Insights on the role of L-lactate as a signaling molecule in skin aging.
Aging
L-lactate
Mito-hormesis
Redox signaling
Skin
Journal
Biogerontology
ISSN: 1573-6768
Titre abrégé: Biogerontology
Pays: Netherlands
ID NLM: 100930043
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
01
11
2022
accepted:
17
01
2023
medline:
5
9
2023
pubmed:
29
1
2023
entrez:
28
1
2023
Statut:
ppublish
Résumé
L-lactate is a catabolite from the anaerobic metabolism of glucose, which plays a paramount role as a signaling molecule in various steps of the cell survival. Its activity, as a master tuner of many mechanisms underlying the aging process, for example in the skin, is still presumptive, however its crucial position in the complex cross-talk between mitochondria and the process of cell survival, should suggest that L-lactate may be not a simple waste product but a fine regulator of the aging/survival machinery, probably via mito-hormesis. Actually, emerging evidence is highlighting that ROS are crucial in the signaling of skin health, including mechanisms underlying wound repair, renewal and aging. The ROS, including superoxide anion, hydrogen peroxide, and nitric oxide, play both beneficial and detrimental roles depending upon their levels and cellular microenvironment. Physiological ROS levels are essential for cutaneous health and the wound repair process. Aberrant redox signaling activity drives chronic skin disease in elderly. On the contrary, impaired redox modulation, due to enhanced ROS generation and/or reduced levels of antioxidant defense, suppresses wound healing via promoting lymphatic/vascular endothelial cell apoptosis and death. This review tries to elucidate this issue.
Identifiants
pubmed: 36708434
doi: 10.1007/s10522-023-10018-1
pii: 10.1007/s10522-023-10018-1
pmc: PMC9883612
doi:
Substances chimiques
Reactive Oxygen Species
0
Superoxides
11062-77-4
Lactates
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
709-726Informations de copyright
© 2023. The Author(s).
Références
Adelsmayr G, Brunner R, Holzinger U (2012) Impact of blood glucose on blood lactate levels in a medical ICU: a retrospective cohort study. Crit Care 16(Suppl 1):P165
pmcid: 3363583
Alves de Souza RW, Gallo D, Lee GR, Katsuyama E, Schaufler A, Weber J, Csizmadia E, Tsokos GC, Koch LG, Britton SL, Wisløff U, Brum PC, Otterbein LE (2021) Skeletal muscle heme oxygenase-1 activity regulates aerobic capacity. Cell Rep 35(3):109018
pubmed: 33882313
Atayik MC, Çakatay U (2022) Mitochondria-targeted senotherapeutic interventions. Biogerontology 23(4):401–423
pubmed: 35781579
Bakula D, Scheibye-Knudsen M (2020) MitophAging: mitophagy in aging and disease. Front Cell Dev Biol 8:239
pubmed: 32373609
pmcid: 7179682
Baldelli S, Aquilano K, Ciriolo MR (2014) PGC-1α buffers ROS-mediated removal of mitochondria during myogenesis. Cell Death Dis 5(11):e1515
pubmed: 25375380
pmcid: 4260723
Balcázar M, Cañizares S, Borja T, Pontón P, Bisiou S, Carabasse E, Bacilieri A, Canavese C, Diaz RF, Cabrera F, Caicedo A (2020) Bases for treating skin aging with artificial mitochondrial transfer/transplant (AMT/T). Front Bioeng Biotechnol 8:919
pubmed: 32903493
pmcid: 7438394
Baltazar F, Afonso J, Costa M, Granja S (2020) Lactate beyond a waste metabolite: metabolic affairs and signaling in malignancy. Front Oncol 10:231
pubmed: 32257942
pmcid: 7093491
Barbosa MC, Grosso RA, Fader CM (2019) Hallmarks of aging: an autophagic perspective. Front Endocrinol (lausanne) 9:790
pubmed: 30687233
Bárcena C, Mayoral P, Quirós PM (2018) Mitohormesis, an antiaging paradigm. Int Rev Cell Mol Biol 340:35–77
pubmed: 30072093
Barzegari A, Aaboulhassanzadeh S, Landon R, Gueguen V, Meddahi-Pellé A, Parvizpour S, Anagnostou F, Pavon-Djavid G (2022) Mitohormesis and mitochondrial dynamics in the regulation of stem cell fate. J Cell Physiol 237(9):3435–3448
pubmed: 35775725
Benton CR, Yoshida Y, Lally J, Han XX, Hatta H, Bonen A (2008) PGC-1alpha increases skeletal muscle lactate uptake by increasing the expression of MCT1 but not MCT2 or MCT4. Physiol Genom 35(1):45–54
Bordon Y (2021) Protect the species with mitohormesis? Nat Rev Immunol 21(7):407
pubmed: 34075228
Brandi J, Cheri S, Manfredi M, Di Carlo C, Vita Vanella V, Federici F, Bombiero E, Bazaj A, Rizzi E, Manna L, Cornaglia G, Marini U, Valenti MT, Marengo E, Cecconi D (2020) Exploring the wound healing, anti-inflammatory, anti-pathogenic and proteomic effects of lactic acid bacteria on keratinocytes. Sci Rep 10(1):11572
pubmed: 32665600
pmcid: 7360600
Brisson L, Bański P, Sboarina M, Dethier C, Danhier P, Fontenille MJ, Van Hée VF, Vazeille T, Tardy M, Falces J, Bouzin C, Porporato PE, Frédérick R, Michiels C, Copetti T, Sonveaux P (2016) Lactate dehydrogenase B controls lysosome activity and autophagy in cancer. Cancer Cell 30(3):418–431
pubmed: 27622334
Brooks GA (2009) Cell-cell and intracellular lactate shuttles. J Physiol 587(Pt 23):5591–5600
pubmed: 19805739
pmcid: 2805372
Brooks GA (2020) Lactate as a fulcrum of metabolism. Redox Biol 35:101454
pubmed: 32113910
pmcid: 7284908
Brouwers MC, Ham JC, Wisse E, Misra S, Landewe S, Rosenthal M, Patel D, Oliver N, Bilo HJ, Murphy E (2015) Elevated lactate levels in patients with poorly regulated type 1 diabetes and glycogenic hepatopathy: a new feature of Mauriac syndrome. Diabetes Care 38(2):e11–e12
pubmed: 25614691
Cai M, Wang H, Song H, Yang R, Wang L, Xue X, Sun W, Hu J (2022) Lactate is answerable for brain function and treating brain diseases: energy substrates and signal molecule. Front Nutr 9:800901
pubmed: 35571940
pmcid: 9099001
Chen YJ, Mahieu NG, Huang X, Singh M, Crawford PA, Johnson SL, Gross RW, Schaefer J, Patti GJ (2016) Lactate metabolism is associated with mammalian mitochondria. Nat Chem Biol 12(11):937–943
pubmed: 27618187
pmcid: 5069139
Chen G, Kroemer G, Mitophagy KO (2020) An emerging role in aging and age-associated diseases. Front Cell Dev Biol 8:200
pubmed: 32274386
pmcid: 7113588
Chirumbolo S, Valdenassi L, Simonetti V, Bertossi D, Ricevuti G, Franzini M, Pandolfi S (2021) Insights on the mechanisms of action of ozone in the medical therapy against COVID-19. Int Immunopharmacol 96:107777
pubmed: 34020394
pmcid: 8112288
Coggan JS, Keller D, Markram H, Schürmann F, Magistretti PJ (2022) Representing stimulus information in an energy metabolism pathway. J Theor Biol 540:111090
pubmed: 35271865
Comstock JP, Udenfriend S (1970) Effect of lactate on collagen proline hydroxylase activity in cultured L-929 fibroblasts. Proc Natl Acad Sci USA 66(2):552–557
pubmed: 5271180
pmcid: 283080
Cui Y, Qin L, Wu J, Qu X, Hou C, Sun W, Li S, Vaughan AT, Li JJ, Liu J (2015) SIRT3 enhances glycolysis and proliferation in SIRT3-expressing gastric cancer cells. PLoS ONE 10(6):e0129834
pubmed: 26121691
pmcid: 4487898
Danby FW (2010) Nutrition and aging skin: sugar and glycation. Clin Dermatol 28(4):409–411. https://doi.org/10.1016/j.clindermatol.2010.03.018
doi: 10.1016/j.clindermatol.2010.03.018
pubmed: 20620757
D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8(10):813–824
pubmed: 17848967
Das CK, Parekh A, Parida PK, Bhutia SK, Mandal M (2019) Lactate dehydrogenase A regulates autophagy and tamoxifen resistance in breast cancer. Biochim Biophys Acta Mol Cell Res 1866(6):1004–1018
pubmed: 30878502
Datta S, Chakrabarti N (2018) Age related rise in lactate and its correlation with lactate dehydrogenase (LDH) status in post-mitochondrial fractions isolated from different regions of brain in mice. Neurochem Int 118:23–33
pubmed: 29678731
Di Marzo N, Chisci E, Giovannoni R (2018) The role of hydrogen peroxide in redox-dependent signaling: homeostatic and pathological responses in mammalian cells. Cells 7(10):156
pubmed: 30287799
pmcid: 6211135
Duda I, Krzych Ł, Jędrzejowska-Szypułka H, Lewin-Kowalik J (2020) Plasma matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1 as prognostic biomarkers in critically ill patients. Open Med (wars) 15:50–56
pubmed: 32190734
Duncan AJ, Bitner-Glindzicz M, Meunier B et al (2009) A nonsense mutation in COQ9 causes autosomal-recessive neonatal-onset primary coenzyme Q10 deficiency: a potentially treatable form of mitochondrial disease. Am J Hum Genet 84:558–566
pubmed: 19375058
pmcid: 2681001
Dunnill C, Patton T, Brennan J, Barrett J, Dryden M, Cooke J, Leaper D, Georgopoulos NT (2017) Reactive oxygen species (ROS) and wound healing: the functional role of ROS and emerging ROS-modulating technologies for augmentation of the healing process. Int Wound J 14(1):89–96
pubmed: 26688157
Durante W, Johnson FK, Johnson RA (2006) Role of carbon monoxide in cardiovascular function. J Cell Mol Med 10(3):672–686
pubmed: 16989727
Eckhart L, Tschachler E, Gruber F (2019) Autophagic control of skin aging. Front Cell Dev Biol 7:143
pubmed: 31417903
pmcid: 6682604
Eltzschig HK (2013) Extracellular adenosine signaling in molecular medicine. J Mol Med (berl) 91(2):141–146
pubmed: 23338058
Feng XE, Liang TG, Gao J, Kong P, Ge R, Li QS (2017) Heme oxygenase-1, a Key enzyme for the cytoprotective actions of halophenols by upregulating Nrf2 expression via activating Erk1/2 and PI3K/Akt in EA.hy926 cells. Oxid Med Cell Longev 2017:7028478
pubmed: 28694915
pmcid: 5488237
Forman HJ, Maiorino M, Ursini F (2010) Signaling functions of reactive oxygen species. Biochemistry 49(5):835–842
pubmed: 20050630
Forsyth JJ, Reilly T (2004) Circadian rhythms in blood lactate concentration during incremental ergometer rowing. Eur J Appl Physiol 92(1–2):69–74
pubmed: 14991328
Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, Cevenini E, Castellani GC, Salvioli S (2007) Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 128(1):92–105
pubmed: 17116321
Freitas-Rodríguez S, Folgueras AR, López-Otín C (2017) The role of matrix metalloproteinases in aging: tissue remodeling and beyond. Biochim Biophys Acta Mol Cell Res 1864(11 Pt A):2015–2025
pubmed: 28499917
Gaál Z, Csernoch L (2020) Impact of sirtuin enzymes on the altered metabolic phenotype of malignantly transformed cells. Front Oncol 10:45
pubmed: 32117717
pmcid: 7033489
Gambini J, Gomez-Cabrera MC, Borras C, Valles SL, Lopez-Grueso R, Martinez-Bello VE, Herranz D, Pallardo FV, Tresguerres JA, Serrano M, Viña J (2011) Free [NADH]/[NAD(+)] regulates sirtuin expression. Arch Biochem Biophys 512(1):24–29
pubmed: 21575591
Gauron C, Rampon C, Bouzaffour M, Ipendey E, Teillon J, Volovitch M, Vriz S (2013) Sustained production of ROS triggers compensatory proliferation and is required for regeneration to proceed. Sci Rep 3:2084
pubmed: 23803955
pmcid: 3694286
Glancy B, Kane DA, Kavazis AN, Goodwin ML, Willis WT, Gladden LB (2021) Mitochondrial lactate metabolism: history and implications for exercise and disease. J Physiol 599(3):863–888
pubmed: 32358865
Go S, Kramer TT, Verhoeven AJ, Oude Elferink RPJ, Chang JC (2021) The extracellular lactate-to-pyruvate ratio modulates the sensitivity to oxidative stress-induced apoptosis via the cytosolic NADH/NAD
pubmed: 33230593
Guerrero-Morín JG, Santillán M (2020) Crosstalk dynamics between the circadian clock and the mTORC1 pathway. J Theor Biol 501:110360
pubmed: 32522472
Gunin AG, Petrov VV, Golubtzova NN, Vasilieva OV, Kornilova NK (2014) Age-related changes in angiogenesis in human dermis. Exp Gerontol 55:143–151
pubmed: 24768823
Haake AR, Roublevskaia I, Cooklis M (1998) Apoptosis: a role in skin aging? J Investig Dermatol Symp Proc 3(1):28–35
pubmed: 9732054
Hamanaka RB, Chandel NS (2013) Mitochondrial metabolism as a regulator of keratinocyte differentiation. Cell Logist 3(1):e25456
pubmed: 24475371
pmcid: 3891634
Hamanaka RB, Glasauer A, Hoover P, Yang S, Blatt H, Mullen AR, Getsios S, Gottardi CJ, DeBerardinis RJ, Lavker RM, Chandel NS (2013) Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci Signal 6(261):ra8
pubmed: 23386745
pmcid: 4017376
Hanisch F, Müller T, Muser A, Deschauer M, Zierz S (2006) Lactate increase and oxygen desaturation in mitochondrial disorders–evaluation of two diagnostic screening protocols. J Neurol 253(4):417–423
pubmed: 16619117
Hashimoto T, Hussien R, Oommen S, Gohil K, Brooks GA (2007) Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis. FASEB J 21(10):2602–2612. https://doi.org/10.1096/fj.07-8174com
doi: 10.1096/fj.07-8174com
pubmed: 17395833
He X, Dong Z, Cao Y, Wang H, Liu S, Liao L, Jin Y, Yuan L, Li B (2019) MSC-derived exosome promotes M2 polarization and enhances cutaneous wound healing. Stem Cells Int 2019:7132708
pubmed: 31582986
pmcid: 6754952
Harman D (1972) Free radical theory of aging: dietary implications. Am J Clin Nutr 25(8):839–843
pubmed: 5046729
Holmberg MJ, Andersen LW, Moskowitz A, Berg KM, Cocchi MN, Chase M, Liu X, Kuhn DM, Grossestreuer AV, Hoeyer-Nielsen AK, Kirkegaard H, Donnino MW (2021) Ubiquinol (reduced coenzyme Q10) as a metabolic resuscitator in post-cardiac arrest: a randomized, double-blind, placebo-controlled trial. Resuscitation 162:388–395
pubmed: 33577964
Hu M, Zhao Y, Cao Y, Tang Q, Feng Z, Ni J, Zhou X (2020) DRP1 promotes lactate utilization in KRAS-mutant non-small-cell lung cancer cells. Cancer Sci 111(10):3588–3599
pubmed: 32767829
pmcid: 7540982
Huang HC, Lee IJ, Huang C, Chang TM (2020) Lactic acid bacteria and lactic acid for skin health and melanogenesis inhibition. Curr Pharm Biotechnol 21(7):566–577
pubmed: 31916515
Huang Z, Zhang Y, Zhou R, Yang L, Pan H (2021) Lactate as potential mediators for exercise-induced positive effects on neuroplasticity and cerebrovascular plasticity. Front Physiol 12:656455
pubmed: 34290615
pmcid: 8287254
Hudson L, Bowman A, Rashdan E, Birch-Machin MA (2016) Mitochondrial damage and ageing using skin as a model organ. Maturitas 93:34–40
pubmed: 27215947
Jang JY, Blum A, Liu J, Finkel T (2018) The role of mitochondria in aging. J Clin Invest 128(9):3662–3670
pubmed: 30059016
pmcid: 6118639
Jenkins G (2002) Molecular mechanisms of skin ageing. Mech Ageing Dev 123(7):801–810
pubmed: 11869737
Jiang Y, Mishima H, Sakai S, Liu YK, Ohyabu Y, Uemura T (2008) Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders. J Orthop Res 26(7):910–917
pubmed: 18302252
Kawalec M, Boratyńska-Jasińska A, Beręsewicz M, Dymkowska D, Zabłocki K, Zabłocka B (2015) Mitofusin 2 deficiency affects energy metabolism and mitochondrial biogenesis in MEF cells. PLoS ONE 10(7):e0134162
pubmed: 26230519
pmcid: 4521854
Kim SY, Nair MG (2019) Macrophages in wound healing: activation and plasticity. Immunol Cell Biol 97(3):258–267
pubmed: 30746824
pmcid: 6426672
Kim HP, Ryter SW, Choi AM (2006) CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46:411–449
pubmed: 16402911
Kitada M, Koya D (2021) Autophagy in metabolic disease and ageing. Nat Rev Endocrinol. https://doi.org/10.1038/s41574-021-00551-9
doi: 10.1038/s41574-021-00551-9
pubmed: 34508250
Kitaoka Y, Takeda K, Tamura Y, Hatta H (2016) Lactate administration increases mRNA expression of PGC-1α and UCP3 in mouse skeletal muscle. Appl Physiol Nutr Metab 41(6):695–698
pubmed: 27218871
Klaus S, Ost M (2020) Mitochondrial uncoupling and longevity—a role for mitokines? Exp Gerontol 130:110796
pubmed: 31786315
Kohl E, Steinbauer J, Landthaler M, Szeimies RM (2011) Skin ageing. J Eur Acad Dermatol Venereol 25(8):873–884
pubmed: 21261751
Kozlov AM, Lone A, Betts DH, Cumming RC (2020) Lactate preconditioning promotes a HIF-1α-mediated metabolic shift from OXPHOS to glycolysis in normal human diploid fibroblasts. Sci Rep 10(1):8388
pubmed: 32433492
pmcid: 7239882
Kruk J, Aboul-Enein HY, Kładna A, Bowser JE (2019) Oxidative stress in biological systems and its relation with pathophysiological functions: the effect of physical activity on cellular redox homeostasis. Free Radic Res 53(5):497–521
pubmed: 31039624
Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309(5733):481–484
pubmed: 16020738
Kida YS, Kawamura T, Wei Z, Sogo T, Jacinto S, Shigeno A, Kushige H, Yoshihara E, Liddle C, Ecker JR, Yu RT, Atkins AR, Downes M, Evans RM (2015) ERRs mediate a metabolic switch required for somatic cell reprogramming to pluripotency. Cell Stem Cell 16(5):547–555
pubmed: 25865501
pmcid: 4427539
Kincaid B, Bossy-Wetzel E (2013) Forever young: SIRT3 a shield against mitochondrial meltdown, aging, and neurodegeneration. Front Aging Neurosci 5:48
pubmed: 24046746
pmcid: 3764375
Kottmann RM, Kulkarni AA, Smolnycki KA, Lyda E, Dahanayake T, Salibi R, Honnons S, Jones C, Isern NG, Hu JZ, Nathan SD, Grant G, Phipps RP, Sime PJ (2012) Lactic acid is elevated in idiopathic pulmonary fibrosis and induces myofibroblast differentiation via pH-dependent activation of transforming growth factor-β. Am J Respir Crit Care Med 186(8):740–751
pubmed: 22923663
pmcid: 3480515
Kwon TG, Zhao X, Yang Q, Li Y, Ge C, Zhao G, Franceschi RT (2011) Physical and functional interactions between Runx2 and HIF-1α induce vascular endothelial growth factor gene expression. J Cell Biochem 112(12):3582–3593
pubmed: 21793044
pmcid: 3202060
Lago JC, Puzzi MB (2019) The effect of aging in primary human dermal fibroblasts. PLoS ONE 14(7):e0219165
pubmed: 31269075
pmcid: 6608952
Lafita-Navarro MC, Perez-Castro L, Zacharias LG, Barnes S, DeBerardinis RJ, Conacci-Sorrell M (2020) The transcription factors aryl hydrocarbon receptor and MYC cooperate in the regulation of cellular metabolism. J Biol Chem 295(35):12398–12407
pubmed: 32611766
pmcid: 7458811
Larsson NG (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem 79:683–706
pubmed: 20350166
Lee TY (2021) Lactate: a multifunctional signaling molecule. Yeungnam Univ J Med 38(3):183–193
pubmed: 33596629
pmcid: 8225492
Lee DE, Ayoub N, Agrawal DK (2016) Mesenchymal stem cells and cutaneous wound healing: novel methods to increase cell delivery and therapeutic efficacy. Stem Cell Res Ther 7:37. https://doi.org/10.1186/s13287-016-0303-6
doi: 10.1186/s13287-016-0303-6
pubmed: 26960535
pmcid: 4784457
Levasseur JE, Alessandri B, Reinert M, Clausen T, Zhou Z, Altememi N, Bullock MR (2006) Lactate, not glucose, up-regulates mitochondrial oxygen consumption both in sham and lateral fluid percussed rat brains. Neurosurgery 59(5):1122–1130 (discussion 1130-1)
pubmed: 17143246
Lezi E, Lu J, Selfridge JE, Burns JM, Swerdlow RH (2013) Lactate administration reproduces specific brain and liver exercise-related changes. J Neurochem 127(1):91–100
pmcid: 4276250
Li X, Yang L, Mao Z, Pan X, Zhao Y, Gu X, Eckel-Mahan K, Zuo Z, Tong Q, Hartig SM, Cheng X, Du G, Moore DD, Bellen HJ, Sesaki H, Sun K (2020) Novel role of dynamin-related-protein 1 in dynamics of ER-lipid droplets in adipose tissue. FASEB J 34(6):8265–8282
pubmed: 32294302
Liang H, Ward WF (2006) PGC-1alpha: a key regulator of energy metabolism. Adv Physiol Educ 30(4):145–151
pubmed: 17108241
Liemburg-Apers DC, Willems PH, Koopman WJ, Grefte S (2015) Interactions between mitochondrial reactive oxygen species and cellular glucose metabolism. Arch Toxicol 89(8):1209–1226
pubmed: 26047665
pmcid: 4508370
Liu YJ, McIntyre RL, Janssens GE, Houtkooper RH (2020a) Mitochondrial fission and fusion: a dynamic role in aging and potential target for age-related disease. Mech Ageing Dev 186:111212
pubmed: 32017944
Liu J, Ding Y, Liu Z, Liang X (2020b) Senescence in mesenchymal stem cells: functional alterations, molecular mechanisms, and rejuvenation strategies. Front Cell Dev Biol 8:258
pubmed: 32478063
pmcid: 7232554
Liu J, Chen S, Biswas S, Nagrani N, Chu Y, Chakrabarti S, Feng B (2020c) Glucose-induced oxidative stress and accelerated aging in endothelial cells are mediated by the depletion of mitochondrial SIRTs. Physiol Rep 8(3):e14331. https://doi.org/10.14814/phy2.14331
doi: 10.14814/phy2.14331
pubmed: 32026628
pmcid: 7002531
Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, Gargiulo G, Testa G, Cacciatore F, Bonaduce D, Abete P (2018) Oxidative stress, aging, and diseases. Clin Interv Aging 13:757–772
pubmed: 29731617
pmcid: 5927356
Lisowski P, Kannan P, Mlody B, Prigione A (2018) Mitochondria and the dynamic control of stem cell homeostasis. EMBO Rep 19(5):e45432
pubmed: 29661859
pmcid: 5934764
Longchamps RJ, Castellani CA, Yang SY, Newcomb CE, Sumpter JA, Lane J, Grove ML, Guallar E, Pankratz N, Taylor KD, Rotter JI, Boerwinkle E, Arking DE (2020) Evaluation of mitochondrial DNA copy number estimation techniques. PLoS ONE 15(1):e0228166
pubmed: 32004343
pmcid: 6994099
Mahbub S, Deburghgraeve CR, Kovacs EJ (2012) Advanced age impairs macrophage polarization. J Interferon Cytokine Res 32(1):18–26
pubmed: 22175541
pmcid: 3255514
Manojlović V, Erčulj F (2019) Using blood lactate concentration to predict muscle damage and jump performance response to maximal stretch-shortening cycle exercise. J Sports Med Phys Fit 59(4):581–586
Manosalva C, Quiroga J, Hidalgo AI, Alarcón P, Anseoleaga N, Hidalgo MA, Burgos RA (2022) Role of lactate in inflammatory processes: friend or foe. Front Immunol 12:808799
pubmed: 35095895
pmcid: 8795514
Mann BE (2010) Carbon monoxide: an essential signalling molecule. In: Jaouen G, Metzler-Nolte N (eds) Medicinal organometallic chemistry. Topics in organometallic chemistry, vol 32. Springer, Berlin. https://doi.org/10.1007/978-3-642-13185-1_10
doi: 10.1007/978-3-642-13185-1_10
Marcheggiani F, Kordes S, Cirilli I, Orlando P, Silvestri S, Vogelsang A, Möller N, Blatt T, Weise JM, Damiani E, Tiano L (2021) Anti-ageing effects of ubiquinone and ubiquinol in a senescence model of human dermal fibroblasts. Free Radic Biol Med 165:282–288
pubmed: 33482334
Matsuo T, Daishaku S, Sadzuka Y (2019) Lactic acid promotes cell survival by blocking autophagy of B16F10 mouse melanoma cells under glucose deprivation and hypoxic conditions. Biol Pharm Bull 42(5):837–839
pubmed: 31061328
Mellem D, Sattler M, Pagel-Wolff S, Jaspers S, Wenck H, Rübhausen MA, Fischer F (2017) Fragmentation of the mitochondrial network in skin in vivo. PLoS ONE 12(6):e0174469
pubmed: 28644888
pmcid: 5482427
Merry TL, Ristow M (2016) Mitohormesis in exercise training. Free Radic Biol Med 98:123–130
pubmed: 26654757
Mills EL, Kelly B, O’Neill LAJ (2017) Mitochondria are the powerhouses of immunity. Nat Immunol 18(5):488–498
pubmed: 28418387
Mortuza R, Chen S, Feng B, Sen S, Chakrabarti S (2013) High glucose induced alteration of SIRTs in endothelial cells causes rapid aging in a p300 and FOXO regulated pathway. PLoS ONE 8(1):e54514
pubmed: 23342163
pmcid: 3546959
Mosienko V, Teschemacher AG, Kasparov S (2015) Is L-lactate a novel signaling molecule in the brain? J Cereb Blood Flow Metab 35(7):1069–1075
pubmed: 25920953
pmcid: 4640281
Müller P, Duderstadt Y, Lessmann V, Müller NG (2020) Lactate and BDNF: key mediators of exercise induced neuroplasticity? J Clin Med 9(4):1136
pubmed: 32326586
pmcid: 7230639
Musci RV, Hamilton KL, Linden MA (2019) Exercise-induced mitohormesis for the maintenance of skeletal muscle and healthspan extension. Sports (basel) 7(7):170
pubmed: 31336753
Nabben M, Hoeks J, Briedé JJ, Glatz JF, Moonen-Kornips E, Hesselink MK, Schrauwen P (2008) The effect of UCP3 overexpression on mitochondrial ROS production in skeletal muscle of young versus aged mice. FEBS Lett 582(30):4147–4152
pubmed: 19041310
Nalbandian M, Takeda M (2016) Lactate as a signaling molecule that regulates exercise-induced adaptations. Biology (basel) 5(4):38
pubmed: 27740597
Ndiaye MA, Nihal M, Wood GS, Ahmad N (2014) Skin, reactive oxygen species, and circadian clocks. Antioxid Redox Signal 20(18):2982–2996
pubmed: 24111846
pmcid: 4038996
Nikooie R, Moflehi D, Zand S (2021) Lactate regulates autophagy through ROS-mediated activation of ERK1/2/m-TOR/p-70S6K pathway in skeletal muscle. J Cell Commun Signal 15(1):107–123
pubmed: 33398722
pmcid: 7905011
Padilla-Sánchez SD, Navarrete D, Caicedo A, Teran E (2020) Circulating cell-free mitochondrial DNA levels correlate with body mass index and age. Biochim Biophys Acta Mol Basis Dis 1866(12):165963
pubmed: 32919035
Park HY, Kim JH, Jung M, Chung CH, Hasham R, Park CS, Choi EH (2011) A long-standing hyperglycaemic condition impairs skin barrier by accelerating skin ageing process. Exp Dermatol 20(12):969–974
pubmed: 22017743
Pellerin L, Connes P, Bisbal C, Lambert K (2022) Editorial: lactate as a major signaling molecule for homeostasis. Front Physiol 13:910567
pubmed: 35755437
pmcid: 9214235
Philp A, Macdonald AL, Watt PW (2005) Lactate–a signal coordinating cell and systemic function. J Exp Biol 208(Pt 24):4561–4575
pubmed: 16326938
Prieto J, Seo AY, León M, Santacatterina F, Torresano L, Palomino-Schätzlein M, Giménez K, Vallet-Sánchez A, Ponsoda X, Pineda-Lucena A, Cuezva JM, Lippincott-Schwartz J, Torres J (2018) MYC induces a hybrid energetics program early in cell reprogramming. Stem Cell Rep 11(6):1479–1492
Prigione A, Rohwer N, Hoffmann S, Mlody B, Drews K, Bukowiecki R, Blümlein K, Wanker EE, Ralser M, Cramer T, Adjaye J (2014) HIF1α modulates cell fate reprogramming through early glycolytic shift and upregulation of PDK1-3 and PKM2. Stem Cells 32(2):364–376
pubmed: 24123565
Ratter JM, Rooijackers HMM, Hooiveld GJ, Hijmans AGM, de Galan BE, Tack CJ, Stienstra R (2018) In vitro and in vivo effects of lactate on metabolism and cytokine production of human primary PBMCs and monocytes. Front Immunol 9:2564
pubmed: 30483253
pmcid: 6240653
Rehan M, Kurundkar D, Kurundkar AR, Logsdon NJ, Smith SR, Chanda D, Bernard K, Sanders YY, Deshane JS, Dsouza KG, Rangarajan S, Zmijewski JW, Thannickal VJ (2021) Restoration of SIRT3 gene expression by airway delivery resolves age-associated persistent lung fibrosis in mice. Nat Aging 1(2):205–217
pubmed: 34386777
pmcid: 8357317
Reilly T, Waterhouse J (2009) Sports performance: is there evidence that the body clock plays a role? Eur J Appl Physiol 106(3):321–332
pubmed: 19418063
Reinke H, Asher G (2019) Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol 20(4):227–241
pubmed: 30635659
Rezvani HR, Ali N, Serrano-Sanchez M, Dubus P, Varon C, Ged C, Pain C, Cario-André M, Seneschal J, Taïeb A, de Verneuil H, Mazurier F (2011) Loss of epidermal hypoxia-inducible factor-1α accelerates epidermal aging and affects re-epithelialization in human and mouse. J Cell Sci 124(Pt 24):4172–4183
pubmed: 22193962
Rigotti G, Chirumbolo S (2019) Biological morphogenetic surgery: a minimally invasive procedure to address different biological mechanisms. Aesthet Surg J 39(7):745–755
pubmed: 30137183
Rockstein M, Brandt KF (1963) Enzyme changes in flight muscle correlated with aging and flight ability in the male housefly. Science 139(3559):1049–1051
pubmed: 13974590
Rogatzki MJ, Ferguson BS, Goodwin ML, Gladden LB (2015) Lactate is always the end product of glycolysis. Front Neurosci 9:22
pubmed: 25774123
pmcid: 4343186
Roger F, Picazo C, Reiter W, Libiad M, Asami C, Hanzén S, Gao C, Lagniel G, Welkenhuysen N, Labarre J, Nyström T, Grøtli M, Hartl M, Toledano MB, Molin M (2020) Peroxiredoxin promotes longevity and H
pubmed: 32662770
pmcid: 7392609
Roland CL, Arumugam T, Deng D, Liu SH, Philip B, Gomez S, Burns WR, Ramachandran V, Wang H, Cruz-Monserrate Z, Logsdon CD (2014) Cell surface lactate receptor GPR81 is crucial for cancer cell survival. Cancer Res 74(18):5301–5310
pubmed: 24928781
pmcid: 4167222
Ross JM, Öberg J, Brené S, Coppotelli G, Terzioglu M, Pernold K, Goiny M, Sitnikov R, Kehr J, Trifunovic A, Larsson NG, Hoffer BJ, Olson L (2010) High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc Natl Acad Sci USA 107(46):20087–20092
pubmed: 21041631
pmcid: 2993405
Savolainen ER, Leo MA, Timpl R, Lieber CS (1984) Acetaldehyde and lactate stimulate collagen synthesis of cultured baboon liver myofibroblasts. Gastroenterology 87(4):777–787
pubmed: 6381214
Schmidt A, Karlson-Stiber C (2008) Caffeine poisoning and lactate rise: an overlooked toxic effect? Acta Anaesthesiol Scand 52(7):1012–1014
pubmed: 18494847
Schneider AM, Özsoy M, Zimmermann FA, Feichtinger RG, Mayr JA, Kofler B, Sperl W, Weghuber D, Mörwald K (2020) Age-related deterioration of mitochondrial function in the intestine. Oxid Med Cell Longev 2020:4898217
pubmed: 32922652
pmcid: 7453234
Seheult J, Fitzpatrick G, Boran G (2017) Lactic acidosis: an update. Clin Chem Lab Med 55(3):322–333
pubmed: 27522622
Selleri S, Bifsha P, Civini S, Pacelli C, Dieng MM, Lemieux W, Jin P, Bazin R, Patey N, Marincola FM, Moldovan F, Zaouter C, Trudeau LE, Benabdhalla B, Louis I, Beauséjour C, Stroncek D, Le Deist F, Haddad E (2016) Human mesenchymal stromal cell-secreted lactate induces M2-macrophage differentiation by metabolic reprogramming. Oncotarget 7(21):30193–30210
pubmed: 27070086
pmcid: 5058674
Smith WP (1996) Epidermal and dermal effects of topical lactic acid. J Am Acad Dermatol 35(3 Pt 1):388–391
pubmed: 8784274
Song J, Lee K, Park SW, Chung H, Jung D, Na YR, Quan H, Cho CS, Che JH, Kim JH, Park JH, Seok SH (2018) Lactic acid upregulates VEGF expression in macrophages and facilitates choroidal neovascularization. Invest Ophthalmol vis Sci 59(8):3747–3754
pubmed: 30046816
Sonveaux P, Copetti T, De Saedeleer CJ, Végran F, Verrax J, Kennedy KM, Moon EJ, Dhup S, Danhier P, Frérart F, Gallez B, Ribeiro A, Michiels C, Dewhirst MW, Feron O (2012) Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS ONE 7(3):e33418
pubmed: 22428047
pmcid: 3302812
Sreedhar A, Aguilera-Aguirre L, Singh KK (2020) Mitochondria in skin health, aging, and disease. Cell Death Dis 11(6):444
pubmed: 32518230
pmcid: 7283348
Srivastava S (2017) The mitochondrial basis of aging and age-related disorders. Genes (basel) 8(12):398
pubmed: 29257072
Stabenow LK, Zibrova D, Ender C, Helbing DL, Spengler K, Marx C, Wang ZQ, Heller R (2022) Oxidative glucose metabolism promotes senescence in vascular endothelial cells. Cells 11(14):2213
pubmed: 35883656
pmcid: 9322806
Stern R, Shuster S, Neudecker BA, Formby B (2002) Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res 276(1):24–31
pubmed: 11978005
Stout R, Birch-Machin M (2019) Mitochondria’s role in skin ageing. Biology (basel) 8(2):29
pubmed: 31083540
Su S, Ndiaye M, Singh CK, Ahmad N (2020) Mitochondrial sirtuins in skin and skin cancers. Photochem Photobiol 96(5):973–980
pubmed: 32124989
pmcid: 7483225
Summermatter S, Santos G, Pérez-Schindler J, Handschin C (2013) Skeletal muscle PGC-1α controls whole-body lactate homeostasis through estrogen-related receptor α-dependent activation of LDH B and repression of LDH A. Proc Natl Acad Sci USA 110(21):8738–8743
pubmed: 23650363
pmcid: 3666691
Sun N, Youle RJ, Finkel T (2016) The mitochondrial basis of aging. Mol Cell 61(5):654–666
pubmed: 26942670
pmcid: 4779179
Tower J (2015) Programmed cell death in aging. Ageing Res Rev 23(Pt A):90–100. https://doi.org/10.1016/j.arr.2015.04.002
doi: 10.1016/j.arr.2015.04.002
pubmed: 25862945
pmcid: 4480161
Tauffenberger A, Fiumelli H, Almustafa S, Magistretti PJ (2019) Lactate and pyruvate promote oxidative stress resistance through hormetic ROS signaling. Cell Death Dis 10(9):653
pubmed: 31506428
pmcid: 6737085
Tran D, Townley JP, Barnes TM, Greive KA (2014) An antiaging skin care system containing alpha hydroxy acids and vitamins improves the biomechanical parameters of facial skin. Clin Cosmet Investig Dermatol 8:9–17
pubmed: 25552908
pmcid: 4277239
Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly-Y M, Gidlöf S, Oldfors A, Wibom R, Törnell J, Jacobs HT, Larsson NG (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429(6990):417–423
pubmed: 15164064
Tuteja N, Chandra M, Tuteja R, Misra MK (2004) Nitric oxide as a unique bioactive signaling messenger in physiology and pathophysiology. J Biomed Biotechnol 2004(4):227–237
pubmed: 15467163
pmcid: 555773
Unternaehrer JJ, Zhao R, Kim K, Cesana M, Powers JT, Ratanasirintrawoot S, Onder T, Shibue T, Weinberg RA, Daley GQ (2014) The epithelial-mesenchymal transition factor SNAIL paradoxically enhances reprogramming. Stem Cell Rep 3(5):691–698
Valiente-Pallejà A, Torrell H, Alonso Y, Vilella E, Muntané G, Martorell L (2020) Increased blood lactate levels during exercise and mitochondrial DNA alterations converge on mitochondrial dysfunction in schizophrenia. Schizophr Res 220:61–68
pubmed: 32327316
Van Hall G (2000) Lactate as a fuel for mitochondrial respiration. Acta Physiol Scand 168(4):643–656
pubmed: 10759601
van Vliet AR, Agostinis P (2018) Mitochondria-associated membranes and ER stress. Curr Top Microbiol Immunol 414:73–102
pubmed: 28349285
van Vliet AR, Verfaillie T, Agostinis P (2014) New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta 1843(10):2253–2262
pubmed: 24642268
Veloz Castillo MF, Magistretti PJ, Calì C (2021) L-lactate: food for thoughts. Mem Behav Metab 11(8):548
Wallace NK, Pollard F, Savenkova M, Karatsoreos IN (2020) Effect of aging on daily rhythms of lactate metabolism in the medial prefrontal cortex of male mice. Neuroscience 448:300–310
pubmed: 32717298
Wagner S, Hussain MZ, Hunt TK, Bacic B, Becker HD (2004) Stimulation of fibroblast proliferation by lactate-mediated oxidants. Wound Repair Regen 12(3):368–373
pubmed: 15225216
Wei YH, Wu SB, Ma YS, Lee HC (2009) Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J 32(2):113–132
pubmed: 19403001
Wei X, Wu YE, Wang W, Zhang S, Liu D, Liu H (2021) Decreased dynamin-related protein 1-related mitophagy induces myocardial apoptosis in the aging heart. Acta Biochim Biophys Sin (shanghai). https://doi.org/10.1093/abbs/gmab112
doi: 10.1093/abbs/gmab112
pubmed: 34693451
Wu Y, Ma W, Liu W, Zhang S (2022) Lactate: a pearl dropped in the ocean: an overlooked signal molecule in physiology and pathology. Cell Biol Int. https://doi.org/10.1002/cbin.11975
doi: 10.1002/cbin.11975
pubmed: 36542640
pmcid: 9826031
Yin M, Zhang Y, Yu H, Li X (2021) Role of hyperglycemia in the senescence of mesenchymal stem cells. Front Cell Dev Biol 9:665412
pubmed: 33968939
pmcid: 8099107
Young A, Oldford C, Mailloux RJ (2020) Lactate dehydrogenase supports lactate oxidation in mitochondria isolated from different mouse tissues. Redox Biol 28:101339
pubmed: 31610469
Yu M (2012) Circulating cell-free mitochondrial DNA as a novel cancer biomarker: opportunities and challenges. Mitochondrial DNA 23(5):329–332
pubmed: 22775429
Zhang S, Duan E (2018) Fighting against skin aging: the way from bench to bedside. Cell Transplant 27(5):729–738
pubmed: 29692196
pmcid: 6047276
Zhang Y, Herman B (2002) Apoptosis and successful aging. Mech Ageing Dev 123(6):563–565
pubmed: 11850019
Zhang D, Lu H, Chen Z, Wang Y, Lin J, Xu S, Zhang C, Wang B, Yuan Z, Feng X, Jiang X, Pan J (2017) High glucose induces the aging of mesenchymal stem cells via Akt/mTOR signaling. Mol Med Rep 16(2):1685–1690
pubmed: 28656269
pmcid: 5562095
Zhang H, Menzies KJ, Auwerx J (2018) The role of mitochondria in stem cell fate and aging. Development 145(8):dev143420
pubmed: 29654217
pmcid: 5964648
Zhang D, Tang Z, Huang H, Zhou G, Cui C, Weng Y, Liu W, Kim S, Lee S, Perez-Neut M, Ding J, Czyz D, Hu R, Ye Z, He M, Zheng YG, Shuman HA, Dai L, Ren B, Roeder RG, Becker L, Zhao Y (2019) Metabolic regulation of gene expression by histone lactylation. Nature 574(7779):575–580
pubmed: 31645732
pmcid: 6818755
Zelenka J, Dvořák A, Alán L (2015) L-lactate protects skin fibroblasts against aging-associated mitochondrial dysfunction via mitohormesis. Oxid Med Cell Longev 2015:351698
pubmed: 26171114
pmcid: 4478408
Zieker D, Küper M, Löffler M, Northoff H, Königsrainer A, Hunt TK, Beckert S, (2009) Lactate induces collagen synthesis, VEGF expression and migration in endothelial cells via generation of superoxide. In: Schumpelick V, Bruch HP, Schackert HK (eds) Chirurgisches forum und DGAV forum 2009. Deutsche Gesellschaft für Chirurgie, vol 38. Springer, Berlin. https://doi.org/10.1007/978-3-642-00625-8_110
doi: 10.1007/978-3-642-00625-8_110