In search of the in vivo identity of mesenchymal stem cells

Stem Cells

Volumn 26, Issue 9, 2008, Pages 2287-2299

  Meirelles, Lindolfo Da Silva ^a   Caplan, Arnold I ^b   Nardi, Nance Beyer ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adult stem cell; Mesenchymal stem cell; Pericyte; Perivascular niche; Tissue repair

Indexed keywords

BLOOD VESSEL; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL ISOLATION; CELL MATURATION; CELL THERAPY; CELL TRANSPLANTATION; ENDOTHELIUM CELL; HOMEOSTASIS; HYPOTHESIS; IMMUNE SYSTEM; IMMUNOREGULATION; IN VIVO STUDY; MESENCHYMAL STEM CELL; PARACRINE SIGNALING; PERICYTE; REVIEW; TISSUE; TISSUE INJURY; TISSUE REPAIR;

ANIMALS; BLOOD VESSELS; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; MESENCHYMAL STEM CELLS; MODELS, BIOLOGICAL; PERICYTES;

EID: 55049092713     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-1122     Document Type: Review

References (208)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
2. Doss MX, Koehler CI, Gissel C et al. Embryonic stem cells: A promising tool for cell replacement therapy. J Cell Mol Med 2004;8:465-473.
3. Verfaillie CM. Adult stem cells: Assessing the case for pluripotency. Trends Cell Biol 2002;12:502-508.
4. Nerem RM. Cell-based therapies: From basic biology to replacement, repair, and regeneration. Biomaterials 2007;28:5074-5077.
5. Asano T, Sasaki K, Kitano Y et al. In vivo tumor formation from primate embryonic stem cells. Methods Mol Biol 2006;329:459-467.
6. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: Stem cells and their niche. Cell 2004;116:769 -778.
7. Paré JF, Sherley JL. Biological principles for ex vivo adult stem cell expansion. Curr Top Dev Biol 2006;73:141-171.
8. Lennon DP, Haynesworth SE, Bruder SP et al. Human and animal mesenchymal progenitor cells from bone marrow: Identification of serum for optimal selection and proliferation. In Vitro Cell Dev Biol Anim 1996;32:602-611.
9. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006;119:2204-2213.
10. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084.
11. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991;9:641-650.
12. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970;3:393-403.
13. Phinney DG. Building a consensus regarding the nature and origin of mesenchymal stem cells. J Cell Biochem Suppl 2002;38:7-12.
14. Krampera M, Marconi S, Pasini A et al. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 2007;40:382-390.
15. Prunet-Marcassus B, Cousin B, Caton D et al. From heterogeneity to plasticity in adipose tissues: Site-specific differences. Exp Cell Res 2006;312:727-736.
16. Mitsiadis TA, Barrandon O, Rochat A et al. Stem cell niches in mammals. Exp Cell Res 2007;313:3377-3385.
17. Sacchetti B, Funari A, Michienzi S et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007;131:324-336.
18. Wilson A, Oser GM, Jaworski M et al. Dormant and self-renewing hematopoietic stem cells and their niches. Ann N Y Acad Sci 2007;1106:64-75.
19. Orkin SH, Zon LI. Hematopoiesis: An evolving paradigm for stem cell biology. Cell 2008;132:631-644.
20. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006;6:93-106.
21. Pedemonte E, Benvenuto F, Casazza S et al. The molecular signature of therapeutic mesenchymal stem cells exposes the architecture of the hematopoietic stem cell niche synapse. BMC Genomics 2007;8:65.
22. Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Res Ther 2007;9:204.
23. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
24. Anjos-Afonso F, Bonnet D. Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 2007;109:1298-1306.
25. Gang EJ, Bosnakovski D, Figueiredo CA et al. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 2007;109:1743-1751.
26. Delorme B, Ringe J, Gallay N et al. Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 2008;111:2631-2635.
27. Wright GJ, Jones M, Puklavec MJ et al. The unusual distribution of the neuronal/lymphoid cell surface CD200 (OX2) glycoprotein is conserved in humans. Immunology 2001;102:173-179.
28. Tallheden T, Dennis JE, Lennon DP et al. Phenotypic plasticity of human articular chondrocytes. J Bone Joint Surg 2003;85-A(suppl 2):93-100.
29. Azizi SA, Stokes D, Augelli BJ et al. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats - Similarities to astrocyte grafts. Proc Natl Acad Sci U S A 1998;95:3908-3913.
30. Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A 1999;96:10711-10716.
31. Lange C, Bassler P, Lioznov MV et al. Liver-specific gene expression in mesenchymal stem cells is induced by liver cells. World J Gastroenterol 2005;11:4497-4504.
32. Sato Y, Araki H, Kato J et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005;106:756-763.
33. Woodbury D, Schwarz EJ, Prockop DJ et al. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000;61:364-370.
34. Coyne TM, Marcus AJ, Woodbury D et al. Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. STEM CELLS 2006;24:2483-2492.
35. Beyer Nardi N, da Silva Meirelles L. Mesenchymal stem cells: Isolation, in vitro expansion and characterization. Handb Exp Pharmacol 2006;249-282.
36. Bobis S, Jarocha D, Majka M. Mesenchymal stem cells: Characteristics and clinical applications. Folia Histochem Cytobiol 2006;44:215-230.
37. Le Blanc K. Mesenchymal stromal cells: Tissue repair and immune modulation. Cytotherapy 2006;8:559-561.
38. Kojima K, Ignotz RA, Kushibiki T et al. Tissue-engineered trachea from sheep marrow stromal cells with transforming growth factor beta2 released from biodegradable microspheres in a nude rat recipient. J Thorac Cardiovasc Surg 2004;128:147-153.
39. Le Blanc K, Rasmusson I, Sundberg B et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363:1439-1441.
40. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007;213:341-347.
41. Haynesworth SE, Goshima J, Goldberg VM et al. Characterization of cells with osteogenic potential from human marrow. Bone 1992;13:81-88.
42. Lennon DP, Caplan AI. Mesenchymal stem cells for tissue engineering. In: Vunjak-Novakovic G, Freshney RI, eds. Culture of Cells for Tissue Engineering. Hoboken, NJ: Wiley, 2006:23-59.
43. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
44. Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: Characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 2004;8:301-316.
45. Horwitz EM, Le Blanc K, Dominici M et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005;7:393-395.
46. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: Paradoxes of passaging. Exp Hematol 2004;32:414-425.
47. Diaz-Romero J, Gaillard JP, Grogan SP et al. Immunophenotypic analysis of human articular chondrocytes: Changes in surface markers associated with cell expansion in monolayer culture. J Cell Physiol 2005;202:731-742.
48. Barbero A, Ploegert S, Heberer M et al. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 2003;48:1315-1325.
49. Watt FM, Hogan BL. Out of Eden: Stem cells and their niches. Science 2000;287:1427-1430.
50. Caplan AI, Bruder SP. Mesenchymal stem cells: Building blocks for molecular medicine in the 21st century. Trends Mol Med 2001;7:259-264.
51. Devine SM, Cobbs C, Jennings M et al. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 2003;101:2999-3001.
52. Kang SK, Lee DH, Bae YC et al. Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol 2003;183:355-366.
53. Mouiseddine M, Francois S, Semont A et al. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br J Radiol 2007;80(spec no 1):S49-S55.
54. Nagaya N, Fujii T, Iwase T et al. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 2004;287:H2670-H2676.
55. Horwitz EM, Prockop DJ, Fitzpatrick LA et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-313.
56. Horwitz EM, Prockop DJ, Gordon PL et al. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood 2001;97:1227-1231.
57. Horwitz EM, Gordon PL, Koo WK et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002;99:8932-8937.
58. Dai WD, Hale SL, Martin BJ et al. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium - Short- and long-term effects. Circulation 2005;112:214-223.
59. Fazel S, Chen LW, Weisel RD et al. Cell transplantation preserves cardiac function after infarction by infarct stabilization: Augmentation by stem cell factor. J Thorac Cardiovasc Surg 2005;130:1310-1318.
60. Noiseux N, Gnecchi M, Lopez-Ilasaca M et al. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 2006;14:840-850.
61. Zhao LR, Duan WM, Reyes M et al. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 2002;174:11-20.
62. Gnecchi M, He HM, Liang OD et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368.
63. Kinnaird T, Stabile E, Burnett MS et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004;94:678-685.
64. Kinnaird T, Stabile E, Burnett MS et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004;109:1543-1549.
65. Tang YL, Zhao Q, Qin XY et al. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 2005;80:229-237.
66. Zhang M, Mal N, Kiedrowski M et al. SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction. FASEB J 2007;21:3197-3207.
67. Redmond DE Jr, Bjugstad KB, Teng YD et al. Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc Natl Acad Sci U S A 2007;104:12175-12180.
68. Fang BJ, Shi MX, Liao LM et al. Systemic infusion of FLK1(+) mesenchymal stem cells ameliorate carbon tetrachloride-induced liver fibrosis in mice. Transplantation 2004;78:83-88.
69. Ortiz LA, Gambelli F, McBride C et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci U S A 2003;100:8407-8411.
70. Fujiyama S, Amano K, Uehira K et al. Bone marrow monocyte lineage cells adhere on injured endothelium in a monocyte chemoattractant protein-1-dependent manner and accelerate reendothelialization as endothelial progenitor cells. Circ Res 2003;93:980-989.
71. Le Blanc K, Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 2007;262:509-525.
72. Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: A new strategy for immunosuppression? Trends Immunol 2007;28:219-226.
73. Di Nicola M, Carlo-Stella C, Magni M et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99:3838-3843.
74. Krampera M, Glennie S, Dyson J et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003;101:3722-3729.
75. Le Blanc K, Tammik L, Sundberg B et al. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003;57:11-20.
76. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
77. Potian JA, Aviv H, Ponzio NM et al. Veto-like activity of mesenchymal stem cells: Functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 2003;171:3426-3434.
78. Djouad F, Plence P, Bony C et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003;102:3837-3844.
79. Maccario R, Podesta M, Moretta A et al. Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 2005;90:516-525.
80. Rasmusson I, Ringden O, Sundberg B et al. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003;76:1208-1213.
81. Spaggiari GM, Capobianco A, Becchetti S et al. Mesenchymal stem cell-natural killer cell interactions: Evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006;107:1484-1490.
82. Corcione A, Benvenuto F, Ferretti E et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006;107:367-372.
83. Jiang XX, Zhang Y, Liu B et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005;105:4120-4126.
84. Zhang W, Ge W, Li C et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 2004;13:263-271.
85. Bartholomew A, Sturgeon C, Siatskas M et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002;30:42-48.
86. Le Blanc K, Gotherstrom C, Ringden O et al. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79:1607-1614.
87. Meisel R, Zibert A, Laryea M et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004;103:4619-4621.
88. Sato K, Ozaki K, Oh I et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007;109:228-234.
89. Ringdén O, Uzunel M, Rasmusson I et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006;81:1390-1397.
90. Ryan JM, Barry FP, Murphy JM et al. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond) 2005;2:8.
91. Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106:1755-1761.
92. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978;4:7-25.
93. Verfaillie CM. Anatomy and physiology of hematopoiesis. In: Hoffman R, Strauss M, Benz EJJ et al., eds. Hematology - Basic Principles and Practice. 3rd ed. Philadelphia: Churchill-Livingstone, 2000:139-154.
94. Braun KM, Niemann C, Jensen UB et al. Manipulation of stem cell proliferation and lineage commitment: Visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 2003;130:5241-5255.
95. Gould E, Reeves AJ, Graziano MSA et al. Neurogenesis in the neocortex of adult primates. Science 1999;286:548-552.
96. Lazarus HM, Haynesworth SE, Gerson SL et al. Human bone marrow-derived mesenchymal (stromal) progenitor cells (MPCs) cannot be recovered from peripheral blood progenitor cell collections. J Hematother 1997;6:447-455.
97. Wexler SA, Donaldson C, Denning-Kendall P et al. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br J Haematol 2003;121:368-374.
98. Rochefort GY, Delorme B, Lopez A et al. Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia. STEM CELLS 2006;24:2202-2208.
99. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001;7:211-228.
100. Nakahara H, Dennis JE, Bruder SP et al. In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res 1991;195:492-503.
101. Nakahara H, Goldberg VM, Caplan AI. Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res 1991;9:465-476.
102. Nakahara H, Goldberg VM, Caplan AI. Culture-expanded periosteal-derived cells exhibit osteochondrogenic potential in porous calcium-phosphate ceramics in vivo. Clin Orthop Relat Res 1992;291-298.
103. Salingcarnboriboon R, Yoshitake H, Tsuji K et al. Establishment of tendon-derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp Cell Res 2003;287:289-300.
104. Seo BM, Miura M, Gronthos S et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004;364:149-155.
105. Kuroda R, Usas A, Kubo S et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum 2006;54:433-442.
106. Lee JY, Qu-Petersen Z, Cao B et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 2000;150:1085-1100.
107. De Bari C, Dell'Accio F, Tylzanowski P et al. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-1942.
108. Toma JG, Akhavan M, Fernandes KJ et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001;3:778-784.
109. Sabatini F, Petecchia L, Tavian M et al. Human bronchial fibroblasts exhibit a mesenchymal stem cell phenotype and multilineage differentiating potentialities. Lab Invest 2005;85:962-971.
110. Bianco P, Cossu G. Uno, nessuno e centomila: Searching for the identity of mesodermal progenitors. Exp Cell Res 1999;251:257-263.
111. Bianco P, Riminucci M, Gronthos S et al. Bone marrow stromal stem cells: Nature, biology, and potential applications. STEM CELLS 2001;19:180-192.
112. Brighton CT, Lorich DG, Kupcha R et al. The pericyte as a possible osteoblast progenitor-cell. Clin Orthop Relat Res 1992;287-299.
113. Doherty MJ, Ashton BA, Walsh S et al. Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res 1998;13:828-838.
114. Farrington-Rock C, Crofts NJ, Doherty MJ et al. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 2004;110:2226-2232.
115. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003;18:696-704.
116. Hirschi KK, D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res 1996;32:687-698.
117. Shepro D, Morel NM. Pericyte physiology. FASEB J 1993;7:1031-1038.
118. Sims DE. The pericyte - A review. Tissue Cell 1986;18:153-174.
119. Pinzani M. Hepatic stellate (ITO) cells: Expanding roles for a liver-specific pericyte. J Hepatol 1995;22:700-706.
120. Schlondorff D. The glomerular mesangial cell: An expanding role for a specialized pericyte. FASEB J 1987;1:272-281.
121. Funk PE, Stephan RP, Witte PL. Vascular cell adhesion molecule 1-positive reticular cells express interleukin-7 and stem cell factor in the bone marrow. Blood 1995;86:2661-2671.
122. Charbord P, Tavian M, Humeau L et al. Early ontogeny of the human marrow from long bones: An immunohistochemical study of hematopoiesis and its microenvironment. Blood 1996;87:4109-4119.
123. Galmiche MC, Koteliansky VE, Briere J et al. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 1993;82:66-76.
124. Schmitt-Gräff A, Skalli O, Gabbiani G. Alpha-smooth muscle actin is expressed in a subset of bone marrow stromal cells in normal and pathological conditions. Virchows Arch B Cell Pathol Incl Mol Pathol 1989;57:291-302.
125. Andreeva ER, Pugach IM, Gordon D et al. Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell 1998;30:127-135.
126. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 2005;97:512-523.
127. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000;6:389-395.
128. Richardson RL, Hausman GJ, Campion DR. Response of pericytes to thermal lesion in the inguinal fat pad of 10-day-old rats. Acta Anat (Basel) 1982;114:41-57.
129. Diaz-Flores L, Gutierrez R, Gonzalez P et al. Inducible perivascular cells contribute to the neochondrogenesis in grafted perichondrium. Anat Rec 1991;229:1-8.
130. Diaz-Flores L, Gutierrez R, Lopez-Alonso A et al. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 1992;280-286.
131. Brighton CT, Hunt RM. Early histologic and ultrastructural changes in microvessels of periosteal callus. J Orthop Trauma 1997;11:244-253.
132. Davidoff MS, Middendorff R, Enikolopov G et al. Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 2004;167:935-944.
133. McCulloch CA. Progenitor cell populations in the periodontal ligament of mice. Anat Rec 1985;211:258 -262.
134. Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. STEM CELLS 2006;24:1529-1538.
135. da Silva Meirelles L, Nardi NB. Murine marrow-derived mesenchymal stem cell: Isolation, in vitro expansion, and characterization. Br J Haematol 2003;123:702-711.
136. Sugiyama T, Kohara H, Noda M et al. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006;25:977-988.
137. Majumdar MK, Thiede MA, Mosca JD et al. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 1998;176:57-66.
138. Muguruma Y, Yahata T, Miyatake H et al. Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment. Blood 2006;107:1878-1887.
139. Abedin M, Tintut Y, Demer LL. Mesenchymal stem cells and the artery wall. Circ Res 2004;95:671-676.
140. Covas DT, Piccinato CE, Orellana MD et al. Mesenchymal stem cells can be obtained from the human saphena vein. Exp Cell Res 2005;309:340-344.
141. Calvi LM, Adams GB, Weibrecht KW et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003;425:841-846.
142. Zhang J, Niu C, Ye L et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003;425:836-841.
143. Goshima J, Goldberg VM, Caplan AI. The osteogenic potential of culture-expanded rat marrow mesenchymal cells assayed in vivo in calcium phosphate ceramic blocks. Clin Orthop Relat Res 1991;298-311.
144. Iyemere VP, Proudfoot D, Weissberg PL et al. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J Intern Med 2006;260:192-210.
145. Chamley-Campbell JH, Campbell GR, Ross R. Phenotype-dependent response of cultured aortic smooth muscle to serum mitogens. J Cell Biol 1981;89:379 -383.
146. Schmitt-Gräff A, Chakroun G, Gabbiani G. Modulation of perisinusoidal cell cytoskeletal features during experimental hepatic fibrosis. Virchows Arch A Pathol Anat Histopathol 1993;422:99-107.
147. Covas DT, Panepucci RA, Fontes AM et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 2008;36:642-654.
148. Choi KS, Shin JS, Lee JJ et al. In vitro trans-differentiation of rat mesenchymal cells into insulin-producing cells by rat pancreatic extract. Biochem Biophys Res Commun 2005;330:1299-1305.
149. Wang B, Han J, Gao Y et al. The differentiation of rat adipose-derived stem cells into OEC-like cells on collagen scaffolds by co-culturing with OECs. Neurosci Lett 2007;421:191-196.
150. Dore-Duffy P, Katychev A, Wang X et al. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 2006;26:613-624.
151. Kordes C, Sawitza I, Muller-Marbach A et al. CD133+ hepatic stellate cells are progenitor cells. Biochem Biophys Res Commun 2007;352:410-417.
152. Minasi MG, Riminucci M, De Angelis L et al. The meso-angioblast: A multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 2002;129:2773-2783.
153. Takashima Y, Era T, Nakao K et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 2007;129:1377-1388.
154. Foster K, Sheridan J, Veiga-Fernandes H et al. Contribution of neural crest-derived cells in the embryonic and adult thymus. J Immunol 2008;180:3183-3189.
155. Etchevers HC, Vincent C, Le Douarin NM et al. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 2001;128:1059-1068.
156. Korn J, Christ B, Kurz H. Neuroectodermal origin of brain pericytes and vascular smooth muscle cells. J Comp Neurol 2002;442:78-88.
157. Quirici N, Soligo D, Bossolasco P et al. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 2002;30:783-791.
158. Cattoretti G, Schiro R, Orazi A et al. Bone marrow stroma in humans: Anti-nerve growth factor receptor antibodies selectively stain reticular cells in vivo and in vitro. Blood 1993;81:1726-1738.
159. Coutinho A. The Le Douarin phenomenon: A shift in the paradigm of developmental self-tolerance. Int J Dev Biol 2005;49:131-136.
160. Raimondi G, Turnquist HR, Thomson AW. Frontiers of immunological tolerance. Methods Mol Biol 2007;380:1-24.
161. Carlan MC, Peres A, Nardi NB. Frequency of B cells in normal mice which recognize self proteins. Braz J Med Biol Res 1997;30:225-230.
162. Mutsaers SE, Bishop JE, McGrouther G et al. Mechanisms of tissue repair: From wound healing to fibrosis. Int J Biochem Cell Biol 1997;29:5-17.
163. Tsirogianni AK, Moutsopoulos NM, Moutsopoulos HM. Wound healing: Immunological aspects. Injury 2006;37(suppl 1):S5-S12.
164. Postlethwaite AE, Shigemitsu H, Kanangat S. Cellular origins of fibroblasts: Possible implications for organ fibrosis in systemic sclerosis. Curr Opin Rheumatol 2004;16:733-738.
165. Rajkumar VS, Sundberg C, Abraham DJ et al. Activation of microvascular pericytes in autoimmune Raynaud's phenomenon and systemic sclerosis. Arthritis Rheum 1999;42:930-941.
166. Sundberg C, Ivarsson M, Gerdin B et al. Pericytes as collagen-producing cells in excessive dermal scarring. Lab Invest 1996;74:452-466.
167. Saile B, Knittel T, Matthes N et al. CD95/CD95L-mediated apoptosis of the hepatic stellate cell. A mechanism terminating uncontrolled hepatic stellate cell proliferation during hepatic tissue repair. Am J Pathol 1997;151:1265-1272.
168. Fujiwara H, Hayashi Y, Sanzen N et al. Regulation of mesodermal differentiation of mouse embryonic stem cells by basement membranes. J Biol Chem 2007;282:29701-29711.
169. Yamashima T, Tonchev AB, Vachkov IH et al. Vascular adventitia generates neuronal progenitors in the monkey hippocampus after ischemia. Hippocampus 2004;14:861-875.
170. Ohab JJ, Fleming S, Blesch A et al. A neurovascular niche for neurogenesis after stroke. J Neurosci 2006;26:13007-13016.
171. English K, Barry FP, Field-Corbett CP et al. IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett 2007;110:91-100.
172. Oh I, Ozaki K, Sato K et al. Interferon-gamma and NF-kappaB mediate nitric oxide production by mesenchymal stromal cells. Biochem Biophys Res Commun 2007;355:956-962.
173. Ryan JM, Barry F, Murphy JM et al. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 2007;149:353-363.
174. Rüster B, Gottig S, Ludwig RJ et al. Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 2006;108:3938-3944.
175. Segers VF, Van Riet I, Andries LJ et al. Mesenchymal stem cell adhesion to cardiac microvascular endothelium: Activators and mechanisms. Am J Physiol Heart Circ Physiol 2006;290:H1370-H1377.
176. Mangi AA, Noiseux N, Kong D et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;9:1195-1201.
177. Mei SH, McCarter SD, Deng Y et al. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. Plos Med 2007;4:e269.
178. Nayak RC, Berman AB, George KL et al. A monoclonal antibody (3G5)-defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med 1988;167:1003-1015.
179. Helmbold P, Wohlrab J, Marsch WC et al. Human dermal pericytes express 3G5 ganglioside - A new approach for microvessel histology in the skin. J Cutan Pathol 2001;28:206-210.
180. Helmbold P, Nayak RC, Marsch WC et al. Isolation and in vitro characterization of human dermal microvascular pericytes. Microvasc Res 2001;61:160-165.
181. Sundberg C, Kowanetz M, Brown LF et al. Stable expression of angiopoietin-1 and other markers by cultured pericytes: Phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab Invest 2002;82:387-401.
182. Brachvogel B, Moch H, Pausch F et al. Perivascular cells expressing annexin A5 define a novel mesenchymal stem cell-like population with the capacity to differentiate into multiple mesenchymal lineages. Development 2005;132:2657-2668.
183. Hegner B, Weber M, Dragun D et al. Differential regulation of smooth muscle markers in human bone marrow-derived mesenchymal stem cells. J Hypertens 2005;23:1191-1202.
184. Bandopadhyay R, Orte C, Lawrenson JG et al. Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J Neurocytol 2001;30:35-44.
185. Vogel W, Grunebach F, Messam CA et al. Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 2003;88:126-133.
186. Aleksandrova MA, Sukhikh GT, Chailakhyan RK et al. Comparative analysis of differentiation and behavior of human neural and mesenchymal stem cells in vitro and in vivo. Bull Exp Biol Med 2006;141:152-160.
187. Alliot F, Rutin J, Leenen PJ et al. Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin. J Neurosci Res 1999;58:367-378.
188. Lardon J, Rooman I, Bouwens L. Nestin expression in pancreatic stellate cells and angiogenic endothelial cells. Histochem Cell Biol 2002;117:535-540.
189. Ozerdem U, Monosov E, Stallcup WB. NG2 proteoglycan expression by pericytes in pathological microvasculature. Microvasc Res 2002;63:129-134.
190. Murfee WL, Skalak TC, Peirce SM. Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: Identifying a venule-specific phenotype. Microcirculation 2005;12:151-160.
191. Schlingemann RO, Rietveld FJ, de Waal RM et al. Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 1990;136:1393-1405.
192. Garlanda C, Dejana E. Heterogeneity of endothelial cells. Specific markers. Arterioscler Thromb Vasc Biol 1997;17:1193-1202.
193. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991;78:55-62.
194. Yamagishi S, Yonekura H, Yamamoto Y et al. Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Invest 1999;79:501-509.
195. Ankoma-Sey V, Wang Y, Dai Z. Hypoxic stimulation of vascular endothelial growth factor expression in activated rat hepatic stellate cells. Hepatology 2000;31:141-148.
196. Müller AM, Hermanns MI, Skrzynski C et al. Expression of the endothelial markers PECAM-1, vWf, and CD34 in vivo and in vitro. Exp Mol Pathol 2002;72:221-229.
197. Skalli O, Pelte MF, Peclet MC et al. Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 1989;37:315-321.
198. Fukasawa K, Fujii H, Saitoh Y et al. Aminopeptidase N (APN/CD13) is selectively expressed in vascular endothelial cells and plays multiple roles in angiogenesis. Cancer Lett 2006;243:135-143.
199. Oishi K, Kamiyashiki T, Ito Y. Isometric contraction of microvascular pericytes from mouse brain parenchyma. Microvasc Res 2007;73:20-28.
200. Haynesworth SE, Baber MA, Caplan AI. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 1992;13:69-80.
201. Fleming JE Jr, Haynesworth SE, Cassiede P et al. Monoclonal antibody against adult marrow-derived mesenchymal stem cells recognizes developing vasculature in embryonic human skin. Dev Dyn 1998;212:119-132.
202. Bardin N, George F, Mutin M et al. S-Endo 1, a pan-endothelial monoclonal antibody recognizing a novel human endothelial antigen. Tissue Antigens 1996;48:531-539.
203. Croitoru-Lamoury J, Lamoury FM, Zaunders JJ et al. Human mesenchymal stem cells constitutively express chemokines and chemokine receptors that can be upregulated by cytokines, IFN-beta, and copaxone. J Interferon Cytokine Res 2007;27:53- 64.
204. Honczarenko M, Le Y, Swierkowski M et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. STEM CELLS 2006;24:1030-1041.
205. Ji JF, He BP, Dheen ST et al. 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 2004;22:415-427.
206. Ponte AL, Marais E, Gallay N et al. The in vitro migration capacity of human bone marrow mesenchymal stem cells: Comparison of chemokine and growth factor chemotactic activities. STEM CELLS 2007;25:1737-1745.
207. Sordi V, Malosio ML, Marchesi F et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005;106:419-427.
208. Chemokine/chemokine receptor nomenclature. Cytokine 2003;21:48-49.