A novel type IIb L-asparaginase from Latilactobacillus sakei LK-145: characterization and application.
Latilactobacillus sakei
l-Asparaginase
Lactic acid bacteria
Leukemia drugs
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
18 May 2024
18 May 2024
Historique:
received:
15
01
2024
accepted:
25
04
2024
revised:
29
03
2024
medline:
18
5
2024
pubmed:
18
5
2024
entrez:
18
5
2024
Statut:
epublish
Résumé
We succeeded in homogeneously expressing and purifying L-asparaginase from Latilactobacillus sakei LK-145 (Ls-Asn1) and its mutated enzymes C196S, C264S, C290S, C196S/C264S, C196S/C290S, C264S/C290S, and C196S/C264S/C290S-Ls-Asn1. Enzymological studies using purified enzymes revealed that all cysteine residues of Ls-Asn1 were found to affect the catalytic activity of Ls-Asn1 to varying degrees. The mutation of Cys196 did not affect the specific activity, but the mutation of Cys264, even a single mutation, significantly decreased the specific activity. Furthermore, C264S/C290S- and C196S/C264S/C290S-Ls-Asn1 almost completely lost their activity, suggesting that C290 cooperates with C264 to influence the catalytic activity of Ls-Asn1. The detailed enzymatic properties of three single-mutated enzymes (C196S, C264S, and C290S-Ls-Asn1) were investigated for comparison with Ls-Asn1. We found that only C196S-Ls-Asn1 has almost the same enzymatic properties as that of Ls-Asn1 except for its increased stability for thermal, pH, and the metals NaCl, KCl, CaCl
Identifiants
pubmed: 38761213
doi: 10.1007/s00203-024-03979-5
pii: 10.1007/s00203-024-03979-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
266Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Aishwarya SS, Selvarajan E, Iyappan S, Rajnish KN (2019) Recombinant L-asparaginase II from Lactobacillus casei subsp. casei ATCC 393 and its anticancer activity. Ind J.microbiol 59:313–320
doi: 10.1007/s12088-019-00806-0
Akdel M, Pires DE, Pardo EP, Jänes J, Zalevsky AO, Mészáros B, Bryant P, Good LL, Laskowski RA, Pozzati G, Shenoy A, Zhu W, Kundrotas P, Serra VR, Rodrigues CH, Dunham AS, Burke D, Borkakoti N, Velankar S, Frost A, Basquin J, Lindorff-Larsen K, Bateman A, Kajava AV, Valencia A, Ovchinnikov S, Durairaj J, Ascher DB, Thornton JM, Davey NE, Stein A, Elofsson A, Croll TI, Beltrao P (2022) A structural biology community assessment of alphafold2 applications. Nat Struct Mol Biol 29(11):1056–1067
doi: 10.1038/s41594-022-00849-w
pubmed: 36344848
pmcid: 9663297
Bansal S, Srivastava A, Mukherjee G, Pandey R, Verma AK, Mishra P, Kundu B (2012) Hyperthermophilic asparaginase mutants with enhanced substrate affinity and antineoplastic activity: structural insights on their mechanism of action. FASEB J 26(3):1161–1171
doi: 10.1096/fj.11-191254
pubmed: 22166247
Borek D, Kozak M, Pei J, Jaskolski M (2014) Crystal structure of active site mutant of antileukemic L-asparaginase reveals conserved zinc-binding site. FEBS J 281(18):4097–4111
doi: 10.1111/febs.12906
pubmed: 25040257
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(248):254
Castro D, Marques ASC, Almeida MR, de Paiva GB, Bento HB, Pedrolli DB, Freire MG, Tavares APM, Santos-Ebinuma VC (2021) L-asparaginase production review: bioprocess design and biochemical characteristics. Appl Microbiol Biotechnol 105:4515–4534
doi: 10.1007/s00253-021-11359-y
pubmed: 34059941
Derst C, Henseling J, Röhm KH (2000) Engineering the substrate specificity of Escherichia coli asparaginase II. selective reduction of glutaminase activity by amino acid replacements at position 248. Protein Sci 9(10):2009–2017
doi: 10.1110/ps.9.10.2009
pubmed: 11106175
pmcid: 2144453
Dübbers A, Würthwein G, Müller HJ, Schulze-Westhoff P, Winkelhorst M, Kurzknabe E, Lanvers C, Pieters R, Kaspers GJ, Creutzig U, Ritter J, Boos J (2000) Asparagine synthetase activity in paediatric acute leukaemias: AML-M5 subtype shows lowest activity. Br J Haematol 109:427–429. https://doi.org/10.1046/j.1365-2141.2000.02015.x
doi: 10.1046/j.1365-2141.2000.02015.x
pubmed: 10848836
Duval M, Suciu S, Ferster A, Rialland X, Nelken B, Lutz P, Benoit Y, Robert A, Manel AM, Vilmer E, Otten J, Phillipe N (2002) Comparison of Escherichia coli- asparaginase with Erwinia-asparaginase in the treatment of childhood lymphoid malignancies: results of a randomized european organization for research and treatment of cancer—children’s leukemia group phase 3 trials. Blood 99:2734–2739
doi: 10.1182/blood.V99.8.2734
pubmed: 11929760
Gaufichon L, Rothstein SJ, Suzuki A (2016) Asparagine Metabolic Pathways in Arabidopsis. Plant Cell Physiol 57:675–689. https://doi.org/10.1093/pcp/pcv184
doi: 10.1093/pcp/pcv184
pubmed: 26628609
Guo J, Coker AR, Wood SP, Cooper JB, Chohan SM, Rashid N, Akhtar M (2017) Structure and function of the thermostable L-asparaginase from Thermococcus kodakarensis. Acta Crystallogr Sect d Struc Biol 73(11):889–895
doi: 10.1107/S2059798317014711
Hawkins DS, Park JR, Thomson BG, Holcenberg FJL, JS, Panosyan EH, Avramis VI, (2004) Asparaginase pharmacokinetics after intensive polyethylene glycoL-conjugated L-asparaginase therapy for children with relapsed acute lymphoblastic leukemia. Clin Cancer Res 10:5335–5341. https://doi.org/10.1158/1078-0432.CCR-04-0222
doi: 10.1158/1078-0432.CCR-04-0222
pubmed: 15328169
Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545-549
doi: 10.1093/nar/gkq366
pubmed: 20457744
pmcid: 2896194
Kato S, Oikawa T (2017) Genome sequence of Lactobacillus sakei LK-145 isolated from a japanese sake cellar as a high producer of d-amino acids. Genome Announc 5:e00656-e717. https://doi.org/10.1128/genomeA.00656-17
doi: 10.1128/genomeA.00656-17
pubmed: 28818888
pmcid: 5604761
Kumar K, Verma N (2012) The various sources and application of L-asparaginase. Asian J Biochem Pharm Res 3:197–205
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
doi: 10.1038/227680a0
pubmed: 5432063
Lubkowski J, Wlodawer A (2021) Structural and biochemical properties of L-asparaginase. FEBS J 288(14):4183–4209
doi: 10.1111/febs.16042
pubmed: 34060231
Maggi M, Chiarelli LR, Valentini G, Scotti C (2015) Engineering of Helicobacter pylori L-asparaginase: characterization of two functionally distinct groups of mutants. PLoS ONE 10(2):e0117025
doi: 10.1371/journal.pone.0117025
pubmed: 25664771
pmcid: 4321988
Maqsood B, Basit A, Khurshid M, Bashir Q (2020) Characterization of a thermostable, allosteric L-asparaginase from Anoxybacillus flavithermus. Int J Biol Macromol 152:584–592
doi: 10.1016/j.ijbiomac.2020.02.246
pubmed: 32097739
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
doi: 10.1093/nar/16.3.1215
pubmed: 3344216
pmcid: 334765
Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M (2022) ColabFold: making protein folding accessible to all. Nat Methods 19:679–682
doi: 10.1038/s41592-022-01488-1
pubmed: 35637307
pmcid: 9184281
Oikawa T, Okajima K, Yamanaka K, Kato S (2022) First enzymological characterization of selenocysteine β-lyase from a lactic acid bacterium, Leuconostoc mesenteroides. Amino Acids 54:787–798. https://doi.org/10.1007/s00726-022-03133-9
doi: 10.1007/s00726-022-03133-9
pubmed: 35122135
Pedreschi F, Kaack K, Granby K (2008) The effect of asparaginase on acrylamide formation in French fries. Food Chem 109:386–392
doi: 10.1016/j.foodchem.2007.12.057
pubmed: 26003362
Pokrovsky VS, Kazanov MD, Dyakov IN, Pokrovskaya MV, Aleksandrova SS (2016) Comparative immunogenicity and structural analysis of epitopes of different bacterial L-asparaginases. BMC Cancer. https://doi.org/10.1186/s12885-016-2125-4
doi: 10.1186/s12885-016-2125-4
pubmed: 26867931
pmcid: 4750198
Ran T, Jiao L, Wang W, Chen J, Chi H, Lu Z, Zhang C, Xu D, Lu F (2020) Structures of L-asparaginase from Bacillus licheniformis reveal an essential residue for its substrate stereoselectivity. J Agric Food Chem 69(1):223–231
doi: 10.1021/acs.jafc.0c06609
pubmed: 33371681
Salzer WL, Asselin BL, Plourde PV, Corn T, Hunger SP (2014) Development of asparaginase Erwinia chrysanthemi for the treatment of acute lymphoblastic leukemia. Ann N Y Acad Sci 1329:81–92
doi: 10.1111/nyas.12496
pubmed: 25098829
Schalk AM, Antansijevic A, Caffrey M, Lavie A (2016) Experimental data in support of a direct displacement mechanism for type I/II L-asparaginases. J Biol Chem 291(10):5088–5100
doi: 10.1074/jbc.M115.699884
pubmed: 26733195
pmcid: 4777844
Sun Z, Qin R, Li D, Ji K, Wang T, Cui Z, Huang Y (2016) A novel bacterial type II L-asparaginase and evaluation of its enzymatic acrylamide reduction in French fries. Int J Biol Macromol 92:232–239
doi: 10.1016/j.ijbiomac.2016.07.031
pubmed: 27402458
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Yao M, Yasutake Y, Morita H, Tanaka I (2005) Structure of the type i L-asparaginase from the hyperthermophilic archaeon pyrococcus horikoshii at 2 16 a resolution. Acta Crystallogr Sec D Biol Crystallogr 61(3):294–330
doi: 10.1107/S0907444904032950