Mesenchymal stromal/stem cells markers in the human bone marrow

Cytotherapy

Volumn 15, Issue 3, 2013, Pages 292-306

  Rasini, Valeria ^a   Dominici, Massimo ^a   Kluba, Torsten ^b   Siegel, Georg ^c   Lusenti, Giulia ^a   Northoff, Hinnak ^c   Horwitz, Edwin M ^d   Schäfer, Richard ^c,e  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Department of Orthopedics ^*  (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone marrow; Histology; In vivo; Markers; MSCs; Pluripotency; Stromal cells

Indexed keywords

5' NUCLEOTIDASE; CD103 ANTIGEN; CD146 ANTIGEN; GANGLIOSIDE GD2; OCTAMER TRANSCRIPTION FACTOR 4; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; STAGE SPECIFIC EMBRYO ANTIGEN 4; TRANSCRIPTION FACTOR NANOG;

ANTIGEN EXPRESSION; ARTICLE; BONE BIOPSY; CONTROLLED STUDY; EX VIVO STUDY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; PRIORITY JOURNAL; STEM CELL EXPANSION; TRABECULAR BONE;

EID: 84875479603     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2012.11.009     Document Type: Article

References (59)

1. Phinney DG, Prockop DJ. Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair-current views. Stem Cells. 2007; 25:2896-902.
2. Dominici M, Hofmann TJ, Horwitz EM. Bone marrow mesenchymal cells: Biological properties and clinical applications. J Biol Regul Homeost Agents. 2001;15:28-37.
3. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999;5:309-13.
4. Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, et al. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 2001;97:1227-31.
5. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet. 2008;371:1579-86.
6. Ball LM, Bernardo ME, Roelofs H, Lankester A, Cometa A, Egeler RM, et al. Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantation. Blood. 2007;110:2764-7.
7. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005;106:1755-61.
8. Schäfer R, Dominici M, Muller I, Dazzi F, Bieback K, Godthardt K, et al. Progress in characterization, preparation and clinical applications of non-hematopoietic stem cells, 29-30 September 2006, Tubingen, Germany. Cytotherapy. 2007;9:397-405.
9. Schäfer R, Dominici M, Müller I, Horwitz E, Asahara T, Bulte J, et al. Basic research and clinical applications of nonhematopoietic stem cells, 4-5 April 2008, Tubingen, Germany. Cytotherapy. 2009;11:245-55.
10. DominiciM,LeBlancK,Müller I,Slaper-Cortenbach I, Marini F, Krause D, et al.Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-7.
11. Phinney DG, Kopen G, Righter W, Webster S, Tremain N, Prockop DJ. Donor variation in the growth properties and osteogenic potential of human marrow stromal cells. J Cell Biochem. 1999;75:424-36.
12. Schäfer R, Schnaidt M, Klaffschenkel RA, Siegel G, Schule M, Radlein MA, et al. Expression of blood group genes by mesenchymal stem cells. Br J Haematol. 2011;153:520-8.
13. Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol. 2002;30:783-91.
14. Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM. Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: A novel surface marker for the identification of MSCs. Blood. 2007;109:4245-8.
15. Giesert C, Marxer A, Sutherland DR, Schuh AC, Kanz L, Buhring HJ. Antibody W7C5 defines a CD109 epitope expressed on CD34? and CD34- hematopoietic and mesenchymal stem cell subsets. Ann N Y Acad Sci. 2003;996:227-30.
16. Bühring HJ, Kuci S, Conze T, Rathke G, Bartolovic K, GrunebachF, et al.CDCP1identifies a broad spectrum of normal and malignant stem/progenitor cell subsets of hematopoietic and nonhematopoietic origin. Stem Cells. 2004;22:334-43.
17. Guillot PV, Gotherstrom C, Chan J, Kurata H, Fisk NM. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells. 2007;25:646-54.
18. BoultingGL, Kiskinis E, CroftGF,AmorosoMW, OakleyDH, Wainger BJ, et al. A functionally characterized test set of human induced pluripotent stemcells.Nat Biotechnol. 2011;29:279-86.
19. Friedenstein AJ,Chailakhjan RK, LalykinaKS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970;3:393-403.
20. Friedenstein AJ, Latzinik NV, Gorskaya Yu F, Luria EA, Moskvina IL. Bone marrow stromal colony formation requires stimulation by haemopoietic cells. Bone Mineral. 1992;18: 199-213.
21. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9: 641-50.
22. Cattoretti G, Schiro R, Orazi A, Soligo D, Colombo MP. Bone marrow stroma in humans: Anti-nerve growth factor receptor antibodies selectively stain reticular cells in vivo and in vitro. Blood. 1993;81:1726-38.
23. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells. 2001;19:180-92.
24. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301-13.
25. Jones E, McGonagle D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford). 2008; 47:126-31.
26. Tormin A, Li O, Brune JC,Walsh S, Schutz B, EhingerM, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood. 2011;117: 5067-77.
27. Travlos GS. Normal structure, function, and histology of the bone marrow. Toxicol Pathol. 2006;34:548-65.
28. D'Amico F, Skarmoutsou E, Stivala F. State of the art in antigen retrieval for immunohistochemistry. J Immunol Methods. 2009;341:1-18.
29. Stagg J, Divisekera U, Duret H, Sparwasser T, Teng MW, Darcy PK, et al. CD73-deficient mice have increased antitumor immunity and are resistant to experimental metastasis. Cancer Res. 2011;71:2892-900.
30. Airas L, Niemela J, SalmiM, PuurunenT, SmithDJ, Jalkanen S. Differential regulation and function of CD73, a glycosylphosphatidylinositol-linked 70-kD adhesion molecule, on lymphocytes and endothelial cells. J Cell Biol. 1997;136:421-31.
31. Dianzani U, Redoglia V, Bragardo M, Attisano C, Bianchi A, Di Franco D, et al. Co-stimulatory signal delivered by CD73 molecule to human CD45RAhiCD45ROlo (naive) CD8? T lymphocytes. J Immunol. 1993;151:3961-70.
32. Wong AP, Keating A, Lu WY, Duchesneau P, Wang X, Sacher A, et al. Identification of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J Clin Invest. 2009;119:336-48.
33. Chu P, Arber DA. Paraffin-section detection of CD10 in 505 nonhematopoietic neoplasms: Frequent expression in renal cell carcinoma and endometrial stromal sarcoma. Am J Clin Pathol. 2000;113:374-82.
34. Bene MC, Faure GC. CD10 in acute leukemias. GEIL (Groupe d'Etude Immunologique des Leucemies). Haematologica. 1997;82:205-10.
35. Ichii M, Oritani K, Yokota T, Zhang Q, Garrett KP, Kanakura Y, et al. The density of CD10 corresponds to commitment and progression in the human B lymphoid lineage. PloS One. 2010;5:e12954.
36. Bühring HJ, Battula VL, Treml S, Schewe B, Kanz L, Vogel W. Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci. 2007;1106:262-71.
37. Bühring HJ, Treml S, Cerabona F, de Zwart P, Kanz L, Sobiesiak M. Phenotypic characterization of distinct human bone marrow-derived MSC subsets. Ann N Y Acad Sci. 2009; 1176:124-34.
38. Jones E, English A, Churchman SM, Kouroupis D, Boxall SA, Kinsey S, et al. Large-scale extraction and characterization of CD271? multipotential stromal cells from trabecular bone in health and osteoarthritis: Implications for bone regeneration strategies based on uncultured or minimally cultured multipotential stromal cells. Arthritis Rheum. 2010;62:1944-54.
39. Battula VL, Treml S, Bareiss PM, Gieseke F, Roelofs H, de Zwart P, et al. Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica. 2009;94:173-84.
40. Zhang ZL, Tong J, Lu RN, Scutt AM, Goltzman D, Miao DS. Therapeutic potential of non-adherent BM-derived mesenchymal stem cells in tissue regeneration. Bone Marrow Transplant. 2009;43:69-81.
41. Baksh D, Davies JE, Zandstra PW. Adult human bone marrow-derived mesenchymal progenitor cells are capable of adhesion-independent survival and expansion. Exp Hematol. 2003;31:723-32.
42. Bianco P, Costantini M, Dearden LC, Bonucci E. Alkaline phosphatase positive precursors of adipocytes in the human bone marrow. Br J Haematol. 1988;68:401-3.
43. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, et al.Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466: 829-34.
44. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131:324-36.
45. Cox G, Boxall SA, Giannoudis PV, Buckley CT, Roshdy T, Churchman SM, et al. High abundance of CD271(?) multipotential stromal cells (MSCs) in intramedullary cavities of long bones. Bone. 2012;50:510-7.
46. Muller G. Take-over: Multiple mechanisms of inter-adipocyte communication. J Mol Cell Biol. 2011;3:382.
47. Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol. 2001;189:54-63.
48. Takedachi M, Oohara H, Smith BJ, Iyama M, Kobashi M, Maeda K, et al. CD73-generated adenosine promotes osteoblast differentiation. J Cell Physiol. 2012;227:2622-31.
49. Traktuev DO, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res. 2008;102:77-85.
50. Lin G, Garcia M, Ning H, Banie L, Guo YL, Lue TF, et al. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 2008;17:1053-63.
51. Lin CS, Xin ZC, Deng CH, Ning H, Lin G, Lue TF. Defining adipose tissue-derived stem cells in tissue and in culture. Histol Histopathol. 2010;25:807-15.
52. Tallone T, Realini C, Bohmler A, Kornfeld C, Vassalli G, Moccetti T, et al. Adult human adipose tissue contains several types of multipotent cells. J Cardiovasc Transl Res. 2011;4: 200-10.
53. Song L, Tuan RS. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J. 2004;18:980-2.
54. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005;122:947-56.
55. Hung SP, Ho JH, Shih YR, Lo T, Lee OK. Hypoxia promotes proliferation and osteogenic differentiation potentials of human mesenchymal stem cells. J Orthop Res. 2012;30:260-6.
56. Roobrouck VD, Clavel C, Jacobs SA, Ulloa-Montoya F, Crippa S, Sohni A, et al. Differentiation potential of humanpostnatal mesenchymal stem cells, mesoangioblasts, and multipotent adult progenitor cells reflected in their transcriptome and partially influenced by the culture conditions. Stem Cells. 2011;29:871-82.
57. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci. 2004;117(Pt 14): 2971-81.
58. Smith JR, Pochampally R, Perry A, Hsu SC, Prockop DJ. Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem Cells. 2004;22:823-31.
59. Kucia M, Zuba-Surma EK, Wysoczynski M, Wu W, Ratajczak J, Machalinski B, et al. Adult marrow-derived very small embryonic-like stem cells and tissue engineering. Exp Opin Biol Ther. 2007;7:1499-514.