A genetic reduction in antioxidant function causes elevated aggression in mice

Journal of Experimental Biology

Volumn 218, Issue 2, 2015, Pages 223-227

  Garratt, Michael ^a,b   Brooks, Robert C ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Dominance; Fitness; Life history; Mouse

Indexed keywords

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

AGGRESSION; ANIMAL; C57BL MOUSE; DEFICIENCY; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; PHYSIOLOGY;

AGGRESSION; ANIMALS; ANTIOXIDANTS; DEFICIENCY; MALE; METABOLISM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATIVE STRESS; PHYSIOLOGY; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

ANIMALIA; MUS;

EID: 84964277248     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.112011     Document Type: Article

References (49)

1. Agarwal, A., Saleh, R. A. and Bedaiwy, M. A. (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79, 829-843.
2. Beckman, K. B. and Ames, B. N. (1998). The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
3. Berry, A. and Cirulli, F. (2013). The p66(Shc) gene paves the way for healthspan: evolutionary and mechanistic perspectives. Neurosci. Biobehav. Rev. 37, 790-802.
4. Bize, P., Devevey, G., Monaghan, P., Doligez, B. and Christe, P. (2008). Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89, 2584-2593.
5. Bouayed, J., Rammal, H. and Soulimani, R. (2009). Oxidative stress and anxiety: relationship and cellular pathways. Oxid. Med. Cell. Longev. 2, 63-67.
6. Briffa, M. and Sneddon, L. U. (2007). Physiological constraints on contest behaviour. Funct. Ecol. 21, 627-637.
7. Bronson, F. H. (1979). The reproductive ecology of the house mouse. Q. Rev. Biol. 54, 265-299.
8. Candolin, U. (2000). Increased signalling effort when survival prospects decrease: male-male competition ensures honesty. Anim. Behav. 60, 417-422.
9. Clutton-Brock, T. H. (1984). Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 123, 212-229.
10. Coccaro, E. F., Lee, R. and Gozal, D. (2014). Elevated plasma oxidative stress markers in individuals with intermittent explosive disorder and correlation with aggression in humans. Biol. Psychiatry 71, 158-165.
11. Cramer, M. J. and Cameron, G. N. (2007). Effects of bot fly, Cuterebra fontinella, parasitism on male aggression and female choice in Peromyscus leucopus. Anim. Behav. 74, 1419-1427.
12. deCarvalho, T. N., Watson, P. J. and Field, S. A. (2004). Costs increase as ritualized fighting progresses within and between phases in the sierra dome spider, Neriene litigiosa. Anim. Behav. 68, 473-482.
13. Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
14. Dugatkin, L. A. (1997). Winner and loser effects and the structure of dominance hierarchies. Behav. Ecol. 8, 583-587.
15. Elchuri, S., Oberley, T. D., Qi, W., Eisenstein, R. S., Jackson Roberts, L., Van Remmen, H., Epstein, C. J. and Huang, T. T. (2005). CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24, 367-380.
16. Garratt, M. and Brooks, R. C. (2012). Oxidative stress and condition-dependent sexual signals: more than just seeing red. Proc. Biol. Sci. 279, 3121-3130.
17. Garratt, M., McArdle, F., Stockley, P., Vasilaki, A., Beynon, R. J., Jackson, M. J. and Hurst, J. L. (2012). Tissue-dependent changes in oxidative damage with male reproductive effort in house mice. Funct. Ecol. 26, 423-433.
18. Garratt, M., Bathgate, R., de Graaf, S. P. and Brooks, R. C. (2013). Copper-zinc superoxide dismutase deficiency impairs sperm motility and in vivo fertility. Reproduction 146, 297-304.
19. Garratt, M., Pichaud, N., Glaros, E. N., Kee, A. J. and Brooks, R. C. (2014). Superoxide dismutase deficiency impairs olfactory sexual signaling and alters bioenergetic function in mice. Proc. Natl Acad. Sci. USA 111, 8119-8124.
20. Haller, J. (1995). Biochemical background for an analysis of cost-benefit interrelations in aggression. Neurosci. Biobehav. Rev. 19, 599-604.
21. Halliwell, B. and Gutteridge, J. M. (1999). Free Radicals in Biology and Medicine. Oxford: Oxford University Press.
22. Halliwell, B. and Whiteman, M. (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br. J. Pharmacol. 142, 231-255.
23. Hamilton, R. T., Walsh, M. E. and Van Remmen, H. (2012). Mouse models of oxidative stress indicate a role for modulating healthy aging. J. Clin. Exp. Pathol. 2012 Suppl. 4, 005.
24. Harman, D. (1956). Aging: A theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
25. Ho, Y. S., Gargano, M., Cao, J., Bronson, R. T., Heimler, I. and Hutz, R. J. (1998). Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J. Biol. Chem. 273, 7765-7769.
26. Hovatta, I., Tennant, R. S., Helton, R., Marr, R. A., Singer, O., Redwine, J. M., Ellison, J. A., Schadt, E. E., Verma, I. M., Lockhart, D. J. et al. (2005). Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438, 662-666.
27. Isaksson, C., While, G., McEvoy, J., van de Crommenacker, J., Olsson, M., Groothuis, T., Komdeur, J. and Wapstra, E. (2011). Aggression, but not testosterone, is associated to oxidative status in a free-living vertebrate. Behaviour 148, 713-731.
28. Jones, R. B. and Nowell, N. W. (1974). A comparison of the aversive and female attractant properties of urine from dominant and subordinate male mice. Anim. Learn. Behav. 2, 141-144.
29. Jones, R. B. and Nowell, N. W. (1989). Aversive potency of urine from dominant and subordinate male laboratory mice (Mus musculus): resolution of a conflict. Aggress. Behav. 15, 291-296.
30. König, M., Zimmer, A. M., Steiner, H., Holmes, P. V., Crawley, J. N., Brownstein, M. J. and Zimmer, A. (1996). Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature 383, 535-538.
31. Kostrominova, T. Y., Pasyk, K. A., Van Remmen, H., Richardson, A. G. and Faulkner, J. A. (2007). Adaptive changes in structure of skeletal muscles from adult Sod1 homozygous knockout mice. Cell Tissue Res. 327, 595-605.
32. Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R. and Lebovitz, R. M. (1998). Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139, 4008-4011.
33. McNamara, J. M. and Houston, A. I. (1996). State-dependent life histories. Nature 380, 215-221.
34. Metcalfe, N. B. and Alonso-Alvarez, C. (2010). Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24, 984-996.
35. Monaghan, P., Metcalfe, N. B. and Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92.
36. Muller, F. L., Song, W., Liu, Y., Chaudhuri, A., Pieke-Dahl, S., Strong, R., Huang, T. T., Epstein, C. J., Roberts, L. J., II, Csete, M. et al. (2006). Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of agedependent skeletal muscle atrophy. Free Radic. Biol. Med. 40, 1993-2004.
37. Novotny, M., Harvey, S. and Jemiolo, B. (1990). Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46, 109-113.
38. Nyberg, J. M., Vekovischeva, O. and Sandnabba, N. K. (2003). Anxiety profiles of mice selectively bred for intermale aggression. Behav. Genet. 33, 503-511.
39. Pérez, V. I., Bokov, A., Van Remmen, H., Mele, J., Ran, Q., Ikeno, Y. and Richardson, A. (2009). Is the oxidative stress theory of aging dead? Biochim. Biophys. 1790, 1005-1014.
40. Pölkki, M., Kortet, R., Hedrick, A. and Rantala, M. J. (2013). Dominance is not always an honest signal of male quality, but females may be able to detect the dishonesty. Biol. Lett. 9, 20121002.
41. Rammal, H., Bouayed, J. and Soulimani, R. (2010). A direct relationship between aggressive behavior in the resident/intruder test and cell oxidative status in adult male mice. Eur. J. Pharmacol. 627, 173-176.
42. Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Wilcox, H. M., Flood, D. G., Beal, M. F., Brown, R. H., Jr et al. (1996). Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13, 43-47.
43. Saleh, R. A. and Agarwal, A. (2002). Oxidative stress and male infertility: from research bench to clinical practice. J. Androl. 23, 737-752.
44. Sikka, S. C., Rajasekaran, M. and Hellstrom, W. J. G. (1995). Role of oxidative stress and antioxidants in male infertility. J. Androl. 16, 464-468.
45. Smith, I. P. and Taylor, A. C. (1993). The energetic cost of agonistic behavior in the velvet swimming crab, Necora (= Liocarcinus) puber (L). Anim. Behav. 45, 375-391.
46. Tsunoda, S., Kawano, N., Miyado, K., Kimura, N. and Fujii, J. (2012). Impaired fertilizing ability of superoxide dismutase 1-deficient mouse sperm during in vitro fertilization. Biol. Reprod. 87, 121.
47. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M. and Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84.
48. Vasilaki, A., van der Meulen, J. H., Larkin, L., Harrison, D. C., Pearson, T., Van Remmen, H., Richardson, A., Brooks, S. V., Jackson, M. J. and McArdle, A. (2010). The age-related failure of adaptive responses to contractile activity in skeletal muscle is mimicked in young mice by deletion of Cu,Zn superoxide dismutase. Aging Cell 9, 979-990.
49. Zhang, Y., Ikeno, Y., Bokov, A., Gelfond, J., Jaramillo, C., Zhang, H.-M., Liu, Y., Qi, W., Hubbard, G., Richardson, A. et al. (2013). Dietary restriction attenuates the accelerated aging phenotype of Sod1(-/-) mice. Free Radic. Biol. Med. 60, 300-306.