Delta2-specific opioid receptor agonist and hibernating woodchuck plasma fraction provide ischemic neuroprotection

Academic Emergency Medicine

Volumn 15, Issue 3, 2008, Pages 250-257

  Govindaswami, Meera ^a,b   Brown, Stephan A ^a   Yu, Jin ^c   Zhu, Hong ^c   Bishop, Paul D ^d   Kindy, Mark S ^c   Oeltgen, Peter R ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d ZYMOGENETICS INC   (United States)

Author keywords

Cerebral ischemia; Focal; Hibernation; Neuroprotection; Nitric oxide; Opioid; Receptors

Indexed keywords

DELTORPHIN; DELTORPHIN D; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; NITRATE; NITRIC OXIDE SYNTHASE; OPIATE AGONIST; UNCLASSIFIED DRUG; DELTA OPIATE RECEPTOR; NEUROPROTECTIVE AGENT; NITRIC OXIDE; OLIGOPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIORAL SCIENCE; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; CELL CULTURE; CONTROLLED STUDY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PLASMA; PRIORITY JOURNAL; ANIMAL; BLOOD; C57BL MOUSE; COMPARATIVE STUDY; DISEASE MODEL; DRUG POTENTIATION; HIBERNATION; MOUSE MUTANT; PHYSIOLOGY; REFERENCE VALUE; SCIURIDAE; SECRETION;

ANIMALS; BRAIN ISCHEMIA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HIBERNATION; MALE; MARMOTA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; OLIGOPEPTIDES; RECEPTORS, OPIOID, DELTA; REFERENCE VALUES;

EID: 48949120278     PISSN: 10696563     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1553-2712.2008.00048.x     Document Type: Article

References (38)

1. Koroshetz WJ, Moskowitz MA. Emerging treatments for stroke in humans. Trends Pharmacol Sci 1996; 17:227-33.
2. Read SJ. Pharmacological therapy for acute stroke. Curr Opin Investig Drugs. 2000; 1:329-39.
3. Dirnagl U, Simon RP, Hallenbeck JM. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 2003; 26:248-54.
4. Schaller B, Graf R. Cerebral ischemia and reperfusion: the pathophysiologic concept as a basis for clinical therapy. J Cereb Blood Flow Metab. 2004; 24:351-71.
5. Nawashiro H, Tasaki K, Reutzler CA, Hallenbeck JM. TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab. 1997; 17:483-90.
6. Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab. 2001; 21:2-14.
7. Belayev L, Marcheselli VL, Khoutorova L, et al. Docosaheyaenoic acid completed to albumin elicits high-grade ischemic neuroprotection. Stroke. 2005; 36:118-23.
8. Ellsworth JL, Garcia R, Yu J, Kindy MS. Fibroblast growth factor-18 reduced infarct volumes and behavioral deficits after transient occlusion of the middle cerebral artery in rats. Stroke. 2003; 34:1-6.
9. Hallenbeck JM. Cytokines, macrophages, and leukocytes in brain ischemia. Neurology. 1997; 49(5 Suppl 4):S5-9.
10. Frerichs KU, Hallenback JM. Hibernation in ground squirrels induces state and species specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J Cereb Blood Flow Metab. 1998; 18:168-75.
11. Oeltgen PR, Nuchols PA, Nilikani SP, Spurrier WA, Su TP. Further studies on hibernation: delta opioid-induced hibernation in summer-active ground squirrels. Life Sci. 1988; 43:1565-74.
12. Chien S, Oeltgen PR, Diana JN, Shi X, Nilikani SP. Two-day preservation of major organs using autoperfusion multiorgan preparation and hibernation induction trigger. A preliminary report. J Thorac Cardiovasc Surg. 1991; 102:224-34.
13. Chien S, Oeltgen PR, Diana JN, Salley R, Su TP. Extension of tissue survival time in multiorgan block preparation using delta opioid DADLE. J Thorac Cardiovasc Surg. 1994; 107:964-7.
14. Oeltgen PR, Horton N, Bolling SR, Su TP. Extended lung preservation with the use of hibernation induction factors. Ann Thorac Surg. 1996; 61:1488-93.
15. Bolling SF, Benedict MB, Tramontini NL, Kilgore KS, Harlow HJ, Oeltgen PR. Hibernation triggers and myocardial protection. Circulation. 1998; 98:11220-3.
16. Bolling SF, Tramontimi NL, Kilgore K, Su TP, Harlow H, Oeltgen PR. Use of "natural" hibernation induction triggers for myocardial protection. Ann Thorac Surg. 1997; 64:623-7.
17. Bolling SF, Su TP, Childs KF, et al. The use of hibernation induction triggers for cardiac transplantation preservation. Transplantation. 1997; 63:326-9.
18. Bolling SF, Badhwar V, Schwartz CF, Oeltgen PR, Kilgore K, Su TP. Opioids confer myocardial tolerance to ischemia: interaction of delta opioids agonists and antagonists. J Thorac Cardiovas Surg. 2001; 122:476-81.
19. Jahania MS, Wedge J, Oeltgen PR, Govindaswami M, Sanchez JA. Hibernation induction trigger reduces infarct size and improves recovery of ventricular function after ischemia in the isolated perfused rat heart [abstract]. Surg Forum. 1999; 50:96-8.
20. Govindaswami M, Sanchez A, Wedge J, et al. Opioid-like hibernation factors provide protection to the ischemic myocardium. In: Heldmaier G, Klingenspor M, eds. Life in the Cold: Eleventh International Hibernation Symposium. Berlin: Springer-Verlag, 2000: pp 377-84.
21. Sigg DC, Coles J, Oeltgen PR, Iaizzo PA. Role of delta-opioid receptor agonists on infarct size reduction in swine. Am J Physiol. 2002; 282:H1953-60.
22. Oeltgen PR, Govindaswami M, Witzke DB. 24-hour pretreatment with delta opioid enhances survival from hemorrhagic shock. Acad Emerg Med. 2006; 13:127-33.
23. Lazarus LH, Bryant SD, Attila M, Salvadori S. Frog skin opioid peptides: a case for environmental mimicry. Health Perspect. 1994; 102(8): 648-53.
24. 2]deltorphin, a 17 amino acid opioid peptide from the skin of the Brazilian hylid frog, Phyllomedusa burmeisteri. Peptides. 1994; 15(2) 199-202.
25. Ohshima H, Tsuda M, Adachi H, Ogurta T, Sugimura T, Esumi H. L-Arginine-dependent formation of N-nitrosamines by the cytosol of macrophages activated with lipopolysaccharide and interferon-γ. Carcinogenesis. 1991; 12(7):1217-20.
26. Dubal DB, Rau SW, Shughrue PJ, et al. Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death. Endocrinology. 2006; 147:3076-84.
27. Ellsworth JL, Garcia R, Yu J, Kindy MS. Time window of fibroblast growth factor-18-mediated neuroprotection after occlusion of the middle cerebral artery in rats. J Cereb Blood Flow Metab. 2004; 24:114-23.
28. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 1994; 265:1883-5.
29. Smith-Sonneborn J, Gottsch H, Cubin E, Oeltgen PR, Thomas P. Alternative strategy for stress tolerance: opioids. J Gerontol A Biol Sci Med Sci. 2004; 59:433-40.
30. Zhao Z, Huang PL, Iadecola C. L-Arginine increases ischemic injury in wild-type mice but not in iNOS-deficient mice. Brain Res. 2003; 966:508-311.
31. Horton ND, Kaftani DJ, Bruce DS, et al. Isolation and partial characterization of an opioid-like 88KDa hibernation related protein. Comp Biochem Physiol. 1998; 119:789-807.
32. del-Zoppo G, Ginis I, Hallenbeck JM, Iadecola C, Wang X, Feuerstein GZ. Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol. 2000; 10:95-112.
33. McCarron RM, Wang L, Siren AL, Spatz M, Hellenbeck JM. Monocyte adhesion to cerebromicrovascular endothelial cells derived from hypertensive and normotensive rats. Am J Physiol. 1994; 267(6 Pt 2):H2491-7.
34. Yasuma Y, McCarron M, Spatz M, Hallenbeck JM. Effects of plasma from hibernating ground squirrels on monocyte endothelial cell adhesive interactions. Am J Physiol. 1997; 273(6 Pt 2):R1861-9.
35. Chien S, Oeltgen PR. Using Hibernation Induction Trigger for Organ Preservation. Xanthus Medical Intelligence Unit Reports. Austin, TX: R.G. Landes Co., 1993, pp 1-118.
36. Adrie C, Bloch KD, Moreno PR, et al. Inhaled nitric oxide increases coronary artery patency after thrombolysis. Circulation. 1996; 94:1919-26.
37. Fox-Robichaud A, Payne D, Hasan SU, et al. Inhaled NO as a viable antiadhesive therapy for ischemia?reperfusion injury of distal microvascular beds. J Clin Invest. 1998; 101:2497-505.
38. Hustad TL, Govindaswami M, Oeltgen PR, Rudich SM, Lentsch AB. A Delta2-opioid agonist inhibits p38 MAPX and suppresses activation of murine macrophages. J Surg Res. 2005; 28:45-9.