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Human muscle spindles: complex morphology and structural organisation
Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Anatomy.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

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.

Place, publisher, year, edition, pages
2004. , 49 p.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 928
Keyword [en]
human, muscle spindle, intrafusal fiber, aging, biceps brachii, deep muscles of the neck, MyHC, mATPase, SERCA
Research subject
Human Anatomy
Identifiers
URN: urn:nbn:se:umu:diva-356ISBN: 91-7305-762-2 (print)OAI: oai:DiVA.org:umu-356DiVA: diva2:143218
Public defence
2004-11-25, Stora föreläsningssalen, Biologihuset, Umeå universitet, Umeå, 09:00 (English)
Opponent
Available from: 2004-11-09 Created: 2004-11-09 Last updated: 2010-08-05Bibliographically approved
List of papers
1. Myosin heavy chain composition of muscle spindles in human biceps brachii
Open this publication in new window or tab >>Myosin heavy chain composition of muscle spindles in human biceps brachii
2002 (English)In: Histochem Cell Biol, Vol. 50, no 2, 171-184 p.Article in journal (Refereed) Published
Abstract [en]

Data on the myosin heavy chain (MyHC) composition of human muscle spindles are scarce in spite of the well-known correlation between MyHC composition and functional properties of skeletal muscle fibers. The MyHC composition of intrafusal fibers from 36 spindles of human biceps brachii muscle was studied in detail by immunocytochemistry with a large battery of antibodies. The MyHC content of isolated muscle spindles was assessed with SDS-PAGE and immunoblots. Four major MyHC isoforms (MyHCI, IIa, embryonic, and intrafusal) were detected with SDS-PAGE. Immunocytochemistry revealed very complex staining patterns for each intrafusal fiber type. The bag(1) fibers contained slow tonic MyHC along their entire fiber length and MyHCI, alpha-cardiac, embryonic, and fetal isoforms along a variable part of their length. The bag(2) fibers contained MyHC slow tonic, I, alpha-cardiac, embryonic, and fetal isoforms with regional variations. Chain fibers contained MyHCIIa, embryonic, and fetal isoforms throughout the fiber, and MyHCIIx at least in the juxtaequatorial region. Virtually each muscle spindle had a different allotment of numbers of bag(1), bag(2) and chain fibers. Taken together, the complexity in intrafusal fiber content and MyHC composition observed indicate that each muscle spindle in the human biceps has a unique identity.

Keyword
human biceps brachii, muscle spindles, intrafusal fiber, bag1 fiber, bag 2 fiber, chain fiber, MyHC
National Category
Medical and Health Sciences Ophthalmology Cell and Molecular Biology
Research subject
Human Anatomy; Ophtalmology
Identifiers
urn:nbn:se:umu:diva-4212 (URN)11799136 (PubMedID)744 (Local ID)744 (Archive number)744 (OAI)
Available from: 2004-11-09 Created: 2004-11-09 Last updated: 2013-04-27
2. Muscle spindles in the deep muscles of the human neck: a morphological and immunocytochemical study
Open this publication in new window or tab >>Muscle spindles in the deep muscles of the human neck: a morphological and immunocytochemical study
2003 (English)In: Journal of Histochemistry and Cytochemistry, ISSN 0022-1554, E-ISSN 1551-5044, Vol. 51, no 2, 175-186 p.Article in journal (Refereed) Published
Abstract [en]

Muscle spindle density is extremely high in the deep muscles of the human neck. However, there is a paucity of information regarding the morphology and immunoreactivity of these muscle spindles. The objective of this study was to investigate the intrafusal fiber content and to assess the myosin heavy chain (MyHC) composition of muscle spindles from human deep neck muscles. In addition to the conventional spindles containing bag(1), bag(2), and chain fibers (b(1)b(2)c spindle), we observed a number of spindles lacking bag(1) (b(2)c spindle) or bag(2) (b(1)c spindle) fibers. Both bag(1) and bag(2) fibers contained slow tonic MyHCs along their entire fiber length and MyHCI, MyHCIIa, embryonic, and alpha-cardiac MyHC isoforms along a variable length of the fibers. Fetal MyHC was present in bag(2) fibers but not in bag(1) fibers. Nuclear chain fibers contained MyHCIIa, embryonic, and fetal isoforms with regional variations. We also compared the present data with our previous results obtained from muscle spindles in human biceps brachii and the first lumbrical muscles. The allotment of numbers of intrafusal fibers and the MyHC composition showed some muscle-related differences, suggesting functional specialization in the control of movement among different human muscles.

Place, publisher, year, edition, pages
Sage Publications, 2003
Keyword
human, muscle spindle, deep neck muscles, mATPase, MyHC, intrafusal fibers
National Category
Medical and Health Sciences Ophthalmology Cell and Molecular Biology
Research subject
Human Anatomy; Ophtalmology
Identifiers
urn:nbn:se:umu:diva-4213 (URN)10.1177/002215540305100206 (DOI)12533526 (PubMedID)
Available from: 2004-11-09 Created: 2004-11-09 Last updated: 2017-12-14Bibliographically approved
3. Fiber content and myosin heavy chain composition of muscle spindles in aged human biceps brachii
Open this publication in new window or tab >>Fiber content and myosin heavy chain composition of muscle spindles in aged human biceps brachii
2005 (English)In: Journal of Histochemistry and Cytochemistry, ISSN 0022-1554, E-ISSN 1551-5044, Vol. 53, no 4, 445-454 p.Article in journal (Refereed) Published
Abstract [en]

The present study investigated potential age-related changes in human muscle spindles with respect to the intrafusal fiber-type content and myosin heavy chain (MyHC) composition in biceps brachii muscle. The total number of intrafusal fibers per spindle decreased significantly with aging, due to a significant reduction in the number of nuclear chain fibers. Nuclear chain fibers in old spindles were short and some showed novel expression of MyHC alpha-cardiac. The expression of MyHC alpha-cardiac in bag1 and bag2 fibers was greatly decreased in the A region. The expression of slow MyHC was increased in nuclear bag1 fibers and that of fetal MyHC decreased in bag2 fibers whereas the patterns of distribution of the remaining MyHC isoforms were generally not affected by aging. We conclude that aging appears to have an important impact on muscle spindle composition. These changes in muscle spindle phenotype may reflect an age-related deterioration in sensory and motor innervation and are likely to have an impact in motor control in the elderly.

Place, publisher, year, edition, pages
Baltimore: Williams & Wilkins Co., 2005
Keyword
Adolescent, Adult, Aged, Aged; 80 and over, Aging, Female, Histocytochemistry, Humans, Male, Middle Aged, Muscle Fibers/*ultrastructure, Muscle Spindles/*chemistry/metabolism/*ultrastructure, Muscle; Skeletal/chemistry/metabolism/*ultrastructure, Myosin Heavy Chains/biosynthesis/*chemistry, Protein Isoforms/biosynthesis/chemistry
National Category
Ophthalmology Cell and Molecular Biology
Research subject
Human Anatomy; Ophtalmology
Identifiers
urn:nbn:se:umu:diva-12681 (URN)doi:10.1369/jhc.4A6257.2005 (DOI)15805419 (PubMedID)
Available from: 2008-01-31 Created: 2008-01-31 Last updated: 2017-12-14Bibliographically approved
4. Distribution of SERCA isoforms in human intrafusal fibers
Open this publication in new window or tab >>Distribution of SERCA isoforms in human intrafusal fibers
2003 (English)In: Histochemistry and Cell Biology, ISSN 0948-6143, E-ISSN 1432-119X, Vol. 120, no 4, 299-306 p.Article in journal (Refereed) Published
Abstract [en]

The sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) is a membrane protein that plays a crucial role in muscle relaxation by transporting cytosolic Ca2+ into the lumen of the sarco/endoplasmic reticulum. In this study, the presence of SERCA1 and SERCA2 was investigated in human intrafusal fibers by immunocytochemistry. Nuclear bag1 fibers contained both SERCA1 and SERCA2 isoforms, with predominant staining seen with SERCA2 in the A and B regions. Most nuclear bag2 fibers also contained SERCA1 and SERCA2 isoforms and their coexistence frequently occurred in the A region. SERCA1 was present whereas SERCA2 was generally absent in the nuclear chain fibers. The staining intensity seen with the SERCA1 monoclonal antibody varied in the order of chain>bag1>bag2. The expression of SERCA1 isoform was found to correlate with the presence of fast myosin heavy chain (MyHC) isoform in nuclear chain fibers, whereas for nuclear bag fibers there was no such apparent correlation between patterns of expression of SERCA and MyHC isoforms. The phenotype revealed for the human bag fibers was very sophisticated and adapted to attain a very wide range of contraction and relaxation velocities.

Place, publisher, year, edition, pages
Springer, 2003
Keyword
Human, Muscle spindle, Intrafusal fibers, SERCA, MyHC
National Category
Ophthalmology Cell and Molecular Biology
Research subject
Human Anatomy; Ophtalmology
Identifiers
urn:nbn:se:umu:diva-4215 (URN)10.1007/s00418-003-0569-5 (DOI)14574585 (PubMedID)744 (Local ID)744 (Archive number)744 (OAI)
Available from: 2004-11-09 Created: 2004-11-09 Last updated: 2017-12-14Bibliographically approved

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