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• W2022336570 abstract "cytokeratin dorsal root ganglia TO THE EDITOR Sensory neurons are localized in dorsal root ganglia (DRG) (Birder and Perl, 1994Birder L.A. Perl E.R. Cutaneous sensory receptors.J Clin Physiol. 1994; 11: 534-552Google Scholar). They are associated with glial cells, like Schwann cells, which are important for synaptic plasticity (Allen and Barres, 2005Allen N.J. Barres B.A. Signaling between glia and neurons: focus on synaptic plasticity.Curr Opin Neurobiol. 2005; 15: 542-548Crossref PubMed Scopus (237) Google Scholar). Synapses between nerve endings and epidermal cells have been shown by confocal scanner laser microscopy and transmission electron microscopy (Merkel, 1875Merkel F. Tastzellen und Tastkorperchen bei den Haustieren und beim Menschen.Arch Mikrosk Anat. 1875; 11: 636-652Crossref Scopus (308) Google Scholar; Hosoi et al., 1993Hosoi J. Murphy G.F. Egan C.L. Lerner E.A. Grabbe S. Asahina A. et al.Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide.Nature. 1993; 363: 159-163Crossref PubMed Scopus (517) Google Scholar; Hilliges et al., 1995Hilliges M. Wang L. Johansson O. Ultrastructural evidence for nerve fibers within all vital layers of the human epidermis.J Invest Dermatol. 1995; 104: 134-137Crossref PubMed Scopus (155) Google Scholar; Hara et al., 1996Hara M. Toyoda M. Yaar M. Bhawan J. Avila E.M. Penner I.R. et al.Innervation of melanocytes in human skin.J Exp Med. 1996; 184: 1385-1395Crossref PubMed Scopus (91) Google Scholar; Gaudillere et al., 1996Gaudillere A. Misery L. Souchier C. Claudy A. Schmitt D. Intimate associations between PGP9.5-positive nerve fibres and Langerhans cells.Br J Dermatol. 1996; 135: 343-344Crossref PubMed Scopus (46) Google Scholar; Chateau and Misery, 2004Chateau Y. Misery L. Connections between nerve endings and epidermal cells: are they synapses?.Exp Dermatol. 2004; 13: 2-4Crossref PubMed Scopus (44) Google Scholar); Through an efferent neurosecretory activity (Ansel et al., 1996Ansel J.C. Kaynard A.H. Armstrong C.A. Olerud J. Bunnett N. Payan D. Skin – nervous system interactions.J Invest Dermatol. 1996; 106: 198-204Crossref PubMed Scopus (183) Google Scholar; Misery, 1997Misery L. Skin, immunity and the nervous system.Br J Dermatol. 1997; 137: 843-850Crossref PubMed Scopus (161) Google Scholar), they modulate skin properties (Misery, 1997Misery L. Skin, immunity and the nervous system.Br J Dermatol. 1997; 137: 843-850Crossref PubMed Scopus (161) Google Scholar; Steinhoff et al., 2003Steinhoff M. Ständer S. Seeliger S. Ansel J.C. Schmelz M. Luger T. Modern aspects of cutaneous neurogenic inflammation.Arch Dermatol. 2003; 139: 1479-1488Crossref PubMed Scopus (273) Google Scholar). Numerous interactions between skin, immunity, and the nervous system allow definition of the neuro-immuno-cutaneous system (Misery, 1997Misery L. Skin, immunity and the nervous system.Br J Dermatol. 1997; 137: 843-850Crossref PubMed Scopus (161) Google Scholar). Because there is no in vitro model for studies on neuro-immuno-cutaneous system, we performed a tri-compartmentalized co-culture, each compartment reproducing epidermis, DRG, and spinal cord, respectively, spontaneously connected by neurites. The functionality of these “synapses” was assessed by electrophysiological studies. Epidermal cells were isolated from skin specimens obtained from healthy humans (Bessou et al., 1995Bessou S. Surleve-Bazeille J.E. Sorbier E. Taieb A. Ex vivo reconstruction of the epidermis with melanocytes and the influence of UVB.Pigment Cell Res. 1995; 8: 241-249Crossref PubMed Scopus (59) Google Scholar). Neurons and glial cells were isolated from DRGs and spinal cords of 2- to 5-day-old Wistar rats (Lindsay et al., 1990Lindsay R.M. Shooter E.M. Radeke M.J. Misko T.P. Dechant G. Thoenen H. et al.Nerve growth factor regulates expression of the nerve growth factor receptor gene in adult sensory neurons.Eur J Neurosci. 1990; 2: 389-396Crossref PubMed Scopus (110) Google Scholar; Stucky and Lewin, 1999Stucky C.L. Lewin G.R. Isolectin B(4)-positive and -negative nociceptors are functionally distinct.J Neurosci. 1999; 19: 6497-6505Crossref PubMed Google Scholar; Wang and Cynader, 1999Wang X.F. Cynader M.S. Effects of astrocytes on neuronal attachment and survival shown in a serum-free co-culture system.Brain Res Brain Res Protoc. 1999; 4: 209-216Crossref PubMed Scopus (20) Google Scholar). Cultures were performed with glial conditioned medium, as described previously (Bottenstein and Sato, 1979Bottenstein J.E. Sato G.H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium.Proc Natl Acad Sci USA. 1979; 76: 514-517Crossref PubMed Scopus (1995) Google Scholar; Wang and Cynader, 1999Wang X.F. Cynader M.S. Effects of astrocytes on neuronal attachment and survival shown in a serum-free co-culture system.Brain Res Brain Res Protoc. 1999; 4: 209-216Crossref PubMed Scopus (20) Google Scholar). Coverslips were sterilized by UV and coated by poly-L-lysine. Two kinds of specific culture dishes were used. A first model was prepared from plastic Petri dishes by drilling three wells connected by channels and attaching a glass coverslip to the outer surface of the dish. A second model consisted of a two-part design, which includes a glass substrate topped by polydimethylsiloxane, including wells and microchannels (Morin et al., 2006Morin F. Nishimura N. Griscom L. Le Pioufle L. Fujita H. Takamura Y. et al.Constraining the connectivity of neuronal networks cultured on microelctrode arrays with microfluidic techniques: a step towards neuron-based functional chips.Biosens Bioelectron. 2006; 21: 1093-1100Crossref PubMed Scopus (109) Google Scholar). We performed a tri-compartmented culture with: 1/cells from spinal cords cells (1 × 106 cells/ml); 2/cells from DRGs (1 × 105 cells/ml); 3/epidermal cells (3 × 106 cells/ml). To provide trophic support, a glial feeder layer was added (Wang and Cynader, 1999Wang X.F. Cynader M.S. Effects of astrocytes on neuronal attachment and survival shown in a serum-free co-culture system.Brain Res Brain Res Protoc. 1999; 4: 209-216Crossref PubMed Scopus (20) Google Scholar). Glial conditioned medium was replaced every 2 days. After 15 days of co-culture, the growth of many neurites, often assembled in bundles, was observed (by phase-contrast microscopy) from the DRG compartment to both equivalents of spinal cord and epidermis and between neurons in the DRG equivalent and neurons. Immunostainings were performed on co-cultures (first model) after 15 days. Primary antibodies recognized protein gene product (PGP) 9.5 (neurons), cytokeratin (CK, keratinocytes), cytokeratin 20 (Merkel cells), chromogranin A (neuro-secretory granules of Merkel cells), glial fibrillary acidic protein (astrocytes and oligodendrocytes), A2B5 (oligodendrocytes), and myelin basic protein. Neurons and glial cells were assembled in clusters in the spinal cord and DRG compartments and PGP9.5+ nerve endings were seen in the epidermal compartment. Neurites were often surrounded by myelin and associated with Schwann cell-shaped cells. By confocal scanner laser microscopy, we could recognize in the epidermal compartment, PGP 9.5+ neurons, CK+ keratinocytes, and CK20+ or chromogranin+ Merkel cells. PGP9.5+ nerve fibers were growing from the DRG compartment to the epidermal cells. Double immunostainings revealed overlapping areas, assessing synapse-like structures between nerve endings and keratinocytes and, more frequently, between nerve endings and Merkel cells. Merkel cells often formed Merkel corpuscles (Figure 1a). Contacts of nerve endings with single Merkel cells were also observed (Figure 1b). Chromogranin A was localized in neuro-secretory granules from Merkel cells, in front of nerve fibers, like in a synaptic organization. Transmission electron microscopy observations after 15 days of co-culture (second model) confirmed confocal scanner laser microscopy data. In the epidermal compartment, keratinocytes, Merkel cells, and melanocytes were present. An epithelial organization was assessed by desmosomes. Melanocytes and Merkel cells express dendrites and, respectively, melanosomes and neuro-secretory granules. Nerve fibers were coursing through epidermal cells. They ended in the contact of keratinocytes and Merkel cells. Electrophysiological measurements were performed after 15 days of co-culture. Electrical activity was recorded from neurites using a macro-patch clamp technique. The signal was recorded via a GeneClamp 500B amplifier. Pipettes were pulled and heat polished from 1.5 mm diameter borosilicate glass with a DMZ – Universal puller. Resistance of the pipettes averaged 1.5 MΩ when filled with recording solution. Currents were low-pass filtered at 5 kHz and digitized at 35 kHz. Giga-seal was checked and leak currents were compensated. The physiological state of the neurite was first checked by recording Na+ and K+ currents, confirming the viability of the neurites and the possibility of electrophysiological measurements. Continuous recordings were made in a cell-attached configuration on nerve fiber-like formations allowing the monitoring of spontaneous activity. Heat stimulus was applied by infusing hot medium (37°C for heat stimulation and 45°C for pain stimulation) in the epidermal cell compartment. Electrophysiological recordings were made in the DRG compartment. Recordings (Figure 2) showed that without external stimulation, no electrical activity could be recorded at 22°C. After heat or painful stimulation, a depolarization was observed and spikes were recorded, corresponding to the triggering of a spontaneous activity. The effects were enhanced with pain stimulation. Ten minutes after stimulation, repetitive electrical activities were still persistent. The spikes progressively disappeared, but could be reinitiated by another heat stimulation, showing the reversibility of the heat effect. Hence, we have performed an in vitro reconstruction of equivalents of spinal cord, DRG, and epidermis connected by neurites. We have obtained a viable in vitro culture model of Merkel cells (Gaudillere and Misery, 1994Gaudillere A. Misery L. Merkel cell.Ann Dermatol Venereol. 1994; 121: 909-917PubMed Google Scholar; Moll et al., 2005Moll I. Roessler M. Brandner J.M. Eispert A.C. Houdek P. Moll R. Human Merkel cells – aspects of cell biology, distribution and functions.Eur J Cell Biol. 2005; 84: 259-271Crossref PubMed Scopus (95) Google Scholar). To our knowledge, the longest previous culture of Merkel cells was 4 days (Fradette et al., 2003Fradette J. Larouche D. Fugere C. Guignard R. Beauparlant A. Couture V. et al.Normal human Merkel cells are present in epidermal cell populations isolated and cultured from glabrous and hairy skin sites.J Invest Dermatol. 2003; 120: 313-317Crossref PubMed Scopus (32) Google Scholar) or 5 days (Vos et al., 1991Vos P. Stark F. Pittman R.N. Merkel cells in vitro: production of nerve growth factor and selective interactions with sensory neurons.Dev Biol. 1991; 144: 281-300Crossref PubMed Scopus (68) Google Scholar), whereas Merkel cells were maintained for 15 days of culture in our hands. Other authors had performed co-cultures with keratinocytes (Fradette et al., 2003Fradette J. Larouche D. Fugere C. Guignard R. Beauparlant A. Couture V. et al.Normal human Merkel cells are present in epidermal cell populations isolated and cultured from glabrous and hairy skin sites.J Invest Dermatol. 2003; 120: 313-317Crossref PubMed Scopus (32) Google Scholar) or sensory nerve endings (Vos et al., 1991Vos P. Stark F. Pittman R.N. Merkel cells in vitro: production of nerve growth factor and selective interactions with sensory neurons.Dev Biol. 1991; 144: 281-300Crossref PubMed Scopus (68) Google Scholar; Shimohira-Yamasaki et al., 2006Shimohira-Yamasaki M. Toda S. Narisawa Y. Sugihara H. Merkel cell–nerve cell interaction undergoes formation of a synapse-like structure in a primary culture.Cell Struct Funct. 2006; 31: 39-45Crossref PubMed Scopus (18) Google Scholar), but our results suggest that the association of keratinocytes and nerve endings is better. Until recently, neurons were the only cells that were never included in reconstructed skin or mucosa (Sivard et al., 2004Sivard P. Berlier W. Picard B. Sabido O. Genin C. Misery L. HIV-1 infection of Langerhans cells in a reconstructed vaginal mucosa.J Infect Dis. 2004; 190: 227-235Crossref PubMed Scopus (30) Google Scholar). Gingras et al., 2003Gingras M. Bergeron J. Dery J. Durham H.D. Berthod F. In vitro development of a tissue-engineered model of peripheral nerve regeneration to study neurite growth.FASEB J. 2003; : 2124-2126PubMed Google Scholar have performed a tissue-engineered model mimicking the integration of nerve endings in reconstructed skin but did not show functional synapse-like structures as we did in this study. Our model of co-culture could be used for studies of the neuro-immuno-cutaneous system (Misery, 1997Misery L. Skin, immunity and the nervous system.Br J Dermatol. 1997; 137: 843-850Crossref PubMed Scopus (161) Google Scholar) by adding external stimuli, drugs, or cosmetics, and it could be an in vitro model of itch (Yosipovitch et al., 2003Yosipovitch G. Greaves M.W. Schmelz M. Itch.Lancet. 2003; 361: 690-694Abstract Full Text Full Text PDF PubMed Scopus (331) Google Scholar. The authors state no conflict of interest. This work was helped by grants from Coloplast Foundation and French Society of Dermatology. We thank Pr Jean-Luc Carré for his help concerning glial cells and Pr Jean-Paul Leroy for electron microscopy." @default.
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• W2022336570 title "In Vitro Reconstruction of Neuro-Epidermal Connections" @default.
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