Integrin α11β1 regulates cancer stromal stiffness and promotes tumorigenicity and metastasis in non-small cell lung cancer

Oncogene

Volumn 35, Issue 15, 2016, Pages 1899-1908

  Navab, R ^a   Strumpf, D ^a   To, C ^a   Pasko, E ^a,b   Kim, K S ^c   Park, C J ^a   Hai, J ^a   Liu, J ^a   Jonkman, J ^a   Barczyk, M ^d   Bandarchi, B ^a   Wang, Y H ^a   Venkat, K ^a   Ibrahimov, E ^a   Pham, N A ^a   Ng, C ^a   Radulovich, N ^a   Zhu, C Q ^a   Pintilie, M ^a   Wang, D ^a   Lu, A ^a   Jurisica, I ^a,b,c   Walker, G C ^c   Gullberg, D ^d   Tsao, M S ^a,b,e   more..

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF BERGEN   (Norway)

^e UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; FIBROBLAST GROWTH FACTOR 2; FIBULIN; FOCAL ADHESION KINASE 1; FOCAL ADHESION KINASE 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTEGRIN; INTEGRIN ALPHA11BETA1; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SEMAPHORIN 3F; SOMATOMEDIN BINDING PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; VASCULOTROPIN A; ALPHA INTEGRIN; BETA1 INTEGRIN; COLLAGEN RECEPTOR; INTEGRIN ALPHA11, MOUSE; PROTEIN KINASE; SCLEROPROTEIN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CANCER GROWTH; CARCINOGENICITY; CELL DIFFERENTIATION; CONTROLLED STUDY; CROSS LINKING; DOWN REGULATION; FIBROBLAST; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; METASTASIS; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR XENOGRAFT; WESTERN BLOTTING; WILD TYPE; ADENOCARCINOMA; ANIMAL; CROSS BREEDING; ELASTICITY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; INBRED MOUSE STRAIN; KNOCKOUT MOUSE; LUNG TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

ADENOCARCINOMA; ANIMALS; ANTIGENS, CD29; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; COLLAGEN; CROSSES, GENETIC; ELASTICITY; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; INTEGRIN ALPHA CHAINS; INTEGRINS; LUNG NEOPLASMS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PROTEIN KINASES; RECEPTORS, COLLAGEN; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 84935472234     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.254     Document Type: Article

References (57)

1. Egeblad M, Ewald AJ, Askautrud HA, Truitt ML, Welm BE, Bainbridge E et al. Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis Model Mech 2008; 1: 155-167; discussion 165.
2. 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; 139: 891-906.
3. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006; 66: 11238-11246.
4. 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: 38.
5. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth - bystanders turning into key players. Curr Opin Genet Dev 2009; 19: 67-73.
6. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007; 9: 1392-1400.
7. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6: 392-401.
8. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012; 21: 418-429.
9. Nakasone ES, Askautrud HA, Kees T, Park JH, Plaks V, Ewald AJ et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012; 21: 488-503.
10. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res 2010; 339: 269-280.
11. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010; 10: 9-22.
12. Gullberg DE, Lundgren-Akerlund E. Collagen-binding I domain integrins - what do they do? Prog Histochem Cytochem 2002; 37: 3-54.
13. Popova SN, Lundgren-Akerlund E, Wiig H, Gullberg D. Physiology and pathology of collagen receptors. Acta Physiol (Oxf) 2007; 190: 179-187.
14. Knight CG, Morton LF, Onley DJ, Peachey AR, Messent AJ, Smethurst PA et al. Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. J Biol Chem 1998; 273: 33287-33294.
15. Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triplehelical) collagens. J Biol Chem 2000; 275: 35-40.
16. Zhang WM, Kapyla J, Puranen JS, Knight CG, Tiger CF, Pentikainen OT et al. alpha 11beta 1 integrin recognizes the GFOGER sequence in interstitial collagens. J Biol Chem 2003; 278: 7270-7277.
17. Jokinen J, Dadu E, Nykvist P, Kapyla J, White DJ, Ivaska J et al. Integrin-mediated cell adhesion to type I collagen fibrils. J Biol Chem 2004; 279: 31956-31963.
18. Popova SN, Barczyk M, Tiger CF, Beertsen W, Zigrino P, Aszodi A et al. Alpha11 beta1 integrin-dependent regulation of periodontal ligament function in the erupting mouse incisor. Mol Cell Biol 2007; 27: 4306-4316.
19. Barczyk MM, Olsen LH, da Franca P, Loos BG, Mustafa K, Gullberg D et al. A role for alpha11beta1 integrin in the human periodontal ligament. J Dent Res 2009; 88: 621-626.
20. Wang KK, Liu N, Radulovich N, Wigle DA, Johnston MR, Shepherd FA et al. Novel candidate tumor marker genes for lung adenocarcinoma. Oncogene 2002; 21: 7598-7604.
21. Zhu CQ, Popova SN, Brown ER, Barsyte-Lovejoy D, Navab R, Shih W et al. Integrin alpha 11 regulates IGF2 expression in fibroblasts to enhance tumorigenicity of human non-small-cell lung cancer cells. Proc Natl Acad Sci USA 2007; 104: 11754-11759.
22. Navab R, Strumpf D, Bandarchi B, Zhu CQ, Pintilie M, Ramnarine VR et al. Prognostic gene-expression signature of carcinoma-associated fibroblasts in nonsmall cell lung cancer. Proc Natl Acad Sci USA 2011; 108: 7160-7165.
23. Pietras K, Ostman A. Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 2010; 316: 1324-1331.
24. Blumbach K, Niehoff A, Belgardt BF, Ehlen HW, Schmitz M, Hallinger R et al. Dwarfism in mice lacking collagen-binding integrins alpha2beta1 and alpha11-beta1 is caused by severely diminished IGF-1 levels. J Biol Chem 2012; 287: 6431-6440.
25. Liu J, Blackhall F, Seiden-Long I, Jurisica I, Navab R, Liu N et al. Modeling of lung cancer by an orthotopically growing H460SM variant cell line reveals novel candidate genes for systemic metastasis. Oncogene 2004; 23: 6316-6324.
26. Zeltz C, Lu N, Gullberg D. Integrin alpha11beta1: a major collagen receptor on fibroblastic cells. Adv Exp Med Biol 2014; 819: 73-83.
27. Zeltz C, Orgel J, Gullberg D. Molecular composition and function of integrin-based collagen glues-Introducing COLINBRIs. Biochim Biophys Acta 2014; 1840: 2533-2548.
28. Tiger CF, Fougerousse F, Grundstrom G, Velling T, Gullberg D. alpha11beta1 integrin is a receptor for interstitial collagens involved in cell migration and collagen reorganization on mesenchymal nonmuscle cells. Dev Biol 2001; 237: 116-129.
29. Popova SN, Rodriguez-Sanchez B, Liden A, Betsholtz C, Van Den Bos T, Gullberg D. The mesenchymal alpha11beta1 integrin attenuates PDGF-BBstimulated chemotaxis of embryonic fibroblasts on collagens. Dev Biol 2004; 270: 427-442.
30. Lu N, Carracedo S, Ranta J, Heuchel R, Soininen R, Gullberg D. The human alpha11 integrin promoter drives fibroblast-restricted expression in vivo and is regulated by TGF-beta1 in a Smad-and Sp1-dependent manner. Matrix Biol 2010; 29: 166-176.
31. Svendsen OS, Barczyk MM, Popova SN, Liden A, Gullberg D, Wiig H. The alpha11beta1 integrin has a mechanistic role in control of interstitial fluid pressure and edema formation in inflammation. Arterioscler Thromb Vasc Biol 2009; 29: 1864-1870.
32. Zweers MC, Davidson JM, Pozzi A, Hallinger R, Janz K, Quondamatteo F et al. Integrin alpha2beta1 is required for regulation of murine wound angiogenesis but is dispensable for reepithelialization. J Invest Dermatol 2007; 127: 467-478.
33. Carracedo S, Lu N, Popova SN, Jonsson R, Eckes B, Gullberg D. The fibroblast integrin alpha11beta1 is induced in a mechanosensitive manner involving activin A and regulates myofibroblast differentiation. J Biol Chem 2010; 285: 10434-10445.
34. Talior-Volodarsky I, Connelly KA, Arora PD, Gullberg D, McCulloch CA. alpha11 integrin stimulates myofibroblast differentiation in diabetic cardiomyopathy. Cardiovasc Res 2012; 96: 265-275.
35. Schulz JN, Zeltz C, Sorensen IW, Barczyk M, Carracedo S, Hallinger R et al. Reduced granulation tissue and wound strength in the absence of alpha11beta1 integrin. J Invest Dermatol 2015; 135: 1435-1444.
36. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF et al. Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 2007; 179: 1275-1287.
37. Tilghman RW, Slack-Davis JK, Sergina N, Martin KH, Iwanicki M, Hershey ED et al. Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J Cell Sci 2005; 118: 2613-2623.
38. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005; 6: 56-68.
39. Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I et al. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc Natl Acad Sci USA 2010; 107: 20009-20014.
40. Yamauchi M, Shiiba M. Lysine hydroxylation and cross-linking of collagen. Methods Mol Biol 2008; 446: 95-108.
41. Wilgus ML, Borczuk AC, Stoopler M, Ginsburg M, Gorenstein L, Sonett JR et al. Lysyl oxidase: a lung adenocarcinoma biomarker of invasion and survival. Cancer 2011; 117: 2186-2191.
42. Xiao Q, Ge G. Lysyl oxidase, extracellular matrix remodeling and cancer metastasis. Cancer Microenviron 2012; 5: 261-273.
43. Cheng T, Liu Q, Zhang R, Zhang Y, Chen J, Yu R et al. Lysyl oxidase promotes bleomycin-induced lung fibrosis through modulating inflammation. J Mol Cell Biol 2014; 6: 506-515.
44. Malkoski SP, Haeger SM, Cleaver TG, Rodriguez KJ, Li H, Lu SL et al. Loss of transforming growth factor beta type II receptor increases aggressive tumor behavior and reduces survival in lung adenocarcinoma and squamous cell carcinoma. Clin Cancer Res 2012; 18: 2173-2183.
45. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009; 15: 35-44.
46. Xing F, Saidou J, Watabe K. Cancer associated fibroblasts (CAFs) in tumor microenvironment. Front Biosci 2010; 15: 166-179.
47. John T, Kohler D, Pintilie M, Yanagawa N, Pham NA, Li M et al. The ability to form primary tumor xenografts is predictive of increased risk of disease recurrence in early-stage non-small cell lung cancer. Clin Cancer Res 2011; 17: 134-141.
48. Navab R, Liu J, Seiden-Long I, Shih W, Li M, Bandarchi B et al. Co-overexpression of Met and hepatocyte growth factor promotes systemic metastasis in NCI-H460 non-small cell lung carcinoma cells. Neoplasia 2009; 11: 1292-1300.
49. Velling T, Kusche-Gullberg M, Sejersen T, Gullberg D. cDNA cloning and chromosomal localization of human alpha(11) integrin. A collagen-binding, I domain-containing, beta(1)-associated integrin alpha-chain present in muscle tissues. J Biol Chem 1999; 274: 25735-25742.
50. Williams RM, Zipfel WR, Webb WW. Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 2005; 88: 1377-1386.
51. Brown E, McKee T, diTomaso E, Pluen A, Seed B, Boucher Y et al. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 2003; 9: 796-800.
52. Campagnola PJ, Loew LM. Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat Biotechnol 2003; 21: 1356-1360.
53. Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Transactions on Systems, Man, and Cybernetics 1973; SMC-3: 610-621.
54. Hutter JL, Bechhoefer J. Calibration of atomic-force microscope tips. Rev Sci Instrum 1993; 64: 1868-1873.
55. Hertz H. Über die Berührung fester elastischer Körper. J Reine Angewandte Mathematik 1882; 92: 156-171.
56. Sneddon I. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 1965; 3: 47-57.
57. Littell RC, Henry PR, Ammerman CB. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 1998; 76: 1216-1231.