p75 and TrkA neurotrophin receptors in human skin after spinal cord and peripheral nerve injury, with special reference to sensory corpuscles

Anatomical Record

Volumn 251, Issue 3, 1998, Pages 371-383

  Lopez S M ^a   Perez Perez M ^b   Marquez J M ^a   Naves, F J ^b   Represa, J ^c   Vega, J A ^b,d  

^a HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^b UNIVERSIDAD DE OVIEDO   (Spain)

^c UNIVERSITY OF VALLADOLID   (Spain)

^d Faculty de Medicina   (Spain)

Author keywords

Cutaneous mechanoreceptors; Nerve en trapment; Nerve section; Neurotrophin receptors; Spinal cord injury

Indexed keywords

NEUROTROPHIN RECEPTOR;

ADULT; ARTICLE; CELLULAR DISTRIBUTION; DEAFFERENTATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; PACINI CORPUSCLE; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DENSITY; SENSORY NERVE; SKIN NERVE; SPINAL CORD INJURY;

ADULT; AGED; CHILD, PRESCHOOL; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOENZYME TECHNIQUES; MALE; MIDDLE AGED; NERVE COMPRESSION SYNDROMES; PACINIAN CORPUSCLES; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR; SKIN; SPINAL CORD INJURIES;

EID: 0031806012     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0185(199807)251:3<371::AID-AR13>3.0.CO;2-L     Document Type: Article

References (80)

1. Airaksinen MS, Koltzenburg M, Lewin GR, Masu Y, Helbig C, Wolf E, Brem G, Toyka KV, Thoenen H, Meyer M. Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 1996;16:287-295.
2. Albers KM, Wright DE, Davis BM. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 1994;14:1422-1432.
3. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davies BM. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J. Cell. Biol. 1996;134:487-497.
4. Anton ES, Weskamp G, Reichardt LF, Matthew WD. Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc. Natl. Acad. Sci. U. S. A. 1994;91:2795-2799.
5. Barbacid M. Neurotrophic factors and their receptors. Curr. Opin. Cell. Biol. 1995;7:148-155.
6. Bergmann I, Priestly JV, McMahon SB, Brocker EB, Toyka KV, Kolzenburg M. Analysis of cutaneous sensory neurons in transgenic mice lacking the low affinity neurotrophin receptor p75. Eur. J. Neurosci. 1997;9:18-28.
7. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu. Rev. Neurosci. 1995;18:23-253.
8. NTR : A receptor after all. Science 1996;272:506-507.
9. Brown PB, Koerber HR, Ritz LA. Somatotopic organization of primary afferent projections to the spinal cord. In: Scott SA, ed. Sensory Neurons: Diversity, Development, and Plasticity. New York: Oxford University Press, 1992: 116-130.
10. Carlstedt T, Lugnegard H, Andersson M. Pacinian corpuscles after nerve repair in humans. Periph. Nerve Repair Regener. 1986;1: 37-40.
11. NTR decide? Neuron 1997;18:187-190.
12. Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhauser N, Bohm-Matthaei R, Baeuerle PA, Barde YA. Selective activation of NF-κB by nerve growth factor through the neurotrophin receptor p75. Science 1996;272:542-545.
13. Chesa PG, Rettig WJ, Thompson TM, Old LJ, Melamed MR. Immunohistochemical analysis of nerve growth factor receptor expression in normal and malignat human tissues. J. Histochem. Cytochem. 1988;36:383-389.
14. Conti G, Baron PL, Scarpini E, Vedeler C, Rostami A, Pleasure D, Scarlato G. Low-affiity nerve growth factor receptor expression in sciatic nerve during P2-peptide induced experimental allergic neuritis. Neurosci. Lett. 1995;199:135-138.
15. Dellon AL, Witebsky FG, Terrill R. The denervated sensory corpuscle. A sequential histological study after nerve division in the rhesus monkey. Plast. Reconstr. Surg. 1975;56:182-193.
16. Del Valle ME, Cabal A, Alvarez-Méndez JC, Calzada B, Haro JJ, Collier W, Vega JA. Effects of denervation on lamellar cells of Meissner-like sensory corpuscles of the rat. An immunohistochemical study. Cell. Mol. Biol. 1993;39:801-807.
17. Di Marco E, Mathor M, Bondanza S, Cutuli N, Marchisio PC, Cancedda R, De LM. Nerve growth factor binds to normal human keratinocytes through high and low affinity receptors and stimulates their growth by a novel autocrine loop. J. Biol. Chem. 1993;268:22838-22846.
18. Donovan MJ, Miranda RC, Kraemer R, McCaffrey TA, Tessarollo L, Mahaedo D, Sharif S, Kaplan DR, Tsoulfas P, Parada L, Toran-Allerand CD, Hajjar DP, Hempstead BL. Neurotrophin and neurotrophin receptors in vascular smooth muscle cells. Am. J. Pathol. 1995;147:309-324.
19. Dubový P. Enzyme histochemistry of cutaneous sensory nerve formations. Microsc. Res. Tech. 1996;34:334-350.
20. Dubový P, Aldskogius H. Degeneration and regeneration of cutaneous sensory nerve formations. Microsc. Res. Tech. 1996;34:362-375.
21. English KB, Harper S, Stayner N, Wanag Z-M, Davies AM. Localization of nerve growth factor (NGF) and low-affinity NGF receptors in touch domes and quantification of NGF mRNA in keratinocytes of adult rats. J. Comp. Neurol. 1994;344:470-480.
22. Fariñas I, Reichardt LF. Neurotrophic factors and their receptors: Implications of genetic studies. Semin. Neurosci. 1996;8:133-143.
23. Frisen J, Verge VM, Cullheim S, Persson H, Fried K, Middlemas DS, Hunter T, Hokfelt T, Risling M. Increased levels of TYkB mRNA and TrkB protein-like immunoreactivity in the injuried rat and cat spinal cord. Proc. Nat.l. Acad. Sci. U. S. A. 1992;89:11282-11286.
24. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O. Verge VM, Persson H. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 1993;123:455-465.
25. Fyffe REW. Laminar organization of primary afferent terminations in the mammalian spinal cord. In: Scott SA ed. Sensory Neurons: Diversity, Development, and Plasticity. New York: Oxford University Press, 1992: 131-139.
26. Halata Z. The mechanoreceptors of the mammalian skin: Ultrastructural and morphological classification. Adv. Anat. Embryol. Cell Biol. 1975;50:7-75.
27. Halata Z, Grim M, Chist B. Origin of spinal cord meninges, sheaths of peripheral nerves, and cutaneous receptors including Merkel cells. An experimental and ultrastructural study with avian chimeras. Anat. Embryol. 1990;182:529-537.
28. Hartschung W, Weihe E, Reincke M. The Merkel cell. In: BereiterHahn J, Matoltsy AG, Richards KS, eds. Biology of the Integument, Vol. 2. Vertebrates. Berlin-Heidelberg: Springer, 1986: 605-620.
29. Helgren ME, Cliffer KD, Torrento K, Cavnor C, Curtis R, DiStefano PS, Weigand SJ, Lindsay RM. Neurotrophin-3 administration atenuates deficits of pyridoxine-induced large-fiber sensory neuropathy. J. Neurosci. 1997;17:372-382.
30. Hoehner JC, Olsen L, Sandstedt B, Kaplan DR, Pahlman S. Association of neurotrophin receptor expression and differentiation in human neuroblastoma. Am. J. Pathol. 1995;147:102-113.
31. Hunt SP, Mantyh PW, Priestley J.V. The organization of biochemically characterized sennsory neurons. In: Scott SA, ed. Sensory Neurons: Diversity, Development, and Plasticity. New York: Oxford University Press, 1992: 60-76.
32. Iggo A, Andres KH. Morphology of cutaneous receptors. Annu. Rev. Neurosci. 1982;5:1-31.
33. Kosima I, Moriguchi T, Soeda S. Electron microscopic observations of degenetation of human Pacinian corpuscles in amputed fingers. Plast. Reconstr. Surg. 1992;84:243-250.
34. Lee K-F, Li E, Huber J, Landis SC, Sharpe AH, Chao MV, Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor leads to deficits in the peripheral sensory nervous system. Cell 1992;69:737-749.
35. Lemke G, Chao M. Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 1988;102:499-504.
36. Lewin GR, Barde YA. Physiology of neurotrophins. Annu. Rev. Neurosci. 1996;19:289-317.
37. Lewin GR, Mendell LM. Nerve growth factor and nociception. Trends Neurosci. 1993;16:353-359.
38. Lindsay RM. Role of neurotrophins and trk receptors in the development and maintenance of sensory neurons: An overview. Philos. Trans. R. Soc. Lond. [Biol.] 1996;351:365-373.
39. Liu HM, Lei HY, Kao KP. Correlation between NGF levels in wound chamber fluid and cytological localization of NGF and NGF receptor in axotomiced rat sciatic nerve. Exp. Neurol. 1995;132:24-32.
40. Malinovsky L. Mechanoreceptors and free nerve endings. In: Bereiter-Hahn J, Matoltsy AG, Richards KS, eds. Biology of the Integument, Vol. 2. Vertebrates. Berlin-Heidelberg: Springer, 1986: 535-560.
41. Malinovsky L. Sensory nerve formations in the skin and their classification. Microsc. Res. Tech. 1996;34:283-301.
42. Marquez J, Pérez-Pérez M, Naves FJ, Vega JA. Effect of spinal cord and peripheral nerve injury on human cutaneous sensory corpuscles: An immunohistochemical study. Journal of the Peripheral Nervous System 1997;2:49-59.
43. Martin P. Wound healing - aiming for perfect skin regeneration. Science 1997;276:75-81.
44. Mearow KM, Kril Y, Diamond J. Increased NGF mRNA expression in denervated rat skin. Neuroreport 1993;4:351-354.
45. Munger BL, Ide C. The structure and function of cutaneous sensory receptors. Arch. Histol. Cytol. 1988;51:1-34.
46. Munson JB, Shelton DL, McMahon SB. Adult mammalian sensory and motor neurons: Role of endogenous neurotrophins and rescue by exogenus neurotrophins after axotomy. J. Neurosci. 1997;17:470-476.
47. Narisawa Y, Hashimoto K, Nihie Y, Pietruk T. Biological significance of dermal Merkel cells in development of cutaneous nerves in human fetal skin. J. Histochem. Cytochem. 1992;40:65-71.
48. Offenhauser N, Bohm-Mattheai R, Tsoulfas P, Parada L, Mayer M. Developmental regulation of full-length trkC in the rat sciatic nerve. Eur. J. Neurosci. 1995;7:917-925.
49. Panus R, Luftl M, Czarnetzki BM. Nerve growth factor modulates keratinocyte proliferation in murine skin organ culture. Br. J. Dermatol. 1994;130:174-180.
50. Perl ER. Function of dorsal root ganglion neurons: An overview. In: Scott SA, ed. Sensory Neurons: Diversity, Development, and Plasticity. New York: Oxford University Press, 1992: 3-23.
51. Ramieri G, Stella M, Calcagni M, Cellino G, Panzica GC. An immunohistochemical study on cutaneous sensory receptors after chronic median nerve compression in man. Acta Anat. (Basel) 1995;152:224-229.
52. Ribeiro da Silva A, Konigsberg RL, Cuello AC. Light and electron microscopic distribution of nerve growth factor receptor-like immunoreactivity in the skin of the rat lower lip. Neuroscience 1991;43: 631-646.
53. Risling M, Dalsgaard CJ, Frisen J, Sjogren AM, Fried K. Substance P-, calciton gene-related peptide-, growth associated protein-43-, and neurotrophin receptor-like immunoreactivity associated with ummyelinated axons in feline ventral roots and pia mater. J. Comp. Neurol. 1994;339:365-386.
54. Rohrer H, Heumann R, Thoenen H. The synthesis of nerve growth factor (NGF) in developing skin is independent of innervation. Dev. Biol. 1988;128:240-244.
55. Saxod R. Development of cutaneous sensory receptors in birds. In: Jacobson M, ed. Handbook of Sensory Physiology. Vol. 9. Development of Sensory Systems. Berlin, Heidelberg, New York: Springer-Verlag, 1978: 337-417.
56. Saxod R. Ontogeny of the cutaneous sensory organs. Microsc. Res. Tech. 1996;34:313-333.
57. Scarpini E, Ross AH, Rosen JL, Brown MJ, Rostami A, Kaprowski H, Lisak RP. Expression of nerve growth factor during human peripheral nerve development. Dev. Biol. 1988;125:301-310.
58. Schatteman GC, Langer T, Lanahan AA, Bothwell MA. Distribution of the p75-kD low-affinity nerve growth factor receptor in the primate peripheral nervous system. Somatosens. Mot. Res. 1993;10:415-432.
59. Shelton DL, Sutherland J, Gripp J, Camerato T, Armanini MP, Phillips HS, Carrol K, Spencer SD, Levinson A-D. Human trks: Molecular cloning, tissues distribution, and expression of extracellular domain immunoadhesins. J. Neurosci. 1995;15:477-491.
60. Shibayama E, Koizumi H. Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am. J. Pathol. 1996;148:1807-1818.
61. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 1994;368:246-249.
62. Snider WD, Wright DE. Neurotrophins cause a new sensation. Neuron 1996;16:229-232.
63. Sobue G, Yasuda T, Mitsuma T, Ross AH, Pleasure D. Expression of nerve growth factor in human peripheral neuropathies. Ann. Neurol. 1988;24:64-72.
64. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM Jr. Expression of nerve growth factor receptors in Schwann cells of axotomized peripheral nerves: Ultrastructural localization, suppression by axonal contact, and binding properties. J. Neurosci. 1988;8:664-681.
65. Terenghi G, Mann D, Kopelman PG, Anand P. trkA and trkC expression is increased in human diabetic skin. Neurosci. Lett. 1997;228: 33-36.
66. Thomas CK, Westling G. Tactile unit properties after human cervical spinal cord injury. Brain 1995;118:1547-1556.
67. Vega JA, Haro JJ, De Lamo A, Ordieres M, Del Valle ME, Calzada B. Distribution of low affinity nerve growth factor receptor (NGFr) immunoreactivity in the human digital skin. Eur. J. Dermatol. 1992;2:509-516.
68. Vega JA, Del Valle ME, Haro JJ, Calzada B, Suárez-Garnacho S, Malinovsky L. Nerve growth factor receptor immunoreactivity in Meissner and Pacinian corpuscles of human digital skin. Anat. Rec. 1993;236:730-736.
69. Vega JA, Del Valle ME, Haro JJ, Naves FJ, Calzada B, Uribelarrea R. The inner-core, outer-core and capsule of human Pacinian corpuscles: An immunohistochemical study. Eur. J. Morphol. 1994a;32: 11-18.
70. Vega JA, Vázquez E, Naves FJ, Calzada B, Del Valle ME, Represa JJ. Immunohistochemical localization of the high-affinity NGF receptor (p140-trkA) in adult dorsal root and sympathetic ganglia, and in the nerves and sensory corpuscles supplying digital skin. Anat. Rec. 1994b;240:579-588.
71. Vega JA, Haro JJ, Del Valle ME. Immunohistochemistry of human cutaneous Meissner and Pacinian corpuscles. Microsc. Res. Tech. 1996a;34:351-361.
72. Vega JA, Llamosas MM, Huerta JJ, García-Fernández JM. Study of human cutaneous sensory corpuscles using double immunolabelling and confocal laser scanning microscopy. Anat. Rec. 1996b;246:557-560.
73. Wada H. Nerve endings in pal skingrafts. Ann. Plast. Surg. 1989;22: 461-466.
74. Wyatt S, Shooter EM, Davies AM. Expression of NGF receptor gene in sensory neurons and their cutaneous targets prior and during innervation. Neuron 1990;2:421-427.
75. Yamamoto M, Kondo H, Iseki S. Nerve growth factor receptor (NGFR)-like immunoreactivity in the perineurial cells in normal and sectioned peripheral nerves of rats. Anat. Rec. 1992;233:301-308.
76. Yamamoto M, Sobue G, Mutoh T, Li M, Doyu M, Mitsuma T, Kimata K. Gene expression of high-(p140trk) and low-affinity nerve growth factor receptor (LNGF) in the adult and aged human peripheral nervous system. Neurosci. Lett. 1993;158:39-43.
77. Yasuda T, Sobue G, Mitsuma T, Takahashi A, Hashizume Y. Nerve growth factor receptor immunoreactivity in human beningn peripherak nerve sheath tumor. Acta Neuropathol. (Berl.) 1989;77:591-598.
78. Zelena J. The effect of long-term denervation in the ultrastructure of Pacinian corpuscles in the cat. Cell Tissue Res. 1984;238:387-394.
79. Zelena J. Nerves and Mechanoreceptors. London: Chapman & Hall, 1994.
80. Zhou X-F, Rush RA. Peripheral projections of rat primary sensory neurons immunoreactive for neurotrophin-3. J. Comp. Neurol. 1995;363:69-77.