Advertisement

Stem Cell Reviews and Reports

, Volume 5, Issue 4, pp 437–445 | Cite as

Bone marrow Derived Pluripotent Cells are Pericytes which Contribute to Vascularization

  • Xiaoxiao Cai
  • Yunfeng LinEmail author
  • Claudia C. Friedrich
  • Craig Neville
  • Irina Pomerantseva
  • Cathryn A. Sundback
  • Parul Sharma
  • Zhiyuan Zhang
  • Joseph P. Vacanti
  • Peter V. Hauschka
  • Brian E. GrottkauEmail author
Article
First Online:

Abstract

Pericytes are essential to vascularization, but the purification and characterization of pericytes remain unclear. Smooth muscle actin alpha (α-SMA) is one maker of pericytes. The aim of this study is to purify the α-SMA positive cells from bone marrow and study the characteristics of these cells and the interaction between α-SMA positive cells and endothelial cells. The bone marrow stromal cells were harvested from α-SMA-GFP transgenic mice, and the α-SMA-GFP positive cells were sorted by FACS. The proliferative characteristics and multilineage differentiation ability of the α-SMA-GFP positive cells were tested. A 3-D culture model was then applied to test their vascularization by loading α-SMA-GFP positive cells and endothelial cells on collagen-fibronectin gel. Results demonstrated that bone marrow stromal cells are mostly α-SMA-GFP positive cells which are pluripotent, and these cells expressed α-SMA during differentiation. The α-SMA-GFP positive cells could stimulate the endothelial cells to form tube-like structures and subsequently robust vascular networks in 3-D culture. In conclusion, the bone marrow derived pluripotent cells are pericytes and can contribute to vascularization.

Keywords

Bone marrow stromal cells Pericytes Multilineage differentiation Endothelial cells Vascularization. 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This work was funded by the Anthony and Constance Franchi Fund for Pediatric Orthopaedics at the MassGeneral Hospital for Children, The Peabody Foundation Inc., the National Natural Science Foundation of China (30801304), Foundation for the Author of National Excellent Doctoral Dissertation of PR China (FANEDD 200977) and Program for New Century Excellent Talents in University (NCET-08-0373).

References

  1. 1.
    Langer, R., & Vacanti, J. P. (1993). Tissue engineering. Science, 260(5110), 920–6.CrossRefPubMedGoogle Scholar
  2. 2.
    Caplan, A. I. (2000). Tissue engineering designs for the future: new logics, old molecules. Tissue Eng, 6(1), 1–8.CrossRefPubMedGoogle Scholar
  3. 3.
    Melero-Martin, J. M., De Obaldia, M. E., Kang, S. Y., et al. (2008). Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res, 103(2), 194–202.CrossRefPubMedGoogle Scholar
  4. 4.
    Traktuev, D. O., Prater, D. N., Merfeld-Clauss, S., et al. (2009). Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res, 104(12), 1410–20.CrossRefPubMedGoogle Scholar
  5. 5.
    Armulik, A., Abramsson, A., & Betsholtz, C. (2005). Endothelial/pericyte interactions. Circ Res, 97(6), 512–23.CrossRefPubMedGoogle Scholar
  6. 6.
    Levenberg, S., Rouwkema, J., Macdonald, M., et al. (2005). Engineering vascularized skeletal muscle tissue. Nat Biotechnol, 23(7), 879–84.CrossRefPubMedGoogle Scholar
  7. 7.
    Crisan, M., Yap, S., Casteilla, L., et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3(3), 301–13.CrossRefPubMedGoogle Scholar
  8. 8.
    Shepherd, B. R., Chen, H. Y., Smith, C. M., Gruionu, G., Williams, S. K., & Hoying, J. B. (2004). Rapid perfusion and network remodeling in a microvascular construct after implantation. Arterioscler Thromb Vasc Biol, 24(5), 898–904.CrossRefPubMedGoogle Scholar
  9. 9.
    Tremblay, P. L., Hudon, V., Berthod, F., Germain, L., & Auger, F. A. (2005). Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am J Transplant, 5(5), 1002–10.CrossRefPubMedGoogle Scholar
  10. 10.
    Koike, N., Fukumura, D., Gralla, O., Au, P., Schechner, J. S., & Jain, R. K. (2004). Tissue engineering: creation of long-lasting blood vessels. Nature, 428(6979), 138–9.CrossRefPubMedGoogle Scholar
  11. 11.
    Nguyen, L. L., & D'Amore, P. A. (2001). Cellular interactions in vascular growth and differentiation. Int Rev Cytol, 204, 1–48.CrossRefPubMedGoogle Scholar
  12. 12.
    Wu, Y., Wang, J., Scott, P. G., & Tredget, E. E. (2007). Bone marrow-derived stem cells in wound healing: a review. Wound Repair Regen, 15(Suppl 1), S18–26.CrossRefPubMedGoogle Scholar
  13. 13.
    Caplan, A. I. (2008). All MSCs are pericytes? Cell Stem Cell, 3(3), 229–30.CrossRefPubMedGoogle Scholar
  14. 14.
    Kalajzic, Z., Li, H., Wang, L. P., et al. (2008). Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population. Bone, 43(3), 501–10.CrossRefPubMedGoogle Scholar
  15. 15.
    Yokota, T., Kawakami, Y., Nagai, Y., et al. (2006). Bone marrow lacks a transplantable progenitor for smooth muscle type alpha-actin-expressing cells. Stem Cells, 24(1), 13–22.CrossRefPubMedGoogle Scholar
  16. 16.
    Cai, X., Lin, Y., Ou, G., et al. (2007). Ectopic osteogenesis and chondrogenesis of bone marrow stromal stem cells in alginate system. Cell Biol Int, 31(8), 776–83.CrossRefPubMedGoogle Scholar
  17. 17.
    Lin, Y., Chen, X., Yan, Z., et al. (2006). Multilineage differentiation of adipose-derived stromal cells from GFP transgenic mice. Mol Cell Biochem, 285(1–2), 69–78.PubMedGoogle Scholar
  18. 18.
    Wu L, Cai X, Dong H, et al. Serum regulates adipogenesis of mesenchymal stem cells via MEK/ERK dependent PPARgamma expression and phosphorylation. J Cell Mol Med 2009.Google Scholar
  19. 19.
    Verseijden F, Posthumus-van Sluijs S, Pavljasevic P, Hofer S, van Osch G, Farrell E. Adult human bone marrow- and adipose tissue-derived stromal cells support the formation of prevascular-like structures from endothelial cells in vitro. Tissue Eng Part A 2009.Google Scholar
  20. 20.
    Lin, Y. F., Jing, W., Wu, L., et al. (2008). Identification of osteo-adipo progenitor cells in fat tissue. Cell Prolif, 41(5), 803–12.CrossRefPubMedGoogle Scholar
  21. 21.
    Tang, W., Zeve, D., Suh, J. M., et al. (2008). White fat progenitor cells reside in the adipose vasculature. Science, 322(5901), 583–6.CrossRefPubMedGoogle Scholar
  22. 22.
    Rodeheffer, M. S., Birsoy, K., & Friedman, J. M. (2008). Identification of white adipocyte progenitor cells in vivo. Cell, 135(2), 240–9.CrossRefPubMedGoogle Scholar
  23. 23.
    von Tell, D., Armulik, A., & Betsholtz, C. (2006). Pericytes and vascular stability. Exp Cell Res, 312(5), 623–9.CrossRefGoogle Scholar
  24. 24.
    Caplan, A. I. (2009). Why are MSCs therapeutic? New data: new insight. J Pathol, 217(2), 318–24.CrossRefPubMedGoogle Scholar
  25. 25.
    Haynesworth, S. E., Baber, M. A., & Caplan, A. I. (1996). Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J Cell Physiol, 166(3), 585–92.CrossRefPubMedGoogle Scholar
  26. 26.
    Rouwkema, J., de Boer, J., & Van Blitterswijk, C. A. (2006). Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. Tissue Eng, 12(9), 2685–93.CrossRefPubMedGoogle Scholar
  27. 27.
    Akita, M., Murata, E., Merker, H. J., & Kaneko, K. (1997). Formation of new capillary-like tubes in a three-dimensional in vitro model (aorta/collagen gel). Ann Anat, 179(2), 137–47.PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media 2009

Authors and Affiliations

  • Xiaoxiao Cai
    • 1
    • 2
  • Yunfeng Lin
    • 1
    • 3
    • 4
    Email author
  • Claudia C. Friedrich
    • 3
  • Craig Neville
    • 3
  • Irina Pomerantseva
    • 3
  • Cathryn A. Sundback
    • 3
  • Parul Sharma
    • 2
  • Zhiyuan Zhang
    • 2
  • Joseph P. Vacanti
    • 3
  • Peter V. Hauschka
    • 2
  • Brian E. Grottkau
    • 4
    Email author
  1. 1.State Key Laboratory of Oral Diseases, West China College of StomatologySichuan UniversityChengduPeople’s Republic of China
  2. 2.Department of Orthopaedic Surgery, Children’s Hospital BostonHarvard Medical SchoolBostonUSA
  3. 3.Center for Regenerative Medicine, Massachusetts General HospitalHarvard Medical SchoolBostonUSA
  4. 4.Department of Orthopaedic Surgery, Mass General Hospital for Children and the Pediatric Orthopaedic Laboratory for Tissue EngineeringHarvard Medical SchoolBostonUSA

Personalised recommendations

Cite article

Buy options