Structural and Functional Evidence for a Substrate Exclusion Mechanism in Mammalian Tolloid Like-1 (TLL-1) Proteinase

Overview

Journal FEBS Lett

Specialty Biochemistry

Date 2010 Jan 2

PMID 20043912

Citations 13

Authors

Richard Berry

Thomas A Jowitt

Laure Garrigue-Antar

Karl E Kadler

Clair Baldock

Affiliations

Soon will be listed here.

Abstract

Bone morphogenetic protein-1 (BMP-1)/tolloid proteinases are fundamental to regulating dorsal ventral patterning and extracellular matrix deposition. In mammals there are four proteinases, the splice variants BMP-1 and mammalian tolloid (mTLD), and tolloid like-1 and -2 (TLL-1/2). BMP-1 has the highest catalytic activity and lacks three non-catalytic domains. We demonstrate that TLL-1, which has intermediate activity, forms a calcium-ion dependent dimer with monomers stacked side-by-side. In contrast, truncated TLL-1 molecules having the same shorter structure as BMP-1 are monomers and have improved activity towards their substrate chordin. The increased activity exceeds not only that of full-length TLL-1 but also BMP-1.

Citing Articles

BMP antagonists in tissue development and disease.

Correns A, Zimmermann L, Baldock C, Sengle G Matrix Biol Plus. 2021; 11:100071.

PMID: 34435185 PMC: 8377005. DOI: 10.1016/j.mbplus.2021.100071.

Characterization of tolloid-mediated cleavage of the GDF8 procomplex.

McCoy J, Goebel E, Thompson T Biochem J. 2021; 478(9):1733-1747.

PMID: 33876824 PMC: 8670536. DOI: 10.1042/BCJ20210054.

Tolloid-Like 1 Negatively Regulates Hepatic Differentiation of Human Induced Pluripotent Stem Cells Through Transforming Growth Factor Beta Signaling.

Kiso A, Toba Y, Tsutsumi S, Deguchi S, Igai K, Koshino S Hepatol Commun. 2020; 4(2):255-267.

PMID: 32025609 PMC: 6996343. DOI: 10.1002/hep4.1466.

Interaction of Complement Defence Collagens C1q and Mannose-Binding Lectin with BMP-1/Tolloid-like Proteinases.

Lacroix M, Tessier A, Dumestre-Perard C, Vadon-Le Goff S, Gout E, Bruckner-Tuderman L Sci Rep. 2017; 7(1):16958.

PMID: 29209066 PMC: 5717261. DOI: 10.1038/s41598-017-17318-w.

Agonists and Antagonists of TGF-β Family Ligands.

Chang C Cold Spring Harb Perspect Biol. 2016; 8(8).

PMID: 27413100 PMC: 4968162. DOI: 10.1101/cshperspect.a021923.

References

Ge G, Hopkins D, Ho W, Greenspan D . GDF11 forms a bone morphogenetic protein 1-activated latent complex that can modulate nerve growth factor-induced differentiation of PC12 cells. Mol Cell Biol. 2005; 25(14):5846-58. PMC: 1168807. DOI: 10.1128/MCB.25.14.5846-5858.2005. View

Ge G, Seo N, Liang X, Hopkins D, Hook M, Greenspan D . Bone morphogenetic protein-1/tolloid-related metalloproteinases process osteoglycin and enhance its ability to regulate collagen fibrillogenesis. J Biol Chem. 2004; 279(40):41626-33. DOI: 10.1074/jbc.M406630200. View

Scott I, Blitz I, Pappano W, Imamura Y, Clark T, Steiglitz B . Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Dev Biol. 1999; 213(2):283-300. DOI: 10.1006/dbio.1999.9383. View

Ge G, Zhang Y, Steiglitz B, Greenspan D . Mammalian tolloid-like 1 binds procollagen C-proteinase enhancer protein 1 and differs from bone morphogenetic protein 1 in the functional roles of homologous protein domains. J Biol Chem. 2006; 281(16):10786-98. DOI: 10.1074/jbc.M511111200. View

Petropoulou V, Garrigue-Antar L, Kadler K . Identification of the minimal domain structure of bone morphogenetic protein-1 (BMP-1) for chordinase activity: chordinase activity is not enhanced by procollagen C-proteinase enhancer-1 (PCPE-1). J Biol Chem. 2005; 280(24):22616-23. DOI: 10.1074/jbc.M413468200. View

Hojima Y, van Der Rest M, Prockop D . Type I procollagen carboxyl-terminal proteinase from chick embryo tendons. Purification and characterization. J Biol Chem. 1985; 260(29):15996-6003. View

Berry R, Jowitt T, Ferrand J, Roessle M, Grossmann J, Canty-Laird E . Role of dimerization and substrate exclusion in the regulation of bone morphogenetic protein-1 and mammalian tolloid. Proc Natl Acad Sci U S A. 2009; 106(21):8561-6. PMC: 2689009. DOI: 10.1073/pnas.0812178106. View

Garrigue-Antar L, Francois V, Kadler K . Deletion of epidermal growth factor-like domains converts mammalian tolloid into a chordinase and effective procollagen C-proteinase. J Biol Chem. 2004; 279(48):49835-41. DOI: 10.1074/jbc.M408134200. View

Bond J, Beynon R . The astacin family of metalloendopeptidases. Protein Sci. 1995; 4(7):1247-61. PMC: 2143163. DOI: 10.1002/pro.5560040701. View

10.

Scott I, Imamura Y, Pappano W, Troedel J, Recklies A, Roughley P . Bone morphogenetic protein-1 processes probiglycan. J Biol Chem. 2000; 275(39):30504-11. DOI: 10.1074/jbc.M004846200. View

11.

Rai N, Nollmann M, Spotorno B, Tassara G, Byron O, Rocco M . SOMO (SOlution MOdeler) differences between X-Ray- and NMR-derived bead models suggest a role for side chain flexibility in protein hydrodynamics. Structure. 2005; 13(5):723-34. DOI: 10.1016/j.str.2005.02.012. View

12.

Ge G, Greenspan D . BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J Cell Biol. 2006; 175(1):111-20. PMC: 2064503. DOI: 10.1083/jcb.200606058. View

13.

Schuck P . Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J. 2000; 78(3):1606-19. PMC: 1300758. DOI: 10.1016/S0006-3495(00)76713-0. View

14.

Wolfman N, McPherron A, Pappano W, Davies M, Song K, Tomkinson K . Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci U S A. 2003; 100(26):15842-6. PMC: 307655. DOI: 10.1073/pnas.2534946100. View

15.

Veitch D, Nokelainen P, McGowan K, Nguyen T, Nguyen N, Stephenson R . Mammalian tolloid metalloproteinase, and not matrix metalloprotease 2 or membrane type 1 metalloprotease, processes laminin-5 in keratinocytes and skin. J Biol Chem. 2002; 278(18):15661-8. DOI: 10.1074/jbc.M210588200. View

16.

Panchenko M, Stetler-Stevenson W, Trubetskoy O, Gacheru S, Kagan H . Metalloproteinase activity secreted by fibrogenic cells in the processing of prolysyl oxidase. Potential role of procollagen C-proteinase. J Biol Chem. 1996; 271(12):7113-9. DOI: 10.1074/jbc.271.12.7113. View

17.

van Heel M, Harauz G, Orlova E, Schmidt R, Schatz M . A new generation of the IMAGIC image processing system. J Struct Biol. 1996; 116(1):17-24. DOI: 10.1006/jsbi.1996.0004. View

18.

Rattenholl A, Pappano W, Koch M, Keene D, Kadler K, Sasaki T . Proteinases of the bone morphogenetic protein-1 family convert procollagen VII to mature anchoring fibril collagen. J Biol Chem. 2002; 277(29):26372-8. DOI: 10.1074/jbc.M203247200. View

19.

Pappano W, Steiglitz B, Scott I, Keene D, Greenspan D . Use of Bmp1/Tll1 doubly homozygous null mice and proteomics to identify and validate in vivo substrates of bone morphogenetic protein 1/tolloid-like metalloproteinases. Mol Cell Biol. 2003; 23(13):4428-38. PMC: 164836. DOI: 10.1128/MCB.23.13.4428-4438.2003. View

20.

Vistica J, Dam J, Balbo A, Yikilmaz E, Mariuzza R, Rouault T . Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal Biochem. 2004; 326(2):234-56. DOI: 10.1016/j.ab.2003.12.014. View