Basic and translational aging research in China: present and future

Xiaojuan He, Moshi Song, Jing Qu, Yansu Guo, Heqi Cao, Ruijuan Sun, Guang-Hui Liu, Yong Shen, Major Program Expert Group

PDF(491 KB)
PDF(491 KB)
Protein Cell ›› 2019, Vol. 10 ›› Issue (7) : 476-484. DOI: 10.1007/s13238-019-0617-0
PERSPECTIVE
PERSPECTIVE

Basic and translational aging research in China: present and future

Author information +
History +

Cite this article

Download citation ▾
Xiaojuan He, Moshi Song, Jing Qu, Yansu Guo, Heqi Cao, Ruijuan Sun, Guang-Hui Liu, Yong Shen, Major Program Expert Group. Basic and translational aging research in China: present and future. Protein Cell, 2019, 10(7): 476‒484 https://doi.org/10.1007/s13238-019-0617-0

References

[1]
Adli M (2018) The CRISPR tool kit for genome editing and beyond. Nat Commun 9(1):1911
CrossRef Google scholar
[2]
Awan HM, Shah A, Rashid F, Shan G(2017) Primate-specific Long Non-coding RNAs and MicroRNAs. Genomics Proteomics Bioinforma 15(3):187–195
CrossRef Google scholar
[3]
Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K, Surani MA (2009) Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 461(7268):1292–1295
CrossRef Google scholar
[4]
Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120(4):513–522
CrossRef Google scholar
[5]
Chen W, Qian W, Wu G, Chen W, Xian B, Chen X, Cao Y, Green CD, Zhao F, Tang K (2015) Three-dimensional human facial morphologies as robust aging markers. Cell Res 25(5):574–587
CrossRef Google scholar
[6]
Chen Y, Li Y, Peng Y, Zheng X, Fan S, Yi Y, Zeng P, Chen H, Kang H, Zhang Y (2018) ΔNp63α down-regulates c-Myc modulator MM1 via E3 ligase HERC3 in the regulation of cell senescence. Cell Death Differ 25(12):2118–2129
CrossRef Google scholar
[7]
Cheng X, He P, Lee T, Yao H, Li R, Shen Y (2014) High activities of BACE1 in Brains with mild cognitive impairment. Am J Pathol 184(1):141–147
CrossRef Google scholar
[8]
Cheng H, Xuan H, Green CD, Han Y, Sun N, Shen H, McDermott J, Bennett DA, Lan F, Han J-DJ (2018) Repression of human and mouse brain inflammaging transcriptome by broad gene-body histone hyperacetylation. Proc Natl Acad Sci 115(29):7611–7616
CrossRef Google scholar
[9]
Davie K, Janssens J, Koldere D, De Waegeneer M, Pech U, Kreft Ł, Aibar S, Makhzami S, Christiaens V, Bravo González-Blas C (2018) A single-cell transcriptome atlas of the aging drosophila brain. Cell 174(4):982–998
CrossRef Google scholar
[10]
Deng T, Huang Y, Weng K, Lin S, Li Y, Shi G, Chen Y, Huang J, Liu D, Ma W (2018) TOE1 acts as a 3’ exonuclease for telomerase RNA and regulates telomere maintenance. Nucleic Acids Res 47(1):391–405
CrossRef Google scholar
[11]
Duan J, Zhang Z, Tong T (2001) Senescence delay of human diploid fibroblast induced by anti-sense p16INK4a expression. J Biol Chem 276(51):48325–48331
CrossRef Google scholar
[12]
Enge M, Arda HE, Mignardi M, Beausang J, Bottino R, Kim SK, Quake SR (2017) Single-cell analysis of human pancreas reveals transcriptional signatures of aging and somatic mutation patterns. Cell 171(2):321–330
CrossRef Google scholar
[13]
Fatehullah A, Tan SH, Barker N (2016) Organoids as an in vitro model of human development and disease. Nat Cell Biol 18(3):246–254
CrossRef Google scholar
[14]
Franceschi C, Campisi J (2014) Chronic inflammation (Inflammaging) and its potential contribution to age-associated diseases. J Gerontol Ser A Biol Sci Med Sci 69(1):S4–S9
CrossRef Google scholar
[15]
Fu L, Xu X, Ren R, Wu J, Zhang W, Yang J, Ren X, Wang S, Zhao Y, Sun L (2016) Modeling xeroderma pigmentosum associated neurological pathologies with patients-derived iPSCs. Protein Cell 7(3):210–221
CrossRef Google scholar
[16]
Gan W, Liu XL, Yu T, Zou YG, Li TT, Wang S, Deng J, Wang LL, Cai JP (2018) Urinary 8-oxo-7,8-dihydroguanosine as a potential biomarker of aging. Front Aging Neurosci 10:34
CrossRef Google scholar
[17]
Gao F, Li G, Liu C, Gao H, Wang H, Liu W, Chen M, Shang Y, Wang L, Shi J (2018a) Autophagy regulates testosterone synthesis by facilitating cholesterol uptake in Leydig cells. J Cell Biol 217(6):2103–2119
CrossRef Google scholar
[18]
Gao J, Feng Z, Wang X, Zeng M, Liu J, Han S, Xu J, Chen L, Cao K, Long J (2018b) SIRT3/SOD2 maintains osteoblast differentiation and bone formation by regulating mitochondrial stress. Cell Death Differ 25(2):229–240
CrossRef Google scholar
[19]
Geng L, Liu Z, Zhang W, Li W, Wu Z, Wang W, Ren R, Su Y, Wang P, Sun L (2018) Chemical screen identifies a geroprotective role of quercetin in premature aging. Protein Cell. https://doi.org/10.1007/s13238-018-0567-y
CrossRef Google scholar
[20]
Guo Y, Nie Q, MacLean AL, Li Y, Lei J, Li S (2017) Multiscale modeling of inflammation-induced tumorigenesis reveals competing oncogenic and oncoprotective roles for inflammation. Cancer Res 77(22):6429–6441
CrossRef Google scholar
[21]
Hammond TR, Dufort C, Dissing-Olesen L, Giera S, Young A, Wysoker A, Walker AJ, Gergits F, Segel M, Nemesh J (2018) Single-cell RNA sequencing of microglia throughout the mouse lifespan and in the injured brain reveals complex cell-state changes. Immunity 50(1):253–271
CrossRef Google scholar
[22]
Han X, Wang R, Zhou Y, Fei L, Sun H, Lai S, Saadatpour A, Zhou Z, Chen H, Ye F (2018) Mapping the mouse cell atlas by microwell-seq. Cell 173(5):1307
CrossRef Google scholar
[23]
Kirkwood TBL (2005) Understanding the odd science of aging. Cell 120(4):437–447
CrossRef Google scholar
[24]
Kubben N, Zhang W, Wang L, Voss TC, Yang J, Qu J, Liu GH, Misteli T (2016) Repression of the antioxidant NRF2 pathway in premature aging. Cell 165(6):1361–1374
CrossRef Google scholar
[25]
Kudlow BA, Kennedy BK, Monnat RJ (2007) Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat Rev Mol Cell Biol 8(5):394–404
CrossRef Google scholar
[26]
Li F, Kim H, Ji Z, Zhang T, Chen B, Ge Y, Hu Y, Feng X, Han X, Xu H (2018) The BUB3-BUB1 complex promotes telomere DNA replication. Mol Cell 70(3):395–407
CrossRef Google scholar
[27]
Liao S, Dong W, Lv L, Guo H, Yang J, Zhao H, Huang R, Yuan Z, Chen Y, Feng S (2017) Heart regeneration in adult Xenopus tropicalis after apical resection. Cell Biosci 7:70
CrossRef Google scholar
[28]
Ling C, Liu Z, Song M, Zhang W, Wang S, Liu X (2019) Modeling CADASIL vascular pathologies with patient-derived induced pluripotent stem cells. Protein Cell 10(4):249–271
CrossRef Google scholar
[29]
Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, Huang JD, Li KM, Chau PY, Chen DJ (2005) Genomic instability in laminopathy-based premature aging. Nat Med 11(7):780–785
CrossRef Google scholar
[30]
Liu GH, Barkho BZ, Ruiz S, Diep D, Qu J, Yang SL, Panopoulos AD, Suzuki K, Kurian L, Walsh C (2011a) Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 472(7342):221–225
CrossRef Google scholar
[31]
Liu GH, Suzuki K, Qu J, Sancho-Martinez I, Yi F, Li M, Kumar S, Nivet E, Kim J, Soligalla RD (2011b) Targeted gene correction of laminopathy-associated LMNA mutations in patientspecific iPSCs. Cell Stem Cell 8(6):688–694
CrossRef Google scholar
[32]
Liu B, Ghosh S, Yang X, Zheng H, Liu X, Wang Z, Jin G, Zheng B, Kennedy BK, Suh Y (2012a) Resveratrol rescues SIRT1-dependent adult stem cell decline and alleviates progeroid features in laminopathy-based progeria. Cell Metab 16(6):738–750
CrossRef Google scholar
[33]
Liu GH, Qu J, Suzuki K, Nivet E, Li M, Montserrat N, Yi F, Xu X, Ruiz S, Zhang W (2012b) Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 491(7425):603–607
CrossRef Google scholar
[34]
Liu GH, Suzuki K, Li M, Qu J, Montserrat N, Tarantino C, Gu Y, Yi F, Xu X, Zhang W (2014a) Modelling Fanconi anemia pathogenesis and therapeutics using integration-free patientderived iPSCs. Nat Commun 5:4330
CrossRef Google scholar
[35]
Liu M, Bai J, He S, Villarreal R, Hu D, Zhang C, Yang X, Liang H, Slaga TJ, Yu Y (2014b) Grb10 promotes lipolysis and thermogenesis by phosphorylation-dependent feedback inhibition of mTORC1. Cell Metab 19(6):967–980
CrossRef Google scholar
[36]
Liu S, Zhang Y, Wang X, Wang Z, Chen D, Zhang B, Tian RR, Wu J, Zhang Y, Xu K (2017) Annotation and cluster analysis of spatiotemporaland sex-related lncRNA expression in rhesus macaque brain. Genome Res 27(9):1608–1620
CrossRef Google scholar
[37]
Liu H, Zhang H, Wu X, Ma D, Wu J, Wang L, Jiang Y, Fei Y, Zhu C, Tan R (2018a) Nuclear cGAS suppresses DNA repair and promotes tumorigenesis. Nature 563(7729):131–136
CrossRef Google scholar
[38]
Liu Y, Liu F, Cao Y, Xu H, Wu Y, Wu S, Liu D, Zhao Y, Songyang Z, Ma W (2018b) Shwachman-diamond syndrome protein SBDS maintains human telomeres by regulating telomerase recruitment. Cell Rep 22(7):1849–1860
CrossRef Google scholar
[39]
López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153(6):1194–1217
CrossRef Google scholar
[40]
López-Otín C, Galluzzi L, Freije JMP, Madeo F, Kroemer G (2016) Metabolic control of longevity. Cell 166(4):802–821
CrossRef Google scholar
[41]
Macosko EZ, Basu A, Satija R, Nemesh J, Shekhar K, Goldman M, Tirosh I, Bialas AR, Kamitaki N, Martersteck EM (2015) Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161(5):1202–1214
CrossRef Google scholar
[42]
Mao C-Z, Zheng L, Zhou Y-M, Wu H-Y, Xia J-B, Liang C-Q, Guo X-F, Peng W-T, Zhao H, Cai W-B (2018) CRISPR/Cas9-mediated efficient and precise targeted integration of donor DNA harboring double cleavage sites in Xenopus tropicalis. FASEB J 32(12):6495–6509
CrossRef Google scholar
[43]
Mendez-Bermudez A, Lototska L, Bauwens S, Giraud-Panis MJ, Croce O, Jamet K, Irizar A, Mowinckel M, Koundrioukoff S, Nottet N (2018) Genome-wide control of heterochromatin replication by the telomere capping protein TRF2. Mol Cell 70(3):449–461
CrossRef Google scholar
[44]
Nelson EE, Winslow JT (2009) Non-human primates: Model animals for developmental psychopathology. Neuropsychopharmacology 34(1):90–105
CrossRef Google scholar
[45]
Pan H, Guan D, Liu X, Li J, Wang L, Wu J, Zhou J, Zhang W, Ren R, Zhang W (2016) SIRT6 safeguards human mesenchymal stem cells from oxidative stress by coactivating NRF2. Cell Res 26(2):190–205
CrossRef Google scholar
[46]
Pas SP (2018) The rise of three-dimensional human brain cultures. Nature 553(7689):437–445
CrossRef Google scholar
[47]
Phillips KA, Bales KL, Capitanio JP, Conley A, Czoty PW, ’t Hart BA, Hopkins WD, Hu SL, Miller LA, Nader MA (2014) Why primate models matter. Am J Primatol 76(9):801–827
CrossRef Google scholar
[48]
Quadrato G, Brown J, Arlotta P (2016) The promises and challenges of human brain organoids as models of neuropsychiatric disease. Nat Med 22(11):1220–1228
CrossRef Google scholar
[49]
Sebastiani P, Solovieff N, DeWan AT, Walsh KM, Puca A, Hartley SW, Melista E, Andersen S, Dworkis DA, Wilk JB (2012) Genetic signatures of exceptional longevity in humans. PLoS One 7(1):e29848
CrossRef Google scholar
[50]
Sen P, Shah PP, Nativio R, Berger SL (2016) Epigenetic mechanisms of longevity and aging. Cell 166(4):822–839
CrossRef Google scholar
[51]
Shekhar K, Lapan SW, Whitney IE, Tran NM, Macosko EZ, Kowalczyk M, Adiconis X, Levin JZ, Nemesh J, Goldman M (2016) Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell 166(5):1308–1323
CrossRef Google scholar
[52]
Shen EZ, Song CQ, Lin Y, Zhang WH, Su PF, Liu WY, Zhang P, Xu J, Lin N, Zhan C (2014) Mitoflash frequency in early adulthood predicts lifespan in caenorhabditis elegans. Nature 508(7494):128–132
CrossRef Google scholar
[53]
Spanjaard B, Hu B, Mitic N, Olivares-Chauvet P, Janjuha S, Ninov N, Junker JP (2018) Simultaneous lineage tracing and cell-type identification using CrIsPr-Cas9-induced genetic scars. Nat Biotechnol 36(5):469–473
CrossRef Google scholar
[54]
Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch BB, Siddiqui A (2009) mRNA-Seq wholetranscriptome analysis of a single cell. Nat Methods 6(5):377–382
CrossRef Google scholar
[55]
Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, Lao K, Surani MA (2010) Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-seq analysis. Cell Stem Cell 6(5):468–478
CrossRef Google scholar
[56]
Tang H, Wang H, Cheng X, Fan X, Yang F, Zhang M, Chen Y, Tian Y, Liu C, Shao D (2018) HuR regulates telomerase activity through TERC methylation. Nat Commun 9(1):2213
CrossRef Google scholar
[57]
Tao R, Zhao Y, Chu H, Wang A, Zhu J, Chen X, Zou Y, Shi M, Liu R, Su N (2017) Genetically encoded fluorescent sensors reveal dynamic regulation of NADPH metabolism. Nat Methods 14(7):720–728
CrossRef Google scholar
[58]
Vallender EJ, Miller GM (2013) Nonhuman primate models in the genomic era: a paradigm shift. ILAR J 54(2):154–165
CrossRef Google scholar
[59]
Wang W, Wu J, Zhang Z, Tong T (2001) Characterization of regulatory elements on the promoter region of p16INK4a that contribute to overexpression of p16 in senescent fibroblasts. J Biol Chem 276(52):48655–48661
CrossRef Google scholar
[60]
Wang H, Diao D, Shi Z, Zhu X, Gao Y, Gao S, Liu X, Wu Y, Rudolph KL, Liu G (2016a) SIRT6 controls hematopoietic stem cell homeostasis through epigenetic regulation of Wnt signaling. Cell Stem Cell 18(4):495–507
CrossRef Google scholar
[61]
Wang H, La Russa M, Qi LS (2016b) CRISPR/Cas9 in genome editing and beyond. Annu Rev Biochem 85:227–264
CrossRef Google scholar
[62]
Wang S, Wang L, Dou L, Guo J, Fang W, Li M, Meng X, Man Y, Shen T, Huang X (2016c) MicroRNA 152 regulates hepatic glycogenesis by targeting PTEN. FEBS J 283(10):1935–1946
CrossRef Google scholar
[63]
Wang L, Yi F, Fu L, Yang J, Wang S, Wang Z, Suzuki K, Sun L, Xu X, Yu Y (2017) CRISPR/Cas9-mediated targeted gene correction in amyotrophic lateral sclerosis patient iPSCs. Protein Cell 8(5):365–378
CrossRef Google scholar
[64]
Wang H, Zuo H, Liu J, Wen F, Gao Y, Zhu X, Liu B, Xiao F, Wang W, Huang G (2018a) Loss of YTHDF2-mediated m6A-dependent mRNA clearance facilitates hematopoietic stem cell regeneration. Cell Res 28(10):1035–1038
CrossRef Google scholar
[65]
Wang XF, Chen XQ, Yu Q, Liu YW, Yang LQ, He YH, Kong QP, Kong QP (2018b) Transcriptome evidence reveals enhanced autophagy-lysosomal function in centenarians. Genome Res 28(11):1601–1610
CrossRef Google scholar
[66]
Wimmer RA, Leopoldi A, Aichinger M, Wick N, Hantusch B, Novatchkova M, Taubenschmid J, Hämmerle M, Esk C, Bagley JA (2019) Human blood vessel organoids as a model of diabetic vasculopathy. Nature 565(7740):505–510
CrossRef Google scholar
[67]
Wu Z, Zhang W, Song M, Wang W, Wei G, Li W, Lei J, Huang Y, Sang Y, Chan P (2018) Differential stem cell aging kinetics in Hutchinson-Gilford progeria syndrome and Werner syndrome. Protein Cell 9(4):333–350
CrossRef Google scholar
[68]
Xie HF, Liu YZ, Du R, Wang B, Chen MT, Zhang YY, Deng HL, Li J (2017) Mir-377 induces senescence in human skin fibroblasts by targeting DNA methyltransferase 1. Cell Death Dis 8(3):e2663
CrossRef Google scholar
[69]
Xu C, Ai D, Suo S, Chen X, Yan Y, Cao Y, Sun N, Chen W, McDermott J, Zhang S (2018a) Accurate drug repositioning through non-tissue-specific core signatures from cancer transcriptomes. Cell Rep 25(2):523–535
CrossRef Google scholar
[70]
Xu D, Jin T, Zhu H, Chen H, Ofengeim D, Zou C, Mifflin L, Pan L, Amin P, Li W (2018b) TBK1 suppresses RIPK1-driven apoptosis and inflammation during development and in aging. Cell 174(6):1477–1491
CrossRef Google scholar
[71]
Xu S, Liu P, Chen Y, Chen Y, Zhang W, Zhao H, Cao Y, Wang F, Jiang N, Lin S (2018c) Foxp2 regulates anatomical features that may be relevant for vocal behaviors and bipedal locomotion. Proc Natl Acad Sci 115(35):8799–8804
CrossRef Google scholar
[72]
Yan S, Tu Z, Liu Z, Fan N, Yang H, Yang S, Yang W, Zhao Y, Ouyang Z, Lai C (2018) A huntingtin knockin pig model recapitulates features of selective neurodegeneration in Huntington’s disease. Cell 173(4):989–1002
CrossRef Google scholar
[73]
Yan P, Li Q, Wang L, Lu P, Suzuki K, Liu Z, Lei J, Li W (2019) FOXO3-engineered human ESC-derived vascular cells promote vascular protection and regeneration. Stem Cell 24(3):447–461
CrossRef Google scholar
[74]
Yang G, Lu X, Yuan L (2014) LncRNA: a link between RNA and cancer. Biochim Biophys Acta Gene Regul Mech 1839(11):1097–1109
CrossRef Google scholar
[75]
Yang J, Li J, Suzuki K, Liu X, Wu J, Zhang W, Ren R, Zhang W, Chan P, Izpisua Belmonte JC (2017) Genetic enhancement in cultured human adult stem cells conferred by a single nucleotide recoding. Cell Res 27(9):1178–1181
CrossRef Google scholar
[76]
Yi Y, Xie H, Xiao X, Wang B, Du R, Liu Y, Li Z, Wang J, Sun L, Deng Z (2018) Ultraviolet a irradiation induces senescence in human dermal fibroblasts by down-regulating DNMT1 via ZEB1. Aging (Albany NY) 10(2):212–228
CrossRef Google scholar
[77]
Yu C, Qu J, Yao X, Li Y, Suzuki K, Benner C, Yuan T, Goebl A, Kim NY, Izpisua Belmonte JC (2014) Targeted gene correction minimally impacts whole-genome mutational load in humandisease-specific induced pluripotent stem cell clones. Cell Stem Cell 15(1):31–36
CrossRef Google scholar
[78]
Yu M, Fu Y, Liang Y, Song H, Yao Y, Wu P, Yao Y, Pan Y, Wen X, Ma L (2017) Suppression of MAPK11 or HIPK3 reduces mutant Huntingtin levels in Huntington’s disease models. Cell Res 27(12):1441–1465
CrossRef Google scholar
[79]
Zeng Z, Zhang Z, Yu H, Corbley MJ, Tang Z, Tong T (1999) Mitochondrial DNA deletions are associated with ischemia and aging in Balb/c mouse brain. J Cell Biochem 73(4):545–553
CrossRef Google scholar
[80]
Zeng Y, Nie C, Min J, Liu X, Li M, Chen H, Xu H, Wang M, Ni T, Li Y (2016) Novel loci and pathways significantly associated with longevity. Sci Rep 6:21243
CrossRef Google scholar
[81]
Zhang X, Chen Z, Chen Y, Tong T (2003) Delivering antisense telomerase RNA by a hybrid adenovirus/adeno-associated virus significantly suppresses the malignant phenotype and enhances cell apoptosis of human breast cancer cells. Oncogene 22(16):2405–2416
CrossRef Google scholar
[82]
Zhang W, Li J, Suzuki K, Qu J, Wang P, Zhou J, Liu X, Ren R, Xu X, Ocampo A (2015) A Werner syndrome stem cell model unveils heterochromatin alterations as a driver of human aging. Science 348(6239):1160–1163
CrossRef Google scholar
[83]
Zhang W, Song M, Qu J, Liu GH (2018a) Epigenetic modifications in cardiovascular aging and diseases. Circ Res 123(7):773–786
CrossRef Google scholar
[84]
Zhang W, Wan H, Feng G, Qu J, Wang J, Jing Y, Ren R, Liu Z, Zhang L, Chen Z (2018b) SIRT6 deficiency results in developmental retardation in cynomolgus monkeys. Nature 560 (7720):661–665
CrossRef Google scholar
[85]
Zhu H, Zou G, Wang N, Zhuang M, Xiong W, Huang G (2017) Single-neuron identification of chemical constituents, physiological changes, and metabolism using mass spectrometry. Proc Natl Acad Sci 114(10):2586–2591
CrossRef Google scholar
[86]
Zou Y, Wang A, Shi M, Chen X, Liu R, Li T, Zhang C, Zhang Z, Zhu L, Ju Z (2018) Analysis of redox landscapes and dynamics in living cells and in vivo using genetically encoded fluorescent sensors. Nat Protoc 13(10):2362–2386
CrossRef Google scholar

RIGHTS & PERMISSIONS

2019 The Author(s) 2019
AI Summary AI Mindmap
PDF(491 KB)

Accesses

Citations

Detail

Sections
Recommended

/