The Gap Between the Physiological and Therapeutic Roles of Mesenchymal Stem Cells

Medicinal Research Reviews

Volumn 34, Issue 5, 2014, Pages 1100-1126

  Galderisi, Umberto ^a,b,c   Giordano, Antonio ^d,e,f  

^a TEMPLE UNIVERSITY   (United States)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c ERCIYES UNIVERSITY   (Turkey)

^d Temple University   (United States)

^e NATIONAL CANCER INSTITUTE   (Italy)

^f UNIVERSITY OF SIENA   (Italy)

Author keywords

Differentiation; Engraftment; Immunomodulation; Paracrine effects; Secretome; Transplants

Indexed keywords

ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL HETEROGENEITY; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; CONNECTIVE TISSUE; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; STEM CELL CULTURE; STEM CELL EXPANSION;

BIOLOGICAL MARKER;

BIOLOGICAL MARKERS; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION;

EID: 84905453740     PISSN: 01986325     EISSN: 10981128     Source Type: Journal    
DOI: 10.1002/med.21322     Document Type: Article

References (135)

1. Friedenstein AJ, Piatetzky S, II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 1966;16(3):381-390.
2. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968;6(2):230-247.
3. Tavassoli M, Crosby WH. Transplantation of marrow to extramedullary sites. Science 1968;161(3836):54-56.
4. Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974;2(2):83-92.
5. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, Robey PG. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997;12(9):1335-1347.
6. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: In vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987;20(3):263-272.
7. Owen M, Friedenstein AJ. Stromal stem cells: Marrow-derived osteogenic precursors. Ciba Found Symp 1988;136:42-60.
8. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991;9(5):641-650.
9. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8(4):315-317.
10. Bianco P, Cao X, Frenette PS, Mao JJ, Robey PG, Simmons PJ, Wang CY. The meaning, the sense and the significance: Translating the science of mesenchymal stem cells into medicine. Nat Med 2013;19(1):35-42.
11. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000;113(Pt 7):1161-1166.
12. Alessio N, Bohn W, Rauchberger V, Rizzolio F, Cipollaro M, Rosemann M, Irmler M, Beckers J, Giordano A, Galderisi U. Silencing of RB1 but not of RB2/P130 induces cellular senescence and impairs the differentiation potential of human mesenchymal stem cells. Cell Mol Life Sci 2013;70(9):1637-1651.
13. Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Science 2003;116(Pt 9):1827-1835.
14. Battula VL, Treml S, Bareiss PM, Gieseke F, Roelofs H, de Zwart P, Muller I, Schewe B, Skutella T, Fibbe WE, Kanz L, Buhring HJ. Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica 2009;94(2):173-184.
15. Jarocha D, Lukasiewicz E, Majka M. Advantage of mesenchymal stem cells (MSC) expansion directly from purified bone marrow CD105+ and CD271+ cells. Folia Histochem Cytobiol 2008;46(3):307-314.
16. Gang EJ, Bosnakovski D, Figueiredo CA, Visser JW, Perlingeiro RC. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 2007;109(4):1743-1751.
17. Bianco P, Robey PG, Saggio I, Riminucci M. "Mesenchymal" stem cells in human bone marrow (skeletal stem cells): A critical discussion of their nature, identity, and significance in incurable skeletal disease. Human Gene Ther 2010;21(9):1057-1066.
18. Russell KC, Tucker HA, Bunnell BA, Andreeff M, Schober W, Gaynor AS, Strickler KL, Lin S, Lacey MR, O'Connor KC. Cell-surface expression of neuron-glial antigen 2 (NG2) and melanoma cell adhesion molecule (CD146) in heterogeneous cultures of marrow-derived mesenchymal stem cells. Tissue Eng Part A 2013;19(19-20):2253-2266.
19. Tormin A, Li O, Brune JC, Walsh S, Schutz B, Ehinger M, Ditzel N, Kassem M, Scheding S. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 2011;117(19):5067-5077.
20. Morikawa S, Mabuchi Y, Kubota Y, Nagai Y, Niibe K, Hiratsu E, Suzuki S, Miyauchi-Hara C, Nagoshi N, Sunabori T, Shimmura S, Miyawaki A, Nakagawa T, Suda T, Okano H, Matsuzaki Y. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009;206(11):2483-2496.
21. Mabuchi Y, Houlihan DD, Akazawa C, Okano H, Matsuzaki Y. Prospective isolation of murine and human bone marrow mesenchymal stem cells based on surface markers. Stem Cells Int 2013;2013:507301.
22. Arai F, Ohneda O, Miyamoto T, Zhang XQ, Suda T. Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med 2002;195(12):1549-1563.
23. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003;18(4):696-704.
24. Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 2008;111(9):4551-4558.
25. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007;131(2):324-336.
26. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003;425(6960):841-846.
27. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003;425(6960):836-841.
28. Muguruma Y, Yahata T, Miyatake H, Sato T, Uno T, Itoh J, Kato S, Ito M, Hotta T, Ando K. Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment. Blood 2006;107(5):1878-1887.
29. Chan CK, Chen CC, Luppen CA, Kim JB, DeBoer AT, Wei K, Helms JA, Kuo CJ, Kraft DL, Weissman IL. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 2009;457(7228):490-494.
30. Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, Mackem S, Carmeliet G, Kronenberg HM. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 2010;19(2):329-344.
31. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010;466(7308):829-834.
32. Chan CK, Lindau P, Jiang W, Chen JY, Zhang LF, Chen CC, Seita J, Sahoo D, Kim JB, Lee A, Park S, Nag D, Gong Y, Kulkarni S, Luppen CA, Theologis AA, Wan DC, DeBoer A, Seo EY, Vincent-Tompkins JD, Loh K, Walmsley GG, Kraft DL, Wu JC, Longaker MT, Weissman IL. Clonal precursor of bone, cartilage, and hematopoietic niche stromal cells. Proc Natl Acad Sci USA 2013;110(31):12643-12648.
33. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004;118(2):149-161.
34. Nakamura Y, Arai F, Iwasaki H, Hosokawa K, Kobayashi I, Gomei Y, Matsumoto Y, Yoshihara H, Suda T. Isolation and characterization of endosteal niche cell populations that regulate hematopoietic stem cells. Blood 2010;116(9):1422-1432.
35. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 2009;460(7252):259-263.
36. Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, Nagasawa T. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 2010;33(3):387-399.
37. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008;3(3):301-313.
38. Covas DT, Piccinato CE, Orellana MD, Siufi JL, Silva WA, Jr., Proto-Siqueira R, Rizzatti EG, Neder L, Silva AR, Rocha V, Zago MA. Mesenchymal stem cells can be obtained from the human saphena vein. Exp Cell Res 2005;309(2):340-344.
39. 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(Pt 11):2204-2213.
40. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000;109(1):235-242.
41. Gang EJ, Jeong JA, Hong SH, Hwang SH, Kim SW, Yang IH, Ahn C, Han H, Kim H. Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells 2004;22(4):617-624.
42. Gong X, Sun Z, Cui D, Xu X, Zhu H, Wang L, Qian W, Han X. Isolation and characterization of lung resident mesenchymal stem cells capable of differentiating into alveolar epithelial type II cells. Cell Biol Int 2012;4:e11.
43. Gullo F, De Bari C. Prospective purification of a subpopulation of human synovial mesenchymal stem cells with enhanced chondro-osteogenic potency. Rheumatology (Oxford) 2013;52(10):1758-1768.
44. Heidari B, Shirazi A, Akhondi MM, Hassanpour H, Behzadi B, Naderi MM, Sarvari A, Borjian S. Comparison of proliferative and multilineage differentiation potential of sheep mesenchymal stem cells derived from bone marrow, liver, and adipose tissue. Avicenna J Med Biotechnol 2013;5(2):104-117.
45. Komada Y, Yamane T, Kadota D, Isono K, Takakura N, Hayashi S, Yamazaki H. Origins and properties of dental, thymic, and bone marrow mesenchymal cells and their stem cells. PloS One 2012;7(11):e46436.
46. Martin J, Helm K, Ruegg P, Varella-Garcia M, Burnham E, Majka S. Adult lung side population cells have mesenchymal stem cell potential. Cytotherapy 2008;10(2):140-151.
47. Perry BC, Zhou D, Wu X, Yang FC, Byers MA, Chu TM, Hockema JJ, Woods EJ, Goebel WS. Collection, cryopreservation, and characterization of human dental pulp-derived mesenchymal stem cells for banking and clinical use. Tissue Eng Part C Methods 2008;14(2):149-156.
48. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 2010;12(2):143-152.
49. Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzl M, Lucas PA, Black AC, Jr. 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 2001;264(1):51-62.
50. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13(12):4279-4295.
51. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001;98(8):2396-2402.
52. Chang CJ, Yen ML, Chen YC, Chien CC, Huang HI, Bai CH, Yen BL. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem cells 2006;24(11):2466-2477.
53. Deng MJ, Jin Y, Shi JN, Lu HB, Liu Y, He DW, Nie X, Smith AJ. Multilineage differentiation of ectomesenchymal cells isolated from the first branchial arch. Tissue Eng 2004;10(9-10):1597-1606.
54. Mendes SC, Robin C, Dzierzak E. Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Development 2005;132(5):1127-1136.
55. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, Nishikawa S. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 2007;129(7):1377-1388.
56. van den Heuvel RL, Versele SR, Schoeters GE, Vanderborght OL. Stromal stem cells (CFU-f) in yolk sac, liver, spleen and bone marrow of pre- and postnatal mice. Br J Haematol 1987;66(1):15-20.
57. Smith LG, Weissman IL, Heimfeld S. Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc Natl Acad Sci USA 1991;88(7):2788-2792.
58. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004;103(5):1669-1675.
59. Sarugaser R, Hanoun L, Keating A, Stanford WL, Davies JE. Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PloS One 2009;4(8):e6498.
60. Jones E, Churchman SM, English A, Buch MH, Horner EA, Burgoyne CH, Reece R, Kinsey S, Emery P, McGonagle D, Ponchel F. Mesenchymal stem cells in rheumatoid synovium: Enumeration and functional assessment in relation to synovial inflammation level. Ann Rheum Dis 2010;69(2):450-457.
61. Dromard C, Bourin P, Andre M, De Barros S, Casteilla L, Planat-Benard V. Human adipose derived stroma/stem cells grow in serum-free medium as floating spheres. Exp Cell Res 2011;317(6):770-780.
62. Maumus M, Peyrafitte JA, D'Angelo R, Fournier-Wirth C, Bouloumie A, Casteilla L, Sengenes C, Bourin P. Native human adipose stromal cells: Localization, morphology and phenotype. Int J Obes 2011;35(9):1141-1153.
63. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008;214(2):413-421.
64. Morikawa S, Mabuchi Y, Niibe K, Suzuki S, Nagoshi N, Sunabori T, Shimmura S, Nagai Y, Nakagawa T, Okano H, Matsuzaki Y. Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun 2009;379(4):1114-1119.
65. Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, Morikawa S, Okada Y, Mabuchi Y, Katoh H, Okada S, Fukuda K, Suda T, Matsuzaki Y, Toyama Y, Okano H. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2008;2(4):392-403.
66. Nagoshi N, Shibata S, Nakamura M, Matsuzaki Y, Toyama Y, Okano H. Neural crest-derived stem cells display a wide variety of characteristics. J Cell Biochem 2009;107(6):1046-1052.
67. Morita Y, Ema H, Nakauchi H. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J Exp Med 2010;207(6):1173-1182.
68. Quesenberry P, Abedi M, Dooner M, Colvin G, Sanchez-Guijo FM, Aliotta J, Pimentel J, Dooner G, Greer D, Demers D, Keaney P, Peterson A, Luo L, Foster B. The marrow cell continuum: Stochastic determinism. Folia Histochem Cytobiol 2005;43(4):187-190.
69. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998;279(5356):1528-1530.
70. Onyia JE, Clapp DW, Long H, Hock JM. Osteoprogenitor cells as targets for ex vivo gene transfer. J Bone Miner Res 1998;13(1):20-30.
71. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 1995;92(11):4857-4861.
72. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5(3):309-313.
73. Chen SL, Fang WW, Ye F, Liu YH, Qian J, Shan SJ, Zhang JJ, Chunhua RZ, Liao LM, Lin S, Sun JP. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004;94(1):92-95.
74. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belem L, Vivacqua R, Rangel FO, Esporcatte R, Geng YJ, Vaughn WK, Assad JA, Mesquita ET, Willerson JT. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003;107(18):2294-2302.
75. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Silva GV, Mesquita CT, Belem L, Vaughn WK, Rangel FO, Assad JA, Carvalho AC, Branco RV, Rossi MI, Dohmann HJ, Willerson JT. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Circulation 2004;110(11 Suppl 1):II213-218.
76. Morigi M, Imberti B, Zoja C, Corna D, Tomasoni S, Abbate M, Rottoli D, Angioletti S, Benigni A, Perico N, Alison M, Remuzzi G. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004;15(7):1794-1804.
77. Qian H, Yang H, Xu W, Yan Y, Chen Q, Zhu W, Cao H, Yin Q, Zhou H, Mao F, Chen Y. Bone marrow mesenchymal stem cells ameliorate rat acute renal failure by differentiation into renal tubular epithelial-like cells. Int J Mol Med 2008;22(3):325-332.
78. Togel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005;289(1):F31-42.
79. Cho KA, Ju SY, Cho SJ, Jung YJ, Woo SY, Seoh JY, Han HS, Ryu KH. Mesenchymal stem cells showed the highest potential for the regeneration of injured liver tissue compared with other subpopulations of the bone marrow. Cell Biol Int 2009;33(7):772-777.
80. Christ B, Dollinger MM. The generation of hepatocytes from mesenchymal stem cells and engraftment into the liver. Curr Opin Organ Transplant 2011;16(1):69-75.
81. Lu HH, Teng GJ, Ju SH, Sun JH, Li AM, Zhang AF. [Committed differentiation of transplanted bone derived mesenchymal stem cells and their potential to amend damaged liver functions: In vivo experiment with mice]. Zhonghua Yi Xue Za Zhi 2007;87(4):223-227.
82. Mohsin S, Shams S, Ali Nasir G, Khan M, Javaid Awan S, Khan SN, Riazuddin S. Enhanced hepatic differentiation of mesenchymal stem cells after pretreatment with injured liver tissue. Differentiation 2011;81(1):42-48.
83. Han F, Wang CY, Yang L, Zhan SD, Zhang M, Tian K. Contribution of murine bone marrow mesenchymal stem cells to pancreas regeneration after partial pancreatectomy in mice. Cell Biol Int 2012;36(9):823-831.
84. Almeida-Porada G, Porada CD, Tran N, Zanjani ED. Cotransplantation of human stromal cell progenitors into preimmune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation. Blood 2000;95(11):3620-3627.
85. Blaber SP, Hill CJ, Webster RA, Say JM, Brown LJ, Wang SC, Vesey G, Herbert BR. Effect of labeling with iron oxide particles or nanodiamonds on the functionality of adipose-derived mesenchymal stem cells. PloS One 2013;8(1):e52997.
86. Guenoun J, Koning GA, Doeswijk G, Bosman L, Wielopolski PA, Krestin GP, Bernsen MR. Cationic Gd-DTPA liposomes for highly efficient labeling of mesenchymal stem cells and cell tracking with MRI. Cell Transplant 2012;21(1):191-205.
87. Yang XF, Xu YF, Zhang YB, Wang HM, Lu NW, Wu YX, Lu X, Cui JP, Shan H, Yan Y, Zhou JX. [Functional improvement of patients with progressive muscular dystrophy by bone marrow and umbilical cord blood mesenchymal stem cell transplantations]. Zhonghua Yi Xue Za Zhi 2009;89(36):2552-2556.
88. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: Paradoxes of passaging. Exp Hematol 2004;32(5):414-425.
89. Devine SM, Bartholomew AM, 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. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol 2001;29(2):244-255.
90. Liu Y, Yan X, Sun Z, Chen B, Han Q, Li J, Zhao RC. Flk-1+ adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx mice. Stem Cells Dev 2007;16(5):695-706.
91. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276(5309):71-74.
92. Rombouts WJ, Ploemacher RE. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003;17(1):160-170.
93. Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, Kobayashi N, Yarmush ML. Mesenchymal stem cells: Mechanisms of immunomodulation and homing. Cell Transplant 2010;19(6):667-679.
94. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5(1):54-63.
95. Grote K, Petri M, Liu C, Jehn P, Spalthoff S, Kokemuller H, Luchtefeld M, Tschernig T, Krettek C, Haasper C, Jagodzinski M. Toll-like receptor 2/6-dependent stimulation of mesenchymal stem cells promotes angiogenesis by paracrine factors. Eur Cells Mater 2013;26:66-79; discussion 79.
96. Hsiao ST, Asgari A, Lokmic Z, Sinclair R, Dusting GJ, Lim SY, Dilley RJ. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev 2012;21(12):2189-2203.
97. Park JH, Hwang I, Hwang SH, Han H, Ha H. Human umbilical cord blood-derived mesenchymal stem cells prevent diabetic renal injury through paracrine action. Diabetes Res Clin Pract 2012;98(3):465-473.
98. Ranganath SH, Levy O, Inamdar MS, Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012;10(3):244-258.
99. Severino V, Alessio N, Farina A, Sandomenico A, Cipollaro M, Peluso G, Galderisi U, Chambery A. Insulin-like growth factor binding proteins 4 and 7 released by senescent cells promote premature senescence in mesenchymal stem cells. Cell Death Dis 2013. doi:10.1042/CBI20120073.
100. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, Marshak DR, Flake AW. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 2000;6(11):1282-1286.
101. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008;8(9):726-736.
102. Bernardo ME, Fibbe WE. Mesenchymal stromal cells: Sensors and switchers of inflammation. Cell Stem Cell 2013;13(4):392-402.
103. Lazarus HM, Koc ON, Devine SM, Curtin P, Maziarz RT, Holland HK, Shpall EJ, McCarthy P, Atkinson K, Cooper BW, Gerson SL, Laughlin MJ, Loberiza FR, Jr., Moseley AB, Bacigalupo A. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol Blood Marrow Transplant 2005;11(5):389-398.
104. Baron F, Storb R. Mesenchymal stromal cells: A new tool against graft-versus-host disease? Biol Blood Marrow Transplant 2012;18(6):822-840.
105. Weng JY, Du X, Geng SX, Peng YW, Wang Z, Lu ZS, Wu SJ, Luo CW, Guo R, Ling W, Deng CX, Liao PJ, Xiang AP. Mesenchymal stem cell as salvage treatment for refractory chronic GVHD. Bone Marrow Transplant 2010;45(12):1732-1740.
106. Wernicke CM, Grunewald TG, Juenger H, Kuci S, Kuci Z, Koehl U, Mueller I, Doering M, Peters C, Lawitschka A, Kolb HJ, Bader P, Burdach S, von Luettichau I. Mesenchymal stromal cells for treatment of steroid-refractory GvHD: A review of the literature and two pediatric cases. Int Arch Med 2011;4(1):27.
107. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W, Ringden O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 2008;371(9624):1579-1586.
108. Wang D, Zhang H, Liang J, Li X, Feng X, Wang H, Hua B, Liu B, Lu L, Gilkeson GS, Silver RM, Chen W, Shi S, Sun L. Allogeneic mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus: 4 years experience. Cell Transplant 2012. doi:10.3727/096368912X658719.
109. Ciccocioppo R, Bernardo ME, Sgarella A, Maccario R, Avanzini MA, Ubezio C, Minelli A, Alvisi C, Vanoli A, Calliada F, Dionigi P, Perotti C, Locatelli F, Corazza GR. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011;60(6):788-798.
110. Herreros MD, Garcia-Arranz M, Guadalajara H, De-La-Quintana P, Garcia-Olmo D, Group FC. Autologous expanded adipose-derived stem cells for the treatment of complex cryptoglandular perianal fistulas: A phase III randomized clinical trial (FATT 1: fistula Advanced Therapy Trial 1) and long-term evaluation. Dis Colon Rectum 2012;55(7):762-772.
111. Bonab MM, Sahraian MA, Aghsaie A, Karvigh SA, Hosseinian SM, Nikbin B, Lotfi J, Khorramnia S, Motamed MR, Togha M, Harirchian MH, Moghadam NB, Alikhani K, Yadegari S, Jafarian S, Gheini MR. Autologous mesenchymal stem cell therapy in progressive multiple sclerosis: an open label study. Curr Stem Cell Res Ther 2012;7(6):407-414.
112. Hare JM, Fishman JE, Gerstenblith G, DiFede Velazquez DL, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, Breton E, Davis-Sproul J, Schulman IH, Byrnes J, Mendizabal AM, Lowery MH, Rouy D, Altman P, Wong Po Foo C, Ruiz P, Amador A, Da Silva J, McNiece IK, Heldman AW, George R, Lardo A. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: The POSEIDON randomized trial. J Am Med Assoc 2012;308(22):2369-2379.
113. Haniffa MA, Wang XN, Holtick U, Rae M, Isaacs JD, Dickinson AM, Hilkens CM, Collin MP. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol 2007;179(3):1595-1604.
114. Haniffa MA, Collin MP, Buckley CD, Dazzi F. Mesenchymal stem cells: The fibroblasts' new clothes? Haematologica 2009;94(2):258-263.
115. Lysy PA, Smets F, Sibille C, Najimi M, Sokal EM. Human skin fibroblasts: From mesodermal to hepatocyte-like differentiation. Hepatology 2007;46(5):1574-1585.
116. Cappellesso-Fleury S, Puissant-Lubrano B, Apoil PA, Titeux M, Winterton P, Casteilla L, Bourin P, Blancher A. Human fibroblasts share immunosuppressive properties with bone marrow mesenchymal stem cells. J Clin Immunol 2010;30(4):607-619.
117. Chhetri DK, Berke GS. Injection of cultured autologous fibroblasts for human vocal fold scars. Laryngoscope 2011;121(4):785-792.
118. Obaid H, Clarke A, Rosenfeld P, Leach C, Connell D. Skin-derived fibroblasts for the treatment of refractory Achilles tendinosis: Preliminary short-term results. J Bone Joint Surg Am 2012;94(3):193-200.
119. Price S. Experimental arthritis: Dermal fibroblasts have MSC-like immunosuppressive effects in vivo. Nat Rev Rheumatol 2011;7(8):437.
120. Galipeau J. The mesenchymal stromal cells dilemma-Does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 2013;15(1):2-8.
121. Cuthbert R, Boxall SA, Tan HB, Giannoudis PV, McGonagle D, Jones E. Single-platform quality control assay to quantify multipotential stromal cells in bone marrow aspirates prior to bulk manufacture or direct therapeutic use. Cytotherapy 2012;14(4):431-440.
122. Kuci Z, Seiberth J, Latifi-Pupovci H, Wehner S, Stein S, Grez M, Bonig H, Kohl U, Klingebiel T, Bader P, Kuci S. Clonal analysis of multipotent stromal cells derived from CD271+ bone marrow mononuclear cells: Functional heterogeneity and different mechanisms of allosuppression. Haematologica 2013;98(10):1609-1616.
123. Krampera M, Galipeau J, Shi Y, Tarte K, Sensebe L, Therapy MSCCotISfC. Immunological characterization of multipotent mesenchymal stromal cells-The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy 2013;15(9):1054-1061.
124. Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009;9(2):81-94.
125. Busletta C, Novo E, Valfre di Bonzo L, Povero D, Paternostro C, Ievolella M, Mareschi K, Ferrero I, Cannito S, Compagnone A, Bandino A, Colombatto S, Fagioli F, Parola M. Dissection of the biphasic nature of hypoxia-induced motogenic action in bone marrow-derived human mesenchymal stem cells. Stem Cells 2011;29(6):952-963.
126. Roemeling-van Rhijn M, Mensah FK, Korevaar SS, Leijs MJ, van Osch GJ, Ijzermans JN, Betjes MG, Baan CC, Weimar W, Hoogduijn MJ. Effects of hypoxia on the immunomodulatory properties of adipose tissue-derived mesenchymal stem cells. Front Immunol 2013;4:203.
127. Valorani MG, Montelatici E, Germani A, Biddle A, D'Alessandro D, Strollo R, Patrizi MP, Lazzari L, Nye E, Otto WR, Pozzilli P, Alison MR. Pre-culturing human adipose tissue mesenchymal stem cells under hypoxia increases their adipogenic and osteogenic differentiation potentials. Cell Prolif 2012;45(3):225-238.
128. Hemeda H, Giebel B, Wagner W. Evaluation of human platelet lysate versus fetal bovine serum for culture of mesenchymal stromal cells. Cytotherapy 2014;16(2):170-180.
129. Galderisi U, Giordano A, Paggi MG. The bad and the good of mesenchymal stem cells in cancer: Boosters of tumor growth and vehicles for targeted delivery of anticancer agents. World J Stem Cells 2010;2(1):5-12.
130. Pinho S, Lacombe J, Hanoun M, Mizoguchi T, Bruns I, Kunisaki Y, Frenette PS. PDGFRα and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med 2013;210(7):1351-1367.
131. Isern J, Martín-Antonio B, Ghazanfari R, Martín AM, López JA, del Toro R, Sánchez-Aguilera A, Arranz L, Martín-Pérez D, Suárez-Lledó M, Marín P, Van Pel M, Fibbe WE, Vázquez J, Scheding S, Urbano-Ispizúa Á, Méndez-Ferrer S. Self-renewing human bone marrow mesenspheres promote hematopoietic stem cell expansion. Cell Rep 2013;3(5):1714-1724.
132. Li H, Zacharaki D, Ghazanfari R, Ekblom M, Méndez-Ferrer S, Scheding S. Primary Linneg/CD45neg/CD271pos/PDGFRαlow/Neg stroma stem cells in adult human bone marrow show a distinct molecular signature and potent hematopoiesis-supporting function. Blood 2013;122(21):3699.
133. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 2005;105(10):3793-3801.
134. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006;25(6):977-988.
135. Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, Nagasawa T, Link DC. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013;495(7440):227-230.