Targeting cholesterol homeostasis to fight hearing loss: A new perspective

Frontiers in Aging Neuroscience

Volumn 7, Issue JAN, 2015, Pages

  Malgrange, Brigitte ^a   Varela Nieto, Isabel ^b   de Medina, Philippe ^c   Paillasse, Michael R ^c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Affichem SA   (France)

Author keywords

Cholesterol homeostasis; Excitotoxicity; Liver X receptor; Oxysterol; Sensorineural hearing loss

Indexed keywords

CHOLESTEROL;

ALZHEIMER DISEASE; BRAIN; CHOLESTEROL HOMEOSTASIS; CHOLESTEROL METABOLISM; DEGENERATIVE DISEASE; HOMEOSTASIS; HUMAN; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; INNER EAR; PARKINSON DISEASE; PERCEPTION DEAFNESS; SHORT SURVEY;

EID: 84922476392     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2015.00003     Document Type: Short Survey

References (75)

1. Adibhatla, R. M., and Hatcher, J. F. (2008). Altered lipid metabolism in brain injury and disorders. Subcell. Biochem. 49, 241-268. doi:10.1007/978-1-4020-8831-5_9
2. Bond, M., Mealing, S., Anderson, R., Elston, J., Weiner, G., Taylor, R. S., et al. (2009). The effectiveness and cost-effectiveness of cochlear implants for severe to profound deafness in children and adults: a systematic review and economic model. Health Technol. Assess. 13, 1-330. doi:10.3310/hta13440
3. Boyles, J. K., Zoellner, C. D., Anderson, L. J., Kosik, L. M., Pitas, R. E., Weisgraber, K. H., et al. (1989). A role for apolipoprotein E, apolipoprotein A-I, and low density lipoprotein receptors in cholesterol transport during regeneration and remyelination of the rat sciatic nerve. J. Clin. Invest. 83, 1015-1031. doi:10.1172/JCI113943
4. Cai, Q., Du, X., Zhou, B., Cai, C., Kermany, M. H., Zhang, C., et al. (2009). Effects of simvastatin on plasma lipoproteins and hearing loss in apolipoprotein E gene-deficient mice. ORL J. Otorhinolaryngol. Relat. Spec. 71, 244-250. doi:10.1159/000236014
5. Cutler, R. G., Pedersen, W. A., Camandola, S., Rothstein, J. D., and Mattson, M. P. (2002). Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis. Ann. Neurol. 52, 448-457. doi:10.1002/ana.10312
6. De Medina, P., Paillasse, M. R., Payre, B., Silvente-Poirot, S., and Poirot, M. (2009). Synthesis of new alkylaminooxysterols with potent cell differentiating activities: identification of leads for the treatment of cancer and neurodegenerative diseases. J. Med. Chem. 52, 7765-7777. doi:10.1021/jm901063e
7. De Medina, P., Paillasse, M. R., Segala, G., Poirot, M., and Silvente-Poirot, S. (2010). Identification and pharmacological characterization of cholesterol-5,6-epoxide hydrolase as a target for tamoxifen and AEBS ligands. Proc. Natl. Acad. Sci. U. S. A. 107, 13520-13525. doi:10.1073/pnas.1002922107
8. De Medina, P., Paillasse, M. R., Segala, G., Voisin, M., Mhamdi, L., Dalenc, F., et al. (2013). Dendrogenin A arises from cholesterol and histamine metabolism and shows cell differentiation and anti-tumour properties. Nat. Commun. 4, 1840. doi:10.1038/ncomms2835
9. Di Berardino, F., Alpini, D., Ambrosetti, U., Amadeo, C., and Cesarani, A. (2007). Sensorineural hearing-loss in the Smith-Lemli-Opitz syndrome. Int. J. Pediatr. Otorhinolaryngol. Extra 2, 169-172. doi:10.1016/j.pedex.2007.05.002
10. Eriksdotter Jonhagen, M., Nordberg, A., Amberla, K., Backman, L., Ebendal, T., Meyerson, B., et al. (1998). Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 9, 246-257. doi:10.1159/000017069
11. Fan, X., Kim, H. J., Bouton, D., Warner, M., and Gustafsson, J. A. (2008). Expression of liver X receptor beta is essential for formation of superficial cortical layers and migration of later-born neurons. Proc. Natl. Acad. Sci. U. S. A. 105, 13445-13450. doi:10.1073/pnas.0806974105
12. Fu, X., Menke, J. G., Chen, Y., Zhou, G., Macnaul, K. L., Wright, S. D., et al. (2001). 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 276, 38378-38387. doi:10.1074/jbc. M105805200
13. Gates, G. A., and Mills, J. H. (2005). Presbycusis. Lancet 366, 1111-1120. doi:10.1016/S0140-6736(05)67423-5
14. Goritz, C., Mauch, D. H., Nagler, K., and Pfrieger, F. W. (2002). Role of glia-derived cholesterol in synaptogenesis: new revelations in the synapse-glia affair. J. Physiol. Paris 96, 257-263. doi:10.1016/S0928-4257(02)00014-1
15. Guo, Y., Zhang, C., Du, X., Nair, U., and Yoo, T. J. (2005). Morphological and functional alterations of the cochlea in apolipoprotein E gene deficient mice. Hear. Res. 208, 54-67. doi:10.1016/j.heares.2005.05.010
16. Harris, J. P., Anderson, J. P., and Novak, R. (1995). An outcomes study of cochlear implants in deaf patients. Audiologic, economic, and quality-of-life changes. Arch. Otolaryngol. Head Neck Surg. 121, 398-404. doi:10.1001/archotol.1995.01890040024004
17. Hayashi, H., Campenot, R. B., Vance, D. E., and Vance, J. E. (2004). Glial lipoproteins stimulate axon growth of central nervous system neurons in compartmented cultures. J. Biol. Chem. 279, 14009-14015. doi:10.1074/jbc. M313828200
18. Hong, C., and Tontonoz, P. (2014). Liver X receptors in lipid metabolism: opportunities for drug discovery. Nat. Rev. Drug Discov. 13, 433-444. doi:10.1038/nrd4280
19. Hu, H., Zhou, Y., Leng, T., Liu, A., Wang, Y., You, X., et al. (2014). The major cholesterol metabolite cholestane-3beta,5alpha,6beta-triol functions as an endogenous neuroprotectant. J. Neurosci. 34, 11426-11438. doi:10.1523/JNEUROSCI.0344-14.2014
20. Huang, P., Chandra, V., and Rastinejad, F. (2010). Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu. Rev. Physiol. 72, 247-272. doi:10.1146/annurev-physiol-021909-135917
21. Ignatius, M. J., Gebicke-Harter, P. J., Skene, J. H., Schilling, J. W., Weisgraber, K. H., Mahley, R. W., et al. (1986). Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl. Acad. Sci. U. S. A. 83, 1125-1129. doi:10.1073/pnas.83.4.1125
22. Janowski, B. A., Willy, P. J., Devi, T. R., Falck, J. R., and Mangelsdorf, D. J. (1996). An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383, 728-731. doi:10.1038/383728a0
23. Jasmin, S. B., Pearson, V., Lalonde, D., Domenger, D., Theroux, L., and Poirier, J. (2014). Differential regulation of ABCA1 and ABCG1 gene expressions in the remodeling mouse hippocampus after entorhinal cortex lesion and liver-X receptor agonist treatment. Brain Res. 1562, 39-51. doi:10.1016/j.brainres.2014.03.016
24. Kang, J., and Rivest, S. (2012). Lipid metabolism and neuroinflammation in Alzheimer's disease: a role for liver X receptors. Endocr. Rev. 33, 715-746. doi:10.1210/er.2011-1049
25. Khalifa, S. A., De Medina, P., Erlandsson, A., El-Seedi, H. R., Silvente-Poirot, S., and Poirot, M. (2014). The novel steroidal alkaloids dendrogenin A and B promote proliferation of adult neural stem cells. Biochem. Biophys. Res. Commun. 446, 681-686. doi:10.1016/j.bbrc.2013.12.134
26. Kikkawa, Y. S., Nakagawa, T., Ying, L., Tabata, Y., Tsubouchi, H., Ido, A., et al. (2014). Growth factor-eluting cochlear implant electrode: impact on residual auditory function, insertional trauma, and fibrosis. J. Transl. Med. 12, 280. doi:10.1186/s12967-014-0280-4
27. Kim, J. H., Ee, S. M., Jittiwat, J., Ong, E. S., Farooqui, A. A., Jenner, A. M., et al. (2011). Increased expression of acyl-coenzyme A: cholesterol acyltransferase-1 and elevated cholesteryl esters in the hippocampus after excitotoxic injury. Neuroscience 185, 125-134. doi:10.1016/j.neuroscience.2011.04.018
28. Kim, J. S. (1999). Sensory symptoms restricted to proximal body parts in small cortical infarction. Neurology 53, 889-890. doi:10.1212/WNL.53.4.889
29. King, K. A., Gordon-Salant, S., Yanjanin, N., Zalewski, C., Houser, A., Porter, F. D., et al. (2014). Auditory phenotype of Niemann-Pick disease, type C1. Ear Hear. 35, 110-117. doi:10.1097/AUD.0b013e3182a362b8
30. Kraus, N., Bradlow, A. R., Cheatham, M. A., Cunningham, J., King, C. D., Koch, D. B., et al. (2000). Consequences of neural asynchrony: a case of auditory neuropathy. J. Assoc. Res. Otolaryngol. 1, 33-45. doi:10.1007/s101620010004
31. Laskowitz, D. T., Sheng, H., Bart, R. D., Joyner, K. A., Roses, A. D., and Warner, D. S. (1997). Apolipoprotein E-deficient mice have increased susceptibility to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 17, 753-758. doi:10.1097/00004647-199707000-00005
32. Leoni, V., and Caccia, C. (2013). 24S-hydroxycholesterol in plasma: a marker of cholesterol turnover in neurodegenerative diseases. Biochimie 95, 595-612. doi:10.1016/j.biochi.2012.09.025
33. Linthicum, F. H. Jr., and Fayad, J. N. (2009). Spiral ganglion cell loss is unrelated to segmental cochlear sensory system degeneration in humans. Otol. Neurotol. 30, 418-422. doi:10.1097/MAO.0b013e31819a8827
34. Liu, J. P., Tang, Y., Zhou, S., Toh, B. H., McLean, C., and Li, H. (2010). Cholesterol involvement in the pathogenesis of neurodegenerative diseases. Mol. Cell. Neurosci. 43, 33-42. doi:10.1016/j.mcn.2009.07.013
35. Ma, M. T., Zhang, J., Farooqui, A. A., Chen, P., and Ong, W. Y. (2010). Effects of cholesterol oxidation products on exocytosis. Neurosci. Lett. 476, 36-41. doi:10.1016/j.neulet.2010.03.078
36. Madden, C., Hilbert, L., Rutter, M., Greinwald, J., and Choo, D. (2002). Pediatric cochlear implantation in auditory neuropathy. Otol. Neurotol. 23, 163-168. doi:10.1097/00129492-200203000-00011
37. Mahley, R. W. (1988). Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622-630. doi:10.1126/science.3283935
38. Martin, R. E., and Bazan, N. G. (1992). Changing fatty acid content of growth cone lipids prior to synaptogenesis. J. Neurochem. 59, 318-325. doi:10.1111/j.1471-4159.1992.tb08906.x
39. Menardo, J., Tang, Y., Ladrech, S., Lenoir, M., Casas, F., Michel, C., et al. (2012). Oxidative stress, inflammation, and autophagic stress as the key mechanisms of premature age-related hearing loss in SAMP8 mouse Cochlea. Antioxid. Redox Signal. 16, 263-274. doi:10.1089/ars.2011.4037
40. Merchant, S. N., Durand, M. L., and Adams, J. C. (2008). Sudden deafness: is it viral? ORL J. Otorhinolaryngol. Relat. Spec. 70, 52-60. doi:10.1159/000111048
41. Moser, T., Predoehl, F., and Starr, A. (2013). Review of hair cell synapse defects in sensorineural hearing impairment. Otol. Neurotol. 34, 995-1004. doi:10.1097/MAO.0b013e3182814d4a
42. Mulas, M. F., Demuro, G., Mulas, C., Putzolu, M., Cavallini, G., Donati, A., et al. (2005). Dietary restriction counteracts age-related changes in cholesterol metabolism in the rat. Mech. Ageing Dev. 126, 648-654. doi:10.1016/j.mad.2004.11.010
43. Nakagawa, T., Kumakawa, K., Usami, S., Hato, N., Tabuchi, K., Takahashi, M., et al. (2014). A randomized controlled clinical trial of topical insulin-like growth factor-1 therapy for sudden deafness refractory to systemic corticosteroid treatment. BMC Med. 12:219. doi:10.1186/s12916-014-0219-x
44. Namjoshi, D. R., Martin, G., Donkin, J., Wilkinson, A., Stukas, S., Fan, J., et al. (2013). The liver X receptor agonist GW3965 improves recovery from mild repetitive traumatic brain injury in mice partly through apolipoprotein E. PLoS ONE 8:e53529. doi:10.1371/journal.pone.0053529
45. Noguchi, N., Saito, Y., and Urano, Y. (2014). Diverse functions of 24(S)-hydroxycholesterol in the brain. Biochem. Biophys. Res. Commun. 446, 692-696. doi:10.1016/j.bbrc.2014.02.010
46. Ohlemiller, K. K., and Gagnon, P. M. (2004). Apical-to-basal gradients in age-related cochlear degeneration and their relationship to "primary" loss of cochlear neurons. J. Comp. Neurol. 479, 103-116. doi:10.1002/cne.20326
47. Ong, W. Y., Kim, J. H., He, X., Chen, P., Farooqui, A. A., and Jenner, A. M. (2010). Changes in brain cholesterol metabolome after excitotoxicity. Mol. Neurobiol. 41, 299-313. doi:10.1007/s12035-010-8099-3
48. Pfrieger, F. W., and Ungerer, N. (2011). Cholesterol metabolism in neurons and astrocytes. Prog. Lipid Res. 50, 357-371. doi:10.1016/j.plipres.2011.06.002
49. Pleis, J. R., and Lethbridge-Cejku, M. (2006). Summary health statistics for U.S. adults: National Health Interview Survey, 2005. Vital Health Stat. 232, 1-153.
50. Ponce, J., De La Ossa, N. P., Hurtado, O., Millan, M., Arenillas, J. F., Davalos, A., et al. (2008). Simvastatin reduces the association of NMDA receptors to lipid rafts: a cholesterol-mediated effect in neuroprotection. Stroke 39, 1269-1275. doi:10.1161/STROKEAHA.107.498923
51. Roehm, P. C., and Hansen, M. R. (2005). Strategies to preserve or regenerate spiral ganglion neurons. Curr. Opin. Otolaryngol. Head Neck Surg. 13, 294-300. doi:10.1097/01.moo.0000180919.68812.b9
52. Ryals, B. M., Dooling, R. J., Westbrook, E., Dent, M. L., Mackenzie, A., and Larsen, O. N. (1999). Avian species differences in susceptibility to noise exposure. Hear. Res. 131, 71-88. doi:10.1016/S0378-5955(99)00022-2
53. Sacchetti, P., Sousa, K. M., Hall, A. C., Liste, I., Steffensen, K. R., Theofilopoulos, S., et al. (2009). Liver X receptors and oxysterols promote ventral midbrain neurogenesis in vivo and in human embryonic stem cells. Cell Stem Cell 5, 409-419. doi:10.1016/j.stem.2009.08.019
54. Schmidt, A., Vogel, R., Holloway, M. K., Rutledge, S. J., Friedman, O., Yang, Z., et al. (1999). Transcription control and neuronal differentiation by agents that activate the LXR nuclear receptor family. Mol. Cell. Endocrinol. 155, 51-60. doi:10.1016/S0303-7207(99)00115-X
55. Schuknecht, H. F., and Gacek, M. R. (1993). Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol. 102, 1-16.
56. Shi, Y., Mantuano, E., Inoue, G., Campana, W. M., and Gonias, S. L. (2009). Ligand binding to LRP1 transactivates Trk receptors by a Src family kinase-dependent pathway. Sci. Signal. 2, ra18. doi:10.1126/scisignal.2000188
57. Shibata, S. B., Budenz, C. L., Bowling, S. A., Pfingst, B. E., and Raphael, Y. (2011). Nerve maintenance and regeneration in the damaged cochlea. Hear. Res. 281, 56-64. doi:10.1016/j.heares.2011.04.019
58. Silvente-Poirot, S., and Poirot, M. (2014). Cancer. Cholesterol and cancer, in the balance. Science 343, 1445-1446. doi:10.1126/science.1252787
59. Sironi, L., Mitro, N., Cimino, M., Gelosa, P., Guerrini, U., Tremoli, E., et al. (2008). Treatment with LXR agonists after focal cerebral ischemia prevents brain damage. FEBS Lett. 582, 3396-3400. doi:10.1016/j.febslet.2008.08.035
60. Sodero, A. O., Vriens, J., Ghosh, D., Stegner, D., Brachet, A., Pallotto, M., et al. (2012). Cholesterol loss during glutamate-mediated excitotoxicity. EMBO J. 31, 1764-1773. doi:10.1038/emboj.2012.31
61. Starr, A., Picton, T. W., Sininger, Y., Hood, L. J., and Berlin, C. I. (1996). Auditory neuropathy. Brain 119(Pt 3), 741-753. doi:10.1093/brain/119.3.741
62. Steffensen, K. R., Jakobsson, T., and Gustafsson, J. A. (2013). Targeting liver X receptors in inflammation. Expert Opin. Ther. Targets 17, 977-990. doi:10.1517/14728222.2013.806490
63. Suzuki, K., Kaneko, M., and Murai, K. (2000). Influence of serum lipids on auditory function. Laryngoscope 110, 1736-1738. doi:10.1097/00005537-200010000-00033
64. Takeno, S., Wake, M., Mount, R. J., and Harrison, R. V. (1998). Degeneration of spiral ganglion cells in the chinchilla after inner hair cell loss induced by carboplatin. Audiol. Neurootol. 3, 281-290. doi:10.1159/000013800
65. Theofilopoulos, S., Griffiths, W. J., Crick, P. J., Yang, S., Meljon, A., Ogundare, M., et al. (2014). Cholestenoic acids regulate motor neuron survival via liver X receptors. J. Clin. Invest. 124, 4829-4842. doi:10.1172/JCI68506
66. Theofilopoulos, S., Wang, Y., Kitambi, S. S., Sacchetti, P., Sousa, K. M., Bodin, K., et al. (2013). Brain endogenous liver X receptor ligands selectively promote midbrain neurogenesis. Nat. Chem. Biol. 9, 126-133. doi:10.1038/nchembio.1156
67. Vance, J. E. (2012). Dysregulation of cholesterol balance in the brain: contribution to neurodegenerative diseases. Dis. Model Mech. 5, 746-755. doi:10.1242/dmm.010124
68. Varela-Nieto, I., Murillo-Cuesta, S., Rodriguez-De La Rosa, L., Lassatetta, L., and Contreras, J. (2013). IGF-I deficiency and hearing loss: molecular clues and clinical implications. Pediatr. Endocrinol. Rev. 4, 460-472.
69. Wang, L., Schuster, G. U., Hultenby, K., Zhang, Q., Andersson, S., and Gustafsson, J. A. (2002). Liver X receptors in the central nervous system: from lipid homeostasis to neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 99, 13878-13883. doi:10.1073/pnas.172510899
70. Weng, T., Devine, E. E., Xu, H., Yan, Z., and Dong, P. (2013). A clinical study of serum lipid disturbance in Chinese patients with sudden deafness. Lipids Health Dis. 12, 95. doi:10.1186/1476-511X-12-95
71. White, J. A., Burgess, B. J., Hall, R. D., and Nadol, J. B. (2000). Pattern of degeneration of the spiral ganglion cell and its processes in the C57BL/6J mouse. Hear. Res. 141, 12-18. doi:10.1016/S0378-5955(99)00204-X
72. Williams, L. R. (1991). Hypophagia is induced by intracerebroventricular administration of nerve growth factor. Exp. Neurol. 113, 31-37. doi:10.1016/0014-4886(91)90143-Z
73. Winkler, J., Ramirez, G. A., Kuhn, H. G., Peterson, D. A., Day-Lollini, P. A., Stewart, G. R., et al. (1997). Reversible Schwann cell hyperplasia and sprouting of sensory and sympathetic neurites after intraventricular administration of nerve growth factor. Ann. Neurol. 41, 82-93. doi:10.1002/ana.410410114
74. Worthington, D. W., and Peters, J. F. (1980). Quantifiable hearing and no ABR: paradox or error? Ear Hear. 1, 281-285. doi:10.1097/00003446-198009000-00009
75. Yoon, C., Van Niekerk, E. A., Henry, K., Ishikawa, T., Orita, S., Tuszynski, M. H., et al. (2013). Low-density lipoprotein receptor-related protein 1 (LRP1)-dependent cell signaling promotes axonal regeneration. J. Biol. Chem. 288, 26557-26568. doi:10.1074/jbc. M113.478552