Desmoglein 2 depletion leads to increased migration and upregulation of the chemoattractant secretoneurin in melanoma cells

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Peitsch, Wiebke K ^a,b   Doerflinger, Yvette ^a,b   Fischer Colbrie, Reiner ^c   Huck, Volker ^a   Bauer, Alexander T ^a   Utikal, Jochen ^a,b   Goerdt, Sergij ^a   Schneider, Stefan W ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

DESMOGLEIN 2; SECRETOGRANIN II; SECRETONEURIN;

ARTICLE; CELL INVASION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MELANOMA CELL; PROTEIN DEPLETION; PROTEIN FUNCTION; RNA INTERFERENCE; SGII GENE; TUMOR CELL LINE; UPREGULATION;

BROMODEOXYURIDINE; CELL LINE, TUMOR; CELL MOVEMENT; DESMOGLEIN 2; ELECTRIC IMPEDANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MELANOMA; MICROSCOPY, FLUORESCENCE; RADIOIMMUNOASSAY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SECRETOGRANIN II;

EID: 84895880924     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089491     Document Type: Article

References (68)

1. Brandner JM, Haass NK (2013) Melanoma's connections to the tumour microenvironment. Pathology 45: 443-452.
2. Kuphal S, Bosserhoff AK (2012) E-cadherin cell-cell communication in melanogenesis and during development of malignant melanoma. Arch Biochem Biophys 524: 43-47.
3. Green KJ, Simpson CL (2007) Desmosomes: new perspectives on a classic. J Invest Dermatol 127: 2499-2515. (Pubitemid 47585074)
4. Tang A, Eller MS, Hara M, Yaar M, Hirohashi S, et al. (1994) E-cadherin is the major mediator of human melanocyte adhesion to keratinocytes in vitro. J Cell Sci 107: 983-992. (Pubitemid 24119356)
5. Nishimura EK, Yoshida H, Kunisada T, Nishikawa SI (1999) Regulation of E- and P-cadherin expression correlated with melanocyte migration and diversification. Dev Biol 215: 155-166.
6. Hsu MY, Wheelock MJ, Johnson KR, Herlyn M (1996) Shifts in cadherin profiles between human normal melanocytes and melanomas. J Investig Dermatol Symp Proc 1: 188-194.
7. Berx G, van Roy (2009) Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol 1: a003129.
8. Li G, Satyamoorthy K, Herlyn M (2001) N-cadherin-mediated intercellular interactions promote survival and migration of melanoma cells. Cancer Res 61: 3819-3825. (Pubitemid 32694999)
9. Qi J, Chen N, Wang J, Siu CH (2005) Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. Mol Biol Cell 16: 4386-4397. (Pubitemid 41262905)
10. Qi J, Wang J, Romanyuk O, Siu CH (2006) Involvement of Src family kinases in N-cadherin phosphorylation and beta-catenin dissociation during transendothelial migration of melanoma cells. Mol Biol Cell 17: 1261-1272. (Pubitemid 43376547)
11. Kuphal S, Poser I, Jobin C, Hellerbrand C, Bosserhoff AK (2004) Loss of E-cadherin leads to upregulation of NFkappaB activity in malignant melanoma. Oncogene 23: 8509-8519. (Pubitemid 39540801)
12. Kuphal S, Bosserhoff AK (2006) Influence of the cytoplasmic domain of E-cadherin on endogenous N-cadherin expression in malignant melanoma. Oncogene 25: 248-259. (Pubitemid 43083686)
13. Maret D, Gruzglin E, Sadr MS, Siu V, Shan W, et al. (2010) Surface expression of precursor N-cadherin promotes tumor cell invasion. Neoplasia 12: 1066-1080.
14. Hsu MY, Meier FE, Nesbit M, Hsu JY, Van Belle P, et al. (2000) E-cadherin expression in melanoma cells restores keratinocyte-mediated growth control and down-regulates expression of invasion-related adhesion receptors. Am J Pathol 156: 1515-1525. (Pubitemid 30646691)
15. Li G, Fukunaga M, Herlyn M (2004) Reversal of melanocytic malignancy by keratinocytes is an E-cadherin-mediated process overriding beta-catenin signaling. Exp Cell Res 297: 142-151. (Pubitemid 38759569)
16. Spangler B, Vardimon L, Bosserhoff AK, Kuphal S (2011) Post-transcriptional regulation controlled by E-cadherin is important for c-Jun activity in melanoma. Pigment Cell Melanoma Res 24: 148-164.
17. Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, et al. (2012) Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 181: 1115-1125.
18. Van Marck V, Stove C, Van Den Bossche K, Stove V, Paredes J, et al. (2005) P-cadherin promotes cell-cell adhesion and counteracts invasion in human melanoma. Cancer Res 65: 8774-8783. (Pubitemid 41379401)
19. Kuphal S, Martyn AC, Pedley J, Crowther LM, Bonazzi VF, et al. (2009) H-cadherin expression reduces invasion of malignant melanoma. Pigment Cell Melanoma Res 22: 296-306.
20. Bosserhoff AK, Ellmann L, Quast AS, Eberle J, Boyle GM, et al. (2013) Loss of T-cadherin (CDH-13) regulates AKT signaling and desensitizes cells to apoptosis in melanoma. Mol Carcinog 2013 Apr 26. doi: 10.1002/mc.22018. [Epub ahead of print]
21. Schmitt CJ, Franke WW, Goerdt S, Falkowska-Hansen B, Rickelt S, et al. (2007) Homo- and heterotypic cell contacts in malignant melanoma cells and desmoglein 2 as a novel solitary surface glycoprotein. J Invest Dermatol 127: 2191-2206. (Pubitemid 47258491)
22. Schäfer S, Koch PJ, Franke WW (1994) Identification of the ubiquitous human desmoglein, Dsg2, and the expression catalogue of the desmoglein subfamily of desmosomal cadherins. Exp Cell Res 211: 391-399. (Pubitemid 24174973)
23. Pieperhoff S, Franke WW (2007) The area composita of adhering junctions connecting heart muscle cells of vertebrates - IV: coalescence and amalgamation of desmosomal and adhaerens junction components - late processes in mammalian heart development. Eur J Cell Biol 86: 377-391. (Pubitemid 46971921)
24. Pieperhoff S, Barth M, Rickelt S, Franke WW (2010) Desmosomal molecules in and out of adhering junctions: normal and diseased states of epidermal, cardiac and mesenchymally derived cells. Dermatol Res Pract 2010: 139167.
25. Peitsch WK, Grund C, Kuhn C, Schnölzer M, Spring H, et al. (1999) Drebrin is widespread actin-associating protein enriched at junctional plaques, defining a specific microfilament anchorage system in polar epithelial cells. Eur J Cell Biol 78: 767-778.
26. Zak J, Schneider SW, Eue I, Ludwig T, Oberleithner H (2000) High-resistance MDCK-C7 monolayers used for measuring invasive potency of tumour cells. Pflugers Arch 440: 179-183. (Pubitemid 30265926)
27. Ludwig T, Ossig R, Graessel S, Wilhelmi M, Oberleithner H, et al. (2002) The electrical resistance breakdown assay determines the role of proteinases in tumor cell invasion. Am J Physiol Renal Physiol 283: F319-327.
28. Schnaeker EM, Ossig R, Ludwig T, Dreier R, Oberleithner H, et al. (2004) Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res 64: 8924-8931. (Pubitemid 39665499)
29. Schneider SW, Ludwig T, Tatenhorst L, Braune S, Oberleithner H, et al. (2004) Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol 107: 272-276. (Pubitemid 38263418)
30. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, et al. (1992) Analysis of gene expression in single live neurons. Proc Natl Acad Sci USA 89: 3010-3014.
31. Kirchmair R, Hogue-Angeletti R, Gutierrez J, Fischer-Colbrie R, Winkler H (1993) Secretoneurin - a neuropeptide generated in brain, adrenal medulla and other endocrine tissues by proteolytic processing of secretogranin II (chromogranin C). Neuroscience 53: 359-365. (Pubitemid 23101320)
32. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, et al. (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4: R28.
33. Fischer-Colbrie R, Kirchmair R, Kähler CM, Wiedermann CJ, Saria A (2005) Secretoneurin: a new player in angiogenesis and chemotaxis linking nerves, blood vessels and the immune system. Curr Protein Pept Sci 6: 373-385. (Pubitemid 41052403)
34. Kähler CM, Bellmann R, Reinisch N, Schratzberger P, Gruber B, et al. (1996). Stimulation of human skin fibroblast migration by the neuropeptide secretoneurin. Eur J Pharmacol 304: 135-139. (Pubitemid 26342683)
35. Kähler CM, Kirchmair R, Kaufmann G, Kähler ST, Reinisch N, et al. (1997) Inhibition of proliferation and stimulation of migration of endothelial cells by secretoneurin in vitro. Arterioscler Thromb Vasc Biol 17: 932-939. (Pubitemid 27209272)
36. Kähler CM, Schratzberger P, Wiedermann CJ (1997) Response of vascular smooth muscle cells to the neuropeptide secretoneurin. A functional role for migration and proliferation in vitro. Arterioscler Thromb Vasc Biol 17: 2029-2035. (Pubitemid 28057104)
37. Helle KB (2010) Regulatory peptides from chromogranin A and secretogranin II: putative modulators of cells and tissues involved in inflammatory conditions. Regul Pept 165: 45-51.
38. Lorch JH, Klessner J, Park JK, Getsios S, Wu YL, et al. (2004) Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens intercellular adhesion in squamous cell carcinoma cells. J Biol Chem 279: 37191-37200. (Pubitemid 39129070)
39. Lorch JH, Thomas TO, Schmoll HJ (2007) Bortezomib inhibits cell-cell adhesion and cell migration and enhances epidermal growth factor receptor inhibitor-induced cell death in squamous cell cancer. Cancer Res 67: 727-734. (Pubitemid 46192213)
40. Schlegel N, Meir M, Heupel WM, Holthöfer B, Leube RE, et al. (2010) Desmoglein 2-mediated adhesion is required for intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 298: G774-783.
41. Hartlieb E, Kempf B, Partilla M, Vigh B, Spindler V, et al. (2013) Desmoglein 2 is less important than desmoglein 3 for keratinocyte cohesion. PLoS One 8: e53739.
42. 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.
43. Dusek RL, Godsel LM, Green KJ (2007) Discriminating roles of desmosomal cadherins: beyond desmosomal adhesion. J Dermatol Sci 45: 7-21. (Pubitemid 44969513)
44. Wang H, Li ZY, Liu Y, Persson J, Beyer I, et al. (2011) Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat Med 17: 96-104.
45. Beyer I, van Rensburg R, Strauss R, Li Z, Wang H, et al. (2011) Epithelial junction opener JO-1 improves monoclonal antibody therapy of cancer. Cancer Res 71: 7080-7090.
46. Beyer I, Cao H, Persson J, Song H, Richter M, et al. (2012) Coadministration of epithelial junction opener JO-1 improves the efficacy and safety of chemotherapeutic drugs. Clin Cancer Res 18: 3340-3351.
47. Brennan D, Hu Y, Joubeh S, Choi YW, Whitaker-Menezes D, et al. (2007) Suprabasal Dsg2 expression in transgenic mouse skin confers a hyperproliferative and apoptosis-resistant phenotype to keratinocytes. J Cell Sci 120: 758-771. (Pubitemid 46523478)
48. Nava P, Laukoetter MG, Hopkins AM, Laur O, Gerner-Smidt K, et al. (2007) Desmoglein-2: a novel regulator of apoptosis in the intestinal epithelium. Mol Biol Cell 18: 4565-4578. (Pubitemid 350060182)
49. Cirillo N, Lanza M, De Rosa A, Cammarota M, La Gatta A, et al. (2008) The most widespread desmosomal cadherin, desmoglein 2, is a novel target of caspase 3-mediated apoptotic machinery. J Cell Biochem 103: 598-606. (Pubitemid 351171930)
50. Eshkind L, Tian Q, Schmidt A, Franke WW, Windoffer R, et al. (2002) Loss of desmoglein 2 suggests essential functions for early embryonic development and proliferation of embryonal stem cells. Eur J Cell Biol 81: 592-598. (Pubitemid 35446792)
51. Brennan D, Hu Y, Joubeh S, Choi YW, Whitaker-Menezes D, et al. (2007) Suprabasal Dsg2 expression in transgenic mouse skin confers a hyperproliferative and apoptosis-resistant phenotype to keratinocytes. J Cell Sci 120: 758-771. (Pubitemid 46523478)
52. Kurzen H, Münzing I, Hartschuh W (2003) Expression of desmosomal proteins in squamous cell carcinomas of the skin. J Cutan Pathol 30: 621-630. (Pubitemid 37372350)
53. Trojan L, Schaaf A, Steidler A, Haak M, Thalmann G, et al. (2005) Identification of metastasis-associated genes in prostate cancer by genetic profiling of human prostate cancer cell lines. Anticancer Res 25: 183-191. (Pubitemid 40470109)
54. Brennan D, Mahoney MG (2009) Increased expression of Dsg2 in malignant skin carcinomas: A tissue-microarray based study. Cell Adh Migr 3: 148-154.
55. Biedermann K, Vogelsang H, Becker I, Plaschke S, Siewert JR, et al. (2005) Desmoglein 2 is expressed abnormally rather than mutated in familial and sporadic gastric cancer. J Pathol 207: 199-206. (Pubitemid 41404150)
56. Yashiro M, Nishioka N, Hirakawa K (2006) Decreased expression of the adhesion molecule desmoglein-2 is associated with diffuse-type gastric carcinoma. Eur J Cancer 14: 2397-2403. (Pubitemid 44307618)
57. Rickelt S, Franke WW, Doerflinger Y, Goerdt S, Brandner JM, et al. (2008) Subtypes of melanocytes and melanoma cells distinguished by their intercellular contacts: heterotypic adherens junctions, adhesive associations, and dispersed desmoglein 2 glycoproteins. Cell Tissue Res 334: 401-422.
58. Reinisch N, Kirchmair R, Kähler CM, Hogue-Angeletti R, Fischer-Colbrie R, et al. (1993) Attraction of human monocytes by the neuropeptide secretoneurin. FEBS Lett 334: 41-44. (Pubitemid 23323034)
59. Schratzberger P, Wöll E, Reinisch N, Kähler CM, Wiedermann CJ (1996) Secretoneurin-induced in vitro chemotaxis of human monocytes is inhibited by pertussis toxin and an inhibitor of protein kinase C. Neurosci Lett 214: 208-210. (Pubitemid 26284469)
60. Dunzendorfer S, Schratzberger P, Reinisch N, Kähler CM, Wiedermann CJ (1998) Secretoneurin, a novel neuropeptide, is a potent chemoattractant for human eosinophils. Blood 91: 1527-1532. (Pubitemid 28110315)
61. Dunzendorfer S, Kaser A, Meierhofer C, Tilg H, Wiedermann CJ (2001) Cutting edge: peripheral neuropeptides attract immature and arrest mature blood-derived dendritic cells. J Immunol 166: 2167-2172. (Pubitemid 32173444)
62. Kähler CM, Schratzberger P, Kaufmann G, Hochleitner B, Bechter O, et al. (2002) Transendothelial migration of leukocytes and signaling mechanisms in response to the neuropeptide secretoneurin. Regul Pept 105: 35-46. (Pubitemid 34164381)
63. Yan S, Wang X, Chai H, Wang H, Yao Q, et al. (2006) Secretoneurin increases monolayer permeability in human coronary artery endothelial cells. Surgery 140: 243-251. (Pubitemid 44176069)
64. Albrecht-Schgoer K, Schgoer W, Holfeld J, Theurl M, Wiedemann D, et al. (2012) The angiogenic factor secretoneurin induces coronary angiogenesis in a model of myocardial infarction by stimulation of vascular endothelial growth factor signaling inendothelial cells. Circulation 126: 2491-2501.
65. Kirchmair R, Egger M, Walter DH, Eisterer W, Niederwanger A, et al. (2004a) Secretoneurin, an angiogenic neuropeptide, induces postnatal vasculogenesis. Circulation 110: 1121-1127. (Pubitemid 39319012)
66. Kirchmair R, Gander R, Egger M, Hanley A, Silver M, et al. (2004b) The neuropeptide secretoneurin acts as a direct angiogenic cytokine in vitro and in vivo. Circulation 109: 777-783. (Pubitemid 38222899)
67. Egger M, Schgoer W, Beer AG, Jeschke J, Leierer J, et al. (2007) Hypoxia upregulates the angiogenic cytokine secretoneurin via an HIF-1alpha- and basic FGF-dependent pathway in muscle cells. FASEB J 21: 2906-2917. (Pubitemid 47372757)
68. Schgoer W, Theurl M, Jeschke J, Beer AG, Albrecht K, et al. (2009) Gene therapy with the angiogenic cytokine secretoneurin induces therapeutic angiogenesis by a nitric oxide-dependent mechanism. Circ Res 105: 994-1002.