Hello. Sign in to personalize your visit. New user? Register now.  
Cell Scale Biomaterial Testing
Tissue Engineering
Human Adipose-Derived Adult Stem Cells Produce Osteoid in Vivo

To cite this article:
Kevin C. Hicok, Tracey V. du Laney, Yang Sheng Zhou, Yuan-Di C. Halvorsen, Daron C. Hitt, Lyndon F. Cooper, Jeffrey M. Gimble. Tissue Engineering. March 2004, 10(3-4): 371-380. doi:10.1089/107632704323061735.

Full Text: • PDF for printing (1,456.4 KB) • PDF w/ links (811.8 KB)


Kevin C. Hicok
Artecel Sciences, Durham, North Carolina
Tracey V. du Laney
Artecel Sciences, Durham, North Carolina
Yang Sheng Zhou
Department of Prosthodontics, School of Stomatology, Peking University, Beijing, China
Yuan-Di C. Halvorsen
Sciences, Durham, North Carolina
Daron C. Hitt
Department of Plastic Surgery, UTHSC, San Antonio, Texas
Lyndon F. Cooper
Department of Prosthodontics, University of North Carolina
Jeffrey M. Gimble
Artecel Sciences, Durham, North Carolina

Adult subcutaneous fat tissue is an abundant source of multipotent cells. Previous studies from our laboratory have shown that, in vitro, adipose-derived adult stem (ADAS) cells express bone marker proteins including alkaline phosphatase, type I collagen, osteopontin, and osteocalcin and produce a mineralized matrix as shown by alizarin red staining. In the current study, the ADAS cell ability to form osteoid in vivo was determined. ADAS cells were isolated from liposuction waste of three individual donors and expanded in vitro before implantation. Equal numbers of cells (3 × 106) were loaded onto either hydroxyapatite/tricalcium phosphate (HA-TCP) cubes or the collagen/HA-TCP composite matrix, Collagraft, and then implanted subcutaneously into SCID mice. After 6 weeks, implants were removed, fixed, and demineralized and sectioned for hematoxylin and eosin staining. Osteoid formation was observed in 80% of HA-TCP implants loaded with ADAS cells. Only 20% of Collagraft implants were positive for the presence of osteoid matrix. Whereas 100% of HA-TCP implants loaded with hFOB 1.19 cells formed osteoid, Collagraft loaded with hFOB 1.19 cells displayed a high degree of adipose tissue within the matrix. Immunostaining of serial sections for human nuclear antigen demonstrated that the osteoid contained human cells. Osteoid formation was not observed in control HA-TCP or Collagraft matrices implanted without cells. In summary, the data demonstrate the ability of ADAS cells to form osteoid matrix in vivo. Because of their abundance and accessibility, ADAS cells may prove to be a novel cell therapeutic for bone repair and regeneration.

Free first page

This paper was cited by:

Tissue Harvest by Means of Suction-Assisted or Third-Generation Ultrasound-Assisted Lipoaspiration Has No Effect on Osteogenic Potential of Human Adipose-Derived Stromal Cells
Nicholas J. Panetta, Deepak M. Gupta, Matthew D. Kwan, Derrick C. Wan, George W. Commons, Michael T. Longaker
Plastic and Reconstructive Surgery. Aug 2009, Vol. 124, No. 1: 65-73
CrossRef
Electrospun composite poly(L-lactic acid)/tricalcium phosphate scaffolds induce proliferation and osteogenic differentiation of human adipose-derived stem cells
S D McCullen, Y Zhu, S H Bernacki, R J Narayan, B Pourdeyhimi, R E Gorga, E G Loboa
Biomedical Materials. Jul 2009, Vol. 4, No. 3: 035002
CrossRef
The effect of age on osteogenic, adipogenic and proliferative potential of female adipose-derived stem cells
Min Zhu, Emil Kohan, James Bradley, Marc Hedrick, Prosper Benhaim, Patricia Zuk
Journal of Tissue Engineering and Regenerative Medicine. Jul 2009, Vol. 3, No. 4: 290-301
CrossRef
Adipose Tissue-Derived Stem Cells and Their Application in Bone and Cartilage Tissue Engineering
Tommaso Rada, Rui L. Reis, Manuela E. Gomes
Tissue Engineering Part B: Reviews. Jun 2009, Vol. 15, No. 2: 113-125
Abstract | Full Text PDF or HTML | Reprints & Permissions
Acceleration of spinal fusion using syngeneic and allogeneic adult adipose derived stem cells in a rat model
Mandi J. Lopez, Kevin R. McIntosh, Nakia D. Spencer, Jade N. Borneman, Ronald Horswell, Paul Anderson, Gang Yu, Lorrie Gaschen, Jeffrey M. Gimble
Journal of Orthopaedic Research. Apr 2009, Vol. 27, No. 3: 366-373
CrossRef
A New Method for Cryopreserving Adipose-Derived Stem Cells: An Attractive and Suitable Large-Scale and Long-Term Cell Banking Technology
Alfredo De Rosa, Francesco De Francesco, Virginia Tirino, Giuseppe A. Ferraro, Vincenzo Desiderio, Francesca Paino, Giuseppe Pirozzi, Francesco D'Andrea, Gianpaolo Papaccio
Tissue Engineering Part C: Methods. , Vol. 0, No. 0
Abstract | Full Text PDF
Progenitor and stem cells for bone and cartilage regeneration
M. K. El Tamer, R. L. Reis
Journal of Tissue Engineering and Regenerative Medicine. Feb 2009: n/a-n/a
CrossRef
Creation of New Bone by the Percutaneous Injection of Human Bone Marrow Stromal Cell and HA/TCP Suspensions
Mahesh H. Mankani, Sergei A. Kuznetsov, Grayson W. Marshall, Pamela Gehron Robey
Tissue Engineering Part A. Dec 2008, Vol. 14, No. 12: 1949-1958
Abstract | Full Text PDF or HTML | Reprints & Permissions
Identification of osteo-adipo progenitor cells in fat tissue
Y. F. Lin, W. Jing, L. Wu, X. Y. Li, Y. Wu, L. Liu, W. Tang, J. Long, W. D. Tian, X. M. Mo
Cell Proliferation. Nov 2008, Vol. 41, No. 5: 803-812
CrossRef
Current Approaches and Challenges in Making a Bio-Tooth
Jinhua Yu, Junnan Shi, Yan Jin
Tissue Engineering Part B: Reviews. Sep 2008, Vol. 14, No. 3: 307-319
Abstract | Full Text PDF | Reprints & Permissions
In Vivo Bone Formation Following Transplantation of Human Adipose–Derived Stromal Cells That Are Not Differentiated Osteogenically
Oju Jeon, Jong Won Rhie, Il-Kuen Kwon, Jae-Hwan Kim, Byung-Soo Kim, Soo-Hong Lee
Tissue Engineering Part A. Aug 2008, Vol. 14, No. 8: 1285-1294
Abstract | Full Text PDF | Reprints & Permissions
Mesenchymal cells for skeletal tissue engineering
Bethany J Slater, Matthew D Kwan, Deepak M Gupta, Nicholas J Panetta, Michael T Longaker
Expert Opinion on Biological Therapy. Aug 2008, Vol. 8, No. 7: 885-893
CrossRef
Tissue Engineering Craniofacial Defects With Adult Stem Cells? Are We Ready Yet?
PATRICIA A. ZUK
Pediatric Research. Jun 2008, Vol. 63, No. 5: 478-486
CrossRef
Adipogenic Human Adenovirus Ad-36 Induces Commitment, Differentiation, and Lipid Accumulation in Human Adipose-Derived Stem Cells
Magdalena Pasarica, Nazar Mashtalir, Emily J. McAllister, Gail E. Kilroy, Juraj Koska, Paska Permana, Barbora de Courten, Minghuan Yu, Eric Ravussin, Jeffery M. Gimble, Nikhil V. Dhurandhar
Stem Cells. May 2008, Vol. 26, No. 4: 969-978
CrossRef
Bone Regeneration in a Rabbit Critical-Sized Skull Defect Using Autologous Adipose-Derived Cells
Claudia Di Bella, Peter Farlie, Anthony J. Penington
Tissue Engineering Part A. Apr 2008, Vol. 14, No. 4: 483-490
Abstract | Full Text PDF | Reprints & Permissions
Role of Gender and Anatomical Region on Induction of Osteogenic Differentiation of Human Adipose-derived Stem Cells
A Emre Aksu, J Peter Rubin, Jason R. Dudas, Kacey G. Marra
Annals of Plastic Surgery. Apr 2008, Vol. 60, No. 3: 306-322
CrossRef
Leporine-Derived Adipose Precursor Cells Exhibit In Vitro Osteogenic Potential
Jason R. Dudas, Joseph E. Losee, Virginia M. Penascino, Darren M. Smith, Gregory M. Cooper, Mark P. Mooney, Shao Jiang, J. Peter Rubin, Kacey G. Marra
Journal of Craniofacial Surgery. Apr 2008, Vol. 19, No. 2: 360-368
CrossRef
Comparison of Osteogenic Ability of Rat Mesenchymal Stem Cells from Bone Marrow, Periosteum, and Adipose Tissue
Ousuke Hayashi, Yoshihiro Katsube, Motohiro Hirose, Hajime Ohgushi, Hiromoto Ito
Calcified Tissue International. Apr 2008, Vol. 82, No. 3: 238-247
CrossRef
Preserved Proliferative Capacity and Multipotency of Human Adipose-Derived Stem Cells after Long-Term Cryopreservation
Koichi Gonda, Tomokuni Shigeura, Takahiro Sato, Daisuke Matsumoto, Hirotaka Suga, Keita Inoue, Noriyuki Aoi, Harunosuke Kato, Katsujiro Sato, Syoko Murase, Isao Koshima, Kotaro Yoshimura
Plastic and Reconstructive Surgery. Mar 2008, Vol. 121, No. 2: 401-410
CrossRef
Genetic Markers of Osteogenesis and Angiogenesis Are Altered in Processed Lipoaspirate Cells when Cultured on Three-Dimensional Scaffolds
Catherine K. Huang, Weibiao Huang, Pat Zuk, Reza Jarrahy, George H. Rudkin, Kenji Ishida, Dean T. Yamaguchi, Timothy A. Miller
Plastic and Reconstructive Surgery. Mar 2008, Vol. 121, No. 2: 411-423
CrossRef
Osteogenic Differentiation of Human Adipose Tissue–Derived Stem Cells Is Modulated by the miR-26a Targeting of the SMAD1 Transcription Factor
Ettore Luzi, Francesca Marini, Silvia Carbonell Sala, Isabella Tognarini, Gianna Galli, Maria Luisa Brandi
Journal of Bone and Mineral Research. Mar 2008, Vol. 23, No. 2: 287-295
CrossRef
Collagen I Gel Can Facilitate Homogenous Bone Formation of Adipose-Derived Stem Cells in PLGA-β-TCP Scaffold
Wei Hao, Yun-Yu Hu, Yi-Yong Wei, Long Pang, Rong Lv, Jian-Ping Bai, Zhuo Xiong, Ming Jiang
Cells Tissues Organs. Feb 2008, Vol. 187, No. 2: 89-102
CrossRef
In vitro Differentiation Potential of Mesenchymal Stem Cells
Jeffrey M. Gimble, Farshid Guilak, Mark E. Nuttall, Solomon Sathishkumar, Martin Vidal, Bruce A. Bunnell
Transfusion Medicine and Hemotherapy. Feb 2008, Vol. 35, No. 3: 228-238
CrossRef
Refining Retinoic Acid Stimulation for Osteogenic Differentiation of Murine Adipose-Derived Adult Stromal Cells
Derrick C. Wan, Matthew T. Siedhoff, Matthew D. Kwan, Randall P. Nacamuli, Benjamin M. Wu, Michael T. Longaker
Tissue Engineering. Jul 2007, Vol. 13, No. 7: 1623-1631
Abstract | Full Text PDF | Reprints & Permissions
Expanded Adipose-Derived Stem Cells Suppress Mixed Lymphocyte Reaction by Secretion of Prostaglandin E2
Lei Cui, Shuo Yin, Wei Liu, Ningli Li, Wenjie Zhang, Yilin Cao
Tissue Engineering. Jun 2007, Vol. 13, No. 6: 1185-1195
Abstract | Full Text PDF | Reprints & Permissions
Biomaterials Approach to Expand and Direct Differentiation of Stem Cells
Chou Chai, Kam W Leong
Molecular Therapy. Apr 2007, Vol. 15, No. 3: 467-480
CrossRef
Investigating the effects of preinduction on human adipose-derived precursor cells in an athymic rat model
David Tai Leong, Mohan Chothirakottu Abraham, Subha Narayan Rath, Thiam-Chye Lim, Fook Tim Chew, Dietmar Werner Hutmacher
Differentiation. Jan 2007, Vol. 74, No. 9-10: 519-529
CrossRef
Cell-Assisted Lipotransfer: Supportive Use of Human Adipose-Derived Cells for Soft Tissue Augmentation with Lipoinjection
Daisuke Matsumoto, Katsujiro Sato, Koichi Gonda, Yasuyuki Takaki, Tomokuni Shigeura, Takahiro Sato, Emiko Aiba-Kojima, Fumiko Iizuka, Keita Inoue, Hirotaka Suga, Kotaro Yoshimura
Tissue Engineering. Dec 2006, Vol. 0, No. 0: 061122053519001
CrossRef
Cell-Assisted Lipotransfer: Supportive Use of Human Adipose-Derived Cells for Soft Tissue Augmentation with Lipoinjection
Daisuke Matsumoto, Katsujiro Sato, Koichi Gonda, Yasuyuki Takaki, Tomokuni Shigeura, Takahiro Sato, Emiko Aiba-Kojima, Fumiko Iizuka, Keita Inoue, Hirotaka Suga, Kotaro Yoshimura
Tissue Engineering. Dec 2006, Vol. 12, No. 12: 3375-3382
Abstract | Full Text PDF | Reprints & Permissions
Structural Fat Grafting: More Than a Permanent Filler
Sydney R. Coleman
Plastic and Reconstructive Surgery. Oct 2006, Vol. 118, No. Suppl: 108S-120S
CrossRef
Species Specificity of Ectopic Bone Formation Using Periosteum-Derived Mesenchymal Progenitor Cells
Jeroen Eyckmans, Frank P. Luyten
Tissue Engineering. Sep 2006, Vol. 0, No. 0: 060913044658046
CrossRef
Species Specificity of Ectopic Bone Formation Using Periosteum-Derived Mesenchymal Progenitor Cells
Jeroen Eyckmans, Frank P. Luyten
Tissue Engineering. Aug 2006, Vol. 12, No. 8: 2203-2213
Abstract | Full Text PDF | Reprints & Permissions
Osteogenic Potentiation of Human Adipose???Derived Stem Cells in a 3-Dimensional Matrix
Joubin S. Gabbay, Justin B. Heller, Scott A. Mitchell, Patricia A. Zuk, Daniel B. Spoon, Kristy L. Wasson, Reza Jarrahy, Prosper Benhaim, James P. Bradley
Annals of Plastic Surgery. Aug 2006, Vol. 57, No. 1: 89-93
CrossRef
Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates
Kotaro Yoshimura, Tomokuni Shigeura, Daisuke Matsumoto, Takahiro Sato, Yasuyuki Takaki, Emiko Aiba-Kojima, Katsujiro Sato, Keita Inoue, Takashi Nagase, Isao Koshima, Koichi Gonda
Journal of Cellular Physiology. Aug 2006, Vol. 208, No. 1: 64-76
CrossRef
Adipose-derived stem cells for the regeneration of damaged tissues
Anna M Parker, Adam J Katz
Expert Opinion on Biological Therapy. Jul 2006, Vol. 6, No. 6: 567-578
CrossRef
Playing with bone and fat
Jeffrey M. Gimble, Sanjin Zvonic, Z. Elizabeth Floyd, Moustapha Kassem, Mark E. Nuttall
Journal of Cellular Biochemistry. Jun 2006, Vol. 98, No. 2: 251-266
CrossRef
The Immunogenicity of Human Adipose-Derived Cells: Temporal Changes In Vitro
Kevin McIntosh, Sanjin Zvonic, Sara Garrett, James B. Mitchell, Z. Elizabeth Floyd, Lora Hammill, Amy Kloster, Yuan Di Halvorsen, Jenny P. Ting, Robert W. Storms, Brian Goh, Gail Kilroy, Xiying Wu, Jeffrey M. Gimble
Stem Cells. Jun 2006, Vol. 24, No. 5: 1246-1253
CrossRef
The Osteogenic Potential of Adipose-Derived Stem Cells for the Repair of Rabbit Calvarial Defects
Jason R. Dudas, Kacey G. Marra, Gregory M. Cooper, Virginia M. Penascino, Mark P. Mooney, Shao Jiang, J Peter Rubin, Joseph E. Losee
Annals of Plastic Surgery. Jun 2006, Vol. 56, No. 5: 543-548
CrossRef
Immunophenotype of Human Adipose-Derived Cells: Temporal Changes in Stromal-Associated and Stem Cell-Associated Markers
James B. Mitchell, Kevin McIntosh, Sanjin Zvonic, Sara Garrett, Z. Elizabeth Floyd, Amy Kloster, Yuan Di Halvorsen, Robert W. Storms, Brian Goh, Gail Kilroy, Xiying Wu, Jeffrey M. Gimble
Stem Cells. Mar 2006, Vol. 24, No. 2: 376-385
CrossRef
Characterization of Osteogenically Induced Adipose Tissue-Derived Precursor Cells in 2-Dimensional and 3-Dimensional Environments
David Tai Leong, Wei Meng Khor, Fook Tim Chew, Thiam-Chye Lim, Dietmar W. Hutmacher
Cells Tissues Organs. Feb 2006, Vol. 182, No. 1: 1-11
CrossRef
Osteogenic Potential of Adult Human Stem Cells of the Lumbar Vertebral Body and the Iliac Crest
Makarand V. Risbud, Irving M. Shapiro, Asha Guttapalli, Alberto Di Martino, Keith G. Danielson, John M. Beiner, Alan Hillibrand, Todd J Albert, D Greg Anderson, Alexander R. Vaccaro
Spine. Feb 2006, Vol. 31, No. 1: 83-89
CrossRef
Gene Therapy Progress and Prospects: In tissue engineering
J Polak, L Hench
Gene Therapy. Jan 2006, Vol. 12, No. 24: 1725-1733
CrossRef
Transport phenomena during freezing of adipose tissue derived adult stem cells
Sreedhar Thirumala, Jeffrey M. Gimble, Ram V. Devireddy
Biotechnology and Bioengineering. Dec 2005, Vol. 92, No. 3: 372-383
CrossRef
Bone induction in craniofacial defects1
RP Nacamuli, MT Longaker
Orthodontics and Craniofacial Research. Dec 2005, Vol. 8, No. 4: 259-266
CrossRef
The Osteogenic Potential of Adipose-Derived Mesenchymal Cells Is Maintained with Aging
Yun-Ying Shi, Randall P. Nacamuli, Ali Salim, Michael T. Longaker
Plastic and Reconstructive Surgery. Dec 2005, Vol. 116, No. 6: 1686-1696
CrossRef
Tissue engineering
Oneida Arosarena
Current Opinion in Otolaryngology & Head and Neck Surgery. Sep 2005, Vol. 13, No. 4: 233-241
CrossRef
Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells
Benedicte Puissant, Corinne Barreau, Philippe Bourin, Cyril Clavel, Jill Corre, Christine Bousquet, Christine Taureau, Beatrice Cousin, Michel Abbal, Patrick Laharrague, Luc Penicaud, Louis Casteilla, Antoine Blancher
British Journal of Haematology. May 2005, Vol. 129, No. 1: 118-129
CrossRef
A perspective on pancreatic stem/progenitor cells
Joel F. Habener
Pediatric Diabetes. 2004, Vol. 5, No. s2: 29
CrossRef
All articles
Previous Next