Adult mesenchymal stem cells and cell-based tissue engineering

Arthritis Research and Therapy

Volumn 5, Issue 1, 2003, Pages 32-45

  Tuan, Rocky S ^a   Boland, Genevieve ^a   Tuli, Richard ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cell differentiation; Cell signaling; Mesenchymal stem cells; Stem cells; Tissue engineering

Indexed keywords

BONE MARROW; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL TYPE; CONNECTIVE TISSUE; DNA FINGERPRINTING; HEMATOPOIETIC STEM CELL; HUMAN; MEDICAL RESEARCH; MESENCHYME CELL; REVIEW; STEM CELL; STROMA; TISSUE ENGINEERING; TISSUE REGENERATION;

ADULT; BONE REGENERATION; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYO; HUMANS; MESODERM; MODELS, BIOLOGICAL; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE ENGINEERING;

EID: 0037963685     PISSN: 14786354     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (150)

1. Lin H: The tao of stem cells in the germline. Annu Rev Genet 1997, 31:455-491.
2. de Wynter EA, Emmerson AJ, Testa NG: Properties of peripheral blood and cord blood stem cells. Baillière's Best Pract Res Clin Haematol 1999, 12:1-17.
3. Dua HS, Azuara-Blanco A: Limbal stem cells of the corneal epithelium. Surv Ophthalmol 2000, 44:415-425.
4. Rao MS: Multipotent and restricted precursors in the central nervous system. Anat Rec 1999, 257:137-148.
5. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M: Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nature Med 2000, 6:1229-1234.
6. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP: Bone marrow as a potential source of hepatic oval cells. Science 1999, 284: 1168-1170.
7. Alison MR, Poulsom R, Jeffery R, Dhillon AP, Quaglia A, Jacob J, Novelli M, Prentice G, Williamson J, Wright NA: Hepatocytes from non-hepatic adult stem cells. Nature 2000, 406:257.
8. Jackson KA, Mi T, Goodell MA: Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci U S A 1999, 96:14482-14486.
9. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL: Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 1999, 283:534-537.
10. 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: 1528-1530.
11. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ: 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.
12. 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.
13. Ito T, Suzuki A, Okabe M, Imai E, Hori M: Application of bone marrow-derived stem cells in experimental nephrology. Exp Nephrol 2001, 9:444-450.
14. Fukuda K: Molecular characterization of regenerated cardiomyocytes derived from adult mesenchymal stem cells. Congenit Anom Kyoto 2002, 42:1-9.
15. 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 1999, 103:697-705.
16. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001, 7:211-228.
17. Nakahara H, Goldberg VM, Caplan AI: Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res 1991, 9:465-476.
18. De Bari C, Dell'Accio F, Luyten FP: Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum 2001, 44:85-95.
19. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP: Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001, 44:1928-1942.
20. Bosch P, Musgrave DS, Lee JY, Cummins J, Shuler T, Ghivizzani TC, Evans T, Robbins TD, Huard J: Osteoprogenitor cells within skeletal muscle. J Orthop Res 2000, 18:933-944.
21. 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: 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, 264:51-62.
22. Diefenderfer DL, Brighton CT: Microvascular pericytes express aggrecan message which is regulated by BMP-2. Biochem Biophys Res Commun 2000, 269:172-178.
23. Brighton CT, Lorich DG, Kupcha R, Reilly TM, Jones AR, Woodbury RA 2nd: The pericyte as a possible osteoblast progenitor cell. Clin Orthop 1992, 275:287-299.
24. Reilly TM, Seldes R, Luchetti W, Brighton CT: Similarities in the phenotypic expression of pericytes and bone cells. Clin Orthop 1998, 346:95-103.
25. Zvaifler NJ, Marinova-Mutafchieva L, Adams G, Edwards CJ, Moss J, Burger JA, Maini RN: Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res 2000, 2:477-488.
26. 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 1999, 284:143-147.
27. 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 2002, 20:1060-1069.
28. Osyczka AM, Noth U, Danielson KG, Tuan RS: Different osteochondral potential of clonal cell lines derived from adult human trabecular bone. Ann N Y Acad Sci 2002, 961:73-77.
29. Tuli R, Seghatoleslami MR, Tuli S, Wang ML, Hozack WJ, Manner PA, Danielson KG, Tuan RS: A simple, high-yield method for obtaining multipotential mesenchymal progenitor cells from trabecular bone. Mol Biotechnol 2002, in press.
30. Friedenstein AJ, Gorskaja JF, Kulagina NN: Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976, 4:267-274.
31. Dexter TM: Stromal cell associated haemopoiesis. J Cell Physiol 1982, 1(suppl):87-94.
32. Rickard DJ, Kassem M, Hefferan TE, Sarkar G, Spelsberg TC, Riggs BL: Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 1996, 11:312-324.
33. Friedenstein AJ, Chailakhyan RK, Gerasimov UV: Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987, 20:263-272.
34. Keating A, Horsfall W, Hawley RG, Toneguzzo F: Effect of different promoters on expression of genes introduced into hematopoietic and marrow stromal cells by electroporation. Exp Hematol 1990, 18:99-102.
35. Wakitani S, Saito T, Caplan AI: Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 1995, 18:1417-1426.
36. Kuznetsov SA, Friedenstein AJ, Robey PG: Factors required for bone marrow stromal fibroblast colony formation in vitro. Br J Haematol 1997, 97:561-570.
37. Digirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ: Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 1999, 107:275-281.
38. Hung SC, Chen NJ, Hsieh SL, Li H, Ma HL, Lo WH: Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 2002, 20:249-258.
39. Caterson EJ, Nesti LJ, Danielson KG, Tuan RS: Human marrow-derived mesenchymal progenitor cells: isolation, culture expansion, and analysis of differentiation. Mol Biotechnol 2002, 20:245-256.
40. Prockop DJ: Marrow stromal cells as stem cells for non-hematopoietic tissues. Science 1997, 276:71-74.
41. Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL: Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 1998, 176:57-66.
42. Majors AK, Boehm CA, Nitto H, Midura RJ, Muschler GF: Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J Orthop Res 1997, 15:546-557.
43. Bruder SP, Jaiswal N, Haynesworth SE: Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 1997, 64:278-294.
44. Simonsen JL, Rosada C, Serakinci N, Justesen J, Stenderup K, Rattan SI, Jensen TG, Kassem M: Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 2002, 20:592-596.
45. Shi S, Gronthos S, Chen S, Reddi A, Counter CM, Robey PG, Wang CY: Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nature Biotechnol 2002, 20:587-591.
46. Osyczka AM, Noth U, O'Connor J, Caterson EJ, Yoon K, Danielson KG, Tuan RS: Multilineage differentiation of adult human bone marrow progenitor cells transduced with human papilloma virus type 16 E6/E7 genes. Calcif Tissue Int 2002, in press.
47. Okamoto T, Aoyama T, Nakayama T, Nakamata T, Hosaka T, Nishijo K, Nakamura T, Kiyono T, Toguchida J: Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun 2002, 295:354-361.
48. Waller EK, Olweus J, Lund-Johansen F, Huang S, Nguyen M, Guo GR, Terstappen L: The "common stem cell" hypothesis reevaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. Blood 1995, 85:2422-2435.
49. Simmons PJ, Gronthos S, Zannettino A, Ohta S, Graves S: Isolation, characterization and functional activity of human marrow stromal progenitors in hemopoiesis. Prog Clin Biol Res 1994, 389:271-280.
50. Simmons PJ, Torok-Storb B: Identification of stromal cell precursors in human bone marrow by a novel monoclonal anti-body, STRO-1. Blood 1991, 78:55-62.
51. Dennis JE, Carbillet JP, Caplan AI, Charbord P: The STRO-1+ marrow cell population is multipotential. Cells Tissues Organs 2002, 170:73-82.
52. Bruder SP, Ricalton NS, Boynton RE, Connolly TJ, Jaiswal N, Zaia J, Barry FP: Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res 1998, 13:655-663.
53. 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.
54. Barry FP, Boynton RE, Haynesworth S, Murphy JM, Zaia J: The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem Biophys Res Commun 1999, 265:134-139.
55. Barry F, Boynton R, Murphy M, Haynesworth S, Zaia J: The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun 2001, 289:519-524.
56. Walsh S, Jefferiss C, Stewart K, Jordan GR, Screen J, Beresford JN: Expression of the developmental markers STRO-1 and alkaline phosphatase in cultures of human marrow stromal cells: regulation by fibroblast growth factor (FGF)-2 and relationship to the expression of FGF receptors 1-4. Bone 2000, 27:185-195.
57. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, Takagishi K, Kato Y: Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 2001, 288: 413-419.
58. Haynesworth SE, Baber MA, Caplan AI: Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1α. J Cell Physiol 1996, 166:585-592.
59. Bellows CG, Heersche JN, Aubin JE: Determination of the capacity for proliferation and differentiation of osteoprogenitor cells in the presence and absence of dexamethasone. Dev Biol 1990, 140:132-138.
60. Liu F, Aubin JE, Malaval L: Expression of leukemia inhibitory factor (LIF)/interleukin-6 family cytokines and receptors during in vitro osteogenesis: differential regulation by dexamethasone and LIF. Bone 2002, 31:212-219.
61. Chung CH, Golub EE, Forbes E, Tokuoka T, Shapiro IM: Mechanism of action of beta-glycerophosphate on bone cell mineralization. Calcif Tissue Int 1992, 51:305-311.
62. Tenenbaum HC, Limeback H, McCulloch CA, Mamujee H, Sukhu B, Torontali M: Osteogenic phase-specific co-regulation of collagen synthesis and mineralization by beta-glycerophosphate in chick periosteal cultures. Bone 1992, 13:129-138.
63. Beck GR, Zerler B, Moran E: Phosphate is a specific signal for induction of osteopontin gene expression. Proc Natl Acad Sci U S A 2000, 97:8352-8357.
64. Fujita T, Izumo N, Fukuyama R, Meguro T, Nakamuta H, Kohno T, Koida M: Phosphate provides an extracellular signal that drives nuclear export of Runx2/Cbfa1 in bone cells. Biochem Biophys Res Commun 2001, 280:348-352.
65. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G: Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
66. Liu P, Oyajobi BO, Russell RG, Scutt A: Regulation of osteogenic differentiation of human bone marrow stromal cells: interaction between transforming growth factor-beta and 1,25(OH)(2) vitamin D(3) in vitro. Calcif Tissue Int 1999, 65:173-180.
67. Hanada K, Dennis JE, Caplan AI: Stimulatory effects of basic fibroblast growth factor and bone morphogenetic protein-2 on osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells. J Bone Miner Res 1997, 12:1606-1614.
68. Little RD, Carulli JP, Del Mastro RG, Dupuis J, Osborne M, Folz C, Manning SP, Swain PM, Zhao SC, Eustace B, Lappe MM, Spitzer L, Zweier S, Braunschweiger K, Benchekroun Y, Hu X, Adair R, Chee L, FitzGerald MG, Tulig C, Caruso A, Tzellas N, Bawa A, Franklin B, McGuire S, Nogues X, Gong G, Allen KM, Anisowicz A, Morales AJ, Lomedico PT, Recker SM, Van Eerdewegh P, Recker RR, Johnson ML: A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am J Hum Genet 2002, 70:11-19.
69. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L: Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 2002, 157:303-314.
70. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH, Lev D, Zacharin M, Oexle K, Marcelino J, Suwairi W, Heeger S, Sabatakos G, Apte S, Adkins WN, Allgrove J, Arslan-Kirchner M, Batch JA, Beighton P, Black GC, Boles RG, Boon LM, Borrone C, Brunner HG, Carle GF, Dallapiccola B, De Paepe A, Floege B, Halfhide ML, Hall B, Hennekam RC, Hirose T, Jans A, Juppner H, Kim CA, Keppler-Noreuil K, Kohlschuetter A, LaCombe D, Lambert M, Lemyre E, Letteboer T, Peltonen L, Ramesar RS, Romanengo M, Somer H, Steichen-Gersdorf E, Steinmann B, Sullivan B, Superti-Furga A, Swoboda W, van den Boogaard MJ, Van Hul W, Vikkula M, Votruba M, Zabel B, Garcia T, Baron R, Olsen BR, Warman ML: LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001, 107:513-523.
71. Rose FR, Oreffo RO: Bone tissue engineering: hope vs hype. Biochem Biophys Res Commun 2002, 292:1-7.
72. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S: The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 1998, 80:985-996.
73. El-Amin SF, Attawia M, Lu HH, Shah AK, Chang R, Hickok NJ, Tuan RS, Laurencin CT: Integrin expression by human osteoblasts cultured on degradable polymeric materials applicable for tissue engineered bone. J Orthop Res 2002, 20: 20-28.
74. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L: Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994, 331:889-895,
75. O'Driscoll SW: The healing and regeneration of articular cartilage. J Bone Joint Surg Am 1998, 80:1795-1812.
76. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU: In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998, 238:265-272.
77. Cassiede P, Dennis JE, Ma F, Caplan AI: Osteochondrogenic potential of marrow mesenchymal progenitor cells exposed to TGF-β1 or PDGF-BB as assayed in vivo and in vitro. J Bone Miner Res 1996, 11:1264-1273.
78. Barry F, Boynton RE, Liu B, Murphy JM: Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res 2001, 268:189-200.
79. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF: Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 1998, 4: 415-428.
80. Sekiya I, Colter DC, Prockop DJ: BMP-6 enhances chondrogenesis in a subpopulation of human marrow stromal cells. Biochem Biophys Res Commun 2001, 284:411-418.
81. Majumdar MK, Wang E, Morris EA: BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J Cell Physiol 2001, 189:275-284.
82. Rudnicki JA, Brown AM: Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Dev Biol 1997, 185:104-118.
83. Tufan AC, Tuan RS: Writ regulation of limb mesenchymal chondrogenesis is accompanied by altered N-cadherin-related functions. FASEB J 2001, 15:1436-1438.
84. Fischer L, Boland G, Tuan RS: Wnt-3A enhances bone morphogenetic protein-2-mediated chondrogenesis of murine C3H10T1/2 mesenchymal cells. J Biol Chem 2002, 277: 30870-30878.
85. Hurvitz JR, Suwairi WM, Van Hul W, El-Shanti H, Superti-Furga A, Roudier J, Holderbaum D, Pauli RM, Herd JK, Van Hul EV, Rezai-Delui H, Legius E, Le Merrer M, Al-Alami J, Bahabri SA, Warman ML: Mutations in the CCN gene family member WISP3 cause progressive pseudorheumatoid dysplasia. Nature Genet 1999, 23:94-98.
86. Pennica D, Swanson TA, Welsh JW, Roy MA, Lawrence DA, Lee J, Brush J, Taneyhill LA, Deuel B, Lew M, Watanabe C, Cohen RL, Melhem MF, Finley GG, Quirke P, Goddard AD, Hillan KJ, Gurney AL, Botstein D, Levine AJ: WISP genes are members of the 43 connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci U S A 1998, 95: 14717-14722.
87. Grotendorst GR: Connective tissue growth factor: a mediator of TGF-beta action on fibroblasts. Cytokine Growth Factor Rev 1997, 8:171-179.
88. Lako M, Strachan T, Bullen P, Wilson DI, Robson SC, Lindsay S: Isolation, characterisation and embryonic expression of WNT11, a gene which maps to 11q13.5 and has possible roles in the development of skeleton, kidney and lung. Gene 1998, 219:101-110.
89. Sekiya I, Vuoristo JT, Larson BL, Prockop DJ: In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci U S A 2002, 99: 4397-4402.
90. Sen M, Lauterbach K, El-Gabalawy H, Firestein GS, Corr M, Carson DA: Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci U S A 2000, 97:2791-2796.
91. Sen M, Chamorro M, Reifert J, Corr M, Carson DA: Blockade of Wnt-5A/frizzled 5 signaling inhibits rheumatoid synoviocyte activation. Arthritis Rheum 2001, 44:772-781.
92. Nakamura K, Shirai T, Morishita S, Uchida S, Saeki-Miura K, Makishima F: p38 mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp Cell Res 1999, 250:351-363.
93. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K: Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 1995, 270:2008-2011.
94. Shibuya H, Yamaguchi K, Shirakabe K, Tonegawa A, Gotoh Y, Ueno N, Irie K, Nishida E, Matsumoto K: TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction. Science 1996, 272:1179-1182.
95. Shirakabe K, Yamaguchi K, Shibuya H, Irie K, Matsuda S, Moriguchi T, Gotoh Y, Matsumoto K, Nishida E: TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J Biol Chem 1997, 272:8141-8144.
96. Moriguchi T, Kuroyanagi N, Yamaguchi K, Gotoh Y, Irie K, Kano T, Shirakabe K, Muro Y, Shibuya H, Matsumoto K, Nishida E, Hagiwara M: A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J Biol Chem 1996, 271:13675-13679.
97. Mucsi I, Skorecki KL, Goldberg HJ: Extracellular signal-regulated kinase and the small GTP-binding protein, Rac, contribute to the effects of transforming growth factor-β1 on gene expression. J Biol Chem 1996, 271:16567-16572.
98. Hartsough MT, Mulder KM: Transforming growth factor-β signaling in epithelial cells. Pharmacol Ther 1997, 75:21-41.
99. Heldin CH, Miyazono K, ten Dijke P: TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
100. Massague J: TGF-β signal transduction. Annu Rev Biochem 1998, 67:753-791.
101. Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G: BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 1995, 9:2808-2820.
102. Kingsley DM, Bland AE, Grubber JM, Marker PC, Russell LB, Copeland NG, Jenkins NA: The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF beta superfamily. Cell 1992, 71:399-410.
103. Yang X, Chen L, Xu X, Li C, Huang C, Deng CX: TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 2001, 153:35-46.
104. Kretzschmar M, Doody J, Massague J: Opposing BMP and EGF signaling pathways converge on the TGF-beta family mediator Smad1. Nature 1997, 389:618-622.
105. de Caestecker MP, Parks WT, Frank CJ, Castagnino P, Bottaro DP, Roberts AB, Lechleider RJ: Smad2 transduces common signals from receptor serine-threonine and tyrosine kinases. Genes Dev 1998, 12:1587-1592.
106. Oberlender SA, Tuan RS: Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 1994, 120:177-187.
107. DeLise AM, Tuan RS: Alterations in the spatiotemporal expression pattern and function of N-cadherin inhibit cellular condensation and chondrogenesis of limb mesenchymal cells in vitro. J Cell Biochem 2002, 87:342-359.
108. DeLise AM, Tuan RS: Analysis of N-cadherin function in limb mesenchymal chondrogenesis in vitro. Develop Dyn 2002, 225:195-204.
109. Stott NS, Jiang TX, Chuong CM: Successive formative stages of precartilaginous mesenchymal condensations in vitro: modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 1999, 180:314-324.
110. Tuli R, Seghatoleslami MR, Tuli S, Howard MS, Danielson KG, Tuan RS: p38 MAP kinase regulation of AP-2 binding in TGF-beta1-stimulated chondrogenesis of human trabecular bone-derived cells. Ann N Y Acad Sci 2002, 961:172-177.
111. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, Goldberg VM: Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994, 76:579-592.
112. Adachi N, Sato K, Usas A, Fu FH, Ochi M, Han CW, Niyibizi C, Huard J: Muscle derived, cell based ex vivo gene therapy for treatment of full thickness articular cartilage defects. J Rheumatol 2002, 29:1920-1930.
113. Caplan AI, Elyaderani M, Mochizuki Y, Wakitani S, Goldberg VM: Principles of cartilage repair and regeneration. Clin Orthop 1997, 342:254-269.
114. Quintavalla J, Uziel-Fusi S, Yin J, Boehnlein E, Pastor G, Blancuzzi V, Singh HN, Kraus KH, O'Byrne E, Pellas TC: Fluorescently labeled mesenchymal stem cells (MSCs) maintain multilineage potential and can be detected following implantation into articular cartilage defects. Biomaterials 2002, 23:109-119.
115. Radice M, Brun P, Cortivo R, Scapinelli R, Battaliard C, Abatangelo G: Hyaluronan-based biopolymers as delivery vehicles for bone-marrow-derived mesenchymal progenitors. J Biomed Mater Res 2000, 50:101-109.
116. Caterson EJ, Nesti LJ, Li WJ, Danielson KG, Albert TJ, Vaccaro AR, Tuan RS: Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam. J Biomed Mater Res 2001, 57:394-403.
117. Noth U, Tuli R, Osyczka AM, Danielson KG, Tuan RS: In vitro engineered cartilage constructs produced by press-coating biodegradable polymer with human mesenchymal stem cells. Tissue Eng 2002, 8:131-144.
118. Li WJ, Laurencin CT, Caterson EJ, Tuan RS, Ko FK: Electrospun nanofibrous structure: A novel scaffold for tissue engineering. J Biomed Mater Res 2002, 60:613-621.
119. Wolfman NM, Hattersley G, Cox K, Celeste AJ, Nelson R, Yamaji N, Dube JL, DiBlasio-Smith E, Nove J, Song JJ, Wozney JM, Rosen V: Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest 1997, 100:321-330.
120. Helm GA, Li JZ, Alden TD, Hudson SB, Beres EJ, Cunningham M, Mikkelsen MM, Pittman DD, Kerns KM, Kallmes DF: A light and electron microscopic study of ectopic tendon and ligament formation induced by bone morphogenetic protein-13 adenoviral gene therapy. J Neurosurg 2001, 95:298-307.
121. Aspenberg P, Forslund C: Enhanced tendon healing with GDF 5 and 6. Acta Orthop Scand 1999, 70:51-54.
122. Young RG, Butler DL, Weber W, Caplan AI, Gordon SL, Fink DJ: Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 1998, 16:406-413.
123. Awad HA, Butler DL, Boivin GP, Smith FN, Malaviya P, Huibregtse B, Caplan AI: Autologous mesenchymal stem cell-mediated repair of tendon. Tissue Eng 1999, 5:267-277.
124. Awad HA, Butler DL, Harris MT, Ibrahim RE, Wu Y, Young RG, Kadiyala S, Boivin GP: In vitro characterization of mesenchymal stem cell-seeded collagen scaffolds for tendon repair: effects of initial seeding density on contraction kinetics. J Biomed Mater Res 2000, 51:233-240.
125. Hsieh AH, Tsai CM, Ma OJ, Lin T, Banes AJ, Villarreal FJ, Akeson WH, Sung KL: Time-dependent increases in type-III collagen gene expression in medical collateral ligament fibroblasts under cyclic strains. J Orthop Res 2000, 18:220-227.
126. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM, Kliewer SA: Peroxisome proliferator-activated receptors α and γ are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 1997, 272:3406-3410.
127. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA: Inhibition of adipogenesis by Wnt signaling. Science 2000, 289:950-953.
128. Park SR, Oreffo RO, Triffitt JT: Interconversion potential of cloned human marrow adipocytes in vitro. Bone 1999, 24:549-554.
129. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME: Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 1992, 102:341-351.
130. Goldring K, Partridge T, Watt D: Muscle stem cells. J Pathol 2002, 197:457-467.
131. Fukuda K: Development of regenerative cardiomyocytes from mesenchymal stem cells for cardiovascular tissue engineering. Artif Organs 2001, 25:187-193.
132. Shake JG, Gruber PJ, Baumgartner WA, Senechal G, Meyers J, Redmond JM, Pittenger MF, Martin BJ: Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg 2002, 73:1919-1926.
133. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P: Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 2002, 106:1913-1918.
134. Akins RE: Can tissue engineering mend broken hearts? Circ Res 2002, 90:120-122.
135. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
136. Nippert I: The pros and cons of human therapeutic cloning in the public debate. J Biotechnol 2002, 98:53-60.
137. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR: Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000, 290:1779-1782.
138. Wada MR, Inagawa-Ogashiwa M, Shimizu S, Yasumoto S, Hashimoto N: Generation of different fates from multipotent muscle stem cells. Development 2002, 129:2987-2995.
139. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM: Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
140. Rosu-Myles M, Khandaker M, Wu DM, Keeney M, Foley SR, Howson-Jan K, Yee IC, Fellows F, Kelvin D, Bhatia M: Characterization of chemokine receptors expressed in primitive blood cells during human hematopoietic ontogeny. Stem Cells 2000, 18:374-381.
141. Hackney JA, Charbord P, Brunk BP, Stoeckert CJ, Lemischka IR, Moore KA: A molecular profile of a hematopoietic stem cell niche. Proc Natl Acad Sci U S A 2002, 99:13061-13066.
142. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR: A stem cell molecular signature. Science 2002, 298:601-604.
143. Bianco P, Costantini M, Dearden LC, Bonucci E: Alkaline phosphatase positive precursors of adipocytes in the human bone marrow. Br J Haematol 1988, 68:401-403.
144. Theise ND, Badve S, Saxena R, Henegariu O, Sell S, Crawford JM, Krause DS: Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000, 31:235-240.
145. Owen M, Friedenstein AJ: Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 1988, 136:42-60.
146. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI: Characterization of cells with osteogenic potential from human marrow. Bone 1992, 13:81-88.
147. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP: Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997, 64:295-312.
148. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL: Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 2000, 9:841-848.
149. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, Huard J: Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 2002, 157:851-864.
150. Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM: Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001, 189:54-63.