Skip to main content

Advertisement

Log in

LncRNA PVT1 delays skin photoaging by sequestering miR-551b-3p to release AQP3 expression via ceRNA mechanism

  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Understanding human skin photoaging requires in-depth knowledge of the molecular and functional mechanisms. Human dermal fibroblasts (HDFs) gradually lose their ability to produce collagen and renew intercellular matrix with aging. Therefore, our study aims to reveal the mechanistic actions of a novel ceRNA network in the skin photoaging by regulating HDF activities. Photoaging-related genes were obtained in silico, followed by GO and KEGG enrichment analyses. Differentially expressed lncRNAs and miRNAs were screened from the GEO database to construct the ceRNA co-expression network. In skin photoaging samples, PVT1 and AQP3 were poorly expressed, while miR-551b-3p was highly expressed. The relationships among the lncRNA, miRNA and mRNA were explored through the ENCORI database and dual luciferase reporter assay. Mechanistically, PVT1 could sequester miR-551b-3p to upregulate the expression of AQP3, which further inactivated the ERK/p38 MAPK signaling pathway. HDFs were selected to construct an in vitro cell skin photoaging model, where the senescence, cell cycle distribution and viability of young and senescent HDFs were detected by SA-β-gal staining, flow cytometry and CCK-8 assay. In vitro cell experiments confirmed that overexpression of PVT1 or AQP3 enhanced viability of young and senescent HDFs and inhibited HDF senescence, while miR-551b-3p upregulation counteracted the effect of PVT1. In conclusion, PVT1-driven suppression of miR-551b-3p induces AQP3 expression to inactivate the ERK/p38 MAPK signaling pathway, thereby inhibiting HDF senescence and ultimately delaying the skin photoaging.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The data that supports the findings of this study are available on request from the corresponding author upon reasonable request.

References

  1. Hahnel E et al (2017) The epidemiology of skin conditions in the aged: a systematic review. J Tissue Viability 26(1):20–28

    Article  PubMed  Google Scholar 

  2. Trautinger F (2001) Mechanisms of photodamage of the skin and its functional consequences for skin ageing. Clin Exp Dermatol 26(7):573–577

    Article  CAS  PubMed  Google Scholar 

  3. Liu W et al (2022) Urolithin A protects human dermal fibroblasts from UVA-induced photoaging through NRF2 activation and mitophagy. J Photochem Photobiol B 232:112462

    Article  CAS  PubMed  Google Scholar 

  4. Gentile P, Garcovich S (2021) Adipose-derived mesenchymal stem cells (AD-MSCs) against Ultraviolet (UV) Radiation Effects and the skin photoaging. Biomedicines 9(5)

  5. Hu S et al (2019) Needle-free injection of Exosomes derived from human dermal fibroblast spheroids ameliorates skin photoaging. ACS Nano 13(10):11273–11282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wlaschek M et al (2021) Connective tissue and fibroblast senescence in skin aging. J Invest Dermatol 141(4S):985–992

    Article  CAS  PubMed  Google Scholar 

  7. Qin H et al (2011) Aquaporin-3 in keratinocytes and skin: its role and interaction with phospholipase D2. Arch Biochem Biophys 508(2):138–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bollag WB et al (2020) Aquaporin-3 in the epidermis: more than skin deep. Am J Physiol Cell Physiol 318(6):C1144–C1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of aquaporin-3-deficient mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 277(48):46616–46621

    Article  CAS  PubMed  Google Scholar 

  10. Hara-Chikuma M, Verkman AS (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med (Berl) 86(2):221–231

    Article  CAS  PubMed  Google Scholar 

  11. Zhang Z et al (2022) Overexpression of Aquaporin-3 alleviates Hyperosmolarity-Induced Nucleus Pulposus Cell apoptosis via regulating the ERK1/2 pathway. Pain Res Manag 2022(1639560

  12. Choi HJ et al (2020) Protection against UVB-Induced photoaging by Nypa fruticans via inhibition of MAPK/AP-1/MMP-1 signaling. Oxid Med Cell Longev 2020(2905362

  13. Xie H et al (2020) A negative Feedback Loop in Ultraviolet A-Induced Senescence in Human dermal fibroblasts formed by SPCA1 and MAPK. Front Cell Dev Biol 8:597993

    Article  PubMed  Google Scholar 

  14. Feitosa R et al (2022) MicroRNA target prediction tools for animals: where we are at and where we are going to - A systematic review. Comput Biol Chem 100:107729

    Article  CAS  PubMed  Google Scholar 

  15. Geng R et al (2021) Boosting the Photoaged skin: the potential role of Dietary Components. Nutrients 13(5)

  16. Chan JJ, Tay Y (2018) Noncoding RNA:RNA Regulatory Networks in Cancer. Int J Mol Sci 19(5)

  17. Yang Z et al (2022) Exosomal microRNA-551b-3p from bone marrow-derived mesenchymal stromal cells inhibits breast cancer progression via regulating TRIM31/Akt signaling. Hum Cell 35(6):1797–1812

    Article  CAS  PubMed  Google Scholar 

  18. Takahara S et al (2020) Altered microRNA profile during fracture healing in rats with diabetes. J Orthop Surg Res 15(1):135

    Article  PubMed  PubMed Central  Google Scholar 

  19. Panda AC et al (2017) Identification of senescence-associated circular RNAs (SAC-RNAs) reveals senescence suppressor CircPVT1. Nucleic Acids Res 45(7):4021–4035

    Article  CAS  PubMed  Google Scholar 

  20. Lee J et al (2021) N(6) -methyladenosine modification of lncRNA Pvt1 governs epidermal stemness. EMBO J 40(8):e106276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xiang Y et al (2021) Age-related elevation of HGF is driven by the reduction of fibroblast size in a YAP/TAZ/CCN2 axis-dependent manner. J Dermatol Sci 102(1):36–46

    Article  CAS  PubMed  Google Scholar 

  22. Shin DJ et al (2014) 20-O-beta-D-glucopyranosyl-20(S)-protopanaxadiol suppresses UV-Induced MMP-1 expression through AMPK-mediated mTOR inhibition as a downstream of the PKA-LKB1 pathway. J Cell Biochem 115(10):1702–1711

    Article  CAS  PubMed  Google Scholar 

  23. Cho EG et al (2021) Panax ginseng-derived extracellular vesicles facilitate Anti-Senescence Effects in Human skin cells: an eco-friendly and sustainable way to Use Ginseng Substances. Cells 10(3)

  24. Liu JZ et al (2019) Rafoxanide promotes apoptosis and autophagy of gastric cancer cells by suppressing PI3K /Akt/mTOR pathway. Exp Cell Res 385(2):111691

    Article  CAS  PubMed  Google Scholar 

  25. Lin J et al (2021) Long non-coding RNA H19 promotes myoblast fibrogenesis via regulating the miR-20a-5p-Tgfbr2 axis. Clin Exp Pharmacol Physiol 48(6):921–931

    Article  CAS  PubMed  Google Scholar 

  26. Zhu X et al (2021) IL-6/STAT3-mediated autophagy participates in the development of age-related glomerulosclerosis. J Biochem Mol Toxicol 35(4):e22698

    Article  CAS  PubMed  Google Scholar 

  27. Tobin DJ (2017) Introduction to skin aging. J Tissue Viability 26(1):37–46

    Article  PubMed  Google Scholar 

  28. Ruiz-Llorente L et al (2018) Thyroid hormone receptors regulate the expression of microRNAs with key roles in skin homeostasis. Thyroid 28(7):921–932

    Article  CAS  PubMed  Google Scholar 

  29. Soheilifar MH et al (2022) Non-coding RNAs in photoaging-related mechanisms: a new paradigm in skin health. Biogerontology 23(3):289–306

    Article  CAS  PubMed  Google Scholar 

  30. Xie H et al (2022) Autophagy induction regulates aquaporin 3-mediated skin fibroblast ageing. Br J Dermatol 186(2):318–333

    Article  CAS  PubMed  Google Scholar 

  31. Kim YH et al (2020) Effect of red ginseng NaturalGEL on skin aging. J Ginseng Res 44(1):115–122

    Article  PubMed  Google Scholar 

  32. Ikarashi N et al (2017) Relationship between aging-related skin dryness and aquaporins. Int J Mol Sci 18(7)

  33. Myung DB et al (2019) Hydrangenol isolated from the Leaves of Hydrangea serrata attenuates wrinkle formation and repairs skin moisture in UVB-Irradiated hairless mice. Nutrients 11(10)

  34. Li Z et al (2022) Ginsenosides repair UVB-induced skin barrier damage in BALB/c hairless mice and HaCaT keratinocytes. J Ginseng Res 46(1):115–125

    Article  PubMed  Google Scholar 

  35. Jin YJ et al (2021) Acer tataricum subsp. ginnala inhibits skin photoaging via regulating MAPK/AP-1, NF-kappaB, and TGFbeta/Smad signaling in UVB-Irradiated human dermal fibroblasts. Molecules 26(3)

  36. Mu J et al (2021) Luteolin prevents UVB-Induced skin photoaging damage by modulating SIRT3/ROS/MAPK signaling: an in vitro and in vivo studies. Front Pharmacol 12:728261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Chen T et al (2016) Protective effect of gelatin peptides from pacific cod skin against photoaging by inhibiting the expression of MMPs via MAPK signaling pathway. J Photochem Photobiol B 165:34–41

    Article  CAS  PubMed  Google Scholar 

  38. Chang W et al (2019) MicroRNA-551b-3p inhibits tumour growth of human cholangiocarcinoma by targeting cyclin D1. J Cell Mol Med 23(8):4945–4954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yuan H et al (2018) Molecular mechanisms of lncRNA SMARCC2/miR-551b-3p/TMPRSS4 axis in gastric cancer. Cancer Lett 418:84–96

    Article  CAS  PubMed  Google Scholar 

  40. Han W et al (2022) Circular RNA PVT1 inhibits tendon stem/progenitor cell senescence by sponging microRNA-199a-5p. Toxicol In Vitro 79:105297

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This study was supported by Project of Hunan Provincial Finance Department (No. 2021CZT04).

Author information

Authors and Affiliations

Authors

Contributions

Hua Tang, Qi Xiong and Ming Yin wrote the paper and conceived and designed the experiments; Hao Feng, Fang Yao and Xiao Xiao analyzed the data; Feng Hu and Yangying Liao collected and provided the sample for this study. All authors have read and approved the final submitted manuscript.

Corresponding author

Correspondence to Yangying Liao.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Supplementary Material 2

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, H., Xiong, Q., Yin, M. et al. LncRNA PVT1 delays skin photoaging by sequestering miR-551b-3p to release AQP3 expression via ceRNA mechanism. Apoptosis 28, 912–924 (2023). https://doi.org/10.1007/s10495-023-01834-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-023-01834-4

Keywords

Navigation