[en] Previous studies have linked cancer cell-associated ADAM28 expression with tumor progression and metastatic dissemination. However, the role of host-derived ADAM28 in cancer dissemination processes remains unclear. Genetically engineered-mice fully deficient for ADAM28 unexpectedly display increased lung colonization by pulmonary, melanoma or breast tumor cells. In experimental tumor cell dissemination models, host ADAM28 deficiency is further associated with a decreased lung infiltration by CD8+ T lymphocytes. Notably, naive ADAM28-deficient mice already display a drastic reduction of CD8+ T cells in spleen which is further observed in lungs. Interestingly, ex vivo CD8+ T cell characterization revealed that ADAM28-deficiency does not impact proliferation, migration nor activation of CD8+ T cells. Our data highlight a functional role of ADAM28 in T cell mobilization and point to an unexpected protective role for host ADAM28 against metastasis.
Disciplines :
Oncology
Author, co-author :
Gérard, Catherine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Hubeau, Céline ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Carnet, Oriane ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Bellefroid, Marine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Sounni, Nor Eddine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire
Blacher, Silvia ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Bendavid, Guillaume ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Moser, Markus; Max-Planck-Institute of Biochemistry, Department of Molecular Medicine, Martinsried, Germany
Fässler, Reinhart; Max-Planck-Institute of Biochemistry, Department of Molecular Medicine, Martinsried, Germany
Noël, Agnès ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Cataldo, Didier ✱; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Rocks, Natacha ✱; Université de Liège - ULiège > Département de pharmacie > Pharmacie galénique
✱ These authors have contributed equally to this work.
Language :
English
Title :
Microenvironment-derived ADAM28 prevents cancer dissemination
Mochizuki S, Shimoda M, Shiomi T, Fujii Y, Okada Y. ADAM28 is activated by MMP-7 (matrilysin-1) and cleaves insulin-like growth factor binding protein-3. Biochem Biophys Res Commun. 2004; 315:79-84. https://doi.org/10.1016/j.bbrc.2004.01.022.
Howard L, Zheng Y, Horrocks M, Maciewicz RA, Blobel C. Catalytic activity of ADAM28. FEBS Lett. 2001; 498:82-86. https://doi.org/10.1016/S0014-5793(01)02506-6.
Mochizuki S, Tanaka R, Shimoda M, Onuma J, Fujii Y, Jinno H, Okada Y. Connective tissue growth factor is a substrate of ADAM28. Biochem Biophys Res Commun. 2010; 402:651-57. https://doi.org/10.1016/j.bbrc.2010.10.077.
Mochizuki S, Soejima K, Shimoda M, Abe H, Sasaki A, Okano HJ, Okano H, Okada Y. Effect of ADAM28 on carcinoma cell metastasis by cleavage of von Willebrand factor. J Natl Cancer Inst. 2012; 104:906-22. https://doi.org/10.1093/jnci/djs232.
Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, Shiomi T, Chijiiwa M, Ikeda T, Kitajima M, Okada Y. ADAM28 is overexpressed in human breast carcinomas: implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res. 2006; 66:9913-20. https://doi.org/10.1158/0008-5472.CAN-06-0377.
Matsuura S, Oda Y, Matono H, Izumi T, Yamamoto H, Tamiya S, Iwamoto Y, Tsuneyoshi M. Overexpression of A disintegrin and metalloproteinase 28 is correlated with high histologic grade in conventional chondrosarcoma. Hum Pathol. 2010; 41:343-51. https://doi.org/10.1016/j.humpath.2009.08.002.
Stokes A, Joutsa J, Ala-Aho R, Pitchers M, Pennington CJ, Martin C, Premachandra DJ, Okada Y, Peltonen J, Grénman R, James HA, Edwards DR, Kähäri VM. Expression profiles and clinical correlations of degradome components in the tumor microenvironment of head and neck squamous cell carcinoma. Clin Cancer Res. 2010; 16:2022-35. https://doi.org/10.1158/1078-0432.CCR-09-2525.
Zhang XH, Wang CC, Jiang Q, Yang SM, Jiang H, Lu J, Wang QM, Feng FE, Zhu XL, Zhao T, Huang XJ. ADAM28 overexpression regulated via the PI3K/Akt pathway is associated with relapse in de novo adult B-cell acute lymphoblastic leukemia. Leuk Res. 2015; 39:1229-38. https://doi.org/10.1016/j.leukres.2015.08.006.
Yang MH, Chu PY, Chen SC, Chung TW, Chen WC, Tan LB, Kan WC, Wang HY, Su SB, Tyan YC. Characterization of ADAM28 as a biomarker of bladder transitional cell carcinomas by urinary proteome analysis. Biochem Biophys Res Commun. 2011; 411:714-20. https://doi.org/10.1016/j.bbrc.2011.07.010.
Ohtsuka T, Shiomi T, Shimoda M, Kodama T, Amour A, Murphy G, Ohuchi E, Kobayashi K, Okada Y. ADAM28 is overexpressed in human non-small cell lung carcinomas and correlates with cell proliferation and lymph node metastasis. Int J Cancer. 2006; 118:263-73. https://doi.org/10.1002/ijc.21324.
Rudnicka C, Mochizuki S, Okada Y, McLaughlin C, Leedman PJ, Stuart L, Epis M, Hoyne G, Boulos S, Johnson L, Schlaich M, Matthews V. Overexpression and knock-down studies highlight that a disintegrin and metalloproteinase 28 controls proliferation and migration in human prostate cancer. Medicine (Baltimore). 2016; 95:e5085. https://doi.org/10.1097/MD.0000000000005085.
Kuroda H, Mochizuki S, Shimoda M, Chijiiwa M, Kamiya K, Izumi Y, Watanabe M, Horinouchi H, Kawamura M, Kobayashi K, Okada Y. ADAM28 is a serological and histochemical marker for non-small-cell lung cancers. Int J Cancer. 2010; 127:1844-56. https://doi.org/10.1002/ijc.25212.
Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002; 2:735-47. https://doi.org/10.1038/nri911.
Pluhar GE, Pennell CA, Olin MR. CD8+ T Cell-Independent Immune-Mediated Mechanisms of Anti-Tumor Activity. Crit Rev Immunol. 2015; 35:153-72.
Johnson SK, Kerr KM, Chapman AD, Kennedy MM, King G, Cockburn JS, Jeffrey RR. Immune cell infiltrates and prognosis in primary carcinoma of the lung. Lung Cancer. 2000; 27:27-35. https://doi.org/10.1016/S0169-5002(99)00095-1.
Donnem T, Al-Saad S, Al-Shibli K, Busund LT, Bremnes RM. Co-expression of PDGF-B and VEGFR-3 strongly correlates with lymph node metastasis and poor survival in non-small-cell lung cancer. Ann Oncol. 2010; 21:223-31. https://doi.org/10.1093/annonc/mdp296.
Al-Shibli KI, Donnem T, Al-Saad S, Persson M, Bremnes RM, Busund LT. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res. 2008; 14:5220-27. https://doi.org/10.1158/1078-0432.CCR-08-0133.
Welsh TJ, Green RH, Richardson D, Waller DA, O'Byrne KJ, Bradding P. Macrophage and mast-cell invasion of tumor cell islets confers a marked survival advantage in non-small-cell lung cancer. J Clin Oncol. 2005; 23:8959-67. https://doi.org/10.1200/JCO.2005.01.4910.
Kawai O, Ishii G, Kubota K, Murata Y, Naito Y, Mizuno T, Aokage K, Saijo N, Nishiwaki Y, Gemma A, Kudoh S, Ochiai A. Predominant infiltration of macrophages and CD8(+) T Cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer. 2008; 113:1387-95. https://doi.org/10.1002/cncr.23712.
Petersen RP, Campa MJ, Sperlazza J, Conlon D, Joshi MB, Harpole DH Jr, Patz EF Jr. Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer. 2006; 107:2866-72. https://doi.org/10.1002/cncr.22282.
Ganesan AP, Johansson M, Ruffell B, Yagui-Beltrán A, Lau J, Jablons DM, Coussens LM. Tumor-infiltrating regulatory T cells inhibit endogenous cytotoxic T cell responses to lung adenocarcinoma. J Immunol. 2013; 191:2009-17. https://doi.org/10.4049/jimmunol.1301317.
Erratum in: J Immunol. 2013 Nov 15;191(10):5319. Beltran, Adam [corrected to Yagui-Beltrán, Adam].
Mochizuki S, Okada Y. ADAMs in cancer cell proliferation and progression. Cancer Sci. 2007; 98:621-28. https://doi.org/10.1111/j.1349-7006.2007.00434.x.
Mullooly M, McGowan PM, Crown J, Duffy MJ. The ADAMs family of proteases as targets for the treatment of cancer. Cancer Biol Ther. 2016; 17:870-80. https://doi.org/10.1080/15384047.2016.1177684.
Wolf MJ, Adili A, Piotrowitz K, Abdullah Z, Boege Y, Stemmer K, Ringelhan M, Simonavicius N, Egger M, Wohlleber D, Lorentzen A, Einer C, Schulz S, et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell. 2014; 26:549-64. https://doi.org/10.1016/j.ccell.2014.09.003.
Miyashita M, Sasano H, Tamaki K, Hirakawa H, Takahashi Y, Nakagawa S, Watanabe G, Tada H, Suzuki A, Ohuchi N, Ishida T. Prognostic significance of tumor-infiltrating CD8+ and FOXP3+ lymphocytes in residual tumors and alterations in these parameters after neoadjuvant chemotherapy in triple-negative breast cancer: a retrospective multicenter study. Breast Cancer Res. 2015; 17:124. https://doi.org/10.1186/s13058-015-0632-x.
Adams S, Goldstein LJ, Sparano JA, Demaria S, Badve SS. Tumor infiltrating lymphocytes (TILs) improve prognosis in patients with triple negative breast cancer (TNBC). Oncoimmunology. 2015; 4:e985930. https://doi.org/10.4161/2162402X.2014.985930.
Andreasson K, Eriksson M, Tegerstedt K, Ramqvist T, Dalianis T. CD4+ and CD8+ T cells can act separately in tumour rejection after immunization with murine pneumotropic virus chimeric Her2/neu virus-like particles. PLoS One. 2010; 5:e11580. https://doi.org/10.1371/journal.pone.0011580.
Reiser J, Banerjee A. Effector, Memory, and Dysfunctional CD8(+) T Cell Fates in the Antitumor Immune Response. J Immunol Res. 2016; 2016:8941260. https://doi.org/10.1155/2016/8941260.
Bridges LC, Tani PH, Hanson KR, Roberts CM, Judkins MB, Bowditch RD. The lymphocyte metalloprotease MDC-L (ADAM 28) is a ligand for the integrin α4β1. J Biol Chem. 2002; 277:3784-92. https://doi.org/10.1074/jbc.M109538200.
Bridges LC, Hanson KR, Tani PH, Mather T, Bowditch RD. Integrin α4β1-dependent adhesion to ADAM 28 (MDC-L) requires an extended surface of the disintegrin domain. Biochemistry. 2003; 42:3734-41. https://doi.org/10.1021/bi026871y.
Bridges LC, Sheppard D, Bowditch RD. ADAM disintegrin-like domain recognition by the lymphocyte integrins α4β1 and α4β7. Biochem J. 2005; 387:101-08. https://doi.org/10.1042/BJ20041444.
Twito T, Chen Z, Khatri I, Wong K, Spaner D, Gorczynski R. Ectodomain shedding of CD200 from the B-CLL cell surface is regulated by ADAM28 expression. Leuk Res. 2013; 37:816-21. https://doi.org/10.1016/j.leukres.2013.04.014.
Zhang Y, Zhu G, Xiao H, Liu X, Han G, Chen G, Hou C, Shen B, Li Y, Ma N, Wang R. CD19 regulates ADAM28-mediated Notch2 cleavage to control the differentiation of marginal zone precursors to MZ B cells. J Cell Mol Med. 2017; 21:3658-69. https://doi.org/10.1111/jcmm.13276.
Hess C, Means TK, Autissier P, Woodberry T, Altfeld M, Addo MM, Frahm N, Brander C, Walker BD, Luster AD. IL-8 responsiveness defines a subset of CD8 T cells poised to kill. Blood. 2004; 104:3463-71. https://doi.org/10.1182/blood-2004-03-1067.
Kerkelä E, Ala-aho R, Klemi P, Grénman S, Shapiro SD, Kähäri VM, Saarialho-Kere U. Metalloelastase (MMP-12) expression by tumour cells in squamous cell carcinoma of the vulva correlates with invasiveness, while that by macrophages predicts better outcome. J Pathol. 2002; 198:258-69. https://doi.org/10.1002/path.1198.
Fröhlich C, Nehammer C, Albrechtsen R, Kronqvist P, Kveiborg M, Sehara-Fujisawa A, Mercurio AM, Wewer UM. ADAM12 produced by tumor cells rather than stromal cells accelerates breast tumor progression. Mol Cancer Res. 2011; 9:1449-61. https://doi.org/10.1158/1541-7786.MCR-11-0100.
Ricciardelli C, Frewin KM, Tan IA, Williams ED, Opeskin K, Pritchard MA, Ingman WV, Russell DL. The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am J Pathol. 2011; 179:3075-85. https://doi.org/10.1016/j.ajpath.2011.08.021.
Acar M, Ocak Z, Erdogan K, Cetin EN, Hatipoglu OF, Uyeturk U, Gunduz E, Gunduz M. The effects of hypericin on ADAMTS and p53 gene expression in MCF-7 breast cancer cells. J BUON. 2014; 19:627-32.
Luque A, Carpizo DR, Iruela-Arispe ML. ADAMTS1/ METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J Biol Chem. 2003; 278:23656-65. https://doi.org/10.1074/jbc.M212964200
López-Otín C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer. 2007; 7:800-08. https://doi.org/10.1038/nrc2228.
Iruela-Arispe ML, Carpizo D, Luque A. ADAMTS1: a matrix metalloprotease with angioinhibitory properties. Ann N Y Acad Sci. 2003; 995:183-90. https://doi.org/10.1111/j.1749-6632.2003.tb03221.x.
Verbisck NV, Costa ET, Costa FF, Cavalher FP, Costa MD, Muras A, Paixão VA, Moura R, Granato MF, Ierardi DF, Machado T, Melo F, Ribeiro KB, et al. ADAM23 negatively modulates alpha(v)beta(3) integrin activation during metastasis. Cancer Res. 2009; 69:5546-52. https://doi.org/10.1158/0008-5472.CAN-08-2976.
Péqueux C, Raymond-Letron I, Blacher S, Boudou F, Adlanmerini M, Fouque MJ, Rochaix P, Noël A, Foidart JM, Krust A, Chambon P, Brouchet L, Arnal JF, Lenfant F. Stromal estrogen receptor-α promotes tumor growth by normalizing an increased angiogenesis. Cancer Res. 2012; 72:3010-19. https://doi.org/10.1158/0008-5472.CAN-11-3768.
Carnet O, Lecomte J, Masset A, Primac I, Durré T, Maertens L, Detry B, Blacher S, Gilles C, Péqueux C, Paupert J, Foidart JM, Jerusalem G, et al. Mesenchymal Stem Cells Shed Amphiregulin at the Surface of Lung Carcinoma Cells in a Juxtacrine Manner. Neoplasia. 2015; 17:552-63. https://doi.org/10.1016/j.neo.2015.07.002.
Fässler R, Schnegelsberg PN, Dausman J, Shinya T, Muragaki Y, McCarthy MT, Olsen BR, Jaenisch R. Mice lacking alpha 1 (IX) collagen develop noninflammatory degenerative joint disease. Proc Natl Acad Sci U S A. 1994; 91:5070-74. https://doi.org/10.1073/pnas.91.11.5070.
Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995; 23:5080-81. https://doi.org/10.1093/nar/23.24.5080.
Rocks N, Bekaert S, Coia I, Paulissen G, Gueders M, Evrard B, Van Heugen JC, Chiap P, Foidart JM, Noel A, Cataldo D. Curcumin-cyclodextrin complexes potentiate gemcitabine effects in an orthotopic mouse model of lung cancer. Br J Cancer. 2012; 107:1083-92. https://doi.org/10.1038/bjc.2012.379.
Donati K, Sépult C, Rocks N, Blacher S, Gérard C, Noel A, Cataldo D. Neutrophil-Derived Interleukin 16 in Premetastatic Lungs Promotes Breast Tumor Cell Seeding. Cancer Growth Metastasis. 2017; 10:1-14. https://doi.org/10.1177/1179064417738513.
Lewis MD, de Leenheer E, Fishman S, Siew LK, Gross G, Wong FS. A reproducible method for the expansion of mouse CD8+ T lymphocytes. J Immunol Methods. 2015; 417:134-38. https://doi.org/10.1016/j.jim.2015.01.004.