Tumor Biology

, Volume 37, Issue 8, pp 11099–11104 | Cite as

Reduced expression of polymeric immunoglobulin receptor (pIgR) in nasopharyngeal carcinoma and its correlation with prognosis

Original Article
  • 207 Downloads

Abstract

Polymeric immunoglobulin receptor (pIgR) is a key component of the mucosal immune system that mediates epithelial transcytosis of immunoglobulins. The expression of pIgR was reported to be up-regulated and related to the prognosis of several human cancers. However, the clinical significance of pIgR in nasopharyngeal carcinoma (NPC) remains unclear. The purpose of this study was to detect the pIgR expression and its prognostic value in NPC. The expression of serum pIgR was measured in NPC patients and healthy controls by real-time quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR) and western blotting analyses. The relationship between its expression and clinical factors was analyzed by chi-square test. Then, the overall survival of patients was assessed by Kaplan-Meier analysis while the prognostic value of serum pIgR was estimated using univariate and multivariate analyses with cox regression analysis. Serum pIgR was down-regulated in NPC patients compared to that in healthy controls both at messenger RNA (mRNA) and protein levels. Especially, its expression was also significantly lower in patients at advantage stages (III–IV) than those at early stages (I–II). And, the low pIgR expression was strongly associated with advanced clinical stages, T stage, N stage, and distant metastasis. Kaplan-Meier analysis demonstrated that patients with low pIgR expression had a significantly shorter overall survival than those with high expression at any stages. Cox regression analysis suggested that pIgR was closely related to the prognosis of NPC. Serum pIgR expression was reduced in NPC, and it could be an independent prognostic predictor for patients with this cancer.

Keywords

Nasopharyngeal carcinoma Polymeric immunoglobulin receptor Prognosis 

Notes

Compliance with ethical standards

Conflicts of interest

None

Ethics, consent, and permissions

The study protocol was approved and supervised by the Ethics Committee of The Affiliated Hospital of Weifang Medical College, and written informed consent was obtained from each participant.

Consent to publish

All authors read and approved the final manuscript.

Funding

None.

References

  1. 1.
    Xu ZJ, Zheng RS, Zhang SW, Zou XN, Chen WQ. Nasopharyngeal carcinoma incidence and mortality in China in 2009. Chin J Cancer. 2013;32(8):453–60. doi: 10.5732/cjc.013.10118.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Cao SM, Simons MJ, Qian CN. The prevalence and prevention of nasopharyngeal carcinoma in China. Chin J Cancer. 2011;30(2):114–9.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Trejaut J, Lee CL, Yen JC, Loo JH, Lin M. Ancient migration routes of Austronesian-speaking populations in oceanic Southeast Asia and Melanesia might mimic the spread of nasopharyngeal carcinoma. Chin J Cancer. 2011;30(2):96–105.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Jia WH, Qin HD. Non-viral environmental risk factors for nasopharyngeal carcinoma: a systematic review. Semin Cancer Biol. 2012;22(2):117–26. doi: 10.1016/j.semcancer.2012.01.009.CrossRefPubMedGoogle Scholar
  5. 5.
    Xiong W, Zeng ZY, Xia JH, Xia K, Shen SR, Li XL, et al. A susceptibility locus at chromosome 3p21 linked to familial nasopharyngeal carcinoma. Cancer Res. 2004;64(6):1972–4.CrossRefPubMedGoogle Scholar
  6. 6.
    Zeng Z, Huang H, Zhang W, Xiang B, Zhou M, Zhou Y, et al. Nasopharyngeal carcinoma: advances in genomics and molecular genetics. Sci China Life Sci. 2011;54(10):966–75. doi: 10.1007/s11427-011-4223-5.CrossRefPubMedGoogle Scholar
  7. 7.
    Ho FC, Tham IW, Earnest A, Lee KM, Lu JJ. Patterns of regional lymph node metastasis of nasopharyngeal carcinoma: a meta-analysis of clinical evidence. BMC Cancer. 2012;12:98. doi: 10.1186/1471-2407-12-98.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Xiao WW, Huang SM, Han F, Wu SX, Lu LX, Lin CG, et al. Local control, survival, and late toxicities of locally advanced nasopharyngeal carcinoma treated by simultaneous modulated accelerated radiotherapy combined with cisplatin concurrent chemotherapy: long-term results of a phase 2 study. Cancer. 2011;117(9):1874–83. doi: 10.1002/cncr.25754.CrossRefPubMedGoogle Scholar
  9. 9.
    Suarez C, Rodrigo JP, Rinaldo A, Langendijk JA, Shaha AR, Ferlito A. Current treatment options for recurrent nasopharyngeal cancer. Eur Arch Otorhinolaryngol. 2010;267(12):1811–24. doi: 10.1007/s00405-010-1385-x.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ma BB, Hui EP, Chan AT. Systemic approach to improving treatment outcome in nasopharyngeal carcinoma: current and future directions. Cancer Sci. 2008;99(7):1311–8. doi: 10.1111/j.1349-7006.2008.00836.x.CrossRefPubMedGoogle Scholar
  11. 11.
    Ocak S, Pedchenko TV, Chen H, Harris FT, Qian J, Polosukhin V, et al. Loss of polymeric immunoglobulin receptor expression is associated with lung tumourigenesis. Eur Respir J. 2012;39(5):1171–80. doi: 10.1183/09031936.00184410.CrossRefPubMedGoogle Scholar
  12. 12.
    Norderhaug IN, Johansen FE, Schjerven H, Brandtzaeg P. Regulation of the formation and external transport of secretory immunoglobulins. Crit Rev Immunol. 1999;19(5–6):481–508.PubMedGoogle Scholar
  13. 13.
    Denning GM. IL-4 and IFN-gamma synergistically increase total polymeric IgA receptor levels in human intestinal epithelial cells. Role of protein tyrosine kinases. J Immunol. 1996;156(12):4807–14.PubMedGoogle Scholar
  14. 14.
    Kvale D, Lovhaug D, Sollid LM, Brandtzaeg P. Tumor necrosis factor-alpha up-regulates expression of secretory component, the epithelial receptor for polymeric Ig. J Immunol. 1988;140(9):3086–9.PubMedGoogle Scholar
  15. 15.
    Rojas R, Apodaca G. Immunoglobulin transport across polarized epithelial cells. Nat Rev Mol Cell Biol. 2002;3(12):944–55. doi: 10.1038/nrm972.CrossRefPubMedGoogle Scholar
  16. 16.
    Kaetzel CS. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol Rev. 2005;206:83–99. doi: 10.1111/j.0105-2896.2005.00278.x.CrossRefPubMedGoogle Scholar
  17. 17.
    Liu F, Ye P, Bi T, Teng L, Xiang C, Wang H, et al. Colorectal polymeric immunoglobulin receptor expression is correlated with hepatic metastasis and poor prognosis in colon carcinoma patients with hepatic metastasis. Hepato-Gastroenterology. 2014;61(131):652–9.PubMedGoogle Scholar
  18. 18.
    Berntsson J, Lundgren S, Nodin B, Uhlen M, Gaber A, Jirstrom K. Expression and prognostic significance of the polymeric immunoglobulin receptor in epithelial ovarian cancer. J Ovarian Res. 2014;7:26. doi: 10.1186/1757-2215-7-26.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Fristedt R, Gaber A, Hedner C, Nodin B, Uhlen M, Eberhard J, et al. Expression and prognostic significance of the polymeric immunoglobulin receptor in esophageal and gastric adenocarcinoma. J Transl Med. 2014;12:83. doi: 10.1186/1479-5876-12-83.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ai J, Tang Q, Wu Y, Xu Y, Feng T, Zhou R, et al. The role of polymeric immunoglobulin receptor in inflammation-induced tumor metastasis of human hepatocellular carcinoma. J Natl Cancer Inst. 2011;103(22):1696–712. doi: 10.1093/jnci/djr360.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Fristedt R, Elebro J, Gaber A, Jonsson L, Heby M, Yudina Y, et al. Reduced expression of the polymeric immunoglobulin receptor in pancreatic and periampullary adenocarcinoma signifies tumour progression and poor prognosis. PLoS One. 2014;9(11):e112728. doi: 10.1371/journal.pone.0112728.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Chang Y, Lee TC, Li JC, Lai TL, Chua HH, Chen CL, et al. Differential expression of osteoblast-specific factor 2 and polymeric immunoglobulin receptor genes in nasopharyngeal carcinoma. Head Neck. 2005;27(10):873–82. doi: 10.1002/hed.20253.CrossRefPubMedGoogle Scholar
  23. 23.
    Su T, Chapin SJ, Bryant DM, Shewan AM, Young K, Mostov KE. Reduced immunoglobulin A transcytosis associated with immunoglobulin A nephropathy and nasopharyngeal carcinoma. J Biol Chem. 2011;286(52):44921–5. doi: 10.1074/jbc.M111.296731.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Mao YP, Xie FY, Liu LZ, Sun Y, Li L, Tang LL, et al. Re-evaluation of 6th edition of AJCC staging system for nasopharyngeal carcinoma and proposed improvement based on magnetic resonance imaging. Int J Radiat Oncol Biol Phys. 2009;73(5):1326–34. doi: 10.1016/j.ijrobp.2008.07.062.CrossRefPubMedGoogle Scholar
  25. 25.
    Zhu Q, Cao SM, Lin HX, Yang Q, Liu SL, Guo L. Overexpression of acylglycerol kinase is associated with poorer prognosis and lymph node metastasis in nasopharyngeal carcinoma. Tumour Biol J Int Soc Oncodev Biol Med. 2015. doi: 10.1007/s13277-015-4148-x.Google Scholar
  26. 26.
    Ooft ML, Braunius WW, Heus P, Stegeman I, van Diest PJ, Grolman W, et al. Prognostic significance of the EGFR pathway in nasopharyngeal carcinoma: a systematic review and meta-analysis. Biomark Med. 2015. doi: 10.2217/bmm.15.68.PubMedGoogle Scholar
  27. 27.
    You B, Shan Y, Shi S, Li X, You Y. Effects of ADAM10 upregulation on progression, migration, and prognosis of nasopharyngeal carcinoma. Cancer Sci. 2015. doi: 10.1111/cas.12800.Google Scholar
  28. 28.
    Bo H, Gong Z, Zhang W, Li X, Zeng Y, Liao Q, et al. Upregulated long non-coding RNA AFAP1-AS1 expression is associated with progression and poor prognosis of nasopharyngeal carcinoma. Oncotarget. 2015;6(24):20404–18.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Zhang Y, Sun H, Wu H, Tan Q, Xiang K. Interleukin 35 is an independent prognostic factor and a therapeutic target for nasopharyngeal carcinoma. Contemp Oncol (Pozn). 2015;19(2):120–4. doi: 10.5114/wo.2014.44754.Google Scholar
  30. 30.
    Wang X, Du J, Gu P, Jin R, Lin X. Polymeric immunoglobulin receptor expression is correlated with poor prognosis in patients with osteosarcoma. Mol Med Rep. 2014;9(6):2105–10. doi: 10.3892/mmr.2014.2110.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Niu H, Wang K, Wang Y. Polymeric immunoglobulin receptor expression is predictive of poor prognosis in glioma patients. Int J Clin Exp Med. 2014;7(8):2185–90.PubMedPubMedCentralGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  1. 1.Department of OtorhinolaryngologyThe Affiliated Hospital of Weifang Medical CollegeWeifangChina
  2. 2.Department of OtorhinolaryngologyWeifang People’s HospitalWeifangChina

Personalised recommendations