Bone marrow and adipose tissue-derived mesenchymal stem sells: How close are they?

Journal of Stem Cells

Volumn 2, Issue 2, 2007, Pages 73-89

  Baptista, Leandra S ^a   Pedrosa, Carolina G S ^a   Silva, Karina R ^a   Otazú, Ivone B ^a   Takiya, Christina M ^a   Dutra, Hélio S ^a   Cláudio da Silva, César ^a   Borojevic, Radovan ^a   Rossi, M Isabel D ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Adipose tissue; Bone marrow; Hematopoiesis; Mesenchymal stem cell; Pericytes

Indexed keywords

OSTEOCALCIN; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; TRANSCRIPTION FACTOR RUNX2;

ADIPOSE TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CHONDROGENESIS; GENE EXPRESSION PROFILING; HEMATOPOIESIS; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; MESENCHYMAL STEM CELL; MESODERM; NONHUMAN; PERICYTE; PHENOTYPE; REGENERATIVE MEDICINE; SMOOTH MUSCLE FIBER; SUBCUTANEOUS TISSUE; VASCULAR SMOOTH MUSCLE;

EID: 77953668752     PISSN: 15568539     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (107)

1. Weiss, L. (1976). The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat. Rec., 186, 161-184.
2. Bianco, P., Riminucci, M., Gronthos, S., and Robey, P. G. (2001). Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells, 19, 180-192.
3. Friedstein, A. J., Chailakhyan, R. K., and Lalykina, K. S. (1970). The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet., 3, 393-402.
4. Castro-Malaspina, H., Gay, R. E., Resnick, G., Kapoor, N., Meyers, P., Chiarieri, D., McKenzie, S., Broxmeyer, H. E., and Moore, M. A. (1980). Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood, 56, 289-301.
5. Caplan, A.I. (1991). Mesenchymal stem cell. J. Orthop. Res., 9, 641-650.
6. Prockop D. J (1997). Marrow stromal cells as stem cells for nonhematopoeitic tissues. Science, 276, 71-74.
7. 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., and Marshak, D. R. (1999). Multilineage potential do adult human mesenchymal stem cells. Science, 284, 143-147.
8. Muraglia, A., Cancedda, R., and Quarto, R. (2000). Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci., 113, 1161-166.
9. Dennis, J. E. and Charbord, P. (2002). Origin and differentiation of human murine stroma. Stem Cells, 20, 205-214.
10. Gronthos, S., Zannetino, A. C., Hay, S. J., Shi, S., Graves, S. E., Kortesidis, A., and Simmons, P. J. (2003). Molecular and cellular characteristics of highly purified stromal stem cells derived from human bone marrow. J Cell Sci., 116, 1827-1835.
11. Toma, C., Pittrieger, M. F., Cahill, K. S., Byrne, B. J., and Kessler, P. D. (2002). Human mesenchymal stem cells differentiate try a cardiomyocyte phenotype in the adult murine heart. Circulation, 105, 93-98.
12. Wang, J.S., Shum-Tim, D., Chedrawy, E., and Chiu, R. C. (2001). The coronary delivery of marrow stromal cells or myocardial regeneration: pathophysiological and therapeutic implications. J Thorac. Cardiovasc. Surg.,122, 699-705.
13. Silva, G. V., Litovsky, S., Assad, J. A.R., Sousa, A. L.S., Martin, B. J., Vela, D., Coulter, S. C., Lin, J., Ober, J., Vaughn, W. K., Branco, R. V.C., Oliveira, E. M., He, R., Geng, Y-J., Willerson, J. T., and Perin, E. C. (2005). Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation, 111, 150-156.
14. Lopes, F. R. P., Campos, L. C. M., Corrêa Jr., J. D., Balduino, A., Lora, S., Langone, F., Borojevic, R., and Martinez, A. M. B. (2006). Bone marrow stromal cells and resorbable collagen guidance tubes enhance sciatic nerve regeneration in mice. Exp. Neurol., 198, 457-468.
15. Gronthos, S. and Zannettino, A. C. W. (2006). Potential of bone marrow stromal stein cells to repair bone defects and fractures. J Stem Cells, 1, 35-45.
16. Al-Khaldi, A., Al-Sabti, H., Galipeau, J., and Lachapelle, K. (2003). Therapeutic angiogenesis using autologous bone marrow stromal cells: Improved blood flow in a chronic limb ischemia model. Ann Thorac. Surg., 75, 204-209.
17. Le Blanc, K. and Ringdén, O. (2006). Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr. Opin. Immunol., 18, 586-591.
18. Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., and Hedrick M. H. (2002). Human adipose tissue is a source of multipotente stem cells. Mol. Biol. Cell, 12, 4279-4295.
19. Huss, R., Lange, C., Weissinger, E. M., Kolb, H-J., and 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.
20. Kuznetsov, S. A., Mankani, M. H., Gronthos, S., Satomura, K., Bianco, P., and Robey, P. G. (2001). Circulating skeletal stem cells. J Cell Biol., 153, 1133-1139.
21. De Bari, C., Dell'Accio, F., Tvlzanowski, P., and Luyten, F. P. (2001). Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis. Rheum., 44, 1928-1942.
22. Young, H. E., Steele, T. A., Bray, R. A., Hudson, J., Floyd, J. A., Hawkins, K., Thomas, K., Austin, T. Edwards, C. Cuzzourl, J., Duenzl, M., Lucas, P. A., and Black, A. C., Jr. (2001). Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat. Rec., 264, 51-62.
23. Shi, S. and Gronthos, S. (2003). Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res., 18, 696-704.
24. Kǒgler, G., Sensken, S., Airey, J. A., Trapp, T., Müchen, M., Feldhahn, N., Liedtke, S., Sorg, R. V., Fischer, J., Rosenbaum, C., Greschat; S., Knipper, A., Bender, J., Degistirici, Ö., Gao, J., Caplan, A. I., Colletti, E. I., Almeida-Porada, G., Müller, H. W., Zanjani, E., and Wernet, P. (2004). A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J. Exp. Med, 200, 123-135.
25. Shih, D. T., Lee, D-C., Chen, S-C., Tsai, R-Y., Huang, C-T., Tsai, C-C., Shen, E-Y., and Chiu, W-T. (2005). Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells, 23, 1012-1020.
26. Silva-Meirelles, L., Chagastelles, P. C., and Nardi, N. B. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci., 119, 2204-2213.
27. Short B., Brouard, N., Occhiodoro-Scott, T., Ramakrishman, A., and Simmons, P. J. (2003). Mesenchymal stem cells. Arch. Med Res., 34, 565-571.
28. Mizimo, H., Zuk, P. A., Zhu, M., Lorenz, P., Benhaim, P., and Hedrick, M. H. (2002). Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr. Surg., 109, 199-209.
29. Dragoo,L. J., Lieberman, J. R., Lee, R. S., Deugarte, D. A., Lee, Y., Zuk, P. A., Hedrick, M. H., and Benhaim, P. (2005). Tissue-engineered bone from BMP-2-transduced stem cells derived from human fat. Plast Reconstr. Surg., 115, 1665-1673.
30. Winter, A., Breit, S., Parsch, D., Benz, K., Steck, E., Haurier, H., Weber, R. M., Ewerbeck, V., and Richter, W. (2003). Cartilage-like gene expression in differentiated human stem cell spheroids. Arthritis. Rheum., 48, 418-429.
31. Rodriguez, A-M., Pisani, D., Dechesne, C. A., Turc-Carel, C., Kurzenne, J-Y., Wdziekonski, B., Villageois, A., Bagnis, C., Breittmayer, J-P., Groux, H., Ailhaud, G., and Dani, C. (2005). Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp. Med, 201, 1397-1495.
32. Planat-Bernard, V., Silvestre, J-S., Cousin, B., André, M., Nibbelink, M., Tamarat, R., Clergue, M., Manneville, C., Saillan-Baffreau, C., Duriez, M., Tedgui, A., Levy, B., Pénicaud, L., and Casteilla, L. (2004). Plasticity of human adipose lineage cells toward endothelial cells. Physiological and therapeutic perspectives. Circulation; 109, 656-663.
33. Le Blanc, K., Rasmusson, I., Sundberg, B., Götherström, C., Hassan, M., Uzunel, M., and Ringdén, O. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 636:1439-1441.
34. Garcia-Olmo, D., Garcia-Arranz; M., Herreros, D., Pascual, I., Peiro, C., and Rodriguez-Montes, J. A. (2004). A phase I clinical trial of the treatment of Crohn's fistula by adipose mesenchymal stem cell transplantation. Dis. Colon Rectum., 48, 1416-1423.
35. Yañez, R., Lamana, M. L., García-Castro, J., Colmenero, I., Ramirez, M., and Bueren, J. A. (2006). Adipose tissue-derived mesenchymal stem cells (AD-MSCS) have immunosuppressive properties applicable for the in vivo control of the graft-versus-host disease (GVHD). Stem Cells, 24, 2582-2591.
36. Beresford, J. N., Benneth, J. H., Devlin, C., Leboy, P. S., and Owen M. E. (1992). Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J. Cell Sci., 102, 341-351.
37. Nuttall, M. E. and Gimble, J. M. (2004). Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr. Op. Pharmacol., 4, 290-294.
38. Kaplan, F. S. (1996). Skin and bones. Arch. Dermatol., 132, 815-818.
39. Shore, E. M., Ahn, J., de Beur, S. J., Li, M., Xu, M., Gardner, R. J. M., Zasloff, M. A., Whyte, M. P., Levine, M. A., and Kaplan, F. S. (2002). Paternally inherited inactivating mutations of the GNAS1 gene in progressive osseous heteroplasia. N. Engl. J. Med., 346, 99-106.
40. Wagner, W., Wein, F., Seckinger, A., Frankhauser, M., Wirkner, U., Krause, U., Blake, J., Schwager, C., Eckstein, V., Ansorge, W., and Ho, H. (2005). Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol., 33, 1402-1416.
41. Shahdadfar, A., Frønsdal, K., Haug, T., Reinholt, F. P., and Brinchmann, J. E. (2005). In vitro expansion of human mesenchymal stem cells: choice of serum Is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells, 23, 1357-1366.
42. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G.M., and Ingber, D. E. (1997). Geometric control of cell life and death. Science, 276, 1425-1428.
43. Lelièvre, S. A., Weaver, V. M., Nickerson, J. A., Larabell, C. A., Bhaumik, A., Petersen, O. W., and Bissel, M. J. (1998). Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proc. Nat. Acad. Sci. USA, 95, 14711-14716.
44. Thomas, C. H., Collier, J. H., Sfeir, C. S., and Healy, K. E. (2002). Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc. Nat. Acad. Sci. USA, 99, 1972-1977.
45. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Developmental Cell, 6, 483-495.
46. Rossi, M. I. D., Barros, A. P. D. N., Baptista, L. S., Garzoni, L. R.,, Meirelles, M. N, Takiya, C. M., Pascarelli, B. M., Dutra, H. S., and Borojevic, R. (2005). Multicellular spheroids of bone marrow stromal cells: a three-dimensional in vitro culture system for the study of hematopoietic cell migration. Braz. J. Med. Biol. Res., 38, 455-462.
47. Chun, T-H., Hotary, K. B., Sabeh, F., Saltiel, A. R., Allen, E. D., and Weiss, S. J. (2006). A pericellular collagenase directs the 3-Dimensional development of white adipose tissue. Cell, 125, 577-591.
48. Dicker, A., Le Blanc, L., Aström, G., van Harmelen, V., Götherström, C., Blomqvist, L., Arner, P., and Rydén, M. (2005). Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp. Cell Res., 308, 283-290.
49. Liu, T. M., Martina, M., Hutmacher, D. W., Hoi, J., Hui, P., Lee, E. H., and Lim, B. (2006). Identification of common pathways mediating differentiation of bone marrow and adipose tissues derived human mesenchymal stem cells (MSCs) into three mesenchymal lineages. Stem Cells, published online doi: 10. 1634/stemcells.2006-0394.
50. Im, G-I., Shin, Y-W., and Lee, K-B. (2005). Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthritis Cartilage, 13, 845-853.
51. Conejero, J. A., Lee, J. A., Parrett, B. M., Terry, M., Wear-Maggitti, K., Grant, R. T., and Breitbart, A. S. (2006). Repair of palatal bone defects using osteogenically differentiated fat-derived stem cells. Plast Reconstr. Surg., 117, 857-863.
52. Hicok, K. C., du Laney, T. V., Zhou, Y. S., Halvorsen, Y-D. C., Hitt, D. C., Cooper, L. F., and Gimble, J. M. (2004). Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng., 10, 371-380.
53. Dominici, M. Le Blanc K., Müeller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Procokop, D. J., and Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, 315-317.
54. Simmons, P. J. and Torok-Storb, B. (1991). Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood, 78, 55-62.
55. De Ugarte, D. A., Alfonso, Z., Zuk, P. A., Elbarbary, A., Zhu, M., Ashjian, P., Benhaim, P., Hedrick, M. H., and Fraser, J. K. (2003). Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol. Lett., 89, 267-270.
56. Minguell, J. J., Erices, A., and Conget, P. (2001). Mesenchymal stem cells. Exp Biol Med, 226, 507-520.
57. Gronthos, S., Franklin, D. M., Leddy, H. A., Robey, P. G., Storms, R. W., Gimble, J. M. (2001). Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell Physiol., 189, 54-63.
58. Mitchell, J. B., McIntosh, K., Zvonic, S., garret, S., Floyd, E., Kloster, A., Di Halvorsen, Y., Storms, R. W., Goh, B., Kilroy, G., Wu, X., and Gimble, J. M. (2006). Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells, 24, 376-385.
59. Boquest, A. C., Shahdadfar A., Fronsdal, K., Sigurjonsson. O., Tunheim, S. H., Collas, P., and Brinchmann, J. E. (2005). Isolation and transcription profiling of purified uncultured human stromal stem cells: Alteration of gene expression after in vitro cell culture. Mol. Biol. Cell, 16, 1131-114 1.
60. Colter, D. C., Class, R., DiGiolamo, C. M., and Prockop, D. J. (2000). Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc. Natl. Acad. Sci. USA, 97, 3213-3218.
61. Zengin, E., Chalajour, F., Gehling, U. M., Ito, W. D., Treede, H., Lauke, H., Weil, J., Reichcrispurner, H., Kilic, N., and Ergün, S. (2006). Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development, 133, 1543-1551.
62. Godin, I. and Cumano, A. (2002). The hare and the tortoise: an embryonic hematopoietic race. Nat. Rev. Immunol., 2, 593-604.
63. Charbord, P., Tavian, M., Humeau, L., and Péault, B. (1996). Early ontogeny of the human marrow from long bones: An immunohistochemical study of hematopoiesis and its microenvironment. Blood, 87, 4109-4119.
64. Arai, F., Ohneda, O., Miyamoto, T., Zhang, X. Q., and Suda, T. (2002). Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp. Med, 195, 1543-1563.
65. Bianco, P. and Cossu, G. (1999). Uno, nessuno e centomila: searching for the identity of mesodermal progenitors. Exp. Cell Res., 251, 257-263.
66. Cossu, G. and Bianco, P. (2003). Mesoangioblasts - vascular progenitors for extravascular mesodermal tissues. Curr. Opin. Genet Dev., 13, 537-542.
67. Diaz-Flores, L., Gutierrez, R., Lopez-Alonso, A., Gonzalez, R., and Varela, H. (1992). Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop. Relat. Res., 75, 280-286.
68. Gregoire, F. M., Smas, C. M., and Sul, H. S. (1998). Understanding adipocyte differentiation. Physiol. Rev., 78, 783-809.
69. Otto, T. C. and Lane, M. D. (2005). Adipose development: From stem cell to adipocyte. Crit. Rev. Biochem. Mol. Biol., 40, 229-242.
70. Kawaguchi, N., Toriyama, K., Nicodemous-Lena, E., Inou, K., Toni, S., and Kitagawa, Y. (1998). De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proc. Natl. Acad Sci. USA, 95, 1062-1066.
71. Iyama, K., Ohzono, K., and Usuku, G. (1979). Electron microscopical studies on the genesis of white adipocytes: differentiation of immature pericytes into adipocytes in transplanted preadipose tissues. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol., 31, 143-1455.
72. Richardson, R. L., Hausman, G. J., and Campion, D. R. (1982). Response of pericytes to thermal lesion in the inguinal fat pad of 10-day-old rats. Acta Anat. (Basel), 114, 41-57.
73. Gerhardt, H. and Betsholtz, C. (2003). Endothelial-pericyte interactions in angiogenesis. Cell Tissue Reg., 314, 15-23.
74. Armulik, A., Abramsson, A., and Betsholtz, C. (2005). Endothelial/ pericytes interactions. Circ. Res., 97, 512-523.
75. Doherty, M. J., Ashton, B. A., Walsh, S., Beresford, J. N., Grant M. E., and Canfield, A. E. (1998). Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res., 13, 828-838.
76. Tintut, Y., Alfonso, Z., Saini, T., Radcliff, K., Watson, K., Boström, K., and Demer, L. L. (2003). Multilineage potential of cells from the artery wall. Circulation 108, 2505-2510.
77. Farrington-Rock, C., Crofts, N. J., Doherty, M. J., Ashton, B. A., Griffin-Jones, C., and Canfield, A. E. (2004). Chondrogenic and adipogenic potential of microvascular pericytes. Circulation, 110: 2226-2232.
78. Etchevers, H. C., Vincent C., Le Douarin, N. M., and Couly, G. F. (2001). The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development, 128, 1059-1068.
79. Mikawa, T. and Gourdie, R. G. (1996). Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with in growth of the epicardial organ. Int. Dev. Biol., 174, 221-232.
80. DeRuiter, M. C., Poelmann, R. E., VanMunsteren, J. C., Mironov, V., Markwald, R. R., and Gittenberger-de Groot A.C. (1997). Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ. Res., 80, 444-451.
81. Drake, D. J., Hungerford, J. E., and Little, C. D. (1998). Morphogenesis of the first blood vessels. Ann. N. Y Acad Sci., 857, 155-179.
82. Hungerford, J. E. and Little, C. D. (1999). Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J Vasc. Res., 36, 2-27.
83. Minasi, M. G., Riminucci, M., DeAngelis, L., Borello, U., Berarducci, B., Innocenzi, A., Caprioli, A., Sirabella, D., Baiocchi, M., De Maria, R., Boratto, R., Jaffredo, T., Broccoli, V., Bianco, P., and Cossu, G. (2002). The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development, 129, 2773-2783.
84. Pouget, C., Gautier, R., Teillet, M-A., and Jaffredo, T. (2006). Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development, 133, 1013-1022.
85. Lamagna, C. and Bergers, G. (2006). The bone marrow constitutes a reservoir of pericytes progenitors. J Leukoc. Biol, 80, 677-681.
86. Erices, A., Conge, P., and Miguell, J. J. (2000). Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol., 109, 235-242.
87. Campagnoli, C., Roberts, I. A. G., Kumar, S., Bennett, P. R., Beflantuono, I., and Fisk, N. M. (2001). Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood, 98, 2396-2402.
88. O'Donoghue, K, Chan, J., Fuente, J. de la, Kennea, N., Sandison, A., Anderson J. R., Roberts, I. A. G., and Fisk, N. M. (2004). Microchimerism in female bone marrow and bone decades after fetal mesenchymal stem-cell trafficking in pregnancy. Lancet, 364, 179-182.
89. Mendes, S. C., Robin, C., and Dzierzak, E. (2004). Mesenchymal progenitor cells localize within heinatopoietic sites throughout ontogeny. Development, 132, 1127-1136.
90. Hong, K. M., Burdick M. D., Phillips, R. J., Heber, D., and Strieter, R, M. (2005). Characterization of human fibrocytes as circulating adipocyte progenitors and the formation of human adipose tissue in SCID mice. FASEB J., 19, 2029-2031.
91. Crossno, J. T. Jr., Majka, S. M., Grazia. T., Gill, R. G., and Klemm, D. J. (2006). Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J Clin. Invest., 116, 320-328.
92. Miura, Y., Gao, Z., Miura, M., Seo, B-M., Sonoyama, W., Chen, W., Gronthos, S., Zhang, L., and Shi, S. (2006). Mesenchymal stem cell-organized bone marrow elements: An alternative hematopoietic progenitor resource. Stem Cells, 24, 2428-2436.
93. Muguruma, Y., Yahata, T., Miyatake, H., Sato, T., Uno, T., Rob, J., Kato, S., Ito, M., Hotta, T., and Ando, K. (2006). Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment. Blood, 107, 1878-1887.
94. Oostendorp, R. A., Harvey, K. N., Kusadasi, N., de Bruijn, M. F. T. R., Saris, C., Ploemacher, R. E., Medvinsky, A. L., and Dzierzak, E. (2002). Stromal cell lines from mouse aorta-gonads-mesonephros subregions are potent supporters of hematopoietic stem cell activity. Blood, 99, 1183-1189.
95. Duran, C., Robin, C, and Dzierzak, E. (2006). Mesenchymal lineage potentials of aorta-gonad-mesonephros stromal clones. Haematologica, 91, 1172-1179.
96. Kim, J. S., Cho, H. H., Kim, Y. J., Seo, S. Y., Kim, H. N., Lee, J. B., Kim, J. H., Chung, J. S., and Jung, J. S. (2005). Human adipose stromal cells expanded in human serum promote engraftment of human peripheral blood hematopoietic stem cells in NOD/SCID mice. Biochem. Biophys. Res. Commun., 329, 25-31.
97. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., and Ferrante, A. W. Jr. (2003). Obesity is associated with macrophage accumulation in adipose tissue. J Clin. Invest., 112, 1798-1808.
98. Xu, H., Barnes, G. T., Yang, O., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., and Chen, H. (2003). Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest., 112, 1821-1830.
99. + cells. Br. J Haematol., 127, 344-347.
100. Ren, D., Collingwood, T. N., Rebar, E. J., Wolffe, A. P., and Camp, H. S. (2002). PPARgamma knockdown by engineered transcription factors: exogeneous PPARgamma2 but not PPARganima1 reactivates adipogenesis. Genes Develop., 16, 27-32.
101. Corre, J., Barreau, C., Cousin, B., Chavoin, J-P., Caton, D., Fournial, G., Penicaud, L., Castetilla, L., and Laharrague, P. (2006). Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J Cell Physiol., 208, 282-288.
102. Taichman, R. S., Reilly, M. J., and Emerson, S. G. (1996) Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood, 87, 518-524.
103. Calvi, L. M., Adams, G. B., Wlbrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C,, Martin, R. P., Schipani, E., Divieti, P., Bringhurst, F. R., Milner, L. A., Kronenberg, H. M., and Scadden, D. T. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature, 425, 841-846.
104. Zhang, J., Niu, C, Ye, L., Huang, H., He, X., Tong, W-G., Rossi, J., Haug, J., Johnson, T., Feng, J. Q., Harris, S., Wiedemann, L. M., Mishina, Y., and Li, L. (2003)Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 425, 836-841.
105. Balduino, A., Hurtado, S. P., Frazão, P., Takiya, C. M., Alves, L. M., Nasciutti, L-E., El-Cheikh, M. C., and Borojevic, R. (2005). Bone marrow subendosteal microenvironment harbours functionally distinct haemosupportive stromal cell populations. Cell Tissue Res, 319,255-266.
106. Atkins, G. J., Kostakis, P., Pan, B., Farrugia, A., Gronthos, S., Evdokiou, A., Harrison, K., Findlay, D. M., and Zannettino, A. C. (2003). RANKL expression is related to the differentiation state of human osteoblasts. J Bone Miner Res., 18, 1088-1098.
107. Corral, D. A., Amling, M., Priemel, M., Loyer, E., Fuchs, S., Ducy, P., Baron, R., and Karsenty, G. (1998). Dissociation between bone resorption and bone formation in osteopenic tiansgenic mice. Proc Natl. Acad Sci. USA, 95,13835-13840.