Pro-metastatic tumor-stroma interactions in breast cancer

Future Oncology

Volumn 8, Issue 11, 2012, Pages 1427-1442

  Gangadhara, Sharath ^a,b   Barrett Lee, Peter ^b   Nicholson, Robert I ^a   Hiscox, Stephen ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b VELINDRE CANCER CENTRE   (United Kingdom)

Author keywords

breast cancer; cancer associated fibroblasts; extracellular matrix; integrins; metastases; tumor microenvironment; tumor progression; tumor associated macrophages

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 6; FIBROBLAST GROWTH FACTOR 2; GELATINASE A; GELATINASE B; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; LAMININ; STROMAL CELL DERIVED FACTOR 1; STROMELYSIN; STROMELYSIN 3; TOLL LIKE RECEPTOR 2; UVOMORULIN; VERSICAN;

ADHESION; ADIPOCYTE; BREAST CANCER; BREAST CARCINOMA; CANCER GROWTH; CANCER INVASION; CAUSE OF DEATH; CELL ADHESION; CELL DEDIFFERENTIATION; CELL INVASION; CELL MIGRATION; DISEASE FREE SURVIVAL; DISTANT METASTASIS; DORMANCY; ENDOTHELIUM CELL; FIBROBLAST; GENE EXPRESSION PROFILING; HUMAN; LYMPH FLOW; LYMPHATIC DRAINAGE; MIGRATION; OVERALL SURVIVAL; OXIDATIVE STRESS; PARACRINE SIGNALING; PERICYTE; PRIMARY TUMOR; PRIORITY JOURNAL; RECURRENT DISEASE; REVIEW; STROMA CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; VENOUS CIRCULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL COMMUNICATION; FEMALE; HUMANS; NEOPLASM METASTASIS; STROMAL CELLS; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT;

EID: 84869158742     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.12.134     Document Type: Review

References (138)

1. Weigelt B, Peterse JL, Van'T Veer LJ. Breast cancer metastasis: Markers and models. Nat. Rev. Cancer 5(8), 591-602 (2005). (Pubitemid 41081385)
2. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 8(2), 98-101 (1989).
3. Ewing J Neoplastic Diseases: A Textbook on Tumors (4th Edition). WB Saunders, PA, USA (1928).
4. Sugarbaker EV. Cancer metastasis: A product of tumor-host interactions. Curr. Probl. Cancer 3(7), 1-59 (1979).
5. Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet. 25(1), 30-38 (2009).
6. Hu M, Polyak K. Molecular characterisation of the tumour microenvironment in breast cancer. Eur. J. Cancer 44(18), 2760-2765 (2008).
7. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int. J. Cancer 123(10), 2229-2238 (2008).
8. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat. Rev. Cancer 4(10), 806-813 (2004). (Pubitemid 39331152)
9. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2(3), 161-174 (2002). (Pubitemid 37328786)
10. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 6(5), 392-401 (2006).
11. Egeblad M, Nakasone ES, Werb Z. Tumors as organs: Complex tissues that interface with the entire organism. Dev. Cell 18(6), 884-901 (2010).
12. Levental KR, Yu H, Kass L et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5), 891-906 (2009).
13. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 4(1), 38 (2006).
14. Bergamaschi A, Tagliabue E, Sorlie T et al. Extracellular matrix signature identifies breast cancer subgroups with different clinical outcome. J. Pathol. 214(3), 357-367 (2008). (Pubitemid 351212391)
15. Casey T, Bond J, Tighe S et al. Molecular signatures suggest a major role for stromal cells in development of invasive breast cancer. Breast Cancer Res. Treat. 114(1), 47-62 (2009).
16. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res. 11(1), R7 (2009).
17. Kang Y, Siegel PM, Shu W et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3(6), 537-549 (2003). (Pubitemid 36808649)
18. Minn AJ, Gupta GP, Siegel PM et al. Genes that mediate breast cancer metastasis to lung. Nature 436(7050), 518-524 (2005). (Pubitemid 41112921)
19. Finak G, Bertos N, Pepin F et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 14(5), 518-527 (2008). (Pubitemid 351655218)
20. Brouty-Boye D. Developmental biology of fibroblasts and neoplastic disease. Prog. Mol. Subcell Biol. 40, 55-77 (2005).
21. Rasanen K, Vaheri A. Activation of fibroblasts in cancer stroma. Exp. Cell. Res. 316(17), 2713-2722 (2010).
22. Desmouliere A, Guyot C, Gabbiani G. The stroma reaction myofibroblast: A key player in the control of tumor cell behavior. Int. J. Dev. Biol. 48(5-6), 509-517 (2004).
23. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 170(6), 1807-1816 (2007). (Pubitemid 47339255)
24. Mcanulty RJ. Fibroblasts and myofibroblasts: Their source, function and role in disease. Int. J. Biochem. Cell. Biol. 39(4), 666-671 (2007).
25. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth - bystanders turning into key players. Curr. Opin. Genet. Dev. 19(1), 67-73 (2009).
26. Tsujino T, Seshimo I, Yamamoto H et al. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin. Cancer Res. 13(7), 2082-2090 (2007). (Pubitemid 46649876)
27. Allinen M, Beroukhim R, Cai L et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6(1), 17-32 (2004). (Pubitemid 38903159)
28. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 454(7203), 436-444 (2008).
29. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW. The macrophage growth factor CSF-1 in mammary gland development and tumor progression. J. Mammary Gland Biol. Neoplasia 7(2), 147-162 (2002). (Pubitemid 38420772)
30. Mantovani A, Allavena P, Sozzani S, Vecchi A, Locati M, Sica A. Chemokines in the recruitment and shaping of the leukocyte infiltrate of tumors. Semin. Cancer Biol. 14(3), 155-160 (2004). (Pubitemid 38586740)
31. Andreu P, Johansson M, Affara NI et al. FcRg activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17(2), 121-134 (2010).
32. Dannenberg AJ, Subbaramaiah K. Targeting cyclooxygenase-2 in human neoplasia: Rationale and promise. Cancer Cell 4(6), 431-436 (2003). (Pubitemid 38050040)
33. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3(6), 401-410 (2003). (Pubitemid 37328844)
34. Lyden D, Hattori K, Dias S et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7(11), 1194-1201 (2001). (Pubitemid 33063774)
35. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 8(8), 618-631 (2008).
36. Rajala MW, Scherer PE. Minireview: The adipocyte - at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144(9), 3765-3773 (2003). (Pubitemid 37088727)
37. Trujillo ME, Scherer PE. Adipose tissue-derived factors: Impact on health and disease. Endocr. Rev. 27(7), 762-778 (2006). (Pubitemid 44936059)
38. Calle EE, Kaaks R. Overweight, obesity and cancer: Epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4(8), 579-591 (2004). (Pubitemid 39025053)
39. Majed B, Moreau T, Senouci K, Salmon RJ, Fourquet A, Asselain B. Is obesity an independent prognosis factor in woman breast cancer? Breast Cancer Res. Treat. 111(2), 329-342 (2008).
40. Dirat B, Bochet L, Escourrou G, Valet P, Muller C. Unraveling the obesity and breast cancer links: A role for cancer-associated adipocytes? Endocr. Dev. 19, 45-52 (2010).
41. Carmichael AR. Obesity and prognosis of breast cancer. Obesity Rev. 7(4), 333-340 (2006). (Pubitemid 44564304)
42. Dirat B, Bochet L, Dabek M et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 71(7), 2455-2465 (2011).
43. Motrescu ER, Rio MC. Cancer cells, adipocytes and matrix metalloproteinase 11: A vicious tumor progression cycle. Biol. Chem. 389(8), 1037-1041 (2008).
44. Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int. J. Oncol. 40(1), 130-138 (2012).
45. Langley RR, Fidler IJ. Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr. Rev. 28(3), 297-321 (2007). (Pubitemid 46984829)
46. Micke P, Ostman A. Tumour-stroma interaction: Cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung Cancer 45(Suppl. 2), S163-S175 (2004). (Pubitemid 39488186)
47. Orimo A, Weinberg RA. Stromal fibroblasts in cancer: A novel tumor-promoting cell type. Cell Cycle 5(15), 1597-1601 (2006). (Pubitemid 44285243)
48. Gaggioli C, Hooper S, Hidalgo-Carcedo C et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell. Biol. 9(12), 1392-1400 (2007). (Pubitemid 350201752)
49. Chiquet M, Gelman L, Lutz R, Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim. Biophys. Acta 1793(5), 911-920 (2009).
50. Kumar S, Weaver VM. Mechanics, malignancy, and metastasis: The force journey of a tumor cell. Cancer Metastasis Rev. 28(1-2), 113-127 (2009).
51. Tschumperlin DJ, Dai G, Maly IV et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429(6987), 83-86 (2004). (Pubitemid 38620555)
52. De Wever O, Nguyen QD, Van Hoorde L et al. Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J. 18(9), 1016-1018 (2004). (Pubitemid 39561510)
53. Olsen CJ, Moreira J, Lukanidin EM, Ambartsumian NS. Human mammary fibroblasts stimulate invasion of breast cancer cells in a three-dimensional culture and increase stroma development in mouse xenografts. BMC Cancer 10, 444 (2010).
54. Shimoda M, Mellody KT, Orimo A. Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Semin. Cell Dev. Biol. 21(1), 19-25 (2010).
55. Ioachim E, Michael M, Stavropoulos NE, Kitsiou E, Salmas M, Malamou-Mitsi V. A clinicopathological study of the expression of extracellular matrix components in urothelial carcinoma. BJU Int. 95(4), 655-659 (2005). (Pubitemid 40311492)
56. Ioachim E, Charchanti A, Briasoulis E et al. Immunohistochemical expression of extracellular matrix components tenascin, fibronectin, collagen type IV and laminin in breast cancer: Their prognostic value and role in tumour invasion and progression. Eur. J. Cancer 38(18), 2362-2370 (2002). (Pubitemid 35387487)
57. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, b-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 28(1-2), 151-166 (2009).
58. Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell. Biol. 139(7), 1861-1872 (1997). (Pubitemid 28079248)
59. Vleminckx K, Vakaet L Jr, Mareel M, Fiers W, Van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66(1), 107-119 (1991). (Pubitemid 121001351)
60. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392(6672), 190-193 (1998). (Pubitemid 28162793)
61. Yoshida R, Kimura N, Harada Y, Ohuchi N. The loss of E-cadherin, a- and b-catenin expression is associated with metastasis and poor prognosis in invasive breast cancer. Int. J. Oncol. 18(3), 513-520 (2001).
62. Borley AC, Hiscox S, Gee J et al. Anti-oestrogens but not oestrogen deprivation promote cellular invasion in intercellular adhesion-deficient breast cancer cells. Breast Cancer Res. 10(6), R103 (2008).
63. Hiscox S, Rakha E, Smith C et al. Loss of E-cadherin expression in clinical breast cancer is associated with an adverse outcome on tamoxifen. Cancer Res. 71(24), Supplement 3 (2011).
64. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5(10), 816-826 (2004). (Pubitemid 39336275)
65. Aplin AE, Howe AK, Juliano RL. Cell adhesion molecules, signal transduction and cell growth. Curr. Opin. Cell Biol. 11(6), 737-744 (1999).
66. Erler JT, Weaver VM. Three-dimensional context regulation of metastasis. Clin. Exp. Metastasis 26(1), 35-49 (2009).
67. Gimond C, Van Der Flier A, Van Delft S et al. Induction of cell scattering by expression of b1 integrins in b1-deficient epithelial cells requires activation of members of the r family of GTPases and downregulation of cadherin and catenin function. J. Cell Biol. 147(6), 1325-1340 (1999). (Pubitemid 30012816)
68. De Jong JS, Van Diest PJ, Van Der Valk P, Baak JP. Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. II: Correlations with proliferation and angiogenesis. J. Pathol. 184(1), 53-57 (1998). (Pubitemid 28086153)
69. Stupp R, Ruegg C. Integrin inhibitors reaching the clinic. J. Clin. Oncol. 25(13), 1637-1638 (2007). (Pubitemid 46797938)
70. Hariharan S, Gustafson D, Holden S et al. Assessment of the biological and pharmacological effects of the an b3 and an b5 integrin receptor antagonist, cilengitide (EMD 121974), in patients with advanced solid tumors. Ann. Oncol. 18(8), 1400-1407 (2007). (Pubitemid 47305015)
71. Cabodi S, Di Stefano P, Leal Mdel P et al. Integrins and signal transduction. Adv. Exp. Med. Biol. 674, 43-54 (2010).
72. Ilic D, Furuta Y, Kanazawa S et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377(6549), 539-544 (1995).
73. Gabarra-Niecko V, Schaller MD, Dunty JM. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 22(4), 359-374 (2003). (Pubitemid 36791892)
74. Parsons JT, Slack-Davis J, Tilghman R, Roberts WG. Focal adhesion kinase: Targeting adhesion signaling pathways for therapeutic intervention. Clin. Cancer Res. 14(3), 627-632 (2008). (Pubitemid 351231140)
75. Kim TH, Kim HI, Soung YH, Shaw LA, Chung J. Integrin (a6b4) signals through Src to increase expression of S100A4, a metastasis-promoting factor: Implications for cancer cell invasion. Mol. Cancer Res. 7(10), 1605-1612 (2009).
76. Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 22(4), 337-358 (2003). (Pubitemid 36791891)
77. Hiscox S, Jordan NJ, Morgan L, Green TP, Nicholson RI. Src kinase promotes adhesion-independent activation of FAK and enhances cellular migration in tamoxifen-resistant breast cancer cells. Clin. Exp. Metastasis 24(3), 157-167 (2007). (Pubitemid 46850227)
78. Schweppe RE, Kerege AA, French JD, Sharma V, Grzywa RL, Haugen BR. Inhibition of Src with AZD0530 reveals the Src-Focal Adhesion kinase complex as a novel therapeutic target in papillary and anaplastic thyroid cancer. J. Clin. Endocrinol. Metab. 94(6), 2199-2203 (2009).
79. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res. Treat. 97(3), 263-274 (2006). (Pubitemid 43945756)
80. Hadler-Olsen E, Fadnes B, Sylte I, Uhlin- Hansen L, Winberg JO. Regulation of matrix metalloproteinase activity in health and disease. FEBS J. 278(1), 28-45 (2011).
81. Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278(1), 16-27 (2011).
82. Coussens LM, Werb Z. Matrix metalloproteinases and the development of cancer. Chem. Biol. 3(11), 895-904 (1996). (Pubitemid 27017088)
83. Basset P, Bellocq JP, Wolf C et al. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348(6303), 699-704 (1990). (Pubitemid 120015135)
84. Zhao YG, Xiao AZ, Park HI et al. Endometase/matrilysin-2 in human breast ductal carcinoma in situ and its inhibition by tissue inhibitors of metalloproteinases-2 and -4: A putative role in the initiation of breast cancer invasion. Cancer Res. 64(2), 590-598 (2004). (Pubitemid 38120898)
85. Lebeau A, Nerlich AG, Sauer U, Lichtinghagen R, Lohrs U. Tissue distribution of major matrix metalloproteinases and their transcripts in human breast carcinomas. Anticancer Res. 19(5B), 4257-4264 (1999).
86. Wiechmann L, Kuerer HM. The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 112(10), 2130-2142 (2008). (Pubitemid 351628621)
87. Cichon MA, Degnim AC, Visscher DW, Radisky DC. Microenvironmental influences that drive progression from benign breast disease to invasive breast cancer. J. Mammary Gland. Biol. Neoplasia 15(4), 389-397 (2010).
88. Schuetz CS, Bonin M, Clare SE et al. Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis. Cancer Res. 66(10), 5278-5286 (2006). (Pubitemid 43844952)
89. Borrello MG, Alberti L, Fischer A et al. Induction of a proinflammatory program in normal human thyrocytes by the RET/PTC1 oncogene. Proc. Natl Acad. Sci. USA 102(41), 14825-14830 (2005). (Pubitemid 41457140)
90. Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat. Med. 13(10), 1211-1218 (2007). (Pubitemid 47530639)
91. Sparmann A, Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 6(5), 447-458 (2004). (Pubitemid 39469981)
92. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30(7), 1073-1081 (2009).
93. Harmey JH, Dimitriadis E, Kay E, Redmond HP, Bouchier-Hayes D. Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor b-1. Ann. Surg. Oncol. 5(3), 271-278 (1998). (Pubitemid 28249320)
94. Doedens AL, Stockmann C, Rubinstein MP et al. Macrophage expression of hypoxia-inducible factor-1 a suppresses T-cell function and promotes tumor progression. Cancer Res. 70(19), 7465-7475 (2010).
95. Pollard JW. Macrophages define the invasive microenvironment in breast cancer. J. Leukoc. Biol. 84(3), 623-630 (2008).
96. Coussens LM, Werb Z. Inflammation and cancer. Nature 420(6917), 860-867 (2002). (Pubitemid 36019639)
97. Leek RD, Talks KL, Pezzella F et al. Relation of hypoxia-inducible factor-2 a (HIF-2 a) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res. 62(5), 1326-1329 (2002). (Pubitemid 34407787)
98. Luo Y, Zhou H, Krueger J et al. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J. Clin. Invest. 116(8), 2132-2141 (2006). (Pubitemid 44162322)
99. Byzova TV, Goldman CK, Pampori N et al. A mechanism for modulation of cellular responses to VEGF: Activation of the integrins. Mol. Cell 6(4), 851-860 (2000).
100. Klein S, Bikfalvi A, Birkenmeier TM, Giancotti FG, Rifkin DB. Integrin regulation by endogenous expression of 18-kDa fibroblast growth factor-2. J. Biol. Chem. 271(37), 22583-22590 (1996). (Pubitemid 26304698)
101. Fernandez-Sauze S, Grall D, Cseh B, Van Obberghen-Schilling E. Regulation of fibronectin matrix assembly and capillary morphogenesis in endothelial cells by Rho family GTPases. Exp. Cell Res. 315(12), 2092-2104 (2009).
102. Jin H, Aiyer A, Su J et al. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature. J. Clin. Invest. 116(3), 652-662 (2006). (Pubitemid 43326874)
103. Stacker SA, Caesar C, Baldwin ME et al. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat. Med. 7(2), 186-191 (2001). (Pubitemid 32148485)
104. Van Zijl F, Mair M, Csiszar A et al. Hepatic tumor-stroma crosstalk guides epithelial to mesenchymal transition at the tumor edge. Oncogene 28(45), 4022-4033 (2009).
105. Orimo A, Gupta PB, Sgroi DC et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121(3), 335-348 (2005). (Pubitemid 40692295)
106. Ao M, Williams K, Bhowmick NA, Hayward SW. Transforming growth factor-b promotes invasion in tumorigenic but not in nontumorigenic human prostatic epithelial cells. Cancer Res. 66(16), 8007-8016 (2006). (Pubitemid 44299165)
107. Bhowmick NA, Chytil A, Plieth D et al. TGF-b signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303(5659), 848-851 (2004). (Pubitemid 38174665)
108. Niu YN, Xia SJ. Stroma-epithelium crosstalk in prostate cancer. Asian J. Androl. 11(1), 28-35 (2009).
109. Hernandez L, Smirnova T, Kedrin D et al. The EGF/CSF-1 paracrine invasion loop can be triggered by heregulin b1 and CXCL12. Cancer Res. 69(7), 3221-3227 (2009).
110. Potter SM, Dwyer RM, Hartmann MC et al. Influence of stromal-epithelial interactions on breast cancer in vitro and in vivo . Breast Cancer Res. Treat. 131(2), 401-411 (2012).
111. Paulsson J, Sjoblom T, Micke P et al. Prognostic significance of stromal platelet-derived growth factor b-receptor expression in human breast cancer. Am. J. Pathol. 175(1), 334-341 (2009).
112. Witkiewicz AK, Dasgupta A, Sotgia F et al. An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers. Am. J. Pathol. 174(6), 2023-2034 (2009).
113. Sotgia F, Martinez-Outschoorn UE, Howell A, Pestell RG, Pavlides S, Lisanti MP. Caveolin-1 and cancer metabolism in the tumor microenvironment: Markers, models, and mechanisms. Annu. Rev. Pathol. 7, 423-467 (2012).
114. Auvinen P, Tammi R, Parkkinen J et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am. J. Pathol. 156(2), 529-536 (2000). (Pubitemid 30643808)
115. Kim MY, Oskarsson T, Acharyya S et al. Tumor self-seeding by circulating cancer cells. Cell 139(7), 1315-1326 (2009).
116. Nguyen DX, Bos PD, Massague J. Metastasis: From dissemination to organ-specific colonization. Nat. Rev. Cancer 9(4), 274-284 (2009).
117. Kaplan RN, Riba RD, Zacharoulis S et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438(7069), 820-827 (2005). (Pubitemid 41753060)
118. Hiratsuka S, Nakamura K, Iwai S et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2(4), 289-300 (2002). (Pubitemid 41043963)
119. Erler JT, Bennewith KL, Cox TR et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15(1), 35-44 (2009).
120. Kim S, Takahashi H, Lin WW et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457(7225), 102-106 (2009).
121. Meltzer A. Dormancy and breast cancer. J. Surg. Oncol. 43(3), 181-188 (1990). (Pubitemid 20096307)
122. Black WC, Welch HG. Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N. Engl. J. Med. 328(17), 1237-1243 (1993). (Pubitemid 23115703)
123. Folkman J, Kalluri R. Cancer without disease. Nature 427(6977), 787 (2004). (Pubitemid 38297724)
124. Allan AL, Vantyghem SA, Tuck AB, Chambers AF. Tumor dormancy and cancer stem cells: Implications for the biology and treatment of breast cancer metastasis. Breast Dis. 26, 87-98 (2006). (Pubitemid 46655481)
125. Naumov GN, Macdonald IC, Weinmeister PM et al. Persistence of solitary mammary carcinoma cells in a secondary site: A possible contributor to dormancy. Cancer Res. 62(7), 2162-2168 (2002). (Pubitemid 34408466)
126. Naumov GN, Townson JL, Macdonald IC et al. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast Cancer Res. Treat. 82(3), 199-206 (2003). (Pubitemid 37521976)
127. Marsden CG, Wright MJ, Pochampally R, Rowan BG. Breast tumor-initiating cells isolated from patient core biopsies for study of hormone action. Methods Mol. Biol. (Clifton, N. J.) 590, 363-375 (2009).
128. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 3(12), 895-902 (2003). (Pubitemid 37500174)
129. Millerot-Serrurot E, Guilbert M, Fourre N et al. 3D collagen type I matrix inhibits the antimigratory effect of doxorubicin. Cancer Cell Int. 10, 26 (2010).
130. Sethi T, Rintoul RC, Moore SM et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: A mechanism for small cell lung cancer growth and drug resistance in vivo. Nat. Med. 5(6), 662-668 (1999). (Pubitemid 29289430)
131. Fridman R, Giaccone G, Kanemoto T, Martin GR, Gazdar AF, Mulshine JL. Reconstituted basement membrane (matrigel) and laminin can enhance the tumorigenicity and the drug resistance of small cell lung cancer cell lines. Proc. Natl Acad. Sci. USA 87(17), 6698-6702 (1990).
132. Berube M, Talbot M, Collin C et al. Role of the extracellular matrix proteins in the resistance of SP6.5 uveal melanoma cells toward cisplatin. Int. J. Oncol. 26(2), 405-413 (2005).
133. Hiscox S, Barrett-Lee P, Nicholson RI. Therapeutic targeting of tumor-stroma interactions. Expert Opin. Ther. Targets 15(5), 609-621 (2011).
134. Stupp R, Hegi ME, Neyns B et al. Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma. J. Clin. Oncol. 28(16), 2712-2718 (2010).
135. Nam JM, Chung Y, Hsu HC, Park CC. b1 integrin targeting to enhance radiation therapy. Int. J. Radiat. Biol. 85(11), 923-928 (2009).
136. Kim TJ, Landen CN, Lin YG et al. Combined anti-angiogenic therapy against VEGF and integrin aVb3 in an orthotopic model of ovarian cancer. Cancer Biol. Ther. 8(23), 2263-2272 (2009).
137. Hehlgans S, Lange I, Eke I, Cordes N. 3D cell cultures of human head and neck squamous cell carcinoma cells are radiosensitized by the focal adhesion kinase inhibitor TAE226. Radiother. Oncol. 92(3), 371-378 (2009).
138. Loeffler M, Kruger JA, Niethammer AG, Reisfeld RA. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J. Clin. Invest. 116(7), 1955-1962 (2006). (Pubitemid 44033319)