Preview

Успехи молекулярной онкологии

Расширенный поиск

Протеогликаны в нормальной физиологии и канцерогенезе

https://doi.org/10.17650/2313-805X-2018-5-1-8-25

Полный текст:

Аннотация

Появление и развитие злокачественных опухолей связано с многочисленными нарушениями физиологии клетки как на геномном, так и на белковом уровнях и затрагивает множество макромолекул, вовлеченных в различные аспекты ее жизнедеятельности. Однако рост злокачественной опухоли и ее метастазирование определяются не только молекулярными характеристиками самой опухолевой клетки, но и ее взаимодействием с окружающим внеклеточным матриксом (ВКМ) – важной и необходимой частью любой ткани. Огромную роль при этом играют сложные белково-углеводные молекулы протеогликанов (ПГ), которые являются одним из основных компонентов ВКМ и присутствуют на поверхности практически всех клеток, во многом определяя межклеточные взаимодействия и взаимодействия клеток с ВКМ. В процессе канцерогенеза происходят значительные нарушения структуры и состава ПГ, которые приводят к нарушению таких взаимодействий и инициируют трансформацию нормального ВКМ в опухолевое микроокружение, максимально адаптированное для поддержания роста опухолевых клеток, развития злокачественной опухоли и распространения патологического процесса путем метастазирования. В настоящее время множество ключевых ПГ идентифицированы как перспективные диагностические и прогностические молекулярные маркеры и целевые молекулы для создания новых противоопухолевых препаратов.

В обзоре рассматриваются основные классы ПГ, их структура, локализация, функциональная роль в нормальных тканях и участие в молекулярных механизмах злокачественной трансформации клеток и прогрессирования опухоли.

Об авторах

А. В. Суховских
ФГБНУ «Научно-исследовательский институт молекулярной биологии и биофизики»; ФГАОУ ВО «Новосибирский национальный исследовательский государственный университет»
Россия

630117 Новосибирск, ул. Тимакова, 2/12

630090 Новосибирск, ул. Пирогова, 2



Э. В. Григорьева
ФГБНУ «Научно-исследовательский институт молекулярной биологии и биофизики»; ФГАОУ ВО «Новосибирский национальный исследовательский государственный университет»
Россия

630117 Новосибирск, ул. Тимакова, 2/12

630090 Новосибирск, ул. Пирогова, 2



Список литературы

1. Iozzo R.V. Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 1998;67:609–52. DOI: 10.1146/annurev.biochem67.1.609. PMID: 9759499.

2. Yu P., Pearson C.S., Geller H.M. Flexible roles for proteoglycan sulfation and receptor signaling. Trends Neurosci 2018;41(1):47–61. DOI: 10.1016/j.tins.2017.10.005. PMID: 29150096.

3. Lindahl U., Couchman J., Kimata K. et al. Proteoglycans and sulfated glycosaminoglycans. Essentials of glycobiology [Internet]. 3rd edn. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press, 2015–2017. Chapter 17, 2017. PMID: 28876828.

4. Iozzo R.V., Schaefer L. Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 2015;42:11–55. DOI: 10.1016/ j.matbio.2015.02.003. PMID: 25701227.

5. Li J.P., Kusche-Gullberg M. Heparan sulfate: biosynthesis, structure, and function. Int Rev Cell Mol Biol 2016;325:215–73. DOI: 10.1016/bs.ircmb.2016.02.009. PMID: 27241222.

6. Mikami T., Kitagawa H. Biosynthesis and function of chondroitin sulfate. Biochim Biophys Acta 2013;1830(10):4719–33. DOI: 10.1016/j.bbagen.2013.06.006. PMID: 23774590.

7. Trowbridge J.M., Gallo R.L. Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology 2002;12(9):117R–25R. PMID: 12213784.

8. Funderburgh J.L. Keratan sulfate: structure, biosynthesis, and function. Glycobiology 2000;10(10):951–8. PMID: 11030741.

9. Afratis N., Gialeli C., Nikitovic D. et al. Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J 2012;279(7):1177–97. DOI: 10.1111/j.1742-4658.2012.08529.x. PMID: 22333131.

10. Medeiros G.F., Mendes A., Castro R.A. et al. Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochim Biophys Acta 2000; 1475(3):287–94. PMID: 10913828.

11. Poulain F.E., Yost H.J. Heparan sulfate proteoglycans: a sugar code for vertebrate development. Development 2015;142(20):3456–67. DOI: 10.1242/ dev.098178. PMID: 26487777.

12. Bernfield M., Götte M., Park P.W. et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999;68:729–77. DOI: 10.1146/annurev.biochem.68.1.729. PMID: 10872465.

13. Couchman J.R. Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 2010;26:89–114. DOI: 10.1146/ annurev-cellbio-100109-104126. PMID: 20565253.

14. Afratis N.A., Nikitovic D., Multhaupt H.A. et al. Syndecans – key regulators of cell signaling and biological functions. FEBS J 2017;284(1):27–41. DOI: 10.1111/febs.13940. PMID: 27790852.

15. Choi Y., Chung H., Jung H. et al. Syndecan as cell surface receptors: unique structure equates with functional diversity. Matrix Biol 2011;30(2):93–9. DOI: 10.1016/j.matbio.2010.10.006. PMID: 21062643.

16. Piperigkou Z., Mohr B., Karamanos N. et al. Shed proteoglycans in tumor stroma. Cell Tissue Res 2016;365(3):643–55. DOI: 10.1007/s00441-016-2452-4. PMID: 27365088.

17. Filmus J., Capurro M., Rast J. Glypicans. Genome Biol 2008;9(5):224. DOI: 10.1186/gb-2008-9-5-224. PMID: 18505598.

18. Capurro M., Martin T., Shi W. et al. Glypican-3 binds to Frizzled and plays a direct role in the stimulation of canonical Wnt signaling. J Cell Sci 2014;127(Pt 7): 1565–75. DOI: 10.1242/jcs.140871. PMID: 24496449.

19. Nicolosi P.A., Dallatomasina A., Perris R. Theranostic impact of NG2/ CSPG4 proteoglycan in cancer. Theranostics 2015;5(5):530–44. DOI: 10.7150/thno.10824. PMID: 25767619.

20. Yadavilli S., Hwang E.I., Packer R.J. et al. The role of NG2 proteoglycan in glioma. Transl Oncol 2016;9(1):57–63. DOI: 10.1016/j.tranon.2015.12.005. PMID: 26947882.

21. Sakry D., Trotter J. The role of the NG2 proteoglycan in OPC and CNS network function. Brain Res 2016;1638(Pt B): 161–6. DOI: 10.1016/j.brainres.2015.06.003. PMID: 26100334.

22. Morath I., Hartmann T.N., Orian-Rousseau V. CD44: more than a mere stem cell marker. Int J Biochem Cell Biol 2016;81(Pt A):166–73. DOI: 10.1016/j.biocel.2016.09.009. PMID: 27640754.

23. Jijiwa M., Demir H., Gupta S. et al. CD44v6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway. PLoS One 2011;6(9):e24217. DOI: 10.1371/journal.pone.0024217. PMID: 21915300.

24. Stanton H., Melrose J., Little C.B. et al. Proteoglycan degradation by the ADAMTS family of proteinases. Biochim Biophys Acta 2011;1812(12):1616–29. DOI: 10.1016/j.bbadis.2011.08.009. PMID: 21914474.

25. Binder M.J., McCoombe S., Williams E.D. et al. The extracellular matrix in cancer progression: role of hyalectan proteoglycans and ADAMTS. Cancer Lett 2017;385:55–64. DOI: 10.1016/j.canlet.2016.11.001. PMID: 27838414.

26. Wight T.N., Kinsella M.G., Evanko S.P. et al. Versican and the regulation of cell phenotype in disease. Biochim Biophys Acta 2014;1840(8):2441–51. DOI: 10.1016/j.bbagen.2013.12.028. PMID: 24401530.

27. Andersson-Sjöland A., Hallgren O., Rolandsson S. et al. Versican in inflammation and tissue remodeling: the impact on lung disorders. Glycobiology 2015;25(3):243–51. DOI: 10.1093/glycob/cwu120. PMID: 25371494.

28. Sivan S.S., Wachtel E., Roughley P. et al. Structure, function, aging and turnover of aggrecan in the intervertebral disc. Biochem J 2006;399(1):29–35. DOI: 10.1016/j.bbagen.2014.07.013. PMID: 25065289.

29. Nia H.T., Ortiz C., Grodzinsky A. Aggrecan: approaches to study biophysical and biomechanical properties. Methods Mol Biol 2015;1229:221–37. DOI: 10.1007/978-1-4939-1714-3_20. PMID: 25325957.

30. Frischknecht R., Seidenbecher C.I. Brevican: a key proteoglycan in the perisynaptic extracellular matrix of the brain. Int J Biochem Cell Biol 2012;44(7):1051–4. DOI: 10.1016/j.biocel.2012.03.022. PMID: 22537913.

31. Chen L., Liao J., Klineberg E. et al. Small leucine-rich proteoglycans (SLRPs): characteristics and function in the intervertebral disc. J Tissue Eng Regen Med 2017;11(3):602–8. DOI: 10.1002/term.2067. PMID: 26370612.

32. Pietraszek-Gremplewicz K., Karamanou K., Niang A. et al. Small leucine-rich proteoglycans and matrix metalloproteinase-14: Key partners? Matrix Biol 2017. DOI: 10.1016/ j.matbio.2017.12.006. PMID: 29253518.

33. Maytin E.V. Hyaluronan: more than just a wrinkle filler. Glycobiology 2016;26(6):553–9. DOI: 10.1093/glycob/ cww033. PMID: 26964566.

34. Pozzi A., Yurchenco P.D., Iozzo R.V. The nature and biology of basement membranes. Matrix Biol 2017;57–58:1–11. DOI: 10.1016/ j.matbio.2016.12.009. PMID: 28040522.

35. McCarthy K.J. The basement membrane proteoglycans perlecan and agrin: something old, something new. Curr Top Membr 2015;76:255–303. DOI: 10.1016/bs.ctm.2015.09.001. PMID: 26610917.

36. Gubbiotti M.A., Neill T., Iozzo R.V. et al. A current view of perlecan in physiology and pathology: a mosaic of functions. Matrix Biol 2017;57–58:285–98. DOI: 10.1016/j.matbio.2016.09.003. PMID: 27613501.

37. Farach-Carson M.C., Warren C.R., Harrington D.A., Carson D.D. Border patrol: insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol 2014;34:64–79. DOI: 10.1016/ j.matbio.2013.08.004. PMID: 24001398.

38. Halfter W., Dong S., Schurer B., Cole G.J. Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 1998;273(39):25404–12. PMID: 9738008.

39. Theocharis A.D., Karamanos N.K. Proteoglycans remodeling in cancer: underlying molecular mechanisms. Matrix Biol 2017. DOI: 10.1016/ j.matbio.2017.10.008. PMID: 29128506.

40. Knelson E.H., Nee J.C., Blobe G.C. Heparan sulfate signaling in cancer. Trends Biochem Sci 2014;39(6):277–88. DOI: 10.1016/j.tibs.2014.03.001. PMID: 24755488.

41. Schaefer L., Tredup C., Gubbiotti M.A. et al. Proteoglycan neofunctions: regulation of inflammation and autophagy in cancer biology. FEBS J 2017;284(1): 10–26. DOI: 10.1111/febs.13963. PMID: 27860287.

42. Neill T., Schaefer L., Iozzo R.V. Decorin as a multivalent therapeutic agent against cancer. Adv Drug Deliv Rev 2016;97: 174–85. DOI: 10.1016/j.addr. 2015.10.016. PMID: 26522384.

43. Reed C.C., Gauldie J., Iozzo R.V. Suppression of tumorigenicity by adenovirus-mediated gene transfer of decorin. Oncogene 2002;21(23):3688–95. DOI: 10.1038/sj.onc.1205470. PMID: 12032837.

44. Goldoni S., Seidler D.G., Heath J. et al. An antimetastatic role for decorin in breast cancer. Am J Pathol 2008;173(3):844–55. DOI: 10.2353/ajpath.2008.080275. PMID: 18688028.

45. Du W.W., Yang W., Yee A.J. Roles of versican in cancer biology – tumorigenesis, progression and metastasis. Histol Histopathol 2013;28(6):701–13. DOI: 10.14670/HH-28.701. PMID: 23519970.

46. Yoneda A., Lendorf M.E., Couchman J.R. et al. Breast and ovarian cancers: a survey and possible roles for the cell surface heparan sulfate proteoglycans. J Histochem Cytochem 2012;60(1):9–21. DOI: 10.1369/0022155411428469. PMID: 22205677.

47. Theocharis A.D., Skandalis S.S., Neill T. et al. Insights into the key roles of proteoglycans in breast cancer biology and translational medicine. Biochim Biophys Acta 2015;1855(2):276–300. DOI: 10.1016/j.bbcan.2015.03.006. PMID: 25829250.

48. Eshchenko T.Y., Rykova V.I., Chernakov A.E. et al. Expression of different proteoglycans in human breast tumors. Biochemistry (Mosc) 2007;72(9): 1016–20. PMID: 17922662.

49. Yang X., Qiu M., Hu J. et al. Glypican-5 is a novel metastasis suppressor gene in non-small cell lung cancer. Cancer Lett 2013;341(2):265–73. DOI: 10.1016/j.canlet.2013.08.020. PMID: 23962560.

50. Melo S., Luecke L., Kahlert C. et al. Glypican1 identifies cancer exosomes and facilitates early detection of cancer. Nature 2015;523(7559):177–82. DOI: 10.1038/nature14581. PMID: 26106858.

51. Gharbaran R. Insights into the molecular roles of heparan sulfate proteoglycans (HSPGs-syndecans) in autocrine and paracrine growth factor signaling in the pathogenesis of Hodgkin’s lymphoma. Tumour Biol 2016;37(9):11573–88. DOI: 10.1007/s13277-016-5118-7. PMID: 27317256.

52. Tsidulko A.Y., Matskova L., Astakhova L.A. et al. Proteoglycan expression correlates with the phenotype of malignant and non-malignant EBV-positive B-cell lines. Oncotarget 2015;6(41):43529–39. DOI: 10.18632/oncotarget.5984. PMID: 26527314.

53. Hu T.H., Huang C.C., Wu C.L. et al. Increased endostatin/collagen XVIII expression correlates with elevated VEGF level and poor prognosis in hepatocellular carcinoma. Mod Pathol 2005;18(5): 663–72. DOI: 10.1038/modpathol. 3800336. PMID: 15605080.

54. Suhovskih A.V., Aidagulova S.V., Kashuba V.I. et al. Proteoglycans as potential microenvironmental biomarkers for colon cancer. Cell Tissue Res 2015;361(3):833–44. DOI: 10.1007/s00441-015-2141-8. PMID: 25715761.

55. Baghy K., Tátrai P., Regős E. et al. Proteoglycans in liver cancer. World J Gastroenterol 2016;22(1):379–93. DOI: 10.3748/wjg.v22.i1.379. PMID: 26755884.

56. Leygue E., Snell L., Dotzlaw H. et al. Lumican and decorin are differentially expressed in human breast carcinoma. J Pathol 2000;192(3):313–20. DOI: 10.1002/1096-9896(200011) 192:33.0.CO;2-B. PMID: 11054714.

57. Weber C.K., Sommer G., Michl P. et al. Biglycan is overexpressed in pancreatic cancer and induces G1-arrest in pancreatic cancer cell lines. Gastroenterology 2001;121(3):657–67. PMID: 11522750.

58. Zimina N.P., Dmitriev I.P., Rykova V.I. Composition and degree of sulfation of glycosaminoglycans from tissues of different animal species: heterogeneity and tissue specificity of heparan sulfates. Biokhimiia 1987;52(6):984–90. PMID: 2959327.

59. Суховских А.В., Григорьева Э.В. Тканеспецифичность экспрессии протеогликанов в различных типах опухолей человека. Успехи молекулярной онкологии 2016;3(1):53–60. [Suhovskih A.V., Grigor’eva E.V. Tissue-specificity of proteoglycans expression in different cancers. Uspekhi molekulyarnoy onkologii = Advances in Molecular Oncology 2016;3(1):53–60. (In Russ.)]. DOI: 10.17650/ 2313-805X.2016.3.1.53-60.

60. Suhovskih A.V., Domanitskaya N.V., Tsidulko A.Y. et al. Tissue-specificity of heparan sulfate biosynthetic machinery in cancer. Cell Adh Migr 2015;9(6):452–9. DOI: 10.1080/19336918.2015.1049801. PMID: 26120938.

61. Kazanskaya G.M., Tsidulko A.Y., Volkov A.M. et al. Heparan sulfate accumulation and perlecan/HSPG2 upregulation in tumour tissue predict low relapse-free survival for patients with glioblastoma. Histochem Cell Biol 2018. DOI: 10.1007/s00418-018-1631-7. PMID: 29322326.

62. Tsidulko A.Y., Kazanskaya G.M., Kostromskaya D.V. et al. Prognostic relevance of NG2/CSPG4, CD44 and Ki67 in patients with glioblastoma. Tumour Biol 2017;39(9):1010428317724282. DOI: 10.1177/1010428317724282. PMID: 28945172.

63. Suhovskih A.V., Kashuba V.I., Klein G., Grigorieva E.V. Prostate cancer cells specifically reorganize epithelial cellfibroblast communication through proteoglycan and junction pathways. Cell Adh Migr 2017;11(1):39–53. DOI: 10.1080/19336918.2016.1182292. PMID: 27111714.

64. Suhovskih A.V., Mostovich L.A., Kunin I.S. et al. Proteoglycan expression in normal human prostate tissue and prostate cancer. ISRN Oncol 2013:680136. DOI: 10.1155/2013/680136. PMID: 23691363.

65. Wang D., Anderson J.C., Gladson C.L. The role of the extracellular matrix in angiogenesis in malignant glioma tumors. Brain Pathol 2005;15(4):318–26. PMID: 16389944.

66. Wade A., Robinson A.E., Engler J.R. et al. Proteoglycans and their roles in brain cancer. FEBS J 2013;280(10):2399–417. DOI: 10.1111/febs.12109.23281850. PMID: 23281850.

67. Yao T., Zhang C.G., Gong M.T. et al. Decorin-mediated inhibition of the migration of U87MG glioma cells involves activation of autophagy and suppression of TGF-β signaling. FEBS Open Bio 2016;6(7):707–19. DOI: 10.1002/2211-5463.12076. PMID: 27398310.

68. Biglari A., Bataille D., Naumann U. et al. Effects of ectopic decorin in modulating intracranial glioma progression in vivo, in a rat syngeneic model. Cancer Gene Ther 2004;11(11):721–32. DOI: 10.1038/ sj.cgt.7700783. PMID: 15475879.

69. Arslan F., BosserhoffA.K., Nickl-Jockschat T. et al. The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-β2. Br J Cancer 2007;96(10):1560–8. DOI: 10.1038/ sj.bjc.6603766. PMID: 17453002.

70. Onken J., Moeckel S., Leukel P. et al. Versican isoform V1 regulates proliferation and migration in high-grade gliomas. J Neurooncol 2014;120(1):73–83. DOI: 10.1007/s11060-014-1545-8. PMID: 25064688.

71. Stallcup W.B., Huang F.J. A role for the NG2 proteoglycan in glioma progression. Cell Adh Migr 2008;2(3):192–201. PMID: 19262111.

72. Higgins S.C., Bolteus A.J., Donovan L.K. et al. Expression of the chondroitin sulphate proteoglycan, NG2, in paediatric brain tumors. Anticancer Res 2014;34(12):6919–24. PMID: 25503117.

73. Svendsen A., Verhoeff J.J., Immervoll H. et al. Expression of the progenitor marker NG2/CSPG4 predicts poor survival and resistance to ionising radiation in glioblastoma. Acta Neuropathol 2011;122(4):495–510. DOI: 10.1007/s00401-011-0867-2. PMID: 21863242.

74. Lu R., Wu C., Guo L. et al. The role of brevican in glioma: promoting tumor cell motility in vitro and in vivo. BMC Cancer 2012;12:607. DOI: 10.1186/1471-2407-12-607. PMID: 23253190.

75. Hu B., Kong L.L., Matthews R.T. The proteoglycan brevican binds to fibronectin after proteolytic cleavage and promotes glioma cell motility. J Biol Chem 2008;283(36):24848–59. DOI: 10.1074/jbc.M801433200. PMID: 18611854.

76. Wiranowska M., Ladd S., Smith S.R. et al. CD44 adhesion molecule and neuro-glial proteoglycan NG2 as invasive markers of glioma. Brain Cell Biol 2006;35(2–3): 159–72. DOI: 10.1007/ s11068-007-9009-0. PMID: 17957481.

77. Radotra B., McCormick D. Glioma invasion in vitro is mediated by CD44–hyaluronan interactions. J Pathol 1997;181(4):434–8. DOI: 10.1002/(SICI)1096-9896(199704) 181:43.0.CO;2-S. PMID: 9196442.

78. Roy A., Attarha S., Weishaupt H. et al. Serglycin as a potential biomarker for glioma: association of serglycin expression, extent of mast cell recruitment and glioblastoma progression. Oncotarget 2017;8(15):24815–27. DOI: 10.18632/oncotarget.15820. PMID: 28445977.

79. Xu Y., Yuan J., Zhang Z. et al. Syndecan-1 expression in human glioma is correlated with advanced tumor progression and poor prognosis. Mol Biol Rep 2012;39(9): 8979–85. DOI: 10.1007/ s11033-012-1767-9. PMID: 22714920.

80. Watanabe A., Mabuchi T., Satoh E. et al. Expresson of syndecans, a heparan sulfate proteoglycan, in malignant gliomas: participation of nuclear factor-κB in upregulation of syndecan-1 expression. J Neurooncol 2006;77(1):25–32. DOI: 10.1007/s11060-005-9010-3. PMID: 16132527.

81. Qiao D., Meyer K., Mundhenke C. et al. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Spеcific role for glypican-1 in glioma angiogenesis. J Biol Chem 2003;278(18):16045–53. DOI: 10.1074/jbc.M211259200. PMID: 12591930.

82. Su G., Meyer K., Nandini C.D. et al. Glypican-1 is frequently overexpressed in human gliomas and enhances FGF-2 signaling in glioma cells. Am J Pathol 2006;168(6):2014–26. DOI: 10.2353/ajpath.2006.050800. PMID: 16723715.

83. Edwards I.J. Proteoglycans in prostate cancer. Nat Rev Urol 2012;9(4):196–206. DOI: 10.1038/nrurol.2012.19. PMID: 22349653.

84. Kiviniemi J., Kallajoki M., Kujala I. et al. Altered expression of syndecan-1 in prostate cancer. APMIS 2004;112(2):89–97. DOI: 10.1111/j.1600-0463.2004. apm1120202.x. PMID: 15056224.

85. Contreras H.R., Ledezma R.A., Vergara J. et al. The expression of syndecan-1 and -2 is associated with Gleason score and epithelial-mesenchymal transition markers, E-cadherin and beta-catenin, in prostate cancer. Urol Oncol 2010;28(5):534–40. DOI: 10.1016/ j.urolonc.2009.03.018. PMID: 19450993.

86. Shariat S.F., Svatek R.S., Kabbani W. et al. Prognostic value of syndecan-1 expression in patients treated with radical prostatectomy. BJU Int 2008;101(2):232–7. DOI: 10.1111/j.1464-410X.2007.07181.x. PMID: 17868422.

87. Zellweger T., Ninck C., Bloch M. et al. Expression patterns of potential therapeutic targets in prostate cancer. Int J Cancer 2005;113(4):619–28. DOI: 10.1002/ijc.20615. PMID: 15472903.

88. Brimo F., Vollmer R.T., Friszt M. et al. Syndecan-1 expression in prostate cancer and its value as biomarker for disease progression. BJU Int 2010;106(3):418–23. DOI: 10.1111/j.1464-410X.2009.09099.x. PMID: 20002675.

89. Truong Q., Justiniano I.O., Nocon A.L. et al. Glypican-1 as a biomarker for prostate cancer: isolation and characterization. J Cancer 2016;7(8):1002–9. DOI: 10.7150/jca.14645. PMID: 27313791.

90. Zhang C., Liu Z., Wang L. et al. Prognostic significance of GPC5 expression in patients with prostate cancer. Tumour Biol 2016;37(5):6413–8. DOI: 10.1007/s13277-015-4499-3. PMID: 26631038.

91. Warren C.R., Grindel B.J., Francis L. et al. Transcriptional activation by NFκB increases perlecan/HSPG2 expression in the desmoplastic prostate tumor microenvironment. J Cell Biochem 2014;115(7):1322–33. DOI: 10.1002/ jcb.24788. PMID: 24700612.

92. Grindel B.J., Martinez J.R., Pennington C.L. et al. Matrilysin/matrix metalloproteinase-7 (MMP7) cleavage of perlecan/HSPG2 creates a molecular switch to alter prostate cancer cell behavior. Matrix Biol 2014;36:64–76. DOI: 10.1016/j.matbio.2014.04.005. PMID: 24833109.

93. Grindel B., Li Q., Arnold R. et al. Perlecan/HSPG2 and matrilysin/MMP-7 as indices of tissue invasion: tissue localization and circulating perlecan fragments in a cohort of 288 radical prostatectomy patients. Oncotarget 2016;7(9):10433–47. DOI: 10.18632/oncotarget.7197. PMID: 26862737.

94. Coulson-Thomas V.J., Gesteira T.F., Coulson-Thomas Y.M. et al. Fibroblast and prostate tumor cell cross-talk: fibroblast differentiation, TGF-β, and extracellular matrix down-regulation. Exp Cell Res 2010;316(19):3207–26. DOI: 10.1016/j.yexcr.2010.08.005. PMID: 20727350.

95. Xu W., Neill T., Yang Y. et al. The systemic delivery of an oncolytic adenovirus expressing decorin inhibits bone metastasis in a mouse model of human prostate cancer. Gene Ther 2015;22(3):247–56. DOI: 10.1038/gt.2014.110. PMID: 25503693.

96. Holland J.W., Meehan K.L., Redmond S.L. et al. Purification of the keratan sulfate proteoglycan expressed in prostatic secretory cells and its identification as lumican. Prostate 2004;59(3):252–9. DOI: 10.1002/pros.20002. PMID: 15042600.

97. Coulson-ThomasV.J., Coulson-ThomasY.M., Gesteira T.F. et al. Lumican expression, localization and antitumor activity in prostate cancer. Exp Cell Res 2013;319(7):967–81. DOI: 10.1016/j.yexcr.2013.01.023. PMID: 23399832.

98. True L.D., Hawley S., Norwood T.H. et al. The accumulation of versican in the nodules of benign prostatic hyperplasia. Prostate 2009;69(2):149–58. DOI: 10.1002/pros.20861. PMID: 18819099.

99. Arichi N., Mitsui Y., Hiraki M. et al. Versican is a potential therapeutic target in docetaxel-resistant prostate cancer. Oncoscience 2015;2(2):193–204. DOI: 10.18632/oncoscience.136. PMID: 25859560.

100. Mulloy B., Lever R., Page C.P. Mast cell glycosaminoglycans. Glycoconj J 2017;34(3):351–61. DOI: 10.1007/ s10719-016-9749-0. PMID: 27900574.

101. Li X.J., Qian C.N. Serglycin in human cancers. Chin J Cancer 2011;30(9):585–9. DOI: 10.5732/cjc.011.10314. PMID: 21880179.

102. Korpetinou A., Skandalis S.S., Labropoulou V.T. et al. Serglycin: at the crossroad of inflammation and malignancy. Front Oncol 2014;3:327. DOI: 10.3389/fonc.2013.00327. PMID: 24455486.

103. Purushothaman A., Toole B.P. Serglycin proteoglycan is required for multiple myeloma cell adhesion, in vivo growth, and vascularization. J Biol Chem 2014;289(9):5499–509. DOI: 10.1074/jbc.M113.532143. PMID: 24403068.

104. Bhavanandan V.P., Davidson E.A. Mucopolysaccharides associated with nuclei of cultured mammalian cells. PNAS 1975;72(6):2032–6. PMID: 124440.

105. Margolis R.K., Crockett C.P., Kiang W.L. et al. Glycosaminoglycans and glycoproteins associated with rat brain nuclei. BBA-General Subjects 1976;451(2):465–9. PMID: 999866.

106. Stein G.S., Roberts R.M., Davis J.L. et al. Are glycoproteins and glycosaminoglycans components of the eukaryotic genome? Nature 1975;258(5536):639–41. PMID: 128700.

107. Hiscock D.R., Yanagishita M., Hascall V.C. Nuclear localization of glycosaminoglycans in rat ovarian granulosa cells. J Biol Chem 1994;269(6):4539–46. PMID: 8308024.

108. Carthy J.M., Abraham T., Meredith A.J. et al. Versican localizes to the nucleus in proliferating mesenchymal cells. Cardiovasc Pathol 2015;24(6):368–74. DOI: 10.1016/j.carpath.2015.07.010. PMID: 26395512.

109. Григорьева Э.В., Рыкова В.И. Ядерные протеогликаны клеток печени мышей: выделение и идентификация. Биохимия 1992;58(8):1165–70. [Grigor’eva E.V., Rykova V.I. Nuclear proteoglycans of murine liver cells: isolation and identification. Biokhimiya = Biochemistry 1992;58(8):1165–70. (In Russ.)].

110. Рыкова В.И., Григорьева Э.В. Состав протеогликанов клеточных ядер гепатомы мыши. Биохимия 1998;63(11):1271–6. [Rykova V.I., Grigor’eva E.V. The composition of proteoglycans of mouse hepatoma cell nuclei. Biokhimiya = Biochemistry 1998;63(11):1271–6. (In Russ.)].

111. Kovalszky I., Hjerpe A., Dobra K. Nuclear translocation of heparan sulfate proteoglycans and their functional significance. Biochem Biophys Acta 2014;1840(8):2491–7. DOI: 10.1016/j.bbagen.2014.04.015. PMID: 24780644.

112. Ishihara M., Fedarko N.S., Conrad H.E. Transport of heparan sulfate into the nuclei of hepatocytes. J Biol Chem 1986;261(29):13575–80. PMID: 2944884.

113. Fedarko N.S., Conrad H.E. A unique heparan sulfate in the nuclei of hepatocytes: structural changes with the growth state of the cells. J Cell Biol 1986;102(2):587–99. PMID: 2935544.

114. Cheng F., Petersson P., Arroyo-Yanguas Y. et al. Differences in the uptake and nuclear localization of anti-proliferative heparan sulfate between human lung fibroblasts and human lung carcinoma cells. J Cell Biochem 2001;83(4):597–606. PMID: 11746503.

115. Stewart M.D., Sanderson R.D. Heparan sulfate in the nucleus and its control of cellular functions. Matrix Biol 2014;35:56–9. DOI: 10.1016/j.matbio. 2013.10.009. PMID: 24309018.

116. Amalric F., Bouche G., Bonnet H. et al. Fibroblast growth factor-2 (FGF-2) in the nucleus: translocation process and targets. Biochem Pharmacol 1994;47(1):111–5. PMID: 8311835.

117. Hsia E., Richardson T.P., Nugent M.A. Nuclear localization of basic fibroblast growth factor is mediated by heparan sulfate proteoglycans through protein kinase C signaling. J Cell Biochem 2003;88(6):1214–25. DOI: 10.1002/jcb.10470. PMID: 12647303.

118. Zong F., Fthenou E., Wolmer N. et al. Syndecan-1 and FGF-2, but not FGF receptor-1, share a common transport route and co-localize with heparanase in the nuclei of mesenchymal tumor cells. PLoS One 2009;4(10):e7346. DOI: 10.1371/journal.pone.0007346. PMID: 19802384.

119. Brockstedt U., Dobra K., Nurminen M. et al. Immunoreactivity to cell surface syndecans in cytoplasm and nucleus: tubulin-dependent rearrangements. Exp Cell Res 2002;274(2):235–45. DOI: 10.1006/excr.2002.5477. PMID: 11900484.

120. Ishihara M., Conrad H.E. Correlations between heparan sulfate metabolism and hepatoma growth. J Cell Physiol 1989;138(3):467–76. DOI: 10.1002/jcp.1041380305. PMID: 2522457.

121. Fedarko N.S., Ishihara M., Conrad H.E. Control of cell division in hepatoma cells by exogenous heparan sulfate proteoglycan. J Cell Physiol 1989;139(2):287–94. DOI: 10.1002/jcp.1041390210. PMID: 2715188.

122. Liang Y., Häring M., Roughley P.J. et al. Glypican and biglycan in the nuclei of neurons and glioma cells: presence of functional nuclear localization signals and dynamic changes in glypican during the cell cycle. J Cell Biol 1997;39(4):851–64. PMID: 9362504.

123. Buczek-Thomas J.A., Hsia E., Rich C.B. et al. Inhibition of histone acetyltransferase by glycosaminoglycans. J Cell Biochem 2008; 105(1):108–20. DOI: 10.1002/jcb.21803. PMID: 18459114.

124. Purushothaman A., Hurst D.R., Pisano C. et al. Heparanase-mediated loss of nuclear syndecan-1 enhances histone acetyltransferase (HAT) activity to promote expression of genes that drive an aggressive tumor phenotype. J Biol Chem 2011;286(35):30377–83. DOI: 10.1074/jbc.M111.254789. PMID: 21757697.

125. Romanato M., Julianelli V., Zappi M. et al. The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo. Hum Reprod 2008;23(5):1145–50. DOI: 10.1093/humrep/den028. PMID: 18287106.

126. Sanchez M.C., Alvarez Sedo C., Julianelli V.L. et al. Dermatan sulfate synergizes with heparin in murine sperm chromatin decondensation. Syst Biol Reprod Med 2013;59(2):82–90. DOI: 10.3109/19396368.2012.756952. PMID: 23301776.

127. Kovalszky I., Dudás J., Oláh-Nagy J. et al. Inhibition of DNA topoisomerase I activity by heparin sulfate and modulation by basic fibroblast growth factor. Mol Cell Biochem 1998;183(1):11–23. PMID: 9655174.

128. Cheng F., Belting M., Fransson L.A. et al. Nucleolin is a nuclear target of heparan sulfate derived from glypican-1. Exp Cell Res 2017;354(1):31–9. DOI: 10.1016/j.yexcr.2017.03.021. PMID: 28300561.

129. Григорьева Э.В., Рыкова В.И. Взаимодействие ядерных протеогликанов с олигорибонуклеотидами. Доклады Академии наук 1997;356(5):693–5. [Grigor’eva E.V., Rykova V.I. Interactions between nuclear proteoglycans and oligoribonucleotides. Doklady Akademii nauk = Proceedings of the Academy of Sciences 1997;356(5):693–5. (In Russ.)].

130. Busch S.J., Martin G.A., Barnhart R.L. et al. Trans-repressor activity of nuclear glycosaminoglycans on Fos and Jun/AP-1 oncoprotein-mediated transcription. J Cell Biol 1992;116(1):31–42. PMID: 1730747.

131. Dudas J., Ramadori G., Knittel T. et al. Effect of heparin and liver heparansulphate on interaction of HepG2-derived transcription factors and their cis-acting elements: altered potential of hepatocellular carcinoma heparansulphate. Biochem J 2000;350(1):245–51. PMID: 10926850.


Для цитирования:


Суховских А.В., Григорьева Э.В. Протеогликаны в нормальной физиологии и канцерогенезе. Успехи молекулярной онкологии. 2018;5(1):8-25. https://doi.org/10.17650/2313-805X-2018-5-1-8-25

For citation:


Suhovskih A.V., Grigorieva E.V. Proteoglycans in normal physiology and carcinogenesis. Advances in molecular oncology. 2018;5(1):8-25. (In Russ.) https://doi.org/10.17650/2313-805X-2018-5-1-8-25

Просмотров: 190


Creative Commons License
Контент доступен под лицензией Creative Commons Attribution 4.0 License.


ISSN 2313-805X (Print)
ISSN 2413-3787 (Online)