Fibroblasts and Mesenchymal Stromal/Stem Cells Are Phenotypically Indistinguishable

Acta Haematologica

Volumn 136, Issue 2, 2016, Pages 85-97

  Denu, Ryan A ^a,b   Nemcek, Steven ^c   Bloom, Debra D ^a   Goodrich, A Daisy ^e   Kim, Jaehyup ^a   Mosher, Deane F ^a   Hematti, Peiman ^a,d  

^a Department of Medicine ^*  (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN   (United States)

^e UNIVERSITY OF NEVADA   (United States)

Author keywords

Fibroblasts; Immunomodulation; Macrophages; Mesenchymal stromal stem cells; Phenotype; Stroma

Indexed keywords

COLLAGEN TYPE 1; FIBRONECTIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 8; MESSENGER RNA;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROCYTE; CONTROLLED STUDY; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INFLAMMATION; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; OSTEOBLAST; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL CULTURE; WESTERN BLOTTING; CELL CULTURE; CYTOLOGY;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLASTS; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS;

EID: 84969705729     PISSN: 00015792     EISSN: 14219662     Source Type: Journal    
DOI: 10.1159/000445096     Document Type: Article

References (61)

1. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A: Clarification of the nomenclature for MSC: The International Society for Cellular Therapy Position Statement. Cytotherapy 2005; 7: 393-395.
2. Friedenstein AJ, Chailakhjan RK, Lalykina KS: The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970; 3: 393-403.
3. Friedenstein AJ: Marrow stromal fibroblasts. Calcif Tissue Int 1995; 56(suppl 1):S17.
4. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV: Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974; 17: 331-340.
5. Friedenstein AJ: Precursor cells of mechanocytes. Int Rev Cytol 1976; 47: 327-359.
6. Friedenstein AJ, Lalykina KS: Thymus cells are inducible to osteogenesis. Eur J Immunol 1972; 2: 602-603.
7. Caplan AI: Mesenchymal stem cells. J Orthop Res 1991; 9: 641-650.
8. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147.
9. Viswanathan S, Keating A, Deans R, Hematti P, Prockop D, Stroncek DF, Stacey G, Weiss DJ, Mason C, Rao MS: Soliciting strategies for developing cell-based reference materials to advance mesenchymal stromal cell research and clinical translation. Stem Cells Dev 2014; 23: 1157-1167.
10. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E: Minimal criteria for defining multipotent mesenchymal stromal cells. International Society for Cellular Therapy Position Statement. Cytotherapy 2006; 8: 315-317.
11. Gurd FB: A histological study of the skin lesions of pellagra. J Exp Med 1911; 13: 98-114.
12. Rinkevich Y, Walmsley GG, Hu MS, Maan ZN, Newman AM, Drukker M, Januszyk M, Krampitz GW, Gurtner GC, Lorenz HP, Weissman IL, Longaker MT: Skin fibrosis. Identification and isolation of a dermal lineage with intrinsic fibrogenic potential. Science 2015; 348:aaa2151.
13. Darby IA, Hewitson TD: Fibroblast differentiation in wound healing and fibrosis. Int Rev Cytol 2007; 257: 143-179.
14. Todaro GJ, Green H: Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 1963; 17: 299-313.
15. Hanson SE, Kim J, Johnson BH, Bradley B, Breunig MJ, Hematti P, Thibeault SL: Characterization of mesenchymal stem cells from human vocal fold fibroblasts. Laryngoscope 2010; 120: 546-551.
16. Sabatini F, Petecchia L, Tavian M, Jodon de Villeroche V, Rossi GA, Brouty-Boye D: Human bronchial fibroblasts exhibit a mesenchymal stem cell phenotype and multilineage differentiating potentialities. Lab Invest 2005; 85: 962-971.
17. Lorenz K, Sicker M, Schmelzer E, Rupf T, Salvetter J, Schulz-Siegmund M, Bader A: Multilineage differentiation potential of human dermal skin-derived fibroblasts. Exp Dermatol 2008; 17: 925-932.
18. Jaager K, Neuman T: Human dermal fibroblasts exhibit delayed adipogenic differentiation compared with mesenchymal stem cells. Stem Cells Dev 2011; 20: 1327-1336.
19. Covas DT, Panepucci RA, Fontes AM, Silva WA, Orellana MD, Freitas MC, Neder L, Santos AR, Peres LC, Jamur MC, Zago MA: Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 2008; 36: 642-654.
20. Haniffa MA, Wang XN, Holtick U, Rae M, Isaacs JD, Dickinson AM, Hilkens CM, Collin MP: Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol 2007; 179: 1595-1604.
21. Alt E, Yan Y, Gehmert S, Song YH, Altman A, Vykoukal D, Bai X: Fibroblasts share mesenchymal phenotypes with stem cells, but lack their differentiation and colony-forming potential. Biol Cell 2011; 103: 197-208.
22. Chang Y, Li H, Guo Z: Mesenchymal stem cell-like properties in fibroblasts. Cell Physiol Biochem 2014; 34: 703-714.
23. Cappellesso-Fleury S, Puissant-Lubrano B, Apoil PA, Titeux M, Winterton P, Casteilla L, Bourin P, Blancher A: Human fibroblasts share immunosuppressive properties with bone marrow mesenchymal stem cells. J Clin Immunol 2010; 30: 607-619.
24. Brendel C, Kuklick L, Hartmann O, Kim TD, Boudriot U, Schwell D, Neubauer A: Distinct gene expression profile of human mesenchymal stem cells in comparison to skin fibroblasts employing cDNA microarray analysis of 9600 genes. Gene Expr 2005; 12: 245-257.
25. Ishii M, Koike C, Igarashi A, Yamanaka K, Pan H, Higashi Y, Kawaguchi H, Sugiyama M, Kamata N, Iwata T, Matsubara T, Nakamura K, Kurihara H, Tsuji K, Kato Y: Molecular markers distinguish bone marrow mesenchymal stem cells from fibroblasts. Biochem Biophys Res Commun 2005; 332: 297-303.
26. Kim J, Hematti P: Mesenchymal stem cell-educated macrophages: A novel type of alternatively activated macrophages. Exp Hematol 2009; 37: 1445-1453.
27. Toledo-Piza AR, Nakano E, Rici RE, Maria DA: Proliferation of fibroblasts and endothelial cells is enhanced by treatment with Phyllocaulis boraceiensis mucus. Cell Prolif 2013; 46: 97-108.
28. Du ZQ, Yang CX, Rothschild MF, Ross JW: Novel microRNA families expanded in the human genome. BMC Genomics 2013; 14: 98.
29. Nichols WW, Murphy DG, Cristofalo VJ, Toji LH, Greene AE, Dwight SA: Characterization of a new human diploid cell strain, IMR-90. Science 1977; 196: 60-63.
30. Tomasini-Johansson BR, Johnson IA, Hoffmann FM, Mosher DF: Quantitative microtiter fibronectin fibrillogenesis assay: use in high throughput screening for identification of inhibitor compounds. Matrix Biol 2012; 31: 360-367.
31. Allen-Hoffmann BL, Schlosser SJ, Brondyk WH, Fahl WE: Fibronectin levels are enhanced in human fibroblasts overexpressing the c-sis protooncogene. J Biol Chem 1990; 265: 5219-5225.
32. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, Richardson A, Weinberg RA: Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 2004; 101: 4966-4971.
33. Bloom DD, Centanni JM, Bhatia N, Emler CA, Drier D, Leverson GE, McKenna DH, Gee AP, Lindblad R, Hei DJ, Hematti P: A reproducible immunopotency assay to measure mesenchymal stromal cell-mediated T-cell suppression. Cytotherapy 2015; 17: 140-151.
34. Kim J, Denu RA, Dollar BA, Escalante LE, Kuether JP, Callander NS, Asimakopoulos F, Hematti P: Macrophages and mesenchymal stromal cells support survival and proliferation of multiple myeloma cells. Br J Haematol 2012; 158: 336-346.
35. Furcht LT, Smith D, Wendelschafer-Crabb G, Mosher DF, Foidart JM: Fibronectin presence in native collagen fibrils of human fibroblasts: immunoperoxidase and immunoferritin localization. J Histochem Cytochem 1980; 28: 1319-1333.
36. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM: Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002; 99: 3838-3843.
37. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG: Identification and characterization of a fibroblast marker: Fsp1. J Cell Biol 1995; 130: 393-405.
38. Mazzucchelli L: Protein S100A4: Too long overlooked by pathologists Am J Pathol 2002; 160: 7-13.
39. Barraclough R: Calcium-binding protein S100A4 in health and disease. Biochim Biophys Acta 1998; 1448: 190-199.
40. Connor NS, Aubin JE, Sodek J: Independent expression of type I collagen and fibronectin by normal fibroblast-like cells. J Cell Sci 1983; 63: 233-244.
41. Ross R: The fibroblast and wound repair. Biol Rev Camb Philos Soc 1968; 43: 51-96.
42. Mosser DM, Edwards JP: Exploring the full spectrum of macrophage activation. Nat Rev 2008; 8: 958-969.
43. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD: Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33: 1402-1416.
44. Wirths S, Malenke E, Kluba T, Rieger S, Muller MR, Schleicher S, Hann von Weyhern C, Nagl F, Fend F, Vogel W, Mayer F, Kanz L, Buhring HJ, Kopp HG: Shared cell surface marker expression in mesenchymal stem cells and adult sarcomas. Stem Cells Transl Med 2013; 2: 53-60.
45. Brohem CA, de Carvalho CM, Radoski CL, Santi FC, Baptista MC, Swinka BB, de A Urban C, de Araujo LR, Graf RM, Feferman IH, Lorencini M: Comparison between fibroblasts and mesenchymal stem cells derived from dermal and adipose tissue. Int J Cosmet Sci 2013; 35: 448-457.
46. Bae S, Ahn JH, Park CW, Son HK, Kim KS, Lim NK, Jeon CJ, Kim H: Gene and micro-RNA expression signatures of human mesenchymal stromal cells in comparison to fibroblasts. Cell Tissue Res 2009; 335: 565-573.
47. Lorenz K, Sicker M, Schmelzer E, Rupf T, Salvetter J, Schulz-Siegmund M, Bader A: Multilineage differentiation potential of human dermal skin-derived fibroblasts. Exp Dermatol 2008; 17: 925-932.
48. Friedenstein AJ, Chailakhyan RK, Gerasimov UV: Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987; 20: 263-272.
49. Sorisky A, Pardasani D, Gagnon A, Smith TJ: Evidence of adipocyte differentiation in human orbital fibroblasts in primary culture. J Clin Endocrinol Metab 1996; 81: 3428-3431.
50. Price S: Experimental arthritis: dermal fibroblasts have MSC-like immunosuppressive effects in vivo. Nat Rev Rheumatol 2011; 7: 437.
51. Jones S, Horwood N, Cope A, Dazzi F: The antiproliferative effect of mesenchymal stem cells is a fundamental property shared by all stromal cells. J Immunol 2007; 179: 2824-2831.
52. Korn JH: Modulation of lymphocyte mitogen responses by cocultured fibroblasts. Cell Immunol 1981; 63: 374-384.
53. Prockop DJ, Oh JY: Mesenchymal stem/stromal cells (MSCS): role as guardians of inflammation. Mol Ther 2012; 20: 14-20.
54. Castro-Malaspina H, Gay RE, Resnick G, Kapoor N, Meyers P, Chiarieri D, McKenzie S, Broxmeyer HE, Moore MA: Characterization of human bone marrow fibroblast colonyforming cells (CFU-F) and their progeny. Blood 1980; 56: 289-301.
55. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO: Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 2002; 99: 12877-12882.
56. Rinn JL, Bondre C, Gladstone HB, Brown PO, Chang HY: Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS Genet 2006; 2:e119.
57. Samuelsson H, Ringden O, Lonnies H, Le Blanc K: Optimizing in vitro conditions for immunomodulation and expansion of mesenchymal stromal cells. Cytotherapy 2009; 11: 129-136.
58. Schellenberg A, Stiehl T, Horn P, Joussen S, Pallua N, Ho AD, Wagner W: Population dynamics of mesenchymal stromal cells during culture expansion. Cytotherapy 2012; 14: 401-411.
59. Kramann R, Schneider RK, DiRocco DP, Machado F, Fleig S, Bondzie PA, Henderson JM, Ebert BL, Humphreys BD: Perivascular Gli1(+) progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 2015; 16: 51-66.
60. Hematti P: Mesenchymal stromal cells and fibroblasts: A case of mistaken identity Cytotherapy 2012; 14: 516-521.
61. Thannickal VJ, Zhou Y, Gaggar A, Duncan SR: Fibrosis: ultimate and proximate causes. J Clin Invest 2014; 124: 4673-4677.