Bi-Directional signaling: Extracellular matrix and integrin regulation of breast tumor progression

Critical Reviews in Eukaryotic Gene Expression

Volumn 23, Issue 2, 2013, Pages 139-157

  Gehler, Scott ^a   Ponik, Suzanne M ^b,c,d   Riching, Kristin M ^b,d,g   Keely, Patricia J ^b,c,d,e,f,g  

^a AUGUSTANA COLLEGE   (United States)

^b Department of Cell and Regenerative Biology ^*  (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d Laboratory for Optical and Computational Instrumentation   (United States)

^e Molecular and Cellular Pharmacology Program   (United States)

^f Cell and Molecular Biology Program   (United States)

^g UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Bi directional signaling; Extracellular matrix; Fak; Integrins; Invasion; Matrix remodeling; Mechanosensor; Mechanotransduction; Morphogenesis; Rhoa; Tumor progression

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; COLLAGEN FIBER; COLLAGEN TYPE 3; COLLAGEN TYPE 5; CRK ASSOCIATED SUBSTRATE PROTEIN; CYCLIN D1; FILAMIN A; FOCAL ADHESION KINASE; INTEGRIN; MATRIX PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PHALLOIDIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SYNDECAN 1; SYNDECAN 4; TRANSCRIPTION FACTOR RUNX2; VINCULIN;

ACTIN FILAMENT; BRANCHING MORPHOGENESIS; BREAST CARCINOMA; BREAST CELL; BREAST TUMOR; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER RECURRENCE; CANCER RISK; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DEATH; CELL FUNCTION; CELL JUNCTION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL COMPOSITION; CONFORMATIONAL TRANSITION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; GENE EXPRESSION; HUMAN; LIGAND BINDING; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; REVIEW; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; TUMOR VOLUME;

ANIMALS; BREAST NEOPLASMS; CELL CYCLE; CELL MOVEMENT; COLLAGEN; DISEASE PROGRESSION; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; INTEGRINS; MATRIX METALLOPROTEINASES; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84875883780     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.2013006647     Document Type: Review

References (150)

1. Hynes RO. Integrins: Bidirectional, allosteric signaling machines. Cell. 2002 Sep 20;110(6):673-87.
2. van der Flier A, Sonnenberg A. Function and interactions of integrins. Cell Tissue Res. 2001 Sep;305(3):285-98.
3. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res. 2010 Jan;339(1):269-80. PubMed PMID: 19693543.
4. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619-47.
5. Geiger B, Yamada KM. Molecular architecture and function of matrix adhesions. Cold Spring Harbor Perspect Biol. 2011 May;3(5):a005033.
6. Zamir E, Geiger B. Components of cell-matrix adhesions. J Cell Sci. 2001 Oct;114(Pt 20):3577-9.
7. Giancotti FG, Ruoslahti E. Integrin signaling. Science. 1999 Aug 13;285(5430):1028-32.
8. Calderwood DA. Integrin activation. J Cell Sci. 2004 Feb 15;117(Pt 5):657-66.
9. Zamir E, Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci. 2001 Oct;114(Pt 20):3583-90.
10. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science. 2001 Nov 23;294(5547):1708-12.
11. Cukierman E, Pankov R, Yamada KM. Cell interactions with three-dimensional matrices. Curr Opin Cell Biol. 2002 Oct;14(5):633-9.
12. Miron-Mendoza M, Seemann J, Grinnell F. Collagen fibril flow and tissue translocation coupled to fibroblast migration in 3D collagen matrices. Mol Biol Cell. 2008 May;19(5):2051-8.
13. Fogerty FJ, Mosher DF. Mechanisms for organization of fibronectin matrix. Cell Differ Dev. 1990 Dec 2;32(3):439-50.
14. Mao Y, Schwarzbauer JE. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 2005 Sep;24(6):389-99.
15. Yurchenco PD. Basement membranes: Cell scaffoldings and signaling platforms. Cold Spring Harbor Perspect Biol. 2011 Feb;3(2): a004911.
16. Ricard-Blum S. The collagen family. Cold Spring Harbor Perspect Biol. 2011 Jan;3(1): a004978.
17. Moschos SJ, Drogowski LM, Reppert SL, Kirkwood JM. Integrins and cancer. Oncology. 2007 Aug;21(9 Suppl 3):13-20.
18. Plantefaber LC, Hynes RO. Changes in integrin receptors on oncogenically transformed cells. Cell. 1989 Jan 27;56(2):281-90.
19. Kyutoku M, Taniyama Y, Katsuragi N, Shimizu H, Kunugiza Y, Iekushi K, et al. Role of periostin in cancer progression and metastasis: Inhibition of breast cancer progression and metastasis by anti-periostin antibody in a murine model. Int J Mol Med. 2011 Aug;28(2):181-6.
20. Dai J, Li B, Shi J, Peng L, Zhang D, Qian W, et al. A humanized anti-osteopontin antibody inhibits breast cancer growth and metastasis in vivo. Cancer Immunol Immunother. 2010 Mar;59(3):355-66.
21. Hancox RA, Allen MD, Holliday DL, Edwards DR, Pennington CJ, Guttery DS, et al. Tumour-associated tenascin-C isoforms promote breast cancer cell invasion and growth by matrix metalloproteinase-dependent and independent mechanisms. Breast Cancer Res. 2009;11(2):R24.
22. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, Park CJ, et al. Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res. 2006 Feb 1;66(3):1526-35.
23. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol. 2003 Nov 10;163(3):583-95.
24. Paszek MJ, Weaver VM. The tension mounts: Mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia. 2004 Oct;9(4):325-42.
25. Guo YP, Martin LJ, Hanna W, Banerjee D, Miller N, Fishell E, et al. Growth factors and stromal matrix proteins associated with mammographic densities. Cancer Epidemiol, Biomarkers Prev. 2001 Mar;10(3):243-8.
26. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005 Nov 18;310(5751):1139-43.
27. Boyd NF, Dite GS, Stone J, Gunasekara A, English DR, McCredie MR, et al. Heritability of mammographic density, a risk factor for breast cancer. N Engl J Med. 2002 Sep 19;347(12):886-94.
28. Boyd NF, Martin LJ, Li Q, Sun L, Chiarelli AM, Hislop G, et al. Mammographic density as a surrogate marker for the effects of hormone therapy on risk of breast cancer. Cancer Epidemiol, Biomarkers Prev. 2006 May;15(5):961-6.
29. Yaghjyan L, Colditz GA, Rosner B, Tamimi RM. Mammographic breast density and breast cancer risk by menopausal status, postmenopausal hormone use and a family history of breast cancer. Cancer, Causes Control. 2012 May;23(5):785-90.
30. Schedin P, O'Brien J, Rudolph M, Stein T, Borges V. Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007 Mar;12(1):71-82.
31. Boyd NF, Lockwood GA, Martin LJ, Byng JW, Yaffe MJ, Tritchler DL. Mammographic density as a marker of susceptibility to breast cancer: A hypothesis. IARC Sci Publ. 2001;154:163-9.
32. Martin LJ, Boyd NF. Mammographic density. Potential mechanisms of breast cancer risk associated with mammographic density: Hypotheses based on epidemiological evidence. Breast Cancer Res. 2008;10(1):201.
33. Ursin G, Hovanessian-Larsen L, Parisky YR, Pike MC, Wu AH. Greatly increased occurrence of breast cancers in areas of mammographically dense tissue. Breast Cancer Res. 2005;7(5):R605 IARC Sci Publ 8.
34. Lopez JI, Kang I, You WK, McDonald DM, Weaver VM. In situ force mapping of mammary gland transformation. Integr Biol (Camb). 2011 Sep;3(9):910-21.
35. Provenzano PP, Eliceiri KW, Keely PJ. Shining new light on 3D cell motility and the metastatic process. Trends Cell Biol. 2009 Nov;19(11):638-48.
36. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005 Sep;8(3):241-54.
37. Walker RA. The complexities of breast cancer desmoplasia. Breast Cancer Res. 2001;3(3):143-5.
38. Jahkola T, Toivonen T, Nordling S, von Smitten K, Virtanen I. Expression of tenascin-C in intraductal carcinoma of human breast: Relationship to invasion. Eur J Cancer. 1998 Oct;34(11):1687-92.
39. Jahkola T, Toivonen T, Virtanen I, von Smitten K, Nordling S, von Boguslawski K, et al. Tenascin-C expression in invasion border of early breast cancer: A predictor of local and distant recurrence. Br J Cancer. 1998 Dec;78(11):1507-13.
40. Jahkola T, Toivonen T, von Smitten K, Virtanen I, Wasenius VM, Blomqvist C. Cathepsin-D, urokinase plasminogen activator and type-1 plasminogen activator inhibitor in early breast cancer: An immunohistochemical study of prognostic value and relations to tenascin-C and other factors. Br J Cancer. 1999 Apr;80(1-2):167-74.
41. Grigoriadis A, Mackay A, Reis-Filho JS, Steele D, Iseli C, Stevenson BJ, et al. Establishment of the epithelialspecific transcriptome of normal and malignant human breast cells based on MPSS and array expression data. Breast Cancer Res. 2006;8(5):R56.
42. Puglisi F, Puppin C, Pegolo E, Andreetta C, Pascoletti G, D'Aurizio F, et al. Expression of periostin in human breast cancer. J Clin Pathol. 2008 Apr;61(4):494-8.
43. Choquet D, Felsenfeld DP, Sheetz MP. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell. 1997 Jan 10;88(1):39-48.
44. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, et al. Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol. 2001 Jun 11;153(6):1175-86.
45. Galbraith CG, Yamada KM, Sheetz MP. The relationship between force and focal complex development. J Cell Biol. 2002 Nov 25;159(4):695-705.
46. Pelham RJ Jr, Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13661-5.
47. Giannone G, Dubin-Thaler BJ, Dobereiner HG, Kieffer N, Bresnick AR, Sheetz MP. Periodic lamellipodial con tractions correlate with rearward actin waves. Cell. 2004 Feb 6;116(3):431-43.
48. Sawada S, Iwasaki Y, Nakabayashi N, Ishihara K. Stress response of adherent cells on a polymer blend surface composed of a segmented polyurethane and MPC copolymers. J Biomed Mater Res A. 2006 Dec 1;79(3):476- 84.
49. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009 Nov 25;139(5):891-906.
50. Nelson CM, Bissell MJ. Of extracellular matrix, scaffolds, and signaling: Tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol. 2006;22:287-309.
51. Butcher DT, Alliston T, Weaver VM. A tense situation: Forcing tumour progression. Nat Rev Cancer. 2009 Feb;9(2):108-22.
52. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta. 2004 Jul 5;1692(2-3):103-19.
53. Geiger B, Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol. 2001 Oct;13(5):584-92.
54. Beacham DA, Cukierman E. Stromagenesis: The changing face of fibroblastic microenvironments during tumor progression. Semin Cancer Biol. 2005 Oct;15(5):329-41.
55. Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol. 2007 Dec;213(3):565-73.
56. Giannone G, Sheetz MP. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 2006 Apr;16(4):213-23.
57. Miranti CK, Brugge JS. Sensing the environment: A historical perspective on integrin signal transduction. Nat Cell Biol. 2002 Apr;4(4):E83-90.
58. Klein EA, Yin L, Kothapalli D, Castagnino P, Byfield FJ, Xu T, et al. Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr Biol. 2009 Sep 29;19(18):1511-8.
59. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene. 2009 Dec 10;28(49):4326-43.
60. Ulrich TA, de Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 2009 May 15;69(10):4167-74.
61. Williams CM, Engler AJ, Slone RD, Galante LL, Schwarzbauer JE. Fibronectin expression modulates mammary epithelial cell proliferation during acinar differentiation. Cancer Res. 2008 May 1;68(9):3185-92.
62. Gehler S, Baldassarre M, Lad Y, Leight JL, Wozniak MA, Riching KM, et al. Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol Biol Cell. 2009 Jul;20(14):3224-38.
63. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, et al. Collagen density promotes mammary tumor initiation and progression. BMC Med. 2008;6:11.
64. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol. 1997 Apr 7;137(1):231-45.
65. White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, et al. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell. 2004 Aug;6(2):159-70.
66. Guo WH, Frey MT, Burnham NA, Wang YL. Substrate rigidity regulates the formation and maintenance of tissues. Biophys J. 2006 Mar 15;90(6):2213-20.
67. Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J. 2000 Jul;79(1):144-52.
68. Menon S, Beningo KA. Cancer cell invasion is enhanced by applied mechanical stimulation. PLoS One. 2011;6(2):e17277.
69. Kostic A, Lynch CD, Sheetz MP. Differential matrix rigidity response in breast cancer cell lines correlates with the tissue tropism. PLoS One. 2009;4(7):e6361.
70. Morini M, Mottolese M, Ferrari N, Ghiorzo F, Buglioni S, Mortarini R, et al. The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer. 2000 Aug 1;87(3):336-42.
71. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell. 2011 Jul 8;146(1):148-63.
72. Saez A, Buguin A, Silberzan P, Ladoux B. Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys J. 2005 Dec;89(6):L52-4.
73. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J. 2007 Dec 15;93(12):4453- 61.
74. Na S, Collin O, Chowdhury F, Tay B, Ouyang M, Wang Y, et al. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc Natl Acad Sci U S A. 2008 May 6;105(18):6626-31.
75. Friedland JC, Lee MH, Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science. 2009 Jan 30;323(5914):642-4.
76. Ehrlicher AJ, Nakamura F, Hartwig JH, Weitz DA, Stossel TP. Mechanical strain in actin networks regulates Fil--GAP and integrin binding to filamin A. Nature. 2011 Oct 13;478(7368):260-3.
77. Tamada M, Sheetz MP, Sawada Y. Activation of a sig naling cascade by cytoskeleton stretch. Dev Cell. 2004 Nov;7(5):709-18.
78. Giannone G, Jiang G, Sutton DH, Critchley DR, Sheetz MP. Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation. J Cell Biol. 2003 Oct 27;163(2):409-19.
79. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. Stretching single talin rod molecules activates vinculin binding. Science. 2009 Jan 30;323(5914):638-41.
80. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol. 2005 Oct 24;171(2):209-15.
81. Razinia Z, Makela T, Ylanne J, Calderwood DA. Filamins in mechanosensing and signaling. Ann Rev Biophys. 2012;41:227-46.
82. Tang Y, Olufemi L, Wang MT, Nie D. Role of Rho GT-- Pases in breast cancer. Front Biosci. 2008;13:759-76.
83. Guilluy C, Garcia-Mata R, Burridge K. Rho protein crosstalk: Another social network? Trends Cell Biol. 2011 Dec;21(12):718-26.
84. Bishop AL, Hall A. Rho GTPases and their effector proteins. Biochem J. 2000 Jun 1;348 Pt 2:241-55.
85. Hall A, Nobes CD. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc London, Ser. B. 2000 Jul 29;355(1399):965-70.
86. Parri M, Chiarugi P. Rac and Rho GTPases in cancer cell motility control. Cell Commun Signaling. 2010;8:23.
87. Fritz G, Just I, Kaina B. Rho GTPases are over-expressed in human tumors. Int J Cancer. 1999 May 31;81(5):682- 7.
88. Fritz G, Brachetti C, Bahlmann F, Schmidt M, Kaina B. Rho GTPases in human breast tumours: Expression and mutation analyses and correlation with clinical parameters. Br J Cancer. 2002 Sep 9;87(6):635-44.
89. Kleer CG, van Golen KL, Zhang Y, Wu ZF, Rubin MA, Merajver SD. Characterization of RhoC expression in benign and malignant breast disease: A potential new marker for small breast carcinomas with metastatic ability. Am J Pathol. 2002 Feb;160(2):579-84.
90. Schnelzer A, Prechtel D, Knaus U, Dehne K, Gerhard M, Graeff H, et al. Rac1 in human breast cancer: Overexpression, mutation analysis, and characterization of a new isoform, Rac1b. Oncogene. 2000 Jun 15;19(26):3013-20.
91. Smith PG, Roy C, Zhang Y., Chauduri S. Mechanical stress increases RhoA activation in airway smooth muscle cells. Am J Respir Cell Mol Biol. 2003 Apr;28(4):436- 42.
92. Kawamura S, Miyamoto S, Brown JH. Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae: Cytoskeletal regulation of ERK translocation. J Biol Chem. 2003 Aug 15;278(33):31111-31117
93. Wojciak-Stothard B, Ridley AJ. Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases. J Cell Biol. 2003 Apr 28;161(2):429-39.
94. Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 2001 Sep 3;20(17):4639-47.
95. Kadler KE, Hill A, Canty-Laird EG. Collagen fibrillogenesis: Fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol. 2008 Oct;20(5):495-501.
96. Zhang Q, Magnusson MK, Mosher DF. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol Biol Cell. 1997 Aug;8(8):1415-25.
97. Samuel MS, Lopez JI, McGhee EJ, Croft DR, Strachan D, Timpson P, et al. Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell. 2011 Jun 14;19(6):776-91.
98. Benitah SA, Valeron PF, van Aelst L, Marshall CJ, Lacal JC. Rho GTPases in human cancer: An unresolved link to upstream and downstream transcriptional regulation. Biochim Biophys Acta. 2004 Dec 17;1705(2):121-32.
99. Sander EE, van Delft S, ten Klooster JP, Reid T, van der Kammen RA, Michiels F, et al. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J Cell Biol. 1998 Nov 30;143(5):1385-98.
100. Lozano E, Betson M, Braga VM. Tumor progression: Small GTPases and loss of cell-cell adhesion. Bioessays. 2003 May;25(5):452-63.
101. Nagy T, Wei H, Shen TL, Peng X, Liang CC, Gan B, et al. Mammary epithelial-specific deletion of the focal adhesion kinase gene leads to severe lobulo-alveolar hypoplasia and secretory immaturity of the murine mammary gland. J Biol Chem. 2007 Oct 26;282(43):31766-76.
102. Lahlou H, Sanguin-Gendreau V, Zuo D, Cardiff RD, McLean GW, Frame MC, et al. Mammary epithelialspecific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20302-7.
103. Provenzano PP, Inman DR, Eliceiri KW, Beggs HE, Keely PJ. Mammary epithelial-specific disruption of focal adhesion kinase retards tumor formation and metastasis in a transgenic mouse model of human breast cancer. Am J Pathol. 2008 Nov;173(5):1551-65.
104. Pylayeva Y, Gillen KM, Gerald W, Beggs HE, Reichardt LF, Giancotti FG. Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J Clin Invest. 2009 Feb;119(2):252-66.
105. Luo M, Fan H, Nagy T, Wei H, Wang C, Liu S, et al. Mammary epithelial-specific ablation of the focal adhesion kinase suppresses mammary tumorigenesis by affecting mammary cancer stem/progenitor cells. Cancer Res. 2009 Jan 15;69(2):466-74.
106. Cance WG, Harris JE, Iacocca MV, Roche E, Yang X, Chang J, et al. Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: Correlation with preinvasive and invasive phenotypes. Clin Cancer Res. 2000 Jun;6(6):2417-23.
107. Zhao JH, Reiske H, Guan JL. Regulation of the cell cycle by focal adhesion kinase. J Cell Biol. 1998 Dec 28;143(7):1997-2008.
108. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, et al. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 1995 Jul 1;55(13):2752-5.
109. Haskell H, Natarajan M, Hecker TP, Ding Q, Stewart J Jr, Grammer JR, et al. Focal adhesion kinase is expressed in the angiogenic blood vessels of malignant astrocytic tumors in vivo and promotes capillary tube formation of brain microvascular endothelial cells. Clin Cancer Res. 2003 Jun;9(6):2157-65.
110. Lark AL, Livasy CA, Dressler L, Moore DT, Millikan RC, Geradts J, et al. High focal adhesion kinase expression in invasive breast carcinomas is associated with an aggressive phenotype. Modern Pathol. 2005 Oct;18(10):1289-94.
111. Matkowskyj KA, Keller K, Glover S, Kornberg L, Tran-Son-Tay R, Benya RV. Expression of GRP and its receptor in well-differentiated colon cancer cells correlates with the presence of focal adhesion kinase phosphorylated at tyrosines 397 and 407. J Histochem Cytochem. 2003 Aug;51(8):1041-8.
112. Oktay MH, Oktay K, Hamele-Bena D, Buyuk A, Koss LG. Focal adhesion kinase as a marker of malignant phenotype in breast and cervical carcinomas. Human Pathol. 2003 Mar;34(3):240-5.
113. Golubovskaya V, Kaur A, Cance W. Cloning and characterization of the promoter region of human focal adhesion kinase gene: Nuclear factor kappa B and p53 binding sites. Biochim Biophys Acta. 2004 May 25;1678(2-3):111-25.
114. Golubovskaya VM, Conway-Dorsey K, Edmiston SN, Tse CK, Lark AA, Livasy CA, et al. FAK overexpression and p53 mutations are highly correlated in human breast cancer. Int J Cancer. 2009 Oct 1;125(7):1735-8.
115. Ayaki M, Komatsu K, Mukai M, Murata K, Kameyama M, Ishiguro S, et al. Reduced expression of focal adhesion kinase in liver metastases compared with matched primary human colorectal adenocarcinomas. Clin Cancer Res. 2001 Oct;7(10):3106-12.
116. Gabriel B, zur Hausen A, Stickeler E, Dietz C, Gitsch G, Fischer DC, et al. Weak expression of focal adhesion kinase (pp125FAK) in patients with cervical cancer is associated with poor disease outcome. Clin Cancer Res. 2006 Apr 15;12(8):2476-83.
117. Lu Z, Jiang G, Blume-Jensen P, Hunter T. Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase. Mol Cell Biol. 2001 Jun;21(12):4016-31.
118. Howe AK, Juliano RL. Distinct mechanisms mediate the initial and sustained phases of integrin-mediated activation of the Raf/MEK/mitogen-activated protein kinase cascade. J Biol Chem. 1998 Oct 16;273(42):27268-74.
119. Lin TH, Aplin AE, Shen Y, Chen Q, Schaller M, Romer L, et al. Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J Cell Biol. 1997 Mar 24;136(6):1385-95.
120. Schlaepfer DD, Hunter T. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J Biol Chem. 1997 May 16;272(20):13189-95.
121. Schlaepfer DD, Jones KC, Hunter T. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: Summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol Cell Biol. 1998 May;18(5):2571-85.
122. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol. 2000 May;2(5):249-56.
123. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006;4(1):38.
124. Provenzano PP, Inman DR, Eliceiri KW, Trier SM, Keely PJ. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophysical J. 2008 Dec;95(11):5374- 84.
125. Conklin MW, Eickhoff JC, Riching KM, Pehlke CA, Eliceiri KW, Provenzano PP, et al. Aligned collagen is a prognostic signature for survival in human breast carcinoma. The Am J Pathol. 2011 Mar;178(3):1221-32.
126. Guilak F. Functional Tissue Engineering. New York: Springer; 2003 pages 207-310.
127. Ogle BM, Mooradian DL. The role of vascular smooth muscle cell integrins in the compaction and mechanical strengthening of a tissue-engineered blood vessel. Tissue Eng. 1999 Aug;5(4):387-402.
128. Isenberg BC, Backman DE, Kinahan ME, Jesudason R, Suki B, Stone PJ, et al. Micropatterned cell sheets with defined cell and extracellular matrix orientation exhibit anisotropic mechanical properties. J Biomech. 2012 Mar 15;45(5):756-61.
129. Yang N, Mosher R, Seo S, Beebe D, Friedl A. Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. The Am J Pathol. 2011 Jan;178(1):325-35.
130. Sander EA, Barocas VH, Tranquillo RT. Initial fiber alignment pattern alters extracellular matrix synthesis in fibroblast-populated fibrin gel cruciforms and correlates with predicted tension. Ann Biomed Eng. 2011 Feb;39(2):714-29.
131. Wang JH, Jia F, Gilbert TW, Woo SL. Cell orientation determines the alignment of cell-produced collagenous matrix. J Biomech. 2003 Jan;36(1):97-102.
132. Beauvais DM, Rapraeger AC. Syndecans in tumor cell adhesion and signaling. Reprod Biol Endocrinol. 2004 Jan 7;2:3.
133. Friedl P, Wolf K. Tube travel: The role of proteases in individual and collective cancer cell invasion. Cancer Res. 2008 Sep 15;68(18):7247-9.
134. Xu B, Chow MJ, Zhang Y. Experimental and modeling study of collagen scaffolds with the effects of crosslinking and fiber alignment. Int J Biomater. 2011;2011:172389.
135. Bass MD, Roach KA, Morgan MR, Mostafavi-Pour Z, Schoen T, Muramatsu T, et al. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. The J Cell Biol. 2007 May 7;177(3):527-38.
136. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002 Mar;2(3):161-74.
137. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006 Mar;25(1):9-34.
138. Kohrmann A, Kammerer U, Kapp M, Dietl J, Anacker J. Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: New findings and review of the literature. BMC Cancer. 2009;9:188.
139. Ahonen M, Baker AH, Kahari VM. Adenovirus-mediated gene delivery of tissue inhibitor of metalloproteinases-3 inhibits invasion and induces apoptosis in melanoma cells. Cancer Res. 1998 Jun 1;58(11):2310-5.
140. Deryugina EI, Luo GX, Reisfeld RA, Bourdon MA, Strongin A. Tumor cell invasion through matrigel is regulated by activated matrix metalloproteinase-2. Anticancer Res. 1997 Sep-Oct;17(5A):3201-10.
141. Ala-Aho R, Johansson N, Baker AH, Kahari VM. Expression of collagenase-3 (MMP-13) enhances invasion of human fibrosarcoma HT-1080 cells. Int J Cancer. 2002 Jan 20;97(3):283-9.
142. Friedl P, Wolf K. Proteolytic interstitial cell migration: A five-step process. Cancer Metastasis Rev. 2009 Jun;28(1-2):129-35.
143. Sabeh F, Shimizu-Hirota R, Weiss SJ. Protease-dependent versus -independent cancer cell invasion programs: Three-dimensional amoeboid movement revisited. J Cell Biol. 2009 Apr 6;185(1):11-9.
144. Ilina O, Bakker GJ, Vasaturo A, Hofmann RM, Friedl P. Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion. Phys Biol. 2011 Feb;8(1):015010.
145. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol. 2004 Feb;16(1):14-23.
146. Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol. 2006 Aug 8;16(15):1515-23.
147. Friedl P, Wolf K. Proteolytic and non-proteolytic migra tion of tumour cells and leucocytes. Biochem Soc Symp. 2003 (70):277-285.
148. Haston WS, Shields JM, Wilkinson PC. Lymphocyte locomotion and attachment on two-dimensional surfaces and in three-dimensional matrices. J Cell Biol. 1982 Mar;92(3):747-52.
149. Harley BA, Kim HD, Zaman MH, Yannas IV, Lauffenburger DA, Gibson LJ. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys J. 2008 Oct;95(8):4013- 24.
150. Liu X, Wu H, Byrne M, Jeffrey J, Krane S, Jaenisch R. A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J Cell Biol. 1995 Jul;130(1):227-37.