Copper‑containing amine oxidase purified from Lathyrus sativus as a modulator of human neutrophil functions

Pietrangeli,Paola; Capuozzo,Elisabetta; Mateescu,Mircea   Alexandru; Marcocci,Lucia

doi:10.3892/ijmm.2020.4535

Copper‑containing amine oxidase purified from Lathyrus sativus as a modulator of human neutrophil functions

Authors:
- Paola Pietrangeli
- Elisabetta Capuozzo
- Mircea Alexandru Mateescu
- Lucia Marcocci
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Affiliations: Department of Biochemical Sciences ‘A. Rossi Fanelli’, Sapienza University of Rome, I‑00185 Rome, Italy, Department of Chemistry, Research Chair on Enteric Dysfunctions ‘Allerdys’ and CERMO‑FC Centre, University of Quebec at Montreal (UQAM), Montreal, (QC) H3C 3P8, Canada
Published online on: March 11, 2020 https://doi.org/10.3892/ijmm.2020.4535
Pages: 1583-1590

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Abstract

Over the last few decades, copper‑containing amine oxidase (Cu‑AO) from vegetal sources, and belonging to the class of diamine oxidase, has been documented to exhibit beneficial effects in both in vivo and ex vivo animal models of inflammatory or allergic conditions, including asthma‑like reaction and myocardial or intestinal ischemia‑reperfusion injuries. The aim of the present study was to assess the potential of vegetal Cu‑AO as an anti‑inflammatory and an antiallergic agent and to clarify its antioxidant properties. In cell‑free systems, the reactive oxygen species and reactive nitrogen species scavenging properties of Cu‑AO that is purified from Lathyrus sativus were investigated. Its effect on the formyl‑methionyl‑leucyl‑phenylalanine peptide (fMLP)‑activated cellular functions of human neutrophils were subsequently analyzed. The obtained results demonstrated that Cu‑AO is not a scavenger of superoxide or nitric oxide, and does not decompose hydrogen peroxide. However, it inhibits the fMLP‑dependent superoxide generation, elastase release and cell migration, and interferes with the process of calcium flux, supporting the idea that plant Cu‑AO can interact with human neutrophils to modulate their inflammatory function. Therefore, the importance of these properties on the possible use of vegetal Cu‑AO to control inflammatory conditions, particularly intestinal inflammation, is discussed in the current study.

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1	Kipanyula MJ, Seke Etet PF, Vecchio L, Farahna M, Nukenine EN and Nwabo Kamdje AH: Signaling pathways bridging microbial-triggered inflammation and cancer. Cell Signal. 25:403–416. 2013. View Article : Google Scholar
2	Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P and Halbwachs-Mecarelli L: Neutrophils: Molecules, functions and pathophysiological aspects. Lab Invest. 80:617–653. 2000. View Article : Google Scholar : PubMed/NCBI
3	Liew PX and Kubes P: The neutrophil’s role during health and disease. Physiol Rev. 99:1223–1248. 2019. View Article : Google Scholar : PubMed/NCBI
4	Tintinger GR, Anderson R and Feldman C: Pharmacological approaches to regulate neutrophil activity. Semin Immunopathol. 35:395–409. 2013. View Article : Google Scholar : PubMed/NCBI
5	Dinallo V, Marafini I, Di Fusco D, Laudisi F, Franzè E, Di Grazia A, Figliuzzi MM, Caprioli F, Stolfi C, Monteleone I and Monteleone G: Neutrophil extracellular traps sustain inflammatory signals in ulcerative colitis. J Crohns Colitis. 27:772–784. 2019. View Article : Google Scholar
6	Mumy KL and McCormick BA: The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol. 9:697–701. 2009. View Article : Google Scholar : PubMed/NCBI
7	Medina MA, Urdiales JL, Rodríguez-Caso C, Ramírez FJ and Sánchez-Jiménez F: Biogenic amines and polyamines: Similar biochemistry for different physiological missions and biomedical applications. Crit Rev Biochem Mol Biol. 38:23–59. 2003. View Article : Google Scholar : PubMed/NCBI
8	Mondovì B, Fogel WA, Federico R, Calinescu C, Mateescu MA, Rosa AC and Masini E: Effects of amine oxidases in allergic and histamine-mediated conditions. Recent Pat Inflamm Allergy Drug Discov. 7:20–34. 2013. View Article : Google Scholar
9	McIntire WS and Hartmann C: Copper containing amine oxidases. Principles and Applications of Quinoproteins. Davidson VL: Marcel Decker; New York, NY: pp. 97–171. 1992
10	Masini E, Vannacci A, Giannini L, Befani O, Nistri S, Mateescu MA, Mannaioni PF, Mondovì B and Federico R: Effect of a plant histaminase on asthmalike reaction induced by inhaled antigen in sensitized guinea pig. Eur J Pharmacol. 502:253–264. 2004. View Article : Google Scholar : PubMed/NCBI
11	Masini E, Pierpaoli S, Marzocca C, Mannaioni PF, Pietrangeli P, Mateescu MA, Zelli M, Federico R and Mondovì B: Protective effects of a plant histaminase in myocardial ischaemia and reperfusion injury in vivo. Biochem Biophys Res Commun. 309:432–439. 2003. View Article : Google Scholar : PubMed/NCBI
12	Masini E, Cuzzocrea S, Bani D, Mazzon E, Muja C, Mastroianni R, Fabrizi F, Pietrangeli P, Marcocci L, Mondovì B, et al: Beneficial effect of a plant histaminase in a rat model of splanchnic artery occlusion and reperfusion. Shock. 27:409–415. 2007. View Article : Google Scholar : PubMed/NCBI
13	Pietrangeli P, Federico R, Mondovì B and Morpurgo L: Substrate specificity of copper-containing plant amine oxidases. J Inorg Biochem. 101:997–1004. 2007. View Article : Google Scholar : PubMed/NCBI
14	Yamaki K, Thorlacius H, Xie X, Lindbom L, Hedqvist P and Raud J: Characteristics of histamine-induced leukocyte rolling in the undisturbed microcirculation of the rat mesentery. Br J Pharmacol. 123:390–399. 1998. View Article : Google Scholar : PubMed/NCBI
15	Mateescu MA, Dumoulin MJ, Wang XT, Nadeau R and Mondovì B: A new physiological role of copper amine oxidases: Cardioprotection against reactive oxygen intermediates. J Physiol Pharmacol. 48(Suppl): S110–S121. 1997.
16	Jalkanen S and Salmi M: VAP-1 and CD73, endothelial cell surface enzymes in leukocyte extravasation. Arterioscler Thromb Vasc Biol. 28:18–26. 2008. View Article : Google Scholar
17	Angelini R, Rea G, Federico R and D’Ovidio R: Spatial distribution and temporal accumulation of mRNA encoding diamine oxidase during lentil (Lens culinaris Medicus) seedling development. Plant Sci. 119:103–113. 1996. View Article : Google Scholar
18	Padiglia A, Cogoni A and Floris G: Characterization of amine oxidases from Pisum, Lens, Lathyrus and Cicer. Phytochemistry. 30:3895–3897. 1991. View Article : Google Scholar
19	Pietrangeli P, Nocera S, Federico R, Mondovì B and Morpurgo L: Inactivation of copper-containing amine oxidases by turnover products. Eur J Biochem. 71:146–152. 2004. View Article : Google Scholar
20	Jumarie C, Séïde M, Marcocci L, Pietrangeli P and Mateescu MA: Diamine oxidase from white pea (Lathyrus sativus) combined with catalase protects the human intestinal Caco-2 cell line from histamine damage. Appl Biochem Biotechnol. 182:1171–1181. 2017. View Article : Google Scholar : PubMed/NCBI
21	Morpurgo L, Agostinelli E, Befani O and Mondovì B: Reactions of bovine serum amine oxidase with NN-diethyldithiocarbamate. Selective removal of one copper ion. Biochem J. 248:865–870. 1987. View Article : Google Scholar : PubMed/NCBI
22	Brumby PE and Massey V: Determination of nonheme iron, total iron, and copper. Methods Enzymol. 10:473–474. 1967.
23	Ferrante A and Thong YH: Optimal conditions for simultaneous purification of mononuclear and polymorphonuclear leucocytes from human blood by the Hypaque-Ficoll method. J Immunol Methods. 36:109–117. 1980. View Article : Google Scholar : PubMed/NCBI
24	Tennant JR: Evaluation of the Trypan Blu technique for determination of cell viability. Transplantation. 2:685–694. 1964. View Article : Google Scholar : PubMed/NCBI
25	McCord JM and Fridovich I: Superoxide Dismutase: An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 24:6049–6055. 1969.
26	Cross AR, Parkinson JF and Jones OT: The superoxide-generating oxidase of leucocytes. NADPH-dependent reduction of flavin and cytochrome b in solubilized preparations. Biochem J. 223:337–344. 1984. View Article : Google Scholar : PubMed/NCBI
27	Margoliash E and Frohwirt N: Spectrum of horse heart cytochrome c. Biochem J. 71:570–572. 1959. View Article : Google Scholar : PubMed/NCBI
28	Marcocci L, Packer L, Droy-Lefaix MT, Sekaki A and Gardès-Albert M: Antioxidant action of Ginkgo biloba extract EGb 761. Methods Enzymol. 234:462–475. 1994. View Article : Google Scholar : PubMed/NCBI
29	Capuozzo E, Pecci L, Giovannitti F, Baseggio Conrado A and Fontana M: Oxidative and nitrative modifications of enkephalins by human neutrophils: effect of nitroenkephalin on leukocyte functional responses. Amino Acids. 43:875–884. 2012. View Article : Google Scholar
30	Salerno C and Capuozzo E: Effects of the semisynthetic bis-indole derivative KAR-2 on store-operated calcium entry in human neutrophils. Arch Biochem Biophys. 537:133–137. 2013. View Article : Google Scholar : PubMed/NCBI
31	Thastrup O, Cullen PJ, Drøbak BK, Hanley MR and Dawson AP: Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA. 87:2466–2470. 1990. View Article : Google Scholar : PubMed/NCBI
32	Clemens RA and Lowell CA: Store-operated calcium signaling in neutrophils. J Leukoc Biol. 98:497–502. 2015. View Article : Google Scholar : PubMed/NCBI
33	Clemens RA and Lowell CA: CRAC channel regulation of innate immune cells in health and disease. Cell Calcium. 78:56–65. 2019. View Article : Google Scholar : PubMed/NCBI
34	Salminen TA, Smith DJ, Jalkanen S and Johnson MS: Structural model of the catalytic domain of an enzyme with cell adhesion activity: Human vascular adhesion protein-1 (HVAP-1) D4 domain is an amine oxidase. Protein Eng. 11:1195–1204. 1998. View Article : Google Scholar
35	Masini E, Vannacci A, Marzocca C, Mannaioni PF, Befani O, Federico R, Toma A and Mondovì B: A plant histaminase modulates cardiac anaphylactic response in guinea pig. Biochem Biophys Res Commun. 296:840–846. 2002. View Article : Google Scholar : PubMed/NCBI
36	Dorward DA, Lucas CD, Chapman GB, Haslett C, Dhaliwal K and Rossi AG: The role of formylated peptides receptor 1 in governing neutrophil function during acute inflammation. Am J Pathol. 185:1172–1184. 2015. View Article : Google Scholar : PubMed/NCBI
37	Futosi K, Fodor S and Mócsai A: Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol. 17:638–650. 2013. View Article : Google Scholar : PubMed/NCBI
38	Yang X, Jin H, Cai X, Li S and Shen Y: Structural and mechanistic insights into the activation of stromal interaction molecule 1 (STIM1). Proc Natl Acad Sci USA. 109:5657–5662. 2012. View Article : Google Scholar : PubMed/NCBI
39	Marcocci L, Pietrangeli P, Befani O, Mavelli I and Mondovì B: Inhibition of bovine serum amine oxidase activity by hemoglobin. Life Chem Rep. 9:171–177. 1991.
40	Dini L, Agostinelli E and Mondoví B: Cultured hepatocytes bind and internalize bovine serum amine oxidase-gold complexes. Biochem Biophys Res Commun. 179:1169–1174. 1991. View Article : Google Scholar : PubMed/NCBI
41	Franc V, Řehulka P, Medda R, Padiglia A, Floris G and Šebela M: Analysis of the glycosylation pattern of plant copper amine oxidases by MALDITOF/TOF-MS coupled manual chromatographic separation of glycans and glycopeptides. Electrophoresis. 34:2357–2367. 2013. View Article : Google Scholar : PubMed/NCBI
42	Wang X, Pietrangeli P, Mateescu MA and Mondovì B: Extended substrate specificity of serum amine oxidase: Possible involvement in protein posttranslational modification. Biochem Biophys Res Commun. 223:91–97. 1996. View Article : Google Scholar : PubMed/NCBI
43	Kivi E, Elima K, Aalto K, Nymalm Y, Auvinen K, Koivunen E, Otto DM, Crocker PR, Salminen TA, Salmi M and Jalkanen S: Human Siglec-10 can bind to vascular adhesion protein-1 and serves as its substrate. Blood. 114:5385–5392. 2009. View Article : Google Scholar : PubMed/NCBI
44	Fournier BM and Parkos CA: The role of neutrophils during intestinal inflammation. Mucosal Immunol. 5:354–366. 2012. View Article : Google Scholar : PubMed/NCBI
45	Calinescu C, Mondovi B, Federico R, Ispas-Szabo P and Mateescu MA: Carboxymethyl starch: Chitosan monolithic matrices containing diamine oxidase and catalase for intestinal delivery. Int J P harm. 428:48–56. 2012. View Article : Google Scholar