Purine nucleoside phosphorylase and xanthine oxidase activities in
erythrocytes and plasma from marine, semiaquatic and
terrestrial mammals
Roberto I. López-Cruz
a
, Myrna Barjau Pérez-Milicua
a
, Daniel E. Crocker
b
, Ramón Gaxiola-Robles
a,c
,
Jaime A. Bernal-Vertiz
d
, Alejandro de la Rosa
e
, José P. Vázquez-Medina
f
, Tania Zenteno-Savín
a,
⁎
a
Centro de Investigaciones Biológicas del Noroeste, S.C., Programa de Planeación Ambiental y Conservación, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur,
La Paz, Baja California Sur, C.P. 23096, Mexico
b
Sonoma State University, Department of Biology, 1801 E. Cotati Ave., Rohnert Park, CA 94928, USA
c
Hospital General de Zona No.1. Instituto Mexicano del Seguro Social, La Paz, Baja California Sur, Mexico
d
Cabo Dolphins, Paseo de la Marina 7A, Cabo San Lucas, Baja California Sur, C.P. 23410, Mexico
e
Acuario de Veracruz A.C., Departamento de Mamíferos Acuáticos, Aves y Reptiles, Veracruz, Veracruz, Mexico
f
Institute for Environmental Medicine, Perelman School of Medicine, University of Pennsylvania, 1 John Morgan Building, 3620 Hamilton Walk, Philadelphia, PA 19104, USA
abstract article info
Article history:
Received 7 December 2013
Received in revised form 29 January 2014
Accepted 3 February 2014
Available online 13 February 2014
Keywords:
Hypoxia
Ischemia/reperfusion
Purine nucleoside phosphorylase
Purine salvage
Xanthine oxidase
Purine nucleoside phosphorylase (PNP) and xanthine oxidase (XO) are key enzymes involved in the purine
salvage pathway. PNP metabolizes purine bases to synthetize purine nucleotides whereas XO catalyzes the oxi-
dation of purines to uric acid. In humans, PNP activity is reported to be high in erythrocytes and XO activity to be
low in plasma; however, XO activity increases after ischemic events. XO activity in plasma of northern elephant
seals has been reported during prolonged fasting and rest and voluntary associated apneas. The objective of this
study was to analyze circulating PNP and XO activities in marine mammals adapted to tolerate repeated cycles of
ischemia/reperfusion associated with diving (bottlenose dolphin, northern elephant seal) in comparison with
semiaquatic (river otter) and terrestrial mammals (human, pig). PNP activities in plasma and erythrocytes, as
well as XO activity in plasma, from all species were quantified by spectrophotometry. No clear relationship in
circulating PNP or XO activity could be established between marine, semiaquatic and terrestrial mammals.
Erythrocytes from bottlenose dolphins and humans are highly permeable to nucleosides and glucose,
intraerythrocyte PNP activity may be related to a release of purine nucleotides from the liver. High-energy
costs will probably mean a higher ATP degradation rate in river otters, as compared to northern elephant seals
or dolphins. Lower erythrocyte PNP activity and elevated plasma XO activity in northern elephant seal could
be associated with fasting and/or sleep- and dive-associated apneas.
© 2014 Elsevier Inc. All rights reserved.
1. Introduction
Breath-hold (apnea) diving is part of the natural history of marine
mammals, including whales and seals. Terrestrial mammals, however,
are susceptible to drastic changes in oxygen levels (Noren et al., 2001;
Ramirez et al., 2007; Zenteno-Savín et al., 2012). Among marine
mammals, breath-holding capacity and diving behavior are species
specific. Bottlenose dolphins (Tursiops truncatus) usually dive from 0.2
to 10 min and to depths between 4 and 700 m (Lockyer and Morris,
1987; Klatsky et al., 2007). Northern elephant seals can perform routine
dives to depths of 400 m lasting for 20–25 min (Le Boeuf et al., 1988,
1993, 2000; Stewart and DeLong, 1995; Stewart, 1997; Davis et al.,
2001). Semiaquatic mammals, such as river otters (Lontra longicaudis
annectens), are also capable of breath-hold diving; however, they usual-
ly dive close to the surface and for very short periods of time (4 min;
Yeates et al., 2007). Humans lose consciousness if the brain is deprived
of oxygen during 15–20 s and suffocate if ventilation is interrupted
during 3–4 min (Ramirez et al., 2007).
Breath-hold diving is characterized by reduced blood flow (ische-
mia) and decreased tissue oxygen content (hypoxia). During a dive,
blood flow to the brain and heart in seals may decrease 50 and 90%, re-
spectively, from pre-dive levels; in kidney, liver and intestines, perfusion
appears to decrease completely (Elsner, 1999; Folkow and Blix, 2010).
The response to ischemia/reperfusion and hypoxia/reoxygenation in-
cludes low heart rate (bradycardia), and peripheral vasoconstriction
Comparative Biochemistry and Physiology, Part A 171 (2014) 31–35
⁎ Corresponding author. Tel.: +52 612 123 8502; fax: +52 612 125 3625.
E-mail addresses: rlopez@cibnor.mx (R.I. López-Cruz), mbarjau@cibnor.mx
(M. Barjau Pérez-Milicua), crocker@sonoma.edu (D.E. Crocker), r.gaxiolar@gmail.com
(R. Gaxiola-Robles), jbernal@cabodolphins.com (J.A. Bernal-Vertiz),
alejandro_delarosat@hotmail.com (A. de la Rosa), joseva@mail.med.upenn.edu
(J.P. Vázquez-Medina), tzenteno04@cibnor.mx (T. Zenteno-Savín).
http://dx.doi.org/10.1016/j.cbpa.2014.02.007
1095-6433/© 2014 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
Comparative Biochemistry and Physiology, Part A
journal homepage: www.elsevier.com/locate/cbpa