Cryo-EM structures demonstrate human IMPDH2 filament assembly tunes allosteric regulation

被引:63
作者
Johnson, Matthew C. [1 ]
Kollman, Justin M. [1 ]
机构
[1] Univ Washington, Dept Biochem, Seattle, WA 98195 USA
来源
ELIFE | 2020年 / 9卷
基金
美国国家卫生研究院;
关键词
INOSINE MONOPHOSPHATE DEHYDROGENASE; METABOLIC ENZYMES; CBS DOMAINS; INOSINE-5'-MONOPHOSPHATE DEHYDROGENASE; 5-MONOPHOSPHATE DEHYDROGENASE; MYCOPHENOLATE-MOFETIL; PROTEIN AGGREGATION; UP-REGULATION; EXPRESSION; PROLIFERATION;
D O I
10.7554/eLife.53243
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Inosine monophosphate dehydrogenase (IMPDH) mediates the first committed step in guanine nucleotide biosynthesis and plays important roles in cellular proliferation and the immune response. IMPDH reversibly polymerizes in cells and tissues in response to changes in metabolic demand. Self-assembly of metabolic enzymes is increasingly recognized as a general mechanism for regulating activity, typically by stabilizing specific conformations of an enzyme, but the regulatory role of IMPDH filaments has remained unclear. Here, we report a series of human IMPDH2 cryo-EM structures in both active and inactive conformations. The structures define the mechanism of filament assembly, and reveal how filament-dependent allosteric regulation of IMPDH2 makes the enzyme less sensitive to feedback inhibition, explaining why assembly occurs under physiological conditions that require expansion of guanine nucleotide pools. Tuning sensitivity to an allosteric inhibitor distinguishes IMPDH from other metabolic filaments, and highlights the diversity of regulatory outcomes that can emerge from self-assembly.
引用
收藏
页数:27
相关论文
共 86 条
[1]   PHENIX: a comprehensive Python']Python-based system for macromolecular structure solution [J].
Adams, Paul D. ;
Afonine, Pavel V. ;
Bunkoczi, Gabor ;
Chen, Vincent B. ;
Davis, Ian W. ;
Echols, Nathaniel ;
Headd, Jeffrey J. ;
Hung, Li-Wei ;
Kapral, Gary J. ;
Grosse-Kunstleve, Ralf W. ;
McCoy, Airlie J. ;
Moriarty, Nigel W. ;
Oeffner, Robert ;
Read, Randy J. ;
Richardson, David C. ;
Richardson, Jane S. ;
Terwilliger, Thomas C. ;
Zwart, Peter H. .
ACTA CRYSTALLOGRAPHICA SECTION D-STRUCTURAL BIOLOGY, 2010, 66 :213-221
[2]   New tools for the analysis and validation of cryo-EM maps and atomic models [J].
Afonine, Pavel V. ;
Klaholz, Bruno P. ;
Moriarty, Nigel W. ;
Poon, Billy K. ;
Sobolev, Oleg V. ;
Terwilliger, Thomas C. ;
Adams, Paul D. ;
Urzhumtsev, Alexandre .
ACTA CRYSTALLOGRAPHICA SECTION D-STRUCTURAL BIOLOGY, 2018, 74 :814-840
[3]   On the molecular pathology of neurodegeneration in IMPDH1-based retinitis pigmentosa [J].
Aherne, A ;
Kennan, A ;
Kenna, PF ;
McNally, N ;
Lloyd, DG ;
Alberts, IL ;
Kiang, AS ;
Humphries, MM ;
Ayuso, C ;
Engel, PC ;
Gu, JJ ;
Mitchell, BS ;
Farrar, GJ ;
Humphries, P .
HUMAN MOLECULAR GENETICS, 2004, 13 (06) :641-650
[4]   Mycophenolate mofetil and its mechanisms of action [J].
Allison, AC ;
Eugui, EM .
IMMUNOPHARMACOLOGY, 2000, 47 (2-3) :85-118
[5]   Reconstituted IMPDH polymers accommodate both catalytically active and inactive conformations [J].
Anthony, Sajitha A. ;
Burrell, Anika L. ;
Johnson, Matthew C. ;
Duong-Ly, Krisna C. ;
Kuo, Yin-Ming ;
Simonet, Jacqueline C. ;
Michener, Peter ;
Andrews, Andrew ;
Kollman, Justin M. ;
Peterson, Jeffrey R. .
MOLECULAR BIOLOGY OF THE CELL, 2017, 28 (20) :2600-2608
[6]   Metabolic regulation via enzyme filamentation [J].
Aughey, Gabriel N. ;
Liu, Ji-Long .
CRITICAL REVIEWS IN BIOCHEMISTRY AND MOLECULAR BIOLOGY, 2016, 51 (04) :282-293
[7]  
Barad BA, 2015, NAT METHODS, V12, P943, DOI [10.1038/NMETH.3541, 10.1038/nmeth.3541]
[8]   Large-scale filament formation inhibits the activity of CTP synthetase [J].
Barry, Rachael M. ;
Bitbol, Anne-Florence ;
Lorestani, Alexander ;
Charles, Emeric J. ;
Habrian, Chris H. ;
Hansen, Jesse M. ;
Li, Hsin-Jung ;
Baldwin, Enoch P. ;
Wingreen, Ned S. ;
Kollman, Justin M. ;
Gitai, Zemer .
ELIFE, 2014, 3 :1-19
[9]   The CBS Domain: A Protein Module with an Emerging Prominent Role in Regulation [J].
Baykov, Alexander A. ;
Tuorninen, Heidi K. ;
Lahti, Reijo .
ACS CHEMICAL BIOLOGY, 2011, 6 (11) :1156-1163
[10]   mTORC1 induces purine synthesis through control of the mitochondrial tetrahydrofolate cycle [J].
Ben-Sahra, Issam ;
Hoxhaj, Gerta ;
Ricoult, Stephane J. H. ;
Asara, John M. ;
Manning, Brendan D. .
SCIENCE, 2016, 351 (6274) :728-733