Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T03:29:28.303Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered Renal Pathology in an Autoimmune Disease Mouse Model After Induction of Diabetes Mellitus

Published online by Cambridge University Press:  28 May 2021

Shiori Hiramatsu ,
Osamu Ichii Open the ORCID record for Osamu Ichii [Opens in a new window] ,
Takashi Namba ,
Yuki Otani ,
Teppei Nakamura ,
Md. Abdul Masum ,
Yaser Hosny Ali Elewa Open the ORCID record for Yaser Hosny Ali Elewa [Opens in a new window]  and
Yasuhiro Kon
Shiori Hiramatsu
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan
Osamu Ichii*
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan Laboratory of Agrobiomedical Science, Faculty of Agriculture, Hokkaido University, Sapporo, Japan
Takashi Namba
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan
Yuki Otani
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan Laboratory of Agrobiomedical Science, Faculty of Agriculture, Hokkaido University, Sapporo, Japan
Teppei Nakamura
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan Department of Biological Safety Research, Chitose Laboratory, Japan Food Research Laboratories, Chitose, Japan
Md. Abdul Masum
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan Department of Anatomy, Histology and Physiology, Faculty of Animal Science and Veterinary Medicine, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
Yaser Hosny Ali Elewa
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan Department of Histology and Cytology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt
Yasuhiro Kon
Affiliation:
Laboratory of Anatomy, Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Kita 18-Nishi 9, Kita-ku, Sapporo060-0818, Japan
*
*Author for correspondence: Osamu Ichii, E-mail: ichi-o@vetmed.hokudai.ac.jp
Get access

Abstract

Diabetes mellitus (DM) is a predisposing factor for renal disorder progression and is referred to as diabetic kidney disease (DKD). However, there are no reports of DKD with an underlying autoimmune disorder. In this study, we compared the pathophysiological changes caused by DM induction after streptozotocin (STZ) injection in comparison with that in a control group receiving citrate buffer (CB) in the autoimmune disease model mice “BXSB/MpJ-Yaa” (Yaa) and the wild-type strain BXSB/MpJ. Both strains showed hyperglycemia after 12 weeks of STZ injection. Interestingly, the Yaa group developed membranous and proliferative glomerulonephritis, which tended to be milder glomerular lesions in the STZ group than in the CB group, as indicated by a decreased mesangial area and ameliorated albuminuria. Statistically, the indices for hyperglycemia and autoimmune abnormalities were negatively and positively correlated with the histopathological parameters for mesangial matrix production and glomerular proliferative lesions, respectively. STZ treatment induced renal tubular anisonucleosis and dilations in both strains, and they were more severe in Yaa. Significantly decreased cellular infiltration was observed in the Yaa group compared to the CB group. Thus, in DKD related to autoimmune nephritis, hyperglycemia modifies its pathology by decreasing the mesangial area and interstitial inflammation and aggravating renal tubular injury.

Keywords

autoimmune diseaseBXSB/MpJ-Yaadiabetes mellitusdiabetic kidney diseasestreptozotocin
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 4 , August 2021 , pp. 897 - 909
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abrass, CK & Cohen, AH (1987). Accelerated glomerulosclerosis in diabetic rats with immune complex injury. Diabetes 36, 1246–1253.CrossRefGoogle ScholarPubMed
Alicic, RZ, Rooney, MT & Tuttle, KR (2017). Diabetic kidney disease: Challenges, progress, and possibilities. Clin J Am Soc Nephrol 12, 2032–2045.CrossRefGoogle ScholarPubMed
Ayo, SH, Radnik, RA, Garoni, JA, Glass, WF, 2nd & Kreisberg, JI (1990). High glucose causes an increase in extracellular matrix proteins in cultured mesangial cells. Am J Pathol 136, 1339–1348.Google ScholarPubMed
Ayo, SH, Radnik, R, Garoni, JA, Troyer, DA & Kreisberg, JI (1991). High glucose increases diacylglycerol mass and activates protein-kinase-C in mesangial cell-cultures. Am J Physiol 261, F571–F577.Google ScholarPubMed
Berbudi, A, Rahmadika, N, Tjahjadi, AI & Ruslami, R (2020). Type 2 diabetes and its impact on the immune system. Curr Diabetes Rev 16, 442–449.CrossRefGoogle ScholarPubMed
Bolzán, AD & Bianchi, MS (2002). Genotoxicity of streptozotocin. Mutat Res Rev Mutat Res 512, 121–134.CrossRefGoogle ScholarPubMed
Chatterjee, S, Khunti, K & Davies, MJ (2017). Type 2 diabetes. Lancet (London, England) 389, 2239–2251.CrossRefGoogle ScholarPubMed
Derylo, B, Babazono, T, Glogowski, E, Kapor-Drezgic, J, Hohman, T & Whiteside, C (1998). High glucose-induced mesangial cell altered contractility: Role of the polyol pathway. Diabetologia 41, 507–515.CrossRefGoogle ScholarPubMed
Dickenmann, M, Oettl, T & Mihatsch, M (2008). Osmotic nephrosis: Acute kidney injury with accumulation of proximal tubular lysosomes due to administration of exogenous solutes. Am J Kidney Dis 51, 491–503.CrossRefGoogle ScholarPubMed
DiMeglio, LA, Evans-Molina, C & Oram, RA (2018). Type 1 diabetes. Lancet (London, England) 391, 2449–2462.CrossRefGoogle ScholarPubMed
Gaulton, GN, Schwartz, JL & Eardley, DD (1985). Assessment of the diabetogenic drugs alloxan and streptozotocin as models for the study of immune defects in diabetic mice. Diabetologia 28, 769–775.Google Scholar
Harding, JL, Pavkov, ME, Magliano, DJ, Shaw, JE & Gregg, EW (2019). Global trends in diabetes complications: A review of current evidence. Diabetologia 62, 3–16.CrossRefGoogle ScholarPubMed
Hirakawa, Y, Tanaka, T & Nangaku, M (2017). Mechanisms of metabolic memory and renal hypoxia as a therapeutic target in diabetic kidney disease. J Diabetes Investig 8, 261–271.CrossRefGoogle ScholarPubMed
Ichii, O, Otsuka, S, Sasaki, N, Yabuki, A, Ohta, H, Takiguchi, M, Hashimoto, Y, Endoh, D & Kon, Y (2010). Local overexpression of interleukin-1 family, member 6 relates to the development of tubulointerstitial lesions. Lab Invest 90, 459–475.CrossRefGoogle ScholarPubMed
Jafar, N, Edriss, H & Nugent, K (2016). The effect of short-term hyperglycemia on the innate immune system. Am J Med Sci 351, 201–211.CrossRefGoogle ScholarPubMed
Jalalah, S (2008). Non-diabetic renal disease in diabetic patients. Saudi J Kidney Dis Transpl 19, 813–816.Google ScholarPubMed
Jensen, H, Doughty, RW, Grant, D & Myhre, O (2013). A modified model of gentamicin induced renal failure in rats: Toxicological effects of the iodinated X-ray contrast media ioversol and potential usefulness for toxicological evaluation of iodinated X-ray contrast media. Exp Toxicol Pathol 65, 601–607.CrossRefGoogle ScholarPubMed
Kanodia, K, Vanikar, A, Nigam, L, Patel, R, Suthar, K & Patel, H (2017). Clinicopathological study of nondiabetic renal disease in type 2 diabetic patients: A single center experience from India. Saudi J Kidney Dis Transpl 28, 1330–1337.CrossRefGoogle ScholarPubMed
Kitada, M, Ogura, Y & Koya, D (2016). Rodent models of diabetic nephropathy: Their utility and limitations. Int J Nephrol Renovasc Dis 9, 279–290.CrossRefGoogle ScholarPubMed
Kuo, T, McQueen, A, Chen, TC & Wang, JC (2015). Regulation of glucose homeostasis by glucocorticoids. Adv Exp Med Biol 872, 99–126.CrossRefGoogle ScholarPubMed
Lenzen, S (2008). The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 51, 216–226.CrossRefGoogle ScholarPubMed
Masum, MA, Ichii, O, Elewa, YHA, Nakamura, T, Otani, Y, Hosotani, M & Kon, Y (2018). Modified scanning electron microscopy reveals pathological crosstalk between endothelial cells and podocytes in a murine model of membranoproliferative glomerulonephritis. Sci Rep 8, 10276.CrossRefGoogle Scholar
Matsushita, K, Takasu, S, Kuroda, K, Ishii, Y, Kijima, A, Ogawa, K & Umemura, T (2018). Mechanisms underlying exacerbation of osmotic nephrosis caused by pre-existing kidney injury. Toxicol Sci 165, 420–430.CrossRefGoogle ScholarPubMed
Moon, J, Jeong, K, Lee, T, Ihm, C, Lim, S & Lee, S (2012). Aberrant recruitment and activation of T cells in diabetic nephropathy. Am J Nephrol 35, 164–174.CrossRefGoogle ScholarPubMed
Muller, YD, Golshayan, D, Ehirchiou, D, Wyss, JC, Giovannoni, L, Meier, R, Serre-Beinier, V, Puga Yung, G, Morel, P, Buhler, LH & Seebach, JD (2011). Immunosuppressive effects of streptozotocin-induced diabetes result in absolute lymphopenia and a relative increase of T regulatory cells. Diabetes 60, 2331–2340.CrossRefGoogle Scholar
Muller-Graff, FT, Fitzner, B, Jaster, R, Vollmar, B & Zechner, D (2018). Impact of hyperglycemia on autoimmune pancreatitis and regulatory T-cells. World J Gastroenterol 24, 3120–3129.CrossRefGoogle ScholarPubMed
Nerhagen, S, Moberg, HL, Boge, GS & Glanemann, B (2021). Prednisolone-induced diabetes mellitus in the cat: A historical cohort. J Feline Med Surg 23, 175–180.CrossRefGoogle ScholarPubMed
Nespoux, J & Vallon, V (2018). SGLT2 inhibition and kidney protection. Clin Sci (Lond) 132, 1329–1339.CrossRefGoogle ScholarPubMed
Ogurtsova, K, da Rocha Fernandes, JD, Huang, Y, Linnenkamp, U, Guariguata, L, Cho, NH, Cavan, D, Shaw, JE & Makaroff, LE (2017). IDF diabetes atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128, 40–50.CrossRefGoogle ScholarPubMed
Olivares, AM, Althoff, K, Chen, GF, Wu, S, Morrisson, MA, DeAngelis, MM & Haider, N (2017). Animal models of diabetic retinopathy. Curr Diab Rep 17, 93.CrossRefGoogle ScholarPubMed
Perazella, MA (2019). Drug-induced acute kidney injury: Diverse mechanisms of tubular injury. Curr Opin Crit Care 25, 550–557.CrossRefGoogle ScholarPubMed
Phillips, AO, Steadman, R, Morrisey, K & Williams, JD (1997). Polarity of stimulation and secretion of transforming growth factor-beta 1 by cultured proximal tubular cells. Am J Pathol 150, 1101–1111.Google ScholarPubMed
Pisitkun, P, Deane, JA, Difilippantonio, MJ, Tarasenko, T, Satterthwaite, AB & Bolland, S (2006). Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312(5780), 1669–1672.CrossRefGoogle ScholarPubMed
Rubinstein, R, Genaro, AM, Motta, A, Cremaschi, G & Wald, MR (2008). Impaired immune responses in streptozotocin-induced type I diabetes in mice. Involvement of high glucose. Clin Exp Immunol 154, 235–246.CrossRefGoogle ScholarPubMed
Sasaki, H, Kimura, J, Nagasaki, K, Marusugi, K, Agui, T & Sasaki, N (2016). Mouse chromosome 2 harbors genetic determinants of resistance to podocyte injury and renal tubulointerstitial fibrosis. BMC Genet 17, 69.CrossRefGoogle ScholarPubMed
Sethi, S & Fervenza, FC (2012). Membranoproliferative glomerulonephritis: A new look at an old entity. New Engl J Med 366, 1119–1131.CrossRefGoogle Scholar
Tamura, J, Konno, A, Hashimoto, Y & Kon, Y (2005). Upregulation of renal renin-angiotensin system in mouse diabetic nephropathy. Jpn J Vet Res 53, 13–26.Google ScholarPubMed
Tervaert, TW, Mooyaart, AL, Amann, K, Cohen, AH, Cook, HT, Drachenberg, CB, Ferrario, F, Fogo, AB, Haas, M, de Heer, E, Joh, K, Noel, LH, Radhakrishnan, J, Seshan, SV, Bajema, IM, Bruijn, JA & Renal Pathology, S (2010). Pathologic classification of diabetic nephropathy. J Am Soc Nephrol 21, 556–563.CrossRefGoogle ScholarPubMed
Wolf, G, Sharma, K, Chen, Y, Ericksen, M & Ziyadeh, FN (1992). High glucose-induced proliferation in mesangial cells is reversed by autocrine TGF-β. Kidney Int 42, 647–656.CrossRefGoogle ScholarPubMed
Zhang, S, Li, R, Dong, W, Yang, H, Zhang, L, Chen, Y, Wang, W, Li, C, Wu, Y, Ye, Z, Zhao, X, Li, Z, Zhang, M, Liu, S & Liang, X (2019). RIPK3 mediates renal tubular epithelial cell apoptosis in endotoxin-induced acute kidney injury. Mol Med Rep 20, 1613–1620.Google Scholar
Zhen, Y, Sun, L, Liu, H, Duan, K, Zeng, C, Zhang, L, Jin, D, Peng, J, Ding, W & Zhao, Y (2012). Alterations of peripheral CD4+CD25+Foxp3+ t regulatory cells in mice with STZ-induced diabetes. Cell Mol Immunol 9, 75–85.CrossRefGoogle Scholar
Ziyadeh, FN, Snipes, ER, Watanabe, M, Alvarez, RJ, Goldfarb, S & Haverty, TP (1990). High sglucose induces cell hypertrophy and stimulates collagen gene transcription in proximal tubule. Am J Physiol 259, F704–F714.Google ScholarPubMed