca, J.D. Haynesworth, S.E. (1997) Monoclonal antibodies reactive with human osteogenic cell surface antigens. Bone, 21, 225 235.
11. Bruder, S.P., Ricalton, N.S., Boynton, R.E., Connolly, T.J., Jaiswal, N., Zaia, J. Barry, F.P. (1998a) Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. Journal of Bone and Mineral Research, 13, 655 663.
12. Bruder, S.P., Jaiswal, N., Ricalton, N.S., Mosca, J.D., Kraus, K.H. Kadiyala, S. (1998b) Mesenchymal stem cells in osteobiology and applied bone regeneration. Clinical Orthopaedics and Related Research, 355 S247 S256.
13. Bulte, J.W., Douglas, T., Witwer, B., Zhang, S.C., Strable, E., Lewis, B.K., Zywicke, H., Miller, B., van Gelderen P., Moskowitz, B.M., Duncan, I.D. Frank, J.A. (2001) Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nature Biotechnology, 19, 1141 1147.
14. Bulte, J.W., Kraitchman, D.L., Mackay, A.M. Pittenger, M.F. (2004) Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood, 104, 3410 3412.
15. Butcher, E.C. (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell, 67, 1033 1036.
16. Campagnoli, C., Fisk, N., Overton, T., Bennett, P., Watts, T. Roberts, I. (2000) Circulating hematopoietic progenitor cells in first trimester fetal blood. Blood, 95, 1967 1972.
17. Campagnoli, C., Roberts, I.A., Kumar, S., Bennett, P.R., Bellantuono, I. Fisk, N.M. (2001) Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood, 98, 2396 2402.
18. Caplan, A.I. (1991) Mesenchymal stem cells. Journal of Orthopaedic Research, 9, 641 650.
19. Cheifetz, S., Bellon, T., Cales, C., Vera, S., Bernabeu, C., Massague, J. Letarte, M. (1992) Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. Journal of Biological Chemistry, 267, 19027 19030.
20. Chen, J., Li, Y., Wang, L., Zhang, Z., Lu, D., Lu, M. Chopp, M. (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke, 32, 1005 1011.
21. Chen, S.L., Fang, W.W., Qian, J., Ye, F., Liu, Y.H., Shan, S.J., Zhang, J.J., Lin, S., Liao, L.M. Zhao, R.C. (2004) Improvement of cardiac function after transplantation of autologous bone marrow mesenchymal stem cells in patients with acute myocardial infarction. Chinese Medical Journal (English), 117, 1443 1448.
22. Choi, C.B., Cho, Y.K., Bhanu Prakash, K.V., Jee, B.K., Han, C.W., Paik, Y.K., Kim, H.Y., Lee, K.H., Chung, N. Rha, H.K. (2006) Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochemical and Biophysical Research Communications, 350, 138 146.
23. Chute, J.P. (2006) Stem cell homing. Current Opinion in Hematology, 13, 399 406.
24. Dai, W., Hale, S.L., Martin, B.J., Kuang, J.Q., Dow, J.S., Wold, L.E. Kloner, R.A. (2005) Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short- and long-term effects. Circulation, 112, 214 223.
25. Devine, S.M., Bartholomew, A.M., Mahmud, N., Nelson, M., Patil, S., Hardy, W., Sturgeon, C., Hewett, T., Chung, T., Stock, W., Sher, D., Weissman, S., Ferrer, K., Mosca, J., Deans, R., Moseley, A. Hoffman, R. (2001) Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Experimental Hematology, 29, 244 255.
26. Elzaouk, L., Moelling, K. Pavlovic, J. (2006) Anti-tumor activity of mesenchymal stem cells producing IL-12 in a mouse melanoma model. Experimental Dermatology, 15, 865 874.
27. Erices, A., Conget, P. Minguell, J.J. (2000) Mesenchymal progenitor cells in human umbilical cord blood. British Journal of Haematology, 109, 235 242.
28. Fernandez, M., Simon, V., Herrera, G., Cao, C., Del, F.H. Minguell, J.J. (1997) Detection of stromal cells in peripheral blood progenitor cell collections from breast cancer patients. Bone Marrow Transplantation, 20, 265 271.
29. Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G. Mavilio, F. (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science, 279, 1528 1530.
30. Friedenstein, A.J., Gorskaja, J.F. Kulagina, N.N. (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Experimental Hematology, 4, 267 274.
31. Gang, E.J., Bosnakovski, D., Figueiredo, C.A., Visser, J.W. Perlingeiro, R.C. (2007) SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood, 109, 1743 1751.
32. Gao, J., Dennis, J.E., Muzic, R.F., Lundberg, M. Caplan, A.I. (2001) The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells, Tissues, Organs, 169, 12 20.
33. Gnecchi, M., He, H., Liang, O.D., Melo, L.G., Morello, F., Mu, H., Noiseux, N., Zhang, L., Pratt, R.E., Ingwall, J.S. Dzau, V.J. (2005) Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nature Medicine, 11, 367 368.
34. Gnecchi, M., He, H., Noiseux, N., Liang, O.D., Zhang, L., Morello, F., Mu, H., Melo, L.G., Pratt, R.E., Ingwall, J.S. Dzau, V.J. (2006) Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB Journal, 20, 661 669.
35. Hauger, O., Frost, E.E., van Heeswijk R., Deminiere, C., Xue, R., Delmas, Y., Combe, C., Moonen, C.T., Grenier, N. Bulte, J.W. (2006) MR evaluation of the glomerular homing of magnetically labeled mesenchymal stem cells in a rat model of nephropathy. Radiology, 238, 200 210.
36. Haynesworth, S.E., Baber, M.A. Caplan, A.I. (1992) Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone, 13, 69 80.
37. Honczarenko, M., Le, Y., Swierkowski, M., Ghiran, I., Glodek, A.M. Silberstein, L.E. (2006) Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells, 24, 1030 1041.
38. Horwitz, E.M., Prockop, D.J., Fitzpatrick, L.A., Koo, W.W., Gordon, P.L., Neel, M., Sussman, M., Orchard, P., Marx, J.C., Pyeritz, R.E. Brenner, M.K. (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nature Medicine, 5, 309 313.
39. Horwitz, E.M., Prockop, D.J., Gordon, P.L., Koo, W.W., Fitzpatrick, L.A., Neel, M.D., McCarville, M.E., Orchard, P.J., Pyeritz, R.E. Brenner, M.K. (2001) Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood, 97, 1227 1231.
40. Horwitz, E.M., Gordon, P.L., Koo, W.K., Marx, J.C., Neel, M.D., McNall, R.Y., Muul, L. Hofmann, T. (2002) Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proceedings of the National Academy of Sciences of the United States of America, 99, 8932 8937.
41. Horwitz, E.M., Le Blanc, K., Dominici, M., Mueller, I., Slaper-Cortenbach, I., Marini, F.C., Deans, R.J., Krause, D.S. Keating, A. (2005) Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy, 7, 393 395.
42. Hou, M., Yang, K.M., Zhang, H., Zhu, W.Q., Duan, F.J., Wang, H., Song, Y.H., Wei, Y.J. Hu, S.S. (2007) Transplantation of mesenchymal stem cells from human bone marrow improves damaged heart function in rats. International Journal of Cardiology, 115, 220 228.
43. Huss, R., Lange, C., Weissinger, E.M., Kolb, H.J. Thalmeier, K. (2000) Evidence of peripheral blood-derived, plastic-adherent CD34(-/low) hematopoietic stem cell clones with mesenchymal stem cell characteristics. Stem Cells, 18, 252 260.
44. In't Anker, P.S., Noort, W.A., Scherjon, S.A., Kleijburg-van der Keur, C., Kruisselbrink, A.B., van Bezooijen, R.L., Beekhuizen, W., Willemze, R., Kanhai, H.H. Fibbe, W.E. (2003) Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica, 88, 845 852.
45. In't Anker, P.S., Scherjon, S.A., Kleijburg-van der Keur, C., de Groot-Swings, G.M., Claas, F.H., Fibbe, W.E. Kanhai, H.H. (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells, 22, 1338 1345.
46. Ivanova, N., Dobrin, R., Lu, R., Kotenko, I., Levorse, J., DeCoste, C., Schafer, X., Lun, Y. Lemischka, I.R. (2006) Dissecting self-renewal in stem cells with RNA interference. Nature, 442, 533 538.
47. Jaiswal, R.K., Jaiswal, N., Bruder, S.P., Mbalaviele, G., Marshak, D.R. Pittenger, M.F. (2000) Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. Journal of Biological Chemistry, 275, 9645 9652.
48. Ji, J.F., He, B.P., Dheen, S.T. Tay, S.S. (2004) Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells, 22, 415 427.
49. Jiang, W.H., Ma, A.Q., Han, K., Liu, Y., Wang, T.Z., Zheng, X.P. Wang, J. (2005) Ultrastructural changes of rat ischemic myocardium after bone marrow mesenchymal stem cell transplantation. Di Yi Jun Yi Da Xue Xue Bao, 25, 1090 1094.
50. Kopen, G.C., Prockop, D.J. Phinney, D.G. (1999) Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proceedings of the National Academy of Sciences of the United States of America, 96, 10711 10716.
51. Kortesidis, A., Zannettino, A., Isenmann, S., Shi, S., Lapidot, T. Gronthos, S. (2005) Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood, 105, 3793 3801.
52. Kraitchman, D.L., Heldman, A.W., Atalar, E., Amado, L.C., Martin, B.J., Pittenger, M.F., Hare, J.M. Bulte, J.W. (2003) In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation, 107, 2290 2293.
53. Krampera, M., Marconi, S., Pasini, A., Galie, M., Rigotti, G., Mosna, F., Tinelli, M., Lovato, L., Anghileri, E., Andreini, A., Pizzolo, G., Sbarbati, A. Bonetti, B. (2006) Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone, 40, 382 390.
54. Kuznetsov, S.A., Mankani, M.H., Gronthos, S., Satomura, K., Bianco, P. Robey, P.G. (2001) Circulating skeletal stem cells. The Journal of Cell Biology, 153, 1133 1140.
55. Lazarus, H.M., Haynesworth, S.E., Gerson, S.L. Caplan, A.I. (1997) Human bone marrow-derived mesenchymal (stromal) progenitor cells (MPCs) cannot be recovered from peripheral blood progenitor cell collections. Journal of Hematotherapy, 6, 447 455.
56. Le Blanc, K., Rasmusson, I., Sundberg, B., Gotherstrom, C., Hassan, M., Uzunel, M. Ringden, O. (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 363, 1439 1441.
57. Lee, R.H., Kim, B., Choi, I., Kim, H., Choi, H.S., Suh, K., Bae, Y.C. Jung, J.S. (2004) Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cellular Physiology and Biochemistry, 14, 311 324.
58. Li, G.R., Deng, X.L., Sun, H., Chung, S.S., Tse, H.F. Lau, C.P. (2006) Ion channels in mesenchymal stem cells from rat bone marrow. Stem Cells, 24, 1519 1528.
59. von Luttichau, I., Notohamiprodjo, M., Wechselberger, A., Peters, C., Henger, A., Seliger, C., Djafarzadeh, R., Huss, R. Nelson, P.J. (2005) Human adult. Stem Cells and Development, 14, 329 336.
60. Majumdar, M.K., Keane-Moore, M., Buyaner, D., Hardy, W.B., Moorman, M.A., McIntosh, K.R. Mosca, J.D. (2003) Characterization and functionality of cell surface molecules on human mesenchymal stem cells. Journal of Biomedical Sciences, 10, 228 241.
61. Makino, S., Fukuda, K., Miyoshi, S., Konishi, F., Kodama, H., Pan, J., Sano, M., Takahashi, T., Hori, S., Abe, H., Hata, J., Umezawa, A. Ogawa, S. (1999) Cardiomyocytes can be generated from marrow stromal cells in vitro. Journal of Clinical Investigation, 103, 697 705.
62. Mansilla, E., Marin, G.H., Drago, H., Sturla, F., Salas, E., Gardiner, C., Bossi, S., Lamonega, R., Guzman, A., Nunez, A., Gil, M.A., Piccinelli, G., Ibar, R. Soratti, C. (2006) Bloodstream cells phenotypically identical to human mesenchymal bone marrow stem cells circulate in large amounts under the influence of acute large skin damage: new evidence for their use in regenerative medicine. Transplantation Proceedings, 38, 967 969.
63. McFarlin, K., Gao, X., Liu, Y.B., Dulchavsky, D.S., Kwon, D., Arbab, A.S., Bansal, M., Li, Y., Chopp, M., Dulchavsky, S.A. Gautam, S.C. (2006) Bone marrow-derived mesenchymal stromal cells accelerate wound healing in the rat. Wound Repair and Regeneration, 14, 471 478.
64. Minguell, J.J., Erices, A. Conget, P. (2001) Mesenchymal stem cells. Experimental Biology and Medicine, 226, 507 520.
65. Miyahara, Y., Nagaya, N., Kataoka, M., Yanagawa, B., Tanaka, K., Hao, H., Ishino, K., Ishida, H., Shimizu, T., Kangawa, K., Sano, S., Okano, T., Kitamura, S. Mori, H. (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nature Medicine, 12, 459 465.
66. Miyasaka, M. Tanaka, T. (2004) Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nature Reviews. Immunology, 4, 360 370.
67. Muller, W.A., Weigl, S.A., Deng, X. Phillips, D.M. (1993) PECAM-1 is required for transendothelial migration of leukocytes. Journal of Experimental Medicine, 178, 449 460.
68. Noiseux, N., Gnecchi, M., Lopez-Ilasaca, M., Zhang, L., Solomon, S.D., Deb, A., Dzau, V.J. Pratt, R.E. (2006) Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Molecular Therapy, 14, 840 850.
69. Ortiz, L.A., Gambelli, F., McBride, C., Gaupp, D., Baddoo, M., Kaminski, N. Phinney, D.G. (2003) Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proceedings of the National Academy of Sciences of the United States of America, 100, 8407 8411.
70. Pereira, R.F., Halford, K.W., O'Hara, M.D., Leeper, D.B., Sokolov, B.P., Pollard, M.D., Bagasra, O. Prockop, D.J. (1995) Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proceedings of the National Academy of Sciences of the United States of America, 92, 4857 4861.
71. Pijnappels, D.A., Schalij, M.J., van Tuyn J., Ypey, D.L., de Vries, A.A., van der Wall, E.E., van der Laarse A. Atsma, D.E. (2006) Progressive increase in conduction velocity across human mesenchymal stem cells is mediated by enhanced electrical coupling. Cardiovascular Research, 72, 282 291.
72. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S. Marshak, D.R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science, 284, 143 147.
73. Purton, L.E., Mielcarek, M. Torok-Storb, B. (1998) Monocytes are the likely candidate 'stromal' cell in G-CSF-mobilized peripheral blood. Bone Marrow Transplantation, 21, 1075 1076.
74. Ramasamy, R., Lam, E.W., Soeiro, I., Tisato, V., Bonnet, D. Dazzi, F. (2006) Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia, 21, 304 310.
75. Rasmusson, I. (2006) Immune modulation by mesenchymal stem cells. Experimental Cell Research, 312, 2169 2179.
76. Rombouts, W.J. Ploemacher, R.E. (2003) Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia, 17, 160 170.
77. Roufosse, C.A., Direkze, N.C., Otto, W.R. Wright, N.A. (2004) Circulating mesenchymal stem cells. The International Journal of Biochemistry and Cell Biology, 36, 585 597.
78. Ruster, B., Gottig, S., Ludwig, R.J., Bistrian, R., Muller, S., Seifried, E., Gille, J. Henschler, R. (2006) Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood, 108, 3938 3944.
79. Schmidt, A., Ladage, D., Steingen, C., Brixius, K., Schinkothe, T., Klinz, F.J., Schwinger, R.H., Mehlhorn, U. Bloch, W. (2006) Mesenchymal stem cells transmigrate over the endothelial barrier. European Journal of Cellular Biology, 85, 1179 1188.
80. Segers, V.F., Van Riet, I., Andries, L.J., Lemmens, K., Demolder, M.J., De Becker, A.J., Kockx, M.M. De Keulenaer, G.W. (2006) Mesenchymal stem cell adhesion to cardiac microvascular endothelium: activators and mechanisms. American Journal of Physiology. Heart and Circulatory Physiology, 290, H1370 H1377.
81. Sekiya, I., Larson, B.L., Smith, J.R., Pochampally, R., Cui, J.G. Prockop, D.J. (2002) Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells, 20, 530 541.
82. Shih, D.T., Lee, D.C., Chen, S.C., Tsai, R.Y., Huang, C.T., Tsai, C.C., Shen, E.Y. Chiu, W.T. (2005) Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells, 23, 1012 1020.
83. Simmons, P.J. Torok-Storb, B. (1991) Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood, 78, 55 62.
84. Sordi, V., Malosio, M.L., Marchesi, F., Mercalli, A., Melzi, R., Giordano, T., Belmonte, N., Ferrari, G., Leone, B.E., Bertuzzi, F., Zerbini, G., Allavena, P., Bonifacio, E. Piemonti, L. (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood, 106, 419 427.
85. Springer, T.A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell, 76, 301 314.
86. Stagg, J. (2007) Immune regulation by mesenchymal stem cells: two sides to the coin. Tissue Antigens, 69, 1 9.
87. Togel, F., Hu, Z., Weiss, K., Isaac, J., Lange, C. Westenfelder, C. (2005) Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. American Journal of Physiology. Renal Physiology, 289, F31 F42.
88. Toma, J.G., Akhavan, M., Fernandes, K.J., Barnabe-Heider, F., Sadikot, A., Kaplan, D.R. Miller, F.D. (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biology, 3, 778 784.
89. Tondreau, T., Lagneaux, L., Dejeneffe, M., Massy, M., Mortier, C., Delforge, A. Bron, D. (2004) Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation, 72, 319 326.
90. Wang, L., Li, Y., Chen, J., Gautam, S.C., Zhang, Z., Lu, M. Chopp, M. (2002a) Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Experimental Hematology, 30, 831 836.
91. Wang, L., Li, Y., Chen, X., Chen, J., Gautam, S.C., Xu, Y. Chopp, M. (2002b) MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology, 7, 113 117.
92. Wang, H.S., Hung, S.C., Peng, S.T., Huang, C.C., Wei, H.M., Guo, Y.J., Fu, Y.S., Lai, M.C. Chen, C.C. (2004) Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells, 22, 1330 1337.
93. Wang, Y., Johnsen, H.E., Mortensen, S., Bindslev, L., Sejersten Ripa, R., Haack-Sorensen, M., Jorgensen, E., Fang, W. Kastrup, J. (2006) Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart, 92, 768 774.
94. Weimar, I.S., Miranda, N., Muller, E.J., Hekman, A., Kerst, J.M., de Gast, G.C. Gerritsen, W.R. (1998) Hepatocyte growth factor/scatter factor (HGF/SF) is produced by human bone marrow stromal cells and promotes proliferation, adhesion and survival of human hematopoietic progenitor cells (CD34+). Experimental Hematology, 26, 885 894.
95. Wexler, S.A., Donaldson, C., Denning-Kendall, P., Rice, C., Bradley, B. Hows, J.M. (2003) Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. British Journal of Haematology, 121, 368 374.
96. Wu, G.D., Nolta, J.A., Jin, Y.S., Barr, M.L., Yu, H., Starnes, V.A. Cramer, D.V. (2003) Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation, 75, 679 685.
97. Wynn, R.F., Hart, C.A., Corradi-Perini, C., O'Neill, L., Evans, C.A., Wraith, J.E., Fairbairn, L.J. 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.
98. Xu, Y., Mirmalek-Sani, S.H., Yang, X., Zhang, J. Oreffo, R.O. (2006) The use of small interfering RNAs to inhibit adipocyte differentiation in human preadipocytes and fetal-femur-derived mesenchymal cells. Experimental Cell Research, 312, 1856 1864.
99. Yamada, Y., Ueda, M., Hibi, H. Baba, S. (2006) A novel approach to periodontal tissue regeneration with mesenchymal stem cells and platelet-rich plasma using tissue engineering technology: A clinical case report. The International Journal of Periodontics & Restorative Dentistry, 26, 363 369.
100. Yang, Y., Relan, N.K., Przywara, D.A. Schuger, L. (1999) Embryonic mesenchymal cells share the potential for smooth muscle differentiation: myogenesis is controlled by the cell's shape. Development, 126, 3027 3033.
101. Ye, Z.Q., Burkholder, J.K., Qiu, P., Schultz, J.C., Shahidi, N.T. Yang, N.S. (1994) Establishment of an adherent cell feeder layer from human umbilical cord blood for support of long-term hematopoietic progenitor cell growth. Proceedings of the National Academy of Sciences of the United States of America, 91, 12140 12144.
102. Yoon, J., Min, B.G., Kim, Y.H., Shim, W.J., Ro, Y.M. Lim, D.S. (2005) Differentiation, engraftment and functional effects of pre-treated mesenchymal stem cells in a rat myocardial infarct model. Acta Cardiology, 60, 277 284.
103. Yu, S., Tanabe, T., Dezawa, M., Ishikawa, H. Yoshimura, N. (2006) Effects of bone marrow stromal cell injection in an experimental glaucoma model. Biochemical and Biophysical Research Communications, 344, 1071 1079.
104. Zuk, P.A., Zhu, M., Ashjian, P., De Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P. Hedrick, M.H. (2002) Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell, 13, 4279 4295.
105. Zvaifler, N.J., Marinova-Mutafchieva, L., Adams, G., Edwards, C.J., Moss, J., Burger, J.A. Maini, R.N. (2000) Mesenchymal precursor cells in the blood of normal individuals. Arthritis Research, 2, 477 488.