Phagocyte—extracellular matrix crosstalk empowers tumor development and dissemination

FEBS Journal

Volumn 285, Issue 4, 2018, Pages 734-751

  Varol, Chen ^a   Sagi, Irit ^b  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

extracellular matrix; matrix metalloproteinases; tumor microenvironment; tumor associated macrophages; tumor associated neutrophils

Indexed keywords

ADAM PROTEIN; ADAMTS PROTEIN; CATHEPSIN; COLLAGEN; MATRIX METALLOPROTEINASE; ANTINEOPLASTIC AGENT;

ANGIOGENESIS; CARCINOGENESIS; CELL ACTIVITY; CELL FUNCTION; CELL INTERACTION; EXTRACELLULAR MATRIX; HUMAN; LEUKOCYTE; METASTASIS; NONHUMAN; PHAGOCYTE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ASSOCIATED NEUTROPHIL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; DRUG EFFECT; METABOLISM; NEOPLASM; PATHOLOGY;

ANTINEOPLASTIC AGENTS; EXTRACELLULAR MATRIX; HUMANS; NEOPLASMS; PHAGOCYTES; TUMOR MICROENVIRONMENT;

EID: 85034739058     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.14317     Document Type: Review

References (182)

1. Mantovani A, Romero P, Palucka AK & Marincola FM (2008) Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 371, 771–783.
2. Bingle L, Brown NJ & Lewis CE (2002) The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 196, 254–265.
3. Zhang QW, Liu L, Gong CY, Shi HS, Zeng YH, Wang XZ, Zhao YW & Wei YQ (2012) Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One 7, e50946.
4. Shen M, Hu P, Donskov F, Wang G, Liu Q & Du J (2014) Tumor-associated neutrophils as a new prognostic factor in cancer: a systematic review and meta-analysis. PLoS One 9, e98259.
5. Biswas SK, Allavena P & Mantovani A (2013) Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol 35, 585–600.
6. Noy R & Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41, 49–61.
7. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4, 71–78.
8. Qian BZ & Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39–51.
9. Shaul ME & Fridlender ZG (2017) Neutrophils as active regulators of the immune system in the tumor microenvironment. J Leukoc Biol 102, 343–349.
10. Mammoto T & Ingber DE (2010) Mechanical control of tissue and organ development. Development 137, 1407–1420.
11. Page-McCaw A, Ewald AJ & Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8, 221–233.
12. Solomonov I, Zehorai E, Talmi-Frank D, Wolf SG, Shainskaya A, Zhuravlev A, Kartvelishvily E, Visse R, Levin Y, Kampf N et al. (2016) Distinct biological events generated by ECM proteolysis by two homologous collagenases. Proc Natl Acad Sci U S A 113, 10884–10889.
13. Lu P, Weaver VM & Werb Z (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196, 395–406.
14. Hanahan D & Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144, 646–674.
15. Pickup MW, Mouw JK & Weaver VM (2014) The extracellular matrix modulates the hallmarks of cancer. EMBO Rep 15, 1243–1253.
16. Hanahan D & Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309–322.
17. Afik R, Zigmond E, Vugman M, Klepfish M, Shimshoni E, Pasmanik-Chor M, Shenoy A, Bassat E, Halpern Z, Geiger T et al. (2016) Tumor macrophages are pivotal constructors of tumor collagenous matrix. J Exp Med 213, 2315–2331.
18. Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, Pamer EG & Li MO (2014) The cellular and molecular origin of tumor-associated macrophages. Science 344, 921–925.
19. Mantovani A, Ming WJ, Balotta C, Abdeljalil B & Bottazzi B (1986) Origin and regulation of tumor-associated macrophages: the role of tumor-derived chemotactic factor. Biochem Biophys Acta 865, 59–67.
20. Mantovani A & Sica A (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 22, 231–237.
21. Grivennikov SI, Greten FR & Karin M (2010) Immunity, inflammation, and cancer. Cell 140, 883–899.
22. Mantovani A, Sozzani S, Locati M, Allavena P & Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23, 549–555.
23. Sica A, Saccani A, Bottazzi B, Polentarutti N, Vecchi A, van Damme J & Mantovani A (2000) Autocrine production of IL-10 mediates defective IL-12 production and NF-kappa B activation in tumor-associated macrophages. J Immunol 164, 762–767.
24. Mantovani A, Savino B, Locati M, Zammataro L, Allavena P & Bonecchi R (2010) The chemokine system in cancer biology and therapy. Cytokine Growth Factor Rev 21, 27–39.
25. Lin EY & Pollard JW (2007) Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res 67, 5064–5066.
26. Schoppmann SF, Birner P, Stockl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K & Kerjaschki D (2002) Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161, 947–956.
27. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M & Naldini L (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8, 211–226.
28. Coffelt SB, Tal AO, Scholz A, De Palma M, Patel S, Urbich C, Biswas SK, Murdoch C, Plate KH, Reiss Y et al. (2010) Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions. Cancer Res 70, 5270–5280.
29. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J & Harris AL (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 56, 4625–4629.
30. 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.
31. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM et al. (2014) Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 513, 559–563.
32. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS & Albelda SM (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16, 183–194.
33. Shaul ME, Levy L, Sun J, Mishalian I, Singhal S, Kapoor V, Horng W, Fridlender G, Albelda SM & Fridlender ZG (2016) Tumor-associated neutrophils display a distinct N1 profile following TGFbeta modulation: a transcriptomics analysis of pro- vs. antitumor TANs. Oncoimmunology 5, e1232221.
34. Andzinski L, Kasnitz N, Stahnke S, Wu CF, Gereke M, von Kockritz-Blickwede M, Schilling B, Brandau S, Weiss S & Jablonska J (2016) Type I IFNs induce anti-tumor polarization of tumor associated neutrophils in mice and human. Int J Cancer 138, 1982–1993.
35. Eruslanov EB, Bhojnagarwala PS, Quatromoni JG, Stephen TL, Ranganathan A, Deshpande C, Akimova T, Vachani A, Litzky L, Hancock WW et al. (2014) Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J Clin Invest 124, 5466–5480.
36. Mishalian I, Bayuh R, Eruslanov E, Michaeli J, Levy L, Zolotarov L, Singhal S, Albelda SM, Granot Z & Fridlender ZG (2014) Neutrophils recruit regulatory T-cells into tumors via secretion of CCL17–a new mechanism of impaired antitumor immunity. Int J Cancer 135, 1178–1186.
37. Rotondo R, Barisione G, Mastracci L, Grossi F, Orengo AM, Costa R, Truini M, Fabbi M, Ferrini S & Barbieri O (2009) IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer 125, 887–893.
38. Nozawa H, Chiu C & Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 103, 12493–12498.
39. Demers M, Wong SL, Martinod K, Gallant M, Cabral JE, Wang Y & Wagner DD (2016) Priming of neutrophils toward NETosis promotes tumor growth. Oncoimmunology 5, e1134073.
40. Berger-Achituv S, Brinkmann V, Abed UA, Kuhn LI, Ben-Ezra J, Elhasid R & Zychlinsky A (2013) A proposed role for neutrophil extracellular traps in cancer immunoediting. Front Immunol 4, 48.
41. Condeelis J & Segall JE (2003) Intravital imaging of cell movement in tumours. Nat Rev Cancer 3, 921–930.
42. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J & Condeelis J (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64, 7022–7029.
43. 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.
44. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA et al. (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438, 820–827.
45. Lim SY, Gordon-Weeks A, Allen D, Kersemans V, Beech J, Smart S & Muschel RJ (2015) Cd11b(+) myeloid cells support hepatic metastasis through down-regulation of angiopoietin-like 7 in cancer cells. Hepatology 62, 521–533.
46. Zhao L, Lim SY, Gordon-Weeks AN, Tapmeier TT, Im JH, Cao Y, Beech J, Allen D, Smart S & Muschel RJ (2013) Recruitment of a myeloid cell subset (CD11b/Gr1 mid) via CCL2/CCR2 promotes the development of colorectal cancer liver metastasis. Hepatology 57, 829–839.
47. Lu X & Kang Y (2009) Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem 284, 29087–29096.
48. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA & Pollard JW (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222–225.
49. Kitamura T, Qian BZ, Soong D, Cassetta L, Noy R, Sugano G, Kato Y, Li J & Pollard JW (2015) CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J Exp Med 212, 1043–1059.
50. Hanna RN, Cekic C, Sag D, Tacke R, Thomas GD, Nowyhed H, Herrley E, Rasquinha N, McArdle S, Wu R et al. (2015) Patrolling monocytes control tumor metastasis to the lung. Science 350, 985–990.
51. Coffelt SB, Kersten K, Doornebal CW, Weiden J, Vrijland K, Hau CS, Verstegen NJ, Ciampricotti M, Hawinkels LJ, Jonkers J et al. (2015) IL-17-producing gammadelta T cells and neutrophils conspire to promote breast cancer metastasis. Nature 522, 345–348.
52. Spiegel A, Brooks MW, Houshyar S, Reinhardt F, Ardolino M, Fessler E, Chen MB, Krall JA, DeCock J, Zervantonakis IK et al. (2016) Neutrophils suppress intraluminal NK cell-mediated tumor cell clearance and enhance extravasation of disseminated carcinoma cells. Cancer Discov 6, 630–649.
53. Park J, Wysocki RW, Amoozgar Z, Maiorino L, Fein MR, Jorns J, Schott AF, Kinugasa-Katayama Y, Lee Y, Won NH et al. (2016) Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci Transl Med 8, 361ra138.
54. Catena R, Bhattacharya N, El Rayes T, Wang S, Choi H, Gao D, Ryu S, Joshi N, Bielenberg D, Lee SB et al. (2013) Bone marrow-derived Gr1+ cells can generate a metastasis-resistant microenvironment via induced secretion of thrombospondin-1. Cancer Discov 3, 578–589.
55. Granot Z, Henke E, Comen EA, King TA, Norton L & Benezra R (2011) Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20, 300–314.
56. Naba A, Clauser KR, Hoersch S, Liu H, Carr SA & Hynes RO (2012) The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol Cell Proteomics 11, M111.014647.
57. Perryman L & Erler JT (2014) Lysyl oxidase in cancer research. Future Oncol 10, 1709–1717.
58. Hoye AM & Erler JT (2016) Structural ECM components in the premetastatic and metastatic niche. Am J Physiol Cell Physiol 310, C955–C967.
59. Mason SD & Joyce JA (2011) Proteolytic networks in cancer. Trends Cell Biol 21, 228–237.
60. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891–906.
61. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG & Keely PJ (2008) Collagen density promotes mammary tumor initiation and progression. BMC Med 6, 11.
62. Bonanno E, Iurlaro M, Madri JA & Nicosia RF (2000) Type IV collagen modulates angiogenesis and neovessel survival in the rat aorta model. In Vitro Cell Dev Biol Anim 36, 336–340.
63. Myers KA, Applegate KT, Danuser G, Fischer RS & Waterman CM (2011) Distinct ECM mechanosensing pathways regulate microtubule dynamics to control endothelial cell branching morphogenesis. J Cell Biol 192, 321–334.
64. Liu J & Agarwal S (2010) Mechanical signals activate vascular endothelial growth factor receptor-2 to upregulate endothelial cell proliferation during inflammation. J Immunol 185, 1215–1221.
65. O'Connor RS, Hao X, Shen K, Bashour K, Akimova T, Hancock WW, Kam LC & Milone MC (2012) Substrate rigidity regulates human T cell activation and proliferation. J Immunol 189, 1330–1339.
66. Leight JL, Wozniak MA, Chen S, Lynch ML & Chen CS (2012) Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 23, 781–791.
67. Pickup MW, Laklai H, Acerbi I, Owens P, Gorska AE, Chytil A, Aakre M, Weaver VM & Moses HL (2013) Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-beta-deficient mouse mammary carcinomas. Cancer Res 73, 5336–5346.
68. Sleeman JP (2012) The metastatic niche and stromal progression. Cancer Metastasis Rev 31, 429–440.
69. Paget S (1989) The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 8, 98–101.
70. 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.
71. Cox TR, Bird D, Baker AM, Barker HE, Ho MW, Lang G & Erler JT (2013) LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res 73, 1721–1732.
72. Elkabets M, Gifford AM, Scheel C, Nilsson B, Reinhardt F, Bray MA, Carpenter AE, Jirstrom K, Magnusson K, Ebert BL et al. (2011) Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J Clin Invest 121, 784–799.
73. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S et al. (2015) Tumour exosome integrins determine organotropic metastasis. Nature 527, 329–335.
74. Hakulinen J, Sankkila L, Sugiyama N, Lehti K & Keski-Oja J (2008) Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem 105, 1211–1218.
75. Mu W, Rana S & Zoller M (2013) Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 15, 875–887.
76. Gilkes DM, Semenza GL & Wirtz D (2014) Hypoxia and the extracellular matrix: drivers of tumour metastasis. Nat Rev Cancer 14, 430–439.
77. Barkan D, Green JE & Chambers AF (2010) Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur J Cancer 46, 1181–1188.
78. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, Webster JD, Hoover S, Simpson RM, Gauldie J et al. (2010) Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 70, 5706–5716.
79. Kessenbrock K, Plaks V & Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52–67.
80. Maquart FX, Pasco S, Ramont L, Hornebeck W & Monboisse JC (2004) An introduction to matrikines: extracellular matrix-derived peptides which regulate cell activity. Implication in tumor invasion. Crit Rev Oncol Hematol 49, 199–202.
81. Deryugina EI & Quigley JP (2010) Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochem Biophys Acta 1803, 103–120.
82. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z et al. (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2, 737–744.
83. Hamano Y, Zeisberg M, Sugimoto H, Lively JC, Maeshima Y, Yang C, Hynes RO, Werb Z, Sudhakar A & Kalluri R (2003) Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 3, 589–601.
84. Murphy G (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat Rev Cancer 8, 929–941.
85. Arribas J & Esselens C (2009) ADAM17 as a therapeutic target in multiple diseases. Curr Pharm Des 15, 2319–2335.
86. Blobel CP (2005) ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 6, 32–43.
87. 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, 6368–6376.
88. Gocheva V & Joyce JA (2007) Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 6, 60–64.
89. Mohamed MM & Sloane BF (2006) Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 6, 764–775.
90. Tan GJ, Peng ZK, Lu JP & Tang FQ (2013) Cathepsins mediate tumor metastasis. World J Biol Chem 4, 91–101.
91. Jiang D & Lim SY (2016) Influence of immune myeloid cells on the extracellular matrix during cancer metastasis. Cancer Microenviron 9, 45–61.
92. Liguori M, Solinas G, Germano G, Mantovani A & Allavena P (2011) Tumor-associated macrophages as incessant builders and destroyers of the cancer stroma. Cancers 3, 3740–3761.
93. Ishihara D, Dovas A, Hernandez L, Pozzuto M, Wyckoff J, Segall JE, Condeelis JS, Bresnick AR & Cox D (2013) Wiskott-Aldrich syndrome protein regulates leukocyte-dependent breast cancer metastasis. Cell Rep 4, 429–436.
94. Yamaguchi H, Pixley F & Condeelis J (2006) Invadopodia and podosomes in tumor invasion. Eur J Cell Biol 85, 213–218.
95. Coussens LM, Tinkle CL, Hanahan D & Werb Z (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481–490.
96. Melani C, Sangaletti S, Barazzetta FM, Werb Z & Colombo MP (2007) Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res 67, 11438–11446.
97. Huang S, Van Arsdall M, Tedjarati S, McCarty M, Wu W, Langley R & Fidler IJ (2002) Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice. J Natl Cancer Inst 94, 1134–1142.
98. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM & Shibuya M (2002) MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2, 289–300.
99. Giraudo E, Inoue M & Hanahan D (2004) An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 114, 623–633.
100. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z et al. (2008) HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13, 206–220.
101. Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, Xiao HL, Wang B, Yi L, Wang QL et al. (2012) Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J Immunol 189, 444–453.
102. Deryugina EI, Zajac E, Juncker-Jensen A, Kupriyanova TA, Welter L & Quigley JP (2014) Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing MMP-9 in the tumor microenvironment. Neoplasia 16, 771–788.
103. Balbin M, Fueyo A, Tester AM, Pendas AM, Pitiot AS, Astudillo A, Overall CM, Shapiro SD & Lopez-Otin C (2003) Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 35, 252–257.
104. Gutierrez-Fernandez A, Fueyo A, Folgueras AR, Garabaya C, Pennington CJ, Pilgrim S, Edwards DR, Holliday DL, Jones JL, Span PN et al. (2008) Matrix metalloproteinase-8 functions as a metastasis suppressor through modulation of tumor cell adhesion and invasion. Cancer Res 68, 2755–2763.
105. Houghton AM, Grisolano JL, Baumann ML, Kobayashi DK, Hautamaki RD, Nehring LC, Cornelius LA & Shapiro SD (2006) Macrophage elastase (matrix metalloproteinase-12) suppresses growth of lung metastases. Cancer Res 66, 6149–6155.
106. Bohrer LR, Chaffee TS, Chuntova P, Brady NJ, Witschen PM, Kemp SE, Nelson AC, Walcheck B & Schwertfeger KL (2016) ADAM17 in tumor associated leukocytes regulates inflammatory mediators and promotes mammary tumor formation. Genes Cancer 7, 240–253.
107. Rego SL, Helms RS & Dreau D (2014) Breast tumor cell TACE-shed MCSF promotes pro-angiogenic macrophages through NF-kappaB signaling. Angiogenesis 17, 573–585.
108. Schlomann U, Koller G, Conrad C, Ferdous T, Golfi P, Garcia AM, Hofling S, Parsons M, Costa P, Soper R et al. (2015) ADAM8 as a drug target in pancreatic cancer. Nat Commun 6, 6175.
109. Romagnoli M, Mineva ND, Polmear M, Conrad C, Srinivasan S, Loussouarn D, Barille-Nion S, Georgakoudi I, Dagg A, McDermott EW et al. (2014) ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis. EMBO Mol Med 6, 278–294.
110. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, Berman T & Joyce JA (2010) IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev 24, 241–255.
111. Salpeter SJ, Pozniak Y, Merquiol E, Ben-Nun Y, Geiger T & Blum G (2015) A novel cysteine cathepsin inhibitor yields macrophage cell death and mammary tumor regression. Oncogene 34, 6066–6078.
112. Vasiljeva O, Papazoglou A, Kruger A, Brodoefel H, Korovin M, Deussing J, Augustin N, Nielsen BS, Almholt K, Bogyo M et al. (2006) Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Res 66, 5242–5250.
113. Shree T, Olson OC, Elie BT, Kester JC, Garfall AL, Simpson K, Bell-McGuinn KM, Zabor EC, Brogi E & Joyce JA (2011) Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 25, 2465–2479.
114. Gocheva V, Chen X, Peters C, Reinheckel T & Joyce JA (2010) Deletion of cathepsin H perturbs angiogenic switching, vascularization and growth of tumors in a mouse model of pancreatic islet cell cancer. Biol Chem 391, 937–945.
115. Smith HW & Marshall CJ (2010) Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 11, 23–36.
116. Xu Y, Hagege J, Doublet JD, Callard P, Sraer JD, Ronne E & Rondeau E (1997) Endothelial and macrophage upregulation of urokinase receptor expression in human renal cell carcinoma. Hum Pathol 28, 206–213.
117. Hildenbrand R, Wolf G, Bohme B, Bleyl U & Steinborn A (1999) Urokinase plasminogen activator receptor (CD87) expression of tumor-associated macrophages in ductal carcinoma in situ, breast cancer, and resident macrophages of normal breast tissue. J Leukoc Biol 66, 40–49.
118. Hildenbrand R, Dilger I, Horlin A & Stutte HJ (1995) Urokinase and macrophages in tumour angiogenesis. Br J Cancer 72, 818–823.
119. Sun Z & Yang P (2004) Role of imbalance between neutrophil elastase and alpha 1-antitrypsin in cancer development and progression. Lancet Oncol 5, 182–190.
120. Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR et al. (2010) Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 16, 219–223.
121. Atai NA, Bansal M, Lo C, Bosman J, Tigchelaar W, Bosch KS, Jonker A, De Witt Hamer PC, Troost D, McCulloch CA et al. (2011) Osteopontin is up-regulated and associated with neutrophil and macrophage infiltration in glioblastoma. Immunology 132, 39–48.
122. Rittling SR & Chambers AF (2004) Role of osteopontin in tumour progression. Br J Cancer 90, 1877–1881.
123. Rich JN, Shi Q, Hjelmeland M, Cummings TJ, Kuan CT, Bigner DD, Counter CM & Wang XF (2003) Bone-related genes expressed in advanced malignancies induce invasion and metastasis in a genetically defined human cancer model. J Biol Chem 278, 15951–15957.
124. Zhou LT, Liu FY, Li Y, Peng YM, Liu YH & Li J (2012) Gpnmb/osteoactivin, an attractive target in cancer immunotherapy. Neoplasma 59, 1–5.
125. Szulzewsky F, Pelz A, Feng X, Synowitz M, Markovic D, Langmann T, Holtman IR, Wang X, Eggen BJ, Boddeke HW et al. (2015) Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1. PLoS One 10, e0116644.
126. Wang K, Seo BR, Fischbach C & Gourdon D (2016) Fibronectin mechanobiology regulates tumorigenesis. Cell Mol Bioeng 9, 1–11.
127. Solinas G, Schiarea S, Liguori M, Fabbri M, Pesce S, Zammataro L, Pasqualini F, Nebuloni M, Chiabrando C, Mantovani A et al. (2010) Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J Immunol 185, 642–652.
128. Sargiannidou I, Zhou J & Tuszynski GP (2001) The role of thrombospondin-1 in tumor progression. Exp Biol Med 226, 726–733.
129. Fang M, Yuan J, Peng C & Li Y (2014) Collagen as a double-edged sword in tumor progression. Tumour Biol 35, 2871–2882.
130. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, Segall JE, Pollard JW & Condeelis J (2007) Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 67, 2649–2656.
131. Burke RM, Madden KS, Perry SW, Zettel ML & Brown EB 3rd (2013) Tumor-associated macrophages and stromal TNF-alpha regulate collagen structure in a breast tumor model as visualized by second harmonic generation. J Biomed Opt 18, 86003.
132. Allaoui R, Bergenfelz C, Mohlin S, Hagerling C, Salari K, Werb Z, Anderson RL, Ethier SP, Jirstrom K, Pahlman S et al. (2016) Cancer-associated fibroblast-secreted CXCL16 attracts monocytes to promote stroma activation in triple-negative breast cancers. Nat Commun 7, 13050.
133. Zhu Y, Herndon JM, Sojka DK, Kim KW, Knolhoff BL, Zuo C, Cullinan DR, Luo J, Bearden AR, Lavine KJ et al. (2017) Tissue-resident macrophages in pancreatic ductal adenocarcinoma originate from embryonic hematopoiesis and promote tumor progression. Immunity 47, 323–338.e6.
134. Nikolic-Paterson DJ, Wang S & Lan HY (2014) Macrophages promote renal fibrosis through direct and indirect mechanisms. Kidney Int Suppl (2011) 4, 34–38.
135. Weitkamp B, Cullen P, Plenz G, Robenek H & Rauterberg J (1999) Human macrophages synthesize type VIII collagen in vitro and in the atherosclerotic plaque. FASEB J 13, 1445–1457.
136. Ingman WV, Wyckoff J, Gouon-Evans V, Condeelis J & Pollard JW (2006) Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev Dyn 235, 3222–3229.
137. Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, Rauterberg J & Lorkowski S (2008) Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol 180, 5707–5719.
138. Puolakkainen PA, Brekken RA, Muneer S & Sage EH (2004) Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis. Mol Cancer Res 2, 215–224.
139. Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR & Colombo MP (2003) Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 198, 1475–1485.
140. Mehta K, Kumar A & Kim HI (2010) Transglutaminase 2: a multi-tasking protein in the complex circuitry of inflammation and cancer. Biochem Pharmacol 80, 1921–1929.
141. Knipper JA, Willenborg S, Brinckmann J, Bloch W, Maass T, Wagener R, Krieg T, Sutherland T, Munitz A, Rothenberg ME et al. (2015) Interleukin-4 receptor alpha signaling in myeloid cells controls collagen fibril assembly in skin repair. Immunity 43, 803–816.
142. Karlmark KR, Weiskirchen R, Zimmermann HW, Gassler N, Ginhoux F, Weber C, Merad M, Luedde T, Trautwein C & Tacke F (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50, 261–274.
143. Lebrun A, Lo Re S, Chantry M, Izquierdo Carerra X, Uwambayinema F, Ricci D, Devosse R, Ibouraadaten S, Brombin L, Palmai-Pallag M et al. (2017) CCR2+ monocytic-myeloid derived immunosuppressive cells (M-MDSC) inhibit collagen degradation and promote lung fibrosis by producing TGF-beta1. J Pathol 243, 320–330.
144. Pickup M, Novitskiy S & Moses HL (2013) The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 13, 788–799.
145. Mazur A, Holthoff E, Vadali S, Kelly T & Post SR (2016) Cleavage of Type I collagen by fibroblast activation protein-alpha enhances class A scavenger receptor mediated macrophage adhesion. PLoS One 11, e0150287.
146. Comito G, Giannoni E, Segura CP, Barcellos-de-Souza P, Raspollini MR, Baroni G, Lanciotti M, Serni S & Chiarugi P (2014) Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene 33, 2423–2431.
147. Gao D, Joshi N, Choi H, Ryu S, Hahn M, Catena R, Sadik H, Argani P, Wagner P, Vahdat LT et al. (2012) Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res 72, 1384–1394.
148. Iijima J, Konno K & Itano N (2011) Inflammatory alterations of the extracellular matrix in the tumor microenvironment. Cancers 3, 3189–3205.
149. Adair-Kirk TL, Atkinson JJ, Kelley DG, Arch RH, Miner JH & Senior RM (2005) A chemotactic peptide from laminin alpha 5 functions as a regulator of inflammatory immune responses via TNF alpha-mediated signaling. J Immunol 174, 1621–1629.
150. 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.
151. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA et al. (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11, 1173–1179.
152. Zhang G, Guo L, Yang C, Liu Y, He Y, Du Y, Wang W & Gao F (2016) A novel role of breast cancer-derived hyaluronan on inducement of M2-like tumor-associated macrophages formation. Oncoimmunology 5, e1172154.
153. Kuang DM, Wu Y, Chen N, Cheng J, Zhuang SM & Zheng L (2007) Tumor-derived hyaluronan induces formation of immunosuppressive macrophages through transient early activation of monocytes. Blood 110, 587–595.
154. del Fresno C, Otero K, Gomez-Garcia L, Gonzalez-Leon MC, Soler-Ranger L, Fuentes-Prior P, Escoll P, Baos R, Caveda L, Garcia F et al. (2005) Tumor cells deactivate human monocytes by up-regulating IL-1 receptor associated kinase-M expression via CD44 and TLR4. J Immunol 174, 3032–3040.
155. de La Motte CA, Hascall VC, Calabro A, Yen-Lieberman B & Strong SA (1999) Mononuclear leukocytes preferentially bind via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(I.C). J Biol Chem 274, 30747–30755.
156. Day AJ & Prestwich GD (2002) Hyaluronan-binding proteins: tying up the giant. J Biol Chem 277, 4585–4588.
157. Kobayashi N, Miyoshi S, Mikami T, Koyama H, Kitazawa M, Takeoka M, Sano K, Amano J, Isogai Z, Niida S et al. (2010) Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res 70, 7073–7083.
158. McWhorter FY, Davis CT & Liu WF (2015) Physical and mechanical regulation of macrophage phenotype and function. Cell Mol Life Sci 72, 1303–1316.
159. Friedl P & Weigelin B (2008) Interstitial leukocyte migration and immune function. Nat Immunol 9, 960–969.
160. Franco C, Britto K, Wong E, Hou G, Zhu SN, Chen M, Cybulsky MI & Bendeck MP (2009) Discoidin domain receptor 1 on bone marrow-derived cells promotes macrophage accumulation during atherogenesis. Circ Res 105, 1141–1148.
161. Postlethwaite AE & Kang AH (1976) Collagen-and collagen peptide-induced chemotaxis of human blood monocytes. J Exp Med 143, 1299–1307.
162. Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, Folkerts G, Nijkamp FP & Blalock JE (2006) A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 12, 317–323.
163. Sangaletti S, Tripodo C, Santangelo A, Castioni N, Portararo P, Gulino A, Botti L, Parenza M, Cappetti B, Orlandi R et al. (2016) Mesenchymal transition of high-grade breast carcinomas depends on extracellular matrix control of myeloid suppressor cell activity. Cell Rep 17, 233–248.
164. Afonso PV, McCann CP, Kapnick SM & Parent CA (2013) Discoidin domain receptor 2 regulates neutrophil chemotaxis in 3D collagen matrices. Blood 121, 1644–1650.
165. Wiesner C, Le-Cabec V, El Azzouzi K, Maridonneau-Parini I & Linder S (2014) Podosomes in space: macrophage migration and matrix degradation in 2D and 3D settings. Cell Adh Migr 8, 179–191.
166. Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I & Le Cabec V (2010) Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol 184, 1049–1061.
167. Kaplan G (1983) In vitro differentiation of human monocytes. Monocytes cultured on glass are cytotoxic to tumor cells but monocytes cultured on collagen are not. J Exp Med 157, 2061–2072.
168. Wesley RB 2nd, Meng X, Godin D & Galis ZS (1998) Extracellular matrix modulates macrophage functions characteristic to atheroma: collagen type I enhances acquisition of resident macrophage traits by human peripheral blood monocytes in vitro. Arterioscler Thromb Vasc Biol 18, 432–440.
169. Perri RT, Kay NE, McCarthy J, Vessella RL, Jacob HS & Furcht LT (1982) Fibronectin enhances in vitro monocyte-macrophage-mediated tumoricidal activity. Blood 60, 430–435.
170. Patel NR, Bole M, Chen C, Hardin CC, Kho AT, Mih J, Deng L, Butler J, Tschumperlin D, Fredberg JJ et al. (2012) Cell elasticity determines macrophage function. PLoS One 7, e41024.
171. Monboisse JC, Garnotel R, Randoux A, Dufer J & Borel JP (1991) Adhesion of human neutrophils to and activation by type-I collagen involving a beta 2 integrin. J Leukoc Biol 50, 373–380.
172. Lebbink RJ, de Ruiter T, Adelmeijer J, Brenkman AB, van Helvoort JM, Koch M, Farndale RW, Lisman T, Sonnenberg A, Lenting PJ et al. (2006) Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 203, 1419–1425.
173. Sangaletti S, Tripodo C, Vitali C, Portararo P, Guarnotta C, Casalini P, Cappetti B, Miotti S, Pinciroli P, Fuligni F et al. (2014) Defective stromal remodeling and neutrophil extracellular traps in lymphoid tissues favor the transition from autoimmunity to lymphoma. Cancer Discov 4, 110–129.
174. Flies DB, Higuchi T, Harris JC, Jha V, Gimotty PA & Adams SF (2016) Immune checkpoint blockade reveals the stimulatory capacity of tumor-associated CD103(+) dendritic cells in late-stage ovarian cancer. Oncoimmunology 5, e1185583.
175. Meyaard L, Hurenkamp J, Clevers H, Lanier LL & Phillips JH (1999) Leukocyte-associated Ig-like receptor-1 functions as an inhibitory receptor on cytotoxic T cells. J Immunol 162, 5800–5804.
176. Garcia-Mendoza MG, Inman DR, Ponik SM, Jeffery JJ, Sheerar DS, Van Doorn RR & Keely PJ (2016) Neutrophils drive accelerated tumor progression in the collagen-dense mammary tumor microenvironment. Breast Cancer Res 18, 49.
177. Mildner A, Schonheit J, Giladi A, David E, Lara-Astiaso D, Lorenzo-Vivas E, Paul F, Chappell-Maor L, Priller J, Leutz A et al. (2017) Genomic characterization of murine monocytes reveals C/EBPbeta transcription factor dependence of Ly6C- cells. Immunity 46, 849–862.e7.
178. Villani AC, Satija R, Reynolds G, Sarkizova S, Shekhar K, Fletcher J, Griesbeck M, Butler A, Zheng S, Lazo S et al. (2017) Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science 356, 1–12.
179. See P, Dutertre CA, Chen J, Gunther P, McGovern N, Irac SE, Gunawan M, Beyer M, Handler K, Duan K et al. (2017) Mapping the human DC lineage through the integration of high-dimensional techniques. Science 356, 1–13.
180. Varol C, Mildner A & Jung S (2015) Macrophages: development and tissue specialization. Annu Rev Immunol 33, 643–675.
181. Lavin Y, Kobayashi S, Leader A, Amir ED, Elefant N, Bigenwald C, Remark R, Sweeney R, Becker CD, Levine JH et al. (2017) Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses. Cell 169, 750–765.e17.
182. Menezes S, Melandri D, Anselmi G, Perchet T, Loschko J, Dubrot J, Patel R, Gautier EL, Hugues S, Longhi MP et al. (2016) The heterogeneity of Ly6Chi monocytes controls their differentiation into iNOS+ macrophages or monocyte-derived dendritic cells. Immunity 45, 1205–1218.