Oxidative stress in the kidney of reproductive male rats during aging
Paulo V.G. Alabarse
a
, Tiago B. Salomon
a, b
, Tássia M. Medeiros
a, b
, Fernanda S. Hackenhaar
a
,
Artur K. Schüller
b
, Guilherme Ehrenbrink
b
, Mara S. Benfato
a,
⁎
a
Programa de Pós-Graduação em Biologia Celular e Molecular, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
b
Laboratório de Estresse Oxidativo, Departamento de Biofísica, IB, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
abstract article info
Article history:
Received 3 December 2010
Received in revised form 6 April 2011
Accepted 12 May 2011
Available online 17 May 2011
Section Editor: Christiaan Leeuwenburgh
Keywords:
Reproduction
Antioxidant enzymes
Antioxidant compounds
Hormones
Oxidative damage
Reproduction alters the male physiology. We performed a comprehensive examination of oxidative stress in
the kidneys of male rats with (experienced) or without (naïve) reproductive activity during aging. Oxidative
stress was assessed by measuring the activity of catalase, glutathione peroxidase, glutathione S-transferase,
and superoxide dismutase, and by measuring protein carbonylation, lipid peroxidation, nitrite and nitrate
levels, vitamin C levels, and glutathione (total, reduced, and oxidized forms) levels, and metabolism was
accessed by aconitase activity in kidney tissue, as well as testosterone and estradiol levels in serum.
Reproductively active animals exhibited increased testosterone levels and altered metabolism. Aging affects
tissues and organs and contributes to their functional decline. Elderly naïve rats showed high nitrite and
nitrate levels. The experienced rats had less damage in elderly ages, probably because they had higher
antioxidant amount and antioxidant enzyme activities at earlier ages, which would have avoided oxidative
damage seen in naïve group, and because of the metabolism decline. Glutathione increase in naïve elder rats
probably was induced for direct protection against oxidative damage and indirect protection by higher
glutathione peroxidase and glutathione S-transferase activities. Linear regression shows that lipid
peroxidation levels explained vitamin C levels (B standardized value of 0.42), indicating that vitamin C was
properly produced or recruited into kidneys to combat lipid peroxidation. Catalase activity reflected the
protein carbonylation and lipid peroxidation levels (B standardized values of 0.28 and 0.48). These results add
comprehensive data regarding changes in oxidative stress during aging, and suggest an explanation for the
costs of reproduction.
© 2011 Elsevier Inc. All rights reserved.
1. Introduction
Reproduction causes changes in male vertebrates, including
morphological, behavioral, and physiological alterations (Miles et al.,
2007). Reproductive success incurs some metabolic costs, and pre-
vious studies have suggested that reproduction causes oxidative stress
(Alonso-Alvarez et al., 2004, 2007; Arenas-Rios et al., 2007; Harshman
and Zera, 2007; Wang et al., 2001; Wiersma et al., 2004). Oxidative
stress is related to aging (Harman, 1956) and is an important
issue because aging is accompanied by an increased incidence of
renal disease and associated morbidity, which pose a pressing problem
in terms of public health and costs (Dowling and Simmons, 2009).
Most studies concerning reproductive activity and oxidative stress
have been restricted to invertebrates such as Drosophila melanogaster
(Harshman and Zera, 2007; Wang et al., 2001) or Caenorhabditis
elegans (Harshman and Zera, 2007), and few studies have addressed
vertebrates (Alonso-Alvarez et al., 2004; Arenas-Rios et al., 2007;
Costantini, 2008; Wiersma et al., 2004; Dowling and Simmons, 2009).
Studies on vertebrates have typically been limited either to females
(lactation, number of litters, size of litter) (Speakman, 2008), or have
related to male behavior (Hull and Dominguez, 2007). We recently
reported an analysis of brains of reproductive male rats during aging,
which is, to our knowledge, the only study focusing on aging and
oxidative stress in breeding male mammals (Alabarse et al., 2011). In
this study, using controlled conditions for temperature, food access,
and light/dark cycle, we identified changes in rat brain associated
with oxidative stress accompanying reproductive experience.
Reactive oxygen species (ROS), which can be produced by mito-
chondria and peroxisomes, can cause oxidative damage including
protein modification and lipid peroxidation (Abegg et al., 2010; Gobe
and Crane, 2010; Gredilla and Barja, 2005; Guevara et al., 2009;
Herlein et al., 2009; Razmara et al., 2007). Inhibition of ROS
production may protect cells from dysfunction and may prevent cell
death. This has been important in kidney research where studies on
antioxidants are focused on developing therapeutic strategies to
prevent renal cell oxidative damage (Gobe and Crane, 2010;
Jankauskas et al., 2010). Among these are studies of metal-induced
renal alterations related to oxidative stress produced by exposure to
cadmium, lead, selenium, iron, and zinc (Gobe and Crane, 2010;
Experimental Gerontology 46 (2011) 773–780
⁎ Corresponding author at: Departamento de Biofísica, IB, Universidade Federal do
Rio Grande do Sul, Av. Bento Gonçalves 9500 prédio 43431, Porto Alegre, RS, 91501-970
Brazil. Tel.: +55 51 33087603; fax: +55 51 33087003.
E-mail address: mara.benfato@ufrgs.br (M.S. Benfato).
0531-5565/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.exger.2011.05.006
Contents lists available at ScienceDirect
Experimental Gerontology
journal homepage: www.elsevier.com/locate/expgero