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@ARTICLE{Tham:178850,
author = {M. Tham$^*$ and H.-J. Stark and A. Jauch and C. Harwood and
E. Pavez Lorie and P. Boukamp$^*$},
title = {{A}dverse {E}ffects of {V}emurafenib on {S}kin {I}ntegrity:
{H}yperkeratosis and {S}kin {C}ancer {I}nitiation {D}ue to
{A}ltered {MEK}/{ERK}-{S}ignaling and {MMP} {A}ctivity.},
journal = {Frontiers in oncology},
volume = {12},
issn = {2234-943X},
address = {Lausanne},
publisher = {Frontiers Media},
reportid = {DKFZ-2022-00306},
pages = {827985},
year = {2022},
note = {#EA:A110#LA:A110#},
abstract = {The BRAF inhibitor vemurafenib, approved for treating
patients with BRAF V600E-mutant and unresectable or
metastatic melanomas, rapidly induces cutaneous adverse
events, including hyperkeratotic skin lesions and cutaneous
squamous cell carcinomas (cSCC). To determine, how
vemurafenib would provoke these adverse events, we utilized
long-term in vitro skin equivalents (SEs) comprising
epidermal keratinocytes and dermal fibroblasts in their
physiological environment. We inserted keratinocytes with
different genetic background [normal keratinocytes: NHEK,
HaCaT (p53/mut), and HrasA5 (p53/mut+Hras/mut)] to analyze
effects depending on the stage of carcinogenesis. We now
show that vemurafenib activates MEK-ERK signaling in both,
keratinocytes, and fibroblasts in vitro and in the in
vivo-like SEs. As a consequence, vemurafenib does not
provide a growth advantage but leads to a differentiation
phenotype, causing accelerated differentiation and
hyperkeratosis in the NHEK and normalized stratification and
cornification in the transformed keratinocytes. Although all
keratinocytes responded very similarly to vemurafenib in
their expression profile, particularly with a significant
induction of MMP1 and MMP3, only the HrasA5 cells revealed a
vemurafenib-dependent pathophysiological shift to tumor
progression, i.e., the initiation of invasive growth. This
was shown by increased proteolytic activity allowing for
penetration of the basement membrane and invasion into the
disrupted underlying matrix. Blocking MMP activity, by the
addition of ilomastat, prevented invasion with all
corresponding degradative activities, thus substantiating
that the RAS-RAF-MEK-ERK/MMP axis is the most important
molecular basis for the rapid switch towards tumorigenic
conversion of the HrasA5 keratinocytes upon vemurafenib
treatment. Finally, cotreatment with vemurafenib and the MEK
inhibitor cobimetinib prevented MEK-ERK hyperactivation and
with that abolished both, the epidermal differentiation and
the tumor invasion phenotype. This suggests that both
cutaneous adverse events are under direct control of
vemurafenib-dependent MEK-ERK hyperactivation and confirms
the dependence on preexisting genetic alterations of the
skin keratinocytes that determine the basis towards
induction of tumorigenic progression.},
keywords = {MEK inhibition (Other) / cutaneous adverse effects (Other)
/ degradome (Other) / matrix metalloproteinase (Other) /
organotypic skin cancer model (Other) / skin cancer (Other)
/ tumor invasion (Other) / vemurafenib (Other)},
cin = {A110},
ddc = {610},
cid = {I:(DE-He78)A110-20160331},
pnm = {311 - Zellbiologie und Tumorbiologie (POF4-311)},
pid = {G:(DE-HGF)POF4-311},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:35174094},
pmc = {pmc:PMC8842679},
doi = {10.3389/fonc.2022.827985},
url = {https://inrepo02.dkfz.de/record/178850},
}