SPARC mediates metastatic cooperation between CSC and non-CSC prostate cancer cell subpopulations

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Mateo, Francesca ^a,b   Meca Cortés, Óscar ^a,b   Celià Terrassa, Toni ^a,h   Fernández, Yolanda ^b,c   Abasolo, Ibane ^b,c   Sánchez Cid, Lourdes ^a,d   Bermudo, Raquel ^d   Sagasta, Amaia ^e   Rodríguez Carunchio, Leonardo ^e   Pons, Mònica ^a   Cánovas, Verónica ^c   Marín Aguilera, Mercedes ^e   Mengual, Lourdes ^d,e   Alcaraz, Antonio ^d,e   Schwartz, Simó ^b   Mellado, Begoña ^e   Aguilera, Kristina Y ^f   Brekken, Rolf ^f   Fernández, Pedro L ^d,e,g   Paciucci, Rosanna ^c   Thomson, Timothy M ^a,b   more..

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^e HOSPITAL CLÍNIC   (Spain)

^f UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^g UNIVERSITY OF BARCELONA   (Spain)

^h PRINCETON UNIVERSITY   (United States)

Author keywords

Cell cooperation; Metastasis; SPARC; Tumor heterogeneity

Indexed keywords

OSTEONECTIN; CONDITIONED MEDIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL SUBPOPULATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METASTASIS POTENTIAL; MOLECULAR CLONING; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR INVASION; CELL PROLIFERATION; CONDITIONED MEDIUM; DRUG EFFECTS; EPITHELIUM; EXTRACELLULAR SPACE; LYMPH NODE METASTASIS; MALE; METABOLISM; PATHOLOGY; PHARMACOLOGY; PROSTATE TUMOR; SECRETION (PROCESS); TUMOR CELL LINE;

MUS;

CELL LINE, TUMOR; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; EPITHELIUM; EXTRACELLULAR SPACE; HUMANS; LYMPHATIC METASTASIS; MALE; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; OSTEONECTIN; PROSTATIC NEOPLASMS;

EID: 84934891309     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-237     Document Type: Article

References (68)

1. Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell 1, 144:646-674. 10.1016/j.cell.2011.02.013
2. Balkwill F: Cancer and the chemokine network. Nat Rev Cancer 1, 4:540-550. 10.1038/nrc1388
3. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, Teng SC, Wu KJ: Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 1, 10:295-305. 10.1038/ncb1691
4. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA: Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 1, 449:557-563. 10.1038/nature06188
5. Merlo LM, Pepper JW, Reid BJ, Maley CC: Cancer as an evolutionary and ecological process. Nat Rev Cancer 1, 6:924-935. 10.1038/nrc2013
6. Moreno E: Is cell competition relevant to cancer? Nat Rev Cancer 1, 8:141-147. 10.1038/nrc2252
7. Axelrod R, Axelrod DE, Pienta KJ: Evolution of cooperation among tumor cells. Proc Natl Acad Sci U S A 1, 103:13474-13479. 10.1073/pnas.0606053103
8. Wu M, Pastor-Pareja JC, Xu T: Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 1, 463:545-548. 10.1038/nature08702
9. Lyons JG, Siew K, O'Grady RL: Cellular interactions determining the production of collagenase by a rat mammary carcinoma cell line. Int J Cancer 1, 43:119-125. 10.1002/ijc.2910430123
10. Martorana AM, Zheng G, Crowe TC, O'Grady RL, Lyons JG: Epithelial cells up-regulate matrix metalloproteinases in cells within the same mammary carcinoma that have undergone an epithelial-mesenchymal transition. Cancer Res 1998, 58:4970-4979.
11. Celia-Terrassa T, Meca-Cortes O, Mateo F, de Paz AM, Rubio N, Arnal-Estape A, Ell BJ, Bermudo R, Diaz A, Guerra-Rebollo M, Lozano JJ, Estarás C, Ulloa C, Álvarez-Simón D, Milà J, Vilella R, Paciucci R, Martínez-Balbás M, de Herreros AG, Gomis RR, Kang Y, Blanco J, Fernández PL, Thomson TM: Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest 1, 122:1849-1868. 10.1172/JCI59218
12. Tsuji T, Ibaragi S, Hu GF: Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 1, 69:7135-7139. 10.1158/0008-5472.CAN-09-1618
13. Sardana G, Marshall J, Diamandis EP: Discovery of candidate tumor markers for prostate cancer via proteomic analysis of cell culture-conditioned medium. Clin Chem 1, 53:429-437. 10.1373/clinchem.2006.077370
14. Sardana G, Jung K, Stephan C, Diamandis EP: Proteomic analysis of conditioned media from the PC1, LNCaP, and 22Rv1 prostate cancer cell lines: discovery and validation of candidate prostate cancer biomarkers. J Proteome Res 2008, 7:3329-3338. 10.1021/pr8003216
15. Kulasingam V, Diamandis EP: Proteomics analysis of conditioned media from three breast cancer cell lines: a mine for biomarkers and therapeutic targets. Mol Cell Proteomics 1, 6:1997-2011. 10.1074/mcp.M600465-MCP200
16. Chen J, Shi D, Liu X, Fang S, Zhang J, Zhao Y: Targeting SPARC by lentivirus-mediated RNA interference inhibits cervical cancer cell growth and metastasis. BMC Cancer 1, 12:464. 10.1186/1471-2407-12-464
17. Chen J, Wang M, Xi B, Xue J, He D, Zhang J, Zhao Y: SPARC is a key regulator of proliferation, apoptosis and invasion in human ovarian cancer. PLoS One 1, 7:e42413. 10.1371/journal.pone.0042413
18. Thomas R, True LD, Bassuk JA, Lange PH, Vessella RL: Differential expression of osteonectin/SPARC during human prostate cancer progression. Clin Cancer Res 2000, 6:1140-1149.
19. Andreasen PA, Kjoller L, Christensen L, Duffy MJ: The urokinase-type plasminogen activator system in cancer metastasis: a review. Int J Cancer 1, 72:1-22. 10.1002/(SICI)1097-0215(19970703)72:1<1::AID-IJC1>3.0.CO;2-Z
20. Teoh-Fitzgerald ML, Fitzgerald MP, Jensen TJ, Futscher BW, Domann FE: Genetic and epigenetic inactivation of extracellular superoxide dismutase promotes an invasive phenotype in human lung cancer by disrupting ECM homeostasis. Mol Cancer Res 1, 10:40-51. 10.1186/1476-4598-10-40
21. Alur M, Nguyen MM, Eggener SE, Jiang F, Dadras SS, Stern J, Kimm S, Roehl K, Kozlowski J, Pins M, Michalak M, Dhir R, Wang Z: Suppressive roles of calreticulin in prostate cancer growth and metastasis. Am J Pathol 1, 175:882-890. 10.2353/ajpath.2009.080417
22. Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, Roberts TM, Sellers WR: Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci U S A 1, 96:2110-2115. 10.1073/pnas.96.5.2110
23. Alachkar H, Santhanam R, Maharry K, Metzeler KH, Huang X, Kohlschmidt J, Mendler JH, Benito JM, Hickey C, Neviani P, Dorrance AM, Anghelina M, Khalife J, Tarighat SS, Volinia S, Whitman SP, Paschka P, Hoellerbauer P, Wu YZ, Han L, Bolon BN, Blum W, Mrózek K, Carroll AJ, Perrotti D, Andreeff M, Caligiuri MA, Konopleva M, Garzon R, Bloomfield CD, Marcucci G: SPARC promotes leukemic cell growth and predicts acute myeloid leukemia outcome. J Clin Invest 1, 124:1512-1524. 10.1172/JCI70921
24. Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN: Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 1, 26:4084-4094. 10.1038/sj.onc.1210181
25. Weaver MS, Workman G, Sage EH: The copper binding domain of SPARC mediates cell survival in vitro via interaction with integrin beta1 and activation of integrin-linked kinase. J Biol Chem 1, 283:22826-22837. 10.1074/jbc.M706563200
26. Golembieski WA, Rempel SA: cDNA array analysis of SPARC-modulated changes in glioma gene expression. J Neurooncol 1, 60:213-226. 10.1023/A:1021167211131
27. Derosa CA, Furusato B, Shaheduzzaman S, Srikantan V, Wang Z, Chen Y, Seifert M, Ravindranath L, Young D, Nau M, Dobi A, Werner T, McLeod DG, Vahey MT, Sesterhenn IA, Srivastava S, Petrovics G: Elevated osteonectin/SPARC expression in primary prostate cancer predicts metastatic progression. Prostate Cancer Prostatic Dis 1, 15:150-156. 10.1038/pcan.2011.61
28. Briganti A, Suardi N, Gallina A, Abdollah F, Novara G, Ficarra V, Montorsi F: Predicting the risk of bone metastasis in prostate cancer. Cancer Treat Rev 2013, 40:3-11.
29. Nakamura K, Yamanouchi K, Nishihara M: Secreted protein acidic and rich in cysteine internalization and its age-related alterations in skeletal muscle progenitor cells. Aging Cell 1, 13:175-184. 10.1111/acel.12168
30. Kzhyshkowska J, Workman G, Cardo-Vila M, Arap W, Pasqualini R, Gratchev A, Krusell L, Goerdt S, Sage EH: Novel function of alternatively activated macrophages: stabilin-1-mediated clearance of SPARC. J Immunol 1, 176:5825-5832. 10.4049/jimmunol.176.10.5825
31. Greaves M, Maley CC: Clonal evolution in cancer. Nature 1, 481:306-313. 10.1038/nature10762
32. Portela M, Casas-Tinto S, Rhiner C, Lopez-Gay JM, Dominguez O, Soldini D, Moreno E: Drosophila SPARC is a self-protective signal expressed by loser cells during cell competition. Dev Cell 1, 19:562-573. 10.1016/j.devcel.2010.09.004
33. Tsuji T, Ibaragi S, Shima K, Hu MG, Katsurano M, Sasaki A, Hu GF: Epithelial-mesenchymal transition induced by growth suppressor p12CDK2-AP1 promotes tumor cell local invasion but suppresses distant colony growth. Cancer Res 1, 68:10377-10386. 10.1158/0008-5472.CAN-08-1444
34. Nagaraju GP, Dontula R, El-Rayes BF, Lakka SS: Molecular mechanisms underlying the divergent roles of SPARC in human carcinogenesis. Carcinogenesis 1, 35:967-973. 10.1093/carcin/bgu072
35. Makridakis M, Roubelakis MG, Bitsika V, Dimuccio V, Samiotaki M, Kossida S, Panayotou G, Coleman J, Candiano G, Anagnou NP, Vlahou A: Analysis of secreted proteins for the study of bladder cancer cell aggressiveness. J Proteome Res 1, 9:3243-3259. 10.1021/pr100189d
36. Bradshaw AD: Diverse biological functions of the SPARC family of proteins. Int J Biochem Cell Biol 1, 44:480-488. 10.1016/j.biocel.2011.12.021
37. Arnold SA, Brekken RA: SPARC: a matricellular regulator of tumorigenesis. J Cell Commun Signal 1, 3:255-273. 10.1007/s12079-009-0072-4
38. Chiodoni C, Colombo MP, Sangaletti S: Matricellular proteins: from homeostasis to inflammation, cancer, and metastasis. Cancer Metastasis Rev 1, 29:295-307. 10.1007/s10555-010-9221-8
39. Chlenski A, Cohn SL: Modulation of matrix remodeling by SPARC in neoplastic progression. Semin Cell Dev Biol 1, 21:55-65. 10.1016/j.semcdb.2009.11.018
40. Podhajcer OL, Benedetti LG, Girotti MR, Prada F, Salvatierra E, Llera AS: The role of the matricellular protein SPARC in the dynamic interaction between the tumor and the host. Cancer Metastasis Rev 1, 27:691-705. 10.1007/s10555-008-9146-7
41. Chen N, Ye XC, Chu K, Navone NM, Sage EH, Yu-Lee LY, Logothetis CJ, Lin SH: A secreted isoform of ErbB3 promotes osteonectin expression in bone and enhances the invasiveness of prostate cancer cells. Cancer Res 1, 67:6544-6548. 10.1158/0008-5472.CAN-07-1330
42. Jacob K, Webber M, Benayahu D, Kleinman HK: Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res 1999, 59:4453-4457.
43. Neuzillet C, Tijeras-Raballand A, Cros J, Faivre S, Hammel P, Raymond E: Stromal expression of SPARC in pancreatic adenocarcinoma. Cancer Metastasis Rev 1, 32:585-602. 10.1007/s10555-013-9439-3
44. Yan Q, Sage EH: SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 1, 47:1495-1506. 10.1177/002215549904701201
45. Yan Q, Weaver M, Perdue N, Sage EH: Matricellular protein SPARC is translocated to the nuclei of immortalized murine lens epithelial cells. J Cell Physiol 1, 203:286-294. 10.1002/jcp.20226
46. Aguilera KY, Rivera LB, Hur H, Carbon JG, Toombs JE, Goldstein CD, Dellinger MT, Castrillon DH, Brekken RA: Collagen signaling enhances tumor progression after anti-VEGF therapy in a murine model of pancreatic ductal adenocarcinoma. Cancer Res 1, 74:1032-1044. 10.1158/0008-5472.CAN-13-2800
47. Brekken RA, Puolakkainen P, Graves DC, Workman G, Lubkin SR, Sage EH: Enhanced growth of tumors in SPARC null mice is associated with changes in the ECM. J Clin Invest 1, 111:487-495. 10.1172/JCI16804
48. Said N, Frierson HF, Sanchez-Carbayo M, Brekken RA, Theodorescu D: Loss of SPARC in bladder cancer enhances carcinogenesis and progression. J Clin Invest 2013, 123:751-766.
49. Said N, Motamed K: Absence of host-secreted protein acidic and rich in cysteine (SPARC) augments peritoneal ovarian carcinomatosis. Am J Pathol 1, 167:1739-1752. 10.1016/S0002-9440(10)61255-2
50. Said N, Frierson HF Jr, Chernauskas D, Conaway M, Motamed K, Theodorescu D: The role of SPARC in the TRAMP model of prostate carcinogenesis and progression. Oncogene 1, 28:3487-3498. 10.1038/onc.2009.205
51. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, De Jesus-Acosta A, Sharma P, Heidari P, Mahmood U, Chin L, Moses HL, Weaver VM, Maitra A, Allison JP, LeBleu VS, Kalluri R: Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 1, 25:719-734. 10.1016/j.ccr.2014.04.005
52. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, Westphalen CB, Kitajewski J, Fernandez-Barrena MG, Fernandez-Zapico ME, Iacobuzio-Donahue C, Olive KP, Stanger BZ: Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 1, 25:735-747. 10.1016/j.ccr.2014.04.021
53. Hanahan D, Coussens LM: Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 1, 21:309-322. 10.1016/j.ccr.2012.02.022
54. Thomas SL, Schultz CR, Mouzon E, Golembieski WA, El Naili R, Radakrishnan A, Lemke N, Poisson LM, Gutierrez JA, Cottingham S, Rempel SA: Loss of Sparc in p53-null astrocytes promotes macrophage activation and phagocytosis resulting in decreased tumor size and tumor cell survival. Brain Pathol 2014. doi:10.1111/bpa.12161
55. Guweidhi A, Kleeff J, Adwan H, Giese NA, Wente MN, Giese T, Buchler MW, Berger MR, Friess H: Osteonectin influences growth and invasion of pancreatic cancer cells. Ann Surg 1, 242:224-234. 10.1097/01.sla.0000171866.45848.68
56. Briggs J, Chamboredon S, Castellazzi M, Kerry JA, Bos TJ: Transcriptional upregulation of SPARC, in response to c-Jun overexpression, contributes to increased motility and invasion of MCF7 breast cancer cells. Oncogene 1, 21:7077-7091. 10.1038/sj.onc.1205857
57. Campo McKnight DA, Sosnoski DM, Koblinski JE, Gay CV: Roles of osteonectin in the migration of breast cancer cells into bone. J Cell Biochem 1, 97:288-302. 10.1002/jcb.20644
58. Shi Q, Bao S, Maxwell JA, Reese ED, Friedman HS, Bigner DD, Wang XF, Rich JN: Secreted protein acidic, rich in cysteine (SPARC), mediates cellular survival of gliomas through AKT activation. J Biol Chem 1, 279:52200-52209. 10.1074/jbc.M409630200
59. Kunigal S, Gondi CS, Gujrati M, Lakka SS, Dinh DH, Olivero WC, Rao JS: SPARC-induced migration of glioblastoma cell lines via uPA-uPAR signaling and activation of small GTPase RhoA. Int J Oncol 2006, 29:1349-1357.
60. McClung HM, Thomas SL, Osenkowski P, Toth M, Menon P, Raz A, Fridman R, Rempel SA: SPARC upregulates MT1-MMP expression, MMP-2 activation, and the secretion and cleavage of galectin-3 in U87MG glioma cells. Neurosci Lett 1, 419:172-177. 10.1016/j.neulet.2007.04.037
61. Prada F, Benedetti LG, Bravo AI, Alvarez MJ, Carbone C, Podhajcer OL: SPARC endogenous level, rather than fibroblast-produced SPARC or stroma reorganization induced by SPARC, is responsible for melanoma cell growth. J Invest Dermatol 1, 127:2618-2628. 10.1038/sj.jid.5700962
62. Ting DT, Wittner BS, Ligorio M, Vincent Jordan N, Shah AM, Miyamoto DT, Aceto N, Bersani F, Brannigan BW, Xega K, Ciciliano JC, Zhu H, MacKenzie OC, Trautwein J, Arora KS, Shahid M, Ellis HL, Qu N, Bardeesy N, Rivera MN, Deshpande V, Ferrone CR, Kapur R, Ramaswamy S, Shioda T, Toner M, Maheswaran S, Haber DA: Single-cell RNA sequencing identifies extracellular matrix gene expression by pancreatic circulating tumor cells. Cell Rep 1, 8:1905-1918. 10.1016/j.celrep.2014.08.029
63. Chapman A, Fernandez Del Ama L, Ferguson J, Kamarashev J, Wellbrock C, Hurlstone A: Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep 2014. doi:10.1016/j.celrep.2014.06.045
64. Cleary AS, Leonard TL, Gestl SA, Gunther EJ: Tumour cell heterogeneity maintained by cooperating subclones in Wnt-driven mammary cancers. Nature 1, 508:113-117. 10.1038/nature13187
65. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, Almeida D, Koller A, Hajjar KA, Stainier DY, Chen EI, Lyden D, Bissell MJ: The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 1, 15:807-817. 10.1038/ncb2767
66. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massague J: Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 1, 17:867-874. 10.1038/nm.2379
67. Elias JE, Gygi SP: Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 1, 4:207-214. 10.1038/nmeth1019
68. Sasaki T, Hohenester E, Gohring W, Timpl R: Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin. EMBO J 1, 17:1625-1634. 10.1093/emboj/17.6.1625