Characterization of human adult stem-cell populations isolated from visceral and subcutaneous adipose tissue

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3494-3505

  Baglioni, Silvana ^a   Francalanci, Michela ^a   Squecco, Roberta ^a   Lombardi, Adriana ^a   Cantini, Giulia ^a   Angeli, Roberta ^a   Gelmini, Stefania ^a   Guasti, Daniele ^a   Benvenuti, Susanna ^a   Annunziato, Francesco ^a   Bani, Daniele ^a   Liotta, Francesco ^a   Francini, Fabio ^a   Perigli, Giuliano ^a   Serio, Mario ^a   Luconi, Michaela ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

ASCs; Immunophenotyping; Mesenchymal stromal cells; Multipotential differentiation

Indexed keywords

5' NUCLEOTIDASE; BETA1 INTEGRIN; CD14 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; ENDOGLIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HERMES ANTIGEN; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; THY 1 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ADIPOCYTE; ADIPOGENESIS; ADULT; ADULT STEM CELL; AGED; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL POPULATION; CHONDROGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; FEMALE; HISTOCHEMISTRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOPHENOTYPING; IN VITRO STUDY; INTRAABDOMINAL FAT; MALE; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NERVE CELL; OSTEOBLAST; POTASSIUM CURRENT; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; STROMA CELL; SUBCUTANEOUS FAT;

ADIPOSE TISSUE; ADULT STEM CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CELLS, CULTURED; COLON; HUMANS; PLURIPOTENT STEM CELLS; SKIN; VISCERA;

EID: 70349695700     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-126946     Document Type: Article

References (52)

1. Trayhurn, P., and Beattie, J. H. (2001) Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc. Nutr. Soc. 60, 329-339 (Pubitemid 32772448)
2. Fonseca-Alaniz, M. H., Takada, J., Alonso-Vale, M. I., and Lima, F. B. (2007) Adipose tissue as an endocrine organ: from theory to practice. J. Pediatr. 83, S192-S203
3. Von Eyben, F. E., Mouritsen, E., Holm, J., Montvilas, P., Dimcevski, G., Suciu, G., Helleberg, I., Kristensen, L., and von Eyben, R. (2003) Intra-abdominal obesity and metabolic risk factors: a study of young adults. Int. J. Obes. Relat. Metab. Disord. 27, 941-949 (Pubitemid 36918616)
4. Pou, K. M., Massaro, J. M., Hoffmann, U., Vasan, R. S., Maurovich-Horvat, P., Larson, M. G., Keaney, J.F. Jr., Meigs, J. B., Lipinska, I., Kathiresan, S., Murabito, J. M., O'Donnell, C. J., Benjamin, E. J., and Fox, C. S. (2007) Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation 116, 1234-1241 (Pubitemid 47517534)
5. Gronthos, S., Franklin, D. M., Leddy, H. A., Robey, P. G., Storms, R. W., and Gimble, J. M. (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell. Physiol. 189, 54-63 (Pubitemid 32830423)
6. Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., and Hedrick, M. H. (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211-228 (Pubitemid 32295155)
7. Mitchell, J. B., McIntosh, K., Zvonic, S., Garrett, S., Floyd, Z. E., Kloster, A., Di Halvorsen, Y., Storms, R. W., Goh, B., Kilroy, G., Wu, X., and Gimble, J. M. (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24, 376-385 (Pubitemid 44464807)
8. Liu, T. M., Martina, M., Hutmacher, D. W., Hui, J. H., Lee, E. H., and Lim, B. (2007) Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells 25, 750-760 (Pubitemid 46354235)
9. Zannettino, A. C., Paton, S., Arthur, A., Khor, F., Itescu, S., Gimble, J. M., and Gronthos, S. (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J. Cell. Physiol. 214, 413-421 (Pubitemid 350308998)
10. Krampera, M., Glennie, S., Dyson, J., Scott, D., Laylor, R., Simpson, E., and Dazzi, F. (2003) Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101, 3722-3729 (Pubitemid 36857965)
11. Benvenuti, S., Saccardi, R., Luciani, P., Urbani, S., Deledda, C., Cellai, I., Francini, F., Squecco, R., Rosati, F., Danza, G., Gelmini, S., Greve, I., Rossi, M., Maggi, R., Serio, M., and Peri, A. (2006) Neuronal differentiation of human mesenchymal stem cells: changes in the expression of the Alzheimer's disease-related gene seladin-1. Exp. Cell Res. 312, 2592-2604 (Pubitemid 44055932)
12. Formigli, L., Francini, F., Tani, A., Squecco, R., Nosi, D., Polidori, L., Nistri, S., Chiappini, L., Cesati, V., Pacini, A., Perna, A. M., Orlandini, G. E., Zecchi-Orlandini, S., and Bani, D. (2005) Morphofunctional integration between skeletal myoblasts and adult cardiomyocytes in coculture is favored by direct cell-cell contacts and relaxin treatment. Am. J. Physiol. Cell Physiol. 288, 795-804 (Pubitemid 40395057)
13. Sartiani, L., Bettiol, E., Stillitano, F., Mugelli, A., Cerbai, E., and Jaconi, M. E. (2007) Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 25, 1136-1144 (Pubitemid 46684873)
14. Lombardi, A., Cantini, G., Piscitelli, E., Gelmini, S., Francalanci, M., Mello, T., Ceni, E., Varano, G., Forti, G., Rotondi, M., Galli, A., Serio, M., and Luconi, M. (2008) A new mechanism involving ERK contributes to rosiglitazone inhibition of tumor necrosis factor-alpha and interferon-γ inflammatory effects in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28, 718-724 (Pubitemid 351651346)
15. Tricarico, C., Salvadori, B., Villari, D., Nicita, G., Della Melina, A., Pinzani, P., Ziche, M., and Pazzagli, M. (1999) Quantitative RT-PCR assay for VEGF mRNA in human tumors of the kidney. Int. J. Biol. Marker. 14, 247-250 (Pubitemid 30064177)
16. Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., and Hedrick, M. H. (2002) Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13, 4279-4295 (Pubitemid 35471185)
17. Halvorsen, Y. D., Bond, A., Sen, A., Franklin, D. M., Lea-Currie, Y. R., Sujkowski, D., Ellis, P. N., Wilkison, W. O., and Gimble, J. M. (2001) Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. Metabolism 50, 407-413 (Pubitemid 32327905)
18. Boushell, L. W., Kaku, M., Mochida, Y., Bagnell, R., and Yamauchi, M. (2008) Immunohistochemical localization of matrixmetalloproteinase- 2 in human coronal dentin. Arch. Oral. Biol. 53, 109-116 (Pubitemid 350296044)
19. Scriba, D., Aprath-Husmann, I., Blum, W. F., and Hauner, H. (2000) Catecholamines suppress leptin release from in vitro differentiated subcutaneous human adipocytes in primary culture via β1- and β2-adrenergic receptors. Eur. J. Endocrinol. 143, 439-445
20. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., and Marshak, D. R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147 (Pubitemid 29282067)
21. Kim, D. H., Yoo, K. H., Choi, K. S., Choi, J., Choi, S. Y., Yang, S. E., Yang, Y. S., Im, H. J., Kim, K. H., Jung, H. L., Sung, K. W., and Koo, H. H. (2005) Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 31, 119-126 (Pubitemid 40910227)
22. Aggarwal, S., and Pittenger, M. F. (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815-1822 (Pubitemid 40223708)
23. Sumanasinghe, R. D., Pfeiler, T. W., Monteiro-Riviere, N. A., and Loboa, E. G. (2009) Expression of proinflammatory cytokines by human mesenchymal stem cells in response to cyclic tensile strain. J. Cell. Physiol. 219, 77-83
24. Pasquinelli, G., Tazzari, P., Ricci, F., Vaselli, C., Buzzi, M., Conte, R., Orrico, C., Foroni, L., Stella, A., Alviano, F., Bagnara, G. P., and Lucarelli, E. (2007) Ultrastructural characteristics of human mesenchymal stromal (stem) cells derived from bone marrow and term placenta. Ultrastruct. Pathol. 31, 23-31 (Pubitemid 46555458)
25. Kilroy, G. E., Foster, S. J., Wu, X., Ruiz, J., Sherwood, S., Heifetz, A., Ludlow, J. W., Stricker, D. M., Potiny, S., Green, P., Halvorsen, Y. D., Cheatham, B., Storms, R. W., and Gimble, J. M. (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J. Cell. Physiol. 212, 702-709 (Pubitemid 47271882)
26. Noël, D., Caton, D., Roche, S., Bony, C., Lehmann, S., Casteilla, L., Jorgensen, C., and Cousin, B. (2008) Cell-specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp. Cell Res. 314, 1575-1584
27. Lapidus, L., Bengtsson, C., Larsson, B., Pennert, K., Rybo, E., and Sjöström, L. (1984) Distribution of adipose tissue and risk of cardiovascular disease and death: a 12-year follow up of participants in the population study of women in Gothenburg, Sweden. Br. Med. J. 289, 1257-1261 (Pubitemid 15217605)
28. Després, J. P. (2006) Is visceral obesity the cause of the metabolic syndrome? Ann. Med. 38, 52-63 (Pubitemid 43177788)
29. Barzilai, N., She, L., Liu, B. Q., Vuguin, P., Cohen, P., Wang, J., and Rossetti, L. (1999) Surgical removal of visceral fat reverses hepatic insulin resistance. Diabetes 48, 94-98 (Pubitemid 29019357)
30. Fujioka, S., Matsuzawa, Y., Tokunaga, K., Kawamoto, T., Kobatake, T., Keno, Y., Kotani, K., Yoshida, S., and Tarui, S. (1991) Improvement of glucose and lipid metabolism associated with selective reduction of intra-abdominal visceral fat in premenopausal women with visceral fat obesity. Int. J. Obes. 15, 853-859
31. Tchkonia, T., Giorgadze, N., Pirtskhalava, T., Tchoukalova, Y., Karagiannides, I., Forse, R. A., DePonte, M., Stevenson, M., Guo, W., Han, J., Waloga, G., Lash, T. L., Jensen, M. D., and Kirkland, J. L. (2002) Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am. J. Physiol. 282, R1286-R1296 (Pubitemid 34664512)
32. Tchkonia, T., Lenburg, M., Thomou, T., Giorgadze, N., Frampton, G., Pirtskhalava, T., Cartwright, A., Cartwright, M., Flanagan, J., Karagiannides, I., Gerry, N., Forse, R. A., Tchoukalova, Y., Jensen, M. D., Pothoulakis, C., and Kirkland, J. L. (2007) Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. Endocrinol. Metab. 292, E298-E307 (Pubitemid 46052953)
33. Van Harmelen, V., Röhrig, K., Hauner, H. (2004) Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects. Metabolism 53, 632-637 (Pubitemid 38596537)
34. Hauner, H., Wabitsch, M., and Pfeiffer, E. F. (1988) Differentiation of adipocyte precursor cells from obese and nonobese adult women and from different adipose tissue sites. Horm. Metab. Res. Suppl. 19, 35-39 (Pubitemid 19005619)
35. Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., Low, W. C., Largaespada, D. A., and Verfaillie, C. M. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49 (Pubitemid 34742565)
36. Wagner, W., Wein, F., Seckinger, A., Frankhauser, M., Wirkner, U., Krause, U., Blake, J., Schwager, C., Eckstein, V., Ansorge, W., and Ho, A. D. (2005) Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 33, 1402-1416 (Pubitemid 41541969)
37. McIntosh, K., Zvonic, S., Garrett, S., Mitchell, J. B., Floyd, Z. E., Hammill, L., Kloster, A., Di Halvorsen, Y., Ting, J. P., Storms, R. W., Goh, B., Kilroy, G., Wu, X., and Gimble, J. M. (2006) The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 24, 1246-1253 (Pubitemid 44464693)
38. Puissant, B., Barreau, C., Bourin, P., Clavel, C., Corre, J., Bousquet, C., Taureau, C., Cousin, B., Abbal, M., Laharrague, P., Penicaud, L., Casteilla, L., and Blancher, A. (2005) Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br. J. Haematol. 129, 118-129 (Pubitemid 40524060)
39. Sengenès, C., Lolmède, K., Zakaroff-Girard, A., Busse, R., and Bouloumié, A. (2005) Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J. Cell. Physiol. 205, 114-122
40. De Ugarte, D. A., Alfonso, Z., Zuk, P. A., Elbarbary, A., Zhu, M., Ashjian, P., Benhaim, P., Hedrick, M. H., and Fraser, J. K. (2003) Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol. Lett. 89, 267-270 (Pubitemid 37222456)
41. Sengenès, C., Miranville, A., Maumus, M., de Barros, S., Busse, R., and Bouloumié, A. (2007) Chemotaxis and differentiation of human adipose tissue CD34+/CD31-progenitor cells: role of stromal derived factor-1 released by adipose tissue capillary endothelial cells. Stem Cells 25, 2269-2276
42. Astori, G., Vignati, F., Bardelli, S., Tubio, M., Gola, M., Albertini, V., Bambi, F., Scali, G., Castelli, D., Rasini, V., Soldati, G., and Moccetti, T. (2007) "In vitro" and multicolor phenotypic characterization of cell subpopulations identified in fresh human adipose tissue stromal vascular fraction and in the derived mesenchymal stem cells. J. Transl. Med. 5, 55-65
43. Boquest, A. C., Noer, A., and Collas, P. (2006) Epigenetic programming of mesenchymal stem cells from human adipose tissue. Stem Cell Rev. 2, 319-329 (Pubitemid 47504962)
44. Pei, D. (2009) Regulation of pluripotency and reprogramming by transcription factors. J. Biol. Chem. 284, 3365-3369
45. Niwa, H., Miyazaki, J., and Smith, A. G. (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372-376 (Pubitemid 30187435)
46. Pan, G., Li, J., Zhou, Y., Zheng, H., and Pei, D. (2006) A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB J. 20, 1730-1732 (Pubitemid 44943786)
47. Bai, X., Ma, J., Pan, Z., Song, Y. H., Freyberg, S., Yan, Y., Vykoukal, D., and Alt, E. (2007) Electrophysiological properties of human adipose tissue-derived stem cells. Am. J. Physiol. Cell Physiol. 293, C1539-C1550 (Pubitemid 350085622)
48. Wang, K., Xue, T., Tsang, S. Y., Van Huizen, R., Wong, C. W., Lai, K. W., Ye, Z., Cheng, L., Au, K. W., Zhang, J., Li, G. R., Lau, C. P., Tse, H. F., and Li, R. A. (2005) Electrophysiological properties of pluripotent human and mouse embryonic stem cells. Stem Cells 23, 1526-1534 (Pubitemid 41741001)
49. Park, K. S., Jung, K. H., Kim, S. H., Kim, K. S., Choi, M. R., Kim, Y., and Chai, Y. G. (2007) Functional expression of ion channels in mesenchymal stem cells derived from umbilical cord vein. Stem Cells 25, 2044-2052 (Pubitemid 47258182)
50. Mantovani, G., Bondioni, S., Alberti, L., Gilardini, L., Invitti, C., Corbetta, S., Zappa, M. A., Ferrero, S., Lania, A. G., Bosari, S., Beck-Peccoz, P., Spada, A. (2009) Protein kinase A regulatory subunits in human adipose tissue: decreased R2B expression and activity in adipocytes from obese subjects. Diabetes 58, 620-626
51. Lu, P., Blesch, A., and Tuszynski, M. H. (2004) Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J. Neurosci. Res. 15, 174-191 (Pubitemid 38859403)
52. Mizuno, H., Zuk, P. A., Zhu, M., Lorenz, H. P., Benhaim, P., and Hedrick, M. H. (2002) Myogenic differentiation by human processed lipoaspirate cells. Plast. Reconstr. Surg. 109, 199-209 (Pubitemid 34056677)