L-asparaginase: therapeutic use and applications in the food industry – a review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i10.18980

Keywords:

Enzyme; L-asparaginase; Acrylamide; Immobilization; Food; Leukemia treatment.

Abstract

L-asparaginase (L-asnase) is an amino hydrolase that has been used in the last decades for leukemia treatment, which boosted scientific studies on production, purification and immobilization of this enzyme. More recently, L-asnase has called food industry attention because of its effect on acrylamide formation in fried and baked foods. Several studies have been carried out in order to evaluate the effect of L-asnase in reducing acrylamide formation in different food models. This review brings up an overview in L-asnase kinetic parameters from different sources, immobilization methods, its therapeutic use in leukemia treatment and food processing applications. This review also discusses acrylamide formation in fried and baked foods. Commercial L-asnase is produced by two microorganisms, Escherichia coli and Erwinia sp. However, studies using different microorganisms have shown the possibility of producing this enzyme from different sources, obtaining enzymes with interesting kinetic properties. Immobilization strategies have provided enzymes with greater activity and stability, which could contribute to maintain L-asnase activity in the body for longer periods. Researches applying L-asnase in food products have shown significant reduction in acrylamide production, above 90% in some cases. For this purpose, during enzyme application some variables must be taken into account, as enzyme dose, food matrix, pretreatment, processing time and temperature. Medical and food applications make L-asnase a multipurpose enzyme. Reducing prices, improving enzyme stability and reducing co-lateral effects in leukemia treatment are still challenges to overcome.

References

Agarwal, S., & Sahu, S. (2014). Safety and Regulatory Aspects of Food Enzymes: An Industrial Perspective. International Journal of Interdisciplinary and Multidisciplinary Studies (IJIMS), 1(6), 253–267. Retrieved from http://www.ijims.com/uploads/0078a9c56ca7560ca162z32.pdf

Agrawal, S., & Kango, N. (2019). Development and catalytic characterization of L-asparaginase nano-bioconjugates. International Journal of Biological Macromolecules, 135, 1142–1150. doi: 10.1016/j.ijbiomac.2019.05.154

Agrawal, S., Sharma, I., Prajapati, B. P., Suryawanshi, R. K., & Kango, N. (2018). Catalytic characteristics and application of L-asparaginase immobilized on aluminum oxide pellets. International Journal of Biological Macromolecules, 114, 504–511. doi: 10.1016/j.ijbiomac.2018.03.081

Ahmad, A., Patta, A. M., & Natsir, H. (2013). Purification and immobilization of L-asparaginase enzyme from the thermophilic bacteria Bacillus licheniformis strain HSA3-1a. International Journal of Pharma and Bio Sciences, 4(4), 274-280.

Aiswarya, R., & Baskar, G. (2018). Microbial production of l-asparaginase and its immobilization on chitosan for mitigation of acrylamide in heat processed carrot slices. Indian Journal of Experimental Biology, 56(7), 504–510.

Aiswarya, Ravi, & Baskar, G. (2018). Enzymatic mitigation of acrylamide in fried potato chips using asparaginase from Aspergillus terreus. International Journal of Food Science and Technology, 53(2), 491–498. doi: 10.1111/ijfs.13608

Alam, S., Ahmad, R., Pranaw, K., Mishra, P., & Khare, S. K. (2018). Asparaginase conjugated magnetic nanoparticles used for reducing acrylamide formation in food model system. Bioresource Technology, 269, 121–126. doi: 10.1016/j.biortech.2018.08.095

Anese, M. (2016). Acrylamide in Coffee and Coffee Substitutes. In V. Gökmen (Ed.), Acrylamide in Food: Analysis, Content and Potential Health Effects (pp. 181–195). Elsevier Inc. doi: 10.1016/B978-0-12-802832-2.00009-7

Anese, M., Quarta, B., & Frias, J. (2011). Modelling the effect of asparaginase in reducing acrylamide formation in biscuits. Food Chemistry, 126(2), 435–440. doi: 10.1016/j.foodchem.2010.11.007

Ashrafi, H., Amini, M., Mohammadi-Samani, S., Ghasemi, Y., Azadi, A., Tabandeh, M. R. & Kamali-Sarvestani (2013). Nanostructure l-asparaginase-fatty acid bioconjugate: Synthesis, preformulation study and biological assessment. International Journal of Biological Macromolecules, 62, 180–187. doi: 10.1016/j.ijbiomac.2013.08.028

Bahreini, E., Aghaiypour, K., Abbasalipourkabir, R., Mokarram, A. R., Goodarzi, M. T., & Saidijam, M. (2014). Preparation and nanoencapsulation of l-asparaginase II in chitosan-tripolyphosphate nanoparticles and in vitro release study. Nanoscale Research Letters, 9(1), 1–13. doi: 10.1186/1556-276X-9-340

Bakshi, A., & Patel, A. K. (2019). Halftoning algorithm using pull-based error diffusion technique. Lecture Notes in Networks and Systems, 56, 411–419. doi: 10.1007/978-981-13-2354-6_43

Balcão, V. M., Mateo, C., Fernández-Lafuente, R., Xavier Malcata, F., & Guisán, J. M. (2001). Structural and functional stabilization of L-asparaginase via multisubunit immobilization onto highly activated supports. Biotechnology Progress, 17(3), 537–542. doi: 10.1021/bp000163r

Baskar, G., Chandhuru, J., Sheraz Fahad, K., Praveen, A. S., Chamundeeswari, M., & Muthukumar, T. (2015). Anticancer activity of fungal l-asparaginase conjugated with zinc oxide nanoparticles. Journal of Materials Science: Materials in Medicine, 26(1), 1–7. doi: 10.1007/s10856-015-5380-z

Batool, T., Makky, E. A., Jalal, M., & Yusoff, M. M. (2016). A Comprehensive Review on l-Asparaginase and Its Applications. Applied Biochemistry and Biotechnology, 178(5), 900–923. doi: 10.1007/s12010-015-1917-3

Bilal, M., Zhao, Y., Rasheed, T., & Iqbal, H. M. N. (2018, December 1). Magnetic nanoparticles as versatile carriers for enzymes immobilization: A review. International Journal of Biological Macromolecules, 120, 2530-25-44. doi: 10.1016/j.ijbiomac.2018.09.025

Blackman, L. D., Varlas, S., Arno, M. C., Houston, Z. H., Fletcher, N. L., Thurecht, K. J. & Hasan, M. (2018). Confinement of Therapeutic Enzymes in Selectively Permeable Polymer Vesicles by Polymerization-Induced Self-Assembly (PISA) Reduces Antibody Binding and Proteolytic Susceptibility. ACS Central Science, 4(6), 718–723. doi: 10.1021/acscentsci.8b00168

Brena, B., González-Pombo, P., & Batista-Viera, F. (2013). Immobilization of enzymes: A literature survey. Methods in Molecular Biology, 1051, 15–31. doi: 10.1007/978-1-62703-550-7_2

Cellesi, F., & Tirelli, N. (2006). Sol-gel synthesis at neutral pH in W/O microemulsion: A method for enzyme nanoencapsulation in silica gel nanoparticles. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 288(1–3), 52–61. doi: 10.1016/j.colsurfa.2006.05.008

Clark, D. S. (1994). Can immobilization be exploited to modify enzyme activity? Trends in Biotechnology, 12(11), 439–443. doi: 10.1016/0167-7799(94)90018-3

Claus, A., Carle, R., & Schieber, A. (2008). Acrylamide in cereal products: A review. Journal of Cereal Science, 47(2), 118–133. doi: 10.1016/j.jcs.2007.06.016

Covini, D., Tardito, S., Bussolati, O., R. Chiarelli, L., V. Pasquetto, M., Digilio, R. & Scotti, C. (2011). Expanding Targets for a Metabolic Therapy of Cancer: L-Asparaginase. Recent Patents on Anti-Cancer Drug Discovery, 7(1), 4–13. doi: 10.2174/157489212798358001

Cruz, M. E. M., Martins, M. B., Corvo, M. L., Gaspar, M. M., Oliveira, E. M. M., & Ferrara, M. A. (2008). Enzimas em medicamentos e diagnósticos. In Bon, E. P. S.; Ferrara, M. A. & Corvo, M. L. (Eds.), Enzimas em Biotecnologia: Produção, Aplicações e Mercado, (pp. 307-331). Interciência.

Desai, S. S., & Hungund, B. S. (2018). Submerged fermentation, purification, and characterization of L-asparaginase from Streptomyces sp. isolated from soil. Journal of Applied Biology & Biotechnology, 6(5), 17–23. doi: 10.7324/jabb.2018.60503

Dias, F. F. G., Bogusz Junior, S., Hantao, L. W., Augusto, F., & Sato, H. H. (2017). Acrylamide mitigation in French fries using native L-asparaginase from Aspergillus oryzae CCT 3940. LWT - Food Science and Technology, 76, 222–229. https://doi.org/10.1016/j.lwt.2016.04.017

Dias, F. F. G., Ruiz, A. L. T. G., Torre, A. Della, & Sato, H. H. (2016). Purification, characterization and antiproliferative activity of L-asparaginase from Aspergillus oryzae CCT 3940 with no glutaminase activity. Asian Pacific Journal of Tropical Biomedicine, 6(9), 785–794. doi:10.1016/j.apjtb.2016.07.007

El-Naggar, N. E. A., Deraz, S. F., Soliman, H. M., El-Deeb, N. M., & El-Ewasy, S. M. (2016). Purification, characterization, cytotoxicity and anticancer activities of L-asparaginase, anti-colon cancer protein, from the newly isolated alkaliphilic Streptomyces fradiae NEAE-82. Scientific Reports, 6(August), 1–16. doi:10.1038/srep32926

El-Refai, H. A., Shafei, M. S., Mostafa, H., El-Refai, A. M. H., Araby, E. M., El-Beih, F. M. & Easa, S. M. (2016). Comparison of free and immobilized L-asparaginase synthesized by gamma-irradiated Penicillium cyclopium. Polish Journal of Microbiology, 65(1), 43–50. doi: 10.5604/17331331.1197274

El-Sharkawy, A. S., Farag, A. M., Embaby, A. M., Saeed, H., & El-Shenawy, M. (2016). Cloning, expression and characterization of aeruginosa EGYII L-Asparaginase from Pseudomonas aeruginosa strain EGYII DSM 101801 in E. coli BL21(DE3) pLysS. Journal of Molecular Catalysis B: Enzymatic, 132, 16–23. doi: 10.1016/j.molcatb.2016.06.011

Elmore, S. J., Koutsidis, G., Dodson, A. T., Mottram, D. S., & Wedzicha, B. L. (2005). Measurement of acrylamide and its precursors in potato, wheat, and rye model systems. Journal of Agricultural and Food Chemistry, 53(4), 1286–1293. doi:10.1021/jf048557b

Erdogan, A., Koytepe, S., Ates, B., Yilmaz, I., & Seckin, T. (2014). Preparation of the L-asparaginase-based biosensor with polyimide membrane electrode for monitoring l-asparagine levels in leukemia. International Journal of Polymeric Materials and Polymeric Biomaterials, 63(17), 909–917. doi: 10.1080/00914037.2014.886228

Feng, Y., Liu, S., Jiao, Y., Gao, H., Wang, M., Du, G., & Chen, J. (2017). Enhanced extracellular production of L-asparaginase from Bacillus subtilis 168 by B. subtilis WB600 through a combined strategy. Applied Microbiology and Biotechnology, 101(4), 1509–1520. doi:10.1007/s00253-016-7816-x

Ghosh, S., Chaganti, S. R., & Prakasham, R. S. (2012). Polyaniline nanofiber as a novel immobilization matrix for the anti-leukemia enzyme l-asparaginase. Journal of Molecular Catalysis B: Enzymatic, 74(1–2), 132–137. doi: 10.1016/j.molcatb.2011.09.009

Granvogl, M., & Schieberle, P. (2006). Thermally generated 3-aminopropionamide as a transient intermediate in the formation of acrylamide. Journal of Agricultural and Food Chemistry, 54(16), 5933–5938. doi: 10.1021/jf061150h

Gurung, N., Ray, S., Bose, S., Rai, V., & K, W. F. (2013). A Broader View: Microbial Enzymes and Their Relevance in Industries , Medicine , and Beyond. BioMed Research International, Article 329121. https://doi.org/10.1155/2013/329121

Hendriksen, H. V., Kornbrust, B. A., Ostergaard, P. R., & Stringer, M. A. (2009). Evaluating the potential for enzymatic acrylamide mitigation in a range of food products using an asparaginase from Aspergillus oryzae. Journal of Agricultural and Food Chemistry, 57(10), 4168–4176. doi: 10.1021/jf900174q

Huang, L., Liu, Y., Sun, Y., Yan, Q., & Jiang, Z. (2014). Biochemical characterization of a novel L-asparaginase with low glutaminase activity from Rhizomucor miehei and its application in food safety and leukemia treatment. Applied and Environmental Microbiology, 80(5), 1561–1569. doi: 10.1128/AEM.03523-13

Husain, I., Sharma, A., Kumar, S., & Malik, F. (2016). Purification and characterization of glutaminase free asparaginase from Enterobacter cloacae: In-vitro evaluation of cytotoxic potential against human myeloid leukemia HL-60 cells. PLoS ONE, 11(2), Article e0148877. doi: 10.1371/journal.pone.0148877

Husain, I., Sharma, A., Kumar, S., & Malik, F. (2016b). Purification and characterization of glutaminase free asparaginase from Pseudomonas otitidis: Induce apoptosis in human leukemia MOLT-4 cells. Biochimie, 121, 38–51. doi: 10.1016/j.biochi.2015.11.012

IARC – International Agency for Research on Cancer (2014). Report of the advisory group to recommend priorities for IARC Monographs during 2015-2019. World Health Organization.

Izadpanah, F., Homaei, A., Fernandes, P., & Javadpour, S. (2018). Marine microbial L-asparaginase: Biochemistry, molecular approaches and applications in tumor therapy and in food industry. Microbiological Research, 208, 99–112. doi: 10.1016/j.micres.2018.01.011

Jaskólski, M., Kozak, M., Lubkowski, J., Palm, G., & Wlodawer, A. (2001). Structures of two highly homologous bacterial L-asparaginases: A case of enantiomorphic space groups. Acta Crystallographica Section D: Biological Crystallography, 57(3), 369–377. doi: 10.1107/S0907444900020175

Jiao, L., Chi, H., Lu, Z., Zhang, C., Chia, S. R., Show, P. L. & Tao, Y., et al. (2020). Characterization of a novel type I L-asparaginase from Acinetobacter soli and its ability to inhibit acrylamide formation in potato chips. Journal of Bioscience and Bioengineering, 129(6), 672–678. doi: 10.1016/j.jbiosc.2020.01.007

Jin, C., Wu, X., & Zhang, Y. Relationship between antioxidants and acrylamide formation: A review. Food Research International, 51, 611-620. doi: 10.1016/j.foodres.2012.12.047

Karamitros, C. S., Yashchenok, A. M., Möhwald, H., Skirtach, A. G., & Konrad, M. (2013). Preserving catalytic activity and enhancing biochemical stability of the therapeutic enzyme asparaginase by biocompatible multilayered polyelectrolyte microcapsules. Biomacromolecules, 14(12), 4398–4406. doi: 10.1021/bm401341k

Kidd, J. G. (1953). Regression of transplanted lymphomas induced in vivo by means of normal guinea pig serum. I. Course of transplanted cancers of various kinds in mice and rats given guinea pig serum, horse serum, or rabbit serum. The Journal of experimental medicine, 98(6), 565–582. doi: 10.1084/jem.98.6.565

Kotzia, G. A., & Labrou, N. E. (2007). l-Asparaginase from Erwinia chrysanthemi 3937: Cloning, expression and characterization. Journal of Biotechnology, 127(4), 657–669. doi: 10.1016/j.jbiotec.2006.07.037

Krishnapura, P. R., & Belur, P. D. (2016). Partial purification and characterization of L-asparaginase from an endophytic Talaromyces pinophilus isolated from the rhizomes of Curcuma amada. Journal of Molecular Catalysis B: Enzymatic, 124, 83–91. doi: 10.1016/j.molcatb.2015.12.007

Krishnapura, P. R., Belur, P. D., & Subramanya, S. (2016). A critical review on properties and applications of microbial l-asparaginases. Critical Reviews in Microbiology, 42(5), 720–737. doi: 10.3109/1040841X.2015.1022505

Kumar, K., & Verma, N. (2012). The Various Sources & Application of L-Asparaginase. Asian Journal of Biochemical and Pharmaceutical Research, 2(3), 197–205.

Kunamneni, A., Ogaugwu, C., & Goli, D. (2018). Enzymes as therapeutic agents. In Nunes, C. S., & Kumar, V. (Eds.), Enzymes in Human and Animal Nutrition: Principles and Perspectives (pp. 301–312). https://doi.org/10.1016/B978-0-12-805419-2.00015-0

Labrou, N. E., & Muharram, M. M. (2016). Biochemical characterization and immobilization of Erwinia carotovora L-asparaginase in a microplate for high-throughput biosensing of L-asparagine. Enzyme and Microbial Technology, 92, 86–93. doi: 10.1016/j.enzmictec.2016.06.013

Li, S., Yang, X., Yang, S., Zhu, M., & Wang, X. (2012). Technology prospecting on enzymes: Application, marketing and engineering. Computational and Structural Biotechnology Journal, 2(3), Article e201209017. doi: 10.5936/csbj.201209017

Lincoln, L., Niyonzima, F., & More, S. (2019). Purification and Properties of a Fungal L-Asparaginase from Trichoderma viride Pers: Sf Grey. Journal of Microbiology, Biotechnology and Food Sciences, 9(6), 310–316.

Liu, J. (2018). Acrylamide is formed in the Maillard reaction. Journal of the science of food and agriculture, 98(1), 448–449. doi: 10.1007/s11947-010-0495-1

Ln, R., Doble, M., Rekha, V. P. B., & Pulicherla, K. K. (2011). In silico engineering of L-asparaginase to have reduced glutaminase side activity for effective treatment of acute lymphoblastic leukemia. Journal of Pediatric Hematology/Oncology, 33(8), 617–621. doi: 10.1097/MPH.0b013e31822aa4ec

Mashburn, L. T., & Wriston, J. C. (1963). Tumor inhibitory effect of L-asparaginase. Biochemical and Biophysical Research Communications, 12(1), 50–55. doi: 10.1016/0003-9861(64)90032-3

Mateo, C., Palomo, J. M., & Fernández-Lorente, G. (2007). Improvement of enzyme activity, stability and selectivity via immobilization techniques. Enzyme and Microbial Technology, 40, 1451-1463. doi: 10.1016/j.enzmictec.2007.01.018

Meena, B., Anburajan, L., Dheenan, P. S., Begum, M., Vinithkumar, N. V., Dharani, G., & Kirubagaran, R. (2015). Novel glutaminase free l-asparaginase from Nocardiopsis alba NIOT-VKMA08: Production, optimization, functional and molecular characterization. Bioprocess and Biosystems Engineering, 38(2), 373–388. doi: 10.1007/s00449-014-1277-3

Meghavarnam, A. K., & Janakiraman, S. (2018). Evaluation of acrylamide reduction potential of L-asparaginase from Fusarium culmorum (ASP-87) in starchy products. LWT - Food Science and Technology, 89, 32–37. doi: 10.1016/j.lwt.2017.09.048

Mesias, M., Delgado-Andrade, C., Holgado, F., & Morales, F. J. (2018). Acrylamide content in French fries prepared in households: A pilot study in Spanish homes. Food Chemistry, 260, 44–52. doi: 10.1016/j.foodchem.2018.03.140

Mesias, M., & Morales, F. J. (2016). Acrylamide in coffee: Estimation of exposure from vending machines. Journal of Food Composition and Analysis, 48, 8–12. doi: 10.1016/j.jfca.2016.02.005

Mohan Kumar, N. S., & Manonmani, H. K. (2013). Purification, characterization and kinetic properties of extracellular l-asparaginase produced by Cladosporium sp. World Journal of Microbiology and Biotechnology, 29(4), 577–587. doi: 10.1007/s11274-012-1213-0

Mohan Kumar, N. S., Shimray, C. A., Indrani, D., & Manonmani, H. K. (2014). Reduction of Acrylamide Formation in Sweet Bread with l-Asparaginase Treatment. Food and Bioprocess Technology, 7(3), 741–748. doi: 10.1007/s11947-013-1108-6

Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2014). PRISMA 2009 Flow Diagram Identification. Annals of Internal Medicine, 151(2), 264–269.

Mottram, D. S., Wedzicha, B. L., & Dodson, A. T. (2002). Food chemistry: Acrylamide is formed in the Maillard reaction. Nature, 419(6906), 448–449. doi: 10.1038/419448a

Mu, X., Qiao, J., Qi, L., Dong, P., & Ma, H. (2014). Poly(2-vinyl-4,4-dimethylazlactone)-functionalized magnetic nanoparticles as carriers for enzyme immobilization and its application. ACS Applied Materials and Interfaces, 6(23), 21346–21354. doi: 10.1021/am5063025

Muslim, S. N., Kadmy, I. M. S. A. L., & Hussein, N. H. (2015). Enhancement of the Activity and Stability of L-Asparaginase Food Additive Purified from Acinetobacter baumannii as Anticarcinogenic in Processed Foods. International Journal of Advances in Chemical Engineering and Biological Sciences, 2(1). Retrieved from https://doi.org/10.15242/ijacebs.c0815019

Mustafa, A., Kamal-Eldin, A., Petersson, E. V., Andersson, R., & Åman, P. (2008). Effect of extraction pH on acrylamide content in fresh and stored rye crisp bread. Journal of Food Composition and Analysis, 21(4), 351–355. doi: 10.1016/j.jfca.2008.01.003

Narta, U. K., Kanwar, S. S., & Azmi, W. (2007). Pharmacological and clinical evaluation of l-asparaginase in the treatment of leukemia. Critical Reviews in Oncology/Hematology, 61(3), 208–221. doi: 10.1016/j.critrevonc.2006.07.009

Onishi, Y., Prihanto, A. A., Yano, S., Takagi, K., Umekawa, M., & Wakayama, M. (2015). Effective treatment for suppression of acrylamide formation in fried potato chips using L-asparaginase from Bacillus subtilis. 3 Biotech, 5(5), 783–789. doi: 10.1007/s13205-015-0278-5

Orhan, H., & Aktaş Uygun, D. (2020). Immobilization of L-Asparaginase on Magnetic Nanoparticles for Cancer Treatment. Applied Biochemistry and Biotechnology, 191(4), 1432–1443. doi: 10.1007/s12010-020-03276-z

Outcome of the public consultation on the draft Scientific Opinion of the EFSA Panel on Contaminants in the Food Chain (CONTAM) on acrylamide in food. (2017) EFSA Supporting Publications, 12(6). https://doi.org/10.2903/sp.efsa.2015.en-817

Panel, E., & Chain, F. (2015). Scientific Opinion on acrylamide in food. EFSA Journal, 13(6). doi: 10.2903/j.efsa.2015.4104

Parker, J. K., Balagiannis, D. P., Higley, J., Smith, G., Wedzicha, B. L., & Mottram, D. S. (2012). Kinetic model for the formation of acrylamide during the finish-frying of commercial French fries. Journal of Agricultural and Food Chemistry, 60(36), 9321–9331. doi: 10.1021/jf302415n

Pedreschi, F., Kaack, K., & Granby, K. (2008). The effect of asparaginase on acrylamide formation in French fries. Food Chemistry, 109(2), 386–392. doi: 10.1016/j.foodchem.2007.12.057

Pedreschi, F., Mariotti, S., Granby, K., & Risum, J. (2011). Acrylamide reduction in potato chips by using commercial asparaginase in combination with conventional blanching. LWT - Food Science and Technology, 44(6), 1473–1476. doi: 10.1016/j.lwt.2011.02.004

Pieters, R., Hunger, S. P., Boos, J., Rizzari, C., Silverman, L., Baruchel, A. & Goekbuget, N., et al. (2011). L-asparaginase treatment in acute lymphoblastic leukemia. Cancer, 117(2), 238–249. doi: 10.1002/cncr.25489

Pourhossein, M., & Korbekandi, H. (2014). Cloning, expression, purification and characterisation of Erwinia carotovora L-asparaginase in Escherichia coli. Advanced Biomedical Research, 3(1), 82. doi: 10.4103/2277-9175.127995

Ramya, L. N., Doble, M., Rekha, V. P. B., & Pulicherla, K. K. (2012). L-asparaginase as potent anti-leukemic agent and its significance of having reduced glutaminase side activity for better treatment of acute lymphoblastic leukemia. Applied Biochemistry and Biotechnology, 167, 2144-2159. doi: 10.1007/s12010-012-9755-z

Ravi, A., & Gurunathan, B. (2018). Acrylamide mitigation in fried kochchi kesel chips using free and immobilized fungal asparaginase. Food Technology and Biotechnology, 56(1), 51–57. doi: 10.17113/ftb.56.01.18.5422

Rigon Zimmer, K., Luís Borré, G., da Silva Trentin, D., Woicickoski Júnior, C., Piccoli Frasson, A., de Arruda Graeff, A. & Gomes, P., et al. (2009). Enzimas microbianas de uso terapêutico e diagnóstico clínico. Revista Liberato, 10(14), 123–137. doi: 10.31514/rliberato.2009v10n14.p123

Rocha Junior, C., & Caseli, L. (2017). Adsorption and enzyme activity of asparaginase at lipid Langmuir and Langmuir-Blodgett films. Materials Science and Engineering C, 73, 579–584. doi: 10.1016/j.msec.2016.12.041

Sanghvi, G., Bhimani, K., Vaishnav, D., Oza, T., Dave, G., Kunjadia, P., & Sheth, N. (2016). Mitigation of acrylamide by l-asparaginase from Bacillus subtilis KDPS1 and analysis of degradation products by HPLC and HPTLC. SpringerPlus, 5(1), Article 533. https://doi.org/10.1186/s40064-016-2159-8

Sanny, M., Luning, P. A., Jinap, S., Bakker, E. J., & Van Boekel, M. A. J. S. (2013). Effect of frying instructions for food handlers on acrylamide concentration in French fries: An explorative study. Journal of Food Protection, 76(3), 462–472.

Şenyuva, H. Z., & Gökmen, V. (2005). Study of acrylamide in coffee using an improved liquid chromatography mass spectrometry method: Investigation of colour changes and acrylamide formation in coffee during roasting. Food Additives and Contaminants, 22(3), 214–220. doi: 10.1080/02652030500109834

Shakambari, G., Birendranarayan, A. K., Angelaa Lincy, M. J., Rai, S. K., Ahamed, Q. T., Ashokkumar, B. & Saravanan, M., et al. (2016). Hemocompatible glutaminase free l-asparaginase from marine Bacillus tequilensis PV9W with anticancer potential modulating p53 expression. RSC Advances, 6(31), 25943–25951. doi: 10.1039/c6ra00727a

Shi, R., Liu, Y., Mu, Q., Jiang, Z., & Yang, S. (2017). Biochemical characterization of a novel L-asparaginase from Paenibacillus barengoltzii being suitable for acrylamide reduction in potato chips and mooncakes. International Journal of Biological Macromolecules, 96, 93–99. doi: 10.1016/j.ijbiomac.2016.11.115

Singh, M., Hassan, N., Verma, D., Thakur, P., Panda, B. P., Panda, A. K., Sharma, R. K., Mirza, A., Mansoor, S., Alrokayan, S. H., Khan, H. A., Ahmad, P., & Iqbal, Z. (2020). Design of expert guided investigation of native L-asparaginase encapsulated long-acting cross-linker-free poly (lactic-co-glycolic) acid nanoformulation in an Ehrlich ascites tumor model. Saudi Pharmaceutical Journal, 28(6), 719–728. doi: 10.1016/j.jsps.2020.04.014

Souza, P. M., de Freitas, M. M., Cardoso, S. L., Pessoa, A., Guerra, E. N. S., & Magalhães, P. O. (2017). Optimization and purification of L-asparaginase from fungi: A systematic review. Critical Reviews in Oncology/Hematology, 120, 194–202. doi: 10.1016/j.critrevonc.2017.11.006

Sukhoverkov, K. V., & Kudryashova, E. V. (2015). PEG-chitosan and glycol-chitosan for improvement of biopharmaceutical properties of recombinant L-asparaginase from Erwinia carotovora. Biochemistry, 80(1), 113–119. doi: 10.1134/S0006297915010137

Tyl, R. W., & Friedman, M. A. (2003). Effects of acrylamide on rodent reproductive performance. Reproductive Toxicology, 17(1), 1–13. doi: 10.1016/S0890-6238(02)00078-3

Ulu, A. (2020). Metal–organic frameworks (MOFs): a novel support platform for ASNase immobilization. Journal of Materials Science, 55(14), 6130–6144. doi: 10.1007/s10853-020-04452-6

Ulu, A., Koytepe, S., & Ates, B. (2016). Synthesis and characterization of biodegradable pHEMA-starch composites for immobilization of L-asparaginase. Polymer Bulletin, 73(7), 1891–1907. doi: 10.1007/s00289-015-1583-1

Vala, A. K., Sachaniya, B., Dudhagara, D., Panseriya, H. Z., Gosai, H., Rawal, R., & Dave, B. P. (2018). Characterization of L-asparaginase from marine-derived Aspergillus niger AKV-MKBU, its antiproliferative activity and bench scale production using industrial waste. International Journal of Biological Macromolecules, 108, 41–46. doi: 10.1016/j.ijbiomac.2017.11.114

Van Den Berg, H. (2011). Asparaginase revisited. Leukemia and Lymphoma, 52 (2), 168-178. doi: 10.3109/10428194.2010.537796

Varma, R., Kanapala, S., V, N. S. B., Bodaiah, B., & Poda, S. (2016). Partial purification , characterization and optimization of anti-leukemic enzyme L-Asparaginase from mangrove soil Actinobacteria. Journal of Pharmacy Research, 10(7), 502–511.

Verma, N., Kumar, K., Kaur, G., & Anand, S. (2007). L-asparaginase: A promising chemotherapeutic agent. Critical Reviews in Biotechnology, 27(1), 45–62. doi: 10.1080/07388550601173926

Xu, F., Oruna-Concha, M. J., & Elmore, J. S. (2016). The use of asparaginase to reduce acrylamide levels in cooked food. Food Chemistry, 210, 163–171. doi: 10.1016/j.foodchem.2016.04.105

Zamora, R., & Hidalgo, F. J. (2008). Contribution of lipid oxidation products to acrylamide formation in model systems. Journal of Agricultural and Food Chemistry, 56, 6075–6080. doi: 10.1021/jf073047d

Zhang, Y. Q., Tao, M. L., Shen, W. De, Zhou, Y. Z., Ding, Y., Ma, Y., & Zhou, W. L. (2004). Immobilization of L-asparaginase on the microparticles of the natural silk sericin protein and its characters. Biomaterials, 25(17), 3751–3759. doi: 10.1016/j.biomaterials.2003.10.019

Zuo, S., Zhang, T., Jiang, B., & Mu, W. (2015). Reduction of acrylamide level through blanching with treatment by an extremely thermostable l-asparaginase during French fries processing. Extremophiles, 19(4), 841–851. doi: 10.1007/s00792-015-0763-0

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21/08/2021

How to Cite

OLIVEIRA, M. D. de .; VAZ, C. J. T. .; OLIVEIRA, L. M. de .; GUIDINI, C. Z. . L-asparaginase: therapeutic use and applications in the food industry – a review. Research, Society and Development, [S. l.], v. 10, n. 10, p. e596101018980, 2021. DOI: 10.33448/rsd-v10i10.18980. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/18980. Acesso em: 17 nov. 2024.

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Exact and Earth Sciences