Histomorphometric and Immunohistochemical Study Comparing the Effect of Diabetes Mellitus on the Acini of the Sublingual and Submandibular Salivary Glands of Albino Rats
DOI:
https://doi.org/10.3889/oamjms.2020.3722Keywords:
stereology, submandibular salivary gland, sublingual salivary gland, diabetes mellitus, proliferating cell nuclear antigen, oxidative stressAbstract
AIM: This study was designed to compare the effect of diabetes on the mucous and seromucous acini of the sublingual (SLG) and the submandibular (SMG) salivary glands of albino rats, respectively.
METHODS: Twenty male albino rats were assigned into two groups; control and diabetic. Three months following the induction of diabetes mellitus (DM), both the SMG and the SLG glands were removed, randomly sectioned and stained with hematoxylin and eosin to estimate the volume-weighted mean volume of the acini of both glands together with examining their morphology. Furthermore, immunohistochemistry was done to examine the expression of the proliferating cell nuclear antigen (PCNA) in both of them.
RESULTS: We found that, unlike the SMG acinar cells, diabetes appeared not to affect both the morphology and the volume of the SLG acini. Interestingly, PCNA expression in diabetic SMG glands acini was significantly higher than diabetic SLG glands acini. Furthermore, we found that the expression pattern of PCNA was significantly higher between the control and diabetic groups in both glands.
CONCLUSION: We concluded that the mucous acini of the SLG glands are less affected by the oxidative damage induced by DM.
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Amerongen AV, Veerman EC. Saliva-the defender of the oral cavity. Oral Dis. 2002;8(1):12-22. https://doi.org/10.1034/j.1601-0825.2002.1o816.x PMid:11936451
Pinkstaff CA. Serous, seromucous, and special serous cells in salivary glands. Microsc Res Tech. 1993;26(1):21-31. https://doi.org/10.1002/jemt.1070260104. PMid:8219371
Ship JA, Fox PC, Baum BJ. How much saliva is enough? “normal†function defined. J Am Dent Assoc. 1991;122(3):63-9.PMid:2019691
de Almeida Pdel V, Grégio AM, Machado MA, de Lima AA, Azevedo LR. Saliva composition and functions: A comprehensive review. J Contemp Dent Pract. 2008;9(3):72-80. PMid:18335122
Anderson LC, Suleiman AH, Garrett JR. Morphological effects of diabetes on the granular ducts and acini of the rat submandibular gland. Microsc Res Tech. 1994;27(1):61-70. https://doi.org/10.1002/jemt.1070270105 PMid:8155905
Nicolau J, de Matos JA, de Souza DN, Neves LB, Lopes AC. Altered glycogen metabolism in the submandibular and parotid salivary glands of rats with streptozotocin-induced diabetes. J Oral Sci. 2005;47(2):111-6. https://doi.org/10.2334/josnusd.47.111 PMid:16050492
Pinkstaff CA. Salivary glands, glycoconjugates and diabetes mellitus. Eur J Morphol. 1996;34(3):187-90. PMid:8874094
Kamata M, Shirakawa M, Kikuchi K, Matsuoka T, Aiyama S. Histological analysis of the sublingual gland in rats with streptozotocin-induced diabetes. Okajimas Folia Anat Jpn. 2007;84(2):71-6. https://doi.org/10.2535/ofaj.84.71 PMid:17969996
Morris PA, Prout RE, Proctor GB, Garrett JR, Anderson LC. Lipid analysis of the major salivary glands in streptozotocin-diabetic rats and the effects of insulin treatment. Arch Oral Biol. 1992;37(6):489-94. https://doi.org/10.1016/0003-9969(92)90105-h PMid:1386216
Diniz SF, Amorim FP, Cavalcante-Neto FF, Bocca AL, Batista AC, Simm GE, et al. Alloxan-induced diabetes delays repair in a rat model of closed tibial fracture. Braz J Med Biol Res. 2008;41(5):373-9. https://doi.org/10.1590/s0100-879x2008005000014 PMid:18488099
Mayhew TM. Quantitative description of the spatial arrangement of organelles in a polarised secretory epithelial cell: The salivary gland acinar cell. J Anat. 1999;194(Pt 2):279-85. https://doi.org/10.1046/j.1469-7580.1999.19420279.x PMid:10337960
Mandarim-de-Lacerda CA. Stereological tools in biomedical research. An Acad Bras Cienc. 2003;75(4):469-86. https://doi.org/10.1590/s0001-37652003000400006 PMid:14605681
Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, et al. The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 1988;96(10):857-81. https://doi.org/10.1111/j.1699-0463.1988.tb00954.x PMid:3056461
Yasser S. Stereological and immunhistochemical study on the submandibular gland of diabetic albino rats. J Am Sci. 2018;14(12);24-33.
Yasser S, Nagy N, Marei M. In vitro characterization of stem cells from human exfoliated deciduous teeth (SHED). Maced J Med Sci. 2012;5:389-96. https://doi.org/10.3889/mjms.1857-5773.2012.0249
Cecchini MP, Merigo F, Cristofoletti M, Osculati F, Sbarbati A. Immunohistochemical localization of Clara cell secretory proteins (CC10-CC26) and annexin-1 protein in rat major salivary glands. J Anat. 2009;214(5):752-8. https://doi.org/10.1111/j.1469-7580.2009.01074.x PMid:19438769
Bocci V. Ossigeno-ozono Terapia. Milano: Casa Editrice Ambrosiana; 2000. p. 1-324.
Bocci V. Ozone as Janus: This controversial gas can be either toxic or medically useful. Mediators Inflamm. 2004;13(1):3-11. https://doi.org/10.1080/0962935062000197083 PMid:15203558
Caldeira EJ, Camilli JA, Cagnon VH. Stereology and ultrastructure of the salivary glands of diabetic Nod mice submitted to long-term insulin treatment. Anat Rec A Discov Mol Cell Evol Biol. 2005;286(2):930-7. https://doi.org/10.1002/ar.a.20236 PMid:16142810
Ekuni D, Endo Y, Irie K, Azuma T, Tamaki N, Tomofuji T, et al. Imbalance of oxidative/anti-oxidative status induced by periodontitis is involved in apoptosis of rat submandibular glands. Arch Oral Biol. 2010;55(2):170-6. https://doi.org/10.1016/j.archoralbio.2009.11.013 PMid:20035925
üyük B, Nazife S, Keleş O, Selli J, Polat E, Ünal B. Effects of diabetes on the post-menopausal rat sublingual glands: A histopathological and stereological examination. J Exp Clin Med. 2015;32:25-30. https://doi.org/10.5152/eurasianjmed.2015.80
Mednieks MI, Szczepanski A, Clark B, Hand AR. Protein expression in salivary glands of rats with streptozotocin diabetes. Int J Exp Pathol. 2009;90(4):412-22. https://doi.org/10.1111/j.1365-2613.2009.00662.x PMid:19659899
Jay D, Hitomi H, Griendling KK. Oxidative stress and diabetic cardiovascular complications. Free Radic Biol Med. 2006;40(2):183-92. https://doi.org/10.1016/j.freeradbiomed.2005.06.018 PMid:16413400
Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417:1-3. PMid:19061483
Krippeit-Drews P, Kramer C, Welker S, Lang F, Ammon HP, Drews G. Interference of H2O2 with stimulus-secretion coupling in mouse pancreatic beta-cells. J Physiol. 1999;514(Pt 2):471-81. https://doi.org/10.1111/j.1469-7793.1999.471ae.x PMid:9852328
Lilliu MA, Loy F, Cossu M, Solinas P, Isola R, Isola M. Morphometric study of diabetes related alterations in human parotid gland and comparison with submandibular gland. Anat Rec (Hoboken). 2015;298(11):1911-8. PMid:26264892
Delporte C. Aquaporins in salivary glands and pancreas. Biochim Biophys Acta. 2014;1840(5):1524-32. PMid:23954206
Wright EM, Loo DD, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev. 2011;91(2):733-94. PMid:21527736
El Sadik A, Mohamed E, El Zainy A. Postnatal changes in the development of rat submandibular glands in offspring of diabetic mothers: Biochemical, histological and ultrastructural study. PLoS One. 2018;13(10):e0205372. https://doi.org/10.1371/journal.pone.0205372 PMid:30304036
Pizzimenti S, Toaldo C, Pettazzoni P, Dianzani MU, Barrera G. The “two-faced†effects of reactive oxygen species and the lipid peroxidation product 4-hydroxynonenal in the hallmarks of cancer. Cancers (Basel). 2010;2(2):338-63. https://doi.org/10.3390/cancers2020338 PMid:24281073
Meira LB, Burgis NE, Samson LD. Base excision repair. Adv Exp Med Biol. 2005;570:125-73. PMid:18727500
Tsai YC, Wang YH, Liu YC. Overexpression of PCNA attenuates oxidative stress-caused delay of gap-filling during repair of UV-induced DNA damage. J Nucleic Acids. 2017;2017:8154646. https://doi.org/10.1155/2017/8154646 PMid:28116145
Ibuki FK, Simões A, Nogueira FN. Antioxidant enzymatic defense in salivary glands of streptozotocin-induced diabetic rats: A temporal study. Cell Biochem Funct. 2010;28(6):503-8. https://doi.org/10.1002/cbf.1683. PMid:20669150
Turner S, Zettler G, Arcos ML, Cremaschi G, Davicino R, Anesini C. Effect of streptozotocin on reactive oxygen species and antioxidant enzyme secretion in rat submandibulary glands: A direct and an indirect relationship between enzyme activation and expression. Eur J Pharmacol. 2011;659(2-3):281-8. https://doi.org/10.1016/j.ejphar.2011.03.015 PMid:21453698
Parlak SN, Tatar A, Keles ON, Selli J, Can I, Unal B. Effects of menopause and diabetes on the rat parotid glands: A histopathological and stereological study. Int J Med Sci Public Health. 2014;3:749-55. https://doi.org/10.5455/ijmsph.2014.040420146
Arnold WH, Orstavik TB, Holck M. A 4-methoxy-2-naphthylamide substrate for the histochemical localization of esteroproteases in the submandibular gland of the rat. Histochem J. 1983;15(2):139-46. https://doi.org/10.1007/bf01042282. PMid:6343305
Chomette G, Auriol M, Vaillant JM, Bertrand JC, Chenal C. Effects of irradiation on the submandibular gland of the rat. An enzyme histochemical and ultrastructural study. Virchows Arch A Pathol Anat Histol. 1981;391(3):291-9. https://doi.org/10.1007/bf00709161. PMid:7281495
Shear M. Substrate film techniques for the histochemical demonstration of amylase and protease in salivary glands. J Dent Res. 1972;51(2):368-80. https://doi.org/10.1177/00220345720510022401 PMid:4501476
Levi B, Werman MJ. Long-term fructose consumption accelerates glycation and several age-related variables in male rats. J Nutr. 1998;128(9):1442-9. https://doi.org/10.1093/jn/128.9.1442. PMid:9732303
Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 2014;224:164-75. https://doi.org/10.1016/j.cbi.2014.10.016 PMid:25452175
Maciejczyk M, Matczuk J, Żendzian-Piotrowska M, Niklińska W, Fejfer K, Szarmach I, et al. Eight-week consumption of high-sucrose diet has a pro-oxidant effect and alters the function of the salivary glands of rats. Nutrients. 2018;10(10):E1530. https://doi.org/10.3390/nu10101530 PMid:30336621
Mahay S, Adeghate E, Lindley MZ, Rolph CE, Singh J. Streptozotocin-induced Type 1 diabetes mellitus alters the morphology, secretory function and acyl lipid contents in the isolated rat parotid salivary gland. Mol Cell Biochem. 2004;261(1-2):175-81. https://doi.org/10.1023/b:mcbi.0000028753.33225.68 PMid:15362501
Iaremenko AI, Kutukova SI. Experimental substantiation of hormone replacing therapy by estrogens in treatment and prevention of inflammatory infectious diseases of maxillo-facial region. Stomatologiia (Mosk). 2007;86(6):13-7 PMid:18163096
Yashida MH, Da Silva Faria AL, Caldeira EJ. Estrogen and insulin replacement therapy modulates the expression of insulin-like growth factor-I receptors in the salivary glands of diabetic mice. Anat Rec (Hoboken). 2011;294:1930-8 https://doi.org/10.1002/ar.21481
Solinas G, Karin M. JNK1 and IKKbeta: Molecular links between obesity and metabolic dysfunction. FASEB J. 2010;24(8):2596-611. https://doi.org/10.1096/fj.09-151340 PMid:20371626
Iervolino A, De La Motte LR, Petrillo F, Prosperi F, Alvino FM, Schiano G, et al. Corrigendum: Integrin beta 1 is crucial for urinary concentrating ability and renal medulla architecture in adult mice. Front Physiol. 2018;9:1676. https://doi.org/10.3389/fphys.2018.01676 PMid:30546318
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