NaHS-Hydrogel and Encapsulated Adipose-Derived Stem Cell Evaluation on an Ex Vivo Second-Degree Burn Model
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Statement
2.2. Skin Explant: Burn Procedure and Culture
2.3. NaHS Hydrogel Treatment
2.4. Origin, Isolation, and Culture of ASCs
2.5. Encapsulation of ASCs in Alginate
2.6. ASC Treatment
2.7. Histological and Immunohistological Analysis of Skin Explants Treated with NaHS and ASCs
2.8. Image Analysis
2.9. Statistical Analysis
3. Results
3.1. Impact of NaHS and Encapsulated ASCs on Epidermis on Second-Degree Ex Vivo Burn Model
3.2. Impact of NaHS and Encapsulated ASCs on Dermis in Second-Degree Ex Vivo Burn Model
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Greenhalgh, D.G. Management of Burns. N. Engl. J. Med. 2019, 380, 2349–2359. [Google Scholar] [CrossRef]
- Finnerty, C.C.; Jeschke, M.G.; Branski, L.K.; Barret, J.P.; Dziewulski, P.; Herndon, D.N. Hypertrophic scarring: The greatest unmet challenge following burn injury. Lancet 2016, 388, 1427–1436. [Google Scholar] [CrossRef] [Green Version]
- Jeschke, M.G.; Shahrokhi, S.; Finnerty, C.C.; Branski, L.K.; Dibildox, M. Wound Coverage Technologies in Burn Care: Established Techniques. J. Burn Care Res. 2018, 39, 313–318. [Google Scholar] [CrossRef] [PubMed]
- Saeidinia, A.; Keihanian, F.; Lashkari, A.P.; Lahiji, H.G.; Mobayyen, M.; Heidarzade, A.; Golchai, J. Partial-thickness burn wounds healing by topical treatment: A randomized controlled comparison between silver sulfadiazine and centiderm. Medicine 2017, 96, e6168. [Google Scholar] [CrossRef]
- Wasiak, J.; Cleland, H.; Campbell, F.; Spinks, A. Dressings for superficial and partial thickness burns. Cochrane Database Syst. Rev. 2013, 2013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Auxenfans, C.; Menet, V.; Catherine, Z.; Shipkov, H.; Lacroix, P.; Bertin-Maghit, M.; Damour, O.; Braye, F. Cultured autologous keratinocytes in the treatment of large and deep burns: A retrospective study over 15 years. Burns 2015, 41, 71–79. [Google Scholar] [CrossRef]
- Coolen, N.A.; Vlig, M.; van den Bogaerdt, A.J.; Middelkoop, E.; Ulrich, M.M.W. Development of an in vitro burn wound model. Wound Repair Regen. 2008, 16, 559–567. [Google Scholar] [CrossRef]
- Emanuelsson, P.; Kratz, G. Characterization of a new in vitro burn wound model. Burns 1997, 23, 32–36. [Google Scholar] [CrossRef]
- Qu, M.; Kruse, S.; Pitsch, H.; Pallua, N.; Nourbakhsh, M. Viability of human composite tissue model for experimental study of burns. Discov. Med. 2016, 22, 19–28. [Google Scholar] [PubMed]
- Holzer, J.C.J.; Tiffner, K.; Kainz, S.; Reisenegger, P.; Bernardelli de Mattos, I.; Funk, M.; Lemarchand, T.; Laaff, H.; Bal, A.; Birngruber, T.; et al. A novel human ex-vivo burn model and the local cooling effect of a bacterial nanocellulose-based wound dressing. Burns 2020. [Google Scholar] [CrossRef] [PubMed]
- Sivamani, R.; Pullar, C.; Manabat-Hidalgo, C.; Rocke, D.; Carlsen, R.; Greenhalgh, D.; Isseroff, R. Stress-Mediated Increases in Systemic and Local Epinephrine Impair Skin Wound Healing: Potential New Indication for Beta Blockers. PLoS Med. 2009, 6, e1000012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gross-Amat, O.; Guillen, M.; Salmon, D.; Nataf, S.; Auxenfans, C. Characterization of a Topically Testable Model of Burn Injury on Human Skin Explants. Int. J. Mol. Sci. 2020, 21, 6956. [Google Scholar] [CrossRef] [PubMed]
- Balaji, S.; Moles, C.M.; Bhattacharya, S.S.; LeSaint, M.; Dhamija, Y.; Le, L.D.; King, A.; Kidd, M.; Bouso, M.F.; Shaaban, A.; et al. Comparison of interleukin 10 homologs on dermal wound healing using a novel human skin ex vivo organ culture model. J. Surg. Res. 2014, 190, 358–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tomic-Canic, M.; Mamber, S.W.; Stojadinovic, O.; Lee, B.; Radoja, N.; McMichael, J. Streptolysin O enhances keratinocyte migration and proliferation and promotes skin organ culture wound healing in vitro. Wound Repair Regen. 2007, 15, 71–79. [Google Scholar] [CrossRef] [PubMed]
- Huang, A.; Seité, S.; Adar, T. The use of balneotherapy in dermatology. Clin. Dermatol. 2018, 36, 363–368. [Google Scholar] [CrossRef]
- Carbajo, J.M.; Maraver, F. Sulphurous Mineral Waters: New Applications for Health. Evid.-Based Complement. Altern. Med. ECAM 2017, 2017, 8034084. [Google Scholar] [CrossRef]
- Carubbi, C.; Gobbi, G.; Bucci, G.; Gesi, M.; Vitale, M.; Mirandola, P. Skin, Inflammation and Sulfurous Waters: What is Known, What is Believed. Eur. J. Inflamm. 2013, 11, 591–599. [Google Scholar] [CrossRef] [Green Version]
- Gianfaldoni, S.; Tchernev, G.; Wollina, U.; Roccia, M.G.; Fioranelli, M.; Gianfaldoni, R.; Lotti, T. History of the Baths and Thermal Medicine. Open Access Maced. J. Med. Sci. 2017, 5, 566–568. [Google Scholar] [CrossRef] [Green Version]
- Parihar, A.; Parihar, M.S.; Milner, S.; Bhat, S. Oxidative stress and anti-oxidative mobilization in burn injury. Burns 2008, 34, 6–17. [Google Scholar] [CrossRef]
- Sahib, A.S.; Al-Jawad, F.H.; Al-Kaisy, A.A. Burns, Endothelial Dysfunction, and Oxidative Stress: The Role of Antioxidants. Ann. Burns Fire Disasters 2009, 22, 6–11. [Google Scholar] [PubMed]
- Sahib, A.S.; Al-Jawad, F.H.; Alkaisy, A.A. Effect of Antioxidants on the Incidence of Wound Infection in Burn Patients. Ann. Burns Fire Disasters 2010, 23, 199–205. [Google Scholar]
- Roshangar, L.; Soleimani Rad, J.; Kheirjou, R.; Reza Ranjkesh, M.; Ferdowsi Khosroshahi, A. Skin Burns: Review of Molecular Mechanisms and Therapeutic Approaches. Wounds Compend. Clin. Res. Pract. 2019, 31, 308–315. [Google Scholar]
- Riyaz, N.; Arakkal, F.R. Spa therapy in dermatology. Indian J. Dermatol. Venereol. Leprol. 2011, 77, 128. [Google Scholar] [CrossRef]
- Fazlzadeh, M.; Rostami, R.; Baghani, A.N.; Hazrati, S.; Mokammel, A. Hydrogen sulfide concentrations in indoor air of thermal springs. Hum. Ecol. Risk Assess. Int. J. 2018, 24, 1441–1452. [Google Scholar] [CrossRef]
- Staffieri, A.; Abramo, A. Sulphurous-arsenical-ferruginous (thermal) water inhalations reduce nasal respiratory resistance and improve mucociliary clearance in patients with chronic sinonasal disease: Preliminary outcomes. Acta Otolaryngol. 2007, 127, 613–617. [Google Scholar] [CrossRef] [PubMed]
- Viegas, J.; Esteves, A.F.; Cardoso, E.M.; Arosa, F.A.; Vitale, M.; Taborda-Barata, L. Biological Effects of Thermal Water-Associated Hydrogen Sulfide on Human Airways and Associated Immune Cells: Implications for Respiratory Diseases. Front. Public Health 2019, 7. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.-D.; Li, J.-Y.; Qin, Y.; Liu, Q.; Liao, Z.-Z.; Xiao, X.-H. Exogenous Hydrogen Sulfide Alleviates-Induced Intracellular Inflammation in HepG2 Cells. Exp. Clin. Endocrinol. Diabetes 2020, 128, 137–143. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Liu, X. Hydrogen sulfide from a NaHS source attenuates dextran sulfate sodium (DSS)-induced inflammation via inhibiting nuclear factor-κB. J. Zhejiang Univ. Sci. B 2016, 17, 209–217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perry, M.M.; Hui, C.K.; Whiteman, M.; Wood, M.E.; Adcock, I.; Kirkham, P.; Michaeloudes, C.; Chung, K.F. Hydrogen sulfide inhibits proliferation and release of IL-8 from human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 2011, 45, 746–752. [Google Scholar] [CrossRef]
- Guan, R.; Wang, J.; Li, D.; Li, Z.; Liu, H.; Ding, M.; Cai, Z.; Liang, X.; Yang, Q.; Long, Z.; et al. Hydrogen sulfide inhibits cigarette smoke-induced inflammation and injury in alveolar epithelial cells by suppressing PHD2/HIF-1α/MAPK signaling pathway. Int. Immunopharmacol. 2020, 81, 105979. [Google Scholar] [CrossRef]
- Li, P.; Guo, X. A review: Therapeutic potential of adipose-derived stem cells in cutaneous wound healing and regeneration. Stem Cell Res. Ther. 2018, 9, 302. [Google Scholar] [CrossRef]
- Salgado, A.J.B.O.G.; Reis, R.L.G.; Sousa, N.J.C.; Gimble, J.M. Adipose tissue derived stem cells secretome: Soluble factors and their roles in regenerative medicine. Curr. Stem Cell Res. Ther. 2010, 5, 103–110. [Google Scholar] [CrossRef] [Green Version]
- Kachgal, S.; Putnam, A.J. Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms. Angiogenesis 2011, 14, 47–59. [Google Scholar] [CrossRef] [Green Version]
- Bertheuil, N.; Chaput, B.; Ménard, C.; Varin, A.; Laloze, J.; Watier, E.; Tarte, K. Adipose mesenchymal stromal cells: Definition, immunomodulatory properties, mechanical isolation and interest for plastic surgery. Ann. Chir. Plast. Esthet. 2019, 64, 1–10. [Google Scholar] [CrossRef]
- Maria, A.T.J.; Toupet, K.; Maumus, M.; Fonteneau, G.; Le Quellec, A.; Jorgensen, C.; Guilpain, P.; Noël, D. Human adipose mesenchymal stem cells as potent anti-fibrosis therapy for systemic sclerosis. J. Autoimmun. 2016, 70, 31–39. [Google Scholar] [CrossRef]
- De Becker, A.; Riet, I.V. Homing and migration of mesenchymal stromal cells: How to improve the efficacy of cell therapy? World J. Stem Cells 2016, 8, 73–87. [Google Scholar] [CrossRef] [PubMed]
- Angoulvant, D.; Ivanes, F.; Ferrera, R.; Matthews, P.G.; Nataf, S.; Ovize, M. Mesenchymal stem cell conditioned media attenuates in vitro and ex vivo myocardial reperfusion injury. J. Heart Lung Transplant. 2011, 30, 95–102. [Google Scholar] [CrossRef] [PubMed]
- Gnecchi, M.; Zhang, Z.; Ni, A.; Dzau, V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 2008, 103, 1204–1219. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Yan, X.; Lin, Y.; Tan, Q. Hepatocyte growth factor secreted from human adipose-derived stem cells inhibits fibrosis in hypertrophic scar fibroblasts. Curr. Mol. Med. 2020. [Google Scholar] [CrossRef] [PubMed]
- Capin, L.; Abbassi, N.; Lachat, M.; Calteau, M.; Barratier, C.; Mojallal, A.; Bourgeois, S.; Auxenfans, C. Encapsulation of Adipose-Derived Mesenchymal Stem Cells in Calcium Alginate Maintains Clonogenicity and Enhances their Secretory Profile. Int. J. Mol. Sci. 2020, 21, 6316. [Google Scholar] [CrossRef]
- Gross-Amat, O.; Guillen, M.; Gimeno, J.-P.; Salzet, M.; Lebonvallet, N.; Misery, L.; Auxenfans, C.; Nataf, S. Molecular Mapping of Hydrogen Sulfide Targets in Normal Human Keratinocytes. Int. J. Mol. Sci. 2020, 21, 4648. [Google Scholar] [CrossRef] [PubMed]
- Zhi, L.; Ang, A.D.; Zhang, H.; Moore, P.K.; Bhatia, M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J. Leukoc. Biol. 2007, 81, 1322–1332. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Sio, S.W.S.; Moochhala, S.; Bhatia, M. Role of hydrogen sulfide in severe burn injury-induced inflammation in mice. Mol. Med. Camb. Mass 2010, 16, 417–424. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Bhatia, M.; Moore, P.K. Hydrogen sulphide—A novel mediator of inflammation? Curr. Opin. Pharmacol. 2006, 6, 125–129. [Google Scholar] [CrossRef]
- Li, L.; Bhatia, M.; Zhu, Y.Z.; Zhu, Y.C.; Ramnath, R.D.; Wang, Z.J.; Anuar, F.B.M.; Whiteman, M.; Salto-Tellez, M.; Moore, P.K. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J. 2005, 19, 1196–1198. [Google Scholar] [CrossRef] [PubMed]
- Guo, L.; Peng, W.; Tao, J.; Lan, Z.; Hei, H.; Tian, L.; Pan, W.; Wang, L.; Zhang, X. Hydrogen Sulfide Inhibits Transforming Growth Factor-β1-Induced EMT via Wnt/Catenin Pathway. PLoS ONE 2016, 11, e0147018. [Google Scholar] [CrossRef] [Green Version]
- Hellmich, M.R.; Szabo, C. Hydrogen Sulfide and Cancer. In Chemistry, Biochemistry and Pharmacology of Hydrogen Sulfide. Handbook of Experimental Pharmacology; Springer: Cham, Switzerland, 2015; Volume 230, pp. 233–241. [Google Scholar] [CrossRef] [Green Version]
- Baskar, R.; Bian, J. Hydrogen sulfide gas has cell growth regulatory role. Eur. J. Pharmacol. 2011, 656, 5–9. [Google Scholar] [CrossRef]
- Eberle, F.C.; Brück, J.; Holstein, J.; Hirahara, K.; Ghoreschi, K. Recent advances in understanding psoriasis. F1000Research 2016, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danilenko, D.M. An Overview of the Pathogenesis of Immune-mediated Skin Injury. Toxicol. Pathol. 2016, 44, 536–544. [Google Scholar] [CrossRef]
- Ud-Din, S.; Bayat, A. Non-animal models of wound healing in cutaneous repair: In silico, in vitro, ex vivo, and in vivo models of wounds and scars in human skin. Wound Repair Regen. 2017, 25, 164–176. [Google Scholar] [CrossRef]
- Daryabeigi, R.; Heidari, M.; Hosseini, S.A.; Omranifar, M. Comparison of healing time of the 2nd degree burn wounds with two dressing methods of fundermol herbal ointment and 1% silver sulfadiazine cream. Iran. J. Nurs. Midwifery Res. 2010, 15, 97–101. [Google Scholar] [PubMed]
- Mojallal, A.; Lequeux, C.; Shipkov, C.; Rifkin, L.; Rohrich, R.; Duclos, A.; Brown, S.; Damour, O. Stem cells, mature adipocytes, and extracellular scaffold: What does each contribute to fat graft survival? Aesthetic Plast. Surg. 2011, 35, 1061–1072. [Google Scholar] [CrossRef] [PubMed]
- de Vos, P.; Lazarjani, H.A.; Poncelet, D.; Faas, M.M. Polymers in cell encapsulation from an enveloped cell perspective. Adv. Drug Deliv. Rev. 2014, 67–68, 15–34. [Google Scholar] [CrossRef]
- De Vos, P.; Hoogmoed, C.G.; Busscher, H.J. Chemistry and biocompatibility of alginate-PLL capsules for immunoprotection of mammalian cells. J. Biomed. Mater. Res. 2002, 60, 252–259. [Google Scholar] [CrossRef] [PubMed]
- Orive, G.; Ponce, S.; Hernández, R.M.; Gascón, A.R.; Igartua, M.; Pedraz, J.L. Biocompatibility of microcapsules for cell immobilization elaborated with different type of alginates. Biomaterials 2002, 23, 3825–3831. [Google Scholar] [CrossRef]
- Puissant, B.; Barreau, C.; Bourin, P.; Clavel, C.; Corre, J.; Bousquet, C.; Taureau, C.; Cousin, B.; Abbal, M.; Laharrague, P.; et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br. J. Haematol. 2005, 129, 118–129. [Google Scholar] [CrossRef]
- McIntosh, K.R. Evaluation of cellular and humoral immune responses to allogeneic adipose-derived stem/stromal cells. In Adipose-Derived Stem Cells. Methods in Molecular Biology; Humana Press: Totowa, NJ, USA, 2011; Volume 702, pp. 133–150. [Google Scholar] [CrossRef]
- Hassan, W.U.; Greiser, U.; Wang, W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 2014, 22, 313–325. [Google Scholar] [CrossRef]
- Saito, Y.; Shimada, M.; Utsunomiya, T.; Ikemoto, T.; Yamada, S.; Morine, Y.; Imura, S.; Mori, H.; Arakawa, Y.; Kanamoto, M.; et al. Homing effect of adipose-derived stem cells to the injured liver: The shift of stromal cell-derived factor 1 expressions. J. Hepato-Biliary-Pancreat. Sci. 2014, 21, 873–880. [Google Scholar] [CrossRef]
- Deng, J.; Shi, Y.; Gao, Z.; Zhang, W.; Wu, X.; Cao, W.; Liu, W. Inhibition of Pathological Phenotype of Hypertrophic Scar Fibroblasts Via Coculture with Adipose-Derived Stem Cells. Tissue Eng. Part A 2018, 24, 382–393. [Google Scholar] [CrossRef]
- Zarei, F.; Abbaszadeh, A. Stem cell and skin rejuvenation. J. Cosmet. Laser Ther. 2018, 20, 193–197. [Google Scholar] [CrossRef] [PubMed]
- Bliley, J.M.; Argenta, A.; Satish, L.; McLaughlin, M.M.; Dees, A.; Tompkins-Rhoades, C.; Marra, K.G.; Rubin, J.P. Administration of adipose-derived stem cells enhances vascularity, induces collagen deposition, and dermal adipogenesis in burn wounds. Burns 2016, 42, 1212–1222. [Google Scholar] [CrossRef] [PubMed]
- Domergue, S.; Bony, C.; Maumus, M.; Toupet, K.; Frouin, E.; Rigau, V.; Vozenin, M.-C.; Magalon, G.; Jorgensen, C.; Noël, D. Comparison between Stromal Vascular Fraction and Adipose Mesenchymal Stem Cells in Remodeling Hypertrophic Scars. PLoS ONE 2016, 11, e0156161. [Google Scholar] [CrossRef] [PubMed]
- Leonov, Y.I.; Shkumat, M.S.; Klymenko, P.P.; Hovorun, M.Y.; Guzyk, M.M.; Kuchmerovska, T.M.; Pishel, I.M. Effect of insulin-like growth factor transgene on wound healing in mice with streptozotocin-induced diabetes. Cytol. Genet. 2015, 49, 19–26. [Google Scholar] [CrossRef] [Green Version]
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Capin, L.; Gross-Amat, O.; Calteau, M.; Rovere, M.-R.; Salmon, D.; Auxenfans, C. NaHS-Hydrogel and Encapsulated Adipose-Derived Stem Cell Evaluation on an Ex Vivo Second-Degree Burn Model. Eur. Burn J. 2021, 2, 9-30. https://doi.org/10.3390/ebj2010002
Capin L, Gross-Amat O, Calteau M, Rovere M-R, Salmon D, Auxenfans C. NaHS-Hydrogel and Encapsulated Adipose-Derived Stem Cell Evaluation on an Ex Vivo Second-Degree Burn Model. European Burn Journal. 2021; 2(1):9-30. https://doi.org/10.3390/ebj2010002
Chicago/Turabian StyleCapin, Lucille, Olivia Gross-Amat, Marie Calteau, Marie-Rose Rovere, Damien Salmon, and Céline Auxenfans. 2021. "NaHS-Hydrogel and Encapsulated Adipose-Derived Stem Cell Evaluation on an Ex Vivo Second-Degree Burn Model" European Burn Journal 2, no. 1: 9-30. https://doi.org/10.3390/ebj2010002
APA StyleCapin, L., Gross-Amat, O., Calteau, M., Rovere, M.-R., Salmon, D., & Auxenfans, C. (2021). NaHS-Hydrogel and Encapsulated Adipose-Derived Stem Cell Evaluation on an Ex Vivo Second-Degree Burn Model. European Burn Journal, 2(1), 9-30. https://doi.org/10.3390/ebj2010002