Cmm Satta – Our understanding of tendon biology continues to advance, leading to opportunities to develop novel, evidence-based, and effective therapies for the treatment of tendon diseases. Implementation of knowledge about tendon stem/progenitor cells (TSPCs) and evaluation of their potential to enhance tendon repair may fill an important gap in this regard. We described the diverse molecular and phenotypic profiles of TSPCs and their pluripotent and secretory activities modulated by culture density. We also examined the different responses to inflammatory stimuli mediated by TNFα and IFNγ in the same experimental setting. We also preliminarily investigated their immunomodulatory activity and role in regulating the degradation of substance P. Our findings indicate that TSPCs cultured at low density (LD) have a cobblestone morphology and reduced tendency to differentiation. A unique immunophenotypic profile was also observed with high secretion and a promising immunomodulatory response when primed with TNFα and IFNγ. In contrast, TSPCs cultured at high density (HD) showed a more elongated fibroblast-like morphology, greater adipose differentiation potential and higher expression of tendon-related genes associated with LD. Finally, HD TSPCs showed immunomodulatory potential when primed with TNFα and IFNγ, which was slightly lower than LD. Shifting from low to high density culture during TSPC expansion showed intermediate features confirming the cellular adaptability of TSPCs. Taken together, these experiments allowed us to identify relevant differences in TSPCs depending on culture conditions. This ability of TSPCs to acquire distinct morphologies, phenotypes, gene expression profiles and functional responses advances our current understanding of tendons at the cellular level and suggests their responsiveness to cues.
Tendon injuries and pathologies are often painful and debilitating conditions that affect both athletes and non-athletes. Historically, tendons were considered to be affected by chronic degenerative events, mainly due to overuse. However, new studies have revealed the presence of immune cells and inflammatory cytokines in tendons that may be a major contributor to tendon-related diseases such as tendinopathy (Millar et al., 2009; Kendal et al. , 2020). The role of inflammation in recruiting immune cells to the site of the lesion is important. The interaction of these cells with tendon cells precedes the establishment of an inflammatory amplification loop involving multiple changes of the tissue matrix (Garcia-Melchor et al., 2021). In a physiological state, the nerve compartments are involved in normal body movements. However, it also plays an important role in the pathogenesis of tendinopathy, as excessive stimulation causes tissue damage and degeneration along with nerve innervation. The release of neuropeptides, such as substance P, stimulates mast cell degranulation, with subsequent release of agents that regulate many cellular activities within the matrix (Scott and Bahr, 2009; Han et al., 2021 ; Millar et al., 2021). Despite much progress in understanding the pathogenesis of tendon diseases, the standard clinical treatment remains unclear (Millar et al., 2021). Basic research supporting tendon biology and related pathologies continues to be pursued to guide the development of new evidence-based therapies.
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New frontiers in tendon-related research focus on the study of rare cell populations hidden in tissues that exhibit stem cell properties that represent an attractive and promising option for the development of more targeted therapies (Bi et al., 2007). The cells belonging to this heterogeneous population are referred to as tendon stem/progenitor cells (TSPCs) (Bi et al., 2007). These are generally defined as clonogenic, self-renewing and multipotent cells and include mesenchymal stem cells (MSCs) such as CD44+, CD90+, CD105+, CD146+, CD31- and CD45- (Lui and Chan, 2011). TSPCs differ from MSCs in their transcriptional profile with higher levels of tendon-related gene expression (Tan et al., 2012). Much progress has been made in identifying and characterizing distinct TSPC subpopulations using single cell analysis, providing a more complete view of TSPC identity (Harvey et al., 2019; Mienaltowski et al., 2019; Kendal et al. al., 2020; Huang et al., 2021). TSPCs have attracted much attention for their important role in tendon development, homeostasis and healing (Bi et al., 2007; Millar et al., 2021). However, many aspects about TSPCs remain controversial because there is no specific marker that uniquely identifies these cells to date.
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It is challenging (Lui, 2013). Overall, more efforts are needed to exploit its potential in the clinical setting. A growing number of studies have revealed that low-density culture methods of isolated tendon cells can be beneficial for the growth of TSPCs (Rui et al., 2010; Mienaltowski et al. ., 2014; Lee et al., 2018; Wu et al. ., 2020).) in culture. However, heterogeneity of related methods is observed in TSPC characterization studies.
(Li et al., 2021). Starting from this premise, we sought to further dissect the role of TSPCs in both physiological and pathological settings by examining the influence of culture conditions on the phenotypic and functional properties of TSPCs. In this regard, TSPC is low (50 cells/cm)
) and transition from low density to high density during cell expansion to obtain a phenotype with hybrid features. The phenotype, transcriptional and secretory profiles of these three groups have been characterized and comprehensively described. We also investigated gene expression and secretory activity responses to inflammatory stimuli. We also co-cultured stimulated T cells to explore their immunomodulatory capacity and function and their ability to degrade nociceptive substance P produced in the early stages of tendinopathy (Backman et al., 2011; Tran et al., 2020).
This study was conducted at the University of Miami (UM-Miami) and the IRCCS Istituto Ortopedico Galeazzi (IOG-Milan). Tendon tissue was obtained at the IOG from a known and unknown human donor prior to optional procedures for waste collection. This protocol was approved by the regional IOG Institutional Review Board (M-SPER-014-Ver.8-08.11.2016). After cell collection, samples were transported to UM-Miami for all other analyses. This study was conducted in accordance with the Declaration of Helsinki.
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Semitendinosus and gracilis tendons were collected from donors (n = 6, male, 33 ± 8 years/o) undergoing elective anterior cruciate ligament (ACL) reconstruction. Harvested samples were enzymatically digested with 0.3% w/v collagenase type I (185 U/mg, Worthington Biochemical Corporation) for 16 h to isolate human tendon stem/progenitor cells (TSPCs) and tendon from the remains of other tissues. TSPC at low concentration (50 cells/cm
, LD TSPC) (Rui et al., 2010; Viganò et al., 2017; Wu et al., 2020) or high density (5000 cells/cm
, HD TSPCs) and low-glucose DMEM containing 20% and 10% FBS, respectively, L-glutamine and penicillin-streptomycin (Life Technology) (GE Healthcare) at 37 °C, 5% CO
. LD TSPCs grew as colonies. When colonies reach a certain size, LDs are isolated and re-inoculated at low or high density (the latter named LDHD). The confluency gauge is based on the percentage of colonies relative to the rest of the surface that have avoided contact between colonies. In contrast, HDs were isolated at 80% confluence and reseeded only at high density. As a result, three groups (LD, HD and LDHD) were subsequently obtained. A schematic of the method used is shown in Figure 1. In passage 2, cells were analyzed for morphology, growth kinetics, and proliferation rate. Each cell culture condition was tested for growth kinetics by the IncuCyte® Live Cell Analysis System. Images at 10x magnification were acquired for morphology and proliferation rate analysis using IncuCyte ZOOM® software (Essen Bioscience).
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Adipogenic, osteogenic and chondrogenic differentiation assays were performed in LD, HD and LDHD. For adipose differentiation, cells were cultured for 14 days in StemPro™ Adipogenic Medium (Gibco). For osteogenic differentiation, cells were cultured in StemPro™ Osteogenic Differentiation Medium for 21 days (Gibco). All cells were fixed with 10% neutral buffered formalin (NBF) for 10 min, washed, and stained with their respective stains. Lipid droplet formation was detected with Oil Red O, whereas calcium deposition was detected with Alizarin Red. Images were captured at 10x magnification and stains were eluted for quantification. Briefly, cells stained with Oil Red O and Alizarin Red were incubated in isopropyl alcohol or 10% cetylpyridinium chloride solution for 1 hour each. Elusion absorbance measurements were read using a plate reader at 584 nm optical density. Destained cells were washed and protein lysates were extracted using Pierce® RIPA buffer (Thermo Fisher Scientific). Lysates were quantified for total protein using the Pierce™ BCA Protein Assay Kit (Thermo Fisher Scientific). Adipogenesis and osteogenesis were expressed as OD values normalized to total protein for each sample.
Cells) MesenCult-ACF differentiation medium (STEMCELL Technologies Inc). After digestion, sulfated glycosaminoglycan (sGAG) was quantified using the Blyscan Glycosaminoglycan Assay (Biocolor) according to the manufacturer’s instructions (1 mg/ml papain solution overnight at 65 °C). DNA was quantified using the Fluorescent DNA Quantitation Kit (Bio-Rad Laboratories). Histology for both hematoxylin and eosin (H&E) and 1% toluidine blue was performed on harvested and cryosectioned cartilage pellets. For each condition, samples in which no difference was induced were used as controls.
Flow cytometry was performed for LD, HD and LDHD using a CytoFLEX flow cytometer (Beckman Coulter Life Sciences). 2×10
Cells were suspended in staining buffer and incubated for 20 min at 4 °C with fluorescently conjugated anti-human antibody: CD90-FITC.
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