Recombinant Snail Sialic Acid Aldolase is Promiscuous towards Aliphatic Aldehydes
Zi-Xuan Hu
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCheng Cheng
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorYu-Qian Li
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorXiao-Han Qi
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorDr. Ting Wang
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCorresponding Author
Prof. Dr. Li Liu
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCorresponding Author
Prof. Dr. Josef Voglmeir
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorZi-Xuan Hu
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCheng Cheng
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorYu-Qian Li
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorXiao-Han Qi
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorDr. Ting Wang
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCorresponding Author
Prof. Dr. Li Liu
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorCorresponding Author
Prof. Dr. Josef Voglmeir
Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorGraphical Abstract
Aldolases reversibly catalyze the cleavage of carbon-carbon bonds. A recombinant snail sialic acid aldolase (sNPL) differs significantly in its carbohydrate substrate promiscuity from other sialic aldolases described so far. In addition, sNPL was able to synthesize a series of 4-hydroxy-2-oxoates using the corresponding aliphatic aldehyde substrates.
Abstract
Aldolases are enzymes that reversibly catalyze the cleavage of carbon-carbon bonds. Here we describe a recombinant sialic acid aldolase originating from the freshwater snail Biomphalaria glabrata (sNPL), and compare its substrate spectrum with a sialic acid aldolase originating from chicken (chNPL). In contrast to vertebrate animals which can synthesize, degrade, and incorporate sialic acids on glycoconjugate ubiquitously, snails (as all mollusks) cannot synthesize sialic acids endogenously, and therefore the biological function and substrate scope of sNPL ought to differ significantly from vertebrate sialic aldolases such as chNPL. sNPL was active towards a series of sialic acid derivatives but was in contrast to chNPL unable to catalyze the cleavage of N-acetylneuraminic acid into N-acetylmannosamine and pyruvate. Interestingly, chNPL and sNPL showed contrasting C4(R)/(S) diastereoselectivity towards the substrates d-mannose and d-galactose in the presence of pyruvate. In addition, sNPL was able to synthesize a series of 4-hydroxy-2-oxoates using the corresponding aliphatic aldehyde substrates in the presence of pyruvate, which could be not achieved by chNPL.
Conflict of interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available in the supplementary material of this article.
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References
- 1R. Schauer, in Advances in Carbohydrate Chemistry and Biochemistry, Vol. 40 (Eds.: R. S. Tipson, D. Horton), Academic Press, 1982, pp. 131–234.
- 2
- 2aO. Campetella, C. A. Buscaglia, J. Mucci, M. S. Leguizamón, Biochim. Biophys. Acta Mol. Basis Dis. 2020, 1, 20;
- 2bA. F. Carlin, S. Uchiyama, Y.-C. Chang, A. L. Lewis, V. Nizet, A. Varki, Blood 2009, 113, 3333–3336.
- 3P. Laborda, S. Y. Wang, J. Voglmeir, Molecules 2016, 21, 1513.
- 4
- 4aV. R. L. J. Bloemendal, S. J. Moons, J. J. A. Heming, M. Chayoua, O. Niesink, J. C. M. van Hest, T. J. Boltje, F. P. J. T. Rutjes, Adv. Synth. Catal. 2019, 361, 2443–2447;
- 4bD. Yi, N. He, M. Kickstein, J. Metzner, M. Weiß, A. Berry, W.-D. Fessner, Adv. Synth. Catal. 2013, 355, 3597–3612;
- 4cN. He, D. Yi, W.-D. Fessner, Adv. Synth. Catal. 2011, 353, 2384–2398;
- 4dY. Zhang, C. Meng, L. Jin, X. Chen, F. Wang, H. Cao, Chem. Commun. 2015, 51, 11654–11657;
- 4eO. Blixt, J. C. Paulson, Adv. Synth. Catal. 2003, 345, 687–690;
- 4fN. Tasnima, H. Yu, X. Yan, W. Li, A. Xiao, X. Chen, Carbohydr. Res. 2019, 472, 115–121;
- 4gA. Santra, A. Xiao, H. Yu, W. Li, Y. Li, L. Ngo, J. B. McArthur, X. Chen, Angew. Chem. Int. Ed. 2018, 57, 2929–2933;
Angew. Chem. 2018, 130, 2979–2983;
10.1002/ange.201712022 Google Scholar
- 4hP. Laborda, Y. M. Lyu, F. Parmeggiani, A. M. Lu, W. J. Wang, Y. Y. Huang, K. Huang, J. Guo, L. Liu, S. L. Flitsch, J. Voglmeir, Angew. Chem. Int. Ed. 2020, 59, 5308–5311;
Angew. Chem. 2020, 132, 5346–5349;
10.1002/ange.201914338 Google Scholar
- 4iZ. P. Cai, L. P. Conway, Y. Y. Huang, W. J. Wang, P. Laborda, T. Wang, A. M. Lu, H. L. Yao, K. Huang, S. L. Flitsch, L. Liu, J. Voglmeir, Molecules 2019, 24, 1368.
- 5J. E. Barnett, D. L. Corina, G. Rasool, Biochem. J. 1971, 125, 275–284.
- 6
- 6aA. D. Daniels, I. Campeotto, M. W. van der Kamp, A. H. Bolt, C. H. Trinh, S. E. V. Phillips, A. R. Pearson, A. Nelson, A. J. Mulholland, A. Berry, ACS Chem. Biol. 2014, 9, 1025–1032;
- 6bW.-D. Fessner, C. Walter, in Bioorganic Chemistry: Models and Applications (Ed.: F. P. Schmidtchen), Springer, Heidelberg, 1997, pp. 97–194.
- 7A. G. Watts, S. G. Withers, Can. J. Chem. 2004, 82, 1581–1588.
- 8
- 8aU. Kragl, A. Gödde, C. Wandrey, N. Lubin, C. Augé, J. Chem. Soc. Perkin Trans. 1 1994, 119–124;
- 8bM. J. Kim, W. J. Hennen, H. M. Sweers, C. H. Wong, J. Am. Chem. Soc. 1988, 110, 6481–6486;
- 8cC. Augé, S. David, C. Gautheron, Tetrahedron Lett. 1984, 25, 4663–4664.
- 9W. Fitz, J.-R. Schwark, C.-H. Wong, J. Org. Chem. 1995, 60, 3663–3670.
- 10W.-D. Fessner, N. He, D. Yi, P. Unruh, M. Knorst, in Cascade Biocatalysis (Eds.: S. Riva, W.-D. Fessner), Wiley-VCH, Weinheim, 2014, pp. 361–392.
10.1002/9783527682492.ch17 Google Scholar
- 11M. J. Nigro, M. A. Palazzolo, D. Colasurdo, A. M. Iribarren, E. S. Lewkowicz, Catal. Commun. 2019, 121, 73–77.
- 12Q. Chen, L. Han, X. Chen, Y. Cui, J. Feng, Q. Wu, D. Zhu, Enzyme Microb. Technol. 2016, 92, 99–106.
- 13P. Laborda, S.-Y. Wang, A.-M. Lu, M. He, X.-C. Duan, Y.-J. Qian, Y.-S. Jung, L. Liu, J. Voglmeir, Adv. Synth. Catal. 2017, 359, 3120–3125.
- 14
- 14aX.-Y. Wen, M. Tarailo-Graovac, K. Brand-Arzamendi, A. Willems, B. Rakic, K. Huijben, A. Da Silva, X. Pan, S. El-Rass, R. Ng, K. Selby, A. M. Philip, J. Yun, X. C. Ye, C. J. Ross, A. M. Lehman, F. Zijlstra, N. Abu Bakar, B. Drögemöller, J. Moreland, W. W. Wasserman, H. Vallance, M. van Scherpenzeel, F. Karbassi, M. Hoskings, U. Engelke, A. de Brouwer, R. A. Wevers, A. V. Pshezhetsky, C. D. M. van Karnebeek, D. J. Lefeber, JCI Insight 2018, 3, e122373;
- 14bU. Sommer, C. Traving, R. Schauer, Glycoconjugate J. 1999, 16, 425–435;
- 14cD. A. Sirbasku, S. B. Binkley, Biochim. Biophys. Acta Enzymol. 1970, 206, 479–482.
- 15
- 15aM. N. Matrosovich, T. Y. Matrosovich, T. Gray, N. A. Roberts, H.-D. Klenk, Proc. Natl. Acad. Sci. USA 2004, 101, 4620–4624;
- 15bA. J. Thompson, J. C. Paulson, J. Biol. Chem. 2021, 296, 22.
- 16R. Schauer, Zoology 2004, 107, 49–64.
- 17E. Drula, M. L. Garron, S. Dogan, V. Lombard, B. Henrissat, N. Terrapon, Nucleic Acids Res. 2022, 50, D571-D577.
- 18
- 18aR. B. Caldwell, A. M. Kierzek, H. Arakawa, Y. Bezzubov, J. Zaim, P. Fiedler, S. Kutter, A. Blagodatski, D. Kostovska, M. Koter, J. Plachy, P. Carninci, Y. Hayashizaki, J. M. Buerstedde, Genome Biol. 2005, 6, 2004–2006;
- 18bC. M. Adema, L. W. Hillier, C. S. Jones, E. S. Loker, M. Knight, P. Minx, G. Oliveira, N. Raghavan, A. Shedlock, L. R. do Amaral, H. D. Arican-Goktas, J. G. Assis, E. H. Baba, O. L. Baron, C. J. Bayne, U. Bickham-Wright, K. K. Biggar, M. Blouin, B. C. Bonning, C. Botka, J. M. Bridger, K. M. Buckley, S. K. Buddenborg, R. Lima Caldeira, J. Carleton, O. S. Carvalho, M. G. Castillo, I. W. Chalmers, M. Christensens, S. Clifton, C. Cosseau, C. Coustau, R. M. Cripps, Y. Cuesta-Astroz, S. F. Cummins, L. di Stephano, N. Dinguirard, D. Duval, S. Emrich, C. Feschotte, R. Feyereisen, P. FitzGerald, C. Fronick, L. Fulton, R. Galinier, S. G. Gava, M. Geusz, K. K. Geyer, G. I. Giraldo-Calderón, M. de Souza Gomes, M. A. Gordy, B. Gourbal, C. Grunau, P. C. Hanington, K. F. Hoffmann, D. Hughes, J. Humphries, D. J. Jackson, L. K. Jannotti-Passos, W. de Jesus Jeremias, S. Jobling, B. Kamel, A. Kapusta, S. Kaur, J. M. Koene, A. B. Kohn, D. Lawson, S. P. Lawton, D. Liang, Y. Limpanont, S. Liu, A. E. Lockyer, T. L. Lovato, F. Ludolf, V. Magrini, D. P. McManus, M. Medina, M. Misra, G. Mitta, G. M. Mkoji, M. J. Montague, C. Montelongo, L. L. Moroz, M. C. Munoz-Torres, U. Niazi, L. R. Noble, F. S. Oliveira, F. S. Pais, A. T. Papenfuss, R. Peace, J. J. Pena, E. A. Pila, T. Quelais, B. J. Raney, J. P. Rast, D. Rollinson, I. C. Rosse, B. Rotgans, E. J. Routledge, K. M. Ryan, L. L. S. Scholte, K. B. Storey, M. Swain, J. A. Tennessen, C. Tomlinson, D. L. Trujillo, E. V. Volpi, A. J. Walker, T. Wang, I. Wannaporn, W. C. Warren, X. J. Wu, T. P. Yoshino, M. Yusuf, S. M. Zhang, M. Zhao, R. K. Wilson, Nat. Commun. 2017, 8, 16153.
- 19K. Nakano, T. Nakano, D. U. Ahn, J. Sim, Can. J. Anim. Sci. 1994, 74, 601–606.
- 20
- 20aS. Basu, M. Sarkar, C. Mandal, Mol. Cell. Biochem. 1986, 71, 149–157;
- 20bR. Brossmer, M. Wagner, E. Fischer, J. Biol. Chem. 1992, 267, 8752–8756;
- 20cC. Liu, S. Jiang, M. Wang, L. Wang, H. Chen, J. Xu, Z. Lv, L. Song, Develop. Comp. Immunol. 2016, 61, 136–144.
- 21
- 21aY. Robledo, I. Marigómez, E. Angulo, M. P. Cajaraville, Cell Tissue Res. 2006, 324, 319;
- 21bE. Staudacher, Biomol. Eng. 2021, 11, 1820.
- 22
- 22aY. Li, H. Yu, H. Cao, K. Lau, S. Muthana, V. K. Tiwari, B. Son, X. Chen, Appl. Microbiol. Biotechnol. 2008, 79, 963–970;
- 22bG. Sánchez-Carrón, M. I. García-García, A. B. López-Rodríguez, S. Jiménez-García, A. Sola-Carvajal, F. García-Carmona, A. Sánchez-Ferrer, Appl. Environ. Microbiol. 2011, 77, 2471–2478;
- 22cR. A. North, S. A. Kessans, S. C. Atkinson, H. Suzuki, A. J. Watson, B. R. Burgess, L. M. Angley, A. O. Hudson, A. Varsani, M. D. Griffin, A. J. Fairbanks, R. C. Dobson, Acta Crystallogr. Sect. F 2013, 69, 306–312;
- 22dJ. P. Kumar, H. Rao, V. Nayak, S. Ramaswamy, Acta Crystallogr. Sect. F 2018, 74, 725–732;
- 22eJ. A. Barbosa, B. J. Smith, R. DeGori, H. C. Ooi, S. M. Marcuccio, E. M. Campi, W. R. Jackson, R. Brossmer, M. Sommer, M. C. Lawrence, J. Mol. Biol. 2000, 303, 405–421.
- 23A. Sola-Carvajal, F. Gil-Ortiz, F. García-Carmona, V. Rubio, Á. Sánchez-Ferrer, Biochem. J. 2014, 462, 499–511.
- 24
- 24aS.-Y. Wang, P. Laborda, A.-M. Lu, M. Wang, X.-C. Duan, L. Liu, J. Voglmeir, J. Carbohydr. Chem. 2016, 35, 423–434;
- 24bS.-Y. Wang, P. Laborda, A.-M. Lu, X.-C. Duan, H.-Y. Ma, L. Liu, J. Voglmeir, Catalysts 2016, 6, 212.
- 25
- 25aJ. L. Reissig, J. L. Strominger, L. F. Leloir, J. Biol. Chem. 1955, 217, 959–966;
- 25bD. Mauzerall, S. Granick, J. Biol. Chem. 1956, 219, 435–446.
- 26F. N. Awad, A. Kulinich, M. J. Yao, X. C. Duan, Z. P. Cai, B. Gu, L. Liu, J. Voglmeir, J. Carbohydr. Chem. 2016, 35, 301–314.
- 27
- 27aM. Wada, C. C. Hsu, D. Franke, M. Mitchell, A. Heine, I. Wilson, C. H. Wong, Bioorg. Med. Chem. 2003, 11, 2091–2098;
- 27bC.-C. Hsu, Z. Hong, M. Wada, D. Franke, C.-H. Wong, Proc. Natl. Acad. Sci. USA 2005, 102, 9122–9126.
- 28R. O. M. A. de Souza, L. S. M. Miranda, U. T. Bornscheuer, Chem. Eur. J. 2017, 23, 12040–12063.
- 29L. Warren, J. Biol. Chem. 1959, 234, 1971–1975.
- 30
- 30aH. L. Yao, L. P. Conway, M. M. Wang, K. Huang, L. Liu, J. Voglmeir, Glycoconjugate J. 2016, 33, 219–226;
- 30bK. R. Anumula, Anal. Biochem. 1995, 230, 24–30.
- 31A. K. Bergfeld, A. N. Samraj, A. Varki, in Glycoscience: Biology and Medicine (Eds.: T. Endo, P. H. Seeberger, G. W. Hart, C.-H. Wong, N. Taniguchi), Springer Japan, Tokyo, 2021, pp. 1–8.
- 32J. Jumper, R. Evans, A. Pritzel, T. Green, M. Figurnov, O. Ronneberger, K. Tunyasuvunakool, R. Bates, A. Žídek, A. Potapenko, A. Bridgland, C. Meyer, S. A. A. Kohl, A. J. Ballard, A. Cowie, B. Romera-Paredes, S. Nikolov, R. Jain, J. Adler, T. Back, S. Petersen, D. Reiman, E. Clancy, M. Zielinski, M. Steinegger, M. Pacholska, T. Berghammer, S. Bodenstein, D. Silver, O. Vinyals, A. W. Senior, K. Kavukcuoglu, P. Kohli, D. Hassabis, Nature 2021, 596, 583–589.
- 33K. Anderson, S. C. Li, Y. T. Li, Anal. Biochem. 2000, 287, 337–339.
- 34P. C. Denny, P. A. Denny, S. E. Allerton, Clin. Chim. Acta 1983, 131, 333–336.
- 35E. F. Pettersen, T. D. Goddard, C. C. Huang, E. C. Meng, G. S. Couch, T. I. Croll, J. H. Morris, T. E. Ferrin, Protein Sci. 2021, 30, 70–82.
- 36E. F. Pettersen, T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, T. E. Ferrin, J. Comput. Chem. 2004, 25, 1605–1612.