Basal caspase-3 activity promotes migration, invasion, and vasculogenic mimicry formation of melanoma cells

Melanoma Research

Volumn 23, Issue 4, 2013, Pages 243-253

  Liu, Yan Rong ^a   Sun, Baocun ^a   Zhao, Xiu Lan ^a   Gu, Qiang ^a   Liu, Zhi Yong ^a   Dong, Xue Yi ^a   Che, Na ^a   Mo, Jing ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

caspase 3; invasion; melanoma; migration; vasculogenic mimicry

Indexed keywords

BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; GELATINASE A; SMALL INTERFERING RNA;

ADULT; APOPTOSIS; ARTICLE; CANCER PATIENT; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN TISSUE; MALE; MELANOMA; MELANOMA CELL; METASTASIS; MICROCIRCULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; MELANOMA; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84879982930     PISSN: 09608931     EISSN: 14735636     Source Type: Journal    
DOI: 10.1097/CMR.0b013e3283625498     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60:277-300.
2. Zbytek B, Carlson JA, Granese J, Ross J, Mihm MC Jr., Slominski A. Current concepts of metastasis in melanoma. Expert Rev Dermatol 2008; 3: 569-585.
3. Nikkola J, Vihinen P, Vuoristo MS, Kellokumpu-Lehtinen P, Kahari VM, Pyrhonen S. High serum levels of matrix metalloproteinase-9 and matrix metalloproteinase-1 are associated with rapid progression in patients with metastatic melanoma. Clin Cancer Res 2005; 11:5158-5166.
4. Candrea E, Senila S, Tatomir C, Cosgarea R. Active and inactive forms of matrix metalloproteinases 2 and 9 in cutaneous melanoma. Int J Dermatol 2012 [Epub ahead of print].
5. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002; 29:15-18.
6. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011; 19:512-526.
7. Murphy EA, Majeti BK, Barnes LA, Makale M, Weis SM, Lutu-Fuga K, et al. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc Natl Acad Sci USA 2008; 105:9343-9348.
8. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155:739-752.
9. Warso MA, Maniotis AJ, Chen X, Majumdar D, Patel MK, Shilkaitis A, et al. Prognostic significance of periodic acid-Schiff-positive patterns in primary cutaneous melanoma. Clin Cancer Res 2001; 7:473-477.
10. Thies A, Mangold U, Moll I, Schumacher U. PAS-positive loops and networks as a prognostic indicator in cutaneous malignant melanoma. J Pathol 2001; 195:537-542.
11. Van Beurden A, Schmitz RF, van Dijk CM, Baeten CI. Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res 2012; 22:424-429.
12. Crawford ED, Seaman JE, Barber AE 2nd, David DC, Babbitt PC, Burlingame AL, et al. Conservation of caspase substrates across metazoans suggests hierarchical importance of signaling pathways over specific targets and cleavage site motifs in apoptosis. Cell Death Differ 2012; 19: 2040-2048.
13. Hyman BT, Yuan J. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci 2012; 13:395-406.
14. Chun HJ, Zheng L, Ahmad M, Wang J, Speirs CK, Siegel RM, et al. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 2002; 419:395-399.
15. Su H, Bidere N, Zheng L, Cubre A, Sakai K, Dale J, et al. Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science 2005; 307:1465-1468.
16. Van Raam BJ, Salvesen GS. Proliferative versus apoptotic functions of caspase-8 Hetero or homo: the caspase-8 dimer controls cell fate. Biochim Biophys Acta 2012; 1824:113-122.
17. Zandy AJ, Lakhani S, Zheng T, Flavell RA, Bassnett S. Role of the executioner caspases during lens development. J Biol Chem 2005; 280:30263-30272.
18. Zermati Y, Garrido C, Amsellem S, Fishelson S, Bouscary D, Valensi F, et al. Caspase activation is required for terminal erythroid differentiation. J Exp Med 2001; 193:247-254.
19. Miura M. Apoptotic and nonapoptotic caspase functions in animal development. Cold Spring Harb Perspect Biol 2012; 4. doi: 10.1101/cshperspect. a008664.
20. Watanabe Y, Akaike T. Possible involvement of caspase-like family in maintenance of cytoskeleton integrity. J Cell Physiol 1999; 179:45-51.
21. Antonopoulos C, Cumberbatch M, Dearman RJ, Daniel RJ, Kimber I, Groves RW. Functional caspase-1 is required for Langerhans cell migration and optimal contact sensitization in mice. J Immunol 2001; 166:3672-3677.
22. Helfer B, Boswell BC, Finlay D, Cipres A, Vuori K, Bong Kang T, et al. Caspase-8 promotes cell motility and calpain activity under nonapoptotic conditions. Cancer Res 2006; 66:4273-4278.
23. Barbero S, Mielgo A, Torres V, Teitz T, Shields DJ, Mikolon D, et al. Caspase-8 association with the focal adhesion complex promotes tumor cell migration and metastasis. Cancer Res 2009; 69:3755-3763.
24. Gdynia G, Grund K, Eckert A, Bock BC, Funke B, Macher-Goeppinger S, et al. Basal caspase activity promotes migration and invasiveness in glioblastoma cells. Mol Cancer Res 2007; 5:1232-1240.
25. Grossman D, Altieri DC. Drug resistance in melanoma: mechanisms, apoptosis, and new potential therapeutic targets. Cancer Metastasis Rev 2001; 20:3-11.
26. Fink D, Schlagbauer-Wadl H, Selzer E, Lucas T, Wolff K, Pehamberger H, et al. Elevated procaspase levels in human melanoma. Melanoma Res 2001; 11:385-393.
27. Woenckhaus C, Giebel J, Failing K, Fenic I, Dittberner T, Poetsch M. Expression of AP-2alpha, c-kit, and cleaved caspase-6 and-3 in naevi and malignant melanomas of the skin. A possible role for caspases in melanoma progression? J Pathol 2003; 201:278-287.
28. Farhana L, Dawson MI, Murshed F, Fontana JA. Maximal adamantyl- substituted retinoid-related molecule-induced apoptosis requires NF-kappaB noncanonical and canonical pathway activation. Cell Death Differ 2011; 18:164-173.
29. Seftor EA, Meltzer PS, Kirschmann DA, Pe'er J, Maniotis AJ, Trent JM, et al. Molecular determinants of human uveal melanoma invasion and metastasis. Clin Exp Metastasis 2002; 19:233-246.
30. Valster A, Tran NL, Nakada M, Berens ME, Chan AY, Symons M. Cell migration and invasion assays. Methods 2005; 37:208-215.
31. Yarbrough WM, Mukherjee R, Stroud RE, Meyer EC, Escobar GP, S ample JA, et al. Caspase inhibition modulates left ventricular remodeling following myocardial infarction through cellular and extracellular mechanisms. J Cardiovasc Pharmacol 2010; 55:408-416.
32. Redondo P, Lloret P, Idoate M, Inoges S. Expression and serum levels of MMP-2 and MMP-9 during human melanoma progression. Clin Exp Dermatol 2005; 30:541-545.
33. Liu JW, Sun P, Yan Q, Paller AS, Gerami P, Ho N, et al. De-N-acetyl GM3 promotes melanoma cell migration and invasion through urokinase plasminogen activator receptor signaling-dependent MMP-2 activation. Cancer Res 2009; 69:8662-8669.
34. Seftor RE, Seftor EA, Koshikawa N, Meltzer PS, Gardner LM, Bilban M, et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 2001; 61:6322-6327.
35. Hess AR, Seftor EA, Seftor RE, Hendrix MJ. Phosphoinositide 3-kinase regulates membrane type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Res 2003; 63:4757-4762.
36. Sun B, Zhang S, Zhang D, Yin X, Wang S, Gu Y, et al. Doxycycline influences microcirculation patterns in B16 melanoma. Exp Biol Med (Maywood) 2007; 232:1300-1307.
37. Lalor SJ, Dungan LS, Sutton CE, Basdeo SA, Fletcher JM, Mills KH. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gammadelta and CD4 T cells that mediate autoimmunity. J Immunol 2011; 186:5738-5748.
38. Dungan LS, Mills KH. Caspase-1-processed IL-1 family cytokines play a vital role in driving innate IL-17. Cytokine 2011; 56:126-132.
39. Huh JR, Vernooy SY, Yu H, Yan N, Shi Y, Guo M, et al. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol 2004; 2:E15.
40. Mukai M, Kusama T, Hamanaka Y, Koga T, Endo H, Tatsuta M, et al. Cross talk between apoptosis and invasion signaling in cancer cells through caspase-3 activation. Cancer Res 2005; 65:9121-9125.
41. Barnhart BC, Legembre P, Pietras E, Bubici C, Franzoso G, Peter ME. CD95 ligand induces motility and invasiveness of apoptosis-resistant tumor cells. EMBO J 2004; 23:3175-3185.
42. Zhao X, Wang D, Zhao Z, Xiao Y, Sengupta S, Zhang R, et al. Caspase-3-dependent activation of calcium-independent phospholipase A2 enhances cell migration in non-apoptotic ovarian cancer cells. J Biol Chem 2006; 281:29357-29368.
43. Yang L, Cao Z, Yan H, Wood WC. Coexistence of high levels of apoptotic signaling and inhibitor of apoptosis proteins in human tumor cells: implication for cancer specific therapy. Cancer Res 2003; 63:6815-6824.
44. Peng XH, Karna P, O'Regan RM, Liu X, Naithani R, Moriarty RM, et al. Down-regulation of inhibitor of apoptosis proteins by deguelin selectively induces apoptosis in breast cancer cells. Mol Pharmacol 2007; 71:101-111.
45. Zheng HC, Sun JM, Wei ZL, Yang XF, Zhang YC, Xin Y. Expression of Fas ligand and caspase-3 contributes to formation of immune escape in gastric cancer. World J Gastroenterol 2003; 9:1415-1420.
46. Vartanian AA, Burova OS, Stepanova EV, Baryshnikov AY. The involvement of apoptosis in melanoma vasculogenic mimicry. Melanoma Res 2007; 17:1-8.
47. Kinosian HJ, Selden LA, Estes JE, Gershman LC. Kinetics of gelsolin interaction with phalloidin-stabilized F-actin. Rate constants for binding and severing. Biochemistry 1996; 35:16550-16556.
48. Furukawa H, Fujita H, Kokubu I, Yamamoto Y, Sasaki S, Chodon T, et al. Identification of a novel gelsolin truncate in the vertical and metastatic phase malignant melanomas. Melanoma Res 2002; 12:523-528.
49. Hofmann UB, Westphal JR, Van Muijen GN, Ruiter DJ. Matrix metalloproteinases in human melanoma. J Invest Dermatol 2000; 115:337-344.
50. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 1998; 187: 1477-1485. Education