Korean J Physiol Pharmacol.  2022 Jul;26(4):287-295. 10.4196/kjpp.2022.26.4.287.

Adipose-derived stem cells decolonize skin Staphylococcus aureus by enhancing phagocytic activity of peripheral blood mononuclear cells in the atopic rats

Affiliations
  • 1Neuroscience Research Institute and Department of Physiology, Korea University College of Medicine, Seoul 02841, Korea
  • 2Glovi Plastic Surgery, Seoul 06031, Korea
  • 3Department of Microbiology, Korea University College of Medicine, Seoul 02841, Korea
  • 4Division of Biological Science and Technology, Science and Technology College, Yonsei University Mirae Campus, Wonju 26493, Korea
  • 5Department of Biomedical Laboratory Science, College of Medical Science, Konyang University, Daejeon 35365, Korea

Abstract

Staphylococcus aureus (S. aureus ) is known to induce apoptosis of host immune cells and impair phagocytic clearance, thereby being pivotal in the pathogenesis of atopic dermatitis (AD). Adipose-derived stem cells (ASCs) exert therapeutic effects against inflammatory and immune diseases. In the present study, we investigated whether systemic administration of ASCs restores the phagocytic activity of peripheral blood mononuclear cells (PBMCs) and decolonizes cutaneous S. aureus under AD conditions. AD was induced by injecting capsaicin into neonatal rat pups. ASCs were extracted from the subcutaneous adipose tissues of naïve rats and administered to AD rats once a week for a month. Systemic administration of ASCs ameliorated AD-like symptoms, such as dermatitis scores, serum IgE, IFN-γ+/IL-4+ cell ratio, and skin colonization by S. aureus in AD rats. Increased FasL mRNA and annexin V+/7-AAD+ cells in the PBMCs obtained from AD rats were drastically reversed when co-cultured with ASCs. In contrast, both PBMCs and CD163+ cells bearing fluorescent zymosan particles significantly increased in AD rats treated with ASCs. Additionally, the administration of ASCs led to an increase in the mRNA levels of antimicrobial peptides, such as cathelicidin and β-defensin, in the skin of AD rats. Our results demonstrate that systemic administration of ASCs led to decolonization of S. aureus by attenuating apoptosis of immune cells in addition to restoring phagocytic activity. This contributes to the improvement of skin conditions in AD rats. Therefore, administration of ASCs may be helpful in the treatment of patients with intractable AD.

Keyword

Adipose-derived stem cells; Antimicrobial peptides; Atopic dermatitis; Phagocytosis; Staphylococcus aureus

Figure

  • Fig. 1 Systemic injection of adipose-derived stem cells (ASCs) ameliorates atopic dermatitis. (A) Schematic illustration of experimental schedule. Atopic dermatitis was induced by subcutaneous injection of capsaicin (50 mg/kg) into newborn rat pups. Four weeks after the treatment, the animals were subjected to evaluation of dermatitis followed by administration of ASCs (1 × 106 cells/10 μl Hartman solution, i.v.), once a week for a month. (B) Amelioration of atopic dermatitis following the four consecutive weekly injection of ASCs. ‘AD’ refers to the control atopic rat, while ‘AD + ASC’ refers to the atopic animals treated with ASCs. The skin lesions were resected from the back of both animals. Scale bar = 200 µm. AD, atopic dermatitis. (C) Changes in dermatitis scores after injection of ASCs. ***p < 0.001, t-test; ###p < 0.001, paired t-test. (D) Serum level of IgE in eight week old rats. **p < 0.01, ***p < 0.001, one-way ANOVA. (E) Increase in IFN-γ+/IL-4+ cell ratio after injection of ASCs in eight week old rats. ** p <0.01, t-test. (F) Populations of total CD163+ cells among the experimental groups. ***p < 0.001, one-way ANOVA.

  • Fig. 2 Deteriorative effect of cutaneous S. aureus on apoptotic cell death and phagocytic activity of the peripheral blood mononuclear cells (PBMCs). (A–D) Skin colonization by S. aureus in the eight-week-old AD rat. Clusters of Gram-positive staphylococci are shown in the superficial layers of the AD rat skins. All the skin samples presented here were obtained from the back of animals. Scale bar = 50 μm. (E) Fractions of Annexin V+/7-AAD+ cells to the total PBMCs in both the naïve and AD rats. (F, G) Populations of the phagocytic PBMCs (F) and CD163+ cells (G), both of which have fluorescent zymosan A bioparticles inside the cells. AD, atopic dermatitis. **p < 0.01, ***p < 0.001, t-test.

  • Fig. 3 Adipose-derived stem cells (ASCs) attenuates apoptotic cell death of the peripheral blood mononuclear cells (PBMCs) and restores phagocytic activity of CD163+ cells when co-cultured with atopic dermatitis (AD) PBMCs. (A) Quantitative analyses for FasL mRNA of the PBMCs. Naïve and AD refers to the monoculture of the PBMCs from the naïve and AD rats, respectively. AD + ASC represents the co-culture of AD PBMCs and ASCs. Upregulation of FasL mRNA expression in the AD PBMCs is partially reversed by co-culture with ASCs. **p < 0.002, ***p < 0.001, one-way ANOVA. (B) Fractions of Annexin V+/7-AAD+ cells to the total PBMCs. #p < 0.05, t-test. (C) Populations of the CD163+ cells bearing fluorescent zymosan A bioparticles inside the cells. #p < 0.05, t-test.

  • Fig. 4 Systemic administration of adipose-derived stem cells (ASCs) attenuates apoptotic cell death of the peripheral blood mononuclear cells (PBMCs) and restores phagocytic activities of both PBMCs and CD163+ cells. (A) Fractions of Annexin V+/7-AAD+ cells to the total PBMCs. ‘AD’ refers to the control atopic rat, while ‘AD + ASC’ refers to the atopic animals treated with ASCs. (B, C) Populations of the phagocytic PBMCs (B) and CD163+ cells (C), both of which bear fluorescent zymosan A bioparticles inside the cells. AD, atopic dermatitis. *p < 0.05, **p < 0.01, ***p < 0.001, one-way ANOVA.

  • Fig. 5 Systemic administration of adipose-derived stem cells (ASCs) lead to decolonization of S. aureus and upregulation of antimicrobial peptides in the atopic dermatitis (AD) rat skins. (A–D) Histological illustrations showing cutaneous colonization by S. aureus. ‘AD’ and ‘AD + ASC’ refer to the control atopic rats and atopic animals treated with ASCs, respectively. Arrow heads indicate clusters of Gram-positive staphylococcal cells visualized by Gram (A, B) and immunofluorescent staining (C, D). The skin lesions were resected from the back of both animals. Scale bar = 200 µm (A, B) or 50 µm (C, D), respectively. (E) Quantitative analysis of cutaneous S. aureus by comparison of colony-forming units (CFU). (F, G) Quantitative analyses of mRNA expression for antimicrobial peptides, cathelicidin (F) and β-defensin (G), in the rat skins. *p < 0.05, ***p < 0.001, t-test.


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