Expression of the low-affinity NGF receptor during human muscle development, regeneration, and in tissue culture
Corresponding Author
Dr. Pierluigi Baron MD, PhD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Istituto di Clinica Neurologica, Università di Milano, Via F. Sforza 35, 20122 Milano, ItalySearch for more papers by this authorDr. Elio Scarpini MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. Gianni Meola MD
Second Division of Neurology, San Donate Hospital, Milan, Italy
Search for more papers by this authorDr. Ignazio Santilli MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. Giancarlo Conti MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. David Pleasure MD
Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorDr. Guglielmo Scarlato MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorCorresponding Author
Dr. Pierluigi Baron MD, PhD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Istituto di Clinica Neurologica, Università di Milano, Via F. Sforza 35, 20122 Milano, ItalySearch for more papers by this authorDr. Elio Scarpini MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. Gianni Meola MD
Second Division of Neurology, San Donate Hospital, Milan, Italy
Search for more papers by this authorDr. Ignazio Santilli MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. Giancarlo Conti MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorDr. David Pleasure MD
Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorDr. Guglielmo Scarlato MD
Institute of Clinical Neurology, Dino Ferrari Center, University of Milan, Milan, Italy
Search for more papers by this authorAbstract
The expression of the low-affinity NGF receptor (LNGFR) during human muscle development, regeneration, and in tissue culture was analyzed using a murine monoclonal antibody to human LNGFR (MAb ME 20.4). Muscle cells from 12–22-week fetuses stained strongly for LNGFR. In adult normal muscle, only intramuscular nerve endings showed immunoreactivity with MAb ME 20.4, but no staining was detected in muscle fibers. In Duchenne muscular dystrophy, immunohistologically demonstrable LNGFR was present in regenerating muscle fibers. In these fibers, LNGFR gene expression was also demonstrated at the transcriptional level using in situ hybridization with riboprobes coding with human LNGFR. Cultures from human fetal and adult muscle were studied by double label indirect immunofluorescence microscopy with MAb ME 20.4 and antisera against human fetal myosin. Most myosin-positive cells, both at the myoblast and myotube stages, displayed surface LNGFR immunostaining. In cells from fetal muscle, LNGFR was detected during the first 2 weeks in vitro, whereas in cells from adult muscle the expression of LNGFR was observed for up to 7 weeks. These findings suggest a potential involvement of LNGFR in human muscle development and regeneration. © 1994 John Wiley & Sons, Inc.
References
- 1 Allen RE, Boxhorn LK: Regulation of skeletal muscle satellite cell Proliferation and differentiation by trasforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 1989; 138: 311–315.
- 2 Baron PL, Meola G, Scarpini E, Moggio M, Santilli I, Scarlato G: Lysosomotropic agents induce morphological and functional changes in human muscle cells in vitro. Eur J Bas Appl Histochem 1991; 35: 423–432.
- 3 Baron PL, Kamholz J, Scherer S, Honda H, Shy M, Scarpini E, Scarlato G, Pleasure D: Appearance of PLP mRNA in specific regions of the developing rat lumbosacral spinal cord as revealed by in situ hybridization. Exp Neurol 1993; 121: 139–147.
- 4 Berg MM, Sternberg DW, Hempstead BL, Chao MV: The low-affinity p75 nerve growth factor (NGF) receptor mediates NGF-induced tyrosine phosphorylation. Proc Natl Acad Sci USA 1991; 88: 7106–7110.
- 5 Berkemeier LR, Winslow JW, Kaplan DR, Nikolics K, Goeddel DV, Rosenthal A: Neurotrophin-5: a novel neurotrophic factor that activities trk and trk B. Neuron 1991; 7: 857–866.
- 6 Bothwell M: Keeping track of neurotrophin receptors. Cell 1991; 65: 915–918.
- 7 Brodie C, Sampson SR: Nerve growth factor supports growth of rat skeletal myotubes in culture. Brain Res 1987; 435: 393–397.
- 8 Brodie C, Sampson SR: Nerve growth factor and fibroblast growth factor influence post-fusion expression of Nachannels in cultured rat skeletal muscle. J Cell Physiol 1990; 144: 492–497.
- 9 Cordon-Cardo C, Tapley P, Jing S, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid M: The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 1991; 66: 173–183.
- 10 Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H: Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 1987; 326: 353–358.
- 11 Davies AM, Lumsden AGS, Rohrer H: Neural crest-derived proprioceptive neurons express nerve growth factor receptors but are not supported by nerve growth factor in culture. Neuroscience 1987; 20: 37–46.
- 12 Delaporte C, Dautreaux B: Differentiation of human muscle cells in the presence of neuronal conditioned medium (NCM), nerve growth factor (NGF) and spinal cord cells (SC). Adv Exp Med Biol 1987; 209: 15–17.
- 13 Ernfors P, Hallbook F, Ebendal T, Shooter EM, Radeke MJ, Misko TP, Persson H: Developmental and regional expression of β-nerve growth factor receptor mRNA in the chick and rat. Neuron 1988; 1: 983–996.
- 14 Green SH, Rydel RE, Connolly JL, Greene LA: PC12 cell mutants that possess low but not high-affinity nerve growth factor receptors neither respond to nor internalize nerve growth factor. J Cell Biol 1986; 102: 830–842.
- 15 Hallbook F, Ibanez C, Persson H: Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in xenopus ovary. Neuron 1991; 6: 845–858.
- 16 Hempstead BL, Schleifer LS, Chao MV: Expression of functional nerve growth factor receptors after gene transfer. Science 1989: 243: 373–375.
- 17 Hempstead BL, Martin-Zanca D, Kaplan DR, Parada LF, Chao MV: High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 1991; 350: 678–683.
- 18 Heumann R, Korsching S, Bandtlow C, Thoenen H: Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol 1987; 104: 1623–1631.
- 19 Hohn A, Leibrock J, Bailey K, Barde YA: Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 1990; 344: 339–341.
- 20 Johnson D, Lanahan A, Buck CR, Sehgal A, Morgan C, Mercer E, Bothwell M, Chao M: Expression and structure of the human NGF receptor. Cell 1986; 47: 545–554.
- 21 Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF: The trk protooncogene product: a signal transducing receptor for nerve growth factor. Science 1991; 252: 554–558.
- 22 Klein R, Jing S, Nanduri V, O'Rourke E, Barbacid M: The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 1991; 65: 189–197.
- 23 Klein R, Nanduri V, Jing S, Lamballe F, Tapley P, Bryant S, Cordon-Cardo C, Jones KR, Reichardt LF, Barbacid M: The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 1991; 66: 395–403.
- 24 Lamballe F, Klein R, Barbacid M: TrkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 1991; 66: 967–979.
- 25 Large TH, Weskamp G, Helder JC, Radeke MJ, Misko TP, Shooter EM, Reichardt LF: Structure and developmental expression of nerve growth factor receptor in the chicken nervous system. Neuron 1989; 2: 1123–1134.
- 26 Lee V, Wu HL, Schlaepfer WW: Monoclonal antibodies recognize individual neurofilament triplet protein. Proc Natl Acad Sci USA 1982; 79: 6089–6092.
- 27 Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde HA: Molecular cloning and expression of brain-derived neurotrophic factor. Nature 1989; 341: 149–152.
- 28 Levi-Montalcini R: The nerve growth factor 35 years later. Science 1987; 237: 1154–1162.
- 29 Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD: Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 1990; 247: 1446–1451.
- 30 Oppenheim RW: The neurotrophic theory and naturally occurring motorneuron death. Trends Neurosci 1989; 12: 252–255.
- 31 Pleasure SJ, Reddy UR, Venkatakrishnan G, Roy AK, Chen J, Ross AH, Trojanowski JQ, Pleasure DE, Lee VMY: Introduction of nerve growth factor (NGF) receptors into a medulloblastoma cell line results in expression of high and low-affinity NGF receptors but not NGF-mediated differentiation. Proc Natl Acad Sci USA 1990; 87: 8496–8500.
- 32 Radeke MJ, Misko TP, Hsu C, Herzenberg LA, Shooter EM: Gene transfer and molecular cloning of the rat nerve growth receptor. Nature 1987; 325: 593–597.
- 33 Radeva V: Effects of the nerve growth factor (NGF) on certain non-neuronal elements. Agressologie 1978; 19: 99–103.
- 34 Rodriguez-Tebar A, Dechant G, Barde YA: Binding of brain derived neurotrophic factor to the nerve growth factor receptor. Neuron 1990; 4: 487–492.
- 35 Ross AH, Grob P, Bothwell M, Elder DE, Ernst CS, Marano N, Ghrist BFD, Slemp CC, Herlyn M, Atkinson BF, Koprowski H: Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proc Natl Acad Sci USA 1984; 81: 6681–6685.
- 36 Scarpini E, Ross AH, Rosen JL, Brown MJ, Rostami A, Koprowski H, Lisak RP: Expression of nerve growth factor receptor during human peripheral nerve development. Dev Biol 1988; 125: 301–310.
- 37 Scarpini E, Beretta S, Ross AH, Moggio M, Jann S, Pleasure D, Scarlato G: Rapid quantitative immunohistochemical assessment of human peripheral neuropathies using a monoclonal antibody against nerve growth factor receptor. J Neurol 1989; 236: 439–444.
- 38 Seilhemeier B, Schachner M: Regulation of neural cell adhesion molecule expression on cultured mouse schwann cells by nerve growth factor. EMBO J 1987; 6: 1611–1616.
- 39 Sobue G, Yasuda T, Mitsuma T, Ross AH, Pleasure D: Expression of nerve growth factor receptor in human peripheral neuropathies. Ann Neurol 1988; 24: 64–72.
- 40 Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, Nikolics K, Parada LF: The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkS tyrosine kinase receptor. Cell 1991; 65: 895–903.
- 41 Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, DiStefano PS, Yancopoulos GD: TrkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 1991; 65: 885–893.
- 42 Sutter A, Riopelle RJ, Harris-Warrick RM, Shooter EM: Nerve growth factor receptors: characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J Biol Chem 1979; 254: 5972–5982.
- 43 Taniuchi M, Clark HB, Johnson EM: Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc Natl Acad Sci USA 1986; 83: 4094–4098.
- 44 Thoenen H, Barde YA: Physiology of nerve growth factor. Physiol Rev 1980; 60: 1284–1335.
- 45 Volpe P, Biral D, Damiani E, Margreth A: Characterization of human muscle myosins with respect to the light chains. Biochem J 1981; 195: 251–258.
- 46 Wheeler EF, Bothwell M: Spatiotemporal patterns of expression of NGF and the low-affinity NGF receptor in rat embryos suggest functional roles in tissue morphogenesis and myogenesis. J Neurosci 1992; 12: 930–945.
- 47 Yan Q, Johnson EM: A quantitative study of the developmental expression of nerve growth factor (NGF) receptor in rats. Dev Biol 1987; 121: 139–148.
- 48 Zhao J, Yoshioka K, Milke T, Kageshita T, Arao T: Nerve growth factor receptor immunoreactivity on the tunica adventitia of intramuscular blood vessels in childhood muscular dystrophies. Neuromusc Dis 1991; 1: 135–141.