The skin as a neurotrophic organ

Neuroscientist

Volumn 13, Issue 4, 2007, Pages 371-382

  Albers, Kathryn M ^a,b   Davis, Brian M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Neurotrophic factors; Sensory neuron; Skin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4;

CELL FUNCTION; CELL LINE; CELL MATURATION; CELL STRUCTURE; CELL TYPE; ENVIRONMENTAL CHANGE; GLIA CELL; HUMAN; MECHANICAL STIMULATION; MECHANORECEPTOR; NERVE CELL DIFFERENTIATION; NERVE FUNCTION; NEUROTROPISM; NOCICEPTIVE RECEPTOR; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SENSORY NERVE CELL; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SKIN; SKIN FUNCTION; SKIN NERVE; SKIN RECEPTOR; STIMULATION; SYMPATHETIC NERVE CELL; THERMAL STIMULATION;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; NEUROGLIA; NEURONS, AFFERENT; SKIN;

EID: 34447339933     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/10738584070130040901     Document Type: Review

References (120)

1. Airaksinen MS, Koltzenburg M., Lewin GR, Masu Y., Helbig C., Wolf E., and others. 1996. Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16 (2). 287 - 95.
2. Airaksinen MS, Saarma M. 2002. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3 (5). 383 - 94.
3. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davis BM 1996. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 134 (2). 487 - 97.
4. Albers KM, Woodbury CJ, Ritter AM, Davis BM, Koerber HR 2006. Glial cell-line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J Neurosci 26 (11). 2981 - 90.
5. Albers KM, Wright DE, Davis BM 1994. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14 (3 Pt 2). 1422 - 32.
6. Anand P. 2004. Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 146: 477 - 92.
7. Anand P., Pandya S., Ladiwala U., Singhal B., Sinicropi DV, Williams-Chestnut RE 1994. Depletion of nerve growth factor in leprosy. Lancet 344 (8915). 129 - 30.
8. Anand P., Terenghi G., Warner G., Kopelman P., Williams-Chestnut RE, Sinicropi DV 1996. The role of endogenous nerve growth factor in human diabetic neuropathy. Nat Med 2 (6). 703 - 7.
9. Andres R., Forgie A., Wyatt S., Chen Q., de Sauvage FJ, Davies AM 2001. Multiple effects of artemin on sympathetic neurone generation, survival and growth. Development 128 (19). 3685 - 95.
10. Angeletti RH, Bradshaw RA 1971. Nerve growth factor from mouse submaxillary gland: amino acid sequence. Proc Natl Acad Sci U S A 68 (10). 2417 - 20.
11. Apfel SC 2002. Nerve growth factor for the treatment of diabetic neuropathy: what went wrong, what went right, and what does the future hold? Int Rev Neurobiol 50: 393 - 413.
12. Baloh RH, Enomoto H., Johnson EM Jr, Milbrandt J. 2000. The GDNF family ligands and receptors-implications for neural development. Curr Opin Neurobiol 10 (1). 103 - 10.
13. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H., Simburger KS, and others. 1998. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 21 (6). 1291 - 302.
14. Barde YA, Edgar D., Thoenen H. 1982. Purification of a new neurotrophic factor from mammalian brain. Embo J 1 (5). 549 - 53.
15. Baudet C., Mikaels A., Westphal H., Johansen J., Johansen TE, Ernfors P. 2000. Positive and negative interactions of GDNF, NTN and ART in developing sensory neuron subpopulations, and their collaboration with neurotrophins. Development 127 (20). 4335 - 44.
16. Bhattacharyya A., Watson FL, Bradlee TA, Pomeroy SL, Stiles CD, Segal RA 1997. Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J Neurosci 17 (18). 7007 - 16.
17. Birren SJ, Lo L., Anderson DJ 1993. Sympathetic neuroblasts undergo a developmental switch in trophic dependence. Development 119 (3). 597 - 610.
18. Botchkarev VA, Metz M., Botchkareva NV, Welker P., Lommatzsch M., Renz H., Paus R. 1999. Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 act as "epitheliotrophins " in murine skin. Lab Invest 79 (5). 557 - 72.
19. Botchkarev VA, Yaar M., Peters EM, Raychaudhuri SP, Botchkareva NV, Marconi A., and others. 2006. Neurotrophins in skin biology and pathology. J Invest Dermatol 126 (8). 1719 - 27.
20. Brennan C., Rivas-Plata K., Landis SC 1999. The p75 neurotrophin receptor influences NT-3 responsiveness of sympathetic neurons in vivo. Nat Neurosci 2 (8). 699 - 705.
21. Buss RR, Sun W., Oppenheim RW 2006. Adaptive roles of programmed cell death during nervous system development (1). Annu Rev Neurosci 29: 1 - 35.
22. Campenot RB, MacInnis BL 2004. Retrograde transport of neurotrophins: fact and function. J Neurobiol 58 (2). 217 - 29.
23. Chen CL, Broom DC, Liu Y., de Nooij JC, Li Z., Cen C., and others. 2006. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49 (3). 365 - 77.
24. Christianson JA, Riekhof JT, Wright DE 2003. Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp Neurol 179 (2). 188 - 99.
25. Christianson JA, Ryals JM, McCarson KE, Wright DE 2003. Beneficial actions of neurotrophin treatment on diabetes-induced hypoalgesia in mice. J Pain 4 (9). 493 - 504.
26. Cohen S. 1960. Purification of a nerve-growth promoting protein from the mouse salivary gland and its neuro-cytotoxic antiserum. Proc Natl Acad Sci U S A 46 (3). 302 - 11.
27. Cowan WM 2001. Viktor Hamburger and Rita Levi-Montalcini: the path to the discovery of nerve growth factor. Annu Rev Neurosci 24: 551 - 600.
28. Crowley C., Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S., Armanini MP, and others. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76 (6). 1001 - 11.
29. 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. Nature 326 (6111). 353 - 8.
30. Davis BM, Albers KM, Seroogy KB, Katz DM 1994. Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349 (3). 464 - 74.
31. Davis BM, Fundin BT, Albers KM, Goodness TP, Cronk KM, Rice FL 1997. Overexpression of nerve growth factor in skin causes preferential increases among innervation to specific sensory targets. J Comp Neurol 387 (4). 489 - 506.
32. Davis BM, Goodness TP, Soria A., Albers KM 1998. Over-expression of NGF in skin causes formation of novel sympathetic projections to trkA-positive sensory neurons. Neuroreport 9 (6). 1103 - 7.
33. Davis BM, Wang HS, Albers KM, Carlson SL, Goodness TP, McKinnon D. 1996. Effects of NGF overexpression on anatomical and physiological properties of sympathetic postganglionic neurons. Brain Res 724 (1). 47 - 54.
34. Davis JB, Gray J., Gunthorpe MJ, Hatcher JP, Davey PT, Overend P., and others. 2000. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (6783). 183 - 7.
35. Dixon JE, McKinnon D. 1994. Expression of the trk gene family of neurotrophin receptors in prevertebral sympathetic ganglia. Brain Res Dev Brain Res 77 (2). 177 - 82.
36. Dyck PJ, Peroutka S., Rask C., Burton E., Baker MK, Lehman KA, and others. 1997. Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans. Neurology 48 (2). 501 - 5.
37. Elitt CM, McIlwrath SL, Lawson JJ, Malin SA, Molliver DC, Cornuet PK, and others. 2006. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J Neurosci 26 (33). 8578 - 87.
38. English KB, Burgess PR, Kavka-Van Norman D. 1980. Development of rat Merkel cells. J Comp Neurol 194 (2). 475 - 96.
39. Enomoto H., Araki T., Jackman A., Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J. 1998. GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21 (2). 317 - 24.
40. Epa WR, Markovska K., Barrett GL 2004. The p75 neurotrophin receptor enhances TrkA signalling by binding to Shc and augmenting its phosphorylation. J Neurochem 89 (2). 344 - 53.
41. Ernfors P., Lee KF, Kucera J., Jaenisch R. 1994. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77 (4). 503 - 12.
42. Facer P., Mann D., Mathur R., Pandya S., Ladiwala U., Singhal B., and others. 2000. Do nerve growth factor-related mechanisms contribute to loss of cutaneous nociception in leprosy? Pain 85 (1 - 2). 231 - 8.
43. Fagan AM, Zhang H., Landis S., Smeyne RJ, Silos-Santiago I., Barbacid M. 1996. TrkA, but not TrkC, receptors are essential for survival of sympathetic neurons in vivo. J Neurosci 16 (19). 6208 - 18.
44. Fan G., Egles C., Sun Y., Minichiello L., Renger JJ, Klein R., and others. 2000. Knocking the NT4 gene into the BDNF locus rescues BDNF deficient mice and reveals distinct NT4 and BDNF activities. Nat Neurosci 3 (4). 350 - 7.
45. Farinas I., Jones KR, Backus C., Wang XY, Reichardt LF 1994. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369 (6482). 658 - 61.
46. Figueiredo HF, Davis BM, Albers KM 2001. Skin-derived nerve growth factor blocks programmed cell death in the trigeminal ganglia but does not enhance neuron proliferation. Mech Dev 109 (2). 205 - 14.
47. Golden JP, DeMaro JA, Osborne PA, Milbrandt J., Johnson EM Jr. 1999. Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol 158 (2). 504 - 28.
48. Gonzalez-Martinez T., Farinas I., Del Valle ME, Feito J., Germana G., Cobo J., Vega JA 2005. BDNF, but not NT-4, is necessary for normal development of Meissner corpuscles. Neurosci Lett 377 (1). 12 - 5.
49. Guha U., Gomes WA, Samanta J., Gupta M., Rice FL, Kessler JA 2004. Target-derived BMP signaling limits sensory neuron number and the extent of peripheral innervation in vivo. Development 131 (5). 1175 - 86.
50. Halata Z., Kucera J., Kucera T., Grim M. 2005. Apoptosis of Merkel cells in neurotrophin-3 null mice. Anat Embryol (Berl) 209 (4). 335 - 40.
51. Hamburger V., Levi-Montalcini R. 1949. Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J Exp Zool 111: 457 - 502.
52. Harper S., Davies AM 1990. NGF mRNA expression in developing cutaneous epithelium related to innervation density. Development 110 (2). 515 - 9.
53. Harrison SM, Davis BM, Nishimura M., Albers KM, Jones ME, Phillips HS 2004. Rescue of NGF-deficient mice I: transgenic expression of NGF in skin rescues mice lacking endogenous NGF. Brain Res Mol Brain Res 122 (2). 116 - 25.
54. Hendry IA, Stockel K., Thoenen H., Iversen LL 1974. The retrograde axonal transport of nerve growth factor. Brain Res 68 (1). 103 - 21.
55. Heuckeroth RO, Enomoto H., Grider JR, Golden JP, Hanke JA, Jackman A., and others. 1999. Gene targeting reveals a critical role for neurturin in the development and maintenance of enteric, sensory, and parasympathetic neurons. Neuron 22 (2). 253 - 63.
56. Honma Y., Araki T., Gianino S., Bruce A., Heuckeroth R., Johnson E., Milbrandt J. 2002. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35 (2). 267 - 82.
57. Horton AR, Barlett PF, Pennica D., Davies AM 1998. Cytokines promote the survival of mouse cranial sensory neurones at different developmental stages. Eur J Neurosci 10 (2). 673 - 9.
58. Huang EJ, Reichardt LF 2001. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677 - 736.
59. Huang EJ, Reichardt LF 2003. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609 - 42.
60. Huang EJ, Wilkinson GA, Farinas I., Backus C., Zang K., Wong SL, Reichardt LF 1999. Expression of Trk receptors in the developing mouse trigeminal ganglion: in vivo evidence for NT-3 activation of TrkA and TrkB in addition to TrkC. Development 126 (10). 2191 - 203.
61. Isaacson LG, Crutcher KA 1998. Uninjured aged sympathetic neurons sprout in response to exogenous NGF in vivo. Neurobiol Aging 19 (4). 333 - 9.
62. Isaacson LG, Ondris D., Crutcher KA 1995. Plasticity of mature sensory cerebrovascular axons following intracranial infusion of nerve growth factor. J Comp Neurol 361 (3). 451 - 60.
63. Isaacson LG, Saffran BN, Crutcher KA 1992. Nerve growth factor-induced sprouting of mature, uninjured sympathetic axons. J Comp Neurol 326 (3). 327 - 36.
64. Jankowski MP, Cornuet PK, McIlwrath S., Koerber HR, Albers KM 2006. SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth. Neuroscience 143 (2). 501 - 14.
65. Johnson EM Jr, Andres RY, Bradshaw RA 1978. Characterization of the retrograde transport of nerve growth factor (NGF) using high specific activity [125I] NGF. Brain Res 150 (2). 319 - 31.
66. Johnson EM Jr, Gorin PD, Brandeis LD, Pearson J. 1980. Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor. Science 210 (4472). 916 - 8.
67. Karanth SS, Springall DR, Kar S., Gibson SJ, Royston JP, Banerjee DK, Polak JM 1990. Time-related decrease of substance P and CGRP in central and peripheral projections of sensory neurones in Mycobacterium leprae infected nude mice: a model for lepromatous leprosy in man. J Pathol 160 (4). 335 - 45.
68. Krimm RF, Davis BM, Noel T., Albers KM 2006. Overexpression of neurotrophin 4 in skin enhances myelinated sensory endings but does not influence sensory neuron number. J Comp Neurol 498 (4). 455 - 65.
69. Krimm RF, Miller KK, Kitzman PH, Davis BM, Albers KM 2001. Epithelial overexpression of BDNF or NT4 disrupts targeting of taste neurons that innervate the anterior tongue. Dev Biol 232 (2). 508 - 21.
70. Lee SE, Shen H., Taglialatela G., Chung JM, Chung K. 1998. Expression of nerve growth factor in the dorsal root ganglion after peripheral nerve injury. Brain Res 796 (1 - 2). 99 - 106.
71. LeMaster AM, Krimm RF, Davis BM, Noel T., Forbes ME, Johnson JE, Albers KM 1999. Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number. J Neurosci 19 (14). 5919 - 31.
72. Levi-Montalcini R. 1987. The nerve growth factor 35 years later. Science 237 (4819). 1154 - 62.
73. Lewin GR, Mendell LM 1994. Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat. J Neurophysiol 71 (3). 941 - 9.
74. Lewin GR, Ritter AM, Mendell LM 1992. On the role of nerve growth factor in the development of myelinated nociceptors. J Neurosci 12 (5). 1896 - 905.
75. Lewin GR, Rueff A., Mendell LM 1994. Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6 (12). 1903 - 12.
76. Lieberman A. 1974. Some factors affecting retrograde neuronal responses to axonal lesions. In: Bellairs R, Gray E, editors. Essays on the nervous system. Oxford, UK: Oxford University Press. p 71 - 105.
77. Lindfors PH, Voikar V., Rossi J., Airaksinen MS 2006. Deficient nonpeptidergic epidermis innervation and reduced inflammatory pain in glial cell line-derived neurotrophic factor family receptor alpha2 knock-out mice. J Neurosci 26 (7). 1953 - 60.
78. Lindsay RM 1988. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci 8 (7). 2394 - 405.
79. Lu J., Zhou XF, Rush RA 2001. Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res 41 (4). 355 - 63.
80. Maisonpierre PC, Belluscio L., Squinto S., Ip NY, Furth ME, Lindsay RM, Yancopoulos GD 1990. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247 (4949 Pt 1). 1446 - 51.
81. Malin SA, Molliver DC, Koerber HR, Cornuet P., Frye R., Albers KM, Davis BM 2006. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26 (33). 8588 - 99.
82. McLachlan EM, Hu P. 1998. Axonal sprouts containing calcitonin gene-related peptide and substance P form pericellular baskets around large diameter neurons after sciatic nerve transection in the rat. Neuroscience 84 (4). 961 - 5.
83. Milbrandt J., de Sauvage FJ, Fahrner TJ, Baloh RH, Leitner ML, Tansey MG, and others. 1998. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 20 (2). 245 - 53.
84. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K., Wen D., and others. 1997. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19 (4). 849 - 61.
85. Moore MW, Klein RD, Farinas I., Sauer H., Armanini M., Phillips H., and others. 1996. Renal and neuronal abnormalities in mice lacking GDNF. Nature 382 (6586). 76 - 9.
86. Nykjaer A., Lee R., Teng KK, Jansen P., Madsen P., Nielsen MS, and others. 2004. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427 (6977). 843 - 8.
87. Orozco OE, Walus L., Sah DW, Pepinsky RB, Sanicola M. 2001. GFRαlpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 13 (11). 2177 - 82.
88. Purves D. 1980. Neuronal competition. Nature 287 (5783). 585 - 6.
89. Ramer MS, Thompson SW, McMahon SB 1999. Causes and consequences of sympathetic basket formation in dorsal root ganglia. Pain Suppl 6: S111-20.
90. Rice FL, Albers KM, Davis BM, Silos-Santiago I., Wilkinson GA, LeMaster AM, and others. 1998. Differential dependency of unmyelinated and A delta epidermal and upper dermal innervation on neurotrophins, trk receptors, and p75LNGFR. Dev Biol 198 (1). 57 - 81.
91. Rich KM, Yip HK, Osborne PA, Schmidt RE, Johnson EM Jr. 1984. Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury. J Comp Neurol 230 (1). 110 - 8.
92. Ritter AM, Lewin GR, Kremer NE, Mendell LM 1991. Requirement for nerve growth factor in the development of myelinated nociceptors in vivo. Nature 350 (6318). 500 - 2.
93. Ritter AM, Lewin GR, Mendell LM 1993. Regulation of myelinated nociceptor function by nerve growth factor in neonatal and adult rats. Brain Res Bull 30 (3 - 4). 245 - 9.
94. Robinson RC, Radziejewski C., Stuart DI, Jones EY 1996. Crystals of the neurotrophins. Protein Sci 5 (5). 973 - 7.
95. Roux PP, Barker PA 2002. Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 67 (3). 203 - 33.
96. Ruocco I., Cuello AC, Ribeiro-Da-Silva A. 2000. Peripheral nerve injury leads to the establishment of a novel pattern of sympathetic fibre innervation in the rat skin. J Comp Neurol 422 (2). 287 - 96.
97. Scott J., Selby M., Urdea M., Quiroga M., Bell GI, Rutter WJ 1983. Isolation and nucleotide sequence of a cDNA encoding the precursor of mouse nerve growth factor. Nature 302 (5908). 538 - 40.
98. Segal RA 2003. Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 26: 299 - 330.
99. Shen H., Chung JM, Coggeshall RE, Chung K. 1999. Changes in trkA expression in the dorsal root ganglion after peripheral nerve injury. Exp Brain Res 127 (2). 141 - 6.
100. Sleeman MW, Anderson KD, Lambert PD, Yancopoulos GD, Wiegand SJ 2000. The ciliary neurotrophic factor and its receptor, CNTFR alpha. Pharm Acta Helv 74 (2 - 3). 265 - 72.
101. Stoeckel K., Schwab M., Thoenen H. 1975. Specificity of retrograde transport of nerve growth factor (NGF) in sensory neurons: a biochemical and morphological study. Brain Res 89 (1). 1 - 14.
102. Stucky CL, Lewin GR 1999. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci 19 (15). 6497 - 505.
103. Stucky CL, Rossi J., Airaksinen MS, Lewin GR 2002. GFR alpha2/neurturin signalling regulates noxious heat transduction in isolectin B4-binding mouse sensory neurons. J Physiol 545 (Pt 1). 43 - 50.
104. Tandrup T., Woolf CJ, Coggeshall RE 2000. Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. J Comp Neurol 422 (2). 172 - 80.
105. Tessarollo L., Vogel KS, Palko ME, Reid SW, Parada LF 1994. Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc Natl Acad Sci U S A 91 (25). 11844 - 8.
106. Thoenen H., Barde YA 1980. Physiology of nerve growth factor. Physiol Rev 60 (4). 1284 - 335.
107. Tomac AC, Agulnick AD, Haughey N., Chang CF, Zhang Y., Backman C., and others. 2002. Effects of cerebral ischemia in mice deficient in Persephin. Proc Natl Acad Sci U S A 99 (14). 9521 - 6.
108. Torcia M., Bracci-Laudiero L., Lucibello M., Nencioni L., Labardi D., Rubartelli A., and others. 1996. Nerve growth factor is an autocrine survival factor for memory B lymphocytes. Cell 85 (3). 345 - 56.
109. Trupp M., Ryden M., Jornvall H., Funakoshi H., Timmusk T., Arenas E., Ibanez CF 1995. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol 130 (1). 137 - 48.
110. Ullrich A., Gray A., Berman C., Coussens L., Dull TJ 1983. Sequence homology of human and mouse beta-NGF subunit genes. Cold Spring Harb Symp Quant Biol 48 Pt 1: 435 - 42.
111. Unsicker K., Krieglstein K. 2000. Co-activation of TGF-ss and cytokine signaling pathways are required for neurotrophic functions. Cytokine Growth Factor Rev 11 (1 - 2). 97 - 102.
112. Valdez G., Akmentin W., Philippidou P., Kuruvilla R., Ginty DD, Halegoua S. 2005. Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors. J Neurosci 25 (21). 5236 - 47.
113. Vargas-Leal V., Bruno R., Derfuss T., Krumbholz M., Hohlfeld R., Meinl E. 2005. Expression and function of glial cell line-derived neurotrophic factor family ligands and their receptors on human immune cells. J Immunol 175 (4). 2301 - 8.
114. Walsh GS, Kawaja MD 1998. Sympathetic axons surround nerve growth factor-immunoreactive trigeminal neurons: observations in mice overexpressing nerve growth factor. J Neurobiol 34 (4). 347 - 60.
115. Wright LL, Cunningham TJ, Smolen AJ 1983. Developmental neuron death in the rat superior cervical sympathetic ganglion: cell counts and ultrastructure. J Neurocytol 12 (5). 727 - 38.
116. Yip HK, Rich KM, Lampe PA, Johnson EM Jr. 1984. The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in rat dorsal root ganglia. J Neurosci 4 (12). 2986 - 92.
117. Zampieri N., Chao MV 2006. Mechanisms of neurotrophin receptor signalling. Biochem Soc Trans 34 (Pt 4). 607 - 11.
118. Zwick M., Davis BM, Woodbury CJ, Burkett JN, Koerber HR, Simpson JF, Albers KM 2002. Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci 22 (10). 4057 - 65.
119. Zwick M., Molliver DC, Lindsay J., Fairbanks CA, Sengoku T., Albers KM, Davis BM 2003. Transgenic mice possessing increased numbers of nociceptors do not exhibit increased behavioral sensitivity in models of inflammatory and neuropathic pain. Pain 106 (3). 491 - 500.
120. Zylka MJ, Dong X., Southwell AL, Anderson DJ 2003. Atypical expansion in mice of the sensory neuron-specific Mrg G protein-coupled receptor family. Proc Natl Acad Sci U S A 100 (17). 10043 - 8.