Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut

Lee, Shin-Hae; Park, Joung-Sun; Kim, Young-Shin; Chung, Hae-Young; Yoo, Mi-Ae

doi:10.1016/J.YEXCR.2012.01.004

Title: Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut

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Abstract

Stem cells are tightly regulated by both intrinsic and extrinsic signals as well as the extracellular matrix (ECM) for tissue homeostasis and regenerative capacity. Matrix metalloproteinases (MMPs), proteolytic enzymes, modulate the turnover of numerous substrates, including cytokine precursors, growth factors, and ECM molecules. However, the roles of MMPs in the regulation of adult stem cells are poorly understood. In the present study, we utilize the Drosophila midgut, which is an excellent model system for studying stem cell biology, to show that Mmp1 is involved in the regulation of intestinal stem cells (ISCs). The results showed that Mmp1 is expressed in the adult midgut and that its expression increases with age and with exposure to oxidative stress. Mmp1 knockdown or Timp-overexpressing flies and flies heterozygous for a viable, hypomorphic Mmp1 allele increased ISC proliferation in the gut, as shown by staining with an anti-phospho-histone H3 antibody and BrdU incorporation assays. Reduced Mmp1 levels induced intestinal hyperplasia, and the Mmp1depletion-induced ISC proliferation was rescued by the suppression of the EGFR signaling pathway, suggesting that Mmp1 regulates ISC proliferation through the EGFR signaling pathway. Furthermore, adult gut-specific knockdown and whole-animal heterozygotes of Mmp1 increased additively sensitivity to paraquat-induced oxidative stress and shortened lifespan.more »« less

Authors:

Lee, Shin-Hae; Park, Joung-Sun ^[1]; Kim, Young-Shin ^[2]; Chung, Hae-Young ^[3]; Yoo, Mi-Ae ^[1]

Department of Molecular Biology, College of Natural Science, Pusan National University, Busan 609-735 (Korea, Republic of)
Research Institute of Genetic Engineering, Pusan National University, Busan 609-735 (Korea, Republic of)
Molecular Inflammation Research Center for Aging Intervention (MRCA), College of Pharmacy, Pusan National University, Busan 609-735 (Korea, Republic of)

Publication Date:: Sat Mar 10 00:00:00 EST 2012

OSTI Identifier:: 22212319

Resource Type:: Journal Article

Journal Name:: Experimental Cell Research

Additional Journal Information:: Journal Volume: 318; Journal Issue: 5; Other Information: Copyright (c) 2012 Elsevier Science B.V., Amsterdam, The Netherlands, All rights reserved.; Country of input: International Atomic Energy Agency (IAEA); Journal ID: ISSN 0014-4827

Country of Publication:: United States

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; ANIMAL TISSUES; ANTIBODIES; CELL PROLIFERATION; DROSOPHILA; ENZYMES; GENE REGULATION; GROWTH FACTORS; HOMEOSTASIS; HYBRIDIZATION; INHIBITION; OXIDATION; STEM CELLS

Citation Formats


                    Lee, Shin-Hae, Park, Joung-Sun, Kim, Young-Shin, Chung, Hae-Young, and Yoo, Mi-Ae. Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut.  United States: N. p., 2012. 
        Web.  doi:10.1016/J.YEXCR.2012.01.004.

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                    Lee, Shin-Hae, Park, Joung-Sun, Kim, Young-Shin, Chung, Hae-Young, & Yoo, Mi-Ae. Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut.  United States.  https://doi.org/10.1016/J.YEXCR.2012.01.004

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                    Lee, Shin-Hae, Park, Joung-Sun, Kim, Young-Shin, Chung, Hae-Young, and Yoo, Mi-Ae. 2012.  
        "Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut".  United States.  https://doi.org/10.1016/J.YEXCR.2012.01.004.

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@article{osti_22212319,

  title        = {Requirement of matrix metalloproteinase-1 for intestinal homeostasis in the adult Drosophila midgut},

  author       = {Lee, Shin-Hae and Park, Joung-Sun and Kim, Young-Shin and Chung, Hae-Young and Yoo, Mi-Ae},

  abstractNote = {Stem cells are tightly regulated by both intrinsic and extrinsic signals as well as the extracellular matrix (ECM) for tissue homeostasis and regenerative capacity. Matrix metalloproteinases (MMPs), proteolytic enzymes, modulate the turnover of numerous substrates, including cytokine precursors, growth factors, and ECM molecules. However, the roles of MMPs in the regulation of adult stem cells are poorly understood. In the present study, we utilize the Drosophila midgut, which is an excellent model system for studying stem cell biology, to show that Mmp1 is involved in the regulation of intestinal stem cells (ISCs). The results showed that Mmp1 is expressed in the adult midgut and that its expression increases with age and with exposure to oxidative stress. Mmp1 knockdown or Timp-overexpressing flies and flies heterozygous for a viable, hypomorphic Mmp1 allele increased ISC proliferation in the gut, as shown by staining with an anti-phospho-histone H3 antibody and BrdU incorporation assays. Reduced Mmp1 levels induced intestinal hyperplasia, and the Mmp1depletion-induced ISC proliferation was rescued by the suppression of the EGFR signaling pathway, suggesting that Mmp1 regulates ISC proliferation through the EGFR signaling pathway. Furthermore, adult gut-specific knockdown and whole-animal heterozygotes of Mmp1 increased additively sensitivity to paraquat-induced oxidative stress and shortened lifespan. Our data suggest that Drosophila Mmp1 is involved in the regulation of ISC proliferation for maintenance of gut homeostasis. -- Highlights: Black-Right-Pointing-Pointer Mmp1 is expressed in the adult midgut. Black-Right-Pointing-Pointer Mmp1 is involved in the regulation of ISC proliferation activity. Black-Right-Pointing-Pointer Mmp1-related ISC proliferation is associated with EGFR signaling. Black-Right-Pointing-Pointer Mmp1 in the gut is required for the intestinal homeostasis and longevity.},

  doi          = {10.1016/J.YEXCR.2012.01.004},

  url          = {https://www.osti.gov/biblio/22212319},
  journal      = {Experimental Cell Research},

  issn         = {0014-4827},

  number       = 5,

  volume       = 318,

  place        = {United States},

  year         = {Sat Mar 10 00:00:00 EST 2012},

  month        = {Sat Mar 10 00:00:00 EST 2012}

}

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