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Research ArticleInflammation, Immunopharmacology, and Asthma

NLRP3 Inflammasome Involvement in the Organ Damage and Impaired Spermatogenesis Induced by Testicular Ischemia and Reperfusion in Mice

Letteria Minutoli, Pietro Antonuccio, Natasha Irrera, Mariagrazia Rinaldi, Alessandra Bitto, Herbert Marini, Gabriele Pizzino, Carmelo Romeo, Antonina Pisani, Giuseppe Santoro, Domenico Puzzolo, Carlo Magno, Francesco Squadrito, Antonio Micali and Domenica Altavilla
Journal of Pharmacology and Experimental Therapeutics December 2015, 355 (3) 370-380; DOI: https://doi.org/10.1124/jpet.115.226936
Letteria Minutoli
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Pietro Antonuccio
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Natasha Irrera
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Mariagrazia Rinaldi
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Alessandra Bitto
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Herbert Marini
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Gabriele Pizzino
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Carmelo Romeo
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Antonina Pisani
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Giuseppe Santoro
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Domenico Puzzolo
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Carlo Magno
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Francesco Squadrito
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Antonio Micali
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Domenica Altavilla
Department of Clinical and Experimental Medicine, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (L.M., N.I., M.R., A.B., H.M., G.P., F.S.); Department of Paediatric, Gynaecological, Microbiological, and Biomedical Sciences, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (P.A., C.R., D.A.); Department of Biomedical Sciences and Morphofunctional Imaging, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (A.P., G.S., D.P., A.M.); and Department of Human Pathology, University of Messina, Azienda Ospedaliera Universitaria Policlinico “G. Martino”, Messina, Italy (C.M.)
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Abstract

We investigated the role of the nucleotide-binding oligomerization domain (NOD)-like receptor family pyrin domain containing 3 (NLRP3) inflammasome during testis ischemia and reperfusion injury (TI/R) in wild-type (WT) and NLRP3 knock-out (KO) mice. WT and KO mice underwent 1 hour testicular ischemia followed by 4 hours and 1 and 7 days of reperfusion or a sham TI/R. Furthermore, two groups of WT mice were treated at the beginning of reperfusion and up to 7 days with two inflammasome inhibitors, BAY 11-7082 (20 mg/kg i.p.) or Brilliant Blue G (45.5 mg/kg i.p.), or vehicle. Animals were killed with a pentobarbital sodium overdose at 4 hours and 1 and 7 days, and bilateral orchidectomies were performed. Biochemical and morphologic studies were carried out in all groups. TI/R in WT mice significantly increased caspase-1 and interleukin (IL)-1β mRNA after 4 hours and IL-18 mRNA at 1 day of reperfusion (P ≤ 0.05). There was also a significant increase in caspase-3 and terminal deoxynucleotidyl transferase–mediated digoxigenin-deoxyuridine nick-end labeling–positive cells, marked histologic damage, and altered spermatogenesis in WT mice in both testes after 1 and 7 days of reperfusion. KO TI/R mice, WT TI/R BAY 11-7082, and Brilliant Blue G treated mice showed a significant reduced IL-1β and IL-18 mRNA expression, blunted caspase-1 and -3 expression, minor histologic damages, low terminal deoxynucleotidyl transferase–mediated digoxigenin-deoxyuridine nick-end labeling activity, and preserved spermatogenesis. These data suggest that the activation of NLRP3 plays a key role in TI/R, and its inhibition might represent a therapeutic target for the management of patients with unilateral testicular torsion.

Footnotes

    • Received June 17, 2015.
    • Accepted September 24, 2015.
  • This work was supported by departmental funding.

  • dx.doi.org/10.1124/jpet.115.226936.

  • Copyright © 2015 by The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 355 (3)
Journal of Pharmacology and Experimental Therapeutics
Vol. 355, Issue 3
1 Dec 2015
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Research ArticleInflammation, Immunopharmacology, and Asthma

Role of NLRP3 Inflammasome in Testicular Ischemia

Letteria Minutoli, Pietro Antonuccio, Natasha Irrera, Mariagrazia Rinaldi, Alessandra Bitto, Herbert Marini, Gabriele Pizzino, Carmelo Romeo, Antonina Pisani, Giuseppe Santoro, Domenico Puzzolo, Carlo Magno, Francesco Squadrito, Antonio Micali and Domenica Altavilla
Journal of Pharmacology and Experimental Therapeutics December 1, 2015, 355 (3) 370-380; DOI: https://doi.org/10.1124/jpet.115.226936

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Research ArticleInflammation, Immunopharmacology, and Asthma

Role of NLRP3 Inflammasome in Testicular Ischemia

Letteria Minutoli, Pietro Antonuccio, Natasha Irrera, Mariagrazia Rinaldi, Alessandra Bitto, Herbert Marini, Gabriele Pizzino, Carmelo Romeo, Antonina Pisani, Giuseppe Santoro, Domenico Puzzolo, Carlo Magno, Francesco Squadrito, Antonio Micali and Domenica Altavilla
Journal of Pharmacology and Experimental Therapeutics December 1, 2015, 355 (3) 370-380; DOI: https://doi.org/10.1124/jpet.115.226936
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