Ontogenetic, gravity-dependent development of rat soleus muscle.

We tested the hypothesis that rat soleus muscle fiber growth and changes in myosin phenotype during the postnatal, preweaning period would be largely independent of weight bearing. The hindlimbs of one group of pups were unloaded intermittently from postnatal day 4 to day 21: the pups were isolated from the dam for 5 h during unloading and returned for nursing for 1 h. Control pups were either maintained with the dam as normal or put on an alternating feeding schedule as described above. The enlargement of mass (approximately 3 times), increase in myonuclear number (approximately 1.6 times) and myonuclear domain (approximately 2.6 times), and transformation toward a slow fiber phenotype (from 56 to 70% fibers expressing type I myosin heavy chain) observed in controls were inhibited by hindlimb unloading. These properties were normalized to control levels or higher within 1 mo of reambulation beginning immediately after the unloading period. Therefore, chronic unloading essentially stopped the ontogenetic developmental processes of 1) net increase in DNA available for transcription, 2) increase in amount of cytoplasm sustained by that DNA pool, and 3) normal transition of myosin isoforms that occur in some fibers from birth to weaning. It is concluded that normal ontogenetic development of a postural muscle is highly dependent on the gravitational environment even during the early postnatal period, when full weight-bearing activity is not routine.

[1]  G. Adams,et al.  Time course of myosin heavy chain transitions in neonatal rats: importance of innervation and thyroid state. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[2]  V R Edgerton,et al.  Modulation of myonuclear number in functionally overloaded and exercised rat plantaris fibers. , 1999, Journal of applied physiology.

[3]  V. Edgerton,et al.  Modulation of MHC isoforms in functionally overloaded and exercised rat plantaris fibers. , 1997, Journal of applied physiology.

[4]  F. Plum Handbook of Physiology. , 1960 .

[5]  J. Wilber,et al.  The effect of caloric deprivation upon thyroid function in the neonatal rat. , 1974, Endocrinology.

[6]  Marc Jamon,et al.  Role of gravity in the development of posture and locomotion in the neonatal rat , 1998, Brain Research Reviews.

[7]  D A Riley,et al.  Effects of hindlimb unloading on neuromuscular development of neonatal rats. , 2000, Brain research. Developmental brain research.

[8]  R E Grindeland,et al.  Growth hormone/IGF-I and/or resistive exercise maintains myonuclear number in hindlimb unweighted muscles. , 1997, Journal of applied physiology.

[9]  F. Haddad,et al.  Effects of spaceflight and thyroid deficiency on rat hindlimb development. II. Expression of MHC isoforms. , 2000, Journal of applied physiology.

[10]  G. Butler-Browne,et al.  Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. , 1984, Developmental biology.

[11]  V R Edgerton,et al.  Regulation of skeletal muscle fiber size, shape and function. , 1991, Journal of biomechanics.

[12]  D B Cheek,et al.  The control of cell mass and replication. The DNA unit--a personal 20-year study. , 1985, Early human development.

[13]  R E Grindeland,et al.  Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. , 1997, The American journal of physiology.

[14]  E. Schultz,et al.  Acute effects of hindlimb unweighting on satellite cells of growing skeletal muscle. , 1994, Journal of applied physiology.

[15]  Kerry Walton,et al.  Postnatal development under conditions of simulated weightlessness and space flight , 1998, Brain Research Reviews.

[16]  J. Altman,et al.  Postnatal development of locomotion in the laboratory rat , 1975, Animal Behaviour.

[17]  K M Baldwin,et al.  Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. , 1994, Journal of applied physiology.

[18]  R. Curless,et al.  Developmental patterns of rat muscle histochemistry. , 1976, Journal of embryology and experimental morphology.

[19]  H. Miyata,et al.  Myosin heavy chain isoform transition in ageing fast and slow muscles of the rat. , 1992, Acta physiologica Scandinavica.

[20]  G. Dormans,et al.  Measurement of piezoelectric coefficients of ferroelectric thin films , 1994 .

[21]  G. Diffee,et al.  Control of myosin heavy chain expression: interaction of hypothyroidism and hindlimb suspension. , 1991, The American journal of physiology.

[22]  V R Edgerton,et al.  Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. , 1992, Journal of applied physiology.

[23]  V R Edgerton,et al.  Myonuclear number and myosin heavy chain expression in rat soleus single muscle fibers after spaceflight. , 1996, Journal of applied physiology.

[24]  K Walton,et al.  Changes in gravity influence rat postnatal motor system development: from simulation to space flight. , 1997, Gravitational and space biology bulletin : publication of the American Society for Gravitational and Space Biology.

[25]  E Schultz,et al.  Unloading of juvenile muscle results in a reduced muscle size 9 wk after reloading. , 2000, Journal of applied physiology.

[26]  E. Ralston,et al.  Nuclear domains in muscle cells , 1989, Cell.

[27]  S. Grillner Control of Locomotion in Bipeds, Tetrapods, and Fish , 1981 .

[28]  V. Edgerton,et al.  Myonuclear domains in muscle adaptation and disease , 1999, Muscle & nerve.

[29]  V R Edgerton,et al.  Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. , 1995, Journal of applied physiology.

[30]  R. Llinás,et al.  Identification of a critical period for motor development in neonatal rats , 1992, Neuroscience.

[31]  E. Schultz,et al.  Hindlimb suspension suppresses muscle growth and satellite cell proliferation. , 1989, Journal of applied physiology.

[32]  M. Taussig The Nervous System , 1991 .