Intra-articular injection of human mesenchymal stem cells (MSCs) promote rat meniscal regeneration by being activated to express Indian hedgehog that enhances expression of type II collagen

Osteoarthritis and Cartilage

Volumn 20, Issue 10, 2012, Pages 1197-1207

  Horie, M ^a,b   Choi, H ^a   Lee, R H ^a   Reger, R L ^a   Ylostalo, J ^a   Muneta, T ^b   Sekiya, I ^b   Prockop, D J ^a  

^a SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Bone morphogenetic protein 2; Indian hedgehog; Meniscus; MSCs; Parathyroid hormone like hormone

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 2; HORMONE; PARATHYROID HORMONE LIKE HORMONE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; KNEE; KNEE MENISCUS; KNEE OSTEOARTHRITIS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE REGENERATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELL COUNT; CELL TRANSPLANTATION; COLLAGEN TYPE II; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HEDGEHOG PROTEINS; HUMANS; INJECTIONS, INTRA-ARTICULAR; MALE; MENISCI, TIBIAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RATS; RATS, INBRED LEW; REGENERATION;

EID: 84865288291     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2012.06.002     Document Type: Article

References (50)

1. Chen F.H., Rousche K.T., Tuan R.S. Technology insight: adult stem cells in cartilage regeneration and tissue engineering. Nat Clin Pract Rheumatol 2006, 2:373-382.
2. Wieland H.A., Michaelis M., Kirschbaum B.J., Rudolphi K.A. Osteoarthritis - an untreatable disease?. Nat Rev Drug Discov 2005, 4:331-344.
3. Sgaglione N.A., Steadman J.R., Shaffer B., Miller M.D., Fu F.H. Current concepts in meniscus surgery: resection to replacement. Arthroscopy 2003, 19(Suppl 1):161-188.
4. Giordano A., Galderisi U., Marino I.R. From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J Cell Physiol 2007, 211:27-35.
5. Prockop D.J., Olson S.D. Clinical trials with adult stem/progenitor cells for tissue repair: let's not overlook some essential precautions. Blood 2007, 109:3147-3151.
6. Abdel-Hamid M., Hussein M.R., Ahmad A.F., Elgezawi E.M. Enhancement of the repair of meniscal wounds in the red-white zone (middle third) by the injection of bone marrow cells in canine animal model. Int J Exp Pathol 2005, 86:117-123.
7. Horie M., Sekiya I., Muneta T., Ichinose S., Matsumoto K., Saito H., et al. Intra-articular injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 2009, 27:878-887.
8. Murphy J.M., Fink D.J., Hunziker E.B., Barry F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 2003, 48:3464-3474.
9. Caplan A.I., Dennis J.E. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006, 98:1076-1084.
10. Prockop D.J., Kota D.J., Bazhanov N., Reger R.L. Evolving paradigms for repair of tissues by adult stem/progenitor cells (MSCs). J Cell Mol Med 2010, 14:2190-2199.
11. Skalnikova H., Motlik J., Gadher S.J., Kovarova H. Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines. Proteomics 2011, 11:691-708.
12. Sekiya I., Larson B.L., Smith J.R., Pochampally R., Cui J.G., Prockop D.J. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002, 20:530-541.
13. Javazon E.H., Colter D.C., Schwarz E.J., Prockop D.J. Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 2001, 19:219-225.
14. Pritzker K.P., Gay S., Jimenez S.A., Ostergaard K., Pelletier J.P., Revell P.A., et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 2006, 14:13-29.
15. Lee R.H., Pulin A.A., Seo M.J., Kota D.J., Ylostalo J., Larson B.L., et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009, 5:54-63.
16. Nishida Y., Sugahara-Kobayashi M., Takahashi Y., Nagata T., Ishikawa K., Asai S. Screening for control genes in mouse hippocampus after transient forebrain ischemia using high-density oligonucleotide array. J Pharmacol Sci 2006, 101:52-57.
17. Baldwin C.T., Reginato A.M., Smith C., Jimenez S.A., Prockop D.J. Structure of cDNA clones coding for human type II procollagen. The alpha 1(II) chain is more similar to the alpha 1(I) chain than two other alpha chains of fibrillar collagens. Biochem J 1989, 262:521-528.
18. Ohtaki H., Ylostalo J.H., Foraker J.E., Robinson A.P., Reger R.L., Shioda S., et al. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A 2008, 105:14638-14643.
19. Ylostalo J., Bazhanov N., Prockop D.J. Reversible commitment to differentiation by human multipotent stromal cells in single-cell-derived colonies. Exp Hematol 2008, 36:1390-1402.
20. Minina E., Kreschel C., Naski M.C., Ornitz D.M., Vortkamp A. Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 2002, 3:439-449.
21. Minina E., Wenzel H.M., Kreschel C., Karp S., Gaffield W., McMahon A.P., et al. BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 2001, 128:4523-4534.
22. Lipinski R.J., Hutson P.R., Hannam P.W., Nydza R.J., Washington I.M., Moore R.W., et al. Dose- and route-dependent teratogenicity, toxicity, and pharmacokinetic profiles of the hedgehog signaling antagonist cyclopamine in the mouse. Toxicol Sci 2008, 104:189-197.
23. Levi B., James A.W., Nelson E.R., Li S., Peng M., Commons G.W., et al. Human adipose-derived stromal cells stimulate autogenous skeletal repair via paracrine Hedgehog signaling with calvarial osteoblasts. Stem Cells Dev 2011, 20:243-257.
24. Fibbe W.E., Nauta A.J., Roelofs H. Modulation of immune responses by mesenchymal stem cells. Ann N Y Acad Sci 2007, 1106:272-278.
25. Le Blanc K. Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 2006, 8:559-561.
26. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008, 8:726-736.
27. Larson B.L., Ylostalo J., Prockop D.J. Human multipotent stromal cells undergo sharp transition from division to development in culture. Stem Cells 2008, 26:193-201.
28. Lee R.H., Hsu S.C., Munoz J., Jung J.S., Lee N.R., Pochampally R., et al. A subset of human rapidly self-renewing marrow stromal cells preferentially engraft in mice. Blood 2006, 107:2153-2161.
29. Katoh Y., Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med 2009, 9:873-886.
30. Lin A.C., Seeto B.L., Bartoszko J.M., Khoury M.A., Whetstone H., Ho L., et al. Modulating hedgehog signaling can attenuate the severity of osteoarthritis. Nat Med 2009, 15:1421-1425.
31. Fischer J., Dickhut A., Rickert M., Richter W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 2010, 62:2696-2706.
32. Sekiya I., Vuoristo J.T., Larson B.L., Prockop D.J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci U S A 2002, 99:4397-4402.
33. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
34. Deschaseaux F., Sensebe L., Heymann D. Mechanisms of bone repair and regeneration. Trends Mol Med 2009, 15:417-429.
35. Bien-Willner G.A., Stankiewicz P., Lupski J.R. SOX9cre1, a cis-acting regulatory element located 1.1 Mb upstream of SOX9, mediates its enhancement through the SHH pathway. Hum Mol Genet 2007, 16:1143-1156.
36. Park J., Zhang J.J., Moro A., Kushida M., Wegner M., Kim P.C. Regulation of Sox9 by Sonic Hedgehog (Shh) is essential for patterning and formation of tracheal cartilage. Dev Dyn 2010, 239:514-526.
37. Kim Y.J., Kim H.J., Im G.I. PTHrP promotes chondrogenesis and suppresses hypertrophy from both bone marrow-derived and adipose tissue-derived MSCs. Biochem Biophys Res Commun 2008, 373:104-108.
38. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
39. Huang W., Chung U.I., Kronenberg H.M., de Crombrugghe B. The chondrogenic transcription factor Sox9 is a target of signaling by the parathyroid hormone-related peptide in the growth plate of endochondral bones. Proc Natl Acad Sci U S A 2001, 98:160-165.
40. Rabie A.B., Hagg U. Factors regulating mandibular condylar growth. Am J Orthod Dentofacial Orthop 2002, 122:401-409.
41. Amling M., Neff L., Tanaka S., Inoue D., Kuida K., Weir E., et al. Bcl-2 lies downstream of parathyroid hormone-related peptide in a signaling pathway that regulates chondrocyte maturation during skeletal development. J Cell Biol 1997, 136:205-213.
42. Feng L., Balakir R., Precht P., Horton W.E. Bcl-2 regulates chondrocyte morphology and aggrecan gene expression independent of caspase activation and full apoptosis. J Cell Biochem 1999, 74:576-586.
43. Aikawa T., Shirasuna K., Iwamoto M., Watatani K., Nakamura T., Okura M., et al. Establishment of bone morphogenetic protein 2 responsive chondrogenic cell line. J Bone Miner Res 1996, 11:544-553.
44. Duprez D.M., Coltey M., Amthor H., Brickell P.M., Tickle C. Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 1996, 174:448-452.
45. Sekiya I., Larson B.L., Vuoristo J.T., Reger R.L., Prockop D.J. Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 2005, 320:269-276.
46. Glansbeek H.L., van Beuningen H.M., Vitters E.L., Morris E.A., van der Kraan P.M., van den Berg W.B. Bone morphogenetic protein 2 stimulates articular cartilage proteoglycan synthesis in vivo but does not counteract interleukin-1alpha effects on proteoglycan synthesis and content. Arthritis Rheum 1997, 40:1020-1028.
47. van Beuningen H.M., Glansbeek H.L., van der Kraan P.M., van den Berg W.B. Differential effects of local application of BMP-2 or TGF-beta 1 on both articular cartilage composition and osteophyte formation. Osteoarthritis Cartilage 1998, 6:306-317.
48. Bhargava M.M., Attia E.T., Murrell G.A., Dolan M.M., Warren R.F., Hannafin J.A. The effect of cytokines on the proliferation and migration of bovine meniscal cells. Am J Sports Med 1999, 27:636-643.
49. Seki K., Hata A. Indian hedgehog gene is a target of the bone morphogenetic protein signaling pathway. J Biol Chem 2004, 279:18544-18549.
50. Cannon W.D., Vittori J.M. The incidence of healing in arthroscopic meniscal repairs in anterior cruciate ligament-reconstructed knees versus stable knees. Am J Sports Med 1992, 20:176-181.