Comparative Proteomic Analysis in Scar-Free Skin Regeneration in Acomys cahirinus and Scarring Mus musculus.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
13 01 2020
Historique:
received: 18 03 2019
accepted: 11 12 2019
entrez: 15 1 2020
pubmed: 15 1 2020
medline: 13 11 2020
Statut: epublish

Résumé

The spiny mouse, Acomys cahirinus displays a unique wound healing ability with regeneration of all skin components in a scar-free manner. To identify orchestrators of this regenerative response we have performed proteomic analyses of skin from Acomys and Mus musculus before and after wounding. Of the ~2000 proteins identified many are expressed at similar levels in Acomys and Mus, but there are significant differences. Following wounding in Mus the complement and coagulation cascades, PPAR signaling pathway and ECM-receptor interactions predominate. In Acomys, other pathways predominate including the Wnt, MAPK, the ribosome, proteasome, endocytosis and tight junction pathways. Notable among Acomys specific proteins are several ubiquitin-associated enzymes and kinases, whereas in Mus immuno-modulation proteins characteristic of inflammatory response are unique or more prominent. ECM proteins such as collagens are more highly expressed in Mus, but likely more important is the higher expression of matrix remodeling proteases in Acomys. Another distinctive difference between Acomys and Mus lies in the macrophage-produced arginase 1 is found in Mus whereas arginase 2 is found in Acomys. Thus, we have identified several avenues for experimental approaches whose aim is to reduce the fibrotic response that the typical mammal displays in response to wounding.

Identifiants

pubmed: 31932597
doi: 10.1038/s41598-019-56823-y
pii: 10.1038/s41598-019-56823-y
pmc: PMC6957500
doi:

Substances chimiques

Proteome 0

Types de publication

Comparative Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

166

Commentaires et corrections

Type : ErratumIn

Références

Clark, R. A. F. & Henson, P. M. The molecular and cellular biology of wound repair. xxii, 597 (Plenum, 1988).
Seifert, A. W. & Maden, M. New insights into vertebrate skin regeneration. Rev. Cell Int. Mol. Biol. 310, 129–1699 (2014).
doi: 10.1016/B978-0-12-800180-6.00004-9
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 7, e32875 (2012).
pubmed: 22485136 pmcid: 3317654 doi: 10.1371/journal.pone.0032875
Levesque, M., Villard, E. & Roy, S. Skin wound healing in axolotls: a scarless process. J. Exp. Zool. Part. B, Mol. Dev. Evol. 314, 684–697 (2010).
doi: 10.1002/jez.b.21371
Larson, B. J., Longaker, M. T. & Lorenz, H. P. Scarless fetal wound healing: a basic science review. Plast. Reconstr. Surg. 126, 1172–1180 (2010).
pubmed: 20885241 pmcid: 4229131 doi: 10.1097/PRS.0b013e3181eae781
Lo, D. D., Zimmermann, A. S., Nauta, A., Longaker, M. T. & Lorenz, H. P. Scarless fetal skin wound healing update. Birth Defects Res. Part C. Embryo Today: Rev. 96, 237–247 (2012).
Satish, L., & Kathju, S. Cellular and molecular characteristics of scarless versus fibrotic wound healing. Derm. Res. Practice. 790234 (2010).
Olutoye, O. O., Barone, E. J., Yager, D. R., Cohen, I. K. & Diegelmann, R. F. Collagen induces cytokine release by fetal platelets: implications in scarless healing. J. Pedia. Surg. 32, 827–30 (1997).
doi: 10.1016/S0022-3468(97)90629-1
Sullivan, K. M., Lorenz, H. P., Meuli, M., Lin, R. Y. & Adzick, N. S. A model of scarless human fetal wound repair is deficient in transforming growth factor beta. J. Pedia. Surg. 30, 198–202 (1995).
doi: 10.1016/0022-3468(95)90560-X
Vorontsova, M. A. & Liosner, L. D. Asexual Propagation and Regeneration (Pergamon 1960).
Seifert, A. W. et al. Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489, 561–565 (2012).
pubmed: 23018966 pmcid: 3480082 doi: 10.1038/nature11499
Clark, L. D., Clark, R. K. & Heber-Katz, E. A new murine model for mammalian wound repair and regeneration. Clin. Immunol. Immunopathol. 88, 35–45 (1998).
pubmed: 9683548 doi: 10.1006/clin.1998.4519
Nelson, A. M. et al. Prostaglandin D2 Inhibits Wound-Induced Hair Follicle Neogenesis through the Receptor, Gpr44. J. Invest. Dermatol. 133, 881 (2013).
pubmed: 23190891 doi: 10.1038/jid.2012.398
Gawriluk, T. R. et al. Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals. Nat. Commun. 7, 11164 (2016).
pubmed: 27109826 pmcid: 4848467 doi: 10.1038/ncomms11164
Santos, D. M. et al. Ear wound regeneration in the african spiny mouse Acomys cahirinus. Regeneration. 3, 52–61 (2016).
doi: 10.1002/reg2.50
Maden., M. Optimal skin regeneration after full thickness thermal burn injury in the spiny mouse, Acomys cahirinus. Burns. 44, 1509–1520 (2018).
pubmed: 29903601 doi: 10.1016/j.burns.2018.05.018
Brant, J. O., Lopez, M.-C., Baker, H. V., Barbazuk, W. B. & Maden, M. A., Comparative analysis of gene expression profiles during skin regeneration in Mus and Acomys. PLoS One. 10, e0142931 (2015).
pubmed: 26606282 pmcid: 4659537 doi: 10.1371/journal.pone.0142931
Brant, J. O., Yoon, J. H., Polvadore, T., Barbazuk, W. B. & Maden, M. Cellular events during scar-free skin regeneration in the spiny mouse, Acomys. Wound. Repair. Regen. 24, 75–88 (2016).
pubmed: 26606280 doi: 10.1111/wrr.12385
Simkin, J., Gawriluk, T. R., Gensel, J. C. & Seifert, A. W. Macrophages are necessary for epimorphic regeneration in African spiny mice. eLife. 6, e24623 (2017).
pubmed: 28508748 pmcid: 5433844 doi: 10.7554/eLife.24623
Brant, J. O. et al. Comparative transcriptomic analysis of dermal wound healing reveals de nove skeletal muscle regeneration in Acomys cahirinus. PLoS One. 14(5), e0216228 (2019).
pubmed: 31141508 pmcid: 6541261 doi: 10.1371/journal.pone.0216228
Bachofner, M. et al. Large-scale quantitative proteomics identifies the ubiquitin ligase Nedd4-1 as an essential regulator of liver regeneration. Dev. Cell. 42, 616–625 (2017).
pubmed: 28890072 doi: 10.1016/j.devcel.2017.07.025
Hsu, Y. C., Li, L. & Fuchs, E. Emerging interactions between skin stem cells and their niches. Nat. Med. 20, 847–856 (2014).
pubmed: 25100530 pmcid: 4358898 doi: 10.1038/nm.3643
Fuchs, E. Scratching the surface of skin development. Nature 445, 834–842 (2007).
pubmed: 17314969 pmcid: 2405926 doi: 10.1038/nature05659
Myung, P. S., Takeo, M., Ito, M. & Atit, R. P. Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. J. Invest. Dermatol. 133, 31–41 (2013).
pubmed: 22810306 doi: 10.1038/jid.2012.230
Okuse, T., Chiba, T., Katsumi, I. & Imai, K. Differential expression and localization of WNTs in an animal model of skin wound healing. Wound. Repair. Regen. 13, 491–497 (2005).
pubmed: 16176457 doi: 10.1111/j.1067-1927.2005.00069.x
Ito, M. et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316–320 (2007).
pubmed: 17507982 doi: 10.1038/nature05766
Stewart, D. C. et al. Unique behavior of dermal cells from regenerative mammal, the African spiny Mouse, in response to substrate stiffness. J. Biomech. 81, 149–154 (2018).
pubmed: 30361050 doi: 10.1016/j.jbiomech.2018.10.005
Kim, S., Wong, P. & Coulombe, P. A. Keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 441, 362–365 (2006).
pubmed: 16710422 doi: 10.1038/nature04659
Staley, J. P. & Woolford, J. J. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr. Opin. Cell Biol. 21, 109–118 (2009).
pubmed: 19167202 pmcid: 2698946 doi: 10.1016/j.ceb.2009.01.003
Gu, L. H. & Coulombe, P. A. Keratin function in skin epithelia: a broadening palette with surprising shades. Curr. Opin. Cell Biol. 19, 13–23 (2006).
pubmed: 17178453 doi: 10.1016/j.ceb.2006.12.007
Gawronska-Kozak, B. & Bukowska, J. Animal models of skin regeneration in animal models for the study of human disease (2nd edition), 343–356 (2017).
Maden, M. et al. Perfect chronic skeletal muscle regeneration in adult spiny mice, Acomys cahirinus. Sci. Rep. 8, 8920 (2018).
pubmed: 29892004 pmcid: 5995887 doi: 10.1038/s41598-018-27178-7
Okamura, D. M. et al. Scarless repair of acute and chronic kidney injury in African Spiny mice (Acomys cahirinus). bioRxiv 315069 (2018).
Yang, Z. & Ming, X. F. Functions of arginase isoforms in macrophage inflammatory responses: impact on cardiovascular diseases and metabolic disorders. Front. Immunol., https://doi.org/10.3389/fimmu.2014.00533 (2014).
Murray, P. & Wynn, T. A. Protective and pathogenic functions of macrophage subsets. Nat. Immunol. 11, 723–737 (2011).
doi: 10.1038/nri3073
Jablonski, K. A. et al. Novel markers to delineate Murine M1 and M2 macrophages. PLoS One. 10, e0145342 (2015).
pubmed: 26699615 pmcid: 4689374 doi: 10.1371/journal.pone.0145342
Gauron, C. et al. Sustained production of ROS triggers compensatory proliferation and is required for regeneration to proceed. Sci. Rep. 3, 2084 (2013).
pubmed: 23803955 pmcid: 3694286 doi: 10.1038/srep02084
Love, N. R. et al. Amputation-induced reactive oxygen species are required for successful xenopus tadpole tail regeneration. Nat. Cell. Biol. 15, 222–228 (2013).
pubmed: 23314862 pmcid: 3728553 doi: 10.1038/ncb2659
Godwin, J. W., Debuque, R., Salimova, E. & Rosenthal, N. A. Heart regeneration in the Salamander relies on macrophage-mediated control of fibroblast activation and the extracellular landscape. NPJ Reg. Med. 2, 22 (2017).
doi: 10.1038/s41536-017-0027-y
LeClair, R. J. et al. Cthrc1 is a novel inhibitor of transforming growth factor-beta signaling and neointimal lesion formation. Circ. Res. 100, 826–833 (2007).
pubmed: 17322174 doi: 10.1161/01.RES.0000260806.99307.72
Cho, K. et al. Quantitative phosphoproteomics of the human neural stem cell differentiation into oligodendrocyte by mass spectrometry. Mass. Spectrom. Lett. 3, 93–100 (2012).
doi: 10.5478/MSL.2012.3.4.93
Eng, J. K., McCormack, A. L. & Yates, J. R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass. Spectrom. 5, 976–8 (1994).
pubmed: 24226387 doi: 10.1016/1044-0305(94)80016-2
Zhang, Y. et al. ProteinInferencer: Confident protein identification and multiple experiment comparison for large scale proteomics projects. J. Proteom. 129, 25–32 (2015).
doi: 10.1016/j.jprot.2015.07.006
Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57, 289–300 (1995).
Zhang, B., Kirov, S. & Snoddy, J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nuceicl. Acids. Res. 33, W741–748 (2005).
doi: 10.1093/nar/gki475
Chong, J. et al. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic. Acids. Res. 46, W486–94 (2018).
pubmed: 29762782 pmcid: 6030889 doi: 10.1093/nar/gky310
Szklarczyk, D. et al. STRINGv10: Protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).
doi: 10.1093/nar/gku1003 pubmed: 25352553
Yoon, J. H. et al. Comparative proteomic profiling of dystroglycan-associated proteins in wild type, mdx, and galgt2 transgenic mouse skeletal muscle. J. Proteome. Res. 11, 4413–4424 (2012).
pubmed: 22775139 pmcid: 3436944 doi: 10.1021/pr300328r

Auteurs

Jung Hae Yoon (JH)

Department of Biology & UF Genetics Institute, 2033 Mowry Road, University of Florida, Gainesville, Florida, 32610, USA.

Kun Cho (K)

Biomedical Omics Group, Korea Basic Science Institute, Ochang, 863-883, Republic of Korea.

Timothy J Garrett (TJ)

Department of Pathology, Immunology, and Laboratory Medicine, University of Florida, Gainesville, Florida, USA.

Paul Finch (P)

School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK.

Malcolm Maden (M)

Department of Biology & UF Genetics Institute, 2033 Mowry Road, University of Florida, Gainesville, Florida, 32610, USA. malcmaden@ufl.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH