Lingual BDNF and NT-3 mRNA expression patterns and their relation to innervation in the human tongue: Similarities and differences compared with rodents

Journal of Comparative Neurology

Volumn 417, Issue 2, 2000, Pages 133-152

  Nosrat, Irina V ^a   Lindskog, Sven ^a   Seiger, Åke ^a   Nosrat, Christopher A ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Development; Gustation; Lingual papillae; Neurotrophin; Taste buds

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEUROTROPHIN 3;

ADULT; ARTICLE; FEMALE; GUSTATORY NERVOUS SYSTEM; HISTOCHEMISTRY; HUMAN; HUMAN EXPERIMENT; MALE; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATOSENSORY SYSTEM; SPECIES DIFFERENCE; TASTE; TASTE BUD; TONGUE;

ADULT; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FETUS; GESTATIONAL AGE; HISTOCYTOCHEMISTRY; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVOUS SYSTEM; NERVOUS SYSTEM PHYSIOLOGY; NEUROTROPHIN 3; RNA, MESSENGER; RODENTIA; THIOLESTER HYDROLASES; TONGUE; UBIQUITIN THIOLESTERASE;

EID: 0034615040     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000207)417:2<133::AID-CNE1>3.0.CO;2-I     Document Type: Article

References (61)

1. Åkesson E, Kjaeldgaard A, Seiger Å. 1998. Human embryonic spinal cord grafts in adult rat spinal cord cavities: survival, growth, and interactions with the host. Exp Neurol 149:262-276.
2. Arvidson K, Friberg U. 1980. Human taste: response and taste bud number in fungiform papillae. Science 209:807-808.
3. Astbäck J, Arvidson K, Johansson O. 1995. Neurochemical markers of human fungiform papillae and taste buds. Regul Pept 59:389-398.
4. Barlow LA, Chien CB, Northcutt RG. 1996. Embryonic taste buds develop in the absence of innervation. Development 122:1103-1111.
5. Bradley RM. 1972. Development of the taste bud and gustatory papillae in human fetuses. In: Bosma JF, editor. Oral sensation and perception. Springfield: Charles C Thomas, p 137-162.
6. Bradley RM, Stern IB. 1967. The development of the human taste bud during the fetal period. J Anat 101:743-752.
7. Choi S, Yates PA, O'Leary DDM. 1998. Localized BDNF application induces branch-like structures along retinal axons. Soc Neurosci Abstr 24:27.
8. Coons AH. 1958. Fluorescent antibody methods. In: Danielli JF, editor. General cytochemical methods. New York: Academic Press. p 399-422.
9. Dagerlind Å, Friberg K, Bean AG, Hökfelt T. 1992. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98:39-49.
10. England MA. 1990. A colour atlas of life before birth, 2nd ed. Aylesbury, England: Hazell.
11. Ernfors P, Ibanez DF, Ebendal T, Olson L, Persson H. 1990. Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor. Proc Natl Acad Sci USA 87: 5454-5458.
12. Falci S, Holtz A, Åkesson E, Azizi M, Ertzgaard P, Hultling C, Kjaeldgaard A, Levi R, Ringdén O, Westgren M, Lammertse D, Seiger Å. 1997. Obliteration of a posttraumatic spinal cord cyst with solid human embryonic spinal cord grafts: first clinical attempt. J Neurotrauma 14:875-884.
13. Farbman AI. 1965. Electron microscope study of the developing taste bud in rat fungiform papilla. Dev Biol 11:110-135.
14. Farbman AI, Mbiene JP. 1991. Early development and innervation of taste bud-bearing papillae on the rat tongue. J Comp Neurol 304: 172-186.
15. Finger TE. 1986. Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallate papillae of the rat. Chem Senses 11:135-144.
16. Fritzsch B, Sarai PA, Barbacid M, Silossantiago I. 1997. Mice with a targeted disruption of the neurotrophin receptor trkB lose their gustatory ganglion cells early but do develop taste buds. Int J Dev Neurosci 15:563-576.
17. Ganchrow JR, Ganchrow D, Oppenheimer M. 1986. Chorda tympani innervation of anterior mandibular taste buds in the chicken. Anat Rec 216:434-439.
18. Ganchrow D, Ganchrow JR, Witt M. 1998. Aspects of chick taste bud development. In: Proceedings of the European Chemoreception Research Organization, XIII Congress, Siena, Italy.
19. GrÅberg J. 1898. Beiträge Zur Genese des Geschmaksorgans. Morph Arbeiten 8:117-131.
20. Hall JM, Hooper JE, Finger TE. 1999. Expression of sonic hedgehog, patched and gli1 in developing taste papillae of the mouse. J Comp Neurol 406:143-155.
21. Hellman TJ. 1927. Die Genes der Zungenpapillen beim Menschen. Uppsala Läk. Förh. 26-27:1-69.
22. Hersch M, Ganchrow D. 1980. Scanning electron microscopy of human embryonic and fetal tongue. Chem Senses 5:331-341.
23. Hilliges M, Astbäck J, Wang L, Arvidson K, Johansson O. 1996. Protein gene product 9.5-immunoreactive nerves and cells in human oral mucosa. Anat Record 245:621-632.
24. Hökfelt T, Fuxe K, Goldstein M, Joh TH. 1973. Immunohistochemical localization of three catecholamine synthesizing enzymes: aspects on methodology. Histochemie 33:231-254.
25. Jones KR, Reichardt LF. 1990. Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc Natl Acad Sci USA 87:8060-8064.
26. Jung H-S, Oropeza V, Thesleff I. 1999. Shh, Bmp-2, Bmp-4 and Fgf-8 are associated with initiation and patterning of mouse tongue papillae. Mech Dev 81:203-206.
27. Kinnamon JC. 1987. Organization and innervation of taste buds. In: Finger TE, Silver WL, editors. Neurobiology of taste and smell. New York: John Wiley & Sons, p 277-297.
28. Kinnamon SC, Margolskee RF. 1996. Mechanisms of taste transduction. Curr Opin Neurobiol 6:506-513.
29. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde YA. 1989. Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341:149-152.
30. Lewin GR, Barde YA. 1996. Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317.
31. Mbiene JP, Mistretta CM. 1997. Initial innervation of embryonic rat tongue and developing taste papillae. Acta Anat 160:139-158.
32. Miller IJ Jr. 1974. Branched chorda tympani neurons and interactions among taste receptors. J Comp Neurol 158:155-166.
33. Miller IJ Jr, Gomez MM, Lubarsky EH. 1978. Distribution of the facial nerve to taste receptors in the rat. Chem Sens Flavour 3:397-411.
34. Mistretta CM. 1991. Developmental neurobiology of the taste system. In: Getchell TV, editor. Smell and taste in health and disease. New York: Raven Press, p 35-64.
35. nd ed. San Diego: Academic Press, p 751-767.
36. Northcutt RG, Barlow LA. 1998. Amphibians provide new insights into taste-bud development. Trends Neurosci 21:38-43.
37. Nosrat CA. 1998. Neurotrophic factors in the tongue; expression patterns, biological activity, relation to innervation and studies of neurotrophin knockout mice. Ann NY Acad Sci 855:28-50.
38. Nosrat CA, Olson L. 1995. Brain-derived neurotrophic factor mRNA is expressed in the developing taste bud-bearing tongue papillae of rat. J Comp Neurol 360:698-704.
39. Nosrat CA, Olson L. 1998. Changes in neurotrophin 3 mRNA expression patterns in the prenatal rat tongue suggest guidance of developing somatosensory nerves to their final targets. Cell Tissue Res 292:619-623.
40. Nosrat CA, Ebendal T, Olson L. 1996. Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation. J Comp Neurol 376:587-602.
41. Nosrat CA, Blomlöf J, Elshamy WM, Ernfors P, Olson L. 1997. Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively. Development 124:1333-1342.
42. Oakley B. 1991. Neuronal-epithelial interactions in mammalian gustatory epithelium. Ciba Found Symp 160:277-287.
43. Oakley B. 1998. Vertebrate taste-bud development: are salamanders the model? Trends Neurosci 21:337.
44. Patapoutian A, Backus C, Kispert A, Reichardt LF. 1999. Regulation of neurotrophin-3 expression by epithelial-mesenchymal interactions: the role of Wnt factors. Science 283:1180-1183.
45. Pirvola U, Ylikoski J, Palgi J, Lehtonen E, Arumae U, Saarma M. 1992. Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglia. Proc Natl Acad Sci USA 89:9915-9919.
46. Ringstedt T, Ibáñez CF, Nosrat CA. 1999. Role of BDNF in target invasion in the gustatory system. J Neurosci 19:3507-3518.
47. Stone LS. 1940. The origin and development of taste organs in salamanders observed in the living condition. J Exp Zool 83:481-506.
48. Wakisaka S, Miyawaki Y, Youn SH, Kato J, Kurisu K. 1996. Protein gene-product 9.5 in developing mouse circumvallate papilla -comparison with neuron-specific enolase and calcitonin gene-related peptide. Anat Embryol 194:365-372.
49. Wakisaka S, Daikoku H, Miyawaki Y, Youn SH, Maeda T, Kurisu K. 1998. Immunohistochemical observation of growth-associated protein 43 (Gap-43) in the developing circumvallate papilla of the rat. Cell Tissue Res 293:499-507.
50. Westgren M, Ek S, Bui T, Jansson B, Kjaeldgaard A, Markling L, Neñ nesmo I, Seiger Å, Sarby B, Thornström S, Ringdén O. 1997. Tissue distribution of transplanted fetal liver cells in the human fetal recipient. Am J Obstet Gynecol 176:49-53.
51. Wetmore C, Olson L. 1995. Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J Comp Neurol 353: 143-159.
52. Wilson PO, Barber PC, Hamid QA, Power BF, Dhillon AP, Rode J, Day IN, Thompson RJ, Polak JM. 1988. The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br J Exp Pathol 69:91-104.
53. Witt M, Kasper M. 1998. Immunohistochemical distribution of CD44 and some of its isoforms during human taste bud development. Histochem Cell Biol 110:95-103.
54. Witt M, Kasper M. 1999. Distribution of cytokeratin filaments and vimentil in developing human taste buds. Anat Embryol 199:291-299.
55. Witt M, Reutter K. 1996. Embryonic and early fetal development of human taste buds: a transmission electron microscopical study. Anat Rec 246:507-523.
56. Witt M, Reutter K. 1997. Scanning electron microscopical studies of developing gustatory papillae in humans. Chem Senses 22:601-612.
57. Witt M, Reutter K. 1998. Innervation of developing human taste buds - an immunohistochemical study. Histochem Cell Biol 109:281-291.
58. Yamasaki H, Kubota Y, Takagi H, Tohyama M. 1984. Immunoelectron-microscopic study on the fine structure of substance-P-containing fibers in the taste buds of the rat. J Comp Neurol 227: 380-392.
59. Ylikoski J, Pirvola U, Moshnyakov M, Palgi J, Arumae U, Saarma M. 1993. Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear. Hear Res 65:69-78.
60. Zalewski AA. 1974. Neuronal and tissue specifications involved in taste bud formation. Ann NY Acad Sci 228:344-349.
61. Zhang CX, Brandemihl A, Lau D, Lawton A, Oakley B. 1997. BDNF is required for the normal development of taste neurons in vivo. Neuroreport 8:1013-1017.