ACS Publications. Most Trusted. Most Cited. Most Read
Spatial Organization of Metabolic Enzyme Complexes in Cells
My Activity
    Current Topic

    Spatial Organization of Metabolic Enzyme Complexes in Cells
    Click to copy article linkArticle link copied!

    View Author Information
    Department of Chemistry and Biochemistry, University of Maryland Baltimore County (UMBC), 1000 Hilltop Circle, Baltimore, Maryland 21250, United States
    *Address: Department of Chemistry and Biochemistry, University of Maryland Baltimore County, 1000 Hilltop Circle, Chemistry 462A, Baltimore, MD 21250. E-mail: [email protected]. Tel.: (+1-410) 455-2514. Fax: (+1-410) 455-1874.
    Other Access Options

    Biochemistry

    Cite this: Biochemistry 2017, 56, 25, 3184–3196
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.biochem.7b00249
    Published June 5, 2017
    Copyright © 2017 American Chemical Society

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    The organization of metabolic multienzyme complexes has been hypothesized to benefit metabolic processes and provide a coordinated way for the cell to regulate metabolism. Historically, their existence has been supported by various in vitro techniques. However, it is only recently that the existence of metabolic complexes inside living cells has come to light to corroborate this long-standing hypothesis. Indeed, subcellular compartmentalization of metabolic enzymes appears to be widespread and highly regulated. On the other hand, it is still challenging to demonstrate the functional significance of these enzyme complexes in the context of the cellular milieu. In this review, we discuss the current understanding of metabolic enzyme complexes by primarily focusing on central carbon metabolism and closely associated metabolic pathways in a variety of organisms, as well as their regulation and functional contributions to cells.

    Copyright © 2017 American Chemical Society

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Cited By

    Click to copy section linkSection link copied!

    This article is cited by 98 publications.

    1. Jason S. Kahn, Yan Xiong, James Huang, Oleg Gang. Cascaded Enzyme Reactions over a Three-Dimensional, Wireframe DNA Origami Scaffold. JACS Au 2022, 2 (2) , 357-366. https://doi.org/10.1021/jacsau.1c00387
    2. Nicoll Zeballos, Eleftheria Diamanti, Ana I. Benítez-Mateos, Claudia Schmidt-Dannert, Fernando López-Gallego. Solid-Phase Assembly of Multienzyme Systems into Artificial Cellulosomes. Bioconjugate Chemistry 2021, 32 (9) , 1966-1972. https://doi.org/10.1021/acs.bioconjchem.1c00327
    3. Nidhi C. Dubey, Bijay P. Tripathi. Nature Inspired Multienzyme Immobilization: Strategies and Concepts. ACS Applied Bio Materials 2021, 4 (2) , 1077-1114. https://doi.org/10.1021/acsabm.0c01293
    4. Maura C. Belanger, Parastoo Anbaei, Austin F. Dunn, Andrew W.L. Kinman, Rebecca R. Pompano. Spatially Resolved Analytical Chemistry in Intact, Living Tissues. Analytical Chemistry 2020, 92 (23) , 15255-15262. https://doi.org/10.1021/acs.analchem.0c03625
    5. Tom A. Young, Vicente Martí-Centelles, Jianzhu Wang, Paul J. Lusby, Fernanda Duarte. Rationalizing the Activity of an “Artificial Diels-Alderase”: Establishing Efficient and Accurate Protocols for Calculating Supramolecular Catalysis. Journal of the American Chemical Society 2020, 142 (3) , 1300-1310. https://doi.org/10.1021/jacs.9b10302
    6. Dan Davidi, Liam M. Longo, Jagoda Jabłońska, Ron Milo, Dan S. Tawfik. A Bird’s-Eye View of Enzyme Evolution: Chemical, Physicochemical, and Physiological Considerations. Chemical Reviews 2018, 118 (18) , 8786-8797. https://doi.org/10.1021/acs.chemrev.8b00039
    7. Guoqiang Zhang, Maureen B. Quin, Claudia Schmidt-Dannert. Self-Assembling Protein Scaffold System for Easy in Vitro Coimmobilization of Biocatalytic Cascade Enzymes. ACS Catalysis 2018, 8 (6) , 5611-5620. https://doi.org/10.1021/acscatal.8b00986
    8. C. Weistuch, S. Pressé. Spatiotemporal Organization of Catalysts Driven by Enhanced Diffusion. The Journal of Physical Chemistry B 2018, 122 (21) , 5286-5290. https://doi.org/10.1021/acs.jpcb.7b06868
    9. Marcelo Perez-Pepe, Ana J. Fernández-Alvarez, Graciela L. Boccaccio. Life and Work of Stress Granules and Processing Bodies: New Insights into Their Formation and Function. Biochemistry 2018, 57 (17) , 2488-2498. https://doi.org/10.1021/acs.biochem.8b00025
    10. Hye-Won Kang, Luan Nguyen, Songon An, Minjoung Kyoung. Mechanistic insights into condensate formation of human liver-type phosphofructokinase by stochastic modeling approaches. Scientific Reports 2024, 14 (1) https://doi.org/10.1038/s41598-024-69534-w
    11. Haoming Wang, John W. Vant, Andrew Zhang, Richard G. Sanchez, Youjun Wu, Mary L. Micou, Vincent Luczak, Zachary Whiddon, Natasha M. Carlson, Seungyoon B. Yu, Mirna Jabbo, Seokjun Yoon, Ahmed A. Abushawish, Majid Ghassemian, Takeya Masubuchi, Quan Gan, Shigeki Watanabe, Eric R. Griffis, Marc Hammarlund, Abhishek Singharoy, Gulcin Pekkurnaz. Organization of a functional glycolytic metabolon on mitochondria for metabolic efficiency. Nature Metabolism 2024, 6 (9) , 1712-1735. https://doi.org/10.1038/s42255-024-01121-9
    12. Jessica Lusty Beech, Anjani K. Maurya, Ronivaldo Rodrigues da Silva, Emmanuel Akpoto, Arun Asundi, Julia Ann Fecko, Neela H. Yennawar, Ritimukta Sarangi, Christopher Tassone, Thomas M. Weiss, Jennifer L. DuBois. Understanding the stability of a plastic‐degrading Rieske iron oxidoreductase system. Protein Science 2024, 33 (6) https://doi.org/10.1002/pro.4997
    13. Niladri Sekhar Mandal, Ayusman Sen, R. Dean Astumian. A molecular origin of non-reciprocal interactions between interacting active catalysts. Chem 2024, 10 (4) , 1147-1159. https://doi.org/10.1016/j.chempr.2023.11.017
    14. Ajita Paliwal, Vartika Paliwal, Smita Jain, Sarvesh Paliwal, Swapnil Sharma. Current Insight on the Role of Glucokinase and Glucokinase Regulatory Protein in Diabetes. Mini-Reviews in Medicinal Chemistry 2024, 24 (7) , 674-688. https://doi.org/10.2174/1389557523666230823151927
    15. Hratch M. Baghdassarian, Nathan E. Lewis. Resource allocation in mammalian systems. Biotechnology Advances 2024, 71 , 108305. https://doi.org/10.1016/j.biotechadv.2023.108305
    16. Drew Wilfahrt, Greg M. Delgoffe. Metabolic waypoints during T cell differentiation. Nature Immunology 2024, 25 (2) , 206-217. https://doi.org/10.1038/s41590-023-01733-5
    17. Naoki Ikari, Katsuko Honjo, Yoko Sagami, Yasuyuki Nakamura, Hirofumi Arakawa. Mieap forms membrane-less organelles involved in cardiolipin metabolism. iScience 2024, 27 (2) , 108916. https://doi.org/10.1016/j.isci.2024.108916
    18. Melissa Campos, Lauren V. Albrecht. Hitting the Sweet Spot: How Glucose Metabolism Is Orchestrated in Space and Time by Phosphofructokinase-1. Cancers 2024, 16 (1) , 16. https://doi.org/10.3390/cancers16010016
    19. Yunlu Jia, Yi Huang, Jin Ma, Shangwei Zhang, Jin Liu, Tianli Li, Lirong Song. Toxicity of the disinfectant benzalkonium chloride (C14) towards cyanobacterium Microcystis results from its impact on the photosynthetic apparatus and cell metabolism. Journal of Environmental Sciences 2024, 135 , 198-209. https://doi.org/10.1016/j.jes.2022.11.007
    20. Eiichiro Ono, Jun Murata. Exploring the Evolvability of Plant Specialized Metabolism: Uniqueness Out Of Uniformity and Uniqueness Behind Uniformity. Plant And Cell Physiology 2023, 64 (12) , 1449-1465. https://doi.org/10.1093/pcp/pcad057
    21. Tomoto Ura, Ako Kagawa, Nanako Sakakibara, Hiromasa Yagi, Naoya Tochio, Takanori Kigawa, Kentaro Shiraki, Tsutomu Mikawa. Activation of L-lactate oxidase by the formation of enzyme assemblies through liquid–liquid phase separation. Scientific Reports 2023, 13 (1) https://doi.org/10.1038/s41598-023-28040-1
    22. Joyce C. Breger, James N. Vranish, Eunkeu Oh, Michael H. Stewart, Kimihiro Susumu, Guillermo Lasarte-Aragonés, Gregory A. Ellis, Scott A. Walper, Sebastián A. Díaz, Shelby L. Hooe, William P. Klein, Meghna Thakur, Mario G. Ancona, Igor L. Medintz. Self assembling nanoparticle enzyme clusters provide access to substrate channeling in multienzymatic cascades. Nature Communications 2023, 14 (1) https://doi.org/10.1038/s41467-023-37255-9
    23. Jiuwang Yu, Hongwei Yuan, Jiarong Guo, Zhiheng Dong, Sha Li, Quan Fu, Bilige Aode, Sachula Baoyin, Lidao Bao, Lan Wu. Combining multi‐omics analysis to identify host‐targeted targets for the control of Brucella infection. Microbial Biotechnology 2023, 16 (12) , 2345-2366. https://doi.org/10.1111/1751-7915.14307
    24. Leila T. Alexander, Janani Durairaj, Andriy Kryshtafovych, Luciano A. Abriata, Yusupha Bayo, Gira Bhabha, Cécile Breyton, Simon G. Caulton, James Chen, Séraphine Degroux, Damian C. Ekiert, Benedikte S. Erlandsen, Peter L. Freddolino, Dominic Gilzer, Chris Greening, Jonathan M. Grimes, Rhys Grinter, Manickam Gurusaran, Marcus D. Hartmann, Charlie J. Hitchman, Jeremy R. Keown, Ashleigh Kropp, Petri Kursula, Andrew L. Lovering, Bruno Lemaitre, Andrea Lia, Shiheng Liu, Maria Logotheti, Shuze Lu, Sigurbjörn Markússon, Mitchell D. Miller, George Minasov, Hartmut H. Niemann, Felipe Opazo, George N. Phillips, Owen R. Davies, Samuel Rommelaere, Monica Rosas‐Lemus, Pietro Roversi, Karla Satchell, Nathan Smith, Mark A. Wilson, Kuan‐Lin Wu, Xian Xia, Han Xiao, Wenhua Zhang, Z. Hong Zhou, Krzysztof Fidelis, Maya Topf, John Moult, Torsten Schwede. Protein target highlights in CASP15 : Analysis of models by structure providers. Proteins: Structure, Function, and Bioinformatics 2023, 91 (12) , 1571-1599. https://doi.org/10.1002/prot.26545
    25. Rémy Cochereau, Viviana Maffeis, Elena C. dos Santos, Emanuel Lörtscher, Cornelia G. Palivan. Polymeric Giant Unilamellar Vesicles with Integrated DNA‐Origami Nanopores: An Efficient Platform for Tuning Bioreaction Dynamics Through Controlled Molecular Diffusion. Advanced Functional Materials 2023, 33 (48) https://doi.org/10.1002/adfm.202304782
    26. Danielle L. Schmitt, Patricia Dranchak, Prakash Parajuli, Dvir Blivis, Ty Voss, Casey L. Kohnhorst, Minjoung Kyoung, James Inglese, Songon An, . High-throughput screening identifies cell cycle-associated signaling cascades that regulate a multienzyme glucosome assembly in human cells. PLOS ONE 2023, 18 (8) , e0289707. https://doi.org/10.1371/journal.pone.0289707
    27. Boyi Gan. The pyrimidinosome: Orchestrating pyrimidine biosynthesis and ferroptosis defense. Molecular Cell 2023, 83 (16) , 2837-2839. https://doi.org/10.1016/j.molcel.2023.07.013
    28. Matthew J. Binder, Anthony M. Pedley. The roles of molecular chaperones in regulating cell metabolism. FEBS Letters 2023, 597 (13) , 1681-1701. https://doi.org/10.1002/1873-3468.14682
    29. Ling Li, Shihong Nie, Ting Du, Jiaxuan Zhao, Xiaoyuan Chen. DNA origami technology for biomedical applications: Challenges and opportunities. MedComm – Biomaterials and Applications 2023, 2 (2) https://doi.org/10.1002/mba2.37
    30. Peter W. Stacpoole, Charles E. McCall. The pyruvate dehydrogenase complex: Life’s essential, vulnerable and druggable energy homeostat. Mitochondrion 2023, 70 , 59-102. https://doi.org/10.1016/j.mito.2023.02.007
    31. Ryotaro Utsumi, Yuki Murata, Sayoko Ito-Harashima, Misaki Akai, Natsuko Miura, Kouichi Kuroda, Mitsuyoshi Ueda, Michihiko Kataoka, . Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies. PLOS ONE 2023, 18 (4) , e0283002. https://doi.org/10.1371/journal.pone.0283002
    32. Encarnación Medina-Carmona, Luis I Gutierrez-Rus, Fadia Manssour-Triedo, Matilda S Newton, Gloria Gamiz-Arco, Antonio J Mota, Pablo Reiné, Juan Manuel Cuerva, Mariano Ortega-Muñoz, Eduardo Andrés-León, Jose Luis Ortega-Roldan, Burckhard Seelig, Beatriz Ibarra-Molero, Jose M Sanchez-Ruiz, . Cell Survival Enabled by Leakage of a Labile Metabolic Intermediate. Molecular Biology and Evolution 2023, 40 (3) https://doi.org/10.1093/molbev/msad032
    33. Rikki M. Garner, Arthur T. Molines, Julie A. Theriot, Fred Chang. Vast heterogeneity in cytoplasmic diffusion rates revealed by nanorheology and Doppelgänger simulations. Biophysical Journal 2023, 122 (5) , 767-783. https://doi.org/10.1016/j.bpj.2023.01.040
    34. Hirofumi Arakawa. MLOs and control of metabolic pathways. 2023, 431-446. https://doi.org/10.1016/B978-0-12-823967-4.00023-3
    35. April L. Darling, Vladimir N. Uversky. Known types of membrane-less organelles and biomolecular condensates. 2023, 271-335. https://doi.org/10.1016/B978-0-12-823967-4.00002-6
    36. Jinmei Wang, Yuan Lu, Pengpeng Cheng, Chuyue Zhang, Lan Tang, Lihua Du, Jinghua Li, Zhimin Ou. Construction of Bi-Enzyme Self-Assembly Clusters Based on SpyCatcher/SpyTag for the Efficient Biosynthesis of (R)-Ethyl 2-hydroxy-4-phenylbutyrate. Biomolecules 2023, 13 (1) , 91. https://doi.org/10.3390/biom13010091
    37. Saima Akhter, Asif Ahmed Sami, Tamanna Islam Toma, Bushrat Jahan, Tahmina Islam. Caffeoyl-CoA 3-O-methyltransferase gene family in jute: Genome-wide identification, evolutionary progression and transcript profiling under different quandaries. Frontiers in Plant Science 2022, 13 https://doi.org/10.3389/fpls.2022.1035383
    38. Isreal Moreno, Irene Rodríguez-Sánchez, Xenia Schafer, Joshua Munger. Human cytomegalovirus induces neuronal enolase to support virally mediated metabolic remodeling. Proceedings of the National Academy of Sciences 2022, 119 (49) https://doi.org/10.1073/pnas.2205789119
    39. Giovanni Giunta, Filipe Tostevin, Sorin Tănase-Nicola, Ulrich Gerland. Optimal spatial allocation of enzymes as an investment problem. Communications Physics 2022, 5 (1) https://doi.org/10.1038/s42005-022-01097-6
    40. Yue Liao, Xia Wang, Hongdou Shen, Ziyang Tai, Qigang Wang. Dynamic assembly and biocatalysis-selected gelation endow self-compartmentalized multienzyme superactivity. Science China Chemistry 2022, 65 (10) , 1985-1993. https://doi.org/10.1007/s11426-022-1330-y
    41. Peng Lin, Hui Yang, Eiji Nakata, Takashi Morii. Mechanistic Aspects for the Modulation of Enzyme Reactions on the DNA Scaffold. Molecules 2022, 27 (19) , 6309. https://doi.org/10.3390/molecules27196309
    42. Jessica Ciesla, Isreal Moreno, Joshua Munger, . TNFα-induced metabolic reprogramming drives an intrinsic anti-viral state. PLOS Pathogens 2022, 18 (7) , e1010722. https://doi.org/10.1371/journal.ppat.1010722
    43. Howard R. Petty. Enzyme trafficking and coclustering precede and accurately predict human breast cancer recurrences: an interdisciplinary review. American Journal of Physiology-Cell Physiology 2022, 322 (5) , C991-C1010. https://doi.org/10.1152/ajpcell.00042.2022
    44. Florian Hinzpeter, Filipe Tostevin, Alexander Buchner, Ulrich Gerland. Trade-offs and design principles in the spatial organization of catalytic particles. Nature Physics 2022, 18 (2) , 203-211. https://doi.org/10.1038/s41567-021-01444-4
    45. Maryam Omidvar, Jakub Zdarta, Sigyn Björk Sigurdardóttir, Manuel Pinelo. Mimicking natural strategies to create multi-environment enzymatic reactors: From natural cell compartments to artificial polyelectrolyte reactors. Biotechnology Advances 2022, 54 , 107798. https://doi.org/10.1016/j.biotechadv.2021.107798
    46. Matthew J. Thomas, Emma R. Cassidy, Devin S. Robinson, Katherine M. Walstrom. Kinetic characterization and thermostability of C. elegans cytoplasmic and mitochondrial malate dehydrogenases. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2022, 1870 (1) , 140722. https://doi.org/10.1016/j.bbapap.2021.140722
    47. Svyatoslav Kondrat, Eric von Lieres. Mechanisms and Effects of Substrate Channelling in Enzymatic Cascades. 2022, 27-50. https://doi.org/10.1007/978-1-0716-2269-8_3
    48. Songon An, Prakash Parajuli, Erin L. Kennedy, Minjoung Kyoung. Multi-dimensional Fluorescence Live-Cell Imaging for Glucosome Dynamics in Living Human Cells. 2022, 15-26. https://doi.org/10.1007/978-1-0716-2269-8_2
    49. Kelly Wallin, Ruijie Zhang, Claudia Schmidt-Dannert. Programmable Self-Assembling Protein Nanomaterials: Current Status and Prospects. 2022, 51-94. https://doi.org/10.1007/978-3-030-92949-7_3
    50. Svyatoslav Kondrat, Ulrich Krauss, Eric von Lieres. Enzyme co-localisation: Mechanisms and benefits. Current Research in Chemical Biology 2022, 2 , 100031. https://doi.org/10.1016/j.crchbi.2022.100031
    51. Giorgio Morello, Clare F. Megarity, Fraser A. Armstrong. The power of electrified nanoconfinement for energising, controlling and observing long enzyme cascades. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-020-20403-w
    52. Tomoto Ura, Shunsuke Tomita, Kentaro Shiraki. Dynamic behavior of liquid droplets with enzyme compartmentalization triggered by sequential glycolytic enzyme reactions. Chemical Communications 2021, 57 (93) , 12544-12547. https://doi.org/10.1039/D1CC04596B
    53. M. Nieves Calvo-Vidal, Nahuel Zamponi, Jan Krumsiek, Max A. Stockslager, Maria V. Revuelta, Jude M. Phillip, Rossella Marullo, Ekaterina Tikhonova, Nikita Kotlov, Jayeshkumar Patel, Shao Ning Yang, Lucy Yang, Tony Taldone, Catherine Thieblemont, John P. Leonard, Peter Martin, Giorgio Inghirami, Gabriela Chiosis, Scott R. Manalis, Leandro Cerchietti. Oncogenic HSP90 Facilitates Metabolic Alterations in Aggressive B-cell Lymphomas. Cancer Research 2021, 81 (20) , 5202-5216. https://doi.org/10.1158/0008-5472.CAN-21-2734
    54. Jason Z. Zhang, Sohum Mehta, Jin Zhang. Liquid–liquid phase separation: a principal organizer of the cell’s biochemical activity architecture. Trends in Pharmacological Sciences 2021, 42 (10) , 845-856. https://doi.org/10.1016/j.tips.2021.07.003
    55. Richard A. Cheung, Alexandra M. Kraft, Howard R. Petty. Relocation of phosphofructokinases within epithelial cells is a novel event preceding breast cancer recurrence that accurately predicts patient outcomes. American Journal of Physiology-Cell Physiology 2021, 321 (4) , C654-C670. https://doi.org/10.1152/ajpcell.00176.2021
    56. Katarina Akhmetova, Maxim Balasov, Igor Chesnokov. Drosophila STING protein has a role in lipid metabolism. eLife 2021, 10 https://doi.org/10.7554/eLife.67358
    57. Vidhi Pareek, Zhou Sha, Jingxuan He, Ned S. Wingreen, Stephen J. Benkovic. Metabolic channeling: predictions, deductions, and evidence. Molecular Cell 2021, 81 (18) , 3775-3785. https://doi.org/10.1016/j.molcel.2021.08.030
    58. Rodrigo Caetano, Yaroslav Ispolatov, Michael Doebeli. Evolution of diversity in metabolic strategies. eLife 2021, 10 https://doi.org/10.7554/eLife.67764
    59. Yuki Yoshimura, Reina Hirayama, Natsuko Miura, Ryotaro Utsumi, Kouichi Kuroda, Mitsuyoshi Ueda, Michihiko Kataoka. Small‐scale hypoxic cultures for monitoring the spatial reorganization of glycolytic enzymes in Saccharomyces cerevisiae. Cell Biology International 2021, 45 (8) , 1776-1783. https://doi.org/10.1002/cbin.11617
    60. SoRi Jang, Zhao Xuan, Ross C. Lagoy, Louise M. Jawerth, Ian J. Gonzalez, Milind Singh, Shavanie Prashad, Hee Soo Kim, Avinash Patel, Dirk R. Albrecht, Anthony A. Hyman, Daniel A. Colón-Ramos. Phosphofructokinase relocalizes into subcellular compartments with liquid-like properties in vivo. Biophysical Journal 2021, 120 (7) , 1170-1186. https://doi.org/10.1016/j.bpj.2020.08.002
    61. Nantaporn Haskins, Shivaprasad Bhuvanendran, Claudio Anselmi, Anna Gams, Tomas Kanholm, Kristen M. Kocher, Jonathan LoTempio, Kylie I. Krohmaly, Danielle Sohai, Nathaniel Stearrett, Erin Bonner, Mendel Tuchman, Hiroki Morizono, Jyoti K. Jaiswal, Ljubica Caldovic. Mitochondrial Enzymes of the Urea Cycle Cluster at the Inner Mitochondrial Membrane. Frontiers in Physiology 2021, 11 https://doi.org/10.3389/fphys.2020.542950
    62. Vidhi Pareek, Anthony M. Pedley, Stephen J. Benkovic. Human de novo purine biosynthesis. Critical Reviews in Biochemistry and Molecular Biology 2021, 56 (1) , 1-16. https://doi.org/10.1080/10409238.2020.1832438
    63. Shi-Jia Lin, Ya-Zhuo Yang, Rui-Min Teng, Hao Liu, Hui Li, Jing Zhuang. Identification and expression analysis of caffeoyl-coenzyme A O-methyltransferase family genes related to lignin biosynthesis in tea plant (Camellia sinensis). Protoplasma 2021, 258 (1) , 115-127. https://doi.org/10.1007/s00709-020-01555-4
    64. Siddhartha Roy, Tapas K. Kundu. An integrative view of chemical biology. 2021, 1-26. https://doi.org/10.1016/B978-0-12-817644-3.00004-0
    65. Kristopher Montrose, Rosa María López Cabezas, Jurgita Paukštytė, Juha Saarikangas. Winter is coming: Regulation of cellular metabolism by enzyme polymerization in dormancy and disease. Experimental Cell Research 2020, 397 (2) , 112383. https://doi.org/10.1016/j.yexcr.2020.112383
    66. Tobias Wunder, Oliver Mueller-Cajar. Biomolecular condensates in photosynthesis and metabolism. Current Opinion in Plant Biology 2020, 58 , 1-7. https://doi.org/10.1016/j.pbi.2020.08.006
    67. A. Gacek-Matthews, Z. Chromiková, M. Sulyok, G. Lücking, I. Barák, M. Ehling-Schulz, . Beyond Toxin Transport: Novel Role of ABC Transporter for Enzymatic Machinery of Cereulide NRPS Assembly Line. mBio 2020, 11 (5) https://doi.org/10.1128/mBio.01577-20
    68. Joshua B. McCluskey, Douglas S. Clark, Dominic J. Glover. Functional Applications of Nucleic Acid–Protein Hybrid Nanostructures. Trends in Biotechnology 2020, 38 (9) , 976-989. https://doi.org/10.1016/j.tibtech.2020.02.007
    69. Cyrielle Doigneaux, Anthony M. Pedley, Ishna N. Mistry, Monika Papayova, Stephen J. Benkovic, Ali Tavassoli. Hypoxia drives the assembly of the multienzyme purinosome complex. Journal of Biological Chemistry 2020, 295 (28) , 9551-9566. https://doi.org/10.1074/jbc.RA119.012175
    70. Maria Wittmiß, Stefan Mikkat, Martin Hagemann, Hermann Bauwe. Stoichiometry of two plant glycine decarboxylase complexes and comparison with a cyanobacterial glycine cleavage system. The Plant Journal 2020, 103 (2) , 801-813. https://doi.org/10.1111/tpj.14773
    71. Theodore Alexandrov. Probing metabolism in time and space. Science 2020, 368 (6488) , 241-242. https://doi.org/10.1126/science.abb3094
    72. Isabelle J. Schalk, Coraline Rigouin, Julien Godet. An overview of siderophore biosynthesis among fluorescent Pseudomonads and new insights into their complex cellular organization. Environmental Microbiology 2020, 22 (4) , 1447-1466. https://doi.org/10.1111/1462-2920.14937
    73. Christina Wege, Claudia Koch. From stars to stripes: RNA‐directed shaping of plant viral protein templates—structural synthetic virology for smart biohybrid nanostructures. WIREs Nanomedicine and Nanobiotechnology 2020, 12 (2) https://doi.org/10.1002/wnan.1591
    74. Aditi Singhal, Kriti Kapil, Ankit Dodla, Sanjay Kumar, Bhaskar Datta. Nucleic Acid Based Nanoconstructs for Environmental Analysis in Atypical Contexts. 2020, 577-596. https://doi.org/10.1007/978-3-030-33774-2_25
    75. E. Espinoza-Simón, N. Chiquete-Félix, L. Morales-García, U. Pedroza-Dávila, X. Pérez-Martínez, D. Araiza-Olivera, F. Torres-Quiroz, S. Uribe-Carvajal. In Saccharomyces cerevisiae, withdrawal of the carbon source results in detachment of glycolytic enzymes from the cytoskeleton and in actin reorganization. Fungal Biology 2020, 124 (1) , 15-23. https://doi.org/10.1016/j.funbio.2019.10.005
    76. Mislav Oreb. Construction of artificial membrane transport metabolons – an emerging strategy in metabolic engineering. FEMS Microbiology Letters 2020, 367 (1) https://doi.org/10.1093/femsle/fnaa027
    77. Véronique Gasser, Morgane Malrieu, Anne Forster, Yves Mély, Isabelle J. Schalk, Julien Godet. In cellulo FRET-FLIM and single molecule tracking reveal the supra-molecular organization of the pyoverdine bio-synthetic enzymes in Pseudomonas aeruginosa. Quarterly Reviews of Biophysics 2020, 53 https://doi.org/10.1017/S0033583519000155
    78. Alexandra Zaharia, Bernard Labedan, Christine Froidevaux, Alain Denise. CoMetGeNe: mining conserved neighborhood patterns in metabolic and genomic contexts. BMC Bioinformatics 2019, 20 (1) https://doi.org/10.1186/s12859-018-2542-2
    79. Yuanyuan Wang, Changsen Bai, Yuxia Ruan, Miao Liu, Qiaoyun Chu, Li Qiu, Chuanzhen Yang, Binghui Li. Coordinative metabolism of glutamine carbon and nitrogen in proliferating cancer cells under hypoxia. Nature Communications 2019, 10 (1) https://doi.org/10.1038/s41467-018-08033-9
    80. Andrij Kuzmak, Sheiliza Carmali, Eric von Lieres, Alan J. Russell, Svyatoslav Kondrat. Can enzyme proximity accelerate cascade reactions?. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-018-37034-3
    81. Daniela Pontiggia, Francesco Spinelli, Claudia Fabbri, Valerio Licursi, Rodolfo Negri, Giulia De Lorenzo, Benedetta Mattei. Changes in the microsomal proteome of tomato fruit during ripening. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-50575-5
    82. Nadja A. Henke, Volker F. Wendisch. Improved Astaxanthin Production with Corynebacterium glutamicum by Application of a Membrane Fusion Protein. Marine Drugs 2019, 17 (11) , 621. https://doi.org/10.3390/md17110621
    83. Suzy Bulot, Stéphane Audebert, Laetitia Pieulle, Farida Seduk, Emilie Baudelet, Leon Espinosa, Marie-Camille Pizay, Luc Camoin, Axel Magalon, . Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in Escherichia coli. mBio 2019, 10 (5) https://doi.org/10.1128/mBio.01832-19
    84. Federica Mura, Grzegorz Gradziuk, Chase P. Broedersz. Mesoscopic non-equilibrium measures can reveal intrinsic features of the active driving. Soft Matter 2019, 15 (40) , 8067-8076. https://doi.org/10.1039/C9SM01169B
    85. Florian Hinzpeter, Filipe Tostevin, Ulrich Gerland. Regulation of reaction fluxes via enzyme sequestration and co-clustering. Journal of The Royal Society Interface 2019, 16 (156) , 20190444. https://doi.org/10.1098/rsif.2019.0444
    86. Hery Rabeharindranto, Sara Castaño-Cerezo, Thomas Lautier, Luis F. Garcia-Alles, Christian Treitz, Andreas Tholey, Gilles Truan. Enzyme-fusion strategies for redirecting and improving carotenoid synthesis in S. cerevisiae. Metabolic Engineering Communications 2019, 8 , e00086. https://doi.org/10.1016/j.mec.2019.e00086
    87. Geng-Min Lin, Robert Warden-Rothman, Christopher A. Voigt. Retrosynthetic design of metabolic pathways to chemicals not found in nature. Current Opinion in Systems Biology 2019, 14 , 82-107. https://doi.org/10.1016/j.coisb.2019.04.004
    88. Claudia Schmid-Dannert, Fernando López-Gallego. Advances and opportunities for the design of self-sufficient and spatially organized cell-free biocatalytic systems. Current Opinion in Chemical Biology 2019, 49 , 97-104. https://doi.org/10.1016/j.cbpa.2018.11.021
    89. Shawn M. Sternisha, Brian G. Miller. Molecular and cellular regulation of human glucokinase. Archives of Biochemistry and Biophysics 2019, 663 , 199-213. https://doi.org/10.1016/j.abb.2019.01.011
    90. Stefan Klumpp, William Bode, Palka Puri. Life in crowded conditions. The European Physical Journal Special Topics 2019, 227 (15-16) , 2315-2328. https://doi.org/10.1140/epjst/e2018-800088-6
    91. Fernando López-Gallego. On-pot and cell-free biocatalysis using coimmobilized enzymes on advanced materials. 2019, 385-411. https://doi.org/10.1016/bs.mie.2018.12.013
    92. Guoqiang Zhang, Sarah Schmidt-Dannert, Maureen B. Quin, Claudia Schmidt-Dannert. Protein-based scaffolds for enzyme immobilization. 2019, 323-362. https://doi.org/10.1016/bs.mie.2018.12.016
    93. Songon An, Miji Jeon, Erin L. Kennedy, Minjoung Kyoung. Phase-separated condensates of metabolic complexes in living cells: Purinosome and glucosome. 2019, 1-17. https://doi.org/10.1016/bs.mie.2019.06.013
    94. Lee J. Sweetlove, Alisdair R. Fernie. The role of dynamic enzyme assemblies and substrate channelling in metabolic regulation. Nature Communications 2018, 9 (1) https://doi.org/10.1038/s41467-018-04543-8
    95. Miji Jeon, Hye-Won Kang, Songon An. A Mathematical Model for Enzyme Clustering in Glucose Metabolism. Scientific Reports 2018, 8 (1) https://doi.org/10.1038/s41598-018-20348-7
    96. Panagiotis L. Kastritis, Anne-Claude Gavin. Enzymatic complexes across scales. Essays in Biochemistry 2018, 62 (4) , 501-514. https://doi.org/10.1042/EBC20180008
    97. Gillian Fitzgerald, Inés Soro-Arnaiz, Katrien De Bock. The Warburg Effect in Endothelial Cells and its Potential as an Anti-angiogenic Target in Cancer. Frontiers in Cell and Developmental Biology 2018, 6 https://doi.org/10.3389/fcell.2018.00100
    98. Danielle L. Schmitt, Anand Sundaram, Miji Jeon, Bao Tran Luu, Songon An, . Spatial alterations of De Novo purine biosynthetic enzymes by Akt-independent PDK1 signaling pathways. PLOS ONE 2018, 13 (4) , e0195989. https://doi.org/10.1371/journal.pone.0195989

    Biochemistry

    Cite this: Biochemistry 2017, 56, 25, 3184–3196
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.biochem.7b00249
    Published June 5, 2017
    Copyright © 2017 American Chemical Society

    Article Views

    3047

    Altmetric

    -

    Citations

    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.