Macrophage depletion in the murine olfactory epithelium leads to increased neuronal death and decreased neurogenesis

Journal of Comparative Neurology

Volumn 501, Issue 2, 2007, Pages 206-218

  Borders, Aaron S ^a,d   Getchell, Marilyn L ^a,b   Etscheidt, Jordan T ^a   Van Rooijen, Nico ^c   Cohen, Donald A ^a   Getchell, Thomas V ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Clodronate; Liposomes; Neuroprotection; Olfactory sensory neurons; Proliferation

Indexed keywords

CLODRONIC ACID; LIPOSOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; MACROPHAGE; MALE; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; SENSORY NERVE CELL;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BROMODEOXYURIDINE; CASPASE 3; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CLODRONIC ACID; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; NEURONS; OLFACTORY BULB; OLFACTORY MARKER PROTEIN; OLFACTORY MUCOSA; ORGANOGENESIS; TIME FACTORS;

EID: 33846898032     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21252     Document Type: Article

References (79)

1. Barouch R, Appel E, Kazimirsky G, Brodie C. 2001. Macrophages express neurotrophins and neurotrophin receptors. Regulation of nitric oxide production by NT-3. J Neuroimmunol 112:72-77.
2. Batchelor PE, Porritt MJ, Martinello P, Parish CL, Liberatore GT, Donnan GA, Howells DW. 2002. Macrophages and microglia produce local trophic gradients that stimulate axonal sprouting toward but not beyond the wound edge. Mol Cell Neurosci 21:436-453.
3. Bauer S, Rasika S, Han J, Mauduit C, Raccurt M, Morel G, Jourdan F, Benahmed M, Moyse E, Patterson PH. 2003. Leukemia inhibitory factor is a key signal for injury-induced neurogenesis in the adult mouse olfactory epithelium. J Neurosci 23:1792-1803.
4. Brück W, Huitinga H, Dijkstra CD. 1996. Liposome-mediated monocyte depletion during wallerian degeneration defines the role of hematogenous phagocytes in myelin removal. J Neurosci Res 46:477-484.
5. Buiakova OI, Rama Krishna NS, Getchell TV, Margolis FL. 1994. Human and rodent OMP genes: conservation of structural and regulatory motifs and cellular localization. Genomics 20:452-462.
6. Buiakova OI, Baker H, Scott JW, Farbman A, Kream R, Grillo M, Franzen L, Richman M, Davis LM, Abbondanzo S, Stewart CL, Margolis FL. 1996. Olfactory marker protein (OMP) gene deletion causes altered physiological acitivity of olfactory sensory neurons. Proc Natl Acad Sci U S A 93:1-6.
7. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M. 2006. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149-160.
8. Calof AL, Hagiwara N, Holcomb JD, Mumm JS, Shou J. 1996. Neurogenesis and cell death in olfactory epithelium. J Neurobiol 30:67-81.
9. Calof AL, Mumm JS, Rim PC, Shou J. 1998. The neuronal stem cell of the olfactory epithelium. J Neurobiol 36:190-205.
10. Calof AL, Bonnin A, Crocker C, Kawauchi S, Murray RC, Shou J, Wu H-H. 2002. Progenitor cells of the olfactory receptor neuron lineage. Microsc Res Tech 58:176-188.
11. Carr VM, Farbman AI. 1992. Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115:55-59.
12. Carter LA, MacDonald JL, Roskams AJ. 2004. Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24:5670-5683.
13. Costanzo RM, Graziadei PPC. 1983. A quantitative analysis of changes in the olfactory epithelium following bulbectomy in hamster. J Comp Neurol 215:370-381.
14. Cowan CM, Thai J, Krajewski S, Reed JC, Nicholson DW, Kaufmann SH, Roskams AJ. 2001. Caspases 3 and 9 send a pro-apoptotic signal from synapse to cell body in olfactory receptor neurons. J Neurosci 21:7099-7109.
15. Crosnier C, Vargesson N, Gschmeissner S, Riza-McNaughton L, Morrison A, Lewis J. 2005. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132:1093-1104.
16. Diez R, Lang RA. 1997. Macrophages induce apoptosis in normal cells in vivo. Development 124:3633-3638.
17. Duffield JS. 2003. The inflammatory macrophage: a story of Jekyll and Hyde. Clin Sci 104:27-38.
18. Fadok VA, Chimini G. 2001. The phagocytosis of apoptotic cells. Semin Immunol 13:365-372.
19. Getchell TV, Getchell ML, Rama Krishna NS. 1996. Human olfactory receptor neurons and their central targets in the bulb differentially express BDNF and its receptor Trk B. Chem Senses 21:605-606.
20. Getchell ML, Boggess M, Pruden SII, Little S, Buch S, Getchell TV. 2002a. Expression of TGF-β type II receptors in the olfactory epithelium and their regulation in TGF-α transgenic mice. Brain Res 945:232-241.
21. Getchell TV, Shah DS, Partin JV, Subhedar NK, Getchell ML. 2002b. Leukemia inhibitory factor mRNA expression is upregulated in macrophages and olfactory receptor neurons after target ablation. J Neurosci Res 67:246-254.
22. Getchell TV, Subhedar NK, Shah DS, Hackley G, Partin JV, Sen G, Getchell ML. 2002c. Chemokine regulation of macrophage recruitment into the olfactory epithelium following target ablation: involvement of macrophage inflammatory protein-1a and monocyte chemoattractant protein-1. J Neurosci Res 70:784-793.
23. Getchell TV, Liu H, Vaishnav RA, Kwong K, Stromberg AJ, Getchell ML. 2005. Temporal profiling of gene expression during neurogenesis and remodeling in the olfactory epithelium at short intervals after target ablation. J Neurosci Res 80:309-329.
24. Getchell ML, Li H, Vaishnav RA, Borders AS, Witta J, Subhedar N, de Villiers W, Stromberg AJ, Getchell TV. 2006. Temporal gene expression profiles of target-ablated olfactory epithelium in mice with disrupted expression of scavenger receptor A: impact on macrophages. Physiol Genomics 27:245-263.
25. Gordon S. 1998. The role of the macrophage in immune regulation. Res Immunol 149:685-688.
26. Gordon S. 2002. Alternative activation of macrophages. Nat Rev Immunol 3:23-35.
27. Graves MC, Fiala M, Dinglasan LV, Liu NQ, Sayre J, Chiappelli F, van Kooten C, Vinters HV. 2004. Inflammation in amyotrophic lateral sclerosis spinal cord and brain is mediated by activated macrophages, mast cells and T cells. Amyotroph Lateral Scler Other Motor Neuron Disord 5:213-219.
28. Graziadei PPC, Monti Graziadei GA. 1978. The olfactory system: a model for the study of neurogenesis and axon regeneration in mammals. In: Cotman CW, editor. Neuronal plasticity. New York: Raven Press. p 131-153.
29. Graziadei PPC, Monti Graziadei GA. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18.
30. Harding J, Graziadei PPC, Monti Graziadei GA, Margolis FL. 1977. Denervation in the primary olfactory pathway of mice. IV. Biochemical and morphological evidence for neuronal replacement following nerve section. Brain Res 132:11-28.
31. Holcomb JD, Mumm JS, Calof AL. 1995. Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro. Dev Biol 172:307-323.
32. Huard JMT, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE. 1998. Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neuronal cells. J Comp Neurol 400:469-486.
33. Jones G, Power C. 2006. Regulation of neural cell survival by HIV-1 infection. Neurobiol Dis 21:1-17.
34. Jung S, Huitinga I, Schmidt B, Zielasek J, Dijkstra CD, Toyka KV, Hartung HP. 1993. Selective elimination of macrophages by dichlormethylene diphosphonate-containing liposomes suppresses experimental autoimmune neuritis. J Neurol Sci 119:195-202.
35. Kadiu I, Glanzer JG, Kipnis J, Gendelman HE, Thomas MP. 2005. Mononuclear phagocytes in the pathogenesis of neurodegenerative diseases. Neurotox Res 8:25-50.
36. Kim EJ, Simpson PJ, Park DJ, Liu BQ, Ronnett GV, Moon C. 2005. Leukemia inhibitory factor is a proliferative factor for olfactory sensory neurons. NeuroReport 16:25-28.
37. Kotter MR, Setzu A, Sim FJ, van Rooijen N, Franklin RJ. 2001. Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination. Glia 35:204-212.
38. Kotter MR, Zhao C, van Rooijen N, Franklin RJ. 2005. Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol Dis 18:166-175.
39. -/- mice and restoration of function by exogenous MIP-1a. Physiol Genomics 20:73-86.
40. Langenhan T, Sendtner M, Holtmann B, Carroll P, Asan E. 2005. Ciliary neurotrophic factor-immunoreactivity in olfactory sensory neurons. Neuroscience 134:1179-1194.
41. Lee AM, Fryer AD, van Rooijen N, Jacoby DB. 2004. Role of macrophages in virus-induced airway hyperresponsiveness and neuronal M2 muscarinic receptor dysfunction. Am J Physiol Lung Cell Mol Physiol 286:1255-1259.
42. Leemans JC, Juffermans NP, Florquin S, van Rooijen N, Vervoordeldonk MJ, Verbon A, van Deventer SJ, van der PT. 2001. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J Immunol 166:4604-4611.
43. Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L. 2003. Neurotrophic properties of olfactory ensheathing glia. Exp Neurol 180:167-171.
44. Liu T, van Rooijen N, Tracey DJ. 2000. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 86:25-32.
45. Lotan M, Schwartz M. 1994. Cross talk between the immune system and the nervous system in response to injury: implications for regeneration. FASEB J 8:1026-1033.
46. Mahanthappa NK, Schwarting GA. 1993. Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-βs. Neuron 10:293-305.
47. Margolis FL. 1988. Molecular cloning of olfactory-specific gene products. In: Margolis FL, Getchell TV, editors. Molecular neurobiology of the olfactory system. New York: Plenum. p 237-265.
48. Martin P, Leibovich SJ. 2005. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 15:599-607.
49. Meda L, Cassatella MA, Szendrei GI, Otvos L, Baron P, Villalba M, Ferrari D, Rossi F. 1995. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
50. Michel D, Moyse E, Brun G, Jourdan F. 1994. Induction of apoptosis in mouse olfactory neuroepithelium by synaptic target ablation. NeuroReport 5:1329-1332.
51. Mitrasinovic OM, Grattan A, Robinson CC, Lapustea NB, Poon C, Ryan H, Phong C, Murphy GM Jr. 2005. Microglia overexpressing the macrophage colony-stimulating factor receptor are neuroprotective in a microglial- hippocampal organtypic coculture system. J Neurosci 25:4442-4451.
52. Miwa T, Uramoto N, Ishimaru T, Furukawa M, Shiba K Morjizumi T. 1998. Retrograde transport of nerve growth factor from olfactory bulb to olfactory epithelium. NeuroReport 9:153-155.
53. Nakagawa T, Suga S, Kawase T, Toda M. 2006. Intracarotid injection of granulocyte-macrophage colony-stimulating factor induces neuroprotection in a rat transient middle cerebral artery occlusion model. Brain Res 1089:179-185.
54. Nan B, Getchell ML, Partin JV, Getchell TV. 2001. Leukemia inhibitory factor and interleukin-6 and their receptors are transiently expressed in the olfactory mucosa following target ablation. J Comp Neurol 435:60-77.
55. Newman MP, Féron F, Mackay-Sim A. 2000. Growth factor regulation of neurogenesis in adult olfactory epithelium. Neuroscience 99:343-350.
56. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT. 1999. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365.
57. Rabinowitz SS, Gordon S. 1991. Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. J Exp Med 174:827-836.
58. Rawson NE, LaMantia AS. 2006. Once and again: retinoic acid signaling in the developing and regenerating olfactory pathway. J Neurobiol 66:653-676.
59. Resendes AR, Majo N, Segales J, Espadamala J, Mateu E, Chianini F, Nofrarias M, Domingo M. 2004. Apoptosis in normal lymphoid organs from healthy normal, conventional pigs at different ages detected by TUNEL and cleaved caspase-3 immunohistochemistry in paraffin-embedded tissues. Vet Immunol Immunopathol 99:203-213.
60. Schwartz M. 2003. Macrophages and microglia in central nervous system injury: are they helpful or harmful? J Cereb Blood Flow Metab 23:385-394.
61. Schwartz M, Moalem G. 2001. Beneficial immune activity after CNS injury: prospects for vaccination. J Neuroimmunol 113:185-192.
62. Schwartz Levey M, Chikaraishi DM, Kauer JS. 1991. Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci 11:3556-3564.
63. Schwob JE. 2002. Neural regeneration and the peripheral olfactory system. Anat Rec 269:33-49.
64. Schwob JE, Szumowski KE, Stasky AA. 1992. Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci 12:3896-3919.
65. Shetty RS, Bose SC, Nickell MD, McIntyre JC, Hardin DH, Harris AM, McClintock TS. 2005. Transcriptional changes during neuronal death and replacement in the olfactory epithelium. Mol Cell Neurosci 30:90-107.
66. Shibata A, Zelivyanskaya M, Limoges J, Carlson KA, Gorantla S, Branecki C, Bishu S, Xiong H, Gendelman HE. 2003. Peripheral nerve induces macrophage neurotrophic activities: regulation of neuronal process outgrowth, intracellular signaling and synaptic function. J Neuroimmunol 142:112-129.
67. Shou J, Murray RC, Rim PC, Calof AL. 2000. Opposing effects of bone morphogenetic proteins on neuron production and survival in the olfactory receptor neuron lineage. Development 127:5403-5413.
68. Simpson PJ, Wang E, Moon C, Matarazzo V, Cohen DR, Liebl DJ, Ronnett GV. 2003. Neurotrophin-3 signaling maintains maturational homeostasis between neuronal populations in the olfactory epithelium. Mol Cell Neurosci 24:858-874.
69. Sunderkotter C, Nikolic T, Dillon MJ, van Rooijen N, Stehling M, Drevets DA, Leenen PJ. 2004. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 172:4410-4417.
70. Suzuki Y, Schafer J, Farbman AI. 1995. Phagocytic cells in the rat olfactory epithelium after bulbectomy. Exp Neurol 136:225-233.
71. Suzuki Y, Takeda M, Farbman AI. 1996. Supporting cells as phagocytes in the olfactory epithelium after bulbectomy. J Comp Neurol 376:509-517.
72. Uramoto N, Miwa T, Donjyo T, Ishimaru T, Furukawa M. 1998. [Study of the function of nerve growth factor in the olfactory tract of the mouse]. Nippon Jibiinkoka Gakkai Kaiho 101:908-915.
73. van Rooijen N, Sanders A. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83-93.
74. van Rooijen N, van Kesteren-Hendrikx E. 2002. Clodronate liposomes: perspectives in research and therapeutics. J Liposome Res 12:81-94.
75. Vigers AJ, Bottger B, Baquet ZC, Finger TE, Jones KR. 2003. Neurotrophin-3 is expressed in a discrete subset of olfactory receptor neurons in the mouse. J Comp Neurol 463:221-235.
76. Woodhall E, West AK, Chuah MI. 2001. Cultured olfactory ensheathing cells express nerve growth factor, brain-derived neurotrophic factor, glia cell line-derived neurotrophic factor and their receptors. Brain Res Mol Brain Res 88:203-213.
77. Wu H-H, Ivkovic S, Murray RC, Jaramillo S, Lyons KM, Johnson JE, Calof AL. 2003. Autoregulation of neurogenesis by GDF11. Neuron 37:197-207.
78. Xu Y, Kulkosky J, Acheampong E, Nunnari G, Sullivan J, Pomerantz R. 2004. HIV-1-mediated apoptosis of neuronal cells: proximal molecular mechanisms of HIV-1-induced encephalopathy. Proc Natl Acad Sci U S A 101:7070-7075.
79. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9:268-275.