Expression of heat shock proteins in mouse skin during wound healing

Journal of Histochemistry and Cytochemistry

Volumn 46, Issue 11, 1998, Pages 1291-1301

  Laplante, Alain F ^a   Moulin, Véronique ^a   Auger, François A ^a   Landry, Jacques ^a   Li, Hui ^a   Morrow, Geneviève ^b   Tanguay, Robert M ^b   Germain, Lucie ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Epidermis; Heat shock proteins; Immunohistochemistry; Keratin; Keratinocytes; Mice; Molecular chaperones; Skin; Wound healing

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; KERATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EPITHELIZATION; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; SKIN INJURY; WOUND HEALING;

ANIMALIA;

EID: 0031793192     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215549804601109     Document Type: Article

References (81)

1. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269:20780-20784
2. Bennett NT, Schultz GS (1993) Growth factors and wound healing: biochemical properties of growth factors and their receptors. Am J Surg 165:728-737
3. Biggiogera M, Tanguay RM, Marin R, Wu Y, Martin TE, Fakan S (1996) Localization of heat shock proteins in mouse male germ cells: an immunoelectron microscopical study. Exp Cell Res 229:77-85
4. Boehncke WH, Dahlke A, Zollner TM, Sterry W (1994) Differential expression of heat shock protein 70 (HSP70) and heat shock cognate protein 70 (HSC70) in human epidermis. Arch Dermatol Res 287:68-71
5. Bramanti TE, Dekker NP, Lozada Nur F, Sauk JJ, Regezi JA (1995) Heat shock (stress) proteins and gamma delta T lymphocytes in oral lichen planus. Oral Surg Oral Med Oral Pathol Oral Radiol Endo 80:698-704
6. Buck RC (1979) Cell migration in repair of mouse corneal epithelium. Invest Ophthalmol Vis Sci 18:767-784
7. Charveron M, Calvo M, Gall Y (1995) Cell stress and implications of the heat-shock response in skin. Cell Biol Toxicol 11:161-165
8. Ciocca DR, Oesterreich S, Chamness GC, McGuire WL, Fuqua SAW (1993) Biological and clinical implications of heat shock protein 27 000 (Hsp27): a review. J Natl Cancer Inst 85:1558-1570
9. Clark RAF (1985) Cutaneous tissue repair: basic biologic considerations. I. J Am Acad Dermatol 13:701-725
10. Clark RAF (1993) Biology of dermal wound repair. Dermatol Clin 11:647-666
11. Craig EA, Weissman JS, Horwich AL (1994) Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78:365-372
12. Croft CB, Tarin D (1970) Ultrastructural studies of wound healing in mouse skin. I. Epithelial behavior. J Anat 106:63-77
13. DiPasquale A (1975) Locomotion of epithelial cells. Exp Cell Res 95:425-139
14. Edwards MJ, Marks R, Dykes PJ, Merrett VR, Morgan HE, O'Donovan MR (1991) Heat shock proteins in cultured human keratinocytes and fibroblasts. J Invest Dermatol 96:392-396
15. Elstner EF (1991) Oxygen radicals - biochemical basis for their efficacy. Klin Wochenschr 69:949-956
16. Frydman J, Nimmesgern E, Ohtsuka K, Hartl FU (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370:111-117
17. Fuchs E (1993) Epidermal differentiation and keratin gene expression. J Cell Sci Suppl 17:197-208
18. Gandour Edwards R, McClaren M, Isseroff RR (1994) Immunolocalization of low-molecular-weight stress protein HSP 27 in normal skin and common cutaneous lesions. Am J Dermatopathol 16:504-509
19. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33-45
20. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110:357-368
21. Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349-384
22. Holbrook KA, Wolff K (1987) The structure and development of skin. In Fitzpatrick TB, Eisen AZ, Wolff K, Freedberg IM, Austen KF, eds. Dermatology in General Medicine. 3rd ed. New York, McGraw-Hill, 93-131
23. Holland DB, Roberts SG, Wood EJ, Cunliffe WJ (1993) Cold shock induces the synthesis of stress proteins in human keratinocytes. J Invest Dermatol 101:196-199
24. Horwich AL, Willison KR (1993) Protein folding in the cell: functions of two families of molecular chaperone, hsp 60 and TF55-TCPl. Phil Trans R Soc Lond [B] 339:313-326
25. Hunt TK, Hussain Z (1992) Wound microenvironment. In Cohen KI, Diegelmann RF, Lindblad WJ, eds. Wound Healing, Biochemical & Clinical Aspects. 1st ed. Philadelphia, WB Saunders, 274-281
26. Huot J, Houle F, Marceau F, Landry J (1997) Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80:383-392
27. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (1995) Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur J Biochem 227:416-427
28. Hutchison KA, Dittmar KD, Czar MJ, Pratt WB (1994) Proof that hsp70 is required for assembly of the glucocorticoid receptor into a heterocomplex with hsp90. J Biol Chem 269:5043-5049
29. Jerome V, Leger J, Devin J, Baulieu EE, Catelli MG (1991) Growth factors acting via tyrosine kinase receptors induce HSP90 alpha gene expression. Growth Factors 4:317-327
30. Jiang CK, Magnaldo T, Ohtsuki M, Freedberg IM, Bernerd F, Blumenberg M (1993) Epidermal growth factor and transforming growth factor α specifically induce the activation- and hyperproliferation-associated keratins 6 and 16. Proc Natl Acad Sci USA 90:6786-6790
31. Kampinga HH (1993) Thermotolerance in mammalian cells: protein denaturation and aggregation, and stress proteins. J Cell Sci 104:11-17
32. Kiritsy CP, Lynch SE (1993) Role of growth factors in cutaneous wound healing: a review. Crit Rev Oral Biol Med 4:729-760
33. Kirsner RS, Eaglstein WH (1993) The wound healing process. Dermatol Clin 11:629-640
34. Krawczyk W (1971) A pattern of epidermal cell migration during wound healing. J Cell Biol 49:247-263
35. 4. Nature 227:680-685
36. Landry J, Huot J (1995) Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27. Biochem Cell Biol 73:703-707
37. Langer T, Neupert W (1991) Heat shock proteins hsp60 and hsp70: their roles in folding, assembly and membrane translocation of proteins. Curr Top Microbiol Immunol 167:3-30
38. Lavoie JN, Hickey E, Weber LA, Landry J (1993) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268:24210-24214
39. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15:505-516
40. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631-677
41. Mansbridge JN, Knapp AM (1987) Changes in keratinocyte maturation during wound healing. J Invest Dermatol 89:253-263
42. Maytin EV (1995) Heat shock proteins and molecular chaperones: implications for adaptive responses in the skin. J Invest Dermatol 104:448-455
43. Maytin EV, Wimberly JM, Anderson RR (1990) Thermotolerance and the heat shock response in normal human keratinocytes in culture. J Invest Dermatol 95:635-642
44. McClaren M, Isseroff RR (1994) Dynamic changes in intracellular localization and isoforms of the 27-kDa stress protein in human keratinocytes. J Invest Dermatol 102:375-381
45. McLaughlin MM, Kumar S, McDonnell PC, Van Horn S, Lee JC, Livi GP, Young PR (1996) Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J Biol Chem 271:8488-8492
46. Michel M, Török N, Godbout M-J, Lussier M, Gaudreau P, Royal A, Germain L (1996) Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage. J Cell Sci 109:1017-1028
47. Minowada G, Welch W (1995a) Variation in the expression and/or phosphorylation of the human low molecular weight stress protein during in vitro cell differentiation. J Biol Chem 270:7047-7054
48. Minowada G, Welch WJ (1995b) Clinical implications of the stress response. J Clin Invest 95:3-12
49. Moll R, Franke WW, Volc-Platzer B, Krepier R (1982) Different keratin polypeptides in epidermis and other epithelia of human skin: a specific cytokeratin of molecular weight 46,000 in epithelia of the pilosebaceous tract and basal cell epitheliomas. J Cell Biol 95:285-295
50. Morcillo G, Diez JL, Carbajal ME, Tanguay RM (1993) HSP90 associates with specific heat shock puffs (hsrω) in polytene chromosomes of Drosophila and Chironomus. Chromosoma 102: 648-659
51. Moulin V (1995) Growth factors in skin wound healing. Eur J Cell Biol 68:1-7
52. Moulin V, Auger FA, O'Connor-McCourt M, Germain L (1997) Fetal and postnatal sera differentially modulate human dermal fibroblast phenotypic and functional features in vitro. J Cell Physiol 171:1-10
53. Muramatsu T, Tada H, Kobayashi N, Yamji M, Shirai T, Ohnishi T (1992) Induction of the 72-kD heat shock protein in organ-cultured normal human skin. J Invest Dermatol 98:786-790
54. Odland G, Ross R (1968) Human wound repair. I. Epidermal regeneration. J Cell Biol 39:135-151
55. Oksala O, Salo T, Tammi R, Hakkinen L, Jalkanen M, Inki P, Larjava H (1995) Expression of proteoglycans and hyaluronan during wound healing. J Histochem Cytochem 43:125-135
56. Ordman LJ, Gillman T (1966) Studies in the healing of cutaneous wounds. I. The healing of incisions through the skin of pigs. Arch Surg 93:857-882
57. Ortonne JP, Loning T, Schmitt D (1981) Immunomorphological and ultrastructural aspects of keratinocyte migration in epidermal wound healing. Virchows Arch 392:217-230
58. Paladini RD, Takahashi K, Bravo NS, Coulombe PA (1996) Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J Cell Biol 132:381-397
59. Pang SC, Daniels WH, Buck RC (1978) Epidermal migration during the healing of suction blisters in rat skin: a scanning and transmission electron microscopic study. Am J Anat 153:177-191
60. Pawar S, Kartha S, Toback FG (1995) Differential gene expression in migrating renal epithelial cells after wounding. J Cell Physiol 165:556-565
61. Pratt WB (1993) The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J Biol Chem 268:21455-21458
62. Radice G (1980) The spreading of epithelial cells during wound closure in Xenopus larvae. Dev Biol 76:26-46
63. Ritossa CF (1962) A new puffing pattern induced by heat shock and DNP in Drosophila. Experientia 18:571-573
64. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda AR (1994) A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78:963-972
65. Rousseau S, Houle F, Landry J, Huot J (1997) p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15:2169-2178
66. Schermer A, Jester JV, Hardy C, Milano D, Sun TT (1989) Transient synthesis of K6 and K16 keratins in regenerating rabbit corneal epithelium: keratin markers for an alternative pathway of keratinocyte differentiation. Differentiation 42:103-110
67. Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265: 12111-12114
68. Shinoda H, Huang CC (1996) Heat shock proteins in middle ear cholesteatoma. Otolaryngol Head Neck Surg 114:77-83
69. Stark HJ, Breitkreutz D, Limat A, Bowden P, Fusenig NE (1987) Keratins of the human hair follicle: "hyperproliferative" keratins consistently expressed in outer root sheath cells in vivo and in vitro. Differentiation 35:236-248
70. Stenn KS, Malhotra R (1992) Epithelialization. In Cohen KI, Diegelmann RF, Lindblad WJ, eds. Wound Healing, Biochemical & Clinical Aspects. 1st ed. Philadelphia, WB Saunders, 115-127
71. Tanguay RM, Wu Y, Khandjian EW (1993) Tissue-specific expression of heat shock proteins of the mouse in the absence of stress. Dev Genet 14:112-118
72. Tarin D, Croft CB (1970) Ultrastructural studies of wound healing in mouse skin. II. Dermo-epidermal interrelationships. J Anat 106:79-91
73. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354
74. Trautinger F, Kindas-Mügge I, Dekrout B, Knobler RM, Metze D (1995) Expression of the 27-kDa heat shock protein in human epidermis and in epidermal neoplasms: an immunohistological study. Br J Dermatol 133:194-202
75. Trautinger F, Trautinger I, Kindas-Mugge I, Metze D, Luger TA (1993) Human keratinocytes in vivo and in vitro constitutively express the 72-kD heat shock protein. J Invest Dermatol 101:334-338
76. Tyner AL, Fuchs E (1986) Evidence for posttranscriptional regulation of the keratins expressed during hyperproliferation and malignant transformation in human epidermis. J Cell Biol 103:1945-1955
77. Vaughan RB, Trinkaus JP (1966) Movements of epithelial cell sheets in vitro. J Cell Sci 1:407-413
78. Wahl LM, Wahl SM (1992) Inflammation. In Cohen KI, Diegelmann RF, Lindblad WJ, eds. Wound Healing, Biochemical & Clinical Aspects. 1st ed. Philadelphia, WB Saunders, 40-62
79. Weiss RA, Eichner R, Sun TT (1984) Monoclonal antibody analysis of keratin expression in epidermal diseases: a 48- and 56-kdalton keratin as molecular markers for hyperproliferative keratinocytes. J Cell Biol 98:1397-1406
80. Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72:1063-1081
81. Winter GD (1972) Epidermal regeneration studied in domestic pig. In Maibach HI, Rovee DT, eds. Epidermal Wound Healing. 1st ed. Chicago, Year Book Medical Publishing, 71-113