Dissimilar differentiation of mesenchymal stem cells from bone marrow, umbilical cord blood, and adipose tissue

Experimental Biology and Medicine

Volumn 233, Issue 7, 2008, Pages 901-913

  Rebelatto, C K ^a   Aguiar, A M ^b,c   Moretao M P ^c   Senegaglia, A C ^a   Hansen, P ^a   Barchiki, F ^a   Oliveira, J ^a   Martins, J ^c   Kuligovski, C ^c   Mansur, F ^c   Christofis, A ^a   Amaral, V F ^a   Brofman, P S ^a   Goldenberg, S ^b,c   Nakao, L S ^a   Correa, A ^c  

^a PONTIFICAL CATHOLIC UNIVERSITY OF PARANÁ   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Instituto de Biologia Molecular do Parana   (Brazil)

Author keywords

Adipose tissue; Bone marrow; Differentiation; Mesenchymal stem cells; Umbilical cord blood

Indexed keywords

COLLAGEN TYPE 2; ALKALINE PHOSPHATASE; MEMBRANE ANTIGEN;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; AGED; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOCHEMISTRY; FLOW CYTOMETRY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MESENCHYMAL STEM CELL; OSTEOBLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL CORD BLOOD; BONE MARROW CELL; CELL CULTURE; CYTOLOGY; FEMALE; FETUS BLOOD; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PREGNANCY;

ADIPOCYTES; ADIPOSE TISSUE; ADULT; AGED; ALKALINE PHOSPHATASE; ANTIGENS, SURFACE; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE II; FEMALE; FETAL BLOOD; HUMANS; MESENCHYMAL STEM CELLS; MIDDLE AGED; OSTEOBLASTS; PREGNANCY;

EID: 47749084684     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0712-RM-356     Document Type: Article

References (82)

1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147, 1999.
2. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte culture and mitogenic response independently of the major histocompatibility complex. Scand J Immunol 57:11-20, 2003.
3. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pveritz RE, Brenner MK. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5: 309-313,1999.
4. Horwitz EM, Gordon PL, Koo WW, Marx JC, Neel M, Mcnall RY, Muul L, Hofmann T. Isolated allogenic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 99: 8932-8937, 2002.
5. Kawate K, Yajima H, Ohgushi H, Kotobuki N, Sigimoto K, Ohmura T, Kobata Y, Shigematsu K, Kawamura K, Tamai K, Takakura Y. Tissue-engineered approach for the treatment of steroid-induced osteonecrosis of the femoral head: transplantation of autologous mesenchymal stem cells cultured with beta-tricalcium phosphate ceramics and free vascularized fibula. Artif Organs 30: 960-962, 2006.
6. Ciapetti G, Ambrosio L, Marietta G, Baldini N, Giunti A. Human bone marrow stromal cells: in vitro expansion and differentiation for bone engineering. Biomaterials 27:6150-6160, 2006.
7. Koc ON, Gerson SL, Cooper BW, Dyhouse SM, Haynesworth SE, Caplan AL, Lazarus HM. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol 18:307-316, 2000.
8. Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 8:559-561, 2006.
9. Gimble JM, Guilak F. Differentiation potential of adipose derived adult stem cell (ADAS) cells. Curr Top Dev Biol 58:137-160, 2003.
10. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416, 2005.
11. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294-1301, 2006.
12. Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, Sano M, Takahashi T, Hori S, Abe H, Hata J, Umezawa A, Ogawa S. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103:697-705, 1999.
13. Toma C, Pittenger KS, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate of a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93-98, 2002.
14. Tomita Y, Makino S, Hakuno D, Hattan N, Kimura K, Miyoshi S, Murata M, Ieda M, Fukuda K. Application of mesenchymal stem cell-derived cardiomyocytes as bio-pacemakers: current status and problems to be solved. Med Biol Eng Comput 45:209-220, 2007.
15. Lee OK, Kuo TK, Chen W-M, Lee K-D, Hsieh S-L, Chen T-H. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103:1669-1675, 2004.
16. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger DR. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275: 9645-9652, 2000.
17. 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 3:393-403, 1970.
18. Zvaifler NJ, Marinova-Matafchieva L, Adams G, Edwards CJ, Moss J, Burger JA, Maini RN. Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res 2:477-488, 2000.
19. Rogers I, Casper RF. Umbilical cord blood stem cells. Best Pract Res Clin Obstet Gynaecol 18:893-908, 2004.
20. Noth U, Osyczka AM, Tuli R, Hickok NJ, Danielson KG, Tuan RS. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res 20:1060-1069, 2002.
21. De Bari C, Delláccio F, Luyten FP. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum 44:85-95, 2001.
22. Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784, 2001.
23. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896-904, 2002.
24. Bieback K, Kern S, Klüter H, Eichler H. Clinical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22:625-634, 2004.
25. Chang Y-J, Shih D, Tseng C-P, Hsieh T-B, Lee D-C, Hwang S-M. Disparate mesenchyme-lineage tendencies in mesenchymal stem cells from human bone marrow and umbilical cord blood. Stem Cells 24: 679-685, 2006.
26. Mueller SM, Glowacki J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 82:583-590, 2001.
27. Kögler G, Sensken S, Airey JA, Trapp T, Müschen M, Feldhahn N, Liedtke S, Sorg RY, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao O, Caplan AI, Colletti EJ, Almeida-Porada G, Müller HW, Zanjani E, Wernet P. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200:123-135, 2004.
28. Gutiérrez-Rodríguez M, Reyes-Maldonado E, Mayani H. Characterization of the adherent cells developed in Dexter-type long-term cultures from human umbilical cord blood. Stem Cells 18:46-52, 2000.
29. Mareschi K, Biasin E, Piacibello W, Aglietta M, Madon E, Fagioli F. Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica 86:1099-1100, 2001.
30. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM. Adult bone marrow is a rich source of human mesenchymal stem cells but umbilical cord and mobilized adult blood are not. Br J Haematol 121:368-374, 2003.
31. Campagnoli C, Roberts LAG, Kumar S, Bennett PR, Bellantuono I, Fisk N. Identification of mesenchymal stem/progenitor cells in human first trimester fetal blood, liver and bone marrow. Blood 98:2396-2402, 2001.
32. Goodwin H, Bicknese A, Chien S, Bogucki BD, Quinn CO, Wall DA. Multilineage differentiation activity by cells isolated from umbilical cord blood: expression of bone, fat and neural markers. Biol Blood Marrow Transplant 7:581-588, 2001.
33. Lee MW, Choi J, Yang MS, Moon YJ, Park JS, Kim HC, Kim YJ. Mesenchymal stem cells from cryopreserved human umbilical cord blood. Biochem Biophys Res Commun 320:273-278, 2004.
34. Wang TT, Tio M, Lee W, Beerheide W, Udolph G. Neural differentiation of mesenchymal-like stem cells from cord blood is mediated by PKA. Biochem Biophys Res Commun 357:1021-1027, 2007.
35. Markov V, Kusumi K, Tadesse MG, William DA, Hall DM, Lounev V, Carlton A, Leonard J, Cohen RI, Rappaport EF, Saitta B. Identification of cord blood-derived mesenchymal stem/stromal cell populations with distinct growth kinetics, differentiation potentials, and gene expression profiles. Stem Cell Dev 16:53-73, 2007.
36. 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 13:4279-4295, 2002.
37. Zuk PA, Zhu M, Mizuno H, Huang JI, Futrell WJ, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-226, 2001.
38. Halvorsen YD, Franklin D, Bond AL, Hitt DC, Auchter C, Boskey AL, Paschalis EP, Wilkison WO, Gimble JM. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7:729-741, 2001.
39. Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg 109:199-209, 2002.
40. Safford KM, Hicok KC, Safford SD, Halvorsen Y-DC, Wilkinson WO, Gimble JM, Rice HE. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun 294: 371-379, 2002.
41. Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnel BA. Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99:1285-1297, 2006.
42. Nardi NB, Meirelles LS. Mesenchymal stem cells: Isolation, in vitro expansion and characterization. In: Handbook of Experimental Pharmacology. New York: Springer, pp249-282, 2005.
43. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 21(Suppl):77-89, 1968.
44. Strutt B, Khalil W, Killinger D. Growth and differentiation of human adipose stromal cells in culture. In: Methods in Molecular Medicine: Human Cell Culture Protocols. New Jersey: Humana Press, pp41-51, 1996.
45. Owens MA, Vall HG, Hurley AA, Wormsley SB. Validation and quality control of immunophenotyping in clinical flow cytometry. J Immunol Methods 243:33-50, 2000.
46. Meirelles LS, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204-2213, 2006.
47. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitors cells. Exp Cell Res 238:268-272, 1998.
48. Nardelli SC, Avila AR, Freund A, Motta MC, Manhães L, Jesus TC, Schenkman S, Fragoso SP, Krieger MA, Goldenberg S, Dallagiovanna B. Small-subunit rRNA processome proteins are translationally regulated during differentiation of Trypanosoma cruzi. Eukaryotic Cell 6:337-345, 2007.
49. Gabbay JS, Heller JB, Mitchell SA, Zuk PA, Spoon DB, Wasson KL, Jarrahy R, Benhaim P, Bradley JP. Osteogenic potentiation of human adipose-derived stem cells in a 3-dimensional matrix. Ann Plast Surg 57: 89-93, 2006.
50. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109:235-242, 2000.
51. Musina RA, Beckchanova ES, Sukhikh GT. Comparison of mesen-chymal stem cells obtained from different human tissues. Cell Technol Biol Med 1:504-509, 2005.
52. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop DJ, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cyto-therapy 8:315-317, 2006.
53. Simmons PJ, Torok-Storb B. CD34 expression by stromal precursors in normal human adult bone marrow. Blood 78:2848-2853, 1991.
54. Dicker A, Le Blanc K, Aström G, van Harmelen V, Gotherström C, Lomqvist L, Arner P, Ryden M. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 308: 283-290, 2005.
55. Boquest AC, Shahdadfar A, Fronsdal K, Sigurjonsson O, Tunheim SH, Collas P, Brichmann JE. Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell 16:1131-1141, 2005.
56. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, Taureau C, Cousin B, Abbal M, Laharrague P, Penicaud L, Casteilla L, Blancher A. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129:118-129, 2005.
57. Katz AJ, Tholpady A, Tholpady SS, Shang H, Ogle RC. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23:412-423, 2005.
58. Yañez R, Laman ML, García-Castro J, Colmenero I, Ramírez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host-disease. Stem Cells 24:2582-2591, 2006.
59. Nishiyama N, Miyoshi S, Hida N, Uyama T, Okamoto K, Ikegami Y, Miyado K, Segawa K, Terai M, Sakamoto M, Ogawa S, Umezawa A. The significant cardiomyogenic potential of human umbilical cord blood-derived mesenchymal stem cells in vitro. Stem Cells 25:2017-2024, 2007.
60. Prat-Vidal C, Roura S, Farré J,Gaílvez C, Llach A, Molina CE, Hove-Madsen L, Garcia J, Cinca J, Bayes-Genis A. Umbilical cord blood-derived stem cells spontaneously express cardiomyogenic traits. Transplant Proc 39:2434-2437, 2007.
61. Varma MJ, Breuls RG, Schouten TE, Jurgens WJ, Bontkes HJ, Schuurhuis GL, van Ham SM, van Milligen FJ. Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 16:91-104, 2007.
62. Colter DC, Class R, Digirolamo CM, Prockop DJ. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci U S A 97:3213-3218, 2000.
63. Aye MT, Hashemi S, Leclair B, Zeibdawi A, Trudel E, Halpenny M, Fuller V, Cheng G. Expression of stem cell factor and c-kit mRNA in cultured endothelial cells, monocytes and cloned human bone marrow stromal cells (CFU-RF). Exp Hematol 20:523-527, 1992.
64. Shahdadfar A, Fronsdal K, Haung T, Reinholt FP, Brinchmann JE. 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, 2005.
65. Sudo K, Kanno M, Miharada K, Ogawa S, Hiroyama T, Saijo K, Nakamura Y. Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adpipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 25: 1610-1617, 2007.
66. Karahuseyinoglu S, Cinar O, Kilic E, Kara F, Akay GG, Demiralp DO, Tukun A, Uckan D, Can A. Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cells 25: 319-331, 2007.
67. Silva WA Jr, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL, Santos AR, Zago MA. The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 21:661-669, 2003.
68. Panepucci RA, Siufi JL, Silva WA, Proto-Siquiera R, Neder L, Orellana M, Rocha V, Covas DT, Zago MA. Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells. Stem Cells 22:1263-1278, 2004.
69. Stein GS, Lian JB. Molecular mechanisms mediating proliferation/ differentiation interrelationships during progressive development of the osteoblast phenotype. Endocrinol Rev 14:424-442, 1993.
70. Plant A, Tobias JH. Characterization of the temporal sequence of osteoblast gene expression during estrogen-induced osteogenesis in female mice. J Cell Biochem 82:683-691, 1991.
71. Harris SE, Guo D, Harris MA, Krishnaswamy A, Lichtler A. Transcriptional regulation of BMP-2 activated genes in osteoblasts using gene expression microarray analysis: role of Dlx2 and Dlx5 transcription factors. Front Biosci 8: S1249-S1265, 2003.
72. Korchynskyi O, Dechering KJ, Sijbers AM, Olijve W, Ten Dijke P. Gene array analysis of bone morphogenetic protein type I receptor-induced osteoblast differentiation. J Bone Miner Res 18:1177-1185, 2003.
73. Peng Y, Kang Q, Cheng H, Li X, Sun MH, Jiang W, Luu HH, Park JY, Haydon RC, He TC. Transcriptional characterization of bone morphogenetic proteins (BMPs)-mediated osteogenic signaling. J Cell Biochem 90:1149-1165, 2003.
74. Roman-Roman S, Garcia T, Jackson A, Theilhaber J, Rawadi G, Connolly T, Spinella-Jaegle S, Kawai S, Courtois B, Bushnell S, Auberval M, Call K, Baron R. Identification of genes regulated during osteoblastic differentiation by genome-wide expression analysis of mouse calvaria primary osteoblasts in vitro. Bone 32:474-482, 2003.
75. Tokalov SV, Grüner S, Schindler S, Wolf G, Baumann M, Abolmaali N. Age-related changes in the frequency of mesenchymal stem cells in the bone marrow of rats. Stem Cells Dev 16:439-446, 2007.
76. Siddappa R, Licht R, van Blitterswijk C, Boer J. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 25:1029-1041, 2007.
77. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AB, Deans R, Marshak DR, Flake AW. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6:1282-1286, 2000.
78. Lee JA, Parrett BM, Conejero JA, Laser J, Chen J, Kogon AJ, Nanda D, Grant RT, Breitbart AS. Biological alchemy: engineering bone and fat from fat-derived stem cells. Ann Plast Surg 50:610-617, 2003.
79. Chen J, Wang C, Lü S, Wu J, Guo X, Duan C, Dong L, Song Y, Zhang J, Jing D, Wu L, Ding J, Li D. In vivo chondrogenesis of adult bone-marrow-derived autologous mesenchymal stem cells. Cell Tissue Res 319:429-438, 2005.
80. Aslan H, Zilberman Y, Kandel L, Liebergall M, Oskouian RJ, Gazit D, Gazit Z. Osteogenic differentiation of noncultured immunoisolated bone marrow-derived CD105+ cells. Stem Cells 24:1728-1737, 2006.
81. Jackson L, Jones DR, Scotting O, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med 53:121-127, 2007.
82. Phinney DG, Proclop DJ. Concise review: mesenchymal stem/multi-potent stromal cells: the state of transdiferrentiation and modes of tissue repair current views. Stem Cells 25:2896-2902, 2007.