Zoological Research ›› 2019, Vol. 40 ›› Issue (3): 236-238.doi: 10.24272/j.issn.2095-8137.2019.031

• Research Highlight • Previous Articles     Next Articles

A transgenic monkey model for the study of human brain evolution

Lei Shi1,2,Bing Su1,2,3()   

  1. 1. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming Yunnan 650223, China
    2. Primate Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming Yunnan 650223, China
    3. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming Yunnan 650223, China
  • Received:2019-04-04 Accepted:2019-04-09 Online:2019-05-18 Published:2019-04-19
  • Contact: Bing Su E-mail:sub@mail.kiz.ac.cn
  • Supported by:
    This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000), the National Natural Science Foundation of China (31730088) and the Youth Innovation Promotion Association of CAS

Abstract:

Why humans have large brains with higher cognitive abilities is a question long asked by scientists. However, much remains unknown, especially the underlying genetic mechanisms. With the use of a transgenic monkey model, we showed that human-specific sequence changes of a key brain development gene (primary microcephaly1, MCPH1) could result in detectable molecular and cognitive changes resembling human neoteny, a notable characteristic developed during human evolution.

Key words: MCPH1, Brain Evolution, Transgenic Monkey, Positive selection, Neoteny

Bufill E , Agustí J , Blesa R . 2011. Human neoteny revisited: The case of synaptic plasticity. American Journal of Human Biology, 23(6): 729–739.
Bustamante CD , Fledel-Alon A , Williamson S , Nielsen R , Hubisz MT , Glanowski S , Tanenbaum DM , White TJ , Sninsky JJ , Hernandez RD , Civello D , Adams MD , Cargill M , Clark AG . 2005. Natural selection on protein-coding genes in the human genome. Nature, 437(7062): 1153–1157.
Chen Y , Yu J , Niu Y , Qin D , Liu H , Li G , Hu Y , Wang J , Lu Y , Kang Y , Jiang Y , Wu K , Li S , Wei J , He J , Wang J , Liu X , Luo Y , Si C , Bai R , Zhang K , Liu J , Huang S , Chen Z , Wang S , Chen X , Bao X , Zhang Q , Li F , Geng R , Liang A , Shen D , Jiang T , Hu X , Ma Y , Ji W , Sun Y . E. 2017. Modeling rett syndrome using TALEN-Edited MECP2 mutant cynomolgus monkeys. Cell, 169(5): 945–955.
Clark AG , Glanowski S , Nielsen R , Thomas PD , Kejariwal A , Todd MA , Tanenbaum DM , Civello D , Lu F , Murphy B , Ferriera S , Wang G , Zheng X , White TJ , Sninsky JJ , Adams MD , Cargill M . 2003. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science, 302(5652): 1960–1963.
Coors ME , Glover JJ , Juengst ET , Sikela JM . 2010. The ethics of using transgenic non-human primates to study what makes us human. Nature Reviews Genetics, 11(9): 658–662.
Enard W , Gehre S , Hammerschmidt K , Hölter SM , Blass T , Somel M , Brückner MK , Schreiweis C , Winter C , Sohr R , Becker L , Wiebe V , Nickel B , Giger T , Müller U , Groszer M , Adler T , Aguilar A , Bolle I , Calzada-Wack J , Dalke C , Ehrhardt N , Favor J , Fuchs H , Gailus-Durner V , Hans W , Hölzlwimmer G , Javaheri A , Kalaydjiev S , Kallnik M , Kling E , Kunder S , Mossbrugger I , Naton B , Racz I , Rathkolb B , Rozman J , Schrewe A , Busch DH , Graw J , Ivandic B , Klingenspor M , Klopstock T , Ollert M , Quintanilla-Martinez L , Schulz H , Wolf E , Wurst W , Zimmer A , Fisher SE , Morgenstern R , Arendt T , de Angelis MH , Fischer J , Schwarz J , Pääbo S . 2009. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell, 137(5): 961–971.
Gruber R , Zhou Z , Sukchev M , Joerss T , Frappart PO , Wang ZQ . 2011. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nature Cell Biology, 13(11): 1325–1334.
Jackson AP , Eastwood H , Bell SM , Adu J , Toomes C , Carr IM , Roberts E , Hampshire DJ , Crow YJ , Mighell AJ , Karbani G , Jafri H , Rashid Y , Mueller RF , Markham AF , Woods CG . 2002. Identification of microcephalin, a protein implicated in determining the size of the human brain. American Journal of Human Genetics, 71(1): 136–142.
Ke Q , Li W , Lai X , Chen H , Huang L , Kang Z , Li K , Ren J , Lin X , Zheng H , Huang W , Ma Y , Xu D , Chen Z , Song X , Lin X , Zhuang M , Wang T , Zhuang F , Xi J , Mao FF , Xia H , Lahn BT , Zhou Q , Yang S , Xiang AP . 2016. TALEN-based generation of a cynomolgus monkey disease model for human microcephaly. Cell Research, 26(9): 1048–1061.
Liu X , Somel M , Tang L , Yan Z , Jiang X , Guo S , Yuan Y , He L , Oleksiak A , Zhang Y , Li N , Hu Y , Chen W , Qiu Z , Paabo S , Khaitovich P . 2012. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Research, 22(4): 611–622.
Liu Z , Li X , Zhang JT , Cai YJ , Cheng TJ , Cheng C , Wang Y , Zhang CC , Nie YH , Chen ZF , Bian WJ , Zhang L , Xiao J , Lu B , Zhang YF , Zhang XD , Sang X , Wu JJ , Xu X , Xiong ZQ , Zhang F , Yu X , Gong N , Zhou WH , Sun Q , Qiu Z . 2016. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature, 530(7588): 98–102.
Luo X , Li M , Su B . 2016. Application of the genome editing tool CRISPR/Cas9 in non-human primates. Zoological Research, 37(4): 214–219.
Qiu P , Jiang J , Liu Z , Cai Y , Huang T , Wang Y , Liu Q , Nie Y , Liu F , Cheng J , Li Q , Tang YC , Poo MM , Sun Q , Chang HC . 2019. BMAL1 knockout macaque monkeys display reduced sleep and psychiatric disorders. National Science Review, 6(1): 87–100.
Shi L , Li M , Lin Q , Qi X , Su B . 2013. Functional divergence of the brain-size regulating gene MCPH1 during primate evolution and the origin of humans. BMC Biology, 11: 62.
Shi L , Luo X , Jiang J , Chen Y , Liu C , Hu T , Li M , Lin Q , Li Y , Huang J , Wang H , Niu Y , Shi Y , Styner M , Wang J , Lu Y , Sun X , Yu H , Ji W , Su B . 2019. Transgenic rhesus monkeys carrying the human MCPH1 gene copies show human-like neoteny of brain development. National Science Review, doi: 10.1093/nsr/nwz043.
doi: 10.1093/nsr/nwz043
Skulachev VP , Holtze S , Vyssokikh MY , Bakeeva LE, Skulachev MV , Markov AV , Hildebrandt TB , Sadovnichii VA . 2017. Neoteny, prolongation of youth: from naked mole rats to “naked apes” (humans). Physiological Reviews, 97(2):699–720.
Wang YQ , Su B . 2004. Molecular evolution of microcephalin, a gene determining human brain size. Human Molecular Genetics, 13(11): 1131–1137.
Yan G , Zhang G , Fang X , Zhang Y , Li C , Ling F , Cooper DN , Li Q , Li Y , van Gool AJ , Du H , Chen J , Chen R , Zhang P , Huang Z , Thompson JR , Meng Y , Bai Y , Wang J , Zhuo M , Wang T , Huang Y , Wei L , Li J , Wang Z , Hu H , Yang P , Le L , Stenson PD , Li B , Liu X , Ball EV , An N , Huang Q , Zhang Y , Fan W , Zhang X , Li Y , Wang W , Katze MG , Su B , Nielsen R , Yang H , Wang J , Wang X , Wang J . 2011. Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nature Biotechnology, 29(11): 1019–1023.
Yang SH , Cheng PH , Banta H , Piotrowska-Nitsche K , Yang JJ , Cheng EC , Snyder B , Larkin K , Liu J , Orkin J , Fang ZH , Smith Y , Bachevalier J , Zola SM , Li SH , Li XJ , Chan AWS . 2008. Towards a transgenic model of Huntington's disease in a non-human primate. Nature, 453(7197): 921–924.
Zhang W , Wan H , Feng G , Qu J , Wang J , Jing Y , Ren R , Liu Z , Zhang L , Chen Z , Wang S , Zhao Y , Wang Z , Yuan Y , Zhou Q , Li W , Liu GH , Hu B . 2018. SIRT6 deficiency results in developmental retardation in cynomolgus monkeys. Nature, 560(7720): 661–665.
Zhang XL , Pang W , Hu XT , Li JL , Yao YG , Zheng YT . 2014. Experimental primates and non-human primate (NHP) models of human diseases in China: current status and progress. Zoological Research, 35(6): 447–464.
[1] Yong-Bo Guo, Yao-Xi He, Chao-Ying Cui, Ouzhuluobu, Baimakangzhuo, Duojizhuoma, Dejiquzong, Bianba, Yi Peng, Cai-juan Bai, Gonggalanzi, Yong-Yue Pan, Qula, Kangmin, Cirenyangji, Baimayangji, Wei Guo, Yangla, Hui Zhang, Xiao-Ming Zhang, Wang-Shan Zheng, Shu-Hua Xu, Hua Chen, Sheng-Guo Zhao, Yuan Cai, Shi-Ming Liu, Tian-Yi Wu, Xue-Bin Qi, Bing Su. GCH1 plays a role in the high-altitude adaptation of Tibetans [J]. Zoological Research, 2017, 38(3): 155-162.
[2] Yan-Ni ZENG, Yong-Yi SHEN, Ya-Ping ZHANG. Genome-wide scan reveals the molecular mechanisms of functional differentiation of Myotis lucifugus and Pteropus vampyrus [J]. Zoological Research, 2013, 34(3): 221-227.
[3] HUANG Lin ,,ZHANG Rui ,SU Bing. A Human-specific Mutation Leads to Reduced Interaction Between miR-124a and One of Its Target Genes, PLOD3 [J]. Zoological Research, 2008, 29(4): 363-367.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] ZHENG Ping-ping,CHEN Wen,LI Jie,RUI Jin-long,NIE Liu-wang *. Construction of a cDNA Library from the Testis and Sequence Analysis of the Ubiquitin Gene from Rana nigromaculata (in English)[J]. Zoological Research, 2007, 28(1): 9 -16 .
[2] XIONG Yu-liang,WANG Wan-yu,YANG Chang-jin,TIEN Yun-fen. Inhibitory Effects of The Elapidae Venoms in The Mice's Sarcoma 180 Ehrilich Ascititers Carcenoma[J]. Zoological Research, 1989, 10(1): 31 -35 .
[3] DING Fang,ZHOU Hong-lin,LIU Yang,MA Lan,SU Ying,DU Ling. Effects of Glucose on Development of ICR Mouse Embryosin vitro[J]. Zoological Research, 2007, 28(5): 501 -506 .
[4] LI Hong-bin, HAN Hui-li, MA Wen-pei, DONG Zhi-fang, XU Lin. Enhancement of GABAA Receptor-Mediated Inhibitory Postsynaptic Currents Induced by “Partial Oxygen-Glucose Deprivation”[J]. Zoological Research, 2007, 28(5): 491 -496 .
[5] LIU Zhao,ZHOU Wei,ZHANG Qing,LI Jin-xiang,LI Ning,ZHANG Reng-gong. Selection and Plant Community Characteristics of Foraging Sites for Hume’s Pheasant (Syramticus humiae) in Nanhua Part of Ailaoshan National Nature Reserve[J]. Zoological Research, 2008, 29(6): 646 -652 .
[6] Prithwiraj Jha,Sudip Barat,Chitta R. Nayak. Fish Production, Water Quality and Bacteriological Parameters of Koi Carp Ponds Under Live-food and Manure Based Management Regimes[J]. Zoological Research, 2008, 29(2): 165 -173 .
[7] 钟 泰,肖 林,霍 晟,向左甫,肖 文,崔亮伟. Altitudinal Range of Black-and-white Snub-nosed Monkeys (Rhinopithecus bieti ) at Baima Snow Mountain, China[J]. Zoological Research, 2008, 29(2): 181 -188 .
[8] DU Chen-guang,YANG Yan-yan,LI Hai-jun,BAO Qing-jiang. Expression of the Ghrelin in Sheep Ooctyes and Pre-implantation Embryos Produced in vivo[J]. Zoological Research, 2008, 29(2): 134 -138 .
[9] ZHANG Heng,FAN Wei,ZHANG Jian. A New Fish Record in the Yangtze Estuary: Slender Mandarinfish Siniperca roulei[J]. Zoological Research, 2009, 30(1): 109 -112 .
[10] ZHOU Wei,LIU Zhao,WU Fei. Growth and Synchrony of Reproductive Organs in Males and Females of Rana pleuraden in Kunming Area, Yunnan[J]. Zoological Research, 2009, 30(1): 99 -104 .