Dynamic interplay between the collagen scaffold and tumor evolution

Current Opinion in Cell Biology

Volumn 22, Issue 5, 2010, Pages 697-706

  Egeblad, Mikala ^a   Rasch, Morten G ^a,b   Weaver, Valerie M ^c  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b FINSEN LABORATORY   (Denmark)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBROMODULIN; INTEGRIN; MATRIX METALLOPROTEINASE; PROTEIN LYSINE 6 OXIDASE; SCAFFOLD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

BASEMENT MEMBRANE; BIOCHEMISTRY; BRANCHING MORPHOGENESIS; BREAST CANCER; CANCER CELL; CANCER INVASION; CANCER RESISTANCE; CARCINOGENESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL INFILTRATION; CELL PROLIFERATION; CELL STRUCTURE; COLLAGEN METABOLISM; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; FIBROSIS; IMMUNOCOMPETENT CELL; LEUKOCYTE; METASTASIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; TISSUE PRESSURE; TREATMENT RESPONSE;

CELL MOVEMENT; COLLAGEN; HUMANS; NEOPLASMS; TISSUE SCAFFOLDS;

EID: 77957221459     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.08.015     Document Type: Review

References (107)

1. Egeblad M., Nakasone E., Werb Z. The tumor as an organ: complex tissues that interface with the entire organism. Dev Cell 2010, 18:884.
2. Ewald A.J., Brenot A., Duong M., Chan B.S., Werb Z. Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 2008, 14:570-581.
3. Wiseman B.S., Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002, 296:1046-1049.
4. Myllyharju J., Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 2004, 20:33-43.
5. Boot-Handford R.P., Tuckwell D.S. Fibrillar collagen: the key to vertebrate evolution? A tale of molecular incest. Bioessays 2003, 25:142-151.
6. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 2003, 3:422-433.
7. Rowe R.G., Weiss S.J. Breaching the basement membrane: who, when and how?. Trends Cell Biol 2008, 18:560-574.
8. Lopez-Novoa J.M., Nieto M.A. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009, 1:303-314.
9. Margadant C., Sonnenberg A. Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep 2010, 11:97-105.
10. Huijbers I.J., Iravani M., Popov S., Robertson D., Al-Sarraj S., Jones C., Isacke C.M. A role for fibrillar collagen deposition and the collagen internalization receptor endo180 in glioma invasion. PLoS One 2010, 5:e9808.
11. Zhu G.G., Risteli L., Makinen M., Risteli J., Kauppila A., Stenback F. Immunohistochemical study of type I collagen and type I pN-collagen in benign and malignant ovarian neoplasms. Cancer 1995, 75:1010-1017.
12. Kauppila S., Stenback F., Risteli J., Jukkola A., Risteli L. Aberrant type I and type III collagen gene expression in human breast cancer in vivo. J Pathol 1998, 186:262-268.
13. Hasebe T., Sasaki S., Imoto S., Mukai K., Yokose T., Ochiai A. Prognostic significance of fibrotic focus in invasive ductal carcinoma of the breast: a prospective observational study. Mod Pathol 2002, 15:502-516.
14. Erler J.T., Weaver V.M. Three-dimensional context regulation of metastasis. Clin Exp Metastasis 2009, 26:35-49.
15. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
16. Tavazoie S.F., Alarcon C., Oskarsson T., Padua D., Wang Q., Bos P.D., Gerald W.L., Massague J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152.
17. Ramaswamy S., Ross K.N., Lander E.S., Golub T.R. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003, 33:49-54.
18. Provenzano P.P., Eliceiri K.W., Campbell J.M., Inman D.R., White J.G., Keely P.J. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 2006, 4:38.
19. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
20. Paszek M.J., Weaver V.M. The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 2004, 9:325-342.
21. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
22. Wozniak M.A., Desai R., Solski P.A., Der C.J., Keely P.J. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 2003, 163:583-595.
23. Chun T.H., Hotary K.B., Sabeh F., Saltiel A.R., Allen E.D., Weiss S.J. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 2006, 125:577-591.
24. Peyrol S., Raccurt M., Gerard F., Gleyzal C., Grimaud J.A., Sommer P. Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am J Pathol 1997, 150:497-507.
25. Santhanam A.N., Baker A.R., Hegamyer G., Kirschmann D.A., Colburn N.H. Pdcd4 repression of lysyl oxidase inhibits hypoxia-induced breast cancer cell invasion. Oncogene 2010, 29:3921-3932.
26. Erler J.T., Bennewith K.L., Cox T.R., Lang G., Bird D., Koong A., Le Q.T., Giaccia A.J. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009, 15:35-44.
27. Erler J.T., Bennewith K.L., Nicolau M., Dornhofer N., Kong C., Le Q.T., Chi J.T., Jeffrey S.S., Giaccia A.J. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440:1222-1226.
28. Akiri G., Sabo E., Dafni H., Vadasz Z., Kartvelishvily Y., Gan N., Kessler O., Cohen T., Resnick M., Neeman M., et al. Lysyl oxidase-related protein-1 promotes tumor fibrosis and tumor progression in vivo. Cancer Res 2003, 63:1657-1666.
29. Velling T., Risteli J., Wennerberg K., Mosher D.F., Johansson S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem 2002, 277:37377-37381.
30. Klotzsch E., Smith M.L., Kubow K.E., Muntwyler S., Little W.C., Beyeler F., Gourdon D., Nelson B.J., Vogel V. Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc Natl Acad Sci U S A 2009, 106:18267-18272.
31. Friedland J.C., Lee M.H., Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science 2009, 323:642-644.
32. Arnold S.A., Rivera L.B., Miller A.F., Carbon J.G., Dineen S.P., Xie Y., Castrillon D.H., Sage E.H., Puolakkainen P., Bradshaw A.D., et al. Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinoma. Dis Model Mech 2010, 3:57-72.
33. Furber J.D. Extracellular glycation crosslinks: prospects for removal. Rejuvenation Res 2006, 9:274-278.
34. Wolff S.P., Jiang Z.Y., Hunt J.V. Protein glycation and oxidative stress in diabetes mellitus and ageing. Free Radic Biol Med 1991, 10:339-352.
35. Coughlin S.S., Calle E.E., Teras L.R., Petrelli J., Thun M.J. Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 2004, 159:1160-1167.
36. Condeelis J., Segall J.E. Intravital imaging of cell movement in tumours. Nat Rev Cancer 2003, 3:921-930.
37. Zaman M.H., Trapani L.M., Sieminski A.L., Mackellar D., Gong H., Kamm R.D., Wells A., Lauffenburger D.A., Matsudaira P. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U S A 2006, 103:10889-10894.
38. Wyckoff J.B., Wang Y., Lin E.Y., Li J.F., Goswami S., Stanley E.R., Segall J.E., Pollard J.W., Condeelis J. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 2007, 67:2649-2656.
39. Wang W., Wyckoff J.B., Frohlich V.C., Oleynikov Y., Huttelmaier S., Zavadil J., Cermak L., Bottinger E.P., Singer R.H., White J.G., et al. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 2002, 62:6278-6288.
40. Giese A., Kluwe L., Laube B., Meissner H., Berens M.E., Westphal M. Migration of human glioma cells on myelin. Neurosurgery 1996, 38:755-764.
41. Desgrosellier J.S., Cheresh D.A. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010, 10:9-22.
42. Vogel W.F., Aszodi A., Alves F., Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol 2001, 21:2906-2917.
43. Makareeva E., Han S., Vera J.C., Sackett D.L., Holmbeck K., Phillips C.L., Visse R., Nagase H., Leikin S Carcinomas, contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion. Cancer Res 2010, 70:4366-4374.
44. Liotta L.A. Tumor invasion and metastases-role of the extracellular matrix: Rhoads Memorial Award lecture. Cancer Res 1986, 46:1-7.
45. Sabeh F., Shimizu-Hirota R., Weiss S.J. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 2009, 185:11-19.
46. Curino A.C., Engelholm L.H., Yamada S.S., Holmbeck K., Lund L.R., Molinolo A.A., Behrendt N., Nielsen B.S., Bugge T.H. Intracellular collagen degradation mediated by uPARAP/Endo180 is a major pathway of extracellular matrix turnover during malignancy. J Cell Biol 2005, 169:977-985.
47. Lu C., Li X.Y., Hu Y., Rowe R.G., Weiss S.J. MT1-MMP controls human mesenchymal stem cell trafficking and differentiation. Blood 2010, 115:221-229.
48. Pilcher B.K., Dumin J.A., Sudbeck B.D., Krane S.M., Welgus H.G., Parks W.C. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 1997, 137:1445-1457.
49. Wolf K., Alexander S., Schacht V., Coussens L.M., von Andrian U.H., van Rheenen J., Deryugina E., Friedl P. Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 2009, 20:931-941.
50. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol 2010, 188:11-19.
51. Friedl P., Wolf K. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res 2008, 68:7247-7249.
52. Wolf K., Wu Y.I., Liu Y., Geiger J., Tam E., Overall C., Stack M.S., Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007, 9:893-904.
53. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., et al. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 2004, 167:769-781.
54. Davis G.E. Affinity of integrins for damaged extracellular matrix: alpha v beta 3 binds to denatured collagen type I through RGD sites. Biochem Biophys Res Commun 1992, 182:1025-1031.
55. Xu J., Rodriguez D., Petitclerc E., Kim J.J., Hangai M., Moon Y.S., Davis G.E., Brooks P.C. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J Cell Biol 2001, 154:1069-1079.
56. Ohuchi E., Imai K., Fujii Y., Sato H., Seiki M., Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 1997, 272:2446-2451.
57. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002, 2:161-174.
58. Messent A.J., Tuckwell D.S., Knauper V., Humphries M.J., Murphy G., Gavrilovic J. Effects of collagenase-cleavage of type I collagen on alpha2beta1 integrin-mediated cell adhesion. J Cell Sci 1998, 111(Pt 8):1127-1135.
59. Stringa E., Knauper V., Murphy G., Gavrilovic J. Collagen degradation and platelet-derived growth factor stimulate the migration of vascular smooth muscle cells. J Cell Sci 2000, 113(Pt 11):2055-2064.
60. Montgomery A.M., Reisfeld R.A., Cheresh D.A. Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen. Proc Natl Acad Sci U S A 1994, 91:8856-8860.
61. Fera E., O'Neil C., Lee W., Li S., Pickering J.G. Fibroblast growth factor-2 and remodeled type I collagen control membrane protrusion in human vascular smooth muscle cells: biphasic activation of Rac1. J Biol Chem 2004, 279:35573-35582.
62. Petitclerc E., Stromblad S., von Schalscha T.L., Mitjans F., Piulats J., Montgomery A.M., Cheresh D.A., Brooks P.C. Integrin alpha(v)beta3 promotes M21 melanoma growth in human skin by regulating tumor cell survival. Cancer Res 1999, 59:2724-2730.
63. Wall S.J., Werner E., Werb Z., DeClerck Y.A. Discoidin domain receptor 2 mediates tumor cell cycle arrest induced by fibrillar collagen. J Biol Chem 2005, 280:40187-40194.
64. Konitsiotis A.D., Raynal N., Bihan D., Hohenester E., Farndale R.W., Leitinger B. Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J Biol Chem 2008, 283:6861-6868.
65. Wu H., Byrne M.H., Stacey A., Goldring M.B., Birkhead J.R., Jaenisch R., Krane S.M. Generation of collagenase-resistant collagen by site-directed mutagenesis of murine pro alpha 1(I) collagen gene. Proc Natl Acad Sci U S A 1990, 87:5888-5892.
66. Seandel M., Noack-Kunnmann K., Zhu D., Aimes R.T., Quigley J.P. Growth factor-induced angiogenesis in vivo requires specific cleavage of fibrillar type I collagen. Blood 2001, 97:2323-2332.
67. Chun T.H., Sabeh F., Ota I., Murphy H., McDonagh K.T., Holmbeck K., Birkedal-Hansen H., Allen E.D., Weiss S.J. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J Cell Biol 2004, 167:757-767.
68. Hamano Y., Zeisberg M., Sugimoto H., Lively J.C., Maeshima Y., Yang C., Hynes R.O., Werb Z., Sudhakar A., Kalluri R. 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 2003, 3:589-601.
69. Cooke V.G., Kalluri R. Chapter 1. Molecular mechanism of type IV collagen-derived endogenous inhibitors of angiogenesis. Methods Enzymol 2008, 444:1-19.
70. Armstrong T., Packham G., Murphy L.B., Bateman A.C., Conti J.A., Fine D.R., Johnson C.D., Benyon R.C., Iredale J.P. Type I collagen promotes the malignant phenotype of pancreatic ductal adenocarcinoma. Clin Cancer Res 2004, 10:7427-7437.
71. Sethi T., Rintoul R.C., Moore S.M., MacKinnon A.C., Salter D., Choo C., Chilvers E.R., Dransfield I., Donnelly S.C., Strieter R., 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 1999, 5:662-668.
72. Heldin C.H., Rubin K., Pietras K., Ostman A. High interstitial fluid pressure-an obstacle in cancer therapy. Nat Rev Cancer 2004, 4:806-813.
73. Svensson L., Aszodi A., Reinholt F.P., Fassler R., Heinegard D., Oldberg A. Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem 1999, 274:9636-9647.
74. Oldberg A., Kalamajski S., Salnikov A.V., Stuhr L., Morgelin M., Reed R.K., Heldin N.E., Rubin K. Collagen-binding proteoglycan fibromodulin can determine stroma matrix structure and fluid balance in experimental carcinoma. Proc Natl Acad Sci U S A 2007, 104:13966-13971.
75. Gade T.P., Buchanan I.M., Motley M.W., Mazaheri Y., Spees W.M., Koutcher J.A. Imaging intratumoral convection: pressure-dependent enhancement in chemotherapeutic delivery to solid tumors. Clin Cancer Res 2009, 15:247-255.
76. McKee T.D., Grandi P., Mok W., Alexandrakis G., Insin N., Zimmer J.P., Bawendi M.G., Boucher Y., Breakefield X.O., Jain R.K. Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 2006, 66:2509-2513.
77. Netti P.A., Berk D.A., Swartz M.A., Grodzinsky A.J., Jain R.K. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000, 60:2497-2503.
78. Brown E., McKee T., diTomaso E., Pluen A., Seed B., Boucher Y., Jain R.K. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 2003, 9:796-800.
79. Minchinton A.I., Tannock I.F. Drug penetration in solid tumours. Nat Rev Cancer 2006, 6:583-592.
80. Loeffler M., Kruger J.A., Niethammer A.G., Reisfeld R.A. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006, 116:1955-1962.
81. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., Madhu B., Goldgraben M.A., Caldwell M.E., Allard D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324:1457-1461.
82. Egeblad M., Ewald A.J., Askautrud H.A., Truitt M.L., Welm B.E., Bainbridge E., Peeters G., Krummel M.F., Werb Z. Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis Model Mech 2008, 1:155-167.
83. Meyaard L. The inhibitory collagen receptor LAIR-1 (CD305). J Leukoc Biol 2008, 83:799-803.
84. Franco C., Britto K., Wong E., Hou G., Zhu S.N., Chen M., Cybulsky M.I., Bendeck M.P. Discoidin domain receptor 1 on bone marrow-derived cells promotes macrophage accumulation during atherogenesis. Circ Res 2009, 105:1141-1148.
85. Postlethwaite A.E., Kang A.H. Collagen- and collagen peptide-induced chemotaxis of human blood monocytes. J Exp Med 1976, 143:1299-1307.
86. Weathington N.M., van Houwelingen A.H., Noerager B.D., Jackson P.L., Kraneveld A.D., Galin F.S., Folkerts G., Nijkamp F.P., Blalock J.E. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 2006, 12:317-323.
87. Kaplan G. 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 1983, 157:2061-2072.
88. Gouon-Evans V., Rothenberg M.E., Pollard J.W. Postnatal mammary gland development requires macrophages and eosinophils. Development 2000, 127:2269-2282.
89. Ingman W.V., Wyckoff J., Gouon-Evans V., Condeelis J., Pollard J.W. Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev Dyn 2006, 235:3222-3229.
90. Atabai K., Jame S., Azhar N., Kuo A., Lam M., McKleroy W., Dehart G., Rahman S., Xia D.D., Melton A.C., et al. Mfge8 diminishes the severity of tissue fibrosis in mice by binding and targeting collagen for uptake by macrophages. J Clin Invest 2009, 119:3713-3722.
91. Leitinger B., Hohenester E. Mammalian collagen receptors. Matrix Biol 2007, 26:146-155.
92. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
93. Egeblad M., Shen H.C., Behonick D.J., Wilmes L., Eichten A., Korets L.V., Kheradmand F., Werb Z., Coussens L.M. Type I collagen is a genetic modifier of matrix metalloproteinase 2 in murine skeletal development. Dev Dyn 2007, 236:1683-1693.
94. Del Buono R., Pignatelli M., Hall P.A. Control of differentiation in a rectal adenocarcinoma cell line: the role of diffusable and cell-associated factors. J Pathol 1991, 164:59-66.
95. Iwasaki H., Suda T. Cancer stem cells and their niche. Cancer Sci 2009, 100:1166-1172.
96. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456:593-598.
97. Kirkland S.C. Type I collagen inhibits differentiation and promotes a stem cell-like phenotype in human colorectal carcinoma cells. Br J Cancer 2009, 101:320-326.
98. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., Lander E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
99. Asselin-Labat M.L., Sutherland K.D., Barker H., Thomas R., Shackleton M., Forrest N.C., Hartley L., Robb L., Grosveld F.G., van der Wees J., et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 2007, 9:201-209.
100. Vaillant F., Asselin-Labat M.L., Shackleton M., Forrest N.C., Lindeman G.J., Visvader J.E. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res 2008, 68:7711-7717.
101. Perentes J.Y., McKee T.D., Ley C.D., Mathiew H., Dawson M., Padera T.P., Munn L.L., Jain R.K., Boucher Y. In vivo imaging of extracellular matrix remodeling by tumor-associated fibroblasts. Nat Methods 2009, 6:143-145.
102. Bissell M.J., Hall H.G., Parry G. How does the extracellular matrix direct gene expression?. J Theor Biol 1982, 99:31-68.
103. Shoulders M.D., Raines R.T. Collagen structure and stability. Annu Rev Biochem 2009, 78:929-958.
104. Vanacore R., Ham A.J., Voehler M., Sanders C.R., Conrads T.P., Veenstra T.D., Sharpless K.B., Dawson P.E., Hudson B.G. A sulfilimine bond identified in collagen IV. Science 2009, 325:1230-1234.
105. Mundel T.M., Kalluri R. Type IV collagen-derived angiogenesis inhibitors. Microvasc Res 2007, 74:85-89.
106. Vogel W.F., Abdulhussein R., Ford C.E. Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 2006, 18:1108-1116.
107. Lebbink R.J., de Ruiter T., Adelmeijer J., Brenkman A.B., van Helvoort J.M., Koch M., Farndale R.W., Lisman T., Sonnenberg A., Lenting P.J., et al. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 2006, 203:1419-1425.