Transcriptional profile of native CD271+ multipotential stromal cells: Evidence for multiple fates, with prominent osteogenic and wnt pathway signaling activity

Arthritis and Rheumatism

Volumn 64, Issue 8, 2012, Pages 2632-2643

  Churchman, Sarah M ^a   Ponchel, Frederique ^a   Boxall, Sally A ^a   Cuthbert, Richard ^a   Kouroupis, Dimitrios ^a   Roshdy, Tarek ^a   Giannoudis, Peter V ^a   Emery, Paul ^a   McGonagle, Dennis ^a   Jones, Elena A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; BONE MORPHOGENETIC PROTEIN 5; CD146 ANTIGEN; CONNEXIN 43; FATTY ACID BINDING PROTEIN 4; INTERLEUKIN 7; LIPOPROTEIN LIPASE; MEMBRANE PROTEIN; MYOD1 PROTEIN; MYOGENIN; NEUROGENIC DIFFERENTIATION FACTOR; OSTEOCALCIN; OSTEONECTIN; OSTEOPONTIN; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROCOLLAGEN C PROTEINASE; PROTEOCHONDROITIN SULFATE; SECRETED FRIZZLED RELATED PROTEIN 3; SMOOTH MUSCLE ACTIN; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN 3; STROMAL CELL DERIVED FACTOR 1; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; UNINDEXED DRUG; WNT PROTEIN;

ADOLESCENT; ADULT; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CHILD; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO CULTURE; MULTIPOTENTIAL STROMAL CELL; NORMAL HUMAN; PERICYTE; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SIGNAL TRANSDUCTION; STROMA CELL;

ADOLESCENT; ADULT; AGED; ANGIOPOIETIN-1; ANTIGENS, CD45; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CXCL12; CHILD; CHILD, PRESCHOOL; FATTY ACID-BINDING PROTEINS; FIBROBLASTS; HUMANS; MIDDLE AGED; MULTIPOTENT STEM CELLS; NERVE TISSUE PROTEINS; OSTEOGENESIS; RECEPTORS, NERVE GROWTH FACTOR; SKIN; STROMAL CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; WNT SIGNALING PATHWAY; YOUNG ADULT;

EID: 84864486162     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.34434     Document Type: Article

References (55)

1. Bianco P, Robey PG, Saggio I, Riminucci M,. "Mesenchymal" stem cells in human bone marrow (skeletal stem cells): a critical discussion of their nature, identity, and significance in incurable skeletal disease. Hum Gene Ther 2010; 21: 1057-66.
2. Deschaseaux F, Pontikoglou C, Sensebe L,. Bone regeneration: the stem/progenitor cells point of view. J Cell Mol Med 2010; 14: 103-15.
3. + cells. Stem Cells 2006; 24: 1728-37.
4. Ma HL, Chen TH, Hung SC,. Development of a new method in promoting fracture healing: multiple cryopreserved bone marrow injections using a rabbit model. Arch Orthop Trauma Surg 2004; 124: 448-54.
5. Hernigou P, Poignard A, Beaujean F, Rouard H,. Percutaneous autologous bone-marrow grafting for nonunions: influence of the number and concentration of progenitor cells. J Bone Joint Surg Am 2005; 87A: 1430-7.
6. Loughlin J, Dowling B, Chapman K, Marcelline L, Mustafa Z, Southam L, et al. Functional variants within the secreted frizzled-related protein 3 gene are associated with hip osteoarthritis in females. Proc Natl Acad Sci U S A 2004; 101: 9757-62.
7. Lories RJ, Boonen S, Peeters J, de Vlam K, Luyten FP,. Evidence for a differential association of the arg200trp single-nucleotide polymorphism in frzb with hip osteoarthritis and osteoporosis. Rheumatology (Oxford) 2006; 45: 113-4.
8. Mareddy A, Crawford R, Brooke G, Xiao Y,. Clonal isolation and characterization of bone marrow stromal cells from patients with osteoarthritis. Tissue Eng 2007; 13: 819-29.
9. Stenderup K, Justesen J, Eriksen EF, Rattan SIS, Kassem M,. Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. J Bone Miner Res 2001; 16: 1120-9.
10. Justesen J, Stenderup K, Eriksen EF, Kassem M,. Maintenance of osteoblastic and adipocytic differentiation potential with age and osteoporosis in human marrow stromal cell cultures. Calcif Tissue Int 2002; 71: 36-44.
11. Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008; 3: e2213.
12. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I,. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004; 22: 675-82.
13. 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 [published erratum appears in Arthritis Rheum 2010;62:3005]. Arthritis Rheum 2010; 62: 1944-54.
14. Halfon S, Abramov N, Grinblat B, Ginis I,. Markers distinguishing mesenchymal stem cells from fibroblasts are downregulated with passaging. Stem Cells Dev 2011; 20: 53-66.
15. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL,. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 2000; 9: 841-8.
16. Bianco P, Riminucci M, Gronthos S, Robey PG,. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001; 19: 180-92.
17. Meirelles LD, Caplan AI, Nardi NB,. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008; 26: 2287-99.
18. Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 2002; 46: 3349-60.
19. Jones EA, English A, Kinsey SE, Straszynski L, Emery P, Ponchel F, et al. Optimization of a flow cytometry-based protocol for detection and phenotypic characterization of multipotent mesenchymal stromal cells from human bone marrow. Cytometry B Clin Cytom 2006; 70: 391-9.
20. Buhring 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.
21. Tormin A, Li O, Brune JC, Walsh S, Schutz B, Ehinger M, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 2011; 117: 5067-77.
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. 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.
24. Tarte K, Gaillard J, Lataillade JJ, Fouillard L, Becker M, Mossafa H, et al. Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 2010; 115: 1549-53.
25. Galotto M, Berisso G, Delfino L, Podesta M, Ottaggio L, Dallorso S, et al. Stromal damage as consequence of high-dose chemo/radiotherapy in bone marrow transplant recipients. Exp Hematol 1999; 27: 1460-6.
26. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T,. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005; 52: 2521-9.
27. Eisen MB, Spellman PT, Brown PO, Botstein D,. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998; 95: 14863-8.
28. Gronthos S, Zannettino AC, Hay SJ, Shi ST, Graves SE, Kortesidis A, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003; 116: 1827-35.
29. 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.
30. Van Lochem EG, van der Velden VH, Wind HK, te Marvelde JG, Westerdaal NA, van Dongen JM,. Immunophenotypic differentiation patterns of normal hematopoiesis in human bone marrow: reference patterns for age-related changes and disease-induced shifts. Cytometry B Clin Cytom 2004; 60B: 1-13.
31. 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.
32. 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.
33. Ninomiya K, Miyamoto T, Imai JI, Fujita N, Suzuki T, Iwasaki R, et al. Osteoclastic activity induces osteomodulin expression in osteoblasts. Biochem Biophys Res Comm 2007; 362: 460-6.
34. Gajko-Galicka A,. Mutations in type I collagen genes resulting in osteogenesis imperfecta in humans. Acta Biochim Pol 2002; 49: 433-41.
35. De Bari C, Dell'Accio F, Karystinou A, Guillot PV, Fisk NM, Jones EA, et al. A biomarker-based mathematical model to predict bone-forming potency of human synovial and periosteal mesenchymal stem cells. Arthritis Rheum 2008; 58: 240-50.
36. Etheridge SL, Spencer GJ, Heath DJ, Genever PG,. Expression profiling and functional analysis of Wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 2004; 22: 849-60.
37. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH,. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004; 10: 55-63.
38. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000; 100: 197-207.
39. Bellantuono I, Aldahmash A, Kassem M,. Aging of marrow stromal (skeletal) stem cells and their contribution to age-related bone loss. Biochim Biophys Acta 2009; 1792: 364-70.
40. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, et al. High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 2002; 346: 1513-21.
41. Hess R, Pino AM, Rios S, Fernandez M, Rodriguez JP,. High affinity leptin receptors are present in human mesenchymal stem cells (MSCs) derived from control and osteoporotic donors. J Cell Biochem 2005; 94: 50-7.
42. Zipori D,. The stem state: mesenchymal plasticity as a paradigm. Curr Stem Cell Res Ther 2006; 1: 95-102.
43. Einhorn TA,. The science of fracture healing. J Orthop Trauma 2005; 19: S4-6.
44. Gimble G, Zvonic S, Floyd Z, Kassem M, Nuttall M,. Playing with bone and fat. J Cell Biochem 2006; 98: 251-66.
45. Kawaguchi J, Kii I, Sugiyama Y, Takeshita S, Kudo A,. The transition of cadherin expression in osteoblast differentiation from mesenchymal cells: consistent expression of cadherin-11 in osteoblast lineage. J Bone Miner Res 2001; 16: 260-9.
46. Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GFM, Chisaka O, et al. Cadherin-11 in synovial lining formation and pathology in arthritis. Science 2007; 315: 1006-10.
47. Cancelas JA, Koevoet WL, de Koning AE, Mayen AE, Rombouts EJ, Ploemacher RE,. Connexin-43 gap junctions are involved in multiconnexin-expressing stromal support of hemopoietic progenitors and stem cells. Blood 2000; 96: 498-505.
48. Jones P, May G, Healy L, Brown J, Hoyne G, Delassus S, et al. Stromal expression of Jagged 1 promotes colony formation by fetal hematopoietic progenitor cells. Blood 1998; 92: 1505-11.
49. Allende ML, Tuymetova G, Lee BG, Bonifacino E, Wu YP, Proia RL,. S1P1 receptor directs the release of immature B cells from bone marrow into blood. J Exp Med 2010; 207: 1113-24.
50. Ishii T, Shimazu Y, Nishiyama I, Kikuta J, Ishii M,. The role of sphingosine 1-phosphate in migration of osteoclast precursors: an application of intravital two-photon microscopy. Mol Cells 2011; 31: 399-403.
51. Crockett JC, Rogers MJ, Coxon FP, Hocking LJ, Helfrich MH,. Bone remodelling at a glance. J Cell Sci 2011; 124: 991-8.
52. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, et al. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 2006; 4: 111-21.
53. Yu YY, Lieu S, Lu CY, Miclau T, Marcucio RS, Colnot C,. Immunolocalization of BMPs, BMP antagonists, receptors, and effectors during fracture repair. Bone 2010; 46: 841-51.
54. Hamidouche Z, Fromigue O, Ringe J, Haeupl T, Marie PJ,. Crosstalks between integrin α5 and IGF2/IGFBP2 signalling trigger human bone marrow-derived mesenchymal stromal osteogenic differentiation. BMC Cell Biol 2010; 11: 44.
55. Kurth TB, Dell'Accio F, Crouch V, Augello A, Sharpe PT, De Bari C,. Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis Rheum 2011; 63: 1289-300.