Regional difference in epidermal thinning after skin denervation

H.-Y. Chiang, I.-T. Huang, W.-P. Chen, Hsiung-Fei Chien, C.-T. Shun, Y.-C. Chang, S.-T. Hsieh

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Denervation of skin has a profound influence on epidermis; epidermal thinning was a consistent finding in rats. However, it is not clear whether the degree of epidermal thinning was similar in the region receiving the same innervation. In mice, how early epidermal nerves were degenerated after nerve injury remained unknown. To address these issues, we transected the sciatic nerve in mice and compared the changes of epidermal thickness in different areas of the hind foot skin. Epidermal nerves degenerated within 48 h after nerve transection, similar to what was observed in rats. Seven days after nerve transection, there was differential thinning of epidermis. The interpad area, in the center of the sciatic nerve-innervated region, exhibited the most profound degree of epidermal thinning (34.6 ± 3.1 vs 47.8 ± 2.4 μm, P <0.01). The heel area, in the periphery of the sciatic nerve-innervated zone, did not show significant thinning of epidermis after denervation (37.3 ± 4.8 vs 41.5 ± 5.1 μm, P > 0.05). The degree of epidermal thinning after denervation in the pad area was the intermediate one: with 98.8 ± 4.8 vs 120.1 ± 7.3 μm, P <0.02, in the fete pegs, and 51.1 ± 4.1 vs 62.1 ± 6.0 μm, P <0.02, in the dermal papilla. The differential thinning was obvious when the thickness of the denervated epidermis was normalized to that of the control epidermis with the ratios of 0.73 ± 0.03 in the interpad area, 0.83 ± 0.04 in the rete peg, 0.85 ± 0.05 in the dermal papilla, and 0.92 ± 0.05 in the heel. Epidermal thinning was reversed by reinnervation of the epidermis after sciatic nerve crush (41.5 ± 1.5 vs 45.0 ± 2.0 μm in the interpad area, P > 0.05). These findings suggest that sensory nerves exhibit trophic influences on the epidermis presumably through the effects of diffusible factors.
Original languageEnglish
Pages (from-to)137-145
Number of pages9
JournalExperimental Neurology
Volume154
Issue number1
DOIs
Publication statusPublished - 1998
Externally publishedYes

Fingerprint

Denervation
Epidermis
Sciatic Nerve
Skin
Foot
Wounds and Injuries

Keywords

  • Axonal degeneration
  • Epidermis
  • Keratinocyte
  • Nerve degeneration
  • Protein gene product 9.5
  • Skin innervation
  • Unmyelinated nerves
  • animal tissue
  • article
  • denervation
  • epidermis
  • immunocytochemistry
  • male
  • mouse
  • nerve transection
  • nonhuman
  • priority journal
  • reinnervation
  • sciatic nerve
  • skin nerve
  • skinfold
  • Animals
  • Calcitonin Gene-Related Peptide
  • Denervation
  • Foot
  • Immunohistochemistry
  • Male
  • Mice
  • Mice, Inbred ICR
  • Nerve Crush
  • Nerve Regeneration
  • Nerve Tissue Proteins
  • Skin
  • Skin Physiology
  • Thiolester Hydrolases
  • Time Factors
  • Ubiquitin Thiolesterase

Cite this

Chiang, H-Y., Huang, I-T., Chen, W-P., Chien, H-F., Shun, C-T., Chang, Y-C., & Hsieh, S-T. (1998). Regional difference in epidermal thinning after skin denervation. Experimental Neurology, 154(1), 137-145. https://doi.org/10.1006/exnr.1998.6896

Regional difference in epidermal thinning after skin denervation. / Chiang, H.-Y.; Huang, I.-T.; Chen, W.-P.; Chien, Hsiung-Fei; Shun, C.-T.; Chang, Y.-C.; Hsieh, S.-T.

In: Experimental Neurology, Vol. 154, No. 1, 1998, p. 137-145.

Research output: Contribution to journalArticle

Chiang, H-Y, Huang, I-T, Chen, W-P, Chien, H-F, Shun, C-T, Chang, Y-C & Hsieh, S-T 1998, 'Regional difference in epidermal thinning after skin denervation', Experimental Neurology, vol. 154, no. 1, pp. 137-145. https://doi.org/10.1006/exnr.1998.6896
Chiang, H.-Y. ; Huang, I.-T. ; Chen, W.-P. ; Chien, Hsiung-Fei ; Shun, C.-T. ; Chang, Y.-C. ; Hsieh, S.-T. / Regional difference in epidermal thinning after skin denervation. In: Experimental Neurology. 1998 ; Vol. 154, No. 1. pp. 137-145.
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title = "Regional difference in epidermal thinning after skin denervation",
abstract = "Denervation of skin has a profound influence on epidermis; epidermal thinning was a consistent finding in rats. However, it is not clear whether the degree of epidermal thinning was similar in the region receiving the same innervation. In mice, how early epidermal nerves were degenerated after nerve injury remained unknown. To address these issues, we transected the sciatic nerve in mice and compared the changes of epidermal thickness in different areas of the hind foot skin. Epidermal nerves degenerated within 48 h after nerve transection, similar to what was observed in rats. Seven days after nerve transection, there was differential thinning of epidermis. The interpad area, in the center of the sciatic nerve-innervated region, exhibited the most profound degree of epidermal thinning (34.6 ± 3.1 vs 47.8 ± 2.4 μm, P <0.01). The heel area, in the periphery of the sciatic nerve-innervated zone, did not show significant thinning of epidermis after denervation (37.3 ± 4.8 vs 41.5 ± 5.1 μm, P > 0.05). The degree of epidermal thinning after denervation in the pad area was the intermediate one: with 98.8 ± 4.8 vs 120.1 ± 7.3 μm, P <0.02, in the fete pegs, and 51.1 ± 4.1 vs 62.1 ± 6.0 μm, P <0.02, in the dermal papilla. The differential thinning was obvious when the thickness of the denervated epidermis was normalized to that of the control epidermis with the ratios of 0.73 ± 0.03 in the interpad area, 0.83 ± 0.04 in the rete peg, 0.85 ± 0.05 in the dermal papilla, and 0.92 ± 0.05 in the heel. Epidermal thinning was reversed by reinnervation of the epidermis after sciatic nerve crush (41.5 ± 1.5 vs 45.0 ± 2.0 μm in the interpad area, P > 0.05). These findings suggest that sensory nerves exhibit trophic influences on the epidermis presumably through the effects of diffusible factors.",
keywords = "Axonal degeneration, Epidermis, Keratinocyte, Nerve degeneration, Protein gene product 9.5, Skin innervation, Unmyelinated nerves, animal tissue, article, denervation, epidermis, immunocytochemistry, male, mouse, nerve transection, nonhuman, priority journal, reinnervation, sciatic nerve, skin nerve, skinfold, Animals, Calcitonin Gene-Related Peptide, Denervation, Foot, Immunohistochemistry, Male, Mice, Mice, Inbred ICR, Nerve Crush, Nerve Regeneration, Nerve Tissue Proteins, Skin, Skin Physiology, Thiolester Hydrolases, Time Factors, Ubiquitin Thiolesterase",
author = "H.-Y. Chiang and I.-T. Huang and W.-P. Chen and Hsiung-Fei Chien and C.-T. Shun and Y.-C. Chang and S.-T. Hsieh",
note = "被引用次數:30 Export Date: 16 March 2016 CODEN: EXNEA 通訊地址: Chiang, H.-Y.; Department of Anatomy, Natl. Taiwan Univ. Coll. of Medicine, 1 Jen-Ai Road, Sec. 1, Taipei 10018, Taiwan 化學物質/CAS: Calcitonin Gene-Related Peptide, 83652-28-2; Nerve Tissue Proteins; Thiolester Hydrolases, EC 3.1.2.-; Ubiquitin Thiolesterase, EC 3.1.2.15 參考文獻: Albers, K.M., Wright, D.E., Davis, B.M., Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system (1994) J. Neurosci., 14, pp. 1422-1432; Benrath, J., Zimmerman, M., Gillardon, F., Substance P and nitric oxide mediate would healing of ultraviolet photodamaged rat skin: Evidence for an effect of nitric oxide on keratinocyte proliferation (1995) Neurosci. Lett., 200, pp. 17-20; Bullock, E.D., Johnson E.M., Jr., Nerve growth factor induces the expression of certain cytokine genes and bcl-2 in mast cells. Potential role in survival promotion (1996) J. Biol. Chem., 271, pp. 27500-27508; Davis, B.M., Lewin, G.R., Mendell, L.M., Jones, M.E., Albers, K.M., Altered expression of nerve growth factor in the skin of transgenic mice leads to changes in response to mechanical stimuli (1993) Neuroscience, 56, pp. 789-792; Devor, M., Schonfeld, D., Seltzer, Z., Wall, P.D., Two modes of cutaneous reinnervation following peripheral nerve injury (1979) J. Comp. Neurol., 185, pp. 211-220; Di Marco, E., Mathor, M., Bondanza, S., Cutuli, N., Marchisio, P.C., Cancedda, R., De Luca, M., Nerve growth factor binds to normal human keratinocytes through high and low affinity receptors and stimulates their growth by a novel autocrine loop (1993) J. Biol. Chem., 268, pp. 22838-22846; Fuchs, E., Epidermal differentiation: The bare essentials (1990) J. Cell Biol., 111, pp. 2807-2814; Galietta, L.J., Barone, V., DeLuca, M., Romeo, G., Characterization of chloride and cation channels in cultured human keratinocytes (1991) Pflugers Arch., 418, pp. 18-25; Grando, S.A., Horton, R.M., Mauro, T.M., Kist, D.A., Lee, T.X., Dahl, M.V., Activation of keratinocyte nicotinic cholinergic receptors stimulates calcium influx and enhances cell differentiation (1996) J. Invest. Dermatol., 107, pp. 412-418; Griffin, J.W., Hoffman, P.N., Degeneration and regeneration in the peripheral nervous system (1993) Peripheral Neuropathy, , Philadelphia: Saunders. p. 361-376; Haegerstrand, A., Jonzon, B., Dalsgaard, C.J., Nilsson, J., Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 5993-5996; Hall, Z.H., Sanes, J.R., Synaptic structure and development: The neuromuscular junction (1993) Cell, 72, pp. 99-121; Hara, M., Toyoda, M., Yaar, M., Bhawan, J., Avila, E.M., Penner, I.R., Gilchrest, B.A., Innervation of melanocytes in human skin (1996) J. Exp. Med., 184, pp. 1385-1395; Hennings, H., Michael, D., Cheng, C., Steinert, P., Holbrook, K., Yuspa, S.H., Calcium regulation of growth and differentiation of mouse epidermal cells in culture (1980) Cell, 19, pp. 245-254; Hsieh, S.T., Choi, S., Lin, W.-M., Chang, Y.-C., McArthur, J.C., Griffin, J.W., Epidermal denervation and its effects on keratinocytes and Langerhans cells (1996) J. Neurocytol., 25, pp. 513-524; Kennedy, W.R., Sakuta, M., Quick, D.C., Rodent eccrine sweat glands: A case of multiple efferent innervation (1984) Neuroscience, 11, pp. 741-749; Kennedy, W.R., Wendelschafer-Crabb, G., Johnson, T., Quantitation of epidermal nerves in diabetic neuropathy (1996) Neurology, 47, pp. 1042-1048; Kopp, D.M., Trachtenberg, J.T., Thompson, W.J., Glial growth factor rescues Schwann cells of mechanoreceptors from denervation-induced apoptosis (1997) J. Neurosci., 17, pp. 6697-6706; Kruger, L., The functional morphology of thin sensory axons: Some principles and problems (1996) Prog. Brain Res., 113, pp. 255-272; Kruger, L., Halata, Z., Structure of nociceptor {"}endings.{"} (1996) The Neurobiology of Nociceptors, pp. 37-71. , C. Belmonte, & F. Cervero. Oxford Univ. Press; Li, Y., Hsieh, S.T., Chien, H.-F., Zhang, X., McArthur, J.C., Griffin, J.W., Sensory and motor denervation influences epidermal thickness in rat foot glabrous skin (1997) Exp. Neurol., 147, pp. 452-462; Lin, W.-M., Hsieh, S.T., Huang, I.-T., Griffin, J.W., Chen, W.P., Ultrastructural localization and regulation of protein gene product 9.5 (1997) Neuroreport, 8, pp. 2999-3004; Lynn, B., Shakhanbeh, J., Substance P content of the skin, neurogenic inflammation and numbers of C-fibres following capsaicin application to a cutaneous nerve in the rabbit (1988) Neuroscience, 24, pp. 769-775; Mauro, T., Dixon, D.B., Hanley, K., Isseroff, R.R., Pappone, P.A., Amiloride blocks a keratinocyte nonspecific cation channel and inhibits Ca++ (1995) J. Invest. Dermatol., 105, pp. 203-208; Mauro, T.M., Isseroff, R.R., Lasarow, R., Pappone, P.A., Ion channels are linked to differentiation in keratinocytes (1993) J. Membr. Biol., 132, pp. 201-209; Mauro, T.M., Pappone, P.A., Isseroff, R.R., Extracellular calcium affects the membrane currents of cultured human keratinocytes (1990) J. Cell. Physiol., 143, pp. 13-20; McCarthy, B., Hsieh, S.T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaluation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; Micevych, P.E., Kruger, L., The status of calcitonin gene-related peptide a an effector peptide (1992) Ann. N.Y. Acad. Sci., 657, pp. 379-396; Mills, L.R., Nurse, C.A., Diamond, J., The neural dependency of Merkel cell development in the rat: The touch domes and foot pads contrasted (1989) Dev. Biol., 136, pp. 61-74; Morohunfola, K.A., Jones, T.E., Munger, B.L., The differentiation of the skin and its appendages. II. Altered development of papillary ridges following neuralectomy (1992) Anat. Rec., 232, pp. 599-611; Navarro, X., Verdu, E., Wendelscafer-Crabb, G., Kennedy, W.R., Innervation of cutaneous structures in the mouse hind paw: A confocal microscopy immunohistochemical study (1995) J. Neurosci. Res., 41, pp. 111-120; Nurse, C.A., MacIntyre, L., Diamond, J., Reinnervation of the rat touch dome restores the Merkel cell population reduced after denervation (1984) Neuroscience, 13, pp. 563-571; Nurse, C.A., MacIntyre, L., Diamond, J., A quantitative study of the time course of the reduction in Merkel cell number within denervated rat touch domes (1984) Neuroscience, 11, pp. 521-533; Pincelli, C., Fntini, F., Romualdi, P., Sevignani, C., Lesa, G., Benassi, L., Giannetti, A., Substance P is diminished and vasoactive intestinal peptide is augmented in psoriatic lesions and these peptides exert disparate effects on the proliferation of cultured human keratinocytes (1992) J. Invest. Dermatol., 98, pp. 421-427; Pincelli, C., Sevignani, C., Manfredini, R., Grande, A., Fantini, F., Bracci-Laudiero, L., Aloe, L., Giannetti, A., Expression and function of nerve growth factor and nerve growth factor receptor on cultured keratinocytes (1994) J. Invest. Dermatol., 103, pp. 13-18; Snider, W.D., Functions of the neurotrophins during nervous system development: What the knockouts are teaching us (1994) Cell, 77, pp. 627-638; Stankovic, N., Johansson, O., Hildebrand, C., Occurrence of epidermal nerve endings in glabrous and hairy skin of the rat foot after sciatic nerve regeneration (1996) Cell Tissue Res., 284, pp. 161-166; Takahashi, K., Nakanishi, S., Imamura, S., Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: Stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors (1993) J. Invest. Dermatol., 101, pp. 646-651; Thomas, P.K., Ochoa, J., Clinical features and differential diagnosis (1993) Peripheral Neuropathy, pp. 749-774. , P.J. Dyck, P.K. Thomas, J.W. Griffin, P.A. Low, & J.F. Poduslo. Philadelphia: Saunders; Wall, J.T., Cusick, C.G., Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats (1984) J. Neurosci., 4, pp. 1499-1515; Wang, L., Hilliges, M., Jernberg, T., Wiegleb-Edstronom, D., Johansson, O., Protein gene product 9.5-immunoreactive nerve fibers and cells in human skin (1990) Cell Tissue Res., 261, pp. 25-33; Wilkinson, K.D., Lee, K., Deshpande, S., Duerksen-Hughes, P., Boss, J.M., Pohl, J., The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase (1989) Science, 246, pp. 670-673; Yaar, M., Grossman, K., Eller, M., Gilchrest, B.A., Evidence for nerve growth factor-mediated paracrine effects in human epidermis (1991) J. Cell Biol., 115, pp. 821-828",
year = "1998",
doi = "10.1006/exnr.1998.6896",
language = "English",
volume = "154",
pages = "137--145",
journal = "Experimental Neurology",
issn = "0014-4886",
publisher = "Academic Press Inc.",
number = "1",

}

TY - JOUR

T1 - Regional difference in epidermal thinning after skin denervation

AU - Chiang, H.-Y.

AU - Huang, I.-T.

AU - Chen, W.-P.

AU - Chien, Hsiung-Fei

AU - Shun, C.-T.

AU - Chang, Y.-C.

AU - Hsieh, S.-T.

N1 - 被引用次數:30 Export Date: 16 March 2016 CODEN: EXNEA 通訊地址: Chiang, H.-Y.; Department of Anatomy, Natl. Taiwan Univ. Coll. of Medicine, 1 Jen-Ai Road, Sec. 1, Taipei 10018, Taiwan 化學物質/CAS: Calcitonin Gene-Related Peptide, 83652-28-2; Nerve Tissue Proteins; Thiolester Hydrolases, EC 3.1.2.-; Ubiquitin Thiolesterase, EC 3.1.2.15 參考文獻: Albers, K.M., Wright, D.E., Davis, B.M., Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system (1994) J. Neurosci., 14, pp. 1422-1432; Benrath, J., Zimmerman, M., Gillardon, F., Substance P and nitric oxide mediate would healing of ultraviolet photodamaged rat skin: Evidence for an effect of nitric oxide on keratinocyte proliferation (1995) Neurosci. Lett., 200, pp. 17-20; Bullock, E.D., Johnson E.M., Jr., Nerve growth factor induces the expression of certain cytokine genes and bcl-2 in mast cells. Potential role in survival promotion (1996) J. Biol. Chem., 271, pp. 27500-27508; Davis, B.M., Lewin, G.R., Mendell, L.M., Jones, M.E., Albers, K.M., Altered expression of nerve growth factor in the skin of transgenic mice leads to changes in response to mechanical stimuli (1993) Neuroscience, 56, pp. 789-792; Devor, M., Schonfeld, D., Seltzer, Z., Wall, P.D., Two modes of cutaneous reinnervation following peripheral nerve injury (1979) J. Comp. Neurol., 185, pp. 211-220; Di Marco, E., Mathor, M., Bondanza, S., Cutuli, N., Marchisio, P.C., Cancedda, R., De Luca, M., Nerve growth factor binds to normal human keratinocytes through high and low affinity receptors and stimulates their growth by a novel autocrine loop (1993) J. Biol. Chem., 268, pp. 22838-22846; Fuchs, E., Epidermal differentiation: The bare essentials (1990) J. Cell Biol., 111, pp. 2807-2814; Galietta, L.J., Barone, V., DeLuca, M., Romeo, G., Characterization of chloride and cation channels in cultured human keratinocytes (1991) Pflugers Arch., 418, pp. 18-25; Grando, S.A., Horton, R.M., Mauro, T.M., Kist, D.A., Lee, T.X., Dahl, M.V., Activation of keratinocyte nicotinic cholinergic receptors stimulates calcium influx and enhances cell differentiation (1996) J. Invest. Dermatol., 107, pp. 412-418; Griffin, J.W., Hoffman, P.N., Degeneration and regeneration in the peripheral nervous system (1993) Peripheral Neuropathy, , Philadelphia: Saunders. p. 361-376; Haegerstrand, A., Jonzon, B., Dalsgaard, C.J., Nilsson, J., Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 5993-5996; Hall, Z.H., Sanes, J.R., Synaptic structure and development: The neuromuscular junction (1993) Cell, 72, pp. 99-121; Hara, M., Toyoda, M., Yaar, M., Bhawan, J., Avila, E.M., Penner, I.R., Gilchrest, B.A., Innervation of melanocytes in human skin (1996) J. Exp. Med., 184, pp. 1385-1395; Hennings, H., Michael, D., Cheng, C., Steinert, P., Holbrook, K., Yuspa, S.H., Calcium regulation of growth and differentiation of mouse epidermal cells in culture (1980) Cell, 19, pp. 245-254; Hsieh, S.T., Choi, S., Lin, W.-M., Chang, Y.-C., McArthur, J.C., Griffin, J.W., Epidermal denervation and its effects on keratinocytes and Langerhans cells (1996) J. Neurocytol., 25, pp. 513-524; Kennedy, W.R., Sakuta, M., Quick, D.C., Rodent eccrine sweat glands: A case of multiple efferent innervation (1984) Neuroscience, 11, pp. 741-749; Kennedy, W.R., Wendelschafer-Crabb, G., Johnson, T., Quantitation of epidermal nerves in diabetic neuropathy (1996) Neurology, 47, pp. 1042-1048; Kopp, D.M., Trachtenberg, J.T., Thompson, W.J., Glial growth factor rescues Schwann cells of mechanoreceptors from denervation-induced apoptosis (1997) J. Neurosci., 17, pp. 6697-6706; Kruger, L., The functional morphology of thin sensory axons: Some principles and problems (1996) Prog. Brain Res., 113, pp. 255-272; Kruger, L., Halata, Z., Structure of nociceptor "endings." (1996) The Neurobiology of Nociceptors, pp. 37-71. , C. Belmonte, & F. Cervero. Oxford Univ. Press; Li, Y., Hsieh, S.T., Chien, H.-F., Zhang, X., McArthur, J.C., Griffin, J.W., Sensory and motor denervation influences epidermal thickness in rat foot glabrous skin (1997) Exp. Neurol., 147, pp. 452-462; Lin, W.-M., Hsieh, S.T., Huang, I.-T., Griffin, J.W., Chen, W.P., Ultrastructural localization and regulation of protein gene product 9.5 (1997) Neuroreport, 8, pp. 2999-3004; Lynn, B., Shakhanbeh, J., Substance P content of the skin, neurogenic inflammation and numbers of C-fibres following capsaicin application to a cutaneous nerve in the rabbit (1988) Neuroscience, 24, pp. 769-775; Mauro, T., Dixon, D.B., Hanley, K., Isseroff, R.R., Pappone, P.A., Amiloride blocks a keratinocyte nonspecific cation channel and inhibits Ca++ (1995) J. Invest. Dermatol., 105, pp. 203-208; Mauro, T.M., Isseroff, R.R., Lasarow, R., Pappone, P.A., Ion channels are linked to differentiation in keratinocytes (1993) J. Membr. Biol., 132, pp. 201-209; Mauro, T.M., Pappone, P.A., Isseroff, R.R., Extracellular calcium affects the membrane currents of cultured human keratinocytes (1990) J. Cell. Physiol., 143, pp. 13-20; McCarthy, B., Hsieh, S.T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaluation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; Micevych, P.E., Kruger, L., The status of calcitonin gene-related peptide a an effector peptide (1992) Ann. N.Y. Acad. Sci., 657, pp. 379-396; Mills, L.R., Nurse, C.A., Diamond, J., The neural dependency of Merkel cell development in the rat: The touch domes and foot pads contrasted (1989) Dev. Biol., 136, pp. 61-74; Morohunfola, K.A., Jones, T.E., Munger, B.L., The differentiation of the skin and its appendages. II. Altered development of papillary ridges following neuralectomy (1992) Anat. Rec., 232, pp. 599-611; Navarro, X., Verdu, E., Wendelscafer-Crabb, G., Kennedy, W.R., Innervation of cutaneous structures in the mouse hind paw: A confocal microscopy immunohistochemical study (1995) J. Neurosci. Res., 41, pp. 111-120; Nurse, C.A., MacIntyre, L., Diamond, J., Reinnervation of the rat touch dome restores the Merkel cell population reduced after denervation (1984) Neuroscience, 13, pp. 563-571; Nurse, C.A., MacIntyre, L., Diamond, J., A quantitative study of the time course of the reduction in Merkel cell number within denervated rat touch domes (1984) Neuroscience, 11, pp. 521-533; Pincelli, C., Fntini, F., Romualdi, P., Sevignani, C., Lesa, G., Benassi, L., Giannetti, A., Substance P is diminished and vasoactive intestinal peptide is augmented in psoriatic lesions and these peptides exert disparate effects on the proliferation of cultured human keratinocytes (1992) J. Invest. Dermatol., 98, pp. 421-427; Pincelli, C., Sevignani, C., Manfredini, R., Grande, A., Fantini, F., Bracci-Laudiero, L., Aloe, L., Giannetti, A., Expression and function of nerve growth factor and nerve growth factor receptor on cultured keratinocytes (1994) J. Invest. Dermatol., 103, pp. 13-18; Snider, W.D., Functions of the neurotrophins during nervous system development: What the knockouts are teaching us (1994) Cell, 77, pp. 627-638; Stankovic, N., Johansson, O., Hildebrand, C., Occurrence of epidermal nerve endings in glabrous and hairy skin of the rat foot after sciatic nerve regeneration (1996) Cell Tissue Res., 284, pp. 161-166; Takahashi, K., Nakanishi, S., Imamura, S., Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: Stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors (1993) J. Invest. Dermatol., 101, pp. 646-651; Thomas, P.K., Ochoa, J., Clinical features and differential diagnosis (1993) Peripheral Neuropathy, pp. 749-774. , P.J. Dyck, P.K. Thomas, J.W. Griffin, P.A. Low, & J.F. Poduslo. Philadelphia: Saunders; Wall, J.T., Cusick, C.G., Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats (1984) J. Neurosci., 4, pp. 1499-1515; Wang, L., Hilliges, M., Jernberg, T., Wiegleb-Edstronom, D., Johansson, O., Protein gene product 9.5-immunoreactive nerve fibers and cells in human skin (1990) Cell Tissue Res., 261, pp. 25-33; Wilkinson, K.D., Lee, K., Deshpande, S., Duerksen-Hughes, P., Boss, J.M., Pohl, J., The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase (1989) Science, 246, pp. 670-673; Yaar, M., Grossman, K., Eller, M., Gilchrest, B.A., Evidence for nerve growth factor-mediated paracrine effects in human epidermis (1991) J. Cell Biol., 115, pp. 821-828

PY - 1998

Y1 - 1998

N2 - Denervation of skin has a profound influence on epidermis; epidermal thinning was a consistent finding in rats. However, it is not clear whether the degree of epidermal thinning was similar in the region receiving the same innervation. In mice, how early epidermal nerves were degenerated after nerve injury remained unknown. To address these issues, we transected the sciatic nerve in mice and compared the changes of epidermal thickness in different areas of the hind foot skin. Epidermal nerves degenerated within 48 h after nerve transection, similar to what was observed in rats. Seven days after nerve transection, there was differential thinning of epidermis. The interpad area, in the center of the sciatic nerve-innervated region, exhibited the most profound degree of epidermal thinning (34.6 ± 3.1 vs 47.8 ± 2.4 μm, P <0.01). The heel area, in the periphery of the sciatic nerve-innervated zone, did not show significant thinning of epidermis after denervation (37.3 ± 4.8 vs 41.5 ± 5.1 μm, P > 0.05). The degree of epidermal thinning after denervation in the pad area was the intermediate one: with 98.8 ± 4.8 vs 120.1 ± 7.3 μm, P <0.02, in the fete pegs, and 51.1 ± 4.1 vs 62.1 ± 6.0 μm, P <0.02, in the dermal papilla. The differential thinning was obvious when the thickness of the denervated epidermis was normalized to that of the control epidermis with the ratios of 0.73 ± 0.03 in the interpad area, 0.83 ± 0.04 in the rete peg, 0.85 ± 0.05 in the dermal papilla, and 0.92 ± 0.05 in the heel. Epidermal thinning was reversed by reinnervation of the epidermis after sciatic nerve crush (41.5 ± 1.5 vs 45.0 ± 2.0 μm in the interpad area, P > 0.05). These findings suggest that sensory nerves exhibit trophic influences on the epidermis presumably through the effects of diffusible factors.

AB - Denervation of skin has a profound influence on epidermis; epidermal thinning was a consistent finding in rats. However, it is not clear whether the degree of epidermal thinning was similar in the region receiving the same innervation. In mice, how early epidermal nerves were degenerated after nerve injury remained unknown. To address these issues, we transected the sciatic nerve in mice and compared the changes of epidermal thickness in different areas of the hind foot skin. Epidermal nerves degenerated within 48 h after nerve transection, similar to what was observed in rats. Seven days after nerve transection, there was differential thinning of epidermis. The interpad area, in the center of the sciatic nerve-innervated region, exhibited the most profound degree of epidermal thinning (34.6 ± 3.1 vs 47.8 ± 2.4 μm, P <0.01). The heel area, in the periphery of the sciatic nerve-innervated zone, did not show significant thinning of epidermis after denervation (37.3 ± 4.8 vs 41.5 ± 5.1 μm, P > 0.05). The degree of epidermal thinning after denervation in the pad area was the intermediate one: with 98.8 ± 4.8 vs 120.1 ± 7.3 μm, P <0.02, in the fete pegs, and 51.1 ± 4.1 vs 62.1 ± 6.0 μm, P <0.02, in the dermal papilla. The differential thinning was obvious when the thickness of the denervated epidermis was normalized to that of the control epidermis with the ratios of 0.73 ± 0.03 in the interpad area, 0.83 ± 0.04 in the rete peg, 0.85 ± 0.05 in the dermal papilla, and 0.92 ± 0.05 in the heel. Epidermal thinning was reversed by reinnervation of the epidermis after sciatic nerve crush (41.5 ± 1.5 vs 45.0 ± 2.0 μm in the interpad area, P > 0.05). These findings suggest that sensory nerves exhibit trophic influences on the epidermis presumably through the effects of diffusible factors.

KW - Axonal degeneration

KW - Epidermis

KW - Keratinocyte

KW - Nerve degeneration

KW - Protein gene product 9.5

KW - Skin innervation

KW - Unmyelinated nerves

KW - animal tissue

KW - article

KW - denervation

KW - epidermis

KW - immunocytochemistry

KW - male

KW - mouse

KW - nerve transection

KW - nonhuman

KW - priority journal

KW - reinnervation

KW - sciatic nerve

KW - skin nerve

KW - skinfold

KW - Animals

KW - Calcitonin Gene-Related Peptide

KW - Denervation

KW - Foot

KW - Immunohistochemistry

KW - Male

KW - Mice

KW - Mice, Inbred ICR

KW - Nerve Crush

KW - Nerve Regeneration

KW - Nerve Tissue Proteins

KW - Skin

KW - Skin Physiology

KW - Thiolester Hydrolases

KW - Time Factors

KW - Ubiquitin Thiolesterase

U2 - 10.1006/exnr.1998.6896

DO - 10.1006/exnr.1998.6896

M3 - Article

VL - 154

SP - 137

EP - 145

JO - Experimental Neurology

JF - Experimental Neurology

SN - 0014-4886

IS - 1

ER -