Adipose-derived stromal/stem cells: A primer

Organogenesis

Volumn 9, Issue 1, 2013, Pages 3-10

  Gimble, Jeffrey M ^a,b,c   Bunnell, Bruce A ^b   Frazier, Trivia ^a   Rowan, Brian ^c   Shah, Forum ^b   Thomas Porch, Caasy ^d   Wu, Xiying ^b  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b LaCell LLC   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TULANE UNIVERSITY   (United States)

Author keywords

Adipokine; Adipose Stromal stem Cells; Experimental Autoimmune Encephalitis; Hematopoietic Stem and Progenitor Cell; Mesenchymal Stem Cell or Multipotent Stromal Cell; Progressive Osseous Heteroplasia

Indexed keywords

INTERLEUKIN 6; UNCOUPLING PROTEIN 1; ADIPOCYTOKINE;

ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; APOPTOSIS; BLOODBORNE BACTERIUM; BROWN ADIPOSE TISSUE; CELL COMPONENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL RENEWAL; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL CULTURE; IMMUNOMODULATION; INNATE IMMUNITY; LIPOSUCTION; LYMPHOCYTE; LYMPHOCYTE SUBPOPULATION; MITOCHONDRIAL MEMBRANE; NONHUMAN; OBESITY; OSTEOCLAST; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; REVIEW; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TRYPTOPHAN METABOLISM; WHITE ADIPOSE TISSUE; ADIPOSE STROMAL/STEM CELLS; ANIMAL; CYTOLOGY; EXPERIMENTAL AUTOIMMUNE ENCEPHALITIS; HEMATOPOIETIC STEM AND PROGENITOR CELL; IMMUNOLOGY; MESENCHYMAL STEM CELL OR MULTIPOTENT STROMAL CELL; PROGRESSIVE OSSEOUS HETEROPLASIA; STEM CELL; STROMA CELL; TUMOR MICROENVIRONMENT;

ADIPOKINE; ADIPOSE STROMAL/STEM CELLS; EXPERIMENTAL AUTOIMMUNE ENCEPHALITIS; HEMATOPOIETIC STEM AND PROGENITOR CELL; MESENCHYMAL STEM CELL OR MULTIPOTENT STROMAL CELL; PROGRESSIVE OSSEOUS HETEROPLASIA;

ADIPOSE TISSUE; ANIMALS; CELLULAR MICROENVIRONMENT; HUMANS; IMMUNOMODULATION; STEM CELL TRANSPLANTATION; STEM CELLS; STROMAL CELLS;

EID: 84876525239     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.24279     Document Type: Review

References (69)

1. Eddy MC, Jan De Beur SM, Yandow SM, McAlister WH, Shore EM, Kaplan FS, et al. Deficiency of the alpha-subunit of the stimulatory G protein and severe extraskeletal ossification. J Bone Miner Res 2000; 15:2074-83; PMID:11092390; http://dx.doi.org/10.1359/jbmr.2000.15.11.2074.
2. Friedenstein AJ. Precursor cells of mechanocytes. Int Rev Cytol 1976; 47:327-59; PMID:11195; http://dx.doi.org/10.1016/S0074-7696(08)60092-3.
3. Owen M. Marrow stromal stem cells. J Cell Sci Suppl 1988; 10:63-76; PMID:3077943. (Pubitemid 19096575)
4. Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 1988; 136:42-60; PMID:3068016.
5. Haynesworth SE, Baber MA, Caplan AI. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 1992; 13:69-80; PMID:1316137; http://dx.doi.org/10.1016/8756-3282(92)90363-2.
6. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9:641-50; PMID:1870029; http://dx.doi.org/10.1002/jor.1100090504.
7. Dennis JE, Haynesworth SE, Young RG, Caplan AI. Osteogenesis in marrow-derived mesenchymal cell porous ceramic composites transplanted sub-cutaneously: effect of fibronectin and laminin on cell retention and rate of osteogenic expression. Cell Transplant 1992; 1:23-32; PMID:1344289.
8. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchy-mal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8:315-7; PMID:16923606; http://dx.doi.org/10.1080/14653240600855905. (Pubitemid 44269669)
9. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, et al. International Society for Cellular Therapy. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005; 7:393-5; PMID:16236628; http://dx.doi.org/10.1080/14653240500319234. (Pubitemid 41671625)
10. Singer NG, Caplan AI. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 2011; 6:457-78; PMID:21073342; http://dx.doi.org/10.114 6/annure v-pathol-011110-130230.
11. Gimble JM, Bunnell BA, Chiu ES, Guilak F. Concise review: Adipose-derived stromal vascular fraction cells and stem cells: let's not get lost in translation. Stem Cells 2011; 29:749-54; PMID:21433220; http://dx.doi.org/10. 1002/stem.629.
12. Cawthorn WP, Scheller EL, MacDougald OA. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J Lipid Res 2012; 53:227-46; PMID:22140268; http://dx.doi.org/10.1194/jlr.R021089.
13. Trayhurn P, Wood IS. Signalling role of adipose tissue: adipokines and inflammation in obesity. Biochem Soc Trans 2005; 33:1078-81; PMID:16246049; http://dx.doi.org/10.1042/BST20051078. (Pubitemid 41659117)
14. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 1994; 372:425-32; PMID:7984236; http://dx.doi.org/10.1038/372425a0. (Pubitemid 24365442)
15. Bray GA, Bellanger T. Epidemiology, trends, and morbidities of obesity and the metabolic syndrome. Endocrine 2006; 29:109-17; PMID:16622298; http://dx.doi.org/10.1385/ENDO:29:1:109. (Pubitemid 43780352)
16. Seale P. Transcriptional control of brown adipocyte development and thermogenesis. Int J Obes (Lond) 2010; 34(Suppl 1):S17-22; PMID:20935660; http://dx.doi.org/10.1038/ijo.2010.178.
17. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008; 454:961-7; PMID:18719582; http://dx.doi.org/10.1038/nature07182.
18. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, et al. Prdm16 determines the ther-mogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 2011; 121:96-105; PMID:21123942; http://dx.doi.org/10. 1172/JCI44271.
19. Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012; 150:366-76; PMID:22796012; http://dx.doi.org/10.1016/j.cell.2012.05.016.
20. Rodbell M. Metabolism of Isolated Fat Cells. I. Effects of Hormones on Glucose Metabolism and Lipolysis. J Biol Chem 1964; 239:375-80; PMID:14169133.
21. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007; 100:1249-60; PMID:17495232; http://dx.doi.org/10.1161/01.RES.0000265074.83288.09. (Pubitemid 46742916)
22. Mitchell JBMK, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, et al. Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 2006; 24:376-85; PMID:16322640; http://dx.doi.org/10.1634/stemcells.2005-0234. (Pubitemid 44464807)
23. Yu GWX, Wu X, Dietrich MA, Polk P, Scott LK, Ptitsyn AA, et al. Yield and characterization of subcutaneous human adipose-derived stem cells by flow cytometric and adipogenic mRNA analyzes. Cytotherapy 2010; 12:538-46; PMID:20380539; http://dx.doi.org/10.3109/14653241003649528.
24. Bourin PBB, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, et al. Stromal cells from the adipose derived stromal vascular fraction (SVF) and cultured adipose-derived stromal/stem cells (ASC): a joint statement of IFATS and ISCT. Cytotherapy, In press.
25. Hicok KC, Hedrick MH. Automated isolation and processing of adipose-derived stem and regenerative cells. Methods Mol Biol 2011; 702:87-105; PMID:21082397; http://dx.doi.org/10.1007/978-1-61737-960-4- 8.
26. Cousin B, André M, Arnaud E, Pénicaud L, Casteilla L. Reconstitution of lethally irradiated mice by cells isolated from adipose tissue. Biochem Biophys Res Commun 2003; 301:1016-22; PMID:12589814; http://dx.doi.org/10.1016/S0006-291X(03)00061-5. (Pubitemid 36279214)
27. Poglio S, De Toni-Costes F, Arnaud E, Laharrague P, Espinosa E, Casteilla L, et al. Adipose tissue as a dedicated reservoir of functional mast cell progenitors. Stem Cells 2010 ; 28:2065-72; PMID:20845475; http://dx.doi.org/10. 1002/stem.523.
28. Han J, Koh YJ, Moon HR, Ryoo HG, Cho CH, Kim I, et al. Adipose tissue is an extramedullary reservoir for functional hematopoietic stem and progenitor cells. Blood 2010; 115:957-64; PMID:19897586; http://dx.doi.org/10.1182/blood- 2009-05-219923.
29. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112:1796-808; PMID:14679176. (Pubitemid 38063703)
30. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112:1821-30; P M I D:14 67917 7. (Pubitemid 38063705)
31. Aron-Wisnewsky J, Tordjman J, Poitou C, Darakhshan F, Hugol D, Basdevant A, et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab 2009; 94:4619-23; PMID:19837929; http://dx.doi.org/10.1210/jc.2009-0925.
32. Yang H, Youm YH, Vandanmagsar B, Ravussin A, Gimble JM, Greenway F, et al. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J Immunol 2010; 185:1836-45; PMID:20581149; http://dx.doi.org/10.4049/jimmu-nol.1000021.
33. Caspar-Bauguil S, Cousin B, Bour S, Casteilla L, Penicaud L, Carpéné C. Adipose tissue lymphocytes: types and roles. J Physiol Biochem 2009; 65:423-36; PMID:20358356; http://dx.doi.org/10.1007/BF03185938.
34. Corre J, Barreau C, Cousin B, Chavoin JP, Caton D, Fournial G, et al. Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J Cell Physiol 2006; 208:282-8; PMID:16619234; http://dx.doi.org/10.1002/jcp.20655. (Pubitemid 43993418)
35. Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, et al. Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hemato-poietic, and pro-inflammatory factors. J Cell Physiol 2007; 212:702-9; PMID:17477371; http://dx.doi.org/10.1002/jcp.21068. (Pubitemid 47271882)
36. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005; 129:118-29; PMID:15801964; htt p://d x.doi.org/10.1111/j.1365-2141.20 05.054 09.x. (Pubitemid 40524060)
37. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, et al. The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 2006; 24:1246-53; PMID:16410391; http://dx.doi.org/10.1634/stemcells. 2005-0235. (Pubitemid 44464693)
38. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng 2007; 13:1185-95; PMID:17518704; http://dx.doi.org/10.1089/ten.2006. 0315. (Pubitemid 46986719)
39. McIntosh KR, Frazier T, Rowan BG, Gimble JM. Evolution and future prospects of adipose-derived immunomodulatory cell therapeutics. Expert Rev Clin Immunol 2013; 9:175-84; PMID:23390948; http://dx.doi.org/10.1586/eci.12.96.
40. Crop MJ, Baan CC, Korevaar SS, Ijzermans JN, Pescatori M, Stubbs A P, et al. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clin Exp Immunol 2010 ; 162:474-86; PMID: 20846162 ; http://d x.doi.org/10.1111/j.1365-2249.2010.04256.x.
41. Crop MJ, Baan CC, Korevaar SS, Ijzermans JN, Weimar W, Hoogduijn MJ. Human adipose tissue-derived mesenchymal stem cells induce explosive T-cell proliferation. Stem Cells Dev 2010; 19:1843-53; PMID:20367242; http://dx.doi.org/10.1089/scd.2009.0368.
42. Shi D, Liao L, Zhang B, Liu R, Dou X, Li J, et al. Human adipose tissue-derived mesenchymal stem cells facilitate the immunosuppressive effect of cyclosporin A on T lymphocytes through Jagged-1-mediated inhibition of NF-κB signaling. Exp Hematol 2011; 39:214-24, e1; PMID:21078360; http://dx.doi.org/10.1016/j.exphem.2010.10.009.
43. Kronsteiner B, Wolbank S, Peterbauer A, Hackl C, Redl H, van Griensven M, et al. Human mesen-chymal stem cells from adipose tissue and amnion influence T-cells depending on stimulation method and presence of other immune cells. Stem Cells Dev 2011; 20:2115-26; PMID:21381973; http://dx.doi.org/10.1089/scd.2011. 0031.
44. Yañez R, Oviedo A, Aldea M, Bueren JA, Lamana ML. Prostaglandin E2 plays a key role in the immu-nosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 2010; 316:3109-23; PMID:20804749; http://dx.doi.org/10.1016/j.yexcr.2010.08.008.
45. Yañez R, Lamana ML, García-Castro J, Colmenero I, Ramírez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosup-pressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006; 24:2582-91; PMID:16873762; http://dx.doi.org/10.1634/stemcells.2006-0228. (Pubitemid 44674320)
46. Cho KS, Park HK, Park HY, Jung JS, Jeon SG, Kim YK, et al. IFATS collection: Immunomodulatory effects of adipose tissue-derived stem cells in an allergic rhinitis mouse model. Stem Cells 2009; 27:259-65; PMID:18832595; http://dx.doi.org/10.1634/stemcells.2008-0283.
47. González MA, Gonzalez-Rey E, Rico L, Büscher D, Delgado M. Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum 2009; 60:1006-19; PMID:19333946; http://dx.doi.org/10.1002/art.24405.
48. Choi EW, Shin IS, Park SY, Park JH, Kim JS, Yoon EJ, et al. Reversal of serologic, immunologic, and his-tologic dysfunction in mice with systemic lupus ery-thematosus by long-term serial adipose tissue-derived mesenchymal stem cell transplantation. Arthritis Rheum 2012; 64:243-53; PMID:21904997; http://dx.doi.org/10.1002/art.33313.
49. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 2009; 27:2624-35; PMID:19676124; http://dx.doi.org/10.1002/stem.194.
50. Gimble JM, Bunnell BA, Casteilla L, Jung JS, Yoshimura K. Phases I-III Clinical Trials Using Adult Stem Cells. Stem Cells Int 2011; 2010:604713; PMID:21461337.
51. Mesimäki K, Lindroos B, Törnwall J, Mauno J, Lindqvist C, Kontio R, et al. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg 2009; 38:201-9; PMID:19168327; http://dx.doi.org/10.1016/j.ijom.2009.01.001.
52. Thesleff T, Lehtimäki K, Niskakangas T, Mannerström B, Miettinen S, Suuronen R, et al. Cranioplasty with adipose-derived stem cells and biomaterial: a novel method for cranial reconstruction. Neurosurgery 2011; 68:1535-40; PMID:21336223; http://dx.doi.org/10.1227/NEU.0b013e31820ee24e.
53. Lendeckel S, Jödicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg 2004; 32:370-3; PMID:15555520; http://dx.doi.org/10.1016/j.jcms.2004.06.002. (Pubitemid 40045639)
54. Ruiz JC, Ludlow JW, Sherwood S, Yu G, Wu X, Gimble JM. Differentiated human adipose-derived stem cells exhibit hepatogenic capability in vitro and in vivo. J Cell Physiol 2010; 225:429-36; PMID:20458738; http://dx.doi.org/10.1002/ jcp.22216.
55. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7:211-28; PMID:11304456; http://dx.doi.org/10.1089/ 107632701300062859. (Pubitemid 32295155)
56. Planat-Bénard V, Menard C, André M, Puceat M, Perez A, Garcia-Verdugo JM, et al. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 2004; 94:223-9; PMID:14656930; http://dx.doi.org/10.1161/01. RES.0000109792.43271.47. (Pubitemid 38197455)
57. Baer PC, Brzoska M, Geiger H. Epithelial differentiation of human adipose-derived stem cells. Methods Mol Biol 2011; 702:289-98; PMID:21082410; http://dx.doi.org/10.1007/978-1-61737-960-4-21.
58. Brzoska M, Geiger H, Gauer S, Baer P. Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun 2005; 330:142-50; PMID:15781243; http://dx.doi.org/10.1016/j.bbrc.2005.02.141. (Pubitemid 40394946)
59. Pelton PD, Zhou L, Demarest KT, Burris TP. PPARgamma activation induces the expression of the adipocyte fatty acid binding protein gene in human monocytes. Biochem Biophys Res Commun 1999; 261:456-8; PMID:10425206; http://dx.doi.org/10.1006/bbrc.1999.1071. (Pubitemid 29392497)
60. Cousin B, André M, Casteilla L, Pénicaud L. Altered macrophage-like functions of pre-adipocytes in inflammation and genetic obesity. J Cell Physiol 2001; 186:380-6; PMID:11169977; http://dx.doi.org/10.1002/1097- 4652(2001)9999:9999000::AID-JCP10383.0.CO;2-T. (Pubitemid 32147721)
61. Levi B, James AW, Nelson ER, Vistnes D, Wu B, Lee M, et al. Human adipose derived stromal cells heal critical size mouse calvarial defects. PLoS One 2010; 5:e11177; PMID:20567510; http://dx.doi.org/10.1371/jour n a l.pone.0 011177.
62. Levi B, James AW, Nelson ER, Li S, Peng M, Commons GW, et al. Human adipose-derived stro-mal cells stimulate autogenous skeletal repair via para-crine Hedgehog signaling with calvarial osteoblasts. Stem Cells Dev 2011; 20:243-57; PMID:20698749; http://dx.doi.org/10.1089/scd.2010.0250.
63. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteo-arthritis. Arthritis Rheum 2003; 48:3464-74; PMID:14673997; http://dx.doi.org/10.1002/a r t.113 65. (Pubitemid 37531912)
64. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 2002; 290:763-9; PMID:11785965; http://dx.doi.org/10.1006/bbrc.2001.6270. (Pubitemid 34687506)
65. Güven S, Mehrkens A, Saxer F, Schaefer DJ, Martinetti R, Martin I, et al. Engineering of large osteogenic grafts with rapid engraftment capacity using mesenchymal and endothelial progenitors from human adipose tissue. Biomaterials 2011; 32:5801-9; PMID:21605897; http://dx.doi.org/10.1016/j.bio- materials.2011.04.064.
66. Papadimitropoulos A, Scherberich A, Güven S, Theilgaard N, Crooijmans HJ, Santini F, et al. A 3D in vitro bone organ model using human progenitor cells. Eur Cell Mater 2011; 21:445-58, discussion 458; PMID:21604244.
67. Ra JC, Kang SK, Shin IS, Park HG, Joo SA, Kim JG, et al. Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells. J Transl Med 2011; 9:181; PMID:22017805.
68. Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, Lee HY, et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev 2011; 20:1297-308; PMID:21303266; http://dx.doi.org/10.1089/scd.2010.0466.
69. Ugras S, Brill E, Jacobsen A, Hafner M, Socci ND, Decarolis PL, et al. Small RNA sequencing and functional characterization reveals MicroRNA-143 tumor suppressor activity in liposarcoma. Cancer Res 2011; 71:5659-69; PMID:21693658; http://dx.doi.org/10.1158/0008-5472.CAN-11-0890.