Advertisement

Biochemistry (Moscow)

, Volume 82, Issue 5, pp 542–555 | Cite as

Types of immune-inflammatory responses as a reflection of cell–cell interactions under conditions of tissue regeneration and tumor growth

  • L. A. Tashireva
  • V. M. Perelmuter
  • V. N. Manskikh
  • E. V. DenisovEmail author
  • O. E. Savelieva
  • E. V. Kaygorodova
  • M. V. Zavyalova
Review

Abstract

Inflammatory infiltration of tumor stroma is an integral reflection of reactions that develop in response to any damage to tumor cells including immune responses to antigens or necrosis caused by vascular disorders. In this review, we use the term “immune-inflammatory response” (IIR) that allows us to give an integral assessment of the cellular composition of the tumor microenvironment. Two main types of IIRs are discussed: type 1 and 2 T-helper reactions (Th1 and Th2), as well as their inducers: immunosuppressive responses and reactions mediated by Th22 and Th17 lymphocytes and capable of modifying the main types of IIRs. Cellular and molecular manifestations of each IIR type are analyzed and their general characteristics and roles in tissue regeneration and tumor growth are presented. Since inflammatory responses in a tumor can also be initiated by innate immunity mechanisms, special attention is given to inflammation based on them. We emphasize that processes accompanying tissue regeneration are prototypes of processes underlying cancer progression, and these processes have the same cellular and molecular substrates. We focus on evidence that tumor progression is mainly contributed by processes specific for the second phase of “wound healing” that are based on the Th2-type IIR. We emphasize that the effect of various types of immune and stroma cells on tumor progression is determined by the ability of the cells and their cytokines to promote or prevent the development of Th1- or Th2-type of IIR. Finally, we supposed that the nonspecific influence on the tumor caused by the cytokine context of the Th1- or Th2-type microenvironment should play a decisive role for suppression or stimulation of tumor growth and metastasis.

Keywords

immune-inflammatory response lymphocyte subpopulations macrophages fibroblasts tissue regeneration tumor progression 

Abbreviations

CCL

C-C motif ligand

CTL

cytotoxic lymphocytes

CXCL

chemokine (C-X-C motif) ligand

DAMP

damage-associated molecular pattern

DC

dendritic cells

EMT

epithelial–mesenchymal transition

GM-CSF

granulocyte-macrophage colony-stimulating factor 2

IFN

interferon

IIR

immune-inflammatory response

IL

interleukin

ILC

innate lymphoid cells

MDSC

myeloid-derived suppressor cells

NK

natural killers

NOS

nitric oxide synthase

PAMP

pathogen-associated molecular pattern

PGE2

prostaglandin E2

TAM

tumor associated macrophages

TCR

T-cell receptor

TGF-β

transforming growth factor β

Th

T helper

TLR

Toll-like receptor

Treg

regulatory T cell

VEGF

vascular endothelial growth factor

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Coussens, L. M., and Werb, Z. (2002) Inflammation and cancer, Nature, 420, 860–867.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Grivennikov, S. I., Greten, F. R., and Karin, M. (2010) Immunity, inflammation, and cancer, Cell, 140, 883–899.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Burgio, E., and Migliore, L. (2015) Towards a systemic paradigm in carcinogenesis: linking epigenetics and genetics, Mol. Biol. Rep., 42, 777–790.PubMedCrossRefGoogle Scholar
  4. 4.
    Khansari, N., Shakiba, Y., and Mahmoudi, M. (2009) Chronic inflammation and oxidative stress as a major cause of agerelated diseases and cancer, Recent Pat. Inflamm. Allergy Drug Discov., 3, 73–80.PubMedCrossRefGoogle Scholar
  5. 5.
    Khan, S., Jain, M., Mathur, V., and Feroz, S. M. (2016) Chronic inflammation and cancer: paradigm on tumor progression, metastasis and therapeutic intervention, Gulf J. Oncol., 1, 86–93.Google Scholar
  6. 6.
    Bondar, T., and Medzhitov, R. (2013) The origins of tumorpromoting inflammation, Cancer Cell, 24, 143–144.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Rakoff-Nahoum, S., and Medzhitov, R. (2008) Role of tolllike receptors in tissue repair and tumorigenesis, Biochemistry (Moscow), 73, 555–561.CrossRefGoogle Scholar
  8. 8.
    Dvorak, H. F. (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing, N. Engl. J. Med., 315, 1650–1659.PubMedCrossRefGoogle Scholar
  9. 9.
    Eming, S. A., Krieg, T., and Davidson, J. M. (2007) Inflammation in wound repair: molecular and cellular mechanisms, J. Invest. Dermatol., 127, 514–525.PubMedCrossRefGoogle Scholar
  10. 10.
    Blanpain, C., and Fuchs, E. (2014) Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration, Science, 344, 1242281.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Arnold, K. M., Opdenaker, L. M., Flynn, D., and Sims-Mourtada, J. (2015) Wound healing and cancer stem cells: inflammation as a driver of treatment resistance in breast cancer, Cancer Growth Metast., 8, 1–13.Google Scholar
  12. 12.
    Arbach, H., Viglasky, V., Lefeu, F., Guinebretiere, J.-M., Ramirez, V., Bride, N., Boualaga, N., Bauchet, T., Peyrat, J.-P., Mathieu, M.-C., Mourah, S., Podgorniak, M.-P., Seignerin, J.-M., Takada, K., and Joab, I. (2006) Epstein–Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol), J. Virol., 80, 845–853.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Li, Y. Y., Ge, Q. X., Cao, J., Zhou, Y. J., Du, Y. L., Shen, B., Wan, Y. J., and Nie, Y. Q. (2016) Association of Fusobacterium nucleatum infection with colorectal cancer in Chinese patients, World J. Gastroenterol., 22, 3227–3233.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Zhang, Q., Jia, Q., Deng, T., Song, B., and Li, L. (2015) Heterogeneous expansion of CD4+ tumorinfiltrating T-lymphocytes in clear cell renal cell carcinomas, Biochem. Biophys. Res. Commun., 458, 70–76.PubMedCrossRefGoogle Scholar
  15. 15.
    Dieu-Nosjean, M. C., Goc, J., Giraldo, N. A., Sautes-Fridman, C., and Fridman, W. H. (2014) Tertiary lymphoid structures in cancer and beyond, Trends Immunol., 35, 571–580.PubMedCrossRefGoogle Scholar
  16. 16.
    Brucklacher-Waldert, V., Carr, E. J., Linterman, M. A., and Veldhoen, M. (2014) Cellular plasticity of CD4+ T cells in the intestine, Front. Immunol., 5, 488–499.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Caza, T., and Landas, S. (2015) Functional and phenotypic plasticity of CD4+ T cell subsets, Biomed Res. Int., 521957.Google Scholar
  18. 18.
    Werb, Z., and Lu, P. (2015) The role of stroma in tumor development, Cancer J., 21, 250–253.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Portou, M. J., Baker, D., Abraham, D., and Tsui, J. (2015) The innate immune system, Tolllike receptors and dermal wound healing: a review, Vascul. Pharmacol., 71, 31–36.PubMedCrossRefGoogle Scholar
  20. 20.
    Moore, K. W., De Waal Malefyt, R., Coffman, R. L., and O’Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor, Annu. Rev. Immunol., 19, 683–765.PubMedCrossRefGoogle Scholar
  21. 21.
    Sionov, R. V., Fridlender, Z. G., and Granot, Z. (2015) The multifaceted roles neutrophils play in the tumor microenvironment, Cancer Microenviron., 8, 125–158.PubMedCrossRefGoogle Scholar
  22. 22.
    Artis, D., and Spits, H. (2015) The biology of innate lymphoid cells, Nature, 517, 293–301.PubMedCrossRefGoogle Scholar
  23. 23.
    Bernink, J. H., Peters, C. P., Munneke, M., te Velde, A. A., Meijer, S. L., Weijer, K., Hreggvidsdottir, H. S., Heinsbroek, S. E., Legrand, N., Buskens, C. J., Bemelman, W. A., Mjosberg, J. M., and Spits, H. (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues, Nat. Immunol., 14, 221–229.PubMedCrossRefGoogle Scholar
  24. 24.
    Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C., Kane, C. M., Fallon, P. G., Pannell, R., Jolin, H. E., and McKenzie, A. N. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity, Nature, 464, 1367–1370.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Buonocore, S., Ahern, P. P., Uhlig, H. H., Ivanov, I. I., Littman, D. R., Maloy, K. J., and Powrie, F. (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology, Nature, 464, 1371–1375.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Vremec, D., and Shortman, K. (2015) What’s in a name? Some early and current issues in dendritic cell nomenclature, Front. Immunol., 6, 267.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Nizzoli, G., Krietsch, J., Weick, A., Steinfelder, S., Facciotti, F., Gruarin, P., Bianco, A., Steckel, B., Moro, M., Crosti, M., Romagnani, C., Stolzel, K., Torretta, S., Pignataro, L., Scheibenbogen, C., Neddermann, P., De Francesco, R., Abrignani, S., and Geginat, J. (2013) Human CD1c+ dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses, Blood, 122, 932–942.PubMedCrossRefGoogle Scholar
  28. 28.
    Hemont, C., Neel, A., Heslan, M., Braudeau, C., and Josien, R. (2013) Human blood mDC subsets exhibit distinct TLR repertoire and responsiveness, J. Leukoc. Biol., 93, 599–609.PubMedCrossRefGoogle Scholar
  29. 29.
    Suga, H., Sugaya, M., Fujita, H., Asano, Y., Tada, Y., Kadono, T., and Sato, S. (2014) TLR4, rather than TLR2, regulates wound healing through TGF-β and CCL5 expression, J. Dermatol. Sci., 73, 117–124.PubMedCrossRefGoogle Scholar
  30. 30.
    Spits, H., and Di Santo, J. P. (2011) The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling, Nat. Immunol., 12, 21–27.PubMedCrossRefGoogle Scholar
  31. 31.
    Gonzalez-Reyes, S., Marin, L., Gonzalez, L., Gonzalez, L. O., del Casar, J. M., Lamelas, M. L., Gonzalez-Quintana, J. M., and Vizoso, F. J. (2010) Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis, BMC Cancer, 10, 665.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Voelcker, V., Gebhardt, C., Averbeck, M., Saalbach, A., Wolf, V., Weih, F., Sleeman, J., Anderegg, U., and Simon, J. (2008) Hyaluronan fragments induce cytokine and metalloprotease upregulation in human melanoma cells in part by signaling via TLR4, Exp. Dermatol., 17, 100–107.PubMedCrossRefGoogle Scholar
  33. 33.
    Liao, S. J., Zhou, Y. H., Yuan, Y., Li D., Wu, F. H., Wang, Q., Zhu, J. H., Yan, B., Wei, J. J., Zhang, G. M., and Feng Z. H. (2012) Triggering of Tolllike receptor 4 on metastatic breast cancer cells promotes ανβ3-mediated adhesion and invasive migration, Breast Cancer Res. Treat., 133, 853–863.PubMedCrossRefGoogle Scholar
  34. 34.
    Jing, Y. Y., Han, Z. P., Sun, K., Zhang, S. S., Hou, J., Liu, Y., Li, R., Gao, L., Zhao, X., Zhao, Q. D., Wu, M. C., and Wei, L. X. (2012) Tolllike receptor 4 signaling promotes epithelialmesenchymal transition in human hepatocellular carcinoma induced by lipopolysaccharide, BMC Med., 10, 98.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Liu, C. Y., Xu, J. Y., Shi, X. Y., Huang, W., Ruan, T. Y., Xie, P., and Ding, J. L. (2013) M2-polarized tumorassociated macrophages promoted epithelialmesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway, Lab. Invest., 93, 844–854.PubMedCrossRefGoogle Scholar
  36. 36.
    Elinav, E., Nowarski, R., Thaiss, C. A., Hu, B., Jin, C., and Flavell, R. A. (2013) Inflammationinduced cancer: crosstalk between tumors, immune cells and microorganisms, Nat. Rev. Cancer, 13, 759–771.PubMedCrossRefGoogle Scholar
  37. 37.
    Gajewski, F., Schreiber, H., and Fu, Y.-X. (2013) Innate and adaptive immune cells in the tumor microenvironment, Nat. Immunol., 14, 1014–1022.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Balkwill, F. R., Capasso, M., and Hagemann, T. (2012) The tumor microenvironment at a glance, J. Cell Sci., 125, 5591–5596.PubMedCrossRefGoogle Scholar
  39. 39.
    Shields, J. D., Kourtis, I. C., Tomei, A. A., Roberts, J. M., and Swartz, M. A. (2010) Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21, Science, 328, 749–752.PubMedCrossRefGoogle Scholar
  40. 40.
    Eisenring, M., vom Berg, J., Kristiansen, G., Saller, E., and Becher, B. (2010) IL-12 initiates tumor rejection via lymphoid tissueinducer cells bearing the natural cytotoxicity receptor NKp46, Nat. Immunol., 11, 1030–1038.PubMedCrossRefGoogle Scholar
  41. 41.
    Braumuller, H., Wieder, T., Brenner, E., Abmann, S., Hahn, M., Alkhaled, M., Schilbach, K., Essmann, F., Kneilling, M., Griessinger, C., Ranta, F., Ullrich, S., Mocikat, R., Braungart, K., Mehra, T., Fehrenbacher, B., Berdel, J., Niessner, H., Meier, F., van den Broek, M., Haring, H. U., Handgretinger, R., Quintanilla-Martinez, L., Fend, F., Pesic, M., Bauer, J., Zender, L., Schaller, M., Schulze-Osthoff, K., and Rocken, M. (2013) T-helper-1-cell cytokines drive cancer into senescence, Nature, 494, 361–365.PubMedCrossRefGoogle Scholar
  42. 42.
    Tachibana, T., Onodera, H., Tsuruyama, T., Mori, A., Nagayama, S., Hiai, H., and Imamura, M. (2005) Increased intratumor Valpha24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas, Clin. Cancer Res., 11, 7322–7327.PubMedCrossRefGoogle Scholar
  43. 43.
    Fridman, W. H., Pages, F., Sautes-Fridman, C., and Galon, J. (2012) The immune contexture in human tumors: impact on clinical outcome, Nat. Rev. Cancer, 12, 298–306.PubMedCrossRefGoogle Scholar
  44. 44.
    Jia, L, and Wu, C. (2014) The biology and functions of Th22 cells, Adv. Exp. Med. Biol., 841, 209–230.PubMedCrossRefGoogle Scholar
  45. 45.
    Fujita, H., Nograles, K. E., Kikuchi, T., Gonzalez, J., Carucci, J. A., and Krueger, J. G. (2009) Human Langerhans cells induce distinct IL-22-producing CD4+ T cells lacking IL-17 production, Proc. Natl. Acad. Sci. USA, 106, 21795–21800.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Simonian, P. L., Wehrmann, F., Roark, C. L., Born, W. K., O’Brien, R. L., and Fontenot, A. P. (2010) γδ T cells protect against lung fibrosis via IL-22, J. Exp. Med., 207, 2239–2253.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Wolk, K., Kunz, S., Asadullah, K., and Sabat, R. (2002) Cutting edge: immune cells as sources and targets of the IL-10 family members? J. Immunol., 168, 5397–5402.PubMedCrossRefGoogle Scholar
  48. 48.
    Sabat, R., Witte, E., Witte, K., and Wolk, K. (2013) in IL-17, IL-22 and Their Producing Cells: Role in Inflammation and Autoimmunity, Springer, Basel, pp. 3–131.Google Scholar
  49. 49.
    Wolk, K., Witte, E., Witte, K., Warszawska, K., and Sabat, R. (2010) Biology of interleukin-22, Semin. Immunopathol., 32, 17–31.PubMedCrossRefGoogle Scholar
  50. 50.
    Eyerich, S., Eyerich, K., Pennino, D., Carbone, T., Nasorri, F., Pallotta, S., Cianfarani, F., Odorisio, T., Traidl-Hoffmann, C., Behrendt, H., Durham, S. R., Schmidt-Weber, C. B., and Cavani, A. (2009) Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling, J. Clin. Invest., 119, 3573–3585.PubMedPubMedCentralGoogle Scholar
  51. 51.
    McGee, H. M., Schmidt, B. A., Booth, C. J., Yancopoulos, G. D., Valenzuela, D. M., Murphy, A. J., Stevens, S., Flavell, R. A., and Horsley, V. (2013) IL-22 promotes fibroblastmediated wound repair in the skin, J. Invest. Dermatol., 133, 1321–1329.PubMedCrossRefGoogle Scholar
  52. 52.
    Reuss, B., Dono, R., and Unsicker, K. (2003) Functions of fibroblast growth factor (FGF)-2 and FGF-5 in astroglial differentiation and bloodbrain barrier permeability: evidence from mouse mutants, J. Neurosci., 23, 6404–6412.PubMedGoogle Scholar
  53. 53.
    Varga, J., and Abraham, D. (2007) Systemic sclerosis: a prototypic multisystem fibrotic disorder, J. Clin. Invest., 117, 557–567.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Hwang, J., Son, K. N., Kim, C. W., Ko, J., Na, D. S., Kwon, B. S., Gho, Y. S., and Kim, J. (2005) Human CC chemokine CCL23, a ligand for CCR1, induces endothelial cell migration and promotes angiogenesis, Cytokine, 30, 254–263.PubMedCrossRefGoogle Scholar
  55. 55.
    Kirchberger, S., Royston, D. J., Boulard, O., Thornton, E., Franchini, F., Szabady, R. L., Harrison, O., and Powrie, F. (2013) Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model, J. Exp. Med., 210, 917–931.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Takahashi, H., Numasaki, M., Lotze, M. T., and Sasaki, H. (2005) Interleukin-17 enhances bFGF, HGF-and VEGF-induced growth of vascular endothelial cells, Immunol. Lett., 98, 189–193.PubMedCrossRefGoogle Scholar
  57. 57.
    Numasaki, M., Fukushi, J., Ono, M., Narula, S. K., Zavodny, P. J., Kudo, T., Robbins, P. D., Tahara, H., and Lotze, M. T. (2003) Interleukin-17 promotes angiogenesis and tumor growth, Blood, 101, 2620–2627.PubMedCrossRefGoogle Scholar
  58. 58.
    Liao, Y., Wang, B., Huang, Z. L., Shi, M., Yu, X. J., Zheng, L., Li, S., and Li, L. (2013) Increased circulating Th17 cells after transarterial chemoembolization correlate with improved survival in stage III hepatocellular carcinoma: a prospective study, PLoS One, 8, e60444.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Zhu, J., and Paul, W. E. (2008) CD4 T cells: fates, functions, and faults, Blood, 112, 1557.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Zhang, Y., Zhang, Y., Gu, W., He, L., and Sun, B. (2014) Th1/Th2 cell’s function in immune system, Adv. Exp. Med. Biol., 841, 45.PubMedCrossRefGoogle Scholar
  61. 61.
    Sica, A., and Mantovani, A. (2012) Macrophage plasticity and polarization: in vivo veritas, J. Clin. Invest., 122, 787–795.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Martinez, F. O., and Gordon, S. (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment, F1000Prime Rep., 6, 13.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Scapini, P., Lapinet-Vera, J. A., Gasperini, S., Calzetti, F., Bazzoni, F., and Cassatella, M. A. (2000) The neutrophil as a cellular source of chemokines, Immunol. Rev., 177, 195–203.PubMedCrossRefGoogle Scholar
  64. 64.
    Fridlender, Z. G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., Worthen, G. S., and Albelda, S. M. (2009) Polarization of tumorassociated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN, Cancer Cell, 16, 183–194.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Sindrilaru, A., Peters, T., Wieschalka, S., Baican, C., Baican, A., Peter, H., Hainzl, A., Schatz, S., Qi, Y., Schlecht, A., Weiss, J. M., Wlaschek, M., Sunderkotter, C., and Scharffetter-Kochanek, K. (2011) An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice, J. Clin. Invest., 121, 985–997.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Barrientos, S., Stojadinovic, O., Golinko, M. S., Brem, H., and Tomic-Canic, M. (2008) Growth factors and cytokines in wound healing, Wound Rep. Regen., 16, 585–601.CrossRefGoogle Scholar
  67. 67.
    Wieder, T., Braumuller, H., Kneilling, M., Pichler, B., and Rocken, M. (2008) T cellmediated help against tumors, Cell Cycle, 7, 2974–2977.PubMedCrossRefGoogle Scholar
  68. 68.
    Hensbergen, P. J., Wijnands, P. G. B., Schreurs, M. W., Scheper, R. J., Willemze, R., and Tensen, C. P. (2005) The CXCR3 targeting chemokine CXCL11 has potent antitumor activity in vivo involving attraction of CD8+ T lymphocytes but not inhibition of angiogenesis, J. Immunother., 28, 343–351.PubMedCrossRefGoogle Scholar
  69. 69.
    Morishima, N., Owaki, T., Asakawa, M., Kamiya, S., Mizuguchi, J., and Yoshimoto, T. (2005) Augmentation of effector CD8+ T cell generation with enhanced granzyme B expression by IL-27, J. Immunol., 175, 1686–1693.PubMedCrossRefGoogle Scholar
  70. 70.
    Shen, M., Hu, P., Donskov, F., Wang, G., Liu, Q., and Du, J. (2014) Tumorassociated neutrophils as a new prognostic factor in cancer: a systematic review and metaanalysis, PLoS One, 9, e98259.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Muranski, P., Boni, A., Antony, P. A., Cassard, L., Irvine, K. R., Kaiser, A., Paulos, C. M., Palmer, D. C., Touloukian, C. E., Ptak, K., Gattinoni, L., Wrzesinski, C., Hinrichs, C. S., Kerstann, K. W., Feigenbaum, L., Chan, C. C., and Restifo, N. P. (2008) Tumorspecific Th17-polarized cells eradicate large established melanoma, Blood, 112, 362–373.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Roberts, S. J., Ng, B. Y., Filler, R. B., Lewis, J., Glusac, E. J., Hayday, A. C., Tigelaar, R. E., and Girardi, M. (2007) Characterizing tumorpromoting T cells in chemically induced cutaneous carcinogenesis, Proc. Natl. Acad. Sci. USA, 104, 6770–6775.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Duffield, J. S., Lupher, M., Thannickal, V. J., and Wynn, T. A. (2013) Host responses in tissue repair and fibrosis, Annu. Rev. Pathol., 8, 241–276.PubMedCrossRefGoogle Scholar
  74. 74.
    Kuang, D. M., Zhao, Q., Peng, C., Xu, J., Zhang, J. P., Wu, C., and Zheng, L. (2009) Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1, J. Exp. Med., 206, 1327–1337.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Eming, S. A., Martin, P., and Tomic-Canic, M. (2014) Wound repair and regeneration: mechanisms, signaling, and translation, Sci. Transl. Med., 6, 265.CrossRefGoogle Scholar
  76. 76.
    Ferrante, C. J., and Leibovich, S. J. (2012) Regulation of macrophage polarization and wound healing, Adv. Wound Care (New Rochelle), 1, 10–16.CrossRefGoogle Scholar
  77. 77.
    Dong, H. P., Elstrand, M. B., Holth, A., Silins, I., Berner, A., Trope, C. G., Davidson, B., and Risberg, B. (2006) NK-and B-cell infiltration correlates with worse outcome in metastatic ovarian carcinoma, Am. J. Clin. Pathol., 125, 451–458.PubMedCrossRefGoogle Scholar
  78. 78.
    Olkhanud, P. B., Damdinsuren, B., Bodogai, M., Gress, R. E., Sen, R., Wejksza, K., Malchinkhuu, E., Wersto, R. P., and Biragyn, A. (2011) Tumorevoked regulatory B cells promote breast cancer metastasis by converting resting CD4+ T cells to T-regulatory cells, Cancer Res., 71, 3505–3515.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Barbera-Guillem, E., Nelson M. B., Barr, B., Nyhus, J. K., May, K. F., Jr., Feng, L., and Sampsel, J. W. (2000) B lymphocyte pathology in human colorectal cancer. Experimental and clinical therapeutic effects of partial B cell depletion, Cancer Immunol. Immunother., 48, 541–549.PubMedCrossRefGoogle Scholar
  80. 80.
    Nielsen, J. S., Sahota, R. A., Milne, K., Kost, S. E., Nesslinger, N. J., Watson, P. H., and Nelson, B. H. (2012) CD20+ tumorinfiltrating lymphocytes have an atypical CD27 memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer, Clin. Cancer Res., 18, 3281–3292.PubMedCrossRefGoogle Scholar
  81. 81.
    Van Herpen, C. M., Van der Voort, R., Van der Laak, J. A., Klasen, I. S., De Graaf, A. O., Van Kempen, L. C., De Vries, I. J., Boer, T. D., Dolstra, H., and Torensma, R. (2008) Intratumoral rhIL-12 administration in head and neck squamous cell carcinoma patients induces B cell activation, Int. J. Cancer, 123, 2354–2361.PubMedCrossRefGoogle Scholar
  82. 82.
    Germain, C., Gnjatic, S., Tamzalit, F., Knockaert, S., Remark, R., Goc, J., Lepelley, A., Becht, E., Katsahian, S., and Bizouard, G. (2014) Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer, Am. J. Respir. Crit. Care Med., 189, 832–844.PubMedCrossRefGoogle Scholar
  83. 83.
    Germain, C., Gnjatic, S., and Dieu-Nosjean, M.-C. (2015) Tertiary lymphoid structureassociated B cells are key players in antitumor immunity, Front. Immunol., 6, 67.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Murdoch, C., Giannoudis, A., and Lewis, C. E. (2004) Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues, Blood, 104, 2224–2234.PubMedCrossRefGoogle Scholar
  85. 85.
    Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., and Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization, Trends Immunol., 25, 677–686.PubMedCrossRefGoogle Scholar
  86. 86.
    Gregory, A. D., and Houghton, A. M. (2011) Tumorassociated neutrophils: new targets for cancer therapy, Cancer Res., 71, 2411–2416.PubMedCrossRefGoogle Scholar
  87. 87.
    Liao, D., Luo, Y., Markowitz, D., Xiang, R., and Reisfeld, R. A. (2009) Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model, PLoS One, 4, e7965.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Atanasov, G., Hau, H. M., Dietel, C., Benzing, C., Krenzien, F., Brandl, A., Wiltberger, G., Matia, I., Prager, I., Schierle, K., Robson, S. C., Reutzel-Selke, A., Pratschke, J., Schmelzle, M., and Jonas, S. (2015) Prognostic significance of macrophage invasion in hilar cholangiocarcinoma, BMC Cancer, 15, 790.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Beyer, M., and Schultze, J. L. (2006) Regulatory T cells in cancer, Blood, 108, 804–811.PubMedCrossRefGoogle Scholar
  90. 90.
    Bilate, A. M., and Lafaille, J. J. (2012) Induced CD4+Foxp3+ regulatory T cells in immune tolerance, Annu. Rev. Immunol., 30, 733–758.PubMedCrossRefGoogle Scholar
  91. 91.
    Thornton, A. M., and Shevach, E. M. (1998) CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production, J. Exp. Med., 188, 287–296.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Crome, S. Q., Clive, B., Wang, A. Y., Kang, C. Y., Chow, V., Yu, J., Lai, A., Ghahary, A., Broady, R., and Levings, M. K. (2010) Inflammatory effects of ex vivo human Th17 cells are suppressed by regulatory T cells, J. Immunol., 185, 3199–3208.PubMedCrossRefGoogle Scholar
  93. 93.
    Murphy, T. J., Choileain, N. Ni., Zang, Y., Mannick, J. A., and Lederer, J. A. (2005) CD4+CD25+ regulatory T cells control innate immune reactivity after injury, J. Immunol., 174, 2957–2963.PubMedCrossRefGoogle Scholar
  94. 94.
    Mailloux, A. W., and Young, M. R. (2010) Regulatory T-cell trafficking: from thymic development to tumorinduced immune suppression, Crit. Rev. Immunol., 30, 435–447.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Sfondrini, L., Rossini, A., Besusso, D., Merlo, A., Tagliabue, E., Menard, S., and Balsari, A. (2006) Antitumor activity of the TLR-5 ligand flagellin in mouse models of cancer, J. Immunol., 176, 6624–6630.PubMedCrossRefGoogle Scholar
  96. 96.
    Huang, Y., Wang, F. M., Wang, T., Wang, Y. J., Zhu, Z. Y., Gao, Y. T., and Du, Z. (2012) Tumorinfiltrating FoxP3+ Tregs and CD8+ T cells affect the prognosis of hepatocellular carcinoma patients, Digestion, 86, 329–337.PubMedCrossRefGoogle Scholar
  97. 97.
    Leong, P. P., Mohammad, R., Ibrahim, N., Ithnin, H., Abdullah, M., Davis, W. C., and Seow, H. F. (2006) Phenotyping of lymphocytes expressing regulatory and effector markers in infiltrating ductal carcinoma of the breast, Immunol. Lett., 102, 229–236.PubMedCrossRefGoogle Scholar
  98. 98.
    Lin, Y. C., Mahalingam, J., Chiang, J. M., Su, P. J., Chu, Y. Y., Lai, H. Y., Fang, J. H., Huang, C. T., Chiu, C. T., and Lin, C. Y. (2013) Activated but not resting regulatory T cells accumulated in tumor microenvironment and correlated with tumor progression in patients with colorectal cancer, Int. J. Cancer, 132, 1341–1350.PubMedCrossRefGoogle Scholar
  99. 99.
    Hoechst, B., Voigtlaender, T., Ormandy, L., Gamrekelashvili, J., Zhao, F., Wedemeyer, H., Lehner, F., Manns, M. P., Greten, T. F., and Korangy, F. (2009) Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor, Hepatology, 50, 799–807.PubMedCrossRefGoogle Scholar
  100. 100.
    Motz, G. T., and Coukos, G. (2011) The parallel lives of angiogenesis and immunosuppression: cancer and other tales, Nat. Rev. Immunol., 11, 702–711.PubMedCrossRefGoogle Scholar
  101. 101.
    Willenborg, S., Lucas, T., van Loo, G., Knipper, J. A., Krieg, T., Haase, I., Brachvogel, B., Hammerschmidt, M., Nagy, A., Ferrara, N., Pasparakis, M., and Eming, S. A. (2012) CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair, Blood, 120, 613–625.PubMedCrossRefGoogle Scholar
  102. 102.
    Huang, B., Pan, P. Y., Li, Q., Sato, A. I., Levy, D. E., Bromberg, J., Divino, C. M., and Chen, S. H. (2006) Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumorinduced T regulatory cells and T-cell energy in tumorbearing host, Cancer Res., 66, 1123–1131.PubMedCrossRefGoogle Scholar
  103. 103.
    Yang, L., and Moses, H. L. (2008) Transforming growth factor beta: tumor suppressor or promoter? Are host immune cells the answer? Cancer Res., 68, 9107–9111.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Bronte, V., Serafini, P., Mazzoni, A., Segal, D. M., and Zanovello, P. (2003) L-arginine metabolism in myeloid cells controls T-lymphocyte functions, Trends Immunol., 24, 301–305.CrossRefGoogle Scholar
  105. 105.
    Hurwitz, A. A., and Watkins, S. K. (2012) Immune suppression in the tumor microenvironment: a role for dendritic cellmediated tolerization of T cells, Cancer Immunol. Immunother., 61, 289–93.PubMedCrossRefGoogle Scholar
  106. 106.
    Van Beek, J. J., Gorris, M. A., Skold, A. E., Hatipoglu, I., Van Acker, H. H., Smits, E. L., De Vries, I. J., and Bakdash, G. (2016) Human blood myeloid and plasmacytoid dendritic cells cross activate each other and synergize in inducing NK cell cytotoxicity, Oncoimmunology, 5, e1227902.PubMedCrossRefGoogle Scholar
  107. 107.
    Miossec, P., and Kolls, J. K. (2012) Targeting IL-17 and TH17 cells in chronic inflammation, Nat. Rev. Drug Discov., 11, 763–776.PubMedCrossRefGoogle Scholar
  108. 108.
    Nyirenda, M. H., Sanvito, L., Darlington, P. J., O’Brien, K., Zhang, G. X., Constantinescu, C. S., Bar-Or, A., and Gran, B. (2011) TLR2 stimulation drives human naive and effector regulatory T cells into a Th17-like phenotype with reduced suppressive function, J. Immunol., 187, 2278–2290.PubMedCrossRefGoogle Scholar
  109. 109.
    Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., and Stockinger, B. (2006) TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells, Immunity, 24, 179–189.PubMedCrossRefGoogle Scholar
  110. 110.
    Miljkovic, D., Cvetkovic, I., Vuckovic, O., Stosic-Grujicic, S., Mostarica Stojkovic, M., and Trajkovic, V. (2003) The role of interleukin-17 in inducible nitric oxide synthasemediated nitric oxide production in endothelial cells, Cell Mol. Life Sci., 60, 518–525.PubMedCrossRefGoogle Scholar
  111. 111.
    Paris, I., Charreau, S., Guignouard, E., Garnier, M., Favot-Laforge, L., Huguier, V., Bernard, F.-X., Morel, F., and Lecron, J.-C. (2012) Critical role of Th17 proinflammatory cytokines to delay skin wound healing, Cytokine, 59, 503.CrossRefGoogle Scholar
  112. 112.
    Bailey, S. R., Nelson, M. H., Himes, R. A., Li, Z., Mehrotra, S., and Paulos, C. M. (2014) Th17 cells in cancer: the ultimate identity crisis, Front. Immunol., 5, 276.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Sallusto, F., and Lanzavecchia, A. (2009) Human Th17 cells in infection and autoimmunity, Microbes Infect., 11, 620–624.PubMedCrossRefGoogle Scholar
  114. 114.
    Lv, L., Pan, K., Li, X. D., She, K. L., Zhao, J. J., Wang, W., Chen, J. G., Chen, Y. B., Yun, J. P., and Xia, J. C. (2011) The accumulation and prognosis value of tumor infiltrating IL-17 producing cells in esophageal squamous cell carcinoma, PLoS One, 6, e18219.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Liu, J., Duan, Y., Cheng, X., Chen, X., Xie, W., Long, H., Lin, Z., and Zhu, B. (2011) IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma, Biochem. Biophys. Res. Commun., 407, 348–354.PubMedCrossRefGoogle Scholar
  116. 116.
    Wang, L., Yi, T., Kortylewski, M., Pardoll, D. M., Zeng, D., and Yu, H. (2009) IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway, J. Exp. Med., 206, 1457–1464.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Guery, L., and Hugues, S. (2015) Th17 cell plasticity and functions in cancer immunity, Biomed. Res. Int., 2015, 314620.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Kim, J. S., Sklarz, T., Banks, L. B., Gohil, M., Waickman, A. T., Skuli, N., Krock, B. L., Luo, C. T., Hu, W., Pollizzi, K. N., Li, M. O., Rathmell, J. C., Birnbaum, M. J., Powell, J. D., Jordan, M. S., and Koretzky, G. A. (2013) Natural and inducible TH17 cells are regulated differently by Akt and mTOR pathways, Nat. Immunol., 14, 611–618.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • L. A. Tashireva
    • 1
  • V. M. Perelmuter
    • 1
  • V. N. Manskikh
    • 2
  • E. V. Denisov
    • 1
    Email author
  • O. E. Savelieva
    • 1
  • E. V. Kaygorodova
    • 1
  • M. V. Zavyalova
    • 1
    • 3
  1. 1.Cancer Research InstituteTomsk National Research Medical Center of the Russian Academy of SciencesTomskRussia
  2. 2.Lomonosov Moscow State UniversityMoscowRussia
  3. 3.Siberian State Medical UniversityTomskRussia

Personalised recommendations