Chondroitin polymerizing factor (CHPF) promotes development of malignant melanoma through regulation of CDK1.
Apoptosis
CDC2 Protein Kinase
/ metabolism
Carcinogenesis
/ metabolism
Cell Line, Tumor
Cell Movement
Cell Proliferation
Disease Progression
Epithelial-Mesenchymal Transition
Female
Gene Expression Regulation, Neoplastic
Gene Knockdown Techniques
Humans
Male
Melanoma
/ enzymology
Middle Aged
N-Acetylgalactosaminyltransferases
Skin
/ metabolism
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
01 07 2020
01 07 2020
Historique:
received:
12
06
2019
accepted:
20
01
2020
revised:
17
01
2020
entrez:
3
7
2020
pubmed:
3
7
2020
medline:
24
3
2021
Statut:
epublish
Résumé
Chondroitin polymerizing factor (CHPF) is an important member of glycosyltransferases involved in the biosynthesis of chondroitin sulfate (CS). However, the relationship between CHPF and malignant melanoma (MM) is still unknown. In this study, it was demonstrated that CHPF was up-regulated in MM tissues compared with the adjacent normal skin tissues and its high expression was correlated with more advanced T stage. Further investigations indicated that the over-expression/knockdown of CHPF could promote/inhibit proliferation, colony formation and migration of MM cells, while inhibiting/promoting cell apoptosis. Moreover, knockdown of CHPF could also suppress tumorigenicity of MM cells in vivo. RNA-sequencing followed by Ingenuity pathway analysis (IPA) was performed for exploring downstream of CHPF and identified CDK1 as the potential target. Furthermore, our study revealed that knockdown of CDK1 could inhibit development of MM in vitro, and alleviate the CHPF over-expression induced promotion of MM. In conclusion, our study showed, as the first time, CHPF as a tumor promotor for MM, whose function was carried out probably through the regulation of CDK1.
Identifiants
pubmed: 32612115
doi: 10.1038/s41419-020-2526-9
pii: 10.1038/s41419-020-2526-9
pmc: PMC7329816
doi:
Substances chimiques
N-Acetylgalactosaminyltransferases
EC 2.4.1.-
chondroitin synthase
EC 2.4.1.175
CDC2 Protein Kinase
EC 2.7.11.22
CDK1 protein, human
EC 2.7.11.22
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
496Références
Network Cancer Genome Atlas. Genomic classification of cutaneous melanoma. Cell 161, 1681–1696 (2015).
doi: 10.1016/j.cell.2015.05.044
Mishra, H. et al. Melanoma treatment: from conventional to nanotechnology. J. Cancer Res. Clin. 144, 1–20 (2018).
doi: 10.1007/s00432-018-2726-1
Koshenkov, V. P., Broucek, J. & Kaufman, H. L. Surgical management of melanoma. Cancer Treat. Res. 167, 149 (2016).
pubmed: 26601862
doi: 10.1007/978-3-319-22539-5_6
Valpione, S. & Campana, L. G. Immunotherapy for advanced melanoma: future directions. Immunotherapy 8, 199–209 (2016).
pubmed: 26809078
doi: 10.2217/imt.15.111
Valsecchi, M. E. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373, 23 (2015).
doi: 10.1056/NEJMoa1504030
Robert, C. et al. Nivolumab in previously untreated melanoma without BRAF mutation. N. Engl. J. Med. 372, 320–330 (2015).
doi: 10.1056/NEJMoa1412082
Wolchok, J. D. et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369, 122–133 (2013).
pubmed: 23724867
pmcid: 5698004
doi: 10.1056/NEJMoa1302369
Baylin, S. B. & Ohm, J. E. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 6, 107 (2006).
pubmed: 16491070
doi: 10.1038/nrc1799
Sugahara, K. et al. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struc Biol. 13, 612–620 (2003).
doi: 10.1016/j.sbi.2003.09.011
Perrimon, N. & Bernfield, M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725–728 (2000).
pubmed: 10783877
doi: 10.1038/35008000
Sugumaran, G., Katsman, M., Sunthankar, P. & Drake, R. R. Biosynthesis of chondroitin sulfate. J. Biol. Chem. 272, 14399–14403 (1997).
pubmed: 9162078
doi: 10.1074/jbc.272.22.14399
Kitagawa, H., Izumikawa, T., Uyama, T. & Sugahara, K. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem. 278, 23666–23671 (2003).
pubmed: 12716890
doi: 10.1074/jbc.M302493200
Toshikazu, Y. et al. Chondroitin sulfate synthase-2: molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. J. Biol. Chem. 278, 30235–30247 (2003).
doi: 10.1074/jbc.M303657200
Ogawa, H. et al. Chondroitin sulfate synthase-2 is necessary for chain extension of chondroitin sulfate but not critical for skeletal development. PLoS ONE 7, e43806 (2012).
pubmed: 22952769
pmcid: 3429490
doi: 10.1371/journal.pone.0043806
Fan, Y. H. et al. Lentivirus‑mediated knockdown of chondroitin polymerizing factor inhibits glioma cell growth in vitro. Oncol. Rep. 38, 1149–1155 (2017).
pubmed: 28627702
doi: 10.3892/or.2017.5731
Hou, X., Zhang, T., Da, Z. & Wu, X. CHPF promotes lung adenocarcinoma proliferation and anti-apoptosis via the MAPK pathway. Pathol. Res Pr. 215, 988–994 (2019).
doi: 10.1016/j.prp.2019.02.005
Saranga-Perry, V., Ambe, C., Zager, J. S. & Kudchadkar, R. R. Recent developments in the medical and surgical treatment of melanoma. CA Cancer J. Clinicians 64, 171–185 (2014).
doi: 10.3322/caac.21224
Choi, J. et al. A common intronic variant of PARP1 confers melanoma risk and mediates melanocyte growth via regulation of MITF. Nat. Genet. 49, 1326 (2017).
pubmed: 28759004
doi: 10.1038/ng.3927
Pérezguijarro, E. et al. Lineage-specific roles of the cytoplasmic polyadenylation factor CPEB4 in the regulation of melanoma drivers. Nat. Commun. 7, 13418 (2016).
doi: 10.1038/ncomms13418
Long, G. V. et al. Prognostic and clinicopathologic associations of oncogenic BRAF in metastatic melanoma. J. Clin. Oncol. 29, 1239–1246 (2011).
pubmed: 21343559
doi: 10.1200/JCO.2010.32.4327
Liu, R. et al. Identification of FLOT2 as a novel target for microRNA-34a in melanoma. J. Cancer Res. Clin. Oncol. 141, 1–14 (2015).
pubmed: 24889505
doi: 10.1007/s00432-014-1708-1
Carvajal, R. D. et al. KIT as a therapeutic target in metastatic melanoma. J. Invest. Dermatol. 130, 2169–72. (2010).
doi: 10.1038/jid.2010.205
Sosman, J. A. et al. Survival in BRAF V600–mutant advanced melanoma treated with vemurafenib. N. Engl. J. Med. 366, 707–714 (2016).
doi: 10.1056/NEJMoa1112302
Mcarthur, G. A. et al. Safety and efficacy of vemurafenib in BRAFV600E and BRAFV600K mutation-positive melanoma (BRIM-3): extended follow-up of a phase 3, randomised, open-label study. Lancet Oncol. 15, 323–332 (2014).
pubmed: 24508103
pmcid: 4382632
doi: 10.1016/S1470-2045(14)70012-9
Hofmann, U. B., Kauczok-Vetter, C. S., Houben, R. & Becker, J. C. Overexpression of the KIT/SCF in uveal melanoma does not translate into clinical efficacy of imatinib mesylate. Clin. Cancer Res. 15, 324–329 (2009).
pubmed: 19118061
doi: 10.1158/1078-0432.CCR-08-2243
Xu, S. et al. CXCR7 promotes melanoma tumorigenesis via Src kinase signaling. Cell Death Dis. 10, 191 (2019).
pubmed: 30804329
pmcid: 6389959
doi: 10.1038/s41419-019-1442-3
Sagwal, S. K., Pasqual-Melo, G., Bodnar, Y., Gandhirajan, R. K. & Bekeschus, S. Combination of chemotherapy and physical plasma elicits melanoma cell death via upregulation of SLC22A16. Cell Death Dis. 9, 1179 (2018).
pubmed: 30518936
pmcid: 6281583
doi: 10.1038/s41419-018-1221-6
Hou X., Zhang T., Da Z., Wu X. CHPF promotes lung adenocarcinoma proliferation and anti-apoptosis via the MAPK pathway. Pathol. Res. Pract. https://doi.org/10.1016/j.prp.2019.02.005 (2019).
Kalathas, D. et al. Chondroitin synthases I, II, III and chondroitin sulfate glucuronyltransferase expression in colorectal cancer. Mol. Med Rep. 4, 363 (2011).
pubmed: 21468578
Kalathas, D. et al. The chondroitin/dermatan sulfate synthesizing and modifying enzymes in laryngeal cancer: expressional and epigenetic studies. Head. Neck Oncol. 2, 27 (2010).
pubmed: 20929582
pmcid: 2958872
doi: 10.1186/1758-3284-2-27
Dmitri, T. et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin. Cancer Res. 11, 7234–7242 (2005).
doi: 10.1158/1078-0432.CCR-05-0683
Raskin, L. et al. Transcriptome profiling identifies HMGA2 as a biomarker of melanoma progression and prognosis. J. Invest. Dermatol. 133, 2585–92. (2013).
pubmed: 23633021
pmcid: 4267221
doi: 10.1038/jid.2013.197
Wicklein, D. et al. CEACAM1 promotes melanoma metastasis and is involved in the regulation of the EMT associated gene network in melanoma cells. Sci. Rep. 8, 11893 (2018).
pubmed: 30089785
pmcid: 6082866
doi: 10.1038/s41598-018-30338-4
Yi, Y. et al. EMT-related transcription factor snail up-regulates FAPα in malignant melanoma cells. Exp. Cell Res. 364, 160–167 (2018).
pubmed: 29410133
doi: 10.1016/j.yexcr.2018.01.039
Pearlman, R. L., De Oca, Mk. Montes, Pal, H. C. & Afaq, F. Potential therapeutic targets of epithelial-mesenchymal transition in melanoma. Cancer Lett. 391, 125–40. (2017).
pubmed: 28131904
pmcid: 5371401
doi: 10.1016/j.canlet.2017.01.029
Kosnopfel, C. et al. YB-1 expression and phosphorylation regulate tumorigenicity and invasiveness in melanoma by influencing EMT. Mol. Cancer Res. 16, 1149 (2018).
pubmed: 29743296
doi: 10.1158/1541-7786.MCR-17-0528
Lim, S. & Kaldis, P. Cdks, cyclins and CKIs: roles beyond cell cycle regulation. Development 140, 3079–3093 (2013).
pubmed: 23861057
doi: 10.1242/dev.091744
Malumbres, M. & Barbacid, M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9, 153–166 (2009).
pubmed: 19238148
doi: 10.1038/nrc2602
Gubern, A. et al. The N-terminal phosphorylation of RB by p38 bypasses its inactivation by CDKs and prevents proliferation in cancer cells. Mol. Cell 64, 25–36 (2016).
pubmed: 27642049
doi: 10.1016/j.molcel.2016.08.015
Gavet, O. & Pines, J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533–543 (2010).
pubmed: 20412769
pmcid: 3325599
doi: 10.1016/j.devcel.2010.02.013
Harley, M. E., Allan, L. A., Sanderson, H. S. & Clarke, P. R. Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest. EMBO J. 29, 2407–2420 (2014).
doi: 10.1038/emboj.2010.112
Johnson, N. et al. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat. Med. 17, 875–882 (2011).
pubmed: 21706030
pmcid: 3272302
doi: 10.1038/nm.2377
Hsieh, J. C. et al. Spontaneous regression of human cancer cells in vitro: potential role of disruption of Cdk1/Cdk4 co-expression. Anticancer Res. 29, 1933–1941 (2009).
Saatci, Ö. et al. Targeting PLK1 overcomes T-DM1 resistance via CDK1-dependent phosphorylation and inactivation of Bcl-2/xL in HER2-positive breast cancer. Oncogene 37, 2251–69. (2018).
pubmed: 29391599
doi: 10.1038/s41388-017-0108-9
Lu, M. et al. Restoring p53 function in human melanoma cells by inhibiting MDM2 and cyclin B1/CDK1-phosphorylated nuclear iASPP. Cancer Cell 23, 618–633 (2013).
pubmed: 23623661
doi: 10.1016/j.ccr.2013.03.013
Ravindran, M. D. et al. CDK1 interacts with Sox2 and promotes tumor initiation in human melanoma. Cancer Res. 78, 6561 (2018).
doi: 10.1158/0008-5472.CAN-18-0330