375
Views
6
CrossRef citations to date
0
Altmetric
Original Research

β-Nicotinamide Mononucleotide (NMN) Administrated by Intraperitoneal Injection Mediates Protection Against UVB-Induced Skin Damage in Mice

, , , , , & ORCID Icon show all
Pages 5165-5182 | Published online: 07 Oct 2021

References

  • Bragazzi NL, Sellami M, Salem I, et al. Fasting and its impact on skin anatomy, physiology, and physiopathology: a comprehensive review of the literature. Nutrients. 2019;11(2):249. doi:10.3390/nu11020249
  • Krutmann J, Bouloc A, Sore G, Bernard BA, Passeron T. The skin aging exposome. J Dermatol Scim. 2017;85(3):152–161. doi:10.1016/j.jdermsci.2016.09.015
  • Oh M, Lee J, Kim YJ, Rhee WJ, Park JH. Exosomes derived from human induced pluripotent stem cells ameliorate the aging of skin fibroblasts. Int J Mol Sci. 2018;19(6):1715. doi:10.3390/ijms19061715
  • Battie C, Jitsukawa S, Bernerd F, Del Bino S, Marionnet C, Verschoore M. New insights in photoaging, UVA induced damage and skin types. Exp Dermatol. 2014;23(Suppl 1):7–12. doi:10.1111/exd.12388
  • Cho S, Kim HH, Lee MJ, et al. Phosphatidylserine prevents UV-induced decrease of type I procollagen and increase of MMP-1 in dermal fibroblasts and human skin in vivo. J Lipid Res. 2008;49(6):1235–1245. doi:10.1194/jlr.M700581-JLR200
  • Baumann L. Skin ageing and its treatment. J Pathol. 2007;211(2):241–251. doi:10.1002/path.2098
  • Akase T, Nagase T, Huang L, et al. Aging-like skin changes induced by ultraviolet irradiation in an animal model of metabolic syndrome. Biol Res Nurs. 2012;14(2):180–187. doi:10.1177/1099800411401013
  • Poddar SK, Sifat AE, Haque S, Nahid NA, Chowdhury S, Mehedi I. Nicotinamide mononucleotide: exploration of diverse therapeutic applications of a potential molecule. Biomolecules. 2019;9(1):34. doi:10.3390/biom9010034
  • Hosseini L, Vafaee MS, Badalzadeh R. Melatonin and nicotinamide mononucleotide attenuate myocardial ischemia/reperfusion injury via modulation of mitochondrial function and hemodynamic parameters in aged rats. J Cardiovasc Pharmacol Ther. 2020;25(3):240–250. doi:10.1177/1074248419882002
  • Wang X, Hu X, Yang Y, Takata T, Sakurai T. Nicotinamide mononucleotide protects against β-amyloid oligomer-induced cognitive impairment and neuronal death. Brain Res. 2016;1643:1–9. doi:10.1016/j.brainres.2016.04.060
  • Yoshino J, Mills KF, Yoon MJ, Imai S. Nicotinamide mononucleotide, a key NAD (+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 2011;14(4):528–536. doi:10.1016/j.cmet.2011.08.014
  • Grolla AA, Miggiano R, Di Marino D, et al. A nicotinamide phosphoribosyltransferase-GAPDH interaction sustains the stress-induced NMN/NAD+ salvage pathway in the nucleus. J Biol Chem. 2020;295(11):3635–3651. doi:10.1074/jbc.RA119.010571
  • Bertoldo MJ, Listijono DR, Ho WJ, et al. NAD+ repletion rescues female fertility during reproductive aging. Cell Rep. 2020;30(6):1670–1681. doi:10.1016/j.celrep.2020.01.058
  • Tarantini S, Valcarcel-Ares MN, Toth P, et al. Nicotinamide mononucleotide (NMN) supplementation rescues cerebromicrovascular endothelial function and neurovascular coupling responses and improves cognitive function in aged mice. Redox Biol. 2019;24:101192. doi:10.1016/j.redox.2019.101192
  • Yu J, Laybutt DR, Kim LJ, et al. Exercise-induced benefits on glucose handling in a model of diet-induced obesity are reduced by concurrent nicotinamide mononucleotide. Am J Physiol Endocrinol Metab. 2021;321(1):E176–E189. doi:10.1152/ajpendo.00446.2020
  • Zhao C, Li W, Duan H, et al. NAD+ precursors protect corneal endothelial cells from UVB-induced apoptosis. Am J Physiol Cell Physiol. 2020;318(4):C796–C805. doi:10.1152/ajpcell.00445.2019
  • Uddin GM, Youngson NA, Doyle BM, Sinclair DA, Morris MJ. Nicotinamide mononucleotide (NMN) supplementation ameliorates the impact of maternal obesity in mice: comparison with exercise. Sci Rep. 2017;7(1):15063. doi:10.1038/s41598-017-14866-z
  • Xie X, Yu C, Zhou J, et al. Nicotinamide mononucleotide ameliorates the depression-like behaviors and is associated with attenuating the disruption of mitochondrial bioenergetics in depressed mice. J Affect Disord. 2020;263:166–174. doi:10.1016/j.jad.2019.11.147
  • Iwaniec UT, Turner RT. Intraperitoneal injection of ethanol results in drastic changes in bone metabolism not observed when ethanol is administered by oral gavage. Alcohol Clin Exp Res. 2013;37(8):1271–1277. doi:10.1111/acer.12105
  • Pugine SM, Brito P, Alba-Loureiro TC, Costa EJ, Curi R, De Melo MP. Effect of indole-3-acetic acid administration by gavage and by subcutaneous injection on rat leukocytes. Cell Biochem Funct. 2007;25(6):723–730. doi:10.1002/cbf.1383
  • Zhou X, Du HH, Ni L, et al. Nicotinamide mononucleotide combined with lactobacillus fermentum TKSN041 reduces the photoaging damage in murine skin by activating AMPK signaling pathway. Front Pharmacol. 2021;12:643089. doi:10.3389/fphar.2021.643089
  • Milton Prabu S, Shagirtha K, Renugadevi J. Quercetin in combination with vitamins (C and E) improves oxidative stress and renal injury in cadmium intoxicated rats. Eur Rev Med Pharmacol Sci. 2010;14:903–914.
  • Ochiai Y, Kaburagi S, Obayashi K, et al. A new lipophilic pro-vitamin C, tetra-isopalmitoyl ascorbic acid (VC-IP), prevents UV-induced skin pigmentation through its anti-oxidative properties. J Dermatol Sci. 2006;44(1):37–44. doi:10.1016/j.jdermsci.2006.07.001
  • Sealey WM, Gatlin DM 3rd. Dietary vitamin C and vitamin E interact to influence growth and tissue composition of juvenile hybrid striped bass (Morone chrysops (female) x M. saxatilis (male)) but have limited effects on immune responses. J Nutr. 2002;132(4):748–755. doi:10.1093/jn/132.4.748
  • Bleilevens C, Doorschodt BM, Fechter T, et al. Influence of vitamin C on antioxidant capacity of in vitro perfused porcine kidneys. Nutrients. 2019;11(8):1774. doi:10.3390/nu11081774
  • Che DN, Xie GH, Cho BO, Shin JY, Kang HJ, Jang SI. Protective effects of grape stem extract against UVB-induced damage in C57BL mice skin. J Photochem Photobiol B Biol. 2017;173:551–559. doi:10.1016/j.jphotobiol.2017.06.042
  • Yi R, Zhang J, Sun P, Qian Y, Zhao X. Protective effects of kuding tea (Ilex kudingcha C. J. Tseng) polyphenols on UVB-induced skin aging in SKH1 hairless mice. Molecules. 2019;24(6):1016. doi:10.3390/molecules24061016
  • Cejka C, Ardan T, Sirc J, et al. Hydration and transparency of the rabbit cornea irradiated with UVB-doses of 0.25 J/cm 2 and 0.5 J/cm 2 compared with equivalent UVB radiation exposure reaching the human cornea from sunlight. Curr Eye Res. 2011;36(7):607–613. doi:10.3109/02713683.2011.574332
  • Irie J, Inagaki E, Fujita M, et al. Effect of oral administration of nicotinamide mononucleotide on clinical parameters and nicotinamide metabolite levels in healthy Japanese men. Endocr J. 2020;67(2):153–160. doi:10.1507/endocrj.EJ19-0313
  • Chagas PM, Fulco B, Sari M, Roehrs JA, Nogueira CW. Bis(phenylimidazoselenazolyl) diselenide elicits antinociceptive effect by modulating myeloperoxidase activity, NOx and NFkB levels in the collagen-induced arthritis mouse model. J Pharm Pharmacol. 2017;69(8):1022–1032. doi:10.1111/jphp.12738
  • Hong S, Lee B, Kim JH, et al. Solanum nigrum linne improves DNCB‑induced atopic dermatitis‑like skin disease in BALB/c mice. Mol Med Rep. 2020;22:2878–2886.
  • De Oliveira NF, Andia DC, Planello AC, et al. TLR2 and TLR4 gene promoter methylation status during chronic periodontitis. J Clin Periodontol. 2011;38(11):975–983. doi:10.1111/j.1600-051X.2011.01765.x
  • Liu J, Ni J, Li LJ, Leng RX, Pan HF, Ye DQ. Decreased UBASH3A mRNA expression levels in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Inflammation. 2015;38(5):1903–1910. doi:10.1007/s10753-015-0170-9
  • Qian Y, Zhang J, Zhou X, et al. Lactobacillus plantarum CQPC11 isolated from Sichuan pickled cabbages antagonizes d-galactose-induced oxidation and aging in mice. Molecules. 2018;23(11):3026. doi:10.3390/molecules23113026
  • Wang R, Yang Z, Zhang J, Mu J, Zhou X, Zhao X. Liver injury induced by carbon tetrachloride in mice is prevented by the antioxidant capacity of anji white tea polyphenols. Antioxidants (Basel). 2019;8(3):64. doi:10.3390/antiox8030064
  • Gilda JE, Gomes AV. Stain-free total protein staining is a superior loading control to β-actin for western blots. Anal Biochem. 2013;440(2):186–188. doi:10.1016/j.ab.2013.05.027
  • Pandey N, Giri S. Melatonin attenuates radiofrequency radiation (900 MHz)-induced oxidative stress, DNA damage and cell cycle arrest in germ cells of male Swiss albino mice. Toxicol Ind Health. 2018;34(5):315–327. doi:10.1177/0748233718758092
  • Gao X, Luo F, Zhao H, Franco JL. Cloves regulate Na+-K+-ATPase to exert antioxidant effect and inhibit UVB light-induced skin damage in mice. Oxid Med Cell Longev. 2021;2021:5197919. doi:10.1155/2021/5197919
  • Park J, Halliday GM, Surjana D, Damian DL. Nicotinamide prevents ultraviolet radiation-induced cellular energy loss. Photochem Photobiol. 2010;86(4):942–948. doi:10.1111/j.1751-1097.2010.00746.x
  • Mori Y, Aki K, Kuge K, et al. UV B-irradiation enhances the racemization and isomerizaiton of aspartyl residues and production of Nε-carboxymethyl lysine (CML) in keratin of skin. J Chromatogr B Analyt Technol Biomed Life Sci. 2011;879(29):3303–3309. doi:10.1016/j.jchromb.2011.05.010
  • Her Y, Shin BN, Lee YL, et al. Oenanthe javanica extract protects mouse skin from UVB radiation via attenuating collagen disruption and inflammation. Int J Mol Sci. 2019;20(6):1435. doi:10.3390/ijms20061435
  • Wu CL, Qiang L, Han W, Ming M, Viollet B, He YY. Role of AMPK in UVB-induced DNA damage repair and growth control. Oncogene. 2013;32(21):2682–2689. doi:10.1038/onc.2012.279
  • Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-κB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal. 2013;25(10):1939–1948. doi:10.1016/j.cellsig.2013.06.007
  • Yu KX, Wong CL, Ahmad R, Jantan I. Larvicidal activity, inhibition effect on development, histopathological alteration and morphological aberration induced by seaweed extracts in Aedes aegypti (Diptera: Culicidae). Asian Pac J Trop Med. 2015;8(12):1006–1012. doi:10.1016/j.apjtm.2015.11.011
  • Kligman LH, Murphy GF. Ultraviolet B radiation increases hairless mouse mast cells in a dose-dependent manner and alters distribution of UV-induced mast cell growth factor. Photochem Photobiol. 1996;63(1):123–127. doi:10.1111/j.1751-1097.1996.tb03002.x
  • Zhang JA, Yin Z, Ma LW, et al. The protective effect of baicalin against UVB irradiation induced photoaging: an in vitro and in vivo study. PLoS One. 2014;9(6):e99703. doi:10.1371/journal.pone.0099703
  • Goerz G, Barnstorf W, Winnekendonk G, et al. Influence of UVA and UVB irradiation on hepatic and cutaneous P450 isoenzymes. Arch Dermatol Res. 1996;289(1):46–51. doi:10.1007/s004030050151
  • Widel M, Krzywon A, Gajda K, Skonieczna M, Rzeszowska-Wolny J. Induction of bystander effects by UVA, UVB, and UVC radiation in human fibroblasts and the implication of reactive oxygen species. Free Radic Biol Med. 2014;68:278–287. doi:10.1016/j.freeradbiomed.2013.12.021
  • You Y, Gao Y, Wang H, et al. Subacute toxicity study of nicotinamide mononucleotide via oral administration. Front Pharmacol. 2020;11:604404. doi:10.3389/fphar.2020.604404
  • Okatan DÖ, Kulaber A, Kerimoglu G, Odacı E. Altered morphology and biochemistry of the female rat liver following 900 megahertz electromagnetic field exposure during mid to late adolescence. Biotech Histochem. 2019;94(6):420–428.7. doi:10.1080/10520295.2019.1580767
  • Terra VA, Souza-Neto FP, Pereira RC, et al. Time-dependent reactive species formation and oxidative stress damage in the skin after UVB irradiation. J Photochem Photobiol B. 2012;109:34–41. doi:10.1016/j.jphotobiol.2012.01.003
  • Wang H, Wei S, Xue X, You Y, Ma Q. Adipose stem cells’ antagonism in glycosylation of D-galactose-induced skin aging of nude mice and its skin recovery function. Int J Immunopathol Pharmacol. 2016;29(3):376–385. doi:10.1177/0394632016634348
  • He J, Xu L, Yang L, Wang X. Epigallocatechin gallate is the most effective catechin against antioxidant stress via hydrogen peroxide and radical scavenging activity. Med Sci Monit. 2018;24:8198–8206. doi:10.12659/MSM.911175
  • Arsov S, Graaff R, van Oeveren W, et al. Advanced glycation end-products and skin autofluorescence in end-stage renal disease: a review. Clin Chem Lab Med. 2014;52(1):11–20. doi:10.1515/cclm-2012-0832
  • Muramatsu S, Suga Y, Mizuno Y, et al. Differentiation-specific localization of catalase and hydrogen peroxide, and their alterations in rat skin exposed to ultraviolet B rays. J Dermatol Sci. 2005;37(3):151–158. doi:10.1016/j.jdermsci.2004.11.001
  • Farina M, Aschner M. Glutathione antioxidant system and methylmercury-induced neurotoxicity: an intriguing interplay. Biochim Biophys Acta Gen Subj. 2019;1863(12):129285. doi:10.1016/j.bbagen.2019.01.007
  • Rahman M, Kundu JK, Shin JW, Na HK, Surh YJ, Aggarwal BB. Docosahexaenoic acid inhibits UVB-induced activation of NF-κB and expression of COX-2 and NOX-4 in HR-1 hairless mouse skin by blocking MSK1 signaling. PLoS One. 2011;6(11):e28065. doi:10.1371/journal.pone.0028065
  • Shats I, Williams JG, Liu J, et al. Bacteria boost mammalian host NAD metabolism by engaging the deamidated biosynthesis pathway. Cell Metab. 2020;31(3):564–579.e7. doi:10.1016/j.cmet.2020.02.001
  • Maurya PK, Prakash S. Decreased activity of Ca++-ATPase and Na+/K+-ATPase during aging in humans. Appl Biochem Biotechnol. 2013;170(1):131–137. doi:10.1007/s12010-013-0172-8
  • Wolf SJ, Estadt SN, Theros J, et al. Ultraviolet light induces increased T cell activation in lupus-prone mice via type I IFN-dependent inhibition of T regulatory cells. J Autoimmun. 2019;103:102291. doi:10.1016/j.jaut.2019.06.002
  • Guo G, Shi F, Zhu J, et al. Piperine, a functional food alkaloid, exhibits inhibitory potential against TNBS-induced colitis via the inhibition of IκB-α/NF-κB and induces tight junction protein (claudin-1, occludin, and ZO-1) signaling pathway in experimental mice. Hum Exp Toxicol. 2020;39(4):477–491. doi:10.1177/0960327119892042
  • Cho BO, Yin HH, Park SH, Byun EB, Ha HY, Jang SI. Anti-inflammatory activity of myricetin from Diospyros lotus through suppression of NF-κB and STAT1 activation and Nrf2-mediated HO-1 induction in lipopolysaccharide-stimulated RAW264.7 macrophages. Biosci Biotechnol Biochem. 2016;80(8):1520–1530. doi:10.1080/09168451.2016.1171697
  • Pikarsky E, Porat RM, Stein I, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature. 2004;431(7007):461–466. doi:10.1038/nature02924
  • Da Silva-ferrada E, Torres-Ramos M, Aillet F, et al. Role of monoubiquitylation on the control of IκBα degradation and NF-κB activity. PLoS One. 2011;6(10):e25397. doi:10.1371/journal.pone.0025397
  • Li L, Ngo H, Hwang E, et al. Conditioned medium from human adipose-derived mesenchymal stem cell culture prevents UVB-induced skin aging in human keratinocytes and dermal fibroblasts. Int J Mol Sci. 2019;21(1):49. doi:10.3390/ijms21010049
  • Chaiprasongsuk A, Janjetovic Z, Kim TK, et al. CYP11A1-derived vitamin D3 products protect against UVB-induced inflammation and promote keratinocytes differentiation. Free Radic Biol Med. 2020;155:87–98. doi:10.1016/j.freeradbiomed.2020.05.016
  • Braidy N, Liu Y. NAD+ therapy in age-related degenerative disorders: a benefit/risk analysis. Exp Gerontol. 2020;132:110831. doi:10.1016/j.exger.2020.110831
  • Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol. 2000;18(1):621–663. doi:10.1146/annurev.immunol.18.1.621
  • Thoma A, Lightfoot AP. NF-kB and inflammatory cytokine signaling: role in skeletal muscle atrophy. Adv Exp Med Biol. 2018;1088:267–279.
  • Zhang M, Wang C, Wu J, et al. The effect and mechanism of KLF7 in the TLR4/NF-κB/IL-6 inflammatory signal pathway of adipocytes. Mediators Inflamm. 2018;2018:1756494. doi:10.1155/2018/1756494
  • Zielinski CE, Mele F, Aschenbrenner D, et al. Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature. 2012;484(7395):514–518. doi:10.1038/nature10957
  • Hu Q, Li L, Zou X, Xu L, Yi P. Berberine attenuated proliferation, invasion and migration by targeting the AMPK/HNF4α/WNT5A pathway in gastric carcinoma. Front Pharmacol. 2018;9:1150. doi:10.3389/fphar.2018.01150
  • Salminen A, Kauppinen A, Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan. J Mol Med (Berl). 2011;89(7):667–676. doi:10.1007/s00109-011-0748-0
  • Wang P, Xu TY, Guan YF, et al. Nicotinamide phosphoribosyltransferase protects against ischemic stroke through SIRT1-dependent adenosine monophosphate-activated kinase pathway. Ann Neurol. 2011;69(2):360–374. doi:10.1002/ana.22236
  • He WY, Zhang B, Zhao WC, et al. mTOR activation due to APPL1 deficiency exacerbates hyperalgesia via Rab5/Akt and AMPK signaling pathway in streptozocin-induced diabetic rats. Mol Pain. 2019;15:1744806919880643. doi:10.1177/1744806919880643
  • Zhang YL, Guo H, Zhang CS, et al. AMP as a low-energy charge signal autonomously initiates assembly of AXIN-AMPK-LKB1 complex for AMPK activation. Cell Metab. 2013;18(4):546–555. doi:10.1016/j.cmet.2013.09.005
  • Jia J, Abudu YP, Claude-Taupin A, et al. Galectins control MTOR and AMPK in response to lysosomal damage to induce autophagy. Autophagy. 2019;15:169–171.
  • Cao C, Lu S, Kivlin R, et al. AMP-activated protein kinase contributes to UV- and H2O2-induced apoptosis in human skin keratinocytes. J Biol Chem. 2008;283(43):28897–28908. doi:10.1074/jbc.M804144200
  • Chandrasekaran K, Anjaneyulu M, Choi J, et al. Role of mitochondria in diabetic peripheral neuropathy: influencing the NAD+-dependent SIRT1-PGC-1α-TFAM pathway. Int Rev Neurobiol. 2019;145:177–209.
  • Jing R, Guo K, Zhong Y, et al. Protective effects of fucoidan purified from Undaria pinnatifida against UV-irradiated skin photoaging. Ann Transl Med. 2021;9(14):1185. doi:10.21037/atm-21-3668
  • Lim CJ, Lee YM, Kang SG, et al. Aquatide activation of SIRT1 reduces cellular senescence through a SIRT1-FOXO1-autophagy axis. Biomol Ther (Seoul). 2017;25(5):511–518. doi:10.4062/biomolther.2017.119