Tumor microenvironment: a main actor in the metastasis process

Springer Science and Business Media LLC - Tập 29 - Trang 381-395 - 2012
Daniela Spano1,2, Massimo Zollo1,2
1Biotecnologie Avanzate, Centro di Ingegneria Genetica (CEINGE), Naples, Italy
2Dipartimento di Biochimica e Biotecnologie Mediche, “Federico II” University of Naples, Naples, Italy

Tóm tắt

Over recent decades, various studies have argued that the metastatic tissue microenvironment is fully controlled by the intrinsic properties of the cancer cells (growth, motility and invasion, angiogenesis, extracellular matrix remodeling, immune escape) and additional cells types. Overall, the extrinsic factors and determinants mediate the contribution of the host microenvironment to metastasis formation. The tumor microenvironment carries out these functions by secretion of molecules that can influence and modulate its phenotype, making these complex interactions the basis for support for the progression of a cancer. Here, we undertake a summary of the “state of the art” of the functions and actions of these cells, as the main actors in the promotion of the formation of the microenvironment of the metastatic niche, and the associated network of interactions. The unraveling of the relationships between tumorigenic cells and their microenvironment represents an important issue for the development of new therapeutic agents that can fight both initiation and recurrence of cancer.

Tài liệu tham khảo

Nguyen DX, Massagué J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8:341–352 Egeblad M, Nakasone ES, Werb Z (2010) Tumors as organs: complex tissues that interface with the entire organism. Dev Cell 18:884–901 Poschke I, Mougiakakos D, Kiessling R (2011) Camouflage and sabotage: tumor escape from the immune system. Cancer Immunol Immunother 60:1161–1171 Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6:392–401 Mishra P, Banerjee D, Ben-Baruch A (2011) Chemokines at the crossroads of tumor-fibroblast interactions that promote malignancy. J Leukoc Biol 89:31–39 Boye K, Maelandsmo GM (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176:528–535 Boye K, Grotterød I, Aasheim HC, Hovig E, Maelandsmo GM (2008) Activation of NF-kappaB by extracellular S100A4: analysis of signal transduction mechanisms and identification of target genes. Int J Cancer 123:1301–1310 Klingelhöfer J, Møller HD, Sumer EU, Berg CH, Poulsen M, Kiryushko D, Soroka V, Ambartsumian N, Grigorian M, Lukanidin EM (2009) Epidermal growth factor receptor ligands as new extracellular targets for the metastasis-promoting S100A4 protein. FEBS J 276:5936–5948 Forst B, Hansen MT, Klingelhöfer J, Møller HD, Nielsen GH, Grum-Schwensen B, Ambartsumian N, Lukanidin E, Grigorian M (2010) Metastasis-inducing S100A4 and RANTES cooperate in promoting tumor progression in mice. PLoS One 5:e10374 Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW (2003) Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 163:2113–2126 Grum-Schwensen B, Klingelhöfer J, Grigorian M, Almholt K, Nielsen BS, Lukanidin E, Ambartsumian N (2010) Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors. Cancer Res 70:936–947 Lotfi R, Lee JJ, Lotze MT (2007) Eosinophilic granulocytes and damage-associated molecular pattern molecules (DAMPs): role in the inflammatory response within tumors. J Immunother 30:16–28 Cheadle EJ, Riyad K, Subar D, Rothwell DG, Ashton G, Batha H, Sherlock DJ, Hawkins RE, Gilham DE (2007) Eotaxin-2 and colorectal cancer: a potential target for immune therapy. Clin Cancer Res 13:5719–5728 Piscaglia AC, Shupe TD, Pani G, Tesori V, Gasbarrini A, Petersen BE (2009) Establishment of cancer cell lines from rat hepatocholangiocarcinoma and assessment of the role of granulocyte-colony stimulating factor and hepatocyte growth factor in their growth, motility and survival. J Hepatol 51:77–92 Shojaei F, Wu X, Qu X, Kowanetz M, Yu L, Tan M, Meng YG, Ferrara N (2009) G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci USA 106:6742–6747 Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M (2010) Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 176:1564–1576 DeNardo DG, Andreu P, Coussens LM (2010) Interactions between lymphocytes and myeloid cells regulate pro- versus anti-tumor immunity. Cancer Metastasis Rev 29:309–316 Murdoch C, Muthana M, Coffelt SB, Lewis CE (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 8:618–631 Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141:39–51 Mantovani A (2010) Molecular pathways linking inflammation and cancer. Curr Mol Med 10:369–373 Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9:239–252 Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444 Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182:4499–4506 Pollard JW (2008) Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol 84:623–630 Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66:605–612 Lin EY, Nguyen AV, Russell RG, Pollard JW (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 193:727–740 Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9:259–270 DeNardo DG, Johansson M, Coussens LM (2008) Immune cells as mediators of solid tumor metastasis. Cancer Metastasis Rev 27:11–18 Balkwill F (2004) Cancer and the chemokine network. Nat Rev Cancer 4:540–550 Allavena P, Sica A, Garlanda C, Mantovani A (2008) The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol Rev 222:155–161 Koide N, Nishio A, Sato T, Sugiyama A, Miyagawa S (2004) Significance of macrophage chemoattractant protein-1 expression and macrophage infiltration in squamous cell carcinoma of the esophagus. Am J Gastroenterol 99:1667–1674 Bingle L, Lewis CE, Corke KP, Reed MW, Brown NJ (2006) Macrophages promote angiogenesis in human breast tumour spheroids in vivo. Br J Cancer 94:101–107 Hotchkiss KA, Ashton AW, Klein RS, Lenzi ML, Zhu GH, Schwartz EL (2003) Mechanisms by which tumor cells and monocytes expressing the angiogenic factor thymidine phosphorylase mediate human endothelial cell migration. Cancer Res 63:527–533 Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4:71–78 Lewis JS, Landers RJ, Underwood JC, Harris AL, Lewis CE (2000) Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol 192:150–158 Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, Bernasconi S, Saccani S, Nebuloni M, Vago L, Mantovani A, Melillo G, Sica A (2003) Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 198:1391–1402 Ji RC (2006) Lymphatic endothelial cells, tumor lymphangiogenesis and metastasis: new insights into intratumoral and peritumoral lymphatics. Cancer Metastasis Rev 25:677–694 Vasiljeva O, Papazoglou A, Krüger A, Brodoefel H, Korovin M, Deussing J, Augustin N, Nielsen BS, Almholt K, Bogyo M, Peters C, Reinheckel T (2006) Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Res 66:5242–5250 Hagemann T, Robinson SC, Schulz M, Trümper L, Balkwill FR, Binder C (2004) Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases. Carcinogenesis 25:1543–1549 Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3:453–458 Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ, Stanley ER, Segall JE, Condeelis JS (2005) Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res 65:5278–5283 Pukrop T, Klemm F, Hagemann T, Gradl D, Schulz M, Siemes S, Trümper L, Binder C (2006) Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc Natl Acad Sci USA 103:5454–5459 Ojalvo LS, Whittaker CA, Condeelis JS, Pollard JW (2010) Gene expression analysis of macrophages that facilitate tumor invasion supports a role for Wnt-signaling in mediating their activity in primary mammary tumors. J Immunol 184:702–712 Solinas G, Germano G, Mantovani A, Allavena P (2009) Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86:1065–1073 Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162–174 Nagaraj S, Gabrilovich DI (2008) Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res 68:2561–2563 Nagaraj S, Gabrilovich DI (2010) Myeloid-derived suppressor cells in human cancer. Cancer J 16:348–353 Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ (2009) Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58:49–59 Yang L, Moses HL (2008) Transforming growth factor beta: tumor suppressor or promoter? Are host immune cells the answer? Cancer Res 68:9107–9111 Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S (2007) Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 67:10019–10026 Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, Gilbert J, Ochoa AC (2005) Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 202:931–939 Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S (2007) Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 67:4507–4513 Cheng P, Corzo CA, Luetteke N, Yu B, Nagaraj S, Bui MM, Ortiz M, Nacken W, Sorg C, Vogl T, Roth J, Gabrilovich DI (2008) Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med 205:2235–2249 Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G (2008) Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 181:4666–4675 Melani C, Chiodoni C, Forni G, Colombo MP (2003) Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 102:2138–2145 Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC (2004) Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6:409–421 Pan PY, Wang GX, Yin B, Ozao J, Ku T, Divino CM, Chen SH (2008) Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 111:219–228 Sawanobori Y, Ueha S, Kurachi M, Shimaoka T, Talmadge JE, Abe J, Shono Y, Kitabatake M, Kakimi K, Mukaida N, Matsushima K (2008) Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 111:5457–5466 Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, Carbone DP, Matrisian LM, Richmond A, Lin PC, Moses HL (2008) Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13:23–35 Hanson EM, Clements VK, Sinha P, Ilkovitch D, Ostrand-Rosenberg S (2009) Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J Immunol 183:937–944 Ostrand-Rosenberg S (2010) Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 59:1593–1600 Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI (2009) Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182:5693–5701 Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber DL, Schneck J, Gabrilovich DI (2007) Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 13:828–835 Serafini P, Mgebroff S, Noonan K, Borrello I (2008) Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 68:5439–5449 Nizar S, Copier J, Meyer B, Bodman-Smith M, Galustian C, Kumar D, Dalgleish A (2009) T-regulatory cell modulation: the future of cancer immunotherapy? Br J Cancer 100:1697–1703 Weller K, Foitzik K, Paus R, Syska W, Maurer M (2006) Mast cells are required for normal healing of skin wounds in mice. FASEB J 20:2366–2368 Williams CM, Galli SJ (2000) The diverse potential effector and immunoregulatory roles of mast cells in allergic disease. J Allergy Clin Immunol 105:847–859 Benoist C, Mathis D (2002) Mast cells in autoimmune disease. Nature 420:875–878 Terada T, Matsunaga Y (2000) Increased mast cells in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. J Hepatol 33:961–966 Strouch MJ, Cheon EC, Salabat MR, Krantz SB, Gounaris E, Melstrom LG, Dangi-Garimella S, Wang E, Munshi HG, Khazaie K, Bentrem DJ (2010) Crosstalk between mast cells and pancreatic cancer cells contributes to pancreatic tumor progression. Clin Cancer Res 16:2257–2265 Melillo RM, Guarino V, Avilla E, Galdiero MR, Liotti F, Prevete N, Rossi FW, Basolo F, Ugolini C, de Paulis A, Santoro M, Marone G (2010) Mast cells have a protumorigenic role in human thyroid cancer. Oncogene 29:6203–6215 Xiang M, Gu Y, Zhao F, Lu H, Chen S, Yin L (2010) Mast cell tryptase promotes breast cancer migration and invasion. Oncol Rep 23:615–619 Dabbous MK, Haney L, Nicolson GL, Eckley D, Woolley DE (1991) Mast cell modulation of tumour cell proliferation in rat mammary adenocarcinoma 13762NF. Br J Cancer 63:873–878 Huang B, Lei Z, Zhang GM, Li D, Song C, Li B, Liu Y, Yuan Y, Unkeless J, Xiong H, Feng ZH (2008) SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood 112:1269–1279 Caughey GH (2007) Mast cell tryptases and chymases in inflammation and host defense. Immunol Rev 217:141–154 Datta YH, Romano M, Jacobson BC, Golan DE, Serhan CN, Ewenstein BM (1995) Peptido-leukotrienes are potent agonists of von Willebrand factor secretion and P-selectin surface expression in human umbilical vein endothelial cells. Circulation 92:3304–3311 Boyce JA (2007) Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol Rev 217:168–185 Crivellato E, Nico B, Ribatti D (2008) Mast cells and tumour angiogenesis: new insight from experimental carcinogenesis. Cancer Lett 269:1–6 Mekori YA, Metcalfe DD (1999) Mast cell-T cell interactions. J Allergy Clin Immunol 104:517–523 Kim BG, Li C, Qiao W, Mamura M, Kasprzak B, Anver M, Wolfraim L, Hong S, Mushinski E, Potter M, Kim SJ, Fu XY, Deng C, Letterio JJ (2006) Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 441:1015–1019 Abraham SN, St John AL (2010) Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol 10:440–452 Conti P, Castellani ML, Kempuraj D, Salini V, Vecchiet J, Tetè S, Mastrangelo F, Perrella A, De Lutiis MA, Tagen M, Theoharides TC (2007) Role of mast cells in tumor growth. Ann Clin Lab Sci 37:315–322 Paget S (1989) The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 8:98–101 Langley RR, Fidler IJ (2011) The seed and soil hypothesis revisited-The role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 128:2527–2535 Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438:820–827 Hiratsuka S, Watanabe A, Aburatani H, Maru Y (2006) Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8:1369–1375 Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10:1349–1355 Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT, Giaccia AJ (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15:35–44 Fogelgren B, Polgár N, Szauter KM, Ujfaludi Z, Laczkó R, Fong KS, Csiszar K (2005) Cellular fibronectin binds to lysyl oxidase with high affinity and is critical for its proteolytic activation. J Biol Chem 280:24690–24697 Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massagué J (2011) Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 17:867–874 Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, Luo JL, Karin M (2009) Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457:102–106 Wai PY, Kuo PC (2008) Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev 27:103–118 Bellahcène A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:212–226 Møller HD, Ralfkjær U, Cremers N, Frankel M, Pedersen RT, Klingelhöfer J, Yanagisawa H, Grigorian M, Guldberg P, Sleeman J, Lukanidin E, Ambartsumian N (2011) Role of fibulin-5 in metastatic organ colonization. Mol Cancer Res 9:553–563 Hernandez L, Smirnova T, Kedrin D, Wyckoff J, Zhu L, Stanley ER, Cox D, Muller WJ, Pollard JW, Van Rooijen N, Segall JE (2009) The EGF/CSF-1 paracrine invasion loop can be triggered by heregulin beta1 and CXCL12. Cancer Res 69:3221–3227 Qian B, Deng Y, Im JH, Muschel RJ, Zou Y, Li J, Lang RA, Pollard JW (2009) A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 4:e6562 Gonda TA, Varro A, Wang TC, Tycko B (2010) Molecular biology of cancer-associated fibroblasts: can these cells be targeted in anti-cancer therapy? Semin Cell Dev Biol 21:2–10 Groot Kormelink T, Abudukelimu A, Redegeld FA (2009) Mast cells as target in cancer therapy. Curr Pharm Des 15:1868–1878 Joseph IB, Isaacs JT (1998) Macrophage role in the anti-prostate cancer response to one class of antiangiogenic agents. J Natl Cancer Inst 90:1648–1653 Robinson SC, Scott KA, Wilson JL, Thompson RG, Proudfoot AE, Balkwill FR (2003) A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res 63:8360–8365 Tadmor T, Attias D, Polliack A (2011) Myeloid-derived suppressor cells—their role in haemato-oncological malignancies and other cancers and possible implications for therapy. Br J Haematol 153:557–567