Tacrine and its analogues impair mitochondrial function and bioenergetics: A lipidomic analysis in rat brain

Journal of Neurochemistry

Volumn 120, Issue 6, 2012, Pages 998-1013

  Melo, Tânia ^a   Videira, Romeu A ^b   André, Sónia ^b   Maciel, Elisabete ^a   Francisco, Carla S ^c   Oliveira Campos, Ana M ^c   Rodrigues, Lígia M ^c   Domingues, Maria R M ^a   Peixoto, Francisco ^b   Oliveira, M Manuel ^d  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

^d NONE   (Portugal)

Author keywords

Alzheimer's disease; Bioenergetic activity; Lipidomics; Non synaptic brain mitochondria; Tacrine

Indexed keywords

8 AMINO 1,5,6,7 TETRAHYDRO 1 PHENYLCYLOPENTA[E]PYRROLO[3,2 B]PYRIDINE 3 CARBONITRILE; 9 AMINO 5,6,7,8 TETRAHYDRO 1 PHENYL 1H PYRROLO[3,2 B]QUINOLINE 3 CARBONITRILE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CARDIOLIPIN; CHOLINESTERASE; CYTOCHROME C OXIDASE; GAMMA GLUTAMYLTRANSFERASE; LIPIDOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TACRINE; TACRINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN MITOCHONDRION; CONTROLLED STUDY; CORRELATION ANALYSIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; LIPID COMPOSITION; LIPIDOMICS; LIVER TOXICITY; MALE; NERVE CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BRAIN; BUTYRYLCHOLINESTERASE; CHOLINESTERASE INHIBITORS; CHOLINESTERASES; CHROMATOGRAPHY, THIN LAYER; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX I; ENERGY METABOLISM; LIVER DISEASES; MALE; MITOCHONDRIA; PHOSPHOLIPIDS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TACRINE;

RATTUS;

EID: 84857915468     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07636.x     Document Type: Article

References (51)

1. Antunes-Madeira M. C., Videira R. A., Klüppel M. L. W. and Madeira V. M. C. (1995) Amiodarone effects on membrane organization evaluated by fluorescence polarization. Int. J. Cardiol. 48, 211-218.
2. Bartlett M. E. and Lewis D. H. (1970) Spectrophotometric determination of phosphate esters in the presence and absence of orthophosphate. Anal. Biochem. 36, 159-167.
3. Battino M., Bertoli E., Formiggini G., Sassi S., Gorini A., Villa R. F. and Lenaz G. (1991) Structural and functional aspects of the respiratory chain of synaptic and nonsynaptic mitochondria derived from selected brain regions. J. Bioenerg. Biomembr. 23, 345-363.
4. Berson A., Renault S., Lettéron P. et al. (1996) Uncoupling of rat and human mitochondria: a possible explanation for tacrine-induced liver dysfunction. Gastroenterology 110, 1878-1890. (Pubitemid 26169225)
5. Bligh E. G. and Dyer W. J. (1959) A rapid method for total lipid extraction and purification. J. Biochem. Physiol. 37, 911-917.
6. Brügger B., Erben G., Sandhoff R., Wieland F. T. and Lehmann W. D. (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospary ionization tandem mass spectrometry. Proc. Natl Acad. Sci. USA 94, 2339-2344. (Pubitemid 27136876)
7. Chicco A. J. and Sparagna G. C. (2007) Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 292, C33-C44. (Pubitemid 46115119)
8. Drukarch B., Leysen J. E. and Stoof J. C. (1988) Further analysis of the neuropharmacological profile of 9-amino-1,2,3,4-tetrahydroacridine (THA), an alleged drug in the treatment of Alzheimer's disease. Life Sci. 42, 1011-1017. (Pubitemid 18065344)
9. Ellman G. L., Courtney K. D., Andres Jr B. and Featherstone R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
10. Fang L., Appenroth D., Decker M., Kiehntopf M., Roegler C., Deufel T., Fleck C., Peng S., Zhang Y. and Lehmann J. (2008) Synthesis and biological evaluation of NO-donor-tacrine hybrids as hepatoprotective anti-Alzheimer drug candidates. J. Med. Chem., 51, 713-716. (Pubitemid 351304679)
11. Fry M. and Green D. E. (1981) Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 256, 1874-1880.
12. Galisteo M., Rissel M., Sergent O., Chevanne M., Cillard J., Guillouzo A. and Lagadic-Gossmann D. (2000) Hepatotoxicity of tacrine: occurrence of membrane fluidity alterations without involvement of lipid peroxidation. J. Pharmacol. Exp. Ther. 294, 160-167. (Pubitemid 30434683)
13. Gornall A. G., Bardawill C. and David M. M. (1949) Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751-756.
14. Hallivel J. V. and Grove E. A. (1989) 9-Amino-1,2,3,4-tetrahydroacridine (THA) blocks agonist-induced potassium conductance in rat hippocampal neurones. Eur. J. Pharmacol. 163, 369-372.
15. Han X. and Gross R. W. (2006) Specific lipid alterations in Alzheimer's disease and diabetes: shotgun global cellular lipidome analyses by electrospray ionization mass spectrometry using intrasource separation, in Functional Lipidomics (Feng L. and Prestwich G. D., eds), pp. 286-306. Taylor & Francis Group, LCC, Boca Raton, FL, USA.
16. Heilbronn E. (1961) Inhibition of cholinesterase by tetrahydroaminoacric. Acta Chem. Scand. 15, 1386-1390.
17. Hsu F.-F. and Turk J. (2005) Studies on phosphatidylserine by tandem quadrupole and multiple stage quadrupole ion-trap mass spectrometry with electrospray ionization: structural characterization and the fragmentation processes. J. Am. Soc. Mass Spectrom. 16, 1510-1522. (Pubitemid 41169860)
18. Hsu F.-F., Turk J., Rhoades E. R., Russell D. G., Shi Y. and Groisman E. A. (2005) Structural characterization of cardiolipin by tandem quadrupole and multiple-stage quadrupole ion-trap mass spectrometry with electrospray ionization. J. Am. Soc. Mass Spectrom. 16, 491-504. (Pubitemid 40410035)
19. Kagan V. E., Borisenko G. G., Tyurina Y. Y., Tyurin V. A., Jiang J., Potapovich A. I., Amoscato A. A. and Fujji Y. (2004) Oxidative lipidomics of apoptosis: redox catalytic interations of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 37, 1963-1985. (Pubitemid 39491317)
20. Kiebish M. A., Han X., Cheng H., Lunceford A., Clarke C. F., Moon H., Chuang J. H. and Seyfried T. N. (2008a) Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J. Neurochem., 106, 299-312. (Pubitemid 351840212)
21. Kiebish M. A., Han X., Cheng H., Chuang J. H. and Seyfried T. N. (2008b) Cardiolipin and electron transport chain abnormalities in mouse brain tumor mitochondria: lipidomic evidence supporting the Warburg theory of cancer. J. Lipid Res. 49, 2545-2556.
22. Kiebish M. A., Han X., Cheng H. and Seyfried T. N. (2009) In vitro growth environment produces lipidomic and electron transport chain abnormalities in mitochondria from non-tumorigenic astrocytes and brain tumours. ASN Neuro 1, 125-135.
23. Kozurkova M., Hamulakova S., Gazova Z., Paulikova H. and Kristian P. (2011) Neuroactive multifunctional tacrine congeners with cholinesterase, anti-amyloid aggregation and neuroprotective properties. Pharmaceuticals 4, 382-418.
24. Lehtonen J. Y. A., Rytömaa M. and Kinnunen P. K. J. (1996) Characteristics of the binding of tacrine to acidic phospholipids. Biophys. J. 70, 2185-2194. (Pubitemid 26133711)
25. Maciel E., da Silva R. N., Simões S., Domingues P. and Domingues M. R. (2011) Phosphatidylserine oxidation by Fenton reaction: recognition of oxidation of serine polar head by TLC and mass spectrometry. J. Am. Soc. Mass Spectrom. 22, 1804-1814.
26. Madeira V. M. C., Antunes-Madeira M. C. and Carvalho A. P. (1974) Activation energies of the ATPase activity of sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 58, 897-904.
27. Mansouri A., Haouzi D., Descatoire V., Demeilliers C., Sutton A., Vadrot N., Fromenty B., Feldmann G., Pessayre D. and Berson A. (2003) Tacrine inhibits topoisomerases and DNA synthesis to cause mitochondrial DNA depletion and apoptosis in mouse liver. Hepatology 38, 715-725. (Pubitemid 37052158)
28. Masson P., Xie W., Froment M.-T. and Lockridge O. (2001) Effects of mutations of active site residues and amino acids interacting with the W loop on substrate activation of butyrylcholinesterase. Biochim. Biophys. Acta 1544, 166-176. (Pubitemid 32121855)
29. Meng Q., Ru J., Zhang G., Shen C., Schmitmeier S. and Bader A. (2007) Re-evaluation of tacrine hepatotoxicity using gel entrapped hepatocytes. Toxicol. Lett. 168, 140-147. (Pubitemid 46054364)
30. Monteiro P., Duarte A. I., Moreno A., Gonçalves L. M. and Providência L. A. (2003) Carvedilol improves energy production during acute global myocardial ischaemia. Eur. J. Pharmacol. 482, 245-253. (Pubitemid 37508518)
31. Osseni R. A., Debbasch C., Christen M. O., Rat P. and Warnet J. M. (1999) Tacrine-induced reactive oxygen species in a human liver cell line: the role of anethole dithiolethione as a scavenger. Toxicol. In Vitro 13, 683-688. (Pubitemid 29354196)
32. Petrosillo G., Casanova G., Matera M., Ruggiero F. M. and Paradies G. (2006) Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release. FEBS Lett. 580, 6311-6316. (Pubitemid 44750914)
33. Pfeiffer K., Gohil V., Stuart R. A., Hunte C., Brandt U., Greenberg M. L. and Schägger H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278, 52873-52880. (Pubitemid 38035887)
34. Pope S., Land J. M. and Heales S. J. (2008) Oxidative stress and mitochondrial dysfunction in neurodegeneration; cardiolipin a critical target? Biochim. Biophys. Acta 1777, 794-799.
35. Proctor G. R. and Harvey A. L. (2000) Synthesis of tacrine analogues and their structure-activity relationships. Curr. Med. Chem. 7, 295-302. (Pubitemid 30396440)
36. Pulfer M. and Murphy R. C. (2003) Electrospray mass spectrometry of phospholipids. Mass Spectrom. Rev. 22, 332-364.
37. Salaheldin A. M., Oliveira-Campos A. M. F., Parpot P., Rodrigues L. M., Oliveira M. M. and Peixoto F. (2010) Synthesis of new tacrine analogues from 4-amino-1H-pyrrole-3-carbonitrile. Helv. Chim. Acta 93, 242-248.
38. Schlame M., Rua D. and Greenberg M. L. (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39, 257-288. (Pubitemid 30224706)
39. Selkoe D. J. (1994) Alzheimer's disease: a central role for amyloid. J. Neuropathol. Exp. Neurol. 53, 438-447.
40. Sergent O., Ekroos K., Lefeuvre-Orfila L., Rissel M., Forsberg G.-B., Oscarsson J., Andersson T. B. and Lagadic-Gossmann D. (2009) Ximelagatran increases membrane fluidity and changes membrane lipid composition in primary human hepatocytes. Toxicol. In Vitro 23, 1305-1310.
41. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A. and Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and Alzheimer disease. Proc. Natl Acad. Sci. USA 88, 10540-10543. (Pubitemid 21915871)
42. Spaldin V., Madden S., Pool W. F., Woolf T. F. and Park B. K. (1994) The effect of enzyme inhibition on the metabolism and activation of tacrine by human liver microsomes. Br. J. Clin. Pharmacol. 38, 15-22. (Pubitemid 24222831)
43. Talesa V. N. (2001) Acetylcholinesterase in Alzheimer's disease. Mech. Ageing Dev. 122, 1961-1969.
44. Terry R. D. (2000) Cell death or synaptic loss in Alzheimer disease. J. Neuropathol. Exp. Neurol. 59, 1118-1119.
45. Tyurin V. A., Tyurina Y. Y., Feng W. et al. (2008) Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis. J. Neurochem. 107, 1614-1633.
46. Tyurina Y. Y., Tyurin V. A., Epperly M. W., Greenberger J. S. and Kagan V. E. (2008) Oxidative lipidomics of gamma-irradiationinduced intestinal injury. Free Radic. Biol. Med. 44, 299-314.
47. Vilela S. M. F., Santos D. J. S. L., Felix L., Almeida J. M., Antunes L. and Peixoto F. (2009) Are fentanyl and remifentanil safe opioids for rat brain mitochondrial bioenergetics? Mitochondrion 9, 247-253.
48. Wallace D. C. (1999) Mitochondrial diseases in man and mouse. Science 283, 1482-1488.
49. Wallace D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407.
50. Walsh D. M. and Selkoe D. J. (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193. (Pubitemid 39348839)
51. Watkins P. B., Zimmerman H. J., Knapp M. J., Gracon S. I. and Lewis K. W. (1994) Hepatotoxic effects of tacrine administration in patients with Alzheimer's disease. JAMA 271, 992-998. (Pubitemid 24099919)