Morphological and molecular changes in the Harderian gland of streptozotocin-induced diabetic rats.
autophagy
mast cells number
oxidative stress
steroidogenic enzymes
type 1 diabetes
Journal
Journal of experimental zoology. Part A, Ecological and integrative physiology
ISSN: 2471-5646
Titre abrégé: J Exp Zool A Ecol Integr Physiol
Pays: United States
ID NLM: 101710204
Informations de publication
Date de publication:
12 2023
12 2023
Historique:
revised:
15
06
2023
received:
23
02
2023
accepted:
21
07
2023
medline:
6
11
2023
pubmed:
31
7
2023
entrez:
31
7
2023
Statut:
ppublish
Résumé
Using a rat model of type 1 diabetes (T1D) obtained by treatment with streptozotocin, an antibiotic that destroys pancreatic β-cells, we evaluated the influence of subsequent hyperglycemia on the morphology and physiology of the Harderian gland (HG). HG is located in the medial corner of the orbit of many terrestrial vertebrates and, in rodents, is characterized by the presence of porphyrins, which being involved in the phototransduction, through photo-oxidation, produce reactive oxygen species activating the autophagy pathway. The study focused on the expression of some morphological markers involved in cell junction formation (occludin, connexin-43, and α-tubulin) and mast cell number (MCN), as well as autophagic and apoptotic pathways. The expression of enzymes involved in steroidogenesis [steroidogenic acute regulatory protein (StAR), and 3β-hydroxysteroid dehydrogenase (3β-HSD)] and the level of lipid peroxidation by thiobarbituric acid reactive species assay were also evaluated. The results strongly indicate, for the first time, that T1D has a negative impact on the pathophysiology of rat HG, as evidenced by increased oxidative stress, morphological and biochemical alterations, hyperproduction and secretion of porphyrins, increased MCN, reduced protein levels of StAR and 3β-HSD, and, finally, induced autophagy and apoptosis. All the combined data support the use of the rat HG as a suitable experimental model to elucidate the molecular damage/survival pathways elicited by stress conditions.
Substances chimiques
Porphyrins
0
Streptozocin
5W494URQ81
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
915-924Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Andjelkovic, M., Skakic, A., Ugrin, M., Spasovski, V., Klaassen, K., Pavlovic, S., & Stojiljkovic, M. (2022). Crosstalk between glycogen-selective autophagy, autophagy and apoptosis as a road towards modifier gene discovery and new therapeutic strategies for glycogen storage diseases. Life, 12, 1396. https://doi.org/10.3390/life12091396
Azad, M. B., Chen, Y., & Gibson, S. B. (2009). Regulation of autophagy by reactive oxygen species (ROS): Implications for cancer progression and treatment. Antioxidants & Redox Signaling, 11, 777-790. https://doi.org/10.1089/ars.2008.2270
Bagheri, M., Amini, A., Abdollahifar, M.-A., Ghoreishi, S. K., Piryaei, A., Pouriran, R., Chien, S., Dadras, S., Rezaei, F., & Bayat, M. (2018). Effects of photobiomodulation on degranulation and number of mast cells and wound strength in skin wound healing of Streptozotocin-induced diabetic rats. Photomedicine and laser surgery, 36, 415-423. https://doi.org/10.1089/pho.2018.4453
Brooks-Worrell, B., & Palmer, J. P. (2011). Is diabetes mellitus a continuous spectrum. Clinical Chemistry, 57, 158-161. https://doi.org/10.1373/clinchem.2010.148270
Buzzell, G. R., Menendez-Pelaez, A., Chlumecky, V., & Reiter, R. J. (1991). Gender differences and time course of castration-induced changes in porphyrins, indoles, and proteins in the Harderian glands of the Syrian hamster. Canadian Journal of Physiology and Pharmacology, 69, 1814-1818. https://doi.org/10.1139/y91-268
Canet, F., Díaz-Pozo, P., Luna-Marco, C., Fernandez-Reyes, M., Vezza, T., Marti, M., Salazar, J. D., Roldan, I., Morillas, C., Rovira-Llopis, S., Rocha, M., & Víctor, V. M. (2022). Mitochondrial redox impairment and enhanced autophagy in peripheral blood mononuclear cells from type 1 diabetic patients. Redox Biology, 58, 102551. https://doi.org/10.1016/j.redox.2022.102551
Castillo, A. F., Orlando, U., Helfenberger, K. E., Poderoso, C., & Podesta, E. J. (2015). The role of mitochondrial fusion and StAR phosphorylation in the regulation of StAR activity and steroidogenesis. Molecular and Cellular Endocrinology, 408, 73-79. https://doi.org/10.1016/j.mce.2014.12.011
Chieffi, G., Baccari, G. C., Di Matteo, L., d'Istria, M., Minucci, S., & Varriale, B. (1996). Cell Biology of the Harderian Gland, International Review of Cytology (pp. 1-80). Elsevier. in. https://doi.org/10.1016/S0074-7696(08)60882-7
Chieffi Baccari, G., Chieffi, G., Di Matteo, L., Dafnis, D., De Rienzo, G., & Minucci, S. (2000). Morphology of the Harderian gland of the Gecko, Tarentola mauritanica. Journal of Morphology, 244, 137-142. https://doi.org/10.1002/(SICI)1097-4687(200005)244:2<137::AID-JMOR4>3.0.CO;2-O
Chieffi Baccari, G., Falvo, S., Di Fiore, M. M., Cioffi, F., Giacco, A., & Santillo, A. (2022). High-fat diet affects autophagy and mitochondrial compartment in rat Harderian gland. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 1025-1038. https://doi.org/10.1002/jez.2646
Coto-Montes, A., Boga, J. A., Tomás-Zapico, C., Rodrı́guez-Colunga, J., Martı́nez-Fraga, J., Tolivia-Cadrecha, D., Menéndez, G., Hardeland, R., & Tolivia, D. (2001). Porphyric enzymes in hamster Harderian gland, a model of damage by porphyrins and their precursors. A chronobiological study on the role of sex differences. Chemico - Biological Interactions, 134, 135-149. https://doi.org/10.1016/s0009-2797(00)00320-3
Coto-Montes, A., & Tomas-Zapico, C. (2006). Could melatonin unbalance the equilibrium between autophagy and invasive processes? Autophagy, 2, 126-128. https://doi.org/10.4161/auto.2.2.2351
d'Istria, M., Chieffi-Baccari, G., Di Matteo, L., Minucci, S., Varriale, B., & Chieffi, G. (1991). Androgen receptor in the Harderian gland of Rana esculenta. Journal of Endocrinology, 129, 227-232. https://doi.org/10.1677/joe.0.1290227
Dias, A. B., de Oliveira, S. A., Cerri, P. S., & Sasso-Cerri, E. (2022). Bilateral asymmetry in bullfrog testes and fat bodies: Correlations with steroidogenic activity, mast cells number and structural proteins. Acta Histochemica, 124, 151873. https://doi.org/10.1016/j.acthis.2022.151873
Djeridane, Y. (1994). The harderian gland and its excretory duct in the Wistar rat. A histological and ultrastructural study. Journal of Anatomy, 184 (Pt 3), 553-566.
Djeridane, Y., & Touitou, Y. (2001). Melatonin synthesis in the rat harderian gland: Age- and time-related effects. Experimental Eye Research, 72, 487-492. https://doi.org/10.1006/exer.2000.0973
Elieh Ali Komi, D., Shafaghat, F., & Haidl, G. (2020). Significance of mast cells in spermatogenesis, implantation, pregnancy, and abortion: Cross talk and molecular mechanisms. American Journal of Reproductive Immunology, 83, e13228. https://doi.org/10.1111/aji.13228
Falvo, S., Chieffi Baccaria, G., Spaziano, G., Rosati, L., Venditti, M., Di Fiore, M. M., & Santillo, A. (2018). StAR protein and steroidogenic enzyme expressions in the rat Harderian gland. Comptes Rendus Biologies, 341, 160-166. https://doi.org/10.1016/j.crvi.2018.02.001
Fiorentino, T., Prioletta, A., Zuo, P., & Folli, F. (2013). Hyperglycemia-induced oxidative stress and its role in diabetes mellitus related cardiovascular diseases. Current Pharmaceutical Design, 19, 5695-5703. https://doi.org/10.2174/1381612811319320005
Furman, B. L. (2015). Streptozotocin-induced diabetic models in mice and rats. Current Protocols in Pharmacology, 70, 5.47.1-5.47.20. https://doi.org/10.1002/0471141755.ph0547s70
García-Macia, M., Rubio-Gonzalez, A., de Luxán-Delgado, B., Potes, Y., Rodríguez-González, S., de Gonzalo-Calvo, D., Boga, J. A., & Coto-Montes, A. (2014). Autophagic and proteolytic processes in the Harderian gland are modulated during the estrous cycle. Histochemistry and Cell Biology, 141, 519-529. https://doi.org/10.1007/s00418-013-1170-1
García-Macia, M., Santos-Ledo, A., Caballero, B., Rubio-González, A., de Luxán-Delgado, B., Potes, Y., Rodríguez-González, S., Boga, J. A., & Coto-Montes, A. (2019). Selective autophagy, lipophagy and mitophagy, in the harderian gland along the oestrous cycle: A potential retrieval effect of melatonin. Scientific Reports, 9, 18597. https://doi.org/10.1038/s41598-019-54743-5
Hoffman, R. A. (1971). Influence of some endocrine glands, hormones and blinding on the histology and porphyrins of the Harderian glands of golden hamsters. American Journal of Anatomy, 132, 463-477. https://doi.org/10.1002/aja.1001320405
Hoffman, W. H., Shacka, J. J., & Andjelkovic, A. V. (2012). Autophagy in the brains of young patients with poorly controlled T1DM and fatal diabetic ketoacidosis. Experimental and Molecular Pathology, 93, 273-280. https://doi.org/10.1016/j.yexmp.2011.10.007
Huang, J., & Brumell, J. H. (2014). Bacteria-autophagy interplay: a battle for survival. Nature Reviews Microbiology, 12, 101-114. https://doi.org/10.1038/nrmicro3160
Hugo, J., Krijt, J., Vokurka, M., & Janousek, V. (1987). Secretory response to light in rat Harderian gland: Possible photoprotective role of Harderian porphyrin. General Physiology and Biophysics, 6, 401-404.
Izzo, G., d'Istria, M., Serino, I., & Minucci, S. (2004). Inhibition of the increased 17β-estradiol-induced mast cell number by melatonin in the testis of the frog Rana esculenta, in vivoandin vitro. Journal of Experimental Biology, 207(Pt 3), 437-441. https://doi.org/10.1242/jeb.00786
Kleinberger, J. W., & Pollin, T. I. (2015). Personalized medicine in diabetes mellitus: Current opportunities and future prospects: Personalized medicine in diabetes mellitus. Annals of the New York Academy of Sciences, 1346, 45-56. https://doi.org/10.1111/nyas.12757
Kong, X.-T., Wang, Z., Mou, J.-J., Li, C.-S., Xue, H.-L., Wu, M., Chen, L., Xu, J.-H., & Xu, L.-X. (2021). Change on apoptosis, autophagy and mitochondria of the Harderian gland in Cricetulus barabensis during age. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 253, 110547. https://doi.org/10.1016/j.cbpb.2020.110547
Lama, S., Vanacore, D., Diano, N., Nicolucci, C., Errico, S., Dallio, M., Federico, A., Loguercio, C., & Stiuso, P. (2019). Ameliorative effect of Silybin on bisphenol A induced oxidative stress, cell proliferation and steroid hormones oxidation in HepG2 cell cultures. Scientific Reports, 9, 3228. https://doi.org/10.1038/s41598-019-40105-8
Lenz, K. M., Pickett, L. A., Wright, C. L., Davis, K. T., Joshi, A., & McCarthy, M. M. (2018). Mast cells in the developing brain determine adult sexual behavior. The Journal of neuroscience, 38, 8044-8059. https://doi.org/10.1523/JNEUROSCI.1176-18.2018
Marrufo, B., Menendez-Pelaez, A., Buzzell, G. R., Gonzalez-Brito, A., & Reiter, R. J. (1989). 5-Dihydrotestosterone administration converts indolamine metabolism and porphyrin content of the female Syrian hamster harderian gland to the male type. Experimental Biology and Medicine, 192, 192-195. https://doi.org/10.3181/00379727-192-42978
Di Matteo, L., Baccari, G. C., Chieffi, P., & Minucci, S. (1995). The effects of testosterone and estradiol on mast cell number in the harderian gland of the frog, Rana esculenta. Zoological Science, 12, 457-466. https://doi.org/10.2108/zsj.12.457
Menendez-Pelaez, A., & Reiter, R. J. (1993). Distribution of melatonin in mammalian tissues: The relative importance of nuclear versus cytosolic localization. Journal of Pineal Research, 15, 59-69. https://doi.org/10.1111/j.1600-079X.1993.tb00511.x
Minucci, S., Di Matteo, L., Chieffi, P., Pierantoni, R., & Fasano, S. (1997). 17β-Estradiol effects on mast cell number and spermatogonial mitotic index in the testis of the frog,Rana esculenta. Journal of Experimental Zoology, 278, 93-100.
Minucci, S., & Venditti, M. (2022). New insight on the in vitro effects of melatonin in preserving human sperm quality. International Journal of Molecular Sciences, 23, 5128. https://doi.org/10.3390/ijms23095128
Monteforte, R., Santillo, A., Lanni, A., D'Aniello, S., & Baccari, G. C. (2008). Morphological and biochemical changes in the Harderian gland of hypothyroid rats. Journal of Experimental Biology, 211, 606-612. https://doi.org/10.1242/jeb.015115
de Morais, R. B., do Couto Muniz, V. P., Nunes Costa, E., Filho, S. R. F., Nakamura Hiraki, K. R., Bispo-da-Silva, L. B., & Coelho Balbi, A. P. (2018). Mast cell population in the development of diabetic nephropathy: Effects of renin angiotensin system inhibition. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie, 107, 1115-1118. https://doi.org/10.1016/j.biopha.2018.08.066
Nicovani, S., & Rudolph, M. I. (2002). Estrogen receptors in mast cells from arterial walls. Biocell: Official Journal of the Sociedades Latinoamericanas de Microscopía Electronica. et. al, 26, 15-24.
Payne, A. P. (1994). The harderian gland: A tercentennial review. Journal of Anatomy, 185(Pt), 1-49.
Payne, A. P., McGadey, J., Moore, M. R., & Thompson, G. (1977). Androgenic control of the harderian gland in the male golden hamster. Journal of Endocrinology, 75, 73-NP. https://doi.org/10.1677/joe.0.0750073
Dos Reis, E. R., Danielli Nicola, E. M., & Humberto Nicola, J. (2005). Harderian gland of wistar rats revised as a protoporphyrin IX producer. Brazilian Journal of Morphological Science, 22, 43-51.
Romano, M. Z., Aniello, F., Venditti, M., & Minucci, S. (2022). Preliminary study of the ameliorative effects of melatonin on cadmium-induced morphological and biochemical alterations in the rat Harderian gland. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 729-738. https://doi.org/10.1002/jez.2609
Rosati, L., Di Fiore, M. M., Prisco, M., Di Giacomo Russo, F., Venditti, M., Andreuccetti, P., Chieffi Baccari, G., & Santillo, A. (2019). Seasonal expression and cellular distribution of star and steroidogenic enzymes in quail testis. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 332, 198-209. https://doi.org/10.1002/jez.b.22896
Rudraraju, M., Narayanan, S. P., & Somanath, P. R. (2020). Regulation of blood-retinal barrier cell-junctions in diabetic retinopathy. Pharmacological Research, 161, 105115. https://doi.org/10.1016/j.phrs.2020.105115
Santillo, A., Burrone, L., Minucci, S., Di Giovanni, M., & Chieffi Baccari, G. (2011). Molecular pathways involved in the cyclic activity of frog (Pelophylax esculentus) Harderian gland: Influence of temperature and testosterone. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 158, 71-76. https://doi.org/10.1016/j.cbpb.2010.09.007
Santillo, A., Chieffi Baccari, G., Minucci, S., Falvo, S., Venditti, M., & Di Matteo, L. (2020). The Harderian gland: Endocrine function and hormonal control. General and Comparative Endocrinology, 297, 113548. https://doi.org/10.1016/j.ygcen.2020.113548
Santos-Ledo, A., Luxán-Delgado, B., Caballero, B., Potes, Y., Rodríguez-González, S., Boga, J. A., Coto-Montes, A., & García-Macia, M. (2021). Melatonin ameliorates autophagy impairment in a metabolic syndrome model. Antioxidants, 10, 796. https://doi.org/10.3390/antiox10050796
Shanas, U., & Terkel, J. (1996). Grooming secretions and seasonal adaptations in the blind mole rat (Spalax ehrenbergi. Physiology & Behavior, 60, 653-656. https://doi.org/10.1016/S0031-9384(96)80044-8
Simon, H. U., Haj-Yehia, A., & Levi-Schaffer, F. (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis, 5, 415-418. https://doi.org/10.1023/a:1009616228304
Spike, R. C., Payne, A. P., Thompson, G. G., & Moore, M. R. (1990). High-performance liquid chromatographic analyses of porphyrins in hamster Harderian glands. Biochimica et Biophysica Acta (BBA) - General Subjects, 1034, 1-3. https://doi.org/10.1016/0304-4165(90)90144-l
Tokarz, V. L., MacDonald, P. E., & Klip, A. (2018). The cell biology of systemic insulin function. Journal of Cell Biology, 217, 2273-2289. https://doi.org/10.1083/jcb.201802095
Tomás-Zapico, C., Caballero, B., Sierra, V., Vega-Naredo, I., Álvarez-García, Ó., Tolivia, D., Rodríguez-Colunga, M. J., & Coto-Montes, A. (2005). Survival mechanisms in a physiological oxidative stress model. The FASEB Journal, 19, 2066-2068. https://doi.org/10.1096/fj.04-3595fje
Vega-Naredo, I., Caballero, B., Sierra, V., Huidobro-Fernández, C., de Gonzalo-Calvo, D., García-Macia, M., Tolivia, D., Rodríguez-Colunga, M. J., & Coto-Montes, A. (2009). Sexual dimorphism of autophagy in Syrian hamster Harderian gland culminates in a holocrine secretion in female glands. Autophagy, 5, 1004-1017. https://doi.org/10.4161/auto.5.7.9610
Vega-Naredo, I., & Coto-Montes, A. (2009). Physiological autophagy in the Syrian hamster Harderian gland. Methods in Enzymology, 452, 457-476. https://doi.org/10.1016/S0076-6879(08)03627-6
Vega-Naredo*, I., & Coto-Montes, A. (2009). Chapter 27 Physiological Autophagy in the Syrian Hamster Harderian Gland, in: Methods in Enzymology (pp. 457-476). Elsevier. https://doi.org/10.1016/S0076-6879(08)03627-6
Venditti, M., Arcaniolo, D., De Sio, M., & Minucci, S. (2022). First evidence of the expression and localization of prothymosin α in human testis and its involvement in testicular cancers. Biomolecules, 12, 1210. https://doi.org/10.3390/biom12091210
Venditti, M., Ben Rhouma, M., Romano, M. Z., Messaoudi, I., Reiter, R. J., & Minucci, S. (2021). Evidence of melatonin ameliorative effects on the blood-testis barrier and sperm quality alterations induced by cadmium in the rat testis. Ecotoxicology and Environmental Safety, 226, 112878. https://doi.org/10.1016/j.ecoenv.2021.112878
Vliagoftis, H., Dimitriadou, V., Boucher, W., Rozniecki, J. J., Correia, I., Raam, S., & Theoharides, T. C. (1992). Estradiol augments while tamoxifen inhibits rat mast cell secretion. International Archives of Allergy and Immunology, 98, 398-409. https://doi.org/10.1159/000236217
Wang, Y., Wang, S., Zhang, W., Liu, J., Yang, Z., & Liu, C. (2021). Notch1 participates in the activation of autophagy in the hippocampus of type I diabetic mice. Neurochemistry International, 150, 105156. https://doi.org/10.1016/j.neuint.2021.105156
Wooding, F. B. P. (1980). Lipid droplet secretion by the rabbit harderian gland. Journal of Ultrastructure Research, 71, 68-78. https://doi.org/10.1016/s0022-5320(80)90037-4
Xu, Q., Wells, C. C., Garman, J. H., Asico, L., Escano, C. S., & Maric, C. (2008). Imbalance in sex hormone levels exacerbates diabetic renal disease. Hypertension, 51, 1218-1224. https://doi.org/10.1161/HYPERTENSIONAHA.107.100594
Xu, X., Wang, J., Guo, X., Chen, Y., Ding, S., Zou, G., Zhu, L., Li, T., & Zhang, X. (2023). GPR30-mediated non-classic estrogen pathway in mast cells participates in endometriosis pain via the production of FGF2. Frontiers in Immunology, 14, 1106771. https://doi.org/10.3389/fimmu.2023.1106771
Yamanaka, K., Chun, S. J., Boillee, S., Fujimori-Tonou, N., Yamashita, H., Gutmann, D. H., Takahashi, R., Misawa, H., & Cleveland, D. W. (2008). Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nature Neuroscience, 11, 251-253. https://doi.org/10.1038/nn2047
Yaribeygi, H., Farrokhi, F. R., Butler, A. E., & Sahebkar, A. (2019). Insulin resistance: Review of the underlying molecular mechanisms. Journal of Cellular Physiology, 234, 8152-8161. https://doi.org/10.1002/jcp.27603
Yaribeygi, H., Katsiki, N., Behnam, B., Iranpanah, H., & Sahebkar, A. (2018). MicroRNAs and type 2 diabetes mellitus: Molecular mechanisms and the effect of antidiabetic drug treatment. Metabolism: Clinical and Experimental, 87, 48-55. https://doi.org/10.1016/j.metabol.2018.07.001
Yoshii, S. R., & Mizushima, N. (2017). Monitoring and measuring autophagy. International Journal of Molecular Sciences, 18, 1865. https://doi.org/10.3390/ijms18091865
Yun, H. R., Jo, Y. H., Kim, J., Shin, Y., Kim, S. S., & Choi, T. G. (2020). Roles of autophagy in oxidative stress. International Journal of Molecular Sciences, 21, 3289. https://doi.org/10.3390/ijms21093289
Zierau, O., Zenclussen, A. C., & Jensen, F. (2012). Role of female sex hormones, estradiol and progesterone, in mast cell behavior. Frontiers in Immunology, 3, 169. https://doi.org/10.3389/fimmu.2012.00169
Ziller, N., Kotolloshi, R., Esmaeili, M., Liebisch, M., Mrowka, R., Baniahmad, A., Liehr, T., Wolf, G., & Loeffler, I. (2020). Sex differences in diabetes- and TGF-β1-induced renal damage. Cells, 9, 2236. https://doi.org/10.3390/cells9102236