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Review Article

The route of autophagy regulation by osteopontin: a review on the linking mechanisms

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Pages 102-108 | Received 02 May 2023, Accepted 15 Nov 2023, Published online: 11 Dec 2023

References

  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147(4):728–741. doi: 10.1016/j.cell.2011.10.026.
  • Martinet W, Agostinis P, Vanhoecke B, et al. Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci. 2009;116(9):697–712. doi: 10.1042/CS20080508.
  • Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. nature. 2008;451(7182):1069–1075. doi: 10.1038/nature06639.
  • Galluzzi L, Pietrocola F, Bravo‐San Pedro JM, et al. Autophagy in malignant transformation and cancer progression. Embo J. 2015;34(7):856–880. doi: 10.15252/embj.201490784.
  • Ktistakis NT, Tooze SA. Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 2016;26(8):624–635. doi: 10.1016/j.tcb.2016.03.006.
  • Amaravadi R, Kimmelman AC, White E. Recent insights into the function of autophagy in cancer. Genes Dev. 2016;30(17):1913–1930. doi: 10.1101/gad.287524.116.
  • Neill T, Schaefer L, Iozzo RV. Instructive roles of extracellular matrix on autophagy. Am J Pathol. 2014;184(8):2146–2153. doi: 10.1016/j.ajpath.2014.05.010.
  • Huveneers S, Danen EH. Adhesion signaling–crosstalk between integrins, SRC and rho. J Cell Sci. 2009;122(Pt 8):1059–1069. doi: 10.1242/jcs.039446.
  • Kawano S, Torisu T, Esaki M, et al. Autophagy promotes degradation of internalized collagen and regulates distribution of focal adhesions to suppress cell adhesion. Biol Open. 2017;6(11):1644–1653. doi: 10.1242/bio.027458.
  • Ailane S, Long P, Jenner P, et al. Expression of integrin and CD 44 receptors recognising osteopontin in the normal and LPS‐lesioned rat substantia nigra. Eur J Neurosci. 2013;38(3):2468–2476. doi: 10.1111/ejn.12231.
  • Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132(1):27–42. doi: 10.1016/j.cell.2007.12.018.
  • Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13(2):132–141. doi: 10.1038/ncb2152.
  • Maiuri MC, Criollo A, Kroemer G. Crosstalk between apoptosis and autophagy within the beclin 1 interactome. Embo J. 2010;29(3):515–516. doi: 10.1038/emboj.2009.377.
  • Mochida K, Oikawa Y, Kimura Y, et al. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015;522(7556):359–362. doi: 10.1038/nature14506.
  • Carlsson SR, Simonsen A. Membrane dynamics in autophagosome biogenesis. J Cell Sci. 2015;128(2):193–205. doi: 10.1242/jcs.141036.
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19(21):5720–5728. doi: 10.1093/emboj/19.21.5720.
  • Stolz A, Ernst A, Dikic I. Cargo recognition and trafficking in selective autophagy. Nat Cell Biol. 2014;16(6):495–501. doi: 10.1038/ncb2979.
  • Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014;127(Pt 1):3–9. doi: 10.1242/jcs.140426.
  • Freeman SA, Grinstein S. Resolution of macropinosomes, phagosomes and autolysosomes: osmotically driven shrinkage enables tubulation and vesiculation. Traffic. 2018;19(12):965–974. doi: 10.1111/tra.12614.
  • Russell RC, Yuan H-X, Guan K-L. Autophagy regulation by nutrient signaling. Cell Res. 2014;24(1):42–57. doi: 10.1038/cr.2013.166.
  • Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol. 2010;12(9):823–830. doi: 10.1038/ncb0910-823.
  • He L, Zhang J, Zhao J, et al. Autophagy: the last defense against cellular nutritional stress. Adv Nutr. 2018;9(4):493–504. doi: 10.1093/advances/nmy011.
  • Galluzzi L, Vicencio JM, Kepp O, et al. To die or not to die: that is the autophagic question. Curr Mol Med. 2008;8(2):78–91. doi: 10.2174/156652408783769616.
  • Hippert MM, O'Toole PS, Thorburn A. Autophagy in cancer: good, bad, or both? Cancer Res. 2006;66(19):9349–9351. doi: 10.1158/0008-5472.CAN-06-1597.
  • Qu X, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003;112(12):1809–1820. doi: 10.1172/JCI20039.
  • Shen Y, Li D-D, Wang L-L, et al. Decreased expression of autophagy-related proteins in malignant epithelial ovarian cancer. Autophagy. 2008;4(8):1067–1068. doi: 10.4161/auto.6827.
  • Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402(6762):672–676. doi: 10.1038/45257.
  • Salminen A, Kaarniranta K, Kauppinen A. Beclin 1 interactome controls the crosstalk between apoptosis, autophagy and inflammasome activation: impact on the aging process. Ageing Res Rev. 2013;12(2):520–534. doi: 10.1016/j.arr.2012.11.004.
  • Hesari Z, Nourbakhsh M, Hosseinkhani S, et al. Down-regulation of NAMPT expression by mir-206 reduces cell survival of breast cancer cells. Gene. 2018;673:149–158. doi: 10.1016/j.gene.2018.06.021.
  • Ghorbanhosseini SS, Nourbakhsh M, Zangooei M, et al. MicroRNA-494 induces breast cancer cell apoptosis and reduces cell viability by inhibition of nicotinamide phosphoribosyltransferase expression and activity. EXCLI Journal. 2019;18:838.
  • Yousefi Z, Nourbakhsh M, Abdolvahabi Z, et al. microRNA-141 is associated with hepatic steatosis by downregulating the sirtuin1/AMP-activated protein kinase pathway in hepatocytes. J Cell Physiol. 2020;235(2):880–890. doi: 10.1002/jcp.29002.
  • White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 2009;15(17):5308–5316. doi: 10.1158/1078-0432.CCR-07-5023.
  • Degenhardt K, Mathew R, Beaudoin B, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell. 2006;10(1):51–64. doi: 10.1016/j.ccr.2006.06.001.
  • Eskelinen E-L. The dual role of autophagy in cancer. Curr Opin Pharmacol. 2011;11(4):294–300. doi: 10.1016/j.coph.2011.03.009.
  • Franzén A, Heinegård D. Isolation and characterization of two sialoproteins present only in bone calcified matrix. Biochem J. 1985;232(3):715–724. doi: 10.1042/bj2320715.
  • Kaleta B, Krata N, Zagożdżon R, et al. Osteopontin gene polymorphism and urinary OPN excretion in patients with immunoglobulin a nephropathy. Cells. 2019;8(6):524. doi: 10.3390/cells8060524.
  • Cho H-J, Cho H-J, Kim H-S. Osteopontin: a multifunctional protein at the crossroads of inflammation, atherosclerosis, and vascular calcification. Curr Atheroscler Rep. 2009;11(3):206–213. doi: 10.1007/s11883-009-0032-8.
  • Wang KX, Denhardt DT. Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 2008;19(5-6):333–345. doi: 10.1016/j.cytogfr.2008.08.001.
  • Denhardt DT, Noda M. Osteopontin expression and function: role in bone remodeling. J Cell Biochem. 1998;72(S30-31):92–102. doi: 10.1002/(SICI)1097-4644(1998)72:30/31+<92::AID-JCB13>3.0.CO;2-A.
  • Singhal H, Bautista DS, Tonkin KS, et al. Elevated plasma osteopontin in metastatic breast cancer associated with increased tumor burden and decreased survival. Clin Cancer Res. 1997;3(4):605–611.
  • Fedarko NS, Jain A, Karadag A, et al. Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin Cancer Res. 2001;7(12):4060–4066.
  • Hotte SJ, Winquist EW, Stitt L, et al. Plasma osteopontin: associations with survival and metastasis to bone in men with hormone‐refractory prostate carcinoma. Cancer. 2002;95(3):506–512. doi: 10.1002/cncr.10709.
  • Denhardt DT, Guo X. Osteopontin: a protein with diverse functions. FASEB J. 1993;7(15):1475–1482. doi: 10.1096/fasebj.7.15.8262332.
  • Kumar V, Behera R, Lohite K, et al. p38 kinase is crucial for osteopontin-induced furin expression that supports cervical cancer progression. Cancer Res. 2010;70(24):10381–10391. doi: 10.1158/0008-5472.CAN-10-1470.
  • Christensen B, Kläning E, Nielsen MS, et al. C-terminal modification of osteopontin inhibits interaction with the αVβ3-integrin. J Biol Chem. 2012;287(6):3788–3797. doi: 10.1074/jbc.M111.277996.
  • Rittling SR. Osteopontin in macrophage function. Expert Rev Mol Med. 2011;13:e15. doi: 10.1017/S1462399411001839.
  • Yokosaki Y, Tanaka K, Higashikawa F, et al. Distinct structural requirements for binding of the integrins αvβ6, αvβ3, αvβ5, α5β1 and α9β1 to osteopontin. Matrix Biol. 2005;24(6):418–427. doi: 10.1016/j.matbio.2005.05.005.
  • Ito K, Kon S, Nakayama Y, et al. The differential amino acid requirement within osteopontin in α4 and α9 integrin-mediated cell binding and migration. Matrix Biol. 2009;28(1):11–19. doi: 10.1016/j.matbio.2008.10.002.
  • Lund SA, Wilson CL, Raines EW, et al. Osteopontin mediates macrophage chemotaxis via α4 and α9 integrins and survival via the α4 integrin. J Cell Biochem. 2013;114(5):1194–1202. doi: 10.1002/jcb.24462.
  • Beausoleil MS, Schulze EB, Goodale D, et al. Deletion of the thrombin cleavage domain of osteopontin mediates breast cancer cell adhesion, proteolytic activity, tumorgenicity, and metastasis. BMC Cancer. 2011;11(1):25. doi: 10.1186/1471-2407-11-25.
  • Štemberger C, Matušan-Ilijaš K, Avirović M, et al. Osteopontin is associated with decreased apoptosis and αv integrin expression in lung adenocarcinoma. Acta Histochem. 2014;116(1):222–229. doi: 10.1016/j.acthis.2013.07.009.
  • Zhang H, Guo M, Chen JH, et al. Osteopontin knockdown inhibits αv,β3 integrin-induced cell migration and invasion and promotes apoptosis of breast cancer cells by inducing autophagy and inactivating the PI3K/akt/mTOR pathway. Cell Physiol Biochem. 2014;33(4):991–1002. doi: 10.1159/000358670.
  • Kocalkova M, Dombrowski F, Vom Dahl S, et al. Involvement of integrins in osmosensing and signaling toward autophagic proteolysis in rat liver. J Biol Chem. 2003;278(29):27088–27095. doi: 10.1074/jbc.M210699200.
  • Ma Y, Li M, Si J, et al. Blockade of Notch3 inhibits the stem-like property and is associated with ALDH1A1 and CD44 via autophagy in non-small lung cancer. Int J Oncol. 2016;48(6):2349–2358. doi: 10.3892/ijo.2016.3464.
  • Wang RC, Wei Y, An Z, et al. Akt-mediated regulation of autophagy and tumorigenesis through beclin 1 phosphorylation. Science. 2012;338(6109):956–959. doi: 10.1126/science.1225967.
  • Luo D-H, Chen Q-Y, Liu H, et al. The independent, unfavorable prognostic factors endothelin a receptor and chemokine receptor 4 have a close relationship in promoting the motility of nasopharyngeal carcinoma cells via the activation of AKT and MAPK pathways. J Transl Med. 2013;11(1):203. doi: 10.1186/1479-5876-11-203.
  • Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the drosophila fat body. Dev Cell. 2004;7(2):167–178. doi: 10.1016/j.devcel.2004.07.009.
  • Torii S, Yoshida T, Arakawa S, et al. Identification of PPM1D as an essential Ulk1 phosphatase for genotoxic stress‐induced autophagy. EMBO Rep. 2016;17(11):1552–1564. doi: 10.15252/embr.201642565.
  • Itakura E, Kishi C, Inoue K, et al. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell. 2008;19(12):5360–5372. doi: 10.1091/mbc.e08-01-0080.
  • Grunt TW, Mariani GL. Novel approaches for molecular targeted therapy of breast cancer: interfering with PI3K/AKT/mTOR signaling. Curr Cancer Drug Targets. 2013;13(2):188–204.
  • Vara JÁF, Casado E, de Castro J, et al. PI3K/akt signalling pathway and cancer. Cancer Treat Rev. 2004;30(2):193–204. doi: 10.1016/j.ctrv.2003.07.007.
  • Zheng YH, Tian C, Meng Y, et al. Osteopontin stimulates autophagy via integrin/CD44 and p38 MAPK signaling pathways in vascular smooth muscle cells. J Cell Physiol. 2012;227(1):127–135. doi: 10.1002/jcp.22709.
  • Denhardt DT, Noda M, O'Regan AW, et al. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest. 2001;107(9):1055–1061. doi: 10.1172/jci12980.
  • Bellahcène A, Castronovo V, Ogbureke KU, et al. Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer. 2008;8(3):212–226. doi: 10.1038/nrc2345.
  • Behera R, Kumar V, Lohite K, et al. Activation of JAK2/STAT3 signaling by osteopontin promotes tumor growth in human breast cancer cells. Carcinogenesis. 2010;31(2):192–200. doi: 10.1093/carcin/bgp289.
  • Zhang R, Pan X, Huang Z, et al. Osteopontin enhances the expression and activity of MMP-2 via the SDF-1/CXCR4 axis in hepatocellular carcinoma cell lines. PLOS One. 2011;6(8):e23831. doi: 10.1371/journal.pone.0023831.
  • Lin Y-H, Yang-Yen H-F. The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/akt signaling pathway. J Biol Chem. 2001;276(49):46024–46030. doi: 10.1074/jbc.M105132200.
  • Hao C, Lane J, Jiang WG. Osteopontin and cancer: insights into its role in drug resistance. Biomedicines. 2023;11(1):197. doi: 10.3390/biomedicines11010197.
  • Yang MC, Wang HC, Hou YC, et al. Blockade of autophagy reduces pancreatic cancer stem cell activity and potentiates the tumoricidal effect of gemcitabine. Mol Cancer. 2015;14(1):179. doi: 10.1186/s12943-015-0449-3.
  • Liu G, Fan X, Tang M, et al. Osteopontin induces autophagy to promote chemo-resistance in human hepatocellular carcinoma cells. Cancer Lett. 2016;383(2):171–182. doi: 10.1016/j.canlet.2016.09.033.
  • Liao H, Zou Z, Liu W, et al. Osteopontin-integrin signaling positively regulates neuroplasticity through enhancing neural autophagy in the peri-infarct area after ischemic stroke. Am J Transl Res. 2022;14(11):7726–7743.
  • Sun C, Enkhjargal B, Reis C, et al. Osteopontin-enhanced autophagy attenuates early brain injury via FAK-ERK pathway and improves Long-Term outcome after subarachnoid hemorrhage in rats. Cells. 2019;8(9):980. doi: 10.3390/cells8090980.
  • Bai RJ, Liu D, Li YS, et al. OPN inhibits autophagy through CD44, integrin and the MAPK pathway in osteoarthritic chondrocytes. Front Endocrinol. 2022;13:919366. doi: 10.3389/fendo.2022.919366.
  • Tang M, Jiang Y, Jia H, et al. Osteopontin acts as a negative regulator of autophagy accelerating lipid accumulation during the development of nonalcoholic fatty liver disease. Artif Cells Nanomed Biotechnol. 2020;48(1):159–168. doi: 10.1080/21691401.2019.1699822.
  • Huang RH, Quan YJ, Chen JH, et al. Osteopontin promotes cell migration and invasion, and inhibits apoptosis and autophagy in colorectal cancer by activating the p38 MAPK signaling pathway. Cell Physiol Biochem. 2017;41(5):1851–1864. doi: 10.1159/000471933.
  • Chang SH, Minai-Tehrani A, Shin JY, et al. Beclin1-induced autophagy abrogates radioresistance of lung cancer cells by suppressing osteopontin. J Radiat Res. 2012;53(3):422–432. doi: 10.1269/jrr.11148.
  • Ge D, Jing Q, Meng N, et al. Regulation of apoptosis and autophagy by sphingosylphosphorylcholine in vascular endothelial cells. J Cell Physiol. 2011;226(11):2827–2833. doi: 10.1002/jcp.22632.
  • Decker JJ, Norby FL, Rooney MR, et al. Metabolic syndrome and risk of ischemic stroke in atrial fibrillation: ARIC study. Stroke. 2019;50(11):3045–3050. doi: 10.1161/STROKEAHA.119.025376.
  • Lin R, Wu S, Zhu D, et al. Osteopontin induces atrial fibrosis by activating akt/GSK-3β/β-catenin pathway and suppressing autophagy. Life Sci. 2020;245:117328. doi: 10.1016/j.lfs.2020.117328.
  • Sun CM, Enkhjargal B, Reis C, et al. Osteopontin attenuates early brain injury through regulating autophagy‐apoptosis interaction after subarachnoid hemorrhage in rats. CNS Neurosci Ther. 2019;25(10):1162–1172. doi: 10.1111/cns.13199.
  • Courter D, Cao H, Kwok S, et al. The RGD domain of human osteopontin promotes tumor growth and metastasis through activation of survival pathways. PLOS One. 2010;5(3):e9633. doi: 10.1371/journal.pone.0009633.
  • Guan J-L. Role of focal adhesion kinase in integrin signaling. Int J Biochem Cell Biol. 1997;29(8–9):1085–1096. doi: 10.1016/s1357-2725(97)00051-4.

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