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Title: New insight into the role of MMP14 in metabolic balance

Abstract

Membrane-anchored matrix metalloproteinase 14 (MMP14) is involved broadly in organ development through both its proteolytic and signal-transducing functions. Knockout of Mmp14 (KO) in mice results in a dramatic reduction of body size and wasting followed by premature death, the mechanism of which is poorly understood. Since the mammary gland develops after birth and is thus dependent for its functional progression on systemic and local cues, we chose it as an organ model for understanding why KO mice fail to thrive. A global analysis of the mammary glands’ proteome in the wild type (WT) and KO mice provided insight into an unexpected role of MMP14 in maintaining metabolism and homeostasis. We performed mass spectrometry and quantitative proteomics to determine the protein signatures of mammary glands from 7 to 11 days old WT and KO mice and found that KO rudiments had a significantly higher level of rate-limiting enzymes involved in catabolic pathways. Glycogen and lipid levels in KO rudiments were reduced, and the circulating levels of triglycerides and glucose were lower. Analysis of the ultrastructure of mammary glands imaged by electron microscopy revealed a significant increase in autophagy signatures in KO mice. Finally, Mmp14 silenced mammary epithelial cells displayed enhanced autophagy.more » Applied to a systemic level, these findings indicate that MMP14 is a crucial regulator of tissue homeostasis. If operative on a systemic level, these findings could explain how Mmp14KO litter fail to thrive due to disorder in metabolism.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [6];  [7];  [5];  [5]
  1. Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Calcutta, Calcutta (India)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. de Sao Paulo, Sao Paulo (Brazil)
  4. Columbia Univ. Medical Center, New York, NY (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Kanazawa Univ., Kanazawa (Japan)
  7. Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1378994
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PeerJ
Additional Journal Information:
Journal Volume: 4; Journal Issue: 7; Journal ID: ISSN 2167-8359
Publisher:
PeerJ Inc.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Mori, Hidetoshi, Bhat, Ramray, Bruni-Cardoso, Alexandre, Chen, Emily I., Jorgens, Danielle M., Coutinho, Kester, Louie, Katherine, Bowen, Benjamin Ben, Inman, Jamie L., Tecca, Victoria, Lee, Sarah J., Becker-Weimann, Sabine, Northen, Trent, Seiki, Motoharu, Borowsky, Alexander D., Auer, Manfred, and Bissell, Mina J. New insight into the role of MMP14 in metabolic balance. United States: N. p., 2016. Web. doi:10.7717/peerj.2142.
Mori, Hidetoshi, Bhat, Ramray, Bruni-Cardoso, Alexandre, Chen, Emily I., Jorgens, Danielle M., Coutinho, Kester, Louie, Katherine, Bowen, Benjamin Ben, Inman, Jamie L., Tecca, Victoria, Lee, Sarah J., Becker-Weimann, Sabine, Northen, Trent, Seiki, Motoharu, Borowsky, Alexander D., Auer, Manfred, & Bissell, Mina J. New insight into the role of MMP14 in metabolic balance. United States. https://doi.org/10.7717/peerj.2142
Mori, Hidetoshi, Bhat, Ramray, Bruni-Cardoso, Alexandre, Chen, Emily I., Jorgens, Danielle M., Coutinho, Kester, Louie, Katherine, Bowen, Benjamin Ben, Inman, Jamie L., Tecca, Victoria, Lee, Sarah J., Becker-Weimann, Sabine, Northen, Trent, Seiki, Motoharu, Borowsky, Alexander D., Auer, Manfred, and Bissell, Mina J. Wed . "New insight into the role of MMP14 in metabolic balance". United States. https://doi.org/10.7717/peerj.2142. https://www.osti.gov/servlets/purl/1378994.
@article{osti_1378994,
title = {New insight into the role of MMP14 in metabolic balance},
author = {Mori, Hidetoshi and Bhat, Ramray and Bruni-Cardoso, Alexandre and Chen, Emily I. and Jorgens, Danielle M. and Coutinho, Kester and Louie, Katherine and Bowen, Benjamin Ben and Inman, Jamie L. and Tecca, Victoria and Lee, Sarah J. and Becker-Weimann, Sabine and Northen, Trent and Seiki, Motoharu and Borowsky, Alexander D. and Auer, Manfred and Bissell, Mina J.},
abstractNote = {Membrane-anchored matrix metalloproteinase 14 (MMP14) is involved broadly in organ development through both its proteolytic and signal-transducing functions. Knockout of Mmp14 (KO) in mice results in a dramatic reduction of body size and wasting followed by premature death, the mechanism of which is poorly understood. Since the mammary gland develops after birth and is thus dependent for its functional progression on systemic and local cues, we chose it as an organ model for understanding why KO mice fail to thrive. A global analysis of the mammary glands’ proteome in the wild type (WT) and KO mice provided insight into an unexpected role of MMP14 in maintaining metabolism and homeostasis. We performed mass spectrometry and quantitative proteomics to determine the protein signatures of mammary glands from 7 to 11 days old WT and KO mice and found that KO rudiments had a significantly higher level of rate-limiting enzymes involved in catabolic pathways. Glycogen and lipid levels in KO rudiments were reduced, and the circulating levels of triglycerides and glucose were lower. Analysis of the ultrastructure of mammary glands imaged by electron microscopy revealed a significant increase in autophagy signatures in KO mice. Finally, Mmp14 silenced mammary epithelial cells displayed enhanced autophagy. Applied to a systemic level, these findings indicate that MMP14 is a crucial regulator of tissue homeostasis. If operative on a systemic level, these findings could explain how Mmp14KO litter fail to thrive due to disorder in metabolism.},
doi = {10.7717/peerj.2142},
journal = {PeerJ},
number = 7,
volume = 4,
place = {United States},
year = {Wed Jul 13 00:00:00 EDT 2016},
month = {Wed Jul 13 00:00:00 EDT 2016}
}

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Works referenced in this record:

Autophagy in the Cellular Energetic Balance
journal, May 2011


Laser Scanning–Based Tissue Autofluorescence/Fluorescence Imaging (LS-TAFI), a New Technique for Analysis of Microanatomy in Whole-Mount Tissues
journal, June 2012

  • Mori, Hidetoshi; Borowsky, Alexander D.; Bhat, Ramray
  • The American Journal of Pathology, Vol. 180, Issue 6
  • DOI: 10.1016/j.ajpath.2012.02.032

Quantitative Proteomics Using 15N SILAC Mouse
journal, July 2013


Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry
journal, February 2007

  • Elias, Joshua E.; Gygi, Steven P.
  • Nature Methods, Vol. 4, Issue 3
  • DOI: 10.1038/nmeth1019

Cellular activation of proMMP-13 by MT1-MMP depends on the C-terminal domain of MMP-13
journal, November 2002


A quantitative analysis software tool for mass spectrometry–based proteomics
journal, March 2008

  • Park, Sung Kyu; Venable, John D.; Xu, Tao
  • Nature Methods, Vol. 5, Issue 4
  • DOI: 10.1038/nmeth.1195

Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity
journal, May 2009


Membrane-type 1 matrix metalloproteinase and cell migration
journal, September 2003

  • Seiki, Motoharu; Mori, Hidetoshi; Kajita, Masahiro
  • Biochemical Society Symposia, Vol. 70
  • DOI: 10.1042/bss0700253

A proteomic approach to identify substrates of matrix metalloproteinase-14 in human plasma
journal, October 2004

  • Hwang, In Kwan; Park, Sung Min; Kim, Se Yeon
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1702, Issue 1
  • DOI: 10.1016/j.bbapap.2004.08.001

A Pericellular Collagenase Directs the 3-Dimensional Development of White Adipose Tissue
journal, May 2006


An Alternative Processing of Integrin α v Subunit in Tumor Cells by Membrane Type-1 Matrix Metalloproteinase
journal, December 2001

  • Ratnikov, Boris I.; Rozanov, Dmitri V.; Postnova, Tanya I.
  • Journal of Biological Chemistry, Vol. 277, Issue 9
  • DOI: 10.1074/jbc.m109580200

Changes in fat cell morphology during lactation in the mouse
journal, December 1973

  • Elias, Joel J.; Pitelka, Dorothy R.; Armstrong, Rosa C.
  • The Anatomical Record, Vol. 177, Issue 4
  • DOI: 10.1002/ar.1091770407

Freeze substitution in 3 hours or less: FREEZE SUBSTIUTION IN 3 HOURS OR LESS
journal, August 2011


Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes
journal, August 2003

  • Toth, Marta; Chvyrkova, Irina; Bernardo, M. Margarida
  • Biochemical and Biophysical Research Communications, Vol. 308, Issue 2
  • DOI: 10.1016/s0006-291x(03)01405-0

Strategies for MMP inhibition in cancer: innovations for the post-trial era
journal, September 2002

  • Overall, Christopher Mark; López-Otín, Carlos
  • Nature Reviews Cancer, Vol. 2, Issue 9
  • DOI: 10.1038/nrc884

Glycolytic defects in muscle: Aspects of collaboration between basic science and clinical medicine
journal, January 1995


Glycolytic defects in muscle: Aspects of collaboration between basic science and clinical medicine
journal, January 1995


Self-organization of engineered epithelial tubules by differential cellular motility
journal, August 2009

  • Mori, H.; Gjorevski, N.; Inman, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 35
  • DOI: 10.1073/pnas.0901269106

Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects
journal, December 2004


Strategies for MMP inhibition in cancer: innovations for the post-trial era
journal, September 2002

  • Overall, Christopher Mark; López-Otín, Carlos
  • Nature Reviews Cancer, Vol. 2, Issue 9
  • DOI: 10.1038/nrc884

Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells
journal, April 2007

  • Yana, I.; Sagara, H.; Takaki, S.
  • Journal of Cell Science, Vol. 120, Issue 9
  • DOI: 10.1242/jcs.000679

Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells
journal, April 2007

  • Yana, I.; Sagara, H.; Takaki, S.
  • Journal of Cell Science, Vol. 120, Issue 9
  • DOI: 10.1242/jcs.000679

Selective high-affinity transport of aspartate by a Drosophila homologue of the excitatory amino-acid transporters
journal, February 2000


Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: roles of adipophilin and lipid metabolism
journal, April 2007

  • Russell, Tanya D.; Palmer, Carol A.; Orlicky, David J.
  • Journal of Lipid Research, Vol. 48, Issue 7
  • DOI: 10.1194/jlr.m600474-jlr200

Sexually Dimorphic Diet-Induced Insulin Resistance in Obese Tissue Inhibitor of Metalloproteinase-2 (TIMP-2)-Deficient Mice
journal, April 2011

  • Jaworski, Diane M.; Sideleva, Olga; Stradecki, Holly M.
  • Endocrinology, Vol. 152, Issue 4
  • DOI: 10.1210/en.2010-1029

Genetic Link Between Obesity and MMP14-Dependent Adipogenic Collagen Turnover
journal, July 2010

  • Chun, T. -H.; Inoue, M.; Morisaki, H.
  • Diabetes, Vol. 59, Issue 10
  • DOI: 10.2337/db10-0073

Method to Correlate Tandem Mass Spectra of Modified Peptides to Amino Acid Sequences in the Protein Database
journal, April 1995

  • Yates, John R.; Eng, Jimmy K.; McCormack, Ashley L.
  • Analytical Chemistry, Vol. 67, Issue 8
  • DOI: 10.1021/ac00104a020

Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure
journal, October 2003


The Low Density Lipoprotein Receptor-related Protein LRP Is Regulated by Membrane Type-1 Matrix Metalloproteinase (MT1-MMP) Proteolysis in Malignant Cells
journal, November 2003

  • Rozanov, Dmitri V.; Hahn-Dantona, Elizabeth; Strickland, Dudley K.
  • Journal of Biological Chemistry, Vol. 279, Issue 6
  • DOI: 10.1074/jbc.m311569200

Mass spectrometry imaging for in situ kinetic histochemistry
journal, April 2013

  • Louie, Katherine B.; Bowen, Benjamin P.; McAlhany, Stephanie
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep01656

Changes in fat cell morphology during lactation in the mouse
journal, December 1973

  • Elias, Joel J.; Pitelka, Dorothy R.; Armstrong, Rosa C.
  • The Anatomical Record, Vol. 177, Issue 4
  • DOI: 10.1002/ar.1091770407

Identification of a mutation in liver glycogen phosphorylase in glycogen storage disease type VI
journal, May 1998


MT1-MMP-Dependent Control of Skeletal Stem Cell Commitment via a β1-Integrin/YAP/TAZ Signaling Axis
journal, May 2013


SnapShot: Branching Morphogenesis
journal, August 2014


Changes in mammary fat pad composition and lipolytic capacity throughout pregnancy
journal, November 2005


A Pericellular Collagenase Directs the 3-Dimensional Development of White Adipose Tissue
journal, May 2006


Fatal infantile form of muscle phosphofructokinase deficiency
journal, November 1986


?-enolase deficiency, a new metabolic myopathy of distal glycolysis
journal, January 2001

  • Comi, Giacomo P.; Fortunato, Francesco; Lucchiari, Sabrina
  • Annals of Neurology, Vol. 50, Issue 2
  • DOI: 10.1002/ana.1095

A matrix metalloproteinase expressed on the surface of invasive tumour cells
journal, July 1994

  • Sato, Hiroshi; Takino, Takahisa; Okada, Yasunori
  • Nature, Vol. 370, Issue 6484
  • DOI: 10.1038/370061a0

Distribution and source of lipoprotein lipase in mouse mammary gland
journal, May 1991


Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine
journal, February 2007


Molecular Mechanisms of Hepatic Steatosis and Insulin Resistance in the AGPAT2-Deficient Mouse Model of Congenital Generalized Lipodystrophy
journal, February 2009


Autophagy in the Cellular Energetic Balance
journal, May 2011


Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry
journal, February 2007

  • Elias, Joshua E.; Gygi, Steven P.
  • Nature Methods, Vol. 4, Issue 3
  • DOI: 10.1038/nmeth1019

A quantitative analysis software tool for mass spectrometry–based proteomics
journal, March 2008

  • Park, Sung Kyu; Venable, John D.; Xu, Tao
  • Nature Methods, Vol. 5, Issue 4
  • DOI: 10.1038/nmeth.1195

Laser Scanning–Based Tissue Autofluorescence/Fluorescence Imaging (LS-TAFI), a New Technique for Analysis of Microanatomy in Whole-Mount Tissues
journal, June 2012

  • Mori, Hidetoshi; Borowsky, Alexander D.; Bhat, Ramray
  • The American Journal of Pathology, Vol. 180, Issue 6
  • DOI: 10.1016/j.ajpath.2012.02.032

SnapShot: Branching Morphogenesis
journal, August 2014


[39] Bandeiraea simplicifolia lectin II
book, January 1978


Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity
journal, May 2009


Effect of diet on exercise tolerance in carnitine palmitoyltransferase II deficiency
journal, August 2003


Metabolic cooperativity between epithelial cells and adipocytes of mice
journal, November 1981


MT1-MMP promotes vascular smooth muscle dedifferentiation through LRP1 processing
journal, December 2008

  • Lehti, K.; Rose, N. F.; Valavaara, S.
  • Journal of Cell Science, Vol. 122, Issue 1
  • DOI: 10.1242/jcs.035279

Matrix Metalloproteinases in Remodeling of the Normal and Neoplastic Mammary Gland
journal, January 1998

  • Rudolph-Owen, Laura A.; Matrisian, Lynn M.
  • Journal of Mammary Gland Biology and Neoplasia, Vol. 3, Issue 2, p. 177-189
  • DOI: 10.1023/A:1018746923474

A Rapid Method of Total Lipid Extraction and Purification
journal, January 1959

  • Bligh, E. G.; Dyer, W. J.
  • Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1
  • DOI: 10.1139/y59-099

AGPAT2 is mutated in congenital generalized lipodystrophy linked to chromosome 9q34
journal, April 2002

  • Agarwal, Anil K.; Arioglu, Elif; de Almeida, Salome
  • Nature Genetics, Vol. 31, Issue 1
  • DOI: 10.1038/ng880

A matrix metalloproteinase expressed on the surface of invasive tumour cells
journal, July 1994

  • Sato, Hiroshi; Takino, Takahisa; Okada, Yasunori
  • Nature, Vol. 370, Issue 6484
  • DOI: 10.1038/370061a0

Interrelationship of glycogen metabolism and lactose synthesis in mammary epithelial cells of mice
journal, November 1980

  • Emerman, J. T.; Bartley, J. C.; Bissell, M. J.
  • Biochemical Journal, Vol. 192, Issue 2
  • DOI: 10.1042/bj1920695

MT1-MMP-Dependent Control of Skeletal Stem Cell Commitment via a β1-Integrin/YAP/TAZ Signaling Axis
journal, May 2013


Histochemical detection of glycogen usingGriffonia simplicifolia agglutinin II
journal, November 1986

  • Hennigar, Randolph A.; Schulte, Bradley A.; Spicer, Samuel S.
  • The Histochemical Journal, Vol. 18, Issue 11-12
  • DOI: 10.1007/bf01675294

Autophagy and Metabolism
journal, December 2010


Validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy
journal, March 2006

  • Overall, Christopher M.; Kleifeld, Oded
  • Nature Reviews Cancer, Vol. 6, Issue 3
  • DOI: 10.1038/nrc1821

Targeting the Warburg Effect That Arises in Tumor Cells Expressing Membrane Type-1 Matrix Metalloproteinase
journal, March 2011

  • Sakamoto, Takeharu; Niiya, Daigo; Seiki, Motoharu
  • Journal of Biological Chemistry, Vol. 286, Issue 16
  • DOI: 10.1074/jbc.M110.188714

Self-organization of engineered epithelial tubules by differential cellular motility
journal, August 2009

  • Mori, H.; Gjorevski, N.; Inman, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 35
  • DOI: 10.1073/pnas.0901269106

An MT1-MMP-PDGF receptor-  axis regulates mural cell investment of the microvasculature
journal, April 2005


Freeze substitution in 3 hours or less: FREEZE SUBSTIUTION IN 3 HOURS OR LESS
journal, August 2011


Hnrpab regulates neural development and neuron cell survival after glutamate stimulation
journal, February 2012


DTASelect and Contrast:  Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002

  • Tabb, David L.; McDonald, W. Hayes; Yates, John R.
  • Journal of Proteome Research, Vol. 1, Issue 1, p. 21-26
  • DOI: 10.1021/pr015504q

A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy
journal, February 2008

  • Lee, I. H.; Cao, L.; Mostoslavsky, R.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 9
  • DOI: 10.1073/pnas.0712145105

An MT1-MMP-PDGF receptor-  axis regulates mural cell investment of the microvasculature
journal, April 2005


?-enolase deficiency, a new metabolic myopathy of distal glycolysis
journal, January 2001

  • Comi, Giacomo P.; Fortunato, Francesco; Lucchiari, Sabrina
  • Annals of Neurology, Vol. 50, Issue 2
  • DOI: 10.1002/ana.1095

MT1-MMP promotes vascular smooth muscle dedifferentiation through LRP1 processing
journal, December 2008

  • Lehti, K.; Rose, N. F.; Valavaara, S.
  • Journal of Cell Science, Vol. 122, Issue 1
  • DOI: 10.1242/jcs.035279

Identification of a mutation in liver glycogen phosphorylase in glycogen storage disease type VI
journal, May 1998


Membrane-type 1 matrix metalloproteinase and cell migration
journal, September 2003

  • Seiki, Motoharu; Mori, Hidetoshi; Kajita, Masahiro
  • Biochemical Society Symposia, Vol. 70
  • DOI: 10.1042/bss0700253

A proteomic approach to identify substrates of matrix metalloproteinase-14 in human plasma
journal, October 2004

  • Hwang, In Kwan; Park, Sung Min; Kim, Se Yeon
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1702, Issue 1
  • DOI: 10.1016/j.bbapap.2004.08.001

Genetic Link Between Obesity and MMP14-Dependent Adipogenic Collagen Turnover
journal, July 2010

  • Chun, T. -H.; Inoue, M.; Morisaki, H.
  • Diabetes, Vol. 59, Issue 10
  • DOI: 10.2337/db10-0073

Mass spectrometry imaging for in situ kinetic histochemistry
journal, April 2013

  • Louie, Katherine B.; Bowen, Benjamin P.; McAlhany, Stephanie
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep01656

Validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy
journal, March 2006

  • Overall, Christopher M.; Kleifeld, Oded
  • Nature Reviews Cancer, Vol. 6, Issue 3
  • DOI: 10.1038/nrc1821

A Rapid Method of Total Lipid Extraction and Purification
journal, August 1959

  • Bligh, E. G.; Dyer, W. J.
  • Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 8
  • DOI: 10.1139/o59-099

Efecto de la suplementación con grasas protegidas sobre parámetros productivos y reproductivos en vacas lactantes
journal, September 2013

  • Duque Q., Mónica; Rosero N., Ricardo; Gallo, Jorge
  • Revista MVZ Córdoba, Vol. 18, Issue 3
  • DOI: 10.21897/rmvz.152

Sexually Dimorphic Diet-Induced Insulin Resistance in Obese Tissue Inhibitor of Metalloproteinase-2 (TIMP-2)-Deficient Mice
journal, April 2011

  • Jaworski, Diane M.; Sideleva, Olga; Stradecki, Holly M.
  • Endocrinology, Vol. 152, Issue 4
  • DOI: 10.1210/en.2010-1029

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journal, September 2017


Pathobiology of the 129:Stat1 −/− mouse model of human age-related ER-positive breast cancer with an immune infiltrate-excluded phenotype
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The Expanding Role of MT1-MMP in Cancer Progression
journal, May 2019

  • Knapinska, Anna M.; Fields, Gregg B.
  • Pharmaceuticals, Vol. 12, Issue 2
  • DOI: 10.3390/ph12020077

Dual functions of ARP101 in targeting membrane type-1 matrix metalloproteinase: Impact on U87 glioblastoma cell invasion and autophagy signaling
journal, October 2018

  • Desjarlais, Michel; Annabi, Borhane
  • Chemical Biology & Drug Design, Vol. 93, Issue 3
  • DOI: 10.1111/cbdd.13410

The Expanding Role of MT1-MMP in Cancer Progression
journal, May 2019

  • Knapinska, Anna M.; Fields, Gregg B.
  • Pharmaceuticals, Vol. 12, Issue 2
  • DOI: 10.3390/ph12020077

Beyond EGFR inhibition: multilateral combat strategies to stop the progression of head and neck cancer
journal, January 2019

  • Byeon, Hyung Kwon; Ku, Minhee; Yang, Jaemoon
  • Experimental & Molecular Medicine, Vol. 51, Issue 1
  • DOI: 10.1038/s12276-018-0202-2

Beyond EGFR inhibition: multilateral combat strategies to stop the progression of head and neck cancer
journal, January 2019

  • Byeon, Hyung Kwon; Ku, Minhee; Yang, Jaemoon
  • Experimental & Molecular Medicine, Vol. 51, Issue 1
  • DOI: 10.1038/s12276-018-0202-2