Regulation of the anti-tumour immune response by cancer-associated fibroblasts

Seminars in Cancer Biology

Volumn 25, Issue , 2014, Pages 69-77

  Harper, James ^a   Sainson, Richard C A ^a  

^a MEDIMMUNE   (United States)

Author keywords

Cancer associated fibroblasts; Immune cells

Indexed keywords

ALPHA INTERFERON; ALPHA SMOOTH MUSCLE ACTIN; B7 ANTIGEN; CALVASCULIN; CD40 ANTIGEN; CD86 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; RANTES; SCATTER FACTOR; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A;

ADAPTIVE IMMUNITY; ANTINEOPLASTIC ACTIVITY; CANCER GROWTH; CANCER THERAPY; CELL ACTIVATION; CELL FUNCTION; CELL INFILTRATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DISEASE COURSE; ENZYME RELEASE; HUMAN; IMMUNE STATUS; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; MOLECULARLY TARGETED THERAPY; MYOFIBROBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; TUMOR MICROENVIRONMENT; ANIMAL; CELLULAR IMMUNITY; FIBROBLAST; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; PATHOLOGY; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; FIBROBLASTS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; IMMUNOTHERAPY; INFLAMMATION; NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 84897506018     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2013.12.005     Document Type: Review

References (108)

1. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
2. Kuperwasser C., et al. Reconstruction of functionally normal and malignant human breast tissues in mice. PNAS 2004, 101:4966-4971.
3. Byzova T.V., et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell 2000, 6:851-860.
4. Berking C., et al. Transforming growth factor-beta1 increases survival of human melanoma through stroma remodeling. Cancer Res 2001, 61:8306-8316.
5. Fukumura D., et al. Tumor induction of VEGF promoter activity in stromal cells. Cell 1998, 94:715-725.
6. Cornil I., et al. Fibroblast cell interactions with human melanoma cells affect tumor cell growth as a function of tumor progression. PNAS 1991, 88:6028-6032.
7. Goh P.P., Sze D.M., Roufogalis B.D. Molecular and cellular regulators of cancer angiogenesis. Curr Cancer Drug Targets 2007, 7:743-758.
8. Servais C., Erez N. From sentinel cells to inflammatory culprits: cancer-associated fibroblasts in tumour-related inflammation. J Pathol 2013, 229:198-207.
9. Gaggioli C., et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007, 9:1392-1400.
10. Barclay W.W., et al. Characterization of adult prostatic progenitor/stem cells exhibiting self-renewal and multilineage differentiation. Stem Cells 2008, 26:600-610.
11. Morrison S.J., Spradling A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132:598-611.
12. Pavlides S., et al. Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the reverse Warburg effect: a transcriptional informatics analysis with validation. Cell Cycle 2010, 9:2201-2219.
13. Dvorak H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986, 315:1650-1659.
14. Feig C., et al. The pancreas cancer microenvironment. Clin Cancer Res 2012, 18:4266-4276.
15. Tripathi M., Billet S., Bhowmick N.A. Understanding the role of stromal fibroblasts in cancer progression. Cell Adhes Migr 2012, 6:231-235.
16. Kraman M., et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010, 330:827-830.
17. Saigusa S., et al. Cancer-associated fibroblasts correlate with poor prognosis in rectal cancer after chemoradiotherapy. Int J Oncol 2011, 38:655-663.
18. Kurose K., et al. Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet 2002, 32:355-357.
19. Direkze N.C., Alison M.R. Bone marrow and tumour stroma: an intimate relationship. Hematol Oncol 2006, 24:189-195.
20. Direkze N.C., et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004, 64:8492-8495.
21. Mishra P.J., et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 2008, 68:4331-4339.
22. Forino M., et al. TGFbeta1 induces epithelial-mesenchymal transition, but not myofibroblast transdifferentiation of human kidney tubular epithelial cells in primary culture. Int J Exp Pathol 2006, 87:197-208.
23. Zeisberg E.M., et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007, 13:952-961.
24. Potenta S., Zeisberg E., Kalluri R. The role of endothelial-to-mesenchymal transition in cancer progression. Br J Cancer 2008, 99:1375-1379.
25. Jotzu C., et al. Adipose tissue-derived stem cells differentiate into carcinoma-associated fibroblast-like cells under the influence of tumor-derived factors. Anal Cell Pathol (Amst) 2010, 33:61-79.
26. Loeffler M., Kruger J.A., Niethammer A.G., Reisfeld R.A. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006, 116:1955-1962.
27. Sugimoto H., Mundel T.M., Kieran M.W., Kalluri R. Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 2006, 5:1640-1646.
28. True L.D., et al. CD90/THY1 is overexpressed in prostate cancer-associated fibroblasts and could serve as a cancer biomarker. Mod Pathol 2010, 23:1346-1356.
29. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006, 6:392-401.
30. De Wever O., Demetter P., Mareel M., Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008, 123:2229-2238.
31. Vicent S., et al. Cross-species functional analysis of cancer-associated fibroblasts identifies a critical role for CLCF1 and IL-6 in non-small cell lung cancer in vivo. Cancer Res 2012, 72:5744-5756.
32. Orimo A., et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
33. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
34. Buckley C.D., et al. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol 2001, 22:199-204.
35. Smith R.S., Smith T.J., Blieden T.M., Phipps R.P. Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am J Pathol 1997, 151:317-322.
36. Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003, 83:835-870.
37. Aggarwal B.B., Vijayalekshmi R.V., Sung B. Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res 2009, 15:425-430.
38. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
39. Peggs K.S., Quezada S.A., Allison J.P. Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy. Immunol Rev 2008, 224:141-165.
40. Loose D., Van de Wiele C. The immune system and cancer. Cancer Biother Radiopharm 2009, 24:369-376.
41. Herrera M., et al. Cancer-associated fibroblast and M2 macrophage markers together predict outcome in colorectal cancer patients. Cancer Sci 2013, 104:437-444.
42. Jung D.W., et al. Tumor-stromal crosstalk in invasion of oral squamous cell carcinoma: a pivotal role of CCL7. Int J Cancer 2010, 127:332-344.
43. Acharyya S., et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150:165-178.
44. De Boeck A., et al. Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression. Proteomics 2013, 13:379-388.
45. Comito G., et al. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene 2013.
46. Tjomsland V., et al. Interleukin 1alpha sustains the expression of inflammatory factors in human pancreatic cancer microenvironment by targeting cancer-associated fibroblasts. Neoplasia 2011, 13:664-675.
47. Roca H., et al. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem 2009, 284:34342-34354.
48. Wu M.H., et al. Targeting galectin-1 in carcinoma-associated fibroblasts inhibits oral squamous cell carcinoma metastasis by downregulating MCP-1/CCL2 expression. Clin Cancer Res 2011, 17:1306-1316.
49. Lin Z.Y., Chuang Y.H., Chuang W.L. Cancer-associated fibroblasts up-regulate CCL2, CCL26, IL6 and LOXL2 genes related to promotion of cancer progression in hepatocellular carcinoma cells. Biomed Pharmacother 2012, 66:525-529.
50. Yoshimura T., et al. Monocyte chemoattractant protein-1/CCL2 produced by stromal cells promotes lung metastasis of 4T1 murine breast cancer cells. PLoS One 2013, 8:e58791.
51. Khazaie K., et al. The significant role of mast cells in cancer. Cancer Metastasis Rev 2011, 30:45-60.
52. Crivellato E., Nico B., Ribatti D. Mast cells and tumour angiogenesis: new insight from experimental carcinogenesis. Cancer Lett 2008, 269:1-6.
53. Ma Y., Hwang R.F., Logsdon C.D., Ullrich S.E. Dynamic mast cell-stromal cell interactions promote growth of pancreatic cancer. Cancer Res 2013, 73:3927-3937.
54. Konno S., Kurokawa M., Uede T., Nishimura M., Huang S.K. Role of osteopontin, a multifunctional protein, in allergy and asthma. Clin Exp Allergy 2011, 41:1360-1366.
55. Sun J., et al. Osteopontin splice variants expressed by breast tumors regulate monocyte activation via MCP-1 and TGF-beta1. Cell Mol Immunol 2013, 10:176-182.
56. Balsamo M., et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. PNAS 2009, 106:20847-20852.
57. Erez N., Truitt M., Olson P., Arron S.T., Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010, 17:135-147.
58. Dienz O., Rincon M. The effects of IL-6 on CD4 T cell responses. Clin Immunol 2009, 130:27-33.
59. De Monte L., et al. Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med 2011, 208:469-478.
60. Liao D., Luo Y., Markowitz D., Xiang R., Reisfeld R.A. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One 2009, 4:e7965.
61. Tran E., et al. Immune targeting of fibroblast activation protein triggers recognition of multipotent bone marrow stromal cells and cachexia. J Exp Med 2013, 210:1125-1135.
62. Anderson I.C., Mari S.E., Broderick R.J., Mari B.P., Shipp M.A. The angiogenic factor interleukin 8 is induced in non-small cell lung cancer/pulmonary fibroblast cocultures. Cancer Res 2000, 60:269-272.
63. Baratelli F., et al. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 2005, 175:1483-1490.
64. Groeger A.L., et al. Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat Chem Biol 2010, 6:433-441.
65. Pena C., et al. STC1 expression by cancer-associated fibroblasts drives metastasis of colorectal cancer. Cancer Res 2013, 73:1287-1297.
66. Wang Y., et al. Stanniocalcin-1 suppresses superoxide generation in macrophages through induction of mitochondrial UCP2. J Leukoc Biol 2009, 86:981-988.
67. Chakraborty A., et al. Stanniocalcin-1 regulates endothelial gene expression and modulates transendothelial migration of leukocytes. Am J Physiol Renal Physiol 2007, 292:F895-F904.
68. Byrne S.N., Knox M.C., Halliday G.M. TGFbeta is responsible for skin tumour infiltration by macrophages enabling the tumours to escape immune destruction. Immunol Cell Biol 2008, 86:92-97.
69. Shangguan L., et al. Inhibition of TGF-beta/Smad signaling by BAMBI blocks differentiation of human mesenchymal stem cells to carcinoma-associated fibroblasts and abolishes their protumor effects. Stem Cells 2012, 30:2810-2819.
70. Kojima Y., et al. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. PNAS 2010, 107:20009-20014.
71. Nazareth M.R., et al. Characterization of human lung tumor-associated fibroblasts and their ability to modulate the activation of tumor-associated T cells. J Immunol 2007, 178:5552-5562.
72. Laouar Y., Sutterwala F.S., Gorelik L., Flavell R.A. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 2005, 6:600-607.
73. Weber F., et al. Transforming growth factor-beta1 immobilises dendritic cells within skin tumours and facilitates tumour escape from the immune system. Cancer Immunol Immunother 2005, 54:898-906.
74. Halliday G.M., Le S. Transforming growth factor-beta produced by progressor tumors inhibits, while IL-10 produced by regressor tumors enhances, Langerhans cell migration from skin. Int Immunol 2001, 13:1147-1154.
75. Bekeredjian-Ding I., et al. Tumour-derived prostaglandin E and transforming growth factor-beta synergize to inhibit plasmacytoid dendritic cell-derived interferon-alpha. Immunology 2009, 128:439-450.
76. Zhang Q., et al. Blockade of transforming growth factor-{beta} signaling in tumor-reactive CD8(+) T cells activates the antitumor immune response cycle. Mol Cancer Ther 2006, 5:1733-1743.
77. Sanjabi S., Mosaheb M.M., Flavell R.A. Opposing effects of TGF-beta and IL-15 cytokines control the number of short-lived effector CD8+ T cells. Immunity 2009, 31:131-144.
78. Thomas D.A., Massague J. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005, 8:369-380.
79. Ahmadzadeh M., Rosenberg S.A. TGF-beta 1 attenuates the acquisition and expression of effector function by tumor antigen-specific human memory CD8 T cells. J Immunol 2005, 174:5215-5223.
80. Fantini M.C., et al. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+ CD25-T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 2004, 172:5149-5153.
81. Shafer-Weaver K.A., et al. Cutting Edge: tumor-specific CD8+ T cells infiltrating prostatic tumors are induced to become suppressor cells. J Immunol 2009, 183:4848-4852.
82. Han Y., Guo Q., Zhang M., Chen Z., Cao X. CD69+ CD4+ CD25-T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-beta 1. J Immunol 2009, 182:111-120.
83. Kinoshita T., et al. Forkhead box P3 regulatory T cells coexisting with cancer associated fibroblasts are correlated with a poor outcome in lung adenocarcinoma. Cancer Sci 2013, 104:409-415.
84. Levental K.R., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
85. Lopez J.I., Kang I., You W.K., McDonald D.M., Weaver V.M. In situ force mapping of mammary gland transformation. Integr Biol (Camb) 2011, 3:910-921.
86. Cox T.R., Erler J.T. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 2011, 4:165-178.
87. Lu P., Weaver V.M., Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012, 196:395-406.
88. Egeblad M., Rasch M.G., Weaver V.M. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 2010, 22:697-706.
89. Olive K.P., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324:1457-1461.
90. Morwood S.R., Nicholson L.B. Modulation of the immune response by extracellular matrix proteins. Arch Immunol Ther Exp (Warsz) 2006, 54:367-374.
91. Sorokin L. The impact of the extracellular matrix on inflammation. Nat Rev Immunol 2010, 10:712-723.
92. Kobayashi N., et al. Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res 2010, 70:7073-7083.
93. Ostman A. PDGF receptors-mediators of autocrine tumor growth and regulators of tumor vasculature and stroma. Cytokine Growth Factor Rev 2004, 15:275-286.
94. Falcon B.L., et al. Increased vascular delivery and efficacy of chemotherapy after inhibition of platelet-derived growth factor-B. Am J Pathol 2011, 178:2920-2930.
95. Pietras K., et al. Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res 2001, 61:2929-2934.
96. Pietras K., et al. Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy. Cancer Res 2002, 62:5476-5484.
97. Palazon A., Aragones J., Morales-Kastresana A., de Landazuri M.O., Melero I. Molecular pathways: hypoxia response in immune cells fighting or promoting cancer. Clin Cancer Res 2012, 18:1207-1213.
98. Hamzah J., et al. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 2008, 453:410-414.
99. Rolny C., et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011, 19:31-44.
100. Ohm J.E., et al. VEGF inhibits T-cell development and may contribute to tumor-induced immune suppression. Blood 2003, 101:4878-4886.
101. Wada J., et al. The contribution of vascular endothelial growth factor to the induction of regulatory T-cells in malignant effusions. Anticancer Res 2009, 29:881-888.
102. Lukashev D., et al. Cutting edge: hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J Immunol 2006, 177:4962-4965.
103. Scott A.M., et al. A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin Cancer Res 2003, 9:1639-1647.
104. Narra K., et al. Phase II trial of single agent Val-boroPro (Talabostat) inhibiting hibroblast activation protein in patients with metastatic colorectal cancer. Cancer Biol Ther 2007, 6:1691-1699.
105. Prieto P.A., et al. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin Cancer Res 2012, 18:2039-2047.
106. Wolchok J.D., et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013, 369:122-133.
107. Hamid O., et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013, 369:134-144.
108. Feig C., et al. Targeting CXCL12 from FAP-expressing carcinoma- associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proceedings of the National Academy of Sciences 2013, 110(50):20212-20217. 10.1073/pnas.1320318110.