Role of the calcium-sensing receptor in calcium regulation of epidermal differentiation and function

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 27, Issue 3, 2013, Pages 415-427

  Tu, Chia Ling ^a   Bikle, Daniel D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

calcium sensing receptor; E cadherin; keratinocyte differentiation; permeability barrier

Indexed keywords

CALCITRIOL; CALCIUM ION; CALCIUM SENSING RECEPTOR; CATENIN; CYTOKERATIN 1; CYTOKERATIN 5; CYTOKERATIN 6; GLUTAMINASE; SPHINGOLIPID; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; UVOMORULIN;

ACTIN FILAMENT; CELL ADHESION; CELL DEATH; CELL DIFFERENTIATION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONFERENCE PAPER; DESMOSOME; EPIDERMIS; HAIR GROWTH; HUMAN; KERATINOCYTE; MEMBRANE STRUCTURE; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSORIASIS; SKIN DISEASE; STRATUM CORNEUM;

EID: 84880296675     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2013.03.002     Document Type: Conference Paper

References (99)

1. G.K. Menon, P.M. Elias, and S.H. Lee Localization of calcium in murine epidermis following disruption and repair of the permeability barrier Cell and Tissue Research 270 1992 503 512
2. H. Hennings, and K.A. Holbrook Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture. An ultrastructural study Experimental Cell Research 143 1983 127 142
3. D.D. Bikle, A. Ratnam, and T. Mauro Changes in calcium responsiveness and handling during keratinocyte differentiation. Potential role of the calcium receptor The Journal of Clinical Investigation 97 1996 1085 1093
4. E. Lee, and S.H. Yuspa Changes in inositol phosphate metabolism are associated with terminal differentiation and neoplasia in mouse keratinocytes Carcinogenesis 12 1991 1651 1658
5. E. Calautti, S. Cabodi, and P.L. Stein Tyrosine phosphorylation and src family kinases control keratinocyte cell-cell adhesion Journal of Cell Biology 141 1998 1449 1465
6. E. Calautti, M. Grossi, and C. Mammucari Fyn tyrosine kinase is a downstream mediator of Rho/PRK2 function in keratinocyte cell-cell adhesion Journal of Cell Biology 156 2002 137 148
7. E. Calautti, J. Li, and S. Saoncella Phosphoinositide 3-kinase signaling to Akt promotes keratinocyte differentiation versus death The Journal of Biological Chemistry 280 2005 32856 32865
8. Z. Xie, and D.D. Bikle The recruitment of phosphatidylinositol 3-kinase to the E-cadherin-catenin complex at the plasma membrane is required for calcium-induced phospholipase C-gamma1 activation and human keratinocyte differentiation The Journal of Biological Chemistry 282 2007 8695 8703
9. Y. Oda, C.L. Tu, and S. Pillai The calcium sensing receptor and its alternatively spliced form in keratinocyte differentiation The Journal of Biological Chemistry 273 1998 23344 23352
10. C.L. Tu, W. Chang, and D.D. Bikle The role of the calcium sensing receptor in regulating intracellular calcium handling in human epidermal keratinocytes The Journal of Investigative Dermatology 127 2007 1074 1083
11. C.L. Tu, W. Chang, and Z. Xie Inactivation of the calcium sensing receptor inhibits E-cadherin-mediated cell-cell adhesion and calcium-induced differentiation in human epidermal keratinocytes The Journal of Biological Chemistry 283 2008 3519 3528
12. C.L. Tu, D.A. Crumrine, and M.Q. Man Ablation of the calcium-sensing receptor in keratinocytes impairs epidermal differentiation and barrier function The Journal of Investigative Dermatology 132 2012 2350 2359
13. E. Fuchs Epidermal differentiation: the bare essentials Journal of Cell Biology 111 1990 2807 2814
14. J. Schweizer, and H. Winter Keratin biosynthesis in normal mouse epithelia and in squamous cell carcinomas. mRNA-dependent alterations of the primary structure of distinct keratin subunits in tumors The Journal of Biological Chemistry 258 1983 13268 13272
15. R.H. Rice, and H. Green Presence in human epidermal cells of a soluble protein precursor of the cross-linked envelope: activation of the cross-linking by calcium ions Cell 18 1979 681 694
16. S.M. Thacher, and R.H. Rice Keratinocyte-specific transglutaminase of cultured human epidermal cells: relation to cross-linked envelope formation and terminal differentiation Cell 40 1985 685 695
17. D. Hohl, U. Lichti, and D. Breitkreutz Transcription of the human loricrin gene in vitro is induced by calcium and cell density and suppressed by retinoic acid The Journal of Investigative Dermatology 96 1991 414 418
18. J.D. Lonsdale-Eccles, K.A. Resing, and R.L. Meek High-molecular-weight precursor of epidermal filaggrin and hypothesis for its tandem repeating structure Biochemistry 23 1984 1239 1245
19. D. Hohl Cornified cell envelope Dermatologica 180 1990 201 211
20. W.M. Holleran, Y. Takagi, and Y. Uchida Epidermal sphingolipids: metabolism, function, and roles in skin disorders FEBS Letters 580 2006 5456 5466
21. K. Sakai, M. Akiyama, and Y. Sugiyama-Nakagiri Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes Experimental Dermatology 16 2007 920 926
22. G. Vielhaber, S. Pfeiffer, and L. Brade Localization of ceramide and glucosylceramide in human epidermis by immunogold electron microscopy The Journal of Investigative Dermatology 117 2001 1126 1136
23. S.J. Miller, R. Aly, and H.R. Shinefeld In vitro and in vivo antistaphylococcal activity of human stratum corneum lipids Archives of Dermatology 124 1988 209 215
24. D.J. Bibel, R. Aly, and H.R. Shinefield Antimicrobial activity of sphingosines The Journal of Investigative Dermatology 98 1992 269 273
25. A. Oren, T. Ganz, and L. Liu In human epidermis, beta-defensin 2 is packaged in lamellar bodies Experimental Molecular Pathology 74 2003 180 182
26. M.H. Braff, A. Di Nardo, and R.L. Gallo Keratinocytes store the antimicrobial peptide cathelicidin in lamellar bodies The Journal of Investigative Dermatology 124 2005 394 400
27. R.I. Lehrer In defense of skin The Journal of Investigative Dermatology 125 2005 viii ix [discussion x-xi]
28. G.K. Menon, S. Grayson, and P.M. Elias Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry The Journal of Investigative Dermatology 84 1985 508 512
29. L. Komuves, Y. Oda, and C.L. Tu Epidermal expression of the full-length extracellular calcium-sensing receptor is required for normal keratinocyte differentiation Journal of Cell Physiology 192 2002 45 54
30. 2+ gradient: measurement using the phasor representation of fluorescent lifetime imaging Biophysical Journal 98 2010 911 921
31. P.M. Elias, P. Nau, and K. Hanley Formation of the epidermal calcium gradient coincides with key milestones of barrier ontogenesis in the rodent The Journal of Investigative Dermatology 110 1998 399 404
32. G.K. Menon, and P.M. Elias Ultrastructural localization of calcium in psoriatic and normal human epidermis Archives of Dermatology 127 1991 57 63
33. G.K. Menon, P.M. Elias, and K.R. Feingold Integrity of the permeability barrier is crucial for maintenance of the epidermal calcium gradient British Journal of Dermatology 130 1994 139 147
34. R.L. Eckert, J.F. Crish, and N.A. Robinson The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation Physiology Review 77 1997 397 424
35. V.M. Braga, K.J. Hodivala, and F.M. Watt Calcium-induced changes in distribution and solubility of cadherins, integrins and their associated cytoplasmic proteins in human keratinocytes Cell Adhesion and Communication 3 1995 201 215
36. S.H. Yuspa, A.E. Kilkenny, and P.M. Steinert Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro Journal of Cell Biology 109 1989 1207 1217
37. S. Jaken, and S.H. Yuspa Early signals for keratinocyte differentiation: role of Ca2+-mediated inositol lipid metabolism in normal and neoplastic epidermal cells Carcinogenesis 9 1988 1033 1038
38. M.J. Berridge Cell signalling. A tale of two messengers Nature 365 1993 388 389
39. S. Pece, and J.S. Gutkind Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation The Journal of Biological Chemistry 275 2000 41227 41233
40. S. Pece, M. Chiariello, and C. Murga Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex The Journal of Biological Chemistry 274 1999 19347 19351
41. Z. Xie, P.A. Singleton, and L.Y. Bourguignon Calcium-induced human keratinocyte differentiation requires src- and fyn-mediated phosphatidylinositol 3-kinase-dependent activation of phospholipase C-gamma1 Molecular Biology of the Cell 16 2005 3236 3246
42. M.J. Berridge Inositol trisphosphate and calcium signalling Nature 361 1993 315 325
43. M.J. Berridge The endoplasmic reticulum: a multifunctional signaling organelle Cell Calcium 32 2002 235 249
44. M.J. Behne, C.L. Tu, and I. Aronchik Human keratinocyte ATP2C1 localizes to the Golgi and controls Golgi Ca2+ stores The Journal of Investigative Dermatology 121 2003 688 694
45. 2+-ATPase SPCA1 Cell Calcium 34 2003 157 162
46. P. Pinton, T. Pozzan, and R. Rizzuto The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum EMBO Journal 17 1998 5298 5308
47. A. Surroca, and D. Wolff Inositol 1,4,5-trisphosphate but not ryanodine-receptor agonists induces calcium release from rat liver Golgi apparatus membrane vesicles Journal of Membrane Biology 177 2000 243 249
48. L. Foggia, and A. Hovnanian Calcium pump disorders of the skin American Journal of Medical Genetics Part C: Seminars in Medical Genetics 131C 2004 20 31
49. J.W. Putney Jr. Capacitative calcium entry: sensing the calcium stores Journal of Cell Biology 169 2005 381 382
50. C.L. Tu, W. Chang, and D.D. Bikle Phospholipase cgamma1 is required for activation of store-operated channels in human keratinocytes The Journal of Investigative Dermatology 124 2005 187 197
51. S. Fatherazi, R.B. Presland, and Belton Evidence that TRPC4 supports the calcium selective I(CRAC)-like current in human gingival keratinocytes Pflugers Archive 453 2007 879 889
52. S. Fatherazi, C.M. Belton, and K.T. Izutsu Sequential activation of store-operated currents in human gingival keratinocytes The Journal of Investigative Dermatology 121 2003 120 131
53. M. Denda, S. Fuziwara, and K. Inoue Influx of calcium and chloride ions into epidermal keratinocytes regulates exocytosis of epidermal lamellar bodies and skin permeability barrier homeostasis The Journal of Investigative Dermatology 121 2003 362 367
54. L. Li, R.W. Tucker, and H. Hennings Chelation of intracellular Ca2+ inhibits murine keratinocyte differentiation in vitro Journal of Cell Physiology 163 1995 105 114
55. S. Pillai, and D.D. Bikle Lanthanum influx into cultured human keratinocytes: effect on calcium flux and terminal differentiation Journal of Cell Physiology 151 1992 623 629
56. S. Pillai, and D.D. Bikle Adenosine triphosphate stimulates phosphoinositide metabolism, mobilizes intracellular calcium, and inhibits terminal differentiation of human epidermal keratinocytes The Journal of Clinical Investigation 90 1992 42 51
57. Z. Xie, and D.D. Bikle Phospholipase C-gamma1 is required for calcium-induced keratinocyte differentiation The Journal of Biological Chemistry 274 1999 20421 20424
58. M.J. Wheelock, and K.R. Johnson Cadherins as modulators of cellular phenotype Annual Review of Cell and Developmental Biology 19 2003 207 235
59. P. Young, O. Boussadia, and H. Halfter E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles EMBO Journal 22 2003 5723 5733
60. C.L. Tinkle, T. Lechler, and H.A. Pasolli Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses Proceedings of the National Academy of Sciences of the United States of America 101 2004 552 557
61. F. Furukawa, K. Fujii, and Y. Horiguchi Roles of E- and P-cadherin in the human skin Microscopy Research and Technique 38 1997 343 352
62. Z. Xie, S.M. Chang, and S.D. Pennypacker Phosphatidylinositol-4-phosphate 5-kinase 1alpha mediates extracellular calcium-induced keratinocyte differentiation Molecular Biology of the Cell 20 2009 1695 1704
63. V.M. Braga, L.M. Machesky, and A. Hall The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts Journal of Cell Biology 137 1997 1421 1431
64. C.L. Tu, W. Chang, and D.D. Bikle The calcium-sensing receptor-dependent regulation of cell-cell adhesion and keratinocyte differentiation requires Rho and filamin A The Journal of Investigative Dermatology 131 2011 1119 1128
65. Y.S. Lee, A.A. Dlugosz, and R. McKay 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 Molecular Carcinogenesis 18 1997 44 53
66. M.F. Denning, A.A. Dlugosz, and E.K. Williams Specific protein kinase C isozymes mediate the induction of keratinocyte differentiation markers by calcium Cell Growth and Differentiation 6 1995 149 157
67. A. Deucher, T. Efimova, and R.L. Eckert Calcium-dependent involucrin expression is inversely regulated by protein kinase C (PKC)alpha and PKCdelta The Journal of Biological Chemistry 277 2002 17032 17040
68. D.C. Ng, S. Shafaee, and D. Lee Requirement of an AP-1 site in the calcium response region of the involucrin promoter The Journal of Biological Chemistry 275 2000 24080 24088
69. S.I. Jang, and P.M. Steinert Loricrin expression in cultured human keratinocytes is controlled by a complex interplay between transcription factors of the Sp1, CREB, AP1, and AP2 families The Journal of Biological Chemistry 277 2002 42268 42279
70. J.F. Welter, J.F. Crish, and C. Agarwal Fos-related antigen (Fra-1), junB, and junD activate human involucrin promoter transcription by binding to proximal and distal AP1 sites to mediate phorbol ester effects on promoter activity The Journal of Biological Chemistry 270 1995 12614 12622
71. N.N. Sinitsyna, T.V. Reznikova, and Q. Qin Arsenite suppression of involucrin transcription through AP1 promoter sites in cultured human keratinocytes Toxicology and Applied Pharmacology 243 2009 275 282
72. E.M. Brown, and R.J. MacLeod Extracellular calcium sensing and extracellular calcium signaling Physiology Review 81 2001 239 297
73. C.L. Tu, Y. Oda, and D.D. Bikle Effects of a calcium receptor activator on the cellular response to calcium in human keratinocytes The Journal of Investigative Dermatology 113 1999 340 345
74. C.L. Tu, W. Chang, and D.D. Bikle The extracellular calcium-sensing receptor is required for calcium-induced differentiation in human keratinocytes The Journal of Biological Chemistry 276 2001 41079 41085
75. C.L. Tu, Y. Oda, and L. Komuves The role of the calcium-sensing receptor in epidermal differentiation Cell Calcium 35 2004 265 273
76. W. Chang, C. Tu, and R. Bajra Calcium sensing in cultured chondrogenic RCJ3.1C5.18 cells Endocrinology 140 1999 1911 1919
77. M. Kanatani, T. Sugimoto, and M. Kanzawa High extracellular calcium inhibits osteoclast-like cell formation by directly acting on the calcium-sensing receptor existing in osteoclast precursor cells Biochemical and Biophysical Research Communications 261 1999 144 148
78. W. Chang, C. Tu, and T.H. Chen Expression and signal transduction of calcium-sensing receptors in cartilage and bone Endocrinology 140 1999 5883 5893
79. J.I. Bruce, X. Yang, and C.J. Ferguson Molecular and functional identification of a Ca2+ (polyvalent cation)-sensing receptor in rat pancreas The Journal of Biological Chemistry 274 1999 20561 20568
80. J.L. Blank, A.H. Ross, and J.H. Exton Purification and characterization of two G-proteins that activate the beta 1 isozyme of phosphoinositide-specific phospholipase C. Identification as members of the Gq class The Journal of Biological Chemistry 266 1991 18206 18216
81. G. Boulay, D.M. Brown, and N. Qin Modulation of Ca(2+) entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca(2+) entry Proceedings of the National Academy of Sciences of the United States of America 96 1999 14955 14960
82. Y. Feng, and C.A. Walsh The many faces of filamin: a versatile molecular scaffold for cell motility and signalling Nature Cell Biology 6 2004 1034 1038
83. Y. Oda, C.L. Tu, and W. Chang The calcium sensing receptor and its alternatively spliced form in murine epidermal differentiation The Journal of Biological Chemistry 275 2000 1183 1190
84. K. Turksen, and T.C. Troy Overexpression of the calcium sensing receptor accelerates epidermal differentiation and permeability barrier formation in vivo Mechanisms of Development 120 2003 733 744
85. C. Ho, D.A. Conner, and M.R. Pollak A mouse model of human familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism Nature Genetics 11 1995 389 394
86. L. Rodriguez, C. Tu, and Z. Cheng Expression and functional assessment of an alternatively spliced extracellular Ca2+-sensing receptor in growth plate chondrocytes Endocrinology 146 2005 5294 5303
87. W. Chang, C. Tu, and T.H. Chen The extracellular calcium-sensing receptor (CaSR) is a critical modulator of skeletal development Science Signaling 1 2008 ra1
88. V. Vasioukhin, L. Degenstein, and B. Wise The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin Proceedings of the National Academy of Sciences of the United States of America 96 1999 8551 8556
89. M.J. Hardman, P. Sisi, and D.N. Banbury Patterned acquisition of skin barrier function during development Development 125 1998 1541 1552
90. D.D. Bikle, E. Gee, and S. Pillai Regulation of keratinocyte growth, differentiation, and vitamin D metabolism by analogs of 1,25-dihydroxyvitamin D The Journal of Investigative Dermatology 101 1993 713 718
91. S. Pillai, D.D. Bikle, and M.J. Su 1,25-Dihydroxyvitamin D3 upregulates the phosphatidylinositol signaling pathway in human keratinocytes by increasing phospholipase C levels The Journal of Clinical Investigation 96 1995 602 609
92. M.J. Su, D.D. Bikle, and M.L. Mancianti 1,25-Dihydroxyvitamin D3 potentiates the keratinocyte response to calcium The Journal of Biological Chemistry 269 1994 14723 14729
93. D.D. Bikle, D. Ng, and Y. Oda The vitamin D response element of the involucrin gene mediates its regulation by 1,25-dihydroxyvitamin D3 The Journal of Investigative Dermatology 119 2002 1109 1113
94. A.V. Ratnam, D.D. Bikle, and J.K. Cho 1,25 Dihydroxyvitamin D3 enhances the calcium response of keratinocytes Journal of Cell Physiology 178 1999 188 196
95. L. Canaff, and G.N. Hendy Human calcium-sensing receptor gene. Vitamin D response elements in promoters P1 and P2 confer transcriptional responsiveness to 1,25-dihydroxyvitamin D The Journal of Biological Chemistry 277 2002 30337 30350
96. Y. Oda, R.J. Chalkley, and A.L. Burlingame The transcriptional coactivator DRIP/mediator complex is involved in vitamin D receptor function and regulates keratinocyte proliferation and differentiation The Journal of Investigative Dermatology 130 2010 2377 2388
97. R. Zineb, B. Zhor, and W. Odile Distinct, tissue-specific regulation of vitamin D receptor in the intestine, kidney, and skin by dietary calcium and vitamin D Endocrinology 139 1998 1844 1852
98. D.D. Bikle, S. Chang, and D. Crumrine 25 Hydroxyvitamin D 1 alpha-hydroxylase is required for optimal epidermal differentiation and permeability barrier homeostasis The Journal of Investigative Dermatology 122 2004 984 992
99. Y. Oda, Y. Uchida, and S. Moradian Vitamin D receptor and coactivators SRC2 and 3 regulate epidermis-specific sphingolipid production and permeability barrier formation The Journal of Investigative Dermatology 129 2009 1367 1378