Combined Transcriptomic and Proteomic Analyses Reveal the Different Responses to UVA and UVB Radiation in Human Keratinocytes.


Journal

Photochemistry and photobiology
ISSN: 1751-1097
Titre abrégé: Photochem Photobiol
Pays: United States
ID NLM: 0376425

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 23 01 2022
accepted: 25 05 2022
pubmed: 1 6 2022
medline: 25 1 2023
entrez: 31 5 2022
Statut: ppublish

Résumé

Ultraviolet (UV) radiation from sunlight is a major risk factor for many cutaneous pathologies including skin aging and cancers. Despite decades of research, the different responses to UVA and UVB in human keratinocytes have not been systemically investigated. Here, we performed multi-omics to characterize the common and different changes in gene transcription and protein expression after exposure to UVB and UVA, respectively. Keratinocyte cells, treated with or without UV, were analyzed by TMT-labeled MS/MS spectra and RNA-sequencing. A common set of genes/proteins was found to be impacted by both UVA and UVB and the other differential genes/proteins showed wavelength specificity. The common set of genes/proteins were mainly involved in keratinization, lipid metabolic processes and stimulus response. The UVB specifically responsive genes/proteins were mainly related to RNA processing, gene silencing regulation and cytoskeleton organization. The UVA specifically responsive genes/proteins were mainly involved in vesicle-mediated transport and oxygen-containing compound response. Meanwhile, the hub differential genes/proteins in each set were identified by protein-protein interaction networks and cluster analysis. This work provided a global view of the similar and differential molecular mechanisms of UVB- and UVA-induced cell damage in keratinocytes, which would be beneficial for further studies in the prevention or treatment of UV-related pathologies.

Identifiants

pubmed: 35638308
doi: 10.1111/php.13658
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

137-152

Informations de copyright

© 2022 The American Society for Photobiology.

Références

Shen, Y., M. Stanislauskas, G. Li, D. Zheng and L. Liu (2017) Epigenetic and genetic dissections of UV-induced global gene dysregulation in skin cells through multi-omics analyses. Sci. Rep. 7, 42646.
Tang, Z., X. Tong, J. Huang, L. Liu, D. Wang and S. Yang (2021) Research progress of keratinocyte-programmed cell death in UV-induced skin photodamage. Photodermatol. Photoimmunol. Photomed. 37, 442-448.
Lee, K., J. Lee, E. Seo, W. Lee, Y. Nam, J. Yang, S.-H. Kee, Y. Seo, J. Park and C. Kim (2005) Analysis of genes responding to ultraviolet B irradiation of HaCaT keratinocytes using a cDNA microarray. Br. J. Dermatol. 152, 52-59.
Welss, T., D. A. Basketter and K. R. Schröder (2004) In vitro skin irritation: Facts and future. State of the art review of mechanisms and models. Toxicol. In Vitro 18, 231-243.
Afaq, F., V. M. Adhami and H. Mukhtar (2005) Photochemoprevention of ultraviolet B signaling and photocarcinogenesis. Mutat. Res. 571, 153-173.
Aubin, F. (2003) Mechanisms involved in ultraviolet light-induced immunosuppression. Eur. J. Dermatol. 13, 515-523.
Pacholczyk, M., J. Czernicki and T. Ferenc (2016) The effect of solar ultraviolet radiation (UVR) on induction of skin cancers. Med. Pr. 67, 255-266.
Lee, J. W., K. Ratnakumar, K. F. Hung, D. Rokunohe and M. Kawasumi (2020) Deciphering UV-induced DNA damage responses to prevent and treat skin cancer. Photochem. Photobiol. 96, 478-499.
Wacker, M. and M. F. Holick (2013) Sunlight and vitamin D: A global perspective for health. Dermatoendocrinol. 5, 51-108.
Kciuk, M., B. Marciniak, M. Mojzych and R. Kontek (2020) Focus on UV-induced DNA damage and repair-Disease relevance and protective strategies. Int. J. Mol. Sci. 21, 7264.
Sinha, R. P. and D. P. Häder (2002) UV-induced DNA damage and repair: A review. Photochem. Photobiol. Sci. 1, 225-236.
Rastogi, R. P., A. Richa, M. B. Kumar and R. P. Sinha (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J. Nucleic Acids 2010, 592980.
Mouret, S., C. Philippe, J. Gracia-Chantegrel, A. Banyasz, S. Karpati, D. Markovitsi and T. Douki (2010) UVA-induced cyclobutane pyrimidine dimers in DNA: A direct photochemical mechanism? Org. Biomol. Chem. 8, 1706-1711.
Zhao, B., P. Shah, L. Qiang, T. C. He, A. Budanov and Y. Y. He (2017) Distinct role of Sesn2 in response to UVB-induced DNA damage and UVA-induced oxidative stress in melanocytes. Photochem. Photobiol. 93, 375-381.
Kaufmann, W. K. and J. E. Cleaver (1981) Mechanisms of inhibition of DNA replication by ultraviolet light in normal human and xeroderma pigmentosum fibroblasts. J. Mol. Biol. 149, 171-187.
Strozyk, E. and D. Kulms (2013) The role of AKT/mTOR pathway in stress response to UV-irradiation: Implication in skin carcinogenesis by regulation of apoptosis, autophagy and senescence. Int. J. Mol. Sci. 14, 15260-15285.
Poon, F., S. Kang and A. L. Chien (2015) Mechanisms and treatments of photoaging. Photodermatol. Photoimmunol. Photomed. 31, 65-74.
Debacq-Chainiaux, F., C. Borlon, T. Pascal, V. Royer, F. Eliaers, N. Ninane, G. Carrard, B. Friguet, F. de Longueville, S. Boffe, J. Remacle and O. Toussaint (2005) Repeated exposure of human skin fibroblasts to UVB at subcytotoxic level triggers premature senescence through the TGF-beta1 signaling pathway. J. Cell Sci. 118, 743-758.
Cavinato, M., R. Koziel, N. Romani, R. Weinmüllner, B. Jenewein, M. Hermann, S. Dubrac, G. Ratzinger, J. Grillari, M. Schmuth and P. Jansen-Dürr (2017) UVB-induced senescence of human dermal fibroblasts involves impairment of proteasome and enhanced autophagic activity. J. Gerontol. A Biol. Sci. Med. Sci. 72, 632-639.
Schuch, A. P., N. C. Moreno, N. J. Schuch, C. F. M. Menck and C. C. M. Garcia (2017) Sunlight damage to cellular DNA: Focus on oxidatively generated lesions. Free Radic. Biol. Med. 107, 110-124.
Wang, P. W., Y. C. Hung, T. Y. Lin, J. Y. Fang, P. M. Yang, M. H. Chen and T. L. Pan (2019) Comparison of the biological impact of UVA and UVB upon the skin with functional proteomics and immunohistochemistry. Antioxidants 8, 569.
Yo, K. and T. M. Rünger (2017) UVA and UVB induce different sets of long noncoding RNAs. J. Invest. Dermatol. 137, 769-772.
Izykowska, I., M. Cegielski, E. Gebarowska, M. Podhorska-Okolow, A. Piotrowska, M. Zabel and P. Dziegiel (2009) Effect of melatonin on human keratinocytes and fibroblasts subjected to UVA and UVB radiation in vitro. In Vivo 23, 739-745.
Han, A. and H. I. Maibach (2004) Management of acute sunburn. Am. J. Clin. Dermatol. 5, 39-47.
Bernard, J. J., R. L. Gallo and J. Krutmann (2019) Photoimmunology: How ultraviolet radiation affects the immune system. Nat. Rev. Immunol. 19, 688-701.
Hruza, L. L. and A. P. Pentland (1993) Mechanisms of UV-induced inflammation. J. Invest. Dermatol. 100, S35-S41.
Damian, D., Y. Matthews, T. Phan and G. Halliday (2011) An action spectrum for ultraviolet radiation-induced immunosuppression in humans. Br. J. Dermatol. 164, 657-659.
Syed, D. N., F. Afaq and H. Mukhtar (2012) Differential activation of signaling pathways by UVA and UVB radiation in normal human epidermal keratinocytes. Photochem. Photobiol. 88, 1184-1190.
Kraemer, A., I. P. Chen, S. Henning, A. Faust, B. Volkmer, M. J. Atkinson, S. Moertl and R. Greinert (2013) UVA and UVB irradiation differentially regulate microRNA expression in human primary keratinocytes. PLoS One 8, e83392.
Shen, Y., A. L. Kim, R. Du and L. Liu (2016) Transcriptome analysis identifies the dysregulation of ultraviolet target genes in human skin cancers. PLoS One 11, e0163054.
Marais, T. L. D., T. Kluz, D. Xu, X. Zhang, L. Gesumaria, M. S. Matsui, M. Costa and H. Sun (2017) Transcription factors and stress response gene alterations in human keratinocytes following solar simulated ultra violet radiation. Sci. Rep. 7, 13622.
Leszczynski, D. (2013) Radiation Proteomics: The Effects of Ionizing and Non-ionizing Radiation on Cells and Tissues. Springer Science & Business Media, Dordrecht.
McArdle, A. J. and S. Menikou (2021) What is proteomics? Archives of disease in childhood. Educat. Pract. 106, 178-181.
Zhou, Z., Y. Li, H. Hao, Y. Wang, Z. Zhou, Z. Wang and X. Chu (2019) Screening hub genes as prognostic biomarkers of hepatocellular carcinoma by bioinformatics analysis. Cell Transplant. 28, 76s-86s.
Livak, K. J. and T. D. Schmittgen (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402-408.
Moravcová, M., A. Libra, J. Dvořáková, A. Víšková, T. Muthný, V. Velebný and L. Kubala (2013) Modulation of keratin 1, 10 and involucrin expression as part of the complex response of the human keratinocyte cell line HaCaT to ultraviolet radiation. Toxicol. Sci. 6, 203.
Dissanayake, N. and R. Mason (1998) Modulation of skin cell functions by transforming growth factor-beta1 and ACTH after ultraviolet irradiation. J. Endocrinol. 159, 153-163.
Ansary, T. M., M. Hossain, K. Kamiya, M. Komine and M. Ohtsuki (2021) Inflammatory molecules associated with ultraviolet radiation-mediated skin aging. Int. J. Mol. Sci. 22, 3974.
Chen, S., X. Wang, M. F. Nisar, M. Lin and J. L. Zhong (2019) Heme oxygenases: Cellular multifunctional and protective molecules against UV-induced oxidative stress. Oxid. Med. Cell. Longev. 2019, 5416728.
Ohnishi, T., M. Hisadome, K. Joji, N. Chiba, M. S. Amir, T. Kanekura and T. Matsuguchi (2021) Ultraviolet B irradiation decreases CXCL10 expression in keratinocytes through endoplasmic reticulum stress. J. Cell. Biochem. 122, 1141-1156.
Kato, M., K. Sato, M. Habuta, H. Fujita, T. Bando, Y. Morizane, F. Shiraga, S. Miyaishi and H. Ohuchi (2019) Localization of the ultraviolet-sensor Opn5m and its effect on myopia-related gene expression in the late-embryonic chick eye. Biochem. Biophys. Rep. 19, 100665.
Muller, H. K. and G. M. Woods (2013) Ultraviolet radiation effects on the proteome of skin cells. Adv. Exp. Med. Biol. 990, 111-119.
Luo, X., D. Cao, H. Li, D. Zhao, H. Xue, J. Niu, L. Chen, F. Zhang and S. Cao (2018) Complementary iTRAQ-based proteomic and RNA sequencing-based transcriptomic analyses reveal a complex network regulating pomegranate (Punica granatum L.) fruit peel colour. Sci. Rep. 8, 12362.
Chen, J., S. S. Liu, A. Kohler, B. Yan, H. M. Luo, X. M. Chen and S. X. Guo (2017) iTRAQ and RNA-seq analyses provide new insights into regulation mechanism of symbiotic germination of dendrobium officinale seeds (orchidaceae). J. Proteome Res. 16, 2174-2187.
Xu, C., S. Luo, L. Wei, H. Wu, W. Gu, W. Zhou, B. Sun, B. Hu, H. Zhou and Y. Liu (2021) Integrated transcriptome and proteome analyses identify novel regulatory network of nucleus pulposus cells in intervertebral disc degeneration. BMC Med. Genom. 14, 1-12.
Nissom, P. M., A. Sanny, Y. J. Kok, Y. T. Hiang, S. H. Chuah, T. K. Shing, Y. Y. Lee, T. K. Wong, W.-s. Hu and M. Y. G. Sim (2006) Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol. Biotechnol. 34, 125-140.
Pandey, A. and M. Mann (2000) Proteomics to study genes and genomes. Nature 405, 837-846.
Shetty, S. and S. Gokul (2012) Keratinization and its disorders. Oman Med. J. 27, 348.
Sano, T., T. Kume, T. Fujimura, H. Kawada, K. Higuchi, M. Iwamura, M. Hotta, T. Kitahara and Y. Takema (2009) Long-term alteration in the expression of keratins 6 and 16 in the epidermis of mice after chronic UVB exposure. Arch. Dermatol. Res. 301, 227-237.
Knöbel, M., E. A. O'Toole and F. J. Smith (2015) Keratins and skin disease. Cell Tissue Res. 360, 583-589.
Popovic, D., D. Vucic and I. Dikic (2014) Ubiquitination in disease pathogenesis and treatment. Nat. Med. 20, 1242-1253.
Bendjennat, M., J. Boulaire, T. Jascur, H. Brickner, V. Barbier, A. Sarasin, A. Fotedar and R. Fotedar (2003) UV irradiation triggers ubiquitin-dependent degradation of p21WAF1 to promote DNA repair. Cell 114, 599-610.
Sugasawa, K., Y. Okuda, M. Saijo, R. Nishi, N. Matsuda, G. Chu, T. Mori, S. Iwai, K. Tanaka and K. Tanaka (2005) UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121, 387-400.
Tsuchiya, Y., T. Asano, K. Nakayama, T. Kato Jr., M. Karin and H. Kamata (2010) Nuclear IKKβ is an adaptor protein for IκBα ubiquitination and degradation in UV-induced NF-κB activation. Mol. Cell 39, 570-582.
Maki, C. G. and P. M. Howley (1997) Ubiquitination of p53 and p21 is differentially affected by ionizing and UV radiation. Mol. Cell. Biol. 17, 355-363.
Kaiser, P., H. A. Mansourl, T. Greeten, B. Auer, M. Schweiger and R. Schneider (1994) The human ubiquitin-conjugating enzyme UbcH1 is involved in the repair of UV-damaged, alkylated and cross-linked DNA. FEBS Lett. 350, 1-4.
Hong, N. H., Y. J. Tak, H. Rhim and S. Kang (2019) Hip2 ubiquitin-conjugating enzyme has a role in UV-induced G1/S arrest and re-entry. Genes Genomics 41, 159-166.
Shaler, T., H. Lin, J. Bakke, S. Chen, A. Grover and P. Chang (2020) Particle radiation-induced dysregulation of protein homeostasis in primary human and mouse neuronal cells. Life Sci. Space Res. 25, 9-17.
Gebhardt, A., M. Habjan, C. Benda, A. Meiler, D. A. Haas, M. Y. Hein, A. Mann, M. Mann, B. Habermann and A. Pichlmair (2015) mRNA export through an additional cap-binding complex consisting of NCBP1 and NCBP3. Nat. Commun. 6, 1-13.
Barbosa, I., N. Haque, F. Fiorini, C. Barrandon, C. Tomasetto, M. Blanchette and H. Le Hir (2012) Human CWC22 escorts the helicase eIF4AIII to spliceosomes and promotes exon junction complex assembly. Nat. Struct. Mol. Biol. 19, 983-990.

Auteurs

Qinqin Zhao (Q)

Characteristic Plants Research and Development Center, Botanee Research Institute, Shanghai Jiyan Bio-Pharmaceutical Development Co., Ltd., Shanghai, China.

Yueyue Chen (Y)

Characteristic Plants Research and Development Center, Botanee Research Institute, Shanghai Jiyan Bio-Pharmaceutical Development Co., Ltd., Shanghai, China.
Yunnan Characteristic Plant Extraction Laboratory, Yunnan Yunke Characteristic Plant Extraction Laboratory Co., Ltd., Kunming, China.

Liping Qu (L)

Characteristic Plants Research and Development Center, Botanee Research Institute, Shanghai Jiyan Bio-Pharmaceutical Development Co., Ltd., Shanghai, China.
Yunnan Characteristic Plant Extraction Laboratory, Yunnan Yunke Characteristic Plant Extraction Laboratory Co., Ltd., Kunming, China.
Yunnan Botanee Bio-technology Group Co., Ltd., Kunming, China.

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