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Cochlear Vascular Pathology and Hearing Loss

  • Xiaorui Shi
Chapter

Abstract

Normal vascular function is essential for hearing. Abnormal blood flow to the cochlea is an etiologic factor contributing to various hearing disorders and vestibular dysfunctions, including noise-induced hearing loss, sudden deafness, presbyacusis, genetically-linked hearing loss, and endolymphatic hydrops such as Meniere’s disease. Progression in blood flow pathology can parallel progression in hair cell loss and hearing impairment. To sustain hearing acuity, a healthy blood flow must be maintained. The blood supply not only provides oxygen and glucose to the hearing organ, it is also responsible for transporting hormones and neurotrophic growth factors to the tissue critical for organ health. Study of the vascular system in the inner ear has a long and rich history. There is a large body of evidence demonstrating a relationship between disturbances in cochlear microcirculatory homeostasis and decreased auditory sensitivity. This chapter focuses on recent discoveries relating the physiopathology of the microvasculature in the cochlear lateral wall to hearing function.

Keywords

Cochlear blood flow Aging Noise Ototoxic drug Hearing loss 

Notes

Acknowledgments

Most of the data presented in this review reflects the efforts of my colleagues and students at the Oregon Hearing Research Center. In particular, the author is deeply indebted to Dr. Alfred Nuttall for stimulating discussion and advice. The author also thanks Mr. Allan Kachelmeier and Ms Janice Moore for editorial assistance, and Christine Casabar for assistance with the references.

This work was supported by National Institutes of Health grants R03 DC008888, DC008888S1, R01 DC010844 (X. Shi), R21 DC1239801 (X. Shi.); P30-DC005983 (Peter Barr-Gillespie); R01 DC000105 (Alfred L. Nuttall); R21 DC016157 (X. Shi.) and R01 DC015781 (X. Shi).

References

  1. Abbott NJ, Rönnbäck L, Hansson E. Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci. 2006;7:41–53.CrossRefPubMedGoogle Scholar
  2. Adams J. Immunocytochemical traits of type IV fibrocytes and their possible relations to cochlear function and pathology. J Assoc Res Otolaryngol. 2009;10:369–82.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Adams JC, Seed B, Lu N, Landry A, Xavier RJ. Selective activation of nuclear factor kappa B in the cochlea by sensory and inflammatory stress. Neuroscience. 2009;160:530–9.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ågrup C, Luxon LM. Immune-mediated inner-ear disorders in neuro-otology. Curr Opin Neurol. 2006;19:26–32.PubMedCrossRefGoogle Scholar
  5. Aksoy F, Dogan R, Ozturan O, Yildirim YS, Veyseller B, Yenigun A, Ozturk B. Betahistine exacerbates amikacin ototoxicity. Ann Otol Rhinol Laryngol. 2015;124:280–7.PubMedCrossRefGoogle Scholar
  6. Angelborg C, Axelsson A, Larsen H-C. Regional blood flow in the rabbit cochlea. Arch Otolaryngol. 1984;110:297–300.PubMedCrossRefGoogle Scholar
  7. Axelsson A. The vascular anatomy of the cochlea in the guinea pig and in man. Acta Otolaryngol. 1968;Suppl 243:3+.Google Scholar
  8. Axelsson A, Dengerink H. The effects of noise on histological measures of the cochlear vasculature and red blood cells: a review. Hear Res. 1987;31:183–91.PubMedCrossRefGoogle Scholar
  9. Axelsson A, Vertes D. Histological findings in cochlear vessels after noise, new perspectives on noise-induced hearing loss. New York: Raven Press; 1982. p. 49–68.Google Scholar
  10. Blank M, Barzilai O, Shoenfeld Y. Molecular mimicry and auto-immunity. Clin Rev Allergy Immunol. 2007;32:111–8.PubMedCrossRefGoogle Scholar
  11. Block ML, Hong J-S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005;76:77–98.PubMedCrossRefGoogle Scholar
  12. Block ML, Zecca L, Hong J-S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8:57–69.PubMedCrossRefGoogle Scholar
  13. Brown JN, Nuttall AL. Autoregulation of cochlear blood flow in guinea pigs. Am J Physiol Heart Circ Physiol. 1994;266:H458–67.CrossRefGoogle Scholar
  14. Brown JN, Miller JM, Nuttall AL. Age-related changes in cochlear vascular conductance in mice. Hear Res. 1995;86:189–94.PubMedCrossRefGoogle Scholar
  15. Bush WD, Simon JD. Quantification of Ca2+ binding to melanin supports the hypothesis that melanosomes serve a functional role in regulating calcium homeostasis. Pigment Cell Res. 2007;20:134–9.PubMedCrossRefGoogle Scholar
  16. Cable J, Steel KP. Identification of two types of melanocyte within the stria vascularis of the mouse inner ear. Pigment Cell Res. 1991;4:87–101.PubMedCrossRefGoogle Scholar
  17. Cadoni G, Fetoni AR, Agostino S, Santis AD, Manna R, Ottaviani F, Paludetti G. Autoimmunity in sudden sensorineural hearing loss: possible role of anti-endothelial cell autoantibodies. Acta Otolaryngol. 2002;122:30–3.CrossRefGoogle Scholar
  18. Campbell KC, Meech RP, Rybak LP, Hughes LF. D-Methionine protects against cisplatin damage to the stria vascularis. Hear Res. 1999;138:13–28.PubMedCrossRefGoogle Scholar
  19. Canlon B. Acoustic overstimulation alters the morphology of the tectorial membrane. Hear Res. 1987;30:127–34.PubMedCrossRefGoogle Scholar
  20. Canlon B. The effect of acoustic trauma on the tectorial membrane, stereocilia, and hearing sensitivity: possible mechanisms underlying damage, recovery, and protection. Scand Audiol Suppl. 1988;27:1–45.PubMedGoogle Scholar
  21. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979;59:527–605.PubMedCrossRefGoogle Scholar
  22. Cardinaal RM, de Groot JC, Huizing EH, Veldman JE, Smoorenburg GF. Dose-dependent effect of 8-day cisplatin administration upon the morphology of the albino guinea pig cochlea. Hear Res. 2000;144:135–46.PubMedCrossRefGoogle Scholar
  23. Carraro M, Harrison RV. Degeneration of stria vascularis in age-related hearing loss; a corrosion cast study in a mouse model. Acta Otolaryngol. 2016;136:385–90.PubMedCrossRefGoogle Scholar
  24. Carraro M, Park AH, Harrison RV. Partial corrosion casting to assess cochlear vasculature in mouse models of presbycusis and CMV infection. Hear Res. 2016;332:95–103.PubMedCrossRefGoogle Scholar
  25. Carraro M, Almishaal A, Hillas E, Firpo M, Park A, Harrison RV. Cytomegalovirus (CMV) infection causes degeneration of cochlear vasculature and hearing loss in a mouse model. J Assoc Res Otolaryngol. 2017;18:263–73.PubMedCrossRefGoogle Scholar
  26. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiological reviews 1979;59:527–605.PubMedCrossRefGoogle Scholar
  27. Chen J, Ingham N, Kelly J, Jadeja S, Goulding D, Pass J, Mahajan VB, Tsang SH, Nijnik A, Jackson IJ. Spinster homolog 2 (spns2) deficiency causes early onset progressive hearing loss. PLoS Genet. 2014;10(10):e1004688.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chéret C, Gervais A, Lelli A, Colin C, Amar L, Ravassard P, Mallet J, Cumano A, Krause K-H, Mallat M. Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase. J Neurosci. 2008;28:12039–51.PubMedCrossRefGoogle Scholar
  29. Cuadros MA, Navascués J. The origin and differentiation of microglial cells during development. Prog Neurobiol. 1998;56:173–89.PubMedCrossRefGoogle Scholar
  30. Cui Q, Yin Y, Benowitz L. The role of macrophages in optic nerve regeneration. Neuroscience. 2009;158:1039–48.PubMedCrossRefGoogle Scholar
  31. Dai C, Gan RZ. Change in cochlear response in an animal model of otitis media with effusion. Audiol Neurootol. 2010;15:155–67.PubMedCrossRefGoogle Scholar
  32. Dai M, Shi X. Fibro-vascular coupling in the control of cochlear blood flow. PLoS One. 2011;6:e20652.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dai M, Shi X. Fibro-vascular coupling in the control of cochlear blood flow. PloS One. 2011;6(6):e20652.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dai CF, Steyger PS. A systemic gentamicin pathway across the stria vascularis. Hear Res. 2008;235:114–24.CrossRefPubMedGoogle Scholar
  35. Dai M, Nuttall A, Yang Y, Shi X. Visualization and contractile activity of cochlear pericytes in the capillaries of the spiral ligament. Hear Res. 2009;254:100–7.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ding D, McFadden SL, Woo JM, Salvi RJ. Ethacrynic acid rapidly and selectively abolishes blood flow in vessels supplying the lateral wall of the cochlea. Hear Res. 2002;173:1–9.PubMedCrossRefGoogle Scholar
  37. Ding D, Jiang H, Wang P, Salvi R. Cell death after co-administration of cisplatin and ethacrynic acid. Hear Res. 2007;226:129–39.PubMedCrossRefGoogle Scholar
  38. Ding D, Allman BL, Salvi R. Review: ototoxic characteristics of platinum antitumor drugs. Anat Rec. 2012;295:1851–67.CrossRefGoogle Scholar
  39. Doherty JK, Linthicum FH Jr. Spiral ligament and stria vascularis changes in cochlear otosclerosis: effect on hearing level. Otol Neurotol. 2004;25:457–64.PubMedCrossRefGoogle Scholar
  40. Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab. 2006;26:613–24.PubMedCrossRefGoogle Scholar
  41. Dräger U. Calcium binding in pigmented and albino eyes. Proc Natl Acad Sci U S A. 1985;82:6716–20.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ekdahl C, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience. 2009;158:1021–9.PubMedCrossRefGoogle Scholar
  43. Frank RN, Dutta S, Mancini MA. Pericyte coverage is greater in the retinal than in the cerebral capillaries of the rat. Invest Ophthalmol Vis Sci. 1987;28:1086–91.PubMedGoogle Scholar
  44. Franz P, Helmreich M, Stach M, Franz-Italon C, Böck P. Distribution of actin and myosin in the cochlear microvascular bed. Acta Otolaryngol. 2004;124:481–5.PubMedCrossRefGoogle Scholar
  45. Freyer L, Aggarwal V, Morrow BE. Dual embryonic origin of the mammalian otic vesicle forming the inner ear. Development. 2011;138:5403–14.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Fujioka M, Kanzaki S, Okano HJ, Masuda M, Ogawa K, Okano H. Proinflammatory cytokines expression in noise-induced damaged cochlea. J Neurosci Res. 2006;83:575–83.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Fujioka M, Okano H, Ogawa K. Inflammatory and immune responses in the cochlea: potential therapeutic targets for sensorineural hearing loss. Front Pharmacol. 2014;5:287.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gatehouse S, Lowe G. Whole blood viscosity and red cell filterability as factors in sensorineural hearing impairment in the elderly. Acta Otolaryngol. 1991;111:37–43.CrossRefGoogle Scholar
  49. Gates GA, Mills JH. Presbycusis. Lancet. 2005;366:1111–20.PubMedCrossRefGoogle Scholar
  50. Goldwyn BG, Quirk WS. Calcium channel blockade reduces noise-induced vascular permeability in cochlear stria vascularis. Laryngoscope. 1997;107:1112–6.PubMedCrossRefGoogle Scholar
  51. Goodall AF. Current understanding of the pathogenesis of autoimmune inner ear disease: a review. Clin Otolaryngol. 2015;40(5):412–9.PubMedCrossRefGoogle Scholar
  52. Gratton MA, Schmiedt RA, Schulte BA. Age-related decreases in endocochlear potential are associated with vascular abnormalities in the stria vascularis [corrected and republished article originallly printed in Hear Res 1996 May;94(1–2):116–24]. Hear Res. 1996;102:181–90.PubMedCrossRefGoogle Scholar
  53. Gratton MA, Schulte BA, Smythe NM. Quantification of the stria vascularis and strial capillary areas in quiet-reared young and aged gerbils. Hear Res. 1997;114:1–9.PubMedCrossRefGoogle Scholar
  54. Greco A, Gallo A, Fusconi M, Marinelli C, Macri G, De Vincentiis M. Meniere’s disease might be an autoimmune condition? Autoimmun Rev. 2012;11:731–8.PubMedCrossRefGoogle Scholar
  55. Greenhalgh SN, Iredale JP, Henderson NC. Origins of fibrosis: pericytes take centre stage. F1000Prime Rep. 2013;5:37.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Greenhalgh SN, Conroy KP, Henderson NC. Healing scars: targeting pericytes to treat fibrosis. QJM. 2015;108:3–7.PubMedCrossRefGoogle Scholar
  57. Greif DM, Eichmann A. Vascular biology: brain vessels squeezed to death. Nature. 2014;508:50–1.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Gyo K. Experimental study of transient cochlear ischemia as a cause of sudden deafness. World J Otorhinolaryngol. 2013;3:1–15.CrossRefGoogle Scholar
  59. Hall CN, Reynell C, Gesslein B, Hamilton NB, Mishra A, Sutherland BA, O’Farrell FM, Buchan AM, Lauritzen M, Attwell D. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;508:55–60.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hanisch U-K, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387–94.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Hawkins JE Jr. The role of vasoconstriction in noise-induced hearing loss. Ann Otol Rhinol Laryngol. 1971;80:903–13.PubMedCrossRefGoogle Scholar
  62. Hawkins J. Comparative otopathology: aging, noise, and ototoxic drugs, otophysiology. Karger Publishers; 1973. p. 125–41.Google Scholar
  63. Hawkins J. Microcirculation in the labyrinth. Eur Arch Otorhinolaryngol. 1976;212:241–51.CrossRefGoogle Scholar
  64. Hess DC, Abe T, Hill WD, Studdard AM, Carothers J, Masuya M, Fleming PA, Drake CJ, Ogawa M. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol. 2004;186:134–44.PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hibino H, Nin F, Tsuzuki C, Kurachi Y. How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus. Pflugers Arch. 2010;459:521–33.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Hilger JA. The common ground of allergy, autonomic dysfunction and endocrine imbalance. Trans Am Acad Ophthalmol Otolaryngol. 1952;57:443–6.Google Scholar
  67. Hillerdal M, Sperber G, Bill A. The microsphere method for measuring low blood flows: theory and computer simulations applied to findings in the rat cochlea. Acta Physiol. 1987;130:229–35.CrossRefGoogle Scholar
  68. Hirose K, Discolo CM, Keasler J, Ransohoff R. Mononuclear phagocytes migrate into the murine cochlea after acoustic trauma. J Comp Neurol. 2005;489(2):180–94.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hirose K, Hartsock JJ, Johnson S, Santi P, Salt AN. Systemic lipopolysaccharide compromises the blood-labyrinth barrier and increases entry of serum fluorescein into the perilymph. J Assoc Res Otolaryngol. 2014;15:707–19.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Honkura Y, Matsuo H, Murakami S, Sakiyama M, Mizutari K, Shiotani A, Yamamoto M, Morita I, Shinomiya N, Kawase T. Nrf2 is a key target for prevention of noise-induced hearing loss by reducing oxidative damage of cochlea. Sci Rep. 2016;6:19329.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hughes G, Kinney S, Barna B, Calabrese L. Autoimmune reactivity in Meniere’s disease: a preliminary report. Laryngoscope. 1983;93:410–7.PubMedCrossRefGoogle Scholar
  72. Hukee MJ, Duvall AJ III. Cochlear vessel permeability to horseradish peroxidase in the normal and acoustically traumatized chinchilla: a reevaluation. Ann Otol Rhinol Laryngol. 1985;94:297–303.PubMedGoogle Scholar
  73. Hultcrantz E, Nuttall AL. Effect of hemodilution on cochlear blood flow measured by laser-Doppler flowmetry. Am J Otolaryngol. 1987;8:16–22.PubMedCrossRefGoogle Scholar
  74. Ingham NJ, Carlisle F, Pearson S, Lewis MA, Buniello A, Chen J, Isaacson RL, Pass J, White JK, Dawson SJ. S1PR2 variants associated with auditory function in humans and endocochlear potential decline in mouse. Sci Rep. 2016;6:28964.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ishibashi T, Takumida M, Akagi N, Hirakawa K, Anniko M. Changes in transient receptor potential vanilloid (TRPV) 1, 2, 3 and 4 expression in mouse inner ear following gentamicin challenge. Acta Otolaryngol. 2009;129:116–26.PubMedCrossRefGoogle Scholar
  76. Ishiyama G, Lopez IA, Ishiyama P, Vinters HV, Ishiyama A. The blood labyrinthine barrier in the human normal and Meniere’s disease macula utricle. Sci Rep. 2017;7:253.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Jabba SV, Oelke A, Singh R, Maganti RJ, Fleming S, Wall SM, Everett LA, Green ED, Wangemann P. Macrophage invasion contributes to degeneration of stria vascularis in Pendred syndrome mouse model. BMC Med. 2006;4:37.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Jamesdaniel S, Hu B, Kermany MH, Jiang H, Ding D, Coling D, Salvi R. Noise induced changes in the expression of p38/MAPK signaling proteins in the sensory epithelium of the inner ear. J Proteomics. 2011;75:410–24.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Jiang Z-G, Shi X-R, Guan B-C, Zhao H, Yang Y-Q. Dihydropyridines inhibit acetylcholine-induced hyperpolarization in cochlear artery via blockade of intermediate-conductance calcium-activated potassium channels. J Pharmacol Exp Ther. 2007;320:544–51.PubMedCrossRefGoogle Scholar
  80. Juhn SK, Rybak LP. Labyrinthine barriers and cochlear homeostasis. Acta Otolaryngol. 1981;91:529–34.PubMedCrossRefGoogle Scholar
  81. Juhn SK, Hunter BA, Odland RM. Blood-labyrinth barrier and fluid dynamics of the inner ear. Int Tinnitus J. 2001;7:72–83.PubMedGoogle Scholar
  82. Kamogashira T, Fujimoto C, Yamasoba T. Reactive oxygen species, apoptosis, and mitochondrial dysfunction in hearing loss. Biomed Res Int. 2015;2015:617207.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Karasawa T, Steyger PS. Intracellular mechanisms of aminoglycoside-induced cytotoxicity. Integr Biol. 2011;3:879–86.CrossRefGoogle Scholar
  84. Karasawa T, Wang Q, Fu Y, Cohen DM, Steyger PS. TRPV4 enhances the cellular uptake of aminoglycoside antibiotics. J Cell Sci. 2008;121:2871–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kaur T, Mukherjea D, Sheehan K, Jajoo S, Rybak LP, Ramkumar V. Short interfering RNA against STAT1 attenuates cisplatin-induced ototoxicity in the rat by suppressing inflammation. Cell Death Dis. 2011;2:e180.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Kellerhals B. Acoustic trauma and cochlear microcirculation. An experimental and clinical study on pathogenesis and treatment of inner ear lesions after acute noise exposure. Adv Otorhinolaryngol. 1972;18:91.PubMedGoogle Scholar
  87. 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;33:51–6.PubMedCrossRefGoogle Scholar
  88. Kim SH, Kim JY, Lee HJ, Gi M, Kim BG, Choi JY. Autoimmunity as a candidate for the etiopathogenesis of Meniere’s disease: detection of autoimmune reactions and diagnostic biomarker candidate. PLoS One. 2014;9(10):e111039.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kim JM, Hong K-S, Song WK, Bae D, Hwang I-K, Kim JS, Chung H-M. Perivascular progenitor cells derived from human embryonic stem cells exhibit functional characteristics of pericytes and improve the retinal vasculature in a rodent model of diabetic retinopathy. Stem Cells Transl Med. 2016;5:1268–76.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Kohn S, Nir I, Fradis M, Podoshin L, David YB, Zidan J, Robinson E. Toxic effects of cisplatin alone and in combination with gentamicin in stria vascularis of guinea pigs. Laryngoscope. 1991;101:709–16.PubMedCrossRefGoogle Scholar
  91. Komune S, Nakagawa T, Hisashi K, Kimituki T, Uemura T. Movement of monovalent ions across the membranes of marginal cells of the stria vascularis in the guinea pig cochlea. ORL J Otorhinolaryngol Relat Spec. 1993;55:61–7.PubMedCrossRefGoogle Scholar
  92. Koo J-W, Wang Q, Steyger PS. Infection-mediated vasoactive peptides modulate cochlear uptake of fluorescent gentamicin. Audiol Neurootol. 2011;16:347–58.PubMedCrossRefGoogle Scholar
  93. Kujawa SG, Liberman MC. Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res. 2015;330:191–9.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Kurata N, Schachern PA, Paparella MM, Cureoglu S. Histopathologic evaluation of vascular findings in the cochlea in patients with presbycusis. JAMA Otolaryngol Head Neck Surg. 2016;142(2):173–8.PubMedCrossRefGoogle Scholar
  95. Lamm K, Arnold W. Successful treatment of noise-induced cochlear ischemia, hypoxia, and hearing loss. Ann N Y Acad Sci. 1999;884:233–48.PubMedCrossRefGoogle Scholar
  96. Lamm K, Arnold W. The effect of blood flow promoting drugs on cochlear blood flow, perilymphatic pO(2) and auditory function in the normal and noise-damaged hypoxic and ischemic guinea pig inner ear. Hear Res. 2000;141:199–219.PubMedCrossRefGoogle Scholar
  97. Laurell G, Viberg A, Teixeira M, Sterkers O, Ferrary E. Blood-perilymph barrier and ototoxicity: an in vivo study in the rat. Acta Otolaryngol. 2000;120:796–803.PubMedCrossRefGoogle Scholar
  98. Le Prell CG, Dolan DF, Schacht J, Miller JM, Lomax MI, Altschuler RA. Pathways for protection from noise induced hearing loss. Noise Health. 2003;5:1–17.PubMedGoogle Scholar
  99. Le Prell CG, Hughes LF, Miller JM. Free radical scavengers vitamins A, C, and E plus magnesium reduce noise trauma. Free Radic Biol Med. 2007a;42:1454–63.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Le Prell CG, Yamashita D, Minami SB, Yamasoba T, Miller JM. Mechanisms of noise-induced hearing loss indicate multiple methods of prevention. Hear Res. 2007b;226:22–43.PubMedCrossRefGoogle Scholar
  101. Li H, Kachelmeier A, Furness DN, Steyger PS. Local mechanisms for loud sound-enhanced aminoglycoside entry into outer hair cells. Front Cell Neurosci. 2015;9:130.PubMedPubMedCentralGoogle Scholar
  102. Liberman LD, Suzuki J, Liberman MC. Erratum to: dynamics of cochlear synaptopathy after acoustic overexposure. J Assoc Res Otolaryngol. 2015;16:221.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Lin DW, Trune DR. Breakdown of stria vascularis blood-labyrinth barrier in C3H/lpr autoimmune disease mice. Otolaryngol Head Neck Surg. 1997;117:530–4.PubMedCrossRefGoogle Scholar
  104. Liu H, Ren J-G, Cooper WL, Hawkins CE, Cowan MR, Tong PY. Identification of the antivasopermeability effect of pigment epithelium-derived factor and its active site. Proc Natl Acad Sci U S A. 2004;101:6605–10.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Liu JT, Chen YL, Chen WC, Chen HY, Lin YW, Wang SH, Man KM, Wan HM, Yin WH, Liu PL. Role of pigment epithelium-derived factor in stem/progenitor cell-associated neovascularization. J Biomed Biotechnol. 2012a;2012:871272.PubMedPubMedCentralGoogle Scholar
  106. Liu S, Agalliu D, Yu C, Fisher M. The role of pericytes in blood-brain barrier function and stroke. Curr Pharm Des. 2012b;18:3653–62.PubMedCrossRefGoogle Scholar
  107. Maddox DE, Shibata S, Goldstein IJ. Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. Proc Natl Acad Sci U S A. 1982;79:166–70.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Marcus DC, Marcus NY, Thalmann R. Changes in cation contents of stria vascularis with ouabain and potassium-free perfusion. Hear Res. 1981;4:149–60.PubMedCrossRefGoogle Scholar
  109. Meech RP, Campbell KC, Hughes LP, Rybak LP. A semiquantitative analysis of the effects of cisplatin on the rat stria vascularis. Hear Res. 1998;124:44–59.PubMedCrossRefGoogle Scholar
  110. Miettinen S, Laurell G, Andersson A, Johansson R, Laurikainen E. Blood flow-independent accumulation of cisplatin in the guinea pig cochlea. Acta Otolaryngol. 1997;117:55–60.PubMedCrossRefGoogle Scholar
  111. Mijovic T, Zeitouni A, Colmegna I. Autoimmune sensorineural hearing loss: the otology–rheumatology interface. Rheumatology. 2013;52(5):780–9. https://doi.org/10.1093/rheumatology/ket009.CrossRefPubMedGoogle Scholar
  112. Miller JM, Brown JN, Schacht J. 8-iso-prostaglandin F2α, a product of noise exposure, reduces inner ear blood flow. Audiol Neurotol. 2003;8:207–21.CrossRefGoogle Scholar
  113. Miller JM, Dengerink H. Control of inner ear blood flow. Am J Otolaryngol. 1988;9:302–16.PubMedCrossRefGoogle Scholar
  114. Misrahy G, Shinabarger E, Arnold J. Changes in cochlear endolymphatic oxygen availability, action potential, and microphonics during and following asphyxia, hypoxia, and exposure to loud sounds. J Acoust Soc Am. 1958;30:701–4.CrossRefGoogle Scholar
  115. Miyao M, Firestein GS, Keithley EM. Acoustic trauma augments the cochlear immune response to antigen. Laryngoscope. 2008;118:1801–8.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Moon S-K, Moon S-K, Park R, Moon S-K, Park R, Lee H-Y, Nam G-J, Cha K, Andalibi A, Lim DJ. Spiral ligament fibrocytes release chemokines in response to otitis media pathogens. Acta Otolaryngol. 2006;126:564–9.PubMedCrossRefGoogle Scholar
  117. Mouadeb DA, Ruckenstein MJ. Antiphospholipid inner ear syndrome. Laryngoscope. 2005;115:879–83.PubMedCrossRefGoogle Scholar
  118. Mudar RA, Husain FT. Neural alterations in acquired age-related hearing loss. Front Psychol. 2016;7:828.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Murillo-Cuesta S, Contreras J, Zurita E, Cediel R, Cantero M, Varela-Nieto I, Montoliu L. Melanin precursors prevent premature age-related and noise-induced hearing loss in albino mice. Pigment Cell Melanoma Res. 2010;23:72–83.PubMedCrossRefGoogle Scholar
  120. Nair TS, Kozma KE, Hoefling NL, Kommareddi PK, Ueda Y, Gong T-W, Lomax MI, Lansford CD, Telian SA, Satar B. Identification and characterization of choline transporter-like protein 2, an inner ear glycoprotein of 68 and 72 kDa that is the target of antibody-induced hearing loss. J Neurosci. 2004;24:1772–9.PubMedCrossRefGoogle Scholar
  121. Nakai Y, Masutani H, Moriguchi M, Matsunaga K, Kato A, Maeda H. Microvasculature of normal and hydropic labyrinth. Scanning Microsc. 1992;6:1097–103; discussion 1103–4.PubMedGoogle Scholar
  122. Nakamoto T, Mikuriya T, Sugahara K, Hirose Y, Hashimoto T, Shimogori H, Takii R, Nakai A, Yamashita H. Geranylgeranylacetone suppresses noise-induced expression of proinflammatory cytokines in the cochlea. Auris Nasus Larynx. 2012;39:270–4.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Nakashima T. Autoregulation of cochlear blood flow. Nagoya J Med Sci. 1999;62:1–9.PubMedGoogle Scholar
  124. Nakashima T, Suzuki T, Iwagaki T, Hibi T. Effects of anterior inferior cerebellar artery occlusion on cochlear blood flow–a comparison between laser-Doppler and microsphere methods. Hear Res. 2001;162:85–90.PubMedCrossRefGoogle Scholar
  125. Nakashima T, Naganawa S, Sone M, Tominaga M, Hayashi H, Yamamoto H, Liu X, Nuttall AL. Disorders of cochlear blood flow. Brain Res Rev. 2003;43:17–28.PubMedCrossRefGoogle Scholar
  126. Neng L, Zhang F, Kachelmeier A, Shi X. Endothelial cell, pericyte, and perivascular resident macrophage-type melanocyte interactions regulate cochlear intrastrial fluid–blood barrier permeability. J Assoc Res Otolaryngol. 2013a;14:175–85.PubMedCrossRefGoogle Scholar
  127. Neng L, Zhang W, Hassan A, Zemla M, Kachelmeier A, Fridberger A, Auer M, Shi X. Isolation and culture of endothelial cells, pericytes and perivascular resident macrophage-like melanocytes from the young mouse ear. Nat Protoc. 2013b;8:709–20.PubMedPubMedCentralCrossRefGoogle Scholar
  128. Neng L, Zhang J, Yang J, Zhang F, Lopez IA, Dong M, Shi X. Structural changes in thestrial blood–labyrinth barrier of aged C57BL/6 mice. Cell Tissue Res. 2015;361(3):685–96.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Nuttall AL. Techniques for the observation and measurement of red blood cell velocity in vessels of the guinea pig cochlea. Hear Res. 1987;27:111–9.PubMedCrossRefGoogle Scholar
  130. Nuttall AL. Sound-induced cochlear ischemia/hypoxia as a mechanism of hearing loss. Noise Health. 1999;2:17.PubMedGoogle Scholar
  131. Nuttall AL, Lawrence M. Endocochlear potential and scala media oxygen tension during partial anoxia. Am J Otolaryngol. 1980;1:147–53.PubMedCrossRefGoogle Scholar
  132. O’Farrell FM, Attwell D. A role for pericytes in coronary no-reflow. Nat Rev Cardiol. 2014;11(7):427–32.PubMedCrossRefGoogle Scholar
  133. O’Malley JT, Nadol JB Jr, McKenna MJ. Anti CD163+, Iba1+, and CD68+ cells in the adult human inner ear: normal distribution of an unappreciated class of macrophages/microglia and implications for inflammatory otopathology in humans. Otol Neurotol. 2016;37:99–108.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Oberman B, Patel V, Cureoglu S, Isildak H. The aetiopathologies of Ménière’s disease: a contemporary review. Acta Otorhinolaryngol Ital. 2017;37(4):250–63.PubMedPubMedCentralGoogle Scholar
  135. Oh G-S, Kim H-J, Choi J-H, Shen A, Kim C-H, Kim S-J, Shin S-R, Hong S-H, Kim Y, Park C. Activation of lipopolysaccharide–TLR4 signaling accelerates the ototoxic potential of cisplatin in mice. J Immunol. 2011;186:1140–50.CrossRefPubMedGoogle Scholar
  136. Ohlemiller KK, Gagnon PM. Genetic dependence of cochlear cells and structures injured by noise. Hear Res. 2007;224:34–50.PubMedPubMedCentralCrossRefGoogle Scholar
  137. Ohlemiller KK, Rice MER, Gagnon PM. Strial microvascular pathology and age-associated endocochlear potential decline in NOD congenic mice. Hear Res. 2008;244:85–97.PubMedPubMedCentralCrossRefGoogle Scholar
  138. Ohlemiller KK, Rybak Rice ME, Lett JM, Gagnon PM. Absence of strial melanin coincides with age-associated marginal cell loss and endocochlear potential decline. Hear Res. 2009;249:1–14.PubMedCrossRefGoogle Scholar
  139. Oishi N, Talaska AE, Schacht J. Ototoxicity in dogs and cats. Vet Clin North Am Small Anim Pract. 2012;42:1259–71.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Ottaviani F, Cadoni G, Marinelli L, Fetoni AR, De Santis A, Romito A, Vulpiani P, Manna R. Anti-endothelial autoantibodies in patients with sudden hearing loss. Laryngoscope. 1999;109:1084–7.PubMedCrossRefGoogle Scholar
  141. Pender D. Endolymphatic hydrops and Ménière’s disease: a lesion meta-analysis. J Laryngol Otol. 2014;128:859–65.PubMedCrossRefGoogle Scholar
  142. Penha R, O’Neill M, Goyri ONJ, Esperanca PJ. Ultrastructural aspects of the microvasculature of the cochlea: the internal spiral network. Otolaryngol Head Neck Surg. 1999;120:725.PubMedCrossRefGoogle Scholar
  143. Peppiatt CM, Howarth C, Mobbs P, Attwell D. Bidirectional control of CNS capillary diameter by pericytes. Nature. 2006;443:700–4.PubMedPubMedCentralCrossRefGoogle Scholar
  144. Pfister F, Feng Y, Vom Hagen F, Hoffmann S, Molema G, Hillebrands J-L, Shani M, Deutch U, Hammes H-P. Pericyte migration: a novel mechanism of pericyte loss in experimental diabetic retinopathy. Diabetes. 2008;57:2495–502.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Plonka P, Passeron T, Brenner M, Tobin D, Shibahara S, Thomas A, Slominski A, Kadekaro A, Hershkovitz D, Peters E. What are melanocytes really doing all day long…? Exp Dermatol. 2009;18:799–819.PubMedCrossRefGoogle Scholar
  146. Prat A, Biernacki K, Wosik K, Antel JP. Glial cell influence on the human blood-brain barrier. Glia. 2001;36:145–55.PubMedCrossRefGoogle Scholar
  147. Prazma J, Carrasco VN, Butler B, Waters G, Anderson T, Pillsbury HC. Cochlear microcirculation in young and old gerbils. Arch Otolaryngol Head Neck Surg. 1990;116:932.PubMedCrossRefPubMedCentralGoogle Scholar
  148. Qu C, Liang F, Smythe NM, Schulte BA. Identification of ClC-2 and CIC-K2 chloride channels in cultured rat type IV spiral ligament fibrocytes. J Assoc Res Otolaryngol. 2007;8:205–19.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Quaegebeur A, Segura I, Carmeliet P. Pericytes: blood-brain barrier safeguards against neurodegeneration? Neuron. 2010;68:321–3.PubMedCrossRefGoogle Scholar
  150. Quintanilla-Dieck L, Larrain B, Trune D, Steyger PS. Effect of systemic lipopolysaccharide-induced inflammation on cytokine levels in the murine cochlea: a pilot study. Otolaryngol Head Neck Surg. 2013. https://doi.org/10.1177/0194599813491712.
  151. Quirk W, Laurikainen E, Avinash G, Nuttall A, Miller J. The role of endothelin on the regulation of cochlear blood flow. Assoc Res Otolaryngol. 1992;15:37.Google Scholar
  152. Rehm HL, Zhang D-S, Brown MC, Burgess B, Halpin C, Berger W, Morton CC, Corey DP, Chen Z-Y. Vascular defects and sensorineural deafness in a mouse model of Norrie disease. J Neurosci. 2002;22:4286–92.PubMedCrossRefGoogle Scholar
  153. Reif R, Zhi Z, Dziennis S, Nuttall AL, Wang RK. Changes in cochlear blood flow in mice due to loud sound exposure measured with Doppler optical microangiography and laser Doppler flowmetry. Quant Imaging Med Surg. 2013;3:235.PubMedPubMedCentralGoogle Scholar
  154. Ruckenstein MJ, Hu L. Antibody deposition in the stria vascularis of the MRL-Fas lpr mouse. Hear Res. 1999;127:137–42.PubMedPubMedCentralCrossRefGoogle Scholar
  155. Rybak LP, Ramkumar V. Ototoxicity. Kidney Int. 2007;72:931–5.PubMedCrossRefGoogle Scholar
  156. Rybak LP, Whitworth CA, Mukherjea D, Ramkumar V. Mechanisms of cisplatin-induced ototoxicity and prevention. Hear Res. 2007;226:157–67.PubMedPubMedCentralCrossRefGoogle Scholar
  157. Sakaguchi N, Spicer SS, Thomopoulos GN, Schulte BA. Immunoglobulin deposition in thickened basement membranes of aging strial capillaries. Hear Res. 1997a;109:83–91.PubMedCrossRefGoogle Scholar
  158. Sakaguchi N, Spicer SS, Thomopoulos GN, Schulte BA. Increased laminin deposition in capillaries of the stria vascularis of quiet-aged gerbils. Hear Res. 1997b;105:44–56.PubMedCrossRefGoogle Scholar
  159. Salt AN, Mleichar I, Thalmann R. Mechanisms of endocochlear potential generation by stria vascularis. Laryngoscope. 1987;97:984–91.PubMedCrossRefGoogle Scholar
  160. Sara S, Teh B, Friedland P. Bilateral sudden sensorineural hearing loss: review. J Laryngol Otol. 2014;128:S8–S15.PubMedCrossRefGoogle Scholar
  161. Sato E, Shick HE, Ransohoff RM, Hirose K. Repopulation of cochlear macrophages in murine hematopoietic progenitor cell chimeras: the role of CX3CR1. J Comp Neurol. 2008;506:930–42.PubMedPubMedCentralCrossRefGoogle Scholar
  162. Schacht J, Talaska AE, Rybak LP. Cisplatin and aminoglycoside antibiotics: hearing loss and its prevention. Anat Rec. 2012;295:1837–50.CrossRefGoogle Scholar
  163. Scheibe F, Haupt H, Ludwig C. Intensity-related changes in cochlear blood flow in the guinea pig during and following acoustic exposure. Eur Arch Otorhinolaryngol. 1993;250:281–5.PubMedPubMedCentralCrossRefGoogle Scholar
  164. Schulte BA, Schmiedt RA. Lateral wall Na, K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils. Hear Res. 1992;61:35–46.PubMedCrossRefGoogle Scholar
  165. Seidman MD, Quirk WS, Shirwany NA. Mechanisms of alterations in the microcirculation of the cochlea, ototoxicity: basic science and clinical applications. Ann N Y Acad Sci. 1999;884:226–32.PubMedPubMedCentralCrossRefGoogle Scholar
  166. Shaddock LC, Hamernik RP, Axelsson A. Cochlear vascular and sensorycell changes induced by elevated temperature and noise. Am J Otolaryngol. 1984;5:99–107.PubMedCrossRefGoogle Scholar
  167. Shepro D, Morel N. Pericyte physiology. FASEB J. 1993;7:1031–8.PubMedCrossRefGoogle Scholar
  168. Shi X. Cochlear pericyte responses to acoustic trauma and the involvement of hypoxia-inducible factor-1alpha and vascular endothelial growth factor. Am J Pathol. 2009;174:1692–704.PubMedPubMedCentralCrossRefGoogle Scholar
  169. Shi X. Resident macrophages in the cochlear blood-labyrinth barrier and their renewal via migration of bone-marrow-derived cells. Cell Tissue Res. 2010;342:21–30.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Shi X. Physiopathology of the cochlear microcirculation. Hear Res. 2011;282:10–24.PubMedPubMedCentralCrossRefGoogle Scholar
  171. Shi X. Pathophysiology of the cochlear intrastrial fluid-blood barrier (review). Hear Res. 2016;338:52–63.PubMedPubMedCentralCrossRefGoogle Scholar
  172. Shi X, Nuttall AL. The demonstration of nitric oxide in cochlear blood vessels in vivo and in vitro: the role of endothelial nitric oxide in venular permeability. Hear Res. 2002;172:73–80.PubMedCrossRefPubMedCentralGoogle Scholar
  173. Shi X, Nuttall AL. Upregulated iNOS and oxidative damage to the cochlear stria vascularis due to noise stress. Brain Res. 2003;967:1–10.CrossRefPubMedGoogle Scholar
  174. Shi X, Nuttall AL. Expression of adhesion molecular proteins in the cochlear lateral wall of normal and PARP-1 mutant mice. Hear Res. 2007;224:1–14.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Shi X, Han W, Yamamoto H, Tang W, Lin X, Xiu R, Trune DR, Nuttall AL. The cochlear pericytes. Microcirculation. 2008;15:515–29.PubMedPubMedCentralCrossRefGoogle Scholar
  176. Sims DE. Diversity within pericytes. Clin Exp Pharmacol Physiol. 2000;27:842–6.PubMedCrossRefPubMedCentralGoogle Scholar
  177. Slominski A. Neuroendocrine activity of the melanocyte. Exp Dermatol. 2009;18:760–3.PubMedPubMedCentralCrossRefGoogle Scholar
  178. Slominski A, Zmijewski MA, Pawelek J. L-tyrosine and L-dihydroxyphenylalanine as hormone-like regulators of melanocyte functions. Pigment Cell Melanoma Res. 2012;25:14–27.PubMedCrossRefPubMedCentralGoogle Scholar
  179. Spicer SS, Schulte BA. Differentiation of inner ear fibrocytes according to their ion transport related activity. Hear Res. 1991;56:53–64.PubMedPubMedCentralCrossRefGoogle Scholar
  180. 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;100:80–100.PubMedPubMedCentralCrossRefGoogle Scholar
  181. Spicer SS, Schulte BA. Spiral ligament pathology in quiet-aged gerbils. Hear Res. 2002;172:172–85.PubMedCrossRefGoogle Scholar
  182. Spicer SS, Schulte BA. Novel structures in marginal and intermediate cells presumably relate to functions of apical versus basal strial strata. Hear Res. 2005;200:87–101.PubMedCrossRefGoogle Scholar
  183. Spiess AC, Lang H, Schulte BA, Spicer S, Schmiedt RA. Effects of gap junction uncoupling in the gerbil cochlea. Laryngoscope. 2002;112:1635–41.PubMedCrossRefPubMedCentralGoogle Scholar
  184. Sprinzl G, Riechelmann H. Current trends in treating hearing loss in elderly people: a review of the technology and treatment options–a mini-review. Gerontology. 2010;56:351–8.PubMedCrossRefPubMedCentralGoogle Scholar
  185. Steel K, Barkway C. Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development. 1989;107:453–63.PubMedPubMedCentralGoogle Scholar
  186. Steel K, Davidson DR, Jackson I. TRP-2/DT, a new early melanoblast marker, shows that steel growth factor (c-kit ligand) is a survival factor. Development. 1992;115:1111–9.PubMedPubMedCentralGoogle Scholar
  187. Sulaimon SS, Kitchell BE. The biology of melanocytes. Vet Dermatol. 2003;14:57–65.PubMedCrossRefPubMedCentralGoogle Scholar
  188. Suzuki M, Yamasoba T, Kaga K. Development of the blood-labyrinth barrier in the rat. Hear Res. 1998;116:107–12.PubMedCrossRefPubMedCentralGoogle Scholar
  189. Suzuki M, Yamasoba T, Ishibashi T, Miller JM, Kaga K. Effect of noise exposure on blood–labyrinth barrier in guinea pigs. Hear Res. 2002;164:12–8.PubMedCrossRefPubMedCentralGoogle Scholar
  190. Tagaya M, Yamazaki M, Teranishi M, Naganawa S, Yoshida T, Otake H, Nakata S, Sone M, Nakashima T. Endolymphatic hydrops and blood–labyrinth barrier in Meniere’s disease. Acta Otolaryngol. 2011;131:474–9.PubMedCrossRefGoogle Scholar
  191. Takahashi M, Harris JP. Anatomic distribution and localization of immunocompetent cells in normal mouse endolymphatic sac. Acta Otolaryngol. 1988;106:409–16.PubMedCrossRefGoogle Scholar
  192. Tavanai E, Mohammadkhani G. Role of antioxidants in prevention of age-related hearing loss: a review of literature. Eur Arch Otorhinolaryngol. 2017;274(4):1821–34.PubMedCrossRefGoogle Scholar
  193. Thomopoulos GN, Spicer SS, Gratton MA, Schulte BA. Age-related thickening of basement membrane in stria vascularis capillaries. Hear Res. 1997;111:31–41.PubMedCrossRefGoogle Scholar
  194. Tornabene SV, Sato K, Pham L, Billings P, Keithley EM. Immune cell recruitment following acoustic trauma. Hear Res. 2006;222:115–24.PubMedPubMedCentralCrossRefGoogle Scholar
  195. Toubi E, Halas K, Ben-David J, Sabo E, Kessel A, Luntz M. Immune-mediated disorders associated with idiopathic sudden sensorineural hearing loss. Ann Otol Rhinol Laryngol. 2004;113:445–9.PubMedCrossRefGoogle Scholar
  196. Trowe M-O, Maier H, Schweizer M, Kispert A. Deafness in mice lacking the T-box transcription factor Tbx18 in otic fibrocytes. Development. 2008;135:1725–34.PubMedCrossRefGoogle Scholar
  197. Trune DR, Nguyen-Huynh A. Vascular pathophysiology in hearing disorders, Semin Hear. Thieme Medical Publishers; 2012. p. 242–50.PubMedPubMedCentralCrossRefGoogle Scholar
  198. Trune DR, Kempton JB, Mitchell CR, Hefeneider SH. Failure of elevated heat shock protein 70 antibodies to alter cochlear function in mice. Hear Res. 1998;116:65–70.PubMedCrossRefGoogle Scholar
  199. Ueda S, Yamagishi S-I, Okuda S. Anti-vasopermeability effects of PEDF in retinal-renal disorders. Curr Mol Med. 2010;10:279–83.PubMedCrossRefGoogle Scholar
  200. Varol C, Mildner A, Jung S. Macrophages: development and tissue specialization. Annu Rev Immunol. 2015;33:643–75.PubMedCrossRefGoogle Scholar
  201. Wakaoka T, Motohashi T, Hayashi H, Kuze B, Aoki M, Mizuta K, Kunisada T, Ito Y. Tracing Sox10-expressing cells elucidates the dynamic development of the mouse inner ear. Hear Res. 2013;302:17–25.PubMedCrossRefGoogle Scholar
  202. Wang Y, Hirose K, Liberman MC. Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J Assoc Res Otolaryng. 2002;3:248–68.CrossRefGoogle Scholar
  203. Wang Q, Steyger PS. Trafficking of systemic fluorescent gentamicin into the cochlea and hair cells. J Assoc Res Otolaryngol. 2009;10:205–19.PubMedPubMedCentralCrossRefGoogle Scholar
  204. Wangemann P. Cochlear blood flow regulation. Adv Otorhinolaryngol. 2002;59:51–7.PubMedGoogle Scholar
  205. Wangemann P, Liu J. Osmotic water permeability of capillaries from the isolated spiral ligament: new in-vitro techniques for the study of vascular permeability and diameter. Hear Res. 1996;95:49–56.PubMedCrossRefGoogle Scholar
  206. Wong ML, Young JS, Nilaver G, Morton JI, Trune DR. Cochlear IgG in the C3H/lpr autoimmune strain mouse. Hear Res. 1992;59:93–100.PubMedCrossRefGoogle Scholar
  207. Wood MB, Zuo J. The contribution of immune infiltrates to ototoxicity and cochlear hair cell loss. Front Cell Neurosci. 2017;11:106.PubMedPubMedCentralCrossRefGoogle Scholar
  208. Wu T, Marcus DC. Age-related changes in cochlear endolymphatic potassium and potential in CD-1 and CBA/CaJ mice. J Assoc Res Otolaryngol. 2003;4:353–62.PubMedPubMedCentralCrossRefGoogle Scholar
  209. Yamamoto H, Omelchenko I, Shi X, Nuttall AL. The influence of NF-kappaB signal-transduction pathways on the murine inner ear by acoustic overstimulation. J Neurosci Res. 2009;87:1832–40.PubMedPubMedCentralCrossRefGoogle Scholar
  210. Yamane H, Nakai Y, Konishi K, Sakamoto H, Matsuda Y, Iguchi H. Strial circulation impairment due to acoustic trauma. Acta Otolaryngol. 1991;111:85–93.PubMedCrossRefGoogle Scholar
  211. Yang Y, Dai M, Wilson TM, Omelchenko I, Klimek JE, Wilmarth PA, David LL, Nuttall AL, Gillespie PG, Shi X. Na+/K+-ATPase alpha1 identified as an abundant protein in the blood-labyrinth barrier that plays an essential role in the barrier integrity. PLoS One. 2011;6:e16547.PubMedPubMedCentralCrossRefGoogle Scholar
  212. Yehudai D, Shoenfeld Y, Toubi E. The autoimmune characteristics of progressive or sudden sensorineural hearing loss. Autoimmunity. 2006;39:153–8.PubMedCrossRefGoogle Scholar
  213. Yorgason JG, Luxford W, Kalinec F. In vitro and in vivo models of drug ototoxicity: studying the mechanisms of a clinical problem. Expert Opin Drug Metab Toxicol. 2011;7:1521–34.PubMedCrossRefGoogle Scholar
  214. Yoshida N, Kristiansen A, Liberman MC. Heat stress and protection from permanent acoustic injury in mice. J Neurosci. 1999;19:10116–24.PubMedCrossRefGoogle Scholar
  215. Young J, Morton J, Nilaver G, Trune D. Distribution of IgG in the inner ear of C3H/lpr autoimmune disease mice. Abst Assoc Res Otolaryngol. 1988;225.Google Scholar
  216. Zhang W, Dai M, Fridberger A, Hassan A, Degagne J, Neng L, Zhang F, He W, Ren T, Trune D, Auer M, Shi X. Perivascular-resident macrophage-like melanocytes in the inner ear are essential for the integrity of the intrastrial fluid-blood barrier. Proc Natl Acad Sci U S A. 2012;109:10388–93.PubMedPubMedCentralCrossRefGoogle Scholar
  217. Zhang F, Dai M, Neng L, Zhang JH, Zhi Z, Fridberger A, Shi X. Perivascular macrophage-like melanocyte responsiveness to acoustic trauma—a salient feature of strial barrier associated hearing loss. FASEB J. 2013;27:3730–40.PubMedPubMedCentralCrossRefGoogle Scholar
  218. Zhang J, Chen S, Hou Z, Cai J, Dong M, Shi X. Lipopolysaccharide-induced middle ear inflammation disrupts the cochlear intra-strial fluid-blood barrier through down-regulation of tight junction proteins. PLoS One. 2015;10(3):e0122572.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Oregon Health & Science UniversityPortlandUSA

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