Fibrocytes in the cochlea of the mammalian inner ear: their molecular architecture, physiological properties, and pathological relevance
Main Article Content
Abstract
Fibroblasts are a cell type that dominates connective tissues in a broad array of organs and plays key roles in formation of the extracellular matrix and wound healing. The cochlea of the mammalian inner ear harbors loose connective tissues such as the spiral ligament and spiral limbus, and their cellular components are called “fibrocytes.” The fibrocytes in the ligament are functionally differentiated and specialized for ion transport that is essential for proper actions of the cochlea. Molecular biological and histological assays have shown that these cells express specific types of ion channels and transporters. Results of in vivo electrophysiological experiments have integrated activities of individual channels and transporters into the ionic flow that circulates throughout the organ and maintains the electrochemical properties in various tissues and extracellular fluids. Moreover, analyses of deafness genes in humans as well as transgenic experiments on mice recently revealed the relevance of fibrocyte dysfunction to hearing disorders. In this review article, we not only describe molecular architecture and physiological and pathological significance of cochlear fibrocytes but also provide insights into next-generation therapies targeting these cells.
Article Details
How to Cite
YOSHIDA, Takamasa et al.
Fibrocytes in the cochlea of the mammalian inner ear: their molecular architecture, physiological properties, and pathological relevance.
Medical Research Archives, [S.l.], v. 5, n. 6, june 2017.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/1335>. Date accessed: 18 apr. 2024.
doi: https://doi.org/10.18103/mra.v5i6.1335.
Keywords
cochlea, fibrocyte, hearing
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
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9. Herzog EL, Bucala R. Fibrocytes in health and disease. Exp Hematol. 2010;38(7):548-556.
10. Keeley EC, Mehrad B, Strieter RM. Fibrocytes: Bringing new insights into mechanisms of inflammation and fibrosis. The International Journal of Biochemistry & Cell Biology. 2010;42(4):535-542.
11. Takahashi T, Kimura RS. The ultrastructure of the spiral ligament in the Rhesus monkey. Acta Otolaryngol. 1970;69(1):46-60.
12. Kimura R, Schuknecht H. The ultrastructure of the human stria vascularis. Part I. Acta Otolaryngol. 1970;69(1-6):415-427.
13. Kimura R, Schuknecht H. The ultrastructure of the human stria vascularis. Part II. Acta Otolaryngol. 1970;70(5-6):301-318.
14. Slepecky NB. Structure of the mammalian cochlea. The cochlea: Springer; 1996:44-129.
15. Kikuchi T, Adams JC, Miyabe Y, So E, Kobayashi T. Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc. 2000;33(2):51-56.
16. Wangemann P. Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol. 2006;576(Pt 1):11-21.
17. Hibino H, Kurachi Y. Molecular and physiological bases of the K+ circulation in the mammalian inner ear. Physiology. 2006;21:336-345.
18. Davis H. Some principles of sensory receptor action. Physiol Rev. 1961;41(2):391-416.
19. Konishi T, Hamrick PE, Walsh PJ. Ion transport in guinea pig cochlea. I. Potassium and sodium transport. Acta Otolaryngol. 1978;86(1-2):22-34.
20. Kikuchi T, Kimura RS, Paul DL, Adams JC. Gap junctions in the rat cochlea: immunohistochemical and ultrastructural analysis. Anat Embryol (Berl). 1995;191(2):101-118.
21. Spicer SS, Schulte BA. The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res. 1996;100(1-2):80-100.
22. Wangemann P. K+ cycling and the endocochlear potential. Hear Res. 2002;165(1-2):1-9.
23. Spicer SS, Schulte BA. Evidence for a medial K+ recycling pathway from inner hair cells. Hear Res. 1998;118(1):1-12.
24. Phippard D, Lu L, Lee D, Saunders JC, Crenshaw EB. Targeted Mutagenesis of the POU-Domain Gene Brn4/Pou3f4 Causes Developmental Defects in the Inner Ear. The Journal of Neuroscience. 1999;19(14):5980-5989.
25. Bibas A, Liang J, Michaels L, Wright A. The development of the stria vascularisin the human foetus. Clin Otolaryngol Allied Sci. 2000;25(2):126-129.
26. Trowe M-O, Maier H, Schweizer M, Kispert A. Deafness in mice lacking the T-box transcription factor Tbx18 in otic fibrocytes. Development. 2008;135(9):1725-1734.
27. Kim JH, Rodriguez-Vazquez JF, Verdugo-Lopez S, Cho KH, Murakami G, Cho BH. Early fetal development of the human cochlea. Anat Rec (Hoboken). 2011;294(6):996-1002.
28. Bohnenpoll T, Trowe M-O, Wojahn I, Taketo MM, Petry M, Kispert A. Canonical Wnt signaling regulates the proliferative expansion and differentiation of fibrocytes in the murine inner ear. Dev Biol. 2014;391(1):54-65.
29. Spicer SS, Schulte BA. Differentiation of inner ear fibrocytes according to their ion transport related activity. Hear Res. 1991;56(1):53-64.
30. Reale E, Luciano L, Franke K, Pannese E, Wermbter G, Iurato S. Intercellular junctions in the vascular stria and spiral ligament. J Ultrastruct Res. 1975;53(3):284-297.
31. Franke K. Fine structure of the tissue lining the cochlear perilymphatic space against the bony labyrinthine capsule. Arch Otorhinolaryngol. 1979;222(3):161-167.
32. Kelly JJ, Forge A, Jagger DJ. Development of gap junctional intercellular communication within the lateral wall of the rat cochlea. Neuroscience. 2011;180:360-369.
33. Lim DJ. Surface ultrastructure of the cochlear perilymphatic space. The Journal of Laryngology & Otology. 1970;84(04):413-428.
34. Iurato S. Submicroscopic structure of the membranous labyrinth 3. The supporting structure of Corti's organ (basilar membrane, limbus spiralis and spiral ligament). Z Zellforsch Mikrosk Anat. 1962;56(1):40-96.
35. Crouch JJ, Sakaguchi N, Lytle C, Schulte BA. Immunohistochemical localization of the Na-K-Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem. 1997;45(6):773-778.
36. Schulte BA, Adams JC. Distribution of immunoreactive Na+,K+-ATPase in gerbil cochlea. J Histochem Cytochem. 1989;37(2):127-134.
37. Nin F, Hibino H, Doi K, Suzuki T, Hisa Y, Kurachi Y. The endocochlear potential depends on two K+ diffusion potentials and an electrical barrier in the stria vascularis of the inner ear. Proc Natl Acad Sci U S A. 2008;105(5):1751-1756.
38. Adachi N, Yoshida T, Nin F, et al. The mechanism underlying maintenance of the endocochlear potential by the K+ transport system in fibrocytes of the inner ear. J Physiol. 2013;591(Pt 18):4459-4472.
39. Yoshida T, Nin F, Ogata G, et al. NKCCs in the fibrocytes of the spiral ligament are silent on the unidirectional K+ transport that controls the electrochemical properties in the mammalian cochlea. Pflugers Arch. 2015;467(7):1577-1589.
40. Hibino H, Higashi‐Shingai K, Fujita A, Iwai K, Ishii M, Kurachi Y. Expression of an inwardly rectifying K+ channel, Kir5. 1, in specific types of fibrocytes in the cochlear lateral wall suggests its functional importance in the establishment of endocochlear potential. Eur J Neurosci. 2004;19(1):76-84.
41. Liang F, Niedzielski A, Schulte BA, Spicer SS, Hazen-Martin DJ, Shen Z. A voltage- and Ca2+-dependent big conductance K channel in cochlear spiral ligament fibrocytes. Pflugers Arch. 2003;445(6):683-692.
42. So E, Kikuchi T, Ishimaru K, Miyabe Y, Kobayashi T. Immunolocalization of voltage-gated potassium channel Kv3.1b subunit in the cochlea. Neuroreport. 2001;12(12):2761-2765.
43. Boettger T, Rust MB, Maier H, et al. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J. 2003;22(20):5422-5434.
44. Hille B. Ion channels of excitable membranes. Vol 507. 3rd ed: Sinauer, Sunderland, MA; 2001.
45. Jaye DA, Xiao Y-F, Sigg DC. Basic Cardiac Electrophysiology: Excitable Membranes. In: Sigg CD, Iaizzo AP, Xiao Y-F, He B, eds. Cardiac Electrophysiology Methods and Models. Boston, MA: Springer US; 2010:41-51.
46. Elmslie KS. Membrane Potential. eLS. Chichester: John Wiley & Sons, Ltd; 2001.
47. Ikeda K, Morizono T. Electrochemical profiles for monovalent ions in the stria vascularis: cellular model of ion transport mechanisms. Hear Res. 1989;39(3):279-286.
48. Nin F, Yoshida T, Sawamura S, et al. The unique electrical properties in an extracellular fluid of the mammalian cochlea; their functional roles, homeostatic processes, and pathological significance. Pflugers Arch - Eur J Physiol. 2016;468(10):1637-1649.
49. Yoshida T, Nin F, Murakami S, et al. The unique ion permeability profile of cochlear fibrocytes and its contribution to establishing their positive resting membrane potential. Pflugers Arch. 2016;468(9):1609-1619.
50. Kelly JJ, Forge A, Jagger DJ. Contractility in type III cochlear fibrocytes is dependent on non-muscle myosin II and intercellular gap junctional coupling. Journal of the Association for Research in Otolaryngology : JARO. 2012;13(4):473-484.
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