A new nonenzymatic method and device to obtain a fat tissue derivative highly enriched in pericyte-like elements by mild mechanical forces from human lipoaspirates

Cell Transplantation

Volumn 22, Issue 11, 2013, Pages 2063-2077

  Bianchi, Francesca ^a,b   Maioli, Margherita ^a,c   Leonardi, Erika ^d   Olivi, Elena ^a,b   Pasquinelli, Gianandrea ^e   Valente, Sabrina ^e   Mendez, Armando J ^d   Ricordi, Camillo ^d   Raffaini, Mirco ^f   Tremolada, Carlo ^f   Ventura, Carlo ^a,b  

^a NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF SASSARI   (Italy)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF BOLOGNA   (Italy)

^f Division of Immunology Transplantation and Infectious Diseases   (Italy)

Author keywords

Adipose tissue; Lipoaspirates; Nonenzymatic isolation; Stem cells; Stromal vascular architecture

Indexed keywords

COLLAGENASE; TISSUE CULTURE MEDIUM; ACTA2 PROTEIN, HUMAN; ACTIN; BIOLOGICAL MARKER; COLLAGEN; PROTEIN S 100;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ARTICLE; BIOTECHNOLOGY; BONE DEVELOPMENT; CADAVER; CAPILLARY; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CHONDROGENESIS; CRYOPRESERVATION; FLOW CYTOMETRY; FORCE; HEMATOPOIESIS; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; PERICYTE; PRIORITY JOURNAL; STROMA; VASCULAR TISSUE; CELL SEPARATION; CYTOLOGY; DEVICES; MECHANICAL STRESS; METABOLISM; PATHOLOGY; PHENOTYPE; PROCEDURES;

ACTINS; ADIPOCYTES; ADIPOSE TISSUE; BIOLOGICAL MARKERS; CADAVER; CELL SEPARATION; COLLAGEN; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; PERICYTES; PHENOTYPE; S100 PROTEINS; STRESS, MECHANICAL;

EID: 84886440936     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X657855     Document Type: Article

References (64)

1. Abderrahim-Ferkoune, A.; Bezy, O.; Astri-Roques, S.; Elabd, C.; Ailhaud, G.; Amri, E. Z. Transdifferentiation of preadipose cells into smooth muscle-like cells: Role of aortic carboxypeptidase-like protein. Exp. Cell Res. 293(2):219-228; 2004
2. Banfi, A.; Bianchi, G.; Galotto, M.; Cancedda, R.; Quarto, R. Bone marrow stromal damage after chemo/radiotherapy: Occurrence, consequences and possibilities of treatment. Leuk. Lymphoma 42(5):863-870; 2001
3. Bonaros, N.; Rauf, R.; Schachner, T.; Laufer, G.; Kocher, A. Enhanced cell therapy for ischemic heart disease. Transplantation 86(9):1151-1160; 2008
4. Burks, C. A.; Bundy, K.; Fotuhi, P.; Alt, E. Characterization of 75:25 poly(llactide-co-epsilon-caprolactone) thin films for the endoluminal delivery of adipose-derived stem cells to abdominal aortic aneurysms. Tissue Eng. 12(9):2591-2600; 2006
5. Cao, Y.; Sun, Z.; Liao, L.; Meng, Y.; Han, Q.; Zhao, R. C. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem. Biophys. Res. Commun. 332(2):370-379; 2005
6. Caplan, A. I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 213(2):341-347; 2007
7. Caplan, A. I.; Dennis, J. E. Mesenchymal stem cells as trophic mediators. J. Cell. Biochem. 98(5):1076-1084; 2006
8. Cavallari, G.; Olivi, E.; Bianchi, F.; Neri, F.; Foroni, L.; Valente, S.; Manna, G. L.; Nardo, B.; Stefoni, S.; Ventura, C. Mesenchymal stem cells and islet cotransplantation in diabetic rats: Improved islet graft revascularization and function by human adipose tissue-derived stem cells preconditioned with natural molecules. Cell Transplant. 21(12):2771-2781; 2012
9. Corre, J.; Barreau, C.; Cousin, B.; Chavoin, J. P.; Caton, D.; Fournial, G.; Penicaud, L.; Casteilla, L.; Laharrague, P. Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J. Cell. Physiol. 208(2):282-288; 2006
10. De Miguel, M. P.; Fuentes-Julián, S.; Blázquez-Martínez, A.; Pascual, C. Y.; Aller, M. A.; Arias, J.; Arnalich-Montiel, F. Immunosuppressive properties of mesenchymal stem cells: Advances and applications. Curr. Mol. Med. 12(5):574-591; 2012
11. De Ugarte, D. A.; Alfonso, Z.; Zuk, P. A.; Elbarbary, A.; Zhu, M.; Ashjian, P.; Benhaim, P.; Hedrick, M. H.; Fraser, J. K. Differential expression of stem cell mobilization- associated molecules on multilineage cells from adipose tissue and bone marrow. Immunol. Lett. 89(2-3):267-270; 2003
12. De Ugarte, D. A.; Morizono, K.; Elbarbary, A.; Alfonso, Z.; Zuk, P. A.; Zhu, M.; Dragoo, J. L.; Ashjian, P.; Thomas, B.; Benhaim, P.; Chen, I.; Fraser, J.; Hedrick, M. H. Comparison of multilineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174(3):101-109; 2003
13. D'Ippolito, G.; Schiller, P. C.; Ricordi, C.; Roos, B. A.; Howard, G. A. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J. Bone. Miner. Res. 14(7):1115-1122; 1999
14. Erickson, G. R.; Gimble, J. M.; Franklin, D. M.; Rice, H. E.; Awad, H.; Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290(2):763-769; 2002
15. Fraser, J. K.; Schreiber, R.; Strem, B.; Zhu, M.; Alfonso, Z.; Wulur, I.; Hedrick, M. H. Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat. Clin. Pract. Cardiovasc. Med. 3 Suppl. 1:S33-S37; 2006
16. Gagnon, A.; Abaiian, K. J.; Crapper, T.; Layne, M. D.; Sorisky, A. Downregulation of aortic carboxypeptidase-like protein during the early phase of 3t3-l1 adipogenesis. Endocrinology 143(7):2478-2485; 2002
17. Gimble, J. M.; Guilak, F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr. Top. Dev. Biol. 58:137-160; 2003
18. Halvorsen, Y. C.; Wilkison, W. O.; Gimble, J. M. Adiposederived stromal cells-their utility and potential in bone formation. Int. J. Obes. Relat. Metab. Disord. 24(suppl 4): S41-S44; 2000
19. Halvorsen, Y. D.; Bond, A.; Sen, A.; Franklin, D. M.; Lea- Currie, Y. R.; Sujkowski, D.; Ellis, P. N.; Wilkison, W. O.; Gimble, J. M. Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: Biochemical, cellular, and molecular analysis. Metabolism 50(4):407-413; 2001
20. Halvorsen, Y. D.; Franklin, D.; Bond, A. L.; Hitt, D. C.; Auchter, C.; Boskey, A. L.; Paschalis, E. P.; Wilkison, W. O.; Gimble, J. M. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissuederived stromal cells. Tissue Eng. 7(6):729-741; 2001
21. Huang, J. I.; Beanes, S. R.; Zhu, M.; Lorenz, H. P.; Hedrick, M. H.; Benhaim, P. Rat extramedullary adipose tissue as a source of osteochondrogenic progenitor cells. Plast. Reconstr. Surg. 109(3):1033-1041; 2002
22. Jack, G. S.; Almeida, F. G.; Zhang, R.; Alfonso, Z. C.; Zuk, P. A.; Rodriguez, L. V. Processed lipoaspirate cells for tissue engineering of the lower urinary tract: Implications for the treatment of stress urinary incontinence and bladder reconstruction. J. Urol. 174(5):2041-2045; 2005
23. Jeon, E. S.; Moon, H. J.; Lee, M. J.; Song, H. Y.; Kim, Y. M.; Bae, Y. C.; Jung, J. S.; Kim, J. H. Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a tgf-{b}-dependent mechanism. J. Cell Sci. 119(Pt 23):4994-5005; 2006
24. Kang, S. K.; Putnam, L. A.; Ylostalo, J.; Popescu, I. R.; Dufour, J.; Belousov, A.; Bunnell, B. A. Neurogenesis of rhesus adipose stromal cells. J. Cell Sci. 117(Pt 18):4289-4299; 2004
25. Kassem, M.; Abdallah, B. M. Human bone-marrow-derived mesenchymal stem cells: Biological characteristics and potential role in therapy of degenerative diseases. Cell Tissue Res. 331(1):157-163; 2008
26. Katz, A. J.; Zang, Z.; Shang, H.; Chamberlain, A. T.; Berr, S. S.; Roy, R. J.; Khurgel, M.; Epstein, F. H.; French, B. A. Serial MRI assessment of human adipose-derived stem cells (HASCS) in a murine model of reperfused myocardial infarction. Adipocytes 2(1):1-10; 2006
27. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Shou, M.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein S. E. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 109(12):1543-1549; 2004
28. Krampera, M.; Marconi, S.; Pasini, A.; Galie, M.; Rigotti, G.; Mosna, F.; Tinelli, M.; Lovato, L.; Anghileri, E.; Andreini, A.; Pizzolo, G.; Sbarbati, A.; Bonetti, B. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 40(2):382-390; 2007
29. Lee, J. H.; Kemp, D. M. Human adipose-derived stem cells display myogenic potential and perturbed function in hypoxic conditions. Biochem. Biophys. Res. Commun. 341(3):882-888; 2006
30. Lee, W. C.; Maul, T. M.; Vorp, D. A.; Rubin, J. P.; Marra, K. G. Effects of uniaxial cyclic strain on adipose-derived stem cell morphology, proliferation, and differentiation. Biomech. Model Mechanobiol. 6(4):265-273; 2007
31. Lee, W. C.; Rubin, J. P.; Marra, K. G. Regulation of alphasmooth muscle actin protein expression in adipose-derived stem cells. Cells Tissues Organs 183(2):80-86; 2006
32. Mangi, A. A.; Noiseux, N.; Kong, D.; He, H.; Rezvani, M.; Ingwall, J. S.; Dzau, V. J. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9(9):1195-201; 2003
33. Miranville, A.; Heeschen, C.; Sengenes, C.; Curat, C. A.; Busse, R.; Bouloumie, A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110(3):349-355; 2004
34. Miyahara, Y.; Nagaya, N.; Kataoka, M.; Yanagawa, B.; Tanaka, K.; Hao, H.; Ishino, K.; Ishida, H.; Shimizu, T.; Kangawa, K.; Sano, S.; Okano, T.; Kitamura, S.; Mori, H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12(4):459-465; 2006
35. Mizuno, H.; Zuk, P. A.; Zhu, M.; Lorenz, H. P.; Benhaim, P.; Hedrick, M. H. Myogenic differentiation by human processed lipoaspirate cells. Plast. Reconstr. Surg. 109(1):199-209; 2002
36. Muschler, G. F.; Nitto, H.; Boehm, C. A.; Easley, K. A. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J. Orthop. Res. 19(1):117-125; 2001
37. Nakagami, H.; Morishita, R.; Maeda, K.; Kikuchi, Y.; Ogihara, T.; Kaneda, Y. Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J. Atheroscler. Thromb. 13(2):77-81; 2006
38. Olson, L. E.; Soriano, P. PDGFRb signaling regulates mural cell plasticity and inhibits fat development. Dev. Cell 20(6):815-826; 2011
39. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29(9):e45; 2001
40. Planat-Benard, V.; Silvestre, J. S.; Cousin, B.; Andre, M.; Nibbelink, M.; Tamarat, R.; Clergue, M.; Manneville, C.; Saillan-Barreau, C.; Duriez, M.; Tedgui, A.; Levy, B.; Penicaud, L.; Casteilla, L. Plasticity of human adipose lineage cells toward endothelial cells: Physiological and therapeutic perspectives. Circulation 109(5):656-663; 2004
41. Rehman, J.; Traktuev, D.; Li, J.; Merfeld-Clauss, S.; Temm- Grove, C. J.; Bovenkerk, J. E.; Pell, C. L.; Johnstone, B. H.; Considine, R. V.; March, K. L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109(10):1292-1298; 2004
42. Roseti, L.; Serra, M.; Tigani, D.; Brognara, I.; Lopriore, A.; Bassi, A.; Fornasari, P. M. Cell manipulation in autologous chondrocyte implantation: From research to cleanroom. Chir. Organi. Mov. 91(3):147-151; 2008
43. Safford, K. M.; Hicok, K. C.; Safford, S. D.; Halvorsen, Y. D.; Wilkison, W. O.; Gimble, J. M.; Rice, H. E. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294(2): 371-379; 2002
44. Safford, K. M.; Rice, H. E. Stem cell therapy for neurologic disorders: Therapeutic potential of adipose-derived stem cells. Curr. Drug Targets 6(1):57-62; 2005
45. Safford, K. M.; Safford, S. D.; Gimble, J. M.; Shetty, A. K.; Rice, H. E. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp. Neurol. 187(2):319-328; 2004
46. Satija, N. K.; Singh, V. K.; Verma, Y. K.; Gupta, P.; Sharma, S.; Afrin, F.; Sharma, M.; Sharma, P.; Tripathi, R. P.; Gurudutta, G. U. Mesenchymal stem cell-based therapy: A new paradigm in regenerative medicine. J. Cell. Mol. Med. 13(11-12):4385-402; 2009
47. Sen, A.; Lea-Currie, Y. R.; Sujkowska, D.; Franklin, D. M.; Wilkison, W. O.; Halvorsen, Y. D.; Gimble, J. M. Adipogenic potential of human adipose derived stromal cells from multiple donors is heterogeneous. J. Cell. Biochem. 81(2):312-319; 2001
48. Sengenes, C.; Lolmede, K.; Zakaroff-Girard, A.; Busse, R.; Bouloumie, A. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J. Cell. Physiol. 205(1):114-122; 2005
49. Seo, M. J.; Suh, S. Y.; Bae, Y. C.; Jung, J. S. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem. Biophys. Res. Commun. 328(1):258-264; 2005
50. Song, Y. H.; Gehmert, S.; Sadat, S.; Pinkernell, K.; Bai, X.; Matthias, N.; Alt, E. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 354(4):999-1003; 2007
51. Stolzing, A.; Jones, E.; McGonagle, D.; Scutt, A. Agerelated changes in human bone marrow-derived mesenchymal stem cells: Consequences for cell therapies. Mech. Ageing Dev. 129(3):163-173; 2008
52. Strem, B. M.; Hicok, K. C.; Zhu, M.; Wulur, I.; Alfonso, Z.; Schreiber, R. E.; Fraser, J. K.; Hedrick, M. H. Multipotential differentiation of adipose tissue-derived stem cells. Keio J. Med. 54(3):132-141; 2005
53. Strem, B. M.; Zhu, M.; Alfonso, Z.; Daniels, E. J.; Schreiber, R.; Beygui, R.; MacLellan, W. R.; Hedrick, M. H.; Fraser, J. K. Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7(3):282-291; 2005
54. Talens-Visconti, R.; Bonora, A.; Jover, R.; Mirabet, V.; Carbonell, F.; Castell, J. V.; Gomez-Lechon, M. J. Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J. Gastroenterol. 12(36):5834-5845; 2006
55. Talens-Visconti, R.; Bonora, A.; Jover, R.; Mirabet, V.; Carbonell, F.; Castell, J. V.; Gomez-Lechon, M. J. Human mesenchymal stem cells from adipose tissue: Differentiation into hepatic lineage. Toxicol. In Vitro 21(2):324-329; 2007
56. Timper, K.; Seboek D.; Eberhardt, M.; Linscheid, P.; Christ- Crain, M.; Keller, U.; Muller, B.; Zulewski, H. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagons expressing cells. Biochem. Biophys. Res. Commun. 341(4):1135-1140; 2006
57. Tremolada, C.; Palmieri, G.; Ricordi, C. Adipocyte transplantation and stem cells: Plastic surgery meets regenerative medicine. Cell Transplant. 19(10):1217-1223; 2010
58. Ventura, C.; Cantoni, S.; Bianchi, F.; Lionetti, V.; Cavallini, C.; Scarlata, I.; Foroni, L.; Maioli, M.; Bonsi, L.; Alviano, F.; Fossati, V.; Bagnara, G. P.; Pasquinelli, G.; Recchia, F. A.; Perbellini, A. Hyaluronan mixed esters of butyric and retinoic Acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J. Biol. Chem. 282(19):14243-4252; 2007.
59. Wickham, M. Q.; Erickson, G. R.; Gimble J. M.; Vail, T. P.; Guilak, F. Multipotent stromal cells derived from the infrapatellar fat pad of the knee. Clin. Orthop. Relat. Res. 412:196-212; 2003
60. Yamada, Y.; Wang, X. D.; Yokoyama, S.; Fukuda, N.; Takakura, N. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem. Biophys. Res. Commun. 342(2):662-670; 2006
61. Yoshimura, K.; Shigeura, T.; Matsumoto, D.; Sato, T.; Takaki, Y.; Aiba-Kojima, E.; Sato, K.; Inoue, K.; Nagase, T.; Koshima, I.; Gonda, K. Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J. Cell. Physiol. 208(1):64-76; 2006
62. Zimmerlin, L.; Donnenberg, V. S.; Pfeifer, M. E.; Meyer, E. M.; Péault, B.; Rubin, J. P.; Donnenberg, A. D. Stromal vascular progenitors in adult human adipose tissue. Cytometry A. 77(1):22-30; 2010
63. Zuk, P. A.; Zhu, M.; Ashjian, P.; De Ugarte, D. A.; Huang, J. I.; Mizuno, H.; Alfonso, Z. C.; Fraser, J. K.; Benhaim, P.; Hedrick, M. H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13(12):4279-4295; 2002
64. Zuk, P. A.; Zhu, M.; Mizuno, H.; Huang, J.; Futrell, J. W.; Katz, A. J.; Benhaim, P.; Lorenz, H. P.; Hedrick, M. H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 7(2):211-228; 2001.