Bioenergetic characteristics of the costal and crural diaphragm in mammals

https://doi.org/10.1016/S0034-5687(97)00051-0Get rights and content

Abstract

These experiments compared oxidative and glycolytic enzyme activity in the costal and crural diaphragm in seven adult mammals (mouse, rat, rabbit, ferret, sheep, pig, cow) ranging in body mass from approximately 0.03 to 422 kg. Segments of the costal and crural diaphragm from the aforementioned species were homogenized to determine the activities of the glycolytic enzyme, lactate dehydrogenase (LDH), and the Krebs cycle enzyme, citrate synthase (CS). The results indicated that metabolic differences between the costal and crural diaphragm do not exist in all mammalian species. Specifically, CS activity differed (P<0.05) between the costal and crural diaphragm (costal approximately 36% greater than crural) in only two species (rat and rabbit). Further, the oxidative capacity of the costal and crural diaphragm was significantly correlated with both breathing frequency and resting metabolic rate (r=0.92–0.57; P<0.05) across the species investigated. In contrast, glycolytic capacity was not significantly correlated (P>0.05) with either breathing frequency or resting metabolic rate.

Introduction

The diaphragm is the principal muscle of inspiration and is considered the most important ventilatory muscle in mammals (Sieck, 1988, DeTroyer et al., 1982). The diaphragm has been classically considered one muscle with a single functional entity. However, recent reports have provided new insights into diaphragmatic structure and function. The diaphragm is now thought to function as two muscles that act differently on the rib cage. For example, DeTroyer et al. (1981), DeTroyer et al. (1982)separately stimulated the costal and crural parts of the diaphragm in anesthetized dogs; the results indicated that the costal and crural parts of the diaphragm have a different mechanical action on the rib cage. Stimulation of the costal diaphragm increased the dimensions of the lower rib cage, whereas stimulation of the crural diaphragm had no effect on the lower rib cage dimensions. In contrast to the costal region, the crural diaphragm has no attachments to the rib cage, and thus may only act on the rib cage by means of changes in pleural or abdominal pressure (DeTroyer et al., 1981, DeTroyer and Estenne, 1988).

In addition to functional differences between the costal and crural diaphragm, recent evidence from our laboratory (Powers et al., 1990b) and work by Sugiura et al. (1992)have demonstrated that metabolic differences exist between these two diaphragmatic regions in the rat. Specifically, the oxidative capacity of the costal diaphragm is significantly higher than the crural diaphragm (Powers et al., 1990b, Sugiura et al., 1992). Also, we have shown that similar costal vs. crural metabolic differences exist in the dog (Powers et al., 1994b). However, at present, it is unknown if these same metabolic differences exist between the costal and crural diaphragm in other mammalian species. Therefore, the purpose of this study was to compare oxidative and glycolytic enzyme activities in seven different mammalian species (mouse, rat, rabbit, ferret, sheep, pig and cow) ranging in body mass from approximately 0.03 to 422 kg. Based upon our previous findings in the rat and dog, we tested the hypothesis that costal vs. crural bioenergetic (i.e. oxidative capacity) differences would exist in these non-primate mammals.

Section snippets

Animals

Sections of the costal and crural diaphragm muscle from seven different adult mammalian species were used for biochemical analyses in this investigation. The mean (±SD) body mass of the species investigated were as follows: Holstein dairy cow (n=8), 420.94±18.34 kg; pigs (n=8), 115±4.47 kg; Hampshire and Suffolk sheep (n=8), 56.9±1.70 kg; New Zealand White rabbits (n=4), 3.45±0.451 kg; ferrets (n=8), 1.41±0.188 kg; Sprague–Dawley rats (n=7), 0.298±0.013 kg; DBA/C57 mice (n=10), 0.032±0.004 kg.

Removal of tissue

Enzyme activities in costal and crural diaphragm

Table 1 contains the mean (±SEM) costal and crural diaphragm LDH and CS enzyme activities across species. Costal vs. crural CS activity differed (P<0.05) in only two species (i.e. rat and rabbit). Also, note that CS activity in both the costal and crural diaphragm was significantly higher in the smaller animals (e.g. mouse, rat, ferret) compared to all animals of larger mass (rabbit, sheep, pig, cow).

Regional diaphragmatic differences in LDH activity existed in two species: LDH activity was

Overview of principal findings

To our knowledge, this is the first study to examine the bioenergetic enzyme activities in both the costal and crural diaphragm across a range of mammalian species differing widely in body mass and resting metabolic rates. The principal finding in these experiments was that metabolic differences between the costal and crural diaphragm do not exist in all mammalian species. Further, the data indicate that the oxidative capacity (represented by CS activity) of both the costal and crural diaphragm

Summary and conclusions

These experiments tested the hypothesis that costal vs. crural oxidative capacity differs in many non-primate mammals. The results indicated that the costal and crural diaphragm oxidative capacity did not differ in five of the seven species investigated. Indeed, oxidative capacity differed between the costal diaphragm and crural diaphragm in only the rat and rabbit. Hence, the hypothesis was not supported.

Further, our data indicate that the oxidative capacity of both the costal and crural

References (22)

  • S.K. Powers et al.

    Regional training-induced alterations in diaphragmatic oxidative and antioxidant enzymes

    Respir. Physiol.

    (1994)
  • C. Watters

    A one-step biuret assay for protein in the presence of detergent

    Anal. Biochem.

    (1978)
  • Bergmeyer, H., 1970. Analysis of lactate dehydrogenase. In: Bergmeyer, H. (Ed.), Methods in Enzymatic Analysis. Verlag...
  • S. Blank et al.

    Biochemical characteristics of mammalian diaphragms

    Respir. Physiol.

    (1988)
  • Breazile, J., 1971. Mechanics of respiration and pulmonary ventilation. In: Breazile, J. (Ed.), Textbook of Veterinary...
  • M.L. Crosfill et al.

    Physical characteristics of the chest and lungs and the work of breathing in different mammalian species

    J. Physiol. (London)

    (1961)
  • A. DeTroyer et al.

    The diaphragm—two muscles

    Science

    (1981)
  • A. DeTroyer et al.

    Action of the costal and crural parts of the diaphragm on the rib cage in the dog

    J. Appl. Physiol.

    (1982)
  • DeTroyer, A., Estenne, M., 1988. Functional anatomy of the respiratory muscles. In: Belman, M. (Ed.), Clinics in Chest...
  • M. Grace et al.

    A comparison of maximal bioenergetic enzyme activities obtained with commonly used homogenization techniques

    J. Sports Med. Phys. Fitness

    (1996)
  • Hochachka, P., Somero, G., 1984. Biochemical Adaptation. Princeton University Press, Princeton, NJ, pp....
  • Cited by (12)

    • Diaphragm: A vital respiratory muscle in mammals

      2016, Annals of Anatomy
      Citation Excerpt :

      In dogs and rats, the glycolytic fast contraction fibers are absent, whereas in other mammals, these fibers represent 20–40% of all diaphragm fibers (Faulkner et al., 1979; Rochester, 1985). In laboratory animals, such as the mouse and rat, the proportion of fast fibers in the respiratory muscles is greater than that in human beings or in large mammals, thus reflecting the idea that volume can decrease from small to large animals (Blank et al., 1988; Hodge et al., 1977; Polla et al., 2004). Some muscular diseases result from mutations in the genes encoding sarcolemic, sarcomeric, and cytosolic muscle proteins, which initiate a process of progressive muscular degeneration and, consequently, a progressive loss of motor skills (Bergman et al., 2002).

    View all citing articles on Scopus
    View full text