The purpose of this review is to discuss molecular factors influencing nerve growth to teeth. The establishment of a sensory pulpal innervation occurs concurrently with tooth development. Epithelial/mesenchymal interactions initiate the tooth primordium and change it into a complex organ. The initial events seem to be controlled by the epithelium, and subsequently, the mesenchyme acquires odontogenic properties. As yet, no single initiating epithelial or mesenchymal factor has been identified. Axons reach the jaws before tooth formation and form terminals near odontogenic sites. In some species, local axons have an initiating function in odontogenesis, but it is not known if this is also the case with mammals. In diphyodont mammals, the primary dentition is replaced by a permanent dentition, which involves a profound remodeling of terminal pulpal axons. The molecular signals underlying this remodeling remain unknown. Due to the senescent deterioration of the dentition, the target area of tooth nerves shrinks with age, and these nerves show marked pathological-like changes. Nerve growth factor and possibly also brain-derived neurotrophic factor seem to be important in the formation of a sensory pulpal innervation. Neurotrophin-3 and -4/5 are probably not involved. In addition, glial cell line-derived neurotrophic factor, but not neurturin, seems to be involved in the control of pulpal axon growth. A variety of other growth factors may also influence developing tooth nerves. Many major extracellular matrix molecules, which can influence growing axons, are present in developing teeth. It is likely that these molecules influence the growing pulpal axons.
References
1.
Aldskogius H., Arvidson J., Grant G. (1992). Axotomy-induced changes in primary sensory neurons. In: Sensory neurons: diversity, development, plasticity. Scott SE, editor. Oxford: Oxford University Press, pp. 363-383.
2.
Asai T., Watanabe K., Ichihara-Tanaka K., Kaneda N., Kojima S., Iguchi A., et al. (1997). Identification of heparin-binding sites in midkine and their role in neurite-promotion. Biochem Biophys Res Commun236:66-70.
3.
Ayer-le Lievre C., Ståhlbom PA, Sara VR ( 1991). Expression of IGF-I and -II mRNA in the brain and craniofacial region of the rat fetus. Development111:105-115.
4.
Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H., Simburger KS, et al. (1998). Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron21:1291-1302.
5.
Barbacid M. (1995). Neurotrophic factors and their receptors. Curr Opin Cell Biol7:148-155.
6.
Berthold CH, Nordborg C., Hildebrand C., Conradi S., Sourander P., Lugnegard H. (1983). Sural nerve biopsies from workers with a history of chronic exposure to organic solvents and from normal control cases. Morphometric and ultrastructural studies. Acta Neuropathol62:73-86.
7.
Bhatnagar M., Cintra A., Tinner B., Agnati LF, Kerezoudis N., Edwall L., et al. (1995). Neurotensin-like immunoreactivity in odontoblasts and their processes in rat maxillary molar teeth and the effect of pulpotomy. Regul Pept58:141-147.
8.
Bongenhielm U., Haegerstrand A., Theodorsson E., Fried K. (1995). Effects of neuropeptides on growth of cultivated rat molar pulp fibroblasts. Regul Pept60:91-98.
9.
Brenan A. (1986). Innervation of the dental pulp during tooth succession in the cat. Brain Res382:250-256.
10.
Byers MR (1980). Development of sensory innervation in dentin. J Comp Neural191:413-427.
11.
Byers MR (1984). Dental sensory receptors. Int Rev Neurobiol25:39-94.
12.
Byers MR, Schatteman GC, Bothwell M. (1990). Multiple functions for NGF receptor in developing, aging and injured rat teeth are suggested by epithelial, mesenchymal and neural immunoreactivity. Development109:461-471.
13.
Byers MR, Wheeler EF, Bothwell M. (1992). Altered expression of NGF and P75 NGF-receptor by fibroblasts of injured teeth precedes sensory nerve sprouting. Growth Factors6:41-52.
14.
Byers MR, O'Neill PC, Nishimura MC, Philips HS, Albers KM (1997). Dependence of dental innervation on NGF: comparison of hetero- and homozygous mice lacking NGF with K14NGF transgenic or hybrid rescued TKO mice (abstract). Soc Neurosci23:1704.
15.
Carter BD, Kaltschmidt C., Kaltschmidt B., Offenhauser N., Bohm-Matthaei R., Baeuerle PA, et al. (1996). Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science272:542-545.
16.
Chai Y., Bringas P. Jr, Mogharei A., Shuler CF, Slavkin HC (1998). PDGF-A and PDGFR-alpha regulate tooth formation via autocrine mechanism during mandibular morphogenesis in vitro. Dev Dyn213:500-51 1.
17.
Chao MV ( 1992). Neurotrophin receptors: a window into neuronal differentiation. Neuron9:583-593.
18.
Chiego DJ Jr (1995). The early distribution and possible role of nerves during odontogenesis. Int J Dev Biol39:191-194.
19.
Christensen LR, Janas MS, Mollgard K., Kjaer I. (1993). An immunocytochemical study of the innervation of developing human fetal teeth using protein gene product 9.5 (PGP 9.5). Arch Oral Biol38:1113-1120.
Creedon DJ, Tansey MG, Baloh RH, Osborne PA, Lampe PA, Fahrner TJ, et al. (1997). Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc Natl Acad Sci USA94:7018-7023.
22.
D'Souza RN, Happonen RP, Ritter NM, Butler WT (1990). Temporal and spatial patterns of transforming growth factor-beta I expression in developing rat molars. Arch Oral Biol35:957-965.
23.
Davies AM (1988). The trigeminal system: an advantageous experimental model for studying neuronal development. Development103:175-183.
24.
Davies AM (1997). Studies of neurotrophin biology in the developing trigeminal system. J Anat191:483-491.
25.
Davies AM, Bandtlow C., Heumann R., Korsching S., Rohrer H., Thoenen H. (1987). Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature326:353-358.
26.
Diamond J., Coughlin M., Macintyre L., Holmes M., Visheau B. (1987). Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proc Natl Acad Sci USA84:6596-6600.
27.
Elshamy WM, Ernfors P. (1996). Requirement of neurotrophin-3 for the survival of proliferating trigeminal ganglion progenitor cells. Development122:2405-2414.
28.
Enokido Y., de Sauvage F., Hongo JA, Ninkina N., Rosenthal A., Buchman VL, et al. (1998). GFR alpha-4 and the tyrosine kinase Ret form a functional receptor complex for persephin. Curr Biol8:1019-1022.
29.
Foster E., Risling M., Fried K. (1995). TrkB-like immunoreactivity in trigeminal sensory nerve fibers of the rat molar tooth pulp: development and response to nerve injury. Brain Res686:123-133.
30.
Fried K. (1984). Structural development of the mental nerve. Anat Rec210:347-355.
31.
Fried K. (1987). Changes in innervation of dentin and pulp with age. Front Oral Physiol6:63-84.
32.
Fried K., Hildebrand C. (1981a). Pulpal axons in developing, mature, and aging feline permanent incisors. A study by electron microscopy. J Comp Neurol203:23-36.
33.
Fried K., Hildebrand C. (1981b). Developmental growth and degeneration of pulpal axons in feline primary incisors. J Comp Neurol203:37-51
34.
Fried K. Hildebrand C. (1982). Qualitative structural development of the feline inferior alveolar nerve. J Anat (Lond)134:517-531.
35.
Fried K., Risling M., Edwall L. Olgart L. (1992). Immunoelectron microscopic localization of laminin and collagen type IV in normal and denervated tooth pulp of the cat. Cell Tissue Res270:157-164.
36.
Fristad I., Heyeraas KJ, Kvinnsland I. (1994). Nerve fibres and cells immunoreactive to neurochemical markers in developing rat molars and supporting tissues. Arch Oral Biol39:633-646.
37.
Gillespie MJ, Stein RB (1983). The relationship between axon diameter, myelin thickness and conduction velocity during atrophy of mammalian peripheral nerves. Brain Res259:41-56.
38.
Glasstone S. ( 1967). Development of teeth in tissue culture. J Dent Res46:858-861.
39.
Granholm A., Srivastava N., Mott J., Henry S., Henry M., Westphal H., et al. (1997). Morphological alterations in the peripheral and central nervous system of mice lacking glial cell line-derived neurotrophic factor (GDNF): immunohistochemical studies. J Neurosci17:1168-1178.
40.
Heikinheimo K. (1994). Stage-specific expression of decapentaplegic-Vg-related genes 2, 4, and 6 (bone morphogenetic proteins 2, 4, and 6) during human tooth morphogenesis. J Dent Res73:590-597.
41.
Hempstead BL Martin-Zanca D., Kaplan DR, Parada LF, Chao MV ( 1991). High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature350:678-683.
42.
Hildebrand C. Fried K. Tuisku F., Johansson CS (1995). Teeth and tooth nerves. Progr Neurobiol45:165-222.
43.
Ibáñez CF, Ernfors P., Timmusk T., Ip NY, Arenas E., Yancopoulos GD, et al. (1993). Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development117:1345-1353.
44.
Imai H. Osumi-Yamashita N., Ninomiya Y., Eto K. (1996). Contribution of early-emigrating midbrain crest cells to the dental mesenchyme of the mandibular molar tooth in rat embryos. Dev Biol176:151-165.
45.
Imai H. Osumi N., Eto K. (1998). Contribution of foregut endoderm to tooth initiation of mandibular incisor in rat embryos Eur J Oral Sci106(Suppl 1): 19-23.
46.
Ishii DN, Glazner GW, Pu S-F. (1994). Role of insulin-like growth factors in peripheral nerve regeneration. Pharm Ther62:125-144.
47.
Iwasaki S. Hattori A., Sato M., Tsujimoto M., Kohno M. (1996). Characterization of the bone morphogenetic protein-2 as a neurotrophic factor. Induction of neuronal differentiation of PC12 cells in the absence of mitogen-activated protein kinase activation. J Biol Chem27117360-17365.
48.
Jaszai J., Farkas L., Gaiter D., Reuss B., Strelau J., Unsicker K., et al. (1998). GDNF-related factor persephin is widely distributed throughout the nervous system. J Neurosci Res53:494-501.
49.
Jing S., Wen D., Yu Y., Holst PL, Luo Y., Fang M., et al. (1996). GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF Cell85:1113-1124.
50.
Jing S., Yu Y., Fang M., Hu Z., Holst PL, Boone T., et al. (1997). GFRalpha-2 and GFRalpha-3 are two new receptors for ligands of the GDNF family. J Biol Chem272:33111-33117.
51.
Johansson C., Stenstrom M., Hildebrand C. (1996). Target influence on aging of myelinated sensory nerve fibres. Neurobiol Aging17:61-66.
52.
Johnson J., Oppenheim R. (1994). Neurotrophins. Keeping track of changing neurotrophic theory. Curr Biol4:662-665.
53.
Karlsson M., Hildebrand C. (1996). Postnatal development and aging of the rat ventral root L5: electron microscopic and immunohistochemical studies. J Comp Neurol364:211-218.
54.
Karlsson U., Johnsen D., Herman AM (1974). Early degenerative alterations in feline resorbing deciduous incisors as observed by electron microscopy. J Dent Res53:1428-1431.
55.
Kettunen P., Thesleff I. (1998). Expression and function of FGFs-4, -8, and -9 suggest functional redundancy and repetitive use as epithelial signals during tooth morphogenesis. Dev Dyn211:256-268.
56.
Klein R., Conway D., Parada LF, Barbacid M. (1990). The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell61:647-656.
57.
Klein RD, Sherman D., Ho WH, Stone D., Bennett GL, Moffat B., et al. (1997). A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature387:717-721.
58.
Kollar EJ, Lumsden AGS (1979). Tooth morphogenesis: the role of the innervation during induction and pattern formation. J Biol Buccale7:49-60.
59.
Kontges G., Lumsden A. (1996). Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development122:3229-3242.
60.
Kotzbauer PT, Lampe PA, Heuckeroth RO, Golden JP, Creedon DJ, Johnson EM Jr, et al. (1996). Neurturin, a relative of glial cell line-derived neurotrophic factor. Nature384:467-470.
61.
Krieglstein K., Unsicker K. (1996). Distinct modulatory actions of TGF-beta and LIF on neurotrophin-mediated survival of developing sensory neurons. Neurochem Res21:843-850.
62.
Lefebvre PP, Leprince P., Weber T., Rigo JM, Delree P., Moonen G. (1990). Neuronotrophic effect of developing otic vesicle on cochleo-vestibular neurons: evidence for nerve growth factor involvement. Brain Res507:254-260.
63.
Lefkowitz W., Bodecker CF, Mardfin DF (1953). Odontogenesis in the rat molar. J Dent Res32:749-772.
64.
Lewin GR, Barde YA (1996). Physiology of the neurotrophins. Ann Rev Neurosci19:289-317.
65.
Lieberman AR (1971). The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol14:49-124.
66.
Lin L-FH, Doherty D., Lile J., Bektesh S., Collins F. (1993). GDNF: a glial cell-line derived neurotrophic factor for midbrain dopaminergic neurons. Science260:1130-1132.
67.
Lindsay RM (1988). Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci8:2394-2405.
68.
Luckenbill-Edds L. (1997). Laminin and the mechanism of neuronal outgrowth. Brain Res Rev23:1-27.
69.
Lumsden AGS (1982). The developing innervation of the lower jaw and its relation to the formation of tooth germs in mouse embryos. In: Teeth: form, function and evolution. Kurten B, editor. New York: Columbia University Press, pp. 32-43.
70.
Lumsden AGS (1987). The neural crest contribution to tooth development in the mammalian embryo. In: Developmental and evolutionary aspects of the neural crest. Maderson P, editor. New York: Wiley, pp. 261-300.
71.
Lumsden AGS (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development103:155-169.
72.
Lumsden AGS, Buchanan JAG (1986). An experimental study of timing and topography of early tooth development in the mouse embryo with an analysis of the role of innervation. Arch Oral Biol31:301-311.
73.
Luukko K. (1997). Immunohistochemical localization of nerve fibres during development of embryonic rat molar using peripherin and protein gene product 9.5 antibodies. Arch Oral Biol42:189-195.
74.
Luukko K., Moshnyakov M., Sainio K., Saarma M., Sariola H., Thesleff I. (1996). Expression of neurotrophin receptors during rat tooth development is developmentally regulated, independent of innervation, and suggests functions in the regulation of morphogenesis and innervation. Dev Dyn206:87-99.
75.
Luukko K., Arumae U., Karavanov A., Moshnyakov M., Sainio K., Sariola H., et al. (1997a). Neurotrophin mRNA expression in the developing tooth suggests multiple roles in innervation and organogenesis. Dev Dyn210:117-129.
76.
Luukko K., Sainio K., Sariola H., Saarma M., Thesleff I. (1997b). Localization of nerve cells in the developing rat tooth. J Dent Res76:1350-1356.
77.
Luukko K., Suvanto P., Saarma M., Thesleff I. (1997c). Expression of GDNF and its receptors in developing tooth is developmentally regulated and suggests multiple roles in innervation and organogenesis. Dev Dyn210:463-471.
78.
Luukko K., Saarma M., Thesleff I. (1998). Neurturin mRNA expression suggests roles in trigeminal innervation of the first branchial arch and in tooth formation. Dev Dyn213:207-219.
79.
Maina F., Klein R. (1999). Hepatocyte growth factor, a versatile signal for developing neurons. Nature Neurosci2:213-217.
80.
Maliartchouk S., Saragovi HU (1997). Optimal nerve growth factor trophic signals mediated by synergy of TrkA and p75 receptor-specific ligands. I Neurosci17:6031-6037.
81.
Martini R. (1994). Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J Neurocytol23:1-28.
82.
Masure S., Cik M., Pangalos MN, Bonaventure P., Verhasselt P., Lesage AS, et al. (1998). Molecular cloning, expression and tissue distribution of glial-cell-line-derived neurotrophic factor family receptor alpha-3 (GFRalpha-3). Eur J Biochem51:622-630.
83.
McMahon SB, Armanini MP, Ling LH, Phillips HS (1994). Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron12:1161-1171.
84.
Middlemas DS, Lindberg RA, Hunter T. (1991). trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol11:143-153.
85.
Milbrandt J., de Sauvage FJ, Fahrner TJ, Baloh RH, Leitner ML, Tansey MG, et al. (1998). Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron20:245-253.
86.
Mina M., Kollar EJ (1987). The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch Oral Biol32:123-127.
87.
Mitsiadis TA, Dicou E., Joffre A., Magloire H. (1992). Immunohistochemical localization of nerve growth factor (NGF) and NGF receptor (NGF-R) in the developing first molar tooth of the rat. Differentiation49:47-61.
88.
Mitsiadis TA, Couble P., Dicou E., Rudkin B., Magloire H. (1993). Patterns of nerve growth factor (NGF), proNGF, and p75 NGF receptor expression in the rat incisor: comparison with expression in the molar. Differentiation54:161-175.
89.
Mitsiadis TA, Salmivirta M., Muramatsu T., Muramatsu H., Rauvala H., Lehtonen E., et al. (1995a). Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development121:37-51.
90.
Mitsiadis TA, Muramatsu T., Muramatsu H., Thesleff I. (1995b). Midkine (MK), a heparin-binding growth/differentiation factor, is regulated by retinoic acid and epithelial-mesenchymal interactions in the developing mouse tooth, and affects cell proliferation and morphogenesis. J Cell Biol129:267-281.
91.
Mohamed SS, Atkinson ME (1983). A histological study of the innervation of developing mouse teeth. J Anat (Lond)136:735-749.
92.
Mohiuddin L., Fernyhough P., Tomlinson DR (1996). Acidic fibroblast growth factor enhances neurite outgrowth and stimulates expression of GAP-43 and T alpha I alpha-tubulin in cultured neurones from adult rat dorsal root ganglia. Neurosci Lett215:111-114.
93.
Moiseiwitsch JR, Raymond JR Tamir H., Lauder JM (1998). Regulation by serotonin of tooth-germ morphogenesis and gene expression in mouse mandibular explant cultures. Arch Oral Biol43:789-800.
94.
Moore MW, Klein RD, Farinas I., Sauer H., Armanini M., Phillips H., et al. (1996). Renal and neuronal abnormalities in mice lacking GDNF. Nature382:76-79.
95.
Naftel JP, Shamssoolari A., Thueson RK (1992). Immunoassay evidence for a role of nerve growth factor in development of dental innervation. Proc Finn Dent Soc88:543-549.
96.
Naftel JP, Qian X.-B, Bernanke JM (1994). Effects of postnatal anti-nerve growth factor serum exposure on development of apical nerves in the rat molar. Dev Brain Res80:54-62.
97.
Nagahama SI, Cunningham ML, Lee MY, Byers MR (1998). Normal development of dental innervation and nerve/tissue interactions in the colony-stimulating factor-I deficient osteopetrotic mouse. Dev Dyn211:52-59.
98.
Nosrat CA, Tomac A., Lindqvist E., Lindskog S., Humpel C., Stromberg I., et al. (1996). Cellular expression of GDNF mRNA suggests multiple functions inside and outside the nervous system. Cell Tissue Res286:191-207.
99.
Nosrat CA Fried K., Olson L. (1997a). Retrograde transport of GDNF from vibrissae and teeth suggests a neurotrophic role for GDNF in the trigeminal system (abstract) Soc Neurosci23:2244.
100.
Nosrat CA, Fried K., Lindskog S., Olson L. (1997b). Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res290:569-580.
101.
Nosrat CA Tomac A., Hoffer BJ, Olson L. (1997c). Cellular and developmental patterns of expression of Ret and GDNFR-a mRNA. Exp Brain Res115:410-422.
102.
Nosrat CA, Fried K., Ebendal T., Olson L. (1998). NGF, BDNF, NT3, NT4 and GDNF in tooth development. Eur J Oral Sci106(Suppl I ) 94-99.
103.
Obara N., Takeda M. (1993a). Expression of neural cell adhesion molecule (NCAM) during the first molar development in the mouse. Anat Embryol187:209-219.
104.
Obara N. Takeda M. ( 1993b). Expression of neural cell adhesion molecule (NCAM) during second- and third-molar development in the mouse. Anat Embryol188:13-20.
105.
Patapoutian A. Backus C., Kispert A., Reichardt LF (1999). Regulation of neurotrophin-3 expression by epithelial-mesenchymal interactions: the role of Wnt factors. Science283:1180-1183.
106.
Paves H. Arumae U., Normet KJ, Saarma M. (1994). Effects of brain-derived neurotrophic factor and neurotrophin-4 on embryonic rat sensory neurons. In: Life and death of the nervous system: role of neurotrophic factors and their receptors. Ibáñez CF, Fuxe K, Hokfelt T, Jörnvall H, Olson L, Ottoson D, editors. Stockholm: Wenner-Gren International Series, pp. 191-202.
107.
Pearson AA (1977). The early innervation of developing deciduous teeth. J Anat123:563-577.
108.
Pichel JG, Shen LY, Sheng HZ, Granholm AC, Drago J., Grinberg A., et al. (1996). Defects in enteric innervation and kidney development in mice lacking GDNE Nature382:73-76.
109.
Purves D., Lichtman JW (1985). Principles of neural development. Sunderland, MA: Sinauer Associates Inc., pp. 3-22.
110.
Qian XB, Naftel JP (1996). Effects of neonatal exposure to anti-nerve growth factor on the number and size distribution of trigeminal neurones projecting to the molar dental pulp in rats. Arch Oral Biol41:359-367.
111.
Rabizadeh S., Oh J., Zhong LT, Yang J., Bitler CM, Butcher LL, et al. (1993). Induction of apoptosis by the low-affinity NGF receptor. Science261:345-348.
112.
Rauvala H., Peng HB ( 1997). HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Progr Neurobiol52:127-144.
113.
Ringstedt T., Ibáñez CF, Nosrat CA (1999). Role of BDNF in target invasion in the gustatory system. J Neurosci19:3507-3518.
114.
Robertson K., Mason I. ( 1997). The GDNF-RET signalling partnership. Trends Genet13:1-3.
115.
Ruch JV ( 1987). Determinisms of odontogenesis. Cell Biol Rev14:1-112.
116.
Sanchez MP, Silos-Santiago I., Frisen J. He B., Lira SA, Barbacid M. (1996). Renal agenesis and the absence of enteric neurons in mice lacking gdnf. Nature382:70-73.
117.
Sawada T., Inoue S. (1997). Basement membrane-like structures occurring on the surface of dental papilla mesenchymal cells during odontogenesis in the monkey Macaca fuscata. Eur J Oral Sci106(Suppl 1):126-131.
118.
Schuchardt A., D'Agati V., Larsson-Blomberg L., Costantini F., Pachnis V. (1994). Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature367:380-383.
119.
Sharpe P. (1995). Homeobox genes and orofacial development. Connect Tissue Res32:17-25.
120.
Shou J., Rim PC, Calof AL (1999). BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nature Neurosci2:339-345.
121.
Snider WD (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell77:627-638.
122.
Stainier DYR, Gilbert W. (1991). Neuronal differentiation and maturation in the mouse trigeminal sensory system in vivo and in vitro. J Comp Neurol311:300-312.
123.
Tabata MJ, Kim K., Liu IG, Yamashita K. Matsumura T., Kato J., et al. (1996). Hepatocyte growth factor is involved in the morphogenesis of tooth germ in murine molars. Development122:1243-1251.
124.
Terling C., Rass A., Mitsiadis TA, Fried K., Lendahl U., Wroblewski J. (1996). Expression of the intermediate filament nestin during rodent tooth development. Int J Dev Biol39:947-956.
125.
Thesleff I. (1976). Differentiation of odontogenic tissues in organ culture. Scand J Dent Res84:353-356.
126.
Thesleff I., Nieminen P. (1996). Tooth morphogenesis and cell differentiation. Curr Opin Cell Biol8:844-850.
127.
Thesleff I., Sharpe P. (1997). Signalling networks regulating dental development. Mech Dev67:111-123.
128.
Thesleff I., Barrach HI, Foidart JM, Vaheri A., Pratt RM, Martin GR (1981). Changes in the distribution of type IV collagen, laminin, proteoglycan, and fibronectin during mouse tooth development. Dev Biol81:182-192.
129.
Thesleff I., Mackie E., Vainio S., Chiquet-Ehrismann R. (1987). Changes in the distribution of tenascin during tooth development. Development101:289-296.
130.
Thesleff I., Vaahtokari A., Partanen AM (1995). Regulation of organogenesis. Common molecular mechanisms regulating the development of teeth and other organs. Int J Dev Biol39:35-50.
131.
Trantor IR, Messer HH, Birner R. (1995). The effects of neuropeptides (calcitonin gene-related peptide and substance P) on cultured human pulp cells. J Dent Res74:1066-1071.
132.
Treanor JJ, Goodman L., de Sauvage F., Stone DM, Poulsen KT, Beck CD, et al. (1996). Characterization of a multicomponent receptor for GDNF. Nature382:80-83.
133.
Trupp M., Ryden M., Jörnvall H., Funakoshi H., Timmusk T., Arenas E., et al. (1995). Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol130:137-148.
134.
Trupp M., Arenas E., Fainzilber M., Nilsson AS, Sieber BA, Grigoriou M., et al. (1996). Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature381:785-789.
135.
Tsoulfas P., Soppet D., Escandon E., Tessarollo L., Mendoza-Ramirez JL, Rosenthal A., et al. (1993). The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to NT-3 in PC12 cells. Neuron10:975-990.
136.
Tsuzuki H., Kitamura H. (1991). Immunohistochemical analysis of pulpal innervation in developing rat molars. Arch Oral Biol36:139-146.
137.
Tucker AS, Matthews KL, Sharpe PT (1998). Transformation of tooth type induced by inhibition of BMP signaling. Science282:1136-1138.
138.
Tuisku F., Hildebrand C. (1994). Evidence for a neural influence on tooth germ generation in a polyphyodont species. Dev Biol165:1-9.
139.
Uddman R., Kato J., Lindgren P., Sundler F., Edvinsson L. (1999). Expression of calcitonin gene-related peptide-I receptor mRNA in human tooth pulp and trigeminal ganglion. Arch Oral Biol44:1-6.
140.
Vaahtokari A., Vainio S., Thesleff I. (1991). Associations between transforming growth factor beta 1 RNA expression and epithelial-mesenchymal interactions during tooth morphogenesis. Development113:985-994.
141.
Vainio S., Karavanova I., Jowett A., Thesleff I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell8:45-58.
142.
Valenzuela DM, Maisonpierre PC, Glass DJ, Rojas E., Nunez L., Kong Y., et al. (1993). Alternative forms of rat trkC with different functional capabilities. Neuron10:963-974.
143.
Weil M., Itin A., Keshet E. (1995). A role for mesenchyme-derived tachykinins in tooth and mammary gland morphogenesis. Development121:2419-2428.
144.
Wells MR, Kraus K., Batter DK, Blunt DG, Weremowitz J., Lynch SE, et al. (1997). Gel matrix vehicles for growth factor application in nerve gap injuries repaired with tubes: a comparison of biomatrix, collagen, and methylcellulose. Exp Neural146:395-402.
145.
Westrum LE, Canfield RC (1979). Normal loss of milk teeth causes degeneration in brain stem. Exp Neurol65:169-177.
146.
Wilkinson GA, Farinas I., Backus C., Yoshida CK, Reichardt LF (1996). Neurotrophin-3 is a survival factor in vivo for early mouse trigeminal neurons. J Neurosci16:7661-7669.
147.
Wilson PA, Hemmati-Brivanlou A. (1995). Induction of epidermis and inhibition of neural fate by Bmp-4. Nature376:331-336.
148.
Zhou H., Welcher AA, Shooter EM (1997). BDNF/NT-4-5 receptor trkB and cadherin participate in cell-cell adhesion. J Neurosci Res49:281-291.
