The structure and organization of lanceolate mechanosensory complexes at mouse hair follicles

eLife

Volumn 2014, Issue 3, 2014, Pages

  Li, Lishi ^a,c   Ginty, David D ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFIMOXIFENE; NERVE GROWTH FACTOR; PROTEIN S 100; PROTEIN TYROSINE KINASE A; TAMOXIFEN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DENERVATION; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; LANCEOLATE ENDING; MECHANORECEPTOR; MECHANOTRANSDUCTION; MOUSE; NERVE ENDING; NERVE FIBER; NERVE FIBER TRANSECTION; NONHUMAN; SCHWANN CELL; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84898734369     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01901.001     Document Type: Article

References (52)

1. Abraira VE, Ginty DD. 2013. The sensory neurons of touch. Neuron 79:618-639. doi: 10.1016/j.neuron.2013.07.051.
2. Banks RW, Cahusac PM, Graca A, Kain N, Shenton F, Singh P, Nja A, Simon A, Watson S, Slater CR, Bewick GS. 2013. Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles. Journal of Physiology 591:2523-2540. doi: 10.1113/jphysiol.2012.243659.
3. Brumovsky P, Watanabe M, Hokfelt T. 2007. Expression of the vesicular glutamate transporters-1 and-2 in adult mouse dorsal root ganglia and spinal cord and their regulation by nerve injury. Neuroscience 147:469-490. doi: 10.1016/j.neuroscience.2007.02.068.
4. Buch T, Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, Jung S, Waisman A. 2005. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nature Methods 2:419-426. doi: 10.1038/nmeth762.
5. Burgeson RE, Christiano AM. 1997. The dermal-epidermal junction. Current Opinion in Cell Biology 9:651-658. doi: 10.1016/S0955-0674(97)80118-4.
6. Burgess PR, Petit D, Warren RM. 1968. Receptor types in cat hairy skin supplied by myelinated fibers. Journal of Neurophysiology 31:833-848.
7. Cauna N. 1969. The fine morphology of the sensory receptor organs in the auricle of the rat. The Journal of Comparative Neurology 136:81-98. doi: 10.1002/cne.901360106.
8. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI, Anderson DJ. 2009. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proceedings of the National Academy of Sciences of the United States of America 106:9075-9080. doi: 10.1073/pnas.0901507106.
9. Chen X, Ye H, Kuruvilla R, Ramanan N, Scangos KW, Zhang C, Johnson NM, England PM, Shokat KM, Ginty DD. 2005. A chemical-genetic approach to studying neurotrophin signaling. Neuron 46:13-21. doi: 10.1016/j.neuron.2005.03.009.
10. Chiang LY, Poole K, Oliveira BE, Duarte N, Sierra YA, Bruckner-Tuderman L, Koch M, Hu J, Lewin GR. 2011. Laminin-332 coordinates mechanotransduction and growth cone bifurcation in sensory neurons. Nature Neuroscience 14:993-1000. doi: 10.1038/nn.2873.
11. Dingemans KP, Van den Bergh Weerman MA. 1990. Rapid contrasting of extracellular elements in thin sections. Ultrastructural Pathology 14:519-527. doi: 10.3109/01913129009076139.
12. Doerflinger NH, Macklin WB, Popko B. 2003. Inducible site-specific recombination in myelinating cells. Genesis 35:63-72. doi: 10.1002/gene.10154.
13. Driskell RR, Giangreco A, Jensen KB, Mulder KW, Watt FM. 2009. Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 136:2815-2823. doi: 10.1242/dev.038620.
14. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925. doi: 10.1038/nature02033.
15. Halata Z. 1993. Sensory innervation of the hairy skin (light-and electronmicroscopic study. The Journal of Investigative Dermatology 101:75S-81S. doi: 10.1111/1523-1747.ep12362877.
16. Hashimoto K. 1972. Fine structure of perifollicular nerve endings in human hair. The Journal of Investigative Dermatology 59:432-441. doi: 10.1111/1523-1747.ep12627604.
17. Heidenreich M, Lechner SG, Vardanyan V, Wetzel C, Cremers CW, De Leenheer EM, Aranguez G, Moreno-Pelayo MA, Jentsch TJ, Lewin GR. 2012. KCNQ4 K(+) channels tune mechanoreceptors for normal touch sensation in mouse and man. Nature Neuroscience 15:138-145. doi: 10.1038/nn.2985.
18. Horch KW, Tuckett RP, Burgess PR. 1977. A key to the classification of cutaneous mechanoreceptors. The Journal of Investigative Dermatology 69:75-82. doi: 10.1111/1523-1747.ep12497887.
19. Hu J, Chiang LY, Koch M, Lewin GR. 2010. Evidence for a protein tether involved in somatic touch. The EMBO Journal 29:855-867. doi: 10.1038/emboj.2009.398.
20. Iggo A, Andres KH. 1982. Morphology of cutaneous receptors. Annual Review of Neuroscience 5:1-31. doi: 10.1146/annurev.ne.05.030182.000245.
21. Jackson PC, Diamond J. 1984. Temporal and spatial constraints on the collateral sprouting of low-threshold mechanosensory nerves in the skin of rats. The Journal of Comparative Neurology 226:336-345. doi: 10.1002/cne.902260304.
22. Jessen KR, Mirsky R. 2005. The origin and development of glial cells in peripheral nerves. Nature Review Neuroscience 6:671-682. doi: 10.1038/nrn1746.
23. Johnson KO. 2001. The roles and functions of cutaneous mechanoreceptors. Current Opinion in Neurobiology 11:455-461. doi: 10.1016/S0959-4388(00)00234-8.
24. Johnson KO, Hsiao SS. 1992. Neural mechanisms of tactual form and texture perception. Annual Review of Neuroscience 15:227-250. doi: 10.1146/annurev.ne.15.030192.001303.
25. Kaidoh T, Inoue T. 2000. Intercellular junctions between palisade nerve endings and outer root sheath cells of rat vellus hairs. The Journal of Comparative Neurology 420:419-427. doi: 10.1002/(SICI)1096-9861(20000515)420:43.0.CO;2-3.
26. Kaidoh T, Inoue T. 2008. N-cadherin expression in palisade nerve endings of rat vellus hairs. The Journal of Comparative Neurology 506:525-534. doi: 10.1002/cne.21550.
27. Kann O, Kovacs R. 2007. Mitochondria and neuronal activity. American Journal of Physiology Cell Physiology 292:C641-C657. doi: 10.1152/ajpcell.00222.2006.
28. Keene DR, Sakai LY, Lunstrum GP, Morris NP, Burgeson RE. 1987. Type VII collagen forms an extended network of anchoring fibrils. The Journal of Cell Biology 104:611-621. doi: 10.1083/jcb.104.3.611.
29. Lechner SG, Lewin GR. 2013. Hairy sensation. Physiology (Bethesda) 28:142-150. doi: 10.1152/physiol.00059.2012.
30. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, Gong S, Jankowski MP, Luo W, Heintz N, Koerber HR, Woodbury CJ, Ginty DD. 2011. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615-1627. doi: 10.1016/j.cell.2011.11.027.
31. Liu Q, Vrontou S, Rice FL, Zylka MJ, Dong X, Anderson DJ. 2007. Molecular genetic visualization of a rare subset of unmyelinated sensory neurons that may detect gentle touch. Nature Neuroscience 10:946-948. doi: 10.1038/nn1937.
32. Low FN. 1962. Microfibrils: fine filamentous components of the tissue space. The Anatomical Record 142:131-137. doi: 10.1002/ar.1091420205.
33. Lumpkin EA, Marshall KL, Nelson AM. 2010. The cell biology of touch. The Journal of Cell Biology 191:237-248. doi: 10.1083/jcb.201006074.
34. Luo W, Enomoto H, Rice FL, Milbrandt J, Ginty DD. 2009. Molecular identification of rapidly adapting mechanoreceptors and their developmental dependence on ret signaling. Neuron 64:841-856. doi: 10.1016/j.neuron.2009.11.003.
35. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience 13:133-140. doi: 10.1038/nn.2467.
36. Maricich SM, Wellnitz SA, Nelson AM, Lesniak DR, Gerling GJ, Lumpkin EA, Zoghbi HY. 2009. Merkel cells are essential for light-touch responses. Science 324:1580-1582. doi: 10.1126/science.1172890.
37. Parakkal PF. 1969. Ultrastructural changes of the basal lamina during the hair growth cycle. The Journal of Cell Biology 40:561-564. doi: 10.1083/jcb.40.2.561.
38. Peters EM, Botchkarev VA, Muller-Rover S, Moll I, Rice FL, Paus R. 2002. Developmental timing of hair follicle and dorsal skin innervation in mice. The Journal of Comparative Neurology 448:28-52. doi: 10.1002/cne.10212.
39. Regauer S, Seiler GR, Barrandon Y, Easley KW, Compton CC. 1990. Epithelial origin of cutaneous anchoring fibrils. The Journal of Cell Biology 111:2109-2115. doi: 10.1083/jcb.111.5.2109.
40. Reynolds ML, Woolf CJ. 1992. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. Journal of Neurocytology 21:50-66. doi: 10.1007/BF01206897.
41. Rice FL, Albrecht PJ. 2008. Cutaneous mechanisms of tactile perception: morphological and chemical organization of the innervation to the skin. In: Basbaum AI, Kaneko A, Shepherd GM, Westheimer G, editors. The senses: a comprehensive reference. San Diego: Academic Press. 6:1-31.
42. Rotolo T, Smallwood PM, Williams J, Nathans J. 2008. Genetically-directed, cell type-specific sparse labeling for the analysis of neuronal morphology. PLOS ONE 3:e4099. doi: 10.1371/journal.pone.0004099.
43. Saito M, Iwawaki T, Taya C, Yonekawa H, Noda M, Inui Y, Mekada E, Kimata Y, Tsuru A, Kohno K. 2001. Diphtheria toxin receptor-mediated conditional and targeted cell ablation in transgenic mice. Nature Biotechnology 19:746-750. doi: 10.1038/90795.
44. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annual Review Neuroscience 22:389-442. doi: 10.1146/annurev.neuro.22.1.389.
45. Schepers AG, Snippert HJ, Stange DE, Van den Born M, Van Es JH, Van de Wetering M, Clevers H. 2012. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337:730-735. doi: 10.1126/science.1224676.
46. Schlake T. 2007. Determination of hair structure and shape. Seminars in Cell & Developmental Biology 18:267-273. doi: 10.1016/j.semcdb.2007.01.005.
47. Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH. 2009. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 462:651-655. doi: 10.1038/nature08505.
48. Takahashi-Iwanaga H. 2000. Three-dimensional microanatomy of longitudinal lanceolate endings in rat vibrissae. The Journal of Comparative Neurology 426:259-269. doi: 10.1002/1096-9861(20001016)426:23.0.CO;2-N.
49. Wende H, Lechner SG, Cheret C, Bourane S, Kolanczyk ME, Pattyn A, Reuter K, Munier FL, Carroll P, Lewin GR, Birchmeier C. 2012. The Transcription factor c-Maf controls touch receptor development and function. Science 335:1373-1376. doi: 10.1126/science.1214314.
50. Woo SH, Baba Y, Franco AM, Lumpkin EA, Owens DM. 2012. Excitatory glutamate is essential for development and maintenance of the piloneural mechanoreceptor. Development 139:740-748. doi: 10.1242/dev.070847.
51. Yamamoto T. 1966. The fine structure of the palisade-type sensory endings in relation ×to hair follicles. Journal of Electron Microscopy 15:158-166.
52. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW. 2012. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 32:3131-3141. doi: 10.1523/JNEUROSCI.4469-11.2012.