The role of dual-specificity phosphatase 3 in melanocytic oncogenesis.
DUSP3
VHR
dual-specificity
melanoma
nevi
oncogene
oncogenesis
oncosuppressor
phosphatase
Journal
Experimental dermatology
ISSN: 1600-0625
Titre abrégé: Exp Dermatol
Pays: Denmark
ID NLM: 9301549
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
08
07
2022
received:
17
12
2021
accepted:
25
07
2022
pubmed:
29
7
2022
medline:
5
10
2022
entrez:
28
7
2022
Statut:
ppublish
Résumé
Dual-specificity phosphatase 3 (DUSP3), also known as Vaccinia H1-related phosphatase, is a protein tyrosine phosphatase that typically performs its major role in the regulation of multiple cellular functions through the dephosphorylation of its diverse and constantly expanding range of substrates. Many of the substrates described so far as well as alterations in the expression or the activity of DUSP3 itself are associated with the development and progression of various types of neoplasms, indicating that DUSP3 may be an important player in oncogenesis and a promising therapeutic target. This review focuses exclusively on DUSP3's contribution to either benign or malignant melanocytic oncogenesis, as many of the established culprit pathways and mechanisms constitute DUSP3's regulatory targets, attempting to synthesize the current knowledge on the matter. The spectrum of the DUSP3 interactions analysed in this review covers substrates implicated in cellular growth, cell cycle, proliferation, survival, apoptosis, genomic stability/repair, adhesion and migration of tumor melanocytes. Furthermore, the speculations raised, based on the evidence to date, may be considered a fundament for potential research regarding the oncogenesis, evolution, management and therapeutics of melanocytic tumors.
Substances chimiques
DUSP3 protein, human
EC 3.1.3.48
Dual Specificity Phosphatase 3
EC 3.1.3.48
Protein Tyrosine Phosphatases
EC 3.1.3.48
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1466-1476Informations de copyright
© 2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Pavic K, Duan G, Köhn M. VHR/DUSP3 phosphatase: structure, function and regulation. FEBS J. 2015;282(10):1871-1890.
Shtivelman E, Davies MQ, Hwu P, et al. Pathways and therapeutic targets in melanoma. Oncotarget. 2014;5(7):1701-1752.
Grant S, Qiao L, Dent P. Roles of ERBB family receptor tyrosine kinases, and downstream signaling pathways, in the control of cell growth and survival. Front Biosci. 2002;7:d376-d389.
Wang JY, Yeh CL, Chou HC, et al. Vaccinia H1-related phosphatase is a phosphatase of ErbB receptors and is down-regulated in non-small cell lung cancer. J Biol Chem. 2011;286(12):10177-10184.
Niu G, Bowman T, Huang M, et al. Roles of activated Src and Stat3 signaling in melanoma tumor cell growth. Oncogene. 2002;21(46):7001-7010.
Oka M, Kikkawa U. Protein kinase C in melanoma. Cancer Metastasis Rev. 2005;24(2):287-300.
Roh MR, Eliades P, Gupta S, Tsao H. Genetics of melanocytic nevi. Pigment Cell Melanoma Res. 2015;28(6):661-672.
Palmieri G, Colombino M, Casula M, Manca A, Mandalà M, Cossu A. Molecular pathways in melanomagenesis: What we learned from next-generation sequencing approaches. Curr Oncol Rep. 2018;20:86.
Greaves WO, Verma S, Patel KP, et al. Frequency and spectrum of BRAF mutations in a retrospective, single-institution study of 1112 cases of melanoma. J Mol Diagn. 2013;15(2):220-226.
Todd JL, Tanner KG, Denu JM. Extracellular regulated kinases (ERK) 1 and ERK2 are authentic substrates for the dual-specificity protein-tyrosine phosphatase VHR. A novel role in down-regulating the ERK pathway. J Biol Chem. 1999;274(19):13271-13280.
Tambe MB, Narvi E, Kallio M. Reduced levels of Dusp3/Vhr phosphatase impair normal spindle bipolarity in an Erk1/2 activity-dependent manner. FEBS Lett. 2016;590(16):2757-2767.
Kang TH, Kim KT. Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat Cell Biol. 2006;8(8):863-869.
Wagner KW, Alam H, Dhar SS, et al. KDM2A promotes lung tumorigenesis by epigenetically enhancing ERK1/2 signaling. J Clin Invest. 2013;123(12):5231-5246.
Michaloglou C, Vredeveld LC, Soengas MS, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436(7051):720-724.
Rahmouni S, Cerignoli F, Alonso A, et al. Loss of the VHR dual-specific phosphatase causes cell-cycle arrest and senescence. Nat Cell Biol. 2006;8(5):524-531.
Mitsui H, Kiecker F, Shemer A, et al. Discrimination of dysplastic nevi from common melanocytic nevi by cellular and molecular criteria. J Invest Dermatol. 2016;136(10):2030-2040.
Davies MA. The role of the PI3K-AKT pathway in melanoma. Cancer J. 2012;18(2):142-147.
Drukker L, Margulis A, Chaouat M, Levitzki R, Maiorenko E, Ben BH. Changes of PI3K/AKT/BCL2 signaling proteins in congenital Giant Nevi: melanocytes contribute to their increased survival and integrity. J Recept Signal Transduct Res. 2013;33(6):359-366.
Curtin JA, Stark MS, Pinkel D, Hayward NK, Bastian BC. PI3-kinase subunits are infrequent somatic targets in melanoma. J Invest Dermatol. 2006;126(7):1660-1663.
Wu H, Goel V, Haluska FG. PTEN signaling pathways in melanoma. Oncogene. 2003;22(20):3113-3122.
Prickett TD, Agrawal NS, Wei X, et al. Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat Genet. 2009;41(10):1127-1132.
Vredeveld LC, Possik PA, Smit MA, et al. Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev. 2012;26(10):1055-1069.
Shao Z, Bao Q, Jiang F, Qian H, Fang Q, Hu X. VS-5584, a novel PI3K-mTOR dual inhibitor, inhibits melanoma cell growth in vitro and in vivo. PLoS One. 2015;10(7):e0132655.
Irvine M, Stewart A, Pedersen B, Boyd S, Kefford R, Rizos H. Oncogenic PI3K/AKT promotes the step-wise evolution of combination BRAF/MEK inhibitor resistance in melanoma. Oncogene. 2018;7(9):72.
Posch C, Moslehi H, Feeney L, et al. Combined targeting of MEK and PI3K/mTOR effector pathways is necessary to effectively inhibit NRAS mutant melanoma in vitro and in vivo. Proc Natl Acad Sci U S A. 2013;110(10):4015-4020.
Ruiz-Saenz A, Dreyer C, Campbell MR, Steri V, Gulizia N, Moasser MM. HER2 amplification in tumors activates PI3K/Akt signaling independent of HER3. Cancer Res. 2018;78(13):3645-3658.
Wheeler M, Domin J. Recruitment of the class II phosphoinositide 3-kinase C2beta to the epidermal growth factor receptor: role of Grb2. Mol Cell Biol. 2001;21(19):6660-6667.
Rodriguez-Viciana P, Warne PH, Dhand R, et al. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 1994;370(6490):527-532.
Jørgensen K, Davidson B, Flørenes VA. Activation of c-jun N-terminal kinase is associated with cell proliferation and shorter relapse-free period in superficial spreading malignant melanoma. Mod Pathol. 2006;19(11):1446-1455.
Alexaki VI, Javelaud D, Mauviel A. JNK supports survival in melanoma cells by controlling cell cycle arrest and apoptosis. Pigment Cell Melanoma Res. 2008;21(4):429-438.
Wang Y, Zhang G, Jin J, Degan S, Tameze Y, Zhang JY. MALT1 promotes melanoma progression through JNK/c-Jun signaling. Oncogene. 2017;6(7):e365.
Lopez-Bergami P, Huang C, Goydos JS, et al. Rewired ERK-JNK signaling pathways in melanoma. Cancer Cell. 2007;11(5):447-460.
Todd JL, Rigas JD, Rafty LA, Denu JM. Dual-specificity protein tyrosine phosphatase VHR down-regulates c-Jun N-terminal kinase (JNK). Oncogene. 2002;21(16):2573-2583.
Cerignoli F, Rahmouni S, Ronai Z, Mustelin T. Regulation of MAP kinases by the VHR dual-specific phosphatase: implications for cell growth and differentiation. Cell Cycle. 2006;5(19):2210-2215.
Alonso A, Saxena M, Williams S, Mustelin T. Inhibitory role for dual specificity phosphatase VHR in T cell antigen receptor and CD28-induced Erk and Jnk activation. J Biol Chem. 2001;276(7):4766-4771.
Estrada Y, Dong J, Ossowski L. Positive crosstalk between ERK and p38 in melanoma stimulates migration and in vivo proliferation. Pigment Cell Melanoma Res. 2009;22(1):66-76.
Khanna P, Yunkunis T, Muddana HS, Peng HH, August A, Dong C. p38 MAP kinase is necessary for melanoma-mediated regulation of VE-cadherin disassembly. Am J Physiol Cell Physiol. 2010;298(5):C1140-C1150.
Wenzina J, Holzner S, Puujalka E, et al. Inhibition of p38/MK2 signaling prevents vascular invasion of melanoma. J Invest Dermatol. 2020;140(4):878-890.e5.
Lee J, Smalley K, Brafford P, Herlyn M. p38 represents a novel therapeutic target for advanced stage melanoma. Cancer Res. 2006;66:10560-10566.
Banik I, Cheng PF, Dooley CM, et al. NRASQ61K melanoma tumor formation is reduced by p38-MAPK14 activation in zebrafish models and NRAS-mutated human melanoma cells. Pigment Cell Melanoma Res. 2021;34(2):150-162.
Ivanov VN, Ronai Z. p38 protects human melanoma cells from UV-induced apoptosis through down-regulation of NF-kappaB activity and Fas expression. Oncogene. 2000;19(26):3003-3012.
Madonna G, Ullman CD, Gentilcore G, Palmieri G, Ascierto PA. NF-κB as potential target in the treatment of melanoma. J Transl Med. 2012;20:53.
Amand M, Erpicum C, Bajou K, et al. DUSP3/VHR is a pro-angiogenic atypical dual-specificity phosphatase. Mol Cancer. 2014;15:108.
Wen SY, Cheng SY, Ng SC, et al. Roles of p38α and p38β mitogen-activated protein kinase isoforms in human malignant melanoma A375 cells. Int J Mol Med. 2019;44(6):2123-2132.
Selzer E, Okamoto I, Lucas T, Kodym R, Pehamberger H, Jansen B. Protein kinase C isoforms in normal and transformed cells of the melanocytic lineage. Melanoma Res. 2002;12(3):201-209.
La Porta CA, Comolli R. Activation of protein kinase C-alpha isoform in murine melanoma cells with high metastatic potential. Clin Exp Metastasis. 1997;15(6):568-579.
Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR. Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem. 2003;278(15):13061-13068.
Xu H, Czerwinski P, Hortmann M, Sohn HY, Förstermann U, Li H. Protein kinase C alpha promotes angiogenic activity of human endothelial cells via induction of vascular endothelial growth factor. Cardiovasc Res. 2008;78(2):349-355.
Olayioye MA, Beuvink I, Horsch K, Daly JM, Hynes NE. ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J Biol Chem. 1999;274(24):17209-17218.
Ren Z, Aerts JL, Vandenplas H, et al. Phosphorylated STAT5 regulates p53 expression via BRCA1/BARD1-NPM1 and MDM2. Cell Death Dis. 2016;7(12):e2560.
Wang W, Edington HD, Rao UN, et al. STAT3 as a biomarker of progression in atypical nevi of patients with melanoma: dose-response effects of systemic IFNalpha therapy. J Invest Dermatol. 2008;128(8):1997-2002.
Igelmann S, Neubauer HA, Ferbeyre G. STAT3 and STAT5 activation in solid cancers. Cancers. 2019;11(10):1428.
Hassel JC, Winnemöller D, Schartl M, Wellbrock C. STAT5 contributes to antiapoptosis in melanoma. Melanoma Res. 2008;18(6):378-385.
Lesinski GB. The potential for targeting the STAT3 pathway as a novel therapy for melanoma. Future Oncol. 2013;9(7):925-927.
Wang W, Edington HD, Rao UN, et al. Modulation of signal transducers and activators of transcription 1 and 3 signaling in melanoma by high-dose IFNalpha2b. Clin Cancer Res. 2007;13(5):1523-1531.
Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798-809.
Verdeil G, Lawrence T, Schmitt-Verhulst AM, Auphan-Anezin N. Targeting STAT3 and STAT5 in tumor-associated immune cells to improve immunotherapy. Cancer. 2019;11(12):1832.
Jardin C, Sticht H. Identification of the structural features that mediate binding specificity in the recognition of STAT proteins by dual-specificity phosphatases. J Biomol Struct Dyn. 2012;29(4):777-792.
Hoyt R, Zhu W, Cerignoli F, Alonso A, Mustelin T, David M. Cutting edge: selective tyrosine dephosphorylation of interferon-activated nuclear STAT5 by the VHR phosphatase. J Immunol. 2007;179(6):3402-3406.
Kim BR, Ha J, Kang E, Cho S. Regulation of signal transducer and activator of transcription 3 activation by dual-specificity phosphatase 3. BMB Rep. 2020;53(6):335-340.
Gartsbein M, Alt A, Hashimoto K, Nakajima K, Kuroki T, Tennenbaum T. The role of protein kinase C delta activation and STAT3 Ser727 phosphorylation in insulin-induced keratinocyte proliferation. J Cell Sci. 2006;119(Pt 3):470-481.
Watson SP, Asazuma N, Atkinson B, et al. The role of ITAM- and ITIM-coupled receptors in platelet activation by collagen. Thromb Haemost. 2001;86(1):276-288.
Ruschel A, Ullrich A. Protein tyrosine kinase Syk modulates EGFR signalling in human mammary epithelial cells. Cell Signal. 2004;16(11):1249-1261.
Huang DY, Chen WY, Chen CL, Wu NL, Lin WW. Synergistic anti-tumour effect of Syk inhibitor and olaparib in squamous cell carcinoma: Roles of Syk in EGFR signalling and PARP1 activation. Cancers. 2020;12(2):489.
Bailet O, Fenouille N, Abbe P, et al. Spleen tyrosine kinase functions as a tumor suppressor in melanoma cells by inducing senescence-like growth arrest. Cancer Res. 2009;69(7):2748-2756.
Wu NL, Huang DY, Wang LF, Kannagi R, Fan YC, Lin WW. Spleen tyrosine kinase mediates EGFR signaling to regulate keratinocyte terminal differentiation. J Invest Dermatol. 2016;136(1):192-201.
Musumeci L, Kuijpers MJ, Gilio K, et al. Dual-specificity phosphatase 3 deficiency or inhibition limits platelet activation and arterial thrombosis. Circulation. 2015;131(7):656-668.
Box JK, Paquet N, Adams MN, et al. Nucleophosmin: from structure and function to disease development. BMC Mol Biol. 2016;17(1):19.
Bernard K, Litman E, Fitzpatrick JL, et al. Functional proteomic analysis of melanoma progression. Cancer Res. 2003;63(20):6716-6725.
Calli AO, Sari A, Evcim G, Altinboga A, Sadullahoglu C, Ermete M. The enigmatic role of nucleophosmin in malignant melanoma: does it have an effect? Indian J Pathol Microbiol. 2011;54(3):482-486.
Terzian T, Torchia EC, Dai D, et al. p53 prevents progression of nevi to melanoma predominantly through cell cycle regulation. Pigment Cell Melanoma Res. 2010;23(6):781-794.
Qin FX, Shao HY, Chen XC, et al. Knockdown of NPM1 by RNA interference inhibits cells proliferation and induces apoptosis in leukemic cell line. Int J Med Sci. 2011;8(4):287-294.
Colombo E, Marine JC, Danovi D, Falini B, Pelicci PG. Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol. 2002;4(7):529-533.
Kurki S, Peltonen K, Latonen L, et al. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell. 2004;5(5):465-475.
Li J, Zhang X, Sejas DP, Bagby GC, Pang Q. Hypoxia-induced nucleophosmin protects cell death through inhibition of p53. J Biol Chem. 2004;279(40):41275-41279.
Maiguel DA, Jones L, Chakravarty D, Yang C, Carrier F. Nucleophosmin sets a threshold for p53 response to UV radiation. Mol Cell Biol. 2004;24(9):3703-3711.
Panico K, Forti FL. Proteomic, cellular, and network analyses reveal new DUSP3 interactions with nucleolar proteins in HeLa cells. J Proteome Res. 2013;12:5851-5866.
Russo LC, Ferruzo PYM, Forti FL. Nucleophosmin protein dephosphorylation by DUSP3 is a fine-tuning regulator of p53 signaling to maintain genomic stability. Front Cell Dev Biol. 2021;11:624933.
Torres TEP, Russo LC, Santos A, et al. Loss of DUSP3 activity radiosensitizes human tumor cell lines via attenuation of DNA repair pathways. Biochim Biophys Acta Gen Subj. 2017;1861(7):1879-1894.
Chiarella S, De Cola A, Scaglione GL, et al. Nucleophosmin mutations alter its nucleolar localization by impairing G-quadruplex binding at ribosomal DNA. Nucleic Acids Res. 2013;41(5):3228-3239.
Ovejero S, Bueno A, Sacristán MP. Working on genomic stability: from the S-phase to mitosis. Genes. 2020;11(2):225.
Stark MS, Denisova E, Kays TA, et al. Mutation signatures in melanocytic nevi reveal characteristics of defective DNA repair. J Invest Dermatol. 2020;140(10):2093-2096.e2.
Landi MT, Baccarelli A, Tarone RE, et al. DNA repair, dysplastic nevi, and sunlight sensitivity in the development of cutaneous malignant melanoma. J Natl Cancer Inst. 2002;94(2):94-101.
Kauffmann A, Rosselli F, Lazar V, et al. High expression of DNA repair pathways is associated with metastasis in melanoma patients. Oncogene. 2008;27(5):565-573.
Forti FL. Combined experimental and bioinformatics analysis for the prediction and identification of VHR/DUSP3 nuclear targets related to DNA damage and repair. Integr Biol. 2015;7(1):73-89.
Russo LC, Farias JO, Forti FL. DUSP3 maintains genomic stability and cell proliferation by modulating NER pathway and cell cycle regulatory proteins. Cell Cycle. 2020;19(12):1545-1561.
Mourmouras V, Cevenini G, Cosci E, et al. Nucleolin protein expression in cutaneous melanocytic lesions. J Cutan Pathol. 2009;36(6):637-646.
Mulnix RE, Pitman RT, Retzer A, et al. hnRNP C1/C2 and Pur-beta proteins mediate induction of senescence by oligonucleotides homologous to the telomere overhang. Onco Targets Ther. 2013;18:23-32.
Steffen J, Varon R, Mosor M, et al. Increased cancer risk of heterozygotes with NBS1 germline mutations in Poland. Int J Cancer. 2004;111(1):67-71.
Hess AR, Postovit LM, Margaryan NV, et al. Focal adhesion kinase promotes the aggressive melanoma phenotype. Cancer Res. 2005;65(21):9851-9860.
Yoon H, Dehart JP, Murphy JM, Lim ST. Understanding the roles of FAK in cancer: inhibitors, genetic models, and new insights. J Histochem Cytochem. 2015;63(2):114-128.
Kishore A, Feng X, Arang N, et al. Identifying novel molecular vulnerabilities to PTK2/FAK inhibition in G α q-driven uveal melanoma using a kinome-wide CRISPR/Cas9 screen. FASEB J. 2019;33:647.15. doi:10.1096/fasebj.2019.33.1_supplement.647.15
Jeong K, Murphy JM, Rodriguez YAR, Kim JS, Ahn EE, Lim SS. FAK inhibition reduces metastasis of α4 integrin-expressing melanoma to lymph nodes by targeting lymphatic VCAM-1 expression. Biochem Biophys Res Commun. 2019;509(4):1034-1040.
Najjar S, Homan S, Sheehan C, Carlson JA. SERINE-910 phosphorylated focal adhesion kinase expression predicts better overall and disease-free survival in melanoma. Appl Immunohistochem Mol Morphol. 2020;28(2):130-138.
Kahana O, Micksche M, Witz IP, Yron I. The focal adhesion kinase (P125FAK) is constitutively active in human malignant melanoma. Oncogene. 2002;21(25):3969-3977.
Chen YR, Chou HC, Yang CH, et al. Deficiency in VHR/DUSP3, a suppressor of focal adhesion kinase, reveals its role in regulating cell adhesion and migration. Oncogene. 2017;36(47):6509-6517.
Pereira NR, Russo LC, Forti FL. UV radiation-induced impairment of cellular morphology and motility is enhanced by DUSP3/VHR loss and FAK activation. Cell Biochem Biophys. 2021;79(2):261-269.
López-Colomé AM, Lee-Rivera I, Benavides-Hidalgo R, López E. Paxillin: a crossroad in pathological cell migration. J Hematol Oncol. 2017;10(1):50.
Mousson A, Legrand M, Steffan T, et al. Inhibiting FAK-paxillin interaction reduces migration and invadopodia-mediated matrix degradation in metastatic melanoma cells. Cancers. 2021;13(8):1871.
Lang R, Raffi FAM. Dual-specificity phosphatases in immunity and infection: an update. Int J Mol Sci. 2019;20(11):2710.