Superficial cells are self-renewing chondrocyte progenitors, which form the articular cartilage in juvenile mice

. 2017 Mar ; 31 (3) : 1067-1084. [epub] 20161213

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid27965322

Articular cartilage has little regenerative capacity. Recently, genetic lineage tracing experiments have revealed chondrocyte progenitors at the articular surface. We further characterized these progenitors by using in vivo genetic approaches. Histone H2B-green fluorescent protein retention revealed that superficial cells divide more slowly than underlying articular chondrocytes. Clonal genetic tracing combined with immunohistochemistry revealed that superficial cells renew their number by symmetric division, express mesenchymal stem cell markers, and generate chondrocytes via both asymmetric and symmetric differentiation. Quantitative analysis of cellular kinetics, in combination with phosphotungstic acid-enhanced micro-computed tomography, showed that superficial cells generate chondrocytes and contribute to the growth and reshaping of articular cartilage. Furthermore, we found that cartilage renewal occurs as the progeny of superficial cells fully replace fetal chondrocytes during early postnatal life. Thus, superficial cells are self-renewing progenitors that are capable of maintaining their own population and fulfilling criteria of unipotent adult stem cells. Furthermore, the progeny of these cells reconstitute adult articular cartilage de novo, entirely substituting fetal chondrocytes.-Li, L., Newton, P. T., Bouderlique, T., Sejnohova, M., Zikmund, T., Kozhemyakina, E., Xie, M., Krivanek, J., Kaiser, J., Qian, H., Dyachuk, V., Lassar, A. B., Warman, M. L., Barenius, B., Adameyko, I., Chagin, A. S. Superficial cells are self-renewing chondrocyte progenitors, which form the articular cartilage in juvenile mice.

Zobrazit více v PubMed

Madry H., Luyten F. P., Facchini A. (2012) Biological aspects of early osteoarthritis. Knee Surg. Sports Traumatol. Arthrosc. 20, 407–422 PubMed

Hall B. K. (2015) Bones and Cartilage: Developmental and Evolutionary Skeletal Biology, 2nd ed., Elsevier, New York

Murray C. J., Vos T., Lozano R., Naghavi M., Flaxman A. D., Michaud C., Ezzati M., Shibuya K., Salomon J. A., Abdalla S., Aboyans V., Abraham J., Ackerman I., Aggarwal R., Ahn S. Y., Ali M. K., Alvarado M., Anderson H. R., Anderson L. M., Andrews K. G., Atkinson C., Baddour L. M., Bahalim A. N., Barker-Collo S., Barrero L. H., Bartels D. H., Basáñez M. G., Baxter A., Bell M. L., Benjamin E. J., Bennett D., Bernabé E., Bhalla K., Bhandari B., Bikbov B., Bin Abdulhak A., Birbeck G., Black J. A., Blencowe H., Blore J. D., Blyth F., Bolliger I., Bonaventure A., Boufous S., Bourne R., Boussinesq M., Braithwaite T., Brayne C., Bridgett L., Brooker S., Brooks P., Brugha T. S., Bryan-Hancock C., Bucello C., Buchbinder R., Buckle G., Budke C. M., Burch M., Burney P., Burstein R., Calabria B., Campbell B., Canter C. E., Carabin H., Carapetis J., Carmona L., Cella C., Charlson F., Chen H., Cheng A. T., Chou D., Chugh S. S., Coffeng L. E., Colan S. D., Colquhoun S., Colson K. E., Condon J., Connor M. D., Cooper L. T., Corriere M., Cortinovis M., de Vaccaro K. C., Couser W., Cowie B. C., Criqui M. H., Cross M., Dabhadkar K. C., Dahiya M., Dahodwala N., Damsere-Derry J., Danaei G., Davis A., De Leo D., Degenhardt L., Dellavalle R., Delossantos A., Denenberg J., Derrett S., Des Jarlais D. C., Dharmaratne S. D., Dherani M., Diaz-Torne C., Dolk H., Dorsey E. R., Driscoll T., Duber H., Ebel B., Edmond K., Elbaz A., Ali S. E., Erskine H., Erwin P. J., Espindola P., Ewoigbokhan S. E., Farzadfar F., Feigin V., Felson D. T., Ferrari A., Ferri C. P., Fèvre E. M., Finucane M. M., Flaxman S., Flood L., Foreman K., Forouzanfar M. H., Fowkes F. G., Fransen M., Freeman M. K., Gabbe B. J., Gabriel S. E., Gakidou E., Ganatra H. A., Garcia B., Gaspari F., Gillum R. F., Gmel G., Gonzalez-Medina D., Gosselin R., Grainger R., Grant B., Groeger J., Guillemin F., Gunnell D., Gupta R., Haagsma J., Hagan H., Halasa Y. A., Hall W., Haring D., Haro J. M., Harrison J. E., Havmoeller R., Hay R. J., Higashi H., Hill C., Hoen B., Hoffman H., Hotez P. J., Hoy D., Huang J. J., Ibeanusi S. E., Jacobsen K. H., James S. L., Jarvis D., Jasrasaria R., Jayaraman S., Johns N., Jonas J. B., Karthikeyan G., Kassebaum N., Kawakami N., Keren A., Khoo J. P., King C. H., Knowlton L. M., Kobusingye O., Koranteng A., Krishnamurthi R., Laden F., Lalloo R., Laslett L. L., Lathlean T., Leasher J. L., Lee Y. Y., Leigh J., Levinson D., Lim S. S., Limb E., Lin J. K., Lipnick M., Lipshultz S. E., Liu W., Loane M., Ohno S. L., Lyons R., Mabweijano J., MacIntyre M. F., Malekzadeh R., Mallinger L., Manivannan S., Marcenes W., March L., Margolis D. J., Marks G. B., Marks R., Matsumori A., Matzopoulos R., Mayosi B. M., McAnulty J. H., McDermott M. M., McGill N., McGrath J., Medina-Mora M. E., Meltzer M., Mensah G. A., Merriman T. R., Meyer A. C., Miglioli V., Miller M., Miller T. R., Mitchell P. B., Mock C., Mocumbi A. O., Moffitt T. E., Mokdad A. A., Monasta L., Montico M., Moradi-Lakeh M., Moran A., Morawska L., Mori R., Murdoch M. E., Mwaniki M. K., Naidoo K., Nair M. N., Naldi L., Narayan K. M., Nelson P. K., Nelson R. G., Nevitt M. C., Newton C. R., Nolte S., Norman P., Norman R., O’Donnell M., O’Hanlon S., Olives C., Omer S. B., Ortblad K., Osborne R., Ozgediz D., Page A., Pahari B., Pandian J. D., Rivero A. P., Patten S. B., Pearce N., Padilla R. P., Perez-Ruiz F., Perico N., Pesudovs K., Phillips D., Phillips M. R., Pierce K., Pion S., Polanczyk G. V., Polinder S., Pope C. A. III, Popova S., Porrini E., Pourmalek F., Prince M., Pullan R. L., Ramaiah K. D., Ranganathan D., Razavi H., Regan M., Rehm J. T., Rein D. B., Remuzzi G., Richardson K., Rivara F. P., Roberts T., Robinson C., De Leòn F. R., Ronfani L., Room R., Rosenfeld L. C., Rushton L., Sacco R. L., Saha S., Sampson U., Sanchez-Riera L., Sanman E., Schwebel D. C., Scott J. G., Segui-Gomez M., Shahraz S., Shepard D. S., Shin H., Shivakoti R., Singh D., Singh G. M., Singh J. A., Singleton J., Sleet D. A., Sliwa K., Smith E., Smith J. L., Stapelberg N. J., Steer A., Steiner T., Stolk W. A., Stovner L. J., Sudfeld C., Syed S., Tamburlini G., Tavakkoli M., Taylor H. R., Taylor J. A., Taylor W. J., Thomas B., Thomson W. M., Thurston G. D., Tleyjeh I. M., Tonelli M., Towbin J. A., Truelsen T., Tsilimbaris M. K., Ubeda C., Undurraga E. A., van der Werf M. J., van Os J., Vavilala M. S., Venketasubramanian N., Wang M., Wang W., Watt K., Weatherall D. J., Weinstock M. A., Weintraub R., Weisskopf M. G., Weissman M. M., White R. A., Whiteford H., Wiebe N., Wiersma S. T., Wilkinson J. D., Williams H. C., Williams S. R., Witt E., Wolfe F., Woolf A. D., Wulf S., Yeh P. H., Zaidi A. K., Zheng Z. J., Zonies D., Lopez A. D., AlMazroa M. A., Memish Z. A. (2012) Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 2197–2223 PubMed

Lotz M., Loeser R. F. (2012) Effects of aging on articular cartilage homeostasis. Bone 51, 241–248 PubMed PMC

Goldring M. B. (2012) Chondrogenesis, chondrocyte differentiation, and articular cartilage metabolism in health and osteoarthritis. Ther. Adv. Musculoskelet. Dis. 4, 269–285 PubMed PMC

Stockwell R. A. (1967) The cell density of human articular and costal cartilage. J. Anat. 101, 753–763 PubMed PMC

Dowthwaite G. P., Bishop J. C., Redman S. N., Khan I. M., Rooney P., Evans D. J. R., Haughton L., Bayram Z., Boyer S., Thomson B., Wolfe M. S., Archer C. W. (2004) The surface of articular cartilage contains a progenitor cell population. J. Cell Sci. 117, 889–897 PubMed

Jiang Y., Tuan R. S. (2015) Origin and function of cartilage stem/progenitor cells in osteoarthritis. Nat. Rev. Rheumatol. 11, 206–212 PubMed PMC

Kozhemyakina E., Zhang M., Ionescu A., Ayturk U. M., Ono N., Kobayashi A., Kronenberg H., Warman M. L., Lassar A. B. (2015) Identification of a Prg4-expressing articular cartilage progenitor cell population in mice. Arthritis Rheumatol. 67, 1261–1273 PubMed PMC

Nakamura E., Nguyen M. T., Mackem S. (2006) Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 235, 2603–2612 PubMed

Livet J., Weissman T. A., Kang H., Draft R. W., Lu J., Bennis R. A., Sanes J. R., Lichtman J. W. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56–62 PubMed

Snippert H. J., van der Flier L. G., Sato T., van Es J. H., van den Born M., Kroon-Veenboer C., Barker N., Klein A. M., van Rheenen J., Simons B. D., Clevers H. (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134–144 PubMed

Kaucka M., Ivashkin E., Gyllborg D., Zikmund T., Tesarova M., Kaiser J., Xie M., Petersen J., Pachnis V., Nicolis S. K., Yu T., Sharpe P., Arenas E., Brismar H., Blom H., Clevers H., Suter U., Chagin A. S., Fried K., Hellander A., Adameyko I. (2016) Analysis of neural crest-derived clones reveals novel aspects of facial development. Sci. Adv. 2, e1600060 PubMed PMC

Tesařová M., Zikmund T., Kaucká M., Adameyko I., Jaroš J., Paloušek D., Škaroupka D., Kaiser J. (2016) Use of micro computed-tomography and 3D printing for reverse engineering of mouse embryo nasal capsule. J. Instrum. 11, C03006

Simons B. D., Clevers H. (2011) Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 145, 851–862 PubMed

Yang L., Tsang K. Y., Tang H. C., Chan D., Cheah K. S. (2014) Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc. Natl. Acad. Sci. USA 111, 12097–12102 PubMed PMC

Archer C. W. (1994) Skeletal development and osteoarthritis. Ann. Rheum. Dis. 53, 624–630 PubMed PMC

Pribylová E., Hert J. (1971) Proliferation zones in articular cartilage of young rabbits. Folia Morphol. (Praha) 19, 233–241 PubMed

Mankin H. J. (1962) Localization of tritiated thymidine in articular cartilage of rabbits. J. Bone Joint Surg. Am. 44, 682–688

Hunziker E. B., Kapfinger E., Geiss J. (2007) The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthritis Cartilage 15, 403–413 PubMed

Yasuhara R., Ohta Y., Yuasa T., Kondo N., Hoang T., Addya S., Fortina P., Pacifici M., Iwamoto M., Enomoto-Iwamoto M. (2011) Roles of β-catenin signaling in phenotypic expression and proliferation of articular cartilage superficial zone cells. Lab. Invest. 91, 1739–1752 PubMed PMC

Duque A., Rakic P. (2011) Different effects of bromodeoxyuridine and [3H]thymidine incorporation into DNA on cell proliferation, position, and fate. J. Neurosci. 31, 15205–15217 PubMed PMC

Pollard D. R., Baran M. M., Bachvarova R. (1976) The effect of 5-bromodeoxyuridine on cell division and differentiation of preimplantation mouse embryos. J. Embryol. Exp. Morphol. 35, 169–178 PubMed

Kolb B., Pedersen B., Ballermann M., Gibb R., Whishaw I. Q. (1999) Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J. Neurosci. 19, 2337–2346 PubMed PMC

Hollibaugh J. T. (1988) Limitations of the [3H]thymidine method for estimating bacterial productivity due to thymidine metabolism. Mar. Ecol. (Berl.) 43, 19–30

Korr H., Kurz C., Seidler T. O., Sommer D., Schmitz C. (1998) Mitochondrial DNA synthesis studied autoradiographically in various cell types in vivo. Braz. J. Med. Biol. Res. 31, 289–298 PubMed

Breunig J. J., Arellano J. I., Macklis J. D., Rakic P. (2007) Everything that glitters isn’t gold: a critical review of postnatal neural precursor analyses. Cell Stem Cell 1, 612–627 PubMed

Klein A. M., Nakagawa T., Ichikawa R., Yoshida S., Simons B. D. (2010) Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 7, 214–224 PubMed

Clayton E., Doupé D. P., Klein A. M., Winton D. J., Simons B. D., Jones P. H. (2007) A single type of progenitor cell maintains normal epidermis. Nature 446, 185–189 PubMed

Doupé D. P., Klein A. M., Simons B. D., Jones P. H. (2010) The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18, 317–323 PubMed

Wang B., Zhao L., Fish M., Logan C. Y., Nusse R. (2015) Self-renewing diploid Axin2+ cells fuel homeostatic renewal of the liver. Nature 524, 180–185 PubMed PMC

Zhang M., Mani S. B., He Y., Hall A. M., Xu L., Li Y., Zurakowski D., Jay G. D., Warman M. L. (2016) Induced superficial chondrocyte death reduces catabolic cartilage damage in murine posttraumatic osteoarthritis. J. Clin. Invest. 126, 2893–2902 PubMed PMC

Lepper C., Partridge T. A., Fan C.-M. (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138, 3639–3646 PubMed PMC

Schoedel K. B., Morcos M. N., Zerjatke T., Roeder I., Grinenko T., Voehringer D., Göthert J. R., Waskow C., Roers A., Gerbaulet A. (2016) The bulk of the hematopoietic stem cell population is dispensable for murine steady-state and stress hematopoiesis. Blood 128, 2285–2296 PubMed

Tian H., Biehs B., Warming S., Leong K. G., Rangell L., Klein O. D., de Sauvage F. J. (2011) A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255–259 PubMed PMC

Rompolas P., Mesa K. R., Greco V. (2013) Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513–518 PubMed PMC

Driskell I., Oeztuerk-Winder F., Humphreys P., Frye M. (2015) Genetically induced cell death in bulge stem cells reveals their redundancy for hair and epidermal regeneration. Stem Cells 33, 988–998 PubMed PMC

Van der Flier L. G., van Gijn M. E., Hatzis P., Kujala P., Haegebarth A., Stange D. E., Begthel H., van den Born M., Guryev V., Oving I., van Es J. H., Barker N., Peters P. J., van de Wetering M., Clevers H. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136, 903–912 PubMed

Tata P. R., Mou H., Pardo-Saganta A., Zhao R., Prabhu M., Law B. M., Vinarsky V., Cho J. L., Breton S., Sahay A., Medoff B. D., Rajagopal J. (2013) Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503, 218–223 PubMed PMC

Pardo-Saganta A., Tata P. R., Law B. M., Saez B., Chow R. Dz., Prabhu M., Gridley T., Rajagopal J. (2015) Parent stem cells can serve as niches for their daughter cells. Nature 523, 597–601 PubMed PMC

Kurth T. B., Dell’accio F., Crouch V., Augello A., Sharpe P. T., De Bari C. (2011) Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis Rheum. 63, 1289–1300 PubMed

Rountree R. B., Schoor M., Chen H., Marks M. E., Harley V., Mishina Y., Kingsley D. M. (2004) BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol. 2, e355 PubMed PMC

Koyama E., Shibukawa Y., Nagayama M., Sugito H., Young B., Yuasa T., Okabe T., Ochiai T., Kamiya N., Rountree R. B., Kingsley D. M., Iwamoto M., Enomoto-Iwamoto M., Pacifici M. (2008) A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev. Biol. 316, 62–73 PubMed PMC

Shwartz Y., Viukov S., Krief S., Zelzer E. (2016) Joint development involves a continuous influx of Gdf5-positive cells. Cell Reports 15, 2577–2587 PubMed PMC

Rhee D. K., Marcelino J., Baker M., Gong Y., Smits P., Lefebvre V., Jay G. D., Stewart M., Wang H., Warman M. L., Carpten J. D. (2005) The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J. Clin. Invest. 115, 622–631 PubMed PMC

Ogawa H., Kozhemyakina E., Hung H. H., Grodzinsky A. J., Lassar A. B. (2014) Mechanical motion promotes expression of Prg4 in articular cartilage via multiple CREB-dependent, fluid flow shear stress-induced signaling pathways. Genes Dev. 28, 127–139 PubMed PMC

Kahn J., Shwartz Y., Blitz E., Krief S., Sharir A., Breitel D. A., Rattenbach R., Relaix F., Maire P., Rountree R. B., Kingsley D. M., Zelzer E. (2009) Muscle contraction is necessary to maintain joint progenitor cell fate. Dev. Cell 16, 734–743 PubMed

Ray A., Singh P. N., Sohaskey M. L., Harland R. M., Bandyopadhyay A. (2015) Precise spatial restriction of BMP signaling is essential for articular cartilage differentiation. Development 142, 1169–1179 PubMed PMC

De Bari C., Dell’Accio F., Tylzanowski P., Luyten F. P. (2001) Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 44, 1928–1942 PubMed

Najít záznam

Citační ukazatele

    Možnosti archivace