Skip to main content
Log in

Effects of freezing and the cryoprotectant lactobionic acid in the structure of GlnK protein evaluated by circular dichroism (CD) and isothermal titration calorimetry (ITC)

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

Freezing is a widely applied method in food preservation. The technique has negative effects on sensory and textural properties of some foods. In this study the effects of the freeze–thaw process and lactobionic acid (LBA) as a cryoprotectant on GlnK protein solution were evaluated by circular dichroism (CD) analysis and isothermal titration calorimetry (ITC). The freeze–thaw cycles caused changes in GlnK conformation and interactions with small ligands (adenosine triphosphate, ATP). CD assay demonstrated changes in the molar ellipticity values of the samples subjected to freezing, indicating conformational changes to the GlnK protein. Additionally, ITC analysis indicated that the freeze–thaw process caused changes in the interaction properties of GlnK with its ligand ATP. LBA cryoprotectant activity was also evaluated and with both of the techniques it was demonstrated that the compound prevented the damage caused by the freeze–thaw process, thereby maintaining the characteristics of the samples.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alvarez MD, Fernández C, Canet W (2010) Oscillatory rheological properties of fresh and frozen/thawed mashed potatoes as modified by different cryoprotectants. Food Bioprocess Technol 3:55–70. doi:10.1007/s11947-007-0051-9

    Article  CAS  Google Scholar 

  • Arcondéguy T, Jack R, Merrick M, Arconde T (2001) P II signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105. doi:10.1128/MMBR.65.1.80

    Article  Google Scholar 

  • Ariyaprakai S, Tananuwong K (2015) Freeze–thaw stability of edible oil-in-water emulsions stabilized by sucrose esters and Tweens. J Food Eng 152:57–64. doi:10.1016/j.jfoodeng.2014.11.023

    Article  CAS  Google Scholar 

  • Bonatto AC, Couto GH, Souza EM, Araújo LM, Pedrosa FO, Noindorf L, Benelli EM (2007) Purification and characterization of the bifunctional uridylyltransferase and the signal transducing proteins GlnB and GlnK from Herbaspirillum seropedicae. Protein Expr Purif 55:293–299. doi:10.1016/j.pep.2007.04.012

    Article  CAS  Google Scholar 

  • Bonatto AC, Souza EM, Oliveira MAS, Monteiro RA, Chubatsu LS, Huergo LF, Pedrosa FO (2012) Uridylylation of Herbaspirillum seropedicae GlnB and GlnK proteins is differentially affected by ATP, ADP and 2-oxoglutarate in vitro. Arch Microbiol 194:643–652. doi:10.1007/s00203-012-0799-9

    Article  CAS  Google Scholar 

  • Brown RK, Brandts JM, O’Brien R, Peters WB (2009) ITC-derived binding constants: using microgram quantities of protein, label-free biosensors techniques and applications. Label-Free Biosens. doi:10.1017/CBO9780511626531.012

    Google Scholar 

  • Cao Z, Liu R, Yang B (2013) Potential toxicity of sarafloxacin to catalase: spectroscopic, ITC and molecular docking descriptions. Spectrochim Acta Part A Mol Biomol Spectrosc 115:457–463. doi:10.1016/j.saa.2013.06.093

    Article  CAS  Google Scholar 

  • Charloux C, Paul M, Loisance D, Astier A (1995) Inhibition of hydroxyl radical production. Free Radic Biol Med 19:699–704

    Article  CAS  Google Scholar 

  • Corrêa DHA, Ramos CHI (2009) The use of circular dichroism spectroscopy to study protein folding, form and function. Afr J Biochem Res 3:164–173

    Google Scholar 

  • Dimitrova MN, Matsumura H, Terezova N, Neytchev V (2002) Binding of globular proteins to lipid membranes studied by isothermal titration calorimetry and fluorescence. Colloids Surf B Biointerfaces 24:53–61. doi:10.1016/S0927-7765(01)00248-X

    Article  CAS  Google Scholar 

  • Furukawa Y, Inohara N, Yokoyama E (2005) Growth patterns and interfacial kinetic supercooling at ice/water interfaces at which anti-freeze glycoprotein molecules are adsorbed. J Cryst Growth 275:167–174. doi:10.1016/j.jcrysgro.2004.10.085

    Article  CAS  Google Scholar 

  • García-Arias MT, Pontes EA, García-Linares MC, García-Fernández MC, Sánchez-Muniz FJ (2003) Grilling of sardine fillets. Effects of frozen and thawed modality on their protein quality. LWT Food Sci Technol 36:763–769. doi:10.1016/S0023-6438(03)00097-5

    Article  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. Proteomics Protoc Handb. doi:10.1385/1-59259-890-0:571

    Google Scholar 

  • Green BA, Ruey JY, Scott EJV (2009) Clinical and cosmeceutical uses of hydroxyacids. Clin Dermatol 27:495–501. doi:10.1016/j.clindermatol.2009.06.023

    Article  Google Scholar 

  • Güler G, Vorob MM, Vogel V, Mäntele W (2016) Proteolytically-induced changes of secondary structural protein conformation of bovine serum albumin monitored by Fourier transform infrared (FT-IR) and UV-circular dichroism spectroscopy. Spectrochim Acta Part A Mol Biomol Spectrosc 161:8–18. doi:10.1016/j.saa.2016.02.013

    Article  Google Scholar 

  • Gutiérrez LF, Hamoudi S, Belkacemi K (2012) Lactobionic acid: a high value-added lactose derivative for food and pharmaceutical applications. Int Dairy J 26:103–111. doi:10.1016/j.idairyj.2012.05.003

    Article  Google Scholar 

  • Herrera JJ, Pastoriza L, Sampedro G (2001) A DSC study on the effects of various maltodextrins and sucrose on protein changes in frozen-stored minced blue whiting muscle. J Sci Food Agric 81:377–384. doi:10.1002/1097-0010(200103)81:4<377:AID-JSFA820>3.0.CO;2-0

    Article  CAS  Google Scholar 

  • Hubálek Z (2003) Protectants used in the cryopreservation of microorganisms. Cryobiology 46:205–229. doi:10.1016/S0011-2240(03)00046-4

    Article  Google Scholar 

  • Iijima T (1998) Thermal analysis of cryoprotective solutions for red blood cells. Cryobiology 36:165–173. doi:10.1006/cryo.1998.2075

    Article  CAS  Google Scholar 

  • Isaacson Y, Salem O, Shepherd RE, Thiel DHV (1989) Lactobionic acid as an iron chelator: a rationale for its effectiveness as an organ preservant. Life Sci 45:2373–2380

    Article  CAS  Google Scholar 

  • Kaale LD, Eikevik TM (2013) A study of the ice crystal sizes of red muscle of pre-rigor Atlantic salmon (Salmo salar) fillets during superchilled storage. J Food Eng 119:544–551. doi:10.1016/j.jfoodeng.2013.06.002

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685

    Article  CAS  Google Scholar 

  • Nielsen PM (2009) Meat based food product comprising lactobionic acid. United States patent application pub. no.: US 2009/0214752 A1. 371: 4–7. http://www.google.ch/patents/US20090214752. Accessed 26 June 2015

  • Park YJ, Kim KH, Lim DW, Lee EK (2015) Effects of pH and protein conformation on in-solution complexation between bovine α-lactalbumin and oleic acid: binding trend analysis by using SPR and ITC. Process Biochem 50:1379–1387. doi:10.1016/j.procbio.2015.05.018

    Article  CAS  Google Scholar 

  • Perozzo R, Folkers G, Scapozza L (2004) Thermodynamics of protein–ligand interactions: history, presence, and future aspects. J Recept Signal Transduct Res 24:1–52. doi:10.1081/RRS-120037896

    Article  CAS  Google Scholar 

  • Radchenko MV, Thornton J, Merrick M (2010) Control of AmtB–GlnK complex formation by intracellular levels of ATP, ADP, and 2-oxoglutarate. J Biol Chem 285:31037–31045. doi:10.1074/jbc.M110.153908

    Article  CAS  Google Scholar 

  • Rawson A, Tiwari BK, Tuohy M, Brunton N (2012) Impact of frozen storage on polyacetylene content, texture and colour in carrots disks. J Food Eng 108:563–569. doi:10.1016/j.jfoodeng.2011.09.003

    Article  CAS  Google Scholar 

  • Rispens T, Lakemond CMM, Derksen NIL, Aalberse RC (2008) Detection of conformational changes in immunoglobulin G using isothermal titration calorimetry with low-molecular-weight probes. Anal Biochem 380:303–309. doi:10.1016/j.ab.2008.06.001

    Article  CAS  Google Scholar 

  • Shepherd RE, Isaacson Y, Chensny L, Zhang S, Kortes R, John K (1993) Lactobionic and gluconic acid complexes of FeII and FeIII; control of oxidation pathways by an organ transplantation preservant. J Inorg Biochem 49:23–48. doi:10.1016/0162-0134(93)80046-C

    Article  CAS  Google Scholar 

  • Sofi FR, Raju CV, Lakshmisha IP, Singh RR (2016) Antioxidant and antimicrobial properties of grape and papaya seed extracts and their application on the preservation of Indian mackerel (Rastrelliger kanagurta) during ice storage. J Food Sci Technol 53:104–117. doi:10.1007/s13197-015-1983-0

    Article  CAS  Google Scholar 

  • Tasic-Kostov M, Pavlovic D, Lukic M, Jaksic I, Arsic I, Savic S (2012) Lactobionic acid as antioxidant and moisturizing active in alkyl polyglucoside-based topical emulsions: the colloidal structure, stability and efficacy evaluation. Int J Cosmet Sci 34:424–434. doi:10.1111/j.1468-2494.2012.00732.x

    Article  CAS  Google Scholar 

  • Wang P, Chen H, Mohanad B, Xu L, Ning Y, Xu J, Wu F, Yang N, Jin Z, Xu X (2014a) Effect of frozen storage on physico-chemistry of wheat gluten proteins: studies on gluten-, glutenin- and gliadin-rich fractions. Food Hydrocolloids 39:187–194. doi:10.1016/j.foodhyd.2014.01.009

    Article  Google Scholar 

  • Wang P, Xu L, Nikoo M, Ocen D, Wu F, Yang N, Jin Z, Xu X (2014b) Effect of frozen storage on the conformational, thermal and microscopic properties of gluten: Comparative studies on gluten-, glutenin- and gliadin-rich fractions. Food Hydrocolloids 35:238–246. doi:10.1016/j.foodhyd.2013.05.015

    Article  Google Scholar 

  • Whamond GS, Thornton JM (2006) An analysis of intron positions in relation to nucleotides, amino acids, and protein secondary structure. J Mol Biol. doi:10.1016/j.jmb.2006.03.029

    Google Scholar 

  • Whitmore L, Wallace B (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392–400. doi:10.1002/bip.20853

    Article  CAS  Google Scholar 

  • Xu Y, Cheah E, Carr PD, Heeswijk WCV, Westerhoff HV, Vasudevan SG, Ollis DL (1998) GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282:149–165. doi:10.1006/jmbi.1998.1979

    Article  CAS  Google Scholar 

  • Zhao J, Dong F, Li Y, Kong B, Liu Q (2015) Effect of freeze–thaw cycles on the emulsion activity and structural characteristics of soy protein isolate. Process Biochem 50:1607–1613. doi:10.1016/j.procbio.2015.06.021

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Graduation Program of Food Engineering (PPGEAL-UFPR), National Institute of Science and Technology on Biological Nitrogen Fixation (INCT-UFPR) and Coordination of Higher Education Personnel Improvement (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcos Rogério Mafra.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Misugi, C.T., Savi, L.K., Iwankiw, P.K. et al. Effects of freezing and the cryoprotectant lactobionic acid in the structure of GlnK protein evaluated by circular dichroism (CD) and isothermal titration calorimetry (ITC). J Food Sci Technol 54, 236–243 (2017). https://doi.org/10.1007/s13197-016-2455-x

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-016-2455-x

Keywords

Navigation