Loss of the tectorial membrane protein CEACAM16 enhances spontaneous, stimulus-frequency, and transiently evoked otoacoustic emissions

Mary Ann Cheatham, Richard J. Goodyear, Kazuaki Homma, P. Kevin Legan, Julia Korchagina, Souvik Naskar, Jonathan H. Siegel, Peter Dallos, Jing Zheng, Guy P. Richardson

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

α-Tectorin (TECTA), β-tectorin (TECTB), and carcinoembryonic antigen-related cell adhesion molecule 16 (CEACAM) are secreted glycoproteins that are present in the tectorial membrane (TM), an extracellular structure overlying the hearing organ of the inner ear, the organ of Corti. Previous studies have shown that TECTA and TECTB are both required for formation of the striated-sheet matrix within which collagen fibrils of the TM are imbedded and that CEACAM16 interacts with TECTA. To learn more about the structural and functional significance of CEACAM16, we created a Ceacam16-null mutant mouse. In the absence of CEACAM16, TECTB levels are reduced, a clearly defined striated-sheet matrix does not develop, and Hensen's stripe, a prominent feature in the basal two-thirds of the TM in WT mice, is absent. CEACAM16 is also shown to interact with TECTB, indicating that it may stabilize interactions between TECTA and TECTB. Although brain-stem evoked responses and distortion product otoacoustic emissions are, for most frequencies, normal in young mice lacking CEACAM16, stimulus-frequency and transiently evoked emissions are larger. We also observed spontaneous otoacoustic emissions (SOAEs) in 70% of the homozygous mice. This incidence is remarkable considering that<3% of WT controls have SOAEs. The predominance of SOAEs >15 k Hz correlates with the loss of Hensen's stripe. Results from mice lacking CEACAM16 are consistent with the idea that the organ of Corti evolved to maximize the gain of the cochlear amplifier while preventing large oscillations. Changes in TM structure appear to influence the balance between energy generation and dissipation such that the system becomes unstable.

Original languageEnglish (US)
Pages (from-to)10325-10338
Number of pages14
JournalJournal of Neuroscience
Volume34
Issue number31
DOIs
StatePublished - Jan 1 2014

Fingerprint

Tectorial Membrane
Membrane Proteins
Organ of Corti
Spontaneous Otoacoustic Emissions
Carcinoembryonic Antigen
Cochlea
Cell Adhesion Molecules
Inner Ear
Hearing
Brain Stem
Glycoproteins
Collagen
Incidence

Keywords

  • CEACAM16
  • Cochlea
  • Hensen's stripe
  • Mouse
  • Otoacoustic emissions
  • Tectorial membrane

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Cheatham, Mary Ann ; Goodyear, Richard J. ; Homma, Kazuaki ; Kevin Legan, P. ; Korchagina, Julia ; Naskar, Souvik ; Siegel, Jonathan H. ; Dallos, Peter ; Zheng, Jing ; Richardson, Guy P. / Loss of the tectorial membrane protein CEACAM16 enhances spontaneous, stimulus-frequency, and transiently evoked otoacoustic emissions. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 31. pp. 10325-10338.
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abstract = "α-Tectorin (TECTA), β-tectorin (TECTB), and carcinoembryonic antigen-related cell adhesion molecule 16 (CEACAM) are secreted glycoproteins that are present in the tectorial membrane (TM), an extracellular structure overlying the hearing organ of the inner ear, the organ of Corti. Previous studies have shown that TECTA and TECTB are both required for formation of the striated-sheet matrix within which collagen fibrils of the TM are imbedded and that CEACAM16 interacts with TECTA. To learn more about the structural and functional significance of CEACAM16, we created a Ceacam16-null mutant mouse. In the absence of CEACAM16, TECTB levels are reduced, a clearly defined striated-sheet matrix does not develop, and Hensen's stripe, a prominent feature in the basal two-thirds of the TM in WT mice, is absent. CEACAM16 is also shown to interact with TECTB, indicating that it may stabilize interactions between TECTA and TECTB. Although brain-stem evoked responses and distortion product otoacoustic emissions are, for most frequencies, normal in young mice lacking CEACAM16, stimulus-frequency and transiently evoked emissions are larger. We also observed spontaneous otoacoustic emissions (SOAEs) in 70{\%} of the homozygous mice. This incidence is remarkable considering that<3{\%} of WT controls have SOAEs. The predominance of SOAEs >15 k Hz correlates with the loss of Hensen's stripe. Results from mice lacking CEACAM16 are consistent with the idea that the organ of Corti evolved to maximize the gain of the cochlear amplifier while preventing large oscillations. Changes in TM structure appear to influence the balance between energy generation and dissipation such that the system becomes unstable.",
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Loss of the tectorial membrane protein CEACAM16 enhances spontaneous, stimulus-frequency, and transiently evoked otoacoustic emissions. / Cheatham, Mary Ann; Goodyear, Richard J.; Homma, Kazuaki; Kevin Legan, P.; Korchagina, Julia; Naskar, Souvik; Siegel, Jonathan H.; Dallos, Peter; Zheng, Jing; Richardson, Guy P.

In: Journal of Neuroscience, Vol. 34, No. 31, 01.01.2014, p. 10325-10338.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Loss of the tectorial membrane protein CEACAM16 enhances spontaneous, stimulus-frequency, and transiently evoked otoacoustic emissions

AU - Cheatham, Mary Ann

AU - Goodyear, Richard J.

AU - Homma, Kazuaki

AU - Kevin Legan, P.

AU - Korchagina, Julia

AU - Naskar, Souvik

AU - Siegel, Jonathan H.

AU - Dallos, Peter

AU - Zheng, Jing

AU - Richardson, Guy P.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - α-Tectorin (TECTA), β-tectorin (TECTB), and carcinoembryonic antigen-related cell adhesion molecule 16 (CEACAM) are secreted glycoproteins that are present in the tectorial membrane (TM), an extracellular structure overlying the hearing organ of the inner ear, the organ of Corti. Previous studies have shown that TECTA and TECTB are both required for formation of the striated-sheet matrix within which collagen fibrils of the TM are imbedded and that CEACAM16 interacts with TECTA. To learn more about the structural and functional significance of CEACAM16, we created a Ceacam16-null mutant mouse. In the absence of CEACAM16, TECTB levels are reduced, a clearly defined striated-sheet matrix does not develop, and Hensen's stripe, a prominent feature in the basal two-thirds of the TM in WT mice, is absent. CEACAM16 is also shown to interact with TECTB, indicating that it may stabilize interactions between TECTA and TECTB. Although brain-stem evoked responses and distortion product otoacoustic emissions are, for most frequencies, normal in young mice lacking CEACAM16, stimulus-frequency and transiently evoked emissions are larger. We also observed spontaneous otoacoustic emissions (SOAEs) in 70% of the homozygous mice. This incidence is remarkable considering that<3% of WT controls have SOAEs. The predominance of SOAEs >15 k Hz correlates with the loss of Hensen's stripe. Results from mice lacking CEACAM16 are consistent with the idea that the organ of Corti evolved to maximize the gain of the cochlear amplifier while preventing large oscillations. Changes in TM structure appear to influence the balance between energy generation and dissipation such that the system becomes unstable.

AB - α-Tectorin (TECTA), β-tectorin (TECTB), and carcinoembryonic antigen-related cell adhesion molecule 16 (CEACAM) are secreted glycoproteins that are present in the tectorial membrane (TM), an extracellular structure overlying the hearing organ of the inner ear, the organ of Corti. Previous studies have shown that TECTA and TECTB are both required for formation of the striated-sheet matrix within which collagen fibrils of the TM are imbedded and that CEACAM16 interacts with TECTA. To learn more about the structural and functional significance of CEACAM16, we created a Ceacam16-null mutant mouse. In the absence of CEACAM16, TECTB levels are reduced, a clearly defined striated-sheet matrix does not develop, and Hensen's stripe, a prominent feature in the basal two-thirds of the TM in WT mice, is absent. CEACAM16 is also shown to interact with TECTB, indicating that it may stabilize interactions between TECTA and TECTB. Although brain-stem evoked responses and distortion product otoacoustic emissions are, for most frequencies, normal in young mice lacking CEACAM16, stimulus-frequency and transiently evoked emissions are larger. We also observed spontaneous otoacoustic emissions (SOAEs) in 70% of the homozygous mice. This incidence is remarkable considering that<3% of WT controls have SOAEs. The predominance of SOAEs >15 k Hz correlates with the loss of Hensen's stripe. Results from mice lacking CEACAM16 are consistent with the idea that the organ of Corti evolved to maximize the gain of the cochlear amplifier while preventing large oscillations. Changes in TM structure appear to influence the balance between energy generation and dissipation such that the system becomes unstable.

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