Cytoglobin, a novel member of the globin family, protects kidney fibroblasts against oxidative stress under ischemic conditions

American Journal of Pathology

Volumn 178, Issue 1, 2011, Pages 128-139

  Nishi, Hiroshi ^a   Inagi, Reiko ^a   Kawada, Norifumi ^b   Yoshizato, Katsutoshi ^c,d   Mimura, Imari ^a   Fujita, Toshiro ^a   Nangaku, Masaomi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

^d PhoenixBio USA Corporation   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOGLOBIN; HYDROGEN PEROXIDE; MESSENGER RNA; SCAVENGER; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL COUNT; CELL VIABILITY; CONTROLLED STUDY; FIBROBLAST; GENE OVEREXPRESSION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; KIDNEY CORTEX; KIDNEY DYSFUNCTION; KIDNEY ISCHEMIA; MALE; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RENAL PROTECTION; REPERFUSION INJURY; TISSUE INJURY; UREA NITROGEN BLOOD LEVEL;

EID: 79251520307     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.011     Document Type: Article

References (47)

1. Hardison RC: A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc Natl Acad Sci USA 1996, 93:5675-5679
2. Wittenberg BA, Wittenberg JB: Transport of oxygen in muscle. Annu Rev Physiol 1989, 51:857-878
3. Kawada N, Kristensen DB, Asahina K, Nakatani K, Minamiyama Y, Seki S, Yoshizato K: Characterization of a stellate cell activation-associated protein (STAP) with peroxidase activity found in rat hepatic stellate cells. J Biol Chem 2001, 276:25318-25323
4. Trent JT III, Hargrove MS: A ubiquitously expressed human hexacoordinate hemoglobin. J Biol Chem 2002, 277:19538-19545
5. Burmester T, Ebner B, Weich B, Hankeln T: Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 2002, 19:416-421 (Pubitemid 34289416)
6. Schmidt M, Gerlach F, Avivi A, Laufs T, Wystub S, Simpson JC, Nevo E, Saaler-Reinhardt S, Reuss S, Hankeln T, Burmester T: Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J Biol Chem 2004, 279:8063-8069
7. Nakatani K, Okuyama H, Shimahara Y, Saeki S, Kim DH, Nakajima Y, Seki S, Kawada N, Yoshizato K: Cytoglobin/STAP, its unique localization in splanchnic fibroblast-like cells and function in organ fibrogenesis. Lab Invest 2004, 84:91-101
8. Pesce A, Bolognesi M, Bocedi A, Ascenzi P, Dewilde S, Moens L, Hankeln T, Burmester T: Neuroglobin and cytoglobin: fresh blood for the vertebrate globin family. EMBO Rep 2002, 3:1146-1151
9. Mammen PP, Shelton JM, Ye Q, Kanatous SB, McGrath AJ, Richardson JA, Garry DJ: Cytoglobin is a stress-responsive hemoprotein expressed in the developing and adult brain. J Histochem Cytochem 2006, 54:1349-1361 (Pubitemid 44788820)
10. Fordel E, Thijs L, Martinet W, Lenjou M, Laufs T, Van Bockstaele D, Moens L, Dewilde S: Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci Lett 2006, 410:146-151
11. Li D, Chen XQ, Li WJ, Yang YH, Wang JZ, Yu AC: Cytoglobin upregulated by hydrogen peroxide plays a protective role in oxidative stress. Neurochem Res 2007, 32:1375-1380
12. Tateaki Y, Ogawa T, Kawada N, Kohashi T, Arihiro K, Tateno C, Obara M, Yoshizato K: Typing of hepatic nonparenchymal cells using fibulin-2 and cytoglobin/STAP as liver fibrogenesis-related markers. Histochem Cell Biol 2004, 122:41-49
13. Shivapurkar N, Stastny V, Okumura N, Girard L, Xie Y, Prinsen C, Thunnissen FB, Wistuba II, Czerniak B, Frenkel E, Roth JA, Liloglou T, Xinarianos G, Field JK, Minna JD, Gazdar AF: Cytoglobin, the newest member of the globin family, functions as a tumor suppressor gene. Cancer Res 2008, 68:7448-7456
14. Halligan KE, Jourd'heuil FL, Jourd'heuil D: Cytoglobin is expressed in the vasculature and regulates cell respiration and proliferation via nitric oxide dioxygenation. J Biol Chem 2009, 284:8539-8547
15. Matsumoto M, Makino Y, Tanaka T, Tanaka H, Ishizaka N, Noiri E, Fujita T, Nangaku M: Induction of renoprotective gene expression by cobalt ameliorates ischemic injury of the kidney in rats. J Am Soc Nephrol 2003, 14:1825-1832
16. Kawakami T, Inagi R, Wada T, Tanaka T, Fujita T, Nangaku M: Indoxyl sulfate inhibits proliferation of human proximal tubular cells via endoplasmic reticulum stress. Am J Physiol Renal Physiol 2010, 299:F568-F576
17. Son D, Kojima I, Inagi R, Matsumoto M, Fujita T, Nangaku M: Chronic hypoxia aggravates renal injury via suppression of Cu/Zn-SOD: a proteomic analysis. Am J Physiol Renal Physiol 2008, 294:F62-F72
18. Kumagai T, Nangaku M, Kojima I, Nagai R, Ingelfinger JR, Miyata T, Fujita T, Inagi R: Glyoxalase I overexpression ameliorates renal ischemia- reperfusion injury in rats. Am J Physiol Renal Physiol 2009, 296:F912-F921
19. Khanna AK, Pieper GM: NADPH oxidase subunits (NOX-1, p22phox. Rac-1) and tacrolimus-induced nephrotoxicity in a rat renal transplant model. Nephrol Dial Transplant 2007, 22:376-385
20. Takeda N, Manabe I, Uchino Y, Eguchi K, Matsumoto S, Nishimura S, Shindo T, Sano M, Otsu K, Snider P, Conway S, Nagai R: Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010, 120:254-265
21. Niwa H, Yamamura K, Miyazaki J: Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991, 108:193-199
22. Miyata T, Inagi R, Nangaku M, Imasawa T, Sato M, Izuhara Y, Suzuki D, Yoshino A, Onogi H, Kimura M, Sugiyama S, Kurokawa K: Overexpression of the serpin megsin induces progressive mesangial cell proliferation and expansion. J Clin Invest 2002, 109:585-593
23. Inoue S, Inoue M, Fujimura S, Nishinakamura R: A mouse line expressing Sall1-driven inducible Cre recombinase in the kidney mesenchyme. Genesis 2010, 48:207-212
24. Cullere X, Lauterbach M, Tsuboi N, Mayadas TN: Neutrophil-selective CD18 silencing using RNA interference in vivo. Blood 2008, 111:3591-3598
25. Sommer M, Schaller R, Funfstuck R, Bohle A, Bohmer FD, Muller GA, Stein G: Abnormal growth and clonal proliferation of fibroblasts in an animal model of unilateral ureteral obstruction. Nephron 1999, 82:39-50 (Pubitemid 29206208)
26. Mimura I, Nangaku M, Nishi H, Inagi R, Tanaka T, Fujita T: Cytoglobin, a novel globin, plays an anti-fibrotic role in the kidney. Am J Physiol Renal Physiol 2010, 299:F1120-1133
27. Joki N, Kaname S, Hirakata M, Hori Y, Yamaguchi T, Fujita T, Katoh T, Kurokawa K: Tyrosine-kinase dependent TGF-beta and extracellular matrix expression by mechanical stretch in vascular smooth muscle cells. Hypertens Res 2000, 23:91-99
28. Nishi H, Inagi R, Kato H, Tanemoto M, Kojima I, Son D, Fujita T, Nangaku M: Hemoglobin is expressed by mesangial cells and reduces oxidant stress. J Am Soc Nephrol 2008, 19:1500-1508
29. Kojima I, Tanaka T, Inagi R, Nishi H, Aburatani H, Kato H, Miyata T, Fujita T, Nangaku M: Metallothionein is upregulated by hypoxia and stabilizes hypoxia-inducible factor in the kidney. Kidney Int 2009, 75:268-277
30. Nangaku M, Quigg RJ, Shankland SJ, Okada N, Johnson RJ, Couser WG: Overexpression of Crry protects mesangial cells from complement- mediated injury. J Am Soc Nephrol 1997, 8:223-233
31. Harris RC, Neilson EG: Toward a unified theory of renal progression. Annu Rev Med 2006, 57:365-380
32. Neilson EG: Mechanisms of disease: fibroblasts; a new look at an old problem. Nat Clin Pract Nephrol 2006, 2:101-108 (Pubitemid 43355218)
33. Fordel E, Geuens E, Dewilde S, Rottiers P, Carmeliet P, Grooten J, Moens L: Cytoglobin expression is upregulated in all tissues upon hypoxia: an in vitro and in vivo study by quantitative real-time PCR. Biochem Biophys Res Commun 2004, 319:342-348
34. Fordel E, Thijs L, Moens L, Dewilde S: Neuroglobin and cytoglobin expression in mice: evidence for a correlation with reactive oxygen species scavenging. Febs J 2007, 274:1312-1317
35. Wystub S, Ebner B, Fuchs C, Weich B, Burmester T, Hankeln T: Interspecies comparison of neuroglobin, cytoglobin and myoglobin: sequence evolution and candidate regulatory elements. Cytogenet Genome Res 2004, 105:65-78
36. Li C, Jackson RM: Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002, 282:C227-241
37. Kojima I, Tanaka T, Inagi R, Kato H, Yamashita T, Sakiyama A, Ohneda O, Takeda N, Sata M, Miyata T, Fujita T, Nangaku M: Protective role of hypoxia-inducible factor-2alpha against ischemic damage and oxidative stress in the kidney. J Am Soc Nephrol 2007, 18:1218-1226
38. Brezis M, Rosen S: Hypoxia of the renal medulla: its implications for disease. N Engl J Med 1995, 332:647-655
39. Nangaku M: Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 2006, 17:17-25
40. Ichimura T, Asseldonk EJ, Humphreys BD, Gunaratnam L, Duffield JS, Bonventre JV: Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest 2008, 118:1657-1668
41. Mayadas TN, Rosetti F, Ernandez T, Sethi S: Neutrophils: game changers in glomerulonephritis?. Trends Mol Med 2010, 16:368-378
42. Forbes JM, Hewitson TD, Becker GJ, Jones CL: Ischemic acute renal failure: long-term histology of cell and matrix changes in the rat. Kidney Int 2000, 57:2375-2385
43. Spurgeon KR, Donohoe DL, Basile DP: Transforming growth factorbeta in acute renal failure: receptor expression, effects on proliferation, cellularity, and vascularization after recovery from injury. Am J Physiol Renal Physiol 2005, 288:F568-577
44. Davies M, Harris S, Rudland P, Barraclough R: Expression of the rat: S-100-related, calcium-binding protein gene, p9Ka, in transgenic mice demonstrates different patterns of expression between these two species. DNA Cell Biol 1995, 14:825-832
45. Flogel U, Godecke A, Klotz LO, Schrader J: Role of myoglobin in the antioxidant defense of the heart. FASEB J 2004, 18:1156-1158 (Pubitemid 39561555)
46. Dewilde S, Kiger L, Burmester T, Hankeln T, Baudin-Creuza V, Aerts T, Marden MC, Caubergs R, Moens L: Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem 2001, 276:38949-38955
47. Sawai H, Makino M, Mizutani Y, Ohta T, Sugimoto H, Uno T, Kawada N, Yoshizato K, Kitagawa T, Shiro Y: Structural characterization of the proximal and distal histidine environment of cytoglobin and neuroglobin. Biochemistry 2005, 44:13257-13265