Ultraviolet-A triggers photoaging in model nematode Caenorhabditis elegans in a DAF-16 dependent pathway

Springer Science and Business Media LLC - Tập 38 - Trang 1-13 - 2016
Mani Iyer Prasanth1, Gunasekaran Santhi Santoshram1, James Prabhanand Bhaskar2, Krishnaswamy Balamurugan1
1Department of Biotechnology, Science Campus, Alagappa University, Karaikudi, India
2ITC - Life Sciences and Technology Centre, ITC Limited, Bangalore, India

Tóm tắt

Ultraviolet radiations (UV) are the primary causative agent for skin aging (photoaging) and cancer, especially UV-A. The mode of action and the molecular mechanism behind the damages caused by UV-A is not well studied, in vivo. The current study was employed to investigate the impact of UV-A exposure using the model organism, Caenorhabditis elegans. Analysis of lifespan, healthspan, and other cognitive behaviors were done which was supported by the molecular mechanism. UV-A exposure on collagen damages the synthesis and functioning which has been monitored kinetically using engineered strain, col-19:: GFP. The study results suggested that UV-A accelerated the aging process in an insulin-like signaling pathway dependent manner. Mutant (daf-2)-based analysis concrete the observations of the current study. The UV-A exposure affected the usual behavior of the worms like pharyngeal movements and brood size. Quantitative PCR profile of the candidate genes during UV-A exposure suggested that continuous exposure has damaged the neural network of the worms, but the mitochondrial signaling and dietary restriction pathway remain unaffected. Western blot analysis of HSF-1 evidenced the alteration in protein homeostasis in UV-A exposed worms. Outcome of the current study supports our view that C. elegans can be used as a model to study photoaging, and the mode of action of UV-A-mediated damages can be elucidated which will pave the way for drug developments against photoaging.

Tài liệu tham khảo

Antebi A (2007) Genetics of aging in Caenorhabditis elegans. PLoS Genet 3(9):1565–1571 Avery L, You YJ (2012) C. elegans Feeding. WormBook 21:1–23 Barcelos RC, Vey LT, Segat HJ, et al. (2014) Cross-generational trans fat intake exacerbates UV radiation-induced damage in rat skin. Food Chem Toxicol 69:38–45 Burke KE, Wei H (2009) Synergistic damage by UVA radiation and pollutants. Toxicol Ind Health 25(4–5):219–224 Brenner S (1974) The genetics of C. elegans. Genetics 77:71–94 Chauhan P, Shakya M (2009) Modeling signaling pathways leading to wrinkle formation: identification of the skin aging target. Indian J Dermatol Venereol Leprol 75(5):463–468 Chiarelli-Neto O, Ferreira AS, Martins WK (2014) Melanin photosensitization and the effect of visible light on epithelial cells. PLoS One 18;9(11):e113266. doi:10.1371/journal.pone.0113266. Chiang WC, Ching TT, Lee HC, Mousigian C, Hsu AL (2012) HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148:322–334 Chondrogianni N, Georgila K, Kourtis N, Tavernarakis N, Gonos ES (2015) 20S proteasome activation promotes life span extension and resistance to proteotoxicity in Caenorhabditis elegans. FASEB J 29(2):611–622 Cizmeli C, Lobel M, Franasiak J, Pastore LM (2013) Levels and associations among self-esteem, fertility distress, coping, and reaction to potentially being a genetic carrier in women with diminished ovarian reserve. Fertil Steril 99(7):2037–2044 Collins JJ, Huang C, Hughes S, Kornfeld K (2008) The measurement and analysis of age-related changes in Caenorhabditis elegans. WormBook 24:1–21 Duan X, Wang QC, Chen KL, Zhu CC, Liu J, Sun SC (2015) Acrylamide toxic effects on mouse oocyte quality and fertility in vivo. Sci Rep 25;5:11562. Durai S, Pandian SK, Balamurugan K (2011) Establishment of a Caenorhabditis elegans infection model for Vibrio alginolyticus. J Basic Microbiol 51(3):243–252 Durai S, Singh N, Kundu S, Balamurugan K (2014) Proteomic investigation of Vibrio alginolyticus challenged Caenorhabditis elegans revealed regulation of cellular homeostasis proteins and their role in supporting innate immune system. Proteomics 14(15):1820–1832 Evans EA, Chen WC, Tan MW (2008) The DAF-2 insulin-like signaling pathway independently regulates aging and immunity in C. elegans. Aging Cell 7(6):879–893 Fawcett EM, Hoyt JM, Johnson JK, Miller DL (2015) Hypoxia disrupts proteostasis in Caenorhabditis elegans. Aging Cell 14(1):92–101 Guha S, Cao M, Kane RM, Savino AM, Zou S, Dong Y (2013) The longevity effect of cranberry extract in Caenorhabditis elegans is modulated by daf-16 and osr-1. Age (Dordr) 35(5):1559–1574 Govorunova EG, Moussaif M, Kullyev A, Nguyen KC, McDonald TV, Hall DH, Sze JY (2010) A homolog of FHM2 is involved in modulation of excitatory neurotransmission by serotonin in C. elegans. PLoS One 5(4):e10368. doi:10.1371/journal.pone.0010368. Hada K, Asahina M, Hasegawa H, Kanaho Y, Slack FJ, Niwa R (2010) The nuclear receptor gene nhr-25 plays multiple roles in the Caenorhabditis elegans heterochronic gene network to control the larva-to-adult transition. Dev Biol 344(2):1100–1109 Hekimi S, Lakowski B, Barnes TM, Ewbank JJ (1998) Molecular genetics of life span in C. elegans: how much does it teach us? Trends Genet 14(1):14–20 Henderson ST, Johnson TE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11:1975–1980 Herndon LA, Schmeissner PA, Dudaronek JM (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419(6909):808–814 Hilliard MA, Bargmann CI, Bazzicalupo P (2002) C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Curr Biol 12(9):730–734 Hofer AM (2005) Another dimension to calcium signaling: a look at extracellular calcium. J Cell Sci 118(Pt 5):855–862 Honda Y, Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13:1385–1393 Hung CF, Chen WY, Aljuffali IA, Lin YK, Shih HC, Fang JY (2015) Skin aging modulates percutaneous drug absorption: the impact of ultraviolet irradiation and ovariectomy. Age (Dordr) 37(2):9757 JebaMercy G, Vigneshwari L, Balamurugan K (2013) A MAP kinase pathway in Caenorhabditis elegans is required for defense against infection by opportunistic Proteus species. Microbes Infect 15(8–9):550–568 Jin C, Li J, Green CD, et al. (2011) Histone demethylase UTX-1 regulates C. elegans life span by targeting the insulin/IGF-1 signaling pathway. Cell Metab 14(2):161–172 Juckett DA (2010) What determines age-related disease: do we know all the right questions? Age (Dordr) 32(2):155–160 Juckett DA, Rosenberg B (1991) An unexpected periodicity among the prevalences of human age-related, mortal diseases. Mech Ageing Dev 59(1–2):139–152 Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512 Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366:461–464 Kesika P, Pandian SK, Balamurugan K (2011) Analysis of Shigella flexneri mediated infections in model organism Caenorhabditis elegans. Scand J Infect Dis 43(4):286–295 Kong S, Chen H, Yu X, et al. (2014) The protective effect of 18β-glycyrrhetinic acid against UV irradiation induced photoaging in mice. Exp Gerontol 61C:147–155 Kuhn J, Schutkowski A, Hirche F, Baur AC, Mielenz N, Stangl GI (2015) Non-linear increase of vitamin D content in eggs from chicks treated with increasing exposure times of ultraviolet light. J Steroid Biochem Mol Biol 148:7–13 Lakowski B, Hekimi S (1996) Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272(5264):1010–1013 Li Y, Paik YK (2011) A potential role for fatty acid biosynthesis genes during molting and cuticle formation in Caenorhabditis elegans. BMB Rep 44(4):285–290 Matsuki M, Kunitomo H, Iino Y (2006) Goalpha regulates olfactory adaptation by antagonizing Gqalpha-DAG signaling in Caenorhabditis elegans. Proc Natl Acad Sci U S A 103(4):1112–1117 MacFarlane DF, Alonso CA (2009) Occurrence of nonmelanoma skin cancers on the hands after UV nail light exposure. Arch Dermatol 145(4):447–449 Maures TJ, Greer EL, Hauswirth AG, Brunet A (2011) The H3K27 demethylase UTX-1 regulates C. elegans lifespan in a germline-independent, insulin-dependent manner. Aging Cell 10(6):980–990 McKenzie RL, Liley JB, Bjorn LO (2009) UV radiation: balancing risks and benefits. Photochem Photobiol 85(1):88–98 McKenzie R, Scragg R, Liley B, Johnston P, Wishart J, Stewart A, Prematunga R (2012) Serum 25-hydroxy vitamin-D responses to multiple UV exposures from solaria: inferences for exposure to sunlight. Photochem Photobiol Sci 11(7):1174–1185 Murphy CT, Hu PJ (2013) Insulin/insulin-like growth factor signaling in C. elegans. WormBook 26:1–43 Pandel R, Poljsak B, Godic A, Dahmane R (2013) Skin photoaging and the role of antioxidants in its prevention. ISRN Dermatol 2013:930164 Patananan AN, Budenholzer LM, Eskin A, Torres ER, Clarke SG (2015) Ethanol-induced differential gene expression and acetyl-CoA metabolism in a longevity model of the nematode Caenorhabditis elegans. Exp Gerontol 61:20–30 Puglia C, Offerta A, Saija A, Trombetta D, Venera C (2014) Protective effect of red orange extract supplementation against UV-induced skin damages: photoaging and solar lentigines. J Cosmet Dermatol 13(2):151–157 Qian H, Xu X, Niklason LE (2015) PCH-2 regulates Caenorhabditis elegans lifespan. Aging (Albany NY) 7(1):1–13 Rabinowitch I, Chatzigeorgiou M, Zhao B, Treinin M, Schafer WR (2014) Rewiring neural circuits by the insertion of ectopic electrical synapses in transgenic C. elegans. Nat Commun 5:4442. Sambongi Y, Nagae T, Liu Y, Yoshimizu T, Takeda K, Wada Y, Futai M (1999) Sensing of cadmium and copper ions by externally exposed ADL, ASE, and ASH neurons elicits avoidance response in Caenorhabditis elegans. Neuroreport 10:753–757 Scerbak C, Vayndorf EM, Parker JA, Neri C, Driscoll M, Taylor BE (2014) Insulin signaling in the aging of healthy and proteotoxically stressed mechanosensory neurons. Front Genet 5:212 Shirai A, Onitsuka M, Maseda H, Omasa T (2015) Effect of polyphenols on reactive oxygen species production and cell growth of human dermal fibroblasts after irradiation with ultraviolet-A light. Biocontrol Sci. 20(1):27–33 Sivamaruthi BS, Ganguli A, Kumar M, Bhaviya S, Pandian SK, Balamurugan K (2011) Caenorhabditis elegans as a model for studying Cronobacter sakazakii ATCC BAA-894 pathogenesis. J Basic Microbiol 51(5):540–549 Sivamaruthi BS, Madhumita R, Balamurugan K, Rajan KE (2015a) Cronobacter sakazakii infection alters serotonin transporter and improved fear memory retention in the rat. Front Pharmacol 4(6):188 Sivamaruthi BS, Prasanth MI, Balamurugan K (2015b) Alterations in Caenorhabditis elegans and Cronobacter sakazakii lipopolysaccharide during interaction. Arch Microbiol 197(2):327–337 Sonani RR, Singh NK, Awasthi A, Prasad B, Kumar J, Madamwar D (2014) Phycoerythrin extends lifespan and healthspan of Caenorhabditis elegans. Age (Dordr) 36(5):9717 Song S, Guo Y, Zhang X, Zhang X, Zhang J, Ma E (2014) Changes to cuticle surface ultrastructure and some biological functions in the nematode Caenorhabditis elegans exposed to excessive copper. Arch Environ Contam Toxicol 66(3):390–399 Srinivasan J, Durak O, Sternberg PW (2008) Evolution of a polymodal sensory response network. BMC Biol 6:52 Swigut T, Wysocka J (2007) H3K27 demethylases, at long last. Cell 131(1):29–32 Thein MC, McCormack G, Winter AD, Johnstone IL, Shoemaker CB, Page AP (2003) Caenorhabditis elegans exoskeleton collagen COL-19: an adult-specific marker for collagen modification and assembly, and the analysis of organismal morphology. Dev Dyn 226(3):523–539 Tissenbaum HA (2012) Genetics, lifespan, healthspan, and the aging process in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 67(5):503–510 Tobin DM, Bargmann CI (2004) Invertebrate nociception: behaviors, neurons and molecules. J Neurobiol 61(1):161–174 Volovik Y, Moll L, Marques FC, Maman M, Bejerano-Sagie M, Cohen E (2014) Differential regulation of the heat shock factor 1 and DAF-16 by neuronal nhl-1 in the nematode C. elegans. Cell Rep 9(6):2192–2205 Wang F, Smith NR, Tran BA, Kang S, Voorhees JJ, Fisher GJ (2014) Dermal damage promoted by repeated low-level UV-A1 exposure despite tanning response in human skin. JAMA Dermatol 150(4):401–406 Wang Q, Wadsworth WG (2002) The C domain of netrin UNC-6 silences calcium/calmodulin-dependent protein kinase- and diacylglycerol-dependent axon branching in Caenorhabditis elegans. J Neurosci 22(6):2274–2282 Watanuki Y, Kageyama K, Takayasu S, Matsuzaki Y, Iwasaki Y, Daimon M (2014) Ultraviolet B radiation-stimulated urocortin 1 is involved in tyrosinase-related protein 1 production in human melanoma HMV-II cells. Peptides 61C:93–97 Yen K, Mobbs CV (2010) Evidence for only two independent pathways for decreasing senescence in Caenorhabditis elegans. Age (Dordr) 32(1):39–49 Zheng S, Liao S, Zou Y, Qu Z, Shen W, Shi Y (2014) Mulberry leaf polyphenols delay aging and regulate fat metabolism via the germline signaling pathway in Caenorhabditis elegans. Age (Dordr) 36(6):9719 Ziegler K, Kurz CL, Cypowyj S, Couillault C, Pophillat M, Pujol N, Ewbank JJ (2009) Antifungal innate immunity in C. elegans: PKCdelta links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 5(4):341–352