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Originally published as MBC in Press, 10.1091/mbc.E02-02-0105 on September 24, 2002
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Vol. 13, Issue 12, 4279-4295, December 2002

Human Adipose Tissue Is a Source of Multipotent Stem Cells

Patricia A. Zuk,*dagger Min Zhu,* Peter Ashjian,* Daniel A. De Ugarte,* Jerry I. Huang,* Hiroshi Mizuno,* Zeni C. Alfonso,Dagger John K. Fraser,Dagger Prosper Benhaim,* and Marc H. Hedrick*

 *Departments of Surgery and Orthopedics, Regenerative Bioengineering and Repair Laboratory, UCLA School of Medicine, Los Angeles, California 90095; and  Dagger Department of Medicine and the Jonsson Comprehensive Cancer Center, Division of Hematology and Oncology, UCLA School of Medicine, Los Angeles, California 90095

Much of the work conducted on adult stem cells has focused on mesenchymal stem cells (MSCs) found within the bone marrow stroma. Adipose tissue, like bone marrow, is derived from the embryonic mesenchyme and contains a stroma that is easily isolated. Preliminary studies have recently identified a putative stem cell population within the adipose stromal compartment. This cell population, termed processed lipoaspirate (PLA) cells, can be isolated from human lipoaspirates and, like MSCs, differentiate toward the osteogenic, adipogenic, myogenic, and chondrogenic lineages. To confirm whether adipose tissue contains stem cells, the PLA population and multiple clonal isolates were analyzed using several molecular and biochemical approaches. PLA cells expressed multiple CD marker antigens similar to those observed on MSCs. Mesodermal lineage induction of PLA cells and clones resulted in the expression of multiple lineage-specific genes and proteins. Furthermore, biochemical analysis also confirmed lineage-specific activity. In addition to mesodermal capacity, PLA cells and clones differentiated into putative neurogenic cells, exhibiting a neuronal-like morphology and expressing several proteins consistent with the neuronal phenotype. Finally, PLA cells exhibited unique characteristics distinct from those seen in MSCs, including differences in CD marker profile and gene expression.


Online version of this article contains supplemental figures and tables. Online version is available at www.molbiolcell.org.

dagger Corresponding author. E-mail address: zukpat{at}yahoo.com.


Molecular Biology of the Cell
Vol. 13, 4279-4295, December 2002
Copyright © 2002 by The American Society for Cell Biology



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Stem CellsHome page
T. M. Liu, M. Martina, D. W. Hutmacher, J. H. P. Hui, E. H. Lee, and B. Lim
Identification of Common Pathways Mediating Differentiation of Bone Marrow- and Adipose Tissue-Derived Human Mesenchymal Stem Cells into Three Mesenchymal Lineages
Stem Cells, March 1, 2007; 25(3): 750 - 760.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
H. Koga, T. Muneta, Y.-J. Ju, T. Nagase, A. Nimura, T. Mochizuki, S. Ichinose, K. von der Mark, and I. Sekiya
Synovial Stem Cells Are Regionally Specified According to Local Microenvironments After Implantation for Cartilage Regeneration
Stem Cells, March 1, 2007; 25(3): 689 - 696.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
L.-E. Zaragosi, N. Billon, G. Ailhaud, and C. Dani
Nucleofection Is a Valuable Transfection Method for Transient and Stable Transgene Expression in Adipose Tissue-Derived Stem Cells
Stem Cells, March 1, 2007; 25(3): 790 - 797.
[Abstract] [Full Text] [PDF]


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Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
J. Halaschek-Wiener and A. Brooks-Wilson
Progeria of Stem Cells: Stem Cell Exhaustion in Hutchinson-Gilford Progeria Syndrome
J. Gerontol. A Biol. Sci. Med. Sci., January 1, 2007; 62(1): 3 - 8.
[Abstract] [Full Text] [PDF]


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Hum Reprod UpdateHome page
C.E. Gargett
Uterine stem cells: What is the evidence?
Hum. Reprod. Update, January 1, 2007; 13(1): 87 - 101.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
Q. He, C. Wan, and G. Li
Concise Review: Multipotent Mesenchymal Stromal Cells in Blood
Stem Cells, January 1, 2007; 25(1): 69 - 77.
[Abstract] [Full Text] [PDF]


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Endocr. Rev.Home page
M. E. Trujillo and P. E. Scherer
Adipose Tissue-Derived Factors: Impact on Health and Disease
Endocr. Rev., December 1, 2006; 27(7): 762 - 778.
[Abstract] [Full Text] [PDF]


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Physiol. GenomicsHome page
C. Rink, S. Roy, S. Khanna, T. Rink, D. Bagchi, and C. K. Sen
Transcriptome of the subcutaneous adipose tissue in response to oral supplementation of type 2 Leprdb obese diabetic mice with niacin-bound chromium
Physiol Genomics, November 21, 2006; 27(3): 370 - 379.
[Abstract] [Full Text] [PDF]


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Eur. J. Cardiothorac. Surg.Home page
K. H. Wu, Y. L. Liu, B. Zhou, and Z. C. Han
Cellular therapy and myocardial tissue engineering: the role of adult stem and progenitor cells
Eur. J. Cardiothorac. Surg., November 1, 2006; 30(5): 770 - 781.
[Abstract] [Full Text] [PDF]


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JDRHome page
J.J. Mao, W.V. Giannobile, J.A. Helms, S.J. Hollister, P.H. Krebsbach, M.T. Longaker, and S. Shi
Craniofacial Tissue Engineering by Stem Cells
Journal of Dental Research, November 1, 2006; 85(11): 966 - 979.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
L.-E. Zaragosi, G. Ailhaud, and C. Dani
Autocrine Fibroblast Growth Factor 2 Signaling Is Critical for Self-Renewal of Human Multipotent Adipose-Derived Stem Cells
Stem Cells, November 1, 2006; 24(11): 2412 - 2419.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
R. Yanez, M. L. Lamana, J. Garcia-Castro, I. Colmenero, M. Ramirez, and J. A. Bueren
Adipose Tissue-Derived Mesenchymal Stem Cells Have In Vivo Immunosuppressive Properties Applicable for the Control of the Graft-Versus-Host Disease
Stem Cells, November 1, 2006; 24(11): 2582 - 2591.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
G. S. Tjabringa, P. S. Vezeridis, B. Zandieh-Doulabi, M. N. Helder, P. I.J.M. Wuisman, and J. Klein-Nulend
Polyamines Modulate Nitric Oxide Production and Cox-2 Gene Expression in Response to Mechanical Loading in Human Adipose Tissue-Derived Mesenchymal Stem Cells
Stem Cells, October 1, 2006; 24(10): 2262 - 2269.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
D. C. Wan, Y.-Y. Shi, R. P. Nacamuli, N. Quarto, K. M. Lyons, and M. T. Longaker
Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling
PNAS, August 15, 2006; 103(33): 12335 - 12340.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
L. V. Rodriguez, Z. Alfonso, R. Zhang, J. Leung, B. Wu, and L. J. Ignarro
Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells
PNAS, August 8, 2006; 103(32): 12167 - 12172.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
X. Wang, F. Li, and C. Niyibizi
Progenitors Systemically Transplanted into Neonatal Mice Localize to Areas of Active Bone Formation In Vivo: Implications of Cell Therapy for Skeletal Diseases
Stem Cells, August 1, 2006; 24(8): 1869 - 1878.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
J. Chan, K. O'Donoghue, M. Gavina, Y. Torrente, N. Kennea, H. Mehmet, H. Stewart, D. J. Watt, J. E. Morgan, and N. M. Fisk
Galectin-1 Induces Skeletal Muscle Differentiation in Human Fetal Mesenchymal Stem Cells and Increases Muscle Regeneration
Stem Cells, August 1, 2006; 24(8): 1879 - 1891.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
C.-C. Chien, B. L. Yen, F.-K. Lee, T.-H. Lai, Y.-C. Chen, S.-H. Chan, and H.-I Huang
In Vitro Differentiation of Human Placenta-Derived Multipotent Cells into Hepatocyte-Like Cells
Stem Cells, July 1, 2006; 24(7): 1759 - 1768.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
R. Sarig, Z. Baruchi, O. Fuchs, U. Nudel, and D. Yaffe
Regeneration and Transdifferentiation Potential of Muscle-Derived Stem Cells Propagated as Myospheres
Stem Cells, July 1, 2006; 24(7): 1769 - 1778.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
H. Aslan, Y. Zilberman, L. Kandel, M. Liebergall, R. J. Oskouian, D. Gazit, and Z. Gazit
Osteogenic Differentiation of Noncultured Immunoisolated Bone Marrow-Derived CD105+ Cells
Stem Cells, July 1, 2006; 24(7): 1728 - 1737.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
S. Kern, H. Eichler, J. Stoeve, H. Kluter, and K. Bieback
Comparative Analysis of Mesenchymal Stem Cells from Bone Marrow, Umbilical Cord Blood, or Adipose Tissue
Stem Cells, May 1, 2006; 24(5): 1294 - 1301.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
K. McIntosh, S. Zvonic, S. Garrett, J. B. Mitchell, Z. E. Floyd, L. Hammill, A. Kloster, Y. Di Halvorsen, J. P. Ting, R. W. Storms, et al.
The Immunogenicity of Human Adipose-Derived Cells: Temporal Changes In Vitro
Stem Cells, May 1, 2006; 24(5): 1246 - 1253.
[Abstract] [Full Text] [PDF]


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J Bone Joint Surg BrHome page
I. Pountos, E. Jones, C. Tzioupis, D. McGonagle, and P. V. Giannoudis
Growing bone and cartilage: THE ROLE OF MESENCHYMAL STEM CELLS
J Bone Joint Surg Br, April 1, 2006; 88-B(4): 421 - 426.
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Am. J. Physiol. Cell Physiol.Home page
P. Malladi, Y. Xu, M. Chiou, A. J. Giaccia, and M. T. Longaker
Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells
Am J Physiol Cell Physiol, April 1, 2006; 290(4): C1139 - C1146.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
J. B. Mitchell, K. McIntosh, S. Zvonic, S. Garrett, Z. E. Floyd, A. Kloster, Y. Di Halvorsen, R. W. Storms, B. Goh, G. Kilroy, et al.
Immunophenotype of Human Adipose-Derived Cells: Temporal Changes in Stromal-Associated and Stem Cell-Associated Markers
Stem Cells, February 1, 2006; 24(2): 376 - 385.
[Abstract] [Full Text] [PDF]


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J Bone Joint Surg BrHome page
S. Y. Lee, M. Miwa, Y. Sakai, R. Kuroda, T. Niikura, and M. Kurosaka
Osteogenic potential of cells in vitro derived from haemarthrosis of the knee induced by injury to the anterior cruciate ligament
J Bone Joint Surg Br, January 1, 2006; 88-B(1): 129 - 133.
[Abstract] [Full Text] [PDF]


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Eur. J. Cardiothorac. Surg.Home page
I. Dimarakis, N. A. Habib, and M. Y.A. Gordon
Adult bone marrow-derived stem cells and the injured heart: just the beginning?
Eur. J. Cardiothorac. Surg., November 1, 2005; 28(5): 665 - 676.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
V. Kindler
Postnatal stem cell survival: does the niche, a rare harbor where to resist the ebb tide of differentiation, also provide lineage-specific instructions?
J. Leukoc. Biol., October 1, 2005; 78(4): 836 - 844.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
D. T.-b. Shih, D.-C. Lee, S.-C. Chen, R.-Y. Tsai, C.-T. Huang, C.-C. Tsai, E.-Y. Shen, and W.-T. Chiu
Isolation and Characterization of Neurogenic Mesenchymal Stem Cells in Human Scalp Tissue
Stem Cells, August 1, 2005; 23(7): 1012 - 1020.
[Abstract] [Full Text] [PDF]


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Mol. Cell. ProteomicsHome page
J. P. DeLany, Z. E. Floyd, S. Zvonic, A. Smith, A. Gravois, E. Reiners, X. Wu, G. Kilroy, M. Lefevre, and J. M. Gimble
Proteomic Analysis of Primary Cultures of Human Adipose-derived Stem Cells: Modulation by Adipogenesis
Mol. Cell. Proteomics, June 1, 2005; 4(6): 731 - 740.
[Abstract] [Full Text] [PDF]


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JEMHome page
A.-M. Rodriguez, D. Pisani, C. A. Dechesne, C. Turc-Carel, J.-Y. Kurzenne, B. Wdziekonski, A. Villageois, C. Bagnis, J.-P. Breittmayer, H. Groux, et al.
Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse
J. Exp. Med., May 2, 2005; 201(9): 1397 - 1405.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
A. J. Katz, A. Tholpady, S. S. Tholpady, H. Shang, and R. C. Ogle
Cell Surface and Transcriptional Characterization of Human Adipose-Derived Adherent Stromal (hADAS) Cells
Stem Cells, March 1, 2005; 23(3): 412 - 423.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
A. C. Boquest, A. Shahdadfar, K. Fronsdal, O. Sigurjonsson, S. H. Tunheim, P. Collas, and J. E. Brinchmann
Isolation and Transcription Profiling of Purified Uncultured Human Stromal Stem Cells: Alteration of Gene Expression after In Vitro Cell Culture
Mol. Biol. Cell, March 1, 2005; 16(3): 1131 - 1141.
[Abstract] [Full Text] [PDF]




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