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2. Reversal of biological age in multiple rat organs by young porcine plasma fraction

Author

Horvath, Steve, Singh, Kavita, Raj, Ken, Khairnar, Shraddha I, Sanghavi, Akshay, Shrivastava, Agnivesh, Zoller, Joseph A, Li, Caesar Z, Herenu, Claudia B, Canatelli-Mallat, Martina, Lehmann, Marianne, Habazin, Siniša, Novokmet, Mislav, Vučković, Frano, Solberg Woods, Leah C, Martinez, Angel Garcia, Wang, Tengfei, Chiavellini, Priscila, Levine, Andrew J, Chen, Hao, Brooke, Robert T, Gordevicius, Juozas, Lauc, Gordan, Goya, Rodolfo G, and Katcher, Harold L

Subjects
Biological Sciences, Biomedical and Clinical Sciences, Genetics, Aging, Inflammatory and immune system, Humans, Rats, Mice, Animals, Swine, Epigenesis, Genetic, Biomarkers, Plasma, Immunoglobulin G, Rejuvenation, Plasma fraction, Epigenetic clock, DNA methylation, Glycans, Rat, Clinical sciences
Abstract

Young blood plasma is known to confer beneficial effects on various organs in mice and rats. However, it was not known whether plasma from young adult pigs rejuvenates old rat tissues at the epigenetic level; whether it alters the epigenetic clock, which is a highly accurate molecular biomarker of aging. To address this question, we developed and validated six different epigenetic clocks for rat tissues that are based on DNA methylation values derived from n = 613 tissue samples. As indicated by their respective names, the rat pan-tissue clock can be applied to DNA methylation profiles from all rat tissues, while the rat brain, liver, and blood clocks apply to the corresponding tissue types. We also developed two epigenetic clocks that apply to both human and rat tissues by adding n = 1366 human tissue samples to the training data. We employed these six rat clocks to investigate the rejuvenation effects of a porcine plasma fraction treatment in different rat tissues. The treatment more than halved the epigenetic ages of blood, heart, and liver tissue. A less pronounced, but statistically significant, rejuvenation effect could be observed in the hypothalamus. The treatment was accompanied by progressive improvement in the function of these organs as ascertained through numerous biochemical/physiological biomarkers, behavioral responses encompassing cognitive functions. An immunoglobulin G (IgG) N-glycosylation pattern shift from pro- to anti-inflammatory also indicated reversal of glycan aging. Overall, this study demonstrates that a young porcine plasma-derived treatment markedly reverses aging in rats according to epigenetic clocks, IgG glycans, and other biomarkers of aging.

Published
2024

3. Stress induced aging in mouse eye

Author

Xu, Qianlan, Rydz, Cezary, Huu, Viet Anh Nguyen, Rocha, Lorena, La Torre, Claudia Palomino, Lee, Irene, Cho, William, Jabari, Mary, Donello, John, Lyon, David C, Brooke, Robert T, Horvath, Steve, Weinreb, Robert N, Ju, Won‐Kyu, Foik, Andrzej, and Skowronska‐Krawczyk, Dorota

Subjects
Biomedical and Clinical Sciences, Ophthalmology and Optometry, Neurosciences, Human Genome, Aging, Prevention, Neurodegenerative, Genetics, Eye Disease and Disorders of Vision, Underpinning research, 2.1 Biological and endogenous factors, Aetiology, 1.1 Normal biological development and functioning, Eye, Mice, Animals, Intraocular Pressure, Retinal Ganglion Cells, Glaucoma, Disease Models, Animal, Chromatin, aging, IOP, retinal ganglion cells, senescence, stress response, Biological Sciences, Medical and Health Sciences, Developmental Biology, Biological sciences, Biomedical and clinical sciences
Abstract

Aging, a universal process that affects all cells in an organism, is a major risk factor for a group of neuropathies called glaucoma, where elevated intraocular pressure is one of the known stresses affecting the tissue. Our understanding of molecular impact of aging on response to stress in retina is very limited; therefore, we developed a new mouse model to approach this question experimentally. Here we show that susceptibility to response to stress increases with age and is primed on chromatin level. We demonstrate that ocular hypertension activates a stress response that is similar to natural aging and involves activation of inflammation and senescence. We show that multiple instances of pressure elevation cause aging of young retina as measured on transcriptional and DNA methylation level and are accompanied by local histone modification changes. Our data show that repeated stress accelerates appearance of aging features in tissues and suggest chromatin modifications as the key molecular components of aging. Lastly, our work further emphasizes the importance of early diagnosis and prevention as well as age-specific management of age-related diseases, including glaucoma.

Published
2022

4. A torpor-like state (TLS) in mice slows blood epigenetic aging and prolongs healthspan

Author

Jayne, Lorna, primary, Lavin-Peter, Aurora, additional, Roessler, Julian, additional, Tyshkovskiy, Alexander, additional, Antoszewski, Mateusz, additional, Ren, Erika, additional, Markovski, Aleksandar, additional, Sun, Senmiao, additional, Yao, Hanqi, additional, Sankaran, Vijay G., additional, Gladyshev, Vadim N., additional, Brooke, Robert T., additional, Horvath, Steve, additional, Griffith, Eric C., additional, and Hrvatin, Sinisa, additional

Published
2024
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6. Reversal of biological age in multiple rat organs by young porcine plasma fraction

Author

Horvath, Steve, primary, Singh, Kavita, additional, Raj, Ken, additional, Khairnar, Shraddha I., additional, Sanghavi, Akshay, additional, Shrivastava, Agnivesh, additional, Zoller, Joseph A., additional, Li, Caesar Z., additional, Herenu, Claudia B., additional, Canatelli-Mallat, Martina, additional, Lehmann, Marianne, additional, Habazin, Siniša, additional, Novokmet, Mislav, additional, Vučković, Frano, additional, Solberg Woods, Leah C., additional, Martinez, Angel Garcia, additional, Wang, Tengfei, additional, Chiavellini, Priscila, additional, Levine, Andrew J., additional, Chen, Hao, additional, Brooke, Robert T., additional, Gordevicius, Juozas, additional, Lauc, Gordan, additional, Goya, Rodolfo G., additional, and Katcher, Harold L., additional

Published
2023
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7. DNA methylation networks underlying mammalian traits

Author

Haghani, Amin, primary, Li, Caesar Z., additional, Robeck, Todd R., additional, Zhang, Joshua, additional, Lu, Ake T., additional, Ablaeva, Julia, additional, Acosta-Rodríguez, Victoria A., additional, Adams, Danielle M., additional, Alagaili, Abdulaziz N., additional, Almunia, Javier, additional, Aloysius, Ajoy, additional, Amor, Nabil M.S., additional, Ardehali, Reza, additional, Arneson, Adriana, additional, Baker, C. Scott, additional, Banks, Gareth, additional, Belov, Katherine, additional, Bennett, Nigel C., additional, Black, Peter, additional, Blumstein, Daniel T., additional, Bors, Eleanor K., additional, Breeze, Charles E., additional, Brooke, Robert T., additional, Brown, Janine L., additional, Carter, Gerald, additional, Caulton, Alex, additional, Cavin, Julie M., additional, Chakrabarti, Lisa, additional, Chatzistamou, Ioulia, additional, Chavez, Andreas S., additional, Chen, Hao, additional, Cheng, Kaiyang, additional, Chiavellini, Priscila, additional, Choi, Oi-Wa, additional, Clarke, Shannon, additional, Cook, Joseph A., additional, Cooper, Lisa N., additional, Cossette, Marie-Laurence, additional, Day, Joanna, additional, DeYoung, Joseph, additional, Dirocco, Stacy, additional, Dold, Christopher, additional, Dunnum, Jonathan L., additional, Ehmke, Erin E., additional, Emmons, Candice K., additional, Emmrich, Stephan, additional, Erbay, Ebru, additional, Erlacher-Reid, Claire, additional, Faulkes, Chris G., additional, Fei, Zhe, additional, Ferguson, Steven H., additional, Finno, Carrie J., additional, Flower, Jennifer E., additional, Gaillard, Jean-Michel, additional, Garde, Eva, additional, Gerber, Livia, additional, Gladyshev, Vadim N., additional, Goya, Rodolfo G., additional, Grant, Matthew J, additional, Green, Carla B., additional, Hanson, M. Bradley, additional, Hart, Daniel W., additional, Haulena, Martin, additional, Herrick, Kelsey, additional, Hogan, Andrew N., additional, Hogg, Carolyn J., additional, Hore, Timothy A., additional, Huang, Taosheng, additional, Izpisua Belmonte, Juan Carlos, additional, Jasinska, Anna J., additional, Jones, Gareth, additional, Jourdain, Eve, additional, Kashpur, Olga, additional, Katcher, Harold, additional, Katsumata, Etsuko, additional, Kaza, Vimala, additional, Kiaris, Hippokratis, additional, Kobor, Michael S., additional, Kordowitzki, Pawel, additional, Koski, William R., additional, Krützen, Michael, additional, Kwon, Soo Bin, additional, Larison, Brenda, additional, Lee, Sang-Goo, additional, Lehmann, Marianne, additional, Lemaître, Jean-François, additional, Levine, Andrew J., additional, Li, Xinmin, additional, Li, Cun, additional, Lim, Andrea R., additional, Lin, David T. S., additional, Lindemann, Dana M., additional, Liphardt, Schuyler W., additional, Little, Thomas J., additional, Macoretta, Nicholas, additional, Maddox, Dewey, additional, Matkin, Craig O., additional, Mattison, Julie A., additional, McClure, Matthew, additional, Mergl, June, additional, Meudt, Jennifer J., additional, Montano, Gisele A., additional, Mozhui, Khyobeni, additional, Munshi-South, Jason, additional, Murphy, William J., additional, Naderi, Asieh, additional, Nagy, Martina, additional, Narayan, Pritika, additional, Nathanielsz, Peter W., additional, Nguyen, Ngoc B., additional, Niehrs, Christof, additional, Nyamsuren, Batsaikhan, additional, O’Brien, Justine K., additional, Ginn, Perrie O’Tierney, additional, Odom, Duncan T, additional, Ophir, Alexander G., additional, Osborn, Steve, additional, Ostrander, Elaine A., additional, Parsons, Kim M., additional, Paul, Kimberly C., additional, Pedersen, Amy B., additional, Pellegrini, Matteo, additional, Peters, Katharina J., additional, Petersen, Jessica L., additional, Pietersen, Darren W., additional, Pinho, Gabriela M., additional, Plassais, Jocelyn, additional, Poganik, Jesse R., additional, Prado, Natalia A., additional, Reddy, Pradeep, additional, Rey, Benjamin, additional, Ritz, Beate R., additional, Robbins, Jooke, additional, Rodriguez, Magdalena, additional, Russell, Jennifer, additional, Rydkina, Elena, additional, Sailer, Lindsay L., additional, Salmon, Adam B., additional, Sanghavi, Akshay, additional, Schachtschneider, Kyle M., additional, Schmitt, Dennis, additional, Schmitt, Todd, additional, Schomacher, Lars, additional, Schook, Lawrence B., additional, Sears, Karen E., additional, Seifert, Ashley W., additional, Shafer, Aaron B.A., additional, Shindyapina, Anastasia V., additional, Simmons, Melanie, additional, Singh, Kavita, additional, Sinha, Ishani, additional, Slone, Jesse, additional, Snell, Russel G., additional, Soltanmohammadi, Elham, additional, Spangler, Matthew L., additional, Spriggs, Maria, additional, Staggs, Lydia, additional, Stedman, Nancy, additional, Steinman, Karen J., additional, Stewart, Donald T, additional, Sugrue, Victoria J., additional, Szladovits, Balazs, additional, Takahashi, Joseph S., additional, Takasugi, Masaki, additional, Teeling, Emma C., additional, Thompson, Michael J., additional, Van Bonn, Bill, additional, Vernes, Sonja C., additional, Villar, Diego, additional, Vinters, Harry V., additional, Vu, Ha, additional, Wallingford, Mary C., additional, Wang, Nan, additional, Wilkinson, Gerald S., additional, Williams, Robert W., additional, Yan, Qi, additional, Yao, Mingjia, additional, Young, Brent G., additional, Zhang, Bohan, additional, Zhang, Zhihui, additional, Zhao, Yang, additional, Zhao, Peng, additional, Zhou, Wanding, additional, Zoller, Joseph A., additional, Ernst, Jason, additional, Seluanov, Andrei, additional, Gorbunova, Vera, additional, Yang, X. William, additional, Raj, Ken, additional, and Horvath, Steve, additional

Published
2023
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8. Father’s care uniquely influences male neurodevelopment

Author

Danoff, Joshua S., primary, Ramos, Erin N., additional, Hinton, Taylor D., additional, Perkeybile, Allison M., additional, Graves, Andrew J., additional, Quinn, Graham C., additional, Lightbody-Cimer, Aaron R., additional, Gordevičius, Juozas, additional, Milčiūtė, Milda, additional, Brooke, Robert T., additional, Carter, C. Sue, additional, Bales, Karen L., additional, Erisir, Alev, additional, and Connelly, Jessica J., additional

Published
2023
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9. A molecular signature defining exercise adaptation with ageing and in vivo partial reprogramming in skeletal muscle

Author

Jones, Ronald G., primary, Dimet‐Wiley, Andrea, additional, Haghani, Amin, additional, da Silva, Francielly Morena, additional, Brightwell, Camille R., additional, Lim, Seongkyun, additional, Khadgi, Sabin, additional, Wen, Yuan, additional, Dungan, Cory M., additional, Brooke, Robert T., additional, Greene, Nicholas P., additional, Peterson, Charlotte A., additional, McCarthy, John J., additional, Horvath, Steve, additional, Watowich, Stanley J., additional, Fry, Christopher S., additional, and Murach, Kevin A., additional

Published
2023
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10. Small extracellular vesicles from young adipose-derived stem cells prevent frailty, improve health span, and decrease epigenetic age in old mice

Author

Sanz-Ros, Jorge, primary, Romero-García, Nekane, additional, Mas-Bargues, Cristina, additional, Monleón, Daniel, additional, Gordevicius, Juozas, additional, Brooke, Robert T., additional, Dromant, Mar, additional, Díaz, Ana, additional, Derevyanko, Aksinya, additional, Guío-Carrión, Ana, additional, Román-Domínguez, Aurora, additional, Inglés, Marta, additional, Blasco, María A., additional, Horvath, Steve, additional, Viña, Jose, additional, and Borrás, Consuelo, additional

Published
2022
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12. DNA methylation clocks for dogs and humans

Author

Horvath, Steve, primary, Lu, Ake T., additional, Haghani, Amin, additional, Zoller, Joseph A., additional, Li, Caesar Z., additional, Lim, Andrea R., additional, Brooke, Robert T., additional, Raj, Ken, additional, Serres-Armero, Aitor, additional, Dreger, Dayna L., additional, Hogan, Andrew N., additional, Plassais, Jocelyn, additional, and Ostrander, Elaine A., additional

Published
2022
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13. Small extracellular vesicles from young mice prevent frailty, improve healthspan and decrease epigenetic age in old mice

Author

Sanz-Ros, Jorge, primary, Mas-Bargues, Cristina, additional, Monleón, Daniel, additional, Gordevicius, Juozas, additional, Brooke, Robert T., additional, Dromant, Mar, additional, Derevyanko, Aksinya, additional, Guío-Carrión, Ana, additional, Román-Domínguez, Aurora, additional, Romero-García, Nekane, additional, Inglés, Marta, additional, Blasco, María A., additional, Horvath, Steve, additional, Viña, Jose, additional, and Borrás, Consuelo, additional

Published
2021
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14. Epigenetic predictors of maximum lifespan and other life history traits in mammals

Author

Li, Caesar Z., primary, Haghani, Amin, additional, Robeck, Todd R., additional, Villar, Diego, additional, Lu, Ake T., additional, Zhang, Joshua, additional, Faulkes, Chris G., additional, Vu, Ha, additional, Ablaeva, Julia, additional, Adams, Danielle M., additional, Ardehali, Reza, additional, Arneson, Adriana, additional, Baker, C. Scott, additional, Belov, Katherine, additional, Blumstein, Daniel T., additional, Bors, Eleanor K., additional, Breeze, Charles E., additional, Brooke, Robert T., additional, Brown, Janine L., additional, Caulton, Alex, additional, Cavin, Julie M., additional, Chatzistamou, Ioulia, additional, Chen, Hao, additional, Chiavellini, Priscila, additional, Choi, Oi-Wa, additional, Clarke, Shannon, additional, DeYoung, Joseph, additional, Emmons, Candice K., additional, Emmrich, Stephan, additional, Fei, Zhe, additional, Ferguson, Steven H., additional, Finno, Carrie J., additional, Flower, Jennifer E., additional, Gaillard, Jean-Michel, additional, Garde, Eva, additional, Gladyshev, Vadim N., additional, Goya, Rodolfo G., additional, Hanson, M. Bradley, additional, Haulena, Martin, additional, Herrick, Kelsey, additional, Hogan, Andrew N., additional, Hogg, Carolyn J., additional, Hore, Timothy A., additional, Jasinska, Anna J., additional, Jones, Gareth, additional, Jourdain, Eve, additional, Kashpur, Olga, additional, Katcher, Harold, additional, Katsumata, Etsuko, additional, Kaza, Vimala, additional, Kiaris, Hippokratis, additional, Kobor, Michael S., additional, Kordowitzki, Pawel, additional, Koski, William R., additional, Larison, Brenda, additional, Lee, Sang-Goo, additional, Lehmann, Marianne, additional, Lemaitre, Jean-Francois, additional, Levine, Andrew J., additional, Li, Cun, additional, Li, Xinmin, additional, Lin, David TS, additional, Lindemann, Dana M., additional, Macoretta, Nicholas, additional, Maddox, Dewey, additional, Matkin, Craig O., additional, Mattison, Julie A., additional, Mergl, June, additional, Meudt, Jennifer J., additional, Montano, Gisele A., additional, Mozhui, Khyobeni, additional, Naderi, Asieh, additional, Nagy, Martina, additional, Narayan, Pritika, additional, Nathanielsz, Peter W., additional, Nguyen, Ngoc B., additional, Niehrs, Christof, additional, Odom, Duncan T, additional, Ophir, Alexander G., additional, Ostrander, Elaine A., additional, O'Tierney Ginn, Perrie, additional, Parsons, Kim M., additional, Paul, Kimberly C., additional, Pellegrini, Matteo, additional, Pinho, Gabriela M., additional, Plassais, Jocelyn, additional, Prado, Natalia A., additional, Rey, Benjamin, additional, Ritz, Beate R., additional, Robbins, Jooke, additional, Rodriguez, Magdalena, additional, Russell, Jennifer, additional, Rydkina, Elena, additional, Sailer, Lindsay L., additional, Salmon, Adam B., additional, Sanghavi, Akshay, additional, Schachtschneider, Kyle M., additional, Schmitt, Dennis, additional, Schomacher, Lars, additional, Schook, Lawrence B., additional, Sears, Karen E., additional, Seifert, Ashley W., additional, Shindyapina, Anastasia V., additional, Singh, Kavita, additional, Sinha, Ishani, additional, Snell, Russel G., additional, Soltanmohammadi, Elham, additional, Spangler, Matthew L., additional, Spriggs, Maria, additional, Steinman, Karen J., additional, Sugrue, Victoria J., additional, Szladovits, Balazs, additional, Takasugi, Masaki, additional, Teeling, Emma C., additional, Van Bonn, Bill, additional, Vernes, Sonja C., additional, Vinters, Harry V., additional, Wallingford, Mary C., additional, Wang, Nan, additional, Wilkinson, Gerald S., additional, Williams, Robert W., additional, Yang, X. William, additional, Young, Brent G., additional, Zhang, Bohan, additional, Zhang, Zhihui, additional, Zhao, Peng, additional, Zhao, Yang, additional, Zhou, Wanding, additional, Zoller, Joseph A., additional, Ernst, Jason, additional, Seluanov, Andrei, additional, Raj, Ken, additional, Gorbunova, Vera, additional, and Horvath, Steve, additional

Published
2021
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15. Epigenetic clock and methylation studies in dogs

Author

Horvath, Steve, primary, Lu, Ake T., additional, Haghani, Amin, additional, Zoller, Joseph A., additional, Brooke, Robert T., additional, Raj, Ken, additional, Plassais, Jocelyn, additional, Hogan, Andrew N., additional, and Ostrander, Elaine A., additional

Published
2021
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17. Reversal of epigenetic aging and immunosenescent trends in humans

Author

Fahy, Gregory M., primary, Brooke, Robert T., additional, Watson, James P., additional, Good, Zinaida, additional, Vasanawala, Shreyas S., additional, Maecker, Holden, additional, Leipold, Michael D., additional, Lin, David T. S., additional, Kobor, Michael S., additional, and Horvath, Steve, additional

Published
2019
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19. A torpor-like state (TLS) in mice slows blood epigenetic aging and prolongs healthspan.

Author

Jayne L, Lavin-Peter A, Roessler J, Tyshkovskiy A, Antoszewski M, Ren E, Markovski A, Sun S, Yao H, Sankaran VG, Gladyshev VN, Brooke RT, Horvath S, Griffith EC, and Hrvatin S

Abstract

Torpor and hibernation are extreme physiological adaptations of homeotherms associated with pro-longevity effects. Yet the underlying mechanisms of how torpor affects aging, and whether hypothermic and hypometabolic states can be induced to slow aging and increase health span, remain unknown. We demonstrate that the activity of a spatially defined neuronal population in the avMLPA, which has previously been identified as a torpor-regulating brain region, is sufficient to induce a torpor like state (TLS) in mice. Prolonged induction of TLS slows epigenetic aging across multiple tissues and improves health span. We isolate the effects of decreased metabolic rate, long-term caloric restriction, and decreased core body temperature (T b ) on blood epigenetic aging and find that the pro-longevity effect of torpor-like states is mediated by decreased T b . Taken together, our findings provide novel mechanistic insight into the pro-longevity effects of torpor and hibernation and support the growing body of evidence that T b is an important mediator of aging processes., Competing Interests: Competing Interests S. Horvath and R.T. Brooke are founders of the non-profit Epigenetic Clock Development Foundation, which licenses several patents from UC Regents including a patent on the mammalian methylation array platform. These patents list S.Horvath as inventor. V.G.S. serves as an advisor to and/or has equity in Branch Biosciences, Ensoma, and Cellarity, all unrelated to this work.

Published
2024
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20. Reversal of Biological Age in Multiple Rat Organs by Young Porcine Plasma Fraction.

Author

Horvath S, Singh K, Raj K, Khairnar S, Sanghavi A, Shrivastava A, Zoller JA, Li CZ, Herenu CB, Canatelli-Mallat M, Lehmann M, Habazin S, Novokmet M, Vučković F, Woods LCS, Martinez AG, Wang T, Chiavellini P, Levine AJ, Chen H, Brooke RT, Gordevicius J, Lauc G, Goya RG, and Katcher HL

Abstract

Young blood plasma is known to confer beneficial effects on various organs in mice and rats. However, it was not known whether plasma from young pigs rejuvenates old rat tissues at the epigenetic level; whether it alters the epigenetic clock, which is a highly accurate molecular biomarker of aging. To address this question, we developed and validated six different epigenetic clocks for rat tissues that are based on DNA methylation values derived from n=613 tissue samples. As indicated by their respective names, the rat pan-tissue clock can be applied to DNA methylation profiles from all rat tissues, while the rat brain-, liver-, and blood clocks apply to the corresponding tissue types. We also developed two epigenetic clocks that apply to both human and rat tissues by adding n=1366 human tissue samples to the training data. We employed these six rat clocks to investigate the rejuvenation effects of a porcine plasma fraction treatment in different rat tissues. The treatment more than halved the epigenetic ages of blood, heart, and liver tissue. A less pronounced, but statistically significant, rejuvenation effect could be observed in the hypothalamus. The treatment was accompanied by progressive improvement in the function of these organs as ascertained through numerous biochemical/physiological biomarkers and behavioral responses to assess cognitive functions. An immunoglobulin G (IgG) N-glycosylation pattern shift from pro- to anti-inflammatory also indicated reversal of glycan aging. Overall, this study demonstrates that a young porcine plasma-derived treatment markedly reverses aging in rats according to epigenetic clocks, IgG glycans, and other biomarkers of aging., Competing Interests: Conflict of Interest Statement Several authors are founders, owners, employees (Harold Katcher and Akshay Sanghavi) or consultants of Yuvan Research (Steve Horvath and Agnivesh Shrivastava) which plans to commercialize the E5 treatment. Other authors (Kavita Singh, Shraddha Khairnar) received financial support from Yuvan Research. Gordan Lauc is a founder and CEO of Genos Ltd., a company specialized in high throughput glycomics. Siniša Habazin, Mislav Novokmet and Frano Vučković are employees of Genos Ltd. The other authors do not have conflict of interest.

Published
2023
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