Dehydroepiandrosterone and neurotrophins favor axonal growth in a sensory neuron-keratinocyte coculture model

Neuroscience

Volumn 159, Issue 2, 2009, Pages 514-525

  Ulmann, L ^a   Rodeau, J L ^a   Danoux, L ^b   Contet Audonneau, J L ^b   Pauly, G ^b   Schlichter, R ^a  

^a CNRS   (France)

^b Division Laboratoires Sérobiologiques ^*  (France)

Author keywords

epidermis; neurite outgrowth; skin; steroid; steroidogenesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; ESTRADIOL; K 252A; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PRASTERONE; PREGNENOLONE; PROGESTERONE; PROTEIN TYROSINE KINASE A;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL LEVEL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVATION; KERATINOCYTE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE; SPINAL GANGLION; STEROIDOGENESIS;

ADJUVANTS, IMMUNOLOGIC; AMINOGLUTETHIMIDE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AROMATASE INHIBITORS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CARBAZOLES; CELL SIZE; CELLS, CULTURED; COCULTURE TECHNIQUES; DEHYDROEPIANDROSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GANGLIA, SPINAL; HUMANS; INDOLE ALKALOIDS; KERATINOCYTES; NERVE GROWTH FACTORS; NEURITES; RATS; RATS, WISTAR; RECEPTOR, TRKA; RECEPTOR, TRKB; SENSORY RECEPTOR CELLS; TIME FACTORS;

EID: 61349157273     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.01.018     Document Type: Article

References (62)

1. Albers K.M., Wright D.E., and Davis B.M. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14 (1994) 1422-1432
2. Albers K.M., Perrone T.N., Goodness T.P., Jones M.E., Green M.A., and Davis B.M. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 134 (1996) 487-497
3. Anand P. Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 146 (2004) 477-492
4. Arnold J.T., and Blackman M.R. Does DHEA exert direct effects on androgen and estrogen receptors, and does it promote or prevent prostate cancer?. Endocrinology 146 (2005) 4565-4567
5. Bennett D.L., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., and Priestley J.V. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18 (1998) 3059-3072
6. Bowie D., Feltz P., and Schlichter R. Subpopulations of neonatal rat sensory neurons express functional neurotransmitter receptors which elevate intracellular calcium. Neuroscience 58 (1994) 141-149
7. Carrer H.F., Cambiasso M.J., Brito V., and Gorosito S. Neurotrophic factors and estradiol interact to control axogenic growth in hypothalamic neurons. Ann N Y Acad Sci 1007 (2003) 306-316
8. Casellas P., Galiegue S., and Basile A.S. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 40 (2002) 475-486
9. Chakrabarti K., Lin R., Schiller N.I., Wang Y., Koubi D., Fan Y.X., Rudkin B.B., Johnson G.R., and Schiller M.R. Critical role for kalirin in nerve growth factor signaling through TrkA. Mol Cell Biol 25 (2005) 5106-5118
10. Charalampopoulos I., Alexaki V.I., Lazaridis I., Dermitzaki E., Avlonitis N., Tsatsanis C., Calogeropoulou T., Margioris A.N., Castanas E., and Gravanis A. G protein-associated, specific membrane binding sites mediate the neuroprotective effect of dehydroepiandrosterone. FASEB J 20 (2006) 577-579
11. Chen F., Knecht K., Birzin E., Fisher J., Wilkinson H., Mojena M., Moreno C.T., Schmidt A., Harada S., Freedman L.P., and Reszka A.A. Direct agonist/antagonist functions of dehydroepiandrosterone. Endocrinology 146 (2005) 4568-4576
12. Collo G., North R.A., Kawashima E., Merlo-Pich E., Neidhart S., Surprenant A., and Buell G. Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16 (1996) 2495-2507
13. Compagnone N.A., and Mellon S.H. Dehydroepiandrosterone: a potential signalling molecule for neocortical organization during development. Proc Natl Acad Sci U S A 95 (1998) 4678-4683
14. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 21 (2000) 1-56
15. Crowley C., Spencer S.D., Nishimura M.C., Chen K.S., Pitts-Meek S., Armanini M.P., Ling L.H., McMahon S.B., Shelton D.L., Levinson A.D., et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76 (1994) 1001-1011
16. Davies A.M., Bandtlow C., Heumann R., Korsching S., Rohrer H., and Thoenen H. Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326 (1987) 353-358
17. De Roo M., Rodeau J.L., and Schlichter R. Dehydroepiandrosterone potentiates native ionotropic ATP receptors containing the P2X2 subunit in rat sensory neurones. J Physiol 552 (2003) 59-71
18. Djouhri L., and Lawson S.N. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 46 (2004) 131-145
19. Elias P.M., Ahn S.K., Denda M., Brown B.E., Crumrine D., Kimutai L.K., Komuves L., Lee S.H., and Feingold K.R. Modulations in epidermal calcium regulate the expression of differentiation-specific markers. J Invest Dermatol 119 (2002) 1128-1136
20. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci 6 (2005) 507-520
21. Fritsch M., Orfanos C.E., and Zouboulis C.C. Sebocytes are the key regulators of androgen homeostasis in human skin. J Invest Dermatol 116 (2001) 793-800
22. Goodness T.P., Albers K.M., Davis F.E., and Davis B.M. Overexpression of nerve growth factor in skin increases sensory neuron size and modulates Trk receptor expression. Eur J Neurosci 9 (1997) 1574-1585
23. Hilliges M., Wang L., and Johansson O. Ultrastructural evidence for nerve fibers within all vital layers of the human epidermis. J Invest Dermatol 104 (1995) 134-137
24. Huang E.J., and Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24 (2001) 677-736
25. Labrie F., Luu-The V., Labrie C., Pelletier G., and El-Alfy M. Intracrinology and the skin. Horm Res 54 (2000) 218-229
26. Lawson S.N. Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P, CGRP and somatostatin. Prog Brain Res 104 (1995) 161-173
27. Lawson S.N. Peptides and cutaneous polymodal nociceptor neurones. Prog Brain Res 113 (1996) 369-385
28. Lee F.S., and Chao M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc Natl Acad Sci U S A 98 (2001) 3555-3560
29. LeMaster A.M., Krimm R.F., Davis B.M., Noel T., Forbes M.E., Johnson J.E., and Albers K.M. Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number. J Neurosci 19 (1999) 5919-5931
30. Lewin G.R., and Mendell L.M. Nerve growth factor and nociception. Trends Neurosci 16 (1993) 353-359
31. Lindsay R.M., Lockett C., Sternberg J., and Winter J. Neuropeptide expression in cultures of adult sensory neurons: modulation of substance P and calcitonin gene-related peptide levels by nerve growth factor. Neuroscience 33 (1989) 53-65
32. Liu D., and Dillon J.S. Dehydroepiandrosterone activates endothelial cell nitric-oxide synthase by a specific plasma membrane receptor coupled to Galpha(i2,3). J Biol Chem 277 (2002) 21379-21388
33. Liu D., and Dillon J.S. Dehydroepiandrosterone stimulates nitric oxide release in vascular endothelial cells: evidence for a cell surface receptor. Steroids 69 (2004) 279-289
34. Liu D., Ren M., Bing X., Stotts C., Deorah S., Love-Homan L., and Dillon J.S. Dehydroepiandrosterone inhibits intracellular calcium release in beta-cells by a plasma membrane-dependent mechanism. Steroids 71 (2006) 691-699
35. Liu J., Rone M.B., and Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem 281 (2006) 38879-38893
36. Luo X.G., Rush R.A., and Zhou X.F. Ultrastructural localization of brain-derived neurotrophic factor in rat primary sensory neurons. Neurosci Res 39 (2001) 377-384
37. Masliah E., Mallory M., Hansen L., Alford M., DeTeresa R., and Terry R. An antibody against phosphorylated neurofilaments identifies a subset of damaged association axons in Alzheimer's disease. Am J Pathol 142 (1993) 871-882
38. Menon G.K., Grayson S., and Elias P.M. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 84 (1985) 508-512
39. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., and Priestley J.V. Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 17 (1997) 8476-8490
40. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., and Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19 (1997) 849-861
41. Oku H., Kumamoto C., Miyagi T., Hiyane T., Nagata J., and Chinen I. Serum-free culture of rat keratinocytes. Iin Vitro Cell Dev Biol Anim 30A (1994) 496-503
42. Papadopoulos V., Lecanu L., Brown R.C., Han Z., and Yao Z.X. Peripheral-type benzodiazepine receptor in neurosteroid biosynthesis, neuropathology and neurological disorders. Neuroscience 138 (2006) 749-756
43. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapere J.J., Lindemann P., Norenberg M.D., Nutt D., Weizman A., Zhang M.R., and Gavish M. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27 (2006) 402-409
44. Piiper A., Dikic I., Lutz M.P., Leser J., Kronenberger B., Elez R., Cramer H., Muller-Esterl W., and Zeuzem S. Cyclic AMP induces transactivation of the receptors for epidermal growth factor and nerve growth factor, thereby modulating activation of MAP kinase, Akt, and neurite outgrowth in PC12 cells. J Biol Chem 277 (2002) 43623-43630
45. Pincelli C., and Marconi A. Autocrine nerve growth factor in human keratinocytes. J Dermatol Sci 22 (2000) 71-79
46. Pincelli C., Sevignani C., Manfredini R., Grande A., Fantini F., Bracci-Laudiero L., Aloe L., Ferrari S., Cossarizza A., and Giannetti A. Expression and function of nerve growth factor and nerve growth factor receptor on cultured keratinocytes. J Invest Dermatol 103 (1994) 13-18
47. Rajagopal R., and Chao M.V. A role for Fyn in Trk receptor transactivation by G protein-coupled receptor signaling. Mol Cell Neurosci 33 (2006) 36-46
48. Rice F.L., Albers K.M., Davis B.M., Silos-Santiago I., Wilkinson G.A., LeMaster A.M., Ernfors P., Smeyne R.J., Aldskogius H., Phillips H.S., Barbacid M., DeChiara T.M., Yancopoulos G.D., Dunne C.E., and Fundin B.T. Differential dependency of unmyelinated and ad epidermal and upper dermal innervation on neurotrophins, trk receptors, and p75LNGFR. Dev Biol 198 (1998) 57-81
49. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 22 (1999) 410-416
50. Schlichter R., Keller A.F., De Roo M., Breton J.D., Inquimbert P., and Poisbeau P. Fast nongenomic effects of steroids on synaptic transmission and role of endogenous neurosteroids in spinal pain pathways. J Mol Neurosci 28 (2006) 33-51
51. Schumacher M., Guennoun R., Mercier G., Desarnaud F., Lacor P., Benavides J., Ferzaz B., Robert F., and Baulieu E.E. Progesterone synthesis and myelin formation in peripheral nerves. Brain Res Brain Res Rev 37 (2001) 343-359
52. Shi F., Corrales C.E., Liberman M.C., and Edge A.S. BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. Eur J Neurosci 26 (2007) 3016-3023
53. Slominski A., and Wortsman J. Neuroendocrinology of the skin. Endocr Rev 21 (2000) 457-487
54. Slominski A., Ermak G., and Mihm M. ACTH receptor, CYP11A1, CYP17 and CYP21A2 genes are expressed in skin. J Clin Endocrinol Metab 81 (1996) 2746-2749
55. Slominski A., Gomez-Sanchez C.E., Foecking M.F., and Wortsman J. Active steroidogenesis in the normal rat skin. Biochim Biophys Acta 1474 (2000) 1-4
56. Swett J.E., Torigoe Y., Elie V.R., Bourassa C.M., and Miller P.G. Sensory neurons of the rat sciatic nerve. Exp Neurol 114 (1991) 82-103
57. Taherzadeh O., Otto W.R., Anand U., Nanchahal J., and Anand P. Influence of human skin injury on regeneration of sensory neurons. Cell Tissue Res 312 (2003) 275-280
58. Thornton P.D., Gerke M.B., and Plenderleith M.B. Histochemical localisation of a galactose-containing glycoconjugate expressed by sensory neurones innervating different peripheral tissues in the rat. J Peripher Nerv Syst 10 (2005) 47-57
59. Tongiorgi E., Armellin M., Giulianini P.G., Bregola G., Zucchini S., Paradiso B., Steward O., Cattaneo A., and Simonato M. Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J Neurosci 24 (2004) 6842-6852
60. Ulmann L., Rodeau J.L., Danoux L., Contet-Audonneau J.L., Pauly G., and Schlichter R. Trophic effects of keratinocytes on the axonal development of sensory neurons in a coculture model. Eur J Neurosci 26 (2007) 113-125
61. Widstrom R.L., and Dillon J.S. Is there a receptor for dehydroepiandrosterone or dehydroepiandrosterone sulfate?. Semin Reprod Med 22 (2004) 289-298
62. Zouboulis C.C. Human skin: an independent peripheral endocrine organ. Horm Res 54 (2000) 230-242