Apoptotic markers and DNA damage are related to late phase of stroke: Involvement of dyslipidemia and inflammation

Physiology and Behavior

Volumn 151, Issue , 2015, Pages 369-378

  Pascotini, Eduardo Tanuri ^a   Flores, Ariane Ethur ^a   Kegler, Aline ^a   Gabbi, Patricia ^a   Bochi, Guilherme Vargas ^a   Algarve, Thais Doeler ^a   Prado, Ana Lucia Cervi ^b   Duarte, Marta M M F ^a   da Cruz, Ivana B M ^a   Moresco, Rafael Noal ^a   Royes, Luiz Fernando Freire ^a   Fighera, Michele Rechia ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b Hospital Universitário de Santa Maria   (Brazil)

Author keywords

Caspases; DNA damage; Dyslipidemia; Inflammation; Oxidative stress; Stroke

Indexed keywords

ACETYLCHOLINESTERASE; ALKALINE PHOSPHATASE; CASPASE 3; CASPASE 8; DICHLORODIHYDROFLUORESCEIN; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NITRATE; NITRITE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; CASPASE; CHOLESTEROL; ORGANIC COMPOUND; PICOGREEN;

ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; BLOOD SAMPLING; CASE CONTROL STUDY; CEREBROVASCULAR ACCIDENT; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DYSLIPIDEMIA; FEMALE; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HUMAN; INFLAMMATION; MALE; MIDDLE AGED; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; STROKE PATIENT; AGED; APOPTOSIS; COMPLICATION; DYSLIPIDEMIAS; METABOLISM; PHYSIOLOGY;

AGED; APOPTOSIS; CASE-CONTROL STUDIES; CASPASES; CHOLESTEROL; DNA DAMAGE; DYSLIPIDEMIAS; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; NITRITES; ORGANIC CHEMICALS; STROKE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84939425132     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.08.005     Document Type: Article

References (58)

1. Alvarez-Sala L.A., Cachofeiro V., Masana L., Suarez C., Pinilla B., Plana N., Trias F., Moreno M.A., Gabus G., Lahera V., Pinto X. Effects of fluvastatin extended-release (80mg) alone and in combination with ezetimibe (10mg) on low-density lipoprotein cholesterol and inflammatory parameters in patients with primary hypercholesterolemia: a 12-week, multicenter, randomized, open-label, parallel-group study. Clin. Ther. 2008, 30:84-97.
2. Bachorik P.S., Albers J.J. Precipitation methods for quantification of lipoproteins. Methods Enzymol. 1986, 129:78-100.
3. Banati R.B., Gehrmann J., Schubert P., Kreutzberg G.W. Cytotoxicity of microglia. Glia 1993, 7(1):111-118.
4. Ben-Assayag E., Shenhar-Tsarfaty S., Ofek K., Soreq L., Bova I., Shopin L., Berg M.G., Berliner S., Shapira I., Bornstein N.M., Soreq H. Serum cholinesterase activities distinguish between stroke patients and controls and predict 12-month mortality. Mol. Med. 2010, 16(7-8):278-286.
5. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405(6785):458-462.
6. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 1999, 15:269-290. Review.
8. Cechetti F., Worm P.V., Lovatel G., Moysés F., Siqueira I.R., Netto C.A. Environmental enrichment prevents behavioral deficits and oxidative stress caused by chronic cerebral hypoperfusion in the rat. Life Sci. 2012, 91:29-36.
9. Chong Z.Z., Li F.Q., Maiese K. Oxidative stress in the brain: Novel cellular targets that govern survival during neurodegenerative disease. Prog. Neurobiol. 2005, 75:207-246.
10. De Silva T.M., Brait V.H., Drummond G.R., Sobey C.G., Miller A.A. Nox2 oxidase activity accounts for the oxidative stress and vasomotor dysfunction in mouse cerebral arteries following ischemic stroke. PlosOne 2011, 6(12).
11. Di Napoli M., Papa F. Inflammation, hemostatic markers, and antithrombotic agents in relation to long-term risk of new cardiovascular events in first-ever ischemic stroke patients. Stroke 2002, 33:1763-1771.
12. Duarte M.M., Moresco R., Duarte T., Santi A., Bagatini M.D., Da Cruz I.B.M., Schetinger M.R.C., Loro V.L. Oxidative stress in hypercholesterolemia and its association with Ala16Val superoxide dismutase gene polymorphism. Clin. Biochem. 2010, 10.1016/j.clinbiochem.2010.07.002.
13. Elkind M.S., Cheng J., Rundek T., Boden-Albala B., Sacco R.L. Leukocyte count predicts outcome after ischemic stroke: the Northern Manhattan Stroke Study. J. Stroke Cerebrovasc. Dis. 2004, 13:220-227.
14. Esposti, MD. (2002) Measuring mitochondrial reactive oxygen species. Methods v. 26, p. 335-340.
15. Friedewald W.T., Levy R.I., Fredrickson D.S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without the use of preparative ultracentrifuge. Clin. Chem. 1972, 18:499-502.
16. Goldstein L.B., Bushnell C.D., Adams R.J., Appel J.L., Braun L.T., Chaturvedi S., Creager M.A., Culebras A., Eckel R.H., Hart R.G., Hinchey J.A., Howard V.J., Jauch E.C., Levine S.R., Meschia J.F., Moore W.S., Nixon J.V., Pearson T.A. Guidelines for the primary prevention of stroke: a Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke 2011, 42(2):517-584.
17. Gross A., Yin X.M., Wang K., Wei M., Jockel J., Milliman C., Erdjument-Bromage H., Tempst P., Korsmeyer J. Caspase cleaved bid targets mitochondria and is required for cytochrome c release, while bcl-xl prevents this release but not tumor necrosis factor-r1/fas death. J of Bio Chem 1999, 274(2):1156-1163. Issue of January 8.
18. Ha T.T., Huy N.T., Murao L.A., Lan N.T., Thuy T.T., Tuan H.M., Nga C.T., Tuong V.V., Dat T.V., Kikuchi M., Yasunami M., Morita K., Huong V.T., Hirayama K. Elevated levels of cell-free circulating DNA in patients with acute dengue virus infection. PLoS One 2011, 6(10):e25969. (2011). 10.1371/journal.pone.0025969.
19. Halvorsen B., Otterdal K., Dahl T.B., Skjelland M., Gullestad L., Oie E., Aukrust P. Atherosclerotic plaque stability-what determines the fate of a plaque?. Prog. Cardiovasc. Dis. 2008, 51:183-194.
20. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 2005, 352:1685-1695.
21. Holm S., Ueland T., Dahl T.B., Michelsen A.E., Skjelland M., Russell D., Nymo S.H., Krohg-Sorensen K., Clausen O.P., Atar D., Januzzi J.L., Aukrust P., Jensen J.K., Halvorsen B. Fatty acid binding protein 4 is associated with carotid atherosclerosis and outcome in patients with acute ischemic stroke. PLoS One 2011, 6(12):e28785. 10.1371/journal.pone.0028785.
22. Kawashima K., Fujii T. Extraneuronal cholinergic system in lymphocytes. Pharmacol. Ther. 2000, 86(1):29-48. (2000 Apr).
23. Kawashima K., Fujii T. The lymphocytic cholinergic system and its contribution to the regulation of immune activity. Life Sci. 2003, 74(6):675-696. See comment in PubMed Commons below.
24. Keles T., Akar Bayram N., Kayhan T., Canbay A., Sahin D., Durmaz T., Ozdemir O., Aydogdu S., Diker E. The comparison of the effects of standard 20mg atorvastatin daily and 20mg atorvastatin every other day on serum LDL-cholesterol and high sensitive C-reactive protein levels. Anadolu Kardiyol Derg 2008, 8:407-412.
25. Lloyd-Jones D., Adams R.J., Brown T.M., Carnethon M., Dai S., De Simone G., Ferguson T.B., Ford E., Furie K., Gillespie C., Go A., Greenlund K., Haase N., Hailpern S., Ho P.M., Howard V., Kissela B., Kittner S., Lackland D., Lisabeth L., Marelli A., McDermott M.M., Meigs J., Mozaffarian D., Mussolino M., Nichol G., Roger V.L., Rosamond W., Sacco R., Sorlie P., Stafford R., Thom T., Wasserthiel-Smoller S., Wong N.D., Wylie-Rosett J. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010, 121:e46-e215. (Epub December 17, 2009).
26. Lambertsen K.L., Biber K., Finsen B. Inflammatory cytokines in experimental and human stroke. J. Cereb. Blood Flow Metab. 2012, 32:1677-1698.
27. Love S. Oxidative stress in brain ischemia. Brain Pathol. 1999, 9:119-131.
28. Mahalle N., Garg M., Kulkarni M., Naik S. Association of inflammatory cytokines with traditional and nontraditional cardiovascular risk factors in Indians with known coronary artery disease. Ann Med Health Sci Res 2014, 4(5):706-712. Sep.
29. Martinez-Hervas S., Real J.T., Ivorra C., Priego A., Chaves F.J., Pallardo F.V., Vina J.R., Redon J., Carmena R., Ascaso J.F. Increased plasma xanthine oxidase activity is related to nuclear factor kappa beta activation and inflammatory markers in familial combined hyperlipidemia. Nutr. Metab. Cardiovasc. Dis. 2010, 20:734-739.
30. McCoy M.K., Tansey M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflammation 2008, 5(45). (Oct 17).
31. Micheau O., Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114(2):181-190. (Jul 25).
32. Miller A.A., Drummond G.R., De Silva T.M., Mast A.E., Hickey H., Willians J.P., Broughton B.R., Sobey C.G. NADPH oxidase activity is higher in cerebral versus systemic arteries of four animal species: role of Nox2. Am J Physiol Heart Circ Physiol 2009, 296:H220-H225.
33. Miller A.A., Drummond G.R., Schmidt H.H., Sobey C.G. NADPH oxidase activity and function are profoundly greater in cerebral versus systemic arteries. Circ. Res. 2005, 97:1055-1062.
34. Miller A.A., Dusting G.J., Roulston C.L., Sobey C.G. NADPH-oxidase activity is elevated in penumbral and non-ischemic cerebral arteries following stroke. Brain Res. 2006, 1111:111-116.
35. Nakajima K., Kohsaka S. Microglia: activation and their significance in the central nervous system. J. Biochem. 2001, 130(2):169-175.
36. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K.J., Yuan J., Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 1998, 18:3659-3668.
37. Norrving B., Kessela B. The global burden of stroke and need for a continuum of care. Neurology 2013, 80(3 Suppl 2):S5-12. (Jan 15).
38. Ofek K., Krabbe K.S., Evron T., Debecco M., Nielsen A.R., Brunnsgaad H., Yirmiya R., Soreq H., Pedersen B.K. Cholinergic status modulations in human volunteers under acute inflammation. J. Mol. Med. 2007, 85:1239-1251.
39. Parizadeh M.R., Azarpazhooh M.R., Mobarra N., Nematy M., Alamdari D.H., Tavalaie S., Sahebkar A., Hassankhani B., Ferns G., Ghayour-Mobarhan M. Prooxidant-antioxidant balance in stroke patients and 6-month prognosis. Clin Lab. 2011, 57(3-4):183-191.
40. Rothwell N., Allan S., Toulmond S. The role of interleukin 1 in acute neurodegeneration and stroke: pathophysiological and therapeutic implications. J. Clin. Invest. 1997, 100(11):2648-2652. (Dec 1).
41. Schneider-Brachert W., Tchikov V., Neumeyer J., Jakob M., Winoto-Morbach S., Held-Feindt J., Heinrich M., Merkel O., Ehrenschwender M., Adam D., Mentlein R., Kabelitz D., Schütze S. Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 2004, 21(3):415-428. (Sep).
42. Shaked I., Meerson A., Wolf Y., Avni R., Greenberg D., Gilboa-Geffen A., Soreq H. MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 2009, 31:965-973. (cover. Accompanied by preview O'Neil, L.A.J. (2009) Boosting the brain's ability to block inflammation via microRNA-132. Immunity 31:854-5).
43. Shichita TG, Sakaguchi TR, Suzuki M, Yoshimura A. (2012) Post-ischemic inflammation in the brain. Frontier In., Volume 3; (Article 132).
44. Sugawara T., Fujimura M., Noshita N., Noshita N., Kim G.W., Saito A., Hayashi T., Narasimhan P., Maier C.M., Chan P.H. Neuronal death/survival signaling pathways in cerebral ischemia. Neuro Rx. 2004, 1:17-25.
45. Tatsch E., Bochi G.V., Pereira Rda S., Kober H., Agertt V.A., de Campos M.M., Gomes P., Duarte M.M., Moresco R.N. A simple and inexpensive automated technique for measurement of serum nitrite/nitrate. Clin. Biochem. 2011, 44(4):348-350. (Mar).
46. Vila N., Castillo J., Davalos A., Chamorro A. Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000, 31:2325-2329.
47. Yamamoto E., Tamamaki N., Nakamura T., Kataoka K., Tokutomi Y., Dong Y.F., Fukuda M., Matsuba S., Ogawa H., Kim-Mitsuyama S. Excess salt causes cerebral neuronal apoptosis and inflammation in stroke-prone hypertensive rats through angiotensin II-induced NADPH oxidase activation. Stroke 2008, 39:3049-3056.
48. Woodruff T.M., Thundyil J., Tang S.C., Sobey C.G., Taylor S.M., Arumugam T.V. Pathophysiology, treatment, and animal and cellular models of humanischemic stroke. Mol. Neurodegener. 2011, 6:11-29.
49. World Health Organization World Health Report 2010, 2010. World Health Organization, Geneva, Switzerland.
50. Zhao Y., Li S., Childs E.E., Kuharsky D., Yin X.M. Activation of pro-death bcl-2 family proteins and mitochondria apoptosis pathway in tumor necrosis factor-a-induced liver injury. J of Bio Chem 2001, 276(29):27422-27427. (Issue of July 20).
51. Allain C.C., Poon L.S., Chan C.S., Richmond W., Fu P.C. Enzymatic determination of total serum cholesterol. Clin Chem 1974 Apr, 20(4):470-475.
52. Libby P. Inflammtion and atherosclerosis. Curr Atheroscler Rep 2002, 6:131-139.
53. Skilton M.R., Moulin P., Sérusclat A., Nony P., Bonnet F. A Comparison of the NCEP-ATPIII, IDF and AHA/NHLBI metabolic syndrome definitions with relation to early carotid atherosclerosis in subjects with hypercholesterolemia or at risk of CVD: evidence of sex-specific differences. Atherosclerosis 2007, 190:416-422.
54. Harrison D., Griendling K.K., Lanmesser U., Hornig B., Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol 2003, 91:7A-11A.
55. Gautier E., Jakubzick C., Randolph G.J. Regulation of the migraton and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol 2009, 29:1412-1418.
56. Scalia R., Appel J.Z., Lefer A.M. Leukocute-endothelium interaction during the early stages of hypercholesterolemia in the rabbit: role of P-selectin, ICAM-1 and VCAM-1. Arterioscler Thromb Vasc Biol 1998, 18:1093-1100.
57. Persson J., Nisson J., Lindholm M.W. Cytokine response to lipoprotein lipid loading in human monocyte derived macrophages. Lipids Health Dis 2006, 5(17):1-8.
58. Emmanuel L. Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol 2009, 29:1412-1418.