The multifaceted role of periostin in priming the tumor microenvironments for tumor progression

Abstract

Tumor microenvironment consists of tumor cells, stromal cells, extracellular matrix and a plethora of soluble components. The complex array of interactions between tumor cells and their surrounding tumor microenvironments contribute to the determination of the fate of tumor cells during tumorigenesis and metastasis. Matricellular protein periostin is generally absent in most adult tissues but is highly expressed in tumor microenvironments. Current evidence reveals that periostin plays a critical role in establishing and remodeling tumor microenvironments such as the metastatic niche, cancer stem cell niche, perivascular niche, pre-metastatic niche, fibrotic microenvironment and bone marrow microenvironment. Here, we summarize the current knowledge of the multifaceted role of periostin in the tumor microenvironments.

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References

  1. 1.

    Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, Psaila B, Kaplan RN, Bromberg JF, Kang Y, Bissell MJ, Cox TR, Giaccia AJ, Erler JT, Hiratsuka S, Ghajar CM, Lyden D (2017) Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer 17:302–317

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Kalluri R (2016) The biology and function of fibroblasts in cancer. Nat Rev Cancer 16:582–598

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68:3201–3207

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Conway SJ, Izuhara K, Kudo Y, Litvin J, Markwald R, Ouyang G, Arron JR, Holweg CT, Kudo A (2014) The role of periostin in tissue remodeling across health and disease. Cell Mol Life Sci 71:1279–1288

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Liu AY, Zheng H, Ouyang G (2014) Periostin, a multifunctional matricellular protein in inflammatory and tumor microenvironments. Matrix Biol 37:150–156

    Article  PubMed  Google Scholar 

  6. 6.

    Ruan K, Bao S, Ouyang G (2009) The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66:2219–2230

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5:329–339

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J (2011) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481:85–89

    Article  PubMed  Google Scholar 

  9. 9.

    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 (2013) The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 15:807–817

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Wang Z, Xiong S, Mao Y, Chen M, Ma X, Zhou X, Ma Z, Liu F, Huang Z, Luo Q, Ouyang G (2016) Periostin promotes immunosuppressive premetastatic niche formation to facilitate breast tumour metastasis. J Pathol 239:484–495

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, Engle D, Campbell F, Palmer D, Ko JH, Tuveson DA, Hirsch E, Mielgo A, Schmid MC (2016) Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nat Cell Biol 18:549–560

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Ma Z, Zhao X, Huang J, Jia X, Deng M, Cui D, Du Z, Fu G, Ouyang G, Xiao C (2017) A critical role of periostin in B-cell acute lymphoblastic leukemia. Leukemia 31:1835–1837

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Wang Z, Ouyang G (2012) Periostin: a bridge between cancer stem cells and their metastatic niche. Cell Stem Cell 10:111–112

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Xu X, Chang W, Yuan J, Han X, Tan X, Ding Y, Luo Y, Cai H, Liu Y, Gao X, Liu Q, Yu Y, Du Y, Wang H, Ma L, Wang J, Chen K, Ding Y, Fu C, Cao G (2016) Periostin expression in intra-tumoral stromal cells is prognostic and predictive for colorectal carcinoma via creating a cancer-supportive niche. Oncotarget 7:798–813

    Article  PubMed  Google Scholar 

  15. 15.

    Qin X, Yan M, Zhang J, Wang X, Shen Z, Lv Z, Li Z, Wei W, Chen W (2016) TGFbeta3-mediated induction of Periostin facilitates head and neck cancer growth and is associated with metastasis. Sci Rep 6:20587

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Wang X, Liu J, Wang Z, Huang Y, Liu W, Zhu X, Cai Y, Fang X, Lin S, Yuan L, Ouyang G (2013) Periostin contributes to the acquisition of multipotent stem cell-like properties in human mammary epithelial cells and breast cancer cells. PLoS One 8:e72962

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Xu D, Xu H, Ren Y, Liu C, Wang X, Zhang H, Lu P (2012) Cancer stem cell-related gene periostin: a novel prognostic marker for breast cancer. PLoS One 7:e46670

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Lambert AW, Wong CK, Ozturk S, Papageorgis P, Raghunathan R, Alekseyev Y, Gower AC, Reinhard BM, Abdolmaleky HM, Thiagalingam S (2016) Tumor cell-derived periostin regulates cytokines that maintain breast cancer stem cells. Mol Cancer Res 14:103–113

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Crane GM, Jeffery E, Morrison SJ (2017) Adult haematopoietic stem cell niches. Nat Rev Immunol 17:573–590

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11:69–82

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Shao R, Bao S, Bai X, Blanchette C, Anderson RM, Dang T, Gishizky ML, Marks JR, Wang XF (2004) Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Mol Cell Biol 24:3992–4003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Liu Y, Li F, Gao F, Xing L, Qin P, Liang X, Zhang J, Qiao X, Lin L, Zhao Q, Du L (2016) Periostin promotes tumor angiogenesis in pancreatic cancer via Erk/VEGF signaling. Oncotarget 7:40148–40159

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Siriwardena BS, Kudo Y, Ogawa I, Kitagawa M, Kitajima S, Hatano H, Tilakaratne WM, Miyauchi M, Takata T (2006) Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer. Br J Cancer 95:1396–1403

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, Rich JN, Bao S (2015) Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol 17:170–182

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438:820–827

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Wculek SK, Malanchi I (2015) Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature 528:413–417

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Liu Y, Cao X (2016) Characteristics and significance of the pre-metastatic niche. Cancer Cell 30:668–681

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Fukuda K, Sugihara E, Ohta S, Izuhara K, Funakoshi T, Amagai M, Saya H (2015) Periostin is a key niche component for wound metastasis of melanoma. PLoS One 10:e0129704

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Vardaki I, Ceder S, Rutishauser D, Baltatzis G, Foukakis T, Panaretakis T (2016) Periostin is identified as a putative metastatic marker in breast cancer-derived exosomes. Oncotarget 7:74966–74978

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Bonnans C, Chou J, Werb Z (2014) Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 15:786–801

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Erkan M, Kleeff J, Gorbachevski A, Reiser C, Mitkus T, Esposito I, Giese T, Büchler MW, Giese NA, Friess H (2007) Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology 132:1447–1464

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Huang Y, Liu W, Xiao H, Maitikabili A, Lin Q, Wu T, Huang Z, Liu F, Luo Q, Ouyang G (2015) Matricellular protein periostin contributes to hepatic inflammation and fibrosis. Am J Pathol 185:786–797

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Li Y, Wu S, Xiong S, Ouyang G (2015) Deficiency of periostin protects mice against methionine-choline-deficient diet-induced non-alcoholic steatohepatitis. J Hepatol 62:495–497

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Wu T, Wu S, Ouyang G (2014) Periostin: a new extracellular regulator of obesity-induced hepatosteatosis. Cell Metab 20:562–564

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Mundy GR (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2:584–593

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Wu T, Ouyang G (2014) Matricellular proteins: multifaceted extracellular regulators in tumor dormancy. Protein Cell 5:249–252

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Contié S, Voorzanger-Rousselot N, Litvin J, Clézardin P, Garnero P (2011) Increased expression and serum levels of the stromal cell-secreted protein periostin in breast cancer bone metastases. Int J Cancer 128:352–360

    Article  PubMed  Google Scholar 

  38. 38.

    Khurana S, Schouteden S, Manesia JK, Santamaria-Martínez A, Huelsken J, Lacy-Hulbert A, Verfaillie CM (2016) Outside-in integrin signalling regulates haematopoietic stem cell function via Periostin–Itgav axis. Nat Commun 7:13500

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massagué J (2011) Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 17:867–874

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, Shi Q, Cao Y, Lathia J, McLendon RE, Hjelmeland AB, Rich JN (2009) Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15:501–513

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Grants from the National Natural Science Foundation of China (Nos. 81572598, 81372841), the Science and Technology Project of Natural Science Foundation of Fujian Province (No. 2016J01639), the Medical Innovations Topic in Fujian Province (No. 2016-CXB-8) and the Open Research Fund of State Key Laboratory of Cellular Stress Biology, Xiamen University (SKLCSB2017KF007).

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Correspondence to Gaoliang Ouyang.

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Cui, D., Huang, Z., Liu, Y. et al. The multifaceted role of periostin in priming the tumor microenvironments for tumor progression. Cell. Mol. Life Sci. 74, 4287–4291 (2017). https://doi.org/10.1007/s00018-017-2646-2

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Keywords

  • Periostin
  • Tumor microenvironment
  • Metastatic niche
  • Cancer stem cell niche
  • Perivascular niche
  • Pre-metastatic niche
  • Fibrotic microenvironment
  • Bone marrow
  • Matricellular protein