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Apis mellifera y miRNAs: modelo natural de longevidad y una perspectiva hologenómica del envejecimiento954 Modelo natural de longevidad y una perspectiva hologenómica del envejecimiento
Publicado:
nov 10, 2021
Palabras clave:
Hologenómica; microbiota; longevidad; microRNAs
Contenido principal del artículo
Resumen
La longevidad de un organismo se favorece cuando existe una adecuada homeostasis entre el huésped y su microbiota intestinal. Existen pocos alimentos con la capacidad de extender el tiempo de vida útil de un organismo, la Jalea Real (JR) en la abeja Apis mellifera es uno de ellos. El potencial nutriepigenético de la JR se encuentra en sus componentes protéicos, ácidos grasos, metabolitos y microRNAs (miRNAs) que la hacen un nutracéutico importante. En esta revisión abordamos un enfoque hologenómico del proceso de envejecimiento y longevidad haciendo énfasis en el uso de los miRNAs presentes en la JR y la posible modulación que éstos podrían tener sobre la microbiota intestinal.
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Roque Ramírez, B. (2021). Apis mellifera y miRNAs: modelo natural de longevidad y una perspectiva hologenómica del envejecimiento: Modelo natural de longevidad y una perspectiva hologenómica del envejecimiento. Revista Del Centro De Investigación De La Universidad La Salle, 14(56), 113–122. https://doi.org/10.26457/recein.v14i56.2860
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Ameling S, Kacprowski T, Chilukoti RK et al. (2015). Associations of circulating plasma microRNAs with age, body mass index and sex in a population-based study. BMC Med Genomics 8:61.
Anderson KE, Ricigliano VA, Mott BM, Copeland DC, Floyd AS, Maes P. (2018). The queen's gut refines with age: longevity phenotypes in a social insect model. Microbiome. 6(1): 108.
Azevedo SV, Hartfelder K. (2008). The insulin signaling pathway in honey bee (Apis mellifera) caste development - differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J Insect Physiol. 54(6):1064-71.
Badal VD, Vaccariello ED, Murray ER, Yu KE, Knight R, Jeste DV, Nguyen TT. (2020). The Gut Microbiome, Aging, and Longevity: A Systematic Review. Nutrients. 12(12): 3759.
Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simões ZL, et al. (2007). Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol. 7:70.
Behrouzi A, Ashrafian F, Mazaheri H, Lari A, Nouri M, Riazi Rad F, Hoseini Tavassol Z, Siadat SD. (2020). The importance of interaction between MicroRNAs and gut microbiota in several pathways. Microb Pathog. 144: 104200.
Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, Capri M, Brigidi P, Candela M. (2016). Gut Microbiota and Extreme Longevity. Curr Biol. 26:1480–1485.
Bitar A, Aung KM, Wai SN, Hammarström ML. (2019). Vibrio cholerae derived outer membrane vesicles modulate the inflammatory response of human intestinal epithelial cells by inducing microRNA-146a. Sci Rep. 10;9(1):7212.
Biton M, Levin A, Slyper M, Alkalay I, Horwitz E, Mor H, Kredo-Russo S, Avnit-Sagi T, Cojocaru G, Zreik F, Bentwich Z, Poy MN, Artis D, Walker MD, Hornstein E, Pikarsky E, Ben-Neriah Y. (2011). Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol. 12(3): 239-46.
Bordone L, Guarente L. (2005). Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol. 6(4):298-305.
Cornara L, Biagi M, Xiao J, Burlando B. (2017). Therapeutic Properties of Bioactive Compounds from Different Honeybee Products. Front Pharmacol 8:412.
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, et al. (2007). Hughes KA, Robinson GE. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A. 104(17):7128-33.
Cridge AG, Lovegrove MR, Skelly JG, Taylor SE, Petersen GEL, et al. (2017). The honeybee as a model insect for developmental genetics. Genesis. 55(5).
D'Antona G, Ragni M, Cardile A, Tedesco L, Dossena M, Bruttini F, Caliaro F, Corsetti G, Bottinelli R, Carruba MO, Valerio A, Nisoli E. (2010). Branched-chain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middle-aged mice. Cell Metab. 12(4):362-372.
De Lencastre, A., Pincus, Z., Zhou, K., Kato, M., Lee, S. S., & Slack, F. J. (2010). MicroRNAs both promote and antagonize longevity in C. elegans. Current Biology, 20(24), 2159-2168.
Driver C, Georgeou A. (2003). Variable effects of vitamin E on Drosophila longevity. Biogerontology. 4(2):91-5.
Ferrucci, L.; Fabbri, E. (2018). Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat. Rev. Cardiol. 15, 505–522.
Guo, X., Su, S., Skogerboe, G., Dai, S., Li, W., Li, Z., Chen, R. (2013). Recipe for a Busy Bee: MicroRNAs in Honey Bee Caste Determination. PLoS ONE. 8(12), e81661.
Henagan TM, Stefanska B, Fang Z, Navard AM, Ye J, Lenard NR, Devarshi PP. (2015). Sodium butyrate epigenetically modulates high-fat diet-induced skeletal muscle mitochondrial adaptation, obesity and insulin resistance through nucleosome positioning. Br J Pharmacol. 172(11):2782-98.
Honda Y, Fujita Y, Maruyama H, Araki Y, Ichihara K, Sato A, Kojima T, Tanaka M, Nozawa Y, Ito M, Honda S. (2011). Lifespan-extending effects of royal jelly and its related substances on the nematode Caenorhabditis elegans. PLoS One. ;6(8): 23527.
Hooten NN, Fitzpatrick M, Wood WH et al. (2013). Age-related changes in microRNA levels in serum. Aging (Albany NY) 5:725–740.
Kenyon CJ. (2010). The genetics of ageing. Nature. 225;464(7288):504-12. Review. Erratum in: Nature. 2010 Sep 30;467(7315):622.
Kenyon C. (2005). The plasticity of aging: insights from long-lived mutants. Cell. 25;120(4):449-60.
Kim M, Benayoun BA. (2020). The microbiome: an emerging key player in aging and longevity. Transl Med Aging. 4: 103-116.
Kolayli S, Sahin H, Can Z, Yildiz O, Malkoc M, Asadov A. (2016). A Member of Complementary Medicinal Food: Anatolian Royal Jellies, Their Chemical Compositions, and Antioxidant Properties. J Evid Based Complementary Altern Med. (4):NP43-8.
Kucharski R, Maleszka J, Foret S, Maleszka R. (2008). Nutritional control of reproductive status in honeybees via DNA methylation. Science. 319(5871):1827-30.
Lee S, Jung JW, Park SB, Roh K, Lee SY, Kim JH, Kang SK, Kang KS. (2011). Histone deacetylase regulates high mobility group A2-targeting microRNAs in human cord blood-derived multipotent stem cell aging. Cell Mol Life Sci. 68(2):325-36.
Leimar O, Hartfelder K, Laubichler MD, Page RE Jr. (2012). Development and evolution of caste dimorphism in honeybees - a modeling approach. Ecol Evol. (12):3098-109.
Lithgow GJ, White TM, Melov S, Johnson TE. (1995). Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci U S A. 1;92(16):7540-4.
Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, Comstock LE, Gandhi R, Weiner HL. (2016). The Host Shapes the Gut Microbiota via Fecal MicroRNA. Cell Host Microbe. Jan 13;19(1): 32-43.
López-Otín, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. (2013). The Hallmarks of Aging. Cell. 153, 1194–1217.
Maori, E., Garbian, Y., Kunik, V., Mozes-Koch, R., Malka, O., Kalev, H., Shafir, S. A (2019). Transmissible RNA Pathway in Honey Bee. Cell Reports. 27(7), 1949–1959.
Nishino J, Kim I, Chada K, Morrison SJ. (2008). Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell. 135(2):227-39.
Painter TS. (1969). The origin of the nucleic Acid bases found in the royal jelly of the honeybee. Proc Natl Acad Sci U S A. 64(1):64-6.
Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, Frederick K, Amdam GV. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS One. 2(6): e509
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Meta HITC, Bork P, Ehrlich SD, Wang J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature.; 464:59–65.
Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. (2016). Bifidobacteria and butyrate- producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 7:979.
Smith-Vikos T, Liu Z, Parsons C et al. (2016) A serum miRNA profile of human longevity: findings from the Baltimore Longitudinal Study of Aging (BLSA). Aging (Albany NY) 8:2971–2987.
Soukas AA, Kane EA, Carr CE, Melo JA, Ruvkun G. (2009). Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev. 23(4):496-511.
Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, et al. (2011). Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. (3):238-43.
Tarpy DR, Mattila HR, Newton ILG. (2015). Development of the honey bee gut microbiome throughout the queen-rearing process. Appl Environ Microbiol. 81:3182–91.
Teng Y, Ren Y, Sayed M, Hu X, Lei C, Kumar A, Hutchins E, Mu J, Deng Z, Luo C, Sundaram K, Sriwastva MK, Zhang L, Hsieh M, Reiman R, Haribabu B, Yan J, Jala VR, Miller DM, Van Keuren-Jensen K, Merchant ML, McClain CJ, Park JW, Egilmez NK, Zhang HG. (2018). Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota. Cell Host Microbe. Nov 14;24(5): 637-652.e8.
Toledano H, D'Alterio C, Czech B, Levine E, Jones DL. (2012). The let-7-Imp axis regulates ageing of the Drosophila testis stem-cell niche. Nature. 485(7400):605-10.
Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, Benes V, Blake J, Pfister S, Eckstein V, Ho AD. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One. 3(5): e2213.
Wang JJ, Li SH, Li AL, Zhang QM, Ni WW, Li MN, Meng XC, Li C, Jiang SL, Pan JC, Li YY. (2018). Effect of Lactobacillus acidophilus KLDS 1.0738 on miRNA expression in in vitro and in vivo models of β-lactoglobulin allergy. Biosci Biotechnol Biochem. 82(11): 1955-1963.
Wang Y, Jorda M, Jones PL, Maleszka R, Ling X, Robertson HM, et al. (2006). Functional CpG methylation system in a social insect. Science. 2006 314(5799):645-7.
Yu JM, Wu X, Gimble JM, Guan X, Freitas MA, Bunnell BA. (2011). Age-related changes in mesenchymal stem cells derived from rhesus macaque bone marrow. Aging Cell. (1):66-79.
Zhang H, Yang H, Zhang C et al. (2015) Investigation of microRNA expression in human serum during the aging process. J Gerontol Ser A 70:102–109.
Zhu K, Liu M, Fu Z, Zhou Z, Kong Y, Liang H, Lin Z, Luo J, et al. (2017). Plant microRNAs in larval food regulate honeybee caste development. PLoS Genet.13(8): e1006946.
Zou S, Sinclair J, Wilson MA, Carey JR, Liedo P, Oropeza A, et al. (2007). Comparative approaches to facilitate the discovery of prolongevity interventions: effects of tocopherols on lifespan of three invertebrate species. Mech Ageing Dev. 128(2):222-6.
Anderson KE, Ricigliano VA, Mott BM, Copeland DC, Floyd AS, Maes P. (2018). The queen's gut refines with age: longevity phenotypes in a social insect model. Microbiome. 6(1): 108.
Azevedo SV, Hartfelder K. (2008). The insulin signaling pathway in honey bee (Apis mellifera) caste development - differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J Insect Physiol. 54(6):1064-71.
Badal VD, Vaccariello ED, Murray ER, Yu KE, Knight R, Jeste DV, Nguyen TT. (2020). The Gut Microbiome, Aging, and Longevity: A Systematic Review. Nutrients. 12(12): 3759.
Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simões ZL, et al. (2007). Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol. 7:70.
Behrouzi A, Ashrafian F, Mazaheri H, Lari A, Nouri M, Riazi Rad F, Hoseini Tavassol Z, Siadat SD. (2020). The importance of interaction between MicroRNAs and gut microbiota in several pathways. Microb Pathog. 144: 104200.
Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, Capri M, Brigidi P, Candela M. (2016). Gut Microbiota and Extreme Longevity. Curr Biol. 26:1480–1485.
Bitar A, Aung KM, Wai SN, Hammarström ML. (2019). Vibrio cholerae derived outer membrane vesicles modulate the inflammatory response of human intestinal epithelial cells by inducing microRNA-146a. Sci Rep. 10;9(1):7212.
Biton M, Levin A, Slyper M, Alkalay I, Horwitz E, Mor H, Kredo-Russo S, Avnit-Sagi T, Cojocaru G, Zreik F, Bentwich Z, Poy MN, Artis D, Walker MD, Hornstein E, Pikarsky E, Ben-Neriah Y. (2011). Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol. 12(3): 239-46.
Bordone L, Guarente L. (2005). Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol. 6(4):298-305.
Cornara L, Biagi M, Xiao J, Burlando B. (2017). Therapeutic Properties of Bioactive Compounds from Different Honeybee Products. Front Pharmacol 8:412.
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, et al. (2007). Hughes KA, Robinson GE. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A. 104(17):7128-33.
Cridge AG, Lovegrove MR, Skelly JG, Taylor SE, Petersen GEL, et al. (2017). The honeybee as a model insect for developmental genetics. Genesis. 55(5).
D'Antona G, Ragni M, Cardile A, Tedesco L, Dossena M, Bruttini F, Caliaro F, Corsetti G, Bottinelli R, Carruba MO, Valerio A, Nisoli E. (2010). Branched-chain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middle-aged mice. Cell Metab. 12(4):362-372.
De Lencastre, A., Pincus, Z., Zhou, K., Kato, M., Lee, S. S., & Slack, F. J. (2010). MicroRNAs both promote and antagonize longevity in C. elegans. Current Biology, 20(24), 2159-2168.
Driver C, Georgeou A. (2003). Variable effects of vitamin E on Drosophila longevity. Biogerontology. 4(2):91-5.
Ferrucci, L.; Fabbri, E. (2018). Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat. Rev. Cardiol. 15, 505–522.
Guo, X., Su, S., Skogerboe, G., Dai, S., Li, W., Li, Z., Chen, R. (2013). Recipe for a Busy Bee: MicroRNAs in Honey Bee Caste Determination. PLoS ONE. 8(12), e81661.
Henagan TM, Stefanska B, Fang Z, Navard AM, Ye J, Lenard NR, Devarshi PP. (2015). Sodium butyrate epigenetically modulates high-fat diet-induced skeletal muscle mitochondrial adaptation, obesity and insulin resistance through nucleosome positioning. Br J Pharmacol. 172(11):2782-98.
Honda Y, Fujita Y, Maruyama H, Araki Y, Ichihara K, Sato A, Kojima T, Tanaka M, Nozawa Y, Ito M, Honda S. (2011). Lifespan-extending effects of royal jelly and its related substances on the nematode Caenorhabditis elegans. PLoS One. ;6(8): 23527.
Hooten NN, Fitzpatrick M, Wood WH et al. (2013). Age-related changes in microRNA levels in serum. Aging (Albany NY) 5:725–740.
Kenyon CJ. (2010). The genetics of ageing. Nature. 225;464(7288):504-12. Review. Erratum in: Nature. 2010 Sep 30;467(7315):622.
Kenyon C. (2005). The plasticity of aging: insights from long-lived mutants. Cell. 25;120(4):449-60.
Kim M, Benayoun BA. (2020). The microbiome: an emerging key player in aging and longevity. Transl Med Aging. 4: 103-116.
Kolayli S, Sahin H, Can Z, Yildiz O, Malkoc M, Asadov A. (2016). A Member of Complementary Medicinal Food: Anatolian Royal Jellies, Their Chemical Compositions, and Antioxidant Properties. J Evid Based Complementary Altern Med. (4):NP43-8.
Kucharski R, Maleszka J, Foret S, Maleszka R. (2008). Nutritional control of reproductive status in honeybees via DNA methylation. Science. 319(5871):1827-30.
Lee S, Jung JW, Park SB, Roh K, Lee SY, Kim JH, Kang SK, Kang KS. (2011). Histone deacetylase regulates high mobility group A2-targeting microRNAs in human cord blood-derived multipotent stem cell aging. Cell Mol Life Sci. 68(2):325-36.
Leimar O, Hartfelder K, Laubichler MD, Page RE Jr. (2012). Development and evolution of caste dimorphism in honeybees - a modeling approach. Ecol Evol. (12):3098-109.
Lithgow GJ, White TM, Melov S, Johnson TE. (1995). Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci U S A. 1;92(16):7540-4.
Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, Comstock LE, Gandhi R, Weiner HL. (2016). The Host Shapes the Gut Microbiota via Fecal MicroRNA. Cell Host Microbe. Jan 13;19(1): 32-43.
López-Otín, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. (2013). The Hallmarks of Aging. Cell. 153, 1194–1217.
Maori, E., Garbian, Y., Kunik, V., Mozes-Koch, R., Malka, O., Kalev, H., Shafir, S. A (2019). Transmissible RNA Pathway in Honey Bee. Cell Reports. 27(7), 1949–1959.
Nishino J, Kim I, Chada K, Morrison SJ. (2008). Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell. 135(2):227-39.
Painter TS. (1969). The origin of the nucleic Acid bases found in the royal jelly of the honeybee. Proc Natl Acad Sci U S A. 64(1):64-6.
Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, Frederick K, Amdam GV. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS One. 2(6): e509
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Meta HITC, Bork P, Ehrlich SD, Wang J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature.; 464:59–65.
Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. (2016). Bifidobacteria and butyrate- producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 7:979.
Smith-Vikos T, Liu Z, Parsons C et al. (2016) A serum miRNA profile of human longevity: findings from the Baltimore Longitudinal Study of Aging (BLSA). Aging (Albany NY) 8:2971–2987.
Soukas AA, Kane EA, Carr CE, Melo JA, Ruvkun G. (2009). Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev. 23(4):496-511.
Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, et al. (2011). Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. (3):238-43.
Tarpy DR, Mattila HR, Newton ILG. (2015). Development of the honey bee gut microbiome throughout the queen-rearing process. Appl Environ Microbiol. 81:3182–91.
Teng Y, Ren Y, Sayed M, Hu X, Lei C, Kumar A, Hutchins E, Mu J, Deng Z, Luo C, Sundaram K, Sriwastva MK, Zhang L, Hsieh M, Reiman R, Haribabu B, Yan J, Jala VR, Miller DM, Van Keuren-Jensen K, Merchant ML, McClain CJ, Park JW, Egilmez NK, Zhang HG. (2018). Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota. Cell Host Microbe. Nov 14;24(5): 637-652.e8.
Toledano H, D'Alterio C, Czech B, Levine E, Jones DL. (2012). The let-7-Imp axis regulates ageing of the Drosophila testis stem-cell niche. Nature. 485(7400):605-10.
Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, Benes V, Blake J, Pfister S, Eckstein V, Ho AD. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One. 3(5): e2213.
Wang JJ, Li SH, Li AL, Zhang QM, Ni WW, Li MN, Meng XC, Li C, Jiang SL, Pan JC, Li YY. (2018). Effect of Lactobacillus acidophilus KLDS 1.0738 on miRNA expression in in vitro and in vivo models of β-lactoglobulin allergy. Biosci Biotechnol Biochem. 82(11): 1955-1963.
Wang Y, Jorda M, Jones PL, Maleszka R, Ling X, Robertson HM, et al. (2006). Functional CpG methylation system in a social insect. Science. 2006 314(5799):645-7.
Yu JM, Wu X, Gimble JM, Guan X, Freitas MA, Bunnell BA. (2011). Age-related changes in mesenchymal stem cells derived from rhesus macaque bone marrow. Aging Cell. (1):66-79.
Zhang H, Yang H, Zhang C et al. (2015) Investigation of microRNA expression in human serum during the aging process. J Gerontol Ser A 70:102–109.
Zhu K, Liu M, Fu Z, Zhou Z, Kong Y, Liang H, Lin Z, Luo J, et al. (2017). Plant microRNAs in larval food regulate honeybee caste development. PLoS Genet.13(8): e1006946.
Zou S, Sinclair J, Wilson MA, Carey JR, Liedo P, Oropeza A, et al. (2007). Comparative approaches to facilitate the discovery of prolongevity interventions: effects of tocopherols on lifespan of three invertebrate species. Mech Ageing Dev. 128(2):222-6.