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Among the genetic causes are mutations of matrix peptidase CLPP, which trigger additional azoospermia. Here, we analyzed the impact of CLPP deficiency on male mouse meiosis stages. Histology, immunocytology, different OMICS and biochemical approaches, and RT-qPCR were employed in CLPP-null mouse testis. Meiotic chromosome pairing and synapsis proceeded normally. However, the foci number of the crossover marker MLH1 was slightly reduced, and foci persisted in diplotene, most likely due to premature desynapsis, associated with an accumulation of the DNA damage marker \u03b3H2AX. No meiotic M-phase cells were detected. Proteome profiles identified strong deficits of proteins involved in male meiotic prophase (HSPA2, SHCBP1L, DMRT7, and HSF5), versus an accumulation of AURKAIP1. Histone H3 cleavage, mtDNA extrusion, and cGAMP increase suggested innate immunity activation. However, the deletion of downstream STING\/IFNAR failed to alleviate pathology. As markers of underlying mitochondrial pathology, we observed an accumulation of PRLTS proteins ERAL1, PEO1, and HARS2. We propose that the loss of CLPP leads to the extrusion of mitochondrial nucleotide-binding proteins to cytosol and nucleus, affecting late meiotic prophase progression, and causing cell death prior to M-phase entry. This phenotype is more severe than in mito-mice or mutator-mice.<\/jats:p>","DOI":"10.3390\/cells12010052","type":"journal-article","created":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T03:02:15Z","timestamp":1671764535000},"page":"52","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["CLPP Depletion Causes Diplotene Arrest; Underlying Testis Mitochondrial Dysfunction Occurs with Accumulation of Perrault Proteins ERAL1, PEO1, and HARS2"],"prefix":"10.3390","volume":"12","author":[{"given":"Jana","family":"Key","sequence":"first","affiliation":[{"name":"Experimental Neurology, Medical Faculty, Goethe University, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suzana","family":"Gispert","sequence":"additional","affiliation":[{"name":"Experimental Neurology, Medical Faculty, Goethe University, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9742-9580","authenticated-orcid":false,"given":"Lieke","family":"Koornneef","sequence":"additional","affiliation":[{"name":"Department of Developmental Biology, Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands"},{"name":"Oncode Institute, Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esther","family":"Sleddens-Linkels","sequence":"additional","affiliation":[{"name":"Department of Developmental Biology, Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aneesha","family":"Kohli","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry II, Goethe University Medical School, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sylvia","family":"Torres-Odio","sequence":"additional","affiliation":[{"name":"Department of Microbial Pathogenesis and Immunology, College of Medicine, Health Science Center, Texas A&M University, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriele","family":"Koepf","sequence":"additional","affiliation":[{"name":"Experimental Neurology, Medical Faculty, Goethe University, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shady","family":"Amr","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry II, Goethe University Medical School, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1551-6865","authenticated-orcid":false,"given":"Marina","family":"Reichlmeir","sequence":"additional","affiliation":[{"name":"Experimental Neurology, Medical Faculty, Goethe University, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick N.","family":"Harter","sequence":"additional","affiliation":[{"name":"Institute of Neurology (Edinger-Institute), University Hospital Frankfurt, Goethe University, Heinrich-Hoffmann-Strasse 7, 60528 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2884-6895","authenticated-orcid":false,"given":"Andrew Phillip","family":"West","sequence":"additional","affiliation":[{"name":"Department of Microbial Pathogenesis and Immunology, College of Medicine, Health Science Center, Texas A&M University, Bryan, TX 77807, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3832-090X","authenticated-orcid":false,"given":"Christian","family":"M\u00fcnch","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry II, Goethe University Medical School, 60590 Frankfurt am Main, Germany"},{"name":"Frankfurt Cancer Institute, 60590 Frankfurt am Main, Germany"},{"name":"Cardio-Pulmonary Institute, 35392 Gie\u00dfen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Willy M.","family":"Baarends","sequence":"additional","affiliation":[{"name":"Department of Developmental Biology, Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"Auburger","sequence":"additional","affiliation":[{"name":"Experimental Neurology, Medical Faculty, Goethe University, 60590 Frankfurt am Main, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"4871","DOI":"10.1093\/hmg\/ddt338","article-title":"Loss of mitochondrial peptidase Clpp leads to infertility, hearing loss plus growth retardation via accumulation of CLPX, mtDNA and inflammatory factors","volume":"22","author":"Gispert","year":"2013","journal-title":"Hum. 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