Synergistic control of keratinocyte adhesion through muscarinic and nicotinic acetylcholine receptor subtypes

Experimental Cell Research

Volumn 294, Issue 2, 2004, Pages 534-549

  Nguyen, Vu Thuong ^a   Chernyavsky, Alexander I ^a   Arredondo, Juan ^a   Bercovich, Dani ^b,c   Orr Urtreger, Avi ^d   Vetter, Douglas E ^e   Wess, Jürgen ^f   Beaudet, Arthur L ^b   Kitajima, Yasuo ^g   Grando, Sergei A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c MIGAL GALILEE TECHNOLOGY CENTER   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^g GIFU UNIVERSITY   (Japan)

Author keywords

E cadherin; Intercellular adhesion; Keratinocytes; Muscarinic cholinergic receptors M3; Nicotinic cholinergic receptors 3 and 9; and catenins

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BETA CATENIN; CHOLINERGIC RECEPTOR; MUSCARINIC M3 RECEPTOR; PLAKOGLOBIN; RECEPTOR SUBTYPE; UVOMORULIN;

ARTICLE; CELL ANCHORAGE; CELL INTERACTION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; RECEPTOR INTRINSIC ACTIVITY; SQUAMOUS EPITHELIUM;

EID: 12144287746     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.12.010     Document Type: Article

References (98)

1. Kowalczyk A.P., Bornslaeger E.A., Norvell S.M., Palka H.L., Green K.J. Desmosomes: intercellular adhesive junctions specialized for attachment of intermediate filaments. Int. Rev. Cytol. 185:1999;237-302.
2. Vasioukhin V., Fuchs E. Actin dynamics and cell-cell adhesion in epithelia. Curr. Opin. Cell Biol. 13:2001;76-84.
3. Mueller H., Franke W.W. Biochemical and immunological characterization of desmoplakins I and II, the major polypeptides of the desmosomal plaque. J. Mol. Biol. 163:1983;647-671.
4. Junctional complexes of epithelial cells. Ciba Found. Symp. 125 (1987) 1-284.
5. Parrish E.P., Marston J.E., Mattey D.L., Measures H.R., Venning R., Garrod D.R. Size heterogeneity, phosphorylation and transmembrane organisation of desmosomal glycoproteins 2 and 3 (desmocollins) in MDCK cells. J. Cell. Sci. 96:1990;239-248.
6. Stappenbeck T.S., Lamb J.A., Corcoran C.M., Green K.J. Phosphorylation of the desmoplakin COOH terminus negatively regulates its interaction with keratin intermediate filament networks. J. Biol. Chem. 269:1994;29351-29354.
7. Pasdar M., Li Z., Chan H. Desmosome assembly and disassembly are regulated by reversible protein phosphorylation in cultured epithelial cells. Cell Motil. Cytoskelet. 30:1995;108-121.
8. Behrens J., Vakaet L., Friis R., Winterhager E., Van Roy F., Mareel M.M., Birchmeier W. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120:1993;757-766.
9. Volberg T., Zick Y., Dror R., Sabanay I., Gilon C., Levitzki A., Geiger B. The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions. EMBO J. 11:1992;1733-1742.
10. Aoyama Y., Owada M.K., Kitajima Y. A pathogenic autoantibody, pemphigus vulgaris-IgG, induces phosphorylation of desmoglein 3, and its dissociation from plakoglobin in cultured keratinocytes. Eur. J. Immunol. 29:1999;2233-2240.
11. Mignogna M.D., Pannone G., Lo Muzio L., Staibano S., Bucci E. Catenin dislocation in oral pemphigus vulgaris. J. Oral Pathol. & Med. 30:2001;268-274.
12. Jamora C., Fuchs E. Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4:2002;E101-E108.
13. Munshi H.G., Ghosh S., Mukhopadhyay S., Wu Y.I., Sen R., Green K.J., Stack M.S. Proteinase suppression by E-cadherin-mediated cell-cell attachment in premalignant oral keratinocytes. J. Biol. Chem. 277:2002;38159-38167.
14. Bhowmick N.A., Ghiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E., Arteaga C.L., Moses H.L. Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell. 12:2001;27-36.
15. Grando S.A., Dahl M.V. Activation of keratinocyte muscarinic acetylcholine receptors reverses pemphigus acantholysis. J. Eur. Acad. Dermatol. Venereol. 2:1993;72-86.
16. Grando S.A., Horton R.M., Pereira E.F.R., Diethelm-Okita B.M., George P.M., Albuquerque E.X., Conti-Fine B.M. A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes. J. Invest. Dermatol. 105:1995;774-781.
17. Grando S.A. Biological functions of keratinocyte cholinergic receptors. J. Investig. Dermatol. Symp. Proc. 2:1997;41-48.
18. Wessler I., Kirkpatrick C.J., Racke K. Non-neuronal acetylcholine, a locally acting molecule, widely distributed in biological systems: expression and function in humans. Pharmacol. Ther. 77:1998;59-79.
19. Kawashima K., Fujii T. Extraneuronal cholinergic system in lymphocytes. Pharmacol. Ther. 86:2000;29-48.
20. Grando S.A., Kawashima K., Wessler I. The non-neuronal cholinergic system in humans. Life Sci. 72:2003;2009-2012.
21. Grando S.A., Horton R.M. The keratinocyte cholinergic system with acetylcholine as an epidermal cytotransmitter. Curr. Opin. Dermatol. 4:1997;262-268.
22. Grando S.A., Kist D.A., Qi M., Dahl M.V. Human keratinocytes synthesize, secrete and degrade acetylcholine. J. Invest. Dermatol. 101:1993;32-36.
23. Klapproth H., Reinheimer T., Metzen J., Munch M., Bittinger F., Kirkpatrick C.J., Hohle K.D., Schemann M., Racke K., Wessler I. Non-neuronal acetylcholine, a signalling molecule synthezised by surface cells of rat and man. Arch. Pharmacol. 355:1997;515-523.
24. Grando S.A., Zelickson B.D., Kist D.A., Weinshenker D., Bigliardi P.L., Wendelschafer-Crabb G., Kennedy W.R., Dahl M.V. Keratinocyte muscarinic acetylcholine receptors: immunolocalization and partial characterization. J. Invest. Dermatol. 104:1995;95-100.
25. Nguyen V.T., Ndoye A., Grando S.A. Novel human α9 acetylcholine receptor regulating keratinocyte adhesion is targeted by pemphigus vulgaris autoimmunity. Am. J. Pathol. 157:2000;1377-1391.
26. Grando S.A. Receptor-mediated action of nicotine in human skin. Int. J. Dermatol. 40:2001;691-693.
27. Ndoye A., Buchli R., Greenberg B., Nguyen V.T., Zia S., Rodriguez J.G., Webber R.J., Lawry M.A., Grando S.A. Identification and mapping of keratinocyte muscarinic acetylcholine receptor subtypes in human epidermis. J. Invest. Dermatol. 111:1998;410-416.
28. Williams C.L., Hayes V.Y., Hummel A.M., Tarara J.E., Halsey T.J. Regulation of E cadherin-mediated adhesion by muscarinic acetylcholine receptors in small cell lung carcinoma. J. Cell Biol. 121:1993;643-654.
29. Zia S., Ndoye A., Nguyen V.T., Grando S.A. Nicotine enhances expression of the α3, α4, α5, and α7 nicotinic receptors modulating calcium metabolism and regulating adhesion and motility of respiratory epithelial cells. Res. Commun. Mol. Pathol. Pharmacol. 97:1997;243-262.
30. Shafer S.H., Puhl H.L., Phelps S.H., Williams C.L. Activation of transfected M1 or M3 muscarinic acetylcholine receptors induces cell-cell adhesion of Chinese hamster ovary cells expressing endogenous cadherins. Exp. Cell Res. 248:1999;148-159.
31. Conroy W.G., Ogden L.F., Berg D.K. Cluster formation of α7-containing nicotinic receptors at interneuronal interfaces in cell culture. Neuropharmacology. 39:2000;2699-2705.
32. Mihovilovic M., Butterworth-Robinette J. Thymic epithelial cell line expresses transcripts encoding alpha-3, alpha-5 and beta-4 subunits of acetylcholine receptors, responds to cholinergic agents and expresses choline acetyl transferase. An in vitro system to investigate thymic cholinergic mechanisms. J. Neuroimmunol. 117:2001;58-67.
33. Dajas-Bailador F.A., Soliakov L., Wonnacott S. Nicotine activates the extracellular signal-regulated kinase 1/2 via the α7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J. Neurochem. 80:2002;520-530.
34. Nakayama H., Numakawa T., Ikeuchi T., Hatanaka H. Nicotine-induced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells. J. Neurochem. 79:2001;489-498.
35. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T., Akaike A. α7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A β-amyloid-induced neurotoxicity. J. Biol. Chem. 276:2001;13541-13546.
36. Brown J.H., McDonough P.M. Muscarinic cholinergic receptor regulation of inositol phospholipid metabolism and calcium mobilization. Brown J.H. The Muscarinic Receptors. 1989;259-308 Humana Press, Clifton.
37. Gusovsky F., Lueders J.E., Kohn E.C., Felder C.C. Muscarinic receptor-mediated tyrosine phosphorylation of phospholipase C-γ. An alternative mechanism for cholinergic-induced phosphoinositide breakdown. J. Biol. Chem. 268:1993;7768-7772.
38. Zheng J.Q., Felder M., Poo M.M. Turning of nerve growth cones induced by neurotransmitters. Nature. 368:1994;140-144.
39. Grando S.A., George P.M., Dahl M.V., Conti-Tronconi B.M. Antibody against keratinocyte nicotinic acetylcholine receptor in patient with coexistent pemphigus foliaceus, myasthenia gravis and thymoma. J. Invest. Dermatol. 102:1994;609. (abstract).
40. Grando S.A. New approaches to the treatment of pemphigus. J. Investig. Dermatol. Symp. Proc. 9:2004;84-91.
41. Nguyen V.T., Arredondo J., Chernyavsky A., Pittelkow M.R., Kitajima Y., Grando S.A. Pemphigus vulgaris acantholysis ameliorated by cholinergic agonists. Arch. Dermatol. 2004;. (in press).
42. Xu W., Gelber S., Orr-Urtreger A., Armstrong D., Lewis R.A., Ou C.N., Patrick J., Role L., De Biasi M., Beaudet A.L. Megacystis, mydriasis, and ion channel defect in mice lacking the a3 neuronal nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. U. S. A. 96:1999;5746-5751.
43. Yamada M., Miyakawa T., Duttaroy A., Yamanaka A., Moriguchi T., Makita R., Ogawa M., Chou C.J., Xia B., Crawley J.N., Felder C.C., Deng C.X., Wess J. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature. 410:2001;207-212.
44. Vetter D.E., Liberman M.C., Mann J., Barhanin J., Boulter J., Brown M.C., Saffiote-Kolman J., Heinemann S.F., Elgoyhen A.B. Role of α9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron. 23:1999;93-103.
45. Arredondo J., Hall L.H., Ndoye A., Nguyen V.T., Chernyavsky A.I., Bercovich D., Orr-Urtreger A., Beaudet A.L., Grando S.A. Central role of fibroblast α3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab. Invest. 83:2003;207-225.
46. Arredondo J., Nguyen V.T., Chernyavsky A.I., Bercovich D., Orr-Urtreger A., Vetter D.E., Grando S.A. Functional role of α7 nicotinic receptor in physiological control of cutaneous homeostasis. Life Sci. 72:2003;2063-2067.
47. Lee Y.S., Dlugosz A.A., McKay R., Dean N.M., Yuspa S.H. Definition by specific antisense oligonucleotides of a role for protein kinase C alpha in expression of differentiation markers in normal and neoplastic mouse epidermal keratinocytes. Mol. Carcinog. 18:1997;44-53.
48. 2+ inhibits murine keratinocyte differentiation in vitro. J. Cell. Physiol. 163:1995;105-114.
49. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215:1990;403-410.
50. Arredondo J., Nguyen V.T., Chernyavsky A.I., Bercovich D., Orr-Urtreger A., Kummer W., Lips K., Vetter D.E., Grando S.A. Central role of α7 nicotinic receptor in differentiation of the stratified squamous epithelium. J. Cell Biol. 159:2002;325-336.
51. Arredondo J., Nguyen V.T., Chernyavsky A.I., Jolkovsky D.L., Pinkerton K.E., Grando S.A. A receptor-mediated mechanism of nicotine toxicity in oral keratinocytes. Lab. Invest. 81:2001;1653-1668.
52. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
53. Nguyen V.T., Arredondo J., Chernyavsky A.I., Kitajima Y., Grando S.A. Keratinocyte acetylcholine receptors regulate cell adhesion. Life Sci. 72:2003;2081-2085.
54. Grando S.A., Crosby A.M., Zelickson B.D., Dahl M.V. Agarose gel keratinocyte outgrowth system as a model of skin re-epithelization: requirement of endogenous acetylcholine for outgrowth initiation. J. Invest. Dermatol. 101:1993;804-810.
55. Chavez-Noriega L.E., Crona J.H., Washburn M.S., Urrutia A., Elliott K.J., Johnson E.C. Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther. 280:1997;346-356.
56. Verbitsky M., Rothlin C.V., Katz E., Belen Elgoyhen A. Mixed nicotinic-muscarinic properties of the α9 nicotinic cholinergic receptor. Neuropharmacology. 39:2000;2515-2524.
57. Quik M., Choremis J., Komourian J., Lukas R.J., Puchacz E. Similarity between rat brain nicotinic α-bungarotoxin receptors and stably expressed α-bungarotoxin binding sites. J. Neurochem. 67:1996;145-154.
58. Rothlin C.V., Katz E., Verbitsky M., Elgoyhen A.B. The α9 nicotinic acetylcholine receptor shares pharmacological properties with type A gamma-aminobutyric acid, glycine, and type 3 serotonin receptors. Mol. Pharmacol. 55:1999;248-254.
59. Calautti E., Grossi M., Mammucari C., Aoyama Y., Pirro M., Ono Y., Li J., Dotto G.P. Fyn tyrosine kinase is a downstream mediator of Rho/PRK2 function in keratinocyte cell-cell adhesion. J. Cell Biol. 156:2002;137-148.
60. Serres M., Filhol O., Lickert H., Grangeasse C., Chambaz E.M., Stappert J., Vincent C., Schmitt D. The disruption of adherens junctions is associated with a decrease of E-cadherin phosphorylation by protein kinase CK2. Exp. Cell Res. 257:2000;255-264.
61. Moon H.S., Choi E.A., Park H.Y., Choi J.Y., Chung H.W., Kim J.I., Park W.I. Expression and tyrosine phosphorylation of E-cadherin, beta- and gamma-catenin, and epidermal growth factor receptor in cervical cancer cells. Gynecol. Oncol. 81:2001;355-359.
62. Hu P., O'Keefe E.J., Rubenstein D.S. Tyrosine phosphorylation of human keratinocyte beta-catenin and plakoglobin reversibly regulates their binding to E-cadherin and alpha-catenin. J. Invest. Dermatol. 117:2001;1059-1067.
63. Lilien J., Balsamo J., Arregui C., Xu G. Turn-off, drop-out: functional state switching of cadherins. Dev. Dyn. 224:2002;18-29.
64. Grando S.A., Arredondo J., Chernyavsky A., Kitajima Y., Nguyen V.T. Mechanisms of pharmacologic regulation of keratinocyte adhesion by cholinergic drugs. (abstract #107) J. Invest. Dermatol. 119:2002;225.
65. Wakita H., Furukawa F., Baba S., Takigawa M. Human squamous-cell- carcinoma cell line (DJM-1) cells synthesize P-cadherin molecules via an elevation of extracellular calcium: calcium regulates P-cadherin-gene expression at the translational level via protein tyrosine phosphorylation. Int. J. Cancer. 73:1997;432-439.
66. Kitajima Y., Owada M.K., Fujisawa Y., Seishima M., Yaoita H., Hirako Y., Owaribe K. A hemidesmosomal transmembrane collagenous molecule, the 180-kDa bullous pemphigoid antigen (BPA II), is phosphorylated with 12-O- tetradecanoylphorbol-13-acetate in a human squamous cell carcinoma cell line (DJM-1). Epithel. Cell Biol. 4:1995;70-75.
67. Kitajima Y., Aoyama Y., Seishima M. Transmembrane signaling for adhesive regulation of desmosomes and hemidesmosomes, and for cell-cell detachment induced by pemphigus IgG in cultured keratinocytes: involvement of protein kinase C. J. Investig. Dermatol. Symp. Proc. 4:1999;137-144.
68. 2+-switch in a human carcinoma cell line. J. Dermatol. Sci. 27:2001;206-214.
69. Wang F., Nelson M.E., Kuryatov A., Olale F., Cooper J., Keyser K., Lindstrom J. Chronic nicotine treatment up-regulates human α3β2 but not α3β4 acetylcholine receptors stably transfected in human embryonic kidney cells. J. Biol. Chem. 273:1998;28721-28732.
70. Nguyen V.T., Hall L.L., Gallacher G., Ndoye A., Jolkovsky D.L., Webber R.J., Buchli R., Grando S.A. Choline acetyltransferase, acetylcholinesterase, and nicotinic acetylcholine receptors of human gingival and esophageal epithelia. J. Dent. Res. 79:2000;939-949.
71. Kwon O.S., Chung J.H., Cho K.H., Suh D.H., Park K.C., Kim K.H., Eun H.E. Nicotine-enhanced epitheliol differentiation in reconstructed human oral mucosa in vitro. Skin Pharmacol. Appl. Skin Physiol. 12:1999;227-234.
72. Arredondo J., Hall L.L., Ndoye A., Chernyavsky A.I., Jolkovsky D.L., Grando S.A. Muscarinic acetylcholine receptors regulating cell cycle progression are expressed in human gingival keratinocytes. J. Periodontal Res. 38:2003;79-89.
73. Klapproth H., Reinheimer T., Metzen J., Muench M., Bittinger F., Kirkpatrick C.J., Racke K., Wessler I. Non-neuronal acetylcholine, a widespread signalling molecule in man. Br. J. Pharmacol. 120:1997;61.
74. Wessler I., Kirkpatrick C.J., Racke K. The cholinergic 'pitfall': acetylcholine, a universal cell molecule in biological systems, including humans. Clin. Exp. Pharmacol. Physiol. 26:1999;198-205.
75. Cavanah D.K., Casale T.B. Cutaneous responses to anticholinergics: evidence for muscarinic receptor subtype participation. J. Allergy Clin. Immunol. 87:1991;971-976.
76. Wessler I. New use of active ingredients which affect non-neuronal acetylcholine functions. PCT Gazette WO 98/00119. 1998;Boehringer Ingelheim KG, Germany.
77. Maus A.D.J., Pereira E.F.R., Karachunski P.I., Horton R.M., Navaneetham D., Macklin K., Cortes W.S., Albuquerque E.X., Conti-Fine B.M. Human and rodent bronchial epithelial cells express functional nicotinic acetylcholine receptors. Mol. Pharmacol. 54:1998;779-788.
78. Saba S.R., Mason R.G. Acetylcholine, cholinesterase activity, and the aggregability of human platelets. Proc. Soc. Exp. Biol. Med. 135:1970;104-107.
79. Kharkevich D.D. Effect of cholinergic stimulation on spontaneous lymphocyte adhesion in vitro. Bull. Eksp. Biol. Med. 104:1987;69-71.
80. Evinger M.J., Ernsberger P., Regunathan S., Joh T.H., Reis D.J. A single transmitter regulates gene expression through two separate mechanisms: cholinergic regulation of phenylethanolamine N-methyltransferase mRNA via nicotinic and muscarinic pathways. J. Neurosci. 14:1994;2106-2116.
81. Falugi C., Pieroni M., Moretti E. Cholinergic molecules and sperm functions. J. Submicrosc. Cytol. Pathol. 25:1993;63-69.
82. Elgoyhen A.B., Johnson D.S., Boulter J., Vetter D.E., Heinemann S. α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell. 79:1994;705-715.
83. Wikstrom M.A., Lawoko G., Heilbronn E. Cholinergic modulation of extracellular ATP-induced cytoplasmic calcium concentrations in cochlear outer hair cells. J. Physiol. (Paris). 92:1998;345-349.
84. Fine J.-D. Immunobullous diseases. Sams W.M., Lynch P.J. Principles and Practice of Dermatology. 1996;455-473 Churchill Livingstone, New York.
85. Farb R.M., Dykes R., Lazarus G.S. Anti-epidermal-cell-surface pemphigus antibody detaches viable epidermal cells from culture plates by activation of proteinase. Proc. Natl. Acad. Sci. U. S. A. 75:1978;459-463.
86. Huelsken J., Vogel R., Brinkmann V., Erdmann B., Birchmeier C., Birchmeier W. Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148:2000;567-578.
87. Hulsken J., Birchmeier W., Behrens J. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J. Cell Biol. 127:1994;2061-2069.
88. Tsiokas L., Watson M. Differential in vivo induction of immediate early genes by oxotremorine in the central nervous system of long- and short-sleep mice. Mol. Pharmacol. 47:1995;272-282.
89. Pinkas-Kramarski R., Stein R., Lindenboim L., Sokolovsky M. Growth factor-like effects mediated by muscarinic receptors in PC12M1 cells. J. Neurochem. 59:1992;2158-2166.
90. Zhang S., Day I., Ye S. Nicotine induced changes in gene expression by human coronary artery endothelial cells. Atherosclerosis. 154:2001;277-283.
91. Zhang S., Day I.N., Ye S. Microarray analysis of nicotine-induced changes in gene expression in endothelial cells. Physiol. Genomics. 5:2001;187-192.
92. von der Kammer H., Mayhaus M., Albrecht C., Enderich J., Wegner M., Nitsch R.M. Muscarinic acetylcholine receptors activate expression of the EGR gene family of transcription factors. J. Biol. Chem. 273:1998;14538-14544.
93. Caulfield M.P. Muscarinic receptors characterization coupling and function. Pharmacol. Ther. 58:1993;319-379.
94. Sheu H.M., Kitajima Y., Yaoita H. Involvement of protein kinase C in translocation of desmoplakins from cytosol to plasma membrane during desmosome formation in human squamous cell carcinoma cells grown in low to normal calcium concentration. Exp. Cell Res. 185:1989;176-190.
95. Jones J.C., Hopkinson S.B., Goldfinger L.E. Structure and assembly of hemidesmosomes. BioEssays. 20:1998;488-494.
96. Amar L.S., Shabana al H.M., Oboeuf M., Martin N., Forest N. Desmosomes are regulated by protein kinase C in primary rat epithelial cells. Cell Adhes. Commun. 5:1998;1-12.
97. Zia S., Ndoye A., Lee T.X., Webber R.J., Grando S.A. Receptor-mediated inhibition of keratinocyte migration by nicotine involves modulations of calcium influx and intracellular concentration. J. Pharmacol. Exp. Ther. 293:2000;973-981.
98. Nguyen V.T., Ndoye A., Hall L.L., Zia S., Arredondo J., Chernyavsky A.I., Kist D.A., Zelickson B.D., Lawry M.A., Grando S.A. Programmed cell death of keratinocytes culminates in apoptotic secretion of a humectant upon secretagogue action of acetylcholine. J. Cell Sci. 114:2001;1189-1204.