Comprehensive immunofluorescence and lectin binding analysis of intervibrissal fur innervation in the mystacial pad of the rat

Journal of Comparative Neurology

Volumn 385, Issue 2, 1997, Pages 185-206

  Fundin, Bengt T ^a   Arvidsson, Jan ^a   Aldskogius, Håkan ^b   Johansson, Olle ^a   Rice, Suzanne N ^d   Rice, Frank L ^c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c ALBANY MEDICAL COLLEGE   (United States)

^d NONE

Author keywords

Autonomic innervation; Hair; Mechanoreceptors; Sensory innervation; Unmyelinated axons

Indexed keywords

LECTIN;

ANIMAL TISSUE; ARTICLE; AUTONOMIC INNERVATION; FEMALE; IMMUNOFLUORESCENCE TEST; LECTIN BINDING; MECHANORECEPTOR; MOUSE; NONHUMAN; NONMYELINATED NERVE; PRIORITY JOURNAL; PROTEIN DETERMINATION; RAT; SENSORY NERVE; SPECIES DIFFERENCE; VIBRISSA;

ANIMALS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; LECTINS; MICE; NEURAL PATHWAYS; RATS; RATS, SPRAGUE-DAWLEY; VIBRISSAE;

EID: 0030755969     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970825)385:2<185::AID-CNE2>3.0.CO;2-Y     Document Type: Article

References (95)

1. Albers, K.M., D.E. Wright, and B.M. Davis (1994) Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14:1422-1432.
2. Andres, K.H. (1966) Uber die Feinstruktur der Rezeptoren on Sinushaaren. Z. Zellforsch. 75:335-365.
3. Ambalavanar, R., and R. Morris (1992) The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience 47:421-429.
4. Arvidsson, J., F.L. Rice, B.T. Fundin, K.M. Albers, I. Silos-Santiago, A.M. Fagan, M. Barbacid, P. Ernfors, and B.M. Davis (1995) Effects of NT3 and trkC manipulations on developing Merkel innervation in the mystacial pad of the mouse. Soc. Neurosci. Abstr. 21:1540.
5. Biemesderfer, D., B.L. Munger, J. Binck, and R. Dubner (1978) The pilo-Ruffini complex: A non-sinus hair associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res. 142:197-222.
6. Brown, A.G., and A. Iggo (1967) A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J. Physiol. 193:707-733.
7. Burgess, P.R., and E.R. Perl (1973) Cutaneous mechanoreceptors and nociceptors. In A. Iggo (ed): Handbook of Sensory Physiology: Somatosensory System. Heidelberg: Springer-Verlag, pp. 29-78.
8. Cauna, N. (1973) The free penicillate nerve endings of the human hairy skin. J. Anat. 115:277-288.
9. Cauna, N. (1976) Morphological basis of sensation in hairy skin. Prog. Brain Res. 43:35-45.
10. Dalsgaard, C.J., J. Jernbeck, W. Stains, J. Kjartansson, A. Haegerstrand, T. Hökfelt, E. Brodin, A.C. Cuello, and J.C. Brown (1989) Calcitonin gene-related peptide-like immunoreactivity in nerve fibers in the human skin. Relation to fibers containing substance P-, somatostatin-and vasoactive intestinal polypeptide-like immunoreactivity. Histochemistry 91:35-38.
11. Davies, A.M., C. Bandtlow, R. Heumann, S. Korsching, H. Rohrer, and H. Thoenen (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353-358.
12. Davies, A.M. (1988) The trigeminal system: An advantageous experimental model for studying neuronal development. Development 103:175-183.
13. Davies, A.M., and A.G.S. Lumsden (1984) Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion. J. Comp. Neurol. 223:124-137.
14. Davis, B.M., B.T. Fundin, K.M. Albers, T.P. Goodness, K.M. Cronk, and F.L. Rice. (1997) Overexpression of NGF in skin increases innervation to specific sensory targets. J. Comp. Neurol. (in press).
15. Dörfl, J. (1985) The innervation of the mystacial region of the white mouse. J. Anat. 142:173-184.
16. Duc, C., I. Barakat-Walter, and B. Droz (1994) Innervation of putative rapidly adapting mechanoreceptors by calbindin-and calretinin-immunoreactive primary sensory neurons in the rat. Eur. J. Neurosci. 6:264-271.
17. Duggan, A.W., P.J. Hope, B. Jarrott, H.G. Schaible, and W.S. Fleetwood (1990) Release, spread and persistence of immunoreactive neurokinin A in the dorsal horn of the cat following noxious cutaneous stimulation. Studies with antibody microprobes. Neuroscience 35:195-202.
18. Elfvin, L.-G., B. Lindh, and T. Hökfelt (1993) The chemical neuroanatomy of sympathetic ganglia. Annu. Rev. Neurosci. 16:471-507.
19. Ernfors, P., J.P. Merlio, and H. Persson (1993) Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 4:1140-1158.
20. Feneley, M.R., J.W. Fawcett, and K.J. Keynes (1991) The role of Schwann cells in the regeneration of peripheral nerve axons through muscle basal lamina grafts. Exp. Neurol. 114:275-285.
21. Ferri, G.-L., A. Sabani, L. Abelli, J.M. Polak, D. Dahl, and M.-M. Portier (1990) Neuronal intermediate filaments in dorsal root ganglia: Differential distribution of peripherin and neurofilament protein and effect of capsaicin. Brain Res. 515:331-335.
22. Fried, K., and M. Risling (1991) Nerve growth factor receptor-like immunoreactivity in primary and permanent canine tooth pulps of the cat. Cell Tissue Res. 264:321-328.
23. Fundin, B.T., F.L. Rice, K. Pfaller, and J. Arvidsson (1994) The innervation of the mystacial pad in the adult rat studied by anterograde transport of HRP conjugates. Exp. Brain Res. 99:233-246.
24. Fundin, B.T., F.L. Rice, I. Silos-Santiago, A.M. Fagan, H. Aldskogius, M. Barbacid, and P. Ernfors (1995) Differential effects of various neurotrophin and trk gene deletions on mechanoreceptors in the mesenchymal sheath affiliated with mouse vibrissal follicles. Soc. Neurosci. Abstr. 21:1540.
25. Fundin, B.T., I. Silos-Santiago, P. Ernfors, A.M. Fagan, H. Aldskogius, T.M. DeChiara, H.S. Philips, M. Barbacid, and F.L. Rice (1997) Differential dependency of developing mechanoreceptors on neurotrophins, trk receptors and p75 LNGFR. Dev. Biol. (in press).
26. Goldstein, M.E., S.B. House, and H. Gainer (1991) NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J. Neurosci. Res. 30:92-104.
27. Habecker, B.A., S.J. Tresser, M.S. Rao, and S.C. Landis (1995) Production of sweat gland cholinergic differentiation factor depends on innervation. Dev. Biol. 167:307-316.
28. Habecker, B.A., and S.C. Landis (1994) Noradrenergic regulation of cholinergic differentiation. Science 264:1602-1604.
29. Halata, Z. (1975) The mechanoreceptors of the mammalian skin. Ultrastructure and morphological classification. Adv. Anat. 50:1-77.
30. Halata, Z. (1993) Sensory innervation of the hairy skin (light-and electron microscopic study. J. Invest. Dermatol. 101:75S-81S.
31. Hensel, H., K.H. Andres, and M. von Düring (1974) Structure and function of cold receptors. Pfluggers Arch. 352:1-10.
32. Hoheisel, U., and S. Mense (1986) Non-myelinated afferent fibers do not originate exclusively from the smallest dorsal root ganglion cells in the cat. Neurosci. Lett. 72:153-157.
33. Hökfelt, T., R. Elde, O. Johansson, R. Luft, G. Nilsson, and A. Arimura (1976) Immunohistochemical evidence for separate populations of somatostatin and substance P-containing neurons in the rat. Neuroscience 1:131-136.
34. Hökfelt, T. (1991) Neuropeptides in perspective: The last ten years. Neuron 7:867-879.
35. Hökfelt, T., X. Zhang, V. Verge, M. Villar, R. Elde, T. Bartfai, X.J. Xu, and Z. Wiesenfeld-Hallin (1993) Coexistence and interaction of neuropeptides with substance P in primary sensory neurons, with special reference to galanin [review]. Regul. Pept. 46:76-80.
36. Hua, X.-Y., E. Theodorsson-Norheim, E. Brodin, J.M. Lundberg, and T. Hökfelt (1985) Multiple tachykinins (neurokinin A, neuropeptide K, and substance P) in capsaicin-sensitive sensory neurons in the guinea-pig. Regul. Pept. 13:1-19.
37. Iggo, A., and K.H. Andres (1982) Morphology of cutaneous receptors. Ann. Rev. Neurosci. 5:1-31.
38. Iggo, A., and A.R. Muir (1969) The structure and function of a slowly-adapting touch corpuscle in hairy skin. J. Physiol. (Lond) 200:763-796.
39. Johansson, O., T. Hökfelt, and R.P. Elde (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13:265-339.
40. Jones, E.G., and I.T. Diamond (1995) The Barrel Cortex of Rodents. New York: Plenum Press, pp. 1-446.
41. Ju, G., T. Hökfelt, E. Brodin, J. Fahrenkrug, J.A. Fischer, P. Frey, R.P. Elde, and J.C. Brown (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide-and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res. 247:417-431.
42. Karanth, S.S., S. Dhital, D.R. Springall, and J.M. Polak (1990) Reinnervation and neuropeptides in mouse skin flaps. J. Auton. Nerv. Syst. 31:127-134.
43. Killackey, H.P., M.F. Jacquin, and R.W. Rhoades (1990) Development of somatosensory system structures. In J.R. Coleman (ed): Development of Sensory Systems in Mammals. New York: John Wiley & Sons, Inc., pp. 403-429.
44. Klein, C.M., K.N. Westlund, and R.E. Coggeshall (1990) Percentages of dorsal root axons immunoreactive for galanin are higher than those immunoreactive for calcitonin gene-related peptide in the rat. Brain Res. 519:97-101.
45. Kruger, L. (1987) Morphological correlates of "free" nerve endings: A reappraisal of thin sensory axon classification. In R.F. Schmidt, H.-G. Schaible, and C. Vahle-Hinz (eds): Fine Afferent Nerve Fibers and Pain. Weinheim: VCH Verlag Chemie, pp. 2-13.
46. Kruger, L. (1988) Morphological features of thin sensory afferent fibers: A new interpretation of 'nociceptor' function. Prog. Brain Res. 74:253-257.
47. Kruger, L., E.R. Perl, and M.J. Sedivec (1981) Fine structure of myelinated mechanical nociceptor endings in cat hairy skin. J. Comp. Neurol. 198:137-154.
48. Kruger, L., J.D. Silverman, P.W. Mantyh, C. Sternini, and N.C. Brecha (1989) Peripheral patterns of calcitonin-gene-related peptide general somatic innervation: Cutaneous and deep terminations. J. Comp. Neurol. 280:291-302.
49. Landis, S.C. (1994) Development of sympathetic neurons: Neurotransmitter plasticity and differentiation factors [review]. Prog. Brain Res. 100:19-23.
50. Landis, S.C., and J.R. Fredieu (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathetic innervation of rat sweat glands. Brain Res. 377:177-181.
51. Lawson, S.N. (1992) Morphological and biochemical cell types of sensory neurons. In S.A. Scott (ed): Sensory Neurons: Diversity, Development and Plasticity. New York: Oxford University Press, pp. 27-59.
52. Lawson, S.N. (1995) Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P. CGRP and somatostatin. Prog. Brain Res. 104:161-173.
53. Lawson, S.N., and P.J. Waddell (1991) Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J. Physiol. (Lond) 435:41-63.
54. Lawson, S.N., A.A. Harper, E.I. Harper, J.A. Garson, and B.H. Anderton (1984) A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones. J. Comp. Neurol. 228:263-272.
55. Lawson, S.N., P.W. McCarthy, and E. Prabhakar (1996) Electrophysiological properties of neurones with CGRP-like immunoreactivity in rat dorsal root ganglia. J. Comp. Neurol. 365:355-366.
56. Le Greves, P., F. Nyberg, L. Terenius, and T. Hökfelt (1985) Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. Eur. J. Pharmacol. 115:309-311.
57. Lindh, B., J.M. Lundberg, and T. Hökfelt (1989) NPY-, galanin-, VIP/PHI-, CGRP-and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections. Cell Tissue Res. 256:259-273.
58. Lynn, B., and S.E. Carpenter (1982) Primary afferent units from the hairy skin of the rat hindlimb. Brain Res. 238:29-43.
59. Maggi, C.A. (1995) Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 45:1-98.
60. Maggi, C., F. Borsini, P. Santicioli, P. Geppetti, L. Abelli, S. Evangelista, S. Manzini, E. Theodorsson-Norheim, V. Somma, F. Amenta, C. Bacciarelli, and A. Meli (1987) Cutaneous lesions in capsaicin-pretreated rats - a trophic role of capsaicin-sensitive afferents? Naunyn-Schmiedberg's Arch. Pharmac. 336:538-545.
61. Mata, M., D. Alessi, and D.J. Fink (1990) S100 is preferentially distributed in myelin-forming Schwann cells. J. Neurocytol. 19:432-442.
62. McCarthy, P.W., and S.N. Lawson (1990) Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 34:623-632.
63. Micevych, P.E., and L. Kruger (1992) The status of calcitonin gene-related peptide as an effector peptide [review]. Ann. NY Acad. Sci. 657:379-396.
64. Mosconi, T.M., and F.L. Rice (1991) Sensory innervation of the mystacial pad fur of the ferret. Neurosci. Lett. 91:199-202.
65. Mosconi, T.M., F.L. Rice, and M.J. Song (1993) Sensory innervation in the inner conical body of the vibrissal follicle-sinus complex of the rat. J. Comp. Neurol. 328:232-251.
66. Munger, B.L., and Z. Halata (1983) The sensory innervation of primate facial skin. I. Hairy skin. Brain Res. Rev. 5:45-80.
67. O'Brien, C., C.J. Woolf, M. Fitzgerald, R.M. Lindsay, and C. Molander (1989) Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience 32:493-502.
68. Oku, R., M. Satoh, N. Fujii, A. Otaka, H. Yajima, and H. Takagi (1987) Calcitonin gene-related peptide promotes mechanical nociception by potentiating the release of substance P from the spinal dorsal horn in rats. Brain Res. 403:350-354.
69. Paul, G., and A.M. Davies (1995) Trigeminal sensory neurons require extrinsic signals to switch neurotrophin dependence during the early stages of target field innervation. Dev. Bull. 171:590-605.
70. Rao, M.S., E. Jaszczak, and S.C. Landis (1994) Innervation of footpads of normal and mutant mice lacking sweat glands. J. Comp. Neurol. 346:613-625.
71. Renehan, W.E., and B.L. Munger (1986) Degeneration and regeneration in the rat trigeminal system. I. Identification and characterization of the multiple afferent innervation of the mystacial vibrissae. J. Comp. Neurol. 246:129-146.
72. Retzius, G. (1882) Anonymous Biologische Untersuchungen. Neue Folge IV. Stockholm: Samson and Wallin, pp. 45-48.
73. Rhoades, R.W., H.P. Killackey, N.L. Chiaia, and M.F. Jacquin (1990) Physiological development and plasticity of somatosensory neurons. In J.R. Coleman (ed): Development of Sensory Systems in Mammals. New York: John Wiley & Sons, Inc., pp. 431-459.
74. Rice, F.L. (1993) Structure, vascularization, and innervation of the mystacial pad of the rat as revealed by the lectin Griffonia simplicifolia. J. Comp. Neurol. 337:386-399.
75. Rice, F.L., and B.L. Munger (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. II. The common fur between the vibrissae. J. Comp. Neurol. 252:186-205.
76. Rice, F.L., E. Kinnman, H. Aldskogius, O. Johansson, and J. Arvidsson (1993) The innervation of the mystacial pad of the rat as revealed by PGP 9.5 immunofluorescence. J. Comp. Neurol. 337:366-385.
77. Rice, F.L., T.A. Henderson, P.A. Osborne, E.M. Johnson, and M.F. Jacquin (1994) Fetal NGF augmentation affects whisker pad innervation density and patterns at birth. Soc. Neurosci. Abstr. 20:1095.
78. Rice, F.L., T.A. Henderson, K.M. Albers, B.M. Davis, J.N. Carlson, and M.F. Jacquin (1995) Differential effects of fetal NGF injections and transgenic NGF enhancement on the innervation of the whisker pad in neonatal rats and mice. Soc. Neurosci. Abstr. 21:1540.
79. Rice, F.L., B.T. Fundin, J. Arvidsson, H. Aldskogius, and O. Johansson (1997) A comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J. Comp. Neurol. 385:149-184.
80. Silverman, J.D., and L. Kruger (1988a) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosen. Res. 5:259-267.
81. Silverman, J.D., and L. Kruger (1988b) Acid phosphatase as a selective marker for a class of small sensory ganglion cells in several mammals: spinal cord distribution, histochemical properties, and relation to fluoride-resistant acid phosphatase (FRAP) of rodents [review]. Somatosen. Res. 5:219-246.
82. Silverman, J.D., and L. Kruger (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J. Comp. Neurol. 280:303-330.
83. Silverman, J.D., and L. Kruger (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: Relation of lectin reactivity to peptide and enzyme markers. J. Neurocytol. 19:789-801.
84. Snow, P.J., and P. Wilson (1991) Plasticity and the mystacial vibrissae of rodents. In H. Autrum, D. Ottoson, E.R. Perl, R.F. Schmidt, H. Shimazu, and W.D. Willis (eds): Progress in Sensory Physiology. New York: Springer-Verlag, pp. 58-116.
85. Troy, C.M., K. Brown, L.A. Greene, and M.L. Shelanski (1990) Ontogeny of the neuronal intermediate filament protein, peripherin, in the mouse embryo. Neuroscience 36:217-237.
86. Urban, L., S.W.N. Thompson, A.J. Fox, S. Jeftinija, and A. Dray (1995) Peptidergic afferents; physiological aspects. In F. Nyberg, H. S. Sharma, and Z. Wiesenfeld-Hallin (eds): Progress in Brain Research. New York: Elsevier Science BV, pp. 255-269.
87. Waite, P.M., and M.F. Jacquin (1992) Dual innervation of the rat vibrissa: Responses of trigeminal ganglion cells projecting through deep or superficial nerves. J. Comp. Neurol. 322:233-245.
88. Wiesenfeld-Hallin, Z., T. Hökfelt, J.M. Lundberg, W.G. Forsmann, M. Reinecke, F.A. Tschopp, and J.A. Fischer (1984) Immunoreactive calcitonin gene-related poptide and substance P co-exist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci. Lett. 52:199-204.
89. Wiesenfeld-Hallin, Z., X.J. Xu, U. Langel, K. Bedecs, T. Hökfelt, and T. Bartfai (1992) Galanin-mediated control of pain: Enhanced role after nerve injury. Proc. Natl. Acad. Sci. USA 89:3334-3337.
90. Wilkinson, G.A., F.L. Rice, B.T. Fundin, I. Silos-Santiago, A.M. Fagan, R. Smeyne, S.D. Click, P. Ernfors, L.F. Reichardt, and M. Barbacid (1995) Differential effects of various neurotrophin and trk gene deletions on the unmyelinated innervation of the epidermis in the mouse whisker pad. Soc. Neurosci. Abstr. 21:1540.
91. Wood, J.W., and B.H. Anderton (1981) Monoclonal antibodies to mammalian neurofilaments. Biosci. Rep. 1:263-298.
92. Woolsey, T.A. (1990) Peripheral alterations and somatosensory development. In J.R. Coleman (ed): Development of Sensory Systems in Mammals. New York: John Wiley & Sons, Inc., pp. 461-503.
93. Woolsey, T.A., C. Welker, and R.H. Schwartz (1975) Comparative anatomical studies of the SmI face cortex with special reference to the occurrence of "barrels" in layer IV. J. Comp. Neurol. 164:79-94.
94. Wright, E.M., K.S. Vogel, and A.M. Davies (1992) Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival. Neuron 9:139-150.
95. Yamamoto, T. (1966) The fine structure of the palisade-type endings in relation to hair follicles. J. Electron Micr. 15:158-166.