https://doi.org/10.4081/ejh.2024.4137
Developmental expression of calretinin in the mouse cochlea
Submitted: 8 September 2024
Accepted: 22 October 2024
Published: 6 November 2024
Accepted: 22 October 2024
Abstract Views: 147
PDF: 52
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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This study investigated the expression of calretinin (CR) in the mouse cochlea from embryonic day 17 (E17) to adulthood through immunofluorescence. At E17, CR immunoreactivity was only detected in the inner hair cells (IHCs). At E19, the IHCs and spiral ganglion neurons (SGNs) begin to express CR. At birth, CR immunoreactivity was confined primarily to the IHCs and the majority of the SGNs, as identified by TUJ1, both the cytoplasm and the nucleus of SGNs exhibited CR positivity. At postnatal day 2 (P2), auditory nerve fibers reaching the IHCs were stained for CR. CR continued to be expressed in the IHCs, whereas only single row of outer hair cells (OHCs) were positive for CR. By P5, CR expression was evident in IHCs and the three rows of OHCs, with SGNs soma and their neurite projections also displaying CR immunoreactivity. From P8 through adulthood, CR expression persisted in the SGNs and their afferent neurite projections to the IHCs, as well as in IHCs and OHCs. Dual labeling of CR with afferent nerve marker neurofilament 200 (NF200) demonstrated that NF 200-positive SGN somas were encompassed by CR-labeled plasma membrane of SGNs, and NF 200 was co-localized with CR in the afferent nerve fibers innervating the IHCs. We also described the expression of peripherin, a marker for type II SGNs, in the mouse cochlea at various postnatal stages. Peripherin showed a distinct spatio-temporal expression compared to CR in auditory nerve fibers. No co-expression of peripherin and CR was detected in adult. Dynamic expression patterns of CR in the embryonic and postnatal cochlea supported its roles in cochlear development.
1. DeFelipe J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 1997;14:1-19.
DOI: https://doi.org/10.1016/S0891-0618(97)10013-8
2. Chen Y, Gu Y, Li Y, Li GL, Chai R, Li W, Li H. Generation of mature and functional hair cells by co-expression of Gfi1, Pou4f3, and Atoh1 in the postnatal mouse cochlea. Cell Rep 2021;35:109016.
DOI: https://doi.org/10.1016/j.celrep.2021.109016
3. Ouji Y, Ishizaka S, Nakamura-Uchiyama F, Wanaka A, Yoshikawa M. Induction of inner ear hair cell-like cells from Math1-transfected mouse ES cells. Cell Death Dis 2013;4:e700.
DOI: https://doi.org/10.1038/cddis.2013.230
4. Huerta JJ, Nori S, Llamosas MM, Vázquez MT, Bronzetti E, Vega JA. Calretinin immunoreactivity in human sympathetic ganglia. Anat Embryol (Berl) 1996;194:373-8.
DOI: https://doi.org/10.1007/BF00198539
5. Ordóñez NG. Value of calretinin immunostaining in diagnostic pathology: a review and update. Appl Immunohistochem Mol Morphol 2014;22:401-15.
DOI: https://doi.org/10.1097/PAI.0b013e31829b6fbd
6. Doglioni C, Dei Tos AP, Laurino L, Iuzzolino P, Chiarelli C, Celio MR, Viale G. Calretinin: a novel immunocytochemical marker for mesothelioma. Am J Surg Pathol 1996;20:1037-46.
DOI: https://doi.org/10.1097/00000478-199609000-00001
7. Rogers JH, Résibois A. Calretinin and calbindin-D28k in rat brain: patterns of partial co-localization. Neuroscience 1992;51:843-65.
DOI: https://doi.org/10.1016/0306-4522(92)90525-7
8. Liu W, Chen H, Zhu X, Yu H. Expression of Calbindin-D28K in the developing and adult mouse cochlea. J Histochem Cytochem 2022;70:583-96.
DOI: https://doi.org/10.1369/00221554221119543
9. Ewert D, Hu N, Du X, Li W, West MB, Choi C, et al. HPN-07, a free radical spin trapping agent, protects against functional, cellular and electrophysiological changes in the cochlea induced by acute acoustic trauma. PLoS One 2017;12:e0183089.
DOI: https://doi.org/10.1371/journal.pone.0183089
10. Foran L, Blackburn K, Kulesza RJ. Auditory hindbrain atrophy and anomalous calcium binding protein expression after neonatal exposure to monosodium glutamate. Neuroscience 2017;344:406-17.
DOI: https://doi.org/10.1016/j.neuroscience.2017.01.004
11. Alvarado JC, Fuentes-Santamaría V, Gabaldón-Ull MC, Jareño-Flores T, Miller JM, Juiz JM. Noise-induced "toughening" effect in wistar rats: enhanced auditory brainstem responses are related to calretinin and nitric oxide synthase upregulation. Front Neuroanat 2016;10:19.
DOI: https://doi.org/10.3389/fnana.2016.00019
12. Wang M, Lin S, Xie R. Apical-basal distribution of different subtypes of spiral ganglion neurons in the cochlea and the changes during aging. PLoS One 2023;18:e0292676.
DOI: https://doi.org/10.1371/journal.pone.0292676
13. Wang M, Zhang C, Lin S, Wang Y, Seicol BJ, Ariss RW, Xie R. Biased auditory nerve central synaptopathy is associated with age-related hearing loss. J Physiol 2021;599:1833-54.
DOI: https://doi.org/10.1113/JP281014
14. Pangršič T, Gabrielaitis M, Michanski S, Schwaller B, Wolf F, Strenzke N, Moser T. EF-hand protein Ca2+ buffers regulate Ca2+ influx and exocytosis in sensory hair cells. Proc Natl Acad Sci USA 2015;112:E1028-37.
DOI: https://doi.org/10.1073/pnas.1416424112
15. Imamura S, Adams JC. Immunolocalization of peptide 19 and other calcium-binding proteins in the guinea pig cochlea. Anat Embryol (Berl) 1996;194:407-18.
DOI: https://doi.org/10.1007/BF00198543
16. Pibiri V, Gerosa C, Vinci L, Faa G, Ambu R. Immunoreactivity pattern of calretinin in the developing human cerebellar cortex. Acta Histochem 2017;119:228-34.
DOI: https://doi.org/10.1016/j.acthis.2017.01.005
17. Coppens AG, Résibois A, Poncelet L. Immunolocalization of calbindin D28k and calretinin in the dog cochlea during postnatal development. Hear Res 2000;145:101-10.
DOI: https://doi.org/10.1016/S0378-5955(00)00077-0
18. Dechesne CJ, Rabejac D, Desmadryl G. Development of calretinin immunoreactivity in the mouse inner ear. J Comp Neurol 1994;346:517-29.
DOI: https://doi.org/10.1002/cne.903460405
19. Kaiser M, Lüdtke TH, Deuper L, Rudat C, Christoffels VM, Kispert A, Trowe MO. TBX2 specifies and maintains inner hair and supporting cell fate in the organ of Corti. Nat Commun 2022;13:7628.
DOI: https://doi.org/10.1038/s41467-022-35214-4
20. Dechesne CJ, Winsky L, Kim HN, Goping G, Vu TD, Wenthold RJ, Jacobowitz DM. Identification and ultrastructural localization of a calretinin-like calcium-binding protein (protein 10) in the guinea pig and rat inner ear. Brain Res 1991;560:139-48.
DOI: https://doi.org/10.1016/0006-8993(91)91224-O
21. Pack AK, Slepecky NB. Cytoskeletal and calcium-binding proteins in the mammalian organ of Corti: cell type-specific proteins displaying longitudinal and radial gradients. Hear Res 1995;91:119-35.
DOI: https://doi.org/10.1016/0378-5955(95)00173-5
22. Sanders TR, Kelley MW. Specification of neuronal subtypes in the spiral ganglion begins prior to birth in the mouse. Proc Natl Acad Sci USA 2022;119:e2203935119.
DOI: https://doi.org/10.1073/pnas.2203935119
23. Hafidi A, Després G, Romand R. Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry. Int J Dev Neurosci 1993; 11:507-12.
DOI: https://doi.org/10.1016/0736-5748(93)90024-8
24. Barclay M, Julien JP, Ryan AF, Housley GD. Type III intermediate filament peripherin inhibits neuritogenesis in type II spiral ganglion neurons in vitro. Neurosci Lett 2010;478:51-5.
DOI: https://doi.org/10.1016/j.neulet.2010.01.063
25. Liu WJ, Ming SS, Zhao XB, Zhu X, Gong YX. Developmental expression of high-mobility group box 1 (HMGB1) in the mouse cochlea. Eur J Histochem 2023;67:3704.
DOI: https://doi.org/10.4081/ejh.2023.3704
26. Shrestha BR, Chia C, Wu L, Kujawa SG, Liberman MC, Goodrich LV. Sensory neuron diversity in the inner ear is shaped by activity. Cell 2018;174:1229-1246.e17.
DOI: https://doi.org/10.1016/j.cell.2018.07.007
27. Spatz WB, Löhle E. Calcium-binding proteins in the spiral ganglion of the monkey, Callithrix jacchus. Hear Res 1995;86:89-99.
DOI: https://doi.org/10.1016/0378-5955(95)00059-D
28. He S, Yang J. Maturation of neurotransmission in the developing rat cochlea: immunohistochemical evidence from differential expression of synaptophysin and synaptobrevin 2. Eur J Histochem 2011;55:e2.
DOI: https://doi.org/10.4081/ejh.2011.e2
29. Drescher MJ, Drescher DG, Khan KM, Hatfield JS, Ramakrishnan NA, Abu-Hamdan MD, Lemonnier LA. Pituitary adenylyl cyclase-activating polypeptide (PACAP) and its receptor (PAC1-R) are positioned to modulate afferent signaling in the cochlea. Neuroscience 2006;142:139-64.
DOI: https://doi.org/10.1016/j.neuroscience.2006.05.065
30. Jovanovic S, Milenkovic I. Purinergic modulation of activity in the developing auditory pathway. Neurosci Bull 2020;36:1285-98.
DOI: https://doi.org/10.1007/s12264-020-00586-4
31. Bazwinsky-Wutschke I, Dehghani F. Impact of cochlear ablation on calretinin and synaptophysin in the gerbil anteroventral cochlear nucleus before the hearing onset. J Chem Neuroanat 2020;104:101746.
DOI: https://doi.org/10.1016/j.jchemneu.2020.101746
32. Benítez-Temiño B, Hernández RG, de la Cruz RR, Pastor AM. BDNF Influence on adult terminal axon sprouting after partial deafferentation. Int J Mol Sci 2023;24:10660.
DOI: https://doi.org/10.3390/ijms241310660
33. Rogers JH. Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 1989;31:697-709.
DOI: https://doi.org/10.1016/0306-4522(89)90434-X
34. Bastianelli E, Pochet R. Calmodulin, calbindin-D28k, calretinin and neurocalcin in rat olfactory bulb during postnatal development. Brain Res Dev Brain Res 1995;87:224-7.
DOI: https://doi.org/10.1016/0165-3806(95)00073-M
35. Liu WJ, Yang J. Preferentially regulated expression of connexin 43 in the developing spiral ganglion neurons and afferent terminals in post-natal rat cochlea. Eur J Histochem 2015;59:2464.
DOI: https://doi.org/10.4081/ejh.2015.2464
36. Rubel EW, Fritzsch B. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 2002;25:51-101.
DOI: https://doi.org/10.1146/annurev.neuro.25.112701.142849
37. Kang KW, Pangeni R, Park J, Lee J, Yi E. Selective loss of calretinin-poor cochlear afferent nerve fibers in streptozotocin-induced hyperglycemic mice. J Nanosci Nanotechnol 2020;20:5515-19.
DOI: https://doi.org/10.1166/jnn.2020.17654
38. Idrizbegovic E, Salman H, Niu X, Canlon B. Presbyacusis and calcium-binding protein immunoreactivity in the cochlear nucleus of BALB/c mice. Hear Res 2006;216-217:198-206.
DOI: https://doi.org/10.1016/j.heares.2006.01.009
39. Idrizbegovic E, Viberg A, Bogdanovic N, Canlon B. Peripheral cell loss related to calcium binding protein immunocytochemistry in the dorsal cochlear nucleus in CBA/CaJ mice during aging. Audiol Neurootol 2001;6:132-9.
DOI: https://doi.org/10.1159/000046820
40. Jankovski A, Garcia C, Soriano E, Sotelo C. Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 1998;10:3853-68.
DOI: https://doi.org/10.1046/j.1460-9568.1998.00397.x
41. von Bohlen Und Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 2007;329:409-20.
DOI: https://doi.org/10.1007/s00441-007-0432-4
42. Gonzalez ABI, Koning HK, Tuz-Sasik MU, Osselen IV, Manuel R, Boije H. Perturbed development of calb2b expressing dI6 interneurons and motor neurons underlies locomotor defects observed in calretinin knock-down zebrafish larvae. Dev Biol 2024;508:77-87.
DOI: https://doi.org/10.1016/j.ydbio.2024.01.001
43. Chen P, Segil N. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 1999;126:1581-90.
DOI: https://doi.org/10.1242/dev.126.8.1581
44. Hackney CM, Mahendrasingam S, Penn A, Fettiplace R. The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 2005;25:7867-75.
DOI: https://doi.org/10.1523/JNEUROSCI.1196-05.2005
45. Zheng JL, Gao WQ. Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. J Neurosci 1997;17:8270-82.
DOI: https://doi.org/10.1523/JNEUROSCI.17-21-08270.1997
46. Singh SK, Gupta UK, Aggarwal R, Rahman RA, Gupta NK, Verma V. Diagnostic role of calretinin in suspicious cases of Hirschsprung's disease. Cureus 2021;13:e13373.
DOI: https://doi.org/10.7759/cureus.13373
47. Brion JP, Résibois A. A subset of calretinin-positive neurons are abnormal in Alzheimer's disease. Acta Neuropathol 1994;88:33-43.
DOI: https://doi.org/10.1007/BF00294357
48. Diez D, Morte B, Bernal J. Single-cell transcriptome profiling of thyroid hormone effectors in the human fetal neocortex: expression of SLCO1C1, DIO2, and THRB in specific cell types. Thyroid 2021;31:1577-88.
DOI: https://doi.org/10.1089/thy.2021.0057
49. Nam SM, Kim YN, Yoo DY, Yi SS, Kim W, Hwang IK, et al. Hypothyroid states mitigate the diabetes-induced reduction of calbindin D-28k, calretinin, and parvalbumin immunoreactivity in type 2 diabetic rats. Neurochem Res 2012;37:253-60.
DOI: https://doi.org/10.1007/s11064-011-0602-3
50. Shiraki A, Akane H, Ohishi T, Wang L, Morita R, Suzuki K, et al. Similar distribution changes of GABAergic interneuron subpopulations in contrast to the different impact on neurogenesis between developmental and adult-stage hypothyroidism in the hippocampal dentate gyrus in rats. Arch Toxicol 2012;86:1559-69.
DOI: https://doi.org/10.1007/s00204-012-0846-y
51. Wallis K, Sjögren M, Hogerlinden MV, Silberberg G, Fisahn A, Nordström K, et al. Locomotor deficiencies and aberrant development of subtype-specific GABAergic interneurons caused by an unliganded thyroid hormone receptor alpha1. J Neurosci 2008;28:1904-15.
DOI: https://doi.org/10.1523/JNEUROSCI.5163-07.2008
52. Barakat-Walter I, Kraftsik R, Kuntzer T, Bogousslavsky J, Magistretti P. Differential effect of thyroid hormone deficiency on the growth of calretinin-expressing neurons in rat spinal cord and dorsal root ganglia. J Comp Neurol 2000;426:519-33.
DOI: https://doi.org/10.1002/1096-9861(20001030)426:4<519::AID-CNE2>3.0.CO;2-6
53. Moser T, Starr A. Auditory neuropathy--neural and synaptic mechanisms. Nat Rev Neurol 2016;12:135-49.
DOI: https://doi.org/10.1038/nrneurol.2016.10
Ethics Approval
All animal studies, including the mice euthanasia procedure, were approved by the Animal Care and Use Committee of the Southeast University, Nanjing, ChinaSupporting Agencies
National Natural Science Foundation of China , Natural Science Foundation of Jiangsu ProvinceHow to Cite
Liu, W., Zhang, Y., Liang, C., & Jiang, X. (2024). Developmental expression of calretinin in the mouse cochlea. European Journal of Histochemistry, 68(4). https://doi.org/10.4081/ejh.2024.4137
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