CAF-secreted annexin A1 induces prostate cancer cells to gain stem cell-like features

Molecular Cancer Research

Volumn 12, Issue 4, 2014, Pages 607-621

  Geary, Lauren A ^a   Nash, Kevin A ^a   Adisetiyo, Helty ^a   Liang, Mengmeng ^a   Liao, Chun Peng ^a   Jeong, Joseph H ^b   Zandi, Ebrahim ^a   Roy Burman, Pradip ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; ATAXIN 1; LIPOCORTIN 1; PROTEIN P63;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN SECRETION; STEM CELL; TUMOR CELL LINE; TUMOR SPHEROID; ANIMAL; CANCER STEM CELL; CASTRATION RESISTANT PROSTATE CANCER; DISEASE MODEL; HUMAN; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ANNEXIN A1; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FIBROBLASTS; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; NEOPLASTIC STEM CELLS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; SIGNAL TRANSDUCTION;

EID: 84899480372     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-13-0469     Document Type: Article

References (49)

1. Crompton MR, Moss SE, Crumpton MJ. Diversity in the lipocortin/calpactin family. Cell 1988;55:1-3.
2. Crumpton MJ, Dedman JR. Protein terminology tangle. Nature 1990;345:212.
3. Raynal P, Pollard HB. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta 1994;1197: 63-93.
4. Blackwell GJ, Carnuccio R, Di Rosa M, Flower RJ, Parente L, Persico P. Macrocortin: a polypeptide causing the anti-phospholipase effect of glucocorticoids. Nature 1980;287:147-9.
5. Miele L, Cordella-Miele E, Facchiano A, Mukherjee AB. Novel antiinflammatory peptides from the region of highest similarity between uteroglobin and lipocortin I. Nature 1988;335:726-30.
6. Gavins FN, Yona S, Kamal AM, Flower RJ, Perretti M. Leukocyte antiadhesive actions of annexin 1: ALXR- and FPR-related anti-inflammatory mechanisms. Blood 2003;101:4140-7.
7. Getting SJ, Flower RJ, Perretti M. Inhibition of neutrophil and monocyte recruitment by endogenous and exogenous lipocortin 1. Br J Pharmacol 1997;120:1075-82.
8. Parente L, Solito E. Annexin 1: more than an anti-phospholipase protein. Inflamm Res 2004;53:125-32.
9. Hsiang CH, Tunoda T, Whang YE, Tyson DR, Ornstein DK. The impact of altered annexin I protein levels on apoptosis and signal transduction pathways in prostate cancer cells. Prostate 2006;66: 1413-24.
10. Skouteris GG, Schroder CH. The hepatocyte growth factor receptor kinase-mediated phosphorylation of lipocortin-1 transduces the proliferating signal of the hepatocyte growth factor. J Biol Chem 1996; 271:27266-73.
11. Christmas P, Callaway J, Fallon J, Jones J, Haigler HT. Selective secretion of annexin 1, a protein without a signal sequence, by the human prostate gland. J Biol Chem 1991;266:2499-507.
12. D'Acquisto F, Perretti M, Flower RJ. Annexin-A1: a pivotal regulator of the innate and adaptive immune systems. Br J Pharmacol 2008; 155:152-69.
13. Perretti M, Croxtall JD, Wheller SK, Goulding NJ, Hannon R, Flower RJ. Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat Med 1996;2:1259-62.
14. Chapman LP, Epton MJ, Buckingham JC, Morris JF, Christian HC. Evidence for a role of the adenosine 50-triphosphate-binding cassette transporter A1 in the externalization of annexin I from pituitary folliculostellate cells. Endocrinology 2003;144:1062-73.
15. Morris JF, Christian HC, Chapman LP, Epton MJ, Buckingham JC, Ozawa H. Steroid effects on secretion from subsets of lactotrophs: role of folliculo-stellate cells and annexin 1. Arch Physiol Biochem 2002; 110:54-61.
16. Payne CM, Morris JF, Solito E, Buckingham JC. Modulators of the SUR2B/Kir6.1 ATP-sensitive K+channel regulate annexin 1 release in the TtT/GF folliculostellate cell line. In 24th Joint Meeting of the British Endocrine Societies 2005. Endocrine Abstracts 2005;9:OC22.
17. Wein S, Fauroux M, Laffitte J, de Nadai P, Guaini C, Pons F. Mediation of annexin 1 secretion by a probenecid-sensitive ABC-transporter in rat inflamed mucosa. Biochem Pharmacol 2004;67:1195-202.
18. John CD, Christian HC, Morris JF, Flower RJ, Solito E, Buckingham JC. Kinase-dependent regulation of the secretion of thyrotrophin and luteinizing hormone by glucocorticoids and annexin 1 peptides. J Neuroendocrinol 2003;15:946-57.
19. Solito E, Christian HC, Festa M, Mulla A, Tierney T, Flower RJ. Posttranslational modification plays an essential role in the translocation of annexin A1 from the cytoplasm to the cell surface. FASEB J 2006; 20:1498-500.
20. Solito E, Mulla A, Morris JF, Christian HC, Flower RJ, Buckingham JC. Dexamethasone induces rapid serine-phosphorylation and membrane translocation of annexin 1 in a human folliculostellate cell line via a novel nongenomic mechanism involving the glucocorticoid receptor, protein kinase C, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase. Endocrinology 2003;144:1164-74.
21. John CD, Gavins FN, Buss NA, Cover PO, Buckingham JC. Annexin A1 and the formyl peptide receptor family: neuroendocrine and metabolic aspects. Curr Opin Pharmacol 2008;8:765-76.
22. Lange C, Starrett DJ, Goetsch J, Gerke V, Rescher U. Transcriptional profiling of human monocytes reveals complex changes in the expression pattern of inflammation-related genes in response to the annexin A1-derived peptide Ac1-25. J Leukoc Biol 2007;82:1592-604.
23. Perretti M, D'Acquisto F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 2009;9:62-70.
24. Tagoe CE, Marjanovic N, Park JY, Chan ES, Abeles AM, Attur M. Annexin-1 mediates TNF-alpha-stimulated matrix metalloproteinase secretion from rheumatoid arthritis synovial fibroblasts. J Immunol 2008;181:2813-20.
25. Ernst S, Lange C, Wilbers A, Goebeler V, Gerke V, Rescher U. An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J Immunol 2004;172:7669-76.
26. Perretti M, Chiang N, La M, Fierro IM, Marullo S, Getting SJ. Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat Med 2002;8:1296-302.
27. Hayhoe RP, Kamal AM, Solito E, Flower RJ, Cooper D, Perretti M. Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement. Blood 2006;107:2123-30.
28. Lim LH, Pervaiz S. Annexin 1: the new face of an old molecule. FASEB J 2007;21:968-75.
29. Kang JS, Calvo BF, Maygarden SJ, Caskey LS, Mohler JL, Ornstein DK. Dysregulation of annexin I protein expression in high-grade prostatic intraepithelial neoplasia and prostate cancer. Clin Cancer Res 2002;8:117-23.
30. Patton KT, Chen HM, Joseph L, Yang XJ. Decreased annexin I expression in prostatic adenocarcinoma and in high-grade prostatic intraepithelial neoplasia. Histopathology 2005;47:597-601.
31. Paweletz CP, Ornstein DK, Roth MJ, Bichsel VE, Gillespie JW, Calvert VS. Loss of annexin 1 correlates with early onset of tumorigenesis in esophageal and prostate carcinoma. Cancer Res 2000; 60:6293-7.
32. Smitherman AB, Mohler JL, Maygarden SJ, Ornstein DK. Expression of annexin I, II and VII proteins in androgen stimulated and recurrent prostate cancer. J Urol 2004;171(2 Pt 1):916-20.
33. Xin W, Rhodes DR, Ingold C, Chinnaiyan AM, Rubin MA. Dysregulation of the annexin family protein family is associated with prostate cancer progression. Am J Pathol 2003;162:255-61.
34. Khau T, Langenbach SY, Schuliga M, Harris T, Johnstone CN, Anderson RL. Annexin-1 signals mitogen-stimulated breast tumor cell proliferation by activation of the formyl peptide receptors (FPRs) 1 and 2. FASEB J 2011;25:483-96.
35. Liao CP, Adisetiyo H, Liang M, Roy-Burman P. Cancer-associated fibroblasts enhance the gland-forming capability of prostate cancer stem cells. Cancer Res 2010;70:7294-303.
36. Liao CP, Liang M, Cohen MB, Flesken-Nikitin A, Jeong JH, Nikitin AY. Mouse models of prostate adenocarcinoma with the capacity to monitor spontaneous carcinogenesis by bioluminescence or fluorescence. Cancer Res 2007;67:7525-33.
37. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J. Prostatespecific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003;4:209-21.
38. Xin L, Lukacs RU, Lawson DA, Cheng D, Witte ON. Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 2007;25:2760-9.
39. Yang S, Pham LK, Liao CP, Frenkel B, Reddi AH, Roy-Burman P. A novel bone morphogenetic protein signaling in heterotypic cell interactions in prostate cancer. Cancer Res 2008;68: 198-205.
40. Liao CP, Liang M, Cohen MB, Flesken-Nikitin A, Jeong JH, Nikitin AY. Mouse prostate cancer cell lines established from primary and postcastration recurrent tumors. Horm Cancer 2010;1:44-54.
41. Burgess RR. Protein precipitation techniques. Methods Enzymol 2009;463:331-42.
42. Lukacs RU, Goldstein AS, Lawson DA, Cheng D, Witte ON. Isolation, cultivation and characterization of adult murine prostate stem cells. Nat Protoc 2010;5:702-13.
43. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON. Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci U S A 2007;104:181-6.
44. Mulholland DJ, Xin L, Morim A, Lawson D, Witte O, Wu H. Lin-Sca-1+CD49f high stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res 2009;69: 8555-62.
45. de Graauw M, van Miltenburg MH, Schmidt MK, Pont C, Lalai R, Kartopawiro J. Annexin A1 regulates TGF-beta signaling and promotes metastasis formation of basal-like breast cancer cells. Proc Natl Acad Sci U S A 2010;107:6340-5.
46. Lawson DA, Xin L, Lukacs R, Xu Q, Cheng D, Witte ON. Prostate stem cells and prostate cancer. Cold Spring Harb Symp Quant Biol 2005; 70:187-96.
47. Bitto E, Li M, Tikhonov AM, Schlossman ML, Cho W. Mechanism of annexin I-mediated membrane aggregation. Biochemistry 2000;39: 13469-77.
48. Lambert O, Gerke V, Bader MF, Porte F, Brisson A. Structural analysis of junctions formed between lipid membranes and several annexins by cryo-electron microscopy. J Mol Biol 1997;272:42-55.
49. Mailliard WS, Haigler HT, Schlaepfer DD. Calcium-dependent binding of S100C to the N-terminal domain of annexin I. J Biol Chem 1996; 271:719-25.