A Beginner's Introduction to Skin Stem Cells and Wound Healing
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
34681688
PubMed Central
PMC8538579
DOI
10.3390/ijms222011030
PII: ijms222011030
Knihovny.cz E-zdroje
- Klíčová slova
- non-healing wounds, skin regeneration, skin stem cells, tissue engineering, wound healing,
- MeSH
- fyziologie kůže MeSH
- hojení ran * MeSH
- kůže zranění MeSH
- lidé MeSH
- mezenchymální kmenové buňky MeSH
- regenerace * MeSH
- tkáňové inženýrství MeSH
- transplantace mezenchymálních kmenových buněk MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The primary function of the skin is that of a physical barrier against the environment and diverse pathogens; therefore, its integrity is essential for survival. Skin regeneration depends on multiple stem cell compartments within the epidermis, which, despite their different transcriptional and proliferative capacity, as well as different anatomical location, fall under the general term of skin stem cells (SSCs). Skin wounds can normally heal without problem; however, some diseases or extensive damage may delay or prevent healing. Non-healing wounds represent a serious and life-threatening scenario that may require advanced therapeutic strategies. In this regard, increased focus has been directed at SSCs and their role in wound healing, although emerging therapeutical approaches are considering the use of other stem cells instead, such as mesenchymal stem cells (MSCs). Given its extensive and broad nature, this review supplies newcomers with an introduction to SSCs, wound healing, and therapeutic strategies for skin regeneration, thus familiarizing the reader with the subject in preparation for future in depth reading.
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Park K. Role of Micronutrients in Skin Health and Function. Biomol. Ther. 2015;23:207–217. doi: 10.4062/biomolther.2015.003. PubMed DOI PMC
Kolarsick P., Kolarsick M., Goodwin C. Anatomy and Physiology of the Skin: Erratum. J. Dermatol. Nurses’ Assoc. 2011;3:366. doi: 10.1097/JDN.0b013e31823cccbe. DOI
Gaur M., Dobke M., Lunyak V. Mesenchymal Stem Cells from Adipose Tissue in Clinical Applications for Dermatological Indications and Skin Aging. Int. J. Mol. Sci. 2017;18:208. doi: 10.3390/ijms18010208. PubMed DOI PMC
Arron S. Anatomy of the Skin and Pathophysiology of Radiation Dermatitis. In: Fowble B., Yom S.S., Yuen F., Arron S., editors. Skin Care in Radiation Oncology. Springer International Publishing; Cham, Switzerland: 2016. pp. 9–14.
McGrath J.A., Uitto J. Anatomy and Organization of Human Skin. In: Burns T., Breathnach S., Cox N., Griffiths C., editors. Rook’s Textbook of Dermatology. Wiley-Blackwell; Oxford, UK: 2010. pp. 1–53.
Garland E.L. Pain Processing in the Human Nervous System. Prim. Care Clin. Off. Pract. 2012;39:561–571. doi: 10.1016/j.pop.2012.06.013. PubMed DOI PMC
Honari G., Maibach H. Applied Dermatotoxicology. Elsevier; Amsterdam, The Netherlands: 2014. Skin Structure and Function; pp. 1–10.
Leung Y., Kandyba E., Chen Y.-B., Ruffins S., Chuong C.-M., Kobielak K. Bifunctional Ectodermal Stem Cells around the Nail Display Dual Fate Homeostasis and Adaptive Wounding Response toward Nail Regeneration. Proc. Natl. Acad. Sci. USA. 2014;111:15114–15119. doi: 10.1073/pnas.1318848111. PubMed DOI PMC
Blanpain C., Fuchs E. Epidermal Homeostasis: A Balancing Act of Stem Cells in the Skin. Nat. Rev. Mol. Cell Biol. 2009;10:207–217. doi: 10.1038/nrm2636. PubMed DOI PMC
Seeger M.A., Paller A.S. The Roles of Growth Factors in Keratinocyte Migration. Adv. Wound Care. 2015;4:213–224. doi: 10.1089/wound.2014.0540. PubMed DOI PMC
Blanpain C., Fuchs E. Epidermal Stem Cells of the Skin. Ann. Rev. Cell Dev. Biol. 2006;22:339–373. doi: 10.1146/annurev.cellbio.22.010305.104357. PubMed DOI PMC
Fuchs E. Skin Stem Cells: Rising to the Surface. J. Cell Biol. 2008;180:273–284. doi: 10.1083/jcb.200708185. PubMed DOI PMC
Racila D., Bickenbach J.R. Are Epidermal Stem Cells Unique with Respect to Aging? Aging. 2009;1:746–750. doi: 10.18632/aging.100082. PubMed DOI PMC
Giangreco A., Qin M., Pintar J.E., Watt F.M. Epidermal Stem Cells Are Retained in Vivo throughout Skin Aging. Aging Cell. 2008;7:250–259. doi: 10.1111/j.1474-9726.2008.00372.x. PubMed DOI PMC
Mistriotis P., Andreadis S.T. Hair Follicle: A Novel Source of Multipotent Stem Cells for Tissue Engineering and Regenerative Medicine. Tissue Eng. Part B Rev. 2013;19:265–278. doi: 10.1089/ten.teb.2012.0422. PubMed DOI PMC
Soteriou D., Kostic L., Sedov E., Yosefzon Y., Steller H., Fuchs Y. Isolating Hair Follicle Stem Cells and Epidermal Keratinocytes from Dorsal Mouse Skin. J. Vis. Exp. 2016;110:53931. doi: 10.3791/53931. PubMed DOI PMC
Jaks V., Barker N., Kasper M., van Es J.H., Snippert H.J., Clevers H., Toftgård R. Lgr5 Marks Cycling, yet Long-Lived, Hair Follicle Stem Cells. Nat. Genet. 2008;40:1291–1299. doi: 10.1038/ng.239. PubMed DOI
Lang D., Mascarenhas J.B., Shea C.R. Melanocytes, Melanocyte Stem Cells, and Melanoma Stem Cells. Clin. Dermatol. 2013;31:166–178. doi: 10.1016/j.clindermatol.2012.08.014. PubMed DOI PMC
Hsu Y.-C., Li L., Fuchs E. Emerging Interactions between Skin Stem Cells and Their Niches. Nat. Med. 2014;20:847–856. doi: 10.1038/nm.3643. PubMed DOI PMC
Firth A.L., Yuan J.X.-J. Identification of Functional Progenitor Cells in the Pulmonary Vasculature. Pulm. Circ. 2012;2:84–100. doi: 10.4103/2045-8932.94841. PubMed DOI PMC
Morgan B.A. The Dermal Papilla: An Instructive Niche for Epithelial Stem and Progenitor Cells in Development and Regeneration of the Hair Follicle. Cold Spring Harb. Perspect. Med. 2014;4:a015180. doi: 10.1101/cshperspect.a015180. PubMed DOI PMC
Mull A., Zolekar A., Wang Y.-C. Understanding Melanocyte Stem Cells for Disease Modeling and Regenerative Medicine Applications. Int. J. Mol. Sci. 2015;16:30458–30469. doi: 10.3390/ijms161226207. PubMed DOI PMC
Achilleos A., Trainor P.A. Neural Crest Stem Cells: Discovery, Properties and Potential for Therapy. Cell Res. 2012;22:288–304. doi: 10.1038/cr.2012.11. PubMed DOI PMC
Zakrzewski W., Dobrzyński M., Szymonowicz M., Rybak Z. Stem Cells: Past, Present, and Future. Stem Cell Res. Ther. 2019;10:68. doi: 10.1186/s13287-019-1165-5. PubMed DOI PMC
Vapniarsky N., Arzi B., Hu J.C., Nolta J.A., Athanasiou K.A. Concise Review: Human Dermis as an Autologous Source of Stem Cells for Tissue Engineering and Regenerative Medicine: Dermis Stem Cells for Tissue Regeneration. Stem Cells Transl. Med. 2015;4:1187–1198. doi: 10.5966/sctm.2015-0084. PubMed DOI PMC
Ojeh N., Pastar I., Tomic-Canic M., Stojadinovic O. Stem Cells in Skin Regeneration, Wound Healing, and Their Clinical Applications. Int. J. Mol. Sci. 2015;16:25476–25501. doi: 10.3390/ijms161025476. PubMed DOI PMC
Legg J., Jensen U.B., Broad S., Leigh I., Watt F.M. Role of Melanoma Chondroitin Sulphate Proteoglycan in Patterning Stem Cells in Human Interfollicular Epidermis. Development. 2003;130:6049–6063. doi: 10.1242/dev.00837. PubMed DOI
Wan H., Stone M.G., Simpson C., Reynolds L.E., Marshall J.F., Hart I.R., Hodivala-Dilke K.M., Eady R.A.J. Desmosomal Proteins, Including Desmoglein 3, Serve as Novel Negative Markers for Epidermal Stem Cell-Containing Population of Keratinocytes. J. Cell Sci. 2003;116:4239–4248. doi: 10.1242/jcs.00701. PubMed DOI
Schneider T.E., Barland C., Alex A.M., Mancianti M.L., Lu Y., Cleaver J.E., Lawrence H.J., Ghadially R. Measuring Stem Cell Frequency in Epidermis: A Quantitative in Vivo Functional Assay for Long-Term Repopulating Cells. Proc. Natl. Acad. Sci. USA. 2003;100:11412–11417. doi: 10.1073/pnas.2034935100. PubMed DOI PMC
Potten C.S., Morris R.J. Epithelial Stem Cells in Vivo. J. Cell Sci. 1988;1988:45–62. doi: 10.1242/jcs.1988.Supplement_10.4. PubMed DOI
Jones P.H., Watt F.M. Separation of Human Epidermal Stem Cells from Transit Amplifying Cells on the Basis of Differences in Integrin Function and Expression. Cell. 1993;73:713–724. doi: 10.1016/0092-8674(93)90251-K. PubMed DOI
Clayton E., Doupé D.P., Klein A.M., Winton D.J., Simons B.D., Jones P.H. A Single Type of Progenitor Cell Maintains Normal Epidermis. Nature. 2007;446:185–189. doi: 10.1038/nature05574. PubMed DOI
Graf T., Stadtfeld M. Heterogeneity of Embryonic and Adult Stem Cells. Cell Stem Cell. 2008;3:480–483. doi: 10.1016/j.stem.2008.10.007. PubMed DOI
Li X., Upadhyay A.K., Bullock A.J., Dicolandrea T., Xu J., Binder R.L., Robinson M.K., Finlay D.R., Mills K.J., Bascom C.C., et al. Skin Stem Cell Hypotheses and Long Term Clone Survival—Explored Using Agent-Based Modelling. Sci. Rep. 2013;3:1904. doi: 10.1038/srep01904. PubMed DOI PMC
Mascré G., Dekoninck S., Drogat B., Youssef K.K., Brohée S., Sotiropoulou P.A., Simons B.D., Blanpain C. Distinct Contribution of Stem and Progenitor Cells to Epidermal Maintenance. Nature. 2012;489:257–262. doi: 10.1038/nature11393. PubMed DOI
Zomer H.D., Trentin A.G. Skin Wound Healing in Humans and Mice: Challenges in Translational Research. J. Dermatol. Sci. 2018;90:3–12. doi: 10.1016/j.jdermsci.2017.12.009. PubMed DOI
Gonzales K.A.U., Fuchs E. Skin and Its Regenerative Powers: An Alliance between Stem Cells and Their Niche. Dev. Cell. 2017;43:387–401. doi: 10.1016/j.devcel.2017.10.001. PubMed DOI PMC
Psarras S., Beis D., Nikouli S., Tsikitis M., Capetanaki Y. Three in a Box: Understanding Cardiomyocyte, Fibroblast, and Innate Immune Cell Interactions to Orchestrate Cardiac Repair Processes. Front. Cardiovasc. Med. 2019;6:32. doi: 10.3389/fcvm.2019.00032. PubMed DOI PMC
Kizil C., Kyritsis N., Brand M. Effects of Inflammation on Stem Cells: Together They Strive? EMBO Rep. 2015;16:416–426. doi: 10.15252/embr.201439702. PubMed DOI PMC
Logan C.Y., Nusse R. The wnt Signaling Pathway in Development and Disease. Ann. Rev. Cell Dev. Biol. 2004;20:781–810. doi: 10.1146/annurev.cellbio.20.010403.113126. PubMed DOI
Nusse R. Wnt Signaling and Stem Cell Control. Cell Res. 2008;18:523–527. doi: 10.1038/cr.2008.47. PubMed DOI
Clevers H. Wnt/β-Catenin Signaling in Development and Disease. Cell. 2006;127:469–480. doi: 10.1016/j.cell.2006.10.018. PubMed DOI
Holland J.D., Klaus A., Garratt A.N., Birchmeier W. Wnt Signaling in Stem and Cancer Stem Cells. Curr. Opin. Cell Biol. 2013;25:254–264. doi: 10.1016/j.ceb.2013.01.004. PubMed DOI
Nusse R., Clevers H. Wnt/β-Catenin Signaling, Disease, and Emerging Therapeutic Modalities. Cell. 2017;169:985–999. doi: 10.1016/j.cell.2017.05.016. PubMed DOI
van Amerongen R., Nusse R. Towards an Integrated View of Wnt Signaling in Development. Development. 2009;136:3205–3214. doi: 10.1242/dev.033910. PubMed DOI
Nelson W.J. Convergence of Wnt—Catenin, and Cadherin Pathways. Science. 2004;303:1483–1487. doi: 10.1126/science.1094291. PubMed DOI PMC
Wehrli M., Dougan S.T., Caldwell K., O’Keefe L., Schwartz S., Vaizel-Ohayon D., Schejter E., Tomlinson A., DiNardo S. Arrow Encodes an LDL-Receptor-Related Protein Essential for Wingless Signalling. Nature. 2000;407:527–530. doi: 10.1038/35035110. PubMed DOI
Tamai K., Semenov M., Kato Y., Spokony R., Liu C., Katsuyama Y., Hess F., Saint-Jeannet J.-P., He X. LDL-Receptor-Related Proteins in Wnt Signal Transduction. Nature. 2000;407:530–535. doi: 10.1038/35035117. PubMed DOI
Wang Y. The Role of Frizzled3 and Frizzled6 in Neural Tube Closure and in the Planar Polarity of Inner-Ear Sensory Hair Cells. J. Neurosci. 2006;26:2147–2156. doi: 10.1523/JNEUROSCI.4698-05.2005. PubMed DOI PMC
Gordon M.D., Nusse R. Wnt Signaling: Multiple Pathways, Multiple Receptors, and Multiple Transcription Factors. J. Biol. Chem. 2006;281:22429–22433. doi: 10.1074/jbc.R600015200. PubMed DOI
Kikuchi A., Yamamoto H., Kishida S. Multiplicity of the Interactions of Wnt Proteins and Their Receptors. Cell. Signal. 2007;19:659–671. doi: 10.1016/j.cellsig.2006.11.001. PubMed DOI
Hsieh J.-C., Kodjabachian L., Rebbert M.L., Rattner A., Smallwood P.M., Samos C.H., Nusse R., Dawid I.B., Nathans J. A New Secreted Protein That Binds to Wnt Proteins and Inhibits Their Activites. Nature. 1999;398:431–436. doi: 10.1038/18899. PubMed DOI
Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., Niehrs C. Dickkopf-1 Is a Member of a New Family of Secreted Proteins and Functions in Head Induction. Nature. 1998;391:357–362. doi: 10.1038/34848. PubMed DOI
Hoang B., Moos M., Vukicevic S., Luyten F.P. Primary Structure and Tissue Distribution of FRZB, a Novel Protein Related to Drosophila Frizzled, Suggest a Role in Skeletal Morphogenesis. J. Biol. Chem. 1996;271:26131–26137. doi: 10.1074/jbc.271.42.26131. PubMed DOI
Rattner A., Hsieh J.-C., Smallwood P.M., Gilbert D.J., Copeland N.G., Jenkins N.A., Nathans J. A Family of Secreted Proteins Contains Homology to the Cysteine-Rich Ligand-Binding Domain of Frizzled Receptors. Proc. Natl. Acad. Sci. USA. 1997;94:2859–2863. doi: 10.1073/pnas.94.7.2859. PubMed DOI PMC
de Lau W., Peng W.C., Gros P., Clevers H. The R-Spondin/Lgr5/Rnf43 Module: Regulator of Wnt Signal Strength. Genes Dev. 2014;28:305–316. doi: 10.1101/gad.235473.113. PubMed DOI PMC
Wilson S., Rydström A., Trimborn T., Willert K., Nusse R., Jessell T.M., Edlund T. The Status of Wnt Signalling Regulates Neural and Epidermal Fates in the Chick Embryo. Nature. 2001;411:325–330. doi: 10.1038/35077115. PubMed DOI
Wilson P.A., Hemmati-Brivanlou A. Induction of Epidermis and Inhibition of Neural Fate by Bmp-4. Nature. 1995;376:331–333. doi: 10.1038/376331a0. PubMed DOI
Fuchs E. Scratching the Surface of Skin Development. Nature. 2007;445:834–842. doi: 10.1038/nature05659. PubMed DOI PMC
Zhu X.-J., Liu Y., Dai Z.-M., Zhang X., Yang X., Li Y., Qiu M., Fu J., Hsu W., Chen Y., et al. BMP-FGF Signaling Axis Mediates Wnt-Induced Epidermal Stratification in Developing Mammalian Skin. PLoS Genet. 2014;10:e1004687. doi: 10.1371/journal.pgen.1004687. PubMed DOI PMC
Huelsken J., Vogel R., Erdmann B., Cotsarelis G., Birchmeier W. β-Catenin Controls Hair Follicle Morphogenesis and Stem Cell Differentiation in the Skin. Cell. 2001;105:533–545. doi: 10.1016/S0092-8674(01)00336-1. PubMed DOI
Niemann C., Owens D.M., Hülsken J., Birchmeier W., Watt F.M. Expression of DeltaNLef1 in Mouse Epidermis Results in Differentiation of Hair Follicles into Squamous Epidermal Cysts and Formation of Skin Tumours. Dev. Camb. Engl. 2002;129:95–109. PubMed
M’Boneko V., Merker H.-J. Development and Morphology of the Periderm of Mouse Embryos (Days 9–12 of Gestation) Cells Tissues Organs. 1988;133:325–336. doi: 10.1159/000146662. PubMed DOI
Popp T., Steinritz D., Breit A., Deppe J., Egea V., Schmidt A., Gudermann T., Weber C., Ries C. Wnt5a/β-Catenin Signaling Drives Calcium-Induced Differentiation of Human Primary Keratinocytes. J. Investig. Dermatol. 2014;134:2183–2191. doi: 10.1038/jid.2014.149. PubMed DOI
Schmidt-Ullrich R., Paus R. Molecular Principles of Hair Follicle Induction and Morphogenesis. BioEssays. 2005;27:247–261. doi: 10.1002/bies.20184. PubMed DOI
van der Veen C., Handjiski B., Paus R., Müller-Röver S., Maurer M., Eichmüller S., Ling G., Hofmann U., Foitzik K., Mecklenburg L. A Comprehensive Guide for the Recognition and Classification of Distinct Stages of Hair Follicle Morphogenesis. J. Investig. Dermatol. 1999;113:523–532. doi: 10.1046/j.1523-1747.1999.00740.x. PubMed DOI
Chen D., Jarrell A., Guo C., Lang R., Atit R. Dermal-Catenin Activity in Response to Epidermal Wnt Ligands Is Required for Fibroblast Proliferation and Hair Follicle Initiation. Development. 2012;139:1522–1533. doi: 10.1242/dev.076463. PubMed DOI PMC
Millar S.E. Molecular Mechanisms Regulating Hair Follicle Development. J. Investig. Dermatol. 2002;118:216–225. doi: 10.1046/j.0022-202x.2001.01670.x. PubMed DOI
Richardson R., Slanchev K., Kraus C., Knyphausen P., Eming S., Hammerschmidt M. Adult Zebrafish as a Model System for Cutaneous Wound-Healing Research. J. Investig. Dermatol. 2013;133:1655–1665. doi: 10.1038/jid.2013.16. PubMed DOI PMC
Seifert A.W., Monaghan J.R., Voss S.R., Maden M. Skin Regeneration in Adult Axolotls: A Blueprint for Scar-Free Healing in Vertebrates. PLoS ONE. 2012;7:e32875. doi: 10.1371/journal.pone.0032875. PubMed DOI PMC
Yokoyama H., Maruoka T., Aruga A., Amano T., Ohgo S., Shiroishi T., Tamura K. Prx-1 Expression in Xenopus Laevis Scarless Skin-Wound Healing and Its Resemblance to Epimorphic Regeneration. J. Investig. Dermatol. 2011;131:2477–2485. doi: 10.1038/jid.2011.223. PubMed DOI
Levy V., Lindon C., Zheng Y., Harfe B.D., Morgan B.A. Epidermal Stem Cells Arise from the Hair Follicle after Wounding. FASEB J. 2007;21:1358–1366. doi: 10.1096/fj.06-6926com. PubMed DOI
Ito M., Liu Y., Yang Z., Nguyen J., Liang F., Morris R.J., Cotsarelis G. Stem Cells in the Hair Follicle Bulge Contribute to Wound Repair but Not to Homeostasis of the Epidermis. Nat. Med. 2005;11:1351–1354. doi: 10.1038/nm1328. PubMed DOI
Levy V., Lindon C., Harfe B.D., Morgan B.A. Distinct Stem Cell Populations Regenerate the Follicle and Interfollicular Epidermis. Dev. Cell. 2005;9:855–861. doi: 10.1016/j.devcel.2005.11.003. PubMed DOI
Jensen K.B., Collins C.A., Nascimento E., Tan D.W., Frye M., Itami S., Watt F.M. Lrig1 Expression Defines a Distinct Multipotent Stem Cell Population in Mammalian Epidermis. Cell Stem Cell. 2009;4:427–439. doi: 10.1016/j.stem.2009.04.014. PubMed DOI PMC
Page M.E., Lombard P., Ng F., Göttgens B., Jensen K.B. The Epidermis Comprises Autonomous Compartments Maintained by Distinct Stem Cell Populations. Cell Stem Cell. 2013;13:471–482. doi: 10.1016/j.stem.2013.07.010. PubMed DOI PMC
Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., Barker N., van de Wetering M., van den Born M., Begthel H., Vries R.G., et al. Lgr6 Marks Stem Cells in the Hair Follicle That Generate All Cell Lineages of the Skin. Science. 2010;327:1385–1389. doi: 10.1126/science.1184733. PubMed DOI
Brownell I., Guevara E., Bai C.B., Loomis C.A., Joyner A.L. Nerve-Derived Sonic Hedgehog Defines a Niche for Hair Follicle Stem Cells Capable of Becoming Epidermal Stem Cells. Cell Stem Cell. 2011;8:552–565. doi: 10.1016/j.stem.2011.02.021. PubMed DOI PMC
Langton A.K., Herrick S.E., Headon D.J. An Extended Epidermal Response Heals Cutaneous Wounds in the Absence of a Hair Follicle Stem Cell Contribution. J. Investig. Dermatol. 2008;128:1311–1318. doi: 10.1038/sj.jid.5701178. PubMed DOI
Ansell D.M., Kloepper J.E., Thomason H.A., Paus R., Hardman M.J. Exploring the “Hair Growth—Wound Healing Connection”: Anagen Phase Promotes Wound Re-Epithelialization. J. Investig. Dermatol. 2011;131:518–528. doi: 10.1038/jid.2010.291. PubMed DOI
Mecklenburg L., Tobin D.J., Müller-Röver S., Handjiski B., Wendt G., Peters E.M.J., Pohl S., Moll I., Paus R. Active Hair Growth (Anagen) Is Associated with Angiogenesis. J. Investig. Dermatol. 2000;114:909–916. doi: 10.1046/j.1523-1747.2000.00954.x. PubMed DOI
Fujiwara H., Ferreira M., Donati G., Marciano D.K., Linton J.M., Sato Y., Hartner A., Sekiguchi K., Reichardt L.F., Watt F.M. The Basement Membrane of Hair Follicle Stem Cells Is a Muscle Cell Niche. Cell. 2011;144:577–589. doi: 10.1016/j.cell.2011.01.014. PubMed DOI PMC
Plikus M.V., Gay D.L., Treffeisen E., Wang A., Supapannachart R.J., Cotsarelis G. Epithelial Stem Cells and Implications for Wound Repair. Semin. Cell Dev. Biol. 2012;23:946–953. doi: 10.1016/j.semcdb.2012.10.001. PubMed DOI PMC
Chen Z., Wang Y., Shi C. Therapeutic Implications of Newly Identified Stem Cell Populations from the Skin Dermis. Cell Transplant. 2015;24:1405–1422. doi: 10.3727/096368914X682431. PubMed DOI
Shih D.T., Lee D.-C., Chen S.-C., Tsai R.-Y., Huang C.-T., Tsai C.-C., Shen E.-Y., Chiu W.-T. Isolation and Characterization of Neurogenic Mesenchymal Stem Cells in Human Scalp Tissue. Stem Cells. 2005;23:1012–1020. doi: 10.1634/stemcells.2004-0125. PubMed DOI
Young H.E., Steele T.A., Bray R.A., Hudson J., Floyd J.A., Hawkins K., Thomas K., Austin T., Edwards C., Cuzzourt J., et al. Human Reserve Pluripotent Mesenchymal Stem Cells Are Present in the Connective Tissues of Skeletal Muscle and Dermis Derived from Fetal, Adult, and Geriatric Donors. Anat. Rec. 2001;264:51–62. doi: 10.1002/ar.1128. PubMed DOI
Shi C.-M., Cheng T.-M., Su Y.-P., Mai Y., Qu J.-F., Ran X.-Z. Transplantation of Dermal Multipotent Cells Promotes the Hematopoietic Recovery in Sublethally Irradiated Rats. J. Radiat. Res. 2004;45:19–24. doi: 10.1269/jrr.45.19. PubMed DOI
Driskell R.R., Clavel C., Rendl M., Watt F.M. Hair Follicle Dermal Papilla Cells at a Glance. J. Cell Sci. 2011;124:1179–1182. doi: 10.1242/jcs.082446. PubMed DOI PMC
Biernaskie J., Paris M., Morozova O., Fagan B.M., Marra M., Pevny L., Miller F.D. SKPs Derive from Hair Follicle Precursors and Exhibit Properties of Adult Dermal Stem Cells. Cell Stem Cell. 2009;5:610–623. doi: 10.1016/j.stem.2009.10.019. PubMed DOI PMC
Driskell R.R., Lichtenberger B.M., Hoste E., Kretzschmar K., Simons B.D., Charalambous M., Ferron S.R., Herault Y., Pavlovic G., Ferguson-Smith A.C., et al. Distinct Fibroblast Lineages Determine Dermal Architecture in Skin Development and Repair. Nature. 2013;504:277–281. doi: 10.1038/nature12783. PubMed DOI PMC
Lichtenberger B.M., Mastrogiannaki M., Watt F.M. Epidermal β-Catenin Activation Remodels the Dermis via Paracrine Signalling to Distinct Fibroblast Lineages. Nat. Commun. 2016;7:10537. doi: 10.1038/ncomms10537. PubMed DOI PMC
Rinkevich Y., Walmsley G.G., Hu M.S., Maan Z.N., Newman A.M., Drukker M., Januszyk M., Krampitz G.W., Gurtner G.C., Lorenz H.P., et al. Identification and Isolation of a Dermal Lineage with Intrinsic Fibrogenic Potential. Science. 2015;348:aaa2151. doi: 10.1126/science.aaa2151. PubMed DOI PMC
Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound Repair and Regeneration. Nature. 2008;453:314–321. doi: 10.1038/nature07039. PubMed DOI
Wong V.W., Rustad K.C., Akaishi S., Sorkin M., Glotzbach J.P., Januszyk M., Nelson E.R., Levi K., Paterno J., Vial I.N., et al. Focal Adhesion Kinase Links Mechanical Force to Skin Fibrosis via Inflammatory Signaling. Nat. Med. 2012;18:148–152. doi: 10.1038/nm.2574. PubMed DOI PMC
Wynn T. Cellular and Molecular Mechanisms of Fibrosis. J. Pathol. 2008;214:199–210. doi: 10.1002/path.2277. PubMed DOI PMC
Larson B.J., Longaker M.T., Lorenz H.P. Scarless Fetal Wound Healing: A Basic Science Review. Plast. Reconstr. Surg. 2010;126:1172–1180. doi: 10.1097/PRS.0b013e3181eae781. PubMed DOI PMC
De Souza K.S., Cantaruti T.A., Azevedo G.M., de Galdino D.A.A., Rodrigues C.M., Costa R.A., Vaz N.M., Carvalho C.R. Improved Cutaneous Wound Healing after Intraperitoneal Injection of Alpha-Melanocyte-Stimulating Hormone. Exp. Dermatol. 2015;24:198–203. doi: 10.1111/exd.12609. PubMed DOI
Singla D.K., Singla R.D., Abdelli L.S., Glass C. Fibroblast Growth Factor-9 Enhances M2 Macrophage Differentiation and Attenuates Adverse Cardiac Remodeling in the Infarcted Diabetic Heart. PLoS ONE. 2015;10:e0120739. doi: 10.1371/journal.pone.0120739. PubMed DOI PMC
Gay D., Kwon O., Zhang Z., Spata M., Plikus M.V., Holler P.D., Ito M., Yang Z., Treffeisen E., Kim C.D., et al. Fgf9 from Dermal Γδ T Cells Induces Hair Follicle Neogenesis after Wounding. Nat. Med. 2013;19:916–923. doi: 10.1038/nm.3181. PubMed DOI PMC
Morris M.W., Allukian M., Herdrich B.J., Caskey R.C., Zgheib C., Xu J., Dorsett-Martin W., Mitchell M.E., Liechty K.W. Modulation of the Inflammatory Response by Increasing Fetal Wound Size or Interleukin-10 Overexpression Determines Wound Phenotype and Scar Formation: Modulation of Inflammation and Fetal Healing. Wound Repair Regen. 2014;22:406–414. doi: 10.1111/wrr.12180. PubMed DOI
Ding J., Ma Z., Liu H., Kwan P., Iwashina T., Shankowsky H.A., Wong D., Tredget E.E. The Therapeutic Potential of a C-X-C Chemokine Receptor Type 4 (CXCR-4) Antagonist on Hypertrophic Scarring in Vivo: CXCR4 Antagonist Minimizes Scar Formation. Wound Repair Regen. 2014;22:622–630. doi: 10.1111/wrr.12208. PubMed DOI
Dulauroy S., Di Carlo S.E., Langa F., Eberl G., Peduto L. Lineage Tracing and Genetic Ablation of ADAM12+ Perivascular Cells Identify a Major Source of Profibrotic Cells during Acute Tissue Injury. Nat. Med. 2012;18:1262–1270. doi: 10.1038/nm.2848. PubMed DOI
Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.-L., Gabbiani G. The Myofibroblast. Am. J. Pathol. 2007;170:1807–1816. doi: 10.2353/ajpath.2007.070112. PubMed DOI PMC
Schmidt B.A., Horsley V. Intradermal Adipocytes Mediate Fibroblast Recruitment during Skin Wound Healing. Development. 2013;140:1517–1527. doi: 10.1242/dev.087593. PubMed DOI PMC
Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F., Mancardi G.L., Pistoia V., et al. Human Mesenchymal Stem Cells Modulate B-Cell Functions. Blood. 2006;107:367–372. doi: 10.1182/blood-2005-07-2657. PubMed DOI
Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., Grisanti S., Gianni A.M. Human Bone Marrow Stromal Cells Suppress T-Lymphocyte Proliferation Induced by Cellular or Nonspecific Mitogenic Stimuli. Blood. 2002;99:3838–3843. doi: 10.1182/blood.V99.10.3838. PubMed DOI
Loots M.A.M., Lamme E.N., Zeegelaar J., Mekkes J.R., Bos J.D., Middelkoop E. Differences in Cellular Infiltrate and Extracellular Matrix of Chronic Diabetic and Venous Ulcers Versus Acute Wounds. J. Investig. Dermatol. 1998;111:850–857. doi: 10.1046/j.1523-1747.1998.00381.x. PubMed DOI
Nuschke A. Activity of Mesenchymal Stem Cells in Therapies for Chronic Skin Wound Healing. Organogenesis. 2014;10:29–37. doi: 10.4161/org.27405. PubMed DOI PMC
Li M., Luan F., Zhao Y., Hao H., Liu J., Dong L., Fu X., Han W. Mesenchymal Stem Cell-Conditioned Medium Accelerates Wound Healing with Fewer Scars: Mesenchymal Stem Cell-Conditioned Medium Enhance Wound Scarless Healing. Int. Wound J. 2017;14:64–73. doi: 10.1111/iwj.12551. PubMed DOI PMC
Cheon S.S., Cheah A.Y.L., Turley S., Nadesan P., Poon R., Clevers H., Alman B.A. β-Catenin Stabilization Dysregulates Mesenchymal Cell Proliferation, Motility, and Invasiveness and Causes Aggressive Fibromatosis and Hyperplastic Cutaneous Wounds. Proc. Natl. Acad. Sci. USA. 2002;99:6973–6978. doi: 10.1073/pnas.102657399. PubMed DOI PMC
Sato M. Upregulation of the Wnt/beta-Catenin Pathway Induced by Transforming Growth Factor-beta In Hypertrophic Scars and Keloids. Acta Derm. Venereol. 2006;86:300–307. doi: 10.2340/00015555-0101. PubMed DOI
Lee W.J., Park J.H., Shin J.U., Noh H., Lew D.H., Yang W.I., Yun C.O., Lee K.H., Lee J.H. Endothelial-to-Mesenchymal Transition Induced by Wnt 3a in Keloid Pathogenesis: EndoMT in Keloids and Dermal Microvascular Endothelial Cells. Wound Repair Regen. 2015;23:435–442. doi: 10.1111/wrr.12300. PubMed DOI
Cheon S.S., Wei Q., Gurung A., Youn A., Bright T., Poon R., Whetstone H., Guha A., Alman B.A. Beta-catenin Regulates Wound Size and Mediates the Effect of TGF-beta in Cutaneous Healing. FASEB J. 2006;20:692–701. doi: 10.1096/fj.05-4759com. PubMed DOI
Akhmetshina A., Palumbo K., Dees C., Bergmann C., Venalis P., Zerr P., Horn A., Kireva T., Beyer C., Zwerina J., et al. Activation of Canonical Wnt Signalling Is Required for TGF-β-Mediated Fibrosis. Nat. Commun. 2012;3:735. doi: 10.1038/ncomms1734. PubMed DOI PMC
Bastakoty D., Saraswati S., Cates J., Lee E., Nanney L.B., Young P.P. Inhibition of Wnt/β-catenin Pathway Promotes Regenerative Repair of Cutaneous and Cartilage Injury. FASEB J. 2015;29:4881–4892. doi: 10.1096/fj.15-275941. PubMed DOI PMC
Lee S.-H., Kim M.-Y., Kim H.-Y., Lee Y.-M., Kim H., Nam K.A., Roh M.R., Min D.S., Chung K.Y., Choi K.-Y. The Dishevelled-Binding Protein CXXC5 Negatively Regulates Cutaneous Wound Healing. J. Exp. Med. 2015;212:1061–1080. doi: 10.1084/jem.20141601. PubMed DOI PMC
Driskell R.R., Watt F.M. Understanding Fibroblast Heterogeneity in the Skin. Trends Cell Biol. 2015;25:92–99. doi: 10.1016/j.tcb.2014.10.001. PubMed DOI
Cho H., Blatchley M.R., Duh E.J., Gerecht S. Acellular and Cellular Approaches to Improve Diabetic Wound Healing. Adv. Drug Deliv. Rev. 2019;146:267–288. doi: 10.1016/j.addr.2018.07.019. PubMed DOI
Kanji S., Das H. Advances of Stem Cell Therapeutics in Cutaneous Wound Healing and Regeneration. Mediat. Inflamm. 2017;2017:5217967. doi: 10.1155/2017/5217967. PubMed DOI PMC
Stojadinovic O., Pastar I., Nusbaum A.G., Vukelic S., Krzyzanowska A., Tomic-Canic M. Deregulation of Epidermal Stem Cell Niche Contributes to Pathogenesis of Nonhealing Venous Ulcers: Epidermal Stem Cells in Venous Ulcers. Wound Repair Regen. 2014;22:220–227. doi: 10.1111/wrr.12142. PubMed DOI PMC
Hoffmeyer K., Raggioli A., Rudloff S., Anton R., Hierholzer A., Del Valle I., Hein K., Vogt R., Kemler R. Wnt/β Catenin Signaling Regulates Telomerase in Stem Cells and Cancer Cells. Science. 2012;336:1549–1554. doi: 10.1126/science.1218370. PubMed DOI
Liu H., Liu Q., Ge Y., Zhao Q., Zheng X., Zhao Y. HTERT Promotes Cell Adhesion and Migration Independent of Telomerase Activity. Sci. Rep. 2016;6:22886. doi: 10.1038/srep22886. PubMed DOI PMC
Liu Q., Sun Y., Lv Y., Le Z., Xin Y., Zhang P., Liu Y. TERT Alleviates Irradiation-Induced Late Rectal Injury by Reducing Hypoxia-Induced ROS Levels through the Activation of NF-ΚB and Autophagy. Int. J. Mol. Med. 2016;38:785–793. doi: 10.3892/ijmm.2016.2673. PubMed DOI PMC
Cao Y., Xu L., Yang X., Dong Y., Luo H., Xing F., Ge Q. The Potential Role of Cycloastragenol in Promoting Diabetic Wound Repair In Vitro. BioMed Res. Int. 2019;2019:7023950. doi: 10.1155/2019/7023950. PubMed DOI PMC
Zhang H., Nie X., Shi X., Zhao J., Chen Y., Yao Q., Sun C., Yang J. Regulatory Mechanisms of the Wnt/β-Catenin Pathway in Diabetic Cutaneous Ulcers. Front. Pharmacol. 2018;9:1114. doi: 10.3389/fphar.2018.01114. PubMed DOI PMC
Gelse K. Collagens—Structure, Function, and Biosynthesis. Adv. Drug Deliv. Rev. 2003;55:1531–1546. doi: 10.1016/j.addr.2003.08.002. PubMed DOI
Eckes B., Zigrino P., Kessler D., Holtkötter O., Shephard P., Mauch C., Krieg T. Fibroblast-Matrix Interactions in Wound Healing and Fibrosis. Matrix Biol. 2000;19:325–332. doi: 10.1016/S0945-053X(00)00077-9. PubMed DOI
Young A., McNaught C.-E. The Physiology of Wound Healing. Surg. Oxf. 2011;29:475–479. doi: 10.1016/j.mpsur.2011.06.011. DOI
Rodrigues M., Kosaric N., Bonham C.A., Gurtner G.C. Wound Healing: A Cellular Perspective. Physiol. Rev. 2019;99:665–706. doi: 10.1152/physrev.00067.2017. PubMed DOI PMC
Brem H., Tomic-Canic M. Cellular and Molecular Basis of Wound Healing in Diabetes. J. Clin. Investig. 2007;117:1219–1222. doi: 10.1172/JCI32169. PubMed DOI PMC
Gadelkarim M., Abushouk A.I., Ghanem E., Hamaad A.M., Saad A.M., Abdel-Daim M.M. Adipose-Derived Stem Cells: Effectiveness and Advances in Delivery in Diabetic Wound Healing. Biomed. Pharmacother. 2018;107:625–633. doi: 10.1016/j.biopha.2018.08.013. PubMed DOI
Hou C., Shen L., Huang Q., Mi J., Wu Y., Yang M., Zeng W., Li L., Chen W., Zhu C. The Effect of Heme Oxygenase-1 Complexed with Collagen on MSC Performance in the Treatment of Diabetic Ischemic Ulcer. Biomaterials. 2013;34:112–120. doi: 10.1016/j.biomaterials.2012.09.022. PubMed DOI
O’Loughlin A., Kulkarni M., Creane M., Vaughan E.E., Mooney E., Shaw G., Murphy M., Dockery P., Pandit A., O’Brien T. Topical Administration of Allogeneic Mesenchymal Stromal Cells Seeded in a Collagen Scaffold Augments Wound Healing and Increases Angiogenesis in the Diabetic Rabbit Ulcer. Diabetes. 2013;62:2588–2594. doi: 10.2337/db12-1822. PubMed DOI PMC
Uccelli A., Moretta L., Pistoia V. Mesenchymal Stem Cells in Health and Disease. Nat. Rev. Immunol. 2008;8:726–736. doi: 10.1038/nri2395. PubMed DOI
Pellegrini G., Ranno R., Stracuzzi G., Bondanza S., Guerra L., Zambruno G., Micali G., De Luca M. The control of epidermal stem cells (holoclones) in the treatment of massive full-thickness burns with autologous keratinocytes cultured on fibrin1. Transplantation. 1999;68:868–879. doi: 10.1097/00007890-199909270-00021. PubMed DOI
Walmsley G.G., Maan Z.N., Wong V.W., Duscher D., Hu M.S., Zielins E.R., Wearda T., Muhonen E., McArdle A., Tevlin R., et al. Scarless Wound Healing: Chasing the Holy Grail. Plast. Reconstr. Surg. 2015;135:907–917. doi: 10.1097/PRS.0000000000000972. PubMed DOI
De Luca M., Pellegrini G., Green H. Regeneration of Squamous Epithelia from Stem Cells of Cultured Grafts. Regen. Med. 2006;1:45–57. doi: 10.2217/17460751.1.1.45. PubMed DOI
Carsin H., Ainaud P., Le Bever H., Rives J.-M., Lakhel A., Stephanazzi J., Lambert F., Perrot J. Cultured Epithelial Autografts in Extensive Burn Coverage of Severely Traumatized Patients: A Five Year Single-Center Experience with 30 Patients. Burns. 2000;26:379–387. doi: 10.1016/S0305-4179(99)00143-6. PubMed DOI
Gallico G.G., O’Connor N.E., Compton C.C., Kehinde O., Green H. Permanent Coverage of Large Burn Wounds with Autologous Cultured Human Epithelium. N. Engl. J. Med. 1984;311:448–451. doi: 10.1056/NEJM198408163110706. PubMed DOI
Jang H., Kim Y.H., Kim M.K., Lee K.H., Jeon S. Wound-Healing Potential of Cultured Epidermal Sheets Is Unaltered after Lyophilization: A Preclinical Study in Comparison to Cryopreserved CES. BioMed Res. Int. 2013;2013:907209. doi: 10.1155/2013/907209. PubMed DOI PMC
Jackson C.J., Tønseth K.A., Utheim T.P. Cultured Epidermal Stem Cells in Regenerative Medicine. Stem Cell Res. Ther. 2017;8:155. doi: 10.1186/s13287-017-0587-1. PubMed DOI PMC
Lootens L., Brusselaers N., Beele H., Monstrey S. Keratinocytes in the Treatment of Severe Burn Injury: An Update. Int. Wound J. 2013;10:6–12. doi: 10.1111/j.1742-481X.2012.01083.x. PubMed DOI PMC
Wurzer P., Keil H., Branski L.K., Parvizi D., Clayton R.P., Finnerty C.C., Herndon D.N., Kamolz L.P. The Use of Skin Substitutes and Burn Care—A Survey. J. Surg. Res. 2016;201:293–298. doi: 10.1016/j.jss.2015.10.048. PubMed DOI
Nicholas M.N., Yeung J. Current Status and Future of Skin Substitutes for Chronic Wound Healing. J. Cutan. Med. Surg. 2017;21:23–30. doi: 10.1177/1203475416664037. PubMed DOI
Varkey M., Ding J., Tredget E.E. Fibrotic Remodeling of Tissue-Engineered Skin with Deep Dermal Fibroblasts Is Reduced by Keratinocytes. Tissue Eng. Part A. 2014;20:716–727. doi: 10.1089/ten.tea.2013.0434. PubMed DOI
Ilic D., Polak J.M. Stem Cells in Regenerative Medicine: Introduction. Br. Med. Bull. 2011;98:117–126. doi: 10.1093/bmb/ldr012. PubMed DOI
Ma S., Xie N., Li W., Yuan B., Shi Y., Wang Y. Immunobiology of Mesenchymal Stem Cells. Cell Death Differ. 2014;21:216–225. doi: 10.1038/cdd.2013.158. PubMed DOI PMC
Lee E.Y., Xia Y., Kim W.-S., Kim M.H., Kim T.H., Kim K.J., Park B.-S., Sung J.-H. Hypoxia-Enhanced Wound-Healing Function of Adipose-Derived Stem Cells: Increase in Stem Cell Proliferation and up-Regulation of VEGF and BFGF. Wound Repair Regen. 2009;17:540–547. doi: 10.1111/j.1524-475X.2009.00499.x. PubMed DOI
Liang X., Ding Y., Zhang Y., Tse H.-F., Lian Q. Paracrine Mechanisms of Mesenchymal Stem Cell-Based Therapy: Current Status and Perspectives. Cell Transplant. 2014;23:1045–1059. doi: 10.3727/096368913X667709. PubMed DOI
Joseph A., Baiju I., Bhat I.A., Pandey S., Bharti M., Verma M., Pratap Singh A., Ansari M.M., Chandra V., Saikumar G., et al. Mesenchymal Stem Cell-conditioned Media: A Novel Alternative of Stem Cell Therapy for Quality Wound Healing. J. Cell. Physiol. 2020;235:5555–5569. doi: 10.1002/jcp.29486. PubMed DOI
Hocking A.M., Gibran N.S. Mesenchymal Stem Cells: Paracrine Signaling and Differentiation during Cutaneous Wound Repair. Exp. Cell Res. 2010;316:2213–2219. doi: 10.1016/j.yexcr.2010.05.009. PubMed DOI PMC
Oliver R.F. Whisker Growth after Removal of the Dermal Papilla and Lengths of Follicle in the Hooded Rat. J. Embryol. Exp. Morphol. 1966;15:331–347. PubMed
Toma J.G., McKenzie I.A., Bagli D., Miller F.D. Isolation and Characterization of Multipotent Skin-Derived Precursors from Human Skin. Stem Cells. 2005;23:727–737. doi: 10.1634/stemcells.2004-0134. PubMed DOI
Fathke C. Contribution of Bone Marrow-Derived Cells to Skin: Collagen Deposition and Wound Repair. Stem Cells. 2004;22:812–822. doi: 10.1634/stemcells.22-5-812. PubMed DOI PMC
Opalenik S.R., Davidson J.M. Fibroblast Differentiation of Bone Marrow-derived Cells during Wound Repair. FASEB J. 2005;19:1561–1563. doi: 10.1096/fj.04-2978fje. PubMed DOI
Seppanen E., Roy E., Ellis R., Bou-Gharios G., Fisk N.M., Khosrotehrani K. Distant Mesenchymal Progenitors Contribute to Skin Wound Healing and Produce Collagen: Evidence from a Murine Fetal Microchimerism Model. PLoS ONE. 2013;8:e62662. doi: 10.1371/journal.pone.0062662. PubMed DOI PMC
Wang Y., Sun Y., Yang X.-Y., Ji S.-Z., Han S., Xia Z.-F. Mobilised Bone Marrow-Derived Cells Accelerate Wound Healing. Int. Wound J. 2013;10:473–479. doi: 10.1111/j.1742-481X.2012.01007.x. PubMed DOI PMC
Badiavas E.V. Treatment of Chronic Wounds with Bone Marrow–Derived Cells. Arch. Dermatol. 2003;139:510. doi: 10.1001/archderm.139.4.510. PubMed DOI
Falanga V., Iwamoto S., Chartier M., Yufit T., Butmarc J., Kouttab N., Shrayer D., Carson P. Autologous Bone Marrow–Derived Cultured Mesenchymal Stem Cells Delivered in a Fibrin Spray Accelerate Healing in Murine and Human Cutaneous Wounds. Tissue Eng. 2007;13:1299–1312. doi: 10.1089/ten.2006.0278. PubMed DOI
McFarlin K., Gao X., Liu Y.B., Dulchavsky D.S., Kwon D., Arbab A.S., Bansal M., Li Y., Chopp M., Dulchavsky S.A., et al. Bone Marrow-Derived Mesenchymal Stromal Cells Accelerate Wound Healing in the Rat. Wound Repair Regen. 2006;14:471–478. doi: 10.1111/j.1743-6109.2006.00153.x. PubMed DOI
Stoff A., Rivera A.A., Sanjib Banerjee N., Moore S.T., Michael Numnum T., Espinosa-de-los-Monteros A., Richter D.F., Siegal G.P., Chow L.T., Feldman D., et al. Promotion of Incisional Wound Repair by Human Mesenchymal Stem Cell Transplantation. Exp. Dermatol. 2009;18:362–369. doi: 10.1111/j.1600-0625.2008.00792.x. PubMed DOI PMC
Uysal C.A., Tobita M., Hyakusoku H., Mizuno H. The Effect of Bone-Marrow-Derived Stem Cells and Adipose-Derived Stem Cells on Wound Contraction and Epithelization. Adv. Wound Care. 2014;3:405–413. doi: 10.1089/wound.2014.0539. PubMed DOI PMC
Kwon D.S., Gao X., Liu Y.B., Dulchavsky D.S., Danyluk A.L., Bansal M., Chopp M., McIntosh K., Arbab A.S., Dulchavsky S.A., et al. Treatment with Bone Marrow-Derived Stromal Cells Accelerates Wound Healing in Diabetic Rats. Int. Wound J. 2008;5:453–463. doi: 10.1111/j.1742-481X.2007.00408.x. PubMed DOI PMC
Villalta S.A., Rinaldi C., Deng B., Liu G., Fedor B., Tidball J.G. Interleukin-10 Reduces the Pathology of Mdx Muscular Dystrophy by Deactivating M1 Macrophages and Modulating Macrophage Phenotype. Hum. Mol. Genet. 2011;20:790–805. doi: 10.1093/hmg/ddq523. PubMed DOI PMC
Ono I., Yamashita T., Hida T., Jin H.-Y., Ito Y., Hamada H., Akasaka Y., Ishii T., Jimbow K. Combined Administration of Basic Fibroblast Growth Factor Protein and the Hepatocyte Growth Factor Gene Enhances the Regeneration of Dermis in Acute Incisional Wounds: Wound Repair and Regeneration. Wound Repair Regen. 2004;12:67–79. doi: 10.1111/j.1067-1927.2004.012113.x-1. PubMed DOI
Booth A.M., Fang Y., Fallon J.K., Yang J.-M., Hildreth J.E.K., Gould S.J. Exosomes and HIV Gag Bud from Endosome-like Domains of the T Cell Plasma Membrane. J. Cell Biol. 2006;172:923–935. doi: 10.1083/jcb.200508014. PubMed DOI PMC
Simons M., Raposo G. Exosomes—Vesicular Carriers for Intercellular Communication. Curr. Opin. Cell Biol. 2009;21:575–581. doi: 10.1016/j.ceb.2009.03.007. PubMed DOI
Lai R.C., Yeo R.W.Y., Lim S.K. Mesenchymal Stem Cell Exosomes. Semin. Cell Dev. Biol. 2015;40:82–88. doi: 10.1016/j.semcdb.2015.03.001. PubMed DOI
Lu K., Li H., Yang K., Wu J., Cai X., Zhou Y., Li C. Exosomes as Potential Alternatives to Stem Cell Therapy for Intervertebral Disc Degeneration: In-Vitro Study on Exosomes in Interaction of Nucleus Pulposus Cells and Bone Marrow Mesenchymal Stem Cells. Stem Cell Res. Ther. 2017;8:108. doi: 10.1186/s13287-017-0563-9. PubMed DOI PMC
Lo Sicco C., Reverberi D., Balbi C., Ulivi V., Principi E., Pascucci L., Becherini P., Bosco M.C., Varesio L., Franzin C., et al. Mesenchymal Stem Cell-Derived Extracellular Vesicles as Mediators of Anti-Inflammatory Effects: Endorsement of Macrophage Polarization: MSC-Derived EVs Promote Macrophage Polarization. Stem Cells Transl. Med. 2017;6:1018–1028. doi: 10.1002/sctm.16-0363. PubMed DOI PMC
Monguió-Tortajada M., Roura S., Gálvez-Montón C., Pujal J.M., Aran G., Sanjurjo L., Franquesa M., Sarrias M.-R., Bayes-Genis A., Borràs F.E. Nanosized UCMSC-Derived Extracellular Vesicles but Not Conditioned Medium Exclusively Inhibit the Inflammatory Response of Stimulated T Cells: Implications for Nanomedicine. Theranostics. 2017;7:270–284. doi: 10.7150/thno.16154. PubMed DOI PMC
Nosbaum A., Prevel N., Truong H.-A., Mehta P., Ettinger M., Scharschmidt T.C., Ali N.H., Pauli M.L., Abbas A.K., Rosenblum M.D. Cutting Edge: Regulatory T Cells Facilitate Cutaneous Wound Healing. J. Immunol. 2016;196:2010–2014. doi: 10.4049/jimmunol.1502139. PubMed DOI PMC
Li X., Jiang C., Zhao J. Human Endothelial Progenitor Cells-Derived Exosomes Accelerate Cutaneous Wound Healing in Diabetic Rats by Promoting Endothelial Function. J. Diabetes Complicat. 2016;30:986–992. doi: 10.1016/j.jdiacomp.2016.05.009. PubMed DOI
Liu Y., Min D., Bolton T., Nube V., Twigg S.M., Yue D.K., McLennan S.V. Increased Matrix Metalloproteinase-9 Predicts Poor Wound Healing in Diabetic Foot Ulcers. Diabetes Care. 2009;32:117–119. doi: 10.2337/dc08-0763. PubMed DOI PMC
Gospodarowicz D. Biological Activities of Fibroblast Growth Factors. Ann. N. Y. Acad. Sci. 1991;638:1–8. doi: 10.1111/j.1749-6632.1991.tb49012.x. PubMed DOI
Guo S., DiPietro L.A. Factors Affecting Wound Healing. J. Dent. Res. 2010;89:219–229. doi: 10.1177/0022034509359125. PubMed DOI PMC
Geiger A., Walker A., Nissen E. Human Fibrocyte-Derived Exosomes Accelerate Wound Healing in Genetically Diabetic Mice. Biochem. Biophys. Res. Commun. 2015;467:303–309. doi: 10.1016/j.bbrc.2015.09.166. PubMed DOI
Zhang J., Guan J., Niu X., Hu G., Guo S., Li Q., Xie Z., Zhang C., Wang Y. Exosomes Released from Human Induced Pluripotent Stem Cells-Derived MSCs Facilitate Cutaneous Wound Healing by Promoting Collagen Synthesis and Angiogenesis. J. Transl. Med. 2015;13:49. doi: 10.1186/s12967-015-0417-0. PubMed DOI PMC
Bekeschus S., von Woedtke T., Emmert S., Schmidt A. Medical Gas Plasma-Stimulated Wound Healing: Evidence and Mechanisms. Redox Biol. 2021;46:102116. doi: 10.1016/j.redox.2021.102116. PubMed DOI PMC
Erel-Akbaba G., Akbaba H. Investigation of the Potential Therapeutic Effect of Cationic Lipoplex Mediated Fibroblast Growth Factor-2 Encoding Plasmid DNA Delivery on Wound Healing. DARU J. Pharm. Sci. 2021:1–12. doi: 10.1007/s40199-021-00410-y. PubMed DOI PMC
Branski L.K., Pereira C.T., Herndon D.N., Jeschke M.G. Gene Therapy in Wound Healing: Present Status and Future Directions. Gene Ther. 2007;14:1–10. doi: 10.1038/sj.gt.3302837. PubMed DOI
Rasouli M., Rahimi A., Soleimani M., Keshel S.H. The Interplay between Extracellular Matrix and Progenitor/Stem Cells during Wound Healing: Opportunities and Future Directions. Acta Histochem. 2021;123:151785. doi: 10.1016/j.acthis.2021.151785. PubMed DOI