The influence of sex on the chondrogenic potential of muscle-derived stem cells implications for cartilage regeneration and repair

Arthritis and Rheumatism

Volumn 58, Issue 12, 2008, Pages 3809-3819

  Matsumoto, Tomoyuki ^a   Kubo, Seiji ^a   Meszaros, Laura B ^a   Corsi, Karin A ^a   Cooper, Gregory M ^a   Li, Guangheng ^a   Usas, Arvydas ^a   Osawa, Aki ^a   Fu, Freddie H ^b   Huard, Johnny ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; BONE MORPHOGENETIC PROTEIN 4; CELL MARKER;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; ARTICULAR CARTILAGE; CELL ADHESION; CELL DIFFERENTIATION; CELL REGENERATION; CHONDROGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FEMUR; GENETIC TRANSDUCTION; HISTOLOGY; IN VITRO STUDY; MALE; MOUSE; MUSCLE; MUSCLE DERIVED STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; STEM CELL;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARTILAGE; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROGENESIS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OSTEOARTHRITIS; RATS; RATS, NUDE; REGENERATION; SEX CHARACTERISTICS; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE ENGINEERING; TRANSDUCTION, GENETIC;

EID: 57349105071     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.24125     Document Type: Article

References (49)

1. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994;331:889-95.
2. Browne JE, Anderson AF, Arciero R, Mandelbaum B, Moseley JB Jr, Micheli LJ, et al. Clinical outcome of autologous chondrocyte implantation at 5 years in US subjects. Clin Orthop Relat Res 2005:237-45.
3. Benz K, Breit S, Lukoschek M, Mau H, Richter W. Molecular analysis of expansion, differentiation, and growth factor treatment of human chondrocytes identifies differentiation markers and growth-related genes. Biochem Biophys Res Commun 2002;293:284-92.
4. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-42.
5. Richter W. Cell-based cartilage repair: illusion or solution for osteoarthritis. Curr Opin Rheumatol 2007;19:451-6.
6. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
7. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG. Circulating skeletal stem cells. J Cell Biol 2001;153:1133-40.
8. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-95.
9. Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 2005;23:220-9.
10. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 2002;157:851-64.
11. Oshima H, Payne TR, Urish KL, Sakai T, Ling Y, Gharaibeh B, et al. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther 2005;12:1130-41.
12. Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, et al. Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell 2005;16:3323-33.
13. Wakitani S, Yamamoto T. Response of the donor and recipient cells in mesenchymal cell transplantation to cartilage defect. Microsc Res Tech 2002;58:14-8.
14. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994;76:579-92.
15. Koga H, Muneta T, Ju YJ, Nagase T, Nimura A, Mochizuki T, et al. Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells 2007;25:689-96.
16. Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002;10:199-206.
17. Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, et al. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007;15:226-31.
18. Cao B, Zheng B, Jankowski RJ, Kimura S, Ikezawa M, Deasy B, et al. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 2003;5:640-6.
19. Jankowski RJ, Deasy BM, Cao B, Gates C, Huard J. The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells. J Cell Sci 2002;115(Pt 22):4361-74.
20. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 2000;150:1085-100.
21. Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, et al. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 2002;110:751-9.
22. Shen HC, Peng H, Usas A, Gearhart B, Cummins J, Fu FH, et al. Ex vivo gene therapy-induced endochondral bone formation: comparison of muscle-derived stem cells and different subpopulations of primary muscle-derived cells. Bone 2004;34:982-92.
23. Wright V, Peng H, Usas A, Young B, Gearhart B, Cummins J, et al. BMP4-expressing muscle-derived stem cells differentiate into osteogenic lineage and improve bone healing in immunocompetent mice. Mol Ther 2002;6:169-78.
24. Adachi N, Sato K, Usas A, Fu FH, Ochi M, Han CW, et al. Muscle derived, cell based ex vivo gene therapy for treatment of full thickness articular cartilage defects. J Rheumatol 2002;29:1920-30.
25. Kuroda R, Usas A, Kubo S, Corsi K, Peng H, Rose T, et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum 2006;54:433-42.
26. Crisostomo PR, Markel TA, Wang M, Lahm T, Lillemoe KD, Meldrum DR. In the adult mesenchymal stem cell population, source gender is a biologically relevant aspect of protective power. Surgery 2007;142:215-21.
27. Horner S, Pasternak G, Hehlmann R. A statistically significant sex difference in the number of colony-forming cells from human peripheral blood. Ann Hematol 1997;74:259-63.
28. Faiola B, Fuller ES, Wong VA, Pluta L, Abernethy DJ, Rose J, et al. Exposure of hematopoietic stem cells to benzene or 1,4-benzoquinone induces gender-specific gene expression. Stem Cells 2004;22:750-8.
29. Deasy BM, Lu A, Tebbets JC, Feduska JM, Schugar RC, Pollett JB, et al. A role for cell sex in stem cell-mediated skeletal muscle regeneration: female cells have higher muscle regeneration efficiency. J Cell Biol 2007;177:73-86.
30. Corsi KA, Pollett JB, Phillippi JA, Usas A, Li G, Huard J. Osteogenic potential of postnatal skeletal muscle-derived stem cells is influenced by donor sex. J Bone Miner Res 2007;22:1592-602.
31. Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, et al. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc 2008;3:1501-9.
32. Peng H, Usas A, Gearhart B, Young B, Olshanski A, Huard J. Development of a self-inactivating tet-on retroviral vector expressing bone morphogenetic protein 4 to achieve regulated bone formation. Mol Ther 2004;9:885-94.
33. Peng H, Chen ST, Wergedal JE, Polo JM, Yee JK, Lau KH, et al. Development of an MFG-based retroviral vector system for secretion of high levels of functionally active human BMP4. Mol Ther 2001;4:95-104.
34. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998;238:265-72.
35. Jadlowiec J, Koch H, Zhang X, Campbell PG, Seyedain M, Sfeir C. Phosphophoryn regulates the gene expression and differentiation of NIH3T3, MC3T3-E1, and human mesenchymal stem cells via the integrin/MAPK signaling pathway. J Biol Chem 2004;279:53323-30.
36. Jadlowiec JA, Zhang X, Li J, Campbell PG, Sfeir C. Extracellular matrix-mediated signaling by dentin phosphophoryn involves activation of the Smad pathway independent of bone morphogenetic protein. J Biol Chem 2006;281:5341-7.
37. O'Driscoll SW, Keeley FW, Salter RB. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion: a follow-up report at one year. J Bone Joint Surg Am 1988;70:595-606.
38. Hatakeyama Y, Tuan RS, Shum L. Distinct functions of BMP4 and GDF5 in the regulation of chondrogenesis. J Cell Biochem 2004;91:1204-17.
39. Hoffman LM, Garcha K, Karamboulas K, Cowan MF, Drysdale LM, Horton WA, et al. BMP action in skeletogenesis involves attenuation of retinoid signaling. J Cell Biol 2006;174:101-13.
40. Sekiya I, Larson BL, Vuoristo JT, Reger RL, Prockop DJ. 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;320:269-76.
41. Shirasawa S, Sekiya I, Sakaguchi Y, Yagishita K, Ichinose S, Muneta T. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem 2006;97:84-97.
42. Semba I, Nonaka K, Takahashi I, Takahashi K, Dashner R, Shum L, et al. Positionally-dependent chondrogenesis induced by BMP4 is co-regulated by Sox9 and Msx2. Dev Dyn 2000;217:401-14.
43. Zheng B, Cao B, Li G, Huard J. Mouse adipose-derived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng 2006;12:1891-901.
44. Hachisuka H, Mochizuki Y, Yasunaga Y, Natsu K, Sharman P, Shinomiya R, et al. Flow cytometric discrimination of mesenchymal progenitor cells from bone marrow-adherent cell populations using CD34/44/45(-) and Sca-1(+) markers. J Orthop Sci 2007;12:161-9.
45. Yoshida S, Shimmura S, Nagoshi N, Fukuda K, Matsuzaki Y, Okano H, et al. Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells 2006;24:2714-22.
46. Felson DT, Lawrence RC, Dieppe PA, Hirsch R, Helmick CG, Jordan JM, et al. Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 2000;133:635-46.
47. Ding C, Cicuttini F, Scott F, Glisson M, Jones G. Sex differences in knee cartilage volume in adults: role of body and bone size, age and physical activity. Rheumatology (Oxford) 2003;42:1317-23.
48. Jones G, Glisson M, Hynes K, Cicuttini F. Sex and site differences in cartilage development: a possible explanation for variations in knee osteoarthritis in later life. Arthritis Rheum 2000;43:2543-9.
49. Csintalan RP, Schulz MM, Woo J, McMahon PJ, Lee TQ. Gender differences in patellofemoral joint biomechanics. Clin Orthop Relat Res 2002:260-9.