Minocycline restores olfactory bulb volume and olfactory behavior after traumatic brain injury in mice

Journal of Neurotrauma

Volumn 29, Issue 2, 2012, Pages 354-361

  Siopi, Eleni ^a   Calabria, Silvia ^a   Plotkine, Michel ^a   Marchand Leroux, Catherine ^a   Jafarian Tehrani, Mehrnaz ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

minocycline; neuroprotection; olfactory avoidance test; olfactory bulb lesion; traumatic brain injury

Indexed keywords

MINOCYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FUNCTION TEST; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; OLFACTORY AVOIDANCE BEHAVIOR; OLFACTORY AVOIDANCE TEST; OLFACTORY BULB; OLFACTORY BULB LESION; SMELLING; SMELLING DISORDER; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; MALE; MICE; MINOCYCLINE; NEUROPROTECTIVE AGENTS; OLFACTION DISORDERS; OLFACTORY BULB; SMELL;

EID: 84856435777     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.2055     Document Type: Article

References (54)

1. Ai, M., Min, S., Grosjean, Y., Leblanc, C., Bell, R., Benton, R., and Suh, G.S. (2010). Acid sensing by the Drosophila olfactory system. Nature 468, 691-695.
2. Buschhüter, D., Smitka, M., Puschmann, S., Gerber, J.C., Witt, M., Abolmaali, N.D., and Hummel, T. (2008). Correlation be-tween olfactory bulb volume and olfactory function. Neuro-image 42, 498-502.
3. Bye, N., Habgood, M.D., Callaway, J.K., Malakooti, N., Potter, A., Kossmann, T., and Morganti-Kossmann, M.C. (2007). Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 204, 220-233. (Pubitemid 46330272)
4. Callahan, C.D., and Hinkebein, J.H. (2002). Assessment of an- osmia after traumatic brain injury: performance characteristics of the University of Pennsylvania Smell Identification Test. J. Head Trauma Rehabil. 17, 251-256. (Pubitemid 34521380)
5. Collet, S., Grulois, V., Bertrand, B., and Rombaux, P. (2009). Post-traumatic olfactory dysfunction: a cohort study and up- date. B-Ent. 5 Suppl. 13, 97-107.
6. Doty, R.L., Li, C., Mannon, L.J., and Yousem, D.M. (1997). Olfactory dysfunction in multiple sclerosis. N. Engl. J. Med. 336, 1918-1919.
7. Doty, R.L. (2001). Olfaction. Annu. Rev. Psychol. 52, 423-452. (Pubitemid 33705579)
8. Drummond, M., Douglas, J., and Olver, J. (2007) Anosmia after traumatic brain injury: A clinical update. Brain Impairment 8, 31-40.
9. Duncan, H.J., and Seiden, A.M. (1995) Long-term follow-up of olfactory loss secondary to head trauma and upper respiratory tract infection. Arch. Otolaryngol. Head Neck Surg. 121,1183- 1187.
10. Ekdahl, C.T., Claasen, J.H., Bonde, S., Kokaia, Z., and Lindvall, O. (2003). Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100, 13632-13637. (Pubitemid 37444791)
11. Ekdahl, C.T., Kokaia, Z., and Lindvall, O. (2009). Brain inflam- mation and adult neurogenesis: the dual role of microglia. Neuroscience 158, 1021-1029.
12. Familian, A., Boshuizen, R.S., Eikelenboom, P., and Veerhuis, R. (2006). Inhibitory effect of minocycline on amyloid beta fibril formation and human microglial activation. Glia 53, 233-240. (Pubitemid 43221345)
13. Fleming, S.M., Tetreault, N.A., Mulligan, C.K., Hutson, C.B., Masliah, E., and Chesselet, M.F. (2008). Olfactory deficits in mice overexpressing human wildtype alpha-synuclein. Eur. J. Neurosci. 28, 247-256.
14. Fortin, A., Lefebvre, M.B., and Ptito, M. (2010). Traumatic brain injury and olfactory deficits: the tale of two smell tests! Brain Inj. 24, 27-33.
15. Fujii, M., Fukazawa, K., Takayasu, S., and Sakagami, M. (2002). Olfactory dysfunction in patients with head trauma. Auris Nasus Larynx 29, 35-40. (Pubitemid 34076551)
16. Glass, C.K., Saijo, K., Winner, B., Marchetto, M.C., and Gage, F.H. (2010). Mechanisms underlying inflammation in neuro- degeneration. Cell 140, 918-934.
17. Haehner, A., Rodewald, A., Gerber, J.C., and Hummel, T. (2008). Correlation of olfactory function with changes in the volume of the human olfactory bulb. Arch. Otolaryngol. Head Neck Surg. 134, 621-624. (Pubitemid 351871022)
18. Haxel, B.R., Grant, L., and Mackay-Sim, A. (2008). Olfactory dysfunction after head injury. J. Head Trauma Rehabil. 23, 407-413.
19. Hebb, A.L., Zacharko, R.M., Dominguez, H., Trudel, F., Laforest, S., and Drolet, G. (2002). Odor-induced variation in anxiety- like behavior in mice is associated with discrete and differ- ential effects on mesocorticolimbic cholecystokinin mRNA expression. Neuropsychopharmacology 27, 744-755. (Pubitemid 35335891)
20. Hellal, F., Pruneau, D., Palmier, B., Faye, P., Croci, N., Plotkine, M., and Marchand-Verrecchia, C. (2003). Detrimental role of bradykinin B2 receptor in a murine model of diffuse brain injury. J. Neurotrauma 20, 841-851. (Pubitemid 37159066)
21. Holbrook, E.H., and Leopold, D.A. (2006). An updated review of clinical olfaction. Curr. Opin. Otolaryngol. Head Neck Surg. 14, 23-28. (Pubitemid 43269488)
22. Homsi, S., Federico, F., Croci, N., Palmier, B., Plotkine, M., Marchand Leroux, C., and Jafarian-Tehrani, M. (2009). Mino- cycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Res. 1291, 122-132.
23. Homsi, S., Piaggio, T., Croci, N., Noble, F., Plotkine, M., Marc- hand Leroux, C., and Jafarian-Tehrani, M. (2010). Blockade of acute microglial activation by minocycline promotes neuro- protection and reduces locomotor hyperactivity after closed head injury in mice: a twelve-week follow-up study. J. Neurotrauma 27, 911-921.
24. Ikeda, K., Sakurada, T., Takasaka, T., Okitsu, T., and Yoshida, S. (1995). Anosmia following head trauma: preliminary study of steroid treatment. Tohoku J. Exp. Med. 177, 343-351. (Pubitemid 26128229)
25. Jiang, R.S., Wu, S.H., Liang, K.L., Shiao, J.Y., Hsin, C.H., and Su, M.C. (2010). Steroid treatment of posttraumatic anosmia. Eur. Arch. Otorhinolaryngol. 267, 1563-1567.
26. Jimenez, D.F., Sundrani, S., and Barone, C.M. (1997). Posttraumatic anosmia in craniofacial trauma. J. Craniomaxillofac Trauma 3, 8-15. (Pubitemid 27446691)
27. Joung, Y.I., Yi, H.J., Lee, S.K., Im, T.H., Cho, S.H., and Ko, Y. (2007). Posttraumatic anosmia and ageusia: Incidence and recovery with relevance to the hemorrhage and fracture on the frontal base. J. Korean Neurosurg. 42, 1-5. (Pubitemid 47288153)
28. Kang, H.M., Jin, J., Lee, S., Ryu, J., and Park, C. (2010). A novel method for olfactory bulbectomy using photochemically in- duced lesion. Neuroreport 21, 179-184.
29. Kelley, B.J., Lifshitz, J., and Povlishock, J.T. (2007). Neuroin- flammatory responses after experimental diffuse traumatic brain injury. J. Neuropathol. Exp. Neurol. 66, 989-1001. (Pubitemid 350060367)
30. Kepecs, A., Uchida, N., and Mainen, Z. (2006). The sniff as a unit of olfactory processing. Chem. Senses 31, 167-179. (Pubitemid 43231442)
31. Kim, H.S., and Suh, Y.H. (2009). Minocycline and neurodegen- erative diseases. Behav. Brain Res. 196, 168-179.
32. Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T., Mori, K., and Sakano, H. (2007). Innate versus learned odour processing in the mouse olfactory bulb. Nature 450, 503-508. (Pubitemid 350190245)
33. Kobayashi, M., and Costanzo, R.M. (2009). Olfactory nerve re-covery following mild and severe injury and the efficacy of dexamethasone treatment. Chem. Senses 34, 573-580.
34. Legg, J.W. (1873). A case of anosmia following a blow. Lancet 2, 659-660.
35. London, B., Nabet, B., Fisher, A.R., White, B., Sammel, M.D., and Doty, R.L. (2008). Predictors of prognosis in patients with ol-factory disturbance. Ann. Neurol. 63, 159-166. (Pubitemid 351355294)
36. Morganti-Kossmann, M.C., Satgunaseelan, L., Bye, N., and Kossmann, T. (2007). Modulation of immune response by head injury. Injury 38, 1392-1400. (Pubitemid 350192405)
37. Mott, A.E., and Leopold, D.A. (1991). Disorders in taste and smell. Med. Clin. North Am. 75, 1321-1353.
38. Mucignat-Caretta, C., Bondi, M., and Caretta, A. (2004). Animal models of depression: olfactory lesions affect amygdala, sub-ventricular zone, and aggression. Neurobiol. Dis. 16, 386-395. (Pubitemid 38757320)
39. Mucignat-Caretta, C., Bondi, M., and Caretta, A. (2006). Time course of alterations after olfactory bulbectomy in mice. Phy-siol. Behav. 89, 637-643. (Pubitemid 44894248)
40. Nyby, J., Kay, E., Bean, N.J., Dahinden, Z., and Kerchner, M. (1985). Male mouse (Mus musculus) attraction to airborne urinary odors of conspecifics and to food odors: effects of food deprivation. J. Comp. Psychol. 99, 479-490.
41. Ogawa, T., and Rutka, J. (1999). Olfactory dysfunction in head injured workers. Acta Otolaryngol. Suppl. 540, 50-57. (Pubitemid 29336473)
42. Ongle, W. (1870). Anosmia or cases illustrating the physiology and pathology of sense of smell. Med. Chir. Trans. 53, 263.
43. Prediger, R.D., Rojas-Mayorquin, A.E., Aguiar, A.S., Jr., Che-varin, C., Mongeau, R., Hamon, M., Lanfumey, L., Del Bel, E., Muramatsu, H., Courty, J., and Raisman-Vozari, R. (2011). Mice with genetic deletion of the heparin-binding growth factor midkine exhibit early preclinical features of Parkinson's disease. J. Neural Transm. (ahead of print)
44. Sanchez Mejia, R.O., Ona, V.O., Li, M., and Friedlander, R.M. (2001). Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dys-function. Neurosurgery 48, 1393-1399; discussion 1399-1401.
45. Siopi, E., Cho, A.H., Homsi, S., Croci, N., Plotkine, M., Marc-hand-Leroux, C., and Jafarian-Tehrani, M. (2011). Minocycline restores sAPPα levels and reduces the late histopathological consequences of traumatic brain injury in mice. J. Neuro-trauma 28, 2135-2145.
46. Slotnick, B.M., and Gutman, L.A. (1977). Evaluation of intranasal zinc sulfate treatment of olfactory discrimination in rats. J. Comp. Physiol. Psychol. 91, 942-950. (Pubitemid 8162746)
47. Sumner, D. (1964) Post-traumatic anosmia. Brain 87, 107-120.
48. Viggiano, D. (2008). The hyperactive syndrome: meta-analysis of genetic alterations, pharmacological treatments and brain lesions which increase locomotor activity. Behav. Brain Res. 194, 1-14.
49. Wachowiak, M., and Shipley, M.T. (2006). Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell. Dev. Biol. 17, 411-423. (Pubitemid 44301929)
50. Wachowiak, M., Wesson, D.W., Pirez, N., Verhagen, J.V., and Carey, R.M. (2009). Low-level mechanisms for processing odor information in the behaving animal. Ann. NY Acad. Sci. 1170, 286-292.
51. Wilson, R.I., and Mainen, Z.F. (2006). Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163-201. (Pubitemid 44476843)
52. Wong, S.T., Trinh, K., Hacker, B., Chan, G.C., Lowe, G., Gaggar, A., Xia, Z., Gold, G.H., and Storm, D.R. (2000). Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27, 487-497.
53. Wu, A.P., and Davidson, T. (2008). Posttraumatic anosmia sec-ondary to central nervous system injury. Am. J. Rhinol. 22, 606-607.
54. Yousem, D.M., Geckle, R.J., Bilker, W.B., McKeown, D.A., and Doty, R.L. (1996). Posttraumatic olfactory dysfunction: MR and clinical evaluation. AJNR Am. J. Neuroradiol. 17, 1171-1179. (Pubitemid 26198528)