Lipopolysaccharide-induced inflammation attenuates taste progenitor cell proliferation and shortens the life span of taste bud cells

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Cohn, Zachary J ^a   Kim, Agnes ^a   Huang, Liquan ^a   Brand, Joseph ^a,b   Wang, Hong ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; BROXURIDINE; CYCLIN B2; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; KI 67 ANTIGEN; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR E2F1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL LABELING; CELL METABOLISM; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; CELLULAR DISTRIBUTION; CIRCUMVALLATE PAPILLA; CONTROLLED STUDY; FOLIATE PAPILLA; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; INFECTION; INFLAMMATION; MALE; MITOSIS INHIBITION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; TASTE BUD; TASTE DISORDER; TONGUE; ANIMAL; CELL COUNT; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM;

ANIMALS; CELL COUNT; CELL PROLIFERATION; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS; TASTE BUDS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77953274301     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-72     Document Type: Article

References (75)

1. De Conno F, Ripamonti C, Sbanotto A, Ventafridda V. Oral complications in patients with advanced cancer. J Palliat Care 1989, 5:7-15.
2. Deems DA, Doty RL, Settle RG, Moore-Gillon V, Shaman P, Mester AF, Kimmelman CP, Brightman VJ, Snow JB. Smell and taste disorders, a study of 750 patients from the University of Pennsylvania Smell and Taste Center. Arch Otolaryngol Head Neck Surg 1991, 117:519-528.
3. Graham CS, Graham BG, Bartlett JA, Heald AE, Schiffman SS. Taste and smell losses in HIV infected patients. Physiol Behav 1995, 58:287-293. 10.1016/0031-9384(95)00049-O, 7568432.
4. Schiffman SS, Graham BG. Taste and smell perception affect appetite and immunity in the elderly. Eur J Clin Nutr 2000, 54:S54-S63.
5. Hoffman HJ, Cruickshanks KJ, Davis B. Perspectives on population-based epidemiological studies of olfactory and taste impairment. Ann N Y Acad Sci 2009, 1170:514-530. 10.1111/j.1749-6632.2009.04597.x, 19686188.
6. Pribitkin E, Rosenthal MD, Cowart BJ. Prevalence and causes of severe taste loss in a chemosensory clinic population. Ann Otol Rhinol Laryngol 2003, 112:971-978.
7. Harris R, Davidson TM, Murphy C, Gilbert PE, Chen M. Clinical evaluation and symptoms of chemosensory impairment: one thousand consecutive cases form the dysfunction clinic in San Diego. Am J Rhinol 2006, 20:101-108.
8. Huque T, Cowart BJ, Dankulich-Nagrudny L, Pribitkin EA, Bayley DL, Spielman AI, Feldman RS, Mackler SA, Brand JG. Sour ageusia in two individuals implicates ion channels of the ASIC and PKD families in human sour taste perception at the anterior tongue. PLoS One 2009, 4(10):e7347. 10.1371/journal.pone.0007347, 2754526, 19812697.
9. Henkin RI, Larson AL, Powell RD. Hypogeusia, dysgeusia, hyposmia, and dysosmia following influenza-like infection. Ann Otol Rhinol Laryngol 1975, 84:672-682.
10. Bartoshuk L, Desnoyers S, Hudson C, Marks L, O'Brien M. Tasting on localized areas. Ann NY Acad Sci 1987, 510:166-168.
11. Mann NM. Management of smell and taste problems. Cleveland Clin J Med 2002, 69:329-336.
12. Wrobel BB, Leopold DA. Clinical assessment of patients with smell and taste disorders. Otolaryngol Clin North Am 2004, 37(6):1127-1142. 10.1016/j.otc.2004.06.010, 15563906.
13. Sherry VW. Taste alterations among patients with cancer. Clin J Oncol Nurs 2002, 6(2):73-77. 10.1188/02.CJON.73-77, 11889680.
14. Weiffenbach JM, Schwartz LK, Atkinson JC, Fox PC. Taste performance in Sjogren's syndrome. Physiol Behav 1995, 57(1):89-96. 10.1016/0031-9384(94)00211-M, 7878130.
15. Wang H, Zhou M, Brand J, Huang L. Inflammation activates the interferon signaling pathways in taste bud cells. J Neurosci 2007, 27(40):10703-10713. 10.1523/JNEUROSCI.3102-07.2007, 2096741, 17913904.
16. Wang H, Zhou M, Brand J, Huang L. Inflammation and taste disorders: mechanisms in taste buds. Ann N Y Acad Sci 2009, 1170:596-603. 10.1111/j.1749-6632.2009.04480.x, 19686199.
17. Hevezi P, Moyer BD, Lu M, Gao N, White E, Echeverri F, Kalabat D, Soto H, Laita B, Li C, et al. Genome-wide analysis of gene expression in primate taste buds reveals links to diverse processes. PLoS One 2009, 4(7):e6395. 10.1371/journal.pone.0006395, 2712080, 19636377.
18. Delay RJ, Kinnamon JC, Roper SD. Ultrastructure of mouse vallate taste buds: II. Cell types and cell lineage. J Comp Neurol 1986, 253(2):242-252. 10.1002/cne.902530210, 3793992.
19. Finger TE. Cell types and lineages in taste buds. Chem Senses 2005, 30:i54-i55. 10.1093/chemse/bjh110, 15738192.
20. Lindemann B. Receptors and transduction in taste. Nature 2001, 413(6852):219-225. 10.1038/35093032, 11557991.
21. Breslin PA, Huang L. Human taste: peripheral anatomy, taste transduction, and coding. Adv Otorhinolaryngol 2006, 63:152-190.
22. Beidler LM, Smallman RL. Renewal of cells within taste buds. J Cell Biol 1965, 27:263-272. 10.1083/jcb.27.2.263, 2106718, 5884625.
23. Conger AD, Wells MA. Radiation and aging effect on taste structure and function. Radiation Research 1969, 37:31-49. 10.2307/3572749, 5762923.
24. Farbman AI. Renewal of taste bud cells in rat circumvallate papillae. Cell Tissue Kinet 1980, 13:349-357.
25. Mistretta CM, Hill DL. Development of the taste system: basic neurobiology. In Handbook of Olfaction and Gustation 2003, 759-782. New York, Marcel Dekker, Doty RL, 2.
26. Cho YK, Farbman AI, Smith DV. The timing of alpha-gustducin expression during cell renewal in rat vallate taste buds. Chem Senses 1998, 23:735-742. 10.1093/chemse/23.6.735, 9915120.
27. Hamamichi R, Asano-Miyoshi M, Emori Y. Taste bud contains both short-lived and long-lived cell populations. Neuroscience 2006, 141(4):2129-2138. 10.1016/j.neuroscience.2006.05.061, 16843606.
28. Zeng Q, Oakley B. p53 and bax: putative death factors in taste cell turnover. J Comp Neurol 1999, 413:168-180. 10.1002/(SICI)1096-9861(19991011)413:1<168::AID-CNE12>3.0.CO;2-Y, 10464378.
29. Zeng Q, Kwan A, Oakley B. Gustatory innervation and bax-dependent caspase-2: participants in the life and death pathways of mouse taste receptor cells. J Comp Neurol 2000, 424:640-650. 10.1002/1096-9861(20000904)424:4<640::AID-CNE6>3.0.CO;2-N, 10931486.
30. Guth L. The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat. Anat Rec 1957, 128:715-731. 10.1002/ar.1091280406, 13478886.
31. Fujimoto S, Murray RG. Fine structure of degeneration and regeneration in denervated rabbit vallate taste buds. Anat Rec 1970, 225:224-231.
32. Takeda M, Suzuki Y, Obara N, Nagai Y. Apoptosis in mouse taste buds after denervation. Cell Tissue Res 1996, 286:55-62. 10.1007/s004410050674, 8781212.
33. Huang YJ, Lu JS. TUNEL staining and electron microscopy studies of apoptotic changes in the guinea pig vallate taste cells after unilateral glossopharyngeal denervation. Anat Embryol 2001, 204:493-501. 10.1007/s429-001-8006-1, 11876535.
34. Hendricks SJ, Brunjes PC, Hill DL. Taste bud cell dynamics during normal and sodium-restricted development. J Comp Neurol 2004, 472:173-182. 10.1002/cne.20064, 15048685.
35. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci USA 2003, 100(14):8514-8519. 10.1073/pnas.1432609100, 166260, 12824464.
36. Tang SC, Lathia JD, Selvaraj PK, Jo DG, Mughal MR, Cheng A, Siler DA, Markesbery WR, Arumugam TV, Mattson MP. Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp Neurol 2008, 213(1):114-121. 10.1016/j.expneurol.2008.05.014, 2597513, 18586243.
37. Lehnardt S, Schott E, Trimbuch T, Laubisch D, Krueger C, Wulczyn G, Nitsch R, Weber JR. A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J Neurosci 2008, 28(10):2320-2331. 10.1523/JNEUROSCI.4760-07.2008, 18322079.
38. Okun E, Griffioen KJ, Lathia JD, Tang SC, Mattson MP, Arumugam TV. Toll-like receptors in neurodegeneration. Brain Res Rev 2009, 59(2):278-292. 10.1016/j.brainresrev.2008.09.001, 2679904, 18822314.
39. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302(5651):1760-1765. 10.1126/science.1088417, 14615545.
40. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 2003, 100(23):13632-13637. 10.1073/pnas.2234031100, 263865, 14581618.
41. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, Jacobsen SE, Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 2006, 26(38):9703-9712. 10.1523/JNEUROSCI.2723-06.2006, 16988041.
42. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 2007, 9(9):1081-1088. 10.1038/ncb1629, 17704767.
43. Whitney NP, Eidem TM, Peng H, Huang Y, Zheng JC. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J Neurochem 2009, 108(6):1343-1359. 10.1111/j.1471-4159.2009.05886.x, 2707502, 19154336.
44. Roper SD. The cell biology of vertebrate taste receptors. Annu Rev Neurosci 1989, 12:329-353. 10.1146/annurev.ne.12.030189.001553, 2648951.
45. Seta Y, Toyono T, Takeda S, Toyoshima K. Expression of Mash1 in basal cells of rate circumvallate taste buds is dependent upon gustatory innervation. FEBS Lett 1999, 444:43-46. 10.1016/S0014-5793(99)00023-X, 10037145.
46. Seta Y, Stoick-Cooper CL, Toyono T, Kataoka S, Toyoshima K, Barlow LA. The bHLH transcription factors, Hes6 and Mash1, are expressed in distinct subsets of cells within adult mouse taste buds. Arch Histol Cytol 2006, 69(3):189-198. 10.1679/aohc.69.189, 17031025.
47. Okubo T, Clark C, Hogan BL. Cell lineage mapping of taste bud cells and keratinocytes in the mouse tongue and soft palate. Stem Cells 2009, 27(2):442-450. 10.1634/stemcells.2008-0611, 19038788.
48. Kawai T, Akira S. TLR signaling. Semin Immunol 2007, 19(1):24-32. 10.1016/j.smim.2006.12.004, 17275323.
49. Hodgson JC. Endotoxin and mammalian host responses during experimental disease. J Comp Pathol 2006, 135(4):157-175. 10.1016/j.jcpa.2006.09.001, 17101336.
50. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003, 421:384-488. 10.1038/nature01339, 12508119.
51. Cavallin MA, McCluskey LP. Upregulation of the chemokine monocyte chemoattractant protein-1 following unilateral nerve injury in the peripheral taste system. Neurosci Lett 2007, 413(3):187-190. 10.1016/j.neulet.2006.11.042, 17174471.
52. Bezencon C, le Coutre J, Damak S. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 2007, 32(1):41-49. 10.1093/chemse/bjl034, 17030556.
53. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol 2006, 4:7. 10.1186/1741-7007-4-7, 1444931, 16573824.
54. Wang H, Iguchi N, Rong Q, Zhou M, Ogunkorode M, Inoue M, Pribitkin EA, Bachmanov AA, Margolskee RF, Pfeifer K, et al. Expression of the voltage-gated potassium channel KCNQ1 in mammalian taste bud cells and the effect of its null-mutation on taste preferences. J Comp Neurol 2009, 512(3):384-398. 10.1002/cne.21899, 2734193, 19006182.
55. Thirumangalathu S, Harlow DE, Driskell AL, Krimm RF, Barlow LA. Fate mapping of mammalian embryonic taste bud progenitors. Development 2009, 136(9):1519-1528. 10.1242/dev.029090, 2674259,2674259, 19363153.
56. Okubo T, Pevny LH, Hogan BL. Sox2 is required for development of taste bud sensory cells. Genes Dev 2006, 20(19):2654-2659. 10.1101/gad.1457106, 1578692, 17015430.
57. Hirota M, Ito T, Okudela K, Kawabe R, Hayashi H, Yazawa T, Fujita K, Kitamura H. Expression of cyclin-dependent kinase inhibitors in taste buds of mouse and hamster. Tissue & Cell 2001, 33:25-32.
58. Miura H, Kusakabe Y, Sugiyama C, Kawamatsu M, Ninomiya Y, Motoyama J, Hino A. Shh and Ptc are associated with taste bud maintenance in the adult mouse. Mech Dev 2001, 106(1-2):143-145. 10.1016/S0925-4773(01)00414-2, 11472844.
59. Kubbutat MH, Key G, Duchrow M, Schluter C, Flad HD, Gerdes J. Epitope analysis of antibodies recognising the cell proliferation associated nuclear antigen previously defined by the antibody Ki-67 (Ki-67 protein). J Clin Pathol 1994, 47(6):524-528. 10.1136/jcp.47.6.524, 494740, 7520455.
60. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 2001, 27(3):247-254. 10.1038/85798, 11242102.
61. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 2009, 28(33):2925-2939. 10.1038/onc.2009.170, 19561645.
62. Draviam VM, Orrechia S, Lowe M, Pardi R, Pines J. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J Cell Biol 2001, 152(5):945-958. 10.1083/jcb.152.5.945, 2198800, 11238451.
63. Crosby ME, Almasan A. Opposing roles of E2Fs in cell proliferation and death. Cancer Biol Ther 2004, 3(12):1208-1211. 2519115, 15662116.
64. Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009, 158(3):1021-1029. 10.1016/j.neuroscience.2008.06.052, 18662748.
65. McCoy MK, Tansey MG. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation 2008, 5:45. 10.1186/1742-2094-5-45, 2577641, 18925972.
66. Vallieres L, Campbell IL, Gage FH, Sawchenko PE. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 2002, 22(2):486-492.
67. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002, 420:860-867. 10.1038/nature01322, 2803035, 12490959.
68. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124(4):783-801. 10.1016/j.cell.2006.02.015, 16497588.
69. Aubert A, Dantzer R. The taste of sickness: lipopolysaccharide-induced finickiness in rats. Physiol Behav 2005, 84:437-444. 10.1016/j.physbeh.2005.01.006, 15763581.
70. Foster RF, Thompson JM, Kaufman SJ. A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using antidesmin and anti-BrdUrd monoclonal antibodies. Dev Biol 1987, 122(1):11-20. 10.1016/0012-1606(87)90327-7, 3297850.
71. George-Weinstein M, Foster RF, Gerhart JV, Kaufman SJ. In vitro and in vivo expression of alpha 7 integrin and desmin define the primary and secondary myogenic lineages. Dev Biol 1993, 156(1):209-229. 10.1006/dbio.1993.1071, 8449367.
72. Liao T, Wang L, Halm ST, Lu L, Fyffe RE, Halm DR. K+ channel KVLQT1 located in the basolateral membrane of distal colonic epithelium is not essential for activating Cl- secretion. Am J Physiol Cell Physiol 2005, 289(3):C564-575. 10.1152/ajpcell.00561.2004, 15843438.
73. Borgs L, Beukelaers P, Vandenbosch R, Nguyen L, Moonen G, Maquet P, Albrecht U, Belachew S, Malgrange B. Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 2009, 10:30. 10.1186/1471-2202-10-30, 2714160, 19327139.
74. kerlund K, Erlandsson Harris H, Tracey KJ, Wang H, Fehniger T, Klareskog L, Andersson J, Andersson U. Anti-inflammatory effects of a new tumour necrosis factor-alpha (TNF-alpha) inhibitor (CNI-1493) in collagen-induced arthritis (CIA) in rats. Clin Exp Immunol 1999, 115(1):32-41. 10.1046/j.1365-2249.1999.00750.x, 1905187, 9933418.
75. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.