Endotoxemia-mediated inflammation potentiates aminoglycoside-induced ototoxicity

Science Translational Medicine

Volumn 7, Issue 298, 2015, Pages

  Koo, Ja Won ^a,b   Quintanilla Dieck, Lourdes ^a   Jiang, Meiyan ^a   Liu, Jianping ^a,c   Urdang, Zachary D ^a   Allensworth, Jordan J ^a   Cross, Campbell P ^a   Li, Hongzhe ^a   Steyger, Peter S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Seoul National University Bundang Hospital   (South Korea)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL2 CHEMOKINE; GENTAMICIN; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; KANAMYCIN; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; AMINOGLYCOSIDE; AUTACOID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY THRESHOLD SHIFT; BLOOD VESSEL PERMEABILITY; CELL DEATH; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG UPTAKE; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE EXPRESSION; GLOMERULUS FILTRATION RATE; HEARING IMPAIRMENT; INFLAMMATION; KIDNEY FAILURE; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; MOUSE; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SEPSIS; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; COMPLICATION; ENDOTOXEMIA; HEARING LOSS, SENSORINEURAL; HUMAN; METABOLISM; PATHOPHYSIOLOGY;

AMINOGLYCOSIDES; ANIMALS; ENDOTOXEMIA; HEARING LOSS, SENSORINEURAL; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MICE; TOLL-LIKE RECEPTOR 4;

EID: 84934782309     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac5546     Document Type: Article

References (88)

1. D. W. Kimberlin, Meningitis in the neonate. Curr. Treat. Options Neurol. 4, 239-248 (2002).
2. E. A. Radigan, N. A. Gilchrist, M. A. Miller, Management of aminoglycosides in the intensive care unit. J. Intensive Care Med. 25, 327-342 (2010).
3. A. G. Cheng, P. R. Johnston, J. Luz, A. Uluer, B. Fligor, G. R. Licameli, M. A. Kenna, D. T. Jones, Sensorineural hearing loss in patients with cystic fibrosis. Otolaryngol. Head Neck Surg. 141, 86-90 (2009).
4. D. M. Pillers, M. R. Schleiss, Gentamicin in the clinical setting. Volta Rev. 105, 205-210 (2005).
5. A. Erenberg, J. Lemons, C. Sia, D. Trunkel, P. Ziring, Newborn and infant hearing loss: Detection and intervention. Task Force on Newborn and Infant Hearing. Pediatrics 103, 527-530 (1999).
6. M. R. Järvelin, E. Mäki-Torkko, M. J. Sorri, P. T. Rantakallio, Effect of hearing impairment on educational outcomes and employment up to the age of 25 years in northern Finland. Br. J. Audiol. 31, 165-175 (1997).
7. C. R. Kennedy, D. C. McCann, M. J. Campbell, C. M. Law, M. Mullee, S. Petrou, P. Watkin, S. Worsfold, H. M. Yuen, J. Stevenson, Language ability after early detection of permanent childhood hearing impairment. N. Engl. J. Med. 354, 2131-2141 (2006).
8. L. Schroeder, S. Petrou, C. Kennedy, D. McCann, C. Law, P. M. Watkin, S. Worsfold, H. M. Yuen, The economic costs of congenital bilateral permanent childhood hearing impairment. Pediatrics 117, 1101-1112 (2006).
9. F. R. Lin, L. Ferrucci, E. J. Metter, Y. An, A. B. Zonderman, S. M. Resnick, Hearing loss and cognition in the Baltimore Longitudinal Study of Aging. Neuropsychology 25, 763-770 (2011).
10. H. Li, P. S. Steyger, Systemic aminoglycosides are trafficked via endolymph into cochlear hair cells. Sci. Rep. 1, 159 (2011).
11. A. Alharazneh, L. Luk, M. Huth, A. Monfared, P. S. Steyger, A. G. Cheng, A. J. Ricci, Functional hair cell mechanotransducer channels are required for aminoglycoside ototoxicity. PLOS One 6, e22347 (2011).
12. W. Marcotti, S. M. van Netten, C. J. Kros, The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels. J. Physiol. 567, 505-521 (2005).
13. Q. Wang, P. S. Steyger, Trafficking of systemic fluorescent gentamicin into the cochlea and hair cells. J. Assoc. Res. Otolaryngol. 10, 205-219 (2009).
14. A. M. Butt, Effect of inflammatory agents on electrical resistance across the blood-brain barrier in pial microvessels of anaesthetized rats. Brain Res. 696, 145-150 (1995).
15. N. J. Abbott, L. Rönnbäck, E. Hansson, Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53 (2006).
16. N. Tsao, H. P. Hsu, C. M. Wu, C. C. Liu, H. Y. Lei, Tumour necrosis factor-a causes an increase in blood-brain barrier permeability during sepsis. J. Med. Microbiol. 50, 812-821 (2001).
17. J. W. Koo, Q. Wang, P. S. Steyger, Infection-mediated vasoactive peptides modulate cochlear uptake of fluorescent gentamicin. Audiol. Neurootol. 16, 347-358 (2011).
18. K. Hirose, S. Z. Li, K. K. Ohlemiller, R. M. Ransohoff, Systemic lipopolysaccharide induces cochlear inflammation and exacerbates the synergistic ototoxicity of kanamycin and furosemide. J. Assoc. Res. Otolaryngol. 15, 555-570 (2014).
19. D. G. Remick, D. E. Newcomb, G. L. Bolgos, D. R. Call, Comparison of the mortality and inflammatory response of two models of sepsis: Lipopolysaccharide vs. cecal ligation and puncture. Shock 13, 110-116 (2000).
20. H. Li, Q. Wang, P. S. Steyger, Acoustic trauma increases cochlear and hair cell uptake of gentamicin. PLOS One 6, e19130 (2011).
21. C. F. Dai, D. Mangiardi, D. A. Cotanche, P. S. Steyger, Uptake of fluorescent gentamicin by vertebrate sensory cells in vivo. Hear. Res. 213, 64-78 (2006).
22. C. F. Dai, P. S. Steyger, A systemic gentamicin pathway across the stria vascularis. Hear. Res. 235, 114-124 (2008).
23. Q. Wang, A. Kachelmeier, P. S. Steyger, Competitive antagonism of fluorescent gentamicin uptake in the cochlea. Hear. Res. 268, 250-259 (2010).
24. K. Balogh Jr., F. Hiraide, D. Ishii, Distribution of radioactive dihydrostreptomycin in the cochlea. An autoradiographic study. Ann. Otol. Rhinol. Laryngol. 79, 641-652 (1970).
25. S. Imamura, J. C. Adams, Distribution of gentamicin in the guinea pig inner ear after local or systemic application. J. Assoc. Res. Otolaryngol. 4, 176-195 (2003).
26. G. P. Richardson, A. Forge, C. J. Kros, J. Fleming, S. D. Brown, K. P. Steel, Myosin VIIA is required for aminoglycoside accumulation in cochlear hair cells. J. Neurosci. 17, 9506-9519 (1997).
27. W. J. Wu, S. H. Sha, J. D. McLaren, K. Kawamoto, Y. Raphael, J. Schacht, Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear. Res. 158, 165-178 (2001).
28. A. Forge, J. Schacht, Aminoglycoside antibiotics. Audiol. Neurootol. 5, 3-22 (2000).
29. J. J. Boffa, W. J. Arendshorst, Maintenance of renal vascular reactivity contributes to acute renal failure during endotoxemic shock. J. Am. Soc. Nephrol. 16, 117-124 (2005).
30. I. Berczi, L. Bertók, T. Bereznai, Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can. J. Microbiol. 12, 1070-1071 (1966).
31. M. S. Exton, Infection-induced anorexia: Active host defence strategy. Appetite 29, 369-383 (1997).
32. S. Studena, J. Martinkova, D. Slizova, O. Krs, M. Senkerik, D. Springer, J. Chládek, A rat model of early sepsis: Relationships between gentamicin pharmacokinetics and systemic and renal effects of bacterial lipopolysaccharide combined with interleukin-2. Biol. Pharm. Bull. 35, 1703-1710 (2012).
33. R. J. Lee, S. Wang, M. J. Turk, P. S. Low, The effects of pH and intraliposomal buffer strength on the rate of liposome content release and intracellular drug delivery. Biosci. Rep. 18, 69-78 (1998).
34. T. Nakamoto, Y. Shiba, C. Hirono, M. Sugita, K. Takemoto, Y. Iwasa, Y. Akagawa, Carbacholinduced fluid movement through methazolamide-sensitive bicarbonate production in rat parotid intralobular ducts: Quantitative analysis of fluorescence images using fluorescent dye sulforhodamine under a confocal laser scanning microscope. Eur. J. Cell Biol. 81, 497-504 (2002).
35. D. W. Lin, D. R. Trune, Breakdown of stria vascularis blood-labyrinth barrier in C3H/lpr autoimmune disease mice. Otolaryngol. Head Neck Surg. 117, 530-534 (1997).
36. P. A. Stewart, E. M. Hayakawa, Interendothelial junctional changes underlie the developmental 'tightening' of the blood-brain barrier. Brain Res. 429, 271-281 (1987).
37. F. P. Miles, A. L. Nuttall, In vivo capillary diameters in the stria vascularis and spiral ligament of the guinea pig cochlea. Hear. Res. 33, 191-200 (1988).
38. R. R. Taylor, G. Nevill, A. Forge, Rapid hair cell loss: A mouse model for cochlear lesions. J. Assoc. Res. Otolaryngol. 9, 44-64 (2008).
39. J. R. Meyers, R. B. MacDonald, A. Duggan, D. Lenzi, D. G. Standaert, J. T. Corwin, D. P. Corey, Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J. Neurosci. 23, 4054-4065 (2003).
40. I. L. Calil, A. C. Zarpelon, A. T. Guerrero, J. C. Alves-Filho, S. H. Ferreira, F. Q. Cunha, T. M. Cunha, W. A. Verri Jr., Lipopolysaccharide induces inflammatory hyperalgesia triggering a TLR4/MyD88- dependent cytokine cascade in the mice paw. PLOS One 9, e90013 (2014).
41. J. E. Juskewitch, B. E. Knudsen, J. L. Platt, K. A. Nath, K. L. Knutson, G. J. Brunn, J. P. Grande, LPS-induced murine systemic inflammation is driven by parenchymal cell activation and exclusively predicted by early MCP-1 plasma levels. Am. J. Pathol. 180, 32-40 (2012).
42. M. Bosmann, N. F. Russkamp, P. A. Ward, Fingerprinting of the TLR4-induced acute inflammatory response. Exp. Mol. Pathol. 93, 319-323 (2012).
43. C. J. MacArthur, D. A. Pillers, J. Pang, J. B. Kempton, D. R. Trune, Altered expression of middle and inner ear cytokines in mouse otitis media. Laryngoscope 121, 365-371 (2011).
44. D. R. Trune, B. E. Larrain, F. A. Hausman, J. B. Kempton, C. J. MacArthur, Simultaneous measurement of multiple ear proteins with multiplex ELISA assays. Hear. Res. 275, 1-7 (2011).
45. S. Rivest, Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 9, 429-439 (2009).
46. J. J. Allensworth, S. R. Planck, J. T. Rosenbaum, H. L. Rosenzweig, Investigation of the differential potentials of TLR agonists to elicit uveitis in mice. J. Leukoc. Biol. 90, 1159-1166 (2011).
47. A. Poltorak, X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, B. Beutler, Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282, 2085-2088 (1998).
48. R. B. Yang, M. R. Mark, A. Gray, A. Huang, M. H. Xie, M. Zhang, A. Goddard, W. I. Wood, A. L. Gurney, P. J. Godowski, Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395, 284-288 (1998).
49. T. Matt, C. L. Ng, K. Lang, S. H. Sha, R. Akbergenov, D. Shcherbakov, M. Meyer, S. Duscha, J. Xie, S. R. Dubbaka, D. Perez-Fernandez, A. Vasella, V. Ramakrishnan, J. Schacht, E. C. Böttger, Dissociation of antibacterial activity and aminoglycoside ototoxicity in the 4-monosubstituted 2-deoxystreptamine apramycin. Proc. Natl. Acad. Sci. U.S.A. 109, 10984-10989 (2012).
50. S. Roy, M. M. Ryals, A. B. Van den Bruele, T. S. Fitzgerald, L. L. Cunningham, Sound preconditioning therapy inhibits ototoxic hearing loss in mice. J. Clin. Invest. 123, 4945-4949 (2013).
51. M. W. Yung, Intratympanic ototoxicity: Influence of post-injection survival period. J. Laryngol. Otol. 101, 1011-1019 (1987).
52. S. L. McFadden, D. Ding, R. Salvi, Anatomical, metabolic and genetic aspects of age-related hearing loss in mice. Audiology 40, 313-321 (2001).
53. D. H. Darrow, E. M. Keithley, J. P. Harris, Effects of bacterial endotoxin applied to the guinea pig cochlea. Laryngoscope 102, 683-688 (1992).
54. C. S. Kim, H. J. Kim, Auditory brain stem response changes after application of endotoxin to the round window membrane in experimental otitis media. Otolaryngol. Head Neck Surg. 112, 557-565 (1995).
55. K. R. Henry, R. A. Chole, M. D. McGinn, D. P. Frush, Increased ototoxicity in both young and old mice. Arch. Otolaryngol. 107, 92-95 (1981).
56. C. L. McClure, Common infections in the elderly. Am. Fam. Physician 45, 2691-2698 (1992).
57. F. A. Manian, W. J. Stone, R. H. Alford, Adverse antibiotic effects associated with renal insufficiency. Rev. Infect. Dis. 12, 236-249 (1990).
58. R. H. Mathog, W. J. Klein Jr., Ototoxicity of ethacrynic acid and aminoglycoside antibiotics in uremia. N. Engl. J. Med. 280, 1223-1224 (1969).
59. N. Fischel-Ghodsian, Genetic factors in aminoglycoside toxicity. Ann. N. Y. Acad. Sci. 884, 99-109 (1999).
60. A. F. Ryan, R. C. Bone, Potentiation of kanamycin ototoxicity by a history of noise exposure. Otolaryngology 86, ORL-125-ORL-128 (1978).
61. G. Kaplanski, B. Granel, T. Vaz, J. M. Durand, Jarisch-Herxheimer reaction complicating the treatment of chronic Q fever endocarditis: Elevated TNFα and IL-6 serum levels. J. Infect. 37, 83-84 (1998).
62. J. L. Shenep, K. A. Mogan, Kinetics of endotoxin release during antibiotic therapy for experimental gram-negative bacterial sepsis. J. Infect. Dis. 150, 380-388 (1984).
63. M. Fujioka, H. Okano, K. Ogawa, Inflammatory and immune responses in the cochlea: Potential therapeutic targets for sensorineural hearing loss. Front. Pharmacol. 5, 287 (2014).
64. G. Laurell, A. Viberg, M. Teixeira, O. Sterkers, E. Ferrary, Blood-perilymph barrier and ototoxicity: An in vivo study in the rat. Acta Otolaryngol. 120, 796-803 (2000).
65. W. A. Banks, M. A. Erickson, The blood-brain barrier and immune function and dysfunction. Neurobiol. Dis. 37, 26-32 (2010).
66. K. E. Driscoll, D. G. Hassenbein, B. W. Howard, R. J. Isfort, D. Cody, M. H. Tindal, M. Suchanek, J. M. Carter, Cloning, expression, and functional characterization of rat MIP-2: A neutrophil chemoattractant and epithelial cell mitogen. J. Leukoc. Biol. 58, 359-364 (1995).
67. A. Harada, N. Sekido, T. Akahoshi, T. Wada, N. Mukaida, K. Matsushima, Essential involvement of interleukin-8 (IL-8) in acute inflammation. J. Leukoc. Biol. 56, 559-564 (1994).
68. R. E. Vandenbroucke, E. Dejonckheere, P. Van Lint, D. Demeestere, E. Van Wonterghem, I. Vanlaere, L. Puimège, F. Van Hauwermeiren, R. De Rycke, C. Mc Guire, C. Campestre, C. López-Otin, P. Matthys, G. Leclercq, C. Libert, Matrix metalloprotease 8-dependent extracellular matrix cleavage at the blood-CSF barrier contributes to lethality during systemic inflammatory diseases. J. Neurosci. 32, 9805-9816 (2012).
69. I. Palmela, H. Sasaki, F. L. Cardoso, M. Moutinho, K. S. Kim, D. Brites, M. A. Brito, Timedependent dual effects of high levels of unconjugated bilirubin on the human blood-brain barrier lining. Front. Cell. Neurosci. 6, 22 (2012).
70. T. Karasawa, Q. Wang, Y. Fu, D. M. Cohen, P. S. Steyger, TRPV4 enhances the cellular uptake of aminoglycoside antibiotics. J. Cell Sci. 121, 2871-2879 (2008).
71. R. Fian, E. Grasser, F. Treiber, R. Schmidt, P. Niederl, C. Rosker, The contribution of TRPV4- mediated calcium signaling to calcium homeostasis in endothelial cells. J. Recept. Signal Transduct. Res. 27, 113-124 (2007).
72. M. Jiang, Q. Wang, T. Karasawa, J. W. Koo, H. Li, P. S. Steyger, Sodium-glucose transporter-2 (SGLT2; SLC5A2) enhances cellular uptake of aminoglycosides. PLOS One 9, e108941 (2014).
73. W. Shi, N. Cui, Z. Wu, Y. Yang, S. Zhang, H. Gai, D. Zhu, C. Jiang, Lipopolysaccharides upregulate Kir6.1/SUR2B channel expression and enhance vascular KATP channel activity via NF-κB-dependent signaling. J. Biol. Chem. 285, 3021-3029 (2010).
74. M. Sakagami, T. Harada, M. Sano, S. Sakai, T. Matsunaga, Quantitative evaluation of pinocytosis of capillaries of the stria vascularis under normal and experimental conditions. Acta Otolaryngol. 103, 189-197 (1987).
75. C. Tiruppathi, J. Shimizu, K. Miyawaki-Shimizu, S. M. Vogel, A. M. Bair, R. D. Minshall, D. Predescu, A. B. Malik, Role of NF-κB-dependent caveolin-1 expression in the mechanism of increased endothelial permeability induced by lipopolysaccharide. J. Biol. Chem. 283, 4210-4218 (2008).
76. J. Schacht, S. Lodhi, N. D. Weiner, Effects of neomycin on polyphosphoinositides in inner ear tissues and monomolecular films. Adv. Exp. Med. Biol. 84, 191-208 (1977).
77. F. Van Bambeke, M. P. Mingeot-Leclercq, A. Schanck, R. Brasseur, P. M. Tulkens, Alterations in membrane permeability induced by aminoglycoside antibiotics: Studies on liposomes and cultured cells. Eur. J. Pharmacol. 247, 155-168 (1993).
78. R. D. Moore, C. R. Smith, P. S. Lietman, Risk factors for the development of auditory toxicity in patients receiving aminoglycosides. J. Infect. Dis. 149, 23-30 (1984).
79. K. R. Henry, M. B. Guess, R. A. Chole, Hyperthermia increases aminoglycoside ototoxicity. Acta Otolaryngol. 95, 323-327 (1983).
80. R. A. Zager, Endotoxemia, renal hypoperfusion, and fever: Interactive risk factors for aminoglycoside and sepsis-associated acute renal failure. Am. J. Kidney Dis. 20, 223-230 (1992).
81. G. S. Oh, H. J. Kim, J. H. Choi, A. Shen, C. H. Kim, S. J. Kim, S. R. Shin, S. H. Hong, Y. Kim, C. Park, S. J. Lee, S. Akira, R. Park, H. S. So, Activation of lipopolysaccharide-TLR4 signaling accelerates the ototoxic potential of cisplatin in mice. J. Immunol. 186, 1140-1150 (2011).
82. K. M. Nicol, C. M. Hackney, E. F. Evans, S. R. Pratt, Behavioural evidence for recovery of auditory function in guinea pigs following kanamycin administration. Hear. Res. 61, 117-131 (1992).
83. L. Chen, S. Xiong, Y. Liu, X. Shang, Effect of different gentamicin dose on the plasticity of the ribbon synapses in cochlear inner hair cells of C57BL/6J mice. Mol. Neurobiol. 46, 487-494 (2012).
84. K. Liu, D. Chen, W. Guo, N. Yu, X. Wang, F. Ji, Z. Hou, W. Y. Yang, S. Yang, Spontaneous and partial repair of ribbon synapse in cochlear inner hair cells after ototoxic withdrawal. Mol. Neurobiol. 10.1007/s12035-014-8951-y (2014).
85. E. C. Oesterle, Changes in the adult vertebrate auditory sensory epithelium after trauma. Hear. Res. 297, 91-98 (2013).
86. K. C. Campbell, R. P. Meech, J. J. Klemens, M. T. Gerberi, S. S. Dyrstad, D. L. Larsen, D. L. Mitchell, M. El-Azizi, S. J. Verhulst, L. F. Hughes, Prevention of noise- and drug-induced hearing loss with D-methionine. Hear. Res. 226, 92-103 (2007).
87. A. H. Sun, L. S. Parnes, D. J. Freeman, Comparative perilymph permeability of cephalosporins and its significance in the treatment and prevention of suppurative labyrinthitis. Ann. Otol. Rhinol. Laryngol. 105, 54-57 (1996).
88. C. Kilkenny, W. J. Browne, I. C. Cuthill, M. Emerson, D. G. Altman, Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLOS Biol. 8, e1000412 (2010).