Somatostatin inhibits cell migration and reduces cell counts of human keratinocytes and delays epidermal wound healing in an ex vivo wound model

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Vockel, Matthias ^a,b,c   Pollok, Simone ^a   Breitenbach, Ute ^b   Ridderbusch, Ina ^a   Kreienkamp, Hans Jürgen ^a   Brandner, Johanna M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b BEIERSDORF AG   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENYLATE CYCLASE; CYCLIC AMP; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; RAC1 PROTEIN; SOMATOSTATIN; SOMATOSTATIN RECEPTOR; SOMATOSTATIN RECEPTOR 1; SOMATOSTATIN RECEPTOR 2; SOMATOSTATIN RECEPTOR 3; SOMATOSTATIN RECEPTOR 4; SOMATOSTATIN RECEPTOR 5;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME INHIBITION; EPIDERMIS; EPITHELIZATION; EX VIVO STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; LAMELLIPODIUM; NONHUMAN; RE-EPITHELIZATION; SIGNAL TRANSDUCTION; WOUND HEALING IMPAIRMENT; BIOLOGICAL MODEL; CELL MOTION; CYTOLOGY; DRUG EFFECT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WOUND HEALING;

CELL MOVEMENT; EPIDERMIS; HUMANS; KERATINOCYTES; MODELS, BIOLOGICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOMATOSTATIN; WOUND HEALING;

EID: 79955879921     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019740     Document Type: Article

References (58)

1. Gurtner GC, Werner S, Barrandon Y, Longaker MT, (2008) Wound repair and regeneration. Nature 453: 314-321.
2. Martin P, (1997) Wound healing-aiming for perfect skin regeneration. Science 276: 75-81.
3. Chernyavsky AI, Arredondo J, Wess J, Karlsson E, Grando SA, (2004) Novel signaling pathways mediating reciprocal control of keratinocyte migration and wound epithelialization through M3 and M4 muscarinic receptors. J Cell Biol 166: 261-272.
4. Pullar CE, Grahn JC, Liu W, Isseroff RR, (2006) Beta2-adrenergic receptor activation delays wound healing. Faseb J 20: 76-86.
5. Taboubi S, Milanini J, Delamarre E, Parat F, Garrouste F, et al. (2007) G alpha(q/11)-coupled P2Y2 nucleotide receptor inhibits human keratinocyte spreading and migration. Faseb J 21: 4047-4058.
6. Patel YC, (1999) Somatostatin and its receptor family. Front Neuroendocrinol 20: 157-198.
7. Patel YC, Greenwood MT, Warszynska A, Panetta R, Srikant CB, (1994) All five cloned human somatostatin receptors (hSSTR1-5) are functionally coupled to adenylyl cyclase. Biochem Biophys Res Commun 198: 605-612.
8. Cattaneo MG, Amoroso D, Gussoni G, Sanguini AM, Vicentini LM, (1996) A somatostatin analogue inhibits MAP kinase activation and cell proliferation in human neuroblastoma and in human small cell lung carcinoma cell lines. FEBS Lett 397: 164-168.
9. Csaba Z, Dournaud P, (2001) Cellular biology of somatostatin receptors. Neuropeptides 35: 1-23.
10. Kreienkamp HJ, Hönck HH, Richter D, (1997) Coupling of rat somatostatin receptor subtypes to a G-protein gated inwardly rectifying potassium channel (GIRK1). FEBS Lett 419: 92-94.
11. Meriney SD, Gray DB, Pilar GR, (1994) Somatostatin-induced inhibition of neuronal Ca2+ current modulated by cGMP-dependent protein kinase. Nature 369: 336-339.
12. Hall RA, Premont RT, Chow CW, Blitzer JT, Pitcher JA, et al. (1998) The beta2-adrenergic receptor interacts with the Na+/H+-exchanger regulatory factor to control Na+/H+ exchange. Nature 392: 626-630.
13. Christenn M, Kindler S, Schulz S, Buck F, Richter D, et al. (2007) Interaction of brain somatostatin receptors with the PDZ domains of PSD-95. FEBS Lett 581: 5173-5177.
14. Liew CW, Vockel M, Glassmeier G, Brandner JM, Fernandez-Ballester GJ, et al. (2009) Interaction of the human somatostatin receptor 3 with the multiple PDZ domain protein MUPP1 enables somatostatin to control permeability of epithelial tight junctions. FEBS Lett 583: 49-54.
15. Wente W, Efanov AM, Treinies I, Zitzer H, Gromada J, et al. (2005) The PDZ/coiled-coil domain containing protein PIST modulates insulin secretion in MIN6 insulinoma cells by interacting with somatostatin receptor subtype 5. FEBS Lett 579: 6305-6310.
16. Gaudillere A, Misery L, Bernard C, Souchier C, Claudy A, et al. (1997) Presence of somatostatin in normal human epidermis. Br J Dermatol 137: 376-380.
17. Hagströmer L, Emtestam L, Stridsberg M, Talme T, (2006) Expression pattern of somatostatin receptor subtypes 1-5 in human skin: an immunohistochemical study of healthy subjects and patients with psoriasis or atopic dermatitis. Exp Dermatol 15: 950-957.
18. Vockel M, Breitenbach U, Kreienkamp HJ, Brandner JM, (2010) Somatostatin regulates tight junction function and composition in human keratinocytes. Exp Dermatol 19: 888-894.
19. Fantini F, Johansson O, (1995) Neurochemical markers in human cutaneous Merkel cells. An immunohistochemical investigation. Exp Dermatol 4: 365-371.
20. Rohrer SP, Birzin ET, Mosley RT, Berk SC, Hutchins SM, et al. (1998) Rapid identification of subtype-selective agonists of the somatostatin receptor through combinatorial chemistry. Science 282: 737-740.
21. Weckbecker G, Lewis I, Albert R, Schmid HA, Hoyer D, et al. (2003) Opportunities in somatostatin research: biological, chemical and therapeutic aspects. Nat Rev Drug Discov 2: 999-1017.
22. Chang L, Karin M, (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
23. Katz M, Amit I, Yarden Y, (2007) Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim Biophys Acta 1773: 1161-1176.
24. Sauer B, Vogler R, Zimmermann K, Fujii M, Anzano MB, et al. (2004) Lysophosphatidic acid interacts with transforming growth factor-beta signaling to mediate keratinocyte growth arrest and chemotaxis. J Invest Dermatol 123: 840-849.
25. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
26. Khurana S, Tomar A, George S, Wang Y, Siddiqui M, et al. (2008) Autotaxin and lysophosphatidic acid stimulate intestinal cell motility by redistribution of the actin modifying protein villin to the developing lamellipodia. Exp Cell Res 314: 530-542.
27. Etienne-Manneville S, Hall A, (2002) Rho GTPases in cell biology. Nature 420: 629-635.
28. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A, (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70: 401-410.
29. Van Leeuwen FN, Olivo C, Grivell S, Giepmans BN, Collard JG, et al. (2003) Rac activation by lysophosphatidic acid LPA1 receptors through the guanine nucleotide exchange factor Tiam1. J Biol Chem 278: 400-406.
30. Johansson O, Vaalasti A, (1987) Immunohistochemical evidence for the presence of somatostatin-containing sensory nerve fibres in the human skin. Neurosci Lett 73: 225-230.
31. Senapati A, Anand P, McGregor GP, Ghatei MA, Thompson RP, et al. (1986) Depletion of neuropeptides during wound healing in rat skin. Neurosci Lett 71: 101-105.
32. Benali N, Cordelier P, Calise D, Pages P, Rochaix P, et al. (2000) Inhibition of growth and metastatic progression of pancreatic carcinoma in hamster after somatostatin receptor subtype 2 (sst2) gene expression and administration of cytotoxic somatostatin analog AN-238. Proc Natl Acad Sci U S A 97: 9180-9185.
33. Bousquet C, Guillermet J, Vernejoul F, Lahlou H, Buscail L, et al. (2004) Somatostatin receptors and regulation of cell proliferation. Dig Liver Dis 36 (Suppl 1): S2-7.
34. Cordelier P, Esteve JP, Bousquet C, Delesque N, O'Carroll AM, et al. (1997) Characterization of the antiproliferative signal mediated by the somatostatin receptor subtype sst5. Proc Natl Acad Sci U S A 94: 9343-9348.
35. Haegerstrand A, Jonzon B, Dalsgaard CJ, Nilsson J, (1989) Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes. Proc Natl Acad Sci U S A 86: 5993-5996.
36. Cattaneo MG, Gentilini D, Vicentini LM, (2006) Deregulated human glioma cell motility: inhibitory effect of somatostatin. Mol Cell Endocrinol 256: 34-39.
37. Pola S, Cattaneo MG, Vicentini LM, (2003) Anti-migratory and anti-invasive effect of somatostatin in human neuroblastoma cells: involvement of Rac and MAP kinase activity. J Biol Chem 278: 40601-40606.
38. McCawley LJ, Li S, Benavidez M, Halbleib J, Wattenberg EV, et al. (2000) Elevation of intracellular cAMP inhibits growth factor-mediated matrix metalloproteinase-9 induction and keratinocyte migration. Mol Pharmacol 58: 145-151.
39. Chen J, Hoffman BB, Isseroff RR, (2002) Beta-adrenergic receptor activation inhibits keratinocyte migration via a cyclic adenosine monophosphate-independent mechanism. J Invest Dermatol 119: 1261-1268.
40. Bartolome R, Wright N, Molina-Ortiz I, Sanchez-Luque F, Teixido J, (2008) Activated G(alpha)13 impairs cell invasiveness through p190RhoGAP-mediated inhibition of RhoA activity. Cancer Res 68: 8221-8230.
41. Lutz S, Freichel-Blomquist A, Yang Y, Rumenapp U, Jakobs KH, et al. (2005) The guanine nucleotide exchange factor p63RhoGEF, a specific link between Gq/11-coupled receptor signaling and RhoA. J Biol Chem 280: 11134-11139.
42. Yamada T, Ohoka Y, Kogo M, Inagaki S, (2005) Physical and functional interactions of the lysophosphatidic acid receptors with PDZ domain-containing Rho guanine nucleotide exchange factors (RhoGEFs). J Biol Chem: pp. 19358-19363.
43. Tscharntke M, Pofahl R, Chrostek-Grashoff A, Smyth N, Niessen C, et al. (2007) Impaired epidermal wound healing in vivo upon inhibition or deletion of Rac1. J Cell Sci 120: 1480-1490.
44. Liu S, Kapoor M, Leask A, (2009) Rac1 expression by fibroblasts is required for tissue repair in vivo. Am J Pathol 174: 1847-1856.
45. Mills GB, Moolenaar WH, (2003) The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3: 582-591.
46. Meyer zu Heringdorf D, Jakobs KH, (2007) Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 1768: 923-940.
47. Vockel M, Breitenbach U, Kreienkamp HJ, Brandner JM, (2010) Somatostatin regulates Tight Junction function and composition in human keratinocytes. Exp Dermato 19: 888-94.
48. Waddell BE, Calton WC Jr, Steinberg SR, Martindale RG, (1997) The adverse effects of octreotide on wound healing in rats. Am Surg 63: 446-449.
49. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601.
50. Kasper M, Jaks V, Are A, Bergstrom A, Schwager A, et al. (2011) Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci U S A 108: 4099-4104.
51. Wong SY, Reiter JF, (2011) From the Cover: Wounding mobilizes hair follicle stem cells to form tumors. Proc Natl Acad Sci U S A 108: 4093-4098.
52. Schafer M, Werner S, (2008) Cancer as an overhealing wound: an old hypothesis revisited. Nat Rev Mol Cell Biol 9: 628-638.
53. Patel YC, Srikant CB, (1994) Subtype selectivity of peptide analogs for all five cloned human somatostatin receptors (hsstr 1-5). Endocrinology 135: 2814-2817.
54. Rheinwald JG, Green H, (1975) Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6: 331-343.
55. Brandner JM, Kief S, Grund C, Rendl M, Houdek P, et al. (2002) Organization and formation of the tight junction system in human epidermis and cultured keratinocytes. Eur J Cell Biol 81: 253-263.
56. Benard V, Bohl BP, Bokoch GM, (1999) Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274: 13198-13204.
57. Brandner JM, Houdek P, Quitschau T, Siemann-Harms U, Ohnemus U, et al. (2006) An ex-vivo model to evaluate dressings & drugs for wound healing. Example: Influence of lucilia sericata extracts on wound healing progress. EWMA J 6: 11-15.
58. Pollok S, Pfeiffer AC, Lobmann R, Wright CS, Moll I, et al. (2010) Connexin 43 mimetic peptide Gap27 reveals potential differences in the role of Cx43 in wound repair between diabetic and non-diabetic cells. J Cell Mol Med.