Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12

BMC Cell Biology

Volumn 10, Issue , 2009, Pages

  Violini, Stefania ^a   Ramelli, Paola ^a   Pisani, Laura F ^a   Gorni, Chiara ^a   Mariani, Paola ^a  

^a PARCO TECNOLOGICO PADANO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 12; DECORIN; GLYCOPROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TENOMODULIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN; HOMEODOMAIN PROTEIN; MEMBRANE PROTEIN; PROTEOGLYCAN; SCLEROPROTEIN; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; HEMATOPOIETIC STEM CELL; HORSE; IN VITRO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOCYTE; PROTEIN EXPRESSION; TENDON; ANIMAL; BONE MARROW CELL; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM;

EQUIDAE;

ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HORSES; MEMBRANE PROTEINS; MESENCHYMAL STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; PROTEOGLYCANS; SOXB1 TRANSCRIPTION FACTORS; TENDONS;

EID: 65549114268     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-10-29     Document Type: Article

References (57)

1. Stevens M Stem cells in regenerative medicine The Pharmaceutical Journal 2005, 275:695-698
2. Mimeault M Batra SK Concise review: Recent advances on the significance of stem cells in tissue regeneration and cancer therapies STEM CELLS 2006, 24:2319-2345. 10.1634/stemcells.2006-0066 16794264
3. Kemp KC Hows J Donaldson C Bone marrow-derived mesenchymal stem cells Leuk Lymphoma 2005, 46:1531-1544. 10.1080/10428190500215076 16236607
4. Helder MN Knippenberg M Klein-Nulend J Wuisman PI Stem Cells from Adipose Tissue Allow Challenging New Concepts for Regenerative Medicine Tissue Eng 2007, 13:1799-1808. 10.1089/ten.2006.0165 17518736
5. Weiss ML Troyer DL Stem cells in the umbilical cord Stem Cell Rev 2006, 2:155-162. 17237554
6. Ilancheran S Michalska A Peh G Wallace EM Pera M Manuelpillai U Stem Cells Derived from Human Fetal Membranes Display Multi-Lineage Differentiation Potential Biol Reprod 2007, 7:577-88. 10.1095/ biolreprod.106.055244
7. Herzog EL Chai L Krause DS Plasticity of marrow-derived stem cells Blood 2003, 102:3483-3492. 10.1182/blood-2003-05-1664 12893756
8. Holtorf HL Jansen JA Mikos AG Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone J Biomed Mater Res A 2005, 72:326-334. 15657936
9. Bernardo ME Emons JA Karperien M Nauta AJ Willemze R Roelofs H Romeo S marchini A Rappold GA Vukevic S Localetlli F Fibbe WE Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources Connect Tissue Res 2007, 48:132-140. 10.1080/03008200701228464 17522996
10. Yoon YS Lee N Scadova H Myocardial regeneration with bone-marrow-derived stem cells Biol Cell 2005, 97:253-263. 10.1042/BC20040099 15762847
11. Potapova IA Gaudette GR Brink PR Robinson RB Rosen MR Cohen IS Doronin SV Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation and survival of endothelial cells in vitro STEM CELLS 2007, 25:1761-1768. 10.1634/stemcells.2007-0022 17395769
12. Bianco P Riminucci M Gronthos S Robey PG Bone marrow stromal stem cells: nature, biology, and potential applications STEM CELLS 2001, 19:180-192. 10.1634/stemcells.19-3-180 11359943
13. Bernard-Beaubois K Hecquet C Houcine O Hayem G Adolphe M Culture and characterization of juvenile rabbit tenocytes Cell Biol Toxicol 1997, 13:103-113. 10.1023/B:CBTO.0000010395.51944.2a 9049100
14. Kannus P Structure of the tendon connective tissue Scand J Med Sci Sports 2000, 10:312-320. 10.1034/j.1600-0838.2000.010006312.x 11085557
15. Rees SG Flannery CR Little CB Hughes CE Caterson B Dent CM Catabolism of aggrecan, decorin and biglycan in tendon Biochem J 2000. 1:181-188. 10.1042/0264-6021:3500181
16. Goh JC Ouyang HW Teoh SH Chan CK Lee EH Tissue-engineering approach to the repair and regeneration of tendons and ligaments Tissue Eng 2003, 9 (Suppl 1):31-44 10.1089/10763270360696969
17. Ahmed T Lutton JD Feldman E Tani K Asano S Abraham NG Gene transfer of alpha interferon into hematopoietic stem cells Leuk Res 1998, 22:119-124. 10.1016/S0145-2126(97)00133-1 9593468
18. Woo SL Hildebrand K Watanabe N Fenwick GA Papageorgiou CD Wang JH Tissue engineering of ligament and tendon healing Clin Orthop Relat Res 1999(Suppl 367):312-323. 10.1097/00003086-199910001-00030
19. Cao Y Vacanti JP Ma X Paige KT Upton J Chowanski Z Schloo B Langer R Vacanti CA Generation of neo-tendon using synthetic polymers seeded with tenocytes Transplant Proc 1994, 26:3390-3392. 7998187
20. Awad HA Butler DL Boivin GP Smith FN Malaviya P Huibregtse B Caplan AI Autologous mesenchymal stem cell-mediated repair of tendon Tissue Eng 1999, 5:267-277. 10.1089/ten.1999.5.267 10434073
21. Koob TJ Willis TA Qiu YS Hernandez DJ Biocompatibility of NDGA-polymerized collagen fibers. II. Attachment, proliferation, and migration of tendon fibroblasts in vitro J Biomed Mater Res 2001, 56:40-48. 10.1002/1097-4636(200107)56:1<40::AID-JBM1066>3.0.CO;2-I 11309789
22. Jozsa L Kvist M Kannus P Vieno T Järvinen M Lehto M Structure and macromolecular composition of the myotendineal junction. Histochemical, immunohistochemical and electron microscopic study of the rat calf muscles Acta Morphol Hung 1991, 39:287-297. 1844341
23. Schwarz R Colarusso L Doty P Maintenance of differentiation in primary cultures of avian tendon cells Exp Cell Res 1976, 102(63):71-10. 1016/ 0014-4827(76)90299-8 976346
24. Friedman MS Long MW Hankenson KD Osteogenic differentiation of human mesenchymal stem cells is regulated by bone morphogenetic protein-6 J Cell Biochem 2006, 98:538-554. 10.1002/jcb.20719 16317727
25. Wozney JM Bone morphogenetic proteins Prog Growth Factor Res 1989, 1:267-280. 10.1016/0955-2235(89)90015-X 2491264
26. Yu Y Bliss JP Bruce WJ Walsh WR Bone morphogenetic proteins and Smad expression in ovine tendon-bone healing Arthroscopy 2007, 23:205-210. 17276229
27. Wang QW Chen ZL Piao YJ Mesenchymal stem cells differentiate into tenocytes by bone morphogenetic protein (BMP) 12 gene transfer J Biosci Bioeng 2005, 100:418-422. 10.1263/jbb.100.418 16310731
28. Lou J Tu Y Burns M Silva MJ Manske P BPM-12 gene transfer augmentation of lacerated tendon repair J Orthop Res 2001, 19:1199-1202. 10.1016/ S0736-0266(01)00042-0 11781024
29. Mays RW van't Hof W Ting AE Perry R Deans R Development of adult pluripotent stem cell therapies for ischemic injury and disease Expert Opin Biol Ther 2007, 7:173-184. 10.1517/14712598.7.2.173 17250456
30. Shi W Wang H Pan G Geng Y Guo Y Pei D Regulation of the pluripotency marker Rex-1 by Nanog and Sox2 J Biol Chem 2006, 281:23319-23325. 10.1074/jbc.M601811200 16714766
31. Shukunami C Takimoto A Oro M Hitakyi Y Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes Dev Biol 2006, 298:234-247. 10.1016/j.ydbio.2006.06.036 16876153
32. Docheva D Hunziker EB Fassler R Fassler R Brandau O Tenomodulin is necessary for tenocyte proliferation and tendon maturation Mol Cell Biol 2005, 2:699-705. 10.1128/MCB.25.2.699-705.2005
33. Franchi M Trire A Quaranta M Orsini E Ottani V Collagen structure of tendon relates to function Scientific World Journal 2007, 7:404-420. 17450305
34. Crossett B Allen WR Stewart F A 19 kDa protein secreted by the endometrium of the mare is a novel member of the lipocalin family Biochem J 1996, 320:137-143. 1217908 8947478
35. Guest DJ Smith MR Allen WR Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: Preliminary study Equine Vet J 2008, 40:178-181. 10.2746/042516408X276942 18267891
36. Smith RK Korda M Blunn GW Goodship AE Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment Equine Vet J 2003, 35:99-102. 10.2746/042516403775467388 12553472
37. Fortier LA Nixon AJ Williams J Cable CS Isolation and chondrocytic differentiation of equine bone marrow-derived mesenchymal stem cells Am J Vet Res 1998, 59:1182-1187. 9736400
38. Vidal MA Kilroy GE Johnson JR Lopez MJ Moore RM Gimble JM Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stromal cells: Adipogenic and osteogenic capacity Vet Surg 2006, 35:601-610. 10.1111/j.1532-950X.2006.00197.x 17026544
39. Lee RH Kim B Choi I Kim H Choi HS Suh K Bae YC Jung JS Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue Cell Physiol Biochem 2004, 14:311-324. 10.1159/ 000080341 15319535
40. Winter A Breit S Parsch D Benz K Steck E Hauner H Weber RM Ewerbeck V Richter W Cartilage-like gene expression in differentiated human stem cell spheroids: A comparison of bone marrow-derived and adipose tissue-derived stromal cells Arthritis Rheum 2003, 48:418-419. 10.1002/ art.10767 12571852
41. Kisiday JD Kopesky PW Evans CH Grodzinsky AJ McIlwraith CW Frisbie DD valuation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures J Orthop Res 2008, 26:E322-331. 10.1002/jor.20508
42. 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, 52:2521-2529. 10.1002/art.21212 16052568
43. Richardson LE Dudhia J Clegg PD Smith R Stem cells in veterinary medicine-attempts at regenerating equine tendon after injury Trends Biotechnol 2007, 25:409-416. 10.1016/j.tibtech.2007.07.009 17692415
44. Reed SA Johnson SE Equine umbilical cord blood contains a population of stem cells that express Oct4 and differentiate into mesodermal and endodermal cell types J Cell Physiol 2008, 215:329-336. 10.1002/ jcp.21312 17929245
45. Kadiyala S Young RG Thiede MA Bruder SP Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro Cell Transplant 1997, 6:125-134. 10.1016/S0963-6897(96)00279-5 9142444
46. Izadpanah R Joswig T Tsien F Dufour J Kirijan JC Bunnel BA Characterization of multipotent mesenchymal stem cells from the bone marrow of rhesus macaques Stem Cells Dev 2005, 14:440-451. 10.1089/ scd.2005.14.440 16137233
47. Saito S Sawai K Minamihashi Am Ugai H Yokoyama KK Derivation, maintenance, and induction of the differentiation in vitro of equine embryonic stem cells Methods Mol Biol 2006, 329:59-79. 16845984
48. Hoynowski SM Fry MM Gardner BM Leming MT Tucker JR Black L Sand T Mitchell KE Characterization and differentiation of equine umbilical cord-derived matrix cells Biochemical and Biophysical Research Communications 2007, 362:347-353. 10.1016/j.bbrc.2007.07.182
49. Anjos-Afonso F Bonnet D Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment Blood 2007, 109:1298-1306. 10.1182/ blood-2006-06-030551 17003364
50. Chong AK Ang AD Goh JC Hui JH Lim AY Lee EH Lim BH Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model J Bone Joint Surg Am 2007, 89:74-81. 10.2106/ JBJS.E.01396 17200313
51. Herthel DJ Enhanced suspenspory ligament healing in 100 horses by stem cell and other bone marrow components Proceedings of the 47th AAEP Annual Convention: November 24-28, 2001 San Diego (CA). American Association of Equine Practitioners 2001, 47:319-321
52. Pacini S Spinabella S Trombi L Fazzi R Galimberti S Dini F Carlucci F Petrini M Suspension of Bone Marrow-Derived Undifferentiated Mesenchymal Stromal Cells for Repair of Superficial Digital Flexor Tendon in Race Horses Tissue Eng 2007, 13:2949-2955. 10.1089/ten.2007.0108 17919069
53. Ouyang HW Goh JC Mo XM Teoh SH Lee EH The efficacy of bone marrow stromal cell-seeded knitted PLGA fiber scaffold for Achilles tendon repair Ann N Y Acad Sci 2002, 961:126-129. 12081880
54. Tasso R Augello A Carida' M Postiglione F Tibiletti MG Bernasconi B Astigiano S Fais F Truini M Cancedda R Pennesi G Development of sarcomas in mice implanted with mesenchymal stem cells seeded onto bioscaffolds Carcinogenesis 2009, 30:150-157. 10.1093/carcin/bgn234 18849298
55. Horisberger MA A method for prolonged survival of primary cell lines In Vitro Cell Dev Biol Anim 2006. 42:143-148. 10.1290/0511081.1 16848633
56. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001, 25:402-408. 10.1006/meth.2001.1262 11846609
57. Sheehan DC Hrapchak BB Theory and practice of histotechnology St. Louis: Mosby 2 1980