Dynamic interplay between sortilin and syndecan-1 contributes to prostate cancer progression.

Male Humans Prostatic Neoplasms Prostate Syndecan-1 / genetics Androgen Antagonists Androgens Integrin beta3 Neoplastic Processes

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
18 08 2023
Historique:
received: 15 03 2023
accepted: 09 08 2023
medline: 21 8 2023
pubmed: 19 8 2023
entrez: 18 8 2023
Statut: epublish

Résumé

Prostate cancer (PCa) development and progression relies on the programming of glucose and lipid metabolism, and this involves alterations in androgen receptor expression and signalling. Defining the molecular mechanism that underpins this metabolic programming will have direct significance for patients with PCa who have a poor prognosis. Here we show that there is a dynamic balance between sortilin and syndecan-1, that reports on different metabolic phenotypes. Using tissue microarrays, we demonstrated by immunohistochemistry that sortilin was highly expressed in low-grade cancer, while syndecan-1 was upregulated in high-grade disease. Mechanistic studies in prostate cell lines revealed that in androgen-sensitive LNCaP cells, sortilin enhanced glucose metabolism by regulating GLUT1 and GLUT4, while binding progranulin and lipoprotein lipase (LPL) to limit lipid metabolism. In contrast, in androgen-insensitive PC3 cells, syndecan-1 was upregulated, interacted with LPL and colocalised with β

Identifiants

DOI: 10.1038/s41598-023-40347-7 PMID: 37596305 PMC: PMC10439187
pubmed: 37596305
doi: 10.1038/s41598-023-40347-7
pii: 10.1038/s41598-023-40347-7
pmc: PMC10439187
doi:

Substances chimiques

sortilin Z020Y8WIJ4
Syndecan-1 0
Androgen Antagonists 0
Androgens 0
Integrin beta3 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

13489

Informations de copyright

© 2023. Springer Nature Limited.

Références

Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).
doi: 10.3322/caac.21660 pubmed: 33538338
Tolkach, Y. & Kristiansen, G. The heterogeneity of prostate cancer: A practical approach. Pathobiology 85, 108–116 (2018).
pubmed: 29393241 doi: 10.1159/000477852
Rebello, R. J. et al. Prostate cancer. Nat. Rev. Dis. Primers 7, 1–27 (2021).
doi: 10.1038/s41572-020-00243-0
Giunchi, F., Fiorentino, M. & Loda, M. The metabolic landscape of prostate cancer. Eur. Urol. Oncol. 2, 28–36 (2019).
pubmed: 30929843 doi: 10.1016/j.euo.2018.06.010
Tennakoon, J. B. et al. Androgens regulate prostate cancer cell growth via an AMPK-PGC-1α-mediated metabolic switch. Oncogene 33, 5251–5261 (2014).
pubmed: 24186207 doi: 10.1038/onc.2013.463
Scaglia, N., Frontini-Loper, Y. R. & Zarda, G. Prostate cancer progression: As a matter of Fats. Front. Oncol. 11, 719865 (2021).
pubmed: 34386430 pmcid: 8353450 doi: 10.3389/fonc.2021.719865
Butler, L. M., Centenera, M. M. & Swinnen, J. V. Androgen control of lipid metabolism in prostate cancer: Novel insights and future applications. Endocr.-Relat. Cancer 23, R219–R227. https://doi.org/10.1530/ERC-15-0556 (2016).
doi: 10.1530/ERC-15-0556 pubmed: 27130044
Volti, G. L. et al. Glucose metabolism in the progression of prostate cancer. Front. Physiol. 8, 97 (2017).
Jeger, J. L. Endosomes, lysosomes, and the role of endosomal and lysosomal biogenesis in cancer development. Mol. Biol. Rep. 47, 9801–9810. https://doi.org/10.1007/s11033-020-05993-4 (2020).
doi: 10.1007/s11033-020-05993-4 pubmed: 33185829
Johnson, I. A. R. D. et al. Altered endosome biogenesis in prostate cancer has biomarker. Mol. Cancer Res. 12, 1851–1862 (2014).
pubmed: 25080433 pmcid: 4757910 doi: 10.1158/1541-7786.MCR-14-0074
Johnson, I. R. D. et al. Endosomal gene expression: A new indicator for prostate cancer patient prognosis?. Oncotarget 6, 37919–37929 (2015).
pubmed: 26473288 pmcid: 4741974 doi: 10.18632/oncotarget.6114
Martini, C. et al. Aberrant protein expression of Appl1, Sortilin and Syndecan-1 during the biological progression of prostate cancer. Pathology 55, 40–51 (2022).
pubmed: 36089417 doi: 10.1016/j.pathol.2022.08.001
Ghaemimanesh, F., Mehravar, M., Milani, S., Poursani, E. M. & Saliminejad, K. The multifaceted role of sortilin/neurotensin receptor 3 in human cancer development. J. Cell Physiol. 236, 6271–6281 (2021).
pubmed: 33634506 doi: 10.1002/jcp.30344
Gharbaran, R. Advances in the molecular functions of syndecan-1 (SDC1/CD138) in the pathogenesis of malignancies. Crit. Rev. Oncol. Hematol. 94, 1–17 (2015).
pubmed: 25563413 doi: 10.1016/j.critrevonc.2014.12.003
Willnow, T. E., Kjølby, M. & Nykjaer, A. Sortilins: New players in lipoprotein metabolism. Curr. Opin. Lipidol. 22, 79–85 (2011).
pubmed: 21124217 doi: 10.1097/MOL.0b013e3283416f2b
Talbot, H. et al. Regulatory roles of sortilin and sorla in immune-related processes. Front. Pharmacol. 9, 1507. https://doi.org/10.3389/fphar.2018.01507 (2019).
doi: 10.3389/fphar.2018.01507 pubmed: 30666202 pmcid: 6330335
Gustafsen, C. et al. Heparan sulfate proteoglycans present PCSK9 to the LDL receptor. Nat. Commun. 8, 503 (2017).
pubmed: 28894089 pmcid: 5593881 doi: 10.1038/s41467-017-00568-7
Logan, J. M. et al. Prediction of prostate cancer biochemical and clinical recurrence is improved by IHC-assisted grading using Appl1, Sortilin and Syndecan-1. Cancers 15, 3215 (2023).
pubmed: 37370825 pmcid: 10296524 doi: 10.3390/cancers15123215
Ouyang, S., Jia, B., Xie, W., Yang, J. & Lv, Y. Mechanism underlying the regulation of sortilin expression and its trafficking function. J. Cell. Physiol. 235, 8958–8971. https://doi.org/10.1002/jcp.29818 (2020).
doi: 10.1002/jcp.29818 pubmed: 32474917
Moya, L. et al. Characterisation of cell lines derived from prostate cancer patients with localised disease. Prostate Cancer Prostatic Dis. https://doi.org/10.1038/s41391-023-00679-x (2023).
doi: 10.1038/s41391-023-00679-x pubmed: 37264224 pmcid: 10449630
Szklarczyk, D. et al. The STRING database in 2021: Customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 49, D605–D612 (2021).
pubmed: 33237311 doi: 10.1093/nar/gkaa1074
Kandror, K. V. The role of sortilin in the “Glut4 Pathway”. Commun. Integr. Biol. 11, e1393592 (2018).
doi: 10.1080/19420889.2017.1393592
Logette, E. et al. A Machine-generated view of the role of blood glucose levels in the severity of COVID-19. Front. Public Health 9, 1–53 (2021).
doi: 10.3389/fpubh.2021.695139
Klip, A., McGraw, T. E. & James, D. E. Thirty sweet years of GLUT4. J. Biol. Chem. 294, 11369–11381 (2019).
pubmed: 31175156 pmcid: 6663870 doi: 10.1074/jbc.REV119.008351
Nielsen, M. S., Jacobsen, C., Olivecrona, G., Gliemann, J. & Petersen, C. M. Sortilin/Neurotensin receptor-3 binds and mediates degradation of lipoprotein lipase. J. Biol. Chem. 274, 8832–8836 (1999).
pubmed: 10085125 doi: 10.1074/jbc.274.13.8832
Tanimoto, R. et al. The perlecan-interacting growth factor progranulin regulates ubiquitination, sorting, and lysosomal degradation of sortilin. Matrix Biol. 64, 27–39 (2017).
pubmed: 28433812 pmcid: 7038787 doi: 10.1016/j.matbio.2017.04.001
Kuemmerle, N. B. et al. Lipoprotein lipase links dietary fat to solid tumor cell proliferation. Mol. Cancer Ther. 10, 427–436 (2011).
pubmed: 21282354 pmcid: 3074101 doi: 10.1158/1535-7163.MCT-10-0802
Gunn, K. H. et al. The structure of helical lipoprotein lipase reveals an unexpected twist in lipase storage. Proc. Natl. Acad. Sci. U S A 117, 10254–10264 (2020).
pubmed: 32332168 pmcid: 7229681 doi: 10.1073/pnas.1916555117
Sundberg, E. L., Deng, Y. & Burd, C. G. Syndecan-1 mediates sorting of soluble lipoprotein lipase with sphingomyelin-rich membrane in the golgi apparatus. Dev. Cell 51, 387-398.e4 (2019).
pubmed: 31543446 pmcid: 6832887 doi: 10.1016/j.devcel.2019.08.014
Matsui, M. et al. Activation of LDL receptor expression by small RNAs complementary to a noncoding transcript that overlaps the LDLR promoter. Chem. Biol. 17, 1344–1355 (2010).
pubmed: 21168770 pmcid: 3071588 doi: 10.1016/j.chembiol.2010.10.009
Banerjee, S. et al. Proteolysis of the low density lipoprotein receptor by bone morphogenetic protein-1 regulates cellular cholesterol uptake. Sci. Rep. 9, 11416 (2019).
pubmed: 31388055 pmcid: 6684651 doi: 10.1038/s41598-019-47814-0
Tang, L., Xu, M., Zhang, L., Qu, L. & Liu, X. Role of αvβ3 in prostate cancer: Metastasis initiator and important therapeutic target. Oncol. Targets Ther. 13, 7411–7422 (2020).
doi: 10.2147/OTT.S258252
Stepp, M. A., Pal-Ghosh, S., Tadvalkar, G. & Pajoohesh-Ganji, A. Syndecan-1 and its expanding list of contacts. Adv. Wound Care (New Rochelle) 4, 235–249 (2015).
pubmed: 25945286 doi: 10.1089/wound.2014.0555
Manon-Jensen, T., Multhaupt, H. A. B. & Couchman, J. R. Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J. 280, 2320–2331 (2013).
pubmed: 23384311 doi: 10.1111/febs.12174
Vaz, C. V. et al. Androgens enhance the glycolytic metabolism and lactate export in prostate cancer cells by modulating the expression of GLUT1, GLUT3, PFK, LDH and MCT4 genes. J. Cancer Res. Clin. Oncol 142, 5–16 (2016).
pubmed: 26048031 doi: 10.1007/s00432-015-1992-4
White, M. A. et al. GLUT12 promotes prostate cancer cell growth and is regulated by androgens and CaMKK2 signaling. Endocr. Relat. Cancer 25, 453–469 (2018).
pubmed: 29431615 pmcid: 5831527 doi: 10.1530/ERC-17-0051
Wang, J. et al. GLUT1 is an AR target contributing to tumor growth and glycolysis in castration-resistant and enzalutamide-resistant prostate cancers. Cancer Lett. 485, 45–55 (2020).
pubmed: 32428663 doi: 10.1016/j.canlet.2020.05.007
Kaddai, V., Le Marchand-Brustel, Y. & Cormont, M. Rab proteins in endocytosis and Glut4 trafficking. Acta Physiol. 192, 75–88 (2008).
doi: 10.1111/j.1748-1716.2007.01787.x
Li, Z. Y. et al. Visualization of GLUT1 trafficking in live cancer cells by the use of a dual-fluorescence reporter. ACS Omega 5, 15911–15921 (2020).
pubmed: 32656411 pmcid: 7345384 doi: 10.1021/acsomega.0c01054
Long, W. & Cheeseman, C. I. Structure of, and functional insight into the GLUT family of membrane transporters. Cell Health Cytoskelet. 7, 167–183. https://doi.org/10.2147/CHC.S60484 (2015).
doi: 10.2147/CHC.S60484
Chen, H. et al. The PI3K/AKT pathway in the pathogenesis of prostate cancer. Front. Biosci. 21, 1084–1091 (2016).
doi: 10.2741/4443
Chen, X. et al. Constitutively active Akt is an important regulator of TRAIL sensitivity in prostate cancer. Oncogene 20, 6073–6083 (2001).
pubmed: 11593415 doi: 10.1038/sj.onc.1204736
Massie, C. E. et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 30, 2719–2733 (2011).
pubmed: 21602788 pmcid: 3155295 doi: 10.1038/emboj.2011.158
Henriques, A. F. A. et al. WNK1 phosphorylation sites in TBC1D1 and TBC1D4 modulate cell surface expression of GLUT1. Arch. Biochem. Biophys. 679, 108223 (2020).
pubmed: 31816312 doi: 10.1016/j.abb.2019.108223
Tanimoto, R. et al. Sortilin regulates progranulin action in castration-resistant prostate cancer cells. Endocrinology 156, 58–70 (2015).
pubmed: 25365768 doi: 10.1210/en.2014-1590
Labbé, D. P. et al. High-fat diet fuels prostate cancer progression by rewiring the metabolome and amplifying the MYC program. Nat. Commun. 10, 12298 (2019).
doi: 10.1038/s41467-019-12298-z
Bruce, K. D., Tang, M., Reigan, P. & Eckel, R. H. Genetic variants of lipoprotein lipase and regulatory factors associated with Alzheimer’s disease risk. Int. J. Mol. Sci. 21, 1–15 (2020).
doi: 10.3390/ijms21218338
Beigneux, A. P. et al. Lipoprotein lipase is active as a monomer. Proc. Natl. Acad. Sci. U S A 116, 6319–6328 (2019).
pubmed: 30850549 pmcid: 6442593 doi: 10.1073/pnas.1900983116
Shimada, K. et al. Syndecan-1, a new target molecule involved in progression of androgen-independent prostate cancer. Cancer Sci. 100, 1248–1254 (2009).
pubmed: 19432893 doi: 10.1111/j.1349-7006.2009.01174.x
Costa-Pinheiro, P. et al. Role of SPTSSB-regulated de Novo sphingolipid synthesis in prostate cancer depends on androgen receptor signaling. iScience 23, 101855 (2020).
pubmed: 33313495 pmcid: 7721643 doi: 10.1016/j.isci.2020.101855
Prabhakaran, S. et al. The incidence of labelling of non-lung adenocarcinomas with antibodies against TTF-1 and diagnostic implications. Appl. Immunohistochem. Mol. Morphol. 28, 471–476 (2020).
pubmed: 31135446 doi: 10.1097/PAI.0000000000000775
Johnson, I. R. D. et al. A paradigm in immunochemistry, revealed by monoclonal antibodies to spatially distinct epitopes on syntenin-1. Int. J. Mol. Sci. 20, 6035 (2019).
pubmed: 31795513 pmcid: 6928784 doi: 10.3390/ijms20236035
Dunn, K. W., Kamocka, M. M. & McDonald, J. H. A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. 300, 723–742. https://doi.org/10.1152/ajpcell.00462.2010 (2011).
doi: 10.1152/ajpcell.00462.2010

Auteurs

Joanna Lazniewska (J)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia. joanna.lazniewska@unisa.edu.au.

Ka Lok Li (KL)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Ian R D Johnson (IRD)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Alexandra Sorvina (A)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Jessica M Logan (JM)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Carmela Martini (C)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Courtney Moore (C)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Ben S-Y Ung (BS)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Litsa Karageorgos (L)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Shane M Hickey (SM)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Sarita Prabhakaran (S)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.
Department of Anatomical Pathology, College of Medicine and Public Health, Flinders University, Bedford Park, SA, 5042, Australia.

Jessica K Heatlie (JK)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Robert D Brooks (RD)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Chelsea Huzzell (C)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia.

Nicholas I Warnock (NI)

Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, SA, 5000, Australia.

Mark P Ward (MP)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Bashir Mohammed (B)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Prerna Tewari (P)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Cara Martin (C)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Sharon O'Toole (S)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Laura Bogue Edgerton (LB)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Mark Bates (M)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Paul Moretti (P)

Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, SA, 5000, Australia.

Stuart M Pitson (SM)

Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, SA, 5000, Australia.

Stavros Selemidis (S)

School of Health and Biomedical Sciences, STEM College, RMIT University, Bundoora, VIC, 3083, Australia.

Lisa M Butler (LM)

South Australian ImmunoGENomics Cancer Institute and Freemasons Centre for Male Health and Wellbeing, University of Adelaide, Adelaide, SA, 5000, Australia.
Solid Tumour Program, Precision Cancer Medicine Theme, South Australian Health and Medical Research Institute, Adelaide, SA, 5000, Australia.

John J O'Leary (JJ)

Department of Histopathology, Trinity College Dublin, Dublin 8, Ireland.

Douglas A Brooks (DA)

Clinical and Health Sciences, University of South Australia, Adelaide, SA, 5000, Australia. doug.brooks@unisa.edu.au.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Dynamic interplay between sortilin and...
questionsmedicales.fr › Maladies urogénitales › Tumeurs de l'appareil urogénital › Tumeurs de l'appareil génital mâle › Tumeurs de la prostate › Dynamic interplay between sortilin and...
questionsmedicales.fr › Tissus › Glandes exocrines › Prostate › Dynamic interplay between sortilin and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Glycoprotéines membranaires › Syndécanes › Syndécane-1 › Dynamic interplay between sortilin and...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Effets physiologiques des médicaments › Hormones, substituts d'hormones et antagonistes d'hormones › Antihormones › Antagonistes des androgènes › Dynamic interplay between sortilin and...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Effets physiologiques des médicaments › Hormones, substituts d'hormones et antagonistes d'hormones › Hormones › Androgènes › Dynamic interplay between sortilin and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs immunologiques › Intégrines › Chaines bêta des intégrines › Intégrine bêta3 › Dynamic interplay between sortilin and...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Processus néoplasiques › Dynamic interplay between sortilin and...