Dynamics of CD44+ bovine nucleus pulposus cells with inflammation – Scientific Reports

  • Comer, C. & Conaghan, P. G. Tackling persistent low back pain in primary care. Practitioner. 253(1721), 32–43 (2009).

    PubMed 

    Google Scholar
     

  • Risbud, M. & Shapiro, I. M. Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat. Rev. Rheumatol. 10(1), 44–56 (2014).

    CAS 
    PubMed 

    Google Scholar
     

  • Le Maitre, C., Hoyland, J. & Freemont, A. Catabolic cytokine expression in degenerate and herniated human intervertebral discs: IL-1beta and TNFalpha expression profile. Arthritis Res. Ther. 9(4), R77 (2007).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Van den Akker, G. G. et al. Novel immortal human cell lines reveal subpopulations in the nucleus pulposus. Arthritis Res. Ther. 16, 1–16 (2014).


    Google Scholar
     

  • Chelberg, M. K., Banks, G. M., Geiger, D. F. & Oegema, T. R. Jr. Identification of heterogeneous cell populations in normal human intervertebral disc. J. Anat. 186(Pt 1), 43 (1995).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tekari, A. et al. Angiopoietin-1 receptor Tie2 distinguishes multipotent differentiation capability in bovine coccygeal nucleus pulposus cells. Stem Cell Res Ther 7(1), 75 (2016).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nakazawa, K. R. et al. Accumulation and localization of macrophage phenotypes with human intervertebral disc degeneration. The Spine J. 18(2), 343–356 (2018).

    PubMed 

    Google Scholar
     

  • Kawakubo, A. et al. Investigation of resident and recruited macrophages following disc injury in mice. J. Orthop. Res. 38(8), 1703–1709 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • Stevens, J. W. et al. CD44 expression in the developing and growing rat intervertebral disc. Dev. Dyn. 219(3), 381–390 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • Piras, M. et al. CD44 is highly expressed in stem/progenitor cells originating the intervertebral discs in the human notochord. Eur. Rev. Med. Pharmacol. Sci. 26(22), 8502–8507 (2022).

    CAS 
    PubMed 

    Google Scholar
     

  • Cherif, H., et al., Single-cell RNA-Seq analysis of cells from degenerating and non-degenerating intervertebral discs from the same individual reveals new biomarkers for intervertebral disc degeneration. Int. J. Mol. Sci. 23(7) (2022).

  • Culty, M. et al. The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J. Cell Biol. 111(6 Pt 1), 2765–2774 (1990).

    CAS 
    PubMed 

    Google Scholar
     

  • Cui, G. H. et al. Exosomes derived from hypoxia-preconditioned mesenchymal stromal cells ameliorate cognitive decline by rescuing synaptic dysfunction and regulating inflammatory responses in APP/PS1 mice. Faseb J. 32(2), 654–668 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • Mariggiò, M. A. et al. Enhancement of fibroblast proliferation, collagen biosynthesis and production of growth factors as a result of combining sodium hyaluronate and aminoacids. Int. J. Immunopathol. Pharmacol. 22(2), 485–492 (2009).

    PubMed 

    Google Scholar
     

  • Fujimoto, T. et al. CD44 binds a chondroitin sulfate proteoglycan, aggrecan. Int. Immunol. 13(3), 359–366 (2001).

    CAS 
    PubMed 

    Google Scholar
     

  • Levesque, M. C. & Haynes, B. F. Cytokine induction of the ability of human monocyte CD44 to bind hyaluronan is mediated primarily by TNF-alpha and is inhibited by IL-4 and IL-13. J. Immunol. 159(12), 6184–6194 (1997).

    CAS 
    PubMed 

    Google Scholar
     

  • Teixeira, G.Q., et al., A degenerative/proinflammatory intervertebral disc organ culture: An ex vivo model for anti-inflammatory drug and cell therapy. Tissue Eng. Part C, Methods 22(1): 8–19 (2016).

  • Molinos, M., et al., Alterations of bovine nucleus pulposus cells with aging. Aging Cell e13873 (2023).

  • Caldeira, J. et al. Matrisome profiling during intervertebral disc development and ageing. Sci. Rep. 7(1), 11629–11629 (2017).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Calió, M., et al., The cellular composition of bovine coccygeal intervertebral discs: A comprehensive single-cell RNAseq analysis. Int. J. Mol. Sci. 22(9) (2021).

  • Elshamly, M. et al. Galectins-1 and -3 in human intervertebral disc degeneration: Non-uniform distribution profiles and activation of disease markers involving NF-κB by Galectin-1. J. Orthop. Res. 37(10), 2204–2216 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cao, S. et al. Major ceRNA regulation and key metabolic signature analysis of intervertebral disc degeneration. BMC Musculoskelet. Disord. 22(1), 249 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rajasekaran, S. et al. Can scoliotic discs be controls for molecular studies in intervertebral disc research? Insights From Proteomics. Global Spine J. 12(4), 598–609 (2022).

    CAS 
    PubMed 

    Google Scholar
     

  • Joos, H. et al. IL-1beta regulates FHL2 and other cytoskeleton-related genes in human chondrocytes. Mol. Med. 14(3–4), 150–159 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klaassen, C. D. & Boles, J. W. The importance of 3‘-phosphoadenosine 5‘-phosphosulfate (PAPS) in the regulation of sulfation. The FASEB J. 11(6), 404–418 (1997).

    CAS 
    PubMed 

    Google Scholar
     

  • Paganini, C., Costantini, R. & Rossi, A. Analysis of proteoglycan synthesis and secretion in cell culture systems. Methods Mol. Biol. 1952, 71–80 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • Silagi, E. S., Shapiro, I. M. & Risbud, M. V. Glycosaminoglycan synthesis in the nucleus pulposus: Dysregulation and the pathogenesis of disc degeneration. Matrix Biol. 71–72, 368–379 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown, R. G., Button, G. M. & Smith, J. T. Changes in collagen metabolism caused by feeding diets low in inorganic sulfur. J. Nutr. 87(2), 228–232 (1965).

    CAS 
    PubMed 

    Google Scholar
     

  • Kobayashi, D., et al., The effect of pantothenic acid deficiency on keratinocyte proliferation and the synthesis of keratinocyte growth factor and collagen in fibroblasts. J. Pharmacol. Sci. advpub, 1101140493–1101140493 (2011).

  • Lakshmi, R., Lakshmi, A. V. & Bamji, M. S. Skin wound healing in riboflavin deficiency. Biochem. Med. Metab. Biol. 42(3), 185–191 (1989).

    CAS 
    PubMed 

    Google Scholar
     

  • Herscovics, A., 3.02 – Glycosidases of the Asparagine-linked Oligosaccharide Processing Pathway, in Comprehensive Natural Products Chemistry, S.D. Barton, K. Nakanishi, and O. Meth-Cohn, Editors. 1999, Pergamon: Oxford. 13–35.

  • Wopereis, S. et al. Mechanisms in protein O-Glycan biosynthesis and clinical and molecular aspects of protein O-Glycan biosynthesis defects: A review. Clin. Chem 52(4), 574–600 (2006).

    CAS 
    PubMed 

    Google Scholar
     

  • Lee, S. et al. Comparison of growth factor and cytokine expression in patients with degenerated disc disease and herniated nucleus pulposus. Clin. Biochem. 42(15), 1504–1511 (2009).

    CAS 
    PubMed 

    Google Scholar
     

  • Peng, J. et al. Inhibition of telomere recombination by inactivation of KEOPS subunit Cgi121 promotes cell longevity. PLoS Gene. 11(3), e1005071–e1005071 (2015).


    Google Scholar
     

  • Zhang, Y., et al., Changes in Nucleus Pulposus Cell Pools in “Healer” Mice for the Repair of Intervertebral Disc Degeneration. Global Spine J. 5(1_suppl), s-0035–1554499-s-0035–1554499 (2015).

  • Vélez-Cruz, R. et al. RB localizes to DNA double-strand breaks and promotes DNA end resection and homologous recombination through the recruitment of BRG1. Genes Dev. 30(22), 2500–2512 (2016).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Harada, H. et al. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 3(4), 413–422 (1999).

    CAS 
    PubMed 

    Google Scholar
     

  • Mukai, J. et al. NADE, a p75NTR-associated Cell Death Executor, Is Involved in Signal Transduction Mediated by the Common Neurotrophin Receptor p75NTR*. J. Biol. Chem. 275(23), 17566–17570 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • Paulson, J. R. Inactivation of Cdk1/Cyclin B in metaphase-arrested mouse FT210 cells induces exit from mitosis without chromosome segregation or cytokinesis and allows passage through another cell cycle. Chromosoma 116(2), 215–225 (2007).

    CAS 
    PubMed 

    Google Scholar
     

  • Kritschil, R. et al. Effects of suppressing bioavailability of insulin-like growth factor on age-associated intervertebral disc degeneration. JOR SPINE 3(4), e1112 (2020).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ouyang, Z.-H. et al. The PI3K/Akt pathway: a critical player in intervertebral disc degeneration. Oncotarget 8(34), 57870–57881 (2017).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Risbud, M.V., et al., Nucleus Pulposus Cells Upregulate PI3K/Akt and MEK/ERK signaling pathways under hypoxic conditions and resist apoptosis induced by serum withdrawal. Spine 30(8) (2005).

  • Zhou, Q. et al. Calcium phosphate cement causes nucleus pulposus cell degeneration through the ERK signaling pathway. Open Life Sci. 15(1), 209–216 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guda, K. et al. Inactivating germ-line and somatic mutations in polypeptide <em>N</em>-acetylgalactosaminyltransferase 12 in human colon cancers. Proc. Natl. Acad. Sci. 106(31), 12921–12925 (2009).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Karamatic Crew, V. et al. New mutations in C1GALT1C1 in individuals with Tn positive phenotype. British J. Haematol. 142(4), 657–667 (2008).


    Google Scholar
     

  • Peluso, G. et al. Loss of the disease-associated glycosyltransferase Galnt3 alters Muc10 glycosylation and the composition of the oral microbiome. J. Biol. Chem. 295(5), 1411–1425 (2020).

    PubMed 

    Google Scholar
     

  • Diaz-Romero, J. et al. Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. J. Cell Physiol. 214(1), 75–83 (2008).

    CAS 
    PubMed 

    Google Scholar
     

  • Wang, H. et al. Distinguishing characteristics of stem cells derived from different anatomical regions of human degenerated intervertebral discs. Eur. Spine J. 25(9), 2691–2704 (2016).

    PubMed 

    Google Scholar
     

  • Zhang, G. et al. CD44 clustering is involved in monocyte differentiation. Acta Biochim. Biophys. Sin. (Shanghai) 46(7), 540–547 (2014).

    CAS 
    PubMed 

    Google Scholar
     

  • Wu, H. et al. Regenerative potential of human nucleus pulposus resident stem/progenitor cells declines with ageing and intervertebral disc degeneration. Int. J. Mol. Med. 42(4), 2193–2202 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • Govindaraju, P. et al. CD44-dependent inflammation, fibrogenesis, and collagenolysis regulates extracellular matrix remodeling and tensile strength during cutaneous wound healing. Matrix Biol.: J. Int. Soc. Matrix Biol. 75–76, 314–330 (2019).


    Google Scholar
     

  • Mahlapuu, M. et al. The forkhead transcription factor Foxf1 is required for differentiation of extra-embryonic and lateral plate mesoderm. Development 128(2), 155–166 (2001).

    CAS 
    PubMed 

    Google Scholar
     

  • Ren, X. et al. FOXF1 transcription factor is required for formation of embryonic vasculature by regulating VEGF signaling in endothelial cells. Circ. Res. 115(8), 709–720 (2014).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fernandes, L.M., et al., Single-cell RNA-seq identifies unique transcriptional landscapes of human nucleus pulposus and annulus fibrosus cells. Sci. Rep. 10(1) (2020).

  • Richardson, S. M. et al. Notochordal and nucleus pulposus marker expression is maintained by sub-populations of adult human nucleus pulposus cells through aging and degeneration. Sci. Rep. 7(1), 1501 (2017).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Grant, M. P. et al. Human cartilaginous endplate degeneration is induced by calcium and the extracellular calcium-sensing receptor in the intervertebral disc. Eur. Cell Mater. 32, 137–151 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • Roberts, S., Ayad, S. & Menage, P. J. Immunolocalisation of type VI collagen in the intervertebral disc. Ann. Rheum. Dis. 50(11), 787–791 (1991).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nerlich, A. G. et al. Immunolocalization of major interstitial collagen types in human lumbar intervertebral discs of various ages. Virchows Archiv. 432(1), 67–76 (1998).

    CAS 
    PubMed 

    Google Scholar
     

  • Chen, P. et al. Collagen VI regulates peripheral nerve regeneration by modulating macrophage recruitment and polarization. Acta Neuropathol. 129(1), 97–113 (2015).

    CAS 
    PubMed 

    Google Scholar
     

  • Stoeckli, E.T., Understanding axon guidance: are we nearly there yet? Development 145(10) (2018).

  • Binch, A. L. A. et al. Nerves are more abundant than blood vessels in the degenerate human intervertebral disc. Arthr. Res. Ther. 17(1), 370 (2015).


    Google Scholar
     

  • Javanmard, D. et al. Investigation of CTNNB1 gene mutations and expression in hepatocellular carcinoma and cirrhosis in association with hepatitis B virus infection. Infect. Agents Cancer 15(1), 37 (2020).

    CAS 

    Google Scholar
     

  • van Neerven, S. M. et al. Apc-mutant cells act as supercompetitors in intestinal tumour initiation. Nature 594(7863), 436–441 (2021).

    ADS 
    PubMed 

    Google Scholar
     

  • Pizzute, T. et al. Impact of Wnt signals on human intervertebral disc cell regeneration. J. Orthop. Res.: Off. Publ. Orthop. Res. Soc. 36(12), 3196–3207 (2018).

    CAS 

    Google Scholar
     

  • Holguin, N. & Silva, M. J. In-vivo nucleus pulposus-specific regulation of adult murine intervertebral disc degeneration via Wnt/Beta-catenin signaling. Sci. Rep. 8(1), 11191 (2018).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aldiri, I. & Vetter, M. L. PRC2 during vertebrate organogenesis: a complex in transition. Dev. Biol. 367(2), 91–99 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deimling, S.J., Olsen, J.B., Tropepe, V., The expanding role of the Ehmt2/G9a complex in neurodevelopment. Neurogenesis (Austin, Tex.) 4(1), e1316888-e1316888 (2017).

  • Ikuno, A. et al. Genome-wide analysis of DNA methylation profile identifies differentially methylated loci associated with human intervertebral disc degeneration. PloS one 14(9), e0222188–e0222188 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Konopka, A. et al. Cleavage of hyaluronan and CD44 adhesion molecule regulate astrocyte morphology via rac1 signalling. PLOS ONE 11(5), e0155053 (2016).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Foger, N., Marhaba, R. & Zoller, M. Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells. J. Cell Sci. 114(6), 1169–1178 (2001).

    CAS 
    PubMed 

    Google Scholar
     

  • Roszkowska, M. et al. CD44: A novel synaptic cell adhesion molecule regulating structural and functional plasticity of dendritic spines. Mol. Biol. Cell 27(25), 4055–4066 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hermiston, M. L., Xu, Z. & Weiss, A. CD45: A critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21, 107–137 (2003).

    CAS 
    PubMed 

    Google Scholar
     

  • Maleki, M. et al. Comparison of mesenchymal stem cell markers in multiple human adult stem cells. Int. J. Stem Cells 7(2), 118–126 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zamoyska, R. Why is there so much CD45 on T cells?. Immunity 27(3), 421–423 (2007).

    CAS 
    PubMed 

    Google Scholar
     

  • Huang, Y. et al. Src-family kinases activation in spinal microglia contributes to central sensitization and chronic pain after lumbar disc herniation. Mol. Pain 13, 1744806917733637 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gao, G. et al. Periodic mechanical stress induces extracellular matrix expression and migration of rat nucleus pulposus cells through Src-GIT1-ERK1/2 signaling pathway. Cell Physiol. Biochem. 50(4), 1510–1521 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • Rangaraju, S. et al. Differential phagocytic properties of CD45(low) microglia and CD45(high) brain mononuclear phagocytes-activation and age-related effects. Front. Immunol. 9, 405 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jersmann, H. P. A. Time to abandon dogma: CD14 is expressed by non-myeloid lineage cells. Immunol. Cell Biol. 83(5), 462–467 (2005).

    CAS 
    PubMed 

    Google Scholar
     

  • Miyagi, M. et al. Role of CD14-positive cells in inflammatory cytokine and pain-related molecule expression in human degenerated intervertebral discs. J. Orthop. Res. 39(8), 1755–1762 (2021).

    CAS 
    PubMed 

    Google Scholar
     

  • Jones, P. et al. Intervertebral disc cells as competent phagocytes in vitro: Implications for cell death in disc degeneration. Arthr. Res. Ther. 10(4), R86 (2008).

    ADS 

    Google Scholar
     

  • Johnson, W. E., Stephan, S. & Roberts, S. The influence of serum, glucose and oxygen on intervertebral disc cell growth in vitro: implications for degenerative disc disease. Arthr. Res. Ther. 10(2), R46 (2008).


    Google Scholar
     

  • Tu, J. et al. Single-cell transcriptome profiling reveals multicellular ecosystem of nucleus pulposus during degeneration progression. Adv. Sci. (Weinh) 9(3), e2103631 (2022).

    PubMed 

    Google Scholar
     

  • Gruber, H. E. et al. Human annulus signaling cues for nerve outgrowth: In vitro studies. J. Orthop. Res. 34(8), 1456–1465 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • Menko, A. S. et al. Resident immune cells of the avascular lens: Mediators of the injury and fibrotic response of the lens. The FASEB J. 35(4), e21341 (2021).

    CAS 
    PubMed 

    Google Scholar