Expression of the immune modulator secretory leukocyte protease inhibitor (SLPI) in colorectal cancer liver metastases and matched primary tumors is associated with a poorer prognosis

References

• Maruyama M, Hay JG, Yoshimura K, Chu CS, Crystal RG. Modulation of secretory leukoprotease inhibitor gene expression in human bronchial epithelial cells by phorbol ester. J Clin Invest. 1994 Jul;94(1):368–10. doi:10.1172/JCI117331.
   PubMed Web of Science ®Google Scholar
• Sallenave JM, Shulmann J, Crossley J, Jordana M, Gauldie J. Regulation of secretory leukocyte proteinase inhibitor (SLPI) and elastase-specific inhibitor (ESI/elafin) in human airway epithelial cells by cytokines and neutrophilic enzymes. Am J Respir Cell Mol Biol. 1994 Dec;11(6):733–741. doi:10.1165/ajrcmb.11.6.7946401.
   PubMed Web of Science ®Google Scholar
• Taggart CC, Cryan SA, Weldon S, Gibbons A, Greene CM, Kelly E, Low TB, O’Neill SJ, McElvaney NG. Secretory leucoprotease inhibitor binds to NF-kappaB binding sites in monocytes and inhibits p65 binding. J Exp Med. 2005 Dec 19;202(12):1659–1668. doi:10.1084/jem.20050768.
   PubMed Web of Science ®Google Scholar
• Thompson RC, Ohlsson K. Isolation, properties, and complete amino acid sequence of human secretory leukocyte protease inhibitor, a potent inhibitor of leukocyte elastase. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6692–6696.
   PubMed Web of Science ®Google Scholar
• Hiemstra PS, Maassen RJ, Stolk J, Heinzel-Wieland R, Steffens GJ, Dijkman JH. Antibacterial activity of antileukoprotease. Infect Immun. 1996 Nov;64(11):4520–4524. doi:10.1128/IAI.64.11.4520-4524.1996.
   PubMed Web of Science ®Google Scholar
• Tomee JF, Hiemstra PS, Heinzel-Wieland R, Kauffman HF. Antileukoprotease: an endogenous protein in the innate mucosal defense against fungi. J Infect Dis. 1997 Sep;176(3):740–747. doi:10.1086/514098.
   PubMed Web of Science ®Google Scholar
• McNeely TB, Dealy M, Dripps DJ, Orenstein JM, Eisenberg SP, Wahl SM. Secretory leukocyte protease inhibitor: a human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vitro. J Clin Invest. 1995 Jul;96(1):456–464. doi:10.1172/JCI118056.
   PubMed Web of Science ®Google Scholar
• Menckeberg CL, Hol J, Simons-Oosterhuis Y, Raatgeep HR, de Ruiter LF, Lindenbergh-Kortleve DJ, Korteland-van Male AM, El Aidy S, Pieter P E van Lierop PPE, Kleerebezem M, et al. Human buccal epithelium acquires microbial hyporesponsiveness at birth, a role for secretory leukocyte protease inhibitor. Gut. 2014;64(6):(Jul):23.
   Google Scholar
• Pernot S, Terme M, Voron T, Colussi O, Marcheteau E, Tartour E Taieb J. Colorectal cancer and immunity: what we know and perspectives. World J Gastroenterol. 2014 Apr 14;20(14):3738–3750. doi:10.3748/wjg.v20.i14.3738.
   PubMed Web of Science ®Google Scholar
• de Vries NL, Swets M, Vahrmeijer AL, Hokland M, Kuppen PJ. The immunogenicity of colorectal cancer in relation to tumor development and treatment. Int J Mol Sci. 2016 Jun 29;17(7):1030. doi:10.3390/ijms17071030.
   PubMed Web of Science ®Google Scholar
• Woo SR, Corrales L, Gajewski TF. Innate immune recognition of cancer. Annu Rev Immunol. 2015;33:445–474. doi:10.1146/annurev-immunol-032414-112043.
   PubMed Web of Science ®Google Scholar
• Liu G, Yang J, Zhao Y, Wang Z, Xing B, Wang L, Shi D. Expression of secretory leukocyte protease inhibitor detected by immunohistochemistry correlating with prognosis and metastasis in colorectal cancer. World J Surg Oncol. 2014 Dec 2;12:369–7819-12-369. doi:10.1186/1477-7819-12-369.
   Web of Science ®Google Scholar
• Cheng WL, Wang CS, Huang YH, Liang Y, Lin PY, Hsueh C, Wu Y-C, Chen W-J, Yu C-J, Lin S-R et al. Overexpression of a secretory leukocyte protease inhibitor in human gastric cancer. Int J Cancer. 2008 Oct 15;123(8):1787–1796. doi:10.1002/ijc.23746.
   PubMed Web of Science ®Google Scholar
• Ameshima S, Ishizaki T, Demura Y, Imamura Y, Miyamori I, Mitsuhashi H. Increased secretory leukoprotease inhibitor in patients with nonsmall cell lung carcinoma. Cancer. 2000 Oct 1;89(7):1448–1456.
   PubMed Web of Science ®Google Scholar
• Shigemasa K, Tanimoto H, Underwood LJ, Parmley TH, Arihiro K, Ohama K, O’Brien TJ. Expression of the protease inhibitor antileukoprotease and the serine protease stratum corneum chymotryptic enzyme (SCCE) is coordinated in ovarian tumors. Int J Gynecol Cancer. 2001 Nov-Dec;11(6):454–461. doi:10.1046/j.1525-1438.2001.01062.x.
   PubMed Web of Science ®Google Scholar
• Wagenblast E, Soto M, Gutierrez-Angel S, Hartl CA, Gable AL, Maceli AR, Erard N, Williams AM, Kim SY, Dickopf S et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature. 2015 Apr 16;520(7547):358–362. doi:10.1038/nature14403.
   PubMed Web of Science ®Google Scholar
• Kozin SV, Maimon N, Wang R, Gupta N, Munn L, Jain RK, Garkavtsev I. Secretory leukocyte protease inhibitor (SLPI) as a potential target for inhibiting metastasis of triple-negative breast cancers. Oncotarget. 2017 Nov 26;8(65):108292–108302. doi:10.18632/oncotarget.22660.
   PubMedGoogle Scholar
• Wang N, Thuraisingam T, Fallavollita L, Ding A, Radzioch D, Brodt P. The secretory leukocyte protease inhibitor is a type 1 insulin-like growth factor receptor-regulated protein that protects against liver metastasis by attenuating the host proinflammatory response. Cancer Res. 2006 Mar 15;66(6):3062–3070. doi:10.1158/0008-5472.CAN-05-2638.
   PubMed Web of Science ®Google Scholar
• Amiano NO, Costa MJ, Reiteri RM, Payes C, Guerrieri D, Tateosian NL, Sánchez ML, Maffia PC, Diament M, Karas R, et al. Anti-tumor effect of SLPI on mammary but not colon tumor growth. J Cell Physiol. 2013 Feb;228(2):469–475. doi:10.1002/jcp.24153.
   PubMed Web of Science ®Google Scholar
• Hackl C, Neumann P, Gerken M, Loss M, Klinkhammer-Schalke M, Schlitt HJ. Treatment of colorectal liver metastases in Germany: a ten-year population-based analysis of 5772 cases of primary colorectal adenocarcinoma. BMC Cancer. 2014 Nov 4;14(1):810–2407-14-810. doi:10.1186/1471-2407-14-810.
   Google Scholar
• Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006 Aug;244(2):254–259. doi:10.1097/01.sla.0000217629.94941.cf.
   PubMed Web of Science ®Google Scholar
• Leporrier J, Maurel J, Chiche L, Bara S, Segol P, Launoy G. A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg. 2006 Apr;93(4):465–474.
   PubMed Web of Science ®Google Scholar
• Engstrand J, Nilsson H, Stromberg C, Jonas E, Freedman J. Colorectal cancer liver metastases - a population-based study on incidence, management and survival. BMC Cancer. 2018 Jan 15;18(1):780173925x. doi:10.1186/s12885-017-3925-x.
   Google Scholar
• Ito K, Govindarajan A, Ito H, Fong Y. Surgical treatment of hepatic colorectal metastasis: evolving role in the setting of improving systemic therapies and ablative treatments in the 21st century. Cancer J. 2010 Mar-Apr;16(2):103–110. doi:10.1097/PPO.0b013e3181d7e8e5.
   PubMed Web of Science ®Google Scholar
• Spolverato G, Ejaz A, Azad N, Pawlik TM. Surgery for colorectal liver metastases: the evolution of determining prognosis. World J Gastrointest Oncol. 2013 Dec 15;5(12):207–221. doi:10.4251/wjgo.v5.i12.207.
   PubMed Web of Science ®Google Scholar
• Goos JA, Coupe VM, Diosdado B, Delis-Van Diemen PM, Karga C, Belien JA, Carvalho B, van den Tol MP, Verheul HMW, Geldof AA et al. Aurora kinase A (AURKA) expression in colorectal cancer liver metastasis is associated with poor prognosis. Br J Cancer. 2013 Oct 29;109(9):2445–2452. doi:10.1038/bjc.2013.608.
   PubMed Web of Science ®Google Scholar
• Simon R, Mirlacher M, Sauter G. Tissue microarrays. BioTechniques. 2004 Jan;36(1):98–105. doi:10.2144/04361RV01.
   PubMed Web of Science ®Google Scholar
• Federation of Dutch Medical Scientific Societies (FDMSS). Human tissue and medical research: code of conduct for responsible use. 2011; https://www.federa.org/code-goed-gebruik-van-lichaamsmateriaal-2011.
   Google Scholar
• Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999 Sep;230(3):309–318. discussion 318-21. doi:10.1097/00000658-199909000-00004.
   PubMed Web of Science ®Google Scholar
• R Core Team, R Foundation for statistical computing, vienna, austria. r: a language and environment for statistical computing. 2018; https://www.R-project.org, version 3.5.1
   Google Scholar
• Therneau TA Package for survival analysis in S. 2015. https://CRAN.R-project.org/package=survival, version 2.38
   Google Scholar
• Therneau TM, Grambsch PM. Modeling survival data: extending the Cox 3. New York: Springer; 2000. ISBN 0-387-98784.
   Google Scholar
• Kassambara A, Kosinski M, Biecek P survminer: drawing survival curves using ‘ggplot2ʹ. 2019. https://CRAN.R-project.org/package=survminer, version 0.4.6
   Google Scholar
• Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Müller M. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinform. 2011 Mar 17;12:77–2105-12-77. doi:10.1186/1471-2105-12-77.
   PubMed Web of Science ®Google Scholar
• Heagerty PJ, Saha-Chaudhuri P survivalROC: time-dependent ROC curve estimation from censored survival data. 2013. https://CRAN.R-project.org/package=survivalROC, version 1.0.3
   Google Scholar
• McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer. 2005 Aug 22;93(4):387–391. doi:10.1038/sj.bjc.6602678.
   PubMed Web of Science ®Google Scholar
• Si-Tahar M, Merlin D, Sitaraman S, Madara JL. Constitutive and regulated secretion of secretory leukocyte proteinase inhibitor by human intestinal epithelial cells. Gastroenterol. 2000 Jun;118(6):1061–1071. doi:10.1016/S0016-5085(00)70359-3.
   PubMed Web of Science ®Google Scholar
• Pagѐs F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, Lagorce C, Wind P, Marliot F, Bruneval P, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol. 2009 Dec 10;27(35):5944–5951. doi:10.1200/JCO.2008.19.6147.
   PubMed Web of Science ®Google Scholar
• Katz SC, Pillarisetty V, Bamboat ZM, Shia J, Hedvat C, Gonen M, Jarnagin W, Fong Y, Blumgart L, D’Angelica M, et al. T cell infiltrate predicts long-term survival following resection of colorectal cancer liver metastases. Ann Surg Oncol. 2009 Sep;16(9):2524–2530. doi:10.1245/s10434-009-0585-3.
   PubMed Web of Science ®Google Scholar
• Xu W, He B, Chiu A, Chadburn A, Shan M, Buldys M, Ding A, Knowles DM, Santini PA, Cerutti A, et al. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol. 2007 Mar;8(3):294–303. doi:10.1038/ni1434.
   PubMed Web of Science ®Google Scholar
• Ding A, Thieblemont N, Zhu J, Jin F, Zhang J, Wright S. Secretory leukocyte protease inhibitor interferes with uptake of lipopolysaccharide by macrophages. Infect Immun. 1999 Sep;67(9):4485–4489. doi:10.1128/IAI.67.9.4485-4489.1999.
   PubMed Web of Science ®Google Scholar
• Goos JA, de Cuba EM, Coupé VM, Diosdado B, Delis-Van Diemen PM, Karga C, Beliën JAM, Oordt CWM, Geldof AA, Meijer GA, et al. Glucose transporter 1 (SLC2A1) and vascular endothelial growth factor A (VEGFA) predict survival after resection of colorectal cancer liver metastasis. Ann Surg. 2016 Jan;263(1):138–145. doi:10.1097/SLA.0000000000001109.
   PubMed Web of Science ®Google Scholar
• Goos JA, Hiemstra AC, Coupé VM, Diosdado B, Kooijman W, Delis-Van Diemen PM, Karga C, Beliën JAM, Menke-van der Houven van Oordt CW, Geldof AA et al. Epidermal growth factor receptor (EGFR) and prostaglandin-endoperoxide synthase 2 (PTGS2) are prognostic biomarkers for patients with resected colorectal cancer liver metastases. Br J Cancer. 2014 Aug 12;111(4):749–755. doi:10.1038/bjc.2014.354.
   PubMed Web of Science ®Google Scholar
• Terme M, Pernot S, Marcheteau E, Sandoval F, Benhamouda N, Colussi O, Dubreuil O, Carpentier AF, Tartour E, Taieb J. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res. 2013 Jan 15;73(2):539–549. doi:10.1158/0008-5472.CAN-12-2325.
   PubMed Web of Science ®Google Scholar
• Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 2007 May 1;67(9):4507–4513. doi:10.1158/0008-5472.CAN-06-4174.
   PubMed Web of Science ®Google Scholar