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Volume 50 Issue 9
Sep.  2023
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Article Contents

Single-cell transcriptomic analysis identifies a highly replicating Cd168+ skeletal stem/progenitor cell population in mouse long bones

doi: 10.1016/j.jgg.2023.04.004 cstr: 32370.14.j.jgg.2023.04.004
Funds:

This work was supported by the National Key R&D Program of China (2022YFA1104100, 2022YFA1103500), the National Natural Sciences Grants China (82172388, 82372373, 81871771), and the Beijing Natural Sciences Foundation (7222123, L212065).

  • Received Date: 2023-01-23
  • Accepted Date: 2023-04-09
  • Rev Recd Date: 2023-04-08
  • Publish Date: 2023-04-17
  • Skeletal stem/progenitor cells (SSPCs) are tissue-specific stem/progenitor cells localized within skeletons and contribute to bone development, homeostasis, and regeneration. However, the heterogeneity of SSPC populations in mouse long bones and their respective regenerative capacity remain to be further clarified. In this study, we perform integrated analysis using single-cell RNA sequencing (scRNA-seq) datasets of mouse hindlimb buds, postnatal long bones, and fractured long bones. Our analyses reveal the heterogeneity of osteochondrogenic lineage cells and recapitulate the developmental trajectories during mouse long bone growth. In addition, we identify a novel Cd168+ SSPC population with highly replicating capacity and osteochondrogenic potential in embryonic and postnatal long bones. Moreover, the Cd168+ SSPCs can contribute to newly formed skeletal tissues during fracture healing. Furthermore, the results of multicolor immunofluorescence show that Cd168+ SSPCs reside in the superficial zone of articular cartilage as well as in growth plates of postnatal mouse long bones. In summary, we identify a novel Cd168+ SSPC population with regenerative potential in mouse long bones, which adds to the knowledge of the tissue-specific stem cells in skeletons.
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  • [1]
    Arnold, M.A., Kim, Y., Czubryt, M.P., Phan, D., McAnally, J., Qi, X., Shelton, J.M., Richardson, J.A., Bassel-Duby, R., Olson, E.N., 2007. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev. Cell 12, 377-389.
    [2]
    Bian, L., Guvendiren, M., Mauck, R.L., Burdick, J.A., 2013. Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis. Proc. Natl. Acad. Sci. U. S. A 110, 10117-10122.
    [3]
    Bondjers, C., Kalen, M., Hellstrom, M., Scheidl, S.J., Abramsson, A., Renner, O., Lindahl, P., Cho, H., Kehrl, J., Betsholtz, C., 2003. Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am. J. Pathol. 162, 721-729.
    [4]
    Brennan-Speranza, T.C., Conigrave, A.D., 2015. Osteocalcin: an osteoblast-derived polypeptide hormone that modulates whole body energy metabolism. Calcif. Tissue Int. 96, 1-10.
    [5]
    Burren, S., Reche, K., Blank, A., Galvan, J.A., Dawson, H., Berger, M.D., Zlobec, I., Lugli, A., 2021. RHAMM in liver metastases of stage IV colorectal cancer with mismatch-repair proficient status correlates with tumor budding, cytotoxic T-cells and PD-1/PD-L1. Pathol. Res. Pract. 223, 153486.
    [6]
    Chan, C.K.F., Gulati, G.S., Sinha, R., Tompkins, J.V., Lopez, M., Carter, A.C., Ransom, R.C., Reinisch, A., Wearda, T., Murphy, M., et al., 2018. Identification of the human skeletal stem cell. Cell 175, 43-56.
    [7]
    Chan, D., Cole, W.G., Chow, C.W., Mundlos, S., Bateman, J.F., 1995. A COL2A1 mutation in achondrogenesis type II results in the replacement of type II collagen by type I and III collagens in cartilage. J. Biol. Chem. 270, 1747-1753.
    [8]
    Chan, C.K.F., Seo, E.Y., Chen, J.Y., Lo, D., McArdle, A., Sinha, R., Tevlin, R., Seita, J., Vincent-Tompkins, J., Wearda, T., Lu, W.-J., Senarath-Yapa, K., Chung, M.T., Marecic, O., Tran, M., Yan, K.S., Upton, R., Walmsley, G.G., Lee, A.S., Sahoo, D., Kuo, C.J., Weissman, I.L., Longaker, M.T., 2015. Identification and specification of the mouse skeletal stem cell. Cell 160, 285-298.
    [9]
    Cheng, S., Li, Z., Gao, R., Xing, B., Gao, Y., Yang, Yu, Qin, S., Zhang, L., Ouyang, H., Du, P., Jiang, L., Zhang, B., Yang, Yue, Wang, X., Ren, X., Bei, J.-X., Hu, X., Bu, Z., Ji, J., Zhang, Z., 2021. A pan-cancer single-cell transcriptional atlas of tumor infiltrating myeloid cells. Cell 184, 792-809.
    [10]
    Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., Forster, I., 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265-277.
    [11]
    Cui, Z., Liao, J., Cheong, N., Longoria, C., Cao, G., DeLisser, H.M., Savani, R.C., 2019. The Receptor for Hyaluronan-Mediated Motility (CD168) promotes inflammation and fibrosis after acute lung injury. Matrix Biol. 78-79, 255-271.
    [12]
    Debnath, S., Yallowitz, A.R., McCormick, J., Lalani, S., Zhang, T., Xu, R., Li, N., Liu, Y., Yang, Y.S., Eiseman, M., Shim, J.-H., Hameed, M., Healey, J.H., Bostrom, M.P., Landau, D.A., Greenblatt, M.B., 2018. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature 562, 133-139.
    [13]
    Depianto, D., Kerns, M.L., Dlugosz, A.A., Coulombe, P.A., 2010. Keratin 17 promotes epithelial proliferation and tumor growth by polarizing the immune response in skin. Nat. Genet. 42, 910-914.
    [14]
    Ding, L., Saunders, T.L., Enikolopov, G., Morrison, S.J., 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457-462.
    [15]
    Dirckx, N., Moorer, M.C., Clemens, T.L., Riddle, R.C., 2019. The role of osteoblasts in energy homeostasis. Nat. Rev. Endocrinol. 15, 651-665.
    [16]
    Doege, K.J., Sasaki, M., Kimura, T., Yamada, Y., 1991. Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. Human-specific repeats, and additional alternatively spliced forms. J. Biol. Chem. 266, 894-902.
    [17]
    Foster, J.W., Dominguez-Steglich, M.A., Guioli, S., Kwok, C., Weller, P.A., Stevanovic, M., Weissenbach, J., Mansour, S., Young, I.D., Goodfellow, P.N., 1994. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372, 525-530.
    [18]
    Greenbaum, A., Hsu, Y.-M.S., Day, R.B., Schuettpelz, L.G., Christopher, M.J., Borgerding, J.N., Nagasawa, T., Link, D.C., 2013. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227-230.
    [19]
    Greenblatt, M.B., Ono, N., Ayturk, U.M., Debnath, S., Lalani, S., 2019. The unmixing problem: a guide to applying single-cell RNA sequencing to bone. J. Bone Miner. Res. 34, 1207-1219.
    [20]
    Gulati, G.S., Murphy, M.P., Marecic, O., Lopez, M., Brewer, R.E., Koepke, L.S., Manjunath, A., Ransom, R.C., Salhotra, A., Weissman, I.L., Longaker, M.T., Chan, C.K.F., 2018. Isolation and functional assessment of mouse skeletal stem cell lineage. Nat. Protoc. 13, 1294-1309.
    [21]
    Hall, L.R., Streuli, M., Schlossman, S.F., Saito, H., 1988. Complete exon-intron organization of the human leukocyte common antigen (CD45) gene. J. Immunol. 141, 2781-2787.
    [22]
    He, J., Yan, J., Wang, J., Zhao, L., Xin, Q., Zeng, Y., Sun, Y., Zhang, H., Bai, Z., Li, Z., Ni, Y., Gong, Y., Li, Y., He, H., Bian, Z., Lan, Y., Ma, C., Bian, L., Zhu, H., Liu, B., Yue, R., 2021. Dissecting human embryonic skeletal stem cell ontogeny by single-cell transcriptomic and functional analyses. Cell Res. 31, 742-757.
    [23]
    Huang, W., Yang, S., Shao, J., Li, Y.-P., 2007. Signaling and transcriptional regulation in osteoblast commitment and differentiation. Front. Biosci. 12, 3068-3092.
    [24]
    Jeffery, E.C., Mann, T.L.A., Pool, J.A., Zhao, Z., Morrison, S.J., 2022. Bone marrow and periosteal skeletal stem/progenitor cells make distinct contributions to bone maintenance and repair. Cell Stem Cell 29, 1547-1561.
    [25]
    Kawanami, A., Matsushita, T., Chan, Y.Y., Murakami, S., 2009. Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum. Biochem. Biophys. Res. Commun. 386, 477-482.
    [26]
    Kelly, N.H., Huynh, N.P.T., Guilak, F., 2020. Single cell RNA-sequencing reveals cellular heterogeneity and trajectories of lineage specification during murine embryonic limb development. Matrix Biol. 89, 1-10.
    [27]
    Koltes, J.E., Kumar, D., Kataria, R.S., Cooper, V., Reecy, J.M., 2015. Transcriptional profiling of PRKG2-null growth plate identifies putative down-stream targets of PRKG2. BMC Res. Notes 8, 177.
    [28]
    Kwon, H.R., Kim, J.H., Woods, J.P., Olson, L.E., 2021. Skeletal stem cell fate defects caused by Pdgfrb activating mutation. Development 148, dev199607.
    [29]
    Leussink, B., Brouwer, A., el Khattabi, M., Poelmann, R.E., Gittenberger-de Groot, A.C., Meijlink, F., 1995. Expression patterns of the paired-related homeobox genes MHox/Prx1 and S8/Prx2 suggest roles in development of the heart and the forebrain. Mech. Dev. 52, 51-64.
    [30]
    Lewandoski, M., Sun, X., Martin, G.R., 2000. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 26, 460-463.
    [31]
    Li, L., Miano, J.M., Cserjesi, P., Olson, E.N., 1996. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ. Res. 78, 188-195.
    [32]
    Li, X., Wang, C.-Y., 2021. From bulk, single-cell to spatial RNA sequencing. Int. J. Oral Sci. 13, 36.
    [33]
    Liu, H., Li, P., Zhang, S., Xiang, J., Yang, R., Liu, J., Shafiquzzaman, M., Biswas, S., Wei, Z., Zhang, Z., Zhou, X., Yin, F., Xie, Y., Goff, S.P., Chen, L., Li, B., 2022. Prrx1 marks stem cells for bone, white adipose tissue and dermis in adult mice. Nat. Genet. 54, 1946-1958.
    [34]
    Long, F., 2011. Building strong bones: molecular regulation of the osteoblast lineage. Nat. Rev. Mol. Cell Biol. 13, 27-38.
    [35]
    Mareel, M., Boterberg, T., Noe, V., Van Hoorde, L., Vermeulen, S., Bruyneel, E., Bracke, M., 1997. E-cadherin/catenin/cytoskeleton complex: a regulator of cancer invasion. J. Cell. Physiol. 173, 271-274.
    [36]
    Markasz, L., Savani, R.C., Jonzon, A., Sindelar, R., 2021. CD44 and RHAMM expression patterns in the human developing lung. Pediatr. Res. 89, 134-142.
    [37]
    Maruyama, T., Stevens, R., Boka, A., DiRienzo, L., Chang, C., Yu, H.-M.I., Nishimori, K., Morrison, C., Hsu, W., 2021. BMPR1A maintains skeletal stem cell properties in craniofacial development and craniosynostosis. Sci. Transl. Med. 13, eabb4416.
    [38]
    Matsushita, Y., Nagata, M., Kozloff, K.M., Welch, J.D., Mizuhashi, K., Tokavanich, N., Hallett, S.A., Link, D.C., Nagasawa, T., Ono, W., Ono, N., 2020. A Wnt-mediated transformation of the bone marrow stromal cell identity orchestrates skeletal regeneration. Nat. Commun. 11, 332.
    [39]
    Matsushita, Y., Ono, W., Ono, N., 2021. Flow cytometry-based analysis of the mouse bone marrow stromal and perivascular compartment. Methods Mol. Biol. 2308, 83-94.
    [40]
    Mejia, J., Salisbury, E., Sonnet, C., Gugala, Z., Olmsted-Davis, E.A., Davis, A.R., 2021. A replicating stem-like cell that contributes to bone morphogenetic protein 2-induced heterotopic bone formation. Stem Cells Transl. Med. 10, 623-635.
    [41]
    Mizoguchi, T., Pinho, S., Ahmed, J., Kunisaki, Y., Hanoun, M., Mendelson, A., Ono, N., Kronenberg, H.M., Frenette, P.S., 2014. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev. Cell 29, 340-349.
    [42]
    Mizuhashi, K., Ono, W., Matsushita, Y., Sakagami, N., Takahashi, A., Saunders, T.L., Nagasawa, T., Kronenberg, H.M., Ono, N., 2018. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature 563, 254-258.
    [43]
    Mo, C., Guo, J., Qin, J., Zhang, X., Sun, Yuxi, Wei, H., Cao, D., Zhang, Yiying, Zhao, C., Xiong, Y., Zhang, Yong, Sun, Yao, Shen, L., Yue, R., 2022. Single-cell transcriptomics of LepR-positive skeletal cells reveals heterogeneous stress-dependent stem and progenitor pools. EMBO J. 41, e108415.
    [44]
    Morikawa, S., Mabuchi, Y., Kubota, Y., Nagai, Y., Niibe, K., Hiratsu, E., Suzuki, S., Miyauchi-Hara, C., Nagoshi, N., Sunabori, T., Shimmura, S., Miyawaki, A., Nakagawa, T., Suda, T., Okano, H., Matsuzaki, Y., 2009. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206, 2483-2496.
    [45]
    Morrison, S.J., Scadden, D.T., 2014. The bone marrow niche for haematopoietic stem cells. Nature 505, 327-334.
    [46]
    Murphy, J.M., Heinegard, R., McIntosh, A., Sterchi, D., Barry, F.P., 1999. Distribution of cartilage molecules in the developing mouse joint. Matrix Biol. 18, 487-497.
    [47]
    Murphy, M.P., Koepke, L.S., Lopez, M.T., Tong, X., Ambrosi, T.H., Gulati, G.S., Marecic, O., Wang, Y., Ransom, R.C., Hoover, M.Y., Steininger, H., Zhao, L., Walkiewicz, M.P., Quarto, N., Levi, B., Wan, D.C., Weissman, I.L., Goodman, S.B., Yang, F., Longaker, M.T., Chan, C.K.F., 2020. Articular cartilage regeneration by activated skeletal stem cells. Nat. Med. 26, 1583-1592.
    [48]
    Muruganandan, S., Pierce, R., Teguh, D.A., Perez, R.F., Bell, N., Nguyen, B., Hohl, K., Snyder, B.D., Grinstaff, M.W., Alberico, H., Woods, D., Kong, Y., Sima, C., Bhagat, S., Ho, K., Rosen, V., Gamer, L., Ionescu, A.M., 2022. A FoxA2+ long-term stem cell population is necessary for growth plate cartilage regeneration after injury. Nat. Commun. 13, 2515.
    [49]
    Nakamura, H., Yukita, A., Ninomiya, T., Hosoya, A., Hiraga, T., Ozawa, H., 2010. Localization of Thy-1-positive cells in the perichondrium during endochondral ossification. J. Histochem. Cytochem. 58, 455-462.
    [50]
    Nakashima, K., Zhou, X., Kunkel, G., Zhang, Z., Deng, J.M., Behringer, R.R., de Crombrugghe, B., 2002. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108, 17-29.
    [51]
    Ortinau, L.C., Wang, H., Lei, K., Deveza, L., Jeong, Y., Hara, Y., Grafe, I., Rosenfeld, S.B., Lee, D., Lee, B., Scadden, D.T., Park, D., 2019. Identification of functionally distinct Mx1+αSMA+ periosteal skeletal stem cells. Cell Stem Cell 25, 784-796.
    [52]
    Rafii, S., Butler, J.M., Ding, B.-S., 2016. Angiocrine functions of organ-specific endothelial cells. Nature 529, 316-325.
    [53]
    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.
    [54]
    Salhotra, A., Shah, H.N., Levi, B., Longaker, M.T., 2020. Mechanisms of bone development and repair. Nat. Rev. Mol. Cell Biol. 21, 696-711.
    [55]
    Shan, G., Meihe, L., Minchao, K., Rui, Z., Xiaopeng, W., Guangjian, Z., Jin, Z., 2022. Identification and validation of Osteopontin and receptor for hyaluronic acid-mediated motility (RHAMM, CD168) for potential immunotherapeutic significance of in lung squamous cell carcinoma. Int. Immunopharm. 107, 108715.
    [56]
    Sims, N.A., Martin, T.J., 2020. Osteoclasts provide coupling signals to osteoblast lineage cells through multiple mechanisms. Annu. Rev. Physiol. 82, 507-529.
    [57]
    Sivaraj, K.K., Jeong, H.-W., Dharmalingam, B., Zeuschner, D., Adams, S., Potente, M., Adams, R.H., 2021. Regional specialization and fate specification of bone stromal cells in skeletal development. Cell Rep. 36, 109352.
    [58]
    Sivaraj, K.K., Majev, P.-G., Jeong, H.-W., Dharmalingam, B., Zeuschner, D., Schroder, S., Bixel, M.G., Timmen, M., Stange, R., Adams, R.H., 2022. Mesenchymal stromal cell-derived septoclasts resorb cartilage during developmental ossification and fracture healing. Nat. Commun. 13, 571.
    [59]
    Soliman, F., Ye, L., Jiang, W., Hargest, R., 2022. Targeting hyaluronic acid and peritoneal dissemination in colorectal cancer. Clin. Colorectal Cancer 21, e126-e134.
    [60]
    Stricker, S., Mathia, S., Haupt, J., Seemann, P., Meier, J., Mundlos, S., 2012. Odd-skipped related genes regulate differentiation of embryonic limb mesenchyme and bone marrow mesenchymal stromal cells. Stem Cell. Dev. 21, 623-633.
    [61]
    Tapscott, S.J., 2005. The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132, 2685-2695.
    [62]
    Tichy, E.D., Mourkioti, F., 2018. Human skeletal stem cells: the markers provide some clues in the hunt for hidden treasure. Cell Stem Cell 23, 462-463.
    [63]
    Tikhonova, A.N., Dolgalev, I., Hu, H., Sivaraj, K.K., Hoxha, E., Cuesta-Dominguez, A., Pinho, S., Akhmetzyanova, I., Gao, J., Witkowski, M., Guillamot, M., Gutkin, M.C., Zhang, Y., Marier, C., Diefenbach, C., Kousteni, S., Heguy, A., Zhong, H., Fooksman, D.R., Butler, J.M., Economides, A., Frenette, P.S., Adams, R.H., Satija, R., Tsirigos, A., Aifantis, I., 2019. The bone marrow microenvironment at single-cell resolution. Nature 569, 222-228.
    [64]
    Tuckermann, J., Adams, R.H., 2021. The endothelium-bone axis in development, homeostasis and bone and joint disease. Nat. Rev. Rheumatol. 17, 608-620.
    [65]
    van Gastel, N., Stegen, S., Eelen, G., Schoors, S., Carlier, A., Daniels, V.W., Baryawno, N., Przybylski, D., Depypere, M., Stiers, P.-J., Lambrechts, Dennis, Van Looveren, R., Torrekens, S., Sharda, A., Agostinis, P., Lambrechts, Diether, Maes, F., Swinnen, J.V., Geris, L., Van Oosterwyck, H., Thienpont, B., Carmeliet, P., Scadden, D.T., Carmeliet, G., 2020. Lipid availability determines fate of skeletal progenitor cells via SOX9. Nature 579, 111-117.
    [66]
    Veis, D.J., O'Brien, C.A., 2023. Osteoclasts, master sculptors of bone. Annu. Rev. Pathol. 18, 257-281.
    [67]
    Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M., Tabin, C.J., 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
    [68]
    Wang, K., Zhang, T., 2016. Prognostic significance of CD168 overexpression in colorectal cancer. Oncol. Lett. 12, 2555-2559.
    [69]
    Wang, S., Jiang, H., Zheng, C., Gu, M., Zheng, X., 2022. Secretion of BMP-2 by tumor-associated macrophages (TAM) promotes microcalcifications in breast cancer. BMC Cancer 22, 34.
    [70]
    Watson, E.C., Adams, R.H., 2018. Biology of bone: the vasculature of the skeletal system. Cold Spring Harb Perspect. Med. 8, a031559.
    [71]
    Wei, B., Jin, J.-P., 2016. TNNT1, TNNT2, and TNNT3: isoform genes, regulation, and structure-function relationships. Gene 582, 1-13.
    [72]
    Winkler, E.A., Bell, R.D., Zlokovic, B.V., 2010. Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling. Mol. Neurodegener. 5, 32.
    [73]
    Wolock, S.L., Krishnan, I., Tenen, D.E., Matkins, V., Camacho, V., Patel, S., Agarwal, P., Bhatia, R., Tenen, D.G., Klein, A.M., Welner, R.S., 2019. Mapping distinct bone marrow niche populations and their differentiation paths. Cell Rep. 28, 302-311.
    [74]
    Worthley, D.L., Churchill, M., Compton, J.T., Tailor, Y., Rao, M., Si, Y., Levin, D., Schwartz, M.G., Uygur, A., Hayakawa, Y., Gross, S., Renz, B.W., Setlik, W., Martinez, A.N., Chen, X., Nizami, S., Lee, H.G., Kang, H.P., Caldwell, J.-M., Asfaha, S., Westphalen, C.B., Graham, T., Jin, G., Nagar, K., Wang, H., Kheirbek, M.A., Kolhe, A., Carpenter, J., Glaire, M., Nair, A., Renders, S., Manieri, N., Muthupalani, S., Fox, J.G., Reichert, M., Giraud, A.S., Schwabe, R.F., Pradere, J.-P., Walton, K., Prakash, A., Gumucio, D., Rustgi, A.K., Stappenbeck, T.S., Friedman, R.A., Gershon, M.D., Sims, P., Grikscheit, T., Lee, F.Y., Karsenty, G., Mukherjee, S., Wang, T.C., 2015. Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 160, 269-284.
    [75]
    Xia, M.Q., Tone, M., Packman, L., Hale, G., Waldmann, H., 1991. Characterization of the CAMPATH-1 (CDw52) antigen: biochemical analysis and cDNA cloning reveal an unusually small peptide backbone. Eur. J. Immunol. 21, 1677-1684.
    [76]
    Xu, Jiaqi, Zhang, Y., Xu, Junchao, Wang, M., Liu, G., Wang, J., Zhao, X., Qi, Y., Shi, J., Cheng, K., Li, Y., Qi, S., Nie, G., 2019. Reversing tumor stemness via orally targeted nanoparticles achieves efficient colon cancer treatment. Biomaterials 216, 119247.
    [77]
    Yang, C., Li, C., Zhang, P., Wu, W., Jiang, X., 2017. Redox responsive hyaluronic acid nanogels for treating RHAMM (CD168) over-expressive cancer, both primary and metastatic tumors. Theranostics 7, 1719-1734.
    [78]
    Yu, W., Schmachtel, T., Fawaz, M., Rieger, M.A., 2022. Isolation of murine bone marrow hematopoietic stem and progenitor cell populations via flow cytometry. Methods Cell Biol. 171, 173-195.
    [79]
    Zhang, C.-H., Gao, Y., Hung, H.-H., Zhuo, Z., Grodzinsky, A.J., Lassar, A.B., 2022a. Creb5 coordinates synovial joint formation with the genesis of articular cartilage. Nat. Commun. 13, 7295.
    [80]
    Zhang, X., Jiang, W., Xie, C., Wu, X., Ren, Q., Wang, F., Shen, X., Hong, Y., Wu, H., Liao, Y., Zhang, Y., Liang, R., Sun, W., Gu, Y., Zhang, T., Chen, Y., Wei, W., Zhang, S., Zou, W., Ouyang, H., 2022b. Msx1+ stem cells recruited by bioactive tissue engineering graft for bone regeneration. Nat. Commun. 13, 5211.
    [81]
    Zhou, B.O., Yue, R., Murphy, M.M., Peyer, J.G., Morrison, S.J., 2014. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 15, 154-168.
    [82]
    Zhu, L.-N., Ren, Y., Chen, J.-Q., Wang, Y.-Z., 2013. Effects of myogenin on muscle fiber types and key metabolic enzymes in gene transfer mice and C2C12 myoblasts. Gene 532, 246-252.
    [83]
    Zhu, S.-W., Wang, S., Wu, Z.-Z., Yang, Q.-C., Chen, D.-R., Wan, S.-C., Sun, Z.-J., 2022. Overexpression of CD168 is related to poor prognosis in oral squamous cell carcinoma. Oral Dis. 28, 364-372.
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