Immunolocalization of tenascin-C, α9 integrin subunit, and αvβ6 integrin during wound healing in human oral mucosa

Journal of Histochemistry and Cytochemistry

Volumn 48, Issue 7, 2000, Pages 985-998

  Häkkinen, Lari ^a   Hildebrand, H Christopher ^a   Berndt, Alexander ^b   Kosmehl, Hartwig ^b   Larjava, Hannu ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Integrins; Tenascin C; Wound repair

Indexed keywords

INTEGRIN; TENASCIN;

ARTICLE; CELL INTERACTION; CELL MIGRATION; HUMAN; HUMAN TISSUE; MOUTH MUCOSA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; WOUND HEALING;

EID: 0343090477     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215540004800712     Document Type: Article

References (66)

1. Aukhil I, Sahlberg C, Thesleff I (1996) Basal layer of epithelium expresses tenascin mRNA during healing of incisional skin wounds. J Periodont Res 31:105-112
2. Balza E, Siri A, Ponassi M, Caocci F, Linnala A, Virtanen I, Zardi L (1993) Production and characterization of monoclonal antibodies specific for different epitopes of human tenascin. FEBS Lett 332:39-43
3. Borsi L, Balza E, Castellani P, Carnemolla B, Ponassi M, Querze G, Zardi L (1994) Cell-cycle dependent alternative splicing of the tenascin primary transcript. Cell Adhes Commun 1:307-317
4. Borsi L, Carnemolla B, Nicolo C, Spina B, Tanara G, Zardi L (1992) Expression of different tenascin isoforms in normal, hyperplastic and neoplastic breast tissues. Int J Cancer 52:688-692
5. Brakebusch C, Hirsch E, Potocnik A, Fassler R (1997) Genetic analysis of beta 1 integrin function: confirmed, new and revised roles for crucial family of cell adhesion molecules. J Cell Sci 110: 2895-2904
6. Breuss JM, Gallo J, DeLisser HM, Klimanskaya IV, Folkesson HG, Pittet JF, Nishimura SL, Aldape K, Landers DV, Carpenter W, Gillett N, Sheppard D, Matthay MA, Abelda SM, Kramer RH, Pytela R (1995) Expression of the β6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodelling. J Cell Sci 108:2241-2251
7. Camper L, Hellman U, Lundgren-Akerlund E (1998) Isolation, cloning, and sequence analysis of the integrin subunit α10, a β1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem 273:20383-20389
8. Chiquet-Ehrismann R, Hagios C, Schenk S (1995) The complexity in regulating the expression of tenascin. BioEssays 17:873-878
9. Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131-139
10. Chiquet-Ehrismann R, Matsuoka Y, Hofer U, Spring J, Bernasconi C, Chiquet M (1991) Tenascin variants: differential binding to fibronectin and distinct distribution in cell cultures and tissues. Cell Regul 2:927-938
11. Chiquet-Ehrismann R, Tannheimer M, Koch M, Brunner A, Spring J, Martin D, Baumgartner S, Chiquet M (1994) Tenascin-C expression by fibroblasts is elevated in stressed collagen gels. J Cell Biol 127:2093-2101
12. Chuong C-M, Chen H-M (1991) Enhanced expression of neural cell adhesion molecules and tenascin (cytotactin) during wound healing. Am J Pathol 138:427-440
13. Clark RAF (1993) Regulation of fibroplasia in cutaneous wound repair. Am J Med Sci 306:42-48
14. Crossin KL (1996) Tenascin: a multifunctional extracellular matrix protein with a restricted distribution in development and disease. J Cell Biochem 61:592-598
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. Desloges N, Basora N, Perrault N, Bouarrouss Y, Sheppard D, Beaulieu J-F (1998) Regulated expression of the integrin α9β1 in the epithelium of the developing human gut and in intestinal cell lines: relation with cell proliferation. J Cell Biochem 71:536-545
17. End P, Panayotou G, Entwistle A, Waterfield MD, Chiquet M (1992) Tenascin: a modulator of cell growth. Eur J Biochem 209:1041-1051
18. Fisher D, Brown-Ludi M, Schulthess T, Chiquet-Ehrismann R (1997a) Concerted action of tenascin-C domains in cell adhesion, anti-adhesion and promotion of neurite growth. J Cell Sci 110:1513-1522
19. Fisher D, Tucker RP, Chiquet-Ehrismann R, Adams JC: (1997b) Cell-adhesive responses to tenascin-C splice variants involve formation of fascin microspikes. Mol Biol Cell 8:2055-2057
20. Haapasalmi K, Zhang K, Tonnesen M, Olerud J, Sheppard D, Salo T, Kramer R, Clark RA, Uitto VJ, Larjava H (1996) Keratinocytes in human wounds express αvβ6 integrin. J Invest Dermatol 106:42-48
21. Hertle MD, Kubler MD, Leigh IM, Watt FM (1992) Aberrant integrin expression during epidermal wound healing and in psoriatic epidermis. J Clin Invest 89:1892-1901
22. Huang XZ, Wu JF, Cass D, Erle DJ, Corry D, Young SG, Farese RV Jr, Sheppard D (1996) Inactivation of the integrin β6 gene reveals a role of epithelial integrins in regulating inflammation in the lungs and skin. J Cell Biol 133:921-928
23. Huang X, Wu J, Zhu W, Pytela R, Sheppard D (1998) Expression of the human integrin β6 subunit in alveolar type II cells and bronchiolar epithelial cells reverses lung inflammation in β6 knock out mice. Am J Respir Cell Mol Biol 19:636-642
24. Jones J, Sugiyama M, Watt FM, Speight PM (1993) Integrin expression in normal, hyperplastic, dysplastic, and malignant oral epithelium. J Pathol 169:235-243
25. Jones J, Watt FM, Speight PM (1997) Changes in the expression of alpha v integrins in oral squamous cell carcinomas. Oral Pathol Med 26:63-68
26. Jones PH, Harper S, Watt FM (1995) Stem cell patterning and fate in human epidermis. Cell 80:83-93
27. Juhasz I, Murphy GF, Yan HC, Herlyn M, Albelda SM (1993) Regulation of extracellular matrix proteins and integrin cell substratum adhesion receptors on epithelium during cutaneous human wound healing in vivo. AmJ Pathol 143:1458-1469
28. Kaplony A, Zimmermann DR, Fisher RW, Imhof BA, Odermatt BF, Winterhalter KH, Vaughan L (1991) Tenascin Mr 220,000 isoform expression correlates with conical cell migration. Development 112:605-614
29. Katz BZ, Yamada KM (1997) Integrins in morphogenesis and signaling. Biochimie 79:467-476
30. Kruse J, Keihauer G, Faissner A, Timpl R, Scharchner M (1985) The Jl glycoprotein: a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature 316:146-148
31. Larjava H, Salo T, Haapasalmi K, Kramer RH, Heino J (1993) Expression of integrins and basement membrane components by wound keratinocytes. J Clin Invest 92:1425-1435
32. Latijnhouwers MA, Bergers M, Ponec M, Dijkman H, Andriessen M, Schalkwijk J (1997) Human epidermal keratinocytes are a source of tenascin-C during wound healing. J Invest Dermatol 108:776-783
33. Latijnhouwers MA, Bergers M, Van Bergen BH, Spruijt Kl, Andriessen MP, Schalkwiljk J (1996) Tenascin expression during wound healing in human skin. J Pathol 178:30-35
34. Lukinmaa P-L, Allemanni G, Waltimo J, Zardi L (1996) Immunoreactivity of renascin-C in dentin matrix in denrinogenesis imperfecta associated with osteogenesis imperfecta. J Dent Res 75: .581-587
35. Luomanen M, Virtanen I (1993) Distribution of tenascin in healing incision, excision and laser wounds. J Oral Pathol Med 22:41-45
36. Mackie EJ, Halfter W, Liveram D (1988) Induction of tenascin in healing wounds. J Cell Biol 107:2757-2767
37. Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is assodated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569-2579
38. Matsuoka Y, Spring J, Ballmer-Hofer K, Chiquet-Ehrismann R (1990) Differential expression of tenascin splicing variants in the chick gizzard and in cell cultures. Cell Differ Dev 32:417-424
39. Mighell AJ, Thompson J, Hume WJ, Markham AF, Robinson PA (1997) Human tenascin-C: identification of a novel type III repeat in oral cancer and of novel splice variants in normal, malignant and reactive oral mucosae. Int J Cancer 72:236-240
40. Moles J-P, Watt FM (1997) The epidermal stem cell compartment: variation in expression levels of E-cadherin and catenins within the hasal layer of human epidermis. J Histochem Cytochem 45: 867-874
41. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Gart C, Matthay MA, Rifkin DB, Sheppard D (1999) The integrin alpha v beta 6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319-328
42. Murphy-Ullrich JE, Lightner VA, Aukhil I, Yan YZ, Erickson HP, Hook M (1991) Focal adhesion integrity is downregulated by the alternatively spliced domain of human tenascin. J Cell Biol 115: 1127-1136
43. Palmer EL, Ruegg C, Ferrando R, Pytela R, Sheppard D (1993) Sequence and tissue distribution of the integrin α9 subunit, a novel partner of ßl that is widely distributed in epithelia and muscle. J Cell Biol 123:1289-1297
44. Phillips GR, Krushcl LA, Crossin KL (1998) Domains of tenascin involved in glioma migration. J Cell Sei 111:1095-1104
45. Prieto AL, Andersson-Fisone C, Crossin KL (1992) Characterization of multiple adhesive and counteradhesive domains in the extracellular matrix protein cytotactin. J Cell Biol 119:663-678
46. Prieto AL, Jones FS, Cunningham, BA, Crossin KL, Edelman GM (1990) Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization. J Cell Biol 111:685-698
47. Przepiorka D, Myerson D (1986) A single-step silver enhancement method permitting rapid diagnosis of cytomegalovirus infection in formalin-fixed, paraffin-embedded tissue sections by in situ hybridization and immunoperoxidase detection. J Histochem Cytochem 34:1731-1734
48. Puchtler H, Sweat F, Doss NO (1963) A one-hour phosphotungstic acid-hematoxylin stain. AmJ Clin Pathol 40:334-337
49. Ramos DM, Chen BL, Boylen K, Stern M, Kramer RH, Sheppard D, Nishimura SL, Greenspan D, Zardi L, Pytela R (1997) Stromal fibroblasts influence oral squamous-cell carcinoma cell interactions with tenascin-C. Int J Cancer 74:369-376
50. Rettig WJ, Erickson HP, Albino AP, Garin-Chesa P (1994) Induction of human tenascin (neuronectin) by growth factors and cytokines: cell type-specific signals and signaling pathways. J Cell Sei 107:487-497
51. Rikimaru K, Moles J-P, Watt FM (1997) Correlation between hyperproliferation and suprahasal integrin expression in human epidermis reconstituted in culture. Exp Dermatol 6:214-221
52. Rowat JS, Squier CA (1986) Rates of epithelial cell proliferation in the oral mucosa and skin of the Tamarin monkey (Saguinus fuscicollis). J Dent Res 65:1326-1331
53. Schenk S, Bruckner-Tuderman L, Chiquet-Ehrismann R (1995) Dermo-epidermal separation is associated with induced tenascin expression in human skin. Br J Dermatol 133:13-22
54. Siri A, Carnemolla B, Saginati M, Leprini A, Casari G, Barella F, Zardi L (1991) Human tenascin primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res 19:525-531
55. Stepp MA, Zhu L (1997) Upregulation of a9 integrin and tenascin during epithelial regeneration after debridement in the cornea. J Histochem Cytochem 45: 189-201
56. Srepp MA, Zhu L, Sheppard D, Cranfill RL (1995) Localized distribution of α9 integrin in the cornea and changes in expression during corneal epithelial cell differentiation. J Histochem Cytochem 43:353-362
57. Taooka Y, Chen J, Yednock T, Sheppard D (1999) The integrin α9β1 mediates adhesion to activated endothelial cells and transendothelial neutrophil migration through interaction with vascular cell adhesion molecule-1. J Cell Biol 145:413-420
58. Thorup AK, Dabelsteen E, Schou S, Gil SG, Carter WG, Reibel J (1997) Differential expression of integrins and laminin-5 in normal oral epithelia. APMIS 105:519-530
59. Tucker RP, Hammarback JA, Jenrath DA, Mackie EJ, Xu Y (1993) Tenascin expression in the mouse: in situ localization and induction in vitro by bFGF. J Cell Sci 104:69-76
60. Wang A, Patrone L, McDonald JA, Sheppard D (1995) Expression of the integrin subunit α9 in the murine embryo. Dev Dyn 204:421-431
61. Weinacker A, Chen A, Agrez M, Cone RI, Nishimura S, Wayner E, Pytela R, Sheppard D (1994) Role of integrin αvβ6 in cell attachment to fibronectin: heterologous expression of intact and secreted forms of the receptor. J Biol Chem 269:6940-6948
62. Whitby DJ, Longaker MT, Harrison MR, Adzick NS, Ferguson MWJ (1991) Rapid epithelialization of fetal wounds is associated with the early deposition of tenascin. J Cell Sci 99:583-586
63. Yokosaki Y, Matsuura N, Higashiyama S, Murakami I, Obara M, Yamakido M, Shigeto N, Chen J, Sheppard D (1998) Identification of the ligand binding site for the integrin α9β1 in the third fibronectin type III repeat of tenascin-C. J Biol Chem 273: 11423-11428
64. Yokosaki Y, Monis H, Chen J, Sheppard J (1996) Differential effects of the integrins α9β1, αvβ3, and αvβ6 on cell proliferative responses to tenascin. J Biol Chem 271:24144-24150
65. Yokosaki Y, Palmer EL, Prieto AL, Crossin KL, Bourdon MA, Pytela R, Sheppard D (1994) The integrin α9β1 mediates cell attachment to a non-RGD site in the third fibronectin type III repeat of tenascin. J Biol Chem 269:26691-26696
66. Zhao Y, Young SL (1995) TGF-beta regulates expression of tenascin alternative-splicing isoforms in fetal lung. Am J Physiol 268: L173-180