Regulation of MicroRNA Machinery and Development by Interspecies S-Nitrosylation

被引:67
作者
Seth, Puneet [1 ,2 ,3 ]
Hsieh, Paishiun N. [4 ,5 ,6 ]
Jamal, Suhib [1 ,2 ,3 ]
Wang, Liwen [7 ]
Gygi, Steven P. [8 ]
Jain, Mukesh K. [4 ,5 ,9 ]
Coller, Jeff [10 ]
Stamler, Jonathan S. [1 ,2 ,3 ,9 ]
机构
[1] Case Western Reserve Univ, Sch Med, Inst Transformat Mol Med, Cleveland, OH 44106 USA
[2] Case Western Reserve Univ, Sch Med, Dept Med, Cleveland, OH 44106 USA
[3] Univ Hosp Cleveland, Med Ctr, Cleveland, OH 44106 USA
[4] Case Western Reserve Univ, Dept Med, Case Cardiovasc Res Inst, 10900 Euclid Ave, Cleveland, OH 44106 USA
[5] Univ Hosp Cleveland, Med Ctr, Harrington Heart & Vasc Inst, 2103 Cornell Rd, Cleveland, OH 44106 USA
[6] Case Western Reserve Univ, Dept Pathol, 10900 Euclid Ave, Cleveland, OH 44106 USA
[7] Case Western Reserve Univ, Sch Med, Ctr Prote & Bioinformat, Cleveland, OH 44106 USA
[8] Harvard Med Sch, Dept Cell Biol, Boston, MA 02115 USA
[9] Univ Hosp Cleveland, Med Ctr, Harrington Discovery Inst, Cleveland, OH 44106 USA
[10] Case Western Reserve Univ, Ctr RNA Sci & Therapeut, Cleveland, OH 44106 USA
关键词
NITRIC-OXIDE; CAENORHABDITIS-ELEGANS; GUT MICROBIOTA; C; ELEGANS; PROTEIN; LET-7; RNA; NITRATE; NITROSATION; PHOSPHORYLATION;
D O I
10.1016/j.cell.2019.01.037
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Bioactive molecules can pass between microbiota and host to influence host cellular functions. However, general principles of interspecies communication have not been discovered. We show here in C. elegans that nitric oxide derived from resident bacteria promotes widespread S-nitrosylation of the host proteome. We further show that microbiota-dependent S-nitrosylation of C. elegans Argonaute protein (ALG-1)-at a site conserved and S-nitrosylated in mammalian Argonaute 2 (AGO2)-alters its function in controlling gene expression via microRNAs. By selectively eliminating nitric oxide generation by the microbiota or S-nitrosylation in ALG-1, we reveal unforeseen effects on host development. Thus, the microbiota can shape the post-translational landscape of the host proteome to regulate microRNA activity, gene expression, and host development. Our findings suggest a general mechanism by which the microbiota may control host cellular functions, as well as a new role for gasotransmitters.
引用
收藏
页码:1014 / +
页数:24
相关论文
共 81 条
  • [1] Single-Nucleotide Variations in Cardiac Arrhythmias: Prospects for Genomics and Proteomics Based Biomarker Discovery and Diagnostics
    Abunimer, Ayman
    Smith, Krista
    Wu, Tsung-Jung
    Lam, Phuc
    Simonyan, Vahan
    Mazumder, Raja
    [J]. GENES, 2014, 5 (02): : 254 - 269
  • [2] Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis
    Adak, S
    Aulak, KS
    Stuehr, DJ
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2002, 277 (18) : 16167 - 16171
  • [3] Casein kinase II promotes target silencing by miRISC through direct phosphorylation of the DEAD-box RNA helicase CGH-1
    Alessi, Amelia F.
    Khivansara, Vishal
    Han, Ting
    Freeberg, Mallory A.
    Moresco, James J.
    Tu, Patricia G.
    Montoye, Eric
    Yates, John R., III
    Karp, Xantha
    Kim, John K.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (52) : E7213 - E7222
  • [4] Identification of S-nitroso-CoA reductases that regulate protein S-nitrosylation
    Anand, Puneet
    Hausladen, Alfred
    Wang, Ya-Juan
    Zhang, Guo-Fang
    Stomberski, Colin
    Brunengraber, Henri
    Hess, Douglas T.
    Stamler, Jonathan S.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (52) : 18572 - 18577
  • [5] Enterotypes of the human gut microbiome
    Arumugam, Manimozhiyan
    Raes, Jeroen
    Pelletier, Eric
    Le Paslier, Denis
    Yamada, Takuji
    Mende, Daniel R.
    Fernandes, Gabriel R.
    Tap, Julien
    Bruls, Thomas
    Batto, Jean-Michel
    Bertalan, Marcelo
    Borruel, Natalia
    Casellas, Francesc
    Fernandez, Leyden
    Gautier, Laurent
    Hansen, Torben
    Hattori, Masahira
    Hayashi, Tetsuya
    Kleerebezem, Michiel
    Kurokawa, Ken
    Leclerc, Marion
    Levenez, Florence
    Manichanh, Chaysavanh
    Nielsen, H. Bjorn
    Nielsen, Trine
    Pons, Nicolas
    Poulain, Julie
    Qin, Junjie
    Sicheritz-Ponten, Thomas
    Tims, Sebastian
    Torrents, David
    Ugarte, Edgardo
    Zoetendal, Erwin G.
    Wang, Jun
    Guarner, Francisco
    Pedersen, Oluf
    de Vos, Willem M.
    Brunak, Soren
    Dore, Joel
    Weissenbach, Jean
    Ehrlich, S. Dusko
    Bork, Peer
    [J]. NATURE, 2011, 473 (7346) : 174 - 180
  • [6] Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments
    Berg, Maureen
    Stenuit, Ben
    Ho, Joshua
    Wang, Andrew
    Parke, Caitlin
    Knight, Matthew
    Alvarez-Cohen, Lisa
    Shapira, Michael
    [J]. ISME JOURNAL, 2016, 10 (08) : 1998 - 2009
  • [7] The human microbiome
    Blum, Hubert E.
    [J]. ADVANCES IN MEDICAL SCIENCES, 2017, 62 (02): : 414 - 420
  • [8] Pairing beyond the Seed Supports MicroRNA Targeting Specificity
    Broughton, James P.
    Lovci, Michael T.
    Huang, Jessica L.
    Yeo, Gene W.
    Pasquinelli, Amy E.
    [J]. MOLECULAR CELL, 2016, 64 (02) : 320 - 333
  • [9] Oral Microbiome and Nitric Oxide: the Missing Link in the Management of Blood Pressure
    Bryan, Nathan S.
    Tribble, Gena
    Angelov, Nikola
    [J]. CURRENT HYPERTENSION REPORTS, 2017, 19 (04)
  • [10] Metformin Retards Aging in C. elegans by Altering Microbial Folate and Methionine Metabolism
    Cabreiro, Filipe
    Au, Catherine
    Leung, Kit-Yi
    Vergara-Irigaray, Nuria
    Cocheme, Helena M.
    Noori, Tahereh
    Weinkove, David
    Schuster, Eugene
    Greene, Nicholas D. E.
    Gems, David
    [J]. CELL, 2013, 153 (01) : 228 - 239