Impact of neonatal malnutrition on expression TLR-9, NF-kB and cytokines of macrophages infected in vitro with methicillin resistant Staphylococcus aureus

Microbial Pathogenesis

Volumn 132, Issue , 2019, Pages 254-260

  Morais, Natália Gomes de ^a   Costa, Thacianna Barreto da ^b   Ferreira de Lima, Luiz Felipe ^c   Basílio, Dyowani dos Santos ^c   Morais, Nadja Nara Gomes de ^d   Paiva Cavalcanti, Milena de ^e   Pereira, Valéria Rêgo Alves ^e   de Castro, Celia Maria Machado Barbosa ^b  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^b FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^c Graduates of the Course of Veterinary Medicine   (Brazil)

^d UNIVERSIDADE FEDERAL RURAL DE PERNAMBUCO   (Brazil)

^e INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Macrophage; Malnutrition; MRSA; Plasticity

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 33; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT GAIN; CELL DEATH; CELL ISOLATION; CONTROLLED STUDY; GENE EXPRESSION; IMMUNE RESPONSE; IN VITRO STUDY; INFECTION SENSITIVITY; INFLAMMATION; MACROPHAGE; MALE; MALNUTRITION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MONONUCLEAR CELL; NEONATAL MALNUTRITION; NEWBORN; NONHUMAN; NUTRITION; PRIORITY JOURNAL; PROTEIN CALORIE MALNUTRITION; PROTEIN EXPRESSION; RAT; ANIMAL; BODY WEIGHT; DOG; GENE EXPRESSION REGULATION; IMMUNOLOGY; LUNG ALVEOLUS MACROPHAGE; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCUS INFECTION; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CYTOKINES; DOGS; GENE EXPRESSION REGULATION; INTERLEUKIN-18; INTERLEUKIN-1BETA; INTERLEUKIN-33; MACROPHAGES; MACROPHAGES, ALVEOLAR; MALE; MALNUTRITION; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; NF-KAPPA B; RATS; RATS, WISTAR; STAPHYLOCOCCAL INFECTIONS; TOLL-LIKE RECEPTOR 9;

EID: 85065520132     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2019.05.009     Document Type: Article

References (51)

1. Reynolds, L.P., Caton, J.S., Role of the pre-and post-natal environment in developmental programming of health and productivity. Mol. Cell. Endocrinol. 354 (2012), 54–59 https://doi.org/10.1016/j.mce.2011.11.013.
2. Sinha, S., Patro, N., Patro, I.K., Maternal protein malnutrition: current and future perspectives of spirulina supplementation in neuroprotection. Front. Neurosci. 12 (2018), 1–18 https://doi.org/10.3389/fnins.2018.00966.
3. Costa, T.B., Morais, N.G., Almeida, T.M., Severo, M.S., De Castro, C.M.M.B., Early malnutrition and production of IFN-γ, 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 (2012), 607–619 https://doi.org/10.1590/S1415-52732012000500006.
4. Vega, C.C., Reyes-Castro, L.A., Rodriguez-Gonzalez, G.L., Bautista, C.J., Vazquez-Martinez, M., Larrea, F., Zambrano, E., Resveratrol partially prevents oxidative stress and metabolic dysfunction in pregnant rats fed a low protein diet and their offspring. J. Physiol. 594:5 (2016), 1483–14992 https://doi.org/10.1113/JP271543.
5. Reyes-Castro, L.A., Padilla-Gomez, E., Parga-Martínez, N.J., Castro-Rodríguez, D.C., Quirarte, G.L., Díaz-Cintra, S., Nathanielsz, P.W., Zambrano, E., Hippocampal Mechanisms in Impaired Spatial Learning and Memory in Male Offspring of Rats Fed a Low-Protein Isocaloric Diet in Pregnancy And/or Lactation, vol. 28, 2017, Wiley, 18–30 2017 https://doi.org/10.1002/hipo.22798.
6. Desai, M., Hales, C.N., Role of fetal and infant growth in programming metabolism in later life. Biol. Ver., 72, 1997 329-248 https://doi.org/10.1017/S0006323196005026.
7. Parker, D., Prince, A., Staphylococcus aureus induces type I IFN signaling in dendritic cells via TLR9. J. Immunol. 189 (2012), 4040–4046 https://doi.org/10.4049/jimmunol.1201055.
8. Morais, N.G., Costa, T.B., Bezerra de Lira, J.M., Albuquerque, S.C.G., Pereira, V.R.A., Paiva-Cavalcanti, M., Castro, C.M.M.B., TLR and NLRP3 inflammasome expression deregulation in macrophages of adult rats subjected to neonatal malnutrition and infected with methicillin-resistant Staphylococcus aureus. Nutrition 33 (2017), 174–180 https://doi.org/10.1016/j.nut.2016.06.005.
9. Alfatemi, S.M.H., Motamedifar, M., Hadi, N., Saraie, H.S.E., Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA)strains. Jundishapur J. Microbiol., 7(6), 2014, e10741, 10.5812/jjm.10741.
10. Cutler, R.R., Relationship between antibiotic resistance, the production of “virulence factors”, and virulence for experimental animals in Staphylococcus aureus. J. Med. Microbiol. 2 (1979), 55–62 htps://dx.doi.org/10.1099/00222615-12-1-55.
11. Morais, N.G., Costa, T.B., Severo, M.S., Castro, C.M.M.B., Long-term effects of neonatal malnutrition on microbicide response, production of cytokines, and survival of macrophages infected by Staphylococcus aureus sensitive/resistant to methicillin. Rev. Nutr.(27), 2014, 557–568 https://doi.org/10.1590/1415-52732014000500005.
12. Morais, N.G., da Costa, T.B., Pedrosa, A.L., de Castro, M.C., da Gonçalves de Albuquerque, S.C., Pereira, V.R., de Paiva Cavalcanti, M., de Castro, C.M., 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. Eur. J. Nutr. 55:1 (2016), 403–411 htps://doi.org/10.1007/s00394-015-0861-x.
13. Van der Meer, A.J., Achouiti, A., Ende, A., Soussan, A.A., Florquin, S., Vos, A., Zeerleder, S.S., Poll, T., Toll-like receptor 9 enhances bacterial clearance and limits lung consolidation in murine pneumonia caused by methicillin-resistant Staphylococcus aureus. Mol. Med. 22 (2016), 292–299 https://doi.org/10.2119/molmed.2015.00242.
14. Mariathasan, S., Monack, D., Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat. Rev. Immunol. 7 (2007), 31–41 https://doi.org/10.1038/nri1997.
15. McGilligan, V.E., Gregory-Ksander, M.S., Li, D., Moore, J.E., Hodges, R.R., Gilmore, M.S., Moore, T.C.B., Dartt, D.A., Staphylococcus aureus activates the NLRP3 inflammasome in human and rat conjunctival goblet cells. PLoS One 8 (2013), 1–13 https://doi.org/10.1371/journal.pone.0074010.
16. Lan, F., Yuan, B., Liu, T., Luo, X., Huang, P., Liu, Y., Dai, L., Yin, H., Interleukin-33 facilitates neutrophil recruitment and bacterial clearance in S. aureus-caused peritonitis. Mol. Immunol.(72), 2016, 74–80 https://doi.org/10.1016/j.molimm.2016.03.004.
17. Lu, J., Ji, J., Meng, H., Wang, D., Jiang, B., Liu, L., Randell, E., Adeli, K., Meng, Q.H., The protective effect and underlying mechanism of metformin on neointima formation in fructose-induced insulin resistant rats. Cardiovasc. Diabetol. 5 (2013), 12–18 https://doi.org/10.1186/1475-2840-12-58.
18. Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3 (2008), 1101–1112, 10.1038/nprot.2008.73.
19. Gonçalves, S.C., Régis-da-Silva, C.G., Brito, M.E.F., Brandão-Filho, S.P., Paiva-Cavalcanti, M., Application of the mammalian glyceraldehyde-3-phosphate dehydrogenase gene for sample quality control in multiplex PCR for diagnosis of leishmaniasis. Venom. Anim. Toxins Incl. Trop. Dis. 18 (2012), 188–197 https://doi.org/10.1590/S1678-91992012000200009.
20. Reyes-Castro, L.A., Padilla-Gomez, E., Parga-Martínez, N.J., Castro-Rodríguez, D.C., Quirarte, G.L., Díaz-Cintra, S., Nathanielsz, P.W., Zambrano, E., Hippocampal mechanisms in impaired spatial learning and memory in male offspring of rats fed a low-protein isocaloric diet in pregnancy and/or lactation. Hippocampus 28 (2018), 18–30 https://doi.org/10.1002/hipo.22798.
21. Gluckman, P.D., Hanson, M.A., Phil, D., Cooper, C., Thornburg, K.L., Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359 (2008), 61–73 doi: 1056/NEJMra0708473.
22. Joshi, S., Garole, V., Daware, M., Girigosavi, S., Rao, S., Maternal protein restriction before pregnancy affects vital organs of offspring in Wistar rats. Metabolism 52:1 (2003), 13–18 https://doi.org/10.1053/meta.2003.50010.
23. Bourke, C.D., Berkley, J.A., Prendergast, A.J., Immune dysfunction as a cause and consequence of malnutrition. Trends Immunol. 37:6 (2016), 386–398 https://doi.org/10.1016/j.it.2016.04.003.
24. Costa, T.B., Morais, N.G., Pedrosa, A.F., Albuquerque, S.C.G., Castro, M.A.A.B., Pereira, V.R.A., Paiva-Cavalcanti, M., Castro, C.M.M.B., Neonatal malnutrition programs the oxidant function of macrophages in response to Candida albicans. Microb. Pathog. 95 (2016), 68–76 https://doi.org/10.1016/j.micpath.2016.02.012.
25. Porto, S., Viana, M.T., Silva, K.M.F., Diniz, M.F.A., De Castro, C.M.M.B., Desnutrição neonatal E microbiota normal da cavidade oral em ratos. Rev. Bras. Nutr. 20:6 (2007), 625–632 https://doi.org/10.1590/S1415-52732007000600005.
26. Fisher, R.E., Steele, M., Karrow, A.A., Fetal programming of the neuroendocrine-immune system and metabolic disease. J. Preg. 1 (2012), 1–11 https://doi.org/10.1155/2012/792934.
27. Jones, K.D.J., Berkley, J.A., Warner, J.O., Perinatal nutrition and immunity to infection. Pediatr. Allergy Immunol. 21:4 (2010), 564–576 https://doi.org/10.1111/j.1399-3038.2010.01002.x.
28. Lucas, A., Long-term programming effects of early nutrition—implications for the preterm infant. J. Perinatol. 25:2 (2005), S2–S6, 10.1038/sj.jp.7211308.
29. Santos, A.C.A., Correia, C.A., Oliveira, D.C., Nogueira-Pedro, A., Borelli, P., Fock, R.A., Intravenous glutamine administration modulates TNF-α/IL-10 ratio and attenuates NFkB phosphorylation in a protein malnutrition model. Inflammation 39:6 (2016), 1883–1891 https://doi.org/10.1007/s10753-016-0424-1.
30. Fock, R.A., Rogero, M.M., Vinolo, M.A., Curi, R., Borges, M.C., Borelli, P., Effects of protein-energy malnutrition on NF-kappaB signalling in murine peritoneal macrophages. Inflammation 33:2 (2010), 101–109 https://doi.org/10.1007/s10753-009-9163-x.
31. Yamada, S., Tokumoto, M., Tatsumoto, N., Tsuruya, K., Kitazono, T., Ooboshi, H., Very low protein diet enhances inflammation, malnutrition, and vascular calcification in uremic rats. Life Sci. 146 (2016), 117–123 https://doi.org/10.1016/j.lfs.2015.12.050.
32. Paparo, L., Costanzo, M.D., Scala, C.D., Cosenza, L., Leone, L., Nocerino, R., Canani, R.B., The influence of early life nutrition on epigenetic regulatory mechanismos of the immune system. Nutrients 6:11 (2014), 4706–4719 https://doi.org/10.3390/nu6114706.
33. Mohamed, W., Domann, E., Chakraborty, T., Mannala, G., Lips, K.S., Heiss, C., Schnettler, R., Alt, V., TLR9 mediates Staphylococcus aureus killing inside osteoblasts via induction of oxidative stress. Mohamed et al. BMC Microbiol. 16 (2016), 230–238 https://doi.org/10.1186/s12866-016-0855-8.
34. Kumagai, Y., Takeuchi, O., Akira, S., TLR9 as a key receptor for the recognition of DNA. Adv. Drug Deliv. Rev. 29:60 (2008), 795–804 https://doi.org/10.1016/j.addr.2007.12.004.
35. Latz, E., The inflammasomes: mechanisms of activation and function. Curr. Opin. Immunol. 22 (2010), 28–33 https://doi.org/10.1016/j.coi.2009.12.004.
36. Bergsbaken, T., Fink, S.L., Cookson, B.T., Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7 (2009), 99–109 https://doi.org/10.1038/nrmicro2070.
37. Willingham, S.B., Bergstralh, D.T., O'Connor, W., Morrison, A.C., Taxman, D.J., Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2 (2007), 147–159 https://doi.org/10.1016/j.chom.2007.07.009.
38. Kaltschmidt, B., Widera, D., Kaltschmidt, C., Signaling via NF-Κb in the Nervous System, vol. 1745, 2005, 287–299 3 https://doi.org/10.1016/j.bbamcr.2005.05.009.
39. Dinarello, C.A., IL-18: a TH1-inducing, proinflammatorycytokine and new member of the IL-1 family. J. Allergy Clin. Immunol. 103:1 (1999), 11–24 1999 Jan https://doi.org/10.1016/S0091-6749(99)70518-X.
40. Dostert, C., Ludigs, K., Guarda, G., Innate and adaptive effects of inflammasomes on T cell responses. Curr. Opin. Immunol. 25:3 (2013), 359–365 https://doi.org/10.1016/j.coi.2013.02.008.
41. Robinson, K.M., Choi, S.M., McHugh, K.J., Mandalapu, S., Enelow, R.I., Kolls, J.K., Alcorn, J.F., Influenza A exacerbates Staphylococcus aureus pneumonia by attenuating IL-1beta production in mice1. J. Immunol. 191:10 (2013), 5153–5159 https://doi.org/10.4049/jimmunol.1301237.
42. Shimada, T., Park, B.G., Wolf, A.J., Brikos, C., Goodridge, H.S., Becker, C.A., et al. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation and IL-1beta secretion. Cell Host Microbe 7:1 (2010), 38–49 https://doi.org/10.1016/j.chom.2009.12.008.
43. Kinoshita, M., Miyazaki, H., Ono, S., Inatsu, A., Nakashima, H., Tsujimoto, H., Shinomiya, N., Saitoh, D., Seki, S., Enhancement of neutrophil function by interleukin-18 therapy protects burn-injured mice from methicillin-resistant Staphylococcus aureus. Infect. Immun. 79 (2011), 2670–2680, 10.1128/IAI.01298-10 2011.
44. Wawrocki, S., Druszczynska, M., Kowalewicz-Kulbat, M., Rudnicka, W., Interleukin 18 (IL-18)as a target for immune intervention. ActBio. Pol. 63:1 (2016), 59–63 https://doi.org/10.18388/abp.2015_1153.
45. Novick, D., Kim, S., Kaplanski, G., Dinarello, C.A., Interleukin-18, more than a Th1 cytokine. Semin. Immunol. 25:6 (2013), 439–448 2013 Dec https://doi.org/10.1016/j.smim.2013.10.014.
46. Soong, G., Chun, J., Parker, D., Prince, A., Staphylococcus aureus activation of caspase 1/calpain signaling mediates invasion through human keratinocytes. J. Infect. Dis. 205:10 (2012), 1571–1579 https://doi.org/10.1093/infdis/jis244.
47. Dinarello, C., Overview of the interleukin-1 family of ligands and receptors. Semin. Immunol. 25:6 (2013), 389–393 https://doi.org/10.1016/j.smim.2013.10.001.
48. Yin, H., Li, X., Hu, S., Liu, T., Yuan, B., Ni, Q., Lan, F., Luo, X., Gu, H., Zheng, F., IL-33 promotes Staphylococcus aureus-infected wound healing in mice. Int. Immunopharmacol. 17:2 (2013), 432–438 https://doi.org/10.1016/j.intimp.2013.07.008.
49. Cayrol, C., Girard, J.P., Interleukin- 33 (IL- 33): a nuclear cytokine from the IL- 1 family. Immunol. Rev. 281 (2018), 154–168 https://doi.org/10.1016/j.intimp.2013.07.008.
50. Neumann, K., Schiller, B., Tiegs, G., NLRP3 inflammasome and IL-33: novel players in sterile liver inflammation. Int. J. Mol. Sci. 19 (2018), 1–26 2018 https://doi.org/10.3390/ijms19092732.
51. Li, C., Li, H., Jiang, Z., Zhang, T., Wang, Y., Li, Z., Wu, Y., Ji, S., Xiao, S., Ryffel, B., Radek, K.A., Xia, Z., Lai, Y., Interleukin-33 antibacterial defense by activation of inducible nitric oxide synthase in skin. PLoS Pathog., 10(2), 2014, e1003918 https://doi.org/10.1371/journal.ppat.1003918.