Inflammation activates the interferon signaling pathways in taste bud cells

Journal of Neuroscience

Volumn 27, Issue 40, 2007, Pages 10703-10713

  Wang, Hong ^a   Zhou, Minliang ^a   Brand, Joseph ^a,b   Huang, Liquan ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytokine; Gene expression; Inflammation; Interferon; Taste bud; Taste disorder

Indexed keywords

CELL ADHESION MOLECULE; GAMMA INTERFERON RECEPTOR; INTERFERON; LIPOPOLYSACCHARIDE; POLYINOSINIC POLYCYTIDYLIC ACID; RECOMBINANT ALPHA INTERFERON; RECOMBINANT GAMMA INTERFERON; STAT1 PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; INFLAMMATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TASTE BUD;

ANIMALS; APOPTOSIS; CELLS, CULTURED; EPITHELIUM; GENE EXPRESSION REGULATION; INFLAMMATION; INTERFERONS; MICE; MICE, INBRED C57BL; MODELS, IMMUNOLOGICAL; POLY I-C; POLYSACCHARIDES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERFERON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TASTE BUDS; TASTE DISORDERS;

EID: 35148889822     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3102-07.2007     Document Type: Article

References (102)

1. Abdollahi M, Radfar M (2003) A review of drug-induced oral reactions. J Contemp Dent Pract 4:10-31.
2. Aubert A, Dantzer R (2005) The taste of sickness: lipopolysaccharide- induced finickiness in rats. Physiol Behav 84:437-444.
3. Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK, Archer DR, Barber GN (2000) Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13:129-141.
4. Banchereau J, Pascual V (2006) Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25:383-392.
5. Bartoshuk L, Desnoyers S, Hudson C, Marks L, O'Brien M (1987) Tasting on localized areas. Ann NY Acad Sci 510:166-168.
6. Begitt A, Meyer T, van Rossum M, Vinkemeier U (2000) Nucleocytoplasmic translocation of Stat1 is regulated by a leucine-rich export signal in the coiled-coil domain. Proc Natl Acad Sci USA 97:10418-10423.
7. Beidler LM, Smallman RL (1965) Renewal of cells within taste buds. J Cell Biol 27:263-272.
8. Bernabei P, Coccia EM, Rigamonti L, Bosticardo M, Forni G, Pestka S, Krause CD, Battistini A, Novelli F (2001) Interferon-γ receptor 2 expression as the deciding factor in human T, B, and myeloid cell proliferation or death. J Leukoc Biol 70:950-960.
9. Brämerson A, Johansson L, EK L, Nordin S, Benda M (2004) Prevalence of olfactory dysfunction: the skövde population-based study. Laryngoscope 114:733-737.
10. Bromley SM (2000) Smell and taste disorders: a primary care approach. Am Fam Physician 61:427-438.
11. Bromley SM, Doty RL (2003) Clinical disorders affecting taste: evaluation and management. In: Handbook of olfaction and gestation, Ed 2 (Doty RL, ed), pp 935-957. New York: Dekker.
12. Cao Y, Shreffler C, Herness S (2002) Localization and functional investigation of the transcription factor CREB in taste receptor cells. NeuroReport 13:1321-1325.
13. Caraglia M, Marra M, Pelaia G, Maselli R, Caputi M, Marsico SA, Abbruzzese A (2005) Alpha-interferon and its effects on signal transduction pathways. J Cell Physiol 202:323-335.
14. Chan CY, Yoo JE, Travers SP (2004) Diverse bitter stimuli elicit highly similar patterns of Fos-like immunoreactivity in the nucleus of the solitary tract. Chem Senses 29:573-581.
15. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, Borden EC (2003) Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237-249.
16. Chin YE, Kitagawa M, Kuida K, Flavell RA, Fu XY (1997) Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol Cell Biol 17:5328-5337.
17. Choubey D, Li SJ, Datta B, Gutterman JU, Lengyel P (1996) Inhibition of E2F-mediated transcription by p202. EMBO J 15:5668-5678.
18. Conger AD, Wells MA (1969) Radiation and aging effect on taste structure and function. Radiat Res 37:31-49.
19. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860-867.
20. Crow MK (2003) Type I interferon and autoimmune disease. Autoimmunity 36:445-446.
21. Cullen MM, Leopold DA (1999) Disorders of smell and taste. Med Clin North Am 83:57-74.
22. Dafny N, Yang PB (2005) Interferon and the central nervous system. Eur J Pharmacol 523:1-15.
23. Darnell JE (1997) STATs and gene regulation. Science 277:1630-1635.
24. Deems DA, Doty RL, Settle RG, Moore-Gillon V, Shaman P, Mester AF, Kimmelman CP, Brightman VJ, Snow JB (1991) Smell and taste disorders, a study of 750 patients from the University of Pennsylvania Smell and Taste Center. Arch Otolaryngol Head Neck Surg 117:519-528.
25. Der SD, Zhou A, Williams BRG, Silverman RH (1998) Identification of genes differentially regulated by interferon α, β, or γ using oligonucleotide arrays. Proc Natl Acad Sci USA 95:15623-15628.
26. Esses BA, Jafek BW, Hommel DJ, Eller PM (1988) Histological and ultrastructural changes of the murine taste bud following ionizing irradiation. Ear Nose Throat J 67:478-493.
27. Federici M, Giustizieri ML, Scarponi C, Girolomoni G, Albanesi C (2002) Impaired IFN-gamma-dependent inflammatory responses in human keratinocytes overexpressing the suppressor of cytokine signaling 1. J Immunol 169:434-442.
28. Finger TE (2005) Cell types and lineages in taste buds. Chem Senses 30:i54-i55.
29. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310:1495-1499.
30. Furuta S, Goto H, Niwa Y, Ohmiya N, Kamiya K, Oguri A, Hayakawa T, Mori N (2002) Interferon-gamma regulates apoptosis by releasing soluble tumor necrosis factor receptors in a gastric epithelial cell line. J Gastroenterol Hepatol 17:1283-1290.
31. Garnier P, Ying W, Swanson RA (2003) Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci 23:7967-7973.
32. Goodspeed RB, Gent JF, Catalanotto FA (1987) Chemosensory dysfunction. Clinical evaluation results from a taste and smell clinic. Postgrad Med 81:251-260.
33. Graham CS, Graham BG, Bartlett JA, Heald AE, Schiffman SS (1995) Taste and smell losses in HIV infected patients. Physiol Behav 58:287-293.
34. Gresser I (1990) Biologic effects of interferons. J Invest Dermatol 95:S66-S71.
35. Guha-Thakurta N, Majde JA (1997) Early induction of proinflammatory cytokine and type I interferon mRNAs following Newcastle disease virus, poly[rI:rC], or low-dose LPS challenge of the mouse. J Interferon Cytokine Res 17:197-204.
36. Hagberg H, Mallard C (2005) Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 18:117-123.
37. Hardy MP, Hertzog PJ, Owczarek CM (2002) Multiple regions within the promoter of the murine Ifnar-2 gene confer basal and inducible expression. Biochem J 365:355-367.
38. Harris R, Davidson TM, Murphy C, Gilbert PE, Chen M (2006) Clinical evaluation and symptoms of chemosensory impairment: one thousand consecutive cases form the dysfunction clinic in San Diego. Am J Rhinol 20:101-108.
39. Heald AE, Pieper CF, Schiffman SS (1998) Taste and smell complaints in HIV-infected patients. AIDS 12:1667-1674.
40. Henkin RI, Larson AL, Powell RD (1975) Hypogeusia, dysgeusia, hyposmia, and dysosmia following influenza-like infection. Ann Otol 84:672-682.
41. Hodgson JC (2006) Endotoxin and mammalian host responses during experimental disease. J Comp Pathol 135:157-175.
42. Hoffman HJ, Ishii EK, MacTurk RH (1998) Age-related changes in the prevalence of smell/taste problems among the United States adult population. Ann NY Acad Sci 855:716-722.
43. Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF (1999) Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci 2:1055-1062.
44. Huang L, Cao J, Wang H, Vo LA, Brand JG (2005) Identification and functional characterization of a voltage-gated chloride channel and its novel splice variant in taste bud cells. J Biol Chem 280:36150-36157.
45. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 104:6436-6441.
46. Jones GJ, Itri LM (1986) Safety and tolerance of recombinant interferon alfa-2a (Roferon-A) in cancer patients. Cancer 57:1709-1715.
47. Kalvakolanu DV (2000) Interferons and cell growth control. Histol Histopathol 15:523-537.
48. Kalvakolanu DV (2003) Alternate interferon signaling pathways. Pharmacol Ther 100:1-29.
49. Kellokumpu-Lehtinen P, Nordman E, Toivanen A (1989) Combined interferon and vinblastine treatment of advanced melanoma: evaluation of the treatment results and the effects of the treatment on immunological functions. Cancer Immunol Immunother 28:213-217.
50. Kern RC, Conley DB, Haines GK, Robinson AM (2004) Pathology of the olfactory mucosa: implications for the treatment of olfactory dysfunction. Laryngoscope 114:279-285.
51. Kimura-Takeuchi M, Majde JA, Toth LA, Krueger JM (1992) The role of double-stranded RNA in induction of the acute-phase response in an abortive influenza virus infection model. J Infect Dis 166:1266-1275.
52. Kinnamon JC, Taylor BJ, Delay RJ, Roper SD (1985) Ultrastructure of mouse vallate taste buds. I. Taste cells and their associated synapses. J Comp Neurol 235:48-60.
53. Konur A, Schulz U, Eissner G, Andreesen R, Holler E (2005) Interferon (IFN)-gamma is a main mediator of keratinocyte (HaCaT) apoptosis and contributes to autocrine IFN-gamma and tumour necrosis factor-alpha production. Br J Dermatol 152:1134-1142.
54. Kraus I, Vitezic D (2000) Anosmia induced with alpha interferon in a patient with chronic hepatitis C. Int J Clin Pharmacol Ther 38:360-361.
55. Landis BN, Konnerth CG, Hummel T (2004) A study on the frequency of olfactory dysfunction. Laryngoscope 114:1764-1769.
56. Landis BN, Beutner D, Frasnelli J, Huttenbrink KB, Hummel T (2005) Gustatory function in chronic inflammatory middle ear diseases. Laryngoscope 115:1124-1127.
57. Lee SB, Rodriguez D, Rodriguez JR, Esteban M (1997) The apoptosis pathway triggered by the interferon-induced protein kinase PKR requires the third basic domain, initiates upstream of Bcl-2, and involves ICE-like proteases. Virology 231:81-88.
58. Lengyel P (1987) Double-stranded RNA and interferon action. J Interferon Res 7:511-519.
59. -ΔΔCt method. Methods 25:402-408.
60. Lutfalla G, Holland SJ, Cinato E, Monneron D, Reboul J, Rogers NC, Smith JM, Stark GR, Gardiner K, Mogensen KE, Kerr IM, Uze G (1995) Mutant U5A cells are complemented by an interferon-αβ receptor subunit generated by alternative processing of a new member of a cytokine receptor gene cluster. EMBO J 14:5100-5108.
61. Majde JA (2000) Viral double-stranded RNA, cytokines, and the flu. J Interferon Cytokine Res 20:250-272.
62. Mann NM (2002) Management of smell and taste problems. Cleveland Clin J Med 69:329-336.
63. Mistretta CM (1984) Aging effects on anatomy and neurophysiology of taste and smell. Gerontology 3:131-136.
64. Mistretta CM, Hill DL (2003) Development of the taste system: basic neurobiology. In: Handbook of olfaction and gustation. Ed 2 (Doty RL, ed), pp 759-782. New York: Dekker.
65. Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM (2002) Prevalence of olfactory impairment in older adults. JAMA 288:2307-2312.
66. Murray RG (1973) The ultrastructure of taste buds. In: The ultrastructure of sensory organs (Friedmann I, ed), pp 1-81. Amsterdam: North Holland Publishing.
67. Nathan C (2002) Points of control in inflammation. Nature 420:846-852.
68. Nelson GM (1998) Biology of taste buds and the clinical problem of taste loss. Anat Rec 253:70-78.
69. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T, Yu VL, Miller DK (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37-43.
70. Norlin EM, Vedin V, Bohm S, Berghard A (2005) Odorant-dependent, spatially restricted induction of c-fos in the olfactory epithelium of the mouse. J Neurochem 93:1594-1602.
71. Novelli F, Bernabei P, Ozmen L, Rigamonti L, Allione A, Pestka S, Garotta G, Forni G (1996) Switching on of the proliferation or apoptosis of activated human T lymphocytes by IFN-gamma is correlated with the differential expression of the alpha- and beta-chains of its receptor. J Immunol 157:1935-1943.
72. Owczarek CM, Hwang SY, Holland KA, Gulluyan LM, Tavaria M, Weaver B, Reich NC, Kola I, Hertzog PJ (1997) Cloning and characterization of soluble and transmembrane isoforms of a novel component of the murine type I interferon receptor, IFNAR 2. J Biol Chem 272:23865-23870.
73. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169-1176.
74. Pestka S (1997) The interferon receptors. Semin Oncol 24:S9-S40.
75. Popko B, Corbin JG, Baerwald KD, Dupree J, Garcia AM (1997) The effects of interferon-gamma on the central nervous system. Mol Neurobiol 14:19-35.
76. Pribitkin E, Rosenthal MD, Cowart BJ (2003) Prevalence and causes of severe taste loss in a chemosensory clinic population. Ann Otol Rhinol Laryngol 112:971-978.
77. Pumplin DW, Getschman E (2000) Synaptic proteins in rat taste bud cells: appearance in the Golgi apparatus and relationship to alpha-gustducin and the Lewis. (b) and A antigens. J Comp Neurol 427:171-184.
78. Royuela M, de Miguel MP, Ruiz A, Fraile B, Arenas MI, Romo E, Paniagua R (2000) Interferon-gamma and its functional receptors overexpression in benign prostatic hyperplasia and prostatic carcinoma: parallelism with c-myc and p53 expression. Eur Cytokine Netw 11:119-127.
79. Saito A, Narasimhan P, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH (2004) Neuroprotective role of a proline-rich Akt substrate in apoptotic neuronal cell death after stroke: relationships with nerve growth factor. J Neurosci 24:1584-1593.
80. Sakaguchi S, Negishi H, Asagiri M, Nakajima C, Mizutani T, Takaoka A, Honda K, Taniguchi T (2003) Essential role of IRF-3 in lipopolysaccharide- induced interferon-beta gene expression and endotoxin shock. Biochem Biophys Res Commun 306:860-866.
81. Sánchez-Gómez MV, Alberdi E, Ibarretxe G, Torre I, Matute C (2003) Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 23:9519-9528.
82. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin- labelled cRNA probes. Histochemistry 100:431-440.
83. Schiffman SS, Graham BG (2000) Taste and smell perception affect appetite and immunity in the elderly. Eur J Clin Nutr 54:S54-S63.
84. Sen GC, Lengyel P (1992) The interferon system. A bird's eye view of its biochemistry. J Biol Chem 267:5017-5020.
85. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116:1793-1801.
86. Spagnoli A, Torello M, Nagalla SR, Horton WA, Pattee P, Hwa V, Chiarelli F, Roberts CT, Rosenfeld RG (2002) Identification of STAT-1 as a molecular target of IGFBP-3 in the process of chondrogenesis. J Biol Chem 277:18860-18867.
87. Stetson DB, Medzhitov R (2006) Type I interferons in host defense. Immunity 25:373-381.
88. Stone LM, Tan SS, Tam PPL, Finger TE (2002) Analysis of cell lineage relationships in taste buds. J Neurosci 22:4522-4529.
89. Tanaka N, Ishihara M, Kitagawa M, Harada H, Kimura T, Matsuyama T, Lamphier MS, Aizawa S, Mak TW, Taniguchi T (1994) Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1. Cell 77:829-839.
90. Taniguchi T, Takaoka A (2001) A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol 2:378-386.
91. Theofilopoulos AN, Baccala R, Beutler B, Kono DH (2005) Type I Interferons (α/β) in Immunity and Autoimmunity. Annu Rev Immunol 23:307-335.
92. Travers SP (2002) Quinine and citric acid elicit distinctive Fos-like immunoreactivity in the rat nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 282:R1798-R1810.
93. van Boxel-Dezaire AHH, Rani MRS, Stark GR (2006) Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25:361-372.
94. Wang H, Liu C, Lu Y, Chatterjee G, Ma XY, Eisenman RN, Lengyel P (2000) The interferon- and differentiation-inducible p202a protein inhibits the transcriptional activity of c-Myc by blocking its association with Max. J Biol Chem 275:27377-27385.
95. Wang H, Ding B, Liu CJ, Ma XY, Deschamps S, Roe BA, Lengyel P (2002) The increase in levels of interferon-inducible proteins p202a and p202b and RNA-dependent protein kinase (PKR) during myoblast differentiation is due to transactivation by MyoD: their tissue distribution in uninfected mice does not depend on interferons. J Interferon Cytokine Res 22:729-737.
96. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384-488.
97. Witt M, Reutter K, Miller IJ (2003) Morphology of the peripheral taste system. In: Handbook of olfaction and gestation, Ed 2 (Doty RL, ed), pp 651-677. New York: Dekker.
98. Yamashita H, Nakagawa K, Tago M, Nakamura N, Shiraishi K, Eda M, Nakata H, Nagamatsu N, Yokoyama R, Onimura M, Ohtomo K (2006) Taste dysfunction in patients receiving radiotherapy. Head Neck 28:508-516.
99. Yee CL, Yang R, Böttger B, Finger TE, Kinnamon JC (2001) "Type III" cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol 440:97-108.
100. Yeh SS, Schuster MW (1999) Geriatric cachexia: the role of cytokines. Am J Clin Nutr 70:183-197.
101. Zeng Q, Oakley B (1999) p53 and Bax: putative death factors in taste cell turnover. J Comp Neurol 413:168-180.
102. Zipp F, Aktas O (2006) The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci 29:518-527.