Matrix metalloproteinase 14 is required for fibrous tissue expansion

Taylor, Susan H.; Yeung, Ching-Yan Chloé; Kalson, Nicholas S.; Lu, Yinhui; Zigrino, Paola; Starborg, Tobias; Warwood, Stacey; Holmes, David; Canty‐Laird, Elizabeth G.; Mauch, Cornelia; Kadler, Karl E.

doi:10.7554/elife.09345

Cited by 45 publications

(48 citation statements)

References 63 publications

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“…Nevertheless, given the broad substrate repertoire of MMP14 and the multiple biological activities that have been assigned to its functions (Ager et al, 2015;Alcaraz et al, 2011;Barbolina and Stack, 2008;Bonnans et al, 2014;Chun et al, 2004;Fahlman et al, 2014;Fu et al, 2013;Itoh, 2015;Kajita et al, 2001;Koshikawa et al, 2000;Koziol et al, 2012;Mori et al, 2009Mori et al, , 2013Rebustini et al, 2009;Rowe and Weiss, 2009;Sabeh et al, 2009;Sakamoto et al, 2014;ShimizuHirota et al, 2012;Simian et al, 2001;Tang et al, 2013;Taylor et al, 2015;Weaver et al, 2014;Yana et al, 2007), we were surprised to find that deleting the proteinase in vivo exerted little, if any, effect on morphogenesis. Likewise, despite an ex vivo requirement for MMP15 in submandibular gland proliferation, matrix remodeling and branching (Rebustini et al, 2009), mammary glands from Mmp15-targeted mice assembled normal ductal networks through P10.…”

Section: Discussionmentioning

confidence: 99%

“…MMP14 and MMP15 have been reported to play diverse roles in a range of morphogenesis-associated processes, including cell adhesion and motility, invasion, proliferation, energy metabolism, senescence, the proteolytic processing of growth factors, cytokines and chemokines, as well as ECM remodeling (Ager et al, 2015;Alcaraz et al, 2011;Barbolina and Stack, 2008;Bonnans et al, 2014;Chun et al, 2004;Fahlman et al, 2014;Fu et al, 2013;Itoh, 2015;Kajita et al, 2001;Koshikawa et al, 2000;Koziol et al, 2012;Mori et al, 2009Mori et al, , 2013Rebustini et al, 2009;Sabeh et al, 2009;Sakamoto et al, 2014;Shimizu-Hirota et al, 2012;Simian et al, 2001;Tang et al, 2013;Taylor et al, 2015;Weaver et al, 2014;Yana et al, 2007). Consistent, in part, with previous reports linking MT-MMPs with epithelial cell branching programs (Alcaraz et al, 2011;Bonnans et al, 2014;Mori et al, 2009Mori et al, , 2013Rebustini et al, 2009;Weaver et al, 2014), we find that MMP14, but not MMP15, is required for mammary epithelial organoid branching through type I collagen barriers in vitro.…”

Section: Discussionmentioning

confidence: 99%

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Functional roles of MMP14 and MMP15 in early postnatal mammary gland development

et al. 2016

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During late embryogenesis, mammary epithelial cells initiate migration programs that drive ductal invasion into the surrounding adipose-rich mesenchyme. Currently, branching morphogenesis is thought to depend on the mobilization of the membrane-anchored matrix metalloproteinases MMP14 (MT1-MMP) and MMP15 (MT2-MMP), which drive epithelial cell invasion by remodeling the extracellular matrix and triggering associated signaling cascades. However, the roles that these proteinases play during mammary gland development in vivo remain undefined. Here, we characterize the impact of global Mmp14 and Mmp15 targeting on early postnatal mammary gland development in mice. Unexpectedly, both Mmp14 −/− and Mmp15 −/− mammary glands retain the ability to generate intact ductal networks. Although neither proteinase is required for branching morphogenesis, transcriptome profiling reveals a key role for MMP14 and MMP15 in regulating mammary gland adipocyte differentiation. Whereas MMP14 promotes the generation of white fat depots crucial for energy storage, MMP15 differentially controls the formation of thermogenic brown fat. Taken together, these data not only indicate that current paradigms relevant to proteinase-dependent morphogenesis need be revisited, but also identify new roles for the enzymes in regulating adipocyte fate determination in the developing mammary gland.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Functional roles of MMP14 and MMP15 in early postnatal mammary gland development

et al. 2016

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“…MT1-MMP knockout mice have arrested tendon development around the time of birth [146]. The knockout mouse tendons had collagen fibrils of ~50 nm diameter that were retained by fibripositors (actin-dependent invaginations of the plasma membrane).…”

Section: The Role Of Collagen Catabolism In Normal Physiologymentioning

confidence: 99%

“…The knockout mouse tendons had collagen fibrils of ~50 nm diameter that were retained by fibripositors (actin-dependent invaginations of the plasma membrane). It was determined that collagenolysis by MT1-MMP was not essential for tendon development, but MT1-MMP processing of fibronectin was, resulting in the release of fibrils from fibripositors [146]. …”

Section: The Role Of Collagen Catabolism In Normal Physiologymentioning

confidence: 99%

Matrix metalloproteinase collagenolysis in health and disease

Amar

Smith

Fields

2017

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

166

108

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The proteolytic processing of collagen (collagenolysis) is critical in development and homeostasis, but also contributes to numerous pathologies. Mammalian interstitial collagenolytic enzymes include members of the matrix metalloproteinase (MMP) family and cathepsin K. While MMPs have long been recognized for their ability to catalyze the hydrolysis of collagen, the roles of individual MMPs in physiological and pathological collagenolysis are less defined. The use of knockout and mutant animal models, which reflect human diseases, has revealed distinct collagenolytic roles for MT1-MMP and MMP-13. A better understanding of temporal and spatial collagen processing, along with the knowledge of the specific MMP involved, will ultimately lead to more effective treatments for cancer, arthritis, cardiovascular conditions, and infectious diseases.

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“…Within the MT-MMP subgroup, membrane type-1 MMP (MT1-MMP) is required for proper tendon development, as the deletion of MT1-MMP in embryonic tendon fibroblasts results in the failure of normal tendon formation (55). MT1-MMP expression has also been shown to correlate with pivotal events in the growth response of mechanically-loaded tendons of adult animals (48).…”

Section: Introductionmentioning

confidence: 99%

Postnatal Tendon Growth and Remodeling Requires Platelet-Derived Growth Factor Receptor Signaling

Sugg

Markworth

Disser

et al. 2017

Preprint

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Platelet-derived growth factor receptor (PDGFR) signaling plays an important role in the fundamental biological activities of many cells that compose musculoskeletal tissues. However, little is known about the role of PDGFR signaling during tendon growth and remodeling in adult animals. Using the hindlimb synergist ablation model of tendon growth, our objectives were to determine the role of PDGFR signaling in the adaptation of tendons subjected to a mechanical growth stimulus, as well as to investigate the biological mechanisms behind this response. We demonstrate that both PDGFRs, PDGFRα and PDGFRβ, are expressed in tendon fibroblasts, and that the inhibition of PDGFR signaling suppresses the normal growth of tendon tissue in response to mechanical growth cues due to defects in fibroblast proliferation and migration. We also identify that membrane type-1 matrix metalloproteinase (MT1-MMP) as an essential proteinase for the migration of tendon fibroblasts through their extracellular matrix. Furthermore, we report that MT1-MMP translation is regulated by PI3K/Akt signaling , while ERK1/2 controls post-translational trafficking of MT1-MMP to the plasma membrane of tendon fibroblasts. Taken together, these findings demonstrate that PDGFR signaling is necessary for postnatal tendon growth and remodeling, and that MT1-MMP is a critical mediator of tendon fibroblast migration and a potential target for the treatment of tendon injuries and diseases. KEYWORDSMatrix metalloproteinase; extracellular matrix; fibroblast; plated-derived growth factor receptor; tenocyte.peer-reviewed)

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Matrix metalloproteinase 14 is required for fibrous tissue expansion

Cited by 45 publications

References 63 publications

Functional roles of MMP14 and MMP15 in early postnatal mammary gland development

Functional roles of MMP14 and MMP15 in early postnatal mammary gland development

Matrix metalloproteinase collagenolysis in health and disease

Postnatal Tendon Growth and Remodeling Requires Platelet-Derived Growth Factor Receptor Signaling

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