Роль лизосом в онкогенезе: акцент на деградацию внеклеточного матрикса
Аннотация
Лизосомы – многофункциональные клеточные органеллы, которые не только обеспечивают деградацию макромолекул люменальными кислыми гидролазами, но также участвуют в регуляции клеточного метаболизма, поддержании ионного гомеостаза и индукции программируемой клеточной гибели. Особый интерес вызывает изучение этого компартмента при различных патологических состояниях, в том числе при развитии онкологических заболеваний различного генеза. Метаболические и морфологические изменения клеток в процессе онкогенеза приводят к рН-зависимому перераспределению лизосом в пределах клетки, сопровождающемуюся секрецией лизосомальных протеаз катепсинов во внеклеточное пространство. Цистеиновые, сериновые и аргининовые катепсины, выделяемые как опухолевыми клетками, так и клетками, ассоциированными с опухолью, катализируют расщепление различных компонентов внеклеточного матрикса и базальной мембраны или протеолитически активируют другие ферменты, также участвующие в этом процессе. При этом лизосомальные протеазы непосредственно влияют на способность клеток к инвазии и метастатический потенциал опухолевого образования. Кроме того, было продемонстрировано прогностическое значение некоторых катепсинов (особенно катепсинов B, K и D), количество и активность которых в опухолевой ткани и в её микроокружении сопряжены со злокачественностью образования, а также с плохим прогнозом по выживаемости пациентов и возможностью возникновения рецидивов.
Об авторах
И. С. Трухан
ФГБНУ «Иркутский научный центр хирургии и травматологии»
Россия
Россия
кандидат биологических наук, старший научный сотрудник
664003, г. Иркутск, ул. Борцов Революции, 1, Россия
Н. Н. Дремина
ФГБНУ «Иркутский научный центр хирургии и травматологии»
Россия
Россия
кандидат биологических наук, старший научный сотрудник
664003, г. Иркутск, ул. Борцов Революции, 1, Россия
И. А. Шурыгина
ФГБНУ «Иркутский научный центр хирургии и травматологии»
Россия
Россия
доктор медицинских наук, профессор РАН, заместитель директора по научной работе
664003, г. Иркутск, ул. Борцов Революции, 1, Россия
Список литературы
1. Ballabio A, Bonifacino JS. Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat Rev Mol Cell Biol. 2020; 21: 101-118. doi: 10.1038/s41580-019-0185-4
2. Lawrence RE, Zoncu R. The lysosome as a cellular centre for signalling, metabolism and quality control. Nat Cell Biol. 2019; 21(2): 133-142. doi: 10.1038/s41556-018-0244-7
3. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell. 2011; 144(5): 646-674. doi: 10.1016/j.cell.2011.02.013
4. Ji K, Mayernik L, Moin K, Sloane BF. Acidosis and proteolysis in the tumor microenvironment. Cancer Metastasis Rev. 2019; 38(1-2): 103-112. doi: 10.1007/s10555-019-09796-3
5. Pavlova NN, Thompson CB. The emerging hallmarks of cancer metabolism. Cell Metab. 2016; 23(1): 27-47. doi: 10.1016/j.cmet.2015.12.006
6. Warburg O. The metabolism of carcinoma cells. Cancer Research. 1925; 9(1), 148-163. doi: 10.1158/jcr.1925.148
7. Pascale RM, Calvisi DF, Simile MM, Feo CF, Feo F. The Warburg effect 97 years after its discovery. Cancers (Basel). 2020; 12(10): 2819. doi: 10.3390/cancers12102819
8. Boedtkjer E, Pedersen SF. The acidic tumor microenvironment as a driver of cancer. Annu Rev Physiol. 2020; 82: 103-126. doi: 10.1146/annurev-physiol-021119-034627
9. Parks SK, Mueller-Klieser W, Pouysségur J. Lactate and acidity in the cancer microenvironment. Annu Rev Cancer Biol. 2020; 4: 141-158. doi: 10.1146/annurev-cancerbio-030419-033556
10. Ko M, Quiñones-Hinojosa A, Rao R. Emerging links between endosomal pH and cancer. Cancer Metastasis Rev. 2020; 39(2): 519-534. doi: 10.1007/s10555-020-09870-1
11. White KA, Grillo-Hill BK, Barber DL. Cancer cell behaviors mediated by dysregulated pH dynamics at a glance. J Cell Sci. 2017; 130(4): 663-669. doi: 10.1242/jcs.195297
12. Heuser J. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J Cell Biol. 1989; 108(3): 855-864. doi: 10.1083/jcb.108.3.855
13. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol. 2013; 14(5): 283-296. doi: 10.1038/nrm3565
14. Rozhin J, Sameni M, Ziegler G, Sloane BF. Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res. 1994; 54(24): 6517-6525.
15. Hazen LG, Bleeker FE, Lauritzen B, Bahns S, Song J, Jonker A, et al. Comparative localization of cathepsin B protein and activity in colorectal cancer. J Histochem Cytochem. 2000; 48(10): 1421-1430. doi: 10.1177/002215540004801012
16. Dykes SS, Steffan JJ, Cardelli JA. Lysosome trafficking is necessary for EGF-driven invasion and is regulated by p38 MAPK and Na+/H+ exchangers. BMC Cancer. 2017; 17(1): 672. doi: 10.1186/s12885-017-3660-3
17. Steffan JJ, Williams BC, Welbourne T, Cardelli JA. HGFinduced invasion by prostate tumor cells requires anterograde lysosome trafficking and activity of Na+–H+ exchangers. J Cell Sci. 2010; 123(Pt 7): 1151-1159. doi: 10.1242/jcs.063644
18. Glunde K, Guggino SE, Solaiyappan M, Pathak AP, Ichikawa Y, Bhujwalla ZM. Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia. 2003; 5(6): 533-545. doi: 10.1016/s1476-5586(03)80037-4
19. Damaghi M, Tafreshi NK, Lloyd MC, Sprung R, Estrella V, Wojtkowiak JW, et al. Chronic acidosis in the tumour microenvironment selects for overexpression of LAMP2 in the plasma membrane. Nat Commun. 2015; 6: 8752. doi: 10.1038/ncomms9752
20. Castro-Gomes T, Corrotte M, Tam C, Andrews NW. Plasma membrane repair is regulated extracellularly by proteases released from lysosomes. PLoS One. 2016; 11(3): e0152583. doi: 10.1371/journal.pone.0152583
21. Sameni M, Elliott E, Ziegler G, Fortgens PH, Dennison C, Sloane BF. Cathepsin B and D are localized at the surface of human breast cancer cells. Pathol Oncol Res. 1995; 1(1): 43-53. doi: 10.1007/BF02893583
22. Paterson EK, Courtneidge SA. Invadosomes are coming: new insights into function and disease relevance. FEBS J. 2018; 285(1): 8-27. doi: 10.1111/febs.14123
23. Brisson L, Reshkin SJ, Goré J, Roger S. pH regulators in invadosomal functioning: Proton delivery for matrix tasting. Eur J Cell Biol. 2012; 91(11-12): 847-860. doi: 10.1016/j.ejcb.2012.04.004
24. Tu C, Ortega-Cava CF, Chen G, Fernandes ND, CavalloMedved D, Sloane BF, et al. Lysosomal cathepsin B participates in the podosome-mediated extracellular matrix degradation and invasion via secreted lysosomes in v-Src fibroblasts. Cancer Res. 2008; 68(22): 9147-9156. doi: 10.1158/0008-5472.CAN-07-5127
25. Kryczka J, Papiewska-Pajak I, Kowalska MA, Boncela J. Cathepsin B is upregulated and mediates ECM degradation in colon adenocarcinoma HT29 cells overexpressing snail. Cells. 2019; 8(3): 203. doi: 10.3390/cells8030203
26. Linder S, Wiesner C, Himmel M. Degrading devices: Invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol. 2011; 27: 185-211. doi: 10.1146/annurev-cellbio-092910-154216
27. Vasiljeva O, Hostetter DR, Moore SJ, Winter MB. The multifaceted roles of tumor-associated proteases and harnessing their activity for prodrug activation. Biol Chem. 2019; 400(8): 965-977. doi: 10.1515/hsz-2018-0451
28. Kramer L, Turk D, Turk B. The future of cysteine cathepsins in disease management. Trends Pharmacol Sci. 2017; 38(10): 873-898. doi: 10.1016/j.tips.2017.06.003
29. Vizovišek M, Fonović M, Turk B. Cysteine cathepsins in extracellular matrix remodeling: Extracellular matrix degradation and beyond. Matrix Biol. 2019; 75-76: 141- 159. doi: 10.1016/j.matbio.2018.01.024
30. Vidak E, Javoršek U, Vizovišek M, Turk B. Cysteine cathepsins and their extracellular roles: Shaping the microenvironment. Cells. 2019; 8(3): 264. doi: 10.3390/cells8030264
31. Yadati T, Houben T, Bitorina A, Shiri-Sverdlov R. The ins and outs of cathepsins: Physiological function and role in disease management. Cells. 2020; 9(7): 1679. doi: 10.3390/cells9071679
32. Verbovšek U, Van Noorden CJ, Lah TT. Complexity of cancer protease biology: Cathepsin K expression and function in cancer progression. Semin Cancer Biol. 2015; 35: 71-84. doi: 10.1016/j.semcancer.2015.08.010
33. Lah TT, Cercek M, Blejec A, Kos J, Gorodetsky E, Somers R, et al. Cathepsin B, a prognostic indicator in lymph node-negative breast carcinoma patients: comparison with cathepsin D, cathepsin L, and other clinical indicators. Clin Cancer Res. 2000; 6(2): 578-584.
34. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, et al. IL-4 induces cathepsin protease activity in tumorassociated macrophages to promote cancer growth and invasion. Genes Dev. 2010; 24(3): 241-255. doi: 10.1101/gad.1874010
35. Tripathi R, Fiore LS, Richards DL, Yang Y, Liu J, Wang C, et al. Abl and Arg mediate cysteine cathepsin secretion to facilitate melanoma invasion and metastasis. Sci Signal. 2018; 11(518): eaao0422. doi: 10.1126/scisignal.aao0422
36. Chen S, Dong H, Yang S, Guo H. Cathepsins in digestive cancers. Oncotarget. 2017; 8(25): 41690-41700. doi: 10.18632/oncotarget.16677
37. da Costa AC, Santa-Cruz F, Mattos LAR, Rêgo Aquino MA, Martins CR, Bandeira Ferraz ÁA, et al. Cathepsin S as a target in gastric cancer. Mol Clin Oncol. 2020; 12(2): 99-103. doi: 10.3892/mco.2019.1958
38. Singh N, Saraya A. Roles of cathepsins in pancreatic cancer. Trop Gastroenterol. 2016; 37(2): 77-85.
39. Fernández PL, Farré X, Nadal A, Fernández E, Peiró N, Sloane BF, et al. Expression of cathepsins B and S in the progression of prostate carcinoma. Int J Cancer. 2001; 95(1): 51-55. doi: 10.1002/1097-0215(20010120)95:1<51::aid-ijc1009>3.0.co;2-j
40. Wang J, Chen L, Li Y, Guan XY. Overexpression of cathepsin Z contributes to tumor metastasis by inducing epithelialmesenchymal transition in hepatocellular carcinoma. PLoS One. 2011; 6(9): e24967. doi: 10.1371/journal.pone.0024967
41. Kuester D, Lippert H, Roessner A, Krueger S. The cathepsin family and their role in colorectal cancer. Pathol Res Pract. 2008; 204(7): 491-500. doi: 10.1016/j.prp.2008.04.010
42. Hölzen L, Parigiani MA, Reinheckel T. Tumor cell- and microenvironment-specific roles of cysteine cathepsins in mouse models of human cancers. Biochim Biophys Acta Proteins Proteom. 2020; 1868(7): 140423. doi: 10.1016/j.bbapap.2020.140423
43. Maacha S, Hong J, von Lersner A, Zijlstra A, Belkhiri A. AXL mediates esophageal adenocarcinoma cell invasion through regulation of extracellular acidification and lysosome trafficking. Neoplasia. 2018; 20(10): 1008-1022. doi: 10.1016/j.neo.2018.08.005
44. Mijanović O, Branković A, Panin AN, Savchuk S, Timashev P, Ulasov I, et al. Cathepsin B: A sellsword of cancer progression. Cancer Lett. 2019; 449: 207-214. doi: 10.1016/j.canlet.2019.02.035
45. Liaudet-Coopman E, Beaujouin M, Derocq D, Garcia M, Glondu-Lassis M, Laurent-Matha V, et al. Cathepsin D: Newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett. 2006; 237(2): 167-179. doi: 10.1016/j.canlet.2005.06.007
46. Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev. 2010; 62(4): 726-759. doi: 10.1124/pr.110.002733
47. Kozlowski L, Wojtukiewicz MZ, Ostrowska H. Cathepsin A activity in primary and metastatic human melanocytic tumors. Arch Dermatol Res. 2000; 292(2-3): 68-71. doi: 10.1007/s004030050012
48. Hu B, Zhu X, Lu J. Cathepsin A knockdown decreases the proliferation and invasion of A549 lung adenocarcinoma cells. Mol Med Rep. 2020; 21(6): 2553-2559. doi: 10.3892/mmr.2020.11068
49. Ni S, Weng W, Xu M, Wang Q, Tan C, Sun H, et al. miR-106b-5p inhibits the invasion and metastasis of colorectal cancer by targeting CTSA. Onco Targets Ther. 2018; 11: 3835-3845. doi: 10.2147/OTT.S172887
50. Toss MS, Miligy IM, Haj-Ahmad R, Gorringe KL, AlKawaz A, Mittal K, et al. The prognostic significance of lysosomal protective protein (cathepsin A) in breast ductal carcinoma in situ. Histopathology. 2019; 74(7): 1025-1035. doi: 10.1111/his.13835
51. Du Z, Liu X, Wei X, Luo H, Li P, Shi M, et al. Quantitative proteomics identifies a plasma multi-protein model for detection of hepatocellular carcinoma. Sci Rep. 2020; 10(1): 15552. doi: 10.1038/s41598-020-72510-9
52. Burster T, Macmillan H, Hou T, Boehm BO, Mellins ED. Cathepsin G: Roles in antigen presentation and beyond. Mol Immunol. 2010; 47(4): 658-665. doi: 10.1016/j.molimm.2009.10.003
53. Gao S, Zhu H, Zuo X, Luo H. Cathepsin G and its role in inflammation and autoimmune diseases. Arch Rheumatol. 2018; 33(4): 498-504. doi: 10.5606/ArchRheumatol.2018.6595
54. Yui S, Osawa Y, Ichisugi T, Morimoto-Kamata R. Neutrophil cathepsin G, but not elastase, induces aggregation of MCF-7 mammary carcinoma cells by a protease activity-dependent cell-oriented mechanism. Mediators Inflamm. 2014; 2014: 971409. doi: 10.1155/2014/971409
55. Maksimowicz T, Chyczewska E, Chyczewski L, Nikliński J, Ostrowska H, Szyszko J, et al. Activity and tissue localization of cathepsin G in non-small cell lung cancer. Rocz Akad Med Bialymst. 1997; 42(Suppl 1): 199-216.
56. Morimoto-Kamata R, Mizoguchi S, Ichisugi T, Yui S. Cathepsin G induces cell aggregation of human breast cancer MCF-7 cells via a 2-step mechanism: Catalytic site-independent binding to the cell surface and enzymatic activity-dependent induction of the cell aggregation. Mediators Inflamm. 2012; 2012: 456462. doi: 10.1155/2012/456462
57. Kim J, Bae JS. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm. 2016; 2016: 6058147. doi: 10.1155/2016/6058147
58. Wilson TJ, Nannuru KC, Singh RK. Cathepsin G-mediated activation of pro-matrix metalloproteinase 9 at the tumor-bone interface promotes transforming growth factor-beta signaling and bone destruction. Mol Cancer Res. 2009; 7(8): 1224-1233. doi: 10.1158/1541-7786.MCR-09-0028
59. Shamamian P, Schwartz JD, Pocock BJ, Monea S, Whiting D, Marcus SG, et al. Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: A role for inflammatory cells in tumor invasion and angiogenesis. J Cell Physiol. 2001; 189(2): 197-206. doi: 10.1002/jcp.10014
60. Drag B, Petersen LC. Activation of pro-urokinase by cathepsin G in the presence of glucosaminoglycans. Fibrinolysis. 1994; 8: 192-199.
61. Bastos P, Magalhães S, Santos LL, Ferreira R, Vitorino R. The role of urinary proteases in bladder cancer. In: Chakraborti S, Dhalla N. Pathophysiological aspects of proteases. Singapore: Springer; 2017. doi: 10.1007/978-981-10-6141-7_4
62. Leto G, Tumminello FM, Crescimanno M, Flandina C, Gebbia N. Cathepsin D expression levels in nongynecological solid tumors: Clinical and therapeutic implications. Clin Exp Metastasis. 2004; 21(2): 91-106. doi: 10.1023/b:clin.0000024740.44602.b7
63. Masson O, Bach AS, Derocq D, Prébois C, LaurentMatha V, Pattingre S, et al. Pathophysiological functions of cathepsin D: Targeting its catalytic activity versus its protein binding activity? Biochimie. 2010; 92(11): 1635-1643. doi: 10.1016/j.biochi.2010.05.009
64. O’Donoghue AJ, Ivry SL, Chaudhury C, Hostetter DR, Hanahan D, Craik CS. Procathepsin E is highly abundant but minimally active in pancreatic ductal adenocarcinoma tumors. Biol Chem. 2016; 397(9): 871-881. doi: 10.1515/hsz-2016-0138
65. Pontious C, Kaul S, Hong M, Hart PA, Krishna SG, Lara LF, et al. Cathepsin E expression and activity: Role in the detection and treatment of pancreatic cancer. Pancreatology. 2019; 19(7): 951-956. doi: 10.1016/j.pan.2019.09.009
66. Benes P, Vetvicka V, Fusek M. Cathepsin D – many functions of one aspartic protease. Crit Rev Oncol Hematol. 2008; 68(1): 12-28. doi: 10.1016/j.critrevonc.2008.02.008
67. Garcia M, Platet N, Liaudet E, Laurent V, Derocq D, Brouillet JP, et al. Biological and clinical significance of cathepsin D in breast cancer metastasis. Stem Cells. 1996; 14(6): 642-650. doi: 10.1002/stem.140642
68. Pranjol ZI, Whatmore JL. Cathepsin D in the tumor microenvironment of breast and ovarian cancers. Adv Exp Med Biol. 2020; 1259: 1-16. doi: 10.1007/978-3-030-43093-1_1
69. Laurent-Matha V, Maruani-Herrmann S, Prébois C, Beaujouin M, Glondu M, Noël A, et al. Catalytically inactive human cathepsin D triggers fibroblast invasive growth. J Cell Biol. 2005; 168(3): 489-499. doi: 10.1083/jcb.200403078
70. Vetvicka V, Vetvickova J, Fusek M. Role of procathepsin D activation peptide in prostate cancer growth. Prostate. 2000; 44(1): 1-7. doi: 10.1002/1097-0045(20000615)44:1<1::aidpros1>3.0.co;2-4
71. Yang L, Cui M, Zhang L, Song L. FOXM1 facilitates gastric cancer cell migration and invasion by inducing cathepsin D. Oncotarget. 2017; 8(40): 68180-68190. doi: 10.18632/oncotarget.19254
72. Kang J, Yu Y, Jeong S, Lee H, Heo HJ, Park JJ, et al. Prognostic role of high cathepsin D expression in breast cancer: A systematic review and meta-analysis. Ther Adv Med Oncol. 2020; 12: 1758835920927838. doi: 10.1177/1758835920927838
73. Gemoll T, Epping F, Heinrich L, Fritzsche B, Roblick UJ, Szymczak S, et al. Increased cathepsin D protein expression is a biomarker for osteosarcomas, pulmonary metastases and other bone malignancies. Oncotarget. 2015; 6(18): 16517-16526. doi: 10.18632/oncotarget.4140
74. Mehrotra S, Wickremesekera SK, Brasch HD, Van Schaijik B, Marsh RW, Tan ST, et al. Expression and localization of cathepsins B, D and G in cancer stem cells in liver metastasis from colon adenocarcinoma. Front Surg. 2018; 5: 40. doi: 10.3389/fsurg.2018.00040
75. Basu S, Cheriyamundath S, Gavert N, Brabletz T, Haase G, Ben-Ze›ev A. Increased expression of cathepsin D is required for L1-mediated colon cancer progression. Oncotarget. 2019; 10(50): 5217-5228. doi: 10.18632/oncotarget.27155
76. Pruitt FL, He Y, Franco OE, Jiang M, Cates JM, Hayward SW. Cathepsin D acts as an essential mediator to promote malignancy of benign prostatic epithelium. Prostate. 2013; 73(5): 476-488. doi: 10.1002/pros.22589. Epub 2012 Sep 19
77. Osmak M, Niksíc D, Brozović A, Ristov AA, Vrhovec I, Skrk J. Drug resistant tumor cells have increased levels of tumor markers for invasion and metastasis. Anticancer Res. 1999; 19(4B): 3193-3197.
78. Roger P, Montcourrier P, Maudelonde T, Brouillet JP, Pages A, Laffargue F, et al. Cathepsin D immunostaining in paraffin-embedded breast cancer cells and macrophages: Correlation with cytosolic assay. Hum Pathol. 1994; 25(9): 863-871. doi: 10.1016/0046-8177(94)90004-3
79. Kirana C, Shi H, Laing E, Hood K, Miller R, Bethwaite P, et al. Cathepsin D expression in colorectal cancer: From proteomic discovery through validation using Western blotting, immunohistochemistry, and tissue microarrays. Int J Proteomics. 2012; 2012: 245819. doi: 10.1155/2012/245819
80. Montcourrier P, Mangeat PH, Valembois C, Salazar G, Sahuquet A, Duperray C, et al. Characterization of very acidic phagosomes in breast cancer cells and their association with invasion. J Cell Sci. 1994; 107(Pt 9): 2381-2391.
Рецензия
Для цитирования:
Трухан И.С., Дремина Н.Н., Шурыгина И.А. Роль лизосом в онкогенезе: акцент на деградацию внеклеточного матрикса. Acta Biomedica Scientifica. 2020;5(6):77-87. https://doi.org/10.29413/ABS.2020-5.6.9
For citation:
Trukhan I.S., Dremina N.N., Shurygina I.A. The Role of Lysosomes in the Cancer Progression: Focus on the Extracellular Matrix Degradation. Acta Biomedica Scientifica. 2020;5(6):77-87. (In Russ.) https://doi.org/10.29413/ABS.2020-5.6.9
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