Isolation and characterization of human mesenchymal stem cells derived from shoulder tissues involved in rotator cuff tears

American Journal of Sports Medicine

Volumn 41, Issue 3, 2013, Pages 657-668

  Utsunomiya, Hajime ^a   Uchida, Soshi ^a   Sekiya, Ichiro ^b   Sakai, Akinori ^a   Moridera, Kuniaki ^a   Nakamura, Toshitaka ^a  

^a UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

biological augmentation; regeneration therapy of shoulder; rotator cuff repair surgery; synovial mesenchymal stem cells (MSCs)

Indexed keywords

BMP2 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM BINDING PROTEIN; CD56 ANTIGEN; CONNEXIN 26; CXCL2 CHEMOKINE; CXCL2 PROTEIN, HUMAN; EPITOPE; GAP JUNCTION PROTEIN; MEMBRANE PROTEIN; NCAM1 PROTEIN, HUMAN; NERVE GROWTH FACTOR; PROTEIN S 100; S 100 CALCIUM BINDING PROTEIN BETA SUBUNIT; S-100 CALCIUM-BINDING PROTEIN BETA SUBUNIT; SERRATE PROTEINS; SIGNAL PEPTIDE; SOMATOMEDIN C;

ADIPOGENESIS; ARTHROSCOPY; ARTICLE; BONE DEVELOPMENT; CELL CULTURE; CELL SURVIVAL; CHONDROGENESIS; CLONOGENIC ASSAY; CYTOLOGY; DNA MICROARRAY; FEMALE; HUMAN; INJURY; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; PHYSIOLOGY; ROTATOR CUFF; SHOULDER; SYNOVIUM; TENDON;

ADIPOGENESIS; ANTIGENS, CD56; ARTHROSCOPY; BONE MORPHOGENETIC PROTEIN 2; CALCIUM-BINDING PROTEINS; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINE CXCL2; CHONDROGENESIS; COLONY-FORMING UNITS ASSAY; CONNEXINS; EPITOPES; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; NERVE GROWTH FACTORS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOGENESIS; ROTATOR CUFF; S100 PROTEINS; SHOULDER JOINT; SYNOVIAL MEMBRANE; TENDONS;

EID: 84874927165     PISSN: 03635465     EISSN: 15523365     Source Type: Journal    
DOI: 10.1177/0363546512473269     Document Type: Article

References (52)

1. Arai F, Ohneda O, Miyamoto T, Zhang XQ, Suda T. Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med. 2002 ; 195 (12). 1549-1563
2. Aubin JE. Osteoprogenitor cell frequency in rat bone marrow stromal populations: role for heterotypic cell-cell interactions in osteoblast differentiation. J Cell Biochem. 1999 ; 72 (3). 396-410
3. Barry FP, Boynton RE, Haynesworth S, Murphy JM, Zaia J. The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem Biophys Res Commun. 1999 ; 265 (1). 134-139
4. Bedi A, Fox AJ, Kovacevic D, Deng XH, Warren RF, Rodeo SA. Doxycycline-mediated inhibition of matrix metalloproteinases improves healing after rotator cuff repair. Am J Sports Med. 2010 ; 38 (2). 308-317
5. Benjamin M, Moriggl B, Brenner E, Emery P, McGonagle D, Redman S. The "enthesis organ" concept: why enthesopathies may not present as focal insertional disorders. Arthritis Rheum. 2004 ; 50 (10). 3306-3313
6. Bi Y, Ehirchiou D, Kilts TM, et al. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med. 2007 ; 13 (10). 1219-1227
7. Boileau P, Brassart N, Watkinson DJ, Carles M, Hatzidakis AM, Krishnan SG. Arthroscopic repair of full-thickness tears of the supraspinatus: does the tendon really heal?. J Bone Joint Surg Am. 2005 ; 87 (6). 1229-1240
8. Calfee RP, Patel A, DaSilva MF, Akelman E. Management of lateral epicondylitis: current concepts. J Am Acad Orthop Surg. 2008 ; 16 (1). 19-29
9. Colter DC, Sekiya I, Prockop DJ. 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. 2001 ; 98 (14). 7841-7845
10. Dalle Carbonare L, Valenti MT, Zanatta M, Donatelli L, Lo Cascio V. Circulating mesenchymal stem cells with abnormal osteogenic differentiation in patients with osteoporosis. Arthritis Rheum. 2009 ; 60 (11). 3356-3365
11. Digirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. 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. 1999 ; 107 (2). 275-281
12. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006 ; 8 (4). 315-317
13. Eghbali-Fatourechi GZ, Lamsam J, Fraser D, Nagel D, Riggs BL, Khosla S. Circulating osteoblast-lineage cells in humans. N Engl J Med. 2005 ; 352 (19). 1959-1966
14. Eghbali-Fatourechi GZ, Modder UI, Charatcharoenwitthaya N, et al. Characterization of circulating osteoblast lineage cells in humans. Bone. 2007 ; 40 (5). 1370-1377
15. Faissner A, Heck N, Dobbertin A, Garwood J. DSD-1-proteoglycan/phosphacan and receptor protein tyrosine phosphatase-beta isoforms during development and regeneration of neural tissues. Adv Exp Med Biol. 2006 ; 557: 25-53
16. Fan J, Varshney RR, Ren L, Cai D, Wang DA. Synovium-derived mesenchymal stem cells: a new cell source for musculoskeletal regeneration. Tissue Eng Part B Rev. 2009 ; 15 (1). 75-86
17. Galatz LM, Ball CM, Teefey SA, Middleton WD, Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am. 2004 ; 86 (2). 219-224
18. Galatz LM, Sandell LJ, Rothermich SY, et al. Characteristics of the rat supraspinatus tendon during tendon-to-bone healing after acute injury. J Orthop Res. 2006 ; 24 (3). 541-550
19. Goutallier D, Postel JM, Gleyze P, Leguilloux P, Van Driessche S. Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears. J Shoulder Elbow Surg. 2003 ; 12 (6). 550-554
20. Gulotta LV, Kovacevic D, Ehteshami JR, Dagher E, Packer JD, Rodeo SA. Application of bone marrow-derived mesenchymal stem cells in a rotator cuff repair model. Am J Sports Med. 2009 ; 37 (11). 2126-2133
21. Gulotta LV, Kovacevic D, Montgomery S, Ehteshami JR, Packer JD, Rodeo SA. Stem cells genetically modified with the developmental gene MT1-MMP improve regeneration of the supraspinatus tendon-to-bone insertion site. Am J Sports Med. 2010 ; 38 (7). 1429-1437
22. Hashimoto T, Nobuhara K, Hamada T. Pathologic evidence of degeneration as a primary cause of rotator cuff tear. Clin Orthop Relat Res. 2003 ; 415: 111-120
23. Hirose K, Kondo S, Choi HR, Mishima S, Iwata H, Ishiguro N. Spontaneous healing process of a supraspinatus tendon tear in rabbits. Arch Orthop Trauma Surg. 2004 ; 124 (6). 374-377
24. Ide J, Kikukawa K, Hirose J, et al. The effect of a local application of fibroblast growth factor-2 on tendon-to-bone remodeling in rats with acute injury and repair of the supraspinatus tendon. J Shoulder Elbow Surg. 2009 ; 18 (3). 391-398
25. Jones EA, Kinsey SE, English A, et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002 ; 46 (12). 3349-3360
26. Ju YJ, Muneta T, Yoshimura H, Koga H, Sekiya I. Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing. Cell Tissue Res. 2008 ; 332 (3). 469-478
27. Koga H, Muneta T, Ju YJ, et al. Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells. 2007 ; 25 (3). 689-696
28. Koga H, Muneta T, Nagase T, et al. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res. 2008 ; 333 (2). 207-215
29. Lafosse L, Brozska R, Toussaint B, Gobezie R. The outcome and structural integrity of arthroscopic rotator cuff repair with use of the double-row suture anchor technique. J Bone Joint Surg Am. 2007 ; 89 (7). 1533-1541
30. Mazzocca AD, McCarthy MB, Chowaniec DM, Cote MP, Arciero RA, Drissi H. Rapid isolation of human stem cells (connective tissue progenitor cells) from the proximal humerus during arthroscopic rotator cuff surgery. Am J Sports Med. 2010 ; 38 (7). 1438-1447
31. Mochizuki T, Muneta T, Sakaguchi Y, et al. Higher chondrogenic potential of fibrous synovium- and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum. 2006 ; 54 (3). 843-853
32. Morito T, Muneta T, Hara K, et al. Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans. Rheumatology (Oxford). 2008 ; 47 (8). 1137-1143
33. Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum. 2002 ; 46 (3). 704-713
34. Nourissat G, Diop A, Maurel N, et al. Mesenchymal stem cell therapy regenerates the native bone-tendon junction after surgical repair in a degenerative rat model. PLoS One. 2010 ; 5 (8). e12248
35. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999 ; 284 (5411). 143-147
36. Prockop DJ, Gregory CA, Spees JL. One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci U S A. 2003 ; 1: 11917-11923
37. Purpura KA, Aubin JE, Zandstra PW. Sustained in vitro expansion of bone progenitors is cell density dependent. Stem Cells. 2004 ; 22 (1). 39-50
38. Rees JD, Maffulli N, Cook J. Management of tendinopathy. Am J Sports Med. 2009 ; 37 (9). 1855-1867
39. Rodeo SA, Potter HG, Kawamura S, Turner AS, Kim HJ, Atkinson BL. Biologic augmentation of rotator cuff tendon-healing with use of a mixture of osteoinductive growth factors. J Bone Joint Surg Am. 2007 ; 89 (11). 2485-2497
40. Sakaguchi Y, Sekiya I, Yagishita K, Ichinose S, Shinomiya K, Muneta T. Suspended cells from trabecular bone by collagenase digestion become virtually identical to mesenchymal stem cells obtained from marrow aspirates. Blood. 2004 ; 104 (9). 2728-2735
41. 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 (8). 2521-2529
42. Seeherman HJ, Archambault JM, Rodeo SA, et al. rhBMP-12 accelerates healing of rotator cuff repairs in a sheep model. J Bone Joint Surg Am. 2008 ; 90 (10). 2206-2219
43. Segawa Y, Muneta T, Makino H, et al. Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. J Orthop Res. 2009 ; 27 (4). 435-441
44. Sekiya I, Colter DC, Prockop DJ. BMP-6 enhances chondrogenesis in a subpopulation of human marrow stromal cells. Biochem Biophys Res Commun. 2001 ; 284 (2). 411-418
45. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ. 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 (6). 530-541
46. Sekiya I, Larson BL, Vuoristo JT, Cui JG, Prockop DJ. Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res. 2004 ; 19 (2). 256-264
47. Sekiya I, Vuoristo JT, Larson BL, Prockop DJ. 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 (7). 4397-4402
48. Shimizu Y, Sakai A, Menuki K, et al. Reduced bone formation in alcohol-induced osteopenia is associated with elevated p21 expression in bone marrow cells in aldehyde dehydrogenase 2-disrupted mice. Bone. 2011 ; 48 (5). 1075-1086
49. Sugaya H, Maeda K, Matsuki K, Moriishi J. Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair: a prospective outcome study. J Bone Joint Surg Am. 2007 ; 89 (5). 953-960
50. Uhthoff HK, Sarkar K. Surgical repair of rotator cuff ruptures: the importance of the subacromial bursa. J Bone Joint Surg Br. 1991 ; 73 (3). 399-401
51. Ulici V, Hoenselaar KD, Gillespie JR, Beier F. The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev Biol. 2008 ; 8: 40
52. Williams GR, Rockwood CA, Bigliani LU, Iannotti JP, Stanwood W. Rotator cuff tears: why do we repair them?. J Bone Joint Surg Am. 2004 ; 86 (12). 2764-2776