The Italian Wall Lizard Podarcis siculus as a Biological Model for Research in Male Reproductive Toxicology
Abstract
:1. Introduction
2. Podarcis siculus Reproductive Cycle
3. Podarcis siculus Spermatogenesis
3.1. Testis Morphology
3.2. Control of Spermatogenesis
4. Impairment of Spermatogenesis
4.1. Imbalance of Physiological Factors That Control Spermatogenesis
4.2. Effects of Pesticides and Herbicides on Spermatogenesis
4.3. Endocrine Disrupting Compounds (EDCs)
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Corti, C.; Biaggini, M.; Capula, M. Podarcis siculus (Rafinesque–Schmaltz, 1810). In Fauna d’ Italia: Reptilia; Corti, C., Capula, M., Luiselli, L., Razzetti, E., Sindaco, R., Eds.; Edizioni Calderini: Bologna, Italy, 2011; Volume 4, pp. 407–417. [Google Scholar]
- Adamopoulou, C.; Paburkefilis, P. Eaten or beaten? Severe population decline of the invasive lizard Podarcis siculus (Rafinesque-Schmaltz, 1810) after an eradication project in Athens, Greece. Herpetozoa 2019, 32, 165–169. [Google Scholar] [CrossRef] [Green Version]
- Burke, R.L.; Hussain, A.A.; Storey, J.M.; Kenneth, B.; Storey, K.B. Freeze Tolerance and Supercooling Ability in the Italian Wall Lizard, Podarcis sicula, Introduced to Long Island, New York. Copeia 2002, 3, 836–842. [Google Scholar] [CrossRef]
- Tuniyev, B.S.; Shagarov, L.M.; Arribas, O.J. Podarcis siculus (Reptilia: Sauria: Lacertidae), a new alien species for Russian fauna. Proc. Zool. Inst. RAS 2020, 324, 364–370. [Google Scholar] [CrossRef]
- Grano, M.; Cattaneo, C.; Cattaneo, A. A case of cannibalism in Podarcis siculus campestris De Betta, 1857 (Reptilia, Lacertidae). Biodivers. J. 2011, 2, 151–152. [Google Scholar]
- Rondinini, C.; Battistoni, A.; Peronace, V.; Teofili, C. Lista Rossa IUCN dei Vertebrati Italiani; Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare: Roma, Italy, 2013. [Google Scholar]
- Sciarrillo, R.; Falzarano, A.; Gallicchio, V.; Mileo, A.; De Falco, M. Toxic effects on the thyroid gland of adult male lizards (Podarcis siculus) in contact with soil contaminated with polychlorinated biphenyls (PCBs). Int. J. Mol. Sci. 2022, 23, 4790. [Google Scholar] [CrossRef] [PubMed]
- Trinchella, F.; Cannetiello, M.; Simoniello, P.; Filosa, S.; Scudiero, R. Differential gene expression profiles in embryos of the lizard Podarcis sicula under in ovo exposure to cadmium. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2010, 151, 33–39. [Google Scholar] [CrossRef] [PubMed]
- Simoniello, P.; Trinchella, F.; Filosa, S.; Scudiero, R.; Magnani, D.; Theil, T.; Motta, C.M. Cadmium contaminated soil affects retinogenesis in lizard embryos. J. Exp. Zool. 2014, 321A, 207–219. [Google Scholar] [CrossRef] [PubMed]
- Simoniello, P.; Motta, C.M.; Scudiero, R.; Trinchella, F.; Filosa, S. Cadmium-induced teratogenicity in lizard embryos: Correlation with metallothionein gene expression. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2011, 153, 119–127. [Google Scholar] [CrossRef]
- Motta, C.M.; Tammaro, S.; Di Lorenzo, M.; Panzuto, R.; Verderame, M.; Migliaccio, V.; Simoniello, P. Spring and Fall recrudescence in Podarcis siculus ovaries: A role for progesterone. Gen. Comp. Endocrinol. 2020, 290, 113393. [Google Scholar] [CrossRef]
- Filosa, S. Biological and cytological aspects of the ovarian cycle in Lacerta sicula sicula Raf. Monit. Zool. Ital. 1973, 7, 151–165. [Google Scholar]
- Angelini, F.; Botte, V.; Boschi, R. The regulation of the reproductive cycle in Podarcis sicula sicula (Reptilia, Lacertidae): Influence on the refractory period on the springtime testicular activity. Monit. Zool. Ital. 1980, 14, 27–40. [Google Scholar]
- Angelini, F. Alcuni dati sull’ influenza della luce, della temperatura e del trattamento ormonale su ciclo sessuale annuale maschile di Lacerta s. sicula Raf. Boll. Zool. 1972, 39, 588–589. [Google Scholar]
- Angelini, F.; Botte, V.; D’Alterio, E. Autumn photothermal regimes and reproductive functions in the female lizard Podarcis S. sicula Raf. Monit. Zool. Ital. 1982, 16, 133–148. [Google Scholar]
- Lofts, B. Reptilian Reproductive Cycles and Environmental Regulators. In Environmental Endocrinology; Proceedings in Life Sciences; Assenmacher, I., Farner, D.S., Eds.; Springer: Berlin/Heidelberg, Germany, 1978. [Google Scholar] [CrossRef]
- Galgano, M.; D’Amore, C. Il ciclo sessuale annuo nel maschio di Lacerta s. sicula Raf. Monit. Zool. Ital. 1954, 62, 320–325. [Google Scholar]
- Angelini, F.; Picariello, O. The course of spermatogenesis in reptilia. Accad. Delle Sci. Fis. E Mat. 1975, 6, 62–107. [Google Scholar]
- Angelini, F.; Botte, V. Spermatogenesis in Reptiles, Dynamic and Regulatory Aspect. In Sex Origin and Evolution; Dallai, R., Ed.; Mucchi Selected Symposia and Monographs UZI: Modena, Italy, 1992; Volume 6, pp. 211–223. [Google Scholar]
- Rosati, L.; Agnese, M.; Di Lorenzo, M.; Barra, T.; Valiante, S.; Prisco, M. Spermatogenesis and regulatory factors in the wall lizard Podarcis sicula. Gen. Comp. Endocrinol. 2020, 298, 113579. [Google Scholar] [CrossRef] [PubMed]
- Angelini, F.; Picariello, O.; Botte, V. Influence of photoperiod and temperature on the testicular activity of the lizard, Lacerta sicula sicula Raf. Boll. Zool. 1976, 43, 111–123. [Google Scholar] [CrossRef] [Green Version]
- Angelini, F.; Ciarcia, G.; Botte, V. Ambient Crues and Sexual Cycle in the Lizard, Podarcis s. sicula Raf. In Endocrine Regulations as Adaptative Mechanisms to Environments; Assenmacher, I., Boissin, J., Eds.; Editions CNRS: Paris, France, 1986; pp. 227–232. [Google Scholar]
- Agnese, M.; Rosati, L.; Muriano, F.; Valiante, S.; Laforgia, V.; Andreuccetti, P.; Prisco, M. Expression of VIP and its receptors in the testis of the spotted ray Torpedo marmorata (Risso 1880). J. Mol. Neurosci. 2012, 48, 638–646. [Google Scholar] [CrossRef]
- Agnese, M.; Rosati, L.; Coraggio, F.; Valiante, S.; Prisco, M. Molecular cloning of VIP and distribution of VIP/VPACR system in the testis of Podarcis sicula. J. Etuniyevxp. Zool. A Ecol. Genet. Physiol. 2014, 321, 334–347. [Google Scholar] [CrossRef]
- Agnese, M.; Rosati, L.; Prisco, M.; Coraggio, F.; Valiante, S.; Scudiero, R.; Laforgia, V.; Andreuccetti, P. The VIP/VPACR system in the reproductive cycle of male lizard Podarcis sicula. Gen. Comp. Endocrinol. 2014, 205, 94–101. [Google Scholar] [CrossRef]
- Rosati, L.; Prisco, M.; Coraggio, F.; Valiante, S.; Scudiero, R.; Laforgia, V.; Andreuccetti, P.; Agnese, M. PACAP and PAC₁ receptor in the reproductive cycle of male lizard Podarcis sicula. Gen. Comp. Endocrinol. 2014, 205, 102–108. [Google Scholar] [CrossRef] [PubMed]
- Rosati, L.; Prisco, M.; Di Fiore, M.M.; Santillo, A.; Sciarrillo, R.; Valiante, S.; Laforgia, V.; Coraggio, F.; Andreuccetti, P.; Agnese, M. Sex steroid hormone secretion in the wall lizard Podarcis sicula testis: The involvement of VIP. J. Exp. Zool. A Ecol. Genet. Physiol. 2015, 323, 714–721. [Google Scholar] [CrossRef] [PubMed]
- Rosati, L.; Prisco, M.; Di Fiore, M.M.; Santillo, A.; Valiante, S.; Andreuccetti, P.; Agnese, M. Role of PACAP on testosterone and 17β-estradiol production in the testis of wall lizard Podarcis sicula. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2016, 191, 180–186. [Google Scholar] [CrossRef]
- Raucci, F.; D’Aniello, S.; Di Fiore, M.M. Endocrine roles of D-aspartic acid in the testis of lizard Podarcis s. sicula. J. Endocrinol. 2005, 187, 347–359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raucci, F.; Di Fiore, M.M. The reproductive activity in the testis of Podarcis s. sicula involves D-aspartic acid: A study on c-kit receptor protein, tyrosine kinase activity and PCNA protein during annual sexual cycle. Gen. Comp. Endocrinol. 2009, 161, 373–383. [Google Scholar] [CrossRef] [PubMed]
- Ciarcia, G.; Facchinetti, F.; Vallarino, M.; Pestarino, M.; Paolucci, M.; Cardone, A.; Fasano, S.; Pierantoni, R.; Genazzani, A.R. Opioid peptides and testicular activity in the lizard Podarcis s. sicula Raf. J. Endocrinol. 1994, 143, 565–571. [Google Scholar] [CrossRef]
- Ciarcia, G.; Cardone, A.; Paolucci, M.; Botte, V. In vitro effects of beta-endorphin on testicular release of androgens in the lizard Podarcis sicula Raf. Mol. Reprod. Dev. 1996, 45, 308–312. [Google Scholar] [CrossRef]
- Comitato, R.; Esposito, T.; Cerbo, G.; Angelini, F.; Varriale, B.; Cardone, A. Impairment of spermatogenesis and enhancement of testicular germ cell apoptosis induced by exogenous all-trans-retinoic acid in adult lizard Podarcis sicula. J. Exp. Zool. A Comp. Exp. Biol. 2006, 305, 288–298. [Google Scholar] [CrossRef]
- Rosati, L.; Agnese, M.; Di Fiore, M.M.; Andreuccetti, P.; Prisco, M. P450 aromatase: A key enzyme in the spermatogenesis of the Italian wall lizard, Podarcis sicula. J. Exp. Biol. 2016, 219, 2402–2408. [Google Scholar] [CrossRef] [Green Version]
- Rosati, L.; Santillo, A.; Di Fiore, M.M.; Andreuccetti, P.; Prisco, M. Testicular steroidogenic enzymes in the lizard Podarcis sicula during the spermatogenic cycle. Comptes Rendus Biol. 2017, 340, 492–498. [Google Scholar] [CrossRef]
- Knotts, L.K.; Glass, J.D. Effects of Photoperiod, Beta-Endorphin, and Naloxone on in Vitro Secretion of Testosterone in White-50 Footed Mouse (Peromyscus Leucopus) Testes. Biol. Reprod. 1988, 39, 205–212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chandrashekar, V.; Bartke, A. The influence of beta-endorphin on testicular endocrine function in adult rats. Biol. Reprod. 1992, 47, 1–5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Esposito, T.; Caccavo, M.; Cianci, A.; Cardone, A.; Angelini, F.; Varriale, B. Sequence analysis of retinoic acid receptor alpha, beta and gamma isoforms in the lizard, Podarcis sicula. J. Steroid. Biochem. Mol. Biol. 2007, 104, 143–153. [Google Scholar] [CrossRef] [PubMed]
- Saffman, E.; Lasko, P. Germline development in vertebrates and invertebrates. Cell. Mol. Life Sci. 1999, 55, 1141–1163. [Google Scholar] [CrossRef] [PubMed]
- Milani, L.; Maurizii, M.G. First evidence of Vasa expression in differentiating male germ cells of a reptile. Mol. Reprod. Dev. 2014, 81, 678. [Google Scholar] [CrossRef] [PubMed]
- Milani, L.; Maurizii, M.G. Vasa expression in spermatogenic cells during the reproductive-cycle phases of Podarcis sicula (Reptilia, Lacertidae). J. Exp. Zool. B Mol. Dev. Evol. 2015, 324, 424–434. [Google Scholar] [CrossRef]
- Carreau, S.; Silandre, D.; Bourguiba, S.; Hamden, K.; Said, L.; Lambard, S.; Galeraud-Denis, I.; Delalande, C. Estrogens and male reproduction: A new concept. Braz. J. Med. Biol. Res. 2007, 40, 761–768. [Google Scholar] [CrossRef] [Green Version]
- Carreau, S.; Bois, C.; Zanatta, L.; Silva, F.R.; Bouraima-Lelong, H.; Delalande, C. Estrogen signaling in testicular cells. Life Sci. 2011, 89, 584–587. [Google Scholar] [CrossRef]
- O’Donnell, L.; Nicholls, P.K.; O’Bryan, M.K.; McLachlan, R.I.; Stanton, P.G. Spermiation: The process of sperm release. Spermatogenesis 2011, 1, 14–35. [Google Scholar] [CrossRef]
- Andò, S.; Panno, M.L.; Ciarcia, G.; Imbrogno, E.; Buffone, M.; Beraldi, E.; Sisci, D.; Angelini, F.; Botte, V. Plasma sex hormone concentrations during the reproductive cycle in the male lizard, Podarcis s. sicula. J. Reprod. Fertil. 1990, 90, 353–360. [Google Scholar] [CrossRef]
- D’Aniello, A. D-Aspartic acid: An endogenous amino acid with an important neuroendocrine role. Brain Res. Rev. 2007, 53, 215–234. [Google Scholar] [CrossRef] [PubMed]
- Cardone, A.; Comitato, R.; Bellini, L.; Angelini, F. Effects of the aromatase inhibitor fadrozole on plasma sex steroid secretion, spermatogenesis and epididymis morphology in the lizard, Podarcis sicula. Mol. Reprod. Dev. 2002, 63, 63–70. [Google Scholar] [CrossRef] [PubMed]
- Verderame, M.; Angelini, F.; Limatola, E. Spermatogenic waves and expression of AR and ERs in germ cells of Podarcis sicula. Int. J. Zool. 2014, 2014, 965617. [Google Scholar] [CrossRef] [Green Version]
- Chieffi, P.; d’Amato, L.C.; Guarino, F.; Salvatiore, G.; Angelini, F. 17β-estradiol induces spermatogonial proliferation through mitogen-activated protein kinase (extracellular signal-regulated kinase 1/2) activity in the lizard (Podarcis s. sicula). Mol. Reprod. Dev. 2002, 61, 218–225. [Google Scholar] [CrossRef] [PubMed]
- Verderame, M.; Limatola, E.; Scudiero, R. Ectopic synthesis of vitellogenin in testis and epididymis of estrogen-treated lizard Podarcis sicula. Gen. Comp. Endocrinol. 2016, 235, 57–63. [Google Scholar] [CrossRef] [PubMed]
- Wallace, R.A. Vitellogenesis and Oocyte Growth in Nonmammalian Vertebrates. In Oogenesis; Developmental Biology; Browder, L.W., Ed.; Springer: Boston, MA, USA, 1985; Volume 1. [Google Scholar] [CrossRef]
- Verderame, M.; Scudiero, R. Estrogen-dependent, extrahepatic synthesis of vitellogenin in male vertebrates: A mini-review. Comptes Rendus Biol. 2017, 340, 139–144. [Google Scholar] [CrossRef]
- Vitiello, I.I.; Baccari, G.C.; di Matteo, L.; Rusciani, A.; Chieffi, P.; Minucci, S. Number of mast cells in the Harderian gland of the lizard Podarcis sicula sicula (Raf): The annual cycle and its relation to environmental factors and estradiol administration. Gen. Comp. Endocrinol. 1997, 107, 394–400. [Google Scholar] [CrossRef]
- Kurosawa, T.; Hiroi, H.; Momoeda, M.; Inoue, S.; Taketani, Y. Clomiphene citrate elicits estrogen agonistic/antagonistic effects differentially via estrogen receptors α and β. Endocr. J. 2010, 57, 517–521. [Google Scholar] [CrossRef] [Green Version]
- Verderame, M.; Scudiero, R.; Limatola, E. Exploring the Role of Estrogens in Lizard Spermatogenesis through the Study of 48 Clomiphene and FSH Effects. Int. J. Endocrinol. 2017, 2017, 4760638. [Google Scholar] [CrossRef] [Green Version]
- Cardone, A.; Comitato, R.; Angelini, F. Spermatogenesis, epididymis morphology and plasma sex steroid secretion in the male lizard Podarcis sicula exposed to diuron. Environ. Res. 2008, 108, 214–223. [Google Scholar] [CrossRef]
- Cardone, A. Testicular toxicity of methyl thiophanate in the Italian wall lizard (Podarcis sicula): Morphological and molecular evaluation. Ecotoxicology 2012, 21, 512–523. [Google Scholar] [CrossRef] [PubMed]
- Cardone, A. Imidacloprid induces morphological and molecular damages on testis of lizard (Podarcis sicula). Ecotoxicology 2015, 24, 94–105. [Google Scholar] [CrossRef] [PubMed]
- Verderame, M.; Chianese, T.; Rosati, L.; Scudiero, R. Molecular and Histological Effects of Glyphosate on Testicular Tissue of the Lizard Podarcis siculus. Int. J. Mol. Sci. 2022, 23, 4850. [Google Scholar] [CrossRef] [PubMed]
- Verderame, M.; Scudiero, R. How Glyphosate Impairs Liver Condition in the Field Lizard Podarcis siculus (Rafinesque-Schmaltz, 1810): Histological and Molecular Evidence. BioMed Res. Int. 2019, 2019, 4746283. [Google Scholar] [CrossRef] [Green Version]
- Lauretta, R.; Sansone, A.; Sansone, M.; Romanelli, F.; Appetecchia, M. Endocrine Disrupting Chemicals: Effects on Endocrine Glands. Front. Endocrinol. 2019, 10, 178. [Google Scholar] [CrossRef]
- Knez, J. Endocrine-disrupting chemicals and male reproductive health. Reprod. Biomed. Online 2013, 26, 440–448. [Google Scholar] [CrossRef] [Green Version]
- Diamanti-Kandarakis, E.; Bourguignon, J.P.; Giudice, L.C.; Hauser, R.; Prins, G.S.; Soto, A.M.; Zoeller, R.T.; Gore, A.C. Endocrine disrupting chemicals: An endocrine society scientific statement. Endocr. Rev. 2009, 30, 293–342. [Google Scholar] [CrossRef]
- Burgos-Aceves, A.B.; Migliaccio, V.; Di Gregorio, I.; Paolella, G.; Lepretti, M.; Faggio, C.; Lionetti, L. 1,1,1-trichloro-2,2-bis (p-chlorophenyl)-ethane (DDT) and 1,1-Dichloro-2,2-bis (p, p’-chlorophenyl) ethylene (DDE) as endocrine disruptors in human and wildlife: A possible implication of mitochondria. Environ. Toxicol. Pharmacol. 2021, 87, 103684. [Google Scholar] [CrossRef]
- Minucci, S.; Vitiello, I.I.; Marmorino, C.; Di Matteo, L.; Baccari, G.C. Mast cell-Leydig cell relationships in the testis of the lizard Podarcis s. sicula Raf: Thermal manipulation, ethane 1,2-dimethane sulphonate (EDS) and sex hormone treatment. Zygote 1995, 3, 259–264. [Google Scholar] [CrossRef]
- Verderame, M.; Limatola, E. Interferences of an environmental pollutant with estrogen-like action in the male reproductive system of the terrestrial vertebrate Podarcis sicula. Gen. Comp. Endocrinol. 2015, 213, 9–15. [Google Scholar] [CrossRef]
- Di Lorenzo, M.; Mileo, A.; Laforgia, V.; De Falco, M.; Rosati, L. Alkyphenol Exposure Alters Steroidogenesis in Male Lizard Podarcis siculus. Animals 2021, 11, 1003. [Google Scholar] [CrossRef] [PubMed]
Compound | Effects | References |
---|---|---|
Neuropeptides | Increase in hormone sex levels (testosterone and 17β-estradiol). | [20,27,28] |
D-aspartate | Increase in testosterone levels. | [29,30,46] |
β-endorphin | Reduction of testosterone levels; reduction of pituitary gonadotropin levels. | [31,32,36,37] |
Fadrozole | Inhibition of P450 aromatase. | [47] |
Tamoxifene | Reduction of mast cell number in the testis and in the Harderian gland. | [53] |
Clomiphene | Increase in 17β-estradiol levels; reduction of the thickness of the seminiferous epithelium; reduction of the secretive activity of the epididymal corpus. | [54,55] |
17 β-estradiol | Reduction of the thickness of the seminiferous epithelium; increase in connective tissue outside the tubules; production of hepatic VTG. | [49,50,52] |
Diuron | Reduction of somatic index; reduction of tubule diameter; reduction of spermatogonia meiotic cells number; hypertrophy of interstitial connective tissue; testicular inflammation; reduction of testosterone levels. | [56] |
Methylthiophanate | Decrease in the expression of androgen and estrogen receptors; reduction of germ cells in all stages of differentiation; reduction of the lumen of the seminiferous tubules. | [57] |
Imidacloprid | Block of spermatogenesis process; reduction of hormone sex levels (testosterone and 17β-estradiol); alteration in the expression of androgen and estrogen receptors. | [58] |
Glyphosate | Increase in estrogen receptor levels; alteration of Connexin 43 distribution; fibrosis in the extratubular spaces. | [59] |
EDS | Reduction of testosterone levels. | [65] |
Nonylphenol | Structural alteration of the testis and epididymis; inhibition of androgen and estrogen receptor expression in germ cells; alteration of steroidogenic enzyme distribution; increase in connective tissue in the interstitial space. | [66,67] |
Octylphenol | Structural alteration of the testis and epididymis; alteration of steroidogenic enzyme distribution; increase in connective tissue in the interstitial space. | [67] |
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Rosati, L.; Chianese, T.; Simoniello, P.; Motta, C.M.; Scudiero, R. The Italian Wall Lizard Podarcis siculus as a Biological Model for Research in Male Reproductive Toxicology. Int. J. Mol. Sci. 2022, 23, 15220. https://doi.org/10.3390/ijms232315220
Rosati L, Chianese T, Simoniello P, Motta CM, Scudiero R. The Italian Wall Lizard Podarcis siculus as a Biological Model for Research in Male Reproductive Toxicology. International Journal of Molecular Sciences. 2022; 23(23):15220. https://doi.org/10.3390/ijms232315220
Chicago/Turabian StyleRosati, Luigi, Teresa Chianese, Palma Simoniello, Chiara Maria Motta, and Rosaria Scudiero. 2022. "The Italian Wall Lizard Podarcis siculus as a Biological Model for Research in Male Reproductive Toxicology" International Journal of Molecular Sciences 23, no. 23: 15220. https://doi.org/10.3390/ijms232315220