Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T06:21:47.187Z Has data issue: false hasContentIssue false

Evaluation of energetic metabolism in the rat brain after meningitis induction by Klebsiella pneumoniae

Published online by Cambridge University Press:  21 February 2013

Tatiana Barichello*
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Lutiana Roque Simões
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Jaqueline S. Generoso
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Mirelle M. Carradore
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Ana Paula Moreira
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Ana Paula Panatto
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Caroline S. Costa
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Álvaro Steckert Filho
Affiliation:
Laboratório de Microbiologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Isabela C. Jeremias
Affiliation:
Laboratório de Fisiopatologia and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Gisele D. Bez
Affiliation:
Laboratório de Fisiopatologia and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
Emilio Streck
Affiliation:
Laboratório de Fisiopatologia and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina, Programa de Pós‐Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, SC, Brazil
*
Professor Tatiana Barichello, PhD, Laboratório de Microbiologia Experimental, PPGCS, UNASAU, Universidade do Extremo Sul Catarinense, 88806–000 Criciúma, SC, Brazil. Tel: +55 48 34312643; Fax: +55 48 3443 4817; E‐mail: [email protected]

Abstract

Background

Bacterial meningitis is an infection of the central nervous system characterised by strong inflammatory response. The brain is highly dependent on ATP, and the cell energy is obtained through oxidative phosphorylation, a process which requires the action of various respiratory enzyme complexes and creatine kinase (CK) as an effective buffering system of cellular ATP levels in tissues that consume high energy.

Objectives

Evaluate the activities of mitochondrial respiratory chain complexes I, II, III, IV and CK activity in hippocampus and cortex of the Wistar rat submitted to meningitis by Klebsiella pneumoniae.

Methods

Adult Wistar rats received either 10 µl of sterile saline as a placebo or an equivalent volume of K. pneumoniae suspension. The animals were killed in different times at 6, 12, 24 and 48 h after meningitis induction. Another group was treated with antibiotic, starting at 16 h and continuing daily until their decapitation at 24 and 48 h after induction.

Results

In the hippocampus, the meningitis group without antibiotic treatment, the complex I was increased at 24 and 48 h, complex II was increased at 48 h, complex III was inhibited at 6, 12, 24 and 48 h and in complex IV all groups with or without antibiotic treatment were inhibited after meningitis induction, in the cortex there was no alteration.

Discussion

Although descriptive, our results show that antibiotic prevented in part the changes of the mitochondrial respiratory chain. The meningitis model could be a good research tool to study the biological mechanisms involved in the pathophysiology of the K. pneumoniae meningitis.

Type
Original Articles
Copyright
Copyright © Scandinavian College of Neuropsychopharmacology 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Kim, KS. Acute bacterial meningitis in infants and children. Lancet Infect Dis 2010;10:3242.Google Scholar
2Klinger, G, Chin, CN, Beyene, J, Perlman, M. Predicting the outcome of neonatal bacterial meningitis. Pediatrics 2000;106:477482.Google Scholar
3Hussen, AS, Shafran, SD. Acute bacterial meningitis in adults. A 12‐year review. Medicine (Baltimore) 2000;79:360368.Google Scholar
4Ko, WC, Paterson, DL, Sagnimeni, AJ et al. Community‐acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg Infect Dis 2002;8:160166.Google Scholar
5Lu, CH, Chang, WN, Chang, HW. Klebsiella meningitis in adults: clinical features, prognostic factors and therapeutic outcomes. J Clin Neurosci 2002;9:533588.Google Scholar
6Barichello, T, Savi, GD, Simões, LR et al. Evaluation of mitochondrial respiratory chain in the brain of rats after pneumococcal meningitis. Brain Res Bull 2010;82:302307.Google Scholar
7Sahly, H, Podschun, R. Clinical, bacteriological, and serological aspects of Klebsiella infections and their spondylarthropathic sequelae. Clin Diagn Lab Immunol 1997;4:393399.Google Scholar
8Liu, YC, Cheng, DL, Lin, CL. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med 1986;146:19131916.Google Scholar
9Su, CM, Chang, WN, Tsai, NW, Huang, CR, Wang, HC, Lu, CH. Clinical features and outcome of community‐acquired bacterial meningitis in adult patients with liver cirrhosis. Am J Med Sci 2010;340:452456.Google Scholar
10Tsai, MH, Lu, CH, Huang, CR et al. Bacterial meningitis in young adults in Southern Taiwan: clinical characteristics and therapeutic outcomes. Infection 2006;34:28.Google Scholar
11Tang, LM, Chen, ST, Hsu, WC, Chen, CM. Klebsiella meningitis in Taiwan: an overview. Epidemiol Infect 1997;119:135142.Google Scholar
12Hirst, RA, Kadioglu, A, O'Callaghan, C, Andrew, PW. The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin Exp Immunol 2004;138:195201.Google Scholar
13Leib, SL, Tauber, MG. Pathogenisis of bacterial meningitis. Infect Dis Clin North Am 1999;13:527548.Google Scholar
14Grandgirard, D, Leib, SL. Meningitis en Neonatos: bench to bedside. Clin Perinatol 2010;37:655676.Google Scholar
15Klein, M, Koedel, U, Pfister, HW. Oxidative stress in pneumococcal meningitis: a future target for adjunctive therapy? Prog Neurobiol 2006;80:269280.Google Scholar
16Sellner, J, Täuber, MG, Leib, SL. Pathogenesis and pathophysiology of bacterial CNS infections. Handb Clin Neurol 2010;96:116.CrossRefGoogle ScholarPubMed
17Tauber, MG, Moser, B. Cytokines and chemokines in meningeal inflammation: biology and clinical implications. Clin Infect Dis 1999;28:112.Google Scholar
18Bessman, SP, Carpenter, CL. The creatine‐creatine phosphate energy shuttle. Annu Rev Biochem 1985;54:831865.Google Scholar
19Schnyder, T, Winkler, H, Gross, H, Eppenberger, HM, Wallimann, T. Crystallization of mitochondrial creatine kinase. Growing of large protein crystals and electron microscopic investigation of microcrystals consisting of octamers. J Biol Chem 1991;266:53185322.Google Scholar
20Wallimann, T, Wyss, M, Brdiczka, D, Nicolay, K, Eppenberger, HM. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 1992;281:2140.Google Scholar
21Brand, MD, Nicholls, DG. Assessing mitochondrial dysfunction in cells. Biochem J 2011;435:297312.Google Scholar
22Barichello, T, Savi, GD, Silva, GZ et al. Antibiotic therapy prevents, in part, the oxidative stress in the rat brain after meningitis induced by Streptococcus pneumoniae. Neurosci Lett 2010;478:9396.Google Scholar
23Irazuzta, JE, Pretzlaff, RK, Zingarelli, B, Xue, V, Zemlan, F. Modulation of nuclear factor‐kB activation and decreased markers of neurological injury associated with hypothermic therapy in experimental bacterial meningitis. Crit Care Med 2002;30:25532559.Google Scholar
24Grandgirard, D, Schürch, C, Cottagnoud, P, Leib, SL. Prevention of brain injury by the nonbacteriolytic antibiotic daptomycin in experimental pneumococcal meningitis. Antimicrob Agents Chemother 2007;51:21732178.CrossRefGoogle ScholarPubMed
25Hoogman, M, van de Beek, M, Weisfelt, M, de Gans, J, Schmand, B. Cognitive outcome in adults after bacterial meningitis. J Neurol Neurosurg Psychiatry 2007;78:10921096.Google Scholar
26Barichello, T, Silva, GZ, Savi, GD et al. Brain creatine kinase activity after meningitis induced by Streptococcus pneumoniae. Brain Res Bull 2009;80:8588.Google Scholar
27Lowry, OH, Rosebough, NG, Farr, AL, Randall, RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265275.Google Scholar
28Cassina, A, Radi, R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 1996;328:309316.Google Scholar
29Fischer, C, Ruitenbeek, W, Berden, JA. Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 1985;153:2336.Google Scholar
30Rustin, P, Chretien, D, Bourgeron, T et al. Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 1994;228:3551.Google Scholar
31Hughes, BP. A method for estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathologic sera. Clin Chim Acta 1962;7:597604.Google Scholar
32Chang, WN, Lu, CH, Huang, CR et al. Clinical characteristics of post‐neurosurgical Klebsiella pneumoniae meningitis in adults and a clinical comparison to the spontaneous form in a Taiwanese population. J Clin Neurosci 2010;17:334338.Google Scholar
33Lu, CH, Chang, WN, Lin, YC et al. Bacterial brain abscess: microbiological features, epidemiological trends and therapeutic outcomes. Q J Med 2002;95:501509.Google Scholar
34Coimbra, RS, Voisin, V, Saizieu Ab, DE et al. Gene expression in cortex and hippocampus during acute pneumococcal meningitis. BMC Biol 2006;4:15.Google Scholar
35Wen, LL, Chiu, CT, Huang, YN, Chang, CF, Wang, JY. Rapid glia expression and release of proinflammatory cytokines in experimental Klebsiella pneumoniae meningoencephalitis. Exp Neurol 2007;205:270278.Google Scholar
36Mitchell, L, Smith, SH, Braun, JS, Herzog, KH, Weber, JR, Tuomanen, EI. Dual phases of apoptosis in pneumococcal meningitis. J Infect Dis 2004;190:20392046.Google Scholar
37Grimwood, K, Anderson, P, Anderson, V, Tan, L, Nolan, T. Twelve year outcomes following bacterial meningitis: further evidence for persisting effects. Arch Dis Child 2000;83:111116.Google Scholar
38Andres, RH, Ducray, AD, Schlattner, U, Wallimann, T, Widmer, HR. Functions and effects of creatine in the central nervous system. Brain Res Bull 2008;76:329343.CrossRefGoogle ScholarPubMed
39Bénit, P, Lebon, S, Rustin, P. Respiratory‐chain diseases related to complex III deficiency. Biochim Biophys Acta 2009;1793:181185.Google Scholar
40Keightley, JA, Anitori, R, Burton, MD, Quan, F, Buist, NR, Kennaway, NG. Mitochondrial encephalomyopathy and complex III deficiency associated with a stop‐codon mutation in the cytochrome b gene. Am J Hum Genet 2000;67:14001410.Google Scholar
41Mourmans, J, Wendel, U, Bentlage, HA et al. Clinical heterogeneity in respiratory chain complex III deficiency in childhood. J Neurol Sci 1997;49:111117.Google Scholar
42Nau, R, Soto, A, Bruck, W. Apoptosis of neurons in the dentate gyrus in humans suffering from bacterial meningitis. J Neuropathol Exp Neurol 1999;58:265274.Google Scholar
43Leib, SL, Heimgartner, C, Bifrare, YD, Loeffler, JM, Täauber, MG. Dexamethasone aggravates hippocampal apoptosis and learning deficiency in pneumococcal meningitis in infant rats. Pediatr Res 2003;4:4.Google Scholar
44Wu, UI, Mai, FD, Sheu, JN et al. Melatonin inhibits microglial activation, reduces pro‐inflammatory cytokine levels, and rescues hippocampal neurons of adult rats with acute Klebsiella pneumoniae meningitis. J Pineal Res 2011;50:5970.Google Scholar
45Barichello, T, Silva, GZ, Batista, AL et al. Early antibiotic administration prevents cognitive impairment induced by meningitis in rats. Neurosci Lett 2009;465:7173.Google Scholar