TY - JOUR
T1 - Identification of Epigenetically Regulated Genes Distinguishing Intracranial from Extracranial Melanoma Metastases
AU - Westphal, Dana
AU - Meinhardt, Matthias
AU - Grützmann, Konrad
AU - Schöne, Lisa
AU - Steininger, Julian
AU - Neuhaus, Lena T.
AU - Wiegel, Miriam
AU - Schrimpf, Daniel
AU - Aust, Daniela E.
AU - Schröck, Evelin
AU - Baretton, Gustavo B.
AU - Beissert, Stefan
AU - Juratli, Tareq A.
AU - Schackert, Gabriele G.
AU - Gravemeyer, Jan
AU - Becker, Jürgen C.
AU - von Deimling, Andreas
AU - Koelsche, Christian
AU - Klink, Barbara
AU - Meier, Friedegund
AU - Schulz, Alexander
AU - Muders, Michael H.
AU - Seifert, Michael
N1 - Funding Information:
We thank Isabell Kolbe from the Department of Dermatology in Dresden for her technical support. We also thank Alexander Krüger from the National Center for Tumor Diseases Dresden for performing RNA sequencing of all samples. We are grateful to Birgit Liebscher, Sylvia Strohbach, Silke Zeugner, and colleagues from the Department of Pathology in Dresden for excellent immunohistochemistry staining and macrodissection of tissues. We would like to thank Silvana Schöneich and Maxi Bergmann from the Tumor and Normal Tissue Bank of the National Center for Tumor Diseases/University Cancer Center site Dresden for organizing the tumor tissue. We kindly acknowledge Antje Habel for DNA extraction before DNA methylation profiling and Melanie Bewerunge-Hudler from the Core Facility Genomics & Proteomics at the German Cancer Research Center for carrying out the hybridization for the methylome array. The authors of this publication were supported by a National Center for Tumor Diseases Proof-of-Concept Trial Research Grant (FM, MHM, MS), a National Center for Tumor Diseases Translational Research Grant in Precision Oncology (LS, FM, MS, GBB), and a Federal Ministry of Education and Research BMBF e:Med Junior Research Alliance Grant (FKZ: 01ZX1913A, DW and FKZ: 01ZX1913B, MS). DW also acknowledges financial support from the Hiege-Stiftung - die Deutsche Hautkrebsstiftung. MHM was also supported by a grant from the Deutsche Forschungsgemeinschaft (project number 2763790). Conceptualization: DW, MM, FM, MHM, MS; Data Curation: DW, MS, MM, JS, LTN, LS, MW, CK, BK; Formal Analysis: DW, MM, KG, LTN, LS, DS, BK, AS, JS, MHM, MS; Funding Acquisition ES, GBB, SB, GGS, AVD, FM, MHM, DW, MS; Methodology: DW, MM, BK, CK, JS, LTN, MS; Resources: DEA, GBB, SB, TAJ, GGS; Writing - Original Draft Preparation: DW, MM, AS, MHM, FM, MS, Writing - Review and Editing: LS, TAJ, JG, JCB
Funding Information:
We thank Isabell Kolbe from the Department of Dermatology in Dresden for her technical support. We also thank Alexander Krüger from the National Center for Tumor Diseases Dresden for performing RNA sequencing of all samples. We are grateful to Birgit Liebscher, Sylvia Strohbach, Silke Zeugner, and colleagues from the Department of Pathology in Dresden for excellent immunohistochemistry staining and macrodissection of tissues. We would like to thank Silvana Schöneich and Maxi Bergmann from the Tumor and Normal Tissue Bank of the National Center for Tumor Diseases/University Cancer Center site Dresden for organizing the tumor tissue. We kindly acknowledge Antje Habel for DNA extraction before DNA methylation profiling and Melanie Bewerunge-Hudler from the Core Facility Genomics & Proteomics at the German Cancer Research Center for carrying out the hybridization for the methylome array. The authors of this publication were supported by a National Center for Tumor Diseases Proof-of-Concept Trial Research Grant (FM, MHM, MS), a National Center for Tumor Diseases Translational Research Grant in Precision Oncology (LS, FM, MS, GBB), and a Federal Ministry of Education and Research BMBF e:Med Junior Research Alliance Grant (FKZ: 01ZX1913A, DW and FKZ: 01ZX1913B, MS). DW also acknowledges financial support from the Hiege-Stiftung - die Deutsche Hautkrebsstiftung. MHM was also supported by a grant from the Deutsche Forschungsgemeinschaft (project number 2763790).
Funding Information:
JCB reports speaker’s bureau honoraria from Amgen, Recordati, and Sanofi; paid consultant/advisory/DSMB board member for Almirall, Boehringer Ingelheim, ICON, InProTher, MerckSerono, Pfizer, 4SC, and Sanofi/Regeneron; and research grants from Bristol-Myers Squibb, Merck Serono, HTG, IQVIA, and Alcedis. The remaining authors state no conflict of interest.
Publisher Copyright:
© 2023 The Authors
PY - 2023/7
Y1 - 2023/7
N2 - Despite remarkable advances in treating patients with metastatic melanoma, the management of melanoma brain metastases remains challenging. Recent evidence suggests that epigenetic reprogramming is an important mechanism for the adaptation of melanoma cells to the brain environment. In this study, the methylomes and transcriptomes of a cohort of matched melanoma metastases were evaluated by integrated omics data analysis. The identified 38 candidate genes displayed distinct promoter methylation and corresponding gene expression changes in intracranial compared with extracranial metastases. The 11 most promising genes were validated on protein level in both tumor and surrounding normal tissue using immunohistochemistry. In accordance with the underlying promoter methylation and gene expression changes, a significantly different protein expression was confirmed for STK10, PDXK, WDR24, CSSP1, NMB, RASL11B, phosphorylated PRKCZ, PRKCZ, and phosphorylated GRB10 in the intracranial metastases. The observed changes imply a distinct intracranial phenotype with increased protein kinase B phosphorylation and a higher frequency of proliferating cells. Knockdown of PRKCZ or GRB10 altered the expression of phosphorylated protein kinase B and decreased the viability of a brain-specific melanoma cell line. In summary, epigenetically regulated cancer-relevant alterations were identified that provide insights into the molecular mechanisms that discriminate brain metastases from other organ metastases, which could be exploited by targeting the affected signaling pathways.
AB - Despite remarkable advances in treating patients with metastatic melanoma, the management of melanoma brain metastases remains challenging. Recent evidence suggests that epigenetic reprogramming is an important mechanism for the adaptation of melanoma cells to the brain environment. In this study, the methylomes and transcriptomes of a cohort of matched melanoma metastases were evaluated by integrated omics data analysis. The identified 38 candidate genes displayed distinct promoter methylation and corresponding gene expression changes in intracranial compared with extracranial metastases. The 11 most promising genes were validated on protein level in both tumor and surrounding normal tissue using immunohistochemistry. In accordance with the underlying promoter methylation and gene expression changes, a significantly different protein expression was confirmed for STK10, PDXK, WDR24, CSSP1, NMB, RASL11B, phosphorylated PRKCZ, PRKCZ, and phosphorylated GRB10 in the intracranial metastases. The observed changes imply a distinct intracranial phenotype with increased protein kinase B phosphorylation and a higher frequency of proliferating cells. Knockdown of PRKCZ or GRB10 altered the expression of phosphorylated protein kinase B and decreased the viability of a brain-specific melanoma cell line. In summary, epigenetically regulated cancer-relevant alterations were identified that provide insights into the molecular mechanisms that discriminate brain metastases from other organ metastases, which could be exploited by targeting the affected signaling pathways.
UR - http://www.scopus.com/inward/record.url?scp=85149672475&partnerID=8YFLogxK
UR - https://pubmed.ncbi.nlm.nih.gov/36716920
U2 - 10.1016/j.jid.2023.01.011
DO - 10.1016/j.jid.2023.01.011
M3 - Article
C2 - 36716920
AN - SCOPUS:85149672475
SN - 0022-202X
VL - 143
SP - 1233-1245.e17
JO - Journal of Investigative Dermatology
JF - Journal of Investigative Dermatology
IS - 7
ER -