Carnosine and the processes of ageing

Maturitas

Volumn 93, Issue , 2016, Pages 28-33

  Hipkiss, Alan R ^a   Baye, Estifanos ^b   de Courten, Barbora ^b,c  

^a ASTON UNIVERSITY   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

^c SOUTHERN HEALTH   (Australia)

Author keywords

Advanced glycation end products; Ageing; Carnosine; Inflammation; Oxidative stress; Signalling pathways

Indexed keywords

4 HYDROXYNONENAL; ACROLEIN; ADVANCED GLYCATION END PRODUCT; CARNOSINE; GLYCERALDEHYDE 3 PHOSPHATE; INITIATION FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN; SMAD3 PROTEIN; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA; TRIOSEPHOSPHATE ISOMERASE;

AGING; ANTIOXIDANT ACTIVITY; APOPTOSIS; CELL DIVISION; DIET SUPPLEMENTATION; ENZYME INHIBITION; GLYCOLYSIS; HUMAN; INTRACELLULAR SIGNALING; LIPID PEROXIDATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; TELOMERE SHORTENING; ANIMAL; DIETARY SUPPLEMENT; INFLAMMATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGING; ANIMALS; CARNOSINE; DIETARY SUPPLEMENTS; HUMANS; INFLAMMATION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84991672210     PISSN: 03785122     EISSN: 18734111     Source Type: Journal    
DOI: 10.1016/j.maturitas.2016.06.002     Document Type: Review

References (75)

1. [1] Tosato, M., Zamboni, V., Ferrini, A., Cesari, M., The aging process and potential interventions to extend life expectancy. Clin. Interv. Aging 2:3 (2007), 401–412.
2. [2] Bauer, K., Carnosine and homocarnosine, the forgotten, enigmatic peptides of the brain. Neurochem. Res. 30:10 (2005), 1339–1345.
3. [3] Boldyrev, A.A., Aldini, G., Derave, W., Physiology and pathophysiology of carnosine. Physiol. Rev. 93:4 (2013), 1803–1845.
4. [4] Wu, J.W., Liu, K.N., How, S.C., Chen, W.A., Lai, C.M., Liu, H.S., Hu, C.J., Wang, S.S., Carnosine's effect on amyloid fibril formation and induced cytotoxicity of lysozyme. PLoS One, 8(12), 2013, e81982.
5. [5] Everaert, I., Mooyaart, A., Baguet, A., Zutinic, A., Baelde, H., Achten, E., Taes, Y., De Heer, E., Derave, W., Vegetarianism, female gender and increasing age, but not CNDP1 genotype, are associated with reduced muscle carnosine levels in humans. Amino Acids 40:4 (2011), 1221–1229.
6. [7] Everaert, I., Taes, Y., De Heer, E., Baelde, H., Zutinic, A., Yard, B., Sauerhofer, S., Vanhee, L., Delanghe, J., Aldini, G., Derave, W., Low plasma carnosinase activity promotes carnosinemia after carnosine ingestion in humans. Am. J. Physiol. Renal Physiol. 302:12 (2012), F1537–F1544.
7. [8] Min, J., Senut, M.C., Rajanikant, K., Greenberg, E., Bandagi, R., Zemke, D., Mousa, A., Kassab, M., Farooq, M.U., Gupta, R., Majid, A., Differential neuroprotective effects of carnosine, anserine, and N-acetyl carnosine against permanent focal ischemia. J. Neurosci. Res. 86:13 (2008), 2984–2991.
8. [9] Kohen, R., Yamamoto, Y., Cundy, K.C., Ames, B.N., Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc. Natl. Acad. Sci. U. S. A. 85:9 (1988), 3175–3179.
9. [10] Lee, J.W., Miyawaki, H., Bobst, E.V., Hester, J.D., Ashraf, M., Bobst, A.M., Improved functional recovery of ischemic rat hearts due to singlet oxygen scavengers histidine and carnosine. J. Mol. Cell. Cardiol. 31:1 (1999), 113–121.
10. [11] Brown, C.E., Interactions among carnosine, anserine, ophidine and copper in biochemical adaptation. J. Theor. Biol. 88:2 (1981), 245–256.
11. [12] Davey, C.L., The effects of carnosine and anserine on glycolytic reactions in skeletal muscle. Arch. Biochem. Biophys. 89 (1960), 296–302.
12. [13] Boldyrev, A.A., Gallant, S.C., Sukhich, G.T., Carnosine, the protective, anti-aging peptide. Biosci. Rep. 19:6 (1999), 581–587.
13. [14] Hipkiss, A.R., Carnosine, a protective, anti-ageing peptide?. Int. J. Biochem. Cell Biol. 30:8 (1998), 863–868.
14. [15] Gallant, S., Semyonova, M., Yuneva, M., Carnosine as a potential anti-senescence drug. Biochemistry (Mosc.) 65:7 (2000), 866–868.
15. [16] Yuneva, M., Bulygina, E., Gallant, S., Kramarenko, G., Stvolinsky, S., Semyonova, M., Boldyrev, A., Effect of carnosine on age-Induced changes in senescence-Accelerated mice. J. Antiaging Med. 2:4 (1999), 337–342.
16. [17] Gopko, A.V., Kulibin, A.Y., Semenova, M.L., Zakhidov, S.T., Carnosine-induced changes in the development of spermatogenic epithelial cells in senescence accelerated SAM mice. Bull. Exp. Biol. Med. 140:2 (2005), 235–237.
17. [18] McFarland, G.A., Holliday, R., Retardation of the senescence of cultured human diploid fibroblasts by carnosine. Exp. Cell Res. 212:2 (1994), 167–175.
18. [19] McFarland, G.A., Holliday, R., Further evidence for the rejuvenating effects of the dipeptide L-carnosine on cultured human diploid fibroblasts. Exp. Gerontol. 34:1 (1999), 35–45.
19. [20] Boldyrev, A.A., Yuneva, M.O., Sorokina, E.V., Kramarenko, G.G., Fedorova, T.N., Konovalova, G.G., Lankin, V.Z., Antioxidant systems in tissues of senescence accelerated mice. Biochemistry (Mosc.) 66:10 (2001), 1157–1163.
20. [21] de Courten, B., Jakubova, M., de Courten, M.P., Kukurova, I.J., Vallova, S., Krumpolec, P., Valkovic, L., Kurdiova, T., Garzon, D., Barbaresi, S., Teede, H.J., Derave, W., Krssak, M., Aldini, G., Ukropec, J., Ukropcova, B., Effects of carnosine supplementation on glucose metabolism: pilot clinical trial. Obesity (Silver Spring) 24:5 (2016), 1027–1034.
21. [22] Menini, S., Iacobini, C., Ricci, C., Blasetti Fantauzzi, C., Pugliese, G., Protection from diabetes-induced atherosclerosis and renal disease by D-carnosine-octylester: effects of early vs late inhibition of advanced glycation end-products in Apoe-null mice. Diabetologia 58:4 (2015), 845–853.
22. [23] Brown, B.E., Kim, C.H., Torpy, F.R., Bursill, C.A., McRobb, L.S., Heather, A.K., Davies, M.J., van Reyk, D.M., Supplementation with carnosine decreases plasma triglycerides and modulates atherosclerotic plaque composition in diabetic apo E(−/−) mice. Atherosclerosis 232:2 (2014), 403–409.
23. [24] Aloisi, A., Barca, A., Romano, A., Guerrieri, S., Storelli, C., Rinaldi, R., Verri, T., Anti-aggregating effect of the naturally occurring dipeptide carnosine on abeta1-42 fibril formation. PLoS One, 8(7), 2013, e68159.
24. [25] Boldyrev, A., Fedorova, T., Stepanova, M., Dobrotvorskaya, I., Kozlova, E., Boldanova, N., Bagyeva, G., Ivanova-Smolenskaya, I., Illarioshkin, S., Carnosine [corrected] increases efficiency of DOPA therapy of Parkinson's disease: a pilot study. [Erratum appears in Rejuvenation Res. 2008 Oct;11(5):988]. Rejuvenation Res. 11:4 (2008), 821–827.
25. [26] Ansurudeen, I., Sunkari, V.G., Grunler, J., Peters, V., Schmitt, C.P., Catrina, S.B., Brismar, K., Forsberg, E.A., Carnosine enhances diabetic wound healing in the db/db mouse model of type 2 diabetes. Amino Acids 43:1 (2012), 127–134.
26. [27] Hisatsune, T., Kaneko, J., Kurashige, H., Cao, Y., Satsu, H., Totsuka, M., Katakura, Y., Imabayashi, E., Matsuda, H., Effect of anserine/carnosine supplementation on verbal episodic memory in elderly people. J. Alzheimers Dis. 50:1 (2015), 149–159.
27. [28] Lombardi, C., Carubelli, V., Lazzarini, V., Vizzardi, E., Bordonali, T., Ciccarese, C., Castrini, A.I., Dei Cas, A., Nodari, S., Metra, M., Effects of oral administration of orodispersible levo-carnosine on quality of life and exercise performance in patients with chronic heart failure. Nutrition 31:1 (2015), 72–78.
28. [29] Rokicki, J., Li, L., Imabayashi, E., Kaneko, J., Hisatsune, T., Matsuda, H., Daily carnosine and anserine supplementation alters verbal episodic memory and resting state network connectivity in healthy elderly adults. Front. Aging Neurosci., 7, 2015, 219.
29. [30] Szczesniak, D., Budzen, S., Kopec, W., Rymaszewska, J., Anserine and carnosine supplementation in the elderly: effects on cognitive functioning and physical capacity. Arch. Gerontol. Geriatr. 59:2 (2014), 485–490.
30. [31] Baraniuk, J.N., El-Amin, S., Corey, R., Rayhan, R., Timbol, C., Carnosine treatment for gulf war illness: a randomized controlled trial. Global J. Health Sci. 5:3 (2013), 69–81.
31. [32] Chengappa, K.N., Turkin, S.R., DeSanti, S., Bowie, C.R., Brar, J.S., Schlicht, P.J., Murphy, S.L., Hetrick, M.L., Bilder, R., Fleet, D., A preliminary randomized, double-blind, placebo-controlled trial of L-carnosine to improve cognition in schizophrenia. Schizophr. Res. 142:1–3 (2012), 145–152.
32. [33] Renner, C., Asperger, A., Seyffarth, A., Meixensberger, J., Gebhardt, R., Gaunitz, F., Carnosine inhibits ATP production in cells from malignant glioma. Neurol. Res. 32:1 (2010), 101–105.
33. [34] Ishikawa, N., Nakamura, K., Izumiyama-Shimomura, N., Aida, J., Matsuda, Y., Arai, T., Takubo, K., Changes of telomere status with aging: an update. Geriatr. Gerontol. Int. 16:Suppl. 1 (2016), 30–42.
34. [35] Shao, L., Li, Q.H., Tan, Z., L-carnosine reduces telomere damage and shortening rate in cultured normal fibroblasts. Biochem. Biophys. Res. Commun. 324:2 (2004), 931–936.
35. [36] Allaman, I., Belanger, M., Magistretti, P.J., Methylglyoxal, the dark side of glycolysis. Front. Neurosci., 9, 2015, 23.
36. [37] Vistoli, G., De Maddis, D., Cipak, A., Zarkovic, N., Carini, M., Aldini, G., Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic. Res. 47:Suppl. 1 (2013), 3–27.
37. [38] Hipkiss, A.R., Michaelis, J., Syrris, P., Non-enzymatic glycosylation of the dipeptide L-carnosine, a potential anti-protein-cross-linking agent. FEBS Lett. 371:1 (1995), 81–85.
38. [39] Aldini, G., Orioli, M., Rossoni, G., Savi, F., Braidotti, P., Vistoli, G., Yeum, K.J., Negrisoli, G., Carini, M., The carbonyl scavenger carnosine ameliorates dyslipidaemia and renal function in Zucker obese rats. J. Cell. Mol. Med. 15:6 (2011), 1339–1354.
39. [40] Bispo, V.S., de Arruda Campos, I.P., Di Mascio, P., Medeiros, M.H., Structural elucidation of a carnosine-acrolein adduct and its quantification in human urine samples. Sci. Rep., 6, 2016, 19348.
40. [41] Brownson, C., Hipkiss, A.R., Carnosine reacts with a glycated protein. Free Radic. Biol. Med. 28:10 (2000), 1564–1570.
41. [42] Schroder, L., Schmitz, C.H., Bachert, P., Carnosine as molecular probe for sensitive detection of Cu(II) ions using localized 1H NMR spectroscopy. J. Inorg. Biochem. 102:2 (2008), 174–183.
42. [43] Ingram, D.K., Roth, G.S., Glycolytic inhibition as a strategy for developing calorie restriction mimetics. Exp. Gerontol. 46:2–3 (2011), 148–154.
43. [44] Asperger, A., Renner, C., Menzel, M., Gebhardt, R., Meixensberger, J., Gaunitz, F., Identification of factors involved in the anti-tumor activity of carnosine on glioblastomas using a proteomics approach. Cancer Invest. 29:4 (2011), 272–281.
44. [45] Iovine, B., Iannella, M.L., Nocella, F., Pricolo, M.R., Bevilacqua, M.A., Carnosine inhibits KRAS-mediated HCT116 proliferation by affecting ATP and ROS production. Cancer Lett. 315:2 (2012), 122–128.
45. [46] Cartwright, S.P., Bill, R.M., Hipkiss, A.R., L-carnosine affects the growth of Saccharomyces cerevisiae in a metabolism-dependent manner. PLoS One, 7(9), 2012, e45006 [Electronic Resource].
46. [47] Baek, S.H., Noh, A.R., Kim, K.A., Akram, M., Shin, Y.J., Kim, E.S., Yu, S.W., Majid, A., Bae, O.N., Modulation of mitochondrial function and autophagy mediates carnosine neuroprotection against ischemic brain damage. Stroke 45:8 (2014), 2438–2443.
47. [48] Holliday, R., McFarland, G.A., Inhibition of the growth of transformed and neoplastic cells by the dipeptide carnosine. Br. J. Cancer 73:8 (1996), 966–971.
48. [49] Gracy, R.W., Talent, J.M., Zvaigzne, A.I., Molecular wear and tear leads to terminal marking and the unstable isoforms of aging. J. Exp. Zool. 282:1–2 (1998), 18–27.
49. [50] Hipkiss, A.R., Energy metabolism and ageing regulation: metabolically driven deamidation of triosephosphate isomerase may contribute to proteostatic dysfunction. Ageing Res. Rev. 10:4 (2011), 498–502.
50. [51] Tajes, M., Eraso-Pichot, A., Rubio-Moscardo, F., Guivernau, B., Ramos-Fernandez, E., Bosch-Morato, M., Guix, F.X., Clarimon, J., Miscione, G.P., Boada, M., Gil-Gomez, G., Suzuki, T., Molina, H., Villa-Freixa, J., Vicente, R., Munoz, F.J., Methylglyoxal produced by amyloid-beta peptide-induced nitrotyrosination of triosephosphate isomerase triggers neuronal death in Alzheimer's disease. J. Alzheimers Dis. 41:1 (2014), 273–288.
51. [52] Crescenzo, R., Bianco, F., Mazzoli, A., Giacco, A., Liverini, G., Iossa, S., Skeletal muscle mitochondrial energetic efficiency and aging. Int. J. Mol. Sci. 16:5 (2015), 10674–10685.
52. [53] Walters, H.E., Deneka-Hannemann, S., Cox, L.S., Reversal of phenotypes of cellular senescence by pan-mTOR inhibition. Aging (Albany NY) 8:2 (2016), 231–244.
53. [54] Hipkiss, A.R., Energy metabolism proteotoxic stress and age-related dysfunction—protection by carnosine. Mol. Aspects Med. 32:4–6 (2011), 267–278.
54. [55] Zhang, Z., Miao, L., Wu, X., Liu, G., Peng, Y., Xin, X., Jiao, B., Kong, X., Carnosine inhibits the proliferation of human gastric carcinoma cells by retarding Akt/mTOR/p70S6K signaling. J. Cancer 5:5 (2014), 382–389.
55. [56] Roberts, A.B., Wakefield, L.M., The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:15 (2003), 8621–8623.
56. [57] Bauge, C., Duval, E., Ollitrault, D., Girard, N., Leclercq, S., Galera, P., Boumediene, K., Type II TGFbeta receptor modulates chondrocyte phenotype. Age (Dordr.) 35:4 (2013), 1105–1116.
57. [58] Doyle, K.P., Cekanaviciute, E., Mamer, L.E., Buckwalter, M.S., TGFbeta signaling in the brain increases with aging and signals to astrocytes and innate immune cells in the weeks after stroke. J. Neuroinflammation, 7, 2010, 62.
58. [59] Bayne, S., Liu, J.P., Hormones and growth factors regulate telomerase activity in ageing and cancer. Mol. Cell. Endocrinol. 240:1–2 (2005), 11–22.
59. [60] Koppel, H., Riedl, E., Braunagel, M., Sauerhoefer, S., Ehnert, S., Godoy, P., Sternik, P., Dooley, S., Yard, B.A., L-carnosine inhibits high-glucose-mediated matrix accumulation in human mesangial cells by interfering with TGF-beta production and signalling. Nephrol. Dial. Transplant. 26:12 (2011), 3852–3858.
60. [61] Baye, E., Ukropcova, B., Ukropec, J., Hipkiss, A., Aldini, G., de Courten, B., Physiological and therapeutic effects of carnosine on cardiometabolic risk and disease. Amino Acids 48:5 (2016), 1131–1149.
61. [62] Higashi, Y., Sukhanov, S., Anwar, A., Shai, S.Y., Delafontaine, P., Aging, atherosclerosis, and IGF-1. J. Gerontol. A Biol. Sci. Med. Sci. 67:6 (2012), 626–639.
62. [63] Noordam, R., Gunn, D.A., Tomlin, C.C., Maier, A.B., Griffiths, T., Catt, S.D., Ogden, S., Slagboom, P.E., Westendorp, R.G., Griffiths, C.E., van Heemst, D., de Craen, A.J., Serum insulin-like growth factor 1 and facial ageing: high levels associate with reduced skin wrinkling in a cross-sectional study. Br. J. Dermatol. 168:3 (2013), 533–538.
63. [64] Forsberg, E.A., Botusan, I.R., Wang, J., Peters, V., Ansurudeen, I., Brismar, K., Catrina, S.B., Carnosine decreases IGFBP1 production in db/db mice through suppression of HIF-1. J. Endocrinol. 225:3 (2015), 159–167.
64. [65] Hipkiss, A.R., Accumulation of altered proteins and ageing: causes and effects. Exp. Gerontol. 41:5 (2006), 464–473.
65. [66] Hipkiss, A.R., Brownson, C., Bertani, M.F., Ruiz, E., Ferro, A., Reaction of carnosine with aged proteins: another protective process?. Ann. N. Y. Acad. Sci. 959 (2002), 285–294.
66. [67] Koziel, R., Ruckenstuhl, C., Albertini, E., Neuhaus, M., Netzberger, C., Bust, M., Madeo, F., Wiesner, R.J., Jansen-Durr, P., Methionine restriction slows down senescence in human diploid fibroblasts. Aging Cell 13:6 (2014), 1038–1048.
67. [68] Howard, A., Rogers, A.N., Role of translation initiation factor 4G in lifespan regulation and age-related health. Ageing Res. Rev. 13 (2014), 115–124.
68. [69] Harris, R.P., Kilby, P.M., Amino acid misincorporation in recombinant biopharmaceutical products. Curr. Opin. Biotechnol. 30 (2014), 45–50.
69. [70] Hipkiss, A.R., On methionine restriction, suppression of mitochondrial dysfunction and aging. Rejuvenation Res. 11:3 (2008), 685–688.
70. [71] Hipkiss, A.R., Can the beneficial effects of methionine restriction in rats be explained in part by decreased methylglyoxal generation resulting from suppressed carbohydrate metabolism?. Biogerontology 13:6 (2012), 633–636.
71. [72] Son, D.O., Satsu, H., Kiso, Y., Totsuka, M., Shimizu, M., Inhibitory effect of carnosine on interleukin-8 production in intestinal epithelial cells through translational regulation. Cytokine 42:2 (2008), 265–276.
72. [73] Zhang, Z.Y., Sun, B.L., Yang, M.F., Li, D.W., Fang, J., Zhang, S., Carnosine attenuates early brain injury through its antioxidative and anti-apoptotic effects in a rat experimental subarachnoid hemorrhage model. Cell. Mol. Neurobiol. 35:2 (2015), 147–157.
73. [74] Mikula-Pietrasik, J., Ksiazek, K., L-Carnosine prevents the pro-cancerogenic activity of senescent peritoneal mesothelium towards ovarian cancer cells. Anticancer Res. 36:2 (2016), 665–671.
74. [75] Baker, D.J., Childs, B.G., Durik, M., Wijers, M.E., Sieben, C.J., Zhong, J., Saltness, R.A., Jeganathan, K.B., Verzosa, G.C., Pezeshki, A., Khazaie, K., Miller, J.D., van Deursen, J.M., Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 530:7589 (2016), 184–189.
75. [76] Verdin, E., NAD(+) in aging, metabolism, and neurodegeneration. Science 350:6265 (2015), 1208–1213.