Advertisement

Neurochemical Research

, Volume 40, Issue 4, pp 864–872 | Cite as

Comparison of Immunoreactivities of Calbindin-D28k, Calretinin and Parvalbumin in the Striatum Between Young, Adult and Aged Mice, Rats and Gerbils

  • Eun Joo Bae
  • Bai Hui Chen
  • Bich Na Shin
  • Jeong Hwi Cho
  • In Hye Kim
  • Joon Ha Park
  • Jae Chul Lee
  • Hyun Jin Tae
  • Soo Young Choi
  • Jong-Dai Kim
  • Yun Lyul Lee
  • Moo-Ho WonEmail author
  • Ji Hyeon AhnEmail author
Original Paper

Abstract

Calcium binding proteins play important roles in all aspects of neural functioning in the central nervous system. In the present study, we examined age-related changes of three different calcium binding proteins calbindin-D28k (CB), calretinin (CR) and parvalbumin (PV) immunoreactivities in the striatum of young (1 month), adult (6 months) and aged (24 months) ages in three species of rodents (mouse, rat and gerbil) using immunohistochemistry and Western blotting. Our results show that the number of CB-immunoreactive neurons was highest in the adult mouse and rat; however, in the gerbil, the number of CB-immunoreactive neurons was not significantly different from each group although the CB immunoreactivity was significantly decreased in the aged group compared with the adult group. The number of CR-immunoreactive neurons in the striatum was significantly highest in all the adult groups, and, especially, the number of CR-immunoreactive neurons and CR immunoreactivity in the aged gerbil were significantly decreased in the aged group compared with the other groups. Finally, we did not found any significant difference in the number of PV-immunoreactive neurons in the striatum with age among the three rodents. On the other hand, we found that protein levels of three calcium binding proteins in all the mouse groups were similar to the immunohistochemical data. These results indicate that the distribution pattern of calcium binding proteins is different according to age; the adult might show an apparent tendency of high expression in the striatum.

Keywords

Striatum Rodents Calbindin-D28k Calretinin Parvalbumin Immunohistochemistry Western blotting 

Notes

Acknowledgments

The authors would like to thank Mr. Seung Uk Lee for his technical help in this study. This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2010-0010580), and by a Priority Research Centers Program Grant (NRF-2009-0093812) through the National Research Foundation of Korea funded by the Ministry of Science, ICT and Future Planning.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Ba M, Kong M, Yang H et al (2006) Changes in subcellular distribution and phosphorylation of GluR1 in lesioned striatum of 6-hydroxydopamine-lesioned and l-dopa-treated rats. Neurochem Res 31:1337–1347CrossRefPubMedGoogle Scholar
  2. 2.
    Bernacer J, Prensa L, Giménez-Amaya JM (2012) Distribution of GABAergic interneurons and dopaminergic cells in the functional territories of the human striatum. PLoS ONE 7:e30504CrossRefPubMedCentralPubMedGoogle Scholar
  3. 3.
    Liu XM, Shu SY, Zeng CC et al (2011) The role of substance P in the marginal division of the neostriatum in learning and memory is mediated through the neurokinin 1 receptor in rats. Neurochem Res 36:1896–1902CrossRefPubMedGoogle Scholar
  4. 4.
    Marazziti D, Baroni S, Pirone A et al (2012) Distribution of serotonin receptor of type 6 (5-HT(6)) in human brain post-mortem. A pharmacology, autoradiography and immunohistochemistry study. Neurochem Res 37:920–927CrossRefPubMedGoogle Scholar
  5. 5.
    Graveland GA, DiFiglia M (1985) The frequency and distribution of medium-sized neurons with indented nuclei in the primate and rodent neostriatum. Brain Res 327:307–311CrossRefPubMedGoogle Scholar
  6. 6.
    Kawaguchi Y, Wilson CJ, Augood SJ et al (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527–535CrossRefPubMedGoogle Scholar
  7. 7.
    Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308CrossRefPubMedGoogle Scholar
  8. 8.
    Young SZ, Lafourcade CA, Platel JC et al (2014) GABAergic striatal neurons project dendrites and axons into the postnatal subventricular zone leading to calcium activity. Front Cell Neurosci 8:10CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325–337CrossRefPubMedGoogle Scholar
  10. 10.
    Rintoul G, Raymond L, Baimbridge K (2001) Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium 29:277–287CrossRefPubMedGoogle Scholar
  11. 11.
    Yuan HH, Chen RJ, Zhu YH et al (2013) The neuroprotective effect of overexpression of calbindin-D(28k) in an animal model of Parkinson’s disease. Mol Neurobiol 47:117–122CrossRefPubMedGoogle Scholar
  12. 12.
    Yenari MA, Minami M, Sun GH et al (2001) Calbindin d28k overexpression protects striatal neurons from transient focal cerebral ischemia. Stroke 32:1028–1035CrossRefPubMedGoogle Scholar
  13. 13.
    Hontanilla B, Parent A, Heras S et al (1998) Distribution of calbindin D-28k and parvalbumin neurons and fibers in the rat basal ganglia. Brain Res Bull 47:107–116CrossRefPubMedGoogle Scholar
  14. 14.
    Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923PubMedGoogle Scholar
  15. 15.
    Litwinowicz B, Labuda C, Kowiański P et al (2003) Developmental pattern of calbindin D28k protein expression in the rat striatum and cerebral cortex. Folia Morphol 62:327–329Google Scholar
  16. 16.
    Gerfen CR, Baimbridge KG, Miller JJ (1985) The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci USA 82:8780–8784CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Oh MM, Oliveira FA, Waters J et al (2013) Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons. J Neurosci 33:7905–7911CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    Vanhooren V, Libert C (2013) The mouse as a model organism in aging research: usefulness, pitfalls and possibilities. Ageing Res Rev 12:8–21CrossRefPubMedGoogle Scholar
  19. 19.
    Demetrius L (2006) Aging in mouse and human systems. Ann N Y Acad Sci 1067:66–82CrossRefPubMedGoogle Scholar
  20. 20.
    Gorbunova V, Bozzella MJ, Seluanov A (2008) Rodents for comparative aging studies: from mice to beavers. Age 30:111–119CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Quinn R (2005) Comparing rat’s to human’s age: how old is my rat in people years? Nutrition 21:775–777CrossRefPubMedGoogle Scholar
  22. 22.
    Lee CH, Ahn JH, Park JH et al (2014) Decreased insulin-like growth factor-I and its receptor expression in the hippocampus and somatosensory cortex of the aged mouse. Neurochem Res 39:770–776CrossRefPubMedGoogle Scholar
  23. 23.
    Ohk TG, Yoo KY, Park SM et al (2012) Neuronal damage using fluoro-jade B histofluorescence and gliosis in the striatum after various durations of transient cerebral ischemia in gerbils. Neurochem Res 37:826–834CrossRefPubMedGoogle Scholar
  24. 24.
    Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60:543–554CrossRefPubMedCentralPubMedGoogle Scholar
  25. 25.
    Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14:685–692CrossRefPubMedGoogle Scholar
  26. 26.
    Kishimoto J, Tsuchiya T, Cox H et al (1998) Age-related changes of calbindin-D28k, calretinin, and parvalbumin mRNAs in the hamster brain. Neurobiol Aging 19:77–82CrossRefPubMedGoogle Scholar
  27. 27.
    Shetty AK, Turner DA (1998) Hippocampal interneurons expressing glutamic acid decarboxylase and calcium-binding proteins decrease with aging in Fischer 344 rats. J Comp Neurol 394:252–269CrossRefPubMedGoogle Scholar
  28. 28.
    Lee CH, Hwang IK, Yoo KY et al (2009) Calbindin d-28k immunoreactivity and its protein level in hippocampal subregions during normal aging in gerbils. Cell Mol Neurobiol 29:665–672CrossRefPubMedGoogle Scholar
  29. 29.
    Bu J, Sathyendra V, Nagykery N et al (2003) Age-related changes in calbindin-D28k calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol 182:220–231CrossRefPubMedGoogle Scholar
  30. 30.
    Villa A, Podini P, Panzeri MC et al (1994) Cytosolic Ca2+ binding proteins during rat brain ageing: loss of calbindin and calretinin in the hippocampus, with no change in the cerebellum. Eur J Neurosci 6:1491–1499CrossRefPubMedGoogle Scholar
  31. 31.
    Lee CH, Hwang IK, Choi JH et al (2010) Age-dependent changes in calretinin immunoreactivity and its protein level in the gerbil hippocampus. Neurochem Res 35:122–129CrossRefPubMedGoogle Scholar
  32. 32.
    Grillner S, Hellgren J, Menard A et al (2005) Mechanisms for selection of basic motor programs—roles for the striatum and pallidum. Trends Neurosci 28:364–370CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Eun Joo Bae
    • 1
  • Bai Hui Chen
    • 2
  • Bich Na Shin
    • 2
  • Jeong Hwi Cho
    • 3
  • In Hye Kim
    • 3
  • Joon Ha Park
    • 3
  • Jae Chul Lee
    • 3
  • Hyun Jin Tae
    • 4
  • Soo Young Choi
    • 4
  • Jong-Dai Kim
    • 5
  • Yun Lyul Lee
    • 2
  • Moo-Ho Won
    • 3
    Email author
  • Ji Hyeon Ahn
    • 3
    Email author
  1. 1.Department of Pediatrics, Chuncheon Sacred Heart Hospital, College of MedicineHallym UniversityChuncheonSouth Korea
  2. 2.Department of Physiology, Institute of Neurodegeneration and Neuroregeneration, College of MedicineHallym UniversityChuncheonSouth Korea
  3. 3.Department of Neurobiology, School of MedicineKangwon National UniversityChuncheonSouth Korea
  4. 4.Department of Biomedical Science, Research Institute for Bioscience and BiotechnologyHallym UniversityChuncheonSouth Korea
  5. 5.Division of Food Biotechnology, School of BiotechnologyKangwon National UniversityChuncheonSouth Korea

Personalised recommendations