A synthetic sandalwood odorant induces wound-healing processes in human keratinocytes via the olfactory receptor OR2AT4

Journal of Investigative Dermatology

Volumn 134, Issue 11, 2014, Pages 2823-2832

  Busse, Daniela ^a   Kudella, Philipp ^a   Grüning, Nana Maria ^a,e   Gisselmann, Günter ^a   Ständer, Sonja ^b   Luger, Thomas ^b   Jacobsen, Frank ^c   Steinsträßer, Lars ^c,f   Paus, Ralf ^d   Gkogkolou, Paraskevi ^b   Böhm, Markus ^b   Hatt, Hanns ^a   Benecke, Heike ^a,g  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f Evangelisches Krankenhaus   (Germany)

^g Center for Nanoscale Microscopy and Molecular Physiology of the Brain   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM; CYCLIC AMP; HERBACEOUS AGENT; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OR2AT4 RECEPTOR; RECEPTOR; RNA; SANDALORE; UNCLASSIFIED DRUG; WOUND HEALING PROMOTING AGENT; OLFACTORY RECEPTOR; OR2AT4 PROTEIN, HUMAN;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL STIMULATION; CONTROLLED STUDY; DRUG RECEPTOR BINDING; EMBRYO; ENZYME PHOSPHORYLATION; EPITHELIZATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KERATINOCYTE; OLFACTORY RECEPTOR; PROTEIN FUNCTION; RNA INTERFERENCE; SANTALUM; SKIN CULTURE; SKIN RECEPTOR; WOUND HEALING; CELL MOTION; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; METABOLISM; MOLECULAR CLONING; ODOR; SIGNAL TRANSDUCTION; SKIN;

CALCIUM; CELL MOVEMENT; CELL PROLIFERATION; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; KERATINOCYTES; MAP KINASE SIGNALING SYSTEM; ODORS; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; RNA INTERFERENCE; SANTALUM; SIGNAL TRANSDUCTION; SKIN; WOUND HEALING;

EID: 84908567248     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.273     Document Type: Article

References (73)

1. Abaffy T, Malhotra A, Luetje CW (2007) The molecular basis for ligand specificity in a mouse olfactory receptor: a network of functionally important residues. J Biol Chem 282:1216-24
2. Adipietro KA, Mainland JD, Matsunami H (2012) Functional evolution of mammalian odorant receptors. PLoS Genet 8:e1002821
3. Ansari KM, Rundhaug JE, Fischer SM (2008) Multiple signaling pathways are responsible for prostaglandin E2-induced murine keratinocyte proliferation. Mol Cancer Res 6:1003-16
4. Bieri S, Monastyrskaia K, Schilling B (2004) Olfactory receptor neuron profiling using sandalwood odorants. Chem Senses 29:483-7
5. Bos JD, Meinardi MM (2000) The 500 Dalton rule for the skin penetration of chemical compounds and drugs. Exp Dermatol 9:165-9
6. Boukamp P, Petrussevska RT, Breitkreutz D., et al (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-71
7. Braun T, Voland P, Kunz L., et al (2007) Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132: 1890-901
8. Chung M, Lee H, Mizuno A., et al (2004) TRPV3 and TRPV4 mediate warmthevoked currents in primary mouse keratinocytes. J Biol Chem 279: 21569-75
9. Denda M (2003) Epidermis of the skin as a self-organizing electrochemical sensor. In: Nakata S (ed.) Chemical Analysis Based on Nonlinearity. NOVA: New York, 132-8
10. Denda M, Inoue K, Fuziwara S., et al (2002) P2X purinergic receptor antagonist accelerates skin barrier repair and prevents epidermal hyperplasia induced by skin barrier disruption. J Invest Dermatol 119:1034-40
11. Denda M, Nakatani M, Ikeyama K., et al (2007) Epidermal keratinocytes as the forefront of the sensory system. Exp Dermatol 16:157-61
12. Denda M, Tsutsumi M (2011) Roles of transient receptor potential proteins (TRPs) in epidermal keratinocytes. Adv Exp Med Biol 704:847-60
13. Denda S, Takei K, Kumamoto J., et al (2012) Oxytocin is expressed in epidermal keratinocytes and released upon stimulation with adenosine 5?-[g-Thio]-Triphosphate in vitro. Exp Dermatol 21:535-7
14. Feingold KR, Denda M (2012) Regulation of permeability barrier homeostasis. Clin Dermatol 30:263-8
15. Feldmesser E, Olender T, Khen M., et al (2006) Widespread ectopic expression of olfactory receptor genes. BMC Genomics 7:121
16. Fitzsimons C, Engel N, Policastro L., et al (2002) Regulation of phospholipase Cactivation by the number of H(2) receptors during Ca(2θ)-induced differentiation of mouse keratinocytes. Bio Chem Pharmacol 63:1785-96
17. Flegel C, Manteniotis S, Osthold S., et al (2013) Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS ONE 8: e55368
18. Flori E, Mastrofrancesco A, Kovacs D., et al (2011) 2,4,6-Octatrienoic acid is a novel promoter of melanogenesis and antioxidant defence in normal human melanocytes via PPAR-g activation. Pigment Cell Melanoma Res 24:618-30
19. Gáspár E, Nguyen-Thi KT, Hardenbicker C., et al (2011) Thyrotropin-releasing hormone selectively stimulates human hair follicle pigmentation. J Invest Dermatol 131:2368-77
20. Gurtner GC, Werner S, Barrandon Y., et al (2008) Wound repair and regeneration. Nature 453:314-21
21. Haynes LW (1992) Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by l-cis-diltiazem. J Gen Physiol 100:783-801
22. Hosokawa R, Urata MM, Ito Y., et al (2005) Functional significance of Smad2 in regulating basal keratinocyte migration During wound healing. J Invest Dermatol 125:1302-9
23. Ikeyama K, Nakatani M, Kumamoto J., et al (2013) Distinct intracellular calcium responses of individual cultured human keratinocytes to air pressure changes. Skin Res Technol 19:346-51
24. Inoue K, Denda M, Tozaki H., et al (2005) Characterization of multiple P2X receptors in cultured normal human epidermal keratinocytes. J Invest Dermatol 124:756-63
25. Inoue K, Koizumi S, Fuziwara S., et al (2002) Functional vanilloid receptors in cultured normal human epidermal keratinocytes. BioChem Biophys Res Commun 291:124-9
26. Jacobsen F, Baraniskin A, Mertens J., et al (2005) Activity of histone H1.2 in infected burn wounds. J Antimicrob Chemother 55:735-41
27. Kang N, Koo J (2012) Olfactory receptors in non-chemosensory tissues. BMB Rep 45:612-22
28. Koizumi H, Ohkawara A (1999) H2 histamine receptor-mediated increase in intracellular Ca2θ in cultured human keratinocytes. J Dermatol Sci 21:127-32
29. Krautwurst D, Yau KW, Reed RR (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917-26
30. Lebonvallet N, Boulais N, Le Gall C., et al (2012) Effects of the re-innervation of organotypic skin explants on the epidermis. Exp Dermatol 21:156-8
31. Lebonvallet N, Pennec J, Le Gall C., et al (2013) Effect of human skin explants on the neurite growth of the PC12 cell line. Exp Dermatol 22:224-5
32. Marshall CJ (1994) MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Genet. Dev 4:82-9
33. McGovern JA, Heinemann JR, Burke LJ., et al (2013) Stratum basale keratinocyte expression of the cell-surface glycoprotein CDCP1 during epidermogenesis and its role in keratinocyte migration. Br J Dermatol 168:496-503
34. Meier NT, Haslam IS, Pattwell DM., et al (2013) Thyrotropin-releasing hormone (TRH) promotes wound re-epithelialisation in frog and human skin. PLoS ONE 8:e73596
35. Mü ller A, Meyer M, Werner S (2012) The roles of receptor tyrosine kinases and their ligands in the wound repair process. Semin Cell Dev Biol 23:963-70
36. Neuhaus EM, Zhang W, Gelis L., et al (2009) Activation of an olfactory receptor inhibits proliferation of prostate cancer cells. J Biol Chem 284:16218-25
37. Oda Y, Timpe LC, McKenzie RC., et al (1997) Alternatively spliced forms of the cGMP-gated channel in human keratinocytes. FEBS Lett 414:140-5
38. Odland G, Ross R (1968) Human wound repair. Epidermal regeneration. J Cell Biol 39:135-51
39. Oka Y, Nakamura A, Watanabe H., et al (2004) An odorant derivative as an antagonist for an olfactory receptor. Chem Senses 29:815-22
40. Paus R (2013) Migrating melanocyte stem cells: masters of disaster?. Nat Med 19:818-9
41. Paus R, Theoharides TC, Arck PC (2006) Neuroimmunoendocrine circuitry of the ?brain-skin connection?. Trends Immunol 27:32-9
42. Plikus MV, Gay DL, Treffeisen E., et al (2012) Epithelial stem cells and implications for wound repair. Semin Cell Dev Biol 23:946-53
43. Plonka PM, Passeron T, Brenner M., et al (2009) What are melanocytes really doing all day longy?. Exp Dermatol 18:799-819
44. Roosterman D, Goerge T, Schneider SW., et al (2006) Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol. Rev 86:1309-79
45. Saito H, Chi Q, Zhuang H., et al (2009) Odor coding by a Mammalian receptor repertoire. Sci Signal 2:ra9
46. Saito H, Kubota M, Roberts RW., et al (2004) RTP family members induce functional expression of mammalian odorant receptors. Cell 119:679-91
47. Samuelov L, Sprecher E, Sugawara K., et al (2013) Topobiology of human pigmentation: P-cadherin selectively stimulates hair follicle melanogenesis. J Invest Dermatol 133:1591-600
48. Scuri M, Samsell L, Piedimonte G (2010) The role of neurotrophins in inflammation and allergy. Inflamm Allergy Drug Targets 9:173-80
49. Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9:726-35
50. Sharma G, He J, Bazan HEP (2003) p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-Talk activation between MAP kinase cascades. J Biol Chem 278: 21989-97
51. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122:3209-13
52. Shibata S, Tada Y, Asano Y., et al (2012) Adiponectin regulates cutaneous wound healing by promoting keratinocyte proliferation and migration via the ERK signaling pathway. J Immunol 189:3231-41
53. Shirokova E, Schmiedeberg K, Bedner P., et al (2005) Identification of specific ligands for orphan olfactory receptors. G protein-dependent agonism and antagonism of odorants. J Biol Chem 280:11807-15
54. Siegel BW, Wiech NL (1976) RMI 12330A: inhibitor of cholera toxin induced intestinal hypersecretion which also inhibits adenylate cyclase activity. Gastroenterology 70:937-45
55. Slominski A, Paus R, Schadendorf D (1993) Melanocytes as "sensory" and regulatory cells in the epidermis. J Theor Biol 164:103-20
56. Slominski A, Wortsman J (2000) Neuroendocrinology of the skin. Endocr Rev 21:457-87
57. Sondersorg AC, Busse D, Neufang G., et al (2014) Chemosensory information processing between keratinocytes and trigeminal neurons. J Biol Chem 28:17529-40
58. Spehr M, Gisselmann G, Poplawski A., et al (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:2054-8
59. Stander S, Moormann C, Schumacher M., et al (2004) Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 13:129-39
60. Stenn K, Depalma L (1988) Re-epithelialiation. In: Clark RAF, Henson PM (eds) The Molecular and Cellular Biology of Wound Repair. Plenum Press: New York, 321-5
61. Stork PJ, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-66
62. Vanderhaeghen P, Schurmans S, Vassart G., et al (1997) Specific repertoire of olfactory receptor genes in the male germ cells of several mammalian species. Genomics 39:239-46
63. Veitinger T, Riffell JR, Veitinger S., et al (2011) Chemosensory Ca2θ dynamics correlate with diverse behavioral phenotypes in human sperm. J Biol Chem 286:17311-25
64. Wallrabenstein I, Kuklan J, Weber L., et al (2013) Human Trace Amine-Associated Receptor TAAR5 Can Be Activated by Trimethylamine. PLoS ONE 8:e54950
65. Wang Z, Yang H, Tachado SD., et al (2006) Phosphatase-mediated crosstalk control of ERK and p38 MAPK signaling in corneal epithelial cells. Invest Ophthalmol Vis Sci 47:5267-75
66. Weinryb I, Michel IM (1974) Interactions of alpha-methylfluorene-2-Acetic acid with adenylate cyclase. BioChem Pharmacol 23:2411-9
67. Wetzel CH, Oles M, Wellerdieck C., et al (1999) Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus Laevis oocytes. J Neurosci 19:7426-33
68. Woodley DT, Chen JD, Kim JP., et al (1993) Re-epithelialization. Human keratinocyte locomotion. Dermatol Clin 11:641-6
69. Zhang X, Bedigian AV, Wang W., et al (2012) G protein-coupled receptors participate in cytokinesis. Cytoskeleton (Hoboken) 69:810-8
70. Zhang X, de La Cruz O, Pinto JM., et al (2007) Characterizing the expression of the human olfactory receptor gene family using a novel DNA microarray. Genome Biol 8:R86
71. Zhao W, Ho L, Varghese M., et al (2013) Decreased level of olfactory receptors in blood cells following traumatic brain injury and potential association with tauopathy. J Alzheimers Dis 34:417-29
72. Zheng J, Trudeau MC, Zagotta WN (2002) Rod cyclic nucleotide-gated channels have a stoichiometry of three CNGA1 subunits and one CNGB1 subunit. Neuron 36:891-6
73. Zufall F, Hatt H, Firestein S (1993) Rapid application and removal of second messengers to cyclic nucleotide-gated channels from olfactory epithelium. Proc Natl Acad Sci USA 90:9335-9