Specification of chondrocytes and cartilage tissues from embryonic stem cells

Development (Cambridge)

Volumn 140, Issue 12, 2013, Pages 2597-2610

  Craft, April M ^a   Ahmed, Nazish ^b   Rockel, Jason S ^c   Baht, Gurpreet S ^c   Alma, Benjamin A ^c   Kandel, Rita A ^b   Grigoriadis, Agamemnon E ^d   Keller, Gordon M ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d GUY S HOSPITAL   (United Kingdom)

Author keywords

Cartilage; Chondrocyte; Embryonic stem cell; Induced pluripotent stem cell; Paraxial; Somite

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CARTILAGE TISSUE; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE EXPRESSION; GROWTH PLATE; IN VITRO STUDY; MESODERM; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE TRANSPLANTATION; TISSUES; VASCULARIZATION;

CARTILAGE; CHONDROCYTE; EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; PARAXIAL; SOMITE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELL LINEAGE; CHONDROCYTES; CHONDROGENESIS; EMBRYONIC STEM CELLS; FEMALE; GROWTH DIFFERENTIATION FACTOR 5; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; MESODERM; MICE; OSTEOBLASTS; OSTEOGENESIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SIGNAL TRANSDUCTION; TIME FACTORS;

ERINACEIDAE; MUS;

EID: 84878280580     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.087890     Document Type: Article

References (64)

1. Ahmed, N., Gan, L., Nagy, A., Zheng, J., Wang, C. and Kandel, R. A. (2009). Cartilage tissue formation using redifferentiated passaged chondrocytes in vitro. Tissue Eng. Part A 15, 665-673.
2. Akiyama, H., Chaboissier, M. C., Martin, J. F., Schedl, A. and de Crombrugghe, B. (2002). The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 16, 2813-2828.
3. Archer, C. W., Dowthwaite, G. P. and Francis-West, P. (2003). Development of synovial joints. Birth Defects 69, 144-155.
4. Blumer, M. J., Longato, S., Schwarzer, C. and Fritsch, H. (2007). Bone development in the femoral epiphysis of mice: the role of cartilage canals and the fate of resting chondrocytes. Dev. Dyn. 236, 2077-2088.
5. Brunet, L. J., McMahon, J. A., McMahon, A. P. and Harland, R. M. (1998). Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280, 1455-1457.
6. Burgess, R., Rawls, A., Brown, D., Bradley, A. and Olson, E. N. (1996). Requirement of the paraxis gene for somite formation and musculoskeletal patterning. Nature 384, 570-573.
7. Bussen, M., Petry, M., Schuster-Gossler, K., Leitges, M., Gossler, A. and Kispert, A. (2004). The T-box transcription factor Tbx18 maintains the separation of anterior and posterior somite compartments. Genes Dev. 18, 1209-1221.
8. Chen, J. K., Taipale, J., Cooper, M. K. and Beachy, P. A. (2002). Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16, 2743-2748.
9. Colnot, C. (2005). Cellular and molecular interactions regulating skeletogenesis. J. Cell. Biochem. 95, 688-697.
10. Dacquin, R., Starbuck, M., Schinke, T. and Karsenty, G. (2002). Mouse alpha1(I)-collagen promoter is the best known promoter to drive efficient Cre recombinase expression in osteoblast. Dev. Dyn. 224, 245-251.
11. Dao, D. Y., Jonason, J. H., Zhang, Y., Hsu, W., Chen, D., Hilton, M. J. and O'Keefe, R. J. (2012). Cartilage-specific β-catenin signaling regulates chondrocyte maturation, generation of ossification centers, and perichondrial bone formation during skeletal development. J. Bone Miner. Res. 27, 1680-1694.
12. Darabi, R., Gehlbach, K., Bachoo, R. M., Kamath, S., Osawa, M., Kamm, K. E., Kyba, M. and Perlingeiro, R. C. (2008). Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat. Med. 14, 134-143.
13. Fehling, H. J., Lacaud, G., Kubo, A., Kennedy, M., Robertson, S., Keller, G. and Kouskoff, V. (2003). Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130, 4217-4227.
14. Fletcher, R. B. and Harland, R. M. (2008). The role of FGF signaling in the establishment and maintenance of mesodermal gene expression in Xenopus. Dev. Dyn. 237, 1243-1254.
15. Gadue, P., Huber, T. L., Paddison, P. J. and Keller, G. M. (2006). Wnt and TGFbeta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Natl. Acad. Sci. USA 103, 16806-16811.
16. Gouon-Evans, V., Boussemart, L., Gadue, P., Nierhoff, D., Koehler, C. I., Kubo, A., Shafritz, D. A. and Keller, G. (2006). BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat. Biotechnol. 24, 1402-1411.
17. Guo, S., Zhou, J., Gao, B., Hu, J., Wang, H., Meng, J., Zhao, X., Ma, G., Lin, C., Xiao, Y. et al. (2010). Missense mutations in IHH impair Indian Hedgehog signaling in C3H10T1/2 cells: implications for brachydactyly type A1, and new targets for Hedgehog signaling. Cell. Mol. Biol. Lett. 15, 153-176.
18. Hatakeyama, Y., Tuan, R. S. and Shum, L. (2004). Distinct functions of BMP4 and GDF5 in the regulation of chondrogenesis. J. Cell. Biochem. 91, 1204-1217.
19. Hirsinger, E., Jouve, C., Dubrulle, J. and Pourquie, O. (2000). Somite formation and patterning. Int. Rev. Cytol. 198, 1-65.
20. Hwang, N. S., Kim, M. S., Sampattavanich, S., Baek, J. H., Zhang, Z. and Elisseeff, J. (2006). Effects of three-dimensional culture and growth factors on the chondrogenic differentiation of murine embryonic stem cells. Stem Cells 24, 284-291.
21. Hwang, Y. S., Polak, J. M. and Mantalaris, A. (2008). In vitro direct chondrogenesis of murine embryonic stem cells by bypassing embryoid body formation. Stem Cells Dev. 17, 971-978.
22. Jukes, J. M., Both, S. K., Leusink, A., Sterk, L. M., van Blitterswijk, C. A. and de Boer, J. (2008). Endochondral bone tissue engineering using embryonic stem cells. Proc. Natl. Acad. Sci. USA 105, 6840-6845.
23. Kattman, S. J., Witty, A. D., Gagliardi, M., Dubois, N. C., Niapour, M., Hotta, A., Ellis, J. and Keller, G. (2011). Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8, 228-240.
24. Kinder, S. J., Tsang, T. E., Quinlan, G. A., Hadjantonakis, A. K., Nagy, A. and Tam, P. P. (1999). The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126, 4691-4701.
25. Knosp, W. M., Saneyoshi, C., Shou, S., Bachinger, H. P. and Stadler, H. S. (2007). Elucidation, quantitative refinement, and in vivo utilization of the HOXA13 DNA binding site. J. Biol. Chem. 282, 6843-6853.
26. Koyama, E., Shibukawa, Y., Nagayama, M., Sugito, H., Young, B., Yuasa, T., Okabe, T., Ochiai, T., Kamiya, N., Rountree, R. B. et al. (2008). A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev. Biol. 316, 62-73.
27. Kramer, J., Hegert, C., Guan, K., Wobus, A. M., Muller, P. K. and Rohwedel, J. (2000). Embryonic stem cell-derived chondrogenic differentiation in vitro: activation by BMP-2 and BMP-4. Mech. Dev. 92, 193-205.
28. Kulesa, P. M. and Fraser, S. E. (2002). Cell dynamics during somite boundary formation revealed by time-lapse analysis. Science 298, 991-995.
29. LaPrade, R. F., Bursch, L. S., Olson, E. J., Havlas, V. and Carlson, C. S. (2008). Histologic and immunohistochemical characteristics of failed articular cartilage resurfacing procedures for osteochondritis of the knee: a case series. Am. J. Sports Med. 36, 360-368.
30. Lawrence, R. C., Felson, D. T., Helmick, C. G., Arnold, L. M., Choi, H., Deyo, R. A., Gabriel, S., Hirsch, R., Hochberg, M. C., Hunder, G. G. et al. (2008). Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum. 58, 26-35.
31. Lawson, K. A., Meneses, J. J. and Pedersen, R. A. (1991). Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
32. Lin, A. C., Seeto, B. L., Bartoszko, J. M., Khoury, M. A., Whetstone, H., Ho, L., Hsu, C., Ali, S. A. and Alman, B. A. (2009). Modulating hedgehog signaling can attenuate the severity of osteoarthritis. Nat. Med. 15, 1421-1425.
33. Long, F., Zhang, X. M., Karp, S., Yang, Y. and McMahon, A. P. (2001). Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128, 5099-5108.
34. Luche, H., Weber, O., Nageswara Rao, T., Blum, C. and Fehling, H. J. (2007). Faithful activation of an extra-bright red fluorescent protein in 'knock-in' Crereporter mice ideally suited for lineage tracing studies. Eur. J. Immunol. 37, 43-53.
35. Mankoo, B. S., Skuntz, S., Harrigan, I., Grigorieva, E., Candia, A., Wright, C. V., Arnheiter, H. and Pachnis, V. (2003). The concerted action of Meox homeobox genes is required upstream of genetic pathways essential for the formation, patterning and differentiation of somites. Development 130, 4655-4664.
36. Minina, E., Wenzel, H. M., Kreschel, C., Karp, S., Gaffield, W., McMahon, A. P. and Vortkamp, A. (2001). BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128, 4523-4534.
37. Murakami, S., Balmes, G., McKinney, S., Zhang, Z., Givol, D. and de Crombrugghe, B. (2004). Constitutive activation of MEK1 in chondrocytes causes Stat1-independent achondroplasia-like dwarfism and rescues the Fgfr3-deficient mouse phenotype. Genes Dev. 18, 290-305.
38. Nakayama, N., Duryea, D., Manoukian, R., Chow, G. and Han, C. Y. (2003). Macroscopic cartilage formation with embryonic stem-cell-derived mesodermal progenitor cells. J. Cell Sci. 116, 2015-2028.
39. Ng, A., Alman, B. and Grynpas, M. (2011). Development and validation of a mouse model of adynamic bone disease (ABD). J. Bone Miner. Res. Suppl. 1.
40. Nostro, M. C., Cheng, X., Keller, G. M. and Gadue, P. (2008). Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2, 60-71.
41. Ormestad, M., Astorga, J. and Carlsson, P. (2004). Differences in the embryonic expression patterns of mouse Foxf1 and -2 match their distinct mutant phenotypes. Dev. Dyn. 229, 328-333.
42. Pacifici, M., Koyama, E., Shibukawa, Y., Wu, C., Tamamura, Y., Enomoto- Iwamoto, M. and Iwamoto, M. (2006). Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Ann. New York Acad. Sci. 1068, 74-86.
43. Pelttari, K., Winter, A., Steck, E., Goetzke, K., Hennig, T., Ochs, B. G., Aigner, T. and Richter, W. (2006). Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 54, 3254-3266.
44. Pelttari, K., Steck, E. and Richter, W. (2008). The use of mesenchymal stem cells for chondrogenesis. Injury 39 Suppl. 1, S58-S65.
45. Rountree, R. B., Schoor, M., Chen, H., Marks, M. E., Harley, V., Mishina, Y. and Kingsley, D. M. (2004). BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol. 2, e355.
46. Singh, M. K., Petry, M., Haenig, B., Lescher, B., Leitges, M. and Kispert, A. (2005). The T-box transcription factor Tbx15 is required for skeletal development. Mech. Dev. 122, 131-144.
47. Stadtfeld, M., Maherali, N., Breault, D. T. and Hochedlinger, K. (2008). Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2, 230-240.
48. Steinert, A. F., Ghivizzani, S. C., Rethwilm, A., Tuan, R. S., Evans, C. H. and Noth, U. (2007). Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res. Ther. 9, 213.
49. Taipale, J., Chen, J. K., Cooper, M. K., Wang, B., Mann, R. K., Milenkovic, L., Scott, M. P. and Beachy, P. A. (2000). Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009.
50. Takakura, N., Yoshida, H., Ogura, Y., Kataoka, H., Nishikawa, S. and Nishikawa, S. (1997). PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. J. Histochem. Cytochem. 45, 883-893.
51. Tam, P. P. and Tan, S. S. (1992). The somitogenetic potential of cells in the primitive streak and the tail bud of the organogenesis-stage mouse embryo. Development 115, 703-715.
52. Tanaka, M., Jokubaitis, V., Wood, C., Wang, Y., Brouard, N., Pera, M., Hearn, M., Simmons, P. and Nakayama, N. (2009). BMP inhibition stimulates WNTdependent generation of chondrogenic mesoderm from embryonic stem cells. Stem Cell Res. 3, 126-141.
53. Tardif, G., Pelletier, J. P., Hum, D., Boileau, C., Duval, N. and Martel-Pelletier, J. (2006). Differential regulation of the bone morphogenic protein antagonist chordin in human normal and osteoarthritic chondrocytes. Ann. Rheum. Dis. 65, 261-264.
54. Tins, B. J., McCall, I. W., Takahashi, T., Cassar-Pullicino, V., Roberts, S., Ashton, B. and Richardson, J. (2005). Autologous chondrocyte implantation in knee joint: MR imaging and histologic features at 1-year follow-up. Radiology 234, 501-508.
55. Tsumaki, N., Nakase, T., Miyaji, T., Kakiuchi, M., Kimura, T., Ochi, T. and Yoshikawa, H. (2002). Bone morphogenetic protein signals are required for cartilage formation and differently regulate joint development during skeletogenesis. J. Bone Miner. Res. 17, 898-906.
56. Visnjic, D., Kalajzic, I., Gronowicz, G., Aguila, H. L., Clark, S. H., Lichtler, A. C. and Rowe, D. W. (2001). Conditional ablation of the osteoblast lineage in Col2.3deltatk transgenic mice. J. Bone Miner. Res. 16, 2222-2231.
57. Yamashita, A., Krawetz, R. and Rancourt, D. E. (2008). Loss of discordant cells during micro-mass differentiation of embryonic stem cells into the chondrocyte lineage. Cell Death Differ. 16, 278-286.
58. Yasuhara, R., Ohta, Y., Yuasa, T., Kondo, N., Hoang, T., Addya, S., Fortina, P., Pacifici, M., Iwamoto, M. and Enomoto-Iwamoto, M. (2011). Roles of betacatenin signaling in phenotypic expression and proliferation of articular cartilage superficial zone cells. Lab. Invest. 91, 1739-1752.
59. Ying, Q. L., Nichols, J., Chambers, I. and Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell selfrenewal in collaboration with STAT3. Cell 115, 281-292.
60. Yoon, B. S., Pogue, R., Ovchinnikov, D. A., Yoshii, I., Mishina, Y., Behringer, R. R. and Lyons, K. M. (2006). BMPs regulate multiple aspects of growth-plate chondrogenesis through opposing actions on FGF pathways. Development 133, 4667-4678.
61. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D. and Peterson, R. T. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41.
62. Zhang, Y., Ryan, J. A., Di Cesare, P. E., Liu, J., Walsh, C. A. and You, Z. (2007). Doublecortin is expressed in articular chondrocytes. Biochem. Biophys. Res. Commun. 363, 694-700.
63. Zhang, Q., Cigan, A. D., Marrero, L., Lopreore, C., Liu, S., Ge, D., Savoie, F. H. and You, Z. (2011). Expression of doublecortin reveals articular chondrocyte lineage in mouse embryonic limbs. Genesis 49, 75-82.
64. Zur Nieden, N. I., Kempka, G., Rancourt, D. E. and Ahr, H. J. (2005). Induction of chondro-, osteo- and adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev. Biol. 5, 1.