Coordinate expression of NGF and α-smooth muscle actin mRNA and protein in cutaneous wound tissue of developing and adult rats

Cell and Tissue Research

Volumn 300, Issue 1, 2000, Pages 97-109

  Hasan, Wohaib ^a   Zhang, Renjie ^a   Liu, Manxi ^a   Warn, J Donald ^a   Smith, Peter G ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Development; In situ hybridization; Macrophages; Myofibroblasts; Nerve growth factor; Rat (Sprague Dawley); Skin; Wound

Indexed keywords

ALPHA ACTIN; CELL MARKER; MESSENGER RNA; NERVE GROWTH FACTOR;

ADIPOCYTE; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KERATINOCYTE; MACROPHAGE; MALE; MYOFIBROBLAST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SCHWANN CELL; SKIN FIBROBLAST; SKIN INJURY; VASCULAR SMOOTH MUSCLE; WOUND HEALING;

ACTINS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MALE; MUSCLE, SMOOTH; NERVE GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY; RNA, COMPLEMENTARY; RNA, MESSENGER; SKIN; WOUND HEALING;

ANIMALIA; EUKARYOTA;

EID: 0034079159     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050051     Document Type: Article

References (78)

1. Anand P, Foley P, Navsaria HA, Sinicropi D, Williams-Chestnut RE, Leigh IM (1995) Nerve growth factor levels in cultured human skin cells: effect of gestation and viral transformation. Neurosci Lett 184:157-160
2. Armstrong JR, Ferguson MWJ (1995) Ontogeny of the skin and the transition from scar-free to scarring phenotype during wound healing in the pouch young of a marsupial, Monodelphis domestica. Dev Biol 169:242-260
3. Babai F, Musevi-Aghdam J, Schurch W, Royal A, Gabbiani G (1990) Coexpression of alpha-sarcomeric actin, alpha-smooth muscle actin and desmin during myogenesis in rat and mouse embryos I. Skeletal muscle. Differentiation 44:132-142
4. Bandtlow CE, Heumann R, Schwab ME, Thoenen H (1987) Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J 6:891-899
5. Barghorn A, Koslowski M, Kromminga R, Hufnagl P, Tennstedt C, Vogel M (1998) Alpha-smooth muscle actin distribution in the pulmonary vasculature comparing hypoplastic and normal fetal lungs. Pediatr Pathol Lab Med 18:5-22
6. Black MA, Lefebvre F-A, Pope L, Lefebvre YA, Walker P (1992) Thyroid hormone and androgen regulation of nerve growth factor gene expression in the mouse submandibular gland. Mol Cell Endocrinol 84:145-154
7. Broker BJ, Reiter D (1994) Fetal wound healing. Otolaryngol Head Neck Surg 110:547-549
8. Brouty-Boye D, Kolonias D, Savaraj N, Lampidis TJ (1992) α-Smooth muscle actin expression in cultured cardiac fibroblasts of newborn rat. In Vitro Cell Dev Biol 28A:293-296
9. Byers MR, Wheeler EF, Bothwell M (1992) Altered expression of NGF and P75 NGF-receptor by fibroblasts of injured teeth precedes sensory nerve sprouting. Growth Factors 6:41-52
10. Carr RW, Delaney CA, Westerman RA, Roberts RG (1993) Denervation impairs cutaneous microvascular function and blister healing in the rat hindlimb. Neuroreport 4:467-470
11. Cass DL, Bullard KM, Sylvester KG, Yang EY, Longaker MT, Adzick NS (1997) Wound size and gestational age modulate scar formation in fetal wound repair. J Pediatr Surg 32:411-415
12. Charrasse S, Jehan F, Confort C, Brachet P, Clos J (1992) Thyroid hormone promotes transient nerve growth factor synthesis in rat cerebellar neuroblasts. Dev Neurosci 14:282-289
13. Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Statistician 35:124-129
14. Constantinou J, Reynolds ML, Woolf CJ, Safieh-Garabedian B, Fitzgerald M (1994) Nerve growth factor levels in developing rat skin: upregulation following skin wounding. Neuroreport 5:2281-2284
15. Darby I, Skalli O, Gabbiani G (1990) α-Smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63:21-29
16. Darby IA, Bisucci T, Hewitson TD, MacLellan DG (1997) Apoptosis is increased in a model of diabetes-impaired wound healing in genetically diabetic mice. Int J Biochem Cell Biol 29:191-200
17. Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (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
18. Desmoulière A, Gabbiani G (1996) The role of the myofibroblast in wound healing. In: Clark RAF (ed) The molecular and cellular biology of wound repair. Plenum Press, New York, pp 391-423
19. Di Marco E, Marchisio PC, Bondanza S, Franzi AT, Cancedda R, De Luca M (1991) Growth-regulated synthesis and secretion of biologically active nerve growth factor by human keratinocytes. J Biol Chem 266:21718-21722
20. Donohue SJ, Head RJ, Stitzel RE (1989) Elevated nerve growth factor levels in young spontaneously hypertensive rats. Hypertension 14:421-426
21. Dunnick CA, Gibran NS, Heimbach DM (1996) Substance P has a role in neurogenic mediation of human burn wound healing. J Burn Care Rehabil 17:390-396
22. Engin C, Demirkan F, Ayhan S, Atabay K, Baran NK (1996) Delayed effect of denervation on wound contraction in rat skin. Plast Reconstr Surg 98:1063-1067
23. English KB, Harper S, Stayner N, Wang Z-M, Davies AM (1994) 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 344: 470-480
24. Gabbiani G (1996) The cellular derivation and the life span of the myofibroblast. Pathol Res Pract 192:708-711
25. Gerstein AD, Phillips TJ, Rogers GS, Gilchrest BA (1993) Wound healing and aging. Dermatol Clin 11:749-757
26. Greenburg G, Hay ED (1986) Cytodifferentiation and tissue phenotype change during transformation of embryonic lens epithelium to mesenchyme-like cells in vitro. Dev Biol 115:363-379
27. Gressner AM (1996) Transdifferentiation of hepatic stellate cells (Ito cells) to myofibroblasts: a key event in hepatic fibrogenesis. Kidney Int Suppl 54:S39-S45
28. Hautekeete ML, Geerts A (1997) The hepatic stellate (Ito) cell: its role in human liver disease. Virchows Arch 430:195-207
29. Hautmann MB, Madsen CS, Owens GK (1997) A transforming growth factor beta (TGFbeta) control element drives TGFbeta-induced stimulation of smooth muscle alpha-actin gene expression in concert with two CArG elements. J Biol Chem 272:10948-10956
30. Honma M, Koizumi F, Wakaki K, Ochiai H (1995) Co-expression of fibroblastic, histiocytic and smooth muscle cell phenotypes on cultured adherent cells derived from human palatine tonsils: a morphological and immunocytochemical study. Pathol Int 45:903-913
31. Jahoda CA, Reynolds AJ, Chaponnier C, Forester JC, Gabbiani G (1991) Smooth muscle alpha-actin is a marker for hair follicle dermis in vivo and in vitro. J Cell Sci 99:627-636
32. Khalil Z, Helme R (1996) Sensory peptides as neuromodulators of wound healing in aged rats. J Gerontol A Biol Sci Med Sci 51:B354-B361
33. Khalil Z, Ralevic V, Bassirat M, Dusting GJ, Helme RD (1994) Effects of ageing on sensory nerve function in rat skin. Brain Res 641:265-272
34. Khan-Dawood FS, Yusoff DM, Tabibzadeh S (1996) Immunohistochemical analysis of the microanatomy of primate ovary. Biol Reprod 54:734-742
35. Krawisz BR, Florine DL, Scott RE (1981) Differentiation of fibroblast-like cells into macrophages. Cancer Res 41:2891-2899
36. Lewin GR, Mendell LM (1993) Nerve growth factor and nociception. Trends Neurosci 16:353-359
37. Li AK, Koroly MJ, Schattenkerk ME, Malt RA, Young M (1980) Nerve growth factor: acceleration of the rate of wound healing in mice. Proc Natl Acad Sci U S A 77:4379-4381
38. Lindholm D, Castren E, Kiefer R, Zafra F, Thoenen H (1992) Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 117:395-400
39. Little JC, Westgate GE, Evans A, Granger SP (1994) Cytokine gene expression in intact anagen rat hair follicles. J Invest Dermatol 103:715-720
40. Liu M, Warn JD, Fan Q, Smith PG (1999) Relationships between nerves and myofibroblasts during cutaneous wound healing in the developing rat. Cell Tissue Res 297:423-433
41. Lorenz HP, Whitby DJ, Longaker MT, Adzick NS (1993) Fetal wound healing. The ontogeny of scar formation in the non-human primate. Ann Surg 217:391-396
42. Lossing C, Hansson H-A (1993) Peptide growth factors and myofibroblasts in capsules around human breast implants. Plast Recon Surg 91:1277-1286
43. Martin P (1997) Wound healing - aiming for perfect skin regeneration. Science 276:75-81
44. Martin P, Hopkinson-Woolley J, McCluskey J (1992) Growth factors and cutaneous wound repair. Prog Growth Factor Res 4:25-44
45. Martin P, Nobes C, McCluskey J, Lewis J (1994) Repair of excisional wounds in the embryo. Eye 8:155-160
46. Matsuda H, Koyama H, Sato H, Sawada J, Itakura A, Tanaka A, Matsumoto M, Konno K, Ushio H, Matsuda K (1998) Role of nerve growth factor in cutaneous wound healing: accelerating effects in normal and healing-impaired diabetic mice. J Exp Med 187:297-306
47. McHugh KM, Lessard JL (1988) The nucleotide sequence of a rat vascular smooth muscle alpha-actin cDNA. Nucleic Acids Res 16:4167
48. Mearow KM, Kril Y, Diamond J (1993) Increased NGF mRNA expression in denervated rat skin. Neuroreport 4:351-354
49. Nechad M, Ruka E, Thibault J (1994) Production of nerve growth factor by brown fat in culture: relation with the in vivo developmental stage of the tissue. Comp Biochem Physiol 107:381-388
50. Nisoli E, Tonello C, Benarese M, Liberini P, Carruba MO (1996) Expression of nerve growth factor in brown adipose tissue: implications for thermogenesis and obesity. Endocrinology 137:495-503
51. Nistal M, Paniagua R, Abaurrea MA (1982) Varicose axons bearing "synaptic" vesicles on the basal lamina of the human seminiferous tubules. Cell Tissue Res 226:75-82
52. Peled A, Zipori D, Abramsky O, Ovadia H, Shezen E (1991) Expression of alpha-smooth muscle actin in murine bone marrow stromal cells. Blood 78:304-309
53. Pincelli C, Yaar M (1997) Nerve growth factor: its significance in cutaneous biology. J Invest Dermatol Symp Proc 2:31-36
54. Ramm GA, Britton RS, O'Neill R, Kohn HD, Bacon BR (1996) Rat liver ferritin selectively inhibits expression of alpha-smooth muscle actin in cultured rat lipocytes. Am J Physiol 270:G370-G375
55. Raychaudhuri SP, Jiang WY, Farber EM (1998) Psoriatic keratinocytes express high levels of nerve growth factor. Acta Derm Venereol (Stockh) 78:84-86
56. Reynolds M, Alvares D, Middleton J, Fitzgerald M (1997) Neonatally wounded skin induces NGF-independent sensory neurite outgrowth in vitro. Brain Res Dev Brain Res 102:275-283
57. Rush RA (1984) Immunohistochemical localization of endogenous nerve growth factor. Nature 312:364-367
58. Saito H (1990) Innervation of the guinea pig spleen studied by electron microscopy. Am J Anat 189:213-235
59. Schmitt Graff A, Desmouliere A, Gabbiani G (1994) Heterogeneity of myofibroblast phenotypic features: an example of fibroblastic cell plasticity. Virchows Arch 425:3-24
60. Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787-2796
61. Skalli O, Pelte M-F, Peclet M-C, Gabbiani G, Bussolati G, Ravazzola M, Orci L (1989) α-Smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37:315-321
62. Smith PG, Fan Q, Zhang R, Warn JD (1998) Cellular terrain surrounding sympathetic nerve pathways in the rat orbit: comparisons of orbital connective tissue and smooth muscle cell phenotypes. J Comp Neurol 400:529-543
63. Smith PG, Fan Q, Zhang R (1999) Phenotypic divergence of smooth muscle target and sympathetic axon pathway tissues in the orbit of the developing rat. J Comp Neurol 408:352-364
64. Snider WD, McMahon SB (1998) Tackling pain at the source: new ideas about nociceptors. Neuron 20:629-632
65. Sugimoto T, Ueyama H, Hosoi H, Inazawa J, Kato T, Kemshead JT, Reynolds CP, Gown AM, Mine H, Sawada T (1991) Alpha-smooth-muscle actin and desmin expressions in human neuroblastoma cell lines. Int J Cancer 48:277-283
66. Tamm ER, Koch TA, Mayer B, Stefani FH, Lütjen-Drecoll E (1995) Innervation of myofibroblast-like scleral spur cells in human and monkey eyes. Invest Ophthalmol Vis Sci 36:1633-1644
67. Toran-Allerand CD (1996) The estrogen/neurotrophin connection during neural development: is co-localization of estrogen receptors with the neurotrophins and their receptors biologically relevant? Dev Neurosci 18:36-48
68. Tsujino K, Yamate J, Tsukamoto Y, Kumagai D, Kannan Y, Jippo T, Kuwamura M, Kotani T, Takeya M, Sakuma S (1997) Establishment and characterization of cell lines derived from a transplantable rat malignant meningioma: morphological heterogeneity and production of nerve growth factor. Acta Neuropathol (Berl) 93:461-470
69. Tsukamoto H, Hayashibe K, Mishima Y, Ichihashi M (1994) The altered expression of alpha-smooth muscle actin in basal cell epithelioma and its surrounding stroma: with special reference to proliferating cell nuclear antigen expression and adenoid differentiation. Br J Dermatol 130:189-194
70. Uusitalo M, Kivela T (1997) Cell types of secondary cataract: an immunohistochemical analysis with antibodies to cytoskeletal elements and macrophages. Graefes Arch Clin Exp Ophthalmol 235:506-511
71. Vyalov S, Desmoulière A, Gabbiani G (1993) GM-CSF-induced granulation tissue formation: relationships between macrophage and myofibroblast accumulation. Virchows Arch B Cell Pathol 63:231-239
72. Wahl SM, McCartney-Francis N, Allen JB, Dougherty EB, Dougherty SF (1990) Macrophage production of TGF-beta and regulation by TGF-beta. Ann N Y Acad Sci 593:188-196
73. Wheeler EF, Bothwell M (1992) 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 12:930-945
74. White FA, Silos-Santiago I, Molliver DC, Nishimura M, Phillips H, Barbacid M, Snider WD (1996) Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J Neurosci 16:4662-4672
75. Woodcock-Mitchell J, Mitchell JJ, Low RB, Kieny M, Sengel P, Rubbia L, Skalli O, Jackson B, Gabbiani G (1988) Alpha-smooth muscle actin is transiently expressed in embryonic rat cardiac and skeletal muscles. Differentiation 39:161-166
76. Yamate J, Iwaki M, Kumagai D, Tsukamoto Y, Kuwamura M, Nakatsuji S, Tsunenari I, Kotani T, Sakuma S (1997) Characteristics of a rat fibrosarcoma-derived transplantable tumour line (SS) and cultured cell lines (SS-P and SS-A3-1) showing myofibroblastic and histiocytic phenotypes. Virchows Arch 431:431-440
77. Young WJ, Smith SM, Chang C (1997) Induction of the intronic enhancer of the human ciliary neurotrophic factor receptor (CNTFRalpha) gene by the TR4 orphan receptor. A member of steroid receptor superfamily. J Biol Chem 272:3109-3116
78. Zettler C, Rush RA (1993) Elevated concentrations of nerve growth factor in heart and mesenteric arteries of spontaneously hypertensive rats. Brain Res 614:15-20