Cellular terrain surrounding sympathetic nerve pathways in the rat orbit: Comparisons of orbital connective tissue and smooth muscle cell phenotypes

Sympathetic axons are abundant within some orbital tissues but are absent from others. This study investigated cellular phenotypes of tissues containing sympathetic nerves en passage and compared these with phenotypes in regions devoid of sympathetic nerves and with smooth muscle targets. Two primary orbital smooth muscle targets, the tarsal muscle and orbital muscle, contained many synaptophysin‐immunoreactive nerves. Target cells had ultrastructural features typical of smooth muscle and were immunoreactive for α‐smooth muscle actin, smooth muscle myosin heavy chain, desmin, vinculin, and laminin, but not non–muscle myosin, vimentin, fibronectin, or type IV collagen; nerve growth factor (NGF) mRNA was detected by reverse transcription–polymerase chain reaction. Periorbital sheath devoid of sympathetic nerves contained elongated fibroblasts that were immunoreactive for vimentin, non–muscle myosin, and fibronectin, but not for α‐smooth muscle actin, smooth muscle myosin heavy chain, vinculin, desmin, laminin, or type IV collagen, and did not express NGF mRNA. Regions of periorbital sheath containing sympathetic nerves had few synaptophysin‐immunoreactive varicosities. Cells in this region contained myofilaments, ribosomes, and rough endoplasmic reticulum and were larger than tarsal muscle cells. They expressed NGF mRNA and showed a unique immunophenotype, reacting for vimentin, α‐smooth muscle actin and myosin heavy chain, desmin, vinculin, laminin, and type IV collagen. This phenotype reflects both fibroblast and smooth muscle features similar to myofibroblasts or transdifferentiated smooth muscle described in other tissues. The spatial association between these cells and sympathetic nerves suggests that they may be involved in axon guidance or maintenance. J. Comp. Neurol. 400:529–543, 1998. © 1998 Wiley‐Liss, Inc.

[1]  F. Marzban,et al.  Parasympathetic varicosity proliferation and synaptogenesis in rat eyelid smooth muscle after sympathectomy , 1998, Brain Research.

[2]  J. Hiebert,et al.  Decreased receptivity of pathway connective tissue to sympathetic nerve ingrowth in the developing rat. , 1997, Brain research. Developmental brain research.

[3]  T. Cowen,et al.  Extracellular matrix molecules influence innervation density in rat cerebral blood vessels , 1996, Brain Research.

[4]  T. Sano,et al.  Myofibroblastic tumor of soft tissue displaying desmin‐positive and actin‐negative immunophenotypes , 1996, Pathology international.

[5]  S. Chacko,et al.  Identification of two types of smooth muscle cells from rabbit urinary bladder. , 1996, Tissue & cell.

[6]  T. T. Dinh,et al.  Myofibroblasts differentiate from fibroblasts when plated at low density. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Q. Fan,et al.  Sympathetic nerve trajectories to rat orbital targets: Role of connective tissue pathways , 1996, The Journal of comparative neurology.

[8]  B. Mayer,et al.  Innervation of myofibroblast-like scleral spur cells in human monkey eyes. , 1995, Investigative ophthalmology & visual science.

[9]  A. Desmoulière,et al.  Factors influencing myofibroblast differentiation during wound healing and fibrosis. , 1995, Cell biology international.

[10]  A. Wein,et al.  Contractility and phenotype transitions in serosal thickening of obstructed rabbit bladder. , 1995, Journal of applied physiology.

[11]  M. Bissell,et al.  The origin of the myofibroblasts in breast cancer. Recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. , 1995, The Journal of clinical investigation.

[12]  K. Albers,et al.  Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons , 1994, The Journal of comparative neurology.

[13]  K. Ligon,et al.  Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. , 1994, Circulation research.

[14]  T. Skalak,et al.  Immunohistochemical identification of arteriolar development using markers of smooth muscle differentiation. Evidence that capillary arterialization proceeds from terminal arterioles. , 1994, Circulation research.

[15]  I. Fristad,et al.  Nerve fibres and cells immunoreactive to neurochemical markers in developing rat molars and supporting tissues. , 1994, Archives of oral biology.

[16]  Elizabeth Simons,et al.  Sensory and autonomic innervation of the rat eyelid: Neuronal origins and peptide phenotypes , 1994, Journal of Chemical Neuroanatomy.

[17]  P. Lefebvre,et al.  Cultured myofibroblasts display a specific phenotype that differentiates them from fibroblasts and smooth muscle cells. , 1994, Dermatology.

[18]  H. Kosmehl,et al.  Appearance of the myofibroblastic phenotype in Dupuytren's disease is associated with a fibronectin, laminin, collagen type IV and tenascin extracellular matrix. , 1994, Pathobiology : journal of immunopathology, molecular and cellular biology.

[19]  A. Chiavegato,et al.  Myofibroblast-derived smooth muscle cells during remodelling of rabbit urinary bladder wall induced by partial outflow obstruction. , 1993, Laboratory investigation; a journal of technical methods and pathology.

[20]  B. Eyden Brief review of the fibronexus and its significance for myofibroblastic differentiation and tumor diagnosis. , 1993, Ultrastructural pathology.

[21]  P. Wood,et al.  Fibroblasts promote Schwann cell basal lamina deposition and elongation in the absence of neurons in culture. , 1993, Developmental biology.

[22]  A. Chiavegato,et al.  Cytoskeletal and cytocontractile protein composition of smooth muscle cells in developing and obstructed rabbit bladder. , 1993, Experimental cell research.

[23]  F. Coignoul,et al.  Immunohistochemical Identification of Myoepithelial, Epithelial, and Connective Tissue Cells in Canine Mammary Tumors , 1993, Veterinary pathology.

[24]  J. Duckett,et al.  Bladder smooth muscle cells in culture: I. Identification and characterization. , 1993, The Journal of urology.

[25]  T. V. D. van den Ingh,et al.  Keratin and vimentin distribution patterns in the epithelial structures of the cannie anal region , 1992, The Anatomical record.

[26]  J. Rohen,et al.  Contractile cells in the human scleral spur. , 1992, Experimental eye research.

[27]  R. Carey,et al.  Expression of alpha-smooth muscle actin in the developing kidney vasculature. , 1992, Hypertension.

[28]  M. Bothwell,et al.  Altered expression of NGF and P75 NGF-receptor by fibroblasts of injured teeth precedes sensory nerve sprouting. , 1992, Growth factors.

[29]  F. Harrison Soluble vertebrate lectins: ubiquitous but inscrutable proteins. , 1991, Journal of cell science.

[30]  H. Kuromi Molecules secreted from target and non-target tissues promote and repel sympathetic fiber distribution in vitro. , 1991, Brain research. Developmental brain research.

[31]  C. Haaksma,et al.  Fibronectin filaments and actin microfilaments are organized into a fibronexus in Dupuytren's diseased tissue , 1991, The Anatomical record.

[32]  R. Romand,et al.  Expression of the β‐nerve growth factor gene in male sex organs of the mouse, rat, and guinea pig , 1991 .

[33]  D. Edgar The expression and distribution of laminin in the developing nervous system , 1991, Journal of Cell Science.

[34]  C. Lance‐Jones,et al.  The influence of presumptive limb connective tissue on motoneuron axon guidance. , 1991, Developmental biology.

[35]  P. Smith,et al.  Smooth muscle growth in the mature rat: role of sympathetic innervation. , 1990, Journal of the autonomic nervous system.

[36]  W. Schürch,et al.  Differentiation repertoire of fibroblastic cells: expression of cytoskeletal proteins as marker of phenotypic modulations. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[37]  M. Hollyday,et al.  Axon guidance in muscleless chick wings: the role of muscle cells in motoneuronal pathway selection and muscle nerve formation , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  G. Gabbiani,et al.  Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[39]  M. Kedinger,et al.  Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. , 1990, Differentiation; research in biological diversity.

[40]  J. Velasco,et al.  Orbital muscle of Müller: observations on human fetuses measuring 35-150 mm. , 1990 .

[41]  W. Schürch,et al.  Myofibroblasts from diverse pathologic settings are heterogeneous in their content of actin isoforms and intermediate filament proteins. , 1989, Laboratory investigation; a journal of technical methods and pathology.

[42]  J. Sanes,et al.  Extracellular matrix molecules that influence neural development. , 1989, Annual review of neuroscience.

[43]  R. A. Smith,et al.  Neuronal maintenance and neurite extension of adult mouse neurones in non-neuronal cell-reduced cultures is dependent on substratum coating. , 1988, Journal of cell science.

[44]  R. Hellweg,et al.  Nerve growth factor synthesis in cultured rat iris: modulation by endogenous transmitter substances. , 1988, Experimental cell research.

[45]  K. Gatter,et al.  Epithelial membrane antigen expression by the perineurium of peripheral nerve and in peripheral nerve tumours , 1988, Histopathology.

[46]  G. Gabbiani,et al.  The biology of the myofibroblast. Relationship to wound contraction and fibrocontractive diseases , 1988 .

[47]  R. Eddy,et al.  Evidence for the nonmuscle nature of the "myofibroblast" of granulation tissue and hypertropic scar. An immunofluorescence study. , 1988, The American journal of pathology.

[48]  C. Haaksma,et al.  Extracellular matrix-cytoskeletal connections at the surface of the specialized contractile fibroblast (myofibroblast) in Dupuytren disease. , 1987, The Journal of bone and joint surgery. American volume.

[49]  Keith A. Crutcher,et al.  Sympathetic sprouting in the central nervous system: a model for studies of axonal growth in the mature mammalian brain , 1987, Brain Research Reviews.

[50]  M. Schwab,et al.  Cellular localization of nerve growth factor synthesis by in situ hybridization. , 1987, The EMBO journal.

[51]  G. Gabbiani,et al.  A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation , 1986, The Journal of cell biology.

[52]  O. Ornatsky,et al.  Meta‐vinculin distribution in adult human tissues and cultured cells , 1986, FEBS letters.

[53]  P. Smith Role of the sympathetic nervous system in functional maturation of Müller's smooth muscle in the rat. , 1985, The Journal of pharmacology and experimental therapeutics.

[54]  Bertram Wiedenmann,et al.  Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles , 1985, Cell.

[55]  D. Edgar Nerve Growth Factors and Molecules of the Extracellular Matrix in Neuronal Development , 1985, Journal of Cell Science.

[56]  L. Landmesser,et al.  Pattern and specificity of axonal outgrowth following varying degrees of chick limb bud ablation , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  S. Kishimoto The regeneration of substance P-containing nerve fibers in the process of burn wound healing in the guinea pig skin. , 1984, The Journal of investigative dermatology.

[58]  Bergen Mp Some histological aspects of the structure of the connective tissue system and its relationships with the blood vessels in the human orbit. , 1982 .

[59]  T. Maeda,et al.  The regeneration of the sympathetic catecholaminergic nerve fibers in the process of burn wound healing in guinea pigs. , 1982, The Journal of investigative dermatology.

[60]  J. Lewis,et al.  Pioneer growth cones in virgin mesenchyme: an electron-microscope study in the developing chick wing. , 1982, Journal of embryology and experimental morphology.

[61]  J. Vandekerckhove,et al.  Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific alpha-type actin. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[62]  H. Thoenen,et al.  Physiology of nerve growth factor. , 1980, Physiological reviews.

[63]  R. Honjin,et al.  The spatial aspect and fine structure of the orbital muscle of the mouse. , 1980, Okajimas folia anatomica Japonica.

[64]  J. Drukker,et al.  The extrinsic innervation of the abdominal organs in the female rat. , 1979, Acta anatomica.

[65]  F. Lucas,et al.  Ultrastructure of chick tendon fibroblast with special reference to secretory mechanism. , 1979, Acta anatomica.

[66]  K Weber,et al.  Different intermediate-sized filaments distinguished by immunofluorescence microscopy. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[67]  R. Bunge,et al.  Evidence that contact with connective tissue matrix is required for normal interaction between Schwann cells and nerve fibers , 1978, The Journal of cell biology.

[68]  R. Campenot,et al.  Local control of neurite development by nerve growth factor. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[69]  P. Bornstein,et al.  Cell surface-associated structural proteins in connective tissue cells. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. E. Azzam,et al.  In vitro response of rabbit utero-ovarian ligament to catecholamines. , 1976, Fertility and sterility.

[71]  D. McDonald,et al.  The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: A quantitative ultrastructural analysis , 1975 .

[72]  V. Everts,et al.  Fine structure of fibroblasts in the periodontal ligament of the rat incisor and their possible role in tooth eruption. , 1974, Archives of oral biology.

[73]  R. S. Bressler Myoid cells in the capsule of the adrenal gland and in monolayers derived from cultured adrenal capsules , 1973, The Anatomical record.

[74]  G. Gabbiani,et al.  Myofibroblasts in an avascular fibrous tissue. , 1973, Laboratory investigation; a journal of technical methods and pathology.

[75]  R. E. Page The distribution and innervation of the extraocular smooth muscle in the orbit of the rat. , 1973, Acta anatomica.

[76]  C. Peracchia,et al.  FIXATION BY MEANS OF GLUTARALDEHYDE-HYDROGEN PEROXIDE REACTION PRODUCTS , 1972, The Journal of cell biology.

[77]  L. Olson,et al.  Ontogenesis of peripheral adrenergic neurons in the rat: pre- and postnatal observations. , 1970, Acta physiologica Scandinavica.

[78]  J. O'Shea An ultrastructural study of smooth muscle‐like cells in the theca externa of ovarian follicles in the rat , 1970, The Anatomical record.

[79]  M. H. Ross,et al.  Perineurium: Evidence for Contractile Elements , 1969, Science.

[80]  M. Stefanini,et al.  Fixation of Ejaculated Spermatozoa for Electron Microscopy , 1967, Nature.