Acknowledgement
This study was supported by a research grant from Inha University.
References
- Zhang R (2016) The ANGPTL3-4-8 model, a molecular mechanism for triglyceride trafficking. Open Biol 6, 150272
- Aryal B, Price NL, Suarez Y and Fernandez-Hernando C (2019) ANGPTL4 in metabolic and cardiovascular disease. Trends Mol Med 25, 723-734 https://doi.org/10.1016/j.molmed.2019.05.010
- Ruscica M, Zimetti F, Adorni MP, Sirtori CR, Lupo MG and Ferri N (2020) Pharmacological aspects of ANGPTL3 and ANGPTL4 inhibitors: new therapeutic approaches for the treatment of atherogenic dyslipidemia. Pharmacol Res 153, 104653
- Sodhi A, Ma T, Menon D et al (2019) Angiopoietin-like 4 binds neuropilins and cooperates with VEGF to induce diabetic macular edema. J Clin Invest 129, 4593-4608 https://doi.org/10.1172/JCI120879
- Xin X, Rodrigues M, Umapathi M et al (2013) Hypoxic retinal Muller cells promote vascular permeability by HIF1-dependent up-regulation of angiopoietin-like 4. Proc Natl Acad Sci U S A 110, E3425-3434
- Tan MJ, Teo Z, Sng MK, Zhu P and Tan NS (2012) Emerging roles of angiopoietin-like 4 in human cancer. Mol Cancer Res 10, 677-688 https://doi.org/10.1158/1541-7786.MCR-11-0519
- Zhang T, Kastrenopoulou A, Larrouture Q, Athanasou NA and Knowles HJ (2018) Angiopoietin-like 4 promotes osteosarcoma cell proliferation and migration and stimulates osteoclastogenesis. BMC Cancer 18, 536
- Nakayama T, Hirakawa H, Shibata K et al (2011) Expression of angiopoietin-like 4 (ANGPTL4) in human colorectal cancer; ANGPTL4 promotes venous invasion and distant metastasis. Oncol Rep 25, 929-935 https://doi.org/10.3892/or.2011.1176
- Nakayama T, Hirakawa H, Shibata K, Abe K, Nagayasu T and Taguchi T (2010) Expression of angiopoietin-like 4 in human gastric cancer: ANGPTL4 promotes venous invasion. Oncol Rep 24, 599-606 https://doi.org/10.3892/or_00000897
- Padua D, Zhang XHF, Wang Q et al (2008) TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin- like 4. Cell 133, 66-77 https://doi.org/10.1016/j.cell.2008.01.046
- Visser KE and Joyce JA (2023) The evolving tumor microenvironment: from cancer initiation to metastatic outgrowth. Cancer Cell 41, 374-403 https://doi.org/10.1016/j.ccell.2023.02.016
- Hanahan D and Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674 https://doi.org/10.1016/j.cell.2011.02.013
- Chiodoni C, Colombo MP and Sangaletti S (2010) Matricellular proteins: from homeostasis to inflammation, cancer, and metastasis. Cancer Metastasis Rev 29, 295-307 https://doi.org/10.1007/s10555-010-9221-8
- Bornstein P (2009) Matricellular proteins: an overview. J Cell Commun Signal 3, 163-165 https://doi.org/10.1007/s12079-009-0069-z
- Xu S, Fang Y, Chang L et al (2023) STAT2-induced linc02231 promotes tumorigenesis and angiogenesis through modulation of hnRNPA1/ANGPTL4 in colorectal cancer. J Gene Med 25, e3506
- Zhu P, Tan MJ, Huang RL et al (2011) Angiopoietin-like 4 protein elevates the prosurvival intracellular O2(-):H2O2 ratio and confers anoikis resistance to tumors. Cancer Cell 19, 401-415 https://doi.org/10.1016/j.ccr.2011.01.018
- Izraely S, Ben-Menachem S, Sagi-Assif O et al (2017) ANGPTL4 promotes the progression of cutaneous melanoma to brain metastasis. Oncotarget 8, 75778-75796 https://doi.org/10.18632/oncotarget.19018
- Gordon ER, Wright CA, James M and Cooper SJ (2023) Transcriptomic and functional analysis of ANGPTL4 overexpression in pancreatic cancer nominates novel drug targets that reverse chemoresistance. BMC Cancer 23, 524
- Hui B, Ji H, Xu Y et al (2019) RREB1-induced upregulation of the lncRNA AGAP2-AS1 regulates the proliferation and migration of pancreatic cancer partly through suppressing ANKRD1 and ANGPTL4. Cell Death Dis 10, 207
- Conway GD, Buzza MS, Martin EW et al (2019) PRSS21/testisin inhibits ovarian tumor metastasis and antagonizes proangiogenic angiopoietins ANG2 and ANGPTL4. J Mol Med (Berl) 97, 691-709 https://doi.org/10.1007/s00109-019-01763-3
- Fang Y, Li X, Cheng H, Zhang L and Hao J (2022) ANGPTL4 regulates lung adenocarcinoma pyroptosis and apoptosis via NLRP3\ASC\Caspase 8 signaling pathway to promote resistance to gefitinib. J Oncol 2022, 3623570
- Zhang Y, Liu X, Zeng L et al (2022) Exosomal protein angiopoietin-like 4 mediated radioresistance of lung cancer by inhibiting ferroptosis under hypoxic microenvironment. Br J Cancer 127, 1760-1772 https://doi.org/10.1038/s41416-022-01956-7
- Kolb R, Kluz P, Tan ZW et al (2019) Obesity-associated inflammation promotes angiogenesis and breast cancer via angiopoietin-like 4. Oncogene 38, 2351-2363 https://doi.org/10.1038/s41388-018-0592-6
- Avalle L, Raggi L, Monteleone E et al (2022) STAT3 induces breast cancer growth via ANGPTL4, MMP13 and STC1 secretion by cancer associated fibroblasts. Oncogene 41, 1456-1467 https://doi.org/10.1038/s41388-021-02172-y
- Xu J, Wu F, Zhu Y et al (2024) ANGPTL4 regulates ovarian cancer progression by activating the ERK1/2 pathway. Cancer Cell Int 24, 54
- Wen L, Zhang Y, Yang B, Han F, Ebadi AG and Toughani M (2020) Knockdown of angiopoietin-like protein 4 suppresses the development of colorectal cancer. Cell Mol Biol (Noisy-le-grand) 66, 117-124 https://doi.org/10.14715/cmb/2020.66.5.21
- Tsai YT, Wu AC, Yang WB et al (2019) ANGPTL4 Induces TMZ resistance of glioblastoma by promoting cancer stemness enrichment via the EGFR/AKT/4E-BP1 cascade. Int J Mol Sci 20, 5625
- Kirby MK, Ramaker RC, Gertz J et al (2016) RNA sequencing of pancreatic adenocarcinoma tumors yields novel expression patterns associated with long-term survival and reveals a role for ANGPTL4. Mol Oncol 10, 1169-1182 https://doi.org/10.1016/j.molonc.2016.05.004
- Argentiero A, De Summa S, Di Fonte R et al (2019) Gene expression comparison between the lymph node-positive and -negative reveals a peculiar immune microenvironment signature and a theranostic role for WNT targeting in pancreatic ductal adenocarcinoma: a pilot study. Cancers (Basel) 11, 942
- Yan HH, Jung KH, Lee JE et al (2021) ANGPTL4 accelerates KRAS(G12D)-induced acinar to ductal metaplasia and pancreatic carcinogenesis. Cancer Lett 519, 185-198 https://doi.org/10.1016/j.canlet.2021.07.036
- Hu Q, Chen S, Li Y et al (2023) ANGPTL4, a direct target of hsa-miR-133a-3p, accelerates lung adenocarcinoma lipid metabolism, proliferation and invasion. Aging 16, 8348-8360 https://doi.org/10.18632/aging.205313
- Kang YT, Li CT, Tang SC et al (2021) Nickel chloride regulates ANGPTL4 via the HIF-1alpha-mediated TET1 expression in lung cells. Toxicol Lett 352, 17-25 https://doi.org/10.1016/j.toxlet.2021.09.007
- Zhao J, Liu J, Wu N et al (2020) ANGPTL4 overexpression is associated with progression and poor prognosis in breast cancer. Oncol Lett 20, 2499-2505 https://doi.org/10.3892/ol.2020.11768
- Tanaka T, Imamura T, Irie A et al (2022) Association of high cellular expression and plasma concentration of angiopoietin-like 4 with tongue cancer lung metastasis and poor prognosis. Oncol Lett 24, 299
- Aung TM, Ciin MN, Silsirivanit A et al (2022) Serum angiopoietin-like protein 4: a potential prognostic biomarker for prediction of vascular invasion and lymph node metastasis in cholangiocarcinoma patients. Front Public Health 10, 836985
- Kamaludin Z, Siddig A, Yaacob NM, Lam AK and Rahman W (2022) Angiopoietin-like protein 4 and insulin-like growth factor-1 expression in invasive breast carcinoma in young women. Pathophysiology 29, 9-23 https://doi.org/10.3390/pathophysiology29010002
- Verine J, Lehmann-Che J, Soliman H et al (2010) Determination of angptl4 mRNA as a diagnostic marker of primary and metastatic clear cell renal-cell carcinoma. PLoS One 5, e10421
- Dong D, Jia L, Zhou Y, Ren L, Li J and Zhang J (2017) Serum level of ANGPTL4 as a potential biomarker in renal cell carcinoma. Urol Oncol 35, 279-285 https://doi.org/10.1016/j.urolonc.2016.12.017
- Zhang Y, Yang X, Liu S et al (2022) Comprehensive analysis of potential prognostic values of ANGPTLs in colorectal cancer. Genes (Basel) 13, 2215
- Nie D, Zheng Q, Liu L, Mao X and Li Z (2019) Upregulated of angiopoietin-like protein 4 predicts poor prognosis in cervical cancer. J Cancer 10, 1896-1901 https://doi.org/10.7150/jca.29916
- Wang FT, Li XP, Pan MS, Hassan M, Sun W and Fan YZ (2021) Identification of the prognostic value of elevated ANGPTL4 expression in gallbladder cancer-associated fibroblasts. Cancer Med 10, 6035-6047 https://doi.org/10.1002/cam4.4150
- Hata S, Nomura T, Iwasaki K et al (2017) Hypoxia-induced angiopoietin-like protein 4 as a clinical biomarker and treatment target for human prostate cancer. Oncol Rep 38, 120-128 https://doi.org/10.3892/or.2017.5669
- An Y, Wang Q, Sun F et al (2020) OSucs: an online prognostic biomarker analysis tool for uterine carcinosarcoma. Genes (Basel) 11, 1040
- Seyfrien TN and Huysentruyt LC (2013) On the origin of cancer metastasis. Crit Rev Oncog 18, 43-73 https://doi.org/10.1615/CritRevOncog.v18.i1-2.40
- Potente M, Gerhardt H and Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887 https://doi.org/10.1016/j.cell.2011.08.039
- Gealekman O, Burkart A, Nicoloro SM, Staraubhaar J and Corvera S (2008) Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am J Physiol Endocrinol Metab 295, E1056-E1064 https://doi.org/10.1152/ajpendo.90345.2008
- Li YK, Gao AB, Zeng T et al (2014) ANGPTL4 accelerates ovarian serous cystadenocarcinoma carcinogenesis and angiogenesis in the tumor microenvironment by activating the JAK2/STAT3 pathway and interacting with ESM1. BMB Rep 47, 512-517
- Huang RL, Teo Z, Chong HC et al (2011) ANGPTL4 modulates vascular junction integrity by integrin signaling and disruption of intercellular VE-cadherin and claudin-5 clusters. Blood 118, 3990-4002 https://doi.org/10.1182/blood-2011-01-328716
- Kim SH, Park YY, Kim SW, Lee JS, Wang D and DuBois RN (2011) ANGPTL4 induction by prostaglandin E2 under hypoxic conditions promotes colorectal cancer progression. Cancer Res 17, 7010-7020 https://doi.org/10.1158/0008-5472.CAN-11-1262
- Gong X, Hou Z, Endsley MP et al (2019) Interaction of tumor cells and astrocytes promotes breast cancer brain metastases through TGF-β2/ANGPTL4 axes. NPJ Precis Oncol 3, 24
- Zhu X, Guo X, Wu S and Wei L (2016) ANGPTL4 Correlates with NSCLC progression and regulates epithelial-mesenchymal transition via ERK pathway. Lung 194, 637-646 https://doi.org/10.1007/s00408-016-9895-y
- Shen CJ, Chan SH, Lee CT, Huang WC, Tsai JP and Chen BK (2017) Oleic acid-induced ANGPTL4 enhances head and neck squamous cell carcinoma anoikis resistance and metastasis via up-regulation of fibronectin. Cancer Lett 386, 110-122 https://doi.org/10.1016/j.canlet.2016.11.012
- Lei X, Shi F, Basu D et al (2011) Proteolytic processing of angiopoietin-like protein 4 by proprotein convertases modulates its inhibitory effects on lipoprotein lipase activity. J Biol Chem 286, 15747-15756 https://doi.org/10.1074/jbc.M110.217638
- Hubers C, Pari AAA, Grieshober D et al (2023) Primary tumor-derived systemic nANGPTL4 inhibits metastasis. J Exp Med 220, e20202595
- Neophytou CM, Panagi M, Stylianopoulos T and Papageorgis P (2021) The role of tumor microenvironment in cancer metastasis: molecular mechanisms and therapeutic opportunities. Cancers (Basel) 13, 2053
- Bajwa P, Kordylewicz K, Bilecz A et al (2023) Cancer-associated mesothelial cell-derived ANGPTL4 and STC1 promote the early steps of ovarian cancer metastasis. JCI Insight 8, e163019
- Zhou S, Tu J, Ding S et al (2020) High expression of angiopoietin-like protein 4 in advanced colorectal cancer and its association with regulatory T cells and M2 macrophages. Pathol Oncol Res 26, 1269-1278 https://doi.org/10.1007/s12253-019-00695-0
- Ding S, Lin Z, Zhang X et al (2023) Deficiency of angiopoietin-like 4 enhances CD8+ T cell bioactivity via metabolic reprogramming for impairing tumour progression. Immunology 170, 28-46 https://doi.org/10.1111/imm.13650
- Theocharis AD, Skandalis SS, Gialeli C and Karamanos NK (2016) Extracellular matrix structure. Advanced Drug Delivery Reviews 97, 4-27 https://doi.org/10.1016/j.addr.2015.11.001
- Jablonska-Trypuc A, Matejczyk M and Rosochacki S (2016) Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. J Enzyme Inhib Med Chem 31, 177-183 https://doi.org/10.3109/14756366.2016.1161620
- Winkler J, Ogunniyan AA, Metcalf KJ and Werb Z (2020) Concepts of extracellular matrix remodelling in tumour progression and metastasis. Nat Commun 11, 5120
- Luo L, Yang JX, Luo T, Liu D, Wu GH and He JM (2021) A study on the mechanism of PP2A in the recovery of SCI in rats through downregulation of MMP-9 via MAPK signaling pathway. Eur Rev Med Pharmacol Sci 25, 7195-7203
- Liao YH, Chiang KH, Huang CR et al (2017) Epidermal growth factor-induced ANGPTL4 enhances anoikis resistance and tumour metastasis in head and neck squamous cell carcinoma. Oncogene 36, 2228-2248 https://doi.org/10.1038/onc.2016.371
- Shen CJ, Chang KY, Lin BW et al (2020) Oleic acid-induced NOX4 is dependent on ANGPTL4 expression to promote human colorectal cancer metastasis. Theranostics 10, 7083-7099 https://doi.org/10.7150/thno.44744
- Karaman S and Detmer M (2014) Mechanisms of lymphatic metastasis. J Clin Invest 124, 922-928 https://doi.org/10.1172/JCI71606
- Huang Z, Xie J, Lin S et al (2016) The downregulation of ANGPTL4 inhibits the migration and proliferation of tongue squamous cell carcinoma. Arch Oral Biol 71, 144-149 https://doi.org/10.1016/j.archoralbio.2016.07.011
- Zhang F, Chen H and Luo D (2023) Lymphovascular or perineural invasion is associated with lymph node metastasis and survival outcomes in patients with gastric cancer. Cancer Med 12, 9401-9408 https://doi.org/10.1002/cam4.5701
- Chen SH, Zhang BY, Zhou B, Zhu CZ, Sun LQ and Feng YJ (2019) Perineural invasion of cancer: a complex crosstalk between cells and molecules in the perineural niche. Am J Cancer Res 9, 1-21
- Mizuno S, Seishima R, Yamasaki J et al (2022) Angiopoietin-like 4 promotes glucose metabolism by regulating glucose transporter expression in colorectal cancer. J cancer Res Clin Oncol 148, 1351-1361 https://doi.org/10.1007/s00432-022-03960-z
- Phan LM, Yeung SC and Lee MH (2014) Cancer metabolic reprogramming: importance, main features, and potentials for precise targeted anti-cancer therapies. Cancer Biol Med 11, 1-19
- Jang M, Kim SS and Lee J (2013) Cancer cell metabolism: implications for therapeutic targets. Exp Mol Med 45, e45
- Park JH, Pyun WY and Park HW (2020) Cancer metabolism: phenotype, signaling and therapeutic targets. Cells 9, 2308
- Ward PS and Thompson CB (2012) Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 21, 297-308 https://doi.org/10.1016/j.ccr.2012.02.014
- Pavlova NN and Thompson CB (2016) The emerging hallmarks of cancer metabolism. Cell Metab 23, 27-47 https://doi.org/10.1016/j.cmet.2015.12.006
- Dijk W and Kersten S (2014) Regulation of lipoprotein lipase by angptl4. Trends Endocrinol Metab 25, 146-155 https://doi.org/10.1016/j.tem.2013.12.005
- Koster A, Chao YB, Mosior M et al (2005) Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology 146, 4943-4950 https://doi.org/10.1210/en.2005-0476
- Dijk W, Beigneux AP, Larsson M, Bensadoun A, Young SG and Kersten S (2016) Angiopoietin-like 4 promotes intracellular degradation of lipoprotein lipase in adipocytes. J Lipid Res 57, 1670-1683 https://doi.org/10.1194/jlr.M067363
- Chong HC, Chan JS, Goh CQ et al (2014) Angiopoietin-like 4 stimulates stat3-mediated iNOS expression and enhances angiogenesis to accelerate wound healing in diabetic mice. Mol Ther 22, 1593-1604 https://doi.org/10.1038/mt.2014.102
- Korecka A, de Wouters T, Cultrone A et al (2013) Angptl4 expression induced by butyrate and rosiglitazone in human intestinal epithelial cells utilizes independent pathways. Am J Physiol Gastrointest Liver Physiol 304, G1025-1037 https://doi.org/10.1152/ajpgi.00293.2012
- Mizuno S, Seishima R, Yamasaki J et al (2022) Angiopoietin-like 4 promotes glucose metabolism by regulating glucose transporter expression in colorectal cancer. J Cancer Res Clin Oncol 148, 1351-1361 https://doi.org/10.1007/s00432-022-03960-z
- Zheng X, Liu R, Zhou C et al (2021) Angptl4-mediated promotion of glycolysis facilitates the colonization of fusobacterium nucleatum in colorectal cancer. Cancer Res 81, 6157-6170 https://doi.org/10.1158/0008-5472.CAN-21-2273
- Zhu C, Teng L, Lai Y et al (2024) Adipose-derived stem cells promote glycolysis and peritoneal metastasis via tgf-β1/smad3/angptl4 axis in colorectal cancer. Cell Mol Life Sci 81, 189
- Xiao S, Nai-Dong W, Jin-Xiang Y et al (2022) Angptl4 regulate glutamine metabolism and fatty acid oxidation in nonsmall cell lung cancer cells. J Cell Mol Med 26, 1876-1885 https://doi.org/10.1111/jcmm.16879
- Cai Z, Li Y, Ma M et al (2023) Adipocytes promote pancreatic cancer migration and invasion through fatty acid metabolic reprogramming. Oncol Rep 50, 141
- Blucher C, Iberl S, Schwagarus N et al (2020) Secreted factors from adipose tissue reprogram tumor lipid metabolism and induce motility by modulating pparα/angptl4 and FAK. Mol Cancer Res 18, 1849-1862 https://doi.org/10.1158/1541-7786.MCR-19-1223
- Lin S, Miao Y, Zheng X et al (2022) Angptl4 negatively regulates the progression of osteosarcoma by remodeling branched-chain amino acid metabolism. Cell Death Discov 8, 225
- Le Jan S, Amy C, Cazes A et al (2003) Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol 162, 1521-1528 https://doi.org/10.1016/S0002-9440(10)64285-X