Functional Live-cell Imaging Demonstrates That Beta1-integrin Promotes Type IV Collagen Degradation by Breast and Prostate Cancer Cells

Overview

Journal Mol Imaging

Publisher Sage Publications

Specialty Radiology

Date 2009 Jan 7

PMID 19123990

Citations 23

Authors

Mansoureh Sameni

Julie Dosescu

Kenneth M Yamada

Bonnie F Sloane

Dora Cavallo-Medved

Affiliations

Soon will be listed here.

Abstract

The ability of tumor cells to adhere to, migrate on, and remodel extracellular matrices is mediated by cell surface receptors such as beta1-integrins. Here we conducted functional live-cell imaging in real time to investigate the effects of modulating beta1-integrin expression and function on proteolytic remodeling of the extracellular matrix. Human breast and prostate cancer cells were grown on reconstituted basement membrane containing a quenched fluorescent form of collagen IV. Generation of cleavage products and the resulting increases in fluorescence were imaged and quantified. Decreases in the expression and activity of beta1-integrin reduced digestion of quenched fluorescent-collagen IV by the breast and prostate cancer cells and correspondingly their invasion through and migration on reconstituted basement membrane. Decreased extracellular matrix degradation also was associated with changes in the constituents of proteolytic pathways: decreases in secretion of the cysteine protease cathepsin B, the matrix metalloproteinase (MMP)-13, and tissue inhibitors of metalloproteinases (TIMP)-1 and 2; a decrease in expression of MMP-14 or membrane type 1 MMP; and an increase in secretion of TIMP-3. This is the first study to demonstrate through functional live-cell imaging that downregulation of beta1-integrin expression and function reduces proteolysis of collagen IV by breast and prostate cancer cells.

Citing Articles

Collagen Remodeling along Cancer Progression Providing a Novel Opportunity for Cancer Diagnosis and Treatment.

Song K, Yu Z, Zu X, Li G, Hu Z, Xue Y Int J Mol Sci. 2022; 23(18).

PMID: 36142424 PMC: 9502421. DOI: 10.3390/ijms231810509.

Advancing cell instructive biomaterials through increased understanding of cell receptor spacing and material surface functionalization.

Maynard S, Winter C, Cunnane E, Stevens M Regen Eng Transl Med. 2021; 7(4):553-547.

PMID: 34805482 PMC: 8594271. DOI: 10.1007/s40883-020-00180-0.

Thermoresponsive Elastin-b-Collagen-Like Peptide Bioconjugate Nanovesicles for Targeted Drug Delivery to Collagen-Containing Matrices.

Luo T, David M, Dunshee L, Scott R, Urello M, Price C Biomacromolecules. 2017; 18(8):2539-2551.

PMID: 28719196 PMC: 5815509. DOI: 10.1021/acs.biomac.7b00686.

Pathomimetic avatars reveal divergent roles of microenvironment in invasive transition of ductal carcinoma in situ.

Sameni M, Cavallo-Medved D, Franco O, Chalasani A, Ji K, Aggarwal N Breast Cancer Res. 2017; 19(1):56.

PMID: 28506312 PMC: 5433063. DOI: 10.1186/s13058-017-0847-0.

Elucidation of the Roles of Tumor Integrin β1 in the Extravasation Stage of the Metastasis Cascade.

Chen M, Lamar J, Li R, Hynes R, Kamm R Cancer Res. 2016; 76(9):2513-24.

PMID: 26988988 PMC: 4873393. DOI: 10.1158/0008-5472.CAN-15-1325.

References

Chirco R, Liu X, Jung K, Kim H . Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev. 2006; 25(1):99-113. DOI: 10.1007/s10555-006-7893-x. View

Goel H, Breen M, Zhang J, Das I, Aznavoorian-Cheshire S, Greenberg N . beta1A integrin expression is required for type 1 insulin-like growth factor receptor mitogenic and transforming activities and localization to focal contacts. Cancer Res. 2005; 65(15):6692-700. DOI: 10.1158/0008-5472.CAN-04-4315. View

Linebaugh B, Sameni M, Day N, Sloane B, Keppler D . Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur J Biochem. 1999; 264(1):100-9. DOI: 10.1046/j.1432-1327.1999.00582.x. View

Mohamed M, Sloane B . Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer. 2006; 6(10):764-75. DOI: 10.1038/nrc1949. View

Weaver V, Petersen O, Wang F, Larabell C, Briand P, Damsky C . Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol. 1997; 137(1):231-45. PMC: 2139858. DOI: 10.1083/jcb.137.1.231. View

Rehn M, Veikkola T, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T . Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci U S A. 2001; 98(3):1024-9. PMC: 14702. DOI: 10.1073/pnas.98.3.1024. View

Guo W, Giancotti F . Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004; 5(10):816-26. DOI: 10.1038/nrm1490. View

Yao E, Zhang H, Chen Y, Lee B, Chew K, Moore D . Increased beta1 integrin is associated with decreased survival in invasive breast cancer. Cancer Res. 2007; 67(2):659-64. DOI: 10.1158/0008-5472.CAN-06-2768. View

Larsen M, Artym V, Green J, Yamada K . The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol. 2006; 18(5):463-71. DOI: 10.1016/j.ceb.2006.08.009. View

10.

Festuccia C, Angelucci A, Gravina G, Eleuterio E, Vicentini C, Bologna M . Bombesin-dependent pro-MMP-9 activation in prostatic cancer cells requires beta1 integrin engagement. Exp Cell Res. 2002; 280(1):1-11. DOI: 10.1006/excr.2002.5609. View

11.

Koblinski J, Dosescu J, Sameni M, Moin K, Clark K, Sloane B . Interaction of human breast fibroblasts with collagen I increases secretion of procathepsin B. J Biol Chem. 2002; 277(35):32220-7. DOI: 10.1074/jbc.M204708200. View

12.

White D, Kurpios N, Zuo D, Hassell J, Blaess S, Mueller U . 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; 6(2):159-70. DOI: 10.1016/j.ccr.2004.06.025. View

13.

Ahmed N, Oliva K, Wang Y, Quinn M, Rice G . Downregulation of urokinase plasminogen activator receptor expression inhibits Erk signalling with concomitant suppression of invasiveness due to loss of uPAR-beta1 integrin complex in colon cancer cells. Br J Cancer. 2003; 89(2):374-84. PMC: 2394266. DOI: 10.1038/sj.bjc.6601098. View

14.

Akiyama S, Yamada S, Chen W, Yamada K . Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J Cell Biol. 1989; 109(2):863-75. PMC: 2115712. DOI: 10.1083/jcb.109.2.863. View

15.

Berry M, Gui G, Wells C, Carpenter R . Integrin expression and survival in human breast cancer. Eur J Surg Oncol. 2004; 30(5):484-9. DOI: 10.1016/j.ejso.2004.01.016. View

16.

Cavallo-Medved D, Dosescu J, Linebaugh B, Sameni M, Rudy D, Sloane B . Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia. 2004; 5(6):507-19. PMC: 1502576. DOI: 10.1016/s1476-5586(03)80035-0. View

17.

Strongin A, Collier I, Bannikov G, Marmer B, Grant G, Goldberg G . Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem. 1995; 270(10):5331-8. DOI: 10.1074/jbc.270.10.5331. View

18.

Cress A, Rabinovitz I, Zhu W, Nagle R . The alpha 6 beta 1 and alpha 6 beta 4 integrins in human prostate cancer progression. Cancer Metastasis Rev. 1995; 14(3):219-28. DOI: 10.1007/BF00690293. View

19.

Sameni M, Moin K, Sloane B . Imaging proteolysis by living human breast cancer cells. Neoplasia. 2001; 2(6):496-504. PMC: 1508086. DOI: 10.1038/sj.neo.7900116. View

20.

Wang F, Hansen R, Radisky D, Yoneda T, Barcellos-Hoff M, Petersen O . Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J Natl Cancer Inst. 2002; 94(19):1494-503. PMC: 2975573. DOI: 10.1093/jnci/94.19.1494. View