Advances in the application of induced pluripotent stem cells in neuromuscular diseases

doi:10.3877/cma.j.issn.2095-1221.2024.06.007

Abstract

Abstract:

Neuromuscular disorders （NMDs） are highly heterogeneous in etiology.Different genetic variants contribute to different disease entities. More than 800 genes for hereditary neuromuscular diseases have been reported. In addition， some disorders， such as congenital nemaline myopathy， is caused by variants of several different genes. Such genetic complexity of the neuromuscular disease presents significant challenges for in vitro disease modeling. However， due to the maintenance of the genetic background of the donor cell during cell reprogramming， induced pluripotent stem cells （iPSCs） has been used broadly in the studies of NMDs. In this paper， the progress in applications of iPSCs technology in the studies of NMDs are reviewed.

Key words: Neuromuscular diseases, iPSCs, Gene mutation, Drug screening

Wenzhu Liu, Yao Tang, Fuchen Liu. Advances in the application of induced pluripotent stem cells in neuromuscular diseases[J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2024, 14(06): 367-373.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhxbygxbzz.cma-cmc.com.cn/EN/10.3877/cma.j.issn.2095-1221.2024.06.007

https://zhxbygxbzz.cma-cmc.com.cn/EN/Y2024/V14/I06/367

References 92

1	Fralish Z， Lotz EM， Chavez T， et al. Neuromuscular development and disease:learning from in vitro and in vivo models［J］. Front Cell Dev Biol， 2021， 9:764732. doi:10.3389/fcell.2021.764732.
2	Deenen JC， Horlings CG， Verschuuren JJ， et al. The epidemiology of neuromuscular disorders:a comprehensive overview of the literature［J］.J Neuromuscul Dis， 2015， 2（1）:73-85.
3	Benarroch L， Bonne G， Rivier， et al. The 2023 version of the gene table of neuromuscular disorders （nuclear genome）［J］. Neuromuscul Disord，2023， 33（1）:76-117.
4	Sato M， Takizawa H， Nakamura A， et al. Application of urinederived stem cells to cellular modeling in neuromuscular and neurodegenerative diseases［J］. Front Mol Neurosci， 2019， 12:297.doi:10.3389/fnmol.2019.00297.
5	Gurdon JB. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles［J］. J Embryol Exp Morphol， 1962，10:622-640.
6	Wilmut I， Schnieke AE， McWhir J， et al. Viable offspring derived from fetal and adult mammalian cells［J］. Nature， 1997， 385（6619）:810-813.
7	Evans MJ， Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos［J］. Nature， 1981， 292（5819）:154-156.
8	Thomson JA， Itskovitz-Eldor J， Shapiro SS， et al. Embryonic stem cell lines derived from human blastocysts［J］. Science， 1998，282（5391）:1145-1147.
9	Tada M， Takahama Y， Abe K， et al. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells［J］. Curr Biol， 2001，11（19）:1553-1558.
10	Takahashi K， Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors［J］.Cell， 2006， 126（4）:663-676.
11	Takahashi K， Tanabe K， Ohnuki M， et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors［J］.Cell， 2007，131（5）:861-872.
12	樊东升，陈璐. 运动神经元病的诊断和分类［J］.中华神经科杂志，2019， 52（12）:1065-1067.
13	Chio A， Logroscino G， Traynor BJ， et al. Global epidemiology of amyotrophic lateral sclerosi: a systematic review of the published literature［J］. Neuroepidemiology， 2013， 41（2）:118-130.
14	Sreedharan J， Brown RJ. Amyotrophic lateral sclerosis:problems and prospects［J］. Ann Neurol， 2013， 74（3）:309-316.
15	Sareen D， O′Rourke JG， Meera P， et al. Targeting RNA foci in iPSC- derived motor neurons from ALS patients with a C9ORF72 repeat expansion［J］. Sci Transl Med， 2013， 5（208）:208ra149.
16	Donnelly CJ， Zhang PW， Pham JT， et al. RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention［J］.Neuron， 2013， 80（2）:415-428.
17	Devlin AC， Burr K， Borooah S， et al. Human iPSC-derived motoneurons harbouring TARDBP or C9ORF72 ALS mutations are dysfunctional despite maintaining viability［J］. Nat Commun， 2015，6:5999.doi:10.1038/ncomms6999.
18	Dafinca R， Scaber J， Ababneh N， et al. C9orf72 hexanucleotide expansions are associated with altered endoplasmic reticulum calcium homeostasis and stress granule formation in induced pluripotent stem cell-derived neurons from patients with amyotrophic lateral sclerosis and frontotemporal dementia［J］. Stem Cells， 2016， 34（8）:2063-2078.
19	Kiskinis E， Sandoe J， Williams LA， et al. Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1［J］. Cell Stem Cell， 2014， 14（6）:781-795.
20	Picchiarelli G， Demestre M， Zuko A， et al. FUS-mediated regulation of acetylcholine receptor transcription at neuromuscular junctions is compromised in amyotrophic lateral sclerosis［J］.Nat Neurosci， 2019，22（11）:1793-1805.
21	Wainger BJ， Kiskinis E， Mellin C， et al. Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons［J］. Cell Rep， 2014， 7（1）:1-11.
22	Osaki T， Uzel S， Kamm RD. Microphysiological 3D model of amyotrophic lateral sclerosis（ ALS） from human iPS-derived muscle cells and optogenetic motor neurons［J］. Sci Adv， 2018， 4（10）:eaat5847.doi:10.1126/sciadv.aat5847.
23	Okano H， Yasuda D， Fujimori K， et al.Ropinirole， a new ALS drug candidate developed using iPSCs［J］.Trends Pharmacol Sci， 2020，41（2）:99-109.
24	Miller T， Cudkowicz M， Shaw PJ， et al. Phase 1-2 trial of antisense oligonucleotide tofersen for SOD1 ALS［J］. N Engl J Med， 2020，383（2）:109-119.
25	Mullard A.ALS antisense drug falters in phase III［J］. Nat Rev Drug Discov， 2021， 20（12）:883-885.
26	Shariati A， Nemati R， Sadeghipour Y， et al. Mesenchymal stromal cells（MSCs） for neurodegenerative disease:A promising frontier［J］. Eur J Cell Biol， 2020， 99（6）:151097. doi:10.1016/j.ejcb.2020.151097.
27	Magota H， Sasaki M， Kataoka-Sasaki Y， et al. Intravenous infusion of mesenchymal stem cells delays disease progression in the SOD1G93A transgenic amyotrophic lateral sclerosis rat model［J］. Brain Res， 2021，1757:147296.
28	Magota H， Sasaki M， Kataoka-Sasaki Y， et al. Repeated infusion of mesenchymal stem cells maintain the condition to inhibit deteriorated motor function， leading to an extended lifespan in the SOD1G93A rat model of amyotrophic lateral sclerosis［J］. Mol Brain， 2021， 14（1）:76.doi:10.1186/s13041-021-00787-6.
29	Andjus P， Kosanovic M， Milicevic K， et al. Extracellular vesicles as innovative tool for diagnosis，regeneration and protection against neurological damage［J］. Int J Mol Sci， 2020， 21（18）:6859. doi:10.3390/ijms21186859.
30	Sykova E， Cizkova D， Kubinova S. Mesenchymal stem cells in treatment of spinal cord injury and amyotrophic lateral sclerosis［J］.Front Cell Dev Biol， 2021， 9:695900.doi:10.3389/fcell.2021.695900.
31	Bonafede R， Mariotti R. ALS pathogenesis and therapeutic approaches:the role of mesenchymal stem cells and extracellular vesicles［J］. Front Cell Neurosci， 2017， 11:80. doi:10.3389/fncel.2017.00080.
32	Bonafede R， Scambi I， Peroni D， et al. Exosome derived from murine adipose-derived stromal cells: Neuroprotective effect on in vitro model of amyotrophic lateral sclerosis［J］. Exp Cell Res， 2016， 340（1）:150-158.
33	Bonafede R， Brandi J， Manfredi M， et al.The anti-apoptotic effect of ASC-exosomes in an in vitro ALS model and their proteomic analysis［J］. Cells， 2019， 8（9）:1087. doi:10.3390/cells8091087.
34	Lee M， Ban JJ， Kim KY， et al. Adipose-derived stem cell exosomes alleviate pathology of amyotrophic lateral sclerosis in vitro［J］. Biochem Biophys Res Commun， 2016， 479（3）:434-439.
35	Kim MJ， Vargas MR， Harlan BA， et al.Nitration and glycation turn mature NGF into a toxic factor for motor neurons: a role for p75（NTR）and RAGE signaling in ALS［J］. Antioxid Redox Signal， 2018，28（18）:1587-1602.
36	Han Q， Ordaz JD， Liu NK， et al. Descending motor circuitry required for NT-3 mediated locomotor recovery after spinal cord injury in mice［J］. Nat Commun， 2019， 10（1）:5815.doi:10.1038/s41467-019-13854-3.
37	Keefe KM， Sheikh IS， Smith GM. Targeting neurotrophins to specific populations of neurons:NGF， BDNF， and NT-3 and their relevance for treatment of spinal cord injury［J］. Int J Mol Sci， 2017， 18（3）:548.doi:10.3390/ijms18030548.
38	Mazzini L， Gelati M， Profico DC， et al. Human neural stem cell transplantation in ALS:initial results from a phase I trial［J］. J Transl Med， 2015， 13:17. doi:10.1186/s12967-014-0371-2.
39	Tadesse T， Gearing M， Senitzer D， et al. Analysis of graft survival in a trial of stem cell transplant in ALS［J］. Ann Clin Transl Neurol， 2014，1（11）:900-908.
40	Popescu IR， Nicaise C， Liu S， et al. Neural progenitors derived from human induced pluripotent stem cells survive and differentiate upon transplantation into a rat model of amyotrophic lateral sclerosis［J］.Stem Cells Transl Med， 2013， 2（3）:167-174.
41	Nizzardo M， Simone C， Rizzo F， et al. Minimally invasive transplantation of iPSC-derived ALDHhiSSCloVLA4+ neural stem cells effectively improves the phenotype of an amyotrophic lateral sclerosis model［J］. Hum Mol Genet， 2014， 23（2）:342-354.
42	Nizzardo M， Bucchia M， Ramirez A， et al. iPSC-derived LewisX+CXCR4+beta1-integrin+ neural stem cells improve the amyotrophic lateral sclerosis phenotype by preserving motor neurons and muscle innervation in human and rodent models［J］. Hum Mol Genet， 2016， 25（15）:3152-3163.
43	Kondo T， Funayama M， Tsukita K， et al.Focal transplantation of human iPSC-derived glial-rich neural progenitors improves lifespan of ALS mice［J］. Stem Cell Reports， 2014， 3（2）:242-249.
44	北京医学会医学遗传学分会，北京罕见病诊疗与保障学会. 脊髓性肌萎缩症遗传学诊断专家共识［J］. 中华医学杂志， 2020，（40）:3130-3140.
45	Adami R， Bottai D. Spinal muscular atrophy modeling and treatment advances by induced pluripotent stem cells sStudies［J］. Stem Cell Rev Rep， 2019， 15（6）:795-813.
46	Birnkrant DJ， Bushby K， Bann CM， et al. Diagnosis and management of Duchenne muscular dystrophy， part 3:primary care， emergency management， psychosocial care， and transitions of care across the lifespan［J］. Lancet Neurol， 2018， 17（5）:445-455.
47	Flanigan KM.Duchenne and Becker muscular dystrophies［J］. Neurol Clin， 2014， 32（3）:671-688.
48	Chang NC， Sincennes MC， Chevalier FP， et al. The dystrophin glycoprotein complex regulates the epigenetic activation of muscle stem cell commitment［J］.Cell Stem Cell，2018，22（5）:755-768.
49	Dumont NA， Wang YX， von Maltzahn J， et al. Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division［J］.Nat Med， 2015， 21（12）:1455-1463.
50	Wang YX， Feige P， Brun CE， et al. EGFR-aurka signaling rescues polarity and regeneration defects in dystrophin-deficient muscle stem cells by increasing asymmetric divisions［J］. Cell Stem Cell， 2019，24（3）:419-432.
51	Shoji E， Sakurai H， Nishino T， et al. Early pathogenesis of duchenne muscular dystrophy modelled in patient-derived human induced pluripotent stem cells［J］. Sci Rep， 2015， 5:12831. doi:10.1038/srep12831.
52	Chemello F， Chai AC， Li H， et al. Precise correction of duchenne muscular dystrophy exon deletion mutations by base and prime editing［J］. Sci Adv， 2021， 7（18）:eabg4910. doi:10.1126/sciadv.abg4910.
53	Sun C， Choi IY， Rovira GY， et al. Duchenne muscular dystrophy hiPSC-derived myoblast drug screen identifies compounds that ameliorate disease in mdx mice［J］. JCI Insight， 2020， 5（11）:e134287.doi:10.1172/jci.insight.134287.
54	Lin B， Li Y， Han L， et al. Modeling and study of the mechanism of dilated cardiomyopathy using induced pluripotent stem cells derived from individuals with duchenne muscular dystrophy［J］. Dis Model Mech， 2015， 8（5）:457-466.
55	Al TZ， immerman JF， Rao J， et al. Prednisolone rescues duchenne muscular dystrophy phenotypes in human pluripotent stem cell-derived skeletal muscle in vitro［J］. Proc Natl Acad Sci USA， 2021， 118（28）:e2022960118.doi: 10.1073/pnas.2022960118.
56	Ebrahimi M， Lad H， Fusto A， et al. De novo revertant fiber formation and therapy testing in a 3D culture model of Duchenne muscular dystrophy skeletal muscle［J］. Acta Biomater， 2021， 132:227-244.
57	Min YL， Li H， Rodriguez-Caycedo C， et al. CRISPR-Cas9 corrects Duchenne muscular dystrophy exon 44 deletion mutations in mice and human cells［J］. Sci Adv， 2019， 5（3）:eaav4324. doi:10.1126/sciadv.aav4324.
58	Gros J， Manceau M， Thome V， et al. A common somitic origin for embryonic muscle progenitors and satellite cells［J］. Nature， 2005，435（7044）:954-958.
59	Picard CA， Marcelle C. Two distinct muscle progenitor populations coexist throughout amniote development［J］. Dev Biol， 2013， 373（1）:141-148.
60	Motohashi N， Asakura Y， Asakura A. Isolation，culture，and transplantation of muscle satellite cells［J］. J Vis Exp， 2014（86）:50846.doi:10.3791/50846.
61	Abujarour R， Bennett M， Valamehr B， et al. Myogenic differentiation of muscular dystrophy-specific induced pluripotent stem cells for use in drug discovery［J］. Stem Cells Transl Med， 2014， 3（2）:149-160.
62	Shoji E， Woltjen K， Sakurai H. Directed myogenic differentiation of human induced pluripotent stem cells［J］. Methods Mol Biol， 2016，1353:89-99.
63	Tanaka A， Woltjen K， Miyake K， et al. Efficient and reproducible myogenic differentiation from human iPS cells:prospects for modeling Miyoshi Myopathy in vitro［J］. PLoS One， 2013， 8（4）:e61540.doi:10.1371/journal.pone.0061540.
64	Shelton M， Kocharyan A， Liu J， et al. Robust generation and expansion of skeletal muscle progenitors and myocytes from human pluripotent stem cells［J］. Methods， 2016， 101:73-84.
65	Choi I Y， Lim H， Estrellas K， et al. Concordant but varied phenotypes among duchenne muscular dystrophy patient-specific myoblasts derived using a human iPSC-based model［J］. Cell Rep， 2016，15（10）:2301-2312.
66	卜碧，李悦.强直性肌营养不良［J］.中华神经科杂志， 2019， 52（8）:654-658.
67	Kawada R， Jonouchi T， Kagita A， et al. Establishment of quantitative and consistent in vitro skeletal muscle pathological models of myotonic dystrophy type 1 using patient-derived iPSCs［J］. Sci Rep， 2023，13（1）:94. doi: 10.1038/s41598-022-26614-z.
68	Xiao H， Wu K， Liang X， et al. Clinical efficacy and safety of eculizumab for treating myasthenia gravis［J］. Front Immunol， 2021，12:715036.doi:10.3389/fimmu.2021.715036.
69	Steinbeck JA， Jaiswal MK， Calder EL， et al. Functional connectivity under optogenetic control allows modeling of human neuromuscular disease［J］. Cell Stem Cell， 2016， 18（1）:134-143.
70	Afshar BM， Lippmann ES， Mulcahy B， et al. A 3D culture model of innervated human skeletal muscle enables studies of the adult neuromuscular junction［J］. Elife， 2019， 8:e44530. doi: 10.7554/eLife.44530.
71	Faustino MJ， Fischer C， Urzi A， et al. Self-Organizing 3D human trunk neuromuscular organoids［J］. Cell Stem Cell， 2020， 26（2）:172-186.
72	Sudres M， Maurer M， Robinet M， et al. Preconditioned mesenchymal stem cells treat myasthenia gravis in a humanized preclinical mode［J］.JCI Insight， 2017， 2（7）:e89665. doi:10.1172/jci.insight.89665.
73	Yu J， Zheng C， Ren X， et al. Intravenous administration of bone marrow mesenchymal stem cells benefits experimental autoimmune myasthenia gravis mice through an immunomodulatory action［J］.Scand J Immunol， 2010， 72（3）:242-249.
74	Hakansson I， Sandstedt A， Lundin F， et al. Successful autologous haematopoietic stem cell transplantation for refractory myasthenia gravis-a case report［J］. Neuromuscul Disord， 2017， 27（1）:90-93.
75	Sossa MC， Pena AM， Salazar LA， et al. Autologous hematopoietic stem cell transplantation in a patient with refractory seropositive myasthenia gravis:a case report［J］. Neuromuscul Disord， 2019， 29（2）:142-145.
76	Haenseler W， Sansom SN， Buchrieser J， et al. A highly efficient human pluripotent stem cell microglia model displays a neuronal-co-culturespecific expression profile and inflammatory response［J］. Stem Cell Reports， 2017， 8（6）:1727-1742.
77	Enright HA， Lam D， Sebastian A， et al. Functional and transcriptional characterization of complex neuronal co-cultures［J］. Sci Rep， 2020，10（1）:11007. doi:10.1038/s41598-020-67691-2.
78	Smethurst P， Risse E， Tyzack GE， et al. Distinct responses of neurons and astrocytes to TDP-43 proteinopathy in amyotrophic lateral sclerosis［J］. Brain， 2020， 143（2）:430-440.
79	Yamanaka S. Induced pluripotent stem cells: past， present， and future［J］. Cell Stem Cell， 2012， 10（6）:678-684.
80	Kilpinen， Goncalves A， Leha A， et al. Common genetic variation drives molecular heterogeneity in human iPSCs［J］. Nature， 2017，546（7658）:370-375.
81	Keenan AB， Jenkins SL， Jagodnik KM， et al. The library of integrated network-based cellular signatures NIH program:system-level cataloging of human cells response to perturbations［J］. Cell Syst， 2018，6（1）:13-24.
82	Thiry L， Hamel R， Pluchino S， et al.Characterization of human iPSC-derived spinal motor neurons by single-cell RNA sequencing［J］.Neuroscience， 2020， 450:57-70.
83	Ho R， Workman MJ， Mathkar P， et al. Cross-comparison of human iPSC motor neuron models of familial and sporadic ALS reveals early and convergent transcriptomic disease signatures［J］.Cell Syst， 2021，12（2）:159-175.
84	Kiskinis E， Sandoe J， Williams LA， et al. Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1［J］. Cell Stem Cell， 2014， 14（6）:781-795.
85	Shi Y， Lin S， Staats KA， et al.Haploinsufficiency leads to neurodegeneration in C9ORF72 ALS/FTD human induced motor neurons［J］. Nat Med， 2018， 24（3）:313-325.
86	Rodrigues DC， Mufteev M， Weatheritt RJ， et al. Shifts in ribosome engagement impact key gene sets in neurodevelopment and ubiquitination in rett syndrome［J］. Cell Rep， 2020， 30（12）:4179-4196.
87	Guo W， Fumagalli L， Prior R， et al. Current advances and limitations in modeling ALS/FTD in a dish using induced pluripotent stem cells［J］.Front Neurosci， 2017， 11:671. doi: 10.3389/fnins.2017.00671.
88	Miller JD， Ganat YM， Kishinevsky S， et al. Human iPSC-based modeling of late-onset disease via progerin-induced aging［J］. Cell Stem Cell， 2013， 13（6）:691-705.
89	Studer L， Vera E Cornacchia D. Programming and reprogramming cellular age in the era of induced pluripotency［J］. Cell Stem Cell， 2015，16（6）:591-600.
90	Hautbergue GM， Castelli LM， Ferraiuolo L， et al. SRSF1-dependent nuclear export inhibition of C9ORF72 repeat transcripts prevents neurodegeneration and associated motor deficits［J］. Nat Commun，2017， 8:16063. doi: 10.1038/ncomms16063.
91	Mertens J， Paquola A， Ku M， et al. Directly reprogrammed human neurons retain aging-associated transcriptomic signatures and reveal age-related nucleocytoplasmic defects［J］.Cell Stem Cell， 2015，17（6）:705-718.
92	Varcianna A， Myszczynska MA， Castelli LM， et al. Micro-RNAs secreted through astrocyte-derived extracellular vesicles cause neuronal network degeneration in C9orf72 ALS［J］. EBio Medicine， 2019，40:626-635.

[1]	Xiaoling Tie, Yi Liu, Ying Yang, Fengyu Che. Clinical features and genetic analysis of Rubinstein-Taybi syndrome：three cases report and literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2024, 20(04): 452-459.
[2]	Hexuan Zhang, Xue Yang, Lyujin Wang, Linjie Li, Xingyu Liu. Screening and genetic mutation analysis of glucose-6-phosphate dehydrogenase deficiency in neonates [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2024, 20(02): 200-208.
[3]	Ming Wu, Fenhua Zhu, Danru Liu, Yeheng Yu, Tong Lin, Jian Li. Children mucolipidosis caused by GNPTAB/GNPTG gene mutations: two cases report and literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2024, 20(02): 185-191.
[4]	Tiantian Chen, Xiaodong Wang, Haiyan Yu. Pregnancy outcome of twin pregnancy with Gitelman syndrome: a case report and literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2023, 19(05): 559-568.
[5]	Lulan Kan, Maoqiang Tian, Yimi Tang. Children with mild Gitelman syndrome presenting with recurrent abdominal pain: a case report and literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2023, 19(04): 473-479.
[6]	Jialin Mu, Xuefei Leng, Fei Tian, Lina Wang, Zhihong Chen. Sotos syndeome with a novel mutation in NSD1 gene: a case report and domestic literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2022, 18(06): 692-702.
[7]	Xufeng Luo, Jianxiang Liao, Zhiqiang Luo, Jing Duan, Yongli Li, Jianfang Xu, Li Chen. Na⁺ channel blockers in treatment of early-onset epileptic encephalopathy caused by SCN2A gene variation: a case report and literature review [J]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2022, 18(05): 585-590.
[8]	Yutao Yuan, Jinlin Xing, Kefei Xie, Kai Yin. Correlation between CT findings and BRAF^V600E gene mutation and central lymph node metastasis in papillary thyroid carcinoma [J]. Chinese Journal of Operative Procedures of General Surgery(Electronic Edition), 2023, 17(06): 611-614.
[9]	Yukang Wu, Jiuhong Kang. Application of pluripotent stem cells in cardiac development and disease research [J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2022, 12(06): 378-382.
[10]	Kai Yan, Yong Fu, Zhengtao Zhang. Predictive model of therapeutic effect of middle and advanced liver cancer and research progress of organoid models of liver cancer [J]. Chinese Journal of Hepatic Surgery(Electronic Edition), 2023, 12(03): 348-351.
[11]	Yao Yao, Yang Gao, Junqi Shan, Xinyu Li, Wei Han, Zengjun Li, Yanlai Sun. A case report of c.531+6T>G heterozygous mutation in familial adenomatous polyposis [J]. Chinese Journal of Colorectal Diseases(Electronic Edition), 2024, 13(01): 72-77.
[12]	Dayang Zhou, Chang Liu, Jian Huang, Ning Xu, Xiang Ji, Kexin Yang, Jibang Peng, Hai Pan, Wenjing Xu, Zhu Zhu. A casereport of BRCA1 p.R166fs mutation in colon cancer [J]. Chinese Journal of Colorectal Diseases(Electronic Edition), 2024, 13(01): 68-71.
[13]	Donglei Zhang, Xiaoyan Liu, Sanyun Wu, Yi Zhou, Xian Zhang. Clinical and genetic analysis of a inherit factor Ⅻ deficiency pedigree and analysis of factor Ⅻ deficiency in the Chinese population [J]. Chinese Journal of Clinical Laboratory Management(Electronic Edition), 2024, 12(03): 162-169.
[14]	Teng Zhang, Yanling Tao. A case of secondary myelodysplastic syndrome in a patient with Shwachman-Diamond syndrome and literature review [J]. Chinese Journal of Diagnostics(Electronic Edition), 2024, 12(03): 178-182.
[15]	Qian Wang, Yongping Wang, Xinpei Li, Chengyan Yang, Hui Xu, Fengjuan Sun, Yaping Liu. Diagnostic characteristics of hypokalemia with gene mutations [J]. Chinese Journal of Diagnostics(Electronic Edition), 2023, 11(02): 115-119.

Please choose a citation manager

Content to export