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Role of Proteases in Tumor Immune Evasion

  • Abir K. Panda
  • Sreeparna Chakraborty
  • Kirti Kajal
  • Dia Roy
  • Tania Sarkar
  • Gaurisankar Sa
Chapter

Abstract

Proteolysis or protein degradation is an important biological function which has been attributed to a major class of enzymes called proteases. In the living system, a fine-tuning between the activity of proteases and their counterparts can be seen, and disruption of this balance leads to the occurrence of various diseases including cancer. Several studies indicate that protease activity highly correlated with cancer advancement. The hallmarks of cancer like tissue evasion and metastasis, apoptosis, angiogenesis largely depend on proteolytic degradation and protease activation. Protease also contributes to avoidance of immune system, one of the emerging hallmarks in cancer progression. The immune system can recognize intracellular pathogens including cancer and elicits an effective immune response to restrict their activity and subsequently protect the host. In cancer microenvironment, immune cells are unable to recognize tumor neoantigens as well as incapable of inducing proper immune response for the clearance of tumor cells. Recent studies found that proteases not only promote tumor cell migration and metastasis it also encourages to maintain the tolerogenic tumor microenvironment by modulation of immune cell functions. Proteases are involved in several immune responses such as antigen processing and presentation, lymphocytes and neutrophil infiltration, activation of dendritic cells. The anomalies of protease actions dampen immune cell activities and establish immune tolerance. Inappropriate protease activities are responsible for inhibiting immunosurveillance and maintaining immune tolerance that ultimately leads to tumor immune evasion. Involvement of proteases in cancer suggests the use of protease inhibitors as anticancer drugs to targets not only tumor cells as well as tolerogenic immune cells to reeducate immune responses and reestablish immune surveillance. This chapter summarizes the current understanding of the interplay between proteases and the immune cells of the body and their involvement in cancer progression.

References

  1. 1.
    Rabinovich GA, Gabrilovich D, Sotomayor EM (2007) Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25:267–296PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3(11):991–998PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Dunn GP, Old LJ, Schreiber RD (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22:329–360PubMedCrossRefGoogle Scholar
  4. 4.
    Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86(3):353–364PubMedCrossRefGoogle Scholar
  5. 5.
    Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331(6024):1565–1570PubMedCrossRefGoogle Scholar
  6. 6.
    Kim R, Emi M, Tanabe K (2007) Cancer immunoediting from immune surveillance to immune escape. Immunology 121(1):1–14PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Zou W (2005) Immunosuppressive networks in the tumor environment and their therapeutic relevance. Nat Rev Cancer 5(4):263–274PubMedCrossRefGoogle Scholar
  8. 8.
    Vinay DS, Ryan EP, Pawelec G et al (2015) Immune evasion in cancer: mechanistic basis and therapeutic strategies. Semin Cancer Biol 35:S185–S198PubMedCrossRefGoogle Scholar
  9. 9.
    Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674CrossRefGoogle Scholar
  10. 10.
    Kim R, Emi M, Tanabe K (2006) Cancer immunosuppression and autoimmune disease: beyond immunosuppressive networks for tumor immunity. Immunology 119(2):254–264PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    López-Otín C, Overall CM (2002) Protease degradomics: a new challenge for proteomics. Nat Rev Mol Cell Biol 3(7):509–519PubMedCrossRefGoogle Scholar
  12. 12.
    Fischer A (1946) Mechanism of the proteolytic activity of malignant tissue cells. Nature 6(157):442CrossRefGoogle Scholar
  13. 13.
    Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161–174CrossRefPubMedGoogle Scholar
  14. 14.
    Mohamed MM, Sloane BF (2006) Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 6(10):764–775PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    López-Otín C, Matrisian LM (2007) Emerging roles of proteases in tumor suppression. Nat Rev Cancer 7(10):800–808PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Borgoño CA, Diamandis EP (2004) The emerging roles of human tissue kallikreins in cancer. Nat Rev Cancer 4(11):876–890PubMedCrossRefGoogle Scholar
  17. 17.
    Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295(5564):2387–2392CrossRefPubMedGoogle Scholar
  18. 18.
    Overall CM, Kleifeld O (2006) Tumour microenvironment—opinion: validating matrix metal lo-proteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 6(3):227–239PubMedCrossRefGoogle Scholar
  19. 19.
    Turk B (2006) Targeting proteases: successes, failures and future prospects. Nat Rev Drug Discov 5(9):785–799CrossRefPubMedGoogle Scholar
  20. 20.
    Goetzl EJ, Banda MJ, Leppert D (1996) Matrix metalloproteinases in immunity. J Immunol 156(1):1–4PubMedGoogle Scholar
  21. 21.
    Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776PubMedCrossRefGoogle Scholar
  23. 23.
    MacKenzie SH, Clark AC (2008) Targeting cell death in tumors by activating caspases. Curr Cancer Drug Targets 8(2):98–109PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Cullen SP, Brunet M, Martin SJ (2010) Granzymes in cancer and immunity. Cell Death Differ 17:616–623PubMedCrossRefGoogle Scholar
  25. 25.
    Walsh CM, Edinger AL (2010) The complex interplay between autophagy, apoptosis, and necrotic signals promotes T-cell homeostasis. Immunol Rev 236:95–109PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Xing Y, Hogquist KA (2016) T-cell tolerance: central and peripheral. Cold Spring Harb Perspect Biol 4:a006957Google Scholar
  27. 27.
    Jameson SC et al (2005) Central tolerance: learning self-control in the thymus. Nat Rev Immunol 5:772–782PubMedCrossRefGoogle Scholar
  28. 28.
    Ghavami S, Hashemi M, Ande SR, Yeganeh B, Xiao W, Eshraghi M, Bus CJ, Kadkhoda K, Wiechec E, Halayko AJ, Los M (2009) Apoptosis and cancer: mutations within caspase genes. J Med Genet 46:497–510PubMedCrossRefGoogle Scholar
  29. 29.
    Mintern JD, Harris J et al (2015) Autophagy and immunity. Immunol Cell Biol 93:1–2PubMedCrossRefGoogle Scholar
  30. 30.
    Nair U et al (2012) A role for Atg8–PE deconjugation in autophagosome biogenesis. Autophagy 8(5):780–793PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Kaminskyy V, Zhivotovsky B et al (2012) Proteases in autophagy. Biochimi Biophys Acta (BBA)-Proteins Proteomics 1824(1):44–50CrossRefGoogle Scholar
  32. 32.
    Yin F, Cadenas E et al (2015) Mitochondria: the cellular hub of the dynamic coordinated network. Antioxid Redox Signal 22(12):961–964PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Lazarou M et al (2015) Keeping the immune system in check: a role for mitophagy. Immunol Cell Biol 93:3–10PubMedCrossRefGoogle Scholar
  34. 34.
    Ma Y, Galluzzi L, Zitvogel L, Kroemer G et al (2013) Autophagy and cellular immune responses. Immunity 39Google Scholar
  35. 35.
    Bohovych I, Chan SS, Khalimonchuk O et al (2015) Mitochondrial protein quality control: the mechanisms guarding mitochondrial health. Antioxid Redox Signal 22(12):977–994PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Brough D et al (2011) Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev 22(4):189–195PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Wei L-X et al (2015) The role of autophagy induced by tumor microenvironment in different cells and stages of cancer. Cell Biosci 13578-015-0005-2Google Scholar
  38. 38.
    Crotzer VL, Blum JS et al (2009) Autophagy and its role in MHC-mediated antigen presentation. J Immunol 182(6):3335–3341PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Rock KL, Farfán-Arribas DJ, Shen L et al (2010) Proteases in MHC class I presentation and cross-presentation. J Immunol 184(1):9–15PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Mah LY, Ryan KM et al (2012) Autophagy and cancer. Cold Spring Harb Perspect Biol 4:a008821PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Mellman I, Steinman RM (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255–258PubMedCrossRefGoogle Scholar
  42. 42.
    Norbury CC, Basta S, Donohue KB (2004) CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304:1318–1321PubMedCrossRefGoogle Scholar
  43. 43.
    Bromley SK, Burack WR, Johnson KG, Somersalo K, Sims TN, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML (2001) The immunological synapse. Annu Rev Immunol 19:375PubMedCrossRefGoogle Scholar
  44. 44.
    Bartmann J, Frankenberger M, Neurohr C, Eickelberg O, Noessner E, von Wulffen W (2016) A novel role of MMP-13 for murine DC function: its inhibition dampens T-cell activation. Int Immunol. doi: 10.1093/intimm/dxw008CrossRefPubMedGoogle Scholar
  45. 45.
    Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133–146PubMedCrossRefGoogle Scholar
  46. 46.
    Quatromoni JG, Eruslanov E et al (2012) Tumor-associated macrophages: function, phenotype, and link to prognosis in human lung cancer. Am J Transl Res 4(4):376–389PubMedPubMedCentralGoogle Scholar
  47. 47.
    Solinas G et al (2009) Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86(5):1065–1073PubMedCrossRefGoogle Scholar
  48. 48.
    Kothari P et al (2014) IL-6-mediated induction of MMP-9 is modulated by JAK-dependent IL-10 expression in macrophages. J Immunol 192(1): 10.4049Google Scholar
  49. 49.
    Trikha P, Carson WE et al (2014) Signaling pathways involved in MDSC regulation. Biochim Biophys Acta 1846(1):55–65PubMedPubMedCentralGoogle Scholar
  50. 50.
    Kessenbrock K, Plaks V, Werb Z et al (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141(1):52–67PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Albeituni SH, Yan J et al (2013) Hampering the immune suppressors: therapeutic targeting of myeloid-derived suppressor cells (MDSC) in cancer. Cancer J 19(6):490–501PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Parker KH et al (2015) Myeloid-derived suppressor cells: critical cells driving immune suppression in the tumor microenvironment. Adv Cancer Res 128:95–139PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Vérollet C, Charrière GM et al (2011) Extracellular proteolysis in macrophage migration: losing grip for a breakthrough. Eur J Immunol (10):2805–13PubMedCrossRefGoogle Scholar
  54. 54.
    Chanmee T et al (2014) Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel) 6(3):1670–1690CrossRefGoogle Scholar
  55. 55.
    Yang M et al (2014) Cathepsin S-mediated autophagic flux in tumor-associated macrophages accelerates tumor development by promoting M2 polarization. Mol Cancer 1476-4598-13-43Google Scholar
  56. 56.
    Shree T et al (2011) Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 25(23):2465–2479PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Rőszer T (2015) Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediat Inflamm 2015:816460CrossRefGoogle Scholar
  58. 58.
    Nizet V et al (2009) Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 9:609–617PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Weidemann A, Johnson RS et al (2008) Biology of HIF-1α. Cell Death Differ 15:621–627PubMedCrossRefGoogle Scholar
  60. 60.
    Lewis CE, Pollard JW et al (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66(2)PubMedCrossRefGoogle Scholar
  61. 61.
    Blum JS, Wearsch PA, Cresswell P (2013) Pathways of antigen processing. Annu Rev Immunol 31:443–473PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Seliger B (2008) Different regulation of MHC class I antigen processing components in human tumors. J Immunotoxicol 5:361–367PubMedCrossRefGoogle Scholar
  63. 63.
    Maupin-Furlow J (2012) Proteasomes and protein conjugation across domains of life. Nat Rev Microbiol 10:100–111CrossRefGoogle Scholar
  64. 64.
    Yewdell J, Lapham C, Bacik I, Spies T, Bennink J (1994) MHC-encoded proteasome subunits LMP2 and LMP7 are not required for efficient antigen presentation. J Immunol 152:1163–1170PubMedGoogle Scholar
  65. 65.
    Cabrera T, Maleno I, Collado A, Lopez Nevot MA, Tait BD, Garrido F (2007) Analysis of HLA class I alterations in tumors: choosing a strategy based on known patterns of underlying molecular mechanisms. Tissue Antigens 69(Suppl 1):264–268PubMedCrossRefGoogle Scholar
  66. 66.
    Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N (2002) ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419:480–483PubMedCrossRefGoogle Scholar
  67. 67.
    Saric T, Chang SC, Hattori A, York IA, Markant S, Rock KL, Tsujimoto M, Goldberg AL (2002) An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 3:1169–1176PubMedCrossRefGoogle Scholar
  68. 68.
    Koopmann JO, Post M, Neefjes JJ, Hammerling GJ, Momburg F (1996) Translocation of long peptides by transporters associated with antigen processing (TAP). Eur J Immunol 26:1720–1728PubMedCrossRefGoogle Scholar
  69. 69.
    Seliger B, Ritz U, Ferrone S (2006) Molecular mechanisms of HLA class I antigen abnormalities following viral infection and transformation. Int J Cancer 118:129–138PubMedCrossRefGoogle Scholar
  70. 70.
    Nie Y, Yang G, Song Y, Zhao X, So C, Liao J, Wang LD, Yang CS (2001) DNA hypermethylation is a mechanism for loss of expression of the HLA class I genes in human esophageal squamous cell carcinomas. Carcinogenesis 22:1615–1623PubMedCrossRefGoogle Scholar
  71. 71.
    Rodriguez T, Mendez R, Del Campo A, Jimenez P, Aptsiauri N, Garrido F, Ruiz-Cabello F (2007) Distinct mechanisms of loss of IFN-gamma mediated HLA class I inducibility in two melanoma cell lines. BMC Cancer 7:34PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Fruci D, Ferracuti S, Limongi MZ, Cunsolo V, Giorda E, Fraioli R, Sibilio L, Carroll O, Hattori A, van Endert PM, Giacomini P (2006) Expression of endoplasmic reticulum aminopeptidases in EBV-B cell lines from healthy donors and in leukemia/lymphoma, carcinoma, and melanoma cell lines. J Immunol 176:4869–4879PubMedCrossRefGoogle Scholar
  73. 73.
    Kehlen A, Lendeckel U, Dralle H, Langner J, Hoang-Vu C (2003) Biological significance of aminopeptidase N/CD13 in thyroid carcinomas. Cancer Res 63:8500–8506PubMedGoogle Scholar
  74. 74.
    Menrad A, Speicher D, Wacker J, Herlyn M (1993) Biochemical and functional characterization of aminopeptidase N expressed by human melanoma cells. Cancer Res 53:1450–1455PubMedGoogle Scholar
  75. 75.
    Marks MS, Blum JS, Cresswell P (1990) Invariant chain trimers are sequestered in the rough endoplasmic reticulum in the absence of association with HLA class II antigens. J Cell Biol 111:839–855PubMedCrossRefGoogle Scholar
  76. 76.
    Roche PA, Cresswell P (1990) Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345:615–618PubMedCrossRefGoogle Scholar
  77. 77.
    Landsverk OJ, Bakke O, Gregers TF (2009) MHC II and the endocytic pathway: regulation by invariant chain. Scand J Immunol 70:184–193PubMedCrossRefGoogle Scholar
  78. 78.
    Riberdy JM, Newcomb JR, Surman MJ, Barbosa JA, Cresswell P (1992) HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360:474–477PubMedCrossRefGoogle Scholar
  79. 79.
    Mohan JF, Petzold SJ, Unanue ER (2011) Register shifting of an insulin peptide-MHC complex allows diabetogenic T cells to escape thymic deletion. J Exp Med 208:2375–2383PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Pu Z, Lovitch SB, Bikoff EK, Unanue ER (2004) T cells distinguish MHC-peptide complexes formed in separate vesicles and edited by H2-DM. Immunity 20:467–476PubMedCrossRefGoogle Scholar
  81. 81.
    Denzin LK, Cresswell P (1995) HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82:155–165PubMedCrossRefGoogle Scholar
  82. 82.
    Kropshofer H, Vogt AB, Moldenhauer G, Hammer J, Blum JS, Hammerling GJ (1996) Editing of the HLA-DR-peptide repertoire by HLA-DM. EMBO J 15:6144–6154PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Denzin LK, Sant’Angelo DB, Hammond C, Surman MJ, Cresswell P (1997) Negative regulation by HLA-DO of MHC class II-restricted antigen processing. Science 278:106–109PubMedCrossRefGoogle Scholar
  84. 84.
    Ham H, Sreelatha A, Orth K (2011) Manipulation of host membranes by bacterial effectors. Nat Rev Microbiol 9:635–646PubMedCrossRefGoogle Scholar
  85. 85.
    Muller S, Dennemarker J, Reinheckel T (2012) Specific functions of lysosomal proteases in endocytic and autophagic pathways. Biochim Biophys Acta 1824:34–43PubMedCrossRefGoogle Scholar
  86. 86.
    Hsing LC, Rudensky AY (2005) The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol Rev 207:229–241PubMedCrossRefGoogle Scholar
  87. 87.
    Maric MA, Taylor MD, Blum JS (1994) Endosomal aspartic proteinases are required for invariant-chain processing. Proc Natl Acad Sci USA 91:2171–2175PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Deussing J, Roth W, Saftig P, Peters C, Ploegh HL, Villadangos JA (1998) Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc Natl Acad Sci USA 95:4516–4521PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Tao K, Stearns NA, Dong J, Wu QL, Sahagian GG (1994) The proregion of cathepsin L is required for proper folding, stability, and ER exit. Arch Biochem Biophys 311:19–27PubMedCrossRefGoogle Scholar
  90. 90.
    Coulombe R, Grochulski P, Sivaraman J, Menard R, Mort JS, Cygler M (1996) Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J 15:5492–5503PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Turk B, Dolenc I, Lenarcic B, Krizaj I, Turk V, Bieth JG, Bjork I (1999) Acidic pH as a physiological regulator of human cathepsin L activity. Eur J Biochem 259:926–932PubMedCrossRefGoogle Scholar
  92. 92.
    Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos JA, Ploegh H, Peters C, Rudensky AY (1998) Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280:450–453PubMedCrossRefGoogle Scholar
  93. 93.
    Shi GP, Villadangos JA, Dranoff G, Small C, Gu L, Haley KJ, Riese R, Ploegh HL, Chapman HA (1999) Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10:197–206PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Manoury B, Hewitt EW, Morrice N, Dando PM, Barrett AJ, Watts C (1998) An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396:695–699PubMedCrossRefGoogle Scholar
  95. 95.
    Antoniou AN, Blackwood SL, Mazzeo D, Watts C (2000) Control of antigen presentation by a single protease cleavage site. Immunity 12:391–398PubMedCrossRefGoogle Scholar
  96. 96.
    Manoury B, Mazzeo D, Fugger L, Viner N, Ponsford M, Streeter H, Mazza G, Wraith DC, Watts C (2002) Destructive processing by asparagine endopeptidase limits presentation of a dominant T cell epitope in MBP. Nat Immunol 3:169–174PubMedCrossRefGoogle Scholar
  97. 97.
    Manoury B, Mazzeo D, Li DN, Billson J, Loak K, Benaroch P, Watts C (2003) Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18:489–498PubMedCrossRefGoogle Scholar
  98. 98.
    Bevec T, Stoka V, Pungercic G, Dolenc I, Turk V (1996) Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J Exp Med 183:1331–1338PubMedCrossRefGoogle Scholar
  99. 99.
    Zavasnik-Bergant V, Schweiger A, Bevec T, Golouh R, Turk V, Kos J (2004) Inhibitory p41 isoform of invariant chain and its potential target enzymes cathepsins L and H in distinct populations of macrophages in human lymph nodes. Immunology 112:378–385PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Storm van’s Gravesande K, Layne MD, Ye Q, Le L, Baron RM, Perrella MA, Santambrogio L, Silverman ES, Riese RJ (2002) IFN regulatory factor-1 regulates IFN-gamma-dependent cathepsin S expression. J Immunol 168:4488–4494PubMedCrossRefGoogle Scholar
  101. 101.
    Thibodeau J, Bourgeois-Daigneault MC, Lapointe R (2012) Targeting the MHC Class II antigen presentation pathway in cancer immunotherapy. Oncoimmunology 1:908–916PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Durrant LG, Ballantyne KC, Armitage NC, Robins RA, Marksman R, Hardcastle JD, Baldwin RW (1987) Quantitation of MHC antigen expression on colorectal tumours and its association with tumour progression. Br J Cancer 56:425–432PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Tabibzadeh SS, Sivarajah A, Carpenter D, Ohlsson-Wilhelm BM, Satyaswaroop PG (1990) Modulation of HLA-DR expression in epithelial cells by interleukin 1 and estradiol-17 beta. J Clin Endocrinol Metab 71:740–747PubMedCrossRefGoogle Scholar
  104. 104.
    Dazzi F, D’Andrea E, Biasi G, De Silvestro G, Gaidano G, Schena M, Tison T, Vianello F, Girolami A, Caligaris-Cappio F (1995) Failure of B cells of chronic lymphocytic leukemia in presenting soluble and alloantigens. Clin Immunol Immunopathol 75:26–32PubMedCrossRefGoogle Scholar
  105. 105.
    Degener T, Momburg F, Moller P (1988) Differential expression of HLA-DR, HLA-DP, HLA-DQ and associated invariant chain (Ii) in normal colorectal mucosa, adenoma and carcinoma. Virchows Arch A Pathol Anat Histopathol 412:315–322PubMedCrossRefGoogle Scholar
  106. 106.
    Thompson JA, Srivastava MK, Bosch JJ, Clements VK, Ksander BR, Ostrand-Rosenberg S (2008) The absence of invariant chain in MHC II cancer vaccines enhances the activation of tumor-reactive type 1 CD4+ T lymphocytes. Cancer Immunol Immunother 57:389–398PubMedCrossRefGoogle Scholar
  107. 107.
    Frolich D, Blassfeld D, Reiter K, Giesecke C, Daridon C, Mei HE, Burmester GR, Goldenberg DM, Salama A, Dorner T (2012) The anti-CD74 humanized monoclonal antibody, milatuzumab, which targets the invariant chain of MHC II complexes, alters B-cell proliferation, migration, and adhesion molecule expression. Arthritis Res Ther 14:R54PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Werle B, Staib A, Julke B, Ebert W, Zladoidsky P, Sekirnik A, Kos J, Spiess E (1999) Fluorometric microassays for the determination of cathepsin L and cathepsin S activities in tissue extracts. Biol Chem 380:1109–1116PubMedCrossRefGoogle Scholar
  109. 109.
    Kos J, Sekirnik A, Kopitar G, Cimerman N, Kayser K, Stremmer A, Fiehn W, Werle B (2001) Cathepsin S in tumours, regional lymph nodes and sera of patients with lung cancer: relation to prognosis. Br J Cancer 85:1193–1200PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Turk V, Turk B, Guncar G, Turk D, Kos J (2002) Lysosomal cathepsins: structure, role in antigen processing and presentation, and cancer. Adv Enzyme Regul 42:285–303PubMedCrossRefGoogle Scholar
  111. 111.
    Felix K, Gaida MM (2016) Neutrophil-derived proteases in the microenvironment of pancreatic cancer—active players in tumor progression. Int J Biol Sci 12(3):302–313PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Hajjar E, Broemstrup T, Kantari C, Witko-Sarsat V, Reuter N (2010) Structures of human proteinase 3 and neutrophil elastase–so similar yet so different. FEBS J277:2238–2254CrossRefGoogle Scholar
  113. 113.
    Sun Z, Yang P (2004) Role of imbalance between neutrophil elastase and alpha 1-antitrypsin in cancer development and progression. Lancet Oncol 5:182–190PubMedCrossRefGoogle Scholar
  114. 114.
    Gaida MM, Steffen TG, Gunther F, Tschaharganeh DF, Felix K, Bergmann F, Schirmacher P, Hansch GM (2012) Polymorphonuclear neutrophils promote dyshesion of tumor cells and elastase-mediated degradation of E-cadherin in pancreatic tumors. Eur J Immunol 42:3369–3380PubMedCrossRefGoogle Scholar
  115. 115.
    Tan GJ, Peng ZK, Lu JP, Tang FQ (2013) Cathepsins mediate tumor metastasis. World J Biol Chem 4:91–101PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Wiedow O, Meyer-Hoffert U (2005) Neutrophil serine proteases: potential key regulators of cell signalling during inflammation. J Intern Med 257:319–328PubMedCrossRefGoogle Scholar
  117. 117.
    Padrines M, Wolf M, Walz A, Baggiolini M (1994) Interleukin-8 processing by neutrophil elastase, cathepsin G and proteinase-3. FEBS Lett 352:231–235PubMedCrossRefGoogle Scholar
  118. 118.
    Chertov O, Ueda H, Xu LL, Tani K, Murphy WJ, Wang JM, Howard OM, Sayers TJ, Oppenheim JJ (1997) Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J Exp Med 186:739–747PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Valkovskaya N, Kayed H, Felix K, Hartmann D, Giese NA, Osinsky SP, Friess H, Kleeff J (2007) ADAM8 expression is associated with increased invasiveness and reduced patient survival in pancreatic cancer. J Cell Mol Med 11:1162–1174PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Stocker W, Bode W (1995) Structural features of a superfamily of zinc-endopeptidases: the metzincins. Curr Opin Struct Biol 5:383–390PubMedCrossRefGoogle Scholar
  121. 121.
    Krampert M, Kuenzle S, Thai SN, Lee N, Iruela-Arispe ML, Werner S (2005) ADAMTS1 proteinase is up-regulated in wounded skin and regulates migration of fibroblasts and endothelial cells. J Biol Chem 280:23844–23852PubMedCrossRefGoogle Scholar
  122. 122.
    Decock J, Obermajer N, Vozelj S, Hendrickx W, Paridaens R, Kos J (2008) Cathepsin B, cathepsin H, cathepsin X and cystatin C in sera of patients with early-stage and inflammatory breast cancer. Int J Biol Markers 23(3):161–168PubMedCrossRefGoogle Scholar
  123. 123.
    Jevnikar Z, Obermajer N, Bogyo M, Kos J (2008) The role of cathepsin X in the migration and invasiveness of T lymphocytes. J Cell Sci 121(16):2652–2661PubMedCrossRefGoogle Scholar
  124. 124.
    Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84(3):359–369PubMedCrossRefGoogle Scholar
  125. 125.
    Kos J, Jevnikar Z, Obermajer N (2009) The role of cathepsin X in cell signaling. Cell Adh Migr 3(2):164–166PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Bauer S, Groh V, Wu J (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727–729PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, Stevanovic S, Rammensee HG, Steinle A (2008) Tumor-associated MICA Is Shed by ADAM proteases. Cancer Res 68(15):6368–6376PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Ding Y, Xu D, Feng G, Bushell A, Muschel RJ, Wood KJ (2009) Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and −9. Diabetes 58:1797–1806PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Lee BK, Kim MJ, Jang HS, Lee HR, Ahn KM, Lee JH, Choung PH (2008) A high concentration of MMP-2/gelatinase A and MMP-9/gelatinase B reduce NK cell-mediated cytotoxicity against an oral squamous cell carcinoma cell line. In Vivo 22:593–597PubMedGoogle Scholar
  130. 130.
    Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D (2004) Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 103:4619–4621PubMedCrossRefGoogle Scholar
  131. 131.
    Sharma S, Yang SC, Zhu L, Reckamp K, Gardner B, Baratelli F, Huang M, Batra RK, Dubinett SM (2005) Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 65:5211–5220PubMedCrossRefGoogle Scholar
  132. 132.
    Ma X, Kundu N, Rifat S, Walser T, Fulton AM (2006) Prostaglandin E receptor EP4 antagonism inhibits breast cancer metastasis. Cancer Res 66:2923–2927PubMedCrossRefGoogle Scholar
  133. 133.
    Kundu N, Ma X, Holt D, Goloubeva O, Ostrand-Rosenberg S, Fulton AM (2009) Antagonism of the prostaglandin E receptor EP4 inhibits metastasis and enhances NK function. Breast Cancer Res Treat 117:235–242PubMedCrossRefGoogle Scholar
  134. 134.
    Peng YP, Zhang JJ, Liang WB, Tu M, Lu ZP, Wei JS, Jiang KR, Gao WT, Wu JL, Xu ZK, Miao Y, Zhu Y (2014) Elevation of MMP-9 and IDO induced by pancreatic cancer cells mediates natural killer cell dysfunction. BMC Cancer 14:738PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Liu Q, Sun Y, Rihn S, Nolting A, Tsoukas PN, Jost S, Cohen K, Walker B, Alter G (2009) Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J Virol 83(17):8705–8712PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Park Y, Jin HS, Aki D et al (2014) The ubiquitin system in immuneregulation. Adv Immunol 124:17–66PubMedCrossRefGoogle Scholar
  137. 137.
    Malynn BA, Ma A (2010) Ubiquitin makes its mark on immune regulation. Immunity 33:843–852PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Van Loosdregt J, Fleskens V, Fu J et al (2013) Foxp3 by the deubiquitinase USP7 increases Treg-cell-suppressive capacity. Immunity 39:259–271PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Shen M, Schmitt S, Buac D et al (2013) Targeting the ubiquitin-proteasome system for cancer therapy. Expert Opin Ther Targets 17:1091–1108PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Harhaj EW, Dixit VM (2011) Deubiquitinases in the regulation of NF-κB signaling. Cell Res 21:22–39PubMedCrossRefGoogle Scholar
  141. 141.
    Coornaert B, Baens M, Heyninck K et al (2008) T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nat Immunol 9:263–271PubMedCrossRefGoogle Scholar
  142. 142.
    Düwel M, Welteke V, Oeckinghaus A et al (2009) A20 negatively regulates T cell receptor signaling to NF-kappaB by cleaving Malt1 ubiquitin chains. J Immunol 182:7718–7728PubMedCrossRefGoogle Scholar
  143. 143.
    Ferch U, Kloo B, Gewies A et al (2009) Inhibition of MALT1 protease activity is selectively toxic for activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 206:2313–2320PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Compagno M, Lim WK, Grunn A et al (2009) Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 459:717–721PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Schmitz R, Hansmann ML, Bohle V et al (2009) TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med 206:981–989PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Goedegebuure P, Mitchem JB, Porembka MR et al (2011) Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr Cancer Drug Targets 11:734–751PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Yu J, Du W, Yan F, Wang Y et al (2013) Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol 190:3783–3797PubMedCrossRefGoogle Scholar
  148. 148.
    Shao B, Wei X, Luo M et al (2015) Inhibition of A20 expression in tumor microenvironment exerts anti-tumor effect through inducing myeloid-derived suppressor cells apoptosis. Sci Rep 5:16437PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Stromnes IM, Blattman JN, Tan X et al (2010) Abrogating Cbl-b in effector CD8 (+) T cells improves the efficacy of adoptive therapy of leukemia in mice. J Clin Invest 120:3722–3734PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Abir K. Panda
    • 1
  • Sreeparna Chakraborty
    • 1
  • Kirti Kajal
    • 1
  • Dia Roy
    • 1
  • Tania Sarkar
    • 1
  • Gaurisankar Sa
    • 1
  1. 1.Division of Molecular MedicineBose InstituteKolkataIndia

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