Advances in Adipose-Derived Stem Cells Isolation, Characterization, and Application in Regenerative Tissue Engineering

Umesh D Wankhade, Michael Shen, Ravindra Kolhe, Sadanand Fulzele, Umesh D Wankhade, Michael Shen, Ravindra Kolhe, Sadanand Fulzele

Abstract

Obesity is a complex, multifactorial disease that has been extensively researched in recent times. Obesity is characterized by excess deposition of adipose tissue in response to surplus energy. Despite the negative connotations of adipose tissue (AT), it serves as a critical endocrine organ. Adipose tissue is a source of several adipokines and cytokines which have been deemed important for both normal metabolic function and disease formation. The discoveries of metabolically active brown AT in adult humans and adipose tissue derived stem cells (ADSC) have been key findings in the past decade with potential therapeutic implications. ADSCs represent an enticing pool of multipotent adult stem cells because of their noncontroversial nature, relative abundance, ease of isolation, and expandability. A decade and a half since the discovery of ADSCs, the scientific community is still working to uncover their therapeutic potential in a wide range of diseases. In this review, we provide an overview of the recent developments in the field of ADSCs and examine their potential use in transplantation and cell-based therapies for the regeneration of diseased organs and systems. We also hope to provide perspective on how to best utilize this readily available, powerful pool of stem cells in the future.

Figures

Figure 1
Figure 1
Schematic diagram for ADSCs isolation from adipose tissue and several uses of ADSCs in tissue regenerative medicine.

References

    1. Gimble J. M. Adipose tissue-derived therapeutics. Expert Opinion on Biological Therapy. 2003;3(5):705–713. doi: 10.1517/14712598.3.5.705.
    1. Bender Kim C. F., Jackson E. L., Woolfenden A. E., et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell. 2005;121(6):823–835. doi: 10.1016/j.cell.2005.03.032.
    1. Crisan M., Yap S., Casteilla L., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301–313. doi: 10.1016/j.stem.2008.07.003.
    1. Kishi K., Imanishi N., Ohara H., et al. Distribution of adipose-derived stem cells in adipose tissues from human cadavers. Journal of Plastic, Reconstructive and Aesthetic Surgery. 2010;63(10):1717–1722. doi: 10.1016/j.bjps.2009.10.020.
    1. Zuk P. A., Zhu M., Mizuno H., et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering. 2001;7(2):211–228. doi: 10.1089/107632701300062859.
    1. Rodbell M. Metabolism of isolated fat cells. I. Effects of hormones on glucose. The Journal of Biological Chemistry. 1964;239:375–380.
    1. Poznanski W. J., Waheed I., Van R. Human fat cell precursors. Morphologic and metabolic differentiation in culture. Laboratory Investigation. 1973;29(5):570–576.
    1. Rodbell M. Metabolism of isolated fat cells. II. The similar effects of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on glucose and amino acid metabolism. The Journal of Biological Chemistry. 1966;241(1):130–139.
    1. Martin R. J., Hausman G. J., Hausman D. B. Regulation of adipose cell development in utero . Experimental Biology and Medicine. 1998;219(3):200–210. doi: 10.3181/00379727-219-44333.
    1. Nnodim J. O. Development of adipose tissues. Anatomical Record. 1987;219(4):331–337. doi: 10.1002/ar.1092190402.
    1. Loh N. Y., Neville M. J., Marinou K., et al. LRP5 regulates human body fat distribution by modulating adipose progenitor biology in a dose- and depot-specific fashion. Cell Metabolism. 2015;21(2):262–272. doi: 10.1016/j.cmet.2015.01.009.
    1. Cypess A. M., Lehman S., Williams G., et al. Identification and importance of brown adipose tissue in adult humans. The New England Journal of Medicine. 2009;360(15):1509–1517. doi: 10.1056/nejmoa0810780.
    1. Nedergaard J., Bengtsson T., Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. The American Journal of Physiology—Endocrinology and Metabolism. 2007;293(2):E444–E452. doi: 10.1152/ajpendo.00691.2006.
    1. Prunet-Marcassus B., Cousin B., Caton D., André M., Pénicaud L., Casteilla L. From heterogeneity to plasticity in adipose tissues: site-specific differences. Experimental Cell Research. 2006;312(6):727–736. doi: 10.1016/j.yexcr.2005.11.021.
    1. Van Harmelen V., Röhrig K., Hauner H. Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects. Metabolism: Clinical and Experimental. 2004;53(5):632–637. doi: 10.1016/j.metabol.2003.11.012.
    1. Rodbell M. Metabolism of isolated fat cells. VI. The effects of insulin, lipolytic hormones, and theophylline on glucose transport and metabolism in ‘ghosts’. The Journal of Biological Chemistry. 1967;242(24):5751–5756.
    1. Rodbell M. Metabolism of isolated fat cells. V. Preparation of ‘ghosts’ and their properties; adenyl cyclase and other enzymes. The Journal of Biological Chemistry. 1967;242(24):5744–5750.
    1. Rodbell M., Jones A. B. Metabolism of isolated fat cells. 3. The similar inhibitory action of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on lipolysis stimulated by lipolytic hormones and theophylline. The Journal of Biological Chemistry. 1966;241(1):140–142.
    1. Rodbell M. The metabolism of isolated fat cells. IV. Regulation of release of protein by lipolytic hormones and insulin. The Journal of Biological Chemistry. 1966;241(17):3909–3917.
    1. Berry R., Rodeheffer M. S. Characterization of the adipocyte cellular lineage in vivo. Nature Cell Biology. 2013;15(3):302–308. doi: 10.1038/ncb2696.
    1. Rodeheffer M. S., Birsoy K., Friedman J. M. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135(2):240–249. doi: 10.1016/j.cell.2008.09.036.
    1. Church C. D., Berry R., Rodeheffer M. S. Isolation and study of adipocyte precursors. Methods in Enzymology. 2014;537:31–46. doi: 10.1016/b978-0-12-411619-1.00003-3.
    1. Nicoletti G. F., De Francesco F., D'Andrea F., Ferraro G. A. Methods and procedures in adipose stem cells: state of the art and perspective for translation medicine. Journal of Cellular Physiology. 2015;230(3):489–495. doi: 10.1002/jcp.24837.
    1. Zimmerlin L., Donnenberg V. S., Pfeifer M. E., et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry Part A. 2010;77(1):22–30. doi: 10.1002/cyto.a.20813.
    1. Zavan B., De Francesco F., D'Andrea F., et al. Persistence of CD34 stem marker in human lipoma: searching for cancer stem cells. International Journal of Biological Sciences. 2015;11(10):1127–1139. doi: 10.7150/ijbs.11946.
    1. Bailey A. M., Kapur S., Katz A. J. Characterization of adipose-derived stem cells: an update. Current Stem Cell Research & Therapy. 2010;5(2):95–102. doi: 10.2174/157488810791268555.
    1. Ong W. K., Tan C. S., Chan K. L., et al. Identification of specific cell-surface markers of adipose-derived stem cells from subcutaneous and visceral fat depots. Stem Cell Reports. 2014;2(2):171–179. doi: 10.1016/j.stemcr.2014.01.002.
    1. Billings E., Jr., May J. W., Jr. Historical review and present status of free fat graft autotransplantation in plastic and reconstructive surgery. Plastic and Reconstructive Surgery. 1989;83(2):368–381. doi: 10.1097/00006534-198902000-00033.
    1. Delay E., Sinna R., Delaporte T., Flageul G., Tourasse C., Tousson G. Patient information before aesthetic lipomodeling (lipoaugmentation): a French plastic surgeon's perspective. Aesthetic Surgery Journal. 2009;29(5):386–395. doi: 10.1016/j.asj.2009.08.007.
    1. Coleman S. R., Saboeiro A. P. Fat grafting to the breast revisited: safety and efficacy. Plastic and Reconstructive Surgery. 2007;119(3):775–787. doi: 10.1097/01.prs.0000252001.59162.c9.
    1. Petit J. Y., Lohsiriwat V., Clough K. B., et al. The oncologic outcome and immediate surgical complications of lipofilling in breast cancer patients: a multicenter study—Milan-Paris-Lyon experience of 646 lipofilling procedures. Plastic and Reconstructive Surgery. 2011;128(2):341–346. doi: 10.1097/prs.0b013e31821e713c.
    1. Rietjens M., De Lorenzi F., Rossetto F., et al. Safety of fat grafting in secondary breast reconstruction after cancer. Journal of Plastic, Reconstructive & Aesthetic Surgery. 2011;64(4):477–483. doi: 10.1016/j.bjps.2010.06.024.
    1. Delay E., Garson S., Tousson G., Sinna R. Fat injection to the breast: technique, results, and indications based on 880 procedures over 10 years. Aesthetic Surgery Journal. 2009;29(5):360–376. doi: 10.1016/j.asj.2009.08.010.
    1. Kølle S.-F. T., Fischer-Nielsen A., Mathiasen A. B., et al. Enrichment of autologous fat grafts with ex-vivo expanded adipose tissue-derived stem cells for graft survival: a randomised placebo-controlled trial. The Lancet. 2013;382(9898):1113–1120. doi: 10.1016/s0140-6736(13)61410-5.
    1. Eljaafari A., Robert M., Chehimi M., et al. Adipose tissue-derived stem cells from obese subjects contribute to inflammation and reduced insulin response in adipocytes through differential regulation of the Th1/Th17 balance and monocyte activation. Diabetes. 2015;64(7):2477–2488. doi: 10.2337/db15-0162.
    1. García-Olmo D., García-Arranz M., García L. G., et al. Autologous stem cell transplantation for treatment of rectovaginal fistula in perianal Crohn's disease: a new cell-based therapy. International Journal of Colorectal Disease. 2003;18(5):451–454. doi: 10.1007/s00384-003-0490-3.
    1. García-Olmo D., García-Arranz M., Herreros D., Pascual I., Peiro C., Rodríguez-Montes J. A. A phase I clinical trial of the treatment of crohn's fistula by adipose mesenchymal stem cell transplantation. Diseases of the Colon and Rectum. 2005;48(7):1416–1423. doi: 10.1007/s10350-005-0052-6.
    1. Garcia-Olmo D., Herreros D., Pascual I., et al. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Diseases of the Colon and Rectum. 2009;52(1):79–86. doi: 10.1007/dcr.0b013e3181973487.
    1. Kuo Y. R., Wang C. T., Cheng J. T., Kao G. S., Chiang Y. C., Wang C. J. Adipose-derived stem cells accelerate diabetic wound healing through the induction of autocrine and paracrine effects. Cell Transplantation. 2016;25(1):71–81. doi: 10.3727/096368915x687921.
    1. Salgado A. J., Reis R. L., Sousa N. J., Gimble J. M. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Current Stem Cell Research Therapy. 2010;5(2):103–110. doi: 10.2174/157488810791268564.
    1. Gronthos S., Franklin D. M., Leddy H. A., Robey P. G., Storms R. W., Gimble J. M. Surface protein characterization of human adipose tissue-derived stromal cells. Journal of Cellular Physiology. 2001;189(1):54–63. doi: 10.1002/jcp.1138.
    1. Cowan C. M., Shi Y.-Y., Aalami O. O., et al. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nature Biotechnology. 2004;22(5):560–567. doi: 10.1038/nbt958.
    1. Lendeckel S., Jödicke A., Christophis P., et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. Journal of Cranio-Maxillofacial Surgery. 2004;32(6):370–373. doi: 10.1016/j.jcms.2004.06.002.
    1. Thesleff T., Lehtimäki K., Niskakangas T., et al. Cranioplasty with adipose-derived stem cells and biomaterial: a novel method for cranial reconstruction. Neurosurgery. 2011;68(6):1535–1540. doi: 10.1227/neu.0b013e31820ee24e.
    1. Ahn H. H., Kim K. S., Lee J. H., et al. In vivo osteogenic differentiation of human adipose-derived stem cells in an injectable in situ-forming gel scaffold. Tissue Engineering—Part A. 2009;15(7):1821–1832. doi: 10.1089/ten.tea.2008.0386.
    1. Jung S.-N., Rhie J. W., Kwon H., et al. In vivo cartilage formation using chondrogenic-differentiated human adipose-derived mesenchymal stem cells mixed with fibrin glue. The Journal of Craniofacial Surgery. 2010;21(2):468–472. doi: 10.1097/scs.0b013e3181cfea50.
    1. Mesimäki K., Lindroos B., Törnwall J., et al. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. International Journal of Oral and Maxillofacial Surgery. 2009;38(3):201–209. doi: 10.1016/j.ijom.2009.01.001.
    1. Ogawa R., Mizuno S. Cartilage regeneration using adipose-derived stem cells. Current Stem Cell Research & Therapy. 2010;5(2):129–132. doi: 10.2174/157488810791268627.
    1. Kim H.-J., Im G.-I. Chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells: greater doses of growth factor are necessary. Journal of Orthopaedic Research. 2009;27(5):612–619. doi: 10.1002/jor.20766.
    1. Knippenberg M., Helder M. N., Doulabi B. Z., Semeins C. M., Wuisman P. I. J. M., Klein-Nulend J. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Engineering. 2005;11(11-12):1780–1788. doi: 10.1089/ten.2005.11.1780.
    1. Desiderio V., De Francesco F., Schiraldi C., et al. Human Ng2+ adipose stem cells loaded in vivo on a new crosslinked hyaluronic acid-lys scaffold fabricate a skeletal muscle tissue. Journal of Cellular Physiology. 2013;228(8):1762–1773. doi: 10.1002/jcp.24336.
    1. McCullen S. D., Zhan J., Onorato M. L., Bernacki S. H., Loboa E. G. Effect of varied ionic calcium on human adipose-derived stem cell mineralization. Tissue Engineering Part A. 2010;16(6):1971–1981. doi: 10.1089/ten.tea.2009.0691.
    1. Mellor L. F., Mohiti-Asli M., Williams J., et al. Extracellular calcium modulates chondrogenic and osteogenic differentiation of human adipose-derived stem cells: a novel approach for osteochondral tissue engineering using a single stem cell source. Tissue Engineering Part A. 2015;21(17-18):2323–2333. doi: 10.1089/ten.tea.2014.0572.
    1. Al Battah F., De Kock J., Vanhaecke T., Rogiers V. Current status of human adipose-derived stem cells: differentiation into hepatocyte-like cells. TheScientificWorldJournal. 2011;11:1568–1581. doi: 10.1100/tsw.2011.146.
    1. Fang B., Li Y., Song Y., et al. Human adipose tissue-derived adult stem cells can lead to multiorgan engraftment. Transplantation Proceedings. 2010;42(5):1849–1856. doi: 10.1016/j.transproceed.2010.01.058.
    1. Tang W. P., Akahoshi T., Piao J. S., et al. Basic fibroblast growth factor-treated adipose tissue-derived mesenchymal stem cell infusion to ameliorate liver cirrhosis via paracrine hepatocyte growth factor. Journal of Gastroenterology and Hepatology. 2015;30(6):1065–1074. doi: 10.1111/jgh.12893.
    1. Young D. A., DeQuach J. A., Christman K. L. Human cardiomyogenesis and the need for systems biology analysis. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. 2011;3(6):666–680. doi: 10.1002/wsbm.141.
    1. Planat-Bénard V., Menard C., André M., et al. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circulation Research. 2004;94(2):223–229. doi: 10.1161/01.res.0000109792.43271.47.
    1. Song Y.-H., Gehmert S., Sadat S., et al. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochemical and Biophysical Research Communications. 2007;354(4):999–1003. doi: 10.1016/j.bbrc.2007.01.095.
    1. Horikoshi-Ishihara H., Tobita M., Tajima S., et al. Coadministration of adipose-derived stem cells and control-released basic fibroblast growth factor facilitates angiogenesis in a murine ischemic hind limb model. Journal of Vascular Surgery. 2015 doi: 10.1016/j.jvs.2015.09.054.
    1. De Francesco F., Tirino V., Desiderio V., et al. Human CD34+/CD90+ ASCs are capable of growing as sphere clusters, producing high levels of VEGF and forming capillaries. PLoS ONE. 2009;4(8) doi: 10.1371/journal.pone.0006537.e6537
    1. De Francesco F., Ricci G., D'Andrea F., Nicoletti G. F., Ferraro G. A. Human adipose stem cells: from bench to bedside. Tissue Engineering, Part B: Reviews. 2015;21(6):572–584. doi: 10.1089/ten.teb.2014.0608.
    1. Friis T., Haack-Sørensen M., Mathiasen A. B., et al. Mesenchymal stromal cell derived endothelial progenitor treatment in patients with refractory angina. Scandinavian Cardiovascular Journal. 2011;45(3):161–168. doi: 10.3109/14017431.2011.569571.
    1. Bai X., Alt E. Myocardial regeneration potential of adipose tissue-derived stem cells. Biochemical and Biophysical Research Communications. 2010;401(3):321–326. doi: 10.1016/j.bbrc.2010.09.012.
    1. Erba P., Terenghi G., Kingham P. J. Neural differentiation and therapeutic potential of adipose tissue derived stem cells. Current Stem Cell Research and Therapy. 2010;5(2):153–160. doi: 10.2174/157488810791268645.
    1. Abdanipour A., Tiraihi T., Delshad A. Trans-differentiation of the adipose tissue-derived stem cells into neuron-like cells expressing neurotrophins by selegiline. Iranian Biomedical Journal. 2011;15:113–121.
    1. Han C., Zhang L., Song L., et al. Human adipose-derived mesenchymal stem cells: a better cell source for nervous system regeneration. Chinese Medical Journal. 2014;127(2):329–337. doi: 10.3760/cma.j.issn.0366-6999.20120064.
    1. Cronk S. M., Kelly-Goss M. R., Ray H. C., et al. Adipose-derived stem cells from diabetic mice show impaired vascular stabilization in a murine model of diabetic retinopathy. Stem Cells Translational Medicine. 2015;4(5):459–467. doi: 10.5966/sctm.2014-0108.
    1. Yamamoto T., Gotoh M., Hattori R., et al. Periurethral injection of autologous adipose-derived stem cells for the treatment of stress urinary incontinence in patients undergoing radical prostatectomy: report of two initial cases. International Journal of Urology. 2010;17(1):75–82. doi: 10.1111/j.1442-2042.2009.02429.x.
    1. Lee P. E., Kung R. C., Drutz H. P. Periurethral autologous fat injection as treatment for female stress urinary incontinence: a randomized double-blind controlled trial. The Journal of Urology. 2001;165(1):153–158. doi: 10.1097/00005392-200101000-00037.
    1. Dicker A., Le Blanc K., Åström G., et al. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Experimental Cell Research. 2005;308(2):283–290. doi: 10.1016/j.yexcr.2005.04.029.
    1. Halvorsen Y.-D. C., Bond A., Sen A., et al. Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. Metabolism: Clinical and Experimental. 2001;50(4):407–413. doi: 10.1053/meta.2001.21690.
    1. Hicok K. C., Du Laney T. V., Zhou Y. S., et al. Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Engineering. 2004;10(3-4):371–380. doi: 10.1089/107632704323061735.
    1. Lee J. A., Parrett B. M., Conejero J. A., et al. Biological alchemy: engineering bone and fat from fat-derived stem cells. Annals of Plastic Surgery. 2003;50(6):610–617. doi: 10.1097/01.sap.0000069069.23266.35.
    1. Dragoo J. L., Choi J. Y., Lieberman J. R., et al. Bone induction by BMP-2 transduced stem cells derived from human fat. Journal of Orthopaedic Research. 2003;21(4):622–629. doi: 10.1016/S0736-0266(02)00238-3.
    1. Dragoo J. L., Lieberman J. R., Lee R. S., et al. Tissue-engineered bone from BMP-2-transduced stem cells derived from human fat. Plastic and Reconstructive Surgery. 2005;115(6):1665–1673. doi: 10.1097/01.PRS.0000161459.90856.AB.
    1. García-Olmo D., Herreros D., De-La-Quintana P., et al. Adipose-derived stem cells in Crohn's rectovaginal fistula. Case Reports in Medicine. 2010;2010:3. doi: 10.1155/2010/961758.961758
    1. Pearl R. A., Leedham S. J., Pacifico M. D. The safety of autologous fat transfer in breast cancer: lessons from stem cell biology. Journal of Plastic, Reconstructive and Aesthetic Surgery. 2012;65(3):283–288. doi: 10.1016/j.bjps.2011.07.017.
    1. Hall B., Andreeff M., Marini F. The participation of mesenchymal stem cells in tumor stroma formation and their application as targeted-gene delivery vehicles. Handbook of Experimental Pharmacology. 2007;180:263–283. doi: 10.1007/978-3-540-68976-8-12.
    1. Sun B., Roh K.-H., Park J.-R., et al. Therapeutic potential of mesenchymal stromal cells in a mouse breast cancer metastasis model. Cytotherapy. 2009;11(3):289–298. doi: 10.1080/14653240902807026.
    1. Schweizer R., Tsuji W., Gorantla V. S., Marra K. G., Rubin J. P., Plock J. A. The role of adipose-derived stem cells in breast cancer progression and metastasis. Stem Cells International. 2015;2015:17. doi: 10.1155/2015/120949.120949

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj