WISP1 promotes bovine MDSC differentiation via recruitment of ANXA1 for the regulation of the TGF-β signalling pathway

Abstract

Skeletal muscle is one of the most important tissues of the human body necessary for sporting activities. The differentiation of muscle-derived satellite cells (MDSCs) plays an important role in the development and regeneration of skeletal muscles. Similarly, the Wnt/β-catenin signalling pathway plays an important role in the process of muscle differentiation. Wnt1-inducible signalling pathway protein-1 (WISP1), a downstream protein of the Wnt/β-catenin signalling pathway and a member of the CCN family that also plays an important role in the differentiation process, and its expression increase during the differentiation of bovine MDSCs. However, its role in MDSC differentiation is poorly understood. Therefore, we investigated the mechanisms regulating this process via Western blot and immunofluorescence staining. Immunoprecipitation and mass spectrometry detected annexin A1 (ANXA1), a protein that interacts with WISP1. To determine whether WISP1 influences TGF-β signalling and differentiation independently of ANXA1, the latter was knocked down, while WISP1 was activated. WISP1 expression increased significantly during bovine MDSC differentiation. However, WISP1 did not affect the TGF-β signalling pathway protein marker when ANXA1 was inhibited. Taken together, WISP1 regulates the TGF-β signalling pathway through ANXA1 recruitment, thereby promoting bovine MDSC differentiation, suggesting the Wnt/β-catenin signalling pathway as another target to promote cell differentiation.

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Data availability

All data generated or analysed during this study are included in this published article and its supplementary information files.

References

  1. 1.

    Frontera WR, Ochala J (2015) Skeletal muscle: a brief review of structure and function. Calcif Tissue Int 96:183–195. https://doi.org/10.1007/s00223-014-9915-y

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Rudolf A, Schirwis E, Giordani L et al (2016) β-catenin activation in muscle progenitor cells regulates tissue repair. Cell Rep 15:1277–1290. https://doi.org/10.1016/j.celrep.2016.04.022

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Ganassi M, Badodi S, Ortuste Quiroga HP et al (2018) Myogenin promotes myocyte fusion to balance fibre number and size. Nat Commun 9:4232. https://doi.org/10.1038/s41467-018-06583-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Li S, Fu Y, Pang Y et al (2019) GRP94 promotes muscle differentiation by inhibiting the PI3K/AKT/mTOR signaling pathway. J Cell Physiol 234:21211–21223. https://doi.org/10.1002/jcp.28727

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Ge Y, Li S, Hu XY et al (2019) TCEA3 promotes differentiation of C2C12 cells via an Annexin A1-mediated transforming growth factor-β signaling pathway. J Cell Physiol 234:10554–10565. https://doi.org/10.1002/jcp.27726

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Li S, Liu D, Fu Y et al (2019) Podocan promotes differentiation of bovine skeletal muscle satellite cells by regulating the Wnt4-β-catenin signaling pathway. Front Physiol 10:1–17. https://doi.org/10.3389/fphys.2019.01010

    Article  Google Scholar 

  7. 7.

    Garcin CL, Habib SJ (2017) A comparative perspective on Wnt/β-catenin signalling in cell fate determination. Asymmetric Cell Div Dev Differ Cancer 61:323–350. https://doi.org/10.1007/978-3-319-53150-2

    CAS  Article  Google Scholar 

  8. 8.

    Kabiri Z, Greicius G, Zaribafzadeh H et al (2018) Wnt signaling suppresses MAPK-driven proliferation of intestinal stem cells. J Clin Invest 128:3806–3812. https://doi.org/10.1172/JCI99325

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Zang S, Liu N, Wang H et al (2014) Wnt signaling is involved in 6-benzylthioinosine-induced AML cell differentiation. BMC Cancer 14:1–10. https://doi.org/10.1186/1471-2407-14-88

    CAS  Article  Google Scholar 

  10. 10.

    Lukjanenko L, Karaz S, Stuelsatz P et al (2019) Aging disrupts muscle stem cell function by impairing matricellular WISP1 secretion from fibro-adipogenic progenitors. Cell Stem Cell 24:433–446. https://doi.org/10.1016/j.stem.2018.12.014

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Pennica D, Swanson TA, Welsh JW et al (1998) WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA 95:14717–14722. https://doi.org/10.1073/pnas.95.25.14717

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Cernea M, Tang W, Guan H, Yang K (2015) Wisp1 mediates Bmp3-stimulated mesenchymal stem cell proliferation. J Mol Endocrinol 56:39–46. https://doi.org/10.1530/JME-15-0217

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Zhang Q, Zhang C, Li X et al (2016) WISP1 is increased in intestinal mucosa and contributes to inflammatory cascades in inflammatory bowel disease. Dis Markers. https://doi.org/10.1155/2016/3547096

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Ferrand N, Béreziat V, Moldes M et al (2017) WISP1/CCN4 inhibits adipocyte differentiation through repression of PPARγ activity. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-01866-2

    CAS  Article  Google Scholar 

  15. 15.

    Yeger H, Perbal B (2007) The ccn family of genes: a perspective on ccn biology and therapeutic potential. J Cell Commun Signal 1:159–164. https://doi.org/10.1007/s12079-008-0022-6

    Article  PubMed  Google Scholar 

  16. 16.

    Holbourn KP, Acharya KR, Perbal B (2008) The CCN family of proteins: structure-function relationships. Trends Biochem Sci 33:461–473. https://doi.org/10.1016/j.tibs.2008.07.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Perbal B (2004) CCN proteins: multifunctional signalling regulators. Lancet 363:62–64. https://doi.org/10.1016/S0140-6736(03)15172-0

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Hu K, Tao Y, Li J et al (2019) A comparative genomic and phylogenetic analysis of the origin and evolution of the CCN gene family. Biomed Res Int. https://doi.org/10.1155/2019/8620878

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Si W, Kang Q, Luu HH et al (2006) CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol 26:2955–2964. https://doi.org/10.1128/mcb.26.8.2955-2964.2006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Nephroblastoma R, Ccn O, Brigstock DR (1999) The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev 20:189–206

    Google Scholar 

  21. 21.

    Hu F, Lin Y, Zuo Y et al (2019) CCN1 induces adipogenic differentiation of fibro/adipogenic progenitors in a chronic kidney disease model. Biochem Biophys Res Commun. https://doi.org/10.1016/j.bbrc.2019.10.047

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Nishida T, Kubota S, Aoyama E et al (2015) CCN family protein 2 (CCN2) promotes the early differentiation, but inhibits the terminal differentiation of skeletal myoblasts. J Biochem 157:91–100. https://doi.org/10.1093/jb/mvu056

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Aoyama E, Kubota S, Khattab HM et al (2015) CCN2 enhances RANKL-induced osteoclast differentiation via direct binding to RANK and OPG. Bone 73:242–248. https://doi.org/10.1016/j.bone.2014.12.058

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Peidl A (2018) A friend in knee: CCN3 may inhibit osteoarthritis progression. J Cell Commun Signal 12:489–490. https://doi.org/10.1007/s12079-017-0446-y

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Feng J, Wang X, Li H et al (2018) Silencing of Annexin A1 suppressed the apoptosis and inflammatory response of preeclampsia rat trophoblasts. Int J Mol Med 42:3125–3134. https://doi.org/10.3892/ijmm.2018.3887

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    de Graauw M, van Miltenburg MH, Schmidt MK et al (2010) Annexin A1 regulates TGF-β signaling and promotes metastasis formation of basal-like breast cancer cells. Proc Natl Acad Sci USA 107:6340–6345. https://doi.org/10.1073/pnas.0913360107

    Article  PubMed  Google Scholar 

  27. 27.

    Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371. https://doi.org/10.1152/physrev.00030.2001

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    De Kroon LMG, Narcisi R, Van Den Akker GGH et al (2017) SMAD3 and SMAD4 have a more dominant role than SMAD2 in TGFβ-induced chondrogenic differentiation of bone marrow-derived mesenchymal stem cells. Sci Rep 7:1–13. https://doi.org/10.1038/srep43164

    Article  Google Scholar 

  29. 29.

    Wang W, Song B, Anbarchian T et al (2016) Smad2 and Smad3 regulate chondrocyte proliferation and differentiation in the growth plate. PLoS Genet 12:1–25. https://doi.org/10.1371/journal.pgen.1006352

    CAS  Article  Google Scholar 

  30. 30.

    Yu M, Wang H, Liu Z et al (2017) Ebp1 regulates myogenic differentiation of myoblast cells via SMAD2/3 signaling pathway. Dev Growth Differ 59:540–551. https://doi.org/10.1111/dgd.12380

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Kurundkar AR, Kurundkar D, Rangarajan S et al (2016) The matricellular protein CCN1 enhances TGF-β1/SMAD3-dependent profibrotic signaling in fibroblasts and contributes to fibrogenic responses to lung injury. FASEB J 30:2135–2150. https://doi.org/10.1096/fj.201500173

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Purohit T, Qin Z, Quan C et al (2017) Smad3-dependent CCN2 mediates fibronectin expression in human skin dermal fibroblasts. PLoS ONE 12:1–17. https://doi.org/10.1371/journal.pone.0173191

    CAS  Article  Google Scholar 

  33. 33.

    Yoshioka Y, Ono M, Maeda A et al (2016) CCN4/WISP-1 positively regulates chondrogenesis by controlling TGF-β3 function. Bone 83:162–170. https://doi.org/10.1016/j.bone.2015.11.007

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Ono M, Inkson CA, Kilts TM et al (2011) WISP-1/CCN4 regulates osteogenesis by enhancing BMP-2 activity. J Bone Miner Res 26:193–208. https://doi.org/10.1002/jbmr.205

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Inkson CA, Ono M, Kuznetsov SA et al (2008) TGF-β1 and WISP-1/CCN-4 can regulate each other’s activity to cooperatively control osteoblast function. J Cell Biochem 104:1865–1878. https://doi.org/10.1002/jcb.21754

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Natural Science Foundation of Heilongjiang Province (Grant No. C2017025).

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CZ, HT, SL, and YY involved in conceptualization; CZ and YZ took part in methodology; CZ and WZ performed formal analysis and investigation; CZ involved in writing—original draft preparation; CZ and YY performed writing—review and editing; and HT and SL participated in supervision.

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Correspondence to Yunqin Yan.

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Zhang, C., Zhang, Y., Zhang, W. et al. WISP1 promotes bovine MDSC differentiation via recruitment of ANXA1 for the regulation of the TGF-β signalling pathway. Mol Cell Biochem 470, 215–227 (2020). https://doi.org/10.1007/s11010-020-03763-1

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Keywords

  • Skeletal muscle
  • Bovine
  • Differentiation
  • WISP1
  • TGF-β
  • ANXA1