Abundant production of brain-derived neurotrophic factor by adult visceral epithelia: Implications for paracrine and target-derived neurotrophic functions

American Journal of Pathology

Volumn 155, Issue 4, 1999, Pages 1183-1193

  Lommatzsch, Marek ^a   Braun, Armin ^a   Mannsfeldt, Anne ^b   Botchkarev, Vladimir A ^a   Botchkareva, Natalia V ^a   Paus, Ralf ^d   Fischer, Axel ^c   Lewin, Gary R ^b   Renz, Harald ^a,e  

^a HUMBOLDT UNIVERSITY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; MOTONEURON; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SENSORY NERVE CELL; SMOOTH MUSCLE FIBER; VISCERA;

EID: 0032848721     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65221-2     Document Type: Article

References (70)

1. Lewin GR, Barde YA: Physiology of the neurotrophins. Annu Rev Neurosci 1996, 19:289-317
2. Martin Zanca D, Hughes SH, Barbacid M: A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences. Nature 1986, 319:743-746
3. Barbacid M: The Trk family of neurotrophin receptors. J Neurobiol 1994, 25:1386-1403
4. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde YA: Molecular cloning and expression of brain-derived neurotrophic factor. Nature 1989, 341:149-152
5. Kalcheim C, Barde YA, Thoenen H, Le Douarin NM: In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells EMBO J 1987, 6:2871-2873
6. Davies AM, Thoenen H, Barde YA: The response of chick sensory neurons to brain-derived neurotrophic factor. J Neurosci 1986, 6:1897-1904
7. Lindsay RM, Thoenen H, Barde YA: Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev Biol 1985, 112:319-328
8. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, Joyner AL, Barbacid M: Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 1993, 75:113-122
9. Ernfors P, Lee KF, Jaenisch R: Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994, 368:147-150
10. ElShamy WM, Ernfors P: Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 complement and cooperate with each other sequentially during visceral neuron development. J Neurosci 1997, 17:8667-8675
11. Snider WD: Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 1994, 77:627-638
12. Erickson JT, Conover JC, Borday V, Champagnat J, Barbacid M, Yancopoulos G, Katz DM: Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing, J Neurosci 1996, 16:5361-5371
13. Brady R, Zaidi SI, Mayer C, Katz DM: BDNF is a target-derived survival factor for arterial baroreceptor and chemoafferent primary sensory neurons. J Neurosci 1999, 19:2131-2142
14. Vogel KS, Davies AM: The duration of neurotrophic factor independence in early sensory neurons is matched to the time course of target field innervation. Neuron 1991, 7:819-830
15. Braun A, Lommatzsch M, Mannsfeldt A, Neuhaus-Steinmetz U, Fischer A, Schnoy N, Lewin GR, Renz H: Cellular sources of enhanced brain-derived neurotrophic factor (BDNF) production in a mouse model of allergic inflammation. Am J Resp Cell Mol Biol 1999, in press.
16. Oddiah D, Anand P, McMahon SB, Rattray M: Rapid increase of NGF, BDNF and NT-3 mRNAs in inflamed bladder. Neuroreport 1998, 9:1455-1458
17. Virchow JC, Julius P, Lommatzsch M, Luttmann W, Renz H, Braun A: Neurotrophins are increased in bronchoalveolar lavage fluid after segmental allergen provocation. Am J Respir Crit Care Med 1998, 158:2002-2005
18. Gonzalez M, Collins WF: Modulation of motoneuron excitability by brain-derived neurotrophic factor. J Neurophysiol 1997, 77:502-506
19. Fernandes KJ, Kobayashi NR, Jasmin BJ, Tetzlaff W: Acetylcholinesterase gene expression in axotomized rat facial motoneurons is differentially regulated by neurotrophins: correlation with trkB and trkC mRNA levels and isoforms. J Neurosci 1998, 18:9936-9947
20. Winter J: Brain derived neurotrophic factor, but not nerve growth factor, regulates capsaicin sensitivity of rat vagal ganglion neurones. Neurosci Lett 1998, 241:21-24
21. Carroll P, Lewin GR, Koltzenburg M, Toyka KV, Thoenen H: A role of BDNF in mechanosensation Nature Neurosci 1998, 1:42-46
22. Heike CJ, Adryan KM, Fedorowicz J, Zhuo H, Park JS, Curtis R, Radley HE, Distefano PS: Axonal transport of neurotrophins by visceral afferent and efferent neurons of the vagus nerve of the rat. J Comp Neurol 1998, 393:102-117
23. Wetmore C, Olson L: Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J Comp Neurol 1995, 353:143-159
24. Zhou XF, Chie ET, Rush RA: Distribution of brain-derived neurotrophic factor in cranial and spinal ganglia. Exp Neurol 1998, 149:237-242
25. Rosenthal A, Goeddel DV, Nguyen T, Martin E, Burton LE, Shih A, Laramee GR, Wurm F, Mason A, Nikolics K, Winslon JW: Primary structure and biological activity of human brain-derived neurotrophic factor. Endocrinology 1991, 129:1289-1294
26. Yamamoto M, Sobue G, Yamamoto K, Terao S, Mitsuma T: Expression of mRNAs for neurotrophic factors (NGF, BDNF, NT-3, and GDNF) and their receptors (p75NGFR, trkA, trkB, and trkC) in the adult human peripheral nervous system and nonneural tissues. Neurochem Res 1996, 21:929-938
27. Robinson M, Adu J, Davies AM: Timing and regulation of trkB and BDNF mRNA expression in placode-derived sensory neurons and their targets. Eur J Neurosci 1996, 8:2399-2406
28. Katoh Semba R, Takeuchi IK, Semba R, Kato K: Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 1997, 69:34-42
29. Acheson A, Barker PA, Alderson RF, Miller FD, Murphy RA: Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: inhibition by antibodies to NGF. Neuron 1991, 7:265-275
30. D'Mello S, Jiang C, Lamberti C, Martin SC, Heinrich G: Differential regulation of the nerve growth factor and brain-derived neurotrophic factor genes in L929 mouse fibroblasts. J Neurosci Res 1992, 33: 519-526
31. Cartwright M, Mikheev AM, Heinrich G: Expression of neurotrophin genes in human fibroblasts: differential regulation of the brain-derived neurotrophic factor gene. Int J Dev Neurosci 1994, 12:685-693
32. Scarisbrick IA, Jones EG, Isackson PJ: Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. J Neurosci 1993, 13:875-893
33. Donovan MJ, Miranda RC, Kraemer R, McCaffrey TA, Tessarollo L, Mahadeo D, Sharif S, Kaplan DR, Tsoulfas P, Parada L: Neurotrophin and neurotrophin receptors in vascular smooth muscle cells. Regulation of expression in response to injury. Am J Pathol 1995, 147:309-324
34. Maroder M, Bellavia D, Meco D, Napolitano M, Stigliano A, Alesse E, Vacca A, Giannini G, Frati L, Gulino A, Screpanti I: Expression of trKB neurotrophin receptor during T cell development role of brain derived neurotrophic factor in immature thymocyte survival. J Immunol 1996, 157:2864-2872
35. Subramaniam A, Jones WK, Gulick J, Wert S, Neumann J, Robbins J: Tissue-specific regulation of the alpha-myosin heavy chain gene promoter in transgenic mice. J Biol Chem 1991, 266:24613-24620
36. Subramaniam A, Birkenberger L, Ecker V, Kudlacz E, Krakowsky J, O'Connor T: Enhanced peripheral innervation in mice overexpressing brain-derived neurotrophic factor. Am J Resp Grit Care Med 1997, 155:A484
37. Schaeren Wiemers N, Gerfin Moser A: 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 1993, 100:431-440
38. Hofer M, Pagliusi SR, Hohn A, Leibrock J, Barde YA: Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 1990, 9:2459-2464
39. Welker P, Foitzik K, Bulfone Paus S, Henz BM, Paus R: Hair cycle-dependent changes in the gene expression and protein content of transforming factor beta 1 and beta 3 in murine skin. Arch Dermatol Res 1997, 289:554-557
40. Botchkarev VA, Eichmuller S, Johansson O, Paus R: Hair cycle-dependent plasticity of skin and hair follicle innervation in normal murine skin. J Comp Neurol 1997, 386:379-395
41. Sendtner M, Holtmann B, Kolbeck R, Thoenen H, Barde YA: Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 1992, 360:757-759
42. Lindner G, Botchkarev VA, Botchkareva NV, Ling G, van der Veen C, Paus R: Analysis of apoptosis during hair follicle regression (catagen) Am J Pathol 1997, 151:1601-1617
43. Braun A, Appel E, Baruch R, Herz U, Botchkarev V, Paus R, Brodie C, Renz H: Role of nerve growth factor in a mouse model of allergic airway inflammation and asthma. Eur J Immunol 1998, 28:3240-3251
44. Shibayama E, Koizumi H: Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am J Pathol 1996, 148:1807-1818
45. McMahon SB, Armanini MP, Ling LH, Phillips HS: Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 1994, 12:1161-1171
46. Nosrat CA, Ebendal T, Olson L: 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 1996, 376:587-602
47. Zhang C, Brandemihl A, Lau D, Lawton A, Oakley B: BDNF is required for the normal development of taste neurons in vivo. Neuroreport 1997, 8:1013-1017
48. Deckner ML, Frisen J, Verge VM, Hokfelt T, Risling M: Localization of neurotrophin receptors in olfactory epithelium and bulb. Neuroreport 1993, 5:301-304
49. Ernfors P, Van De Water T, Loring J, Jaenisch R: Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 1995, 14:1153-1164
50. Schecterson LC, Bothwell M: Neurotrophin and neurotrophin receptor mRNA expression in developing inner ear. Hear Res 1994, 73:92-100
51. Vazquez E, Van de Water TR, Del Valle M, Vega JA, Staecker H, Giraldez F, Represa J: Pattern of trkB protein-like immunoreactivity in vivo and the in vitro effects of brain-derived neurotrophic factor (BDNF) on developing cochlear and vestibular neurons. Anat Embryol Berl 1994, 189:157-167
52. Pirvola U, Arumae U, Moshnyakov M, Palgi J, Saarma M, Ylikoski J: Coordinated expression and function of neurotrophins and their receptors in the rat inner ear during target innervation. Hear Res 1994, 75:131-144
53. Zhuo H, Heike CJ: Presence and localization of neurotrophin receptor tyrosine kinase (TrkA, TrkB, TrkC) mRNAs in visceral afferent neurons of the nodose and petrosal ganglia. Mol Brain Res 1996, 38:63-70
54. Kashiba H, Ueda Y, Ueyama T, Nemoto K, Senba E: Relationship between BDNF- and trk-expressing neurones in rat dorsal root ganglion: an analysis by in situ hybridization. Neuroreport 1997, 8:1229-1234
55. Mendell LW: Neurotrophins and sensory neurons: role in development, maintenance and injury: a thematic summary. Philos Trans R Soc Lond B Biol Sci 1996, 351:463-467
56. Sternini C, Su D, Arakawa J, de Giorgio R, Rickman DW, Davis BM, Albers KM, Brecha NC: Cellular localization of Pan-trk immunoreactivity and trkC mRNA in the enteric nervous system. J Comp Neurol 1996, 368:597-607
57. Hoehner JC, Wester T, Pahlman S, Olsen L: Localization of neurotrophins and their high-affinity receptors during human enteric nervous system development. Gastroenterology 1996, 110:756-767
58. Nawa H, Carnahan J, Gall C: BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur J Neurosci 1995, 7:1527-1535
59. Janig W: Neurobiology of visceral afferent neurons: neuroanatomy, functions, organ regulations and sensations. Biol Psychol 1996, 42: 29-51
60. Rice FL, Albers KM, Davis BM, Silos Santiago I, Wilkinson GA, LeMaster AM, Ernfors P, Smeyne RJ, Aldskogius H, Phillips HS, Barbacid M, DeChiara TM, Yancopoulos GD, Dunne CE, Fundin BT: Differential dependency of unmyelinated and A delta epidermal and upper dermal innervation on neurotrophins, trk receptors, and P75LNGFR. Dev Biol 1998, 198:57-81
61. Fundin BT, Silos Santiago I, Ernfors P, Fagan AM, Aldskogius H, DeChiara TM, Phillips HS, Barbacid M, Yancopoulos GD, Rice FL: Differential dependency of cutaneous mechanoreceptors on neurotrophins, trk receptors, and P75 LNGFR. Dev Biol 1997, 190:94-116
62. Botchkarev VA, Botchkareva NV, Lommatzscri M, Peters EMJ, Lewin GR, Subramaniam A, Braun A, Renz H, Paus R: BDNF overexpression induces differential increases among subsets of sympathetic innervation in murine back skin. Eur J Neurosci 1998, 10:3276-3283
63. Arenas E, Akerud P, Wong V, Boylan C, Persson H, Lindsay RM, Altar CA: Effects of BDNF and NT-4/5 on striatonigral neuropeptides or nigral GABA neurons in vivo. Eur J Neurosci 1996, 8:1707-1717
64. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T: Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 1995, 92:8856-8860
65. Kang H, Schuman EM: Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995, 267:1658-1662
66. Kerschensteiner M, Gallmeier E, Behrens L, Leal W, Misgeld T, Klinkert WE, Kolbeck R, Hoppe E, Oropeza-Wekerle RL, Bartke I, Stadelmann C, Lassmann H, Wekerle H, Hohlfeld R: Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation? J Exp Med 1999, 189:865-870
67. Dmitrieva N, Shelton D, Rice AS, McMahon SB: The role of nerve growth factor in a model of visceral inflammation. Neuroscience 1997, 78:449-459
68. Seidl K, Erck C, Buchberger A: Evidence for the participation of nerve growth factor and its low-affinity receptor (p75NTR) in the regulation of the myogenic program. J Cell Physiol 1998, 176:10-21
69. Erck C, Meisinger C, Grothe C, Seidl K: Regulation of nerve growth factor and its low-affinity receptor (p75NTR) during myogenic differentiation. J Cell Physiol 1998, 176:22-31
70. Botchkarev VA, Metz M, Botchkareva NV, Welker P, Lommatzsch M, Renz H, Paus R: Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 act as "epitheliotrophins" in murine skin. Lab Invest 1999, 79:557-572