Nucleobindin-1 Regulates ECM Degradation by Promoting Intra-Golgi Trafficking of MMPs

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2020 Jun 2

PMID 32479594

Citations 19

Authors

Natalia Pacheco-Fernandez

Mehrshad Pakdel

Birgit Blank

Ismael Sanchez-Gonzalez

Kathrin Weber

Mai Ly Tran

Tobias Karl-Heinz Hecht

Renate Gautsch

Gisela Beck

Franck Perez

Angelika Hausser

Stefan Linder

Julia von Blume

Affiliations

Soon will be listed here.

Abstract

Matrix metalloproteinases (MMPs) degrade several ECM components and are crucial modulators of cell invasion and tissue organization. Although much has been reported about their function in remodeling ECM in health and disease, their trafficking across the Golgi apparatus remains poorly understood. Here we report that the cis-Golgi protein nucleobindin-1 (NUCB1) is critical for MMP2 and MT1-MMP trafficking along the Golgi apparatus. This process is Ca2+-dependent and is required for invasive MDA-MB-231 cell migration as well as for gelatin degradation in primary human macrophages. Our findings emphasize the importance of NUCB1 as an essential component of MMP transport and its overall impact on ECM remodeling.

Citing Articles

Molecular tag for promoting -glycan maturation in the cargo receptor-mediated secretion pathway.

Yagi H, Yamada R, Saito T, Honda R, Nakano R, Inutsuka K iScience. 2024; 27(12):111457.

PMID: 39717080 PMC: 11664129. DOI: 10.1016/j.isci.2024.111457.

Deciphering the dual nature of nesfatin-1: a tale of zinc ion's Janus-faced influence.

Lenda R, Zhukova L, Ozyhar A, Bystranowska D Cell Commun Signal. 2024; 22(1):298.

PMID: 38812013 PMC: 11134965. DOI: 10.1186/s12964-024-01675-x.

Identification of a short, single site matriglycan that maintains neuromuscular function in the mouse.

Yang T, Chandel I, Gonzales M, Okuma H, Prouty S, Zarei S bioRxiv. 2024; .

PMID: 38187633 PMC: 10769215. DOI: 10.1101/2023.12.20.572361.

Research progress and application of single-cell sequencing in head and neck malignant tumors.

Qu S, Gong M, Deng Y, Xiang Y, Ye D Cancer Gene Ther. 2023; 31(1):18-27.

PMID: 37968342 PMC: 10794142. DOI: 10.1038/s41417-023-00691-2.

The RNA-Binding and RNA-Melting Activities of the Multifunctional Protein Nucleobindin 1.

Mikhaylina A, Svoeglazova A, Stolboushkina E, Tishchenko S, Kostareva O Int J Mol Sci. 2023; 24(7).

PMID: 37047165 PMC: 10093973. DOI: 10.3390/ijms24076193.

References

Gueye Y, Ferhat L, Sbai O, Bianco J, Ould-Yahoui A, Bernard A . Trafficking and secretion of matrix metalloproteinase-2 in olfactory ensheathing glial cells: A role in cell migration?. Glia. 2011; 59(5):750-70. DOI: 10.1002/glia.21146. View

Jacob A, Linklater E, Bayless B, Lyons T, Prekeris R . The role and regulation of Rab40b-Tks5 complex during invadopodia formation and cancer cell invasion. J Cell Sci. 2016; 129(23):4341-4353. PMC: 5201011. DOI: 10.1242/jcs.193904. View

de Alba E, Tjandra N . Structural studies on the Ca2+-binding domain of human nucleobindin (calnuc). Biochemistry. 2004; 43(31):10039-49. DOI: 10.1021/bi049310a. View

Wiesner C, El Azzouzi K, Linder S . A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages. J Cell Sci. 2013; 126(Pt 13):2820-33. DOI: 10.1242/jcs.122358. View

Scherer P, Lederkremer G, Williams S, Fogliano M, Baldini G, Lodish H . Cab45, a novel (Ca2+)-binding protein localized to the Golgi lumen. J Cell Biol. 1996; 133(2):257-68. PMC: 2120788. DOI: 10.1083/jcb.133.2.257. View

Dancourt J, Zheng H, Bottanelli F, Allgeyer E, Bewersdorf J, Graham M . Small cargoes pass through synthetically glued Golgi stacks. FEBS Lett. 2016; 590(12):1675-86. PMC: 4925213. DOI: 10.1002/1873-3468.12210. View

Ton V, Rao R . Functional expression of heterologous proteins in yeast: insights into Ca2+ signaling and Ca2+-transporting ATPases. Am J Physiol Cell Physiol. 2004; 287(3):C580-9. DOI: 10.1152/ajpcell.00135.2004. View

Vandooren J, Van den Steen P, Opdenakker G . Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): the next decade. Crit Rev Biochem Mol Biol. 2013; 48(3):222-72. DOI: 10.3109/10409238.2013.770819. View

Lavoie C, Meerloo T, Lin P, Farquhar M . Calnuc, an EF-hand Ca(2+)-binding protein, is stored and processed in the Golgi and secreted by the constitutive-like pathway in AtT20 cells. Mol Endocrinol. 2002; 16(11):2462-74. DOI: 10.1210/me.2002-0079. View

10.

van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le Cabec V . Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol. 2009; 184(2):1049-61. DOI: 10.4049/jimmunol.0902223. View

11.

Jacob A, Jing J, Lee J, Schedin P, Gilbert S, Peden A . Rab40b regulates trafficking of MMP2 and MMP9 during invadopodia formation and invasion of breast cancer cells. J Cell Sci. 2013; 126(Pt 20):4647-58. PMC: 3795337. DOI: 10.1242/jcs.126573. View

12.

Monteiro P, Rosse C, Castro-Castro A, Irondelle M, Lagoutte E, Paul-Gilloteaux P . Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol. 2013; 203(6):1063-79. PMC: 3871436. DOI: 10.1083/jcb.201306162. View

13.

Deng Y, Rivera-Molina F, Toomre D, Burd C . Sphingomyelin is sorted at the trans Golgi network into a distinct class of secretory vesicle. Proc Natl Acad Sci U S A. 2016; 113(24):6677-82. PMC: 4914164. DOI: 10.1073/pnas.1602875113. View

14.

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

15.

Wiesner C, Faix J, Himmel M, Bentzien F, Linder S . KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood. 2010; 116(9):1559-69. DOI: 10.1182/blood-2009-12-257089. View

16.

Murphy D, Courtneidge S . The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol. 2011; 12(7):413-26. PMC: 3423958. DOI: 10.1038/nrm3141. View

17.

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

18.

Malhotra V, Serafini T, Orci L, Shepherd J, Rothman J . Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell. 1989; 58(2):329-36. DOI: 10.1016/0092-8674(89)90847-7. View

19.

Wiech H, Geier B, Paschke T, Spang A, Grein K, Steinkotter J . Characterization of green alga, yeast, and human centrins. Specific subdomain features determine functional diversity. J Biol Chem. 1996; 271(37):22453-61. DOI: 10.1074/jbc.271.37.22453. View

20.

Leung A, Ramesh N, Vogel C, Unniappan S . Nucleobindins and encoded peptides: From cell signaling to physiology. Adv Protein Chem Struct Biol. 2019; 116:91-133. DOI: 10.1016/bs.apcsb.2019.02.001. View