Abstract
The recognition that heme oxygenase (HO) activity is induced when tissues are exposed to heme and other insults raised the question of the functional significance of such induction.1–4 Evidence attesting to the cytoprotective effects of such induction of HO was first presented in the glycerol model of acute renal failure wherein the kidney is exposed acutely to a large burden of heme proteins originating from damaged skeletal muscle and red blood cells;5 examination of the induction of HO-1 in this disease model was predicated, in part, on the recognized toxicity of heme when present in inordinate amounts in tissues.6
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abraham N.G. Lin J.H.-C, Schwartzman M.L. Levere R.D., and Shibahara S.: The physiological significance of heme oxygenase. Int J Biochem 20:543–558, 1988.
Maines M.D.: Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2:2557–2568, 1988.
Keyse S.M. and Tyrrell R.M.: Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide and sodium arsenite. Proc Natl Acad Sci, USA 86:99–103, 1989.
Stocker R.: Induction of haem oxygenase as a defense against oxidative stress. Free Rad Res Comms 9:101–112, 1990.
Nath K.A., Balla G., Vercellotti G.M., Balla J., Jacob H.S., Levitt M.D., and Rosenberg M.E.: Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90:267–270, 1992.
Nath K.A., Agarwal A., and Vogt B.: Functional consequences of induction of heme oxygenase. In: Contemporary Issues in Nephrology. “Acute renal failure: emerging concepts and therapeutic strategies” Goligorsky MS (ed), Series Editor J Stein, Churchill Livingstone, chapter 5, p 97–118, 1995.
Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., and Vercellotti G.M.: Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 267:18148–18153, 1992.
Balla J., Jacob H.S., Balla G., Nath K.A., Eaton J.W., and Vercellotti G.M.: Endothelial-cell heme uptake from heme proteins: Induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci 90:9285–9289, 1993.
Vogt B.A., Alam J., Croatt A.J., Vercellotti G.M., and Nath K.A.: Acquired resistance to acute oxidative stress: possible role of heme oxygenase and ferritin. Lab Invest 72:474–483, 1995.
Nath K.A., Balla J., Croatt A.J., and Vercellotti G.M.: Heme protein-mediated renal injury: a protective role for 21-aminosteroids in vitro and in vivo. Kidney Int 47:592–602, 1995.
Balla J., Nath K.A., Balla G., Juckett M.B., Jacob H.S., and Vercellotti G.M.: Endothelial cell heme oxygenase and ferritin induction in rat lung by hemoglobin in vivo. Am J Physiol 268:L321–L327, 1995.
Vogt B.A., Shanley T.P., Croatt A.J., Alam J., Johnson K.J., and Nath K.A.: Glomerular inflammation induces resistance to tubular injury in the rat: a novel form of acquired heme oxygenase-dependent resistance to renal injury. J Clin Invest 98:2139–2145, 1996.
Nath K.A.: Adaptation to the nephrotoxicity of heme proteins. Exp Nephrol 4:139–143, 1996.
Nath K.A., Grande J.P., Croatt A.J., Likely S., Hebbel R.P., and Enright H.: Intracellular targets in heme protein induced renal injury. Kidney Int: 53:100–111, 1998.
Warden D.H., Croatt A.J., Katusic Z.S., and Nath K.A.: Physiologic characterization of acute reversible systemic hypertension in a model of heme protein-induced renal injury. Am J Physiol 277:F58–F65, 1999.
Nath K.A., Croatt A.J., Haggard J.J., and Grande J.P.: Renal response to repetitive exposure to heme proteins: Chronic injury induced by an acute insult. Kidney Int 57:2423–2433, 2000.
Nath K.A., Haggard J.J., Croatt A.J., Grande J.P., Poss K.D., and Alam J.: The indispensability of heme oxygenase-1 (HO-1) in protecting against heme protein-induced toxicity in vivo. Am J Pathol 156:1527–1535,2000.
Nath K.A., Vercellotti G., Grande J.P., Miyoshi H., Paya C.V., Manivel J.C., Haggard J.J., Croatt A.J., Payne W.D., and Alam J.: Heme protein-induced chronic renal inflammation: Suppressive effect of induced heme oxygenase-1. Kidney Int 59:106–117, 2001.
Leung N., Croatt A.J., Haggard J.J., Grande J.P., and Nath K.A.: Acute cholestatic liver disease protects against glycerol-induced acute renal failure in the rat: a novel form of acquired renal resistance to injury. Kidney Int 60:1047–1057, 2001.
Nath K.A., Grande J.P., Haggard J.J., Croatt A.J., Katusic Z.S., Solovey A., and Hebbel R.P.: Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease. Am J Pathol 158:893–903,2001.
Hebbel R.P. and Eaton J.W.: Pathobiology of heme interaction with the erythrocyte membrane. Semin Hematol 26:136–149, 1989.
Muller-Eberhard U. and Fraig M.: Bioactivity of heme and its containment. Am J Hematol 42:59–62, 1993.
Dhar, G.J., Bossenmaier I., Cardinal R., Petryka Z.J., and Watson C.J.: Transitory renal failure following rapid administration of a relatively large amount of hematin in a patient with acute intermittent porphyria in clinical remission. Acta Med Scan 203:437–443, 1978.
Balla G., Vercellotti G.M., Muller-Eberhard U., Eaton J., and Jacob H.S.: Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab Invest 64:648–655, 1991.
Abraham N.G., Lavrovsky Y., Schwartzman M.L., Stoltz R.A., Levere R.D., Gerritsen M.E., Shibahara S., and Kappas A.: Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci, USA 92:6798–6802, 1995.
Eisenstein R.S., Garcia-Mayol D., Pettingell W., and Munro H.N.: Regulation of ferritin and heme oxygenase synthesis in rat fìbroblasts by different forms of iron. Proc Natl Acad Sci, USA 88:688–692, 1991.
Ferris C.D., Jaffrey S.R., Sawa A., Takahashi M., Brady S.D., Barrow R.K., Tysoe S.A., Wolosker H., Baranano D.E., Dore S., Poss K.D., and Snyder S.H.: Haem oxygenase-1 prevents cell death by regulating cellular iron. Nature Cell Biol 1:152–157, 1999.
Barañano D.E., Wolosker H., Bae B.I., Barrow R.K., Snyder S.H., and Ferris C.D.: A mammalian iron ATPase induced by iron. J Biol Chem 275:15166–15173, 2000.
Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., and Ames B.N.: Bilirubin is an anti-oxidant of possible physiologic significance. Science 235:1043–1046, 1987.
Stocker R., Glazer A.N., and Ames B.N.: Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci, USA 84:5918–5922, 1987.
Llesuy S.F. and Tomaro M.L.: Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim Biophys Acta 1223:9–14, 1994.
Eguchi D., Weiler D., Alam J., Nath K., and Katusic Z.S.: Protective effect of heme oxyenase-1 gene transfer against oxyhemoglobin-induced endothelial dysfunction. J Cereb Blood Flow Metab 21:1215–1222,2001.
Motterlini R., Gonzales A., Foresti R., Clark J.E., Green C.J., and Winslow R.M.: Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res 83:568–577, 1998.
Hill P.A., Davies D.J., Kincaid-Smith P., and Ryan G.B.: Ultrastructural changes in renal tubules associated with glomerular bleeding. Kidney Int 36:992–997, 1989.
Madsen K.M., Applegate C.W., and Tisher C.C.: Phagocytosis of erythrocytes by the proximal tubule of the rat kidney. Cell Tissue Res 226:363–374, 1982.
Saborio P. and Scheinman J.I.: Sickle cell nephropathy. J Am Soc Nephrol 10:187–192, 1999.
Clark D.A., Butler S.A., Braren V., Hartmann R.C., and Jenkins Jr D.E.: The kidney in paroxysmal nocturnal hemoglobinuria. Blood 57:83–89, 1981.
Ohta K., Yachie A., Fujimoto K., Kaneda H., Wada T., Toma T., Seno A., Kasahara Y., Yokoyama H., Seki H., and Koizumi S.: Tubular injury as a cardinal pathologic feature in human heme oxygenase-1 deficiency. Am J Kidney Dis 35:863–870, 2000.
Morimoto K., Ohta K., Yachie A., Yang Y., Shimizu M., Goto C., Toma T., Kasahara Y., Yokoyama H., Miyata T., Seki H., and Koizumi S.: Cytoprotective role of heme oxygenase (HO)-l in human kidney with various renal diseases. Kidney Int 60:1858–1866, 2001.
Wenzel U.O. and Abboud H.E.: Chemokines and renal disease. Am J Kid Dis 26:982–994, 1995.
Tesch G.H., Schwarting A., Kinoshita K., Lan H.Y., Rollins B.J., and Kelley V.R.: Monocyte chemoattractant protein-1 promotes macrophage-mediated tubular injury, but not glomerular injury, in nephrotoxic serum nephritis. J Clin Invest 103:73–80, 1999.
Wada T., Furuichi K., Segawa-Takeda C., Shimizu M., Sakai N., Takeda S.-L., Takasawa K., Kida H., Kobayashi K.-I., Mukaida N., Ohmoto Y., Matsuhima K., and Yokoyama H.: MIP-1α and MCP-1 contribute to crescents and interstitial lesions in human crescentic glomerulonephritis. Kidney Int 56:995–1003, 1999.
Ishikawa Y., Sugiyama H., Stylianou E., Kitamura M.: Bioflavonoid quercetin inhibits interleukin-1-induced transcriptional expression of monocyte chemoattractant protein-1 in glomerular cells via suppression of nuclear factor-κB. J Am Soc Nephrol 10:2290–2296, 1999.
Gu L., Tseng S.C., and Rollins B.J.: Monocyte hemoattractant protein-1. Chem Immunol 72:7–29, 1999.
Morita T. and Kourembanas S.: Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest 96:2676–2682, 1995.
Otterbein L.E., Bach F.H., Alam J., Soares M., Tao L.H., Wysk M., Davis R.J., Flavell R.A., and Choi A.M.: Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nature Med 6:422–428, 2000.
Otterbein L.E. and Choi A.M.: Heme oxygenase: color of defense against cellular stress. Am J Physiol 279:L1029–L1037, 2000.
Hayashi S., Takamiya R., Yamaguchi T., Matsumoto K., Tojo S.J., Tamatani T., Kitajima M., Makino N., Ishimura Y., and Suematsu M.: Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress. Circ Res 85:663–671, 1999.
Kwak J.Y., Takeshige K., Cheung B.S., and Minakami S.: Bilirubin inhibits the activation of super-oxide-producing NADPH oxidase in a neutrophil cell-free system. Biochem Biophys Acta 1076: 369–373, 1991.
Frank A.D., Wagener T.G., Da Silva J.-L., Farley T., De Witte T., Kappas A., and Abraham N.G.: Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Therap 291:416–423, 1999.
Maines M.D., Mayer R.D., Ewing J.F., and McCoubrey W.K. Jr: Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: Possible role of heme as both promoter of tissue damage and regulator of HSP32. J Pharmacol Exp Therap 264:457–462, 1993.
Agarwal A., Balla J., Alam J., Croatt A.J., and Nath K.A.: Induction of heme oxygenase in toxic renal injury: a protective role in cisplatin nephrotoxicity in the rat. Kidney Int 48:1298–1307, 1995.
Shiraishi F., Curtis L.M., Truong L., Poss K., Visner G.A., Madsen K., Nick H.S., and Agarwal A.: Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol 278:F726–F36, 2000.
Nath K.A., Croatt A.J., Likely S., Behrens T.W., and Warden D.: Renal oxidant injury and oxidant response induced by mercury. Kidney Int 50:1032–1043, 1996.
Agarwal A., Kim Y., Matas A.J., Alam J., and Nath K.A.: Gas-generating systems in acute renal allograft rejection in the rat: co-induction of heme oxygenase and nitric oxide synthase. Transplantation 61:93–98, 1996.
Mosley K., Wembridge D.E., Cattell V., and Cook H.T.: Heme oxygenase is induced in nephrotoxic nephritis and hemin, a stimulator of heme oxygenase synthesis, ameliorates disease. Kidney Int 53:672–678, 1998.
Datta P.K., Koukouritaki S.B., Hopp K.A., and Lianos E.A.: Heme oxygenase-1 induction attenuates inducible nitric oxide synthase expression and proteinuria in glomerulonephritis. J Am Soc Nephrol 10:2540–2550, 1999.
Haugen E.N., Croatt A.J., and Nath K.A.: Angiotensin II induces renal oxidant stress in vivo and heme oxygenase-1 in vivo and in vitro. Kidney Int 58:144–152, 2000.
Kawada N., Moriyama T., Ando A., Fukunaga M., Miyata T., Kurokawa K., Imai E., and Hori M.: Increased oxidative stress in mouse kidneys with unilateral ureteral obstruction. Kidney Int 56:1004–1013, 1999.
Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., and Koizumi S.: Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103:129–135, 1999.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer Science+Business Media New York
About this chapter
Cite this chapter
Pittock, S.T., Nath, K.A. (2002). Induction of Heme Oxygenase-1 as a Protective Response Against Heme Protein-Induced Renal Injury. In: Abraham, N.G. (eds) Heme Oxygenase in Biology and Medicine. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0741-3_20
Download citation
DOI: https://doi.org/10.1007/978-1-4615-0741-3_20
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5219-8
Online ISBN: 978-1-4615-0741-3
eBook Packages: Springer Book Archive