3,071
Views
52
CrossRef citations to date
0
Altmetric
Research article

Triple knockdown of CDC37, HSP90-alpha and HSP90-beta diminishes extracellular vesicles-driven malignancy events and macrophage M2 polarization in oral cancer

, , , , , , , , , , , , , , , & ORCID Icon show all
Article: 1769373 | Received 01 Jul 2019, Accepted 04 May 2020, Published online: 31 May 2020

References

  • Thery C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.
  • Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–21.
  • van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018 Apr;19(4):213–228.
  • Seyama M, Yoshida K, Yoshida K, et al. Outer membrane vesicles of Porphyromonas gingivalis attenuate insulin sensitivity by delivering gingipains to the liver. Biochim Biophys Acta Mol Basis Dis. 2020 Feb 20;1866(6):1–12.
  • Okusha Y, Eguchi T, Tran MT, et al. Extracellular vesicles enriched with moonlighting metalloproteinase are highly transmissive, pro-tumorigenic, and trans-activates cellular communication network factor (CCN2/CTGF): CRISPR against cancer. Cancers (Basel). 2020;12(4):1–27.
  • Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015 Nov 19;527(7578):329–335.
  • Franzen CA, Blackwell RH, Todorovic V, et al. Urothelial cells undergo epithelial-to-mesenchymal transition after exposure to muscle invasive bladder cancer exosomes. Oncogenesis. 2015 Aug;17(4):e163.
  • Fujiwara T, Eguchi T, Sogawa C, et al. Carcinogenic epithelial-mesenchymal transition initiated by oral cancer exosomes is inhibited by anti-EGFR antibody cetuximab. Oral Oncol. 2018;86:251–257.
  • Clayton A, Turkes A, Navabi H, et al. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005 Aug 15;118(Pt 16):3631–3638.
  • Eguchi T, Sogawa C, Ono K, et al. Cell stress induced stressome release including damaged membrane vesicles and extracellular HSP90 by prostate cancer cells. Cells. 2020;9(3):1–24.
  • Eguchi T, Ono K, Kawata K. Regulatory roles of HSP90-Rich extracellular vesicles. In: Asea AAA and Kaur P, editors. heat shock protein 90 in human diseases and disorders. Heat shock proteins. Vol. 19. Cham, Swizerland: Springer Nature; 2019. p. 3–17.
  • Ono K, Eguchi T, Sogawa C, et al. HSP-enriched properties of extracellular vesicles involve survival of metastatic oral cancer cells. J Cell Biochem. 2018 Sep;119(9):7350–7373.
  • Eguchi T, Sogawa C, Okusha Y, et al. Organoids with cancer stem cell-like properties secrete exosomes and HSP90 in a 3D nanoenvironment. Plos One. 2018 Feb 7;13(2):e0191109.
  • Calderwood SK. Molecular cochaperones: tumor growth and cancer treatment. Scientifica (Cairo). 2013;2013:217513.
  • Neckers L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med. 2002;8(4 Suppl):S55–61.
  • Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005 Oct;5(10):761–772.
  • Taha EA, Ono K, Eguchi T. Roles of extracellular HSPs as biomarkers in immune surveillance and immune evasion [Review]. Int J Mol Sci. 2019 Sep 17;20(18):1–32.
  • Eustace BK, Sakurai T, Stewart JK, et al. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol. 2004 6;Jun(6):507–514.
  • Nolan KD, Franco OE, Hance MW, et al. Tumor-secreted Hsp90 subverts polycomb function to drive prostate tumor growth and invasion. J Biol Chem. 2015 Mar 27;290(13):8271–8282.
  • Hance MW, Dole K, Gopal U, et al. Secreted Hsp90 is a novel regulator of the epithelial to mesenchymal transition (EMT) in prostate cancer. J Biol Chem. 2012 Nov 02;287(45):37732–37744.
  • Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009 Jun;28(1–2):15–33.
  • Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008 May 16;133(4):704–715.
  • Fujiwara T, Eguchi T, Sogawa C, et al. Anti-EGFR antibody cetuximab is secreted by oral squamous cell carcinoma and alters EGF-driven mesenchymal transition. Biochem Biophys Res Commun. 2018;503(3):1267–1272. 2018 Available online 13 July.
  • Eguchi T, Taha EA, Calderwood SK, et al. A novel model of cancer drug resistance: oncosomal release of cytotoxic and antibody-based drugs [Review]. Biology (Basel). 2020 Mar 5;9(3):1–22.
  • Zheng X, Carstens JL, Kim J, et al. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015 Nov 26;527(7579):525–530.
  • Nieto MA, Huang RY, Jackson RA, et al. Emt: 2016. Cell. 2016 Jun 30;166(1):21–45.
  • Blackwell RH, Foreman KE, Gupta GN. The role of cancer-derived exosomes in tumorigenicity & epithelial-to-mesenchymal transition. Cancers (Basel). 2017. 10. 9(8):Aug.
  • Gray PJ, Prince T, Cheng J, et al. Targeting the oncogene and kinome chaperone CDC37. Nat Rev Cancer. 2008;8:491–495.
  • Gray PJ Jr., Stevenson MA, Calderwood SK. Targeting Cdc37 inhibits multiple signaling pathways and induces growth arrest in prostate cancer cells. Cancer Res. 2007 Dec 15;67(24):11942–11950.
  • Calderwood SK. Cdc37 as a co-chaperone to Hsp90. Subcell Biochem. 2015;78:103–112.
  • Kimura Y, Rutherford SL, Miyata Y, et al. Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Dev. 1997;11:1775–1785.
  • Roe SM, Ali MMU, Meyer P, et al. The mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50 cdc37. Cell. 2004;116:87–98.
  • Chua HL, Bhat-Nakshatri P, Clare SE, et al. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene. 2007 Feb 01;26(5):711–724.
  • Wu Y, Deng J, Rychahou PG, et al. Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion. Cancer Cell. 2009 May 05;15(5):416–428.
  • Li CW, Xia W, Huo L, et al. Epithelial-mesenchymal transition induced by TNF-alpha requires NF-kappaB-mediated transcriptional upregulation of Twist1. Cancer Res. 2012 Mar 01;72(5):1290–1300.
  • Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011 Oct 14;11(11):723–737.
  • Lan J, Sun L, Xu F, et al. M2 macrophage-derived exosomes promote cell migration and invasion in colon cancer. Cancer Res. 2019 Jan 1;79(1):146–158.
  • Wang X, Luo G, Zhang K, et al. Hypoxic tumor-derived exosomal miR-301a mediates M2 macrophage polarization via PTEN/PI3Kgamma to promote pancreatic cancer metastasis. Cancer Res. 2018 Aug 15;78(16):4586–4598.
  • Zheng P, Chen L, Yuan X, et al. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res. 2017 Apr 13;36(1):53.
  • Taha EA, Lu Y, Eguchi T. Exosomes“The little thing that matter the most”in tumor immunology and microenvironment. In: kagiya T, editor. Exosomes and microvesicles: role in disease and clinical applications. Hauppauge, New York: Nova Science Publishers; 2020.
  • Wang F, Li B, Wei Y, et al. Tumor-derived exosomes induce PD1(+) macrophage population in human gastric cancer that promotes disease progression. Oncogenesis. 2018 May 25;7(5):41.
  • Pirila E, Vayrynen O, Sundquist E, et al. Macrophages modulate migration and invasion of human tongue squamous cell carcinoma. PLoS One. 2015;10(3):e0120895.
  • Ono K, Eguchi T, Sogawa C, et al. HSP-enriched properties of extracellular vesicles involve survival of metastatic oral cancer cells. J Cell Biochem. 2018 May 16;119(9):7350–7362.
  • Eguchi T, Prince TL, Tran MT, et al. MZF1 and SCAND1 Reciprocally Regulate CDC37 Gene Expression in Prostate Cancer. Cancers (Basel). 2019 Jun 8;11(6):1–15.
  • Namba Y, Sogawa C, Okusha Y, et al. Depletion of lipid efflux pump ABCG1 triggers the intracellular accumulation of extracellular vesicles and reduces aggregation and tumorigenesis of metastatic cancer cells. Front Oncol. 2018;8(376):1–16.
  • Taha EA, Sogawa C, Okusha Y, et al. Knockout of MMP3 weakens solid tumor organoids and cancer extracellular vesicles. Cancers, in press.
  • Lai CP, Kim EY, Badr CE, et al. Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat Commun. 2015 May;13(6):7029.
  • Lai CP, Mardini O, Ericsson M, et al. Dynamic biodistribution of extracellular vesicles in vivo using a multimodal imaging reporter. ACS Nano. 2014 Jan 28;8(1):483–494.
  • Eguchi T, Kubota S, Kawata K, et al. Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol Cell Biol. 2008 Apr;28(7):2391–2413.
  • Arai K, Eguchi T, Rahman MM, et al. A novel high-throughput 3D screening system for EMT inhibitors: a pilot screening discovered the EMT inhibitory activity of CDK2 inhibitor SU9516. PLoS One. 2016;11(9):e0162394.
  • Sogawa C, Eguchi T, Tran MT, et al. Antiparkinson drug benztropine suppresses tumor growth, circulating tumor cells, and metastasis by acting on SLC6A3/DAT and reducing STAT3. Cancers (Basel). 2020;12(2):1–22.
  • Sogawa C, Eguchi T, Okusha Y, et al. A reporter system evaluates tumorigenesis, metastasis, beta-catenin/MMP regulation, and druggability. Tissue Eng Part A. 2019 Feb 8;25(19–20):1413–1425.
  • Yoshida S, Kawai H, Eguchi T, et al. Tumor angiogenic inhibition triggered necrosis (TAITN) in oral cancer. Cells. 2019 Jul 22;8(7):1–15.
  • Okusha Y, Eguchi T, Sogawa C, et al. The intranuclear PEX domain of MMP involves proliferation, migration, and metastasis of aggressive adenocarcinoma cells. J Cell Biochem. 2018 Sep;119(9):7363–7376.
  • Eguchi T, Sogawa C, Ono K, et al. CDC37 and HSP90 are essential for stressome release and tumor progression in resistant prostate cancer. 11 February 2020 by MDPI (Preprints). doi:10.20944/preprints202002.0148.v1.
  • Litvinov SV, Velders MP, Bakker HA, et al. Ep-CAM: a human epithelial antigen is a homophilic cell-cell adhesion molecule. J Cell Biol. 1994 Apr;125(2):437–446.
  • Munz M, Baeuerle PA, Gires O. The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res. 2009 Jul 15;69(14):5627–5629.
  • Zona L, Tawar RG, Zeisel MB, et al. CD81-receptor associations–impact for hepatitis C virus entry and antiviral therapies. Viruses. 2014 Feb 18;6(2):875–892.
  • van Niel G, Charrin S, Simoes S, et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell. 2011 Oct 18;21(4):708–721.
  • Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009 May 15;315(9):1584–1592.
  • Li W, Li Y, Guan S, et al. Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. Embo J. 2007 Mar 7;26(5):1221–1233.
  • de la Mare JA, Jurgens T, Edkins AL. Extracellular Hsp90 and TGFbeta regulate adhesion, migration and anchorage independent growth in a paired colon cancer cell line model. BMC Cancer. 2017 Mar 16;17(1):202.
  • Capaldo CT, Nusrat A. Claudin switching: physiological plasticity of the Tight Junction. Semin Cell Dev Biol. 2015 Jun;42:22–29.
  • Le Naour F, Zoller M. The tumor antigen EpCAM: tetraspanins and the tight junction protein claudin-7, new partners, new functions. Front Biosci. 2008 May 1;13:5847–5865.
  • Luo Y, Zhou H, Krueger J, et al. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest. 2006 Aug;116(8):2132–2141.
  • Sung BH, Ketova T, Hoshino D, et al. Directional cell movement through tissues is controlled by exosome secretion. Nat Commun. 2015 May;13(6):7164.
  • Ham S, Lima LG, Chai EPZ, et al. Breast cancer-derived exosomes alter macrophage polarization via gp130/STAT3 Signaling. Front Immunol. 2018;9:871.
  • Kanlikilicer P, Bayraktar R, Denizli M, et al. Exosomal miRNA confers chemo resistance via targeting Cav1/p-gp/M2-type macrophage axis in ovarian cancer. EBioMedicine. 2018;38:100–112.
  • de Vrij J, Maas SL, Kwappenberg KM, et al. Glioblastoma-derived extracellular vesicles modify the phenotype of monocytic cells. Int J Cancer. 2015 Oct 1;137(7):1630–1642.
  • Fujii N, Shomori K, Shiomi T, et al. Cancer-associated fibroblasts and CD163-positive macrophages in oral squamous cell carcinoma: their clinicopathological and prognostic significance. J Oral Pathol Med. 2012 Jul;41(6):444–451.
  • Calderwood SK, Gong J, Murshid A. Extracellular HSPs: the Complicated Roles of Extracellular HSPs in Immunity. Front Immunol. 2016;7:159.
  • Murshid A, Gong J, Calderwood SK. Hsp90-peptide complexes stimulate antigen presentation through the class II pathway after binding scavenger receptor SREC-I. Immunobiology. 2014 Dec;219(12):924–931.
  • Furuta K, Eguchi T. Roles of heat shock proteins on antigen presentation. In: Asea AAA, Kaur P, editors. Heat shock proteins in cancer therapeutics. heat shock proteins. 2020, in press. Cham, Switzerland: Springer Nature.
  • Udono H, Srivastava PK. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J Immunol. 1994 Jun 1;152(11):5398–5403.
  • Basu S, Binder RJ, Ramalingam T, et al. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity. 2001 Mar;14(3):303–313.
  • Murshid A, Gong J, Calderwood SK. Heat shock protein 90 mediates efficient antigen cross presentation through the scavenger receptor expressed by endothelial cells-I. J Immunol. 2010 Sep 1;185(5):2903–2917.
  • Murshid A, Borges TJ, Bonorino C, et al. Immunological outcomes mediated upon binding of heat shock proteins to scavenger receptors SCARF1 and LOX-1, and endocytosis by mononuclear phagocytes. Front Immunol. 2019;10:3035.
  • Saha B, Momen-Heravi F, Furi I, et al. Extracellular vesicles from mice with alcoholic liver disease carry a distinct protein cargo and induce macrophage activation through heat shock protein 90. Hepatology. 2018 May;67(5):1986–2000.
  • Hemler ME. Tetraspanin proteins promote multiple cancer stages. Nat Rev Cancer. 2014 Jan;14(1):49–60.
  • Charrin S, Jouannet S, Boucheix C, et al. Tetraspanins at a glance. J Cell Sci. 2014 Sep 1;127(Pt 17):3641–3648.