Skip to main content

Advertisement

SpringerLink
Log in

Chronic SIV and morphine treatment increases heat shock protein 5 expression at the synapse

  • Short Communication
  • Published:
Journal of NeuroVirology Aims and scope Submit manuscript

Abstract

The abuse of opiates such as morphine in synergy with HIV infection accelerates neurocognitive impairments and neuropathology in the CNS of HIV-infected subjects, collectively referred to as HAND. To identify potential pathogenic markers associated with HIV and morphine in perturbing the synaptic architecture, we performed quantitative mass spectrometry proteomics on purified synaptosomes isolated from the caudate of two groups of rhesus macaques chronically infected with SIV differing by one regimen—morphine treatment. The upregulation of heat shock 70-kDa protein 5 in the SIV + morphine group points to increased cellular stress during SIV/morphine interaction thus leading to CNS dysfunction.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Ammon S, Mayer P, Riechert U, Tischmeyer H, Hollt V (2003) Microarray analysis of genes expressed in the frontal cortex of rats chronically treated with morphine and after naloxone precipitated withdrawal. Brain Res Mol Brain Res 112:113–125

    Article  CAS  PubMed  Google Scholar 

  • Anthony IC, Arango JC, Stephens B, Simmonds P, Bell JE (2008) The effects of illicit drugs on the HIV infected brain. Front Biosci 13:1294–1307

    Article  CAS  PubMed  Google Scholar 

  • Bell JE, Donaldson YK, Lowrie S, McKenzie CA, Elton RA, Chiswick A, Brettle RP, Ironside JW, Simmonds P (1996) Influence of risk group and zidovudine therapy on the development of HIV encephalitis and cognitive impairment in AIDS patients. AIDS 10:493–499

    Article  CAS  PubMed  Google Scholar 

  • Bell JE, Brettle RP, Chiswick A, Simmonds P (1998) HIV encephalitis, proviral load and dementia in drug users and homosexuals with AIDS. Effect of neocortical involvement. Brain 121(Pt 11):2043–2052

    Article  PubMed  Google Scholar 

  • Bell JE, Arango JC, Anthony IC (2006) Neurobiology of multiple insults: HIV-1-associated brain disorders in those who use illicit drugs. J Neuroimmune Pharmacol 1:182–191

    Article  PubMed  Google Scholar 

  • Bokhari SM, Hegde R, Callen S, Yao H, Adany I, Li Q, Li Z, Pinson D, Yeh HW, Cheney PD, Buch S (2011) Morphine potentiates neuropathogenesis of SIV infection in rhesus macaques. J Neuroimmune Pharmacol 6:626–639

    Article  PubMed Central  PubMed  Google Scholar 

  • Bruce-Keller AJ, Turchan-Cholewo J, Smart EJ, Geurin T, Chauhan A, Reid R, Xu R, Nath A, Knapp PE, Hauser KF (2008) Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 Tat transgenic mice. Glia 56:1414–1427

    Article  PubMed Central  PubMed  Google Scholar 

  • Buch SK, Khurdayan VK, Lutz SE, Knapp PE, El-Hage N, Hauser KF (2007) Glial-restricted precursors: patterns of expression of opioid receptors and relationship to human immunodeficiency virus-1 Tat and morphine susceptibility in vitro. Neuroscience 146:1546–1554

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chiesi A, Vella S, Dally LG, Pedersen C, Danner S, Johnson AM, Schwander S, Goebel FD, Glauser M, Antunes F et al (1996) Epidemiology of AIDS dementia complex in Europe. AIDS in Europe Study Group. J Acquir Immune Defic Syndr Hum Retrovirol 11:39–44

    Article  CAS  PubMed  Google Scholar 

  • Costa BM, Yao H, Yang L, Buch S (2013) Role of endoplasmic reticulum (ER) stress in cocaine-induced microglial cell death. J Neuroimmune Pharmacol 8:705–714

    Article  PubMed Central  PubMed  Google Scholar 

  • Crews L, Patrick C, Achim CL, Everall IP, Masliah E (2009) Molecular pathology of neuro-AIDS (CNS-HIV). Int J Mol Sci 10:1045–1063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goodkin K, Shapshak P, Metsch LR, McCoy CB, Crandall KA, Kumar M, Fujimura RK, McCoy V, Zhang BT, Reyblat S, Xin KQ, Kumar AM (1998) Cocaine abuse and HIV-1 infection: epidemiology and neuropathogenesis. J Neuroimmunol 83:88–101

    Article  CAS  PubMed  Google Scholar 

  • Gurwell JA, Nath A, Sun Q, Zhang J, Martin KM, Chen Y, Hauser KF (2001) Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 Tat protein in striatal neurons in vitro. Neuroscience 102:555–563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hauser KF, Hahn YK, Adjan VV, Zou S, Buch SK, Nath A, Bruce-Keller AJ, Knapp PE (2009) HIV-1 Tat and morphine have interactive effects on oligodendrocyte survival and morphology. Glia 57:194–206

    Article  PubMed Central  PubMed  Google Scholar 

  • Hauser KF, Fitting S, Dever SM, Podhaizer EM, Knapp PE (2012) Opiate drug use and the pathophysiology of neuroAIDS. Curr HIV Res 10:435–452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hellmuth J, Milanini B, Valcour V (2014) Interactions between ageing and NeuroAIDS. Curr Opin HIV AIDS 9:527–532

    Article  CAS  PubMed  Google Scholar 

  • Hollenbach R, Sagar D, Khan ZK, Callen S, Yao H, Shirazi J, Buch S, Jain P (2014) Effect of morphine and SIV on dendritic cell trafficking into the central nervous system of rhesus macaques. J Neurovirol 20:175–183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jayanthi S, Deng X, Noailles PA, Ladenheim B, Cadet JL (2004) Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB J 18:238–251

    Article  CAS  PubMed  Google Scholar 

  • Khurdayan VK, Buch S, El-Hage N, Lutz SE, Goebel SM, Singh IN, Knapp PE, Turchan-Cholewo J, Nath A, Hauser KF (2004) Preferential vulnerability of astroglia and glial precursors to combined opioid and HIV-1 Tat exposure in vitro. Eur J Neurosci 19:3171–3182

    Article  PubMed Central  PubMed  Google Scholar 

  • Kumar R, Torres C, Yamamura Y, Rodriguez I, Martinez M, Staprans S, Donahoe RM, Kraiselburd E, Stephens EB, Kumar A (2004) Modulation by morphine of viral set point in rhesus macaques infected with simian immunodeficiency virus and simian-human immunodeficiency virus. J Virol 78:11425–11428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma R, Yang L, Niu F, Buch S (2014) HIV Tat-mediated induction of human brain microvascular endothelial cell apoptosis involves endoplasmic reticulum stress and mitochondrial dysfunction. Mol Neurobiol

  • Nath A, Maragos WF, Avison MJ, Schmitt FA, Berger JR (2001) Acceleration of HIV dementia with methamphetamine and cocaine. J Neurovirol 7:66–71

    Article  CAS  PubMed  Google Scholar 

  • Pendyala G, Buescher JL, Fox HS (2012a) Methamphetamine and inflammatory cytokines increase neuronal Na+/K+−ATPase isoform 3: relevance for HIV associated neurocognitive disorders. PLoS One 7, e37604

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pendyala G, Ninemire C, Fox HS (2012b) Protective role for the disulfide isomerase PDIA3 in methamphetamine neurotoxicity. PLoS One 7, e38909

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pendyala G, Buescher JL, Fox HS (2014) Isolation of synaptosomes from archived brain tissues. In: Xiong HGH (ed) Current laboratory methods in neuroscience research. Springer, New York, pp 145–152

    Chapter  Google Scholar 

  • Perez-Casanova A, Husain K, Noel RJ Jr, Rivera-Amill V, Kumar A (2008) Interaction of SIV/SHIV infection and morphine on plasma oxidant/antioxidant balance in macaque. Mol Cell Biochem 308:169–175

    Article  CAS  PubMed  Google Scholar 

  • Raghavan R, Cheney PD, Raymond LA, Joag SV, Stephens EB, Adany I, Pinson DM, Li Z, Marcario JK, Jia F, Wang C, Foresman L, Berman NE, Narayan O (1999) Morphological correlates of neurological dysfunction in macaques infected with neurovirulent simian immunodeficiency virus. Neuropathol Appl Neurobiol 25:285–294

    Article  CAS  PubMed  Google Scholar 

  • Reddy PV, Pilakka-Kanthikeel S, Saxena SK, Saiyed Z, Nair MP (2012) Interactive effects of morphine on HIV infection: role in HIV-associated neurocognitive disorder. AIDS Res Treat 2012:953678

    PubMed Central  PubMed  Google Scholar 

  • Shapshak P, Kangueane P, Fujimura RK, Commins D, Chiappelli F, Singer E, Levine AJ, Minagar A, Novembre FJ, Somboonwit C, Nath A, Sinnott JT (2011) Editorial neuroAIDS review. AIDS 25:123–141

    Article  PubMed Central  PubMed  Google Scholar 

  • Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 6:1638–1655

    Article  CAS  PubMed  Google Scholar 

  • Tagawa Y, Hiramatsu N, Kasai A, Hayakawa K, Okamura M, Yao J, Kitamura M (2008) Induction of apoptosis by cigarette smoke via ROS-dependent endoplasmic reticulum stress and CCAAT/enhancer-binding protein-homologous protein (CHOP). Free Radic Biol Med 45:50–59

    Article  CAS  PubMed  Google Scholar 

  • Thomas M, George NI, Saini UT, Patterson TA, Hanig JP, Bowyer JF (2010) Endoplasmic reticulum stress responses differ in meninges and associated vasculature, striatum, and parietal cortex after a neurotoxic amphetamine exposure. Synapse 64:579–593

    Article  CAS  PubMed  Google Scholar 

  • Trusina A, Papa FR, Tang C (2008) Rationalizing translation attenuation in the network architecture of the unfolded protein response. Proc Natl Acad Sci U S A 105:20280–20285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Turchan-Cholewo J, Dimayuga FO, Ding Q, Keller JN, Hauser KF, Knapp PE, Bruce-Keller AJ (2008) Cell-specific actions of HIV-Tat and morphine on opioid receptor expression in glia. J Neurosci Res 86:2100–2110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Turchan-Cholewo J, Dimayuga FO, Gupta S, Keller JN, Knapp PE, Hauser KF, Bruce-Keller AJ (2009) Morphine and HIV-Tat increase microglial-free radical production and oxidative stress: possible role in cytokine regulation. J Neurochem 108:202–215

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tyor WR, Hwang HY, Fritz-French C (2012) Morphine exposure during HIV encephalitis in SCID mice. Neurochem Res 37:2836–2841

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu L, Han F, Mandal A, Rao GN, Zhang X (2010) Diazoxide attenuates hypothermic preservation-induced renal injury via down-regulation of CHOP and caspase-12. Nephrol Dial Transplant 25:3859–3867

    Article  CAS  PubMed  Google Scholar 

  • Yao H, Duan M, Hu G, Buch S (2011) Platelet-derived growth factor B chain is a novel target gene of cocaine-mediated Notch1 signaling: implications for HIV-associated neurological disorders. J Neurosci 31:12449–12454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. LeeAnn Higgins of the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance in data acquisition. Funding for this study was supported by grants DA020392, DA023397, and DA024442 to SJB from the National Institutes of Health.

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Department of Anesthesiology, University of Nebraska Medical Center, Omaha, NE, USA

    Gurudutt Pendyala & Steven J. Lisco

  2. Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, 985880 Nebraska Medical Center, Omaha, NE, 68198, USA

    Gurudutt Pendyala, Palsamy Periyasamy, Shannon Callen, Howard S. Fox & Shilpa J. Buch

Authors
  1. Gurudutt Pendyala
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Palsamy Periyasamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shannon Callen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Howard S. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steven J. Lisco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shilpa J. Buch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shilpa J. Buch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Complete list of synaptic proteins identified between the two groups of monkeys. Unpaired Student’s t test was used to determine the significance. (XLS 438 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pendyala, G., Periyasamy, P., Callen, S. et al. Chronic SIV and morphine treatment increases heat shock protein 5 expression at the synapse. J. Neurovirol. 21, 592–598 (2015). https://doi.org/10.1007/s13365-015-0356-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13365-015-0356-9

Keywords

Search

Navigation