Tumor-conditioned macrophages secrete migration-stimulating factor: A new marker for M2-polarization, influencing tumor cell motility

Journal of Immunology

Volumn 185, Issue 1, 2010, Pages 642-652

  Solinas, Graziella ^a   Schiarea, Silvia ^b   Liguori, Manuela ^a   Fabbri, Marco ^a,d   Pesce, Samantha ^a   Zammataro, Luca ^a   Pasqualini, Fabio ^a   Nebuloni, Manuela ^c   Chiabrando, Chiara ^b   Mantovani, Alberto ^a,b   Allavena, Paola ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d JOINT RESEARCH CENTRE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR; FIBRONECTIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; ISOPROTEIN; MIGRATION STIMULATING FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; ONCOFETAL ANTIGEN; OSTEOACTIVIN; OSTEOPONTIN; SELENOPROTEIN; SELENOPROTEIN 1; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; MIGRATION STIMULATING FACTOR, HUMAN; TUMOR MARKER; TUMOR PROTEIN;

ANGIOGENESIS; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CELL SHAPE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MACROPHAGE; MASS; METASTASIS; MICROENVIRONMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA ANALYSIS; STROMA CELL; TUMOR CELL; TUMOR GROWTH; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; CELL LINE; CELL MOTION; CELL STRAIN HCT116; CELL STRAIN HT29; COCULTURE; CULTURE MEDIUM; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY; SECRETION; TUMOR CELL LINE;

CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL MOVEMENT; CELL POLARITY; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYTOKINES; HCT116 CELLS; HT29 CELLS; HUMANS; MACROPHAGES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; TUMOR MARKERS, BIOLOGICAL;

EID: 77956212940     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000413     Document Type: Article

References (108)

1. Sica, A., T. Schioppa, A. Mantovani, and P. Allavena. 2006. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur. J. Cancer 42: 717-727.
2. Steidl, C., T. Lee, S. P. Shah, P. Farinha, G. Han, T. Nayar, A. Delaney, S. J. Jones, J. Iqbal, D. D. Weisenburger, et al. 2010. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N. Engl. J. Med. 362: 875-885.
3. Condeelis, J., and J. W. Pollard. 2006. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266.
4. An, T., U. Sood, T. Pietruk, G. Cummings, K. Hashimoto, and J. D. Crissman. 1987. In situ quantitation of inflammatory mononuclear cells in ductal infiltrating breast carcinoma. Relation to prognostic parameters. Am. J. Pathol. 128: 52-60.
5. Bingle, L., N. J. Brown, and C. E. Lewis. 2002. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196: 254-265.
6. Tsutsui, S., K. Yasuda, K. Suzuki, K. Tahara, H. Higashi, and S. Era. 2005. Macrophage infiltration and its prognostic implications in breast cancer: the relationship with VEGF expression and microvessel density. Oncol. Rep. 14: 425-431.
7. Pollard, J. W. 2008. Macrophages define the invasive microenvironment in breast cancer. J. Leukoc. Biol. 84: 623-630.
8. Paik, S., S. Shak, G. Tang, C. Kim, J. Baker, M. Cronin, F. L. Baehner, M. G. Walker, D. Watson, T. Park, et al. 2004. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351: 2817-2826.
9. Dave, S. S., G. Wright, B. Tan, A. Rosenwald, R. D. Gascoyne, W. C. Chan, R. I. Fisher, R. M. Braziel, L. M. Rimsza, T. M. Grogan, et al. 2004. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N. Engl. J. Med. 351: 2159-2169.
10. Lin, E. Y., A. V. Nguyen, R. G. Russell, and J. W. Pollard. 2001. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193: 727-740.
11. Lazennec, G., and A. Richmond. 2010. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol. Med. 16: 133-144.
12. Solinas, G., G. Germano, A. Mantovani, and P. Allavena. 2009. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J. Leukoc. Biol. 86: 1065-1073.
13. DeNardo, D. G., M. Johansson, and L. M. Coussens. 2008. Immune cells as mediators of solid tumor metastasis. Cancer Metastasis Rev. 27: 11-18.
14. Mantovani, A., T. Schioppa, C. Porta, P. Allavena, and A. Sica. 2006. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 25: 315-322.
15. Pollard, J. W. 2004. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4: 71-78.
16. Talmadge, J. E., M. Donkor, and E. Scholar. 2007. Inflammatory cell infiltration of tumors: Jekyll or Hyde. Cancer Metastasis Rev. 26: 373-400.
17. Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature 454: 436-444.
18. Hagemann, T., S. C. Robinson, M. Schulz, L. Trümper, F. R. Balkwill, and C. Binder. 2004. Enhanced invasiveness of breast cancer cell lines upon cocultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases. Carcinogenesis 25: 1543-1549.
19. Biswas, S. K., L. Gangi, S. Paul, T. Schioppa, A. Saccani, M. Sironi, B. Bottazzi, A. Doni, B. Vincenzo, F. Pasqualini, et al. 2006. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 107: 2112-2122.
20. Ojalvo, L. S., C. A. Whittaker, J. S. Condeelis, and J. W. Pollard. 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.
21. Joyce, J. A., and J. W. Pollard. 2009. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9: 239-252.
22. Erler, J. T., K. L. Bennewith, T. R. Cox, G. Lang, D. Bird, A. Koong, Q. T. Le, and A. J. Giaccia. 2009. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15: 35-44.
23. Hiratsuka, S., A. Watanabe, H. Aburatani, and Y. Maru. 2006. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8: 1369-1375.
24. Kaplan, R. N., S. Rafii, and D. Lyden. 2006. Preparing the "soil": the pre-metastatic niche. Cancer Res. 66: 11089-11093.
25. Kaplan, R. N., R. D. Riba, S. Zacharoulis, A. H. Bramley, L. Vincent, C. Costa, D. D. MacDonald, D. K. Jin, K. Shido, S. A. Kerns, et al. 2005. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827.
26. Murdoch, C., M. Muthana, S. B. Coffelt, and C. E. Lewis. 2008. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 8: 618-631.
27. Padua, D., X. H. Zhang, Q. Wang, C. Nadal, W. L. Gerald, R. R. Gomis, and J. Massagué. 2008. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133: 66-77. (Pubitemid 351442989)
28. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555.
29. Ghassabeh, G. H., P. De Baetselier, L. Brys, W. Noël, J. A. Van Ginderachter, S. Meerschaut, A. Beschin, F. Brombacher, and G. Raes. 2006. Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 108: 575-583.
30. Nevala, W. K., C. M. Vachon, A. A. Leontovich, C. G. Scott, M. A. Thompson, and S. N. Markovic; Melanoma Study Group of the Mayo Clinic Cancer Center. 2009. Evidence of systemic Th2-driven chronic inflammation in patients with metastatic melanoma. Clin. Cancer Res. 15: 1931-1939.
31. Deepak, P., S. Kumar, and A. Acharya. 2007. Interleukin-13-induced type II polarization of inflammatory macrophages is mediated through suppression of nuclear factor-kappaB and preservation of IkappaBalpha in a T cell lymphoma. [Published retraction appears in 2009 Clin. Exp. Immunol. 158: 334.] Clin. Exp. Immunol. 149: 378-386.
32. Cheadle, E. J., K. Riyad, D. Subar, D. G. Rothwell, G. Ashton, H. Batha, D. J. Sherlock, R. E. Hawkins, and D. E. Gilham. 2007. Eotaxin-2 and colorectal cancer: a potential target for immune therapy. Clin. Cancer Res. 13: 5719-5728.
33. DeNardo, D. G., J. B. Barreto, P. Andreu, L. Vasquez, D. Tawfik, N. Kolhatkar, and L. M. Coussens. 2009. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16: 91-102.
34. Goerdt, S., and C. E. Orfanos. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10: 137-142.
35. Gabrilovich, D. I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9: 162-174.
36. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964.
37. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
38. Mantovani, A., A. Sica, and M. Locati. 2005. Macrophage polarization comes of age. Immunity 23: 344-346.
39. Martinez, F. O., L. Helming, and S. Gordon. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27: 451-483.
40. Van Ginderachter, J. A., K. Movahedi, G. Hassanzadeh Ghassabeh, S. Meerschaut, A. Beschin, G. Raes, and P. De Baetselier. 2006. Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 211: 487-501.
41. Saccani, A., T. Schioppa, C. Porta, S. K. Biswas, M. Nebuloni, L. Vago, B. Bottazzi, M. P. Colombo, A. Mantovani, and A. Sica. 2006. p50 nuclear factor-kappaB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance. Cancer Res. 66: 11432-11440.
42. Porta, C., M. Rimoldi, G. Raes, L. Brys, P. Ghezzi, D. Di Liberto, F. Dieli, S. Ghisletti, G. Natoli, P. De Baetselier, et al. 2009. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc. Natl. Acad. Sci. USA 106: 14978-14983.
43. Bouhlel, M. A., B. Derudas, E. Rigamonti, R. Dièvart, J. Brozek, S. Haulon, C. Zawadzki, B. Jude, G. Torpier, N. Marx, et al. 2007. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 6: 137-143.
44. Van Ginderachter, J. A., K. Movahedi, J. Van den Bossche, and P. De Baetselier. 2008. Macrophages, PPARs, and Cancer. PPAR Res. 2008: 169414.
45. Van Ginderachter, J. A., S. Meerschaut, Y. Liu, L. Brys, K. De Groeve, G. Hassanzadeh Ghassabeh, G. Raes, and P. De Baetselier. 2006. Peroxisome proliferator-activated receptor gamma (PPARgamma) ligands reverse CTL suppression by alternatively activated (M2) macrophages in cancer. Blood 108: 525-535.
46. Odegaard, J. I., R. R. Ricardo-Gonzalez, M. H. Goforth, C. R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A. W. Ferrante, and A. Chawla. 2007. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120.
47. Kuroda, E., V. Ho, J. Ruschmann, F. Antignano, M. Hamilton, M. J. Rauh, A. Antov, R. A. Flavell, L. M. Sly, and G. Krystal. 2009. SHIP represses the generation of IL-3-induced M2 macrophages by inhibiting IL-4 production from basophils. J. Immunol. 183: 3652-3660.
48. Roca, H., Z. S. Varsos, S. Sud, M. J. Craig, C. Ying, and K. J. Pienta. 2009. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J. Biol. Chem. 284: 34342-34354.
49. Perrier, P., F. O. Martinez, M. Locati, G. Bianchi, M. Nebuloni, G. Vago, F. Bazzoni, S. Sozzani, P. Allavena, and A. Mantovani. 2004. Distinct transcriptional programs activated by interleukin-10 with or without lipopolysaccharide in dendritic cells: induction of the B cell-activating chemokine, CXC chemokine ligand 13. J. Immunol. 172: 7031-7042.
50. Jolliffe, I. T. 2002. Principal Component Analysis. Springer, New York.
51. Pixley, F. J., and E. R. Stanley. 2004. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol. 14: 628-638.
52. Kzhyshkowska, J., S. Mamidi, A. Gratchev, E. Kremmer, C. Schmuttermaier, L. Krusell, G. Haus, J. Utikal, K. Schledzewski, J. Scholtze, and S. Goerdt. 2006. Novel stabilin-1 interacting chitinase-like protein (SI-CLP) is up-regulated in alternatively activated macrophages and secreted via lysosomal pathway. Blood 107: 3221-3228.
53. Martinez, F. O., S. Gordon, M. Locati, and A. Mantovani. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177: 7303-7311.
54. Raychaudhuri, S., J. M. Stuart, and R. B. Altman. 2000. Principal components analysis to summarize microarray experiments: application to sporulation time series. Pac. Symp. Biocomput. 5: 455-466.
55. Reiner, A., D. Yekutieli, and Y. Benjamini. 2003. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375. (Pubitemid 36284936)
56. Astrof, S., and R. O. Hynes. 2009. Fibronectins in vascular morphogenesis. Angiogenesis 12: 165-175.
57. Balza, E., F. Sassi, E. Ventura, A. Parodi, S. Fossati, W. Blalock, B. Carnemolla, P. Castellani, L. Zardi, and L. Borsi. 2009. A novel human fi- bronectin cryptic sequence unmasked by the insertion of the angiogenesis- associated extra type III domain B. Int. J. Cancer 125: 751-758.
58. Ffrench-Constant, C., L. Van de Water, H. F. Dvorak, and R. O. Hynes. 1989. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J. Cell Biol. 109: 903-914.
59. Kornblihtt, A. R., C. G. Pesce, C. R. Alonso, P. Cramer, A. Srebrow, S. Werbajh, and A. F. Muro. 1996. The fibronectin gene as a model for splicing and transcription studies. FASEB J. 10: 248-257.
60. Castellani, P., G. Viale, A. Dorcaratto, G. Nicolo, J. Kaczmarek, G. Querze, and L. Zardi. 1994. The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis. Int. J. Cancer 59: 612-618.
61. Labat-Robert, J. 2002. Fibronectin in malignancy. Semin. Cancer Biol. 12: 187-195.
62. Schor, S. L., I. R. Ellis, S. J. Jones, R. Baillie, K. Seneviratne, J. Clausen, K. Motegi, B. Vojtesek, K. Kankova, E. Furrie, et al. 2003. Migration-stimulating factor: a genetically truncated onco-fetal fibronectin isoform expressed by carcinoma and tumor-associated stromal cells. Cancer Res. 63: 8827-8836.
63. Steinbrenner, H., and H. Sies. 2009. Protection against reactive oxygen species by selenoproteins. Biochim. Biophys. Acta 1790: 1478-1485.
64. Bosschaerts, T., M. Guilliams, W. Noel, M. Hérin, R. F. Burk, K. E. Hill, L. Brys, G. Raes, G. H. Ghassabeh, P. De Baetselier, and A. Beschin. 2008. Alternatively activated myeloid cells limit pathogenicity associated with African trypanosomiasis through the IL-10 inducible gene selenoprotein P. J. Immunol. 180: 6168-6175.
65. Rich, J. N., Q. Shi, M. Hjelmeland, T. J. Cummings, C. T. Kuan, D. D. Bigner, C. M. Counter, and X. F. Wang. 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.
66. Ogawa, T., T. Nikawa, H. Furochi, M. Kosyoji, K. Hirasaka, N. Suzue, K. Sairyo, S. Nakano, T. Yamaoka, M. Itakura, et al. 2005. Osteoactivin upregulates expression of MMP-3 and MMP-9 in fibroblasts infiltrated into denervated skeletal muscle in mice. Am. J. Physiol. Cell Physiol. 289: C697-C707.
67. Furochi, H., S. Tamura, K. Takeshima, K. Hirasaka, R. Nakao, K. Kishi, and T. Nikawa. 2007. Overexpression of osteoactivin protects skeletal muscle from severe degeneration caused by long-term denervation in mice. J. Med. Invest. 54: 248-254.
68. Pahl, M. V., N. D. Vaziri, J. Yuan, and S. G. Adler. 2010. Upregulation of monocyte/macrophage HGFIN (Gpnmb/Osteoactivin) expression in end-stage renal disease. Clin. J. Am. Soc. Nephrol. 5: 56-61.
69. Weterman, M. A., N. Ajubi, I. M. van Dinter, W. G. Degen, G. N. van Muijen, D. J. Ruitter, and H. P. Bloemers. 1995. nmb, a novel gene, is expressed in low-metastatic human melanoma cell lines and xenografts. Int. J. Cancer 60: 73-81.
70. Loging, W. T., A. Lal, I. M. Siu, T. L. Loney, C. J. Wikstrand, M. A. Marra, C. Prange, D. D. Bigner, R. L. Strausberg, and G. J. Riggins. 2000. Identifying potential tumor markers and antigens by database mining and rapid expression screening. Genome Res. 10: 1393-1402.
71. Onaga, M., A. Ido, S. Hasuike, H. Uto, A. Moriuchi, K. Nagata, T. Hori, K. Hayash, and H. Tsubouchi. 2003. Osteoactivin expressed during cirrhosis development in rats fed a choline-deficient, L-amino acid-defined diet, accelerates motility of hepatoma cells. J. Hepatol. 39: 779-785.
72. Shikano, S., M. Bonkobara, P. K. Zukas, and K. Ariizumi. 2001. Molecular cloning of a dendritic cell-associated transmembrane protein, DC-HIL, that promotes RGD-dependent adhesion of endothelial cells through recognition of heparan sulfate proteoglycans. J. Biol. Chem. 276: 8125-8134.
73. Haylock, D. N., and S. K. Nilsson. 2006. Osteopontin: a bridge between bone and blood. Br. J. Haematol. 134: 467-474.
74. O'Regan, A. W., G. J. Nau, G. L. Chupp, and J. S. Berman. 2000. Osteopontin (Eta-1) in cell-mediated immunity: teaching an old dog new tricks. Immunol. Today 21: 475-478.
75. Shinohara, M. L., L. Lu, J. Bu, M. B. Werneck, K. S. Kobayashi, L. H. Glimcher, and H. Cantor. 2006. Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nat. Immunol. 7: 498-506.
76. Rangaswami, H., A. Bulbule, and G. C. Kundu. 2006. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 16: 79-87.
77. Shinohara, M. L., M. Jansson, E. S. Hwang, M. B. Werneck, L. H. Glimcher, and H. Cantor. 2005. T-bet-dependent expression of osteopontin contributes to T cell polarization. Proc. Natl. Acad. Sci. USA 102: 17101-17106.
78. Diao, H., S. Kon, K. Iwabuchi, C. Kimura, J. Morimoto, D. Ito, T. Segawa, M. Maeda, J. Hamuro, T. Nakayama, et al. 2004. Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 21: 539-550.
79. Denhardt, D. T., M. Noda, A. W. O'Regan, D. Pavlin, and J. S. Berman. 2001. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J. Clin. Invest. 107: 1055-1061.
80. Scatena, M., L. Liaw, and C. M. Giachelli. 2007. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler. Thromb. Vasc. Biol. 27: 2302-2309.
81. Hur, E. M., S. Youssef, M. E. Haws, S. Y. Zhang, R. A. Sobel, and L. Steinman. 2007. Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat. Immunol. 8: 74-83.
82. Senger, D. R., C. A. Perruzzi, C. F. Gracey, A. Papadopoulos, and D. G. Tenen. 1988. Secreted phosphoproteins associated with neoplastic transformation: close homology with plasma proteins cleaved during blood coagulation. Cancer Res. 48: 5770-5774.
83. Brown, L. F., A. Papadopoulos-Sergiou, B. Berse, E. J. Manseau, K. Tognazzi, C. A. Perruzzi, H. F. Dvorak, and D. R. Senger. 1994. Osteopontin expression and distribution in human carcinomas. Am. J. Pathol. 145: 610-623.
84. Bellahcène, A., and V. Castronovo. 1995. Increased expression of osteonectin and osteopontin, two bone matrix proteins, in human breast cancer. Am. J. Pathol. 146: 95-100.
85. Hirota, S., A. Ito, J. Nagoshi, M. Takeda, A. Kurata, Y. Takatsuka, K. Kohri, S. Nomura, and Y. Kitamura. 1995. Expression of bone matrix protein messenger ribonucleic acids in human breast cancers. Possible involvement of osteopontin in development of calcifying foci. Lab. Invest. 72: 64-69.
86. Singhal, H., D. S. Bautista, K. S. Tonkin, F. P. O'Malley, A. B. Tuck, A. F. Chambers, and J. F. Harris. 1997. Elevated plasma osteopontin in metastatic breast cancer associated with increased tumor burden and decreased survival. Clin. Cancer Res. 3: 605-611.
87. Tuck, A. B., F. P. O'Malley, H. Singhal, J. F. Harris, K. S. Tonkin, N. Kerkvliet, Z. Saad, G. S. Doig, and A. F. Chambers. 1998. Osteopontin expression in a group of lymph node negative breast cancer patients. Int. J. Cancer 79: 502-508.
88. Casson, A. G., S. M. Wilson, J. A. McCart, F. P. O'Malley, H. Ozcelik, M. S. Tsao, and A. F. Chambers. 1997. ras mutation and expression of the ras-regulated genes osteopontin and cathepsin L in human esophageal cancer. Int. J. Cancer 72: 739-745.
89. Gotoh, M., M. Sakamoto, K. Kanetaka, M. Chuuma, and S. Hirohashi. 2002. Overexpression of osteopontin in hepatocellular carcinoma. Pathol. Int. 52: 19-24.
90. Kazanecki, C. C., D. J. Uzwiak, and D. T. Denhardt. 2007. Control of osteopontin signaling and function by post-translational phosphorylation and protein folding. J. Cell. Biochem. 102: 912-924.
91. Liaw, L., M. P. Skinner, E. W. Raines, R. Ross, D. A. Cheresh, S. M. Schwartz, and C. M. Giachelli. 1995. The adhesive and migratory effects of osteopontin are mediated via distinct cell surface integrins. Role of alpha v beta 3 in smooth muscle cell migration to osteopontin in vitro. J. Clin. Invest. 95: 713-724.
92. Weber, G. F., S. Ashkar, M. J. Glimcher, and H. Cantor. 1996. Receptor-ligand interaction between CD44 and osteopontin (Eta-1). Science 271: 509-512.
93. Kaczmarek, J., P. Castellani, G. Nicolo, B. Spina, G. Allemanni, and L. Zardi. 1994. Distribution of oncofetal fibronectin isoforms in normal, hyperplastic and neoplastic human breast tissues. Int. J. Cancer 59: 11-16. (Pubitemid 24310940)
94. Oyama, F., S. Hirohashi, Y. Shimosato, K. Titani, and K. Sekiguchi. 1990. Oncodevelopmental regulation of the alternative splicing of fibronectin pre-messenger RNA in human lung tissues. Cancer Res. 50: 1075-1078.
95. Oyama, F., S. Hirohashi, Y. Shimosato, K. Titani, and K. Sekiguchi. 1989. Deregulation of alternative splicing of fibronectin pre-mRNA in malignant human liver tumors. J. Biol. Chem. 264: 10331-10334.
96. Zardi, L., B. Carnemolla, A. Siri, T. E. Petersen, G. Paolella, G. Sebastio, and F. E. Baralle. 1987. Transformed human cells produce a new fibronectin isoform by preferential alternative splicing of a previously unobserved exon. EMBO J. 6: 2337-2342.
97. Schwarzbauer, J. E., R. S. Patel, D. Fonda, and R. O. Hynes. 1987. Multiple sites of alternative splicing of the rat fibronectin gene transcript. EMBO J. 6: 2573-2580.
98. Gutman, A., and A. R. Kornblihtt. 1987. Identification of a third region of cell-specific alternative splicing in human fibronectin mRNA. Proc. Natl. Acad. Sci. USA 84: 7179-7182.
99. Midulla, M., R. Verma, M. Pignatelli, M. A. Ritter, N. S. Courtenay-Luck, and A. J. George. 2000. Source of oncofetal ED-B-containing fibronectin: implications of production by both tumor and endothelial cells. Cancer Res. 60: 164-169.
100. Schor, S. L., A. M. Schor, G. Rushton, and L. Smith. 1985. Adult, foetal and transformed fibroblasts display different migratory phenotypes on collagen gels: evidence for an isoformic transition during foetal development. J. Cell Sci. 73: 221-234.
101. Schor, S. L., A. M. Schor, A. M. Grey, and G. Rushton. 1988. Foetal and cancer patient fibroblasts produce an autocrine migration-stimulating factor not made by normal adult cells. J. Cell Sci. 90: 391-399.
102. Schor, S. L., and A. M. Schor. 2001. Phenotypic and genetic alterations in mammary stroma: implications for tumour progression. Breast Cancer Res. 3: 373-379.
103. Schor, S. L., A. M. Schor, A. M. Grey, J. Chen, G. Rushton, M. E. Grant, and I. Ellis. 1989. Mechanism of action of the migration stimulating factor produced by fetal and cancer patient fibroblasts: effect on hyaluronic and synthesis. In Vitro Cell. Dev. Biol. 25: 737-746.
104. Ellis, I., A. M. Grey, A. M. Schor, and S. L. Schor. 1992. Antagonistic effects of TGF-beta 1 and MSF on fibroblast migration and hyaluronic acid synthesis. Possible implications for dermal wound healing. J. Cell Sci. 102: 447-456.
105. Houard, X., S. Germain, M. Gervais, A. Michaud, F. van den Brûle, J. M. Foidart, A. Noël, C. Monnot, and P. Corvol. 2005. Migration-stimulating factor displays HEXXH-dependent catalytic activity important for promoting tumor cell migration. Int. J. Cancer 116: 378-384.
106. Qian, B., Y. Deng, J. H. Im, R. J. Muschel, Y. Zou, J. Li, R. A. Lang, and J. W. Pollard. 2009. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS ONE 4: e6562.
107. Hu, H., Y. Ran, Y. Zhang, Z. Zhou, S. J. Harris, L. Yu, L. Sun, J. Pan, J. Liu, J. Lou, and Z. Yang. 2009. Antibody library-based tumor endothelial cells surface proteomic functional screen reveals migration-stimulating factor as an anti-angiogenic target. Mol. Cell. Proteomics 8: 816-826.
108. Picardo, M., S. L. Schor, A. M. Grey, A. Howell, I. Laidlaw, J. Redford, and A. M. Schor. 1991. Migration stimulating activity in serum of breast cancer patients. Lancet 337: 130-133.