Skin exposure to UVB light induces a skin-brain-gonad axis and sexual behavior

Roma Parikh; Eschar Sorek; Shivang Parikh; Keren Michael; Lior Bikovski; Sagi Tshori; Galit Shefer; Shira Mingelgreen; Taiba Zornitzki; Hilla Knobler; Gabriel Chodick; Mariya Mardamshina; Arjan Boonman; Noga Kronfeld-Schor; Hadas Bar-Joseph; Dalit Ben-Yosef; Hadar Amir; Mor Pavlovsky; Hagit Matz; Tom Ben-Dov; Tamar Golan; Eran Nizri; Daphna Liber; Yair Liel; Ronen Brenner; Yftach Gepner; Orit Karnieli-Miller; Rina Hemi; Ruth Shalgi; Tali Kimchi; Ruth Percik; Aron Weller; Carmit Levy

doi:10.1016/j.celrep.2021.109579

Skin exposure to UVB light induces a skin-brain-gonad axis and sexual behavior

Roma Parikh, Eschar Sorek, Shivang Parikh, Keren Michael, Lior Bikovski, Sagi Tshori, Galit Shefer, Shira Mingelgreen, Taiba Zornitzki, Hilla Knobler, Gabriel Chodick, Mariya Mardamshina, Arjan Boonman, Noga Kronfeld-Schor, Hadas Bar-Joseph, Dalit Ben-Yosef, Hadar Amir, Mor Pavlovsky, Hagit Matz, Tom Ben-DovTamar Golan, Eran Nizri, Daphna Liber, Yair Liel, Ronen Brenner, Yftach Gepner, Orit Karnieli-Miller, Rina Hemi, Ruth Shalgi, Tali Kimchi, Ruth Percik, Aron Weller, Carmit Levy

Department of Psychology

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

Ultraviolet (UV) light affects endocrinological and behavioral aspects of sexuality via an unknown mechanism. Here we discover that ultraviolet B (UVB) exposure enhances the levels of sex-steroid hormones and sexual behavior, which are mediated by the skin. In female mice, UVB exposure increases hypothalamus-pituitary-gonadal axis hormone levels, resulting in larger ovaries; extends estrus days; and increases anti-Mullerian hormone (AMH) expression. UVB exposure also enhances the sexual responsiveness and attractiveness of females and male-female interactions. Conditional knockout of p53 specifically in skin keratinocytes abolishes the effects of UVB. Thus, UVB triggers a skin-brain-gonadal axis through skin p53 activation. In humans, solar exposure enhances romantic passion in both genders and aggressiveness in men, as seen in analysis of individual questionaries, and positively correlates with testosterone level. Our findings suggest opportunities for treatment of sex-steroid-related dysfunctions.

Original language	English
Article number	109579
Journal	Cell Reports
Volume	36
Issue number	8
DOIs	https://doi.org/10.1016/j.celrep.2021.109579
State	Published - 24 Aug 2021

Bibliographical note

Funding Information:
The authors thank Prof. Eli Pikarsky (The Hebrew University of Jerusalem, Israel) for the gift of the p53-floxed mice and Prof. Itai Ben-Porath for the gift of K14 CRE mice (The Hebrew University of Jerusalem, Israel). C.L. thanks Prof. Yossi Yovel (Department of Zoology, Faculty of Life Sciences, Tel Aviv University) for providing the recording instrument and analysis and Prof. Uri Alon, Prof. Noam Sobel (Weizmann Institute of Science, Israel) for useful discussions, and Yuval and Omer Levy for infinite joy. C.L. acknowledges grant support from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant 726225 ) and the Israel Science Foundation (ISF) (grant 2017/20 ). R. Parikh is the recipient of a CBRC 2020 travel grant and 3 rd Esther and Zvi Weinstat Graduate Student Award, 2021, and would like to thank her family for their love and support. Research in A.W.’s lab is supported in part by the ISF (grant 1781/16 ), Israel Ministry of Science and Technology (grants 3-13608 and 84/19 ), and EPM Inc.

Funding Information:
The authors thank Prof. Eli Pikarsky (The Hebrew University of Jerusalem, Israel) for the gift of the p53-floxed mice and Prof. Itai Ben-Porath for the gift of K14 CRE mice (The Hebrew University of Jerusalem, Israel). C.L. thanks Prof. Yossi Yovel (Department of Zoology, Faculty of Life Sciences, Tel Aviv University) for providing the recording instrument and analysis and Prof. Uri Alon, Prof. Noam Sobel (Weizmann Institute of Science, Israel) for useful discussions, and Yuval and Omer Levy for infinite joy. C.L. acknowledges grant support from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant 726225) and the Israel Science Foundation (ISF) (grant 2017/20). R. Parikh is the recipient of a CBRC 2020 travel grant and 3rd Esther and Zvi Weinstat Graduate Student Award, 2021, and would like to thank her family for their love and support. Research in A.W.?s lab is supported in part by the ISF (grant 1781/16), Israel Ministry of Science and Technology (grants 3-13608 and 84/19), and EPM Inc., R. Parikh, conceptualization, methodology, validation, formal analysis, investigation, writing ? original draft, and visualization. E.S. conceptualization and formal analysis. S.P. methodology and validation (human cohort study). K.M. D.L. and O.K.-M. formal analysis (human questionnaire). L.B. and A.W. methodology and resources. S.T. G.S. S.M. T.Z. H.K. and G.C. investigation and formal analysis (human testosterone data). M.M. formal analysis (mass spectrometry). A.B. resources (ultrasonic vocalization). N.K.-S. writing ? review & editing. H.B.-J. formal analysis (ovary cross sections). D.B.-Y. H.A. and T.G. writing ? review & editing. H.M. and M.P. resources (human questionnaire data from phototherapy clinic). Y.L. R.B. and E.N. visualization. Y.G. formal analysis (human epidemiological data). R.H. investigation. R.S. methodology and writing ? review & editing (ovarian experiments). T.K. visualization (sexual behavioral data). R. Percik, investigation and writing ? review & editing. C.L. conceptualization, methodology, writing ? original draft, visualization, supervision, project administration, and funding acquisition. All authors reviewed the final draft and approved it. The authors declare no competing interests.

Publisher Copyright:
© 2021 The Authors

Keywords

HPG axis
UVB
behavioral
hormones
p53
questionnaires
sexuality
skin
solar
testosterone

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10.1016/j.celrep.2021.109579

Cite this

Parikh, R., Sorek, E., Parikh, S., Michael, K., Bikovski, L., Tshori, S., Shefer, G., Mingelgreen, S., Zornitzki, T., Knobler, H., Chodick, G., Mardamshina, M., Boonman, A., Kronfeld-Schor, N., Bar-Joseph, H., Ben-Yosef, D., Amir, H., Pavlovsky, M., Matz, H., ... Levy, C. (2021). Skin exposure to UVB light induces a skin-brain-gonad axis and sexual behavior. Cell Reports, 36(8), [109579]. https://doi.org/10.1016/j.celrep.2021.109579

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abstract = "Ultraviolet (UV) light affects endocrinological and behavioral aspects of sexuality via an unknown mechanism. Here we discover that ultraviolet B (UVB) exposure enhances the levels of sex-steroid hormones and sexual behavior, which are mediated by the skin. In female mice, UVB exposure increases hypothalamus-pituitary-gonadal axis hormone levels, resulting in larger ovaries; extends estrus days; and increases anti-Mullerian hormone (AMH) expression. UVB exposure also enhances the sexual responsiveness and attractiveness of females and male-female interactions. Conditional knockout of p53 specifically in skin keratinocytes abolishes the effects of UVB. Thus, UVB triggers a skin-brain-gonadal axis through skin p53 activation. In humans, solar exposure enhances romantic passion in both genders and aggressiveness in men, as seen in analysis of individual questionaries, and positively correlates with testosterone level. Our findings suggest opportunities for treatment of sex-steroid-related dysfunctions.",

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Parikh, R, Sorek, E, Parikh, S, Michael, K, Bikovski, L, Tshori, S, Shefer, G, Mingelgreen, S, Zornitzki, T, Knobler, H, Chodick, G, Mardamshina, M, Boonman, A, Kronfeld-Schor, N, Bar-Joseph, H, Ben-Yosef, D, Amir, H, Pavlovsky, M, Matz, H, Ben-Dov, T, Golan, T, Nizri, E, Liber, D, Liel, Y, Brenner, R, Gepner, Y, Karnieli-Miller, O, Hemi, R, Shalgi, R, Kimchi, T, Percik, R, Weller, A & Levy, C 2021, 'Skin exposure to UVB light induces a skin-brain-gonad axis and sexual behavior', Cell Reports, vol. 36, no. 8, 109579. https://doi.org/10.1016/j.celrep.2021.109579

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AU - Parikh, Roma

AU - Sorek, Eschar

AU - Parikh, Shivang

AU - Michael, Keren

AU - Bikovski, Lior

AU - Tshori, Sagi

AU - Shefer, Galit

AU - Mingelgreen, Shira

AU - Zornitzki, Taiba

AU - Knobler, Hilla

AU - Chodick, Gabriel

AU - Mardamshina, Mariya

AU - Boonman, Arjan

AU - Kronfeld-Schor, Noga

AU - Bar-Joseph, Hadas

AU - Ben-Yosef, Dalit

AU - Amir, Hadar

AU - Pavlovsky, Mor

AU - Matz, Hagit

AU - Ben-Dov, Tom

AU - Golan, Tamar

AU - Nizri, Eran

AU - Liber, Daphna

AU - Liel, Yair

AU - Brenner, Ronen

AU - Gepner, Yftach

AU - Karnieli-Miller, Orit

AU - Hemi, Rina

AU - Shalgi, Ruth

AU - Kimchi, Tali

AU - Percik, Ruth

AU - Weller, Aron

AU - Levy, Carmit

PY - 2021/8/24

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N2 - Ultraviolet (UV) light affects endocrinological and behavioral aspects of sexuality via an unknown mechanism. Here we discover that ultraviolet B (UVB) exposure enhances the levels of sex-steroid hormones and sexual behavior, which are mediated by the skin. In female mice, UVB exposure increases hypothalamus-pituitary-gonadal axis hormone levels, resulting in larger ovaries; extends estrus days; and increases anti-Mullerian hormone (AMH) expression. UVB exposure also enhances the sexual responsiveness and attractiveness of females and male-female interactions. Conditional knockout of p53 specifically in skin keratinocytes abolishes the effects of UVB. Thus, UVB triggers a skin-brain-gonadal axis through skin p53 activation. In humans, solar exposure enhances romantic passion in both genders and aggressiveness in men, as seen in analysis of individual questionaries, and positively correlates with testosterone level. Our findings suggest opportunities for treatment of sex-steroid-related dysfunctions.

AB - Ultraviolet (UV) light affects endocrinological and behavioral aspects of sexuality via an unknown mechanism. Here we discover that ultraviolet B (UVB) exposure enhances the levels of sex-steroid hormones and sexual behavior, which are mediated by the skin. In female mice, UVB exposure increases hypothalamus-pituitary-gonadal axis hormone levels, resulting in larger ovaries; extends estrus days; and increases anti-Mullerian hormone (AMH) expression. UVB exposure also enhances the sexual responsiveness and attractiveness of females and male-female interactions. Conditional knockout of p53 specifically in skin keratinocytes abolishes the effects of UVB. Thus, UVB triggers a skin-brain-gonadal axis through skin p53 activation. In humans, solar exposure enhances romantic passion in both genders and aggressiveness in men, as seen in analysis of individual questionaries, and positively correlates with testosterone level. Our findings suggest opportunities for treatment of sex-steroid-related dysfunctions.

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KW - hormones

KW - p53

KW - questionnaires

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KW - skin

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Skin exposure to UVB light induces a skin-brain-gonad axis and sexual behavior

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