Tumor-derived osteopontin reprograms normal mammary fibroblasts to promote inflammation and tumor growth in breast cancer

Cancer Research

Volumn 75, Issue 6, 2015, Pages 963-973

  Sharon, Yoray ^a   Raz, Yael ^a,b   Cohen, Noam ^a   Ben Shmuel, Amir ^a   Schwartz, Hila ^a   Geiger, Tamar ^a   Erez, Neta ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b LIS MATERNITY HOSPITAL   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; OSTEOPONTIN; VITRONECTIN RECEPTOR; CD44 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CONTROLLED STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEOMICS; TUMOR GROWTH; ANIMAL; BREAST TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; CELL LINE, TUMOR; CELLULAR REPROGRAMMING; FEMALE; FIBROBLASTS; HUMANS; INFLAMMATION; INTEGRIN ALPHAVBETA3; MICE; OSTEOPONTIN;

EID: 84926074364     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1990     Document Type: Article

References (50)

1. Walker RA. The complexities of breast cancer desmoplasia. Breast Cancer Res 2001;3:143-5.
2. Anderberg C, Pietras K. On the origin of cancer-associated fibroblasts. Cell Cycle 2009;8:1461-2.
3. Servais C, Erez N. From sentinel cells to inflammatory culprits: cancer-associated fibroblasts in tumour-related inflammation. JPathol 2013;229:198-207.
4. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nature reviews Cancer 2006;6:392-401.
5. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr Opin Genet Dev 2009;19:67-73.
6. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010;17:135-47.
7. Erez N, Glanz S, Raz Y, Avivi C, Barshack I. Cancer-associated fibroblasts express proinflammatory factors in human breast and ovarian tumors. Bioche Biophys Res Commun 2013;437:397-402.
8. Anborgh PH, Mutrie JC, Tuck AB, Chambers AF. Role of the metastasis-promoting protein osteopontin in the tumour microenvironment. J Cell Mol Med 2010;14:2037-44.
9. Weber GF, Lett GS, Haubein NC. Osteopontin is a marker for cancer aggressiveness and patient survival. Br J Cancer 2010;103:861-9.
10. Patani N, Jouhra F, Jiang W, Mokbel K. Osteopontin expression profiles predict pathological and clinical outcome in breast cancer. Anticancer Res 2008;28:4105-10.
11. Rangaswami H, Bulbule A, Kundu GC. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biology 2006;16:79-87.
12. Li NY, Weber CE, Mi Z, Wai PY, Cuevas BD, Kuo PC. Osteopontin upregulates critical epithelial-mesenchymal transition transcription factors to induce an aggressive breast cancer phenotype. J Am Coll Surg 2013;217:17-26.
13. McAllister SS, Gifford AM, Greiner AL, Kelleher SP, Saelzler MP, Ince TA, et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008;133:994-1005.
14. Shevde LA, Das S, Clark DW, Samant RS. Osteopontin: an effector and an effect of tumor metastasis. Curr Mol Med 2010;10:71-81.
15. Anderberg C, Li H, Fredriksson L, Andrae J, Betsholtz C, Li X, et al. Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts. Cancer Res 2009;69:369-78.
16. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008;26:1367-72.
17. Borowsky AD, Namba R, Young LJ, Hunter KW, Hodgson JG, Tepper CG, et al. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis 2005;22:47-59.
18. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011;19:257-72.
19. Pazolli E, Alspach E, Milczarek A, Prior J, Piwnica-Worms D, Stewart SA. Chromatin remodeling underlies the senescence-associated secretory phenotype of tumor stromal fibroblasts that supports cancer progression. Cancer Res 2012;72:2251-61.
20. Pazolli E, Luo X, Brehm S, Carbery K, Chung JJ, Prior JL, et al. Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Res 2009;69:1230-9.
21. Barker HE, Bird D, Lang G, Erler JT. Tumor-secreted LOXL2 activates fibroblasts through FAK signaling. Mol Cancer Res 2013;11:1425-36.
22. Cooke ME, Sakai T, Mosher DF. Contraction of collagen matrices mediated by alpha2beta1A and alpha(v)beta3 integrins. J Cell Sci 2000;113:2375-83.
23. Kojima Y, Acar A, Eaton EN, Mellody KT, Scheel C, Ben-Porath I, et al. Autocrine TGF-beta and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc Natl Acad Sci U S A 2010;107:20009-14.
24. Rouabhia M, Park H, Meng S, Derbali H, Zhang Z. Electrical stimulation promotes wound healing by enhancing dermal fibroblast activity and promoting myofibroblast transdifferentiation. PloS ONE 2013;8:e71660.
25. Shukla A, Edwards R, Yang Y, Hahn A, Folkers K, Ding J, et al. CLIC4 regulates TGF-beta-dependent myofibroblast differentiation to produce a cancer stroma. Oncogene 2014;33:842-50.
26. Rodrigues LR, Teixeira JA, Schmitt FL, Paulsson M, Lindmark-Mansson H. The role of osteopontin in tumor progression and metastasis in breast cancer. Cancer Epidemiol, Biomarkers Prev 2007;16:1087-97.
27. 3 integrin expression in human lung fibroblasts via a β3 integrin-, c-Src-, and p38 MAPK-dependent pathway. J Biol Chem 2008;283:12898-908.
28. Janssen ML, Oyen WJ, Dijkgraaf I, Massuger LF, Frielink C, Edwards DS, et al. Tumor targeting with radiolabeled alpha(v)beta(3) integrin binding peptides in a nude mouse model. Cancer Res 2002;62:6146-51.
29. Fong YC, Liu SC, Huang CY, Li TM, Hsu SF, Kao ST, et al. Osteopontin increases lung cancer cells migration via activation of the alphavbeta3 integrin/FAK/Akt and NF-kappaB-dependent pathway. Lung Cancer 2009;64:263-70.
30. Lin YH, Yang-Yen HF. The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J Biol Chem 2001;276:46024-30.
31. Augsten M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Frontiers Oncol 2014;4:62.
32. Elkabets M, Gifford AM, Scheel C, Nilsson B, Reinhardt F, Bray MA, et al. Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J Clin Invest 2011;121:784-99.
33. Polanska UM, Orimo A. Carcinoma-associated fibroblasts: nonneoplastic tumour-promoting mesenchymal cells. J Cell Physiol 2013;228:1651-7.
34. Anderson IC, Mari SE, Broderick RJ, Mari BP, Shipp MA. The angiogenic factor interleukin 8 is induced in non-small cell lung cancer/pulmonary fibroblast cocultures. Cancer Res 2000;60:269-72.
35. Hawinkels LJ, Paauwe M, Verspaget HW, Wiercinska E, van der Zon JM, van der Ploeg K, et al. Interaction with colon cancer cells hyperactivates TGF-beta signaling in cancer-associated fibroblasts. Oncogene 2014;33:97-107.
36. Sato N, Maehara N, Goggins M. Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res 2004;64:6950-6.
37. Bohonowych JE, Hance MW, Nolan KD, Defee M, Parsons CH, Isaacs JS. Extracellular Hsp90 mediates an NF-kappaB dependent inflammatory stromal program: implications for the prostate tumor microenvironment. The Prostate 2014;74:395-407.
38. Calon A, Espinet E, Palomo-Ponce S, Tauriello DV, Iglesias M, Cespedes MV, et al. Dependency of colorectal cancer on a TGF-beta-driven program in stromal cells for metastasis initiation. Cancer Cell 2012;22:571-84.
39. Tchou J, Kossenkov AV, Chang L, Satija C, Herlyn M, Showe LC, et al. Human breast cancer associated fibroblasts exhibit subtype specific gene expression profiles. BMC Med Genomics 2012;5:39.
40. Kale S, Raja R, Thorat D, Soundararajan G, Patil TV, Kundu GC. Osteopontin signaling upregulates cyclooxygenase-2 expression in tumor-associated macrophages leading to enhanced angiogenesis and melanoma growth via alpha9beta1 integrin. Oncogene 2014;33:2295-306.
41. Rao G, Wang H, Li B, Huang L, Xue D, Wang X, et al. Reciprocal interactions between tumor-associated macrophages and CD44-positive cancer cells via osteopontin/CD44 promote tumorigenicity in colorectal cancer. Clin Cancer Res 2013;19:785-97.
42. Weber GF, Lett GS, Haubein NC. Categorical meta-analysis of Osteopontin as a clinical cancer marker. Oncology Reports 2011;25:433-41.
43. Gotoh M, Sakamoto M, Kanetaka K, Chuuma M, Hirohashi S. Overexpression of osteopontin in hepatocellular carcinoma. Pathology International 2002;52:19-24.
44. Lenga Y, Koh A, Perera AS, McCulloch CA, Sodek J, Zohar R. Osteopontin expression is required for myofibroblast differentiation. Circulation Res 2008;102:319-27.
45. Anwar A, Li M, Frid MG, Kumar B, Gerasimovskaya EV, Riddle SR, et al. Osteopontin is an endogenous modulator of the constitutively activated phenotype of pulmonary adventitial fibroblasts in hypoxic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2012;303:L1-L11.
46. Cox TR, Bird D, Baker AM, Barker HE, Ho MW, Lang G, et al. LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res 2013;73:1721-32.
47. Chakraborty G, Jain S, Patil TV, Kundu GC. Downregulation of osteopontin attenuates breast tumour progression in vivo. J Cell Mol Med 2008;12:2305-18.
48. Mi Z, Guo H, Russell MB, Liu Y, Sullenger BA, Kuo PC. RNA aptamer blockade of osteopontin inhibits growth and metastasis of MDA-MB231 breast cancer cells. Mol Ther 2009;17:153-61.
49. Andrews S, Ford D, Martin P. Knockdown of osteopontin reduces the inflammatory response and subsequent size of postsurgical adhesions in a murine model. Am J Pathol 2012;181:1165-72.
50. Mori R, Shaw TJ, Martin P. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med 2008;205:43-51.