Microtubule‑severing protein Katanin p60 ATPase‑containing subunit A‑like 1 is involved in pole‑based spindle organization during mouse oocyte meiosis

Gao,Lei‑Lei; Xu,Fei; Jin,Zhen; Ying,Xiao‑Yan; Liu,Jin‑Wei

doi:10.3892/mmr.2019.10605

Microtubule‑severing protein Katanin p60 ATPase‑containing subunit A‑like 1 is involved in pole‑based spindle organization during mouse oocyte meiosis

Authors:
- Lei‑Lei Gao
- Fei Xu
- Zhen Jin
- Xiao‑Yan Ying
- Jin‑Wei Liu
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Affiliations: Department of Gynecology, Zhejiang Provincial People's Hospital, People's Hospital of Hangzhou Medical College, Hangzhou, Zhejiang 310014, P.R. China, Department of Gynecology, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, Zhejiang 310015, P.R. China, Reproductive Genetic Center, Suzhou Municipal Hospital, Suzhou Hospital of Nanjing, Nanjing, Jiangsu 215000, P.R. China, Department of Gynecology, The Second Affiliated Hospital, Nanjing Medical University, Nanjing, Jiangsu 210011, P.R. China
Published online on: August 22, 2019 https://doi.org/10.3892/mmr.2019.10605
Pages: 3573-3582

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Abstract

Microtubule‑severing proteins (MTSPs) are a group of microtubule‑associated proteins essential for multiple microtubule‑related processes, including mitosis and meiosis. Katanin p60 ATPase‑containing subunit A‑like 1 (p60 katanin‑like 1) is an MTSP that maintains the density of spindle microtubules at the poles in mitotic cells; however, to date, there have been no studies about its role in female meiosis. Using in vitro‑matured (IVM) oocytes as a model, it was first revealed that p60 katanin‑like 1 was predominant in the ovaries and oocytes, indicating its essential roles in oocyte meiosis. It was also revealed that p60 katanin‑like 1 was concentrated at the spindle poles and co‑localized and interacted with γ‑tubulin, indicating that it may be involved in pole organization. Next, specific siRNA was used to deplete p60 katanin‑like 1; the spindle organization was severely disrupted and characterized by an abnormal width:length ratio, multipolarity and extra aster microtubules out of the main spindles. Finally, it was determined that p60 katanin‑like 1 knockdown retarded oocyte meiosis, reduced fertilization, and caused abnormal mitochondrial distribution. Collectively, these results indicated that p60 katanin‑like 1 is essential for oocyte meiosis by ensuring the integrity of the spindle poles.

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1	Sferra A, Fattori F, Rizza T, Flex E, Bellacchio E, Bruselles A, Petrini S, Cecchetti S, Teson M, Restaldi F, et al: Defective kinesin binding of TUBB2A causes progressive spastic ataxia syndrome resembling sacsinopathy. Hum Mol Genet. 27:1892–1904. 2018. View Article : Google Scholar : PubMed/NCBI
2	Luscan R, Mechaussier S, Paul A, Tian G, Gerard X, Defoort-Dellhemmes S, Loundon N, Audo I, Bonnin S, LeGargasson JF, et al: Mutations in TUBB4B cause a distinctive sensorineural disease. Am J Hum Genet. 101:1006–1012. 2017. View Article : Google Scholar : PubMed/NCBI
3	Feng R, Sang Q, Kuang Y, Sun X, Yan Z, Zhang S, Shi J, Tian G, Luchniak A, Fukuda Y, et al: Mutations in TUBB8 and human oocyte meiotic arrest. N Engl J Med. 374:223–232. 2016. View Article : Google Scholar : PubMed/NCBI
4	Martin M and Akhmanova A: Coming into focus: Mechanisms of microtubule minus-end organization. Trends Cell Biol. 28:574–588. 2018. View Article : Google Scholar : PubMed/NCBI
5	Aher A and Akhmanova A: Tipping microtubule dynamics, one protofilament at a time. Curr Opin Cell Biol. 50:86–93. 2018. View Article : Google Scholar : PubMed/NCBI
6	Akhmanova A and Steinmetz MO: Control of microtubule organization and dynamics: Two ends in the limelight. Nat Rev Mol Cell Biol. 16:711–726. 2015. View Article : Google Scholar : PubMed/NCBI
7	Huynh W and Vale RD: Disease-associated mutations in human BICD2 hyperactivate motility of dynein-dynactin. J Cell Biol. 216:3051–3060. 2017. View Article : Google Scholar : PubMed/NCBI
8	Lewis WR, Malarkey EB, Tritschler D, Bower R, Pasek RC, Porath JD, Birket SE, Saunier S, Antignac C, Knowles MR, et al: Mutation of growth arrest specific 8 reveals a role in motile cilia function and human disease. PLoS Genet. 12:e10062202016. View Article : Google Scholar : PubMed/NCBI
9	Decker JM, Kruger L, Sydow A, Dennissen FJ, Siskova Z, Mandelkow E and Mandelkow EM: The Tau/A152T mutation, a risk factor for frontotemporal-spectrum disorders, leads to NR2B receptor-mediated excitotoxicity. EMBO Rep. 17:552–569. 2016. View Article : Google Scholar : PubMed/NCBI
10	Frickey T and Lupas AN: Phylogenetic analysis of AAA proteins. J Struct Biol. 146:2–10. 2004. View Article : Google Scholar : PubMed/NCBI
11	Vale RD: AAA proteins. Lords of the ring. J Cell Biol. 150:F13–E19. 2000. View Article : Google Scholar : PubMed/NCBI
12	Buster D, McNally K and McNally FJ: Katanin inhibition prevents the redistribution of gamma-tubulin at mitosis. J Cell Sci. 115:1083–1092. 2002.PubMed/NCBI
13	Sharp DJ and Ross JL: Microtubule-severing enzymes at the cutting edge. J Cell Sci. 125:2561–2569. 2012. View Article : Google Scholar : PubMed/NCBI
14	Zhang D, Rogers GC, Buster DW and Sharp DJ: Three microtubule severing enzymes contribute to the ‘Pacman-flux’ machinery that moves chromosomes. J Cell Biol. 177:231–242. 2007. View Article : Google Scholar : PubMed/NCBI
15	Zhang D, Grode KD, Stewman SF, Diaz-Valencia JD, Liebling E, Rath U, Riera T, Currie JD, Buster DW, Asenjo AB, et al: Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat Cell Biol. 13:361–370. 2011. View Article : Google Scholar : PubMed/NCBI
16	Srayko M, O'Toole ET, Hyman AA and Muller-Reichert T: Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol. 16:1944–1949. 2006. View Article : Google Scholar : PubMed/NCBI
17	Errico A, Ballabio A and Rugarli EI: Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet. 11:153–163. 2002. View Article : Google Scholar : PubMed/NCBI
18	Banks G, Lassi G, Hoerder-Suabedissen A, Tinarelli F, Simon MM, Wilcox A, Lau P, Lawson TN, Johnson S, Rutman A, et al: A missense mutation in Katnal1 underlies behavioural, neurological and ciliary anomalies. Mol Psychiatry. 23:713–722. 2018. View Article : Google Scholar : PubMed/NCBI
19	Mishra-Gorur K, Caglayan AO, Schaffer AE, Chabu C, Henegariu O, Vonhoff F, Akgümüş GT, Nishimura S, Han W, Tu S, et al: Mutations in KATNB1 cause complex cerebral malformations by disrupting asymmetrically dividing neural progenitors. Neuron. 84:1226–1239. 2014. View Article : Google Scholar : PubMed/NCBI
20	Mao CX, Xiong Y, Xiong Z, Wang Q, Zhang YQ and Jin S: Microtubule-severing protein Katanin regulates neuromuscular junction development and dendritic elaboration in Drosophila. Development. 141:1064–1074. 2014. View Article : Google Scholar : PubMed/NCBI
21	Stewart A, Tsubouchi A, Rolls MM, Tracey WD and Sherwood NT: Katanin p60-like1 promotes microtubule growth and terminal dendrite stability in the larval class IV sensory neurons of Drosophila. J Neurosci. 32:11631–11642. 2012. View Article : Google Scholar : PubMed/NCBI
22	O'Donnell L, Rhodes D, Smith SJ, Merriner DJ, Clark BJ, Borg C, Whittle B, O'Connor AE, Smith LB, McNally FJ, et al: An essential role for katanin p80 and microtubule severing in male gamete production. PLoS Genet. 8:e10026982012. View Article : Google Scholar : PubMed/NCBI
23	Smith LB, Milne L, Nelson N, Eddie S, Brown P, Atanassova N, O'Bryan MK, O'Donnell L, Rhodes D, Wells S, et al: KATNAL1 regulation of sertoli cell microtubule dynamics is essential for spermiogenesis and male fertility. PLoS Genet. 8:e10026972012. View Article : Google Scholar : PubMed/NCBI
24	Chen B, Zhang Z, Sun X, Kuang Y, Mao X, Wang X, Yan Z, Li B, Xu Y, Yu M, et al: Biallelic mutations in PATL2 cause female infertility characterized by oocyte maturation arrest. Am J Hum Genet. 101:609–615. 2017. View Article : Google Scholar : PubMed/NCBI
25	Nguyen AL, Marin D, Zhou A, Gentilello AS, Smoak EM, Cao Z, Fedick A, Wang Y, Taylor D, Scott RT Jr, et al: Identification and characterization of Aurora kinase B and C variants associated with maternal aneuploidy. Mol Hum Reprod. 23:406–416. 2017. View Article : Google Scholar : PubMed/NCBI
26	Caburet S, Arboleda VA, Llano E, Overbeek PA, Barbero JL, Oka K, Harrison W, Vaiman D, Ben-Neriah Z, García-Tuñón I, et al: Mutant cohesin in premature ovarian failure. N Engl J Med. 370:943–949. 2014. View Article : Google Scholar : PubMed/NCBI
27	Sonbuchner TM, Rath U and Sharp DJ: KL1 is a novel microtubule severing enzyme that regulates mitotic spindle architecture. Cell Cycle. 9:2403–2411. 2010. View Article : Google Scholar : PubMed/NCBI
28	Pimenta-Marques A, Bento I, Lopes CA, Duarte P, Jana SC and Bettencourt-Dias M: A mechanism for the elimination of the female gamete centrosome in Drosophila melanogaster. Science. 353:aaf48662016. View Article : Google Scholar : PubMed/NCBI
29	Connolly AA, Osterberg V, Christensen S, Price M, Lu C, Chicas-Cruz K, Lockery S, Mains PE and Bowerman B: Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1. Mol Biol Cell. 25:1298–1311. 2014. View Article : Google Scholar : PubMed/NCBI
30	Kim JS, Kim EJ, Oh JS, Park IC and Hwang SG: CIP2A modulates cell-cycle progression in human cancer cells by regulating the stability and activity of Plk1. Cancer Res. 73:6667–6678. 2013. View Article : Google Scholar : PubMed/NCBI
31	Patel H, Zich J, Serrels B, Rickman C, Hardwick KG, Frame MC and Brunton VG: Kindlin-1 regulates mitotic spindle formation by interacting with integrins and Plk-1. Nat Commun. 4:20562013. View Article : Google Scholar : PubMed/NCBI
32	Eot-Houllier G, Venoux M, Vidal-Eychenie S, Hoang MT, Giorgi D and Rouquier S: Plk1 regulates both ASAP localization and its role in spindle pole integrity. J Biol Chem. 285:29556–29568. 2010. View Article : Google Scholar : PubMed/NCBI
33	Zhou CX, Shi LY, Li RC, Liu YH, Xu BQ, Liu JW, Yuan B, Yang ZX, Ying XY and Zhang D: GTPase-activating protein Elmod2 is essential for meiotic progression in mouse oocytes. Cell Cycle. 16:852–860. 2017. View Article : Google Scholar : PubMed/NCBI
34	Zhang XL, Liu P, Yang ZX, Zhao JJ, Gao LL, Yuan B, Shi LY, Zhou CX, Qiao HF, Liu YH, et al: Pnma5 is essential to the progression of meiosis in mouse oocytes through a chain of phosphorylation. Oncotarget. 8:96809–96825. 2017.PubMed/NCBI
35	Dinkelmann MV, Zhang H, Skop AR and White JG: SPD-3 is required for spindle alignment in Caenorhabditis elegans embryos and localizes to mitochondria. Genetics. 177:1609–1620. 2007. View Article : Google Scholar : PubMed/NCBI
36	Kong XW, Wang DH, Zhou CJ, Zhou HX and Liang CG: Loss of function of KIF1B impairs oocyte meiotic maturation and early embryonic development in mice. Mol Reprod Dev. 83:1027–1040. 2016. View Article : Google Scholar : PubMed/NCBI
37	Maccarinelli F, Regoni M, Carmona F, Poli M, Meyron-Holtz EG and Arosio P: Mitochondrial ferritin deficiency reduces male fertility in mice. Reprod Fertil Dev. 29:2005–2010. 2017. View Article : Google Scholar : PubMed/NCBI
38	Wang M, Huang YP, Wu H, Song K, Wan C, Chi AN, Xiao YM and Zhao XY: Mitochondrial complex I deficiency leads to the retardation of early embryonic development in Ndufs4 knockout mice. Peer J. 5:e33392017. View Article : Google Scholar : PubMed/NCBI
39	May-Panloup P, Boucret L, Chao de la Barca JM, Desquiret-Dumas V, Ferre-L'Hotellier V, Moriniere C, Descamps P, Procaccio V and Reynier P: Ovarian ageing: The role of mitochondria in oocytes and follicles. Hum Reprod Update. 22:725–743. 2016. View Article : Google Scholar : PubMed/NCBI
40	Ben-Meir A, Burstein E, Borrego-Alvarez A, Chong J, Wong E, Yavorska T, Naranian T, Chi M, Wang Y, Bentov Y, et al: Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell. 14:887–895. 2015. View Article : Google Scholar : PubMed/NCBI
41	Bartolak-Suki E, Imsirovic J, Nishibori Y, Krishnan R and Suki B: Regulation of mitochondrial structure and dynamics by the cytoskeleton and mechanical factors. Int J Mol Sci. 18(pii): E18122017. View Article : Google Scholar : PubMed/NCBI
42	Fu L, Dong Q, He J, Wang X, Xing J, Wang E, Qiu X and Li Q: SIRT4 inhibits malignancy progression of NSCLCs, through mitochondrial dynamics mediated by the ERK-Drp1 pathway. Oncogene. 36:2724–2736. 2017. View Article : Google Scholar : PubMed/NCBI
43	Wang C, Du W, Su QP, Zhu M, Feng P, Li Y, Zhou Y, Mi N, Zhu Y, Jiang D, et al: Dynamic tubulation of mitochondria drives mitochondrial network formation. Cell Res. 25:1108–1120. 2015. View Article : Google Scholar : PubMed/NCBI
44	Fu C, Jain D, Costa J, Velve-Casquillas G and Tran PT: mmb1p binds mitochondria to dynamic microtubules. Curr Biol. 21:1431–1439. 2011. View Article : Google Scholar : PubMed/NCBI