Low molecular weight heparin prevents lipopolysaccharide induced-hippocampus-dependent cognitive impairments in mice

International Journal of Clinical and Experimental Pathology

Volumn 8, Issue 8, 2015, Pages 8881-8891

  Li, Renqi ^a   Tong, Jianhua ^a   Tan, Yuanhui ^a   Zhu, Sihai ^a   Yang, Jianjun ^a   Ji, Muhuo ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Cognitive impairments; Hippocampus; LMWH; Sepsis

Indexed keywords

ANTICOAGULANT AGENT; LIPOPOLYSACCHARIDE; LOW MOLECULAR WEIGHT HEPARIN;

ANIMAL; ANIMAL BEHAVIOR; BLOOD BRAIN BARRIER; C57BL MOUSE; COGNITIVE DEFECT; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; OXIDATIVE STRESS; PATHOLOGY; SEPSIS ASSOCIATED ENCEPHALOPATHY; WESTERN BLOTTING;

ANIMALS; ANTICOAGULANTS; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEPARIN, LOW-MOLECULAR-WEIGHT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; OXIDATIVE STRESS; SEPSIS-ASSOCIATED ENCEPHALOPATHY;

EID: 85012978098     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (35)

1. Iwashyna TJ, Ely EW, Smith DM, Langa KM. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 2010; 304: 1787-1794.
2. Gilmore EJ, Gaspard N, Choi HA, Cohen E, Burkart KM, Chong DH, Claassen J, Hirsch LJ. Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring. Intensive Care Med 2015; 41: 686-94.
3. Shah FA, Pike F, Alvarez K, Angus D, Newman AB, Lopez O, Tate J, Kapur V, Wilsdon A, Krishnan JA, Hansel N, Au D, Avdalovic M, Fan VS, Barr RG, Yende S. Bidirectional relationship between cognitive function and pneumonia. Am J Respir Crit Care Med 2013; 188: 586-592.
4. Widmann CN, Heneka MT. Long-term cerebral consequences of sepsis. Lancet Neurol 2014; 13: 630-636.
5. Hughes CG, Morandi A, Girard TD, Riedel B, Thompson JL, Shintani AK, Pun BT, Ely EW, Pandharipande PP. Association between endothelial dysfunction and acute brain dysfunction during critical illness. Anesthesiology 2013; 118: 631-639.
6. Li LF, Yang CT, Huang CC, Liu YY, Kao KC, Lin HC. Low-molecular-weight heparin reduces hyperoxia-augmented ventilator-induced lung injury via serine/threonine kinase-protein kinase B. Respir Res 2011; 12: 90.
7. Slofstra SH, van't Veer C, Buurman WA, Reitsma PH, ten Cate H, Spek CA. Low molecular weight heparin attenuates multiple organ failure in a murine model of disseminated intravascular coagulation. Crit Care Med 2005; 33: 1365-1370.
8. Li LF, Huang CC, Lin HC, Tsai YH, Quinn DA, Liao SK. Unfractionated heparin and enoxaparin reduce high-stretch ventilation augmented lung injury: a prospective, controlled animal experiment. Crit Care 2009; 13: R108.
9. Trzeciak S, Dellinger RP. Other supportive therapies in sepsis: an evidence-based review. Crit Care Med 2004; 32: S571-577.
10. Wahl F, Grosjean-Piot O, Bareyre F, Uzan A, Stutzmann JM. Enoxaparin reduces brain edema, cerebral lesions, and improves motor and cognitive impairments induced by a traumatic brain injury in rats. J Neurotrauma 2000; 17: 1055-1065.
11. Wildhagen KC, García de Frutos P, Reuteling-Sperger CP, Schrijver R, Aresté C, Ortega-Gómez A, Deckers NM, Hemker HC, Soehnlein O, Nicolaes GA. Nonanticoagulant heparin prevents histone-mediated cytotoxicity in vitro and improves survival in sepsis. Blood 2014; 123: 1098-1101.
12. Timmer NM, van Dijk L, van der Zee CE, Kiliaan A, de Waal RM, Verbeek MM. Enoxaparin treatment administered at both early and late stages of amyloid β deposition improves cognition of APPswe/PS1dE9 mice with differential effects on brain Aβ levels. Neurobiol Dis 2010; 40: 340-347.
13. Anderson ST, Commins S, Moynagh PN, Coogan AN. Lipopolysaccharide-induced sep sis induces long-lasting affective changes in the mouse. Brain Behav Immun 2015; 43: 98-109.
14. Wu J, Dong L, Zhang M, Jia M, Zhang G, Qiu L, Ji M, Yang J. Class I histone deacetylase inhibitor valproic acid reverses cognitive deficits in a mouse model of septic encephalopathy. Neurochem Res 2013; 38: 2440-2449.
15. Ji M, Dong L, Jia M, Liu W, Zhang M, Ju L, Yang J, Xie Z, Yang J. Epigenetic enhancement of brain-derived neurotrophic factor signaling pathway improves cognitive impairments induced by isoflurane exposure in aged rats. Mol Neurobiol 2014; 50: 937-944.
16. Czerniawski J, Guzowski JF. Acute neuroinflammation impairs context discrimination memory and disrupts pattern separation processes in hippocampus. J Neurosci 2014; 34: 12470-12480.
17. Li GM, Ji MH, Sun XJ, Zeng QT, Tian M, Fan YX, Li WY, Li N, Yang JJ. Effects of hydrogen-rich saline treatment on polymicrobial sepsis. J Surg Res 2013; 181: 279-286.
18. Hernandes MS, D'Avila JC, Trevelin SC, Reis PA, Kinjo ER, Lopes LR, Castro-Faria-Neto HC, Cunha FQ, Britto LR, Bozza FA. The role of Nox2-derived ROS in the development of cognitive impairment after sepsis. J Neuroin-flammation 2014; 11: 36.
19. Mina F, Comim CM, Dominguini D, Cassol-Jr OJ, Dall Igna DM, Ferreira GK, Silva MC, Galant LS, Streck EL, Quevedo J, Dal-Pizzol F. Il1-β involvement in cognitive impairment after sepsis. Mol Neurobiol 2014; 49: 1069-1076.
20. Terrando N, Rei Fidalgo A, Vizcaychipi M, Cibelli M, Ma D, Monaco C, Feldmann M, Maze M. The impact of IL-1 modulation on the development of lipopolysaccharide-induced cognitive dysfunction. Crit Care 2010; 14: R88.
21. Beurel E, Jope RS. Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J Neuroinflammation 2009; 6: 9.
22. Chavan SS, Huerta PT, Robbiati S, Valdes-Ferrer SI, Ochani M, Dancho M, Frankfurt M, Volpe BT, Tracey KJ, Diamond B. HMGB1 mediates cognitive impairment in sepsis survivors. Mol Med 2012; 18: 930-937.
23. Sparkman NL, Kohman RA, Garcia AK, Boehm GW. Peripheral lipopolysaccharide administration impairs two-way active avoidance conditioning in C57BL/6J mice. Physiol Behav 2005; 85: 278-288.
24. Wang YJ, Lu J, Wu DM, Zheng ZH, Zheng YL, Wang XH, Ruan J, Sun X, Shan Q, Zhang ZF. Ursolic acid attenuates lipopolysaccharide-induced cognitive deficits in mouse brain through suppressing p38/NF-κB mediated inflammatory pathways. Neurobiol Learn Mem. 2011; 96: 156-165.
25. Hong ZY, Shi XR, Zhu K, Wu TT, Zhu YZ. SCM-198 inhibits microglial overactivation and attenuates Aβ (1-40)-induced cognitive impairments in rats via JNK and NF-κB pathways. J Neuroinflammation 2014; 11: 147.
26. Clark PR, Kim RK, Pober JS, Kluger MS. Tumor Necrosis Factor Disrupts Claudin-5 Endothelial Tight Junction Barriers in Two Distinct NF-κB-Dependent Phases. PLoS One 2015; 10: e0120075.
27. Coletta C, Módis K, Oláh G, Brunyánszki A, Herzig DS, Sherwood ER, Ungvári Z, Szabo C. Endothelial dysfunction is a potential contributor to multiple organ failure and mortality in aged mice subjected to septic shock: preclinical studies in a murine model of cecal ligation and puncture. Crit Care 2014; 18: 511.
28. Vassiliou AG, Mastora Z, Orfanos SE, Jahaj E, Maniatis NA, Koutsoukou A, Armaganidis A, Kotanidou A. Elevated biomarkers of endothelial dysfunction/activation at ICU admission are associated with sepsis development. Cytokine 2014; 69: 240-247.
29. Fox ED, Heffernan DS, CioffiWG, Reichner JS. Neutrophils from critically ill septic patients mediate profound loss of endothelial barrier integrity. Crit Care 2013; 17: R226.
30. Wang Y, Braun Oö, Zhang S, Norström E, Thorlacius H. Monocytes regulate systemic coagulation and inflammation in abdominal sepsis. Am J Physiol Heart Circ Physiol 2015; 308: H540-547.
31. Imamura Y, Wang H, Matsumoto N, Muroya T, Shimazaki J, Ogura H, Shimazu T. Interleukin-1β causes long-term potentiation deficiency in a mouse model of septic encephalopathy. Neuroscience 2011; 187: 63-69.
32. Flierl MA, Stahel PF, Rittirsch D, Huber-Lang M, Niederbichler AD, Hoesel LM, Touban BM, Morgan SJ, Smith WR, Ward PA, Ipaktchi K. Inhibition of complement C5a prevents breakdown of the blood-brain barrier and pituitary dysfunction in experimental sepsis. Crit Care 2009; 13: R12.
33. Weberpals M, Hermes M, Hermann S, Kummer MP, Terwel D, Semmler A, Berger M, Schäfers M, Heneka MT. NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J Neurosci 2009; 29: 14177-14184.
34. Vasconcelos AR, Yshii LM, Viel TA, Buck HS, Mattson MP, Scavone C, Kawamoto EM. Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment. J Neuroinflammation 2014; 11: 85.
35. Bilbo SD, Barrientos RM, Eads AS, Northcutt A, Watkins LR, Rudy JW, Maier SF. Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav Immun 2008; 22: 451-455.