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  • 1 Tanta University, Egypt
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Diabetic nephropathy (DN) is one of the most common microvascular diabetic complications. This study was designed to evaluate the possible protective effect and underlying mechanisms of HO-1 induction in streptozotocin (STZ)-induced early DN in rats. The diabetic rats were divided into three groups: STZ-diabetic, cobalt protoporphyrin (CoPP)-treated diabetic, and zinc protoporphyrin IX (ZnPP)-treated diabetic groups. Compared to the STZ-diabetic group, CoPP-induced HO-1 upregulation improved the diabetic state and renal functional parameters, suppressed the renal proinflammatory marker, NF-κB, abrogated the elevated renal hydroxyprolin, and decreased the enhanced renal nicotinamide adenine dinucleotide phosphate oxidase activity with parallel reduction of urinary oxidative stress markers. On the contrary, treatment with ZnPP abrogated HO-1 levels, aggravated the diabetic condition with further increases in renal oxidative stress, fibrotic and inflammatory markers, and exacerbated renal dysfunction in diabetic animals. These findings suggest that the reduced diabetic renal injury upon HO-1 induction implicates the role of HO-1 induction as a potential treatment for DN.

  • 1.

    Bak I , Czompa A , Juhasz B , Lekli I , Tosaki A : Reduction of reperfusion-induced ventricular fibrillation and infarct size via heme oxygenase-1 overexpression in isolated mouse hearts. J. Cell. Mol. Med. 14(9), 22682272 (2010)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Bak I , Szendrei L , Turoczi T , Papp G , Joo F , Das DK , de Leiris J , Der P , Juhasz B , Varga E , Bacskay I , Balla J , Kovacs P , Tosaki A : Heme oxygenase-1 related carbon monoxide production and ventricular fibrillation in isolated ischemic/reperfused mouse myocardium. FASEB J. 17, 21332135 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Bradford MM : Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248254 (1976)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Brosius FC : New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy. Rev. Endocr. Metab. Disord. 9, 245254 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Chen P , Chen JB , Chen WY , Zheng QL , Wang YQ , Xu XJ : Effects of quercetin on nuclear factor-κB p65 expression in renal ubiquitin-proteasome system of diabetic rats. Zhonghua Nei Ke Za Zhi 51, 460465 (2012)

    • Search Google Scholar
    • Export Citation
  • 6.

    Datla SR , Dusting GJ , Mori TA , Taylor C , Croft KD , Jiang F : Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension 50, 636642 (2007)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Di Noia MA , Van Driesche S , Palmieri F , Yang LM , Quan S , Goodman AI , Abraham NG : Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J. Biol. Chem. 281(23), 1568715693 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Dong H , Huang H , Yun X , Kim DS , Yue Y , Wu H , Sutter A , Chavin KD , Otterbein LE , Adams DB , Kim YB , Wang H : Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinology 155(3), 818828 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Elmarakby AA , Faulkner J , Baban B , Saleh MA , Sullivan JC : Induction of hemeoxygenase-1 reduces glomerular injury and apoptosis in diabetic spontaneously hypertensive rats. Am. J. Physiol. Renal Physiol. 302, F791F800 (2012)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Elmarakby AA , Faulkner J , Pye C , Rouch K , Alhashim A , Maddipati KR , Baban B : Role of haem oxygenase in the renoprotective effects of soluble epoxide hydrolase inhibition in diabetic spontaneously hypertensive rats. Clin. Sci. (Lond.) 125, 349359 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Farhangkhoee H , Khan ZA , Mukherjee S , Cukiernik M , Barbin YP , Karmazyn M , Chakrabarti S : Heme oxygenase in diabetes-induced oxidative stress in the heart. J. Mol. Cell. Cardiol. 35(12), 14391448 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Fu XJ , Peng YP , Hu YP , Shi YZ , Yao M , Zhang X : NADPH oxidase 1 and its derived reactive oxygen species mediated tissue injury and repair. Oxid. Med. Cell. Longev. 2014, 282854 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Gong LM , Du JB , Shi L , Shi Y , Tang CS : Effects of endogenous carbon monoxide on collagen synthesis in pulmonary artery in rats under hypoxia. Life Sci. 74, 12251241 (2004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Graça-Souza AV , Arruda MA , de Freitas MS , Barja-Fidalgo C , Oliveira PL : Neutrophil activation by heme: implications for inflammatory processes. Blood 99, 41604165 (2002)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Holmes BF , Sparling DP , Olson AL , Winder WW , Dohm GL : Regulation of muscle GLUT4 enhancer factor and myocyte enhancer factor 2 by AMP-activated protein kinase. Am. J. Physiol. Endocrinol. Metab. 289(6), E1071E1076 (2005)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Inguaggiato P , Gonzalez-Michaca L , Croatt AJ , Haggard JJ , Alam J , Nath KA. : Cellular overexpression of heme oxygenase-1 up-regulates p21 and confers resistance to apoptosis. Kidney Int. 60, 21812191 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Jiang F : NADPH oxidase in the kidney: a Janus in determining cell fate. Kidney Int. 75, 135137 (2009)

  • 18.

    Kanasaki K , Taduri G , Koya D : Diabetic nephropathy: the role of inflammation in fibroblast activation and kidney fibrosis. Front. Endocrinol. (Lausanne) 4, 7 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Kaneto H , Nakatani Y , Kawamori D , Miyatsuka T , Matsuoka TA , Matsuhisa M , Yamasaki Y : Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic β-cell dysfunction and insulin resistance. Int. J. Biochem. Cell Biol. 38, 782793 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Kapturczak MH , Wasserfall C , Brusko T , Campbell-Thompson M , Ellis TM , Atkinson MA , Agarwal A : Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am. J. Pathol. 165, 10451053 (2004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Karihaloo A : Anti-fibrosis therapy and diabetic nephropathy. Curr. Diab. Rep. 12(4), 414422 (2012)

  • 22.

    Kim DH , Burgess AP , Li M , Tsenovoy PL , Addabbo F , McClung JA , Puri N , Abraham NG : Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines tumor necrosis factor-α and interleukin-6 in Zucker rats and reduce adipogenesis in human mesenchymal stem cells. J. Pharmacol. Exp. Ther. 325, 833840 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Kim M , Moon H , Hong S : Determination of urinary 8-hydroxy-2- deoxy guanosine as a DNA damage marker. Am. Clin. Lab. 4245 (2001)

  • 24.

    Kuhlmann J , Neumann-Haefelin C , Belz U , Kalisch J , Juretschke HP , Stein M , Kleinschmidt E , Kramer W , Herling AW : Intramyocellular lipid and insulin resistance: a longitudinal in vivo 1H-spectroscopic study in Zucker diabetic fatty rats. Diabetes 52, 138144 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Lee JI , Ganster RW , Geller DA , Burckart GJ , Thomson AW , Lu L : Cyclosporine inhibits the expression of co-stimulatory molecules on in vitro generated dendritic cells: association with reduced nuclear translocation of nuclear factor kappa B. Transplantation 68, 12551263 (1999)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Li L , Grenard P , Nhieu JT , Julien B , Mallat A , Habib A , Lotersztajn S : Heme oxygenase-1 is an antifibrogenic protein in human hepatic myofibroblasts. Gastroenterology 125, 460469 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Liu X , Wei J , Peng DH , Layne MD , Yet SF : Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 54(3), 778784 (2005)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Mancuso C , Santangelo R , Calabrese V : The heme oxygenase/biliverdin reductase system: a potential drug target in Alzheimer s disease. J. Biol. Regul. Homeost. Agents 27(2 Suppl.), 7587 (2013)

    • Search Google Scholar
    • Export Citation
  • 29.

    Mann JFE , Rossing P , Wiåcek A , Rosivall L , Mark P , Mayer G : Diagnosis and treatment of early renal disease in patients with type 2 diabetes mellitus: what are the clinical needs? Nephrol. Dial. Transplant. 30(Suppl. 4), iv1iv5 (2015)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Mezzano S , Aros C , Droguett A , Burgos ME , Ardiles L , Flores C , Schneider H , Ruiz-Ortega M , Egido J : NF-kappaB activation and overexpression of regulated genes in human diabetic nephropathy. Nephrol Dial. Transplant. 19, 25052512 (2004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Milne GI , Sanchez SC , Musiek ES , Morrow JD : Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat. Protoc. 2, 211226 (2007)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Mishra M , Ndisang JF : A critical and comprehensive insight on heme oxygenase and related products including carbon monoxide, bilirubin, biliverdin and ferritin in type-1 and type-2 diabetes. Curr. Pharm. Des. 20, 13701391 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Mosén H , Salehi A , Alm P , Henningsson R , Jimenez-Feltström J , Ostenson CG , Efendic S , Lundquist I : Defective glucose-stimulated insulin release in the diabetic Goto-Kakizaki (GK) rat coincides with reduced activity of the islet carbon monoxide signaling pathway. Endocrinology 146, 15531558 (2005)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Moujalled DM , Cook WD , Okamoto T , Murphy J , Lawlor KE , Vince JE , Vaux DL : TNF can activate RIPK3 and cause programmed necrosis in the absence of RIPK1. Cell Death Dis. 4, e465 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Mozaffari MS , Baban B , Liu JY , Abebe W , Sullivan JC , El-Marakby A : Mitochondrial complex I and NAD(P)H oxidase are major sources of exacerbated oxidative stress in pressure-overloaded ischemic-reperfused hearts. Basic Res. Cardiol. 106(2), 287297 (2011)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Ndisang JF : Role of heme oxygenase in inflammation, insulin-signalling, diabetes and obesity. Mediators Inflamm. 2010, 359732 (2010)

  • 37.

    Ndisang JF , Jadhav A : Heme oxygenase system enhances insulin sensitivity and glucose metabolism in streptozotocin-induced diabetes. Am. J. Physiol. Endocrinol. Metab. 296(4), E829E841 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Ndisang JF , Jadhav A : Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulin-resistant diabetes in Goto-Kakizaki rats. Endocrinology 150(6), 26272636 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Ndisang JF , Jadhav A , Mishra M : The heme oxygenase system suppresses perirenal visceral adiposity, abates renal inflammation and ameliorates diabetic nephropathy in Zucker diabetic fatty rats. PLoS One 9(1), e87936 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Ndisang JF , Lane N , Jadhav A : The heme oxygenase system abates hyperglycemia in Zucker diabetic fatty rats by potentiating insulin-sensitizing pathways. Endocrinology 150(5), 20982108 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Olson NC , Callas PW , Hanley AJ , Festa A , Haffner SM , Wagenknecht LE , Tracy RP : The insulin resistance atherosclerosis study. J. Clin. Endocrinol. Metab. 97(3), 10321040 (2012)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Pae HO , Kim EC , Chung HT : Heme oxygenase-1 and carbon monoxide: emerging therapeutic targets in inflammation and allergy. Recent Pat Inflamm. Allergy Drug Discov. 2, 159165 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Pan Y , Zhang X , Wang Y , Cai L , Ren L , Tang L , Wang J , Zhao Y , Wang Y , Liu Q , Li X , Liang G : Targeting JNK by a new curcumin analog to inhibit NF-kB-mediated expression of cell adhesion molecules attenuates renal macrophage infiltration and injury in diabetic mice. PLoS One 8(11), e79084 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Rücker M , Schäfer T , Roesken F , Spitzer WJ , Bauer M , Menger MD : Reduction of inflammatory response in composite flap transfer by local stress conditioning-induced heat-shock protein 32. Surgery 129, 292301 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Saleh MA , Boesen EI , Pollock JS , Savin VJ , Pollock DM : Endothelin-1 increases glomerular permeability and inflammation independent of blood pressure in the rat. Hypertension 56(5), 942949 (2010)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Sasaki T , Takahashi T , Maeshima K , Shimizu H , Toda Y , Morimatsu H , Takeuchi M , Yokoyama M , Akagi R , Morita K : Heme arginate pretreatment attenuates pulmonary NF-κB and AP-1 activation induced by hemorrhagic shock via heme oxygenase-1 induction. Med. Chem. 2, 271274 (2006)

    • Search Google Scholar
    • Export Citation
  • 47.

    Sauvanet JP : Chronic kidney disease, an often underestimated complication of diabetes. Soins 794, S4S11 (2015)

  • 48.

    Sharma S , Kulkarni SK , Chopra K : Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 33, 940945 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Silva G , Cunha A , Grégoire IP , Seldon MP , Soares MP : The antiapoptotic effect of heme oxygenase-1 in endothelial cells involves the degradation of p38 alpha MAPK isoform. J. Immunol. 177, 18941903 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50.

    Somania R , Singhai AK , Shivgunde P , Jain D : Asparagus racemosus Willd (Liliaceae) ameliorates early diabetic nephropathy in STZ induced diabetic rats. Indian J. Exp. Biol. 50, 469475 (2012)

    • Search Google Scholar
    • Export Citation
  • 51.

    Song R , Kubo M , Morse D , Zhou Z , Zhang X , Dauber JH , Fabisiak J , Alber SM , Watkins SC , Zuckerbraun BS , Otterbein LE , Ning W , Oury TD , Lee PJ , McCurry KR , Choi AM : Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and antiapoptotic effects. Am. J. Pathol. 163, 231242 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 52.

    Su N , Li HY , Huang MF , Jiang ZP , Zhou TB : Association of monocyte chemoattractant protein-1 2518G/A gene polymorphism with diabetic nephropathy risk. J. Recept. Signal Transduct. Res. 35, 9497 (2015)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 53.

    Su X , Chen X , Liu L , Chang X , Yu X , Sun K : Intracellular adhesion molecule-1 K469E gene polymorphism and risk of diabetic microvascular complications: a meta-analysis. PLoS One 8(7), e69940 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54.

    Sun X , Pi J , Liu W , Hudson LG , Liu KJ , Feng C : Induction of heme oxygenase 1 by arsenite inhibits cytokine induced monocyte adhesion to human endothelial cells. Toxicol. Appl. Pharmacol. 236, 202209 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55.

    Tang SC , Leung J , Lai KN : Diabetic tubulopathy: an emerging entity. Contrib. Nephrol. 170, 124134 (2011)

  • 56.

    Tesch GH , Schwarting A , Kinoshita K , Lan HY , Rollins BJ , Kelley VR : Monocyte chemoattractant protein-1 promotes macrophage-mediated tubular, but not glomerular injury, in nephrotoxic serum nephritis. J. Clin. Invest. 103, 7380 (1999)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 57.

    Therrien FJ , Agharazii M , Lebel M , Larivière R : Neutralization of tumor necrosis factor-alpha reduces renal fibrosis and hypertension in rats with renal failure. Am. J. Nephrol. 36(2), 151161 (2012)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 58.

    Varley H (1980): Non-protein nitrogen, urea, urate, creatine and creatinine. In: Practical and Clinical Biochemistry, ed Varley H, White Friars Press, London, pp. 452488

    • Search Google Scholar
    • Export Citation
  • 59.

    Virella G , Lopes-Virella MF : The role of the immune system in the pathogenesis of diabetic complications. Front. Endocrinol. (Lausanne) 5, 126 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60.

    Wagener F , da Silva JL , Farley T , de Witte T , Kappas A , Abraham NG : Differential effects of heme oxygenase isoforms on heme mediation endothelial intracellular adhesion molecule 1 expression. J. Pharmacol. Exp. Ther. 291, 416423 (1999)

    • Search Google Scholar
    • Export Citation
  • 61.

    Weis N , Weigert A , von Knethen A , Brüne B : Heme oxygenase-1 contributes to an alternative macrophage activation profile induced by apoptotic cell supernatants. Mol. Biol. Cell 20, 12801288 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62.

    Woessner JF : The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch. Biochem. Biophys. 93, 440447 (1961)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 63.

    Wu H , Kong L , Zhou S , Cui W , Xu F , Luo M , Li X , Tan Y , Miao L : The role of microRNAs in diabetic nephropathy. J. Diabetes Res. 2014, 920134 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64.

    Yi B , Hu X , Zhang H , Huang J , Liu J , Hu J , Li W , Huang L : Nuclear NF-κB p65 in peripheral blood mononuclear cells correlates with urinary MCP-1, RANTES and the severity of type 2 diabetic nephropathy. PLoS One 9(6), e99633 (2014)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 65.

    Zhang Z , Yuan W , Sun L , Szeto FL , Wong KE , Li X , Kong J , Li YC : 1, 25-Dihydroxy vitamin D3 targeting of NF-κB suppresses high glucose-induced MCP-1 expression in mesangial cells. Kidney Int. 72, 193201 (2007)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66.

    Zhou D , Brown SA , Yu T , Chen G , Barve S , Kang BC , Thompson JS : A high dose of ionizing radiation induces tissue specific activation of nuclear factor-κB in vivo. Radiat. Res. 151, 703709 (1999)

    • Crossref
    • Search Google Scholar
    • Export Citation
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