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FULLTEXT01.Pdf Umeå University Medical Dissertations Department of Integrative Medical Biology, Section for Anatomy, Umeå University and Centre for Musculoskeletal Research, Gävle University, Umeå, Sweden HUMAN MUSCLE SPINDLES Complex morphology and structural organisation Jing-Xia Liu Umeå 2004 Copyright © by Jing-Xia Liu, 2004 ISSN 0346-6612 ISBN 91-7305-762-2 Printed by VMC, KBC, Umeå University, Umeå 2004 2 In memory of my father 3 TABLE OF CONTENTS ABBREVIATIONS 5 ABSTRACT 6 ORIGINAL PAPERS 7 INTRODUCTION 9 The Muscle Spindle 9 Skeletal muscle structure and sarcomeric proteins 13 Sarcoplasmic reticulum and SERCA isoforms 16 Aging 17 AIMS OF THE STUDY 20 MATERIAL AND METHODS 21 Muscle specimens 21 Tissue processing 21 Antibodies and labeling 21 Biochemistry 22 Enzymehistochemistry and immunocytochemistry 23 Statistical analyses 23 RESULTS 24 Intrafusal fiber composition 24 Complex muscle spindles 25 mATPase activity 26 MyHC composition of isolated muscle spindles 26 MyHC composition of intrafusal fibers 26 SERCA composition of intrafusal fibers 29 DISCUSSION 30 Human muscle spindle identity: BB versus DN 30 MyHC composition of isolated muscle spindles 31 MyHC composition of intrafusal fibers 32 Effects of aging on muscle spindles 33 SERCA isoforms 34 Future perspectives 35 SUMMARY 36 CONCLUSIONS 37 ACKNOWLEDGEMENTS 38 REFERENCES 41 PAPER I PAPER II PAPER III PAPER IV 4 ABBREVIATIONS ALD Anterior latissimus dorsi BB Biceps brachii CSA Cross-sectional area DN Deep muscles of the neck EDTA Ethylene diamine tetra-acetic acid mAb Monoclonal antibody mATPase Myosin adenosine triphosphatase MyHC Myosin heavy chain MyLC Myosin light chain MyHCα-c α-cardiac MyHC MyHCemb Embryonic MyHC MyHCfet Fetal MyHC MyHCeom Extraocular MyHC MyHCm Masticatory MyHC MyHCsto Slow tonic MyHC NT-3 Neurotrophin-3 PAP Peroxidase-antiperoxidase PBS Phosphate buffer saline SERCA Sarco/endoplasmic reticulum ATPase SERCA1 SERCA fast isoform SERCA2 SERCA slow isoform SDS-PAGE Sodium dodecyl sulfate polyacrylamide gel electrophoresis SR Sarcoplasmic reticulum 5 ABSTRACT Muscle spindles are skeletal muscle mechanoreceptors that mediate the stretch reflex and provide axial and limb position information to the central nervous system. They have been proposed to play a major role in the pathophysiology of muscle pain. Knowledge about the normal human muscle spindles is needed in order to understand their role in muscle disease or dysfunction. The aim of this study was to investigate the fiber content and MyHC composition of the muscle spindles in the human biceps brachii (BB) and deep muscles of the neck (DN); to determine whether there are age-related changes in human muscle spindles with respect to structure and MyHC composition; to investigate the distribution of SERCA isoforms and to evaluate whether there is a coordinated expression of SERCA and MyHC isoforms in intrafusal fibers. The myosin heavy chain (MyHC) content correlates to contraction velocity and force and the sarcoplasmic reticulum Ca2+ ATPase (SERCA) is a major determinant of muscle fiber relaxation velocity. Muscle specimens obtained from young and old subjects were serially sectioned and the pattern of distribution of different proteins along the length of the intrafusal fibers was revealed by immunocytochemistry. The MyHC content of single muscle spindles was assessed with SDS-PAGE and immunoblots. There were clear differences between BB and DN with regard to the morphology and MyHC composition of muscle spindles. Virtually each muscle spindle in the BB, but not in the DN, had a unique allotment of numbers of bag1, bag2 and chain fibers. In DN, a number of muscle spindles lacked either bag1 or bag2 fibers. Four major MyHC isoforms (MyHCI, IIa, α-cardiac and intrafusal) were detected by SDS-PAGE. In both BB and DN, immunocytochemistry revealed co-expression of several MyHC isoforms in each intrafusal fiber and regional heterogeneity. Both nuclear bag1 and bag2 fibers contained slow tonic MyHC uniformly and MyHCI, α-cardiac, embryonic and fetal with regional variations. Nuclear chain fibers contained MyHCIIa, embryonic and fetal and in the BB also MyHCIIx. The total number of intrafusal fibers per spindle decreased significantly with aging, due to a significant reduction in the number of nuclear chain fibers. The patterns of MyHC expression were also affected by aging. The bag1 fibers predominantly contained both SERCA isoforms in the encapsulated region. The bag2 fibers were more heterogeneous in their SERCA composition and 16-27% of them lacked both isoforms. Chain fibers contained SERCA1. There was a poor correlation between the MyHC and SERCA isoforms in nuclear bag fibers, whereas a strong correlation existed between MyHCIIa and SERCA1 in the nuclear chain fibers. Human muscle spindles, each being unique, proved to be more complex than anticipated. The clear differences shown between the BB and DN muscle spindles suggest functional specialization in the control of movement among different human muscles. Aging apparently had profound effects on intrafusal fiber content and MyHC composition. The age-related changes in muscle spindle phenotype may reflect deterioration in sensory and motor innervation and are likely to have a detrimental impact on motor control in the elderly. Key words: human, muscle spindle, intrafusal fiber, aging, biceps brachii, deep muscles of the neck, MyHC, mATPase, SERCA. 6 ORIGINAL PAPERS This thesis is based on the following papers, which are referred to in the text by their Roman numerals: I. Liu J-X, Eriksson P-O, Thornell L-E, Pedrosa-Domellöf F. Myosin heavy chain composition of muscle spindles in human biceps brachii. J Histochem Cytochem 50: 171-84, 2002. II. Liu J-X, Thornell L-E, Pedrosa-Domellöf F. Muscle spindles in the deep muscles of the human neck. A morphological and immunocytochemical study. J Histochem Cytochem 51: 175-86, 2003. III. Liu J-X, Eriksson P-O, Thornell L-E, Pedrosa-Domellöf F. Fiber content and myosin heavy chain composition of muscle spindles in aged human biceps brachii. J Histochem Cytochem 52: 2004. IV. Liu J-X, Thornell L-E, Pedrosa-Domellöf F. Distribution of SERCA isoforms in human intrafusal fibers. Histochem Cell Biol 120: 299-306, 2003. 7 8 INTRODUCTION The Muscle Spindle Muscle spindles, proprioceptive organs in skeletal muscles, were first described in the middle of the nineteenth century (Kühnne, 1863; Weismann, 1861) and our understanding of their functional role has increased markedly over the last 40 years. Muscle spindles have been postulated to be of importance for the control of movement and posture in mammals (Matthews, 1981). This has recently been firmly verified in neurotrophin-3-deficient mice which were unable to support their weight and had an abnormal posture due to the absent proprioceptive afferents and muscle spindles in their limbs (Ernfors et al., 1994; Walro and Kucera, 1999). Muscle spindles have also been proposed to play a central role in regulating muscle tone and in the pathophysiology of work-related chronic muscle disorders (Johansson et al., 1999; Johansson and Sojka, 1991; Matre et al., 1998; Thornell et al., 2003a). Previous human studies have demonstrated that muscles rich in spindles including the small muscles of the neck are particularly associated with chronic muscle pain (Johansson and Sojka, 1991). In order to understand the possible roles of muscle spindles in pathological conditions, basic knowledge of their structure and composition is essential. In particular, it is important to elucidate the molecular basis of the particular muscle spindle phenotype. Figure 1. Muscle spindle and its innervation Muscle spindles are located within muscles and run in parallel with the extrafusal fibers. Muscle spindles consist of a bundle of small-diameter muscle fibers which are surrounded by a multi-layered spindle shaped capsule derived from the perineurium. These muscle 9 fibers are therefore referred to as intrafusal fibers (for review see Barker and Banks, 1994). Two types of intrafusal fibers are distinguished according to their size and the arrangement of their central nuclei. The larger, often longer fibers displaying a wide equatorial accumulation of nuclei are called nuclear bag fibers whereas the smaller, usually shorter fibers containing a central row of nuclei are called nuclear chain fibers. Three types of intrafusal fibers, namely nuclear bag1 (dynamic bag1), nuclear bag2 (static bag2) and nuclear chain (static chain) fibers, have been identified on the basis of both their mATPase activities (Ovalle and Smith, 1972) and their physiological properties (Barker and Banks, 1994; Boyd, 1962; Matthews, 1981). Three regions have been distinguished in a given muscle spindle (Figure 1). They are defined as follows: the A region, including the equator (EQ) and the juxtaequatorial parts (Aj), containing the periaxial fluid space; the B region, extending from the end of the periaxial fluid space to the end of the capsule, and the extracapsular C region (Barker and Banks 1994). Each region can be further subdivided into an inner (proximal to the equator) and outer (distal to the equator) portion. Muscle spindles are sensory mechanoreceptors that relay information about muscle length and changes in muscle length to the central nervous system (Barker and Banks, 1994; Matthews, 1981). Intrafusal fibers receive both sensory and motor innervation (Figure 1). One single primary afferent (Ia) commonly innervates all intrafusal fibers in the spindle. In addition, one or more secondary afferent nerve fibers (II) may
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