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Periostin, tenascin, osteopontin isoforms in long- and non-long survival patients with pancreatic cancer: a pilot study

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Abstract

Pancreatic adenocarcinoma (PDAC) is the most frequent histological type of malignancy in the pancreas. Extracellular matrix (ECM), plays a critical role during the process of human carcinogenesis and the possible diversity in matricellular proteins composition of ECM may have a significant impact on the clinical course of PDAC. Aim of this paper was to evaluate the expression of three matricellular proteins, including Periostin (POSTN), Tenascin (TNS) and Osteopontin (OPN), in PDAC from long-survival (LS) and non-long survival (NLS) patients. A total of 30 PDAC were analyzed, 15 from patients that survived more than 60 months after surgery (LS) and 15 that died from the disease within 24 (NLS). RNA was extracted and OPN, TNS and POSTN mRNA levels were evaluated by qRT-PCR. LS and NLS samples showed the same type of POSTN and TN isoforms. On the contrary, OPN seems to be preferentially expressed in NLS PDAC. Moreover, OPNb and OPNc isoforms were expressed exclusively in NLS samples. In conclusion, Our data led to hypothesize a possible relationship between the expression of different isoforms of each of these proteins and the clinical outcome of patients with PDAC.

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References

  1. Yeo TP (2015) Demographics, epidemiology, and inheritance of pancreatic ductal adenocarcinoma. Semin Oncol 42(1):8–18. https://doi.org/10.1053/j.seminoncol.2014.12.002

    Article  PubMed  Google Scholar 

  2. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63(1):11–30. https://doi.org/10.3322/caac.21166

    Article  PubMed  Google Scholar 

  3. Bonnans C, Chou J, Werb Z (2014) Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 15(12):786–801. https://doi.org/10.1038/nrm3904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241–254. https://doi.org/10.1016/j.ccr.2005.08.010

    Article  CAS  PubMed  Google Scholar 

  5. Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15(12):802–812. https://doi.org/10.1038/nrm3896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mecham RP (2012) Overview of extracellular matrix. Curr Protoc Cell Biol. https://doi.org/10.1002/0471143030.cb1001s57

    Article  PubMed  Google Scholar 

  7. Lu P, Takai K, Weaver VM, Werb Z (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a005058

    Article  PubMed  PubMed Central  Google Scholar 

  8. Chong HC, Tan CK, Huang RL, Tan NS (2012) Matricellular proteins: a sticky affair with cancers. J Oncol 2012:351089. https://doi.org/10.1155/2012/351089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Murphy-Ullrich JE, Sage EH (2014) Revisiting the matricellular concept. Matrix Biol 37:1–14. https://doi.org/10.1016/j.matbio.2014.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fiorino S, Bacchi-Reggiani ML, Birtolo C, Acquaviva G, Visani M, Fornelli A, Masetti M, Tura A, Sbrignadello S, Grizzi F, Patrinicola F, Zanello M, Mastrangelo L, Lombardi R, Benini C, Di Tommaso L, Bondi A, Monetti F, Siopis E, Orlandi PE, Imbriani M, Fabbri C, Giovanelli S, Domanico A, Accogli E, Di Saverio S, Grifoni D, Cennamo V, Leandri P, Jovine E, de Biase D (2018) Matricellular proteins and survival in patients with pancreatic cancer: a systematic review. Pancreatology 18(1):122–132. https://doi.org/10.1016/j.pan.2017.11.001

    Article  CAS  PubMed  Google Scholar 

  11. Kudo A (2017) Introductory review: periostin-gene and protein structure. Cell Mol Life Sci 74(23):4259–4268. https://doi.org/10.1007/s00018-017-2643-5

    Article  CAS  PubMed  Google Scholar 

  12. Briones-Orta MA, Avendano-Vazquez SE, Aparicio-Bautista DI, Coombes JD, Weber GF, Syn WK (2017) Osteopontin splice variants and polymorphisms in cancer progression and prognosis. Biochim Biophys Acta Rev Cancer 1868(1):93–108 A. https://doi.org/10.1016/j.bbcan.2017.02.005

    Article  CAS  PubMed  Google Scholar 

  13. Giusca SE, Amalinei C, Lozneanu L, Ciobanu Apostol D, Andriescu EC, Scripcariu A, Balan R, Avadanei ER, Caruntu ID (2017) Heterogeneous periostin expression in different histological variants of papillary thyroid carcinoma. Biomed Res Int 2017:8701386. https://doi.org/10.1155/2017/8701386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ben QW, Jin XL, Liu J, Cai X, Yuan F, Yuan YZ (2011) Periostin, a matrix specific protein, is associated with proliferation and invasion of pancreatic cancer. Oncol Rep 25(3):709–716. https://doi.org/10.3892/or.2011.1140

    Article  CAS  PubMed  Google Scholar 

  15. Siddiqui AA, Jones E, Andrade D, Shah A, Kowalski TE, Loren DE, Chipitsyna G, Arafat HA (2014) Osteopontin splice variant as a potential marker for metastatic disease in pancreatic adenocarcinoma. J Gastroenterol Hepatol 29(6):1321–1327. https://doi.org/10.1111/jgh.12561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Juuti A, Nordling S, Louhimo J, Lundin J, Haglund C (2004) Tenascin C expression is upregulated in pancreatic cancer and correlates with differentiation. J Clin Pathol 57(11):1151–1155. https://doi.org/10.1136/jcp.2003.015818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Xu Y, Li Z, Jiang P, Wu G, Chen K, Zhang X, Li X (2015) The co-expression of MMP-9 and Tenascin-C is significantly associated with the progression and prognosis of pancreatic cancer. Diagn Pathol 10:211. https://doi.org/10.1186/s13000-015-0445-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Viloria K, Munasinghe A, Asher S, Bogyere R, Jones L, Hill NJ (2016) A holistic approach to dissecting SPARC family protein complexity reveals FSTL-1 as an inhibitor of pancreatic cancer cell growth. Sci Rep 6:37839. https://doi.org/10.1038/srep37839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bosman FT, Carneiro F, Hruban HR, Theise ND (2010) WHO classification of tumours of the digestive system. IARC, Lyon

    Google Scholar 

  20. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (2010) AJCC cancer staging manual. Springer, New York

    Google Scholar 

  21. Masetti M, Acquaviva G, Visani M, Tallini G, Fornelli A, Ragazzi M, Vasuri F, Grifoni D, Di Giacomo S, Fiorino S, Lombardi R, Tuminati D, Ravaioli M, Fabbri C, Bacchi-Reggiani ML, Pession A, Jovine E, de Biase D (2018) Long-term survivors of pancreatic adenocarcinoma show low rates of genetic alterations in KRAS, TP53 and SMAD4. Cancer Biomark 21(2):323–334. https://doi.org/10.3233/CBM-170464

    Article  CAS  PubMed  Google Scholar 

  22. Kardosh A, Lichtensztajn DY, Gubens MA, Kunz PL, Fisher GA, Clarke CA (2018) Long-term survivors of pancreatic cancer: a California population-based study. Pancreas 47(8):958–966. https://doi.org/10.1097/MPA.0000000000001133

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bai Y, Nakamura M, Zhou G, Li Y, Liu Z, Ozaki T, Mori I, Kakudo K (2010) Novel isoforms of periostin expressed in the human thyroid. Jpn Clin Med 1:13–20. https://doi.org/10.4137/JCM.S5899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ingber DE, Wang N, Stamenovic D (2014) Tensegrity, cellular biophysics, and the mechanics of living systems. Rep Prog Phys 77(4):046603. https://doi.org/10.1088/0034-4885/77/4/046603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Erkan M, Kleeff J, Gorbachevski A, Reiser C, Mitkus T, Esposito I, Giese T, Buchler MW, Giese NA, Friess H (2007) Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology 132(4):1447–1464. https://doi.org/10.1053/j.gastro.2007.01.031

    Article  CAS  PubMed  Google Scholar 

  26. Saxena S, Gandhi A, Lim PW, Relles D, Sarosiek K, Kang C, Chipitsyna G, Sendecki J, Yeo CJ, Arafat HA (2013) RAN GTPase and osteopontin in pancreatic cancer. Pancreat Disord Ther 3(1):113

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ferreira LB, Eloy C, Pestana A, Lyra J, Moura M, Prazeres H, Tavares C, Sobrinho-Simoes M, Gimba E, Soares P (2016) Osteopontin expression is correlated with differentiation and good prognosis in medullary thyroid carcinoma. Eur J Endocrinol 174(4):551–561. https://doi.org/10.1530/EJE-15-0577

    Article  CAS  PubMed  Google Scholar 

  28. Ratajczak-Wielgomas K, Dziegiel P (2015) The role of periostin in neoplastic processes. Folia Histochem Cytobiol 53(2):120–132. https://doi.org/10.5603/FHC.a2015.0014

    Article  CAS  PubMed  Google Scholar 

  29. Adams M, Jones JL, Walker RA, Pringle JH, Bell SC (2002) Changes in tenascin-C isoform expression in invasive and preinvasive breast disease. Cancer Res 62(11):3289–3297

    CAS  PubMed  Google Scholar 

  30. Ferreira LB, Tavares C, Pestana A, Pereira CL, Eloy C, Pinto MT, Castro P, Batista R, Rios E, Sobrinho-Simoes M, Gimba ER, Soares P (2016) Osteopontin-a splice variant is overexpressed in papillary thyroid carcinoma and modulates invasive behavior. Oncotarget 7(32):52003–52016. https://doi.org/10.18632/oncotarget.10468

    Article  PubMed  PubMed Central  Google Scholar 

  31. Morra L, Rechsteiner M, Casagrande S, von Teichman A, Schraml P, Moch H, Soltermann A (2012) Characterization of periostin isoform pattern in non-small cell lung cancer. Lung Cancer 76(2):183–190. https://doi.org/10.1016/j.lungcan.2011.10.013

    Article  PubMed  Google Scholar 

  32. Latijnhouwers MA, de Jongh GJ, Bergers M, de Rooij MJ, Schalkwijk J (2000) Expression of tenascin-C splice variants by human skin cells. Arch Dermatol Res 292(9):446–454. https://doi.org/10.1007/s004030000152

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Dr. Simonetta Righi (Biblioteca Centralizzata, Policlinico S. Orsola-Malpighi, Università di Bologna, Bologna, Italy) and Dr. Claudia Benini (Surgery Unit Azienda USL-Maggiore Hospital, Bologna, Italy) for their support in the search of scientific bibliography and technical help.

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Correspondence to Sirio Fiorino or Dario de Biase.

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All information regarding the human material was managed using anonymous numerical codes. All samples were handled in compliance with the Helsinki Declaration (http://www.wma.net/en/30publications/10policies/b3/). The study was approved by the internal review board committee (Azienda USL of Bologna, number 15035).

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Fiorino, S., Visani, M., Masetti, M. et al. Periostin, tenascin, osteopontin isoforms in long- and non-long survival patients with pancreatic cancer: a pilot study. Mol Biol Rep 47, 8235–8241 (2020). https://doi.org/10.1007/s11033-020-05763-2

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