Comparative Transcriptomic Profiling of Hydrogen Peroxide Signaling Networks in Zebrafish and Human Keratinocytes: Implications Toward Conservation, Migration and Wound Healing

Overview

Journal Sci Rep

Specialty Science

Date 2016 Feb 6

PMID 26846883

Citations 32

Authors

Thomas S Lisse

Benjamin L King

Sandra Rieger

Affiliations

Soon will be listed here.

Abstract

Skin wounds need to be repaired rapidly after injury to restore proper skin barrier function. Hydrogen peroxide (H2O2) is a conserved signaling factor that has been shown to promote a variety of skin wound repair processes, including immune cell migration, angiogenesis and sensory axon repair. Despite growing research on H2O2 functions in wound repair, the downstream signaling pathways activated by this reactive oxygen species in the context of injury remain largely unknown. The goal of this study was to provide a comprehensive analysis of gene expression changes in the epidermis upon exposure to H2O2 concentrations known to promote wound repair. Comparative transcriptome analysis using RNA-seq data from larval zebrafish and previously reported microarray data from a human epidermal keratinocyte line shows that H2O2 activates conserved cell migration, adhesion, cytoprotective and anti-apoptotic programs in both zebrafish and human keratinocytes. Further assessment of expression characteristics and signaling pathways revealed the activation of three major H2O2-dependent pathways, EGF, FOXO1, and IKKα. This study expands on our current understanding of the clinical potential of low-level H2O2 for the promotion of epidermal wound repair and provides potential candidates in the treatment of wound healing deficits.

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References

Lisse T, Saini V, Zhao H, Luderer H, Gori F, Demay M . The vitamin D receptor is required for activation of cWnt and hedgehog signaling in keratinocytes. Mol Endocrinol. 2014; 28(10):1698-706. PMC: 4179637. DOI: 10.1210/me.2014-1043. View

Gauron C, Rampon C, Bouzaffour M, Ipendey E, Teillon J, Volovitch M . Sustained production of ROS triggers compensatory proliferation and is required for regeneration to proceed. Sci Rep. 2013; 3:2084. PMC: 3694286. DOI: 10.1038/srep02084. View

Hamill K, McLean W . The alpha-3 polypeptide chain of laminin 5: insight into wound healing responses from the study of genodermatoses. Clin Exp Dermatol. 2005; 30(4):398-404. DOI: 10.1111/j.1365-2230.2005.01842.x. View

Kanther M, Sun X, Muhlbauer M, Mackey L, Flynn 3rd E, Bagnat M . Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract. Gastroenterology. 2011; 141(1):197-207. PMC: 3164861. DOI: 10.1053/j.gastro.2011.03.042. View

Ohtani K, Iwanaga R, Nakamura M, Ikeda M, Yabuta N, Tsuruga H . Cell growth-regulated expression of mammalian MCM5 and MCM6 genes mediated by the transcription factor E2F. Oncogene. 1999; 18(14):2299-309. DOI: 10.1038/sj.onc.1202544. View

Takahashi S, Takahashi Y, Yoshimi T, Miura T . Oxygen tension regulates heme oxygenase-1 gene expression in mammalian cell lines. Cell Biochem Funct. 1998; 16(3):183-93. DOI: 10.1002/(SICI)1099-0844(199809)16:3<183::AID-CBF784>3.0.CO;2-0. View

Xu X, Zhu F, Zhang M, Zeng D, Luo D, Liu G . Stromal cell-derived factor-1 enhances wound healing through recruiting bone marrow-derived mesenchymal stem cells to the wound area and promoting neovascularization. Cells Tissues Organs. 2012; 197(2):103-13. DOI: 10.1159/000342921. View

Lu J, Goldstein K, Chen P, Huang S, Gelbert L, Nagpal S . Transcriptional profiling of keratinocytes reveals a vitamin D-regulated epidermal differentiation network. J Invest Dermatol. 2005; 124(4):778-85. DOI: 10.1111/j.0022-202X.2005.23641.x. View

Robinson M, McCarthy D, Smyth G . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26(1):139-40. PMC: 2796818. DOI: 10.1093/bioinformatics/btp616. View

10.

Paulsen C, Truong T, Garcia F, Homann A, Gupta V, Leonard S . Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol. 2011; 8(1):57-64. PMC: 3528018. DOI: 10.1038/nchembio.736. View

11.

Gough D, Cotter T . Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis. 2011; 2:e213. PMC: 3219092. DOI: 10.1038/cddis.2011.96. View

12.

Lisse T, Hewison M . Vitamin D: a new player in the world of mTOR signaling. Cell Cycle. 2011; 10(12):1888-9. PMC: 3154412. DOI: 10.4161/cc.10.12.15620. View

13.

Sen C, Roy S . OxymiRs in cutaneous development, wound repair and regeneration. Semin Cell Dev Biol. 2012; 23(9):971-80. PMC: 3762568. DOI: 10.1016/j.semcdb.2012.09.012. View

14.

Rao G, Berk B . Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res. 1992; 70(3):593-9. DOI: 10.1161/01.res.70.3.593. View

15.

Arita-Okubo S, Kim-Kaneyama J, Lei X, Fu W, Ohnishi K, Takeya M . Role of Hic-5 in the formation of microvilli-like structures and the monocyte-endothelial interaction that accelerates atherosclerosis. Cardiovasc Res. 2015; 105(3):361-71. DOI: 10.1093/cvr/cvv003. View

16.

Morano K . New tricks for an old dog: the evolving world of Hsp70. Ann N Y Acad Sci. 2007; 1113:1-14. DOI: 10.1196/annals.1391.018. View

17.

Thomas P, Kejariwal A, Campbell M, Mi H, Diemer K, Guo N . PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 2003; 31(1):334-41. PMC: 165562. DOI: 10.1093/nar/gkg115. View

18.

Liu B, Xia X, Zhu F, Park E, Carbajal S, Kiguchi K . IKKalpha is required to maintain skin homeostasis and prevent skin cancer. Cancer Cell. 2008; 14(3):212-25. PMC: 7263012. DOI: 10.1016/j.ccr.2008.07.017. View

19.

Reichard J, Motz G, Puga A . Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1. Nucleic Acids Res. 2007; 35(21):7074-86. PMC: 2175339. DOI: 10.1093/nar/gkm638. View

20.

Wang Y, Chen S, Li H . Hydrogen peroxide stress stimulates phosphorylation of FoxO1 in rat aortic endothelial cells. Acta Pharmacol Sin. 2010; 31(2):160-4. PMC: 4002846. DOI: 10.1038/aps.2009.201. View