BST-2 Binding with Cellular MT1-MMP Blocks Cell Growth and Migration Via Decreasing MMP2 Activity

Overview

Journal J Cell Biochem

Specialties Biochemistry
Cell Biology

Date 2011 Nov 9

PMID 22065321

Citations 11

Authors

Gongping Gu

Dejian Zhao

Ziming Yin

Ping Liu

Affiliations

Soon will be listed here.

Abstract

MT1-MMP (membrane type 1-matrix metalloproteinase) plays important roles in cell growth and tumor invasion via mediating cleavage of MMP2/gelatinase A and a variety of substrates including type I collagen. BST-2 (bone marrow stromal cell antigen 2) is a membrane tetherin whose expression dramatically reduces the release of a broad range of enveloped viruses including HIV from infected cells. In this study, we provided evidence that both transient and IFN-α induced BST-2 could decrease the activity of MMP2 via binding to cellular MT1-MMP on its C-terminus and inhibiting its proteolytic activity; and finally block cell growth and migration. Zymography gel and Western blot experiments demonstrated that BST-2 decreased MMP2 activity, but no effect on the expression of MMP2 and MT1-MMP genes. Confocal and immunoprecipitation data showed that BST-2 co-localized and interacted with MT1-MMP. This interaction inhibited the proteolytic enzyme activity of MT1-MMP, and blocked the activation of proMMP2. Experimental results of C-terminus deletion mutant of MT1-MMP showed that activity of MMP2 was no change and also no interaction existed between the mutant and BST-2 after co-transfection with the mutant and BST-2. It meant that C-terminus of MT1-MMP played a key role in the interaction with BST-2. In addition, cell growth in 3D type I collagen gel lattice and cell migration were all inhibited by BST-2. Taken together, BST-2, as a membrane protein and a tetherin of enveloped viruses, was a novel inhibitor of MT1-MMP and could be considerable as an inhibitor of cancer cell growth and migration on clinic.

Citing Articles

Novel Diagnostic Biomarker BST2 Identified by Integrated Transcriptomics Promotes the Development of Endometriosis via the TNF-α/NF-κB Signaling Pathway.

Jiang L, Wang S, Xia X, Zhang T, Wang X, Zeng F Biochem Genet. 2024; 63(1):354-377.

PMID: 38441813 DOI: 10.1007/s10528-024-10666-z.

In Silico Analysis of Genes Associated with the Pathogenesis of Odontogenic Keratocyst.

Ramirez-Martinez C, Legorreta-Villegas I, Mejia-Velazquez C, Portilla-Robertson J, Gaitan-Cepeda L, Paramo-Sanchez J Int J Mol Sci. 2024; 25(4).

PMID: 38397053 PMC: 10889808. DOI: 10.3390/ijms25042379.

Bone marrow stromal cell antigen 2: Tumor biology, signaling pathway and therapeutic targeting (Review).

Yu H, Bian Q, Wang X, Wang X, Lai L, Wu Z Oncol Rep. 2024; 51(3).

PMID: 38240088 PMC: 10828922. DOI: 10.3892/or.2024.8704.

Transcription factor old astrocyte specifically induced substance is a novel regulator of kidney fibrosis.

Yamamoto A, Morioki H, Nakae T, Miyake Y, Harada T, Noda S FASEB J. 2020; 35(2):e21158.

PMID: 33150680 PMC: 7821213. DOI: 10.1096/fj.202001820R.

Proteomic Profiling of Small Extracellular Vesicles Secreted by Human Pancreatic Cancer Cells Implicated in Cellular Transformation.

Servage K, Stefanius K, Gray H, Orth K Sci Rep. 2020; 10(1):7713.

PMID: 32382024 PMC: 7205864. DOI: 10.1038/s41598-020-64718-6.

References

Bravo-Cordero J, Marrero-Diaz R, Megias D, Genis L, Garcia-Grande A, Garcia M . MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 2007; 26(6):1499-510. PMC: 1829373. DOI: 10.1038/sj.emboj.7601606. View

Jiang A, Lehti K, Wang X, Weiss S, Keski-Oja J, Pei D . Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proc Natl Acad Sci U S A. 2001; 98(24):13693-8. PMC: 61103. DOI: 10.1073/pnas.241293698. View

Will H, Atkinson S, Butler G, Smith B, Murphy G . The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. J Biol Chem. 1996; 271(29):17119-23. DOI: 10.1074/jbc.271.29.17119. View

Jiang A, Pei D . Distinct roles of catalytic and pexin-like domains in membrane-type matrix metalloproteinase (MMP)-mediated pro-MMP-2 activation and collagenolysis. J Biol Chem. 2003; 278(40):38765-71. DOI: 10.1074/jbc.M306618200. View

Mercure M, Ginnan R, Singer H . CaM kinase II delta2-dependent regulation of vascular smooth muscle cell polarization and migration. Am J Physiol Cell Physiol. 2008; 294(6):C1465-75. PMC: 3689296. DOI: 10.1152/ajpcell.90638.2007. View

Lehti K, Lohi J, Juntunen M, Pei D, Keski-Oja J . Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J Biol Chem. 2002; 277(10):8440-8. DOI: 10.1074/jbc.M109128200. View

Wainwright D, Balyasnikova I, Han Y, Lesniak M . The expression of BST2 in human and experimental mouse brain tumors. Exp Mol Pathol. 2011; 91(1):440-6. PMC: 3139740. DOI: 10.1016/j.yexmp.2011.04.012. View

Evans D, Serra-Moreno R, Singh R, Guatelli J . BST-2/tetherin: a new component of the innate immune response to enveloped viruses. Trends Microbiol. 2010; 18(9):388-96. PMC: 2956607. DOI: 10.1016/j.tim.2010.06.010. View

Uekita T, Itoh Y, Yana I, Ohno H, Seiki M . Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J Cell Biol. 2002; 155(7):1345-56. PMC: 2199326. DOI: 10.1083/jcb.200108112. View

10.

dOrtho M, Will H, Atkinson S, Butler G, Messent A, Gavrilovic J . Membrane-type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur J Biochem. 1998; 250(3):751-7. DOI: 10.1111/j.1432-1033.1997.00751.x. View

11.

Neil S, Zang T, Bieniasz P . Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature. 2008; 451(7177):425-30. DOI: 10.1038/nature06553. View

12.

Hlubek F, Spaderna S, Jung A, Kirchner T, Brabletz T . Beta-catenin activates a coordinated expression of the proinvasive factors laminin-5 gamma2 chain and MT1-MMP in colorectal carcinomas. Int J Cancer. 2003; 108(2):321-6. DOI: 10.1002/ijc.11522. View

13.

Zhou Z, Apte S, Soininen R, Cao R, Baaklini G, Rauser R . Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A. 2000; 97(8):4052-7. PMC: 18145. DOI: 10.1073/pnas.060037197. View

14.

Kang T, Yi J, Yang W, Wang X, Jiang A, Pei D . Functional characterization of MT3-MMP in transfected MDCK cells: progelatinase A activation and tubulogenesis in 3-D collagen lattice. FASEB J. 2000; 14(15):2559-68. DOI: 10.1096/fj.00-0269com. View

15.

Galvez B, Matias-Roman S, Yanez-Mo M, Vicente-Manzanares M, Sanchez-Madrid F, Arroyo A . Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. Mol Biol Cell. 2003; 15(2):678-87. PMC: 329288. DOI: 10.1091/mbc.e03-07-0516. View

16.

Liu P, Yang J, Pei J, Pei D, Wilson M . Regulation of MT1-MMP activity by β-catenin in MDCK non-cancer and HT1080 cancer cells. J Cell Physiol. 2010; 225(3):810-21. PMC: 2939945. DOI: 10.1002/jcp.22292. View

17.

Seiki M . The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr Opin Cell Biol. 2002; 14(5):624-32. DOI: 10.1016/s0955-0674(02)00363-0. View

18.

Nawrocki-Raby B, Gilles C, Polette M, Martinella-Catusse C, Bonnet N, Puchelle E . E-Cadherin mediates MMP down-regulation in highly invasive bronchial tumor cells. Am J Pathol. 2003; 163(2):653-61. PMC: 1868220. DOI: 10.1016/S0002-9440(10)63692-9. View

19.

Seiki M . Membrane-type 1 matrix metalloproteinase: a key enzyme for tumor invasion. Cancer Lett. 2003; 194(1):1-11. DOI: 10.1016/s0304-3835(02)00699-7. View

20.

Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G . Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic. 2003; 4(10):694-709. DOI: 10.1034/j.1600-0854.2003.00129.x. View