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Original Research

Suppression of prostate cancer and amelioration of the immunosuppressive tumor microenvironment through selective immunoproteasome inhibition

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Article: 2156091 | Received 24 Feb 2022, Accepted 02 Dec 2022, Published online: 15 Dec 2022

References

  • de Bono JS, Guo C, Gurel B, De Marzo AM, Sfanos KS, Mani RS, Gil J, Drake CG, Alimonti A. Prostate carcinogenesis: inflammatory storms. Nat Rev Cancer. 2020;20(8):455–14. doi:10.1038/s41568-020-0267-9.
  • Sfanos KS, Yegnasubramanian S, Nelson WG, De Marzo AM. The inflammatory microenvironment and microbiome in prostate cancer development. Nat Rev Urol. 2018;15:11–24.
  • Zhang Q, Liu S, Zhang Q, Xiong Z, Wang AR, Myers L, et al. Interleukin-17 promotes development of castration-resistant prostate cancer potentially through creating an immunotolerant and pro-angiogenic tumor microenvironment. Prostate. 2014;74:869–879.
  • Zhang Q, Liu S, Ge D, Cunningham DM, Huang F, Ma L, et al. Targeting Th17-IL-17 pathway in prevention of micro-invasive prostate cancer in a mouse model. Prostate. 2017;77:888–899.
  • Sfanos KS, Bruno TC, Maris CH, Xu L, Thoburn CJ, DeMarzo AM, et al. Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin Cancer Res: an Offl J Am Assoc Cancer Res. 2008;14:3254–3261.
  • Derhovanessian E, Adams V, Hahnel K, Groeger A, Pandha H, Ward S, et al. Pretreatment frequency of circulating IL-17+ CD4+ T-cells, but not Tregs, correlates with clinical response to whole-cell vaccination in prostate cancer patients. Int J Cancer. 2009;125:1372–1379.
  • Garcia AJ, Ruscetti M, Arenzana TL, Tran LM, Bianci-Frias D, Sybert E, et al. Pten null prostate epithelium promotes localized myeloid-derived suppressor cell expansion and immune suppression during tumor initiation and progression. Mol Cell Biol. 2014;34:2017–2028.
  • Lorente D, Mateo J, Templeton AJ, Zafeiriou Z, Bianchini D, Ferraldeschi R, et al. Baseline neutrophil-lymphocyte ratio (NLR) is associated with survival and response to treatment with second-line chemotherapy for advanced prostate cancer independent of baseline steroid use. Ann Oncol. 2015;26:750–755.
  • Calcinotto A, Spataro C, Zagato E, Di Mitri D, Gil V, Crespo M, et al. IL-23 secreted by myeloid cells drives castration-resistant prostate cancer. Nature. 2018;559:363–369.
  • Collins GA, Goldberg AL. The logic of the 26S proteasome. Cell. 2017;169:792–806.
  • Muchamuel T, Basler M, Aujay MA, Suzuki E, Kalim KW, Lauer C, et al. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat Med. 2009;15:781–787.
  • Groettrup M, Kirk CJ, Basler M. Proteasomes in immune cells: more than peptide producers? Nat Rev Immunol. 2010;10:72–77.
  • Basler M, Mundt S, Muchamuel T, Moll C, Jiang J, Groettrup M, et al. Inhibition of the immunoproteasome ameliorates experimental autoimmune encephalomyelitis. EMBO Mol Med. 2014;6:226–238.
  • Basler M, Dajee M, Moll C, Groettrup M, Kirk CJ. Prevention of experimental colitis by a selective inhibitor of the immunoproteasome. J Immunol. 2010;185:634–641.
  • Basler M, Claus M, Klawitter M, Goebel H, Groettrup M. Immunoproteasome inhibition selectively kills human CD14(+) monocytes and as a result dampens IL-23 secretion. J Immunol. 2019;203:1776–1785.
  • Basler M, Lindstrom MM, LaStant JJ, Bradshaw JM, Owens TD, Schmidt C, et al. Co-inhibition of immunoproteasome subunits LMP2 and LMP7 is required to block autoimmunity. EMBO Rep. 2018;19.
  • Koerner J, Brunner T, Groettrup M. Inhibition and deficiency of the immunoproteasome subunit LMP7 suppress the development and progression of colorectal carcinoma in mice. Oncotarget. 2017;8:50873–50888.
  • Vachharajani N, Joeris T, Luu M, Hartmann S, Pautz S, Jenike E, et al. Prevention of colitis-associated cancer by selective targeting of immunoproteasome subunit LMP7. Oncotarget. 2017;8:50447–50459.
  • Li N, Grivennikov SI, Karin M. The unholy trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell. 2011;19:429–431.
  • Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MJ, et al. Metastatic prostate cancer in a transgenic mouse. Cancer Res. 1996;56:4096–4102.
  • Fehling HJ, Swat W, Laplace C, Kuehn R, Rajewsky K, Mueller U, et al. MHC class I expression in mice lacking proteasome subunit LMP-7. Science. 1994;265:1234–1237.
  • Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A. 1995;92:3439–3443.
  • Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Meth. 1999;223:77–92.
  • Berman-Booty LD, Sargeant AM, Rosol TJ, Rengel RC, Clinton SK, Chen CS, et al. A review of the existing grading schemes and a proposal for a modified grading scheme for prostatic lesions in TRAMP mice. Toxicol Pathol. 2012;40:5–17.
  • Wikström P, Lindahl C, Bergh A. Characterization of the autochthonous transgenic adenocarcinoma of the mouse prostate (TRAMP) as a model to study effects of castration therapy. Prostate. 2005;62:148–164.
  • Li J, Koerner J, Basler M, Brunner T, Kirk CJ, Groettrup M. Immunoproteasome inhibition induces plasma cell apoptosis and preserves kidney allografts by activating the unfolded protein response and suppressing plasma cell survival factors. Kidney Int. 2019;95:611–623.
  • Kaplan-Lefko PJ, Chen TM, Ittmann MM, Barrios RJ, Ayala GE, Huss WJ, et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003;55:219–237.
  • Hossain DM, Pal SK, Moreira D, Duttagupta P, Zhang Q, Won H, et al. TLR9-targeted STAT3 silencing abrogates immunosuppressive activity of myeloid-derived suppressor cells from prostate cancer patients. Clin Cancer Res: an Offl J Am Assoc Cancer Res. 2015;21:3771–3782.
  • Comito G, Giannoni E, Segura CP, Barcellos-de-Souza P, Raspollini MR, Baroni G, et al. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene. 2014;33:2423–2431.
  • Nonomura N, Takayama H, Nakayama M, Nakai Y, Kawashima A, Mukai M, et al. Infiltration of tumour-associated macrophages in prostate biopsy specimens is predictive of disease progression after hormonal therapy for prostate cancer. BJU Int. 2011;107:1918–1922.
  • Gingrich JR, Barrios RJ, Kattan MW, Nahm HS, Finegold MJ, Greenberg NM. Androgen-independent prostate cancer progression in the TRAMP model. Cancer Res. 1997;57:4687–4691.
  • Chiaverotti T, Couto SS, Donjacour A, Mao JH, Nagase H, Cardiff RD, et al. Dissociation of epithelial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer. Am J Pathol. 2008;172:236–246.
  • Basler M, Mundt S, Bitzer A, Schmidt C, Groettrup M. The immunoproteasome: a novel drug target for autoimmune diseases. Clin Exp Rheumatol. 2015;33:S74–79.
  • Lickliter J, Anderl J, Kirk CJ, Wang J, Bomba D. KZR-616, a Selective Inhibitor of the Immunoproteasome, shows a promising safety and target inhibition profile in a phase I, double-blind, single (SAD) and multiple ascending dose (MAD) study in healthy volunteers arthritis rheumatol. 2017;Vol. 69 suppl 10:Abstract 2587.
  • Kuroda K, Liu H. The proteasome inhibitor, bortezomib, induces prostate cancer cell death by suppressing the expression of prostate-specific membrane antigen, as well as androgen receptor. Int JOncol. 2019;54:1357–1366.
  • Gopalakrishnan S, Ediga HH, Reddy SS, Reddy GB, Ismail A. Procyanidin-B2 enriched fraction of cinnamon acts as a proteasome inhibitor and anti-proliferative agent in human prostate cancer cells. IUBMB Life. 2018;70:445–457.
  • Papandreou CN, Daliani DD, Nix D, Yang H, Madden T, Wang X, et al. Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. J Clin Oncol. 2004;22:2108–2121.
  • Wehenkel M, Ban JO, Ho YK, Carmony KC, Hong JT, Kim KB. A selective inhibitor of the immunoproteasome subunit LMP2 induces apoptosis in PC-3 cells and suppresses tumour growth in nude mice. Br J Cancer. 2012;107:53–62.
  • Visekruna A, Slavova N, Dullat S, Grone J, Kroesen AJ, Ritz JP, et al. Expression of catalytic proteasome subunits in the gut of patients with Crohn’s disease. Int J Colorectal Dis. 2009;24:1133–1139.
  • Kremer M, Henn A, Kolb C, Basler M, Moebius J, Guillaume B, et al. Reduced immunoproteasome formation and accumulation of immunoproteasomal precursors in the brains of lymphocytic choriomeningitis virus-infected mice. J Immunol. 2010;185:5549–5560.
  • Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013;12:703–719.
  • Iea S. The level of myeloid derived-suppressor cells in peripheral blood of patients with prostate cancerafter various types of therapy. Pol J Pathol. 2020;71:46–54.
  • Santegoets SJ, Stam AG, Lougheed SM, Gall H, Jooss K, Sacks N, et al. Myeloid derived suppressor and dendritic cell subsets are related to clinical outcome in prostate cancer patients treated with prostate GVAX and ipilimumab. J Immunother Cancer. 2014;2:31.
  • Chi N, Tan Z, Ma K, Bao L, Yun Z. Increased circulating myeloid-derived suppressor cells correlate with cancer stages, interleukin-8 and −6 in prostate cancer. Int J Clin Exp Med. 2014;7:3181–3192.
  • Sanaei MJ, Salimzadeh L, Bagheri N. Crosstalk between myeloid-derived suppressor cells and the immune system in prostate cancer: mDSCs and immune system in Prostate cancer. J Leukocyte Biol. 2020;107:43–56.
  • Veglia F, Sanseviero E, Gabrilovich DI. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat Rev Immunol. 2021;21:485–498.
  • Lu X, Horner JW, Paul E, Shang X, Troncoso P, Deng P, et al. Effective combinatorial immunotherapy for castration-resistant prostate cancer. Nature. 2017;543:728–732.
  • Gupta S, Adhami VM, Subbarayan M, MacLennan GT, Lewin JS, Hafeli UO, et al. Suppression of prostate carcinogenesis by dietary supplementation of celecoxib in transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 2004;64:3334–3343.
  • Hayashi T, Fujita K, Nojima S, Hayashi Y, Nakano K, Ishizuya Y, et al. High-fat diet-induced inflammation accelerates prostate cancer growth via IL6 signaling. Clin Cancer Res. 2018;24:4309–4318.
  • He D, Li H, Yusuf N, Elmets CA, Li J, Mountz JD, et al. IL-17 promotes tumor development through the induction of tumor promoting microenvironments at tumor sites and myeloid-derived suppressor cells. J Immunol. 2010;184:2281–2288.
  • Abida W, Cyrta J, Heller G, Prandi D, Armenia J, Coleman I, Cieslik M, Benelli M, Robinson D, Van Allen EM, et al. Genomic correlates of clinical outcome in advanced prostate cancer. Proc. Natl. Acad. Sci. U. S. A. 2019;166:11428–11436.
  • Zhang Q, Liu S, Parajuli KR, Zhang W, Zhang K, Mo Z, Liu J, Chen Z, Yang S, Wang AR, et al. Interleukin-17 promotes prostate cancer via MMP7-induced epithelial-to-mesenchymal transition. Oncogene. 2017;36:687–699.
  • Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Théodore C, James ND, Turesson I, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl. J. Med. 2004;351:1502–1512.