Immunoreactivities of calbindin‑D28k, calretinin and parvalbumin in the somatosensory cortex of rodents during normal aging

Ahn,Ji  Hyeon; Hong,Seongkweon; Park,Joon  Ha; Kim,In  Hye; Cho,Jeong  Hwi; Lee,Tae‑Kyeong; Lee,Jae‑Chul; Chen,Bai  Hui; Shin,Bich‑Na; Bae,Eun  Joo; Jeon,Yong  Hwan; Kim,Young‑Myeong; Won,Moo‑Ho; Choi,Soo  Young

doi:10.3892/mmr.2017.7573

Immunoreactivities of calbindin‑D28k, calretinin and parvalbumin in the somatosensory cortex of rodents during normal aging

Authors:
- Ji Hyeon Ahn
- Seongkweon Hong
- Joon Ha Park
- In Hye Kim
- Jeong Hwi Cho
- Tae‑Kyeong Lee
- Jae‑Chul Lee
- Bai Hui Chen
- Bich‑Na Shin
- Eun Joo Bae
- Yong Hwan Jeon
- Young‑Myeong Kim
- Moo‑Ho Won
- Soo Young Choi
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Affiliations: Department of Biomedical Science and Research Institute for Bioscience and Biotechnology, Hallym University, Chuncheon, Gangwon 24252, Republic of Korea, Department of Surgery, School of Medicine, Kangwon National University, Chuncheon, Gangwon 24341, Republic of Korea, Department of Neurobiology, School of Medicine, Kangwon National University, Chuncheon, Gangwon 24341, Republic of Korea, Department of Histology and Embryology, Institute of Neuroscience, Wenzhou Medical University, Wenzhou, Zhejiang 325035, P.R. China, Department of Physiology, College of Medicine, Hallym University, Chuncheon, Gangwon 24252, Republic of Korea, Department of Pediatrics, Chuncheon Sacred Heart Hospital, College of Medicine, Hallym University, Chuncheon, Gangwon 24253, Republic of Korea, Department of Radiology, School of Medicine, Kangwon National University, Chuncheon, Gangwon 24289, Republic of Korea, Department of Molecular and Cellular Biochemistry, School of Medicine, Kangwon National University, Chuncheon, Gangwon 24341, Republic of Korea
Published online on: September 21, 2017 https://doi.org/10.3892/mmr.2017.7573
Pages: 7191-7198
Copyright: © Ahn et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Calbindin‑D28k (CB), calretinin (CR) and parvalbumin (PV), which regulate cytosolic free Ca2+ concentrations in neurons, are chemically expressed in γ‑aminobutyric acid (GABA)ergic neurons that regulate the degree of glutamatergic excitation and output of projection neurons. The present study investigated age‑associated differences in CB, CR and PV immunoreactivities in the somatosensory cortex in three species (mice, rats and gerbils) of young (1 month), adult (6 months) and aged (24 months) rodents, using immunohistochemistry and western blotting. Abundant CB‑immunoreactive neurons were distributed in layers II and III, and age‑associated alterations in their number were different according to the species. CR‑immunoreactive neurons were not abundant in all layers; however, the number of CR‑immunoreactive neurons was the highest in all adult species. Many PV‑immunoreactive neurons were identified in all layers, particularly in layers II and III, and they increased in all layers with age in all species. The present study demonstrated that the distribution pattern of CB‑, CR‑ and PV‑containing neurons in the somatosensory cortex were apparently altered in number with normal aging, and that CB and CR exhibited a tendency to decrease in aged rodents, whereas PV tended to increase with age. These results indicate that CB, CR and PV are markedly altered in the somatosensory cortex, and this change may be associated with normal aging. These findings may aid the elucidation of the mechanisms of aging and geriatric disease.

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1	Aronoff R and Petersen CC: Layer, column and cell-type specific genetic manipulation in mouse barrel cortex. Front Neurosci. 2:64–71. 2008. View Article : Google Scholar : PubMed/NCBI
2	DeFelipe J and Fariñas I: The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol. 39:563–607. 1992. View Article : Google Scholar : PubMed/NCBI
3	Kawaguchi Y and Kubota Y: GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex. 7:476–486. 1997. View Article : Google Scholar : PubMed/NCBI
4	Hioki H: Compartmental organization of synaptic inputs to parvalbumin-expressing GABAergic neurons in mouse primary somatosensory cortex. Anat Sci Int. 90:7–21. 2015. View Article : Google Scholar : PubMed/NCBI
5	Lehmann K, Steinecke A and Bolz J: GABA through the ages: Regulation of cortical function and plasticity by inhibitory interneurons. Neural Plast. 2012:8927842012. View Article : Google Scholar : PubMed/NCBI
6	Kawaguchi Y, Wilson CJ, Augood SJ and Emson PC: Striatal interneurones: Chemical, physiological and morphological characterization. Trends Neurosci. 18:527–535. 1995. View Article : Google Scholar : PubMed/NCBI
7	Baimbridge KG, Celio MR and Rogers JH: Calcium-binding proteins in the nervous system. Trends Neurosci. 15:303–308. 1992. View Article : Google Scholar : PubMed/NCBI
8	Burgoyne RD: Neuronal calcium sensor proteins: Generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci. 8:182–193. 2007. View Article : Google Scholar : PubMed/NCBI
9	Arundine M and Tymianski M: Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium. 34:325–337. 2003. View Article : Google Scholar : PubMed/NCBI
10	Oh MM, Oliveira FA, Waters J and Disterhoft JF: Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons. J Neurosci. 33:7905–7911. 2013. View Article : Google Scholar : PubMed/NCBI
11	Kuchibhotla KV, Goldman ST, Lattarulo CR, Wu HY, Hyman BT and Bacskai BJ: Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron. 59:214–225. 2008. View Article : Google Scholar : PubMed/NCBI
12	Villa A, Podini P, Panzeri MC, Racchetti G and Meldolesi J: 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. 6:1491–1499. 1994. View Article : Google Scholar : PubMed/NCBI
13	Kishimoto J, Tsuchiya T, Cox H, Emson PC and Nakayama Y: Age-related changes of calbindin-D28k, calretinin and parvalbumin mRNAs in the hamster brain. Neurobiol Aging. 19:77–82. 1998. View Article : Google Scholar : PubMed/NCBI
14	Gonchar Y, Wang Q and Burkhalter A: Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 1:32008. View Article : Google Scholar : PubMed/NCBI
15	Litwinowicz B, Labuda C, Kowiański P, Spodnik JH, Ludkiewicz B, Wójcik S and Moryś J: Developmental pattern of calbindin D28k protein expression in the rat striatum and cerebral cortex. Folia Morphol (Warsz). 62:327–329. 2003.PubMed/NCBI
16	Bu J, Sathyendra V, Nagykery N and Geula C: Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol. 182:220–231. 2003. View Article : Google Scholar : PubMed/NCBI
17	Selakovic V, Balind Rauš S, Radenovic L, Prolić Z and Janać B: Age-dependent effects of ELF-MF on oxidative stress in the brain of Mongolian gerbils. Cell Biochem Biophys. 66:513–521. 2013. View Article : Google Scholar : PubMed/NCBI
18	Lores-Arnaiz S, Lombardi P, Karadayian AG, Orgambide F, Cicerchia D and Bustamante J: Brain cortex mitochondrial bioenergetics in synaptosomes and non-synaptic mitochondria during aging. Neurochem Res. 41:353–363. 2016. View Article : Google Scholar : PubMed/NCBI
19	Zheng T, Lv Q, Lei X, Yin X and Zhang B: Spatial distribution of 5-hydroxymethyl cytosine in rat brain and temporal distribution in striatum. Neurochem Res. 40:688–697. 2015. View Article : Google Scholar : PubMed/NCBI
20	Vanhooren V and Libert C: The mouse as a model organism in aging research: Usefulness, pitfalls and possibilities. Ageing Res Rev. 12:8–21. 2013. View Article : Google Scholar : PubMed/NCBI
21	Quinn R: Comparing rat's to human's age: How old is my rat in people years? Nutrition. 21:775–777. 2005. View Article : Google Scholar : PubMed/NCBI
22	Demetrius L: Aging in mouse and human systems. Ann N Y Acad Sci. 1067:66–82. 2006. View Article : Google Scholar : PubMed/NCBI
23	Gorbunova V, Bozzella MJ and Seluanov A: Rodents for comparative aging studies: From mice to beavers. Age (Dordr). 30:111–119. 2008. View Article : Google Scholar : PubMed/NCBI
24	Institute of Laboratory Animal Research, Committee for the Update of the Guide for the Care and Use of Laboratory Animals, National Research Council, . Guide for the care and use of laboratory animals. 8th edition. Washington, (DC): National Academies Press; pp. 2202011
25	Bae EJ, Chen BH, Shin BN, Cho JH, Kim IH, Park JH, Lee JC, Tae HJ, Choi SY, Kim JD, et al: Comparison of immunoreactivities of calbindin-D28k, calretinin and parvalbumin in the striatum between young, adult and aged mice, rats and gerbils. Neurochem Res. 40:864–872. 2015. View Article : Google Scholar : PubMed/NCBI
26	Keith BJ and George P Franklin: The Mouse Brain in Stereotaxic Coordinates. San Diego, California: Academic Press, Inc.; pp. 20–39. 1997
27	George P and Charles W: The Rat Brain in Stereotaxic Coordinates. 2nd. San Diego, California: Academic Press, Inc.; pp. 11–24. 1986
28	William JL, Peter L and Anthony MV: A stereotaxic Atlas of the Mongolian Gerbil Brain (Meriones unguiculatus). Ann Arbor, Michigan: Ann Arbor Science Publishers Inc.; pp. 36–60. 1974
29	Lee JC, Ahn JH, Lee DH, Yan BC, Park JH, Kim IH, Cho GS, Kim YM, Lee B, Park CW, et al: Neuronal damage and gliosis in the somatosensory cortex induced by various durations of transient cerebral ischemia in gerbils. Brain Res. 1510:78–88. 2013. View Article : Google Scholar : PubMed/NCBI
30	Shetty AK and Turner DA: Hippocampal interneurons expressing glutamic acid decarboxylase and calcium-binding proteins decrease with aging in Fischer 344 rats. J Comp Neurol. 394:252–269. 1998. View Article : Google Scholar : PubMed/NCBI
31	Lee CH, Hwang IK, Yoo KY, Choi JH, Park OK, Lee JC, Jeong YG, Lee IS and Won MH: Calbindin d-28k immunoreactivity and its protein level in hippocampal subregions during normal aging in gerbils. Cell Mol Neurobiol. 29:665–672. 2009. View Article : Google Scholar : PubMed/NCBI
32	Lee CH, Hwang IK, Choi JH, Yoo KY, Park OK, Huh SO, Lee YL, Shin HC and Won MH: Age-dependent changes in calretinin immunoreactivity and its protein level in the gerbil hippocampus. Neurochem Res. 35:122–129. 2010. View Article : Google Scholar : PubMed/NCBI
33	Pugliese M, Carrasco J, Geloso MC, Mascort J, Michetti F and Mahy N: γ-aminobutyric acidergic interneuron vulnerability to aging in canine prefrontal cortex. J Neurosci Res. 77:913–920. 2004. View Article : Google Scholar : PubMed/NCBI
34	DeFelipe J and Fariñas I: The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol. 39:563–607. 1992. View Article : Google Scholar : PubMed/NCBI
35	Meskenaite V: Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol. 379:113–132. 1997. View Article : Google Scholar : PubMed/NCBI
36	Ferrer-Blasco T, González-Méijome JM and Montés-Micó R: Age-related changes in the human visual system and prevalence of refractive conditions in patients attending an eye clinic. J Cataract Refract Surg. 34:424–432. 2008. View Article : Google Scholar : PubMed/NCBI
37	Lehmann K, Schmidt KF and Löwel S: Vision and visual plasticity in ageing mice. Restor Neurol Neurosci. 30:161–178. 2012.PubMed/NCBI
38	Hua T, Li X, He L, Zhou Y, Wang Y and Leventhal AG: Functional degradation of visual cortical cells in old cats. Neurobiol Aging. 27:155–162. 2006. View Article : Google Scholar : PubMed/NCBI
39	Leventhal AG, Wang Y, Pu M, Zhou Y and Ma Y: GABA and its agonists improved visual cortical function in senescent monkeys. Science. 300:812–815. 2003. View Article : Google Scholar : PubMed/NCBI