GH32 family activity: a topological approach through protein contact networks

Plant Molecular Biology

Volumn 92, Issue 4-5, 2016, Pages 401-410

  Cimini, Sara ^a   Di Paola, Luisa ^a   Giuliani, Alessandro ^b   Ridolfi, Alessandra ^a   De Gara, Laura ^a  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Clustering; Fructans; GH32 family; Protein Contact Networks

Indexed keywords

GLYCOSIDASE; PLANT PROTEIN;

CHEMISTRY; ENZYME SPECIFICITY; KINETICS; METABOLISM;

GLYCOSIDE HYDROLASES; KINETICS; PLANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84981186544     PISSN: 01674412     EISSN: 15735028     Source Type: Journal    
DOI: 10.1007/s11103-016-0515-2     Document Type: Article

References (38)

1. Altenbach D, Nüesch E, Meyer AD, Boller T, Wiemken A (2004) The large subunit determines catalytic specificity of barley sucrose:fructan 6-fructosyltransferase and fescue sucrose:sucrose 1-fructosyltransferase. FEBS Lett 567(2–3):214–218. doi:10.1016/j.febslet.2004.04.064
2. Amitai G, Shemesh A, Sitbon E, Shklar M, Netanely D, Venger I, Pietrokovski S (2004) Network analysis of protein structures identifies functional residues. J Mol Biol 344(4):1135–1146. doi:10.1016/j.jmb.2004.10.055
3. Bhattacharyya, M, Ghosh S, Vishveshwara S (2016) Protein structure and function: looking through the network of side-chain interactions. Curr Protein Pept Sci 17(1):4–25
4. Cimini S, Locato V, Vergauwen R, Paradiso A, Cecchini C, Vandenpoel L, Verspreet J et al (2015) Fructan biosynthesis and degradation as part of plant metabolism controlling sugar fluxes during durum wheat kernel maturation. Front Plant Sci 6:89. doi:10.3389/fpls.2015.00089
5. Cumbo F, Paci P, Santoni D, Di Paola L, Giuliani A. 2014. GIANT: a cytoscape plugin for modular networks. PLoS One. doi:10.1371/journal.pone.0105001
6. De Ruvo M, Giuliani A, Paci P, Santoni D, Di Paola L (2012) Shedding light on protein–ligand binding by graph theory: the topological nature of allostery. Biophys Chem 165–166:21–29. doi:10.1016/j.bpc.2012.03.001
7. Ende VW, Coopman M, Clerens S, Vergauwen R, Roy KL, Lammens W, Van Laere A (2011) Unexpected presence of graminan- and levan-type fructans in the evergreen frost-hardy eudicot pachysandra terminalis (Buxaceae): purification, cloning, and functional analysis of a 6-SST/6-SFT enzyme. Plant Physiol 155(1):603–614. doi:10.1104/pp.110.162222
8. Giuliani, A, Paola LD (2016) Protein as networks: will contact maps hold the promise to represent the ‘structural-formula’ of protein molecules? Curr Protein Pept Sci 17(1):3
9. Giuliani A, Paola LD, Setola R (2009) Proteins as networks: a mesoscopic approach using haemoglobin molecule as case study. Curr Proteomics 6(4):235–245
10. Guimerà R, Sales-Pardo M, Amaral LAN (2006) Classes of complex networks defined by role-to-role connectivity profiles. Nat Phys 3:63–69
11. Gutman I, Zhou B (2006) Laplacian energy of a graph. Linear Algebra Appl 414(1):29–37. doi:10.1016/j.laa.2005.09.008
12. Henrissat B (1991) A classification of glycosyl hydrolases based sequence similarities amino acid. Biochem J 280(Pt 2):309–316. doi:10.1007/s007920050009
13. Hothorn M, Van Den Edne W, Lammens W, Rybin V, Scheffzek K (2010) Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc Natl Acad Sci USA. doi:10.1073/pnas.1004481107
14. Krishnan A, Zbilut JP, Tomita M, Giuliani A (2008) Proteins as networks: usefulness of graph theory in protein science. Curr Protein Pept Sci 9:28–38
15. Lammens W, Roy KL, Van Laere A, Rabijns A, Van Den Ende W (2008) Crystal structures of arabidopsis thaliana cell-wall invertase mutants in complex with sucrose. J Mol Biol 377(2):378–385. doi:10.1016/j.jmb.2007.12.074
16. Lammens W, Roy KL, Schroeven L, Van Laere A, Rabijns A, Van Den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60(3):727–740. doi:10.1093/jxb/ern333
17. Lammens W, Roy KL, Yuan S, Vergauwen R, Rabijns A, Van Laere A, Strelkov SV, Van Den Ende W (2012) Crystal structure of 6-SST/6-SFT from pachysandra terminalis, a plant fructan biosynthesizing enzyme in complex with its acceptor substrate 6-kestose. Plant J 70(2):205–219. doi:10.1111/j.1365-313X.2011.04858.x
18. Le Roy K Verhaest M, Rabijns A, Clerens S, Van Laere A, Van Den Ende W (2007) N-Glycosylation affects substrate specificity of chicory fructan 1-exohydrolase: evidence for the presence of an inulin binding cleft. New Phytol 176:317–324. doi:10.1111/j.1469-8137.2007.02174.x
19. Maiti R, Van Domselaar GH, Zhang H, Wishart DS (2004) SuperPose: a simple server for sophisticated structural superposition. Nucleic Acids Res 32:W590–W594. doi:10.1093/nar/gkh477
20. Matrai J, Lammens W, Jonckheer A, Le Roy K, Rabijns A, Van den Ende W, De Maeyer M (2007) An alternate sucrose binding mode in the e203q arabidopsis invertase mutant: an X-ray crystallography and docking study. Proteins 71:552–564 http://www.rcsb.org/pdb/explore/explore.do?structureId=2OXB
21. Minic Z (2008) Physiological roles of plant glycoside hydrolases. Planta 723–740. doi:10.1007/s00425-007-0668-y
22. Oliva G, Di Paola L, Giuliani A, Pascucci F, Setola R (2013) Assessing protein resilience via a complex network approach. In: IEEE 2nd Network Science Workshop (NSW), pp 131–137
23. Paci P, Di Paola L, Santoni D, De Ruvo M, Giuliani A (2012) Structural and functional analysis of hemoglobin and serum albumin through protein long-range interaction networks. Curr Proteomics 9(3):160–166
24. Paola DL, De Ruvo M, Paci P, Santoni D, Giuliani A (2013) Protein contact networks: an emerging paradigm in chemistry. Chem Rev 113(3):1598–1613. doi:10.1021/cr3002356
25. Paola DL, Platania CBiancaM, Oliva G, Setola R, Pascucci F, Giuliani A (2015) Characterization of protein–protein interfaces through a protein contact network approach. Front Bioeng Biotechnol 3:1–10. doi:10.3389/fbioe.2015.00170
26. Paola D, Luisa GM, Di Venere A, Giuliani A (2016) Exploring the stability of dimers through protein structure topology. Curr Protein Pept Sci 17(1):30–36. doi:10.2174/1389203716666150923104054
27. Platania CBM, Di Paola L, Leggio GM, Romano GL, Drago F, Salomone S, Bucolo C (2015) Molecular features of interaction between VEGFA and anti-angiogenic drugs used in retinal diseases: a computational approach. Front Pharmacol 6:248
28. Pons T, Naumoff DG, Martínez-Fleites C, Hernández L (2004) Three acidic residues are at the active site of a beta-propeller architecture in glycoside hydrolase families 32, 43, 62, and 68. Proteins 54(3):424–432. doi:10.1002/prot.10604
29. Tasdighian S, Paola LD, De Ruvo M, Paci P, Santoni D, Palumbo P, Mei G, Di Venere A, Giuliani A (2014) Modules identification in protein structures: the topological and geometrical solutions. J Chem Inf Model 54:159–168. doi:10.1021/ci400218v
30. Todeschini R, Consonni V (2000) Handbook of molecular descriptors. In: Manhold R, Kubinyi H, Timmermann H (eds) Methods and principles in medicinal chemistry, vol 11. Wiley VCH, Weinheim
31. Trollope KM, van Wyk N, Kotjomela MA, Volschenk H (2015) Sequence and structure-based prediction of fructosyltransferase activity for functional sub-classification of fungal GH32 enzymes. FEBS J. doi:10.1111/febs.13536
32. Tsai CJ, del Sol A, Nussinov R (2008) Allostery: absence of a change in shape does not imply that allostery is not at play. J Mol Biol 378(1):1–11
33. Ullman JD, Yannakakis M (1991) High-probability parallel transitive-closure algorithms. SIAM J Comput 20(1):100–125
34. Verhaest M, Ende WV, Roy KL, De Ranter CJ, Van Laere A, Rabijns A (2005a) X-ray diffraction structure of a plant glycosyl hydrolase family 32 protein: fructan 1-exohydrolase IIa of Cichorium intybus. Plant J Cell Mol Biol 41(3):400–411. doi:10.1111/j.1365-313X.2004.02304.x
35. Verhaest M, Le Roy K, Stefaan S, De Coninck B, Lammens W, De Ranter CJ, Van Laere A, Van Den Ende W, Rabijns A (2005b) Crystallization and preliminary x-ray diffraction study of a cell-wall invertase from Arabidopsis thaliana. Acta Crystallogr 61:766–768. doi:10.1107/S1744309105021421
36. Verhaest M, Lammens W, Le Roy K, De Coninck B, De Ranter CJ, Van Laere A, Van Den Ende W, Rabijns A (2006a) X-ray diffraction structure of a cell-wall invertase from Arabidopsis thaliana. Acta Crystallogr 62(Pt 12):1555–1563. doi:10.1107/S0907444906044489
37. Verhaest M, Lammens W, Le Roy K, De Ranter CJ, Van Laere A, Rabijns A, Van den Ende W (2007) Insights into the fine architecture of the active site of chicory fructan 1-exohydrolase: 1-kestose as substrate vs sucrose as inhibitor. New Phytol 174(1):90–100. doi:10.1111/j.1469-8137.2007.01988.x
38. Verspreet J, Cimini S (2013) Fructan metabolism in developing wheat (Triticum aestivum L.) kernels. Plant Cell 54(12):2047–2057. doi:10.1093/pcp/pct144