The Structure of Maltooctaose-Bound Escherichia coli Branching Enzyme Suggests a Mechanism for Donor Chain Specificity
Abstract
:1. Introduction
2. Results
2.1. Overall Structure and Packing of M8-Bound EcBE
2.2. Sugar Binding in Sites I–V
2.3. Binding in Sites VIII–XII
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Crystallization and Data Collection
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Zeeman, S.C.; Delatte, T.; Messerli, G.; Umhang, M.; Stettler, M.; Mettler, T.; Streb, S.; Reinhold, H.; Kotting, O. Starch breakdown: Recent discoveries suggest distinct pathways and novel mechanisms. Funct. Plant Biol. 2007, 34, 465–473. [Google Scholar] [CrossRef] [PubMed]
- Tester, R.F.; Karkalas, J.; Qi, X. Starch—Composition, fine structure and architecture. J. Cereal Sci. 2004, 39, 151–165. [Google Scholar] [CrossRef]
- Villwock, K.; BeMiller, J.N. The Architecture, Nature, and Mystery of Starch Granules. Part 2. Starch-Starke 2022, 74. [Google Scholar] [CrossRef]
- Yoo, S.H.; Keppel, C.; Spalding, M.; Jane, J.L. Effects of growth condition on the structure of glycogen produced in cyanobacterium Synechocystis sp PCC6803. Int. J. Biol. Macromol. 2007, 40, 498–504. [Google Scholar] [CrossRef] [PubMed]
- Sawada, T.; Nakamura, Y.; Ohdan, T.; Saitoh, A.; Francisco, P.B., Jr.; Suzuki, E.; Fujita, N.; Shimonaga, T.; Fujiwara, S.; Tsuzuki, M.; et al. Diversity of reaction characteristics of glucan branching enzymes and the fine structure of alpha-glucan from various sources. Arch. Biochem. Biophys. 2014, 562, 9–21. [Google Scholar] [CrossRef]
- Wang, L.; Wise, M.J. Glycogen with short average chain length enhances bacterial durability. Naturwissenschaften 2011, 98, 719–729. [Google Scholar] [CrossRef]
- Wilson, W.A.; Roach, P.J.; Montero, M.; Baroja-Fernandez, E.; Munoz, F.J.; Eydallin, G.; Viale, A.M.; Pozueta-Romero, J. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol. Rev. 2010, 34, 952–985. [Google Scholar] [CrossRef]
- Li, R.Q.; Zheng, W.Y.; Jiang, M.; Zhang, H.L. A review of starch biosynthesis in cereal crops and its potential breeding applications in rice (Oryza Sativa L.). Peerj 2021, 9, e12678. [Google Scholar] [CrossRef]
- Diez, M.D.A.; Peiru, S.; Demonte, A.M.; Gramajo, H.; Iglesias, A.A. Characterization of Recombinant UDP- and ADP-Glucose Pyrophosphorylases and Glycogen Synthase To Elucidate Glucose-1-Phosphate Partitioning into Oligo- and Polysaccharides in Streptomyces coelicolor. J. Bacteriol. 2012, 194, 1485–1493. [Google Scholar] [CrossRef]
- Tetlow, I.J.; Emes, M.J. A Review of Starch-branching Enzymes and Their Role in Amylopectin Biosynthesis. Iubmb Life 2014, 66, 546–558. [Google Scholar] [CrossRef]
- Ebrecht, A.C.; Solamen, L.; Hill, B.L.; Iglesias, A.A.; Olsen, K.W.; Ballicora, M.A. Allosteric Control of Substrate Specificity of the Escherichia coil ADP-Glucose Pyrophosphorylase. Front. Chem. 2017, 5, 41. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Wang, M.M.; Wise, M.J.; Liu, Q.H.; Yang, T.; Zhu, Z.B.; Li, C.C.; Tan, X.L.; Tang, D.Q.; Wang, W. Recent progress in the structure of glycogen serving as a durable energy reserve in bacteria. World J. Microbiol. Biotechnol. 2020, 36, 14. [Google Scholar] [CrossRef]
- Klotz, A.; Forchhammer, K. Glycogen, a major player for bacterial survival and awakening from dormancy. Future Microbiol. 2017, 12, 101–104. [Google Scholar] [CrossRef] [PubMed]
- Wang, L. Exploring the Genetic Basis for the Sit-and-Wait Hypothesis: Abiotic Stress Resistance and Energy Storage Mechanisms; University of Western Australia: Crawley, Australia, 2013. [Google Scholar]
- Wang, L.; Regina, A.; Butardo, V.M.; Kosar-Hashemi, B.; Larroque, O.; Kahler, C.M.; Wise, M.J. Influence of in situ progressive N-terminal is still controversial truncation of glycogen branching enzyme in Escherichia coli DH5 alpha on glycogen structure, accumulation, and bacterial viability. BMC Microbiol. 2015, 15, 96. [Google Scholar] [CrossRef] [PubMed]
- Grundel, M.; Scheunemann, R.; Lockau, W.; Zilliges, Y. Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp PCC 6803. Microbiol. Sgm 2012, 158, 3032–3043. [Google Scholar] [CrossRef] [PubMed]
- Bains, G. Probing the Allosteric Sites of the Agrobacterium tumefaciens ADP-Glucose Pyrophosphorylase; California State University: Fullerton, CA, USA, 2012. [Google Scholar]
- Urbano, S.B.; Albarracin, V.; Ordonez, O.F.; Farias, M.E.; Alvarez, H.M. Lipid storage in high-altitude Andean Lakes extremophiles and its mobilization under stress conditions in Rhodococcus sp A5, a UV-resistant actinobacterium. Extremophiles 2013, 17, 217–227. [Google Scholar] [CrossRef]
- Jo, H.J.; Park, S.; Jeong, H.G.; Kim, J.W.; Park, J.T. Vibrio vulnificus glycogen branching enzyme preferentially transfers very short chains: N1 domain determines the chain length transferred. FEBS Lett. 2015, 589, 1089–1094. [Google Scholar] [CrossRef]
- Han, A.-R.; Lee, Y.-J.; Wang, T.; Kim, J.-W. Glycogen Metabolism in Vibrio vulnificus Affected by malP and malQ. Microbiol. Biotechnol. Lett. 2018, 46, 29–39. [Google Scholar] [CrossRef]
- Martinez-Garcia, M.; Kormpa, A.; van der Maarel, M. The glycogen of Galdieria sulphuraria as alternative to starch for the production of slowly digestible and resistant glucose polymers. Carbohydr. Polym. 2017, 169, 75–82. [Google Scholar] [CrossRef]
- Martinez-Garcia, M.; Stuart, M.C.A.; van der Maarel, M.J.E. Characterization of the highly branched glycogen from the thermoacidophilic red microalga Galdieria sulphuraria and comparison with other glycogens. Int. J. Biol. Macromol. 2016, 89, 12–18. [Google Scholar] [CrossRef]
- Ban, X.F.; Dhoble, A.S.; Li, C.M.; Gu, Z.B.; Hong, Y.; Cheng, L.; Holler, T.P.; Kaustubh, B.; Li, Z.F. Bacterial 1,4-alpha-glucan branching enzymes: Characteristics, preparation and commercial applications. Crit. Rev. Biotechnol. 2020, 40, 380–396. [Google Scholar] [CrossRef] [PubMed]
- Blesak, K.; Janecek, S. Two potentially novel amylolytic enzyme specificities in the prokaryotic glycoside hydrolase a-amylase family GH57. Microbiol. Sgm 2013, 159, 2584–2593. [Google Scholar] [CrossRef] [PubMed]
- Abad, M.C.; Binderup, K.; Rios-Steiner, J.; Arni, R.K.; Preiss, J.; Geiger, J.H. The X-ray crystallographic structure of Escherichia coli branching enzyme. J. Biol. Chem. 2002, 277, 42164–42170. [Google Scholar] [CrossRef] [PubMed]
- Chaen, K.; Noguchi, J.; Nakashima, T.; Kakuta, Y.; Kimura, M. Crystal structure of the branching enzyme I (BEI) from Oryza sativa L. Acta Crystallogr. A Found. Adv. 2011, 67, C777–C778. [Google Scholar] [CrossRef]
- Froese, D.S.; Michaeli, A.; McCorvie, T.J.; Krojer, T.; Sasi, M.; Melaev, E.; Goldblum, A.; Zatsepin, M.; Lossos, A.; Alvarez, R.; et al. Structural basis of glycogen branching enzyme deficiency and pharmacologic rescue by rational peptide design. Hum. Mol. Genet. 2015, 24, 5667–5676. [Google Scholar] [CrossRef] [PubMed]
- Gavgani, H.N.; Fawaz, R.; Ehyaei, N.; Walls, D.; Pawlowski, K.; Fulgos, R.; Park, S.; Assar, Z.; Ghanbarpour, A.; Geiger, J.H. A structural explanation for the mechanism and specificity of plant branching enzymes I and IIb. J. Biol. Chem. 2022, 298. [Google Scholar] [CrossRef] [PubMed]
- Hayashi, M.; Suzuki, R.; Colleoni, C.; Ball, S.G.; Fujita, N.; Suzuki, E. Crystallization and crystallographic analysis of branching enzymes from Cyanothece sp ATCC 51142. Acta Crystallogr. Sect. F Struct. Biol. Commun. 2015, 71, 1109–1113. [Google Scholar] [CrossRef]
- Hayashi, M.; Suzuki, R.; Colleoni, C.; Ball, S.G.; Fujita, N.; Suzuki, E. Bound Substrate in the Structure of Cyanobacterial Branching Enzyme Supports a New Mechanistic Model. J. Biol. Chem. 2017, 292, 5465–5475. [Google Scholar] [CrossRef]
- Pal, K.; Kumar, S.; Sharma, S.; Garg, S.K.; Alam, M.S.; Xu, H.E.; Agrawal, P.; Swaminathan, K. Crystal Structure of Full-length Mycobacterium tuberculosis H37Rv Glycogen Branching Enzyme Insights of N-terminal beta-sandwich in substrate specificity and enzymatic activity. J. Biol. Chem. 2010, 285, 20897–20903. [Google Scholar] [CrossRef]
- Conchou, L.; Martin, J.; Goncalves, I.R.; Galisson, F.; Violot, S.; Guilliere, F.; Aghajari, N.; Ballut, L. The Candida glabrata glycogen branching enzyme structure reveals unique features of branching enzymes of the Saccharomycetaceae phylum. Glycobiology 2022, 32, 343–355. [Google Scholar] [CrossRef]
- Wang, Z.; Xin, C.H.; Li, C.M.; Gu, Z.B.; Cheng, L.; Hong, Y.; Ban, X.F.; Li, Z.F. Expression and characterization of an extremely thermophilic 1,4-alpha-glucan branching enzyme from Rhodothermus obamensis STB05. Protein Expr. Purif. 2019, 164. [Google Scholar] [CrossRef]
- Huang, L.C.; Tan, H.Y.; Zhang, C.Q.; Li, Q.F.; Liu, Q.Q. Starch biosynthesis in cereal endosperms: An updated review over the last decade. Plant Commun. 2021, 2. [Google Scholar] [CrossRef]
- Utsumi, Y.; Utsumi, C.; Tanaka, M.; Takahashi, S.; Okamoto, Y.; Ono, M.; Nakamura, Y.; Seki, M. Suppressed expression of starch branching enzyme 1 and 2 increases resistant starch and amylose content and modifies amylopectin structure in cassava. Plant Mol. Biol. 2022, 108, 413–427. [Google Scholar] [CrossRef]
- Nakamura, Y.; Kubo, A.; Ono, M.; Yashiro, K.; Matsuba, G.; Wang, Y.F.; Matsubara, A.; Mizutani, G.; Matsuki, J.; Kainuma, K. Changes in fine structure of amylopectin and internal structures of starch granules in developing endosperms and culms caused by starch branching enzyme mutations of japonica rice. Plant Mol. Biol. 2022, 108, 481–496. [Google Scholar] [CrossRef] [PubMed]
- Sawada, T.; Itoh, M.; Nakamura, Y. Contributions of Three Starch Branching Enzyme Isozymes to the Fine Structure of Amylopectin in Rice Endosperm. Front. Plant Sci. 2018, 9. [Google Scholar] [CrossRef] [PubMed]
- Sheng, F.; Yep, A.; Feng, L.; Preiss, J.; Geiger, J.H. Oligosaccharide binding in Escherichia coli glycogen synthase. Biochemistry 2009, 48, 10089–10097. [Google Scholar] [CrossRef] [PubMed]
- Sheng, F.; Jia, X.; Yep, A.; Preiss, J.; Geiger, J.H. The crystal structures of the open and catalytically competent closed conformation of Escherichia coli glycogen synthase. J Biol Chem 2009, 284, 17796–17807. [Google Scholar] [CrossRef]
- Jin, X.; Ballicora, M.A.; Preiss, J.; Geiger, J.H. Crystal structure of potato tuber ADP-glucose pyrophosphorylase. EMBO J 2005, 24, 694–704. [Google Scholar] [CrossRef] [PubMed]
- Geiger, J.H. Sugar tongs get a grip on the starch granule in barley alpha-amylase 1. Structure 2003, 11, 903–904. [Google Scholar] [CrossRef]
- Abad, M.C.; Binderup, K.; Preiss, J.; Geiger, J.H. Crystallization and preliminary X-ray diffraction studies of Escherichia coli branching enzyme. Acta Cryst. D Biol Cryst. 2002, 58, 359–361. [Google Scholar] [CrossRef]
- Feng, L.; Fawaz, R.; Hovde, S.; Gilbert, L.; Chiou, J.; Geiger, J.H. Crystal Structures of Escherichia coli Branching Enzyme in Complex with Linear Oligosaccharides. Biochemistry 2015, 54, 6207–6218. [Google Scholar] [CrossRef] [PubMed]
- Feng, L.; Fawaz, R.; Hovde, S.; Sheng, F.; Nosrati, M.; Geiger, J.H. Crystal structures of Escherichia coli branching enzyme in complex with cyclodextrins. Acta Crystallogr. Sect. D Struct. Biol. 2016, 72, 641–647. [Google Scholar] [CrossRef] [PubMed]
Site | Residue | Molecules in A.S. 1 | Number of Glucoses |
---|---|---|---|
I | W586 | A, B | 5, 7 |
II | W595 | A, B, C | 1, 2, 2 |
III | W478 | B | 1 |
IV | W159 | A | 3 |
V | W544 | A, C | 1, 3 |
VI | W628 | None | 0 2 |
VII | W262 | None | 0 2 |
VIII | Y499 | B | 5 |
IX | H685 | A, C | 5, 4 |
X | W278 | A | 2 |
XI | H613 | B | 1 |
XII | F294 | A | 1 |
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Fawaz, R.; Bingham, C.; Nayebi, H.; Chiou, J.; Gilbert, L.; Park, S.H.; Geiger, J.H. The Structure of Maltooctaose-Bound Escherichia coli Branching Enzyme Suggests a Mechanism for Donor Chain Specificity. Molecules 2023, 28, 4377. https://doi.org/10.3390/molecules28114377
Fawaz R, Bingham C, Nayebi H, Chiou J, Gilbert L, Park SH, Geiger JH. The Structure of Maltooctaose-Bound Escherichia coli Branching Enzyme Suggests a Mechanism for Donor Chain Specificity. Molecules. 2023; 28(11):4377. https://doi.org/10.3390/molecules28114377
Chicago/Turabian StyleFawaz, Remie, Courtney Bingham, Hadi Nayebi, Janice Chiou, Lindsey Gilbert, Sung Hoon Park, and James H. Geiger. 2023. "The Structure of Maltooctaose-Bound Escherichia coli Branching Enzyme Suggests a Mechanism for Donor Chain Specificity" Molecules 28, no. 11: 4377. https://doi.org/10.3390/molecules28114377