Protein Oxidative Damage in UV-Related Skin Cancer and Dysplastic Lesions Contributes to Neoplastic Promotion and Progression

Antonella Tramutola, Susanna Falcucci, Umberto Brocco, Francesca Triani, Chiara Lanzillotta, Michele Donati, Chiara Panetta, Fabiola Luzi, Federica Iavarone, Federica Vincenzoni, Massimo Castagnola, Marzia Perluigi, Fabio Di Domenico, Federico De Marco, Antonella Tramutola, Susanna Falcucci, Umberto Brocco, Francesca Triani, Chiara Lanzillotta, Michele Donati, Chiara Panetta, Fabiola Luzi, Federica Iavarone, Federica Vincenzoni, Massimo Castagnola, Marzia Perluigi, Fabio Di Domenico, Federico De Marco

Abstract

The ultraviolet (UV) component of solar radiation is the major driving force of skin carcinogenesis. Most of studies on UV carcinogenesis actually focus on DNA damage while their proteome-damaging ability and its contribution to skin carcinogenesis have remained largely underexplored. A redox proteomic analysis of oxidized proteins in solar-induced neoplastic skin lesion and perilesional areas has been conducted showing that the protein oxidative burden mostly concerns a selected number of proteins participating to a defined set of functions, namely: chaperoning and stress response; protein folding/refolding and protein quality control; proteasomal function; DNA damage repair; protein- and vesicle-trafficking; cell architecture, adhesion/extra-cellular matrix (ECM) interaction; proliferation/oncosuppression; apoptosis/survival, all of them ultimately concurring either to structural damage repair or to damage detoxication and stress response. In peri-neoplastic areas the oxidative alterations are conducive to the persistence of genetic alterations, dysfunctional apoptosis surveillance, and a disrupted extracellular environment, thus creating the condition for transformant clones to establish, expand and progress. A comparatively lower burden of oxidative damage is observed in neoplastic areas. Such a finding can reflect an adaptive selection of best fitting clones to the sharply pro-oxidant neoplastic environment. In this context the DNA damage response appears severely perturbed, thus sustaining an increased genomic instability and an accelerated rate of neoplastic evolution. In conclusion UV radiation, in addition to being a cancer-initiating agent, can act, through protein oxidation, as a cancer-promoting agent and as an inducer of genomic instability concurring with the neoplastic progression of established lesions.

Keywords: cancer promotion; carcinogenesis; protein damage; protein oxidation; redox proteomics; skin cancer; solar radiation; stress response.; ultraviolet.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Histopathological presentation tissue samples and pathological diagnosis (SCC: squamous cell carcinoma) (BCC: basal-like cell carcinoma). Low magnification pictures on the left hand side (Pts 5; 8; 10; 12 and 16, 4× magnification; pts. 7 and 14 magnification 1.5×). On right hand side particulars at higher magnification (pts 5 and 12, 20×; pts 7 and 14, 4×; Pts 8, 10 and 16, 10×).
Figure 2
Figure 2
BstUI restriction fragment length polymorphism (RFLP) analysis of p53 codon 72 dimorphism. The presence of a guanosine at nucleotide 216 in the exon 4th amplicon can be revealed BstUI restriction. Thus, the presence of two 131 and 208 bp bands in digested lane (D) stands for the R72 variant (black circle) whereas the full length 339 bp undigested band indicates the P72 variant (red circle). Both digested and undigested bands in D lanes indicate Pro/Arg heterozygous (blue box). (U) Undigested DNA.
Figure 3
Figure 3
Slot blot analysis of total protein carbonylation. Panel A (left hand side): Slot blot of a representative sample from non-photo exposed (NPE), perilesional (PL) and lesional (L) groups. A triplicate of 4 samples per group is showed. Panel B (right hand side): Densitometric analysis of total protein carbonylation in NPE, PL and L groups. NPE is set as 100%. The bars show the averages of 7 samples per group ± standard error of the mean (SEM); * p < 0.05, ** p < 0.01.
Figure 4
Figure 4
Two-dimensional (2D) electrophoresis images. Panel A: Workflow of redox proteomics approach employed in the study. Panel B: Representative 2D gel from NPE samples showing position and ID number of the spots identified to be differentially carbonylated in both PL vs. NPE and PL vs. L comparison groups. Proteins matching ID spots numbers are reported in Table 2. Panel C: Representative 2D blots from NPE, PL and L samples showing the different amount of total protein carbonylation.
Figure 5
Figure 5
STRING analysis PL vs. NPE. Panel A: Network statistics reporting data concerning the number of nodes and edges, the average node degree, the average local clustering coefficient, the expected number of edges and the PPI enrichment p-value. Panel B: Network interaction image showing nodes and edges between the proteins identified. The thickness of the line indicates the strength of the interaction between the proteins. The colours of the sphere indicate the biological processes to which the protein belongs. Panel C: Network interaction table reports all the significant interactions (min 0.4) between the protein of the PL vs. NPE network. Panel D: Biological process table reports the main pathways to which the protein of the networks belongs. For each biological process identified, the corresponding Gene Ontology (GO) pathway, the number and identity of proteins and the false discovery rate is reported.
Figure 6
Figure 6
STRING analysis PL vs. L. Panel A: Network statistics reporting data concerning the number of nodes and edges, the average node degree, the average local clustering coefficient, the expected number of edges and the PPI enrichment p-value. Panel B: Network interaction image showing nodes and edges between the proteins identified. The thickness of the line indicates the strength of the interaction between the proteins. The colours of the sphere indicate the biological processes to which the protein belongs. Panel C: Network interaction table reporting all the significant interactions (min 0.4) between the protein of the PL vs. NPE network. Panel D: Biological process table reporting the main pathways to which the protein of the networks belongs. For each biological process identified, the corresponding GO pathway, the number and identity of proteins and the false discovery rate is reported.

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