Skip to main content
SpringerLink
Log in

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

  • Published:
AGE Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Antebi A (2007) Genetics of aging in Caenorhabditis elegans. PLoS Genet 3(9):1565–1571

    Article  CAS  PubMed  Google Scholar 

  • Avery L, You YJ (2012) C. elegans Feeding. WormBook 21:1–23

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Burke KE, Wei H (2009) Synergistic damage by UVA radiation and pollutants. Toxicol Ind Health 25(4–5):219–224

    Article  CAS  PubMed  Google Scholar 

  • Brenner S (1974) The genetics of C. elegans. Genetics 77:71–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins JJ, Huang C, Hughes S, Kornfeld K (2008) The measurement and analysis of age-related changes in Caenorhabditis elegans. WormBook 24:1–21

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fawcett EM, Hoyt JM, Johnson JK, Miller DL (2015) Hypoxia disrupts proteostasis in Caenorhabditis elegans. Aging Cell 14(1):92–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Herndon LA, Schmeissner PA, Dudaronek JM (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419(6909):808–814

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hofer AM (2005) Another dimension to calcium signaling: a look at extracellular calcium. J Cell Sci 118(Pt 5):855–862

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Juckett DA (2010) What determines age-related disease: do we know all the right questions? Age (Dordr) 32(2):155–160

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lakowski B, Hekimi S (1996) Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272(5264):1010–1013

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacFarlane DF, Alonso CA (2009) Occurrence of nonmelanoma skin cancers on the hands after UV nail light exposure. Arch Dermatol 145(4):447–449

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKenzie RL, Liley JB, Bjorn LO (2009) UV radiation: balancing risks and benefits. Photochem Photobiol 85(1):88–98

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Murphy CT, Hu PJ (2013) Insulin/insulin-like growth factor signaling in C. elegans. WormBook 26:1–43

    Article  Google Scholar 

  • Pandel R, Poljsak B, Godic A, Dahmane R (2013) Skin photoaging and the role of antioxidants in its prevention. ISRN Dermatol 2013:930164

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Qian H, Xu X, Niklason LE (2015) PCH-2 regulates Caenorhabditis elegans lifespan. Aging (Albany NY) 7(1):1–13

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Sivamaruthi BS, Prasanth MI, Balamurugan K (2015b) Alterations in Caenorhabditis elegans and Cronobacter sakazakii lipopolysaccharide during interaction. Arch Microbiol 197(2):327–337

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan J, Durak O, Sternberg PW (2008) Evolution of a polymodal sensory response network. BMC Biol 6:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Swigut T, Wysocka J (2007) H3K27 demethylases, at long last. Cell 131(1):29–32

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tissenbaum HA (2012) Genetics, lifespan, healthspan, and the aging process in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 67(5):503–510

    Article  PubMed  Google Scholar 

  • Tobin DM, Bargmann CI (2004) Invertebrate nociception: behaviors, neurons and molecules. J Neurobiol 61(1):161–174

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yen K, Mobbs CV (2010) Evidence for only two independent pathways for decreasing senescence in Caenorhabditis elegans. Age (Dordr) 32(1):39–49

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Caenorhabditis Genetics Center, which is funded by the National Institute of Health, National Center for Research Resources for providing C. elegans N2 WT, mutant strains and E. coli OP50. KB thankfully acknowledges the ITC India Ltd., Department of Biotechnology (DBT), University Grants Commission (UGC), Indian Council of Medical Research (ICMR) and Council of Scientific and Industrial Research (CSIR), Department of Science and Technology (DST), Government of India, New Delhi, India, for the financial assistances. PMI wishes to thank ITC and CSIR, India, for the financial assistance (AU-ITC JRF & CSIR-SRF). The authors also gratefully acknowledge the use of the Bioinformatics Infrastructure Facility, Alagappa University funded by the Department of Biotechnology, Ministry of Science and Technology, Government of India (No. BT/BI/25/015/2012), the Instrumentation Facility provided by DST, Government of India through PURSE [Grant No.SR/S9Z-23/2010/42(G)] & FIST (Grant No.SR-FST/LSI-087/2008) and UGC, New Delhi through SAP-DRS1 [Grant No.F.3-28/2011(SAP-II)].

Author information

Authors and Affiliations

  1. Department of Biotechnology, Science Campus, Alagappa University, Karaikudi, Tamil Nadu, -630 004, India

    Mani Iyer Prasanth, Gunasekaran Santhi Santoshram & Krishnaswamy Balamurugan

  2. ITC - Life Sciences and Technology Centre, ITC Limited, No. 3, 1st Main, Peenya Industrial Area, Bangalore, Karnataka, 560058, India

    James Prabhanand Bhaskar

Authors
  1. Mani Iyer Prasanth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gunasekaran Santhi Santoshram
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James Prabhanand Bhaskar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Krishnaswamy Balamurugan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Krishnaswamy Balamurugan.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prasanth, M.I., Santoshram, G.S., Bhaskar, J.P. et al. Ultraviolet-A triggers photoaging in model nematode Caenorhabditis elegans in a DAF-16 dependent pathway. AGE 38, 27 (2016). https://doi.org/10.1007/s11357-016-9889-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11357-016-9889-y

Keywords

Search

Navigation

-