The caveolin-1 scaffolding domain peptide decreases phosphatidylglycerol levels and inhibits calcium-induced differentiation in mouse keratinocytes

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Qin, Haixia ^b   Bollag, Wendy B ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 3; CALCIUM; CAVEOLIN 1; GLYCEROL; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPASE D2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR CALCIUM; KERATINOCYTE; LIPID RAFT; MITOSIS INHIBITION; MOUSE; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CAVEOLIN 1; CELL DIFFERENTIATION; DNA REPLICATION; ENZYME ACTIVATION; GLYCEROL; GLYCEROPHOSPHOLIPIDS; KERATINOCYTES; MICE; PEPTIDE FRAGMENTS; PHOSPHATIDYLGLYCEROLS; TRANSGLUTAMINASES;

EID: 84893371677     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080946     Document Type: Article

References (75)

1. Bikle DD (2004) Vitamin D regulated keratinocyte differentiation. J Cell Biochem 92: 436-444. doi:10.1002/jcb.20095. PubMed: 15156556.
2. Bikle DD, Xie Z, Tu CL (2012) Calcium regulation of keratinocyte differentiation. Expert. Rev Endocrinol Metab 7: 461-472. doi:10.1586/eem.12.34.
3. Menon GK, Grayson S, Elias PM (1985) Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 84: 508-512. doi: 10.1111/1523-1747.ep12273485. PubMed: 3998499. (Pubitemid 15053207)
4. Menon GK, Price LF, Bommannan B, Elias PM, Feingold KR (1994) Selective obliteration of the epidermal calcium gradient leads to enhanced lamellar body secretion. J Invest Dermatol 102: 789-795. doi: 10.1111/1523-1747.ep12377921. PubMed: 8176264. (Pubitemid 24144263)
5. Menon GK, Elias PM, Lee SH, Feingold KR (1992) Localization of calcium in murine epidermis folowing disruption and repair of the permeability barrier. Cell Tissue Res 270: 503-512. doi:10.1007/BF00645052. PubMed: 1486603.
6. Tu CL, Oda Y, Bikle DD (1999) Effects of a calcium receptor activator on the cellular response to calcium in human keratinocytes. J Invest Dermatol 113: 340-345. doi:10.1046/j.1523-1747.1999.00698.x. PubMed: 10469331. (Pubitemid 29449071)
7. Punnonen K, Denning M, Lee E, Li L, Rhee SG et al. (1993) Keratinocyte differentiation is associated with changes in the expression and regulation of phospholipase C isoenzymes. J Invest Dermatol 101: 719-726. doi:10.1111/1523- 1747.ep12371682. PubMed: 8228334. (Pubitemid 23322030)
8. Lee E, Yuspa SH (1991) Changes in inositol phosphate metabolism are associated with terminal differentiation and neoplasia in mouse keratinocytes. Carcinogenesis 12: 1651-1658. doi:10.1093/carcin/12.9.1651. PubMed: 1893524.
9. Tu CL, Chang W, Bikle DD (2007) The role of the calcium sensing receptor in regulating intracellular calcium handling in human epidermal keratinocytes. J Invest Dermatol 127: 1074-1083. doi:10.1038/sj.jid.5700633. PubMed: 17124506. (Pubitemid 46625129)
10. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687-698. doi:10.1038/nrm1469. PubMed: 15340377. (Pubitemid 39208179)
11. Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118: 3225-3232. doi:10.1242/jcs.02519. PubMed: 16079275.
12. Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68: 425-458. doi:10.1146/annurev.biochem.68.1.425. PubMed: 10872456. (Pubitemid 29449199)
13. Verkman AS, Mitra AK (2000) Structure and function of aquaporin water channels. Am J Physiol Renal Physiol 278: F13-F28. PubMed: 10644652. (Pubitemid 30106122)
14. Hatakeyama S, Yoshida Y, Tani T, Koyama Y, Nihei K et al. (2001) Cloning of a new aquaporin (AQP10) abundantly expressed in duodenum and jejunum. Biochem Biophys Res Commun 287: 814-819. doi:10.1006/bbrc.2001.5661. PubMed: 11573934. (Pubitemid 32953546)
15. Yang B, Verkman AS (1997) Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes. J Biol Chem 272: 16140-16146. doi:10.1074/jbc.272.26.16140. PubMed: 9195910. (Pubitemid 27276428)
16. Hara-Chikuma M, Verkman AS (2005) Aquaporin-3 functions as a glycerol transporter in mammalian skin. Biol Cell 97: 479-486. doi: 10.1042/BC20040104. PubMed: 15966863. (Pubitemid 40936590)
17. Sougrat R, Morand M, Gondran C, Barré P, Gobin R et al. (2002) Functional expression of AQP3 in human skin epidermis and reconstructed epidermis. J Invest Dermatol 118: 678-685. doi: 10.1046/j.1523-1747.2002.01710. x. PubMed: 11918716. (Pubitemid 34309989)
18. Voss KE, Bollag RJ, Fussell N, By C, Sheehan DJ, et al (2011) Abnormal aquaporin-3 protein expression in hyperproliferative skin disorders. Arch Dermatol Res 303: 591-600. doi:10.1007/s00403-011-1136-x. PubMed: 21400035.
19. Qin H, Zheng X, Zhong X, Shetty AK, Elias PM et al. (2011) Aquaporin-3 in keratinocytes and skin: Its role and interaction with phospholipase D2. Arch Biochem Biophys 508: 138-143. doi:10.1016/j.abb.2011.01.014. PubMed: 21276418.
20. Hara M, Verkman AS (2003) Glycerol replacement corrects defective skin hydration, elasticity, and barrier function in aquaporin-3-deficient mice. Proc Natl Acad Sci U S A 100: 7360-7365. doi:10.1073/pnas.1230416100. PubMed: 12771381. (Pubitemid 36706442)
21. Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of aquaporin-3-deficient mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 277: 46616-46621. doi: 10.1074/jbc.M209003200. PubMed: 12270942. (Pubitemid 35417661)
22. Banno Y (2002) Regulation and possible role of mammalian phospholipase D in cellular functions. J Biochem 131: 301-306. doi: 10.1093/oxfordjournals. jbchem.a003103. PubMed: 11872157.
23. Nozawa Y (2002) Roles of phospholipase D in apoptosis and prosurvival. Biochim Biophys Acta 1585: 77-86. doi:10.1016/S1388-1981(02)00327-X. PubMed: 12531540.
24. Frohman MA, Morris AJ (1999) Phospholipase D structure and regulation. Chem Phys Lipids 98: 127-140. doi:10.1016/S0009-3084(99)00025-0. PubMed: 10358935. (Pubitemid 29150401)
25. Colley WC, Sung TC, Roll R, Jenco J, Hammond SM et al. (1997) Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr Biol 7: 191-201. doi:10.1016/S0960-9822(97)70090-3. PubMed: 9395408. (Pubitemid 27164725)
26. Zheng X, Ray S, Bollag WB (2003) Modulation of phospholipase Dmediated phosphatidylglycerol formation by differentiating agents in primary mouse epidermal keratinocytes. Biochim Biophys Acta 1643: 25-36. doi:10.1016/j.bbamcr. 2003.08.006. PubMed: 14654225. (Pubitemid 37494889)
27. Zheng X, Bollag WB (2003) Aquaporin 3 colocates with phospholipase D2 in caveolin-rich membrane microdomains and is regulated by keratinocyte differentiation. J Invest Dermatol 121: 1487-1495. doi: 10.1111/j.1523-1747. 2003.12614.x. PubMed: 14675200. (Pubitemid 38005503)
28. Bollag WB, Xie D, Zheng X, Zhong X (2007) A potential role for the phospholipase D2-aquaporin-3 signaling module in early keratinocyte differentiation: production of a phosphatidylglycerol signaling lipid. J Invest Dermatol 127: 2823-2831. PubMed: 17597824. (Pubitemid 350134818)
29. Severs NJ (1988) Caveolae: static inpocketings of the plasma membrane, dynamic vesicles or plain artifact? J Cell Sci 90 (3): 341-348.
30. Anderson RG, Jacobson K (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296: 1821-1825. doi:10.1126/science.1068886. PubMed: 12052946. (Pubitemid 34596260)
31. Parton RG (1996) Caveolae and caveolins. Curr Opin Cell Biol 8: 542-548. doi:10.1016/S0955-0674(96)80033-0. PubMed: 8791446.
32. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39. doi:10.1038/35036052. PubMed: 11413487.
33. Galbiati F, Razani B, Lisanti MP (2001) Emerging themes in lipid rafts and caveolae. Cell 106: 403-411. doi:10.1016/S0092-8674(01)00472-X. PubMed: 11525727. (Pubitemid 32786984)
34. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA et al. (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19: 7289-7304. PubMed: 10523618. (Pubitemid 29493393)
35. Smart EJ, Ying Ys, Donzell WC, Anderson RG (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271: 29427-29435. doi:10.1074/jbc.271.46.29427. PubMed: 8910609.
36. Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273: 5419-5422. doi:10.1074/jbc.273.10.5419. PubMed: 9488658. (Pubitemid 28123999)
37. Monier S, Parton RG, Vogel F, Behlke J, Henske A et al. (1995) VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 6: 911-927. doi:10.1091/mbc.6.7.911. PubMed: 7579702.
38. Sargiacomo M, Scherer PE, Tang Z, Kübler E, Song KS et al. (1995) Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci U S A 92: 9407-9411. doi:10.1073/pnas.92.20. 9407. PubMed: 7568142.
39. Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F et al. (1997) Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272: 29337-29346. doi:10.1074/jbc.272.46.29337. PubMed: 9361015. (Pubitemid 27498228)
40. Mineo C, James GL, Smart EJ, Anderson RG (1996) Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J Biol Chem 271: 11930-11935. doi:10.1074/jbc.271.20.11930. PubMed: 8662667. (Pubitemid 26157268)
41. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272: 6525-6533. doi:10.1074/jbc.272.10.6525. PubMed: 9045678. (Pubitemid 27118133)
42. Karpen HE, Bukowski JT, Hughes T, Gratton JP, Sessa WC et al. (2001) The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane. J Biol Chem 276: 19503-19511. doi:10.1074/jbc.M010832200. PubMed: 11278759.
43. Liou JY, Deng WG, Gilroy DW, Shyue SK, Wu KK (2001) Colocalization and interaction of cyclooxygenase-2 with caveolin-1 in human fibroblasts. J Biol Chem 276: 34975-34982. doi:10.1074/jbc.M105946200. PubMed: 11432874.
44. Razani B, Lisanti MP (2001) Two distinct caveolin-1 domains mediate the functional interaction of caveolin-1 with protein kinase A. Am J Physiol Cell Physiol 281: C1241-C1250. PubMed: 11546661.
45. Veldman RJ, Maestre N, Aduib OM, Medin JA, Salvayre R et al. (2001) A neutral sphingomyelinase resides in sphingolipid-enriched microdomains and is inhibited by the caveolin-scaffolding domain: potential implications in tumour necrosis factor signalling. Biochem J 355: 859-868. PubMed: 11311151. (Pubitemid 32434106)
46. Czarny M, Fiucci G, Lavie Y, Banno Y, Nozawa Y et al. (2000) Phospholipase D2: functional interaction with caveolin in low-density membrane microdomains. FEBS Lett 467: 326-332. doi:10.1016/S0014-5793(00)01174-1. PubMed: 10675563. (Pubitemid 30081759)
47. Czarny M, Lavie Y, Fiucci G, Liscovitch M (1999) Localization of phospholipase D in detergent-insoluble, caveolin-rich membrane domains. Modulation by caveolin-1 expression and caveolin-182-101. J Biol Chem 274: 2717-2724. doi:10.1074/jbc.274.5.2717. PubMed: 9915802. (Pubitemid 29075351)
48. Yuspa SH, Harris CC (1974) Altered differentiation of mouse epidermal cells treated with retinyl acetate in vitro. Exp Cell Res 86: 95-105. doi: 10.1016/0014-4827(74)90653-3. PubMed: 4857507.
49. Griner RD, Qin F, Jung E, Sue-Ling CK, Crawford KB et al. (1999) 1,25-dihydroxyvitamin D3 induces phospholipase D-1 expression in primary mouse epidermal keratinocytes. J Biol Chem 274: 4663-4670. doi:10.1074/jbc.274.8.4663. PubMed: 9988703.
50. Yuspa SH, Kilkenny AE, Steinert PM, Roop DR (1989) Expression of murine epidermal differentiation markers is tightly regulated by restricted calcium concentrations in vitro. J Cell Biol 109: 1207-1217. doi:10.1083/jcb.109.3.1207. PubMed: 2475508. (Pubitemid 19220102)
51. Zheng X, Ray S, Bollag WB (2003) Modulation of phospholipase Dmediated phosphatidylglycerol formation by differentiating agents in primary mouse epidermal keratinocytes. Biochim Biophys Acta 1643: 25-36. doi:10.1016/j.bbamcr. 2003.08.006. PubMed: 14654225. (Pubitemid 37494889)
52. Bollag WB (1998) Measurement of phospholipase D activity. Methods Mol Biol 105: 151-160. PubMed: 10427558.
53. Tu CL, Crumrine DA, Man MQ, Chang W, Elalieh H et al. (2012) Ablation of the calcium-sensing receptor in keratinocytes impairs epidermal differentiation and barrier function. J Invest Dermatol 132: 2350-2359. doi:10.1038/jid.2012. 159. PubMed: 22622426.
54. Menon GK, Grayson S, Elias PM (1985) Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 84: 508-512. doi: 10.1111/1523-1747.ep12273485. PubMed: 3998499. (Pubitemid 15053207)
55. Forslind B (1987) Quantitative X-ray microanalysis of skin. Particle probe evaluation of the skin barrier function. Acta Derm Venereol Suppl (Stockh) 134: 1-8.
56. Hennings H, Holbrook KA, Yuspa SH (1983) Factors influencing calcium-induced terminal differentiation in cultured mouse epidermal cells. J Cell Physiol 116: 265-281. doi:10.1002/jcp.1041160303. PubMed: 6885930. (Pubitemid 13002689)
57. Pillai S, Bikle DD (1991) Role of intracellular-free calcium in the cornified envelope formation of keratinocytes: differences in the mode of action of extracellular calcium and 1,25 dihydroxyvitamin D3. J Cell Physiol 146: 94-100. doi:10.1002/jcp.1041460113. PubMed: 1990023. (Pubitemid 21910029)
58. Yuspa SH, Kilkenny AE, Steinert PM, Roop DR (1989) Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro. J Cell Biol 109: 1207-1217. doi:10.1083/jcb.109.3.1207. PubMed: 2475508. (Pubitemid 19220102)
59. Su MJ, Bikle DD, Mancianti ML, Pillai S (1994) 1,25-Dihydroxyvitamin D3 potentiates the keratinocyte response to calcium. J Biol Chem 269: 14723-14729. PubMed: 7910167.
60. Zheng X, Bollinger Bollag W (2003) Aquaporin 3 colocates with phospholipase d2 in caveolin-rich membrane microdomains and is downregulated upon keratinocyte differentiation. J Invest Dermatol 121: 1487-1495. doi:10.1111/j.1523-1747.2003.12614.x. PubMed: 14675200. (Pubitemid 38005503)
61. Bollag WB, Xie D, Zheng X, Zhong X (2007) A potential role for the phospholipase D2-aquaporin-3 signaling module in early keratinocyte differentiation: Production of a novel phosphatidylglycerol lipid signal. J Invest Dermatol 127: 2823-2831. PubMed: 17597824. (Pubitemid 350134818)
62. Schlegel A, Lisanti MP (2000) A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo. J Biol Chem 275: 21605-21617. doi:10.1074/jbc.M002558200. PubMed: 10801850. (Pubitemid 30481867)
63. Schlegel A, Schwab RB, Scherer PE, Lisanti MP (1999) A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro. J Biol Chem 274: 22660-22667. doi:10.1074/jbc.274.32.22660. PubMed: 10428847.
64. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW (2008) Caveolin-1 and -2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol Biol Cell 19: 912-928. PubMed: 18162583. (Pubitemid 351481808)
65. Brennan D, Peltonen S, Dowling A, Medhat W, Green KJ et al. (2012) A role for caveolin-1 in desmoglein binding and desmosome dynamics. Oncogene 31: 1636-1648. doi:10.1038/onc.2011.346. PubMed: 21841821.
66. Capozza F, Williams TM, Schubert W, McClain S, Bouzahzah B et al. (2003) Absence of caveolin-1 sensitizes mouse skin to carcinogeninduced epidermal hyperplasia and tumor formation. Am J Pathol, 162: 2029-2039. PubMed: 12759258. (Pubitemid 36613059)
67. Trimmer C, Sotgia F, Lisanti MP, Capozza F (2013) Cav1 inhibits benign skin tumor development in a two-stage carcinogenesis model by suppressing epidermal proliferation. Am J Transl Res 5: 80-91. PubMed: 23390568.
68. Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J et al. (2004) Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J Biol Chem 279: 51630-51646. doi:10.1074/jbc.M409214200. PubMed: 15355971. (Pubitemid 40017914)
69. Roelandt T, Giddelo C, Heughebaert C, Denecker G, Hupe M et al. (2009) The "caveolae brake hypothesis" and the epidermal barrier. J Invest Dermatol 129: 927-936. doi:10.1038/jid.2008.328. PubMed: 19005485.
70. Campbell L, Laidler P, Watson RE, Kirby B, Griffiths CE et al. (2002) Downregulation and altered spatial pattern of caveolin-1 in chronic plaque psoriasis. Br J Dermatol 147: 701-709. doi:10.1046/j.1365-2133.2002.05009.x. PubMed: 12366416. (Pubitemid 35286155)
71. Hansen LA, Alexander N, Hogan ME, Sundberg JP, Dlugosz A et al. (1997) Genetically null mice reveal a central role for epidermal growth factor receptor in the differentiation of the hair follicle and normal hair development. Am J Pathol 150: 1959-1975. PubMed: 9176390. (Pubitemid 27233070)
72. Murillas R, Larcher F, Conti CJ, Santos M, Ullrich A et al. (1995) Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. EMBO J 14: 5216-5223. PubMed: 7489711.
73. Kim JH, Kim JH, Ohba M, Suh PG, Ryu SH (2005) Novel functions of the phospholipase D2-Phox homology domain in protein kinase Czeta activation. Mol Cell Biol 25: 3194-3208. doi:10.1128/MCB.25.8.3194-3208.2005. PubMed: 15798205. (Pubitemid 40464321)
74. Parmentier JH, Pavicevic Z, Malik KU (2006) ANG II stimulates phospholipase D through PKCzeta activation in VSMC: implications in adhesion, spreading, and hypertrophy. Am J Physiol Heart Circ Physiol 290: H46-H54. PubMed: 16113073.
75. Murray NR, Fields AP (1998) Phosphatidylglycerol is a physiologic activator of nuclear protein kinase C. J Biol Chem 273: 11514-11520. doi:10.1074/jbc.273.19.11514. PubMed: 9565565. (Pubitemid 28272046)