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PMID: 22203954 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Targeting protein-trafficking pathways alters melanoma treatment sensitivity.

Huang ZM, Chinen M, Chang PJ, Xie T, Zhong L, Demetriou S, Patel MP, Scherzer R, Sviderskaya EV, Bennett DC, Millhauser GL, Oh DH, Cleaver JE, Wei ML

Abstract

Protein-trafficking pathways are targeted here in human melanoma cells using methods independent of oncogene mutational status, and the ability to up-regulate and down-regulate tumor treatment sensitivity is demonstrated. Sensitivity of melanoma cells to cis-diaminedichloroplatinum II (cDDP, cis-platin), carboplatin, dacarbazine, or temozolomide together with velaparib, an inhibitor of poly (ADP ribose) polymerase 1, is increased by up to 10-fold by targeting genes that regulate both protein trafficking and the formation of melanosomes, intracellular organelles unique to melanocytes and melanoma cells. Melanoma cells depleted of either of the protein-trafficking regulators vacuolar protein sorting 33A protein (VPS33A) or cappuccino protein (CNO) have increased nuclear localization of cDDP, increased nuclear DNA damage by platination, and increased apoptosis, resulting in increased treatment sensitivity. Depleted cells also exhibit a decreased proportion of intracellular, mature melanosomes compared with undepleted cells. Modulation of protein trafficking via cell-surface signaling by binding the melanocortin 1 receptor with the antagonist agouti-signaling protein decreased the proportion of mature melanosomes formed and increased cDDP sensitivity, whereas receptor binding with the agonist melanocyte-stimulating hormone resulted in an increased proportion of mature melanosomes formed and in decreased sensitivity (i.e., increased resistance) to cDDP. Mutation of the protein-trafficking gene Hps6, known to impair the formation of mature melanosomes, also increased cDDP sensitivity. Together, these results indicate that targeting protein-trafficking molecules markedly increases melanoma treatment sensitivity and influences the degree of melanosomes available for sequestration of therapeutic agents.

MeSH Terms
Amino Acid Sequence Antineoplastic Agents/pharmacology Carboplatin/pharmacology Cell Line, Tumor Cisplatin/pharmacology DNA Repair Dacarbazine/analogs & derivatives,pharmacology Down-Regulation/drug effects Drug Resistance, Neoplasm/drug effects,physiology Humans Immunoblotting Intracellular Signaling Peptides and Proteins/genetics Melanoma/drug therapy Melanosomes/drug effects Microscopy, Electron Microscopy, Fluorescence Molecular Sequence Data Mutation/genetics Protein Transport/genetics RNA Interference Receptor, Melanocortin, Type 1/metabolism Temozolomide Up-Regulation/drug effects Vesicular Transport Proteins/deficiency,genetics
Chemicals
Antineoplastic Agents BLOC1S4 protein, human HPS6 protein, human Intracellular Signaling Peptides and Proteins Receptor, Melanocortin, Type 1 VPS33A protein, human Vesicular Transport Proteins Dacarbazine Carboplatin Cisplatin Temozolomide
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Huang Zhi-ming
Department of Dermatology, University of California, San Francisco, CA 94115, USA.
Chinen Milka
Chang Philip J
Xie Tong
Zhong Lily
Demetriou Stephanie
Patel Mira P
Scherzer Rebecca
Sviderskaya Elena V
Bennett Dorothy C
Millhauser Glenn L
Oh Dennis H
Cleaver James E
Wei Maria L
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-01-10
Epub
2011-00-27
Pages
553-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3258646
Subset
IM
Grants
NIDDK NIH HHS · R01 DK064265 · United States
Wellcome Trust · 078327 · United Kingdom
NIDDK NIH HHS · DK064265 · United States
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