Skip to main content
SpringerLink
Log in

Delta Opioid Receptor in Cerebral Preconditioning

  • Chapter
  • First Online:
Neural Functions of the Delta-Opioid Receptor

  • 425 Accesses

Abstract

Cerebral infarction is a leading cause of morbidity and mortality in the United States. Activation of the delta-opioid receptor has been shown to decrease damage in many models of cerebral protection. In this chapter we gather the work that has been done on the topic, including work to establish the efficacy of the delta-opioid receptor in protection in animals, and the work done to elucidate potential mechanisms. However, most of the previous work was performed in rodents. Testing whether activation of the delta-opioid receptor can induce neuroprotection in large animals and then in humans is needed to fully establish its usefulness in clinical practice.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

ATP:

Adenosine triphosphate

Bcl2:

B-cell lymphoma-2

BNTX:

7-Benzylidenenaltrexone

DADLE:

[D-Ala2, D-Leu5]-enkephalinamide

DOR:

Delta opioid receptor

ERK:

Extracellular signal-regulated kinases

GABA:

Gamma-aminobutyric acid

HIF-1 α:

Hypoxia-inducible factor-1α

HPC:

Hypoxic preconditioning

mitoKATP :

Mitochondrial ATP-activated potassium channel

NMDA:

N-methyl-D-aspartate

OGD:

Oxygen-glucose deprivation

PKC:

Protein kinase C

Trk:

Tropomyosine receptor kinase

References

  • Bhuiyan MIH, Kim YJ (2010) Mechanisms and prospects of ischemic tolerance induced by cerebral preconditioning. Int Neurourol J 14:203–212

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruer U, Weih MK, Isaev NK, Meisel A, Ruscher K, Bergk A, Trendelenburg G, Wiegand F, Victorov IV, Dirnagl U (1997) Induction of tolerance in rat cortical neurons: hypoxic preconditioning. FEBS Lett 414:117–121

    Article  PubMed  CAS  Google Scholar 

  • Chao D, Donnelly DF, Feng Y, Bazzy-Asaad A, Xia Y (2006) Cortical [delta]-opioid receptors potentiate K+ homeostasis during anoxia and oxygen-glucose deprivation. J Cereb Blood Flow Metab 27:356–368

    Article  PubMed  Google Scholar 

  • Chao D, Bazzy-Asaad A, Balboni G, Xia Y (2007) δ-, But not μ-, opioid receptor stabilizes K+ homeostasis by reducing Ca2+ influx in the cortex during acute hypoxia. J Cell Physiol 212:60–67

    Article  PubMed  CAS  Google Scholar 

  • Chao D, Bazzy-Asaad A, Balboni G, Salvadori S, Xia Y (2008) Activation of DOR attenuates anoxic K+ derangement via inhibition of Na + entry in mouse cortex. Cereb Cortex 18:2217–2227

    Article  PubMed  PubMed Central  Google Scholar 

  • Chao D, He X, Yang Y, Bazzy-Asaad A, Lazarus LH, Balboni G, Kim DH, Xia Y (2012) DOR activation inhibits anoxic/ischemic Na + influx through Na + channels via PKC mechanisms in the cortex. Exp Neurol 236:228–239

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dahl N, Balfour W (1964) Prolonged anoxic survival due to anoxia pre-exposure: brain atp, lactate, and pyruvate. Am J Physiology 207:452–456

    CAS  Google Scholar 

  • Gao CJ, Li JP, Wang W, Lu BC, Niu L, Zhu C, Wei YY, Zhang T, Wu SX, Chai W, Li YQ (2010) Effects of intracerebroventricular application of the delta opioid receptor agonist [d-Ala2, d-Leu5] enkephalin on neurological recovery following asphyxial cardiac arrest in rats. Neuroscience 168:531–542

    Article  PubMed  CAS  Google Scholar 

  • Gao CJ, Niu L, Ren PC, Wang W, Zhu C, Li YQ, Chai W, Sun XD (2012) Hypoxic preconditioning attenuates global cerebral ischemic injury following asphyxial cardiac arrest through regulation of delta opioid receptor system. Neuroscience 202:352–362

    Article  PubMed  CAS  Google Scholar 

  • Ginis I, Jaiswal R, Klimanis D, Liu J, Greenspon J, Hallenbeck JM (2002) TNF-[agr]-induced tolerance to ischemic injury involves differential control of NF-[kgr]B transactivation[colon] the role of NF-[kgr]B association with p300 adaptor. J Cereb Blood Flow Metab 22:142–152

    Article  PubMed  CAS  Google Scholar 

  • Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2013) Heart disease and stroke statistics: 2013 update: a report from the American Heart Association. Circulation 127:e6–e245

    Article  PubMed  Google Scholar 

  • Grabb MC, Choi DW (1999) Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 19:1657–1662

    PubMed  CAS  Google Scholar 

  • Hansen A (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65:101–148

    PubMed  CAS  Google Scholar 

  • Heurteaux C, Lauritzen I, Widmann C, Lazdunski M (1995) Essential role of adenosine, adenosine A1 receptors, and ATP-sensitive K+ channels in cerebral ischemic preconditioning. Proc Natl Acad Sci U S A 92:4666–4670

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang H, Gao TM, Gong L, Zhuang Z, Li X (2001) Potassium channel blocker TEA prevents CA1 hippocampal injury following transient forebrain ischemia in adult rats. Neurosci Lett 305: 83–86

    Google Scholar 

  • Ikeda Y, Miura T, Sakamoto J, Miki T, Tanno M, Kobayashi H, Ohori K, Takahashi A, Shimamoto K (2006) Activation of ERK and suppression of calcineurin are interacting mechanisms of cardioprotection afforded by δ-opioid receptor activation. Basic Res Cardiol 101:418–426

    Google Scholar 

  • Iwata M, Inoue S, Kawaguchi M, Nakamura M, Konishi N, Furuya H (2007) Effects of delta-opioid receptor stimulation and inhibition on hippocampal survival in a rat model of forebrain ischaemia. Br J Anaesth 99:538–546

    Article  PubMed  CAS  Google Scholar 

  • Kang X, Chao D, Gu Q, Ding G, Wang Y, Balboni G, Lazarus L, Xia Y (2009) Delta-opioid receptors protect from anoxic disruption of Na+ homeostasis via Na+ channel regulation. Cell Mol Life Sci 66:3505–3516

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kapinya KJ, Lowl D, Futterer C, Maurer M, Waschke KF, Isaev NK, Dirnagl U (2002) Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 33:1889–1898

    Article  PubMed  CAS  Google Scholar 

  • Kitagawa K, Matsumoto M, Kuwabara K, Tagaya M, Ohtsuki T, Hata R, Ueda H, Handa N, Kimura K, Kamada T (1991) ‘Ischemic tolerance’ phenomenon detected in various brain regions. Brain Res 561:203–211

    Article  PubMed  CAS  Google Scholar 

  • Kume M, Yamamoto Y, Saad S, Gomi T, Kimoto S, Shimabukuro T, Yagi T, Nakagami M, Takada Y, Morimoto T, Yamaoka Y (1996) Ischemic preconditioning of the liver in rats: implications of heat shock protein induction to increase tolerance of ischemia-reperfusion injury. J Lab Clin Med 128:251–258

    Google Scholar 

  • Lim YJ, Zheng S, Zuo Z (2004) Morphine preconditions purkinje cells against cell death under in vitro simulated ischemia-reperfusion conditions. Anesthesiology 100:562–568

    Google Scholar 

  • Liu D, Slevin JR, Lu C, Chan SL, Hansson M, Elmér E, Mattson MP (2003) Involvement of mitochondrial K+ release and cellular efflux in ischemic and apoptotic neuronal death. J Neurochem 86:966–979

    Google Scholar 

  • Ma M-C, Qian H, Ghassemi F, Zhao P, Xia Y (2005) Oxygen-sensitive delta-opioid receptor-regulated survival and death signals: novel insights into neuronal preconditioning and protection. J Biol Chem 280:16208–16218

    Google Scholar 

  • Marini A, Popolo M, Pan H, Blondeau N, Lipsky R (2008) Brain adaptation to stressful stimuli: a new perspective on potential therapeutic approaches based on BDNF and NMDA receptors. CNS Neurol Disord Drug Targets 7:382–390

    Article  PubMed  CAS  Google Scholar 

  • Moncayo J, de Freitas G, Bogousslavsky J, Altieri M, van Melle G (2000) Do transient ischemic attacks have a neuroprotective effect? Neurology 54:2089–2094

    Google Scholar 

  • Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136

    Google Scholar 

  • Narita M, Kuzumaki N, Miyatake M, Sato F, Wachi H, Seyama Y, Suzuki T (2006) Role of δ-opioid receptor function in neurogenesis and neuroprotection. J Neurochem 97:1494–1505

    Article  PubMed  CAS  Google Scholar 

  • Pasupathy S, Homer-Vanniasinkam S (2005) Ischaemic preconditioning protects against ischaemia/reperfusion injury: emerging concepts. Eur J Vasc Endovasc Surg 29:106–115

    Google Scholar 

  • Peng P-H, Huang H-S, Lee Y-J, Chen Y-S, Ma M-C (2009) Novel role for the δ-opioid receptor in hypoxic preconditioning in rat retinas. J Neurochem 108:741–754

    Google Scholar 

  • Schwartz-Bloom RD, Sah R (2001) gamma-Aminobutyric acid(A) neurotransmission and cerebral ischemia. J Neurochem 77:353–371

    Google Scholar 

  • Sommer C, Kiessling M (2002) Ischemia and ischemic tolerance induction differentially regulate protein expression of GluR1, GluR2, and AMPA receptor binding protein in the gerbil hippocampus: GluR2 (GluR-B) reduction does not predict neuronal death. Stroke 33:1093–1100

    Google Scholar 

  • Sommer C, Fahrner A, Kiessling M (2003) Postischemic neuroprotection in the ischemia-tolerant state gerbil hippocampus is associated with increased ligand binding to inhibitory GABA(A) receptors. Acta Neuropathol 105:197–202

    Google Scholar 

  • Stagliano NE, Perez-Pinzon MA, Moskowitz MA, Huang PL (1999) Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 19:757–761

    Google Scholar 

  • Su D-S, Wang Z-H, Zheng Y-J, Zhao Y-H, Wang X-R (2007) Dose-dependent neuroprotection of delta opioid peptide [d-Ala2, d-Leu5] enkephalin in neuronal death and retarded behavior induced by forebrain ischemia in rats. Neurosci Lett 423:113–117

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Calderone A , Jover T, Grooms SY, Yokota H, Zukin RS, Bennett MV (2002) Ischemic preconditioning acts upstream of GluR2 down-regulation to afford neuroprotection in the hippocampal CA1. Proc Natl Acad Sci USA 99:2362–2367

    Google Scholar 

  • Tian X, Guo J, Zhu M, Li M, Wu G, Xia Y (2013) δ-Opioid receptor activation rescues the functional TrkB receptor and protects the brain from ischemia-reperfusion injury in the rat. PLoS One 8:e69252

    Google Scholar 

  • Toosy N, McMorris EL, Grace PA, Mathie RT (1999) Ischaemic preconditioning protects the rat kidney from reperfusion injury. BJU Int. 84:489–494

    Google Scholar 

  • Wei L, Yu SP, Gottron F, Snider BJ, Zipfel GJ, Choi DW (2003) Potassium channel blockers attenuate hypoxia- and ischemia-induced neuronal death in vitro and in vivo. Stroke 34: 1281–1286

    Google Scholar 

  • Weih M, Bergk A, Isaev NK, Ruscher K, Megow D, Riepe M, Meisel A, Victorov IV, Dirnagi U (1999) Induction of ischemic tolerance in rat cortical neurons by 3-nitropropionic acid: chemical preconditioning. Neurosci Lett 272:207–210

    Google Scholar 

  • Xu G-P, Dave KR, Vivero R, Schmidt-Kastner R, Sick TJ, Perez-Pinzon MA (2002) Improvement in neuronal survival after ischemic preconditioning in hippocampal slice cultures. Brain Res 952:153–158

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Xia X, Zhang Y, Wang Q, Li L, Luo G, Xia Y (2009) δ-Opioid receptor activation attenuates oxidative injury in the ischemic rat brain. BMC Biol 7:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Gibney GT, Zhao P, Xia Y (2002) Neuroprotective role of delta-opioid receptors in cortical neurons. Am J Physiol Cell Physiol 282:C1225–C1234

    Article  PubMed  CAS  Google Scholar 

  • Zhao P, Huang Y, Zuo Z (2006) Opioid preconditioning induces opioid receptor-dependent delayed neuroprotection against ischemia in rats. J Neuropathol Exp Neurol 65:945–952

    Article  PubMed  CAS  Google Scholar 

  • Zhu M, Li M-W, Tian X-S, Ou X-M, Zhu C-Q, Guo J-C (2009) Neuroprotective role of delta-opioid receptors against mitochondrial respiratory chain injury. Brain Res 1252:183–191

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the National Institutes of Health, American Heart Association-Mid-Atlantic Affiliate and International Anesthesia Research Society for the grants supporting research in Dr. Zhiyi Zuo’s laboratory. The support of the Department of Anesthesiology, University of Virginia, is also greatly appreciated.

Author information

Authors and Affiliations

  1. Department of Anesthesiology, University of Virginia, Charlottesville, VA, 22903, USA

    Jason Eli Maas M.D., Ph.D. & Zhiyi Zuo M.D., Ph.D.

Authors
  1. Jason Eli Maas M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhiyi Zuo M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jason Eli Maas M.D., Ph.D. .

Editor information

Editors and Affiliations

  1. Univ of Texas Med Schl, Houston, Texas, USA

    Ying Xia

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Maas, J.E., Zuo, Z. (2015). Delta Opioid Receptor in Cerebral Preconditioning. In: Xia, Y. (eds) Neural Functions of the Delta-Opioid Receptor. Springer, Cham. https://doi.org/10.1007/978-3-319-25495-1_12

Download citation

Publish with us

Policies and ethics

Search

Navigation