An inflammatory vicious cycle: Fibroblasts and immune cell recruitment in cancer

Experimental Cell Research

Volumn 319, Issue 11, 2013, Pages 1596-1603

  Raz, Yael ^a,b   Erez, Neta ^b  

^a LIS MATERNITY HOSPITAL   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Cancer; Cancer associated fibroblasts; Inflammation; Microenvironment

Indexed keywords

FIBRONECTIN; INTERLEUKIN 1; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN;

ADAPTIVE IMMUNITY; ANGIOGENESIS; BREAST CARCINOMA; CARCINOGENESIS; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; FIBROBLAST; HUMAN; HYPOXEMIA; IMMUNOCOMPETENT CELL; MACROPHAGE; MACROPHAGE MIGRATION; METASTASIS; NEOPLASM; NONHUMAN; PERITONEUM MAST CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TH1 TH2 BALANCE; TH17 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR PROMOTION;

CANCER; CANCER-ASSOCIATED FIBROBLASTS; INFLAMMATION; MICROENVIRONMENT;

ANIMALS; FIBROBLASTS; HUMANS; INFLAMMATION; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84879607721     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.03.022     Document Type: Review

References (76)

1. Colotta F., Allavena P., Sica A., Garlanda C., Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009, 30:1073-1081.
2. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
3. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
4. Erez N., Coussens L.M. Leukocytes as paracrine regulators of metastasis and determinants of organ-specific colonization, International journal of cancer. J. Int. Cancer 2011, 128:2536-2544.
5. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Sem. Cancer Biol. 2012, 22:33-40.
6. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
7. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
8. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 2009, 9:239-252.
9. Acharyya S., Oskarsson T., Vanharanta S., Malladi S., Kim J., Morris P.G., Manova-Todorova K., Leversha M., Hogg N., Seshan V.E., Norton L., Brogi E., Massague J. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150:165-178.
10. DeNardo D.G., Brennan D., Rexhapaj E., Ruffel B., Shiao S., Gallagher W.M., Wadhani N., Kial S.D., Junaid S.A., Rugo H.S., Hwang E.S., Jirstrom K., West B., Coussens L.M. Leukocyte complexity in breast cancer predicts overall survival and functionally regulates response to chemotherapy. Cancer Discovery 2011, 1:54-67.
11. Shree T., Olson O.C., Elie B.T., Kester J.C., Garfall A.L., Simpson K., Bell-McGuinn K.M., Zabor E.C., Brogi E., Joyce J.A. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev. 2011, 25:2465-2479.
12. DeNardo D.G., Barreto J.B., Andreu P., Vasquez L., Tawfik D., Kolhatkar N., Coussens L.M. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009, 16:91-102.
13. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
14. Ruffell B., DeNardo D.G., Affara N.I., Coussens L.M. Lymphocytes in cancer development: polarization towards pro-tumor immunity. Cytokine Growth Factor Rev. 2010, 21:3-10.
15. Anderberg C., Pietras K. On the origin of cancer-associated fibroblasts. Cell Cycle 2009, 8:1461-1462.
16. Allinen M., Beroukhim R., Cai L., Brennan C., Lahti-Domenici J., Huang H., Porter D., Hu M., Chin L., Richardson A., Schnitt S., Sellers W.R., Polyak K. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004, 6:17-32.
17. Bhowmick N.A., Neilson E.G., Moses H.L. Stromal fibroblasts in cancer initiation and progression. Nature 2004, 432:332-337.
18. Orimo A., Gupta P.B., Sgroi D.C., Arenzana-Seisdedos F., Delaunay T., Naeem R., Carey V.J., Richardson A.L., Weinberg R.A. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
19. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
20. Erler J.T., Weaver V.M. Three-dimensional context regulation of metastasis. Clin. Exp. Metastasis 2009, 26:35-49.
21. Goetz J.G., Minguet S., Navarro-Lerida I., Lazcano J.J., Samaniego R., Calvo E., Tello M., Osteso-Ibanez T., Pellinen T., Echarri A., Cerezo A., Klein-Szanto A.J., Garcia R., Keely P.J., Sanchez-Mateos P., Cukierman E., Del Pozo M.A. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
22. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
23. Cirri P., Chiarugi P. Cancer associated fibroblasts: the dark side of the coin. Am. J. Cancer Res. 2011, 1:482-497.
24. Strell C., Rundqvist H., Ostman A. Fibroblasts-a key host cell type in tumor initiation, progression, and metastasis. Upsala J. Med. Sci. 2012, 117:187-195.
25. Rasanen K., Vaheri A. Activation of fibroblasts in cancer stroma. Exp. Cell Res. 2010, 316:2713-2722.
26. Sica A., Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 2012, 122:787-795.
27. Melgarejo E., Medina M.A., Sanchez-Jimenez F., Urdiales J.L. Monocyte chemoattractant protein-1: a key mediator in inflammatory processes. Int. J. Biochem. Cell Biol. 2009, 41:998-1001.
28. Ksiazkiewicz M., Gottfried E., Kreutz M., Mack M., Hofstaedter F., Kunz-Schughart L.A. Importance of CCL2-CCR2A/2B signaling for monocyte migration into spheroids of breast cancer-derived fibroblasts. Immunobiology 2010, 215:737-747.
29. Silzle T., Kreutz M., Dobler M.A., Brockhoff G., Knuechel R., Kunz-Schughart L.A. Tumor-associated fibroblasts recruit blood monocytes into tumor tissue. Eur. J. Immunol. 2003, 33:1311-1320.
30. Hembruff S.L., Jokar I., Yang L., Cheng N. Loss of transforming growth factor-beta signaling in mammary fibroblasts enhances CCL2 secretion to promote mammary tumor progression through macrophage-dependent and -independent mechanisms. Neoplasia 2010, 12:425-433.
31. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
32. Ren G., Zhao X., Wang Y., Zhang X., Chen X., Xu C., Yuan Z.R., Roberts A.I., Zhang L., Zheng B., Wen T., Han Y., Rabson A.B., Tischfield J.A., Shao C., Shi Y. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFalpha. Cell Stem Cell 2012, 11:812-824.
33. Augsten M., Hagglof C., Olsson E., Stolz C., Tsagozis P., Levchenko T., Frederick M.J., Borg A., Micke P., Egevad L., Ostman A. CXCL14 is an autocrine growth factor for fibroblasts and acts as a multi-modal stimulator of prostate tumor growth. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3414-3419.
34. 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.
35. Begley L.A., Kasina S., MacDonald J., Macoska J.A. The inflammatory microenvironment of the aging prostate facilitates cellular proliferation and hypertrophy. Cytokine 2008, 43:194-199.
36. Kobayashi N., Miyoshi S., Mikami T., Koyama H., Kitazawa M., Takeoka M., Sano K., Amano J., Isogai Z., Niida S., Oguri K., Okayama M., McDonald J.A., Kimata K., Taniguchi S., Itano N. Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res. 2010, 70:7073-7083.
37. Chen G.Y., Nunez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
38. Chomarat P., Banchereau J., Davoust J., Palucka A.K. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 2000, 1:510-514.
39. Cheng J.D., Dunbrack R.L., Valianou M., Rogatko A., Alpaugh R.K., Weiner L.M. Promotion of tumor growth by murine fibroblast activation protein, a serine protease, in an animal model. Cancer Res. 2002, 62:4767-4772.
40. 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.
41. Paunescu V., Bojin F.M., Tatu C.A., Gavriliuc O.I., Rosca A., Gruia A.T., Tanasie G., Bunu C., Crisnic D., Gherghiceanu M., Tatu F.R., Tatu C.S., Vermesan S. Tumour-associated fibroblasts and mesenchymal stem cells: more similarities than differences. J. Cell. Mol. Med. 2011, 15:635-646.
42. Kim J.H., Oh S.H., Kim E.J., Park S.J., Hong S.P., Cheon J.H., Kim T.I., Kim W.H. The role of myofibroblasts in upregulation of S100A8 and S100A9 and the differentiation of myeloid cells in the colorectal cancer microenvironment. Biochem. Biophys. Res. Commun. 2012, 423:60-66.
43. Khazaie K., Blatner N.R., Khan M.W., Gounari F., Gounaris E., Dennis K., Bonertz A., Tsai F.N., Strouch M.J., Cheon E., Phillips J.D., Beckhove P., Bentrem D.J. The significant role of mast cells in cancer. Cancer Metastasis Rev. 2011, 30:45-60.
44. Liu J., Zhang Y., Zhao J., Yang Z., Li D., Katirai F., Huang B. Mast cell: insight into remodeling a tumor microenvironment. Cancer Metastasis Rev. 2011, 30:177-184.
45. Jippo-Kanemoto T., Adachi S., Ebi Y., Matsuda H., Kasugai T., Nishikawa S., Kitamura Y. BALB/3T3 fibroblast-conditioned medium attracts cultured mast cells derived from W/W but not from mi/mi mutant mice, both of which are deficient in mast cells. Blood 1992, 80:1933-1939.
46. Hugo H.J., Lebret S., Tomaskovic-Crook E., Ahmed N., Blick T., Newgreen D.F., Thompson E.W., Ackland M.L. Contribution of fibroblast and mast cell (afferent) and tumor (efferent) IL-6 effects within the tumor microenvironment. Cancer Microenviron. Off. J. Int. Cancer Microenviron. Soc. 2012.
47. Misiak-Tloczek A., Brzezinska-Blaszczyk E. IL-6, but not IL-4, stimulates chemokinesis and TNF stimulates chemotaxis of tissue mast cells: involvement of both mitogen-activated protein kinases and phosphatidylinositol 3-kinase signalling pathways. Acta Pathol. Microbiol. Immunol. Scand. 2009, 117:558-567.
48. Gyotoku E., Morita E., Kameyoshi Y., Hiragun T., Yamamoto S., Hide M. The IL-6 family cytokines, interleukin-6, interleukin-11, oncostatin M, and leukemia inhibitory factor, enhance mast cell growth through fibroblast-dependent pathway in mice. Arch. Dermatol. Res. 2001, 293:508-514.
49. Brzezinska-Blaszczyk E., Pietrzak A., Misiak-Tloczek A.H. Tumor necrosis factor (TNF) is a potent rat mast cell chemoattractant. J. Interferon Cytokine Res. Off. J. Int. Soc. Interferon Cytokine Res. 2007, 27:911-919.
50. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., Zhu Z., Hicklin D., Wu Y., Port J.L., Altorki N., Port E.R., Ruggero D., Shmelkov S.V., Jensen K.K., Rafii S., Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
51. Barnas J.L., Simpson-Abelson M.R., Yokota S.J., Kelleher R.J., Bankert R.B. T cells and stromal fibroblasts in human tumor microenvironments represent potential therapeutic targets. Cancer Microenviron. Off. J. Int. Cancer Microenviron. Soc. 2010, 3:29-47.
52. Mishra S.K., Siddique H.R., Saleem M. S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence. Cancer Metastasis Rev. 2012, 31:163-172.
53. Boye K., Maelandsmo G.M. S100A4 and metastasis: a small actor playing many roles. Am. J. Pathol. 2010, 176:528-535.
54. Grum-Schwensen B., Klingelhofer J., Grigorian M., Almholt K., Nielsen B.S., Lukanidin E., Ambartsumian N. Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors. Cancer Res. 2010, 70:936-947.
55. De Monte L., Reni M., Tassi E., Clavenna D., Papa I., Recalde H., Braga M., Di Carlo V., Doglioni C., Protti M.P. 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.
56. Su X., Ye J., Hsueh E.C., Zhang Y., Hoft D.F., Peng G. Tumor microenvironments direct the recruitment and expansion of human Th17 cells. J. Immunol. 2010, 184:1630-1641.
57. Barnas J.L., Simpson-Abelson M.R., Brooks S.P., Kelleher R.J., Bankert R.B. Reciprocal functional modulation of the activation of T lymphocytes and fibroblasts derived from human solid tumors. J. Immunol. 2010, 185:2681-2692.
58. Yang L., Pang Y., Moses H.L. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 2010, 31:220-227.
59. Benito-Miguel M., Garcia-Carmona Y., Balsa A., Perez de Ayala C., Cobo-Ibanez T., Martin-Mola E., Miranda-Carus M.E. A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+CD25+ regulatory T cells and CD4+CD25- responder T cells. J. Immunol. 2009, 183:8268-8279.
60. Tan W., Zhang W., Strasner A., Grivennikov S., Cheng J.Q., Hoffman R.M., Karin M. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature 2011.
61. Filer A., Raza K., Salmon M., Buckley C.D. The role of chemokines in leucocyte-stromal interactions in rheumatoid arthritis. Front. Biosci. J. Virtual Libr. 2008, 13:2674-2685.
62. Buckley C.D., Pilling D., Lord J.M., Akbar A.N., Scheel-Toellner D., Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol. 2001, 22:199-204.
63. Parsonage G., Filer A.D., Haworth O., Nash G.B., Rainger G.E., Salmon M., Buckley C.D. A stromal address code defined by fibroblasts. Trends Immunol. 2005, 26:150-156.
64. Servais C., Erez N. From sentinel cells to inflammatory culprits: cancer-associated fibroblasts in tumour-related inflammation. J. Pathol. 2013, 229:198-207.
65. Ostman A., Augsten M. Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr. Opin. Genet. Dev. 2009, 19:67-73.
66. Zhu Y., Zhu M., Lance P. IL1beta-mediated stromal COX-2 signaling mediates proliferation and invasiveness of colonic epithelial cancer cells. Exp. Cell Res. 2012, 318:2520-2530.
67. Jiang L., Gonda T.A., Gamble M.V., Salas M., Seshan V., Tu S., Twaddell W.S., Hegyi P., Lazar G., Steele I., Varro A., Wang T.C., Tycko B. Global hypomethylation of genomic DNA in cancer-associated myofibroblasts. Cancer Res. 2008, 68:9900-9908.
68. del Rey M.J., Izquierdo E., Caja S., Usategui A., Santiago B., Galindo M., Pablos J.L. Human inflammatory synovial fibroblasts induce enhanced myeloid cell recruitment and angiogenesis through a hypoxia-inducible transcription factor 1alpha/vascular endothelial growth factor-mediated pathway in immunodeficient mice. Arthritis Rheum. 2009, 60:2926-2934.
69. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
70. Bonafoux D., Lee W.C. Strategies for TGF-beta modulation: a review of recent patents. Exp. Opin. Ther. Pat. 2009, 19:1759-1769.
71. Buijs J.T., Stayrook K.R., Guise T.A. TGF-beta in the bone microenvironment: role in breast cancer metastases. Cancer Microenviron. Off. J. Int. Cancer Microenviron. Soc. 2011, 4:261-281.
72. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230.
73. Scott A.M., Wiseman G., Welt S., Adjei A., Lee F.T., Hopkins W., Divgi C.R., Hanson L.H., Mitchell P., Gansen D.N., Larson S.M., Ingle J.N., Hoffman E.W., Tanswell P., Ritter G., Cohen L.S., Bette P., Arvay L., Amelsberg A., Vlock D., Rettig W.J., Old L.J. A phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2003, 9:1639-1647.
74. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat. Rev. Cancer 2004, 4:11-22.
75. Lewis A.M., Varghese S., Xu H., Alexander H.R. Interleukin-1 and cancer progression: the emerging role of interleukin-1 receptor antagonist as a novel therapeutic agent in cancer treatment. J. Transl. Med. 2006, 4:48.
76. Jones S.A., Scheller J., Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 2011, 121:3375-3383.