Interleukin-6 induces the lineage commitment of bone marrow-derived mesenchymal multipotent cells through down-regulation of Sox2 by osteogenic transcription factors

FASEB Journal

Volumn 28, Issue 7, 2014, Pages 3273-3286

  Yoon, Dong Suk ^a,b   Kim, Yun Hee ^a   Lee, Seulgi ^a,b   Lee, Kyoung Mi ^a,b   Park, Kwang Hwan ^a,b   Jang, Yeonsue ^a   Lee, Jin Woo ^a,b  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

Cell cell interaction; Dlx5; Heterogeneous population; Runx2; Stemness

Indexed keywords

CYTOKINE; INTERLEUKIN 6; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX2;

ADULT; ARTICLE; BONE DEVELOPMENT; CELL CULTURE; CELL INTERACTION; CELL LOSS; CELL POPULATION; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MALE; MULTIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; UPREGULATION;

CELL-CELL INTERACTION; DLX5; HETEROGENEOUS POPULATION; RUNX2; STEMNESS;

ADULT; BONE MARROW; CELL AGING; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CYTOKINES; DOWN-REGULATION; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; INTERLEUKIN-6; MALE; MIDDLE AGED; MULTIPOTENT STEM CELLS; OSTEOGENESIS; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION; YOUNG ADULT;

EID: 84903749600     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-248567     Document Type: Article

References (67)

1. Haynesworth, S. E., Goshima, J., Goldberg, V. M., and Caplan, A. I. (1992) Characterization of cells with osteogenic potential from human marrow. Bone 13, 81-88
2. Jaiswal, N., Haynesworth, S. E., Caplan, A. I., and Bruder, S. P. (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J. Cell. Biochem. 64, 295-312 (Pubitemid 27065443)
3. Kuznetsov, S. A., Krebsbach, P. H., Satomura, K., Kerr, J., Riminucci, M., Benayahu, D., and Robey, P. G. (1997) Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J. Bone Miner. Res. 12, 1335-1347 (Pubitemid 27375376)
4. Wang, W. G., Lou, S. Q., Ju, X. D., Xia, K., andXia, J. H. (2003) In vitro chondrogenesis of human bone marrow-derived mesenchymal progenitor cells in monolayer culture: activation by transfection with TGF-ß2. Tissue Cell 35, 69-77 (Pubitemid 36329262)
5. Yoo, J. U., Barthel, T. S., Nishimura, K., Solchaga, L., Caplan, A. I., Goldberg, V. M., and Johnstone, B. (1998) The chondro-genic potential of human bone-marrow-derived mesenchymal progenitor cells. J. Bone Joint Surg. Am. 80, 1745-1757 (Pubitemid 29013807)
6. Johnstone, B., Hering, T. M., Caplan, A. I., Goldberg, V. M., and Yoo, J. U. (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238, 265-272 (Pubitemid 28366150)
7. Minguell, J. J., Erices, A., and Conget, P. (2001) Mesenchymal stem cells. Exp. Biol. Med. (Maywood) 226, 507-520 (Pubitemid 32524497)
8. Lazarus, H. M., Haynesworth, S. E., Gerson, S. L., Rosenthal, N. S., and Caplan, A. I. (1995) Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 16, 557-564
9. Conget, P. A., and Minguell, J. J. (1999) Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J. Cell. Physiol. 181, 67-73 (Pubitemid 29400373)
10. Prockop, D. J. (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276, 71-74 (Pubitemid 27161245)
11. 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)
12. 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)
13. Neubauer, M., Hacker, M., Bauer-Kreisel, P., Weiser, B., Fischbach, C, Schulz, M. B., Goepferich, A., and Blunk, T. (2005) Adipose tissue engineering based on mesenchymal stem cells and basic fibroblast growth factor in vitro. Tissue Eng. 11, 1840-1851 (Pubitemid 43120196)
14. Hayflick, L. (1965) The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636
15. Ksiazek, K. (2009) A comprehensive review on mesenchymal stem cell growth and senescence. Rejuv. Res. 12, 105-116
16. Baxter, M. A., Wynn, R. F., Jowitt, S. N., Wraith, J. E., Fairbairn, L. J., and Bellantuono, I. (2004) Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22, 675-682 (Pubitemid 39172200)
17. Rombouts, W. J., and Ploemacher, R. E. (2003) Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 17, 160-170 (Pubitemid 36175902)
18. Digirolamo, C. M., Stokes, D., Colter, D., Phinney, D. G., Class, R., and Prockop, D.J. (1999) Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br. J. Haematol. 107, 275-281 (Pubitemid 29530211)
19. Bruder, S. P., Jaiswal, N., and Haynesworth, S. E. (1997) Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J. Cell. Biochem. 64, 278-294 (Pubitemid 27065442)
20. Mets, T., and Verdonk, G. (1981) In vitro aging of human bone marrow derived stromal cells. Mech. Ageing Dev. 16, 81-89 (Pubitemid 11084624)
21. Yoon, D. S., Kim, Y H., Jung, H. S., Paik, S., and Lee, J. W. (2011) Importance of Sox2 in maintenance of cell proliferation and multipotency of mesenchymal stem cells in low-density culture. Cell Prolif. 44, 428-440
22. Nelson, P. J., and Daniel, T. O. (2002) Emerging targets: molecular mechanisms of cell contact-mediated growth control. Kidney Int. 61, S99-105
23. Takai, Y., Miyoshi, J., Ikeda, W., and Ogita, H. (2008) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 9, 603-615 (Pubitemid 352032927)
24. Ho, J. H., Chen, Y F., Ma, W. H., Tseng, T. C, Chen, M. H., and Lee, O. K. (2011) Cell contact accelerates replicative senescence of human mesenchymal stem cells independent of telomere shortening and p53 activation: roles of Ras and oxidative stress. Cell Transplant. 20, 1209-1220
25. Coppe, J. P., Desprez, P. Y., Krtolica, A., and Campisi, J. (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Ann. Rev. Pathol. 5, 99-118
26. Parrinello, S., Coppe, J. P., Krtolica, A., and Campisi, J. (2005) Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. J. Cell Sci. 118, 485-496 (Pubitemid 40310116)
27. Coppe, J. P., Patil, C. K., Rodier, F., Sun, Y, Munoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P. Y, and Campisi, J. (2008) Senescence-associated secretory phenotypes reveal cell-nonau-tonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868
28. Cheleuitte, D., Mizuno, S., and Glowacki, J. (1998) In vitro secretion of cytokines by human bone marrow: effects of age and estrogen status. J. Clin. Endocrinol. Metab. 83, 2043-2051 (Pubitemid 28496335)
29. Krtolica, A., and Campisi, J. (2003) Integrating epithelial cancer, aging stroma and cellular senescence. Advances Gerontol. 11, 109-116
30. Kurz, D. J., Decary, S., Hong, Y, and Erusalimsky, J. D. (2000) Senescence-associated ß-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J. Cell Sci. 113, 3613-3622
31. Stenderup, K., Justesen, J., Clausen, C, and Kassem, M. (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919-926 (Pubitemid 37543568)
32. Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C, Medrano, E. E., Linskens, M., Rubelj, I., and Pereira-Smith, O. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U.S.A. 92, 9363-9367
33. Hayflick, L., and Moorhead, P. S. (1961) The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585-621
34. Sethe, S., Scutt, A., and Stolzing, A. (2006) Aging of mesenchymal stem cells. Ageing Res. Rev. 5, 91-116 (Pubitemid 43139669)
35. Li, Z., Liu, C., Xie, Z., Song, P., Zhao, R. C, Guo, L., Liu, Z., and Wu, Y. (2011) Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One 6, e20526
36. Behbahaninia, M., Ramey, W. L., Sindhwani, M. K., and Kalani, M. Y (2011) Differential expression of pluripotency factors Sox2 and Oct4 regulate neuronal and mesenchymal lineages. Neurosurgery 69, N19
37. Park, S. B., Seo, K. W., So, A. Y, Seo, M. S., Yu, K. R., Kang, S. K., and Kang, K. S. (2012) SOX2 has a crucial role in the lineage determination and proliferation of mesenchymal stem cells through Dickkopf-1 and c-MYC. Cell Death Differ. 19, 534-545
38. Yu, K. R., Yang, S. R., Jung, J. W., Kim, H., Ko, K., Han, D. W., Park, S. B., Choi, S. W., Kang, S. K., Scholer, H., and Kang, K. S. (2012) CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 30, 876-887
39. Go, M. J., Takenaka, C., and Ohgushi, H. (2008) Forced expression of Sox2 or Nanog in human bone marrow derived mesenchymal stem cells maintains their expansion and differentiation capabilities. Exp. Cell Res. 314, 1147-1154
40. Colter, D. C, Sekiya, I., and Prockop, D.J. (2001) Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl. Acad. Sci. U.S.A. 98, 7841-7845 (Pubitemid 32642648)
41. Krtolica, A., and Campisi, J. (2002) Cancer and aging: a model for the cancer promoting effects of the aging stroma. Int. J. Biochem. Cell Biol. 34, 1401-1414 (Pubitemid 35251811)
42. Wajapeyee, N., Serra, R. W., Zhu, X., Mahalingam, M., and Green, M. R. (2008) Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132, 363-374 (Pubitemid 351191995)
43. Kojima, H., Kunimoto, H., Inoue, T., and Nakajima, K. (2012) The STAT3-IGFBP5 axis is critical for IL-6/gp130-induced premature senescence in human fibroblasts. Cell Cycle 11, 730-739
44. Wakahara, R., Kunimoto, H., Tanino, K., Kojima, H., Inoue, A., Shintaku, H., and Nakajima, K. (2012) Phospho-Ser727 of STAT3 regulates STAT3 activity by enhancing dephosphoryla-tion of phospho-Tyr705 largely through TC45. Genes Cells 17, 132-145
45. Mihara, M., Kasutani, K., Okazaki, M., Nakamura, A., Kawai, S., Sugimoto, M., Matsumoto, Y., and Ohsugi, Y. (2005) Tocili-zumab inhibits signal transduction mediated by both mIL-6R and sIL-6R, but not by the receptors of other members of IL-6 cytokine family. Int. Immunopharmacol. 5, 1731-1740 (Pubitemid 41116745)
46. Banfi, A., Muraglia, A., Dozin, B., Mastrogiacomo, M., Can-cedda, R., and Quarto, R. (2000) Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp. Hematol. 28, 707-715 (Pubitemid 30398528)
47. Stolzing, A., Jones, E., McGonagle, D., and Scutt, A. (2008) Age-related changes in human bone marrow-derived mesenchy-mal stem cells: consequences for cell therapies. Mech. Ageing Dev. 129, 163-173
48. Nishida, S., Endo, N., Yamagiwa, H., Tanizawa, T., and Taka-hashi, H. E. (1999) Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J. Bone Miner. Metab. 17, 171-177 (Pubitemid 29403926)
49. Erices, A., Conget, P., Rojas, C., and Minguell, J. J. (2002) Gp130 activation by soluble interleukin-6 receptor/interleukin-6 enhances osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. Exp. Cell Res. 280, 24-32 (Pubitemid 35230364)
50. Iwasaki, K., Komaki, M., Mimori, K., Leon, E., Izumi, Y., and Ishikawa, I. (2008) IL-6 induces osteoblastic differentiation of periodontal ligament cells. J. Dental Res. 87, 937-942
51. Heymann, D., and Rousselle, A. V. (2000) gp130 Cytokine family and bone cells. Cytokine 12, 1455-1468
52. Bellido, T., Borba, V. Z., Roberson, P., and Manolagas, S. C. (1997) Activation of the Janus kinase/STAT (signal transducer and activator of transcription) signal transduction pathway by interleukin-6-type cytokines promotes osteoblast differentiation. Endocrinology 138, 3666-3676 (Pubitemid 27351915)
53. Nicolaidou, V., Wong, M. M., Redpath, A. N., Ersek, A., Baban, D. F., Williams, L. M., Cope, A. P., and Horwood, N. J. (2012) Monocytes induce STAT3 activation in human mesenchymal stem cells to promote osteoblast formation. PLoS One 7, e39871
54. Hideshima, T., Nakamura, N., Chauhan, D., and Anderson, K. C. (2001) Biologic sequelae of interleukin-6 induced PI3-K/Akt signaling in multiple myeloma. Oncogene 20, 5991-6000 (Pubitemid 32955041)
55. Astle, M. V., Hannan, K. M., Ng, P. Y., Lee, R. S., George, A. J., Hsu, A. K., Haupt, Y., Hannan, R. D., and Pearson, R. B. (2012) AKT induces senescence in human cells via mTORC1 and p53 in the absence of DNA damage: implications for targeting mTOR during malignancy. Oncogene 31, 1949-1962
56. Mukherjee, A., and Rotwein, P. (2009) Akt promotes BMP2-mediated osteoblast differentiation and bone development. J. Cell Sci. 122, 716-726
57. Itahana, K, Dimri, G., and Campisi, J. (2001) Regulation of cellular senescence by p53. Eur. J. Biochem. 268, 2784-2791 (Pubitemid 32862960)
58. Rufini, A., Tucci, P., Celardo, I., and Melino, G. (2013) Senescence and aging: the critical roles of p53. Oncogene 32, 5129-5143
59. Wagner, W., Horn, P., Castoldi, M., Diehlmann, A., Bork, S., Saffrich, R., Benes, V., Blake, J., Pfister, S., Eckstein, V., and Ho, A. D. (2008) Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3, e2213
60. Kozhevnikova, M. N., Mikaelian, A. S., Paiushina, O. V., and Starostin, V. I. (2008) [Comparative characterization of mesenchymal bone marrow stromal cells at early and late stages of culturing]. Izv. Akad. Nauk Ser. Biol. Mar.-Apr., 156-162
61. Galderisi, U., Helmbold, H., Squillaro, T., Alessio, N., Komm, N., Khadang, B., Cipollaro, M., Bohn, W., and Giordano, A (2009) In vitro senescence of rat mesenchymal stem cells is accompanied by downregulation of stemness-related and DNA damage repair genes. Stem Cells Dev. 18, 1033-1042
62. Zaidi, S. K, Pande, S., Pratap, J., Gaur, T., Grigoriu, S., Ali, S. A., Stein, J. L., Lian, J. B., van Wijnen, A. J., and Stein, G. S. (2007) Runx2 deficiency and defective subnuclear targeting bypass senescence to promote immortalization and tumorigenic potential. Proc. Natl. Acad. Sci. U.S.A. 104, 19861-19866
63. Muraglia, A., Perera, M., Verardo, S., Liu, Y., Cancedda, R., Quarto, R., and Corte, G. (2008) DLX5 overexpression impairs osteogenic differentiation of human bone marrow stromal cells. Eur. J. Cell Biol. 87, 751-761
64. Lee, M. H., Kim, Y.J., Kim, H.J., Park, H. D., Kang, A. R., Kyung, H. M., Sung, J. H., Wozney, J. M., Kim, H. J., and Ryoo, H. M. (2003) BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-ß 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J. Biol. Chem. 278, 34387-34394 (Pubitemid 37553284)
65. Kim, Y J., Lee, M. H., Wozney, J. M., Cho, J. Y., and Ryoo, H. M. (2004) Bone morphogenetic protein-2-induced alkaline phos phatase expression is stimulated by Dlx5 and repressed by Msx2. J. Biol. Chem. 279, 50773-50780 (Pubitemid 40017815)
66. Ryoo, H. M., Hoffmann, H. M., Beumer, T., Frenkel, B., Towler, D. A., Stein, G. S., Stein, J. L., van Wijnen, A. J., and Lian, J. B. (1997) Stage-specific expression of Dlx-5 during osteoblast differentiation: involvement in regulation of osteocalcin gene expression. Mol. Endocrinol. 11, 1681-1694 (Pubitemid 27435416)
67. Basu-Roy, U., Ambrosetti, D., Favaro, R., Nicolis, S. K, Man-sukhani, A., and Basilico, C. (2010) The transcription factor Sox2 is required for osteoblast self-renewal. Cell Death Differ. 17, 1345-1353