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Published in: European Journal of Nutrition 1/2016

01-02-2016 | Original Contribution

Effect of neonatal malnutrition on expression of nitric oxide synthase enzyme, production of free radicals and in vitro viability of alveolar macrophages infected with methicillin-sensitive and methicillin-resistant Staphylococcus aureus

Authors: Natália Gomes de Morais, Thacianna Barreto da Costa, Amanda Lúcia Farias Pedrosa, Maria Carolina Accioly Brelaz de Castro, Suênia Cunha da Gonçalves de Albuquerque, Valéria Rêgo Alves Pereira, Milena de Paiva Cavalcanti, Célia Maria Machado Barbosa de Castro

Published in: European Journal of Nutrition | Issue 1/2016

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Abstract

Objective

Evaluate the effects of neonatal malnutrition on the microbicidal response and viability of in vitro macrophages infected with Staphylococcus aureus sensitive/resistant to methicillin.

Methods

Male Wistar rats (n = 24) were divided into two distinct groups: nourished (rats breast-fed by mothers undergoing diet with 17 % casein) and malnourished (rats breast-fed by mothers undergoing diet with 8 % casein). Macrophages were recovered after surgical tracheostomy procedure by collecting bronchoalveolar lavage. Four systems were established: negative control, composed only by phagocytes; positive control, macrophages plus lipopolysaccharide; and two test systems, macrophages plus Staphylococcus aureus sensitive and resistant to methicillin. Plates were incubated at 37 °C for 24 h. After this period, tests for the analysis of cell viability and microbicidal response were performed. In the statistical analysis, the Student’s t and ANOVA tests were used, accepting p < 0.05.

Results

The neonatal malnutrition impaired the animals’ body weight. There was a lower expression of the inducible nitric oxide enzyme (iNOS), nitric oxide production, and viability of macrophages infected with methicillin-resistant Staphylococcus aureus. However, increased production of superoxide anion in the malnourished group was detected.

Conclusion

Neonatal malnutrition focusing on critical periods of development promoted lower expression of iNOS, nitric oxide production, cell viability, and exacerbated reactive oxygen species production. The high levels of reactive oxygen species may favor the onset of serious and systemic infections with fatal outcome if associated with methicillin-resistant Staphylococcus aureus.
Literature
1.
go back to reference Pereira KNF, Vitoriano ILS, Melo MPP, Aragão RS, Toscano AE, Silva HJ, De Castro RM (2009) Effects of malnutrition and/or neonatal inhibition of serotonin reuptake in neuromuscular development of the gastrointestinal tract: review of literature. Neurobiology 72(2):215–221 Pereira KNF, Vitoriano ILS, Melo MPP, Aragão RS, Toscano AE, Silva HJ, De Castro RM (2009) Effects of malnutrition and/or neonatal inhibition of serotonin reuptake in neuromuscular development of the gastrointestinal tract: review of literature. Neurobiology 72(2):215–221
2.
5.
go back to reference Cruviel WM, Júnior DM, Araújo JAP, Catelan TTT, Souza AWS, Silva NP, Andrade LEC (2010) Fundamentos da imunidade inata com ênfase nos mecanismos moleculares e celulares da resposta inflamatória. Rev Bras Reumatol 50(4):434–461 Cruviel WM, Júnior DM, Araújo JAP, Catelan TTT, Souza AWS, Silva NP, Andrade LEC (2010) Fundamentos da imunidade inata com ênfase nos mecanismos moleculares e celulares da resposta inflamatória. Rev Bras Reumatol 50(4):434–461
6.
go back to reference França TGD, Ishikawa LLW, Zorzella-Pezavento SFG, Chiuso-Minicucci F, Guerino CPF, Cunha MLRS, Sartori A (2009) Immunization protected well nourished mice but not undernourished ones from lung injury in Methicillin-resistant Staphylococcus aureus (MRSA) infection. BMC Microbiol 9:240. doi:10.1186/1471-2180-9-240 CrossRef França TGD, Ishikawa LLW, Zorzella-Pezavento SFG, Chiuso-Minicucci F, Guerino CPF, Cunha MLRS, Sartori A (2009) Immunization protected well nourished mice but not undernourished ones from lung injury in Methicillin-resistant Staphylococcus aureus (MRSA) infection. BMC Microbiol 9:240. doi:10.​1186/​1471-2180-9-240 CrossRef
8.
go back to reference Zecconi A, Scali F (2013) Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunol Lett 150(1–2):12–22CrossRef Zecconi A, Scali F (2013) Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunol Lett 150(1–2):12–22CrossRef
9.
go back to reference Faria NA, Oliveira DC, Westh H, Monnet DL, Larsen AR, Skov R, De Lencastre H (2005) Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol 43:1836–1842CrossRef Faria NA, Oliveira DC, Westh H, Monnet DL, Larsen AR, Skov R, De Lencastre H (2005) Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol 43:1836–1842CrossRef
10.
go back to reference Gordon RJ, Lowy FD (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 16:209–213CrossRef Gordon RJ, Lowy FD (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 16:209–213CrossRef
11.
go back to reference Shibabaw A, Abebe T, Mihret A (2014) Antimicrobial susceptibility pattern of nasal Staphylococcus aureus among Dessie Referral Hospital health care workers, Dessie, Northeast Ethiopia. Internat J Infect Dis, 2:1–4. doi:10.1016/j.ijid.2014.03.1386 Shibabaw A, Abebe T, Mihret A (2014) Antimicrobial susceptibility pattern of nasal Staphylococcus aureus among Dessie Referral Hospital health care workers, Dessie, Northeast Ethiopia. Internat J Infect Dis, 2:1–4. doi:10.​1016/​j.​ijid.​2014.​03.​1386
12.
go back to reference Morais NG, Costa TB, Almeida TM, Severo MS, De Castro CMMB (2013) Parâmetros imunológicos de macrófagos frente à infecção por Staphylococcus aureus meticilina sensível/resistente. J Bras Patol Med Lab 49(2):84–90. doi:10.1590/S1676-24442013000200002 CrossRef Morais NG, Costa TB, Almeida TM, Severo MS, De Castro CMMB (2013) Parâmetros imunológicos de macrófagos frente à infecção por Staphylococcus aureus meticilina sensível/resistente. J Bras Patol Med Lab 49(2):84–90. doi:10.​1590/​S1676-2444201300020000​2 CrossRef
13.
go back to reference Too HP (2003) Real time PCR quantification of GFR-2 alternatively spliced isoforms in murine brain and peripheral tissues. Mol Brain Res Amst 114:146–154CrossRef Too HP (2003) Real time PCR quantification of GFR-2 alternatively spliced isoforms in murine brain and peripheral tissues. Mol Brain Res Amst 114:146–154CrossRef
14.
go back to reference Gonçalves SC, Régis-da-Silva CG, Brito MEF, Brandão-Filho SP, Paiva-Cavalcanti M (2012) Application of the mammalian glyceraldehyde-3-phosphate dehydrogenase gene for sample quality control in multiplex PCR for diagnosis of leishmaniasis. J Venom Anim Toxins incl Trop Dis 18(2):188–197CrossRef Gonçalves SC, Régis-da-Silva CG, Brito MEF, Brandão-Filho SP, Paiva-Cavalcanti M (2012) Application of the mammalian glyceraldehyde-3-phosphate dehydrogenase gene for sample quality control in multiplex PCR for diagnosis of leishmaniasis. J Venom Anim Toxins incl Trop Dis 18(2):188–197CrossRef
15.
go back to reference Araujo FRG, De Castro CMMB, Rocha JA, Sampaio B, Diniz MFA, Eve LB, Montarroyos UR (2012) Perialveolar bacterial microbiota and bacteraemia after dental alveolitis in adult rats that had been subjected to neonatal malnutrition. Br J Nutr 107:996–1005. doi:10.1017/S000711451100393X CrossRef Araujo FRG, De Castro CMMB, Rocha JA, Sampaio B, Diniz MFA, Eve LB, Montarroyos UR (2012) Perialveolar bacterial microbiota and bacteraemia after dental alveolitis in adult rats that had been subjected to neonatal malnutrition. Br J Nutr 107:996–1005. doi:10.​1017/​S000711451100393​X CrossRef
16.
go back to reference Costa TB, Morais NG, Almeida TM, Severo MS, De Castro CMMB (2012) Early malnutrition and production of IFN-δ, IL-12 and IL-10 by macrophages/lymphocytes: in vitro study of cell infection by methicillin-sensitive and methicillin-resistant Staphylococcus aureus. Rev Nutr 25(5):607–619. doi:10.1590/S1415-52732012000500006 CrossRef Costa TB, Morais NG, Almeida TM, Severo MS, De Castro CMMB (2012) Early malnutrition and production of IFN-δ, IL-12 and IL-10 by macrophages/lymphocytes: in vitro study of cell infection by methicillin-sensitive and methicillin-resistant Staphylococcus aureus. Rev Nutr 25(5):607–619. doi:10.​1590/​S1415-5273201200050000​6 CrossRef
17.
go back to reference Porto SMMS, Viana MT, Silva KMF, Diniz MFA, De Castro CMMB (2007) Desnutrição neonatal e microbiota normal da cavidade oral em ratos. Rev Bras Nutr 20(6):625–632 Porto SMMS, Viana MT, Silva KMF, Diniz MFA, De Castro CMMB (2007) Desnutrição neonatal e microbiota normal da cavidade oral em ratos. Rev Bras Nutr 20(6):625–632
18.
go back to reference Jones KDJ, Berkley JA, Warner JO (2013) Perinatal nutrition and immunity to infection. Pediatr Allergy Immunol 21(4):564–576 Jones KDJ, Berkley JA, Warner JO (2013) Perinatal nutrition and immunity to infection. Pediatr Allergy Immunol 21(4):564–576
19.
go back to reference Mcgettrick AF, O’neill LAJ (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22(1):20–27CrossRef Mcgettrick AF, O’neill LAJ (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22(1):20–27CrossRef
21.
go back to reference Ferreira WTS, Galvão BA, Ferraz PKN, De Castro CMMB, De Castro RM (2008) Perinatal malnutrition programs sustained alterations in nitric oxide release by activated macrophages in response to fluoxetine in adult rat. NeuroImmunoModulation 23:120–129 Ferreira WTS, Galvão BA, Ferraz PKN, De Castro CMMB, De Castro RM (2008) Perinatal malnutrition programs sustained alterations in nitric oxide release by activated macrophages in response to fluoxetine in adult rat. NeuroImmunoModulation 23:120–129
22.
go back to reference Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield C, Bazer FW, Wu G (2009) Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 17(2):282–302CrossRef Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield C, Bazer FW, Wu G (2009) Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 17(2):282–302CrossRef
23.
go back to reference Foster TJ (2009) Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion. J Vet Dermatol 20(5–6):456–470CrossRef Foster TJ (2009) Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion. J Vet Dermatol 20(5–6):456–470CrossRef
24.
go back to reference Kim JJ, Jo EJ (2013) NLRP3 inflammasome and host protection against bacterial infection. Korean Med Sci 28:1415–1423CrossRef Kim JJ, Jo EJ (2013) NLRP3 inflammasome and host protection against bacterial infection. Korean Med Sci 28:1415–1423CrossRef
25.
go back to reference Pumerantz A, Muppidi K, Agnihotri S, Guerrac C, Venketaraman V, Wangb J, Betageri G (2010) Preparation of liposomal vancomycin and intracellular killing of meticillin-resistant Staphylococcus aureus (MRSA). Internat J Antimicrob Agents 32:1–5 Pumerantz A, Muppidi K, Agnihotri S, Guerrac C, Venketaraman V, Wangb J, Betageri G (2010) Preparation of liposomal vancomycin and intracellular killing of meticillin-resistant Staphylococcus aureus (MRSA). Internat J Antimicrob Agents 32:1–5
26.
go back to reference Richardson AR, Libby SJ, Fang FC (2008) A nitric oxide-inducible lactate dehydrogenase enables staphylococcus aureus to resist innate immunity. Science 319:1–21. doi:10.1126/science.1155207 Richardson AR, Libby SJ, Fang FC (2008) A nitric oxide-inducible lactate dehydrogenase enables staphylococcus aureus to resist innate immunity. Science 319:1–21. doi:10.​1126/​science.​1155207
27.
go back to reference Macedo EMC, Amorim MAF, Silva ACS, Castro CMMB (2010) Effects of copper, zinc and magnesium deficiency on the immune system of severely malnourished children. Rev Paul Pediatr 28(3):329–336CrossRef Macedo EMC, Amorim MAF, Silva ACS, Castro CMMB (2010) Effects of copper, zinc and magnesium deficiency on the immune system of severely malnourished children. Rev Paul Pediatr 28(3):329–336CrossRef
28.
go back to reference Sarni ROS, Souza FIS, Cocco RR, Mallozi MC, Solé D (2010) Micronutrients, immunologic system and allergic diseases. Rev Bras Alerg Imunopatol 33(1):8–13 Sarni ROS, Souza FIS, Cocco RR, Mallozi MC, Solé D (2010) Micronutrients, immunologic system and allergic diseases. Rev Bras Alerg Imunopatol 33(1):8–13
29.
go back to reference Köhler J, Breitbacha K (2011) NADPH-oxidase but not inducible nitric oxide synthase contributes to resistance in a murine Staphylococcus aureus Newman pneumonia model. Microbes Infect 13(11):914–922CrossRef Köhler J, Breitbacha K (2011) NADPH-oxidase but not inducible nitric oxide synthase contributes to resistance in a murine Staphylococcus aureus Newman pneumonia model. Microbes Infect 13(11):914–922CrossRef
30.
go back to reference Kurokawa K, Gong J, Ryu K, Zheng L, Chae J, Kim M, Lee BL (2011) Biochemical characterization of evasion from peptidoglycan recognition by Staphylococcus aureus D-alanylated wall teichoic acid in insect innate immunity. Dev Comp Immunol 35(8):835–839CrossRef Kurokawa K, Gong J, Ryu K, Zheng L, Chae J, Kim M, Lee BL (2011) Biochemical characterization of evasion from peptidoglycan recognition by Staphylococcus aureus D-alanylated wall teichoic acid in insect innate immunity. Dev Comp Immunol 35(8):835–839CrossRef
31.
go back to reference Graves SF, Kobayashi SD, DeLeo FR (2010) Community-associated methicillin resistantStaphylococcus aureus immune evasion and virulence. J Mol Med 88:109–114CrossRef Graves SF, Kobayashi SD, DeLeo FR (2010) Community-associated methicillin resistantStaphylococcus aureus immune evasion and virulence. J Mol Med 88:109–114CrossRef
33.
go back to reference Rivadeneira DE, Grobmyer SR, Naama HA, Mackrell PJ, Mestre JR, Stapleton PP, Daly JM (2010) Malnutrition-induced macrophage apoptosis. Surgery 129(5):617–625CrossRef Rivadeneira DE, Grobmyer SR, Naama HA, Mackrell PJ, Mestre JR, Stapleton PP, Daly JM (2010) Malnutrition-induced macrophage apoptosis. Surgery 129(5):617–625CrossRef
34.
go back to reference Grivicich I, Regner A, Rocha AB (2007) Apoptosis: programmed cell death. R Bras Cancer 53(3):335–343 Grivicich I, Regner A, Rocha AB (2007) Apoptosis: programmed cell death. R Bras Cancer 53(3):335–343
35.
go back to reference Ribeiro R, Sousa DWN, Oliveira TS, Fernandes KPS, Junior JAS (2012) Intense physical activity: role of nitric oxide in apoptosis. Ter Man 10(48):1–5 Ribeiro R, Sousa DWN, Oliveira TS, Fernandes KPS, Junior JAS (2012) Intense physical activity: role of nitric oxide in apoptosis. Ter Man 10(48):1–5
36.
37.
go back to reference Carvalho RLB, Berezin EM, Mimica ML (2012) Detection of lukS-PV and lukF-PV in Staphylococcus aureus pediatric isolates. Arq Med Hosp Fac Cienc Med Santa Casa São Paulo 57(2):59–62 Carvalho RLB, Berezin EM, Mimica ML (2012) Detection of lukS-PV and lukF-PV in Staphylococcus aureus pediatric isolates. Arq Med Hosp Fac Cienc Med Santa Casa São Paulo 57(2):59–62
38.
go back to reference Kobayashi SD, DeLeo FR (2009) Role of neutrophils in innate immunity: a systems biology-level approach. Wiley Interdiscip Rev Syst Biol Med 1:309–333CrossRef Kobayashi SD, DeLeo FR (2009) Role of neutrophils in innate immunity: a systems biology-level approach. Wiley Interdiscip Rev Syst Biol Med 1:309–333CrossRef
Metadata
Title
Effect of neonatal malnutrition on expression of nitric oxide synthase enzyme, production of free radicals and in vitro viability of alveolar macrophages infected with methicillin-sensitive and methicillin-resistant Staphylococcus aureus
Authors
Natália Gomes de Morais
Thacianna Barreto da Costa
Amanda Lúcia Farias Pedrosa
Maria Carolina Accioly Brelaz de Castro
Suênia Cunha da Gonçalves de Albuquerque
Valéria Rêgo Alves Pereira
Milena de Paiva Cavalcanti
Célia Maria Machado Barbosa de Castro
Publication date
01-02-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2016
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0861-x

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