title: piRNA-associated proteins and retrotransposons are differentially expressed in murine testis and ovary of aryl hydrocarbon receptor deficient mice.
abstract: Previous studies suggested that the aryl hydrocarbon receptor (AhR) contributes to mice reproduction and fertility. However, the mechanisms involved remain mostly unknown. Retrotransposon silencing by Piwi-interacting RNAs (piRNAs) is essential for germ cell maturation and, remarkably, AhR has been identified as a regulator of murine B1-SINE retrotransposons. Here, using littermate AhR+/+and AhR-/-mice, we report that AhR regulates the general course of spermatogenesis and oogenesis by a mechanism likely to be associated with piRNA-associated proteins, piRNAs and retrotransposons. piRNA-associated proteins MVH and Miwi are upregulated in leptotene to pachytene spermatocytes with a more precocious timing in AhR-/-than in AhR+/+testes. piRNAs and transcripts from B1-SINE, LINE-1 and IAP retrotransposons increased at these meiotic stages in AhR-null testes. Moreover, B1-SINE transcripts colocalize with MVH and Miwi in leptonema and pachynema spermatocytes. Unexpectedly, AhR-/-males have increased sperm counts, higher sperm functionality and enhanced fertility than AhR+/+mice. In contrast, piRNA-associated proteins and B1-SINE and IAP-derived transcripts are reduced in adult AhR-/-ovaries. Accordingly, AhR-null female mice have lower numbers of follicles when compared with AhR+/+mice. Thus, AhR deficiency differentially affects testis and ovary development possibly by a process involving piRNA-associated proteins, piRNAs and transposable elements.
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Eva M
authors.initials: EM
authors.lastname: Rico-Leo
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Nuria
authors.initials: N
authors.lastname: Moreno-Marín
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Francisco J
authors.initials: FJ
authors.lastname: González-Rico
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Eva
authors.initials: E
authors.lastname: Barrasa
authors.affiliation: Laboratorio de Reproducción y Espermatología Equina, Hospital Veterinario, Universidad de Extremadura, Cáceres, Spain.
authors.forename: Cristina
authors.initials: C
authors.lastname: Ortega-Ferrusola
authors.affiliation: Laboratorio de Reproducción y Espermatología Equina, Hospital Veterinario, Universidad de Extremadura, Cáceres, Spain.
authors.forename: Patricia
authors.initials: P
authors.lastname: Martín-Muñoz
authors.affiliation: Departamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Luis O
authors.initials: LO
authors.lastname: Sánchez-Guardado
authors.affiliation: Departamento de Fisiología, Universidad de Salamanca, Salamanca, Spain.|Instituto de Biología Molecular y Celular del Cáncer (CSIC-Universidad de Salamanca), Salamanca, Spain.
authors.forename: Elena
authors.initials: E
authors.lastname: Llano
authors.affiliation: Servicio de Técnicas Aplicadas a las Biociencias (STAB), Universidad de Extremadura, Badajoz, Spain.
authors.forename: Alberto
authors.initials: A
authors.lastname: Alvarez-Barrientos
authors.affiliation: Servicio de Anatomía Patológica, Hospital Universitario Infanta Cristina, Badajoz 06074, Spain.
authors.forename: Ascensión
authors.initials: A
authors.lastname: Infante-Campos
authors.affiliation: Servicio de Anatomía Patológica, Hospital Universitario Infanta Cristina, Badajoz 06074, Spain.
authors.forename: Inmaculada
authors.initials: I
authors.lastname: Catalina-Fernández
authors.affiliation: Departamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Matías
authors.initials: M
authors.lastname: Hidalgo-Sánchez
authors.affiliation: Reproductive Biology Group, Division of Developmental Biology, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands.
authors.forename: Dirk G
authors.initials: DG
authors.lastname: de Rooij
authors.affiliation: Instituto de Biología Molecular y Celular del Cáncer (CSIC-Universidad de Salamanca), Salamanca, Spain.
authors.forename: Alberto M
authors.initials: AM
authors.lastname: Pendás
authors.affiliation: Laboratorio de Reproducción y Espermatología Equina, Hospital Veterinario, Universidad de Extremadura, Cáceres, Spain.
authors.forename: Fernando J
authors.initials: FJ
authors.lastname: Peña
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain.
authors.forename: Jaime M
authors.initials: JM
authors.lastname: Merino
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain pmfersal@unex.es.
authors.forename: Pedro M
authors.identifier: 0000-0003-2839-5027
authors.initials: PM
authors.lastname: Fernández-Salguero
mesh_terms: D000818:Animals; D060565:Argonaute Proteins / Q000235:genetics* / Q000378:metabolism; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics*; D053487:DEAD-box RNA Helicases / Q000235:genetics* / Q000378:metabolism; D005260:Female; D005298:Fertility; D018507:Gene Expression Regulation, Developmental; D055786:Gene Knockout Techniques; D008297:Male; D008540:Meiosis; D051379:Mice; D010053:Ovary / Q000378:metabolism*; D034741:RNA, Small Interfering / Q000378:metabolism; D018336:Receptors, Aryl Hydrocarbon / Q000235:genetics*; D018626:Retroelements / Q000235:genetics*; D013737:Testis / Q000378:metabolism*; D015854:Up-Regulation
chemical_list: D060565:Argonaute Proteins; D051792:Basic Helix-Loop-Helix Proteins; D053487:DEAD-box RNA Helicases; D034741:RNA, Small Interfering; D018336:Receptors, Aryl Hydrocarbon; D018626:Retroelements; C484722:Ahr protein, mouse; C448522:Piwil1 protein, mouse; C090864:Ddx4 protein, mouse
keywords: aryl hydrocarbon receptor; fertility; nuage proteins; ovary; repetitive elements; spermatogenesis