Cytochrome c oxidase subunit 4 isoform 2-knockout mice show reduced enzyme activity, airway hyporeactivity, and lung pathology

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3916-3930

  Hüttemann, Maik ^a   Lee, Icksoo ^a   Gao, Xiufeng ^a   Pecina, Petr ^a,j   Pecinova, Alena ^a,j   Liu, Jenney ^a   Aras, Siddhesh ^a   Sommer, Natascha ^b   Sanderson, Thomas H ^a   Tost, Monica ^c,k   Neff, Frauke ^c   Aguilar Pimentel, Juan Antonio ^d,e   Becker, Lore ^c,g   Naton, Beatrix ^c   Rathkolb, Birgit ^c,h   Rozman, Jan ^c,e   Favor, Jack ^c   Hans, Wolfgang ^c   Prehn, Cornelia ^c   Puk, Oliver ^c   Schrewe, Anja ^c   Sun, Minxuan ^c   Höfler, Heinz ^c,f   Adamski, Jerzy ^c,e   Bekeredjian, Raffi ⁱ   Graw, Jochen ^c   Adler, Thure ^c   Busch, Dirk H ^e   Klingenspor, Martin ^e   Klopstock, Thomas ^g   Ollert, Markus ^d,e   Wolf, Eckhard ^h   Fuchs, Helmut ^c   Gailus Durner, Valérie ^c   Hrabě De Angelis, Martin ^c,e   Weissmann, Norbert ^b   Doan, Jeffrey W ^a   Bassett, David J P ^a   Grossman, Lawrence I ^a   more..

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d Department of Dermatology and Allergy ^*  (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^h UNIVERSITY OF MUNICH   (Germany)

ⁱ UNIVERSITY OF HEIDELBERG   (Germany)

^j INSTITUTE OF MATHEMATICS   (Czech Republic)

^k UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

more..

Author keywords

Asthma; CCO4 2; COX4 2; COX4i2; Inflammation; Oxidative phosphorylation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 4I2; UNCLASSIFIED DRUG;

AIRWAY HYPOREACTIVITY; AIRWAY RESISTANCE; ALLOSTERISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; CRYSTAL; ENERGY COST; ENZYME ACTIVITY; ENZYME ISOLATION; FEMALE; GENE INACTIVATION; GLUCOSE TOLERANCE; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; LIVER; LONG TERM CARE; LUNG FUNCTION; LUNG PARENCHYMA; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHENOTYPE; PINCH STRENGTH; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; WILD TYPE;

ANIMALS; BASE SEQUENCE; BLOTTING, NORTHERN; BLOTTING, WESTERN; DNA PRIMERS; ELECTRON TRANSPORT COMPLEX IV; LUNG; MICE; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION;

MUS;

EID: 84865798029     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-203273     Document Type: Article

References (67)

1. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136-1144
2. Villani, G., Greco, M., Papa, S., and Attardi, G. (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 273, 31829-31836
3. Acin-Perez, R., Bayona-Bafaluy, M. P., Bueno, M., Machicado, C., Fernandez-Silva, P., Perez-Martos, A., Montoya, J., Lopez-Perez, M. J., Sancho, J., and Enriquez, J. A. (2003) An intragenic suppressor in the cytochrome c oxidase I gene of mouse mitochondrial DNA. Hum. Mol. Genet. 12, 329-339
4. Villani, G., and Attardi, G. (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc. Natl. Acad. Sci. U. S. A. 94, 1166-1171
5. Piccoli, C., Scrima, R., Boffoli, D., and Capitanio, N. (2006) Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state. Biochem. J. 396, 573-583
6. Dalmonte, M. E., Forte, E., Genova, M. L., Giuffre, A., Sarti, P., and Lenaz, G. (2009) Control of respiration by cytochrome c oxidase in intact cells: role of the membrane potential. J. Biol. Chem. 284, 32331-32335
7. Pacelli, C., Latorre, D., Cocco, T., Capuano, F., Kukat, C., Seibel, P., and Villani, G. (2010) Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 11, 334-341
8. Hinkle, P. C., Kumar, M. A., Resetar, A., and Harris, D. L. (1991) Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry 30, 3576-3582
9. Hüttemann, M., Lee, I., Pecinova, A., Pecina, P., Przyklenk, K., and Doan, J. W. (2008) Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J. Bioenerg. Biomembr. 40, 445-456
10. Grossman, L. I., and Lomax, M. I. (1997) Nuclear genes for cytochrome c oxidase. Biochim. Biophys. Acta 1352, 174-192
11. Hüttemann, M., Jaradat, S., and Grossman, L. I. (2003) Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb - the counterpart to testes-specific cytochrome c? Mol. Reprod. Dev. 66, 8-16
12. Hüttemann, M., Schmidt, T. R., and Grossman, L. I. (2003) A third isoform of cytochrome c oxidase subunit VIII is present in mammals. Gene 312, 95-102
13. Napiwotzki, J., Shinzawa-Itoh, K., Yoshikawa, S., and Kadenbach, B. (1997) ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem. 378, 1013-1021
14. Arnold, S., and Kadenbach, B. (1999) The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett. 443, 105-108
15. Acin-Perez, R., Gatti, D. L., Bai, Y., and Manfredi, G. (2011) Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab. 13, 712-719
16. Hüttemann, M., Kadenbach, B., and Grossman, L. I. (2001) Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267, 111-123
17. Lee, I., Salomon, A. R., Yu, K., Samavati, L., Pecina, P., Pecinova, A., and Hüttemann, M. (2009) Isolation of regulatory-competent, phosphorylated cytochrome c oxidase. Methods Enzymol. 457, 193-210
18. Lee, I., Salomon, A. R., Ficarro, S., Mathes, I., Lottspeich, F., Grossman, L. I., and Hüttemann, M. (2005) cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J. Biol. Chem. 280, 6094-6100
19. Tybulewicz, V. L., Crawford, C. E., Jackson, P. K., Bronson, R. T., and Mulligan, R. C. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl protooncogene. Cell 65, 1153-1163
20. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
21. Bassett, D. J., Elbon, C. L., and Reichenbaugh, S. S. (1992) Respiratory activity of lung mitochondria isolated from oxygen-exposed rats. Am. J. Physiol. 263, L439-445
22. Fisher, A. B., Scarpa, A., LaNoue, K. F., Bassett, D., and Williamson, J. R. (1973) Respiration of rat lung mitochondria and the influence of Ca 2+ on substrate utilization. Biochemistry 12, 1438-1445
23. Lee, I., Pecinova, A., Pecina, P., Neel, B. G., Araki, T., Kucherlapati, R., Roberts, A. E., and Hüttemann, M. (2010) A suggested role for mitochondria in Noonan syndrome. Biochim. Biophys. Acta 1802, 275-283
24. Weissmann, N., Akkayagil, E., Quanz, K., Schermuly, R. T., Ghofrani, H. A., Fink, L., Hanze, J., Rose, F., Seeger, W., and Grimminger, F. (2004) Basic features of hypoxic pulmonary vasoconstriction in mice. Respir. Physiol. Neurobiol. 139, 191-202
25. Weissmann, N., Dietrich, A., Fuchs, B., Kalwa, H., Ay, M., Dumitrascu, R., Olschewski, A., Storch, U., Mederos y Schnitzler, M., Ghofrani, H. A., Schermuly, R. T., Pinkenburg, O., Seeger, W., Grimminger, F., and Gudermann, T. (2006) Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc. Natl. Acad. Sci. U. S. A. 103, 19093-19098
26. Bassett, D., Hirata, F., Gao, X., Kannan, R., Kerr, J., Doyon-Reale, N., Wilson, S., and Lieh-Lai, M. (2010) Reversal of methylprednisolone effects in allergen-exposed female BALB/c mice. J. Toxicol. Environ. Health A. 73, 711-724
27. Birrell, M. A., Battram, C. H., Woodman, P., McCluskie, K., and Belvisi, M. G. (2003) Dissociation by steroids of eosinophilic inflammation from airway hyperresponsiveness in murine airways. Respir. Res. 4, 3
28. DeLorme, M. P., and Moss, O. R. (2002) Pulmonary function assessment by whole-body plethysmography in restrained versus unrestrained mice. J. Pharmacol. Toxicol. Methods 47, 1-10
29. Hamelmann, E., Schwarze, J., Takeda, K., Oshiba, A., Larsen, G. L., Irvin, C. G., and Gelfand, E. W. (1997) Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156, 766-775
30. Whitehead, G. S., Walker, J. K., Berman, K. G., Foster, W. M., and Schwartz, D. A. (2003) Allergen-induced airway disease is mouse strain dependent. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L32-L42
31. Hahn, Y. S., Taube, C., Jin, N., Takeda, K., Park, J. W., Wands, J. M., Aydintug, M. K., Roark, C. L., Lahn, M., O'Brien, R. L., Gelfand, E. W., and Born, W. K. (2003) V gamma 4+ gamma delta T cells regulate airway hyperreactivity to methacholine in ovalbumin-sensitized and challenged mice. J. Immunol. 171, 3170-3178
32. DeLorme, M. P., Yang, H., Elbon-Copp, C., Gao, X., Barraclough-Mitchell, H., and Bassett, D. J. (2002) Hyperresponsive airways correlate with lung tissue inflammatory cell changes in ozone-exposed rats. J. Toxicol. Environ. Health A 65, 1453-1470
33. Holt, P. G., Degebrodt, A., Venaille, T., O'Leary, C., Krska, K., Flexman, J., Farrell, H., Shellam, G., Young, P., Penhale, J., Robertson, T., and Papadimitriou, J. M. (1985) Preparation of interstitial lung cells by enzymatic digestion of tissue slices: preliminary characterization by morphology and performance in functional assays. Immunology 54, 139-147
34. Schultheis, A. H., and Bassett, D. J. (1994) Guinea pig lung inflammatory cell changes following acute ozone exposure. Lung 172, 169-181
35. Li, C. Y., Lam, K. W., and Yam, L. T. (1973) Esterases in human leukocytes. J. Histochem. Cytochem. 21, 1-12
36. Gailus-Durner, V., Fuchs, H., Becker, L., Bolle, I., Brielmeier, M., Calzada-Wack, J., Elvert, R., Ehrhardt, N., Dalke, C., Franz, T. J., Grundner-Culemann, E., Hammelbacher, S., Hölter, S. M., Hölzlwimmer, G., Horsch, M., Javaheri, A., Kalaydjiev, S. V., Klempt, M., Kling, E., Kunder, S., Lengger, C., Lisse, T., Mijalski, T., Naton, B., Pedersen, V., Prehn, C., Przemeck, G., Rácz, I., Reinhard, C., Reitmeir, P., Schneider, I., Schrewe, A., Steinkamp, R., Zybill, C., Adamski, J., Beckers, J., Behrendt, H., Favor, J., Graw, J., Heldmaier, G., Höfler, H., Ivandic, B., Katus, H., Kirchhof, P., Klingenspor, M., Klopstock, T., Lengeling, A., Müller, W., Ohl, F., Ollert, M., Quintanilla-Martinez, L., Schmidt, J., Schulz, H., Wolf, E., Wurst, W., Zimmer, A., Busch, D. H., and Hrabě de Angelis, M. (2005) Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat. Methods 2, 403-404
37. Fuchs, H., Gailus-Durner, V., Adler, T., Aguilar-Pimentel, J. A., Becker, L., Calzada-Wack, J., Da Silva-Buttkus, P., Neff, F., Gotz, A., Hans, W., Hölter, S. M., Horsch, M., Kastenmüller, G., Kemter, E., Lengger, C., Maier, H., Matloka, M., Moller, G., Naton, B., Prehn, C., Puk, O., Rácz, I., Rathkolb, B., Römisch-Margl, W., Rozman, J., Wang-Sattler, R., Schrewe, A., Stöger, C., Tost, M., Adamski, J., Aigner, B., Beckers, J., Behrendt, H., Busch, D. H., Esposito, I., Graw, J., Illig, T., Ivandic, B., Klingenspor, M., Klopstock, T., Kremmer, E., Mempel, M., Neschen, S., Ollert, M., Schulz, H., Suhre, K., Wolf, E., Wurst, W., Zimmer, A., and Hrabě de Angelis, M. (2011) Mouse phenotyping. Methods 53, 120-135
38. Pecinova, A., Drahota, Z., Nuskova, H., Pecina, P., and Houstek, J. (2011) Evaluation of basic mitochondrial functions using rat tissue homogenates. Mitochondrion 11, 722-728
39. Rosai, J., Ed. (2004) Rosai and Ackerman's Surgical Pathology, Edinburgh, Mosby
40. Ludwig, B., Bender, E., Arnold, S., Hüttemann, M., Lee, I., and Kadenbach, B. (2001) Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem 2, 392-403
41. Dudley, R. (1998) Atmospheric oxygen, giant Paleozoic insects and the evolution of aerial locomotor performance. J. Exp. Biol. 201(Pt. 8), 1043-1050
42. Hüttemann, M., Lee, I., Liu, J., and Grossman, L. I. (2007) Transcription of mammalian cytochrome c oxidase subunit IV-2 is controlled by a novel conserved oxygen responsive element. FEBS J. 274, 5737-5748
43. Fukuda, R., Zhang, H., Kim, J. W., Shimoda, L., Dang, C. V., and Semenza, G. L. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129, 111-122
44. Benard, G., Faustin, B., Passerieux, E., Galinier, A., Rocher, C., Bellance, N., Delage, J. P., Casteilla, L., Letellier, T., and Rossignol, R. (2006) Physiological diversity of mitochondrial oxidative phosphorylation. Am. J. Physiol. Cell Physiol. 291, C1172-C1182
45. Vijayasarathy, C., Biunno, I., Lenka, N., Yang, M., Basu, A., Hall, I. P., and Avadhani, N. G. (1998) Variations in the subunit content and catalytic activity of the cytochrome c oxidase complex from different tissues and different cardiac compartments. Biochim. Biophys. Acta 1371, 71-82
46. Holgate, S. T. (2005) Exacerbations: the asthma paradox. Am. J. Respir. Crit. Care Med. 172, 941-943
47. Shanske, A. L., Shanske, S., Silvestri, G., Tanji, K., Wertheim, D., and Lipper, S. (1993) MELAS point mutation with unusual clinical presentation. Neuromuscul. Disord 3, 191-193
48. Kiernan, M. C., Bullpitt, P., and Chan, J. H. (2004) Mitochondrial dysfunction and rod-like lesions associated with administration of beta2 adrenoceptor agonist formoterol. Neuromuscul. Disord 14, 375-377
49. Trian, T., Benard, G., Begueret, H., Rossignol, R., Girodet, P. O., Ghosh, D., Ousova, O., Vernejoux, J. M., Marthan, R., Tunon-de-Lara, J. M., and Berger, P. (2007) Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J. Exp. Med. 204, 3173-3181
50. Yamano, K., Inoue, M., Masaki, S., Saki, M., Ichimura, M., and Satoh, M. (2005) Human adenosine A(3) receptor leads to intracellular Ca(2+) mobilization but is insufficient to activate the signaling pathway via phosphoinositide 3-kinase gamma in mice. Biochem. Pharmacol. 70, 1487-1496
51. Robb-Gaspers, L. D., Burnett, P., Rutter, G. A., Denton, R. M., Rizzuto, R., and Thomas, A. P. (1998) Integrating cytosolic calcium signals into mitochondrial metabolic responses. EMBO J. 17, 4987-5000
52. Wesley, U. V., Bove, P. F., Hristova, M., McCarthy, S., and van der Vliet, A. (2007) Airway epithelial cell migration and wound repair by ATP-mediated activation of dual oxidase 1. J. Biol. Chem. 282, 3213-3220
53. Weller, P. F., Bach, D. S., and Austen, K. F. (1984) Biochemical characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase). J. Biol. Chem. 259, 15100-15105
54. Ackerman, S. J., Liu, L., Kwatia, M. A., Savage, M. P., Leonidas, D. D., Swaminathan, G. J., and Acharya, K. R. (2002) Charcot-Leyden crystal protein (galectin-10) is not a dual function galectin with lysophospholipase activity but binds a lysophospholipase inhibitor in a novel structural fashion. J. Biol. Chem. 277, 14859-14868
55. Corteling, R., and Trifilieff, A. (2004) Gender comparison in a murine model of allergen-driven airway inflammation and the response to budesonide treatment. BMC Pharmacol. 4, 4
56. Okuyama, K., Wada, K., Chihara, J., Takayanagi, M., and Ohno, I. (2008) Sex-related splenocyte function in a murine model of allergic asthma. Clin. Exp. Allergy 38, 1212-1219
57. Carey, M. A., Card, J. W., Voltz, J. W., Arbes, S. J., Jr., Germolec, D. R., Korach, K. S., and Zeldin, D. C. (2007) It's all about sex: gender, lung development and lung disease. Trends Endocrinol. Metab. 18, 308-313
58. Monteseirin, J. (2009) Neutrophils and asthma. J. Investig. Allergol. Clin. Immunol. 19, 340-354
59. Alphonse, M. P., Saffar, A. S., Shan, L., HayGlass, K. T., Simons, F. E., and Gounni, A. S. (2008) Regulation of the high affinity IgE receptor (Fc epsilonRI) in human neutrophils: role of seasonal allergen exposure and Th-2 cytokines. PLoS One 3, e1921
60. Saffar, A. S., Alphonse, M. P., Shan, L., Hayglass, K. T., Simons, F. E., and Gounni, A. S. (2007) IgE modulates neutrophil survival in asthma: role of mitochondrial pathway. J. Immunol. 178, 2535-2541
61. Molloy, E. J., O'Neill, A. J., Grantham, J. J., Sheridan-Pereira, M., Fitzpatrick, J. M., Webb, D. W., and Watson, R. W. (2003) Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood 102, 2653-2659
62. Marin, D. P., Bolin, A. P., de Cassia Macedo dos Santos, R., Curi, R., and Otton, R. (2010) Testosterone suppresses oxidative stress in human neutrophils. Cell Biochem. Funct. 28, 394-402
63. Driscoll, M. D., Sathya, G., Muyan, M., Klinge, C. M., Hilf, R., and Bambara, R. A. (1998) Sequence requirements for estrogen receptor binding to estrogen response elements. J. Biol. Chem. 273, 29321-29330
64. Mason, C. E., Shu, F. J., Wang, C., Session, R. M., Kallen, R. G., Sidell, N., Yu, T., Liu, M. H., Cheung, E., and Kallen, C. B. (2010) Location analysis for the estrogen receptor-alpha reveals binding to diverse ERE sequences and widespread binding within repetitive DNA elements. Nucleic Acids Res. 38, 2355-2368
65. Roemgens, A., Singh, S., Beyer, C., and Arnold, S. (2011) Inducers of chemical hypoxia act in a gender- and brain region-specific manner on primary astrocyte viability and cytochrome c oxidase. Neurotox. Res. 20, 1-14
66. Stirone, C., Duckles, S. P., Krause, D. N., and Procaccio, V. (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol. Pharmacol. 68, 959-965
67. Shteyer, E., Saada, A., Shaag, A., Al-Hijawi, F. A., Kidess, R., Revel-Vilk, S., and Elpeleg, O. (2009) Exocrine pancreatic insufficiency, dyserythropoeitic anemia, and calvarial hyperostosis are caused by a mutation in the COX4I2 gene. Am. J. Hum. Genet. 84, 412-417