Stem cell-conditioned medium accelerates distraction osteogenesis through multiple regenerative mechanisms

Bone

Volumn 61, Issue , 2014, Pages 82-90

  Ando, Yuji ^a   Matsubara, Kohki ^a   Ishikawa, Jun ^a   Fujio, Masahito ^a   Shohara, Ryutaro ^a   Hibi, Hideharu ^a   Ueda, Minoru ^a   Yamamoto, Akihito ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Bone marrow stromal cells; Cell recruitment; Distraction osteogenesis; Endothelial progenitor cells; Secretome; Stem cell conditioned medium

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD31 ANTIGEN; INTERLEUKIN 3; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; RANTES; STEM CELL ANTIGEN 1; STROMAL CELL DERIVED FACTOR 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW CELL; BONE MARROW STROMAL CELL; BONE REGENERATION; CALLUS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; DISTRACTION OSTEOGENESIS; ENDOTHELIAL PROGENITOR CELL; FEMALE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL CONDITIONED MEDIUM; MOLECULAR DYNAMICS; MONONUCLEAR CELL; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOBLAST; PARACRINE SIGNALING; STROMA CELL; UMBILICAL VEIN ENDOTHELIAL CELL;

BONE MARROW STROMAL CELLS; CELL RECRUITMENT; DISTRACTION OSTEOGENESIS; ENDOTHELIAL PROGENITOR CELLS; SECRETOME; STEM CELL-CONDITIONED MEDIUM;

ANIMALS; BONE AND BONES; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED ICR; OSTEOBLASTS; OSTEOGENESIS; OSTEOGENESIS, DISTRACTION;

EID: 84893416030     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.12.029     Document Type: Article

References (68)

1. Ilizarov G.A. Clinical application of the tension-stress effect for limb lengthening. Clin Orthop Relat Res 1990, 8-26.
2. McCarthy J.G., Stelnicki E.J., Mehrara B.J., Longaker M.T. Distraction osteogenesis of the craniofacial skeleton. Plast Reconstr Surg 2001, 107:1812-1827.
3. Samchukov M.L., Makarov M.R., Cherkashin A.M., Birch J.G. Distraction osteogenesis of the orthopedic skeleton: basic principles and clinical applications 2008.
4. Ai-Aql Z.S., Alagl A.S., Graves D.T., Gerstenfeld L.C., Einhorn T.A. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res 2008, 87:107-118.
5. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008, 8:726-736.
6. Tolar J., Le Blanc K., Keating A., Blazar B.R. Concise review: hitting the right spot with mesenchymal stromal cells. Stem Cells 2010, 28:1446-1455.
7. Bruder S.P., Jaiswal N., Ricalton N.S., Mosca J.D., Kraus K.H., Kadiyala S. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 1998, S247-S256.
8. Takamine Y., Tsuchiya H., Kitakoji T., Kurita K., Ono Y., Ohshima Y., et al. Distraction osteogenesis enhanced by osteoblastlike cells and collagen gel. Clin Orthop Relat Res 2002, 240-246.
9. Kitoh H., Kitakoji T., Tsuchiya H., Katoh M., Ishiguro N. Distraction osteogenesis of the lower extremity in patients with achondroplasia/hypochondroplasia treated with transplantation of culture-expanded bone marrow cells and platelet-rich plasma. J Pediatr Orthop 2007, 27:629-634.
10. Kitoh H., Kitakoji T., Tsuchiya H., Katoh M., Ishiguro N. Transplantation of culture expanded bone marrow cells and platelet rich plasma in distraction osteogenesis of the long bones. Bone 2007, 40:522-528.
11. Kinoshita K., Hibi H., Yamada Y., Ueda M. Promoted new bone formation in maxillary distraction osteogenesis using a tissue-engineered osteogenic material. J Craniofac Surg 2008, 19:80-87.
12. Kotobuki N., Katsube Y., Katou Y., Tadokoro M., Hirose M., Ohgushi H. In vivo survival and osteogenic differentiation of allogeneic rat bone marrow mesenchymal stem cells (MSCs). Cell Transplant 2008, 17:705-712.
13. Zimmermann C.E., Gierloff M., Hedderich J., Acil Y., Wiltfang J., Terheyden H. Survival of transplanted rat bone marrow-derived osteogenic stem cells in vivo. Tissue Eng Part A 2011, 17:1147-1156.
14. Ranganath S.H., Levy O., Inamdar M.S., Karp J.M. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012, 10:244-258.
15. Timmers L., Lim S.K., Arslan F., Armstrong J.S., Hoefer I.E., Doevendans P.A., et al. Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium. Stem Cell Res 2007, 1:129-137.
16. Parekkadan B., van Poll D., Suganuma K., Carter E.A., Berthiaume F., Tilles A.W., et al. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS One 2007, 2:e941.
17. Bi B., Schmitt R., Israilova M., Nishio H., Cantley L.G. Stromal cells protect against acute tubular injury via an endocrine effect. J Am Soc Nephrol 2007, 18:2486-2496.
18. van Koppen A., Joles J.A., van Balkom B.W., Lim S.K., de Kleijn D., Giles R.H., et al. Human embryonic mesenchymal stem cell-derived conditioned medium rescues kidney function in rats with established chronic kidney disease. PLoS One 2012, 7:e38746.
19. Cho Y.J., Song H.S., Bhang S., Lee S., Kang B.G., Lee J.C., et al. Therapeutic effects of human adipose stem cell-conditioned medium on stroke. J Neurosci Res 2012, 90:1794-1802.
20. Bai L., Lennon D.P., Caplan A.I., DeChant A., Hecker J., Kranso J., et al. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 2012, 15:862-870.
21. Yamagata M., Yamamoto A., Kako E., Kaneko N., Matsubara K., Sakai K., et al. Human dental pulp-derived stem cells protect against hypoxic-ischemic brain injury in neonatal mice. Stroke 2013, 44:551-554.
22. Ionescu L., Byrne R.N., van Haaften T., Vadivel A., Alphonse R.S., Rey-Parra G.J., et al. Stem cell conditioned medium improves acute lung injury in mice: in vivo evidence for stem cell paracrine action. Am J Physiol Lung Cell Mol Physiol 2012, 303:L967-L977.
23. Tay B.K., Le A.X., Gould S.E., Helms J.A. Histochemical and molecular analyses of distraction osteogenesis in a mouse model. J Orthop Res 1998, 16:636-642.
24. Isefuku S., Joyner C.J., Simpson A.H. A murine model of distraction osteogenesis. Bone 2000, 27:661-665.
25. Fujio M., Yamamoto A., Ando Y., Shohara R., Kinoshita K., Kaneko T., et al. Stromal cell-derived factor-1 enhances distraction osteogenesis-mediated skeletal tissue regeneration through the recruitment of endothelial precursors. Bone 2011, 49:693-700.
26. Kawamoto T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol 2003, 66:123-143.
27. Watson S.L., Marcal H., Sarris M., Di Girolamo N., Coroneo M.T., Wakefield D. The effect of mesenchymal stem cell conditioned media on corneal stromal fibroblast wound healing activities. Br J Ophthalmol 2010, 94:1067-1073.
28. Chen L., Tredget E.E., Wu P.Y., Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3:e1886.
29. Matsumoto S., Shibuya I., Kusakari S., Segawa K., Uyama T., Shimada A., et al. Membranous osteogenesis system modeled with KUSA-A1 mature osteoblasts. Biochim Biophys Acta 2005, 1725:57-63.
30. Cho T.J., Kim J.A., Chung C.Y., Yoo W.J., Gerstenfeld L.C., Einhorn T.A., et al. Expression and role of interleukin-6 in distraction osteogenesis. Calcif Tissue Int 2007, 80:192-200.
31. Miyazaki T., Miyauchi S., Tawada A., Anada T., Matsuzaka S., Suzuki O. Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation. J Cell Physiol 2008, 217:769-777.
32. Li G., Simpson A.H., Kenwright J., Triffitt J.T. Assessment of cell proliferation in regenerating bone during distraction osteogenesis at different distraction rates. J Orthop Res 1997, 15:765-772.
33. Li G., Simpson A.H., Kenwright J., Triffitt J.T. Effect of lengthening rate on angiogenesis during distraction osteogenesis. J Orthop Res 1999, 17:362-367.
34. Richards M., Kozloff K.M., Goulet J.A., Goldstein S.A. Increased distraction rates influence precursor tissue composition without affecting bone regeneration. J Bone Miner Res 2000, 15:982-989.
35. Morikawa S., Mabuchi Y., Kubota Y., Nagai Y., Niibe K., Hiratsu E., et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009, 206:2483-2496.
36. Karp J.M., Leng Teo G.S. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009, 4:206-216.
37. Marsell R., Einhorn T.A. The biology of fracture healing. Injury 2011, 42:551-555.
38. Shirley D., Marsh D., Jordan G., McQuaid S., Li G. Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 2005, 23:1013-1021.
39. Matsumoto T., Mifune Y., Kawamoto A., Kuroda R., Shoji T., Iwasaki H., et al. Fracture induced mobilization and incorporation of bone marrow-derived endothelial progenitor cells for bone healing. J Cell Physiol 2008, 215:234-242.
40. Lee D.Y., Cho T.J., Kim J.A., Lee H.R., Yoo W.J., Chung C.Y., et al. Mobilization of endothelial progenitor cells in fracture healing and distraction osteogenesis. Bone 2008, 42:932-941.
41. Asahara T., Kawamoto A., Masuda H. Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells 2011, 29:1650-1655.
42. Bachmann M.F., Kopf M., Marsland B.J. Chemokines: more than just road signs. Nat Rev Immunol 2006, 6:159-164.
43. Yadav A., Saini V., Arora S. MCP-1: chemoattractant with a role beyond immunity: a review. Clin Chim Acta 2010, 411:1570-1579.
44. Deshmane S.L., Kremlev S., Amini S., Sawaya B.E. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009, 29:313-326.
45. Nishimoto N. Interleukin-6 as a therapeutic target in candidate inflammatory diseases. Clin Pharmacol Ther 2010, 87:483-487.
46. Ohnishi S., Yasuda T., Kitamura S., Nagaya N. Effect of hypoxia on gene expression of bone marrow-derived mesenchymal stem cells and mononuclear cells. Stem Cells 2007, 25:1166-1177.
47. Kinnaird T., Stabile E., Burnett M.S., Lee C.W., Barr S., Fuchs S., et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004, 94:678-685.
48. Oskowitz A., McFerrin H., Gutschow M., Carter M.L., Pochampally R. Serum-deprived human multipotent mesenchymal stromal cells (MSCs) are highly angiogenic. Stem Cell Res 2011, 6:215-225.
49. Strum J.C., Johnson J.H., Ward J., Xie H., Feild J., Hester A., et al. MicroRNA 132 regulates nutritional stress-induced chemokine production through repression of SirT1. Mol Endocrinol 2009, 23:1876-1884.
50. Lee S.H., Lee Y.J., Song C.H., Ahn Y.K., Han H.J. Role of FAK phosphorylation in hypoxia-induced hMSCS migration: involvement of VEGF as well as MAPKS and eNOS pathways. Am J Physiol Cell Physiol 2010, 298:C847-C856.
51. Belema-Bedada F., Uchida S., Martire A., Kostin S., Braun T. Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2008, 2:566-575.
52. Schenk S., Mal N., Finan A., Zhang M., Kiedrowski M., Popovic Z., et al. Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor. Stem Cells 2007, 25:245-251.
53. Anton K., Banerjee D., Glod J. Macrophage-associated mesenchymal stem cells assume an activated, migratory, pro-inflammatory phenotype with increased IL-6 and CXCL10 secretion. PLoS One 2012, 7:e35036.
54. Yao J.S., Zhai W., Young W.L., Yang G.Y. Interleukin-6 triggers human cerebral endothelial cells proliferation and migration: the role for KDR and MMP-9. Biochem Biophys Res Commun 2006, 342:1396-1404.
55. Dentelli P., Del Sorbo L., Rosso A., Molinar A., Garbarino G., Camussi G., et al. Human IL-3 stimulates endothelial cell motility and promotes in vivo new vessel formation. J Immunol 1999, 163:2151-2159.
56. Ishida Y., Kimura A., Kuninaka Y., Inui M., Matsushima K., Mukaida N., et al. Pivotal role of the CCL5/CCR5 interaction for recruitment of endothelial progenitor cells in mouse wound healing. J Clin Invest 2012, 122:711-721.
57. Bellido T., Borba V.Z., Roberson P., Manolagas S.C. Activation of the Janus kinase/STAT (signal transducer and activator of transcription) signal transduction pathway by interleukin-6-type cytokines promotes osteoblast differentiation. Endocrinology 1997, 138:3666-3676.
58. Li Y., Backesjo C.M., Haldosen L.A., Lindgren U. IL-6 receptor expression and IL-6 effects change during osteoblast differentiation. Cytokine 2008, 43:165-173.
59. Barhanpurkar A.P., Gupta N., Srivastava R.K., Tomar G.B., Naik S.P., Joshi S.R., et al. IL-3 promotes osteoblast differentiation and bone formation in human mesenchymal stem cells. Biochem Biophys Res Commun 2012, 418:669-675.
60. Hong K.H., Ryu J., Han K.H. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood 2005, 105:1405-1407.
61. McGonigle J.S., Giachelli C.M., Scatena M. Osteoprotegerin and RANKL differentially regulate angiogenesis and endothelial cell function. Angiogenesis 2009, 12:35-46.
62. Cohen T., Nahari D., Cerem L.W., Neufeld G., Levi B.Z. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 1996, 271:736-741.
63. Bauer S.M., Bauer R.J., Liu Z.J., Chen H., Goldstein L., Velazquez O.C. Vascular endothelial growth factor-C promotes vasculogenesis, angiogenesis, and collagen constriction in three-dimensional collagen gels. J Vasc Surg 2005, 41:699-707.
64. Distler J.H., Hirth A., Kurowska-Stolarska M., Gay R.E., Gay S., Distler O. Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 2003, 47:149-161.
65. Wang Y., Yan W., Lu X., Qian C., Zhang J., Li P., et al. Overexpression of osteopontin induces angiogenesis of endothelial progenitor cells via the avbeta3/PI3K/AKT/eNOS/NO signaling pathway in glioma cells. Eur J Cell Biol 2011, 90:642-648.
66. Ikebuchi K., Wong G.G., Clark S.C., Ihle J.N., Hirai Y., Ogawa M. Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc Natl Acad Sci U S A 1987, 84:9035-9039.
67. Maddaluno M., Di Lauro M., Di Pascale A., Santamaria R., Guglielmotti A., Grassia G., et al. Monocyte chemotactic protein-3 induces human coronary smooth muscle cell proliferation. Atherosclerosis 2011, 217:113-119.
68. Ouyang W., Rutz S., Crellin N.K., Valdez P.A., Hymowitz S.G. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 2011, 29:71-109.