Beta-caryophyllene enhances wound healing through multiple routes
Autoři:
Sachiko Koyama aff001; Anna Purk aff002; Manpreet Kaur aff003; Helena A. Soini aff004; Milos V. Novotny aff004; Keith Davis aff005; C. Cheng Kao aff006; Hiroaki Matsunami aff007; Anthony Mescher aff008
Působiště autorů:
Medical Sciences, School of Medicine, Indiana University, Bloomington, IN, United States of America
aff001; School of Public Health, Indiana University, Bloomington, IN, United States of America
aff002; Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, United States of America
aff003; Department of Chemistry, and Institute for Pheromone Research, Indiana University, Bloomington, Indiana, United States of America
aff004; Department of Biology, Biotechnology Program, Indiana University, Bloomington, IN, United States of America
aff005; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, Indiana, United States of America
aff006; Department of Molecular Genetics and Microbiology, School of Medicine, Duke University, Durham, North Carolina, United States of America
aff007; Department of Anatomy and Cell Biology, School of Medicine, Indiana University, Bloomington, Indiana, United States of America
aff008
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0216104
Souhrn
Beta-caryophyllene is an odoriferous bicyclic sesquiterpene found in various herbs and spices. Recently, it was found that beta-caryophyllene is a ligand of the cannabinoid receptor 2 (CB2). Activation of CB2 will decrease pain, a major signal for inflammatory responses. We hypothesized that beta-caryophyllene can affect wound healing by decreasing inflammation. Here we show that cutaneous wounds of mice treated with beta-caryophyllene had enhanced re-epithelialization. The treated tissue showed increased cell proliferation and cells treated with beta-caryophyllene showed enhanced cell migration, suggesting that the higher re-epithelialization is due to enhanced cell proliferation and cell migration. The treated tissues also had up-regulated gene expression for hair follicle bulge stem cells. Olfactory receptors were not involved in the enhanced wound healing. Transient Receptor Potential channel genes were up-regulated in the injured skin exposed to beta-caryophyllene. Interestingly, there were sex differences in the impact of beta- caryophyllene as only the injured skin of female mice had enhanced re-epithelialization after exposure to beta-caryophyllene. Our study suggests that chemical compounds included in essential oils have the capability to improve wound healing, an effect generated by synergetic impacts of multiple pathways.
Klíčová slova:
Epidermis – Hair follicles – Inflammation – Wound healing – Hedgehog signaling – Oils – Cell proliferation – Olfactory receptors
Zdroje
1. Koyama S. Primer Effects by Murine Pheromone Signaling. Pheromonal Influences on Reproductive Conditions. Springer International Publishing AG, Vienna: Springer Briefs in Animal Sciences, Springer; 2016.
2. Kim JT, Ren CJ, Fielding GA, Pitti A, Kasumi T, Wajda M, Lebovits A, Bekker A. Treatment with lavender aromatherapy in the post-anesthesia care unitreduces opioid requirements of morbidly obese patients undergoing laparoscopic adjustable gastric banding. Obes Surg. 2007;17(7): 920–925. doi: 10.1007/s11695-007-9170-7 17894152
3. Marzouk T, Barakat R, Ragab A, Badria F, Badawy A. Lavender-thymol as a new topical aromatherapy preparation for episiotomy: a randomized clinical trial. J Obstet Gynaecol. 2015;35(5): 472–475. doi: 10.3109/01443615.2014.970522 25384116
4. Malcolm BJ, Tallian K. Essential oil of lavender in anxiety disorders: ready for prime time? Ment Health Clin. 2017;7(4): 147–155. doi: 10.9740/mhc.2017.07.147 29955514
5. Nasiri A, Mahmodi MA. Aromatherapy massage with lavender essential oil and the prevention of disability in ADL in patients with osteoarthritis of the knee: a randomized controlled clinical trial. Complement Ther Clin Pract. 2018;30: 116–121. doi: 10.1016/j.ctcp.2017.12.012 29389470
6. Schneider R, Singer N, Singer T. Medical aromatherapy revisited- basic mechanisms, critique, and a new development. Hum Psychopharmacol Clin Exp. 2019;34: e2683.
7. Mazutti d Silva SM, Rezende Costa CR, Gelfuso GM, Silva Guerra EN, de Medeiros Nobreg YK. Et al. Wound healing effect of essential oil extracted from Eugenia dysenterica DC (Myrtaceae) leaves. Molecules. 2019; 24: 2.
8. Tanbirul Haque ASM, Moon JN, Saravana PS, Tilahun A, Chun B-S. Composition of Asarum heterotropoides var. mandshuricum radix oil from different extraction methods and activities against human body odor-producing bacteria. J Food Drug Anal. 2016; 24(4): 813–821. doi: 10.1016/j.jfda.2016.04.006 28911620
9. El-Jalel LFA, Elkady WM, Gonaid MH, El-Gareeb KA. Differences in chemical composition and antimicrobial activity of Thymus capitatus essential oil at different altitudes. Future J. Pharm Sci. 2018; 4(2): 156–160.
10. Lee L-S, Kim S-H, Kim Y-B, Kim Y-C. Quantitative analysis of major constituents in green tea with different plucking periods and their antioxidant activity. Molecules. 2014; 19: 9173–9186. doi: 10.3390/molecules19079173 24988187
11. Chamorro ER, Ballerini G, Sequeira AF, Velasco GA, Zalazar MF. Chemical composition of essential oil from Tagetes minuta L. leaves and flowers. J. Argentine Chem Soc. 2008; 96(1–2): 80–86.
12. Lis A, Swaczyna A, Krajewska A, Mellor K. Chemical composition of the essential oils from twigs, leaves, and cones of Thuja plicata and its cultivar varieties “fastigiata”, “kornik,” and “zebrina”. Nat. Prod. Comm. 2019; 2019: 1–5.
13. Ma D-L, Chan DS-H, Wei G, Zhong H-J, Yang H. et al. Virtual screening and optimization of Type II inhibitors of JAK2 from a natural product library. Chem. Commun. 2014; 50: 13885–13888.
14. Yang C, Wang W, Chen L, Liang J, Lin S. et al. Discovery of a VHL and HIF1alpha interaction inhibitor with in vivo angiogenic activity via structure-based virtual screening. Chem. Comm. 2016; 52:12837–12840. doi: 10.1039/c6cc04938a 27709157
15. Khazneh E, Hribova P, Hosek J, Suchy P, Kollar P. et al. The chemical composition of Achillea wilhelmsii C. Koch and its desirable effects on hyperglycemia, inflammatory mediators and hypercholesterolemia as risk factors for cardiometabolic disease. Molecules. 2016; 21(4): 404. doi: 10.3390/molecules21040404 27023504
16. Yu SH, Seol GH. Lavandula angustifolia Mill. Oil and its active constituent linalyl acetate alleviate pain and urinary residual sense after colorectal cancer surgery: a randomised controlled trial. Evid. Based Complement. Alternat. Med. 2017; 2017: 3954181. doi: 10.1155/2017/3954181 28154606
17. de Freitas Souza C, Descovi S, Baldissera MD, Bertolin K, Bianchini AE. et al. Involvement of HPI-axis in anesthesia with Lippia alba essential oil citral and linalool chemotypes: gene expression in the secondary responses in silver catfish. Fish Physiol. Biochem. 2019; 45(1): 155–166. doi: 10.1007/s10695-018-0548-3 30120603
18. Kang N, Koo J. Olfactory receptors in non-chemosensory tissues. BMB Rep. 2012;45(11): 612–622. doi: 10.5483/BMBRep.2012.45.11.232 23186999
19. Chen Z, Zhao H, Fu N, Chen L. The diversified function and potential therapy of ectopic olfactory receptors in non-olfactory tissues. J Cell Physiol. 2018;233(3): 2104–2115. doi: 10.1002/jcp.25929 28338216
20. Gertsch J, Leonti M, Raduner S, Racz I, Chen JZ, Xie XQ, Altmann K-H, Karsak M, Zimmer A. Beta-caryophyllene is a dietary cannabinoid. Proc Natl Acad Sci USA. 2008;105: 9099–9104. doi: 10.1073/pnas.0803601105 18574142
21. Zheng JL, Yu TS, Li XN, Fan YY, Ma WX, Du Y, Zhao R, Guan D-W. Cannabinoid receptor type 2 is time-dependently expressed during skin wound healing in mice. Int J Legal Med. 2012;126(5): 807–814. doi: 10.1007/s00414-012-0741-3 22814434
22. Li SS, Wang LL, Liu M, Jiang SK, Zhang M, Tian ZL, Wang M, Li J-Y, Zhao R, Guan D-W. Cannabinoid CB2 receptors are involved in the regulation of fibrogenesis during skin repair in mice. Mol Med Rep. 2016;13(4): 3441–3450. doi: 10.3892/mmr.2016.4961 26935001
23. Wang LL, Zhao R, Li JY, Liu M, Wang M, Zhang MZ, Dong W-W, Jiang S-K, Xhang M, Tian Z-L, Liu C-S, Guan D-W. Pharmacological activation of cannabinoid 2 receptor attenuates inflammation, fibrogenesis and promotes re-epithelialization during skin wound healing. Eur J Pharmacol. 2016;786: 128–136. doi: 10.1016/j.ejphar.2016.06.006 27268717
24. Amorim JL, Figueiredo JB, Amaral ACF, Barros EGO, Pelmero C, MPalantinos MA, Ramos AdS, Ferreira JLP, Silva JRdA, Benjamim CF, Basso SL, Nasciutti LE, Fernandes PD. Wound healing properties of Copaifera paupera in diabetic mice. PloS One. 2017;12(10): e0187380. doi: 10.1371/journal.pone.0187380 29088304
25. Gonzalez AC, Costa TF, Andrade ZA, Medrado AR. Wound healing–A literature review. An Bras Dermatol. 2016;91(5): 614–620. doi: 10.1590/abd1806-4841.20164741 27828635
26. Landen NX, Li D, Stahle M. Transition from inflammation to proliferation: a critical step during wound healing. Cell Mol Life Sci. 2016;73: 3861–3885. doi: 10.1007/s00018-016-2268-0 27180275
27. Rittie L. Cellular mechanisms of skin repair in humans and other animals. J Cell Commun Signal. 2016;10: 103–120. doi: 10.1007/s12079-016-0330-1 27170326
28. Sorg H, Tilkorn DJ, Hager S, Hauser J. Skin wound healing: an update on current knowledge and concepts. Eur Surg Res. 2017;58(1–2): 81–94. doi: 10.1159/000454919 27974711
29. Braiman-Wiksman L, Solomonik I, Spira R, Tennenbaum T. Novel insights into wound healing sequence of events. Toxicol Pathol. 2007; 35: 767–779. doi: 10.1080/01926230701584189 17943650
30. Tracy LE, Minasian RA, Caterson EJ. Extracellular matrix and dermal fibroblast function in the healing wound. Adv Wound Care (New Rochelle). 2016; 5(3): 119–136.
31. Kezic S, Jakasa I. Filaggrin and skin barrier function. Curr Probl Dermatol. 2016; 49: 1–7. doi: 10.1159/000441539 26844893
32. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MWJ. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med. 1997;3(11): 1209–1215. doi: 10.1038/nm1197-1209 9359694
33. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev. 1999; 79(4): 1283–1316. doi: 10.1152/physrev.1999.79.4.1283 10508235
34. Horikawa S, Ishii Y, Hamashima T, Yamamoto S, Mori H, Fujimori T, Shen J, Inoue R, Nishizono H, Itoh H, Majima M, Abraham D, Miyawaki T, Sasahara M. PDGFRα plays a crucial role in connective tissue remodeling. Sci Rep. 2016; 5:17948. doi: 10.1038/Srep17948
35. Ivaska J, Pallari HM, Nevo J, Eriksson JE. Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res. 2007; 313(10): 2050–2062. doi: 10.1016/j.yexcr.2007.03.040 17512929
36. Cheng F, Shen Y, Mohanasundaram P, Lindstrom M, Ivaska J, Ny T, Eriksson JE. Vimentin coordinates fibroblast proliferation and keratinocyte differentiation in wound healing via TGF-β-slug signaling. Proc Natl Acad Sci U S A. 2016; 113(30): E4320–4327. doi: 10.1073/pnas.1519197113 27466403
37. Solanas G., Benitah S.A. Regenerating the skin: a task for the heterogeneous stem cell pool and surrounding niche. Nat Rev Mol Cell Biol 2013; 14: 737–748. doi: 10.1038/nrm3675 24064540
38. Kretzschmar K., Watt F.M. Markers of epidermal stem cell subpopulations in adult mammalian skin. Cold Spring Harb Perspect Med 2014; 4: a013631. doi: 10.1101/cshperspect.a013631 24993676
39. Watt F.M. Mammalian skin cell biology: At the interface between laboratory and clinic. Science 2014; 346: 937–940. doi: 10.1126/science.1253734 25414300
40. Aragona M, Dekoninck S, Rulands S, Lenglez S, Mascre G, Simons BD, Blanpain C. Defining stem cell dynamics and migration during wound healing in mouse skin epidermis. Nat Comm. 2017;8: Article number 14684.
41. Ito M., Liu Y., Yang Z., Nguyen J., Liang F., Morris R.J., Cotsarelis G. Stem cells in the hair follicle bulge contribute to repair but not to homeostasis of epidermis. Nat Med 2005; 11: 1351–1354. doi: 10.1038/nm1328 16288281
42. Pertwee R, Griffin G, Fernando S, Li X, Hill A, Makriyannis A. AM630, a competitive cannabinoid receptor antagonist. Life Sci. 1995; 56(23–24): 1949–1955. doi: 10.1016/0024-3205(95)00175-6 7776818
43. Huffman JW. CB2 receptor ligands. Mini Rev Med Chem. 2005; 5(7): 641–649. doi: 10.2174/1389557054368844 16026310
44. Wu DD, Inwin DM, Zhang YP. Molecular evolution of the keratin associated protein gene family in mammals, role in the evolution of mammalian hair. BMC Evol Biol. 2008; 8: 241. doi: 10.1186/1471-2148-8-241 18721477
45. Fujikawa H, Fujimoto A, Farooq M, Ito N, Shimomura Y. Characterization of the human hair keratin-associated protein 2 (KRTAP2) gene family. J Invest Dermatol. 2012;132: 1806–1813 doi: 10.1038/jid.2012.73 22495175
46. Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. Molecular cloning of a gene encoding a new type of metalloproteinase-disintegrin family protein with thrombospondin motifs as an inflammation associated gene. J Biol Chem. 1997; 272(1): 556–562. doi: 10.1074/jbc.272.1.556 8995297
47. Grotewold L, Plum M, Dildrop R, Peters T, Ruther U. Bambi is coexpressed with Bmp-4 during mouse embryogenesis. Mech Dev. 2001; 100(2): 327–330. doi: 10.1016/s0925-4773(00)00524-4 11165491
48. Liu YH, Ma L, Wu LY, Luo W, Kundu R, Sangiorgi F, Snead ML, Maxson R. Regulation of the Msx2 homeobox gene during mouse embryogenesis: a transgene with 439 bp of 5’ flanking sequence is expressed exclusively in the apical ectodermal ridge of the developing limb. Mech Dev. 1994; 48(3): 187–197. doi: 10.1016/0925-4773(94)90059-0 7893602
49. Morasso MI, Markova NG, Sargent TD. Regulation of epidermal differentiation by a Distal-less homeodomain gene. J Cell Biol. 1996; 135(6 Pt 2): 1879–1887. doi: 10.1083/jcb.135.6.1879 8991098
50. Dong S, Yng S, Kojima T, Shiraiwa M, Kawada A, Mechin MC, Adoue V, Chavanas S, Serre G, Simon M, Takahara H. Crucial roles of MZF1 and Sp1 in the transcriptional regulation of the peptidylarginine deiminase type I gene (PADI1) in human keratinocytes. J Invet Dermatol. 2008; 128(3): 549–557.
51. Jave-Suarez LF, Winter H, Langbein L, Rogers MA, Schweizer J. HOXC13 is involved in the regulation of human hair keratin gene expression. J Biol Chem. 2002; 277(5): 3718–3726. doi: 10.1074/jbc.M101616200 11714694
52. Breen EC, Tang K. Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro. J Cell Biochem. 2003; 88(4): 848–854. doi: 10.1002/jcb.10398 12577318
53. Kondo T, Ohshima T. The dynamics of inflammatory cytokines in the healing process of mouse skin wound: a preliminary study for possible wound age determination. Int J Legal Med. 1996; 108: 231–236. doi: 10.1007/bf01369816 8721421
54. St Laurent G III, Seilheimer B, Tackett M, Zhou J, Shtokalo D. Vyatkin Y, Ri M, Toma I, Jones D, McCaffrey TA. Deep sequencing transcriptome analysis of murine wound healing: effects of a multicomponent, multitarget natural product therapy-Tr14. Front Mol Biosci. 2017;17: https://doi.org/10.3389/fmolb.2017.00057.
55. Premkumar LS. Transient receptor potential channels as targets for phytochemicals. ACS Chem Neurosci. 2014; 5(11): 1117–1130. doi: 10.1021/cn500094a 24926802
56. Caterina MJ. TRP channel cannabinoid receptors in skin sensation, homeostasis, and inflammation. ACS Chem Neurosci. 2014; 5(11): 1107–1116. doi: 10.1021/cn5000919 24915599
57. Premkumar LS, Abooj M. TRP channels and analgesia. Life Sci. 2013; 92(8–9): 415–424. doi: 10.1016/j.lfs.2012.08.010 22910182
58. Colonna M, Facchetti F. TREM-1 (triggering receptor expressed on myeloid cells): a new player in acute inflammatory responses. J Infect Dis. 2003; 187 Suppl 2: S397–401.
59. Johnson RL, Riddle RD, Laufer E, Tabin C. Sonic hedgehog: a key mediator of anterior-posterior patterning of the limb and dorso-ventral patterning of axial embryonic structures. Biochem Soc Trans. 1994; 22(3): 569–574. doi: 10.1042/bst0220569 7821639
60. Eaton S. Planar polarization of drosophila and vertebrate epithelia. Curr Opin Cell Biol. 1997; 9(6): 880–886.
61. Maddaluno L, Urwyler C, Werner S. Fibroblast growth factors: key players in regeneration and tissue repair. Development, 2017; 144(22): 4047–4060. doi: 10.1242/dev.152587 29138288
62. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009; 17(1): 9–26. doi: 10.1016/j.devcel.2009.06.016 19619488
63. Abe Y., Tanaka N. Roles of hedgehog signaling pathway in epidermal and hair follicle development, homeostasis, and cancer. J Dev Biol 2017; 5: E12 doi: 10.3390/jdb5040012 29615568
64. Brownell I. Guevara E., Bai C.B., Loomis C.A., Joyner A.L. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011; 8(5): 552–565. doi: 10.1016/j.stem.2011.02.021 21549329
65. Caddy J., Wilanowski T., Darido C., Dworkin S., Ting S.B. Zhao Q, Rank G, Auden A, Srivastava S, Papenfuss TA, Murdoch JN, Humbert PO, Boulos N, Weber T, Zuo J, Cunningham JM, Jane SM. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev Cell 2010; 19(1): 138–147. doi: 10.1016/j.devcel.2010.06.008 20643356
66. Bayly R., Axelrod J.D. Pointing in the right direction: new developments in the field of planar cell polarity. Nat Rev Genet 2011; 12(6): 385–391. doi: 10.1038/nrg2956 21502960
67. Munoz-Soriano V., Belacortu Y., Paricio N. Planar cell polarity signaling in collective cell movements during morphogenesis and disease. Curr Genomics 2012; 13(8): 609–622. doi: 10.2174/138920212803759721 23730201
68. Richardson R., Metzger M., Knyphausen P., Ramezani T., Slanchev K., Kraus C., Schmelzer E., Hammerschmidt M. Re-epithelialization of cutaneous wounds in adult zebrafish combines mechenisms of wound closure in embryonic and adult mammals. Development 2016; 143: 2077–2088. doi: 10.1242/dev.130492 27122176
69. Azzi L, El-Alfy M, Martel C, Labrie F. Gender differences in mouse skin morphology and specific effects of sex steroids and dehydroepiandrosterone. J. Invest. Dermatol. 2005;124(1): 22–27. doi: 10.1111/j.0022-202X.2004.23545.x 15654949
70. Ashcroft GS, Mills SJ. Androgen receptor-mediated inhibition of cutaneous wound healing. J Clin Invest. 2002;110(5), 615–624. doi: 10.1172/JCI15704 12208862
71. Gilliver SC, Ashcroft GS. Sex steroids and cutaneous wound healing: the contrasting influences of estrogens and androgens. Climacteric. 2007;10(4) 276–288. doi: 10.1080/13697130701456630 17653954
72. Busse D, Kudella P, Gruening NM, Gisselmann G, Stander S, Luger T, Jacobsen F, Steinstrasser L, Paus R, Gkogkolou P, Bohm M, Hatt H, Benecke H. A synthetic sandalwood odorant induces wound-healing processes in human keratinocytes via the olfactory receptor OR2AT4. J Invest Dermatol. 2014;134(11): 2823–2832. doi: 10.1038/jid.2014.273 24999593
73. Harada H, Kashiwadani H, Kanmura Y, Kuwaki T. Linalool odor-induced anxiolytic effects in mice. Front Behav Neurosci. 2018;12: 241 doi: 10.3389/fnbeh.2018.00241 30405369
74. Jiang Y, Gong NN, Hu XS, Ni MJ, Pasi R, Matsunami H. Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo. Nat Neurosci. 2015;18: 1446–1454. doi: 10.1038/nn.4104 26322927
75. Sicard G, Holley A. Receptor cell responses to odorants: similarities and differences among odorants. Brain Res. 1985;292: 283–296.
76. Fleischer J, Breer H, Strotmann J. Mammalian olfactory receptors. Front Cell Neurosci. 2009;3: 9. doi: 10.3389/neuro.03.009.2009 19753143
77. Mahmoud MF, Swefy SE, Hasan RA, Ibrahim A. Role of cannabinoid receptors in hepatic fibrosis and apoptosis associated with bile duct ligation in rats. Eur J Pharmacol. 2014;742: 118–124. doi: 10.1016/j.ejphar.2014.08.021 25179573
78. Yang M, Lv Y, Tian X, Lou J, An R, Zhang Q, Li M, Dong Z. Neuroprotective effect of β-caryophyllene on cerebral ischemia-reperfusion injury via regulation of necroptotic neuronal death and inflammation: In vivo and in vitro. Front. Neurosci. 2017;11: 583. doi: 10.3389/fnins.2017.00583 29123466
79. Fuchs Y., Brown S., Gorenc T., Rodriguez J., Fuchs E., Steller H. Sept4/ARTS regulates stem cell apoptosis and skin regeneration. Science 2013; 341: 286–289. doi: 10.1126/science.1233029 23788729
80. Wilgus TA, Bergdall VK, DiPietro LA, Oberyszyn TM. Hydrogen peroxide disrupts scarless fetal wound repair. Wound Repair Regen. 2005;13(5): 513–519. doi: 10.1111/j.1067-1927.2005.00072.x 16176460
81. Mescher AL. Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration. Regeneration. 2017;4: 39–53. doi: 10.1002/reg2.77 28616244
82. Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M. Olfactory receptors are displayed on dog mature sperm cells. J Cell Biol. 1993;123(6 Pt1): 1441–1452.
83. Vosshall LB. Olfaction: attracting both sperm and the nose. Curr Biol. 2004;14(21): R918–920. doi: 10.1016/j.cub.2004.10.013 15530382
84. Adams RP. Identification of essential oil components by gas chromatography/ quadrupole mass spectroscopy. Carol Streams: Allured Publishing Corporation; 2001.
85. Jemiolo B, Harvey S, Novotny M. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc Natl Acad Sci USA. 1986;83(12): 4576–4579. doi: 10.1073/pnas.83.12.4576 3459193
86. Harvey S, Jemiolo B, Novotny M. Pattern of volatile compounds in dominant and subordinate male urine. J Chem Ecol. 1989;15(7): 2061–2072. doi: 10.1007/BF01207438 24272296
87. Lausberg H, Sloetjes H. Coding gestural behavior with NEUROGES—ELAN system. Behav Res Methods. 2009;41(3): 841–849. doi: 10.3758/BRM.41.3.841 19587200
88. Grant EG, Mackintosh JH. A comparison of the social posture of common laboratory rodents. Behaviour, 1963;21: 247–259.
89. Wilson RC, Vacek T, Lanier DL, Dewsbury DA. Open-field behavior in muroid rodents. Behav Biol. 1976;17: 495–506. doi: 10.1016/s0091-6773(76)90901-9 788698
90. Weyers P, Janke W, Macht M, Weijers HG. Social and non-social open field behaviours of rats under light and noise stimulation. Behav Processes. 1994;31: 257–268. doi: 10.1016/0376-6357(94)90011-6 24924938
91. Sköld M, Karlberg AT, Matura M, Börje A. The fragrance chemical beta-caryophyllene-air oxidation and skin sensitization. Food Chem Toxicol. 2005;44: 538–545. doi: 10.1016/j.fct.2005.08.028 16226832
92. Kalueff AV, Tuohimaa P. Grooming analysis algorithm for neurobehavioural stress research. Brain Res Brain Res Protoc. 2004;13(3): 151–158. doi: 10.1016/j.brainresprot.2004.04.002 15296852
93. Smolinsky AN, Bergner CL, LaPorte JL, Kalueff AV. Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. In: Gould TD, editor. Mood and Anxiety Related Phenotypes in Mice, Neuromethods 2017,42, doi: 10.1007/978-1-60761-303-9_2, Humana Press.
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