Skip to main content

Advertisement

Log in

Methamphetamine-Induced Toxicity in Indusium Griseum of Mice is Associated with Astro- and Microgliosis

  • Short Report/Rapid Communication
  • Published:
Neurotoxicity Research Aims and scope Submit manuscript

Abstract

The indusium griseum (IG), a thin layer of gray matter in contact with the dorsal surface of the corpus callosum and the lateral gray matter of the cingulate gyrus, has a common origin with hippocampus and shows similar organization with the dentate gyrus. Although some studies have examined the effect of methamphetamine (METH), an addictive and an illegal psychostimulant on this structure, quantitative effects and possible mechanism of actions of METH in this area are lacking. By applying two different protocols of equivalent METH administration (i.e., a high dose of 1 × 30 mg/kg and a lower and repeated injection dose of 3 × 10 mg/kg) and using a specific silver staining method in mice, we demonstrate that this drug produces degeneration in IG with both protocols, without affecting the dopaminergic system. Moreover, we observed quantitative increases in labeling of GFAP and Iba-1, markers of astro- and microgliosis, respectively, which suggest astrogliosis and microgliosis. Thus, our study provides morphological and semi-quantitative evidence that METH induces neurodegeneration in IG and that this damage is associated with astrogliosis and microgliosis in this area.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Adamek GD, Shipley MT, Sanders MS (1984) The indusium griseum in the mouse: architecture, Timm’s histochemistry and some afferent connections. Brain Res Bull 12(6):657–668

    Article  CAS  PubMed  Google Scholar 

  • Ali SF, Newport GD, Holson RR, Slikker W Jr, Bowyer JF (1994) Low environmental temperatures or pharmacologic agents that produce hypothermia decrease methamphetamine neurotoxicity in mice. Brain Res 658:33–38

    Article  CAS  PubMed  Google Scholar 

  • Ares-Santos S, Granado N, Oliva I, O’Shea E, Martin ED, Colado MI, Moratalla R (2012) Dopamine D(1) receptor deletion strongly reduces neurotoxic effects of methamphetamine. Neurobiol Dis 45(2):810–820

    Article  CAS  PubMed  Google Scholar 

  • Ares-Santos S, Granado N, Espadas I, Martinez-Murillo R, Moratalla R (2014) Methamphetamine causes degeneration of dopamine cell bodies and terminals of the nigrostriatal pathway evidenced by silver staining. Neuropsychopharmacology 39(5):1066–1080

    Article  CAS  PubMed  Google Scholar 

  • Cadet JL, Jayanthi S, Deng X (2005) Methamphetamine-induced neuronal apoptosis involves the activation of multiple death pathways. Neurotox Res 8:199–206

    Article  CAS  PubMed  Google Scholar 

  • de Olmos JS, Beltramino CA, de Olmos de Lorenzo S (1994) Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicol Teratol 16:545–561

    Article  PubMed  Google Scholar 

  • Deng X, Wang Y, Chou J, Cadet JL (2001) Methamphetamine causes widespread apoptosis in the mouse brain: evidence from using an improved TUNEL histochemical method. Mole Brain Res 93:64–69

    Article  CAS  Google Scholar 

  • Deng X, Ladenheim B, Jayanthi S, Cadet JL (2007) Methamphetamine administration causes death of dopaminergic neurons in the mouse olfactory bulb. Biol Psychiatry 61(11):1235–1243

    Article  CAS  PubMed  Google Scholar 

  • Granado N, Escobedo I, O’Shea E, Colado I, Moratalla R (2008) Early loss of dopaminergic terminals in striosomes after MDMA administration to mice. Synapse 62:80–84

    Article  CAS  PubMed  Google Scholar 

  • Granado N, Ares-Santos S, O’Shea E, Vicario-Abejón C, Colado MI, Moratalla R (2010) Selective vulnerability in striosomes and in the nigrostriatal dopaminergic pathway after methamphetamine administration : early loss of TH in striosomes after methamphetamine. Neurotox Res 18(1):48–58

    Article  PubMed Central  PubMed  Google Scholar 

  • Granado N, Ares-Santos S, Oliva I, O’Shea E, Martin ED, Colado MI, Moratalla R (2011a) Dopamine D2-receptor knockout mice are protected against dopaminergic neurotoxicity induced by methamphetamine or MDMA. Neurobiol Dis 42(3):391–403

    Article  CAS  PubMed  Google Scholar 

  • Granado N, Lastres-Becker I, Ares-Santos S, Oliva I, Martin E, Cuadrado A, Moratalla R (2011b) Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum. Glia 59(12):1850–1863

    Article  PubMed  Google Scholar 

  • Grant G, Holländer H, Aldskogius H (2004) Suppressive silver methods—a tool for identifying axotomy-induced neuron degeneration. Brain Res Bull 62(4):261–269

    Article  CAS  PubMed  Google Scholar 

  • Kelly KA, Miller DB, Bowyer JF, O’Callaghan JP (2012) Chronic exposure to corticosterone enhances the neuroinflammatory and neurotoxic responses to methamphetamine. J Neurochem 122(5):995–1009

    Article  CAS  PubMed  Google Scholar 

  • Krasnova IN, Cadet JL (2009) Methamphetamine toxicity and messengers of death. Brain Res Rev 60(2):379–407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laplante F, Mnie-Filali O, Sullivan RM (2013) A neuroanatomical and neurochemical study of the indusium griseum and anterior hippocampal continuation: comparison with dentate gyrus. J Chem Neuroanat 50–51:39–47

    Article  PubMed  Google Scholar 

  • Mahoney JJ, Jackson BJ, Kalechstein AD, De La Garza R, Newton TF (2011) Acute, low-dose methamphetamine administration improves attention/information processing speed and working memory in methamphetamine-dependent individuals displaying poorer cognitive performance at baseline. Prog Neuropsychopharmacol Biol Psychiatry 35(2):459–465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsumoto RR, Seminerio MJ, Turner RC, Robson MJ, Nguyen L, Miller DB, O’Callaghan JP (2014) Methamphetamine-induced toxicity: an updated review on issues related to hyperthermia. Pharmacol Ther 144(1):28–40

    Article  CAS  PubMed  Google Scholar 

  • Nakada T (1999) High-field, high-resolution MR imaging of the human indusium griseum. AJNR Am J Neuroradiol 20(3):524–525

    CAS  PubMed  Google Scholar 

  • O’Callaghan JP, Miller DB (1994) Neurotoxicity profiles of substituted amphetamines in the C57BL/6 J mouse. J Pharmacol Exp Ther 270(2):741–751

    PubMed  Google Scholar 

  • O’Callaghan JP, Kelly KA, VanGilder RL, Sofroniew MV, Miller DB (2014) Early activation of STAT3 regulates reactive astrogliosis induced by diverse forms of neurotoxicity. PLoS ONE 9(7):e102003

    Article  PubMed Central  PubMed  Google Scholar 

  • Ortiz O, Delgado-Garcı´a JM, Espadas I, Bahı´ A, Trullas R, Dreyer JL et al (2010) Associative learning and CA3-CA1 synaptic plasticity are impaired in D1R null, Drd1a −/− mice and in hippocampal siRNA silenced Drd1a mice. J Neurosci 30:12288–12300

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • Recinto P, Samant AR, Chavez G, Kim A, Yuan CJ, Soleiman M, Grant Y, Edwards S, Wee S, Koob GF, George O, Mandyam CD (2012) Levels of neural progenitors in the hippocampus predict memory impairment and relapse to drug seeking as a function of excessive methamphetamine self-administration. Neuropsychopharmacology 37(5):1275–1287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu JK, Cho T, Wang YT, McLarnon JG (2009) Neural progenitor cells attenuate inflammatory reactivity and neuronal loss in an animal model of inflamed AD brain. J Neuroinflammation 23(6):39

    Article  Google Scholar 

  • Schmued LC, Bowyer JF (1997) Methamphetamine exposure can produce neuronal degeneration in mouse hippocampal remnants. Brain Res 759(1):135–140

    Article  CAS  PubMed  Google Scholar 

  • Scott JC, Woods SP, Matt GE, Meyer RA, Heaton RK, Atkinson JH, Grant I (2007) Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychol Rev 17(3):275–297

    Article  PubMed  Google Scholar 

  • Shipley MT, Ennis M, Puche AC (2004) Olfactory system. In: Paxinos G (ed) The rat nervous system. Elsevier Academic Press, San Diego, pp 923–964

    Google Scholar 

  • Simões PF, Silva AP, Pereira FC, Marques E, Grade S, Milhazes N, Borges F, Ribeiro CF, Macedo TR (2007) Methamphetamine induces alterations on hippocampal NMDA and AMPA receptor subunit levels and impairs spatial working memory. Neuroscience 150(2):433–441

    Article  PubMed  Google Scholar 

  • Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35

    Article  PubMed Central  PubMed  Google Scholar 

  • Sonsalla PK, Nicklas WJ, Heikkila RE (1989) Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity. Science 243:398–400

    Article  CAS  PubMed  Google Scholar 

  • Sriram K, Miller DB, O’Callaghan JP (2006) Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem 96(3):706–718

    Article  CAS  PubMed  Google Scholar 

  • Switzer RC (2000) Application of silver degeneration stains for neurotoxicity testing. Toxicol Pathol 28:70–83

    Article  CAS  PubMed  Google Scholar 

  • UNODC (2013) World Drug Report 2013 (United Nations publication, Sales No. E.13.XI.6). http://www.unodc.org/unodc/secured/wdr/wdr2013/World_Drug_Report_2013.pdf

  • Woods SP, Rippeth JD, Conover E, Gongvatana A, Gonzalez R, Carey CL, Cherner M, Heaton RK, Grant I, HIV Neurobehavioral Research Center Group (2005) Deficient strategic control of verbal encoding and retrieval in individuals with methamphetamine dependence. Neuropsychology 19(1):35–43

    Article  PubMed  Google Scholar 

  • Wyss JM, Sripanidkulchai K (1983) The indusium griseum and anterior hippocampal continuation in the rat. J Comp Neurol 219:251–272

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Spanish Ministerios de Economía y Competitividad and Sanidad Política Social e Igualdad, Instituto de Salud Carlos III Grant No. SAF2013-48532, Plan Nacional Sobre Drogas No. 2012/071, Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas Ref. No. CB06/05/0055, and Comunidad de Madrid Ref. No. S2011/BMD-2336 to RM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosario Moratalla.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carmena, A., Granado, N., Ares-Santos, S. et al. Methamphetamine-Induced Toxicity in Indusium Griseum of Mice is Associated with Astro- and Microgliosis. Neurotox Res 27, 209–216 (2015). https://doi.org/10.1007/s12640-014-9505-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12640-014-9505-9

Keywords

Navigation