Abstract
Alzheimer’s disease (AD) is a paramount chronic neurodegenerative condition that has been affecting elderly people since the 1900s. It causes memory loss, disorientation, and poor mental function. AD is considered to be one of the most serious problems that dementia sufferers face. Despite extensive investigation, the pathological origin of Alzheimer’s disease remains a mystery. The amyloid cascade theory and the vascular hypothesis, which stresses the buildup of Aβ plaques, have dominated research into dementia and aging throughout history. However, research into this task failed to yield the long-awaited therapeutic miracle lead for Alzheimer’s disease. Perhaps a hypothetical fragility in the context of Alzheimer’s disease was regarded as a state distinct from aging in general, as suggested by the angiogenesis hypothesis, which suggests that old age is one state associated with upregulation of angiogenic growth factors, resulting in decreased microcirculation throughout the body. There has also been evidence that by controlling or inhibiting the components involved in the sequence of events that cause angiogenesis, there is a visible progression in AD patients. In Alzheimer’s disease, one such antiangiogenic drug is being used.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable
References
Abdollahi A (2004) Antiangiogenic signaling network induced by endostatin
Abdollahi A, Hahnfeldt P, Maercker C, Gröne HJ, Debus J, Ansorge W, Folkman J, Hlatky L, Huber PE (2004) Endostatin’s antiangiogenic signaling network. Mol Cell 13(5):649–663. https://doi.org/10.1016/s1097-2765(04)00102-9
Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE (2000) Inflammation and Alzheimer’s disease. Neurobiol Aging 21(3):383–421. https://doi.org/10.1016/s0197-4580(00)00124-x
Ambrose CT (2016) Angiogenesis, aging, and Alzheimer’s disease. Am Sci 104(2):82–85. https://doi.org/10.1511/2016.119.82
Bächinger HP (2005) Collagen: primer in structure, processing and assembly (Vol. 247). Springer Science & Business Media
Bayer TA, Wirths O, Majtényi K, Hartmann T, Multhaup G, Beyreuther K, Czech C (2001) Key factors in Alzheimer’s disease: β-amyloid precursor protein processing, metabolism and intraneuronal transport. Brain Pathol 11(1):1–11. https://doi.org/10.1111/j.1750-3639.2001.tb00376.x
Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood–brain barrier disorder in Alzheimer’s disease. Acta Neuropathol 118(1):103–113. https://doi.org/10.1007/s00401-009-0522-3
Beyreuther K, Bush AI, Dyrks T, Hilbich C, KöNIG GE, MöNNING UR, Multhaup G, Prior R, Rumble B, Schubert W, Small DH (1991) Mechanisms of amyloid deposition in Alzheimer’s disease. Ann N Y Acad Sci 640(1):129–139. https://doi.org/10.1111/j.1749-6632.1991.tb00204.x
Blackhall FH, Merry CL, Lyon M, Jayson GC, Folkman J, Javaherian K, Gallagher JT (2003) Binding of endostatin to endothelial heparan sulphate shows a differential requirement for specific sulphates. Biochem J 375(1):131–139. https://doi.org/10.1042/bj20030730
Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med 343(7):450–456. https://doi.org/10.1056/nejm200008173430701
Boscolo E, Folin M, Nico B, Grandi C, Mangieri D, Longo V, Scienza R, Zampieri P, Conconi MT, Parnigotto PP, Ribatti D (2007) β amyloid angiogenic activity in vitro and in vivo. Int J Mol Med 19(4):581–587. https://doi.org/10.3892/ijmm.19.4.581
Brkic M, Balusu S, Libert C, Vandenbroucke RE (2015) Friends or foes: matrix metalloproteinases and their multifaceted roles in neurodegenerative diseases. Mediat Inflamm 11:2015–2027. https://doi.org/10.1155/2015/620581
Chakraborty A, Kamermans A, van Het Hof B, Castricum K, Aanhane E, van Horssen J, Thijssen VL, Scheltens P, Teunissen CE, Fontijn RD, van der Flier WM (2018) Angiopoietin like-4 as a novel vascular mediator in capillary cerebral amyloid angiopathy. Brain. 141(12):3377–3388. https://doi.org/10.1093/brain/awy274
Chang R, Yee KL, Sumbria RK (2017) Tumor necrosis factor α inhibition for Alzheimer’s disease. J Cent Nerv Syst Dis 9:1179573517709278. https://doi.org/10.1177/1179573517709278
Chen M, Bao L, Zhao M, Cao J, Zheng H (2020) Progress in research on the role of FGF in the formation and treatment of corneal neovascularization. Front Pharmacol 11. https://doi.org/10.3389/fphar.2020.00111
Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22(4):201–207. https://doi.org/10.1016/s0165-6147(00)01676-x
Damian AM, Jacobson SA, Hentz JG, Belden CM, Shill HA, Sabbagh MN, Caviness JN, Adler CH (2011) The Montreal Cognitive Assessment and the mini-mental state examination as screening instruments for cognitive impairment: item analyses and threshold scores. Dement Geriatr Cogn Disord 31(2):126–131. https://doi.org/10.1159/000323867
De Jong GI, De Vos RA, Steur EJ, Luiten PG (1997) Cerebrovascular hypoperfusion: a risk factor for Alzheimer’s disease? Animal model and postmortem human studies. Ann N Y Acad Sci 826(1):56–74. https://doi.org/10.1111/j.1749-6632.1997.tb48461.x
Deininger MH, Fimmen BA, Thal DR, Schluesener HJ, Meyermann R (2002) Aberrant neuronal and paracellular deposition of endostatin in brains of patients with Alzheimer’s disease. J Neurosci 22(24):10621–10626. https://doi.org/10.1523/jneurosci.22-24-10621.2002
Del Bo R, Ghezzi S, Scarpini E, Bresolin N, Comi GP (2009) VEGF genetic variability is associated with increased risk of developing Alzheimer’s disease. J Neurol Sci 283(1-2):66–68. https://doi.org/10.1016/j.jns.2009.02.318
Desai BS, Schneider JA, Li JL, Carvey PM, Hendey B (2009) Evidence of angiogenic vessels in Alzheimer’s disease. J Neural Transm 116(5):587–597. https://doi.org/10.1007/s00702-009-0226-9
Dhanabal M, Ramchandran R, Volk R, Stillman IE, Lombardo M, Iruela-Arispe ML, Simons M, Sukhatme VP (1999a) Endostatin: yeast production, mutants, and antitumor effect in renal cell carcinoma. Cancer Res 59(1):189–197. https://doi.org/10.1006/bbrc.1999.0595
Dhanabal M, Ramchandran R, Waterman MJ, Lu H, Knebelmann B, Segal M, Sukhatme VP (1999b) Endostatin induces endothelial cell apoptosis. J Biol Chem 274(17):11721–11726. https://doi.org/10.1074/jbc.274.17.11721
Dickstein DL, Biron KE, Ujiie M, Pfeifer CG, Jeffries AR, Jefferies WA (2006) Aβ peptide immunization restores blood-brain barrier integrity in Alzheimer disease. FASEB J 20(3):426–433. https://doi.org/10.1096/fj.05-3956com
Dickstein DL, Walsh J, Brautigam H, Stockton SD Jr, Gandy S, Hof PR (2010) Role of vascular risk factors and vascular dysfunction in Alzheimer’s disease. 77(1):82–102. https://doi.org/10.1002/msj.20155
Digtyar AV, Pozdnyakova NV, Feldman NB, Lutsenko SV, Severin SE (2007) Endostatin: current concepts about its biological role and mechanisms of action. Biochem Mosc 72(3):235–246. https://doi.org/10.1134/s0006297907030017
Ding YH, Javaherian K, Lo KM, Chopra R, Boehm T, Lanciotti J, Harris BA, Li Y, Shapiro R, Hohenester E, Timpl R (1998) Zinc-dependent dimers observed in crystals of human endostatin. Proc Natl Acad Sci 95(18):10443–10448. https://doi.org/10.1073/pnas.95.18.10443
Dixelius J, Larsson H, Sasaki T, Holmqvist K, Lu L, Engström A, Timpl R, Welsh M, Claesson-Welsh L (2000) Endostatin-induced tyrosine kinase signaling through the Shb adaptor protein regulates endothelial cell apoptosis. Blood: J Am Soc Hematol 95(11):3403–3411. https://doi.org/10.1182/blood.v95.11.3403.011k07_3403_3411
Dixelius J, Cross M, Matsumoto T, Sasaki T, Timpl R, Claesson-Welsh L (2002) Endostatin regulates endothelial cell adhesion and cytoskeletal organization. Cancer Res 62(7):1944–1947
Eriksson K, Magnusson P, Dixelius J, Claesson-Welsh L, Cross MJ (2003) Angiostatin and endostatin inhibit endothelial cell migration in response to FGF and VEGF without interfering with specific intracellular signal transduction pathways. FEBS Lett 536(1-3):19–24. https://doi.org/10.1016/s0014-5793(03)00003-6
Evans DA, Funkenstein HH, Albert MS, Scherr PA, Cook NR, Chown MJ, Hebert LE, Hennekens CH, Taylor JO (1989) Prevalence of Alzheimer’s disease in a community population of older persons: higher than previously reported. Jama 262(18):2551–2556. https://doi.org/10.1001/jama.1989.03430180093036
Fagiani E, Christofori G (2013) Angiopoietins in angiogenesis. Cancer Lett 328(1):18–26. https://doi.org/10.1016/j.canlet.2012.08.018
Faye C, Moreau C, Chautard E, Jetne R, Fukai N, Ruggiero F, Humphries MJ, Olsen BR, Ricard-Blum S (2009) Molecular interplay between endostatin, integrins, and heparan sulfate. J Biol Chem 284(33):22029–22040. https://doi.org/10.1074/jbc.m109.002840
Felbor U, Dreier L, Bryant RA, Ploegh HL, Olsen BR, Mothes W (2000) Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J 19(6):1187–1194. https://doi.org/10.1093/emboj/19.6.1187
Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77(7):527–543
Ferreras M, Felbor U, Lenhard T, Olsen BR, Delaissé JM (2000) Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett 486(3):247–251. https://doi.org/10.1016/s0014-5793(00)02249-3
Fiedler U, Augustin HG (2006) Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol 27(12):552–558. https://doi.org/10.1016/j.it.2006.10.004
Fillit H, Ding W, Buee L, Kalman J, Altstiel L, Lawlor B, Wolf-Klein G (1991) Elevated circulating tumor necrosis factor levels in Alzheimer’s disease. Neurosci Lett 129(2):318–320. https://doi.org/10.1016/0304-3940(91)90490-k
Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM (1998) Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 152(1):307–317
Gebbink MF, Voest EE, Reijerkerk A (2004) Do antiangiogenic protein fragments have amyloid properties? Blood 104(6):1601–1605. https://doi.org/10.1182/blood-2004-02-0433
Glabe CC (2005) Amyloid accumulation and pathogenesis of Alzheimer’s disease: significance of monomeric, oligomeric and fibrillar Aβ. In: Alzheimer’s Disease. Springer, Boston, pp 167–177. https://doi.org/10.1007/0-387-23226-5_8
Gordon MK, Hahn RA (2010) Collagens. Cell Tissue Res 339(1):247–257. https://doi.org/10.1007/s00441-009-0844-4
Goto Y, Takahashi N, Fink AL (1990) Mechanism of acid-induced folding of proteins. Biochemistry. 29(14):3480–3488. https://doi.org/10.1021/bi00466a009
Gupta-Bansal R, Frederickson RC, Brunden KR (1995) Proteoglycan-mediated inhibition of Aβ proteolysis. A potential cause of senile plaque accumulation. J Biol Chem 270(31):18666–18671. https://doi.org/10.1074/jbc.270.31.18666
Gurnik S, Devraj K, Macas J, Yamaji M, Starke J, Scholz A, Sommer K, Di Tacchio M, Vutukuri R, Beck H, Mittelbronn M (2016) Angiopoietin-2-induced blood–brain barrier compromise and increased stroke size are rescued by VE-PTP-dependent restoration of Tie2 signaling. Acta Neuropathol 131(5):753–773. https://doi.org/10.1007/s00401-016-1551-3
Hardy J, Duff K, Hardy KG, Perez-Tur J, Hutton M (1998) Genetic dissection of Alzheimer’s disease and related dementias: amyloid and its relationship to tau. Nat Neurosci 1(5):355–358. https://doi.org/10.1038/1565
He Y, Zhou H, Tang H, Luo Y (2006) Deficiency of disulfide bonds facilitating fibrillogenesis of endostatin. J Biol Chem 281(2):1048–1057. https://doi.org/10.1074/jbc.m507745200
Hohenester E, Sasaki T, Olsen BR, Timpl R (1998) Crystal structure of the angiogenesis inhibitor endostatin at 1.5 Å resolution. EMBO J 17(6):1656–1664. https://doi.org/10.2210/pdb1koe/pdb
Hohman TJ, Bell SP, Jefferson AL (2015) The role of vascular endothelial growth factor in neurodegeneration and cognitive decline: exploring interactions with biomarkers of Alzheimer disease. JAMA Neurol 72(5):520–529. https://doi.org/10.1001/jamaneurol.2014.4761
Holton JL, Ghiso J, Lashley T, Rostagno A, Guerin CJ, Gibb G, Houlden H, Ayling H, Martinian L, Anderton BH, Wood NW (2001) Regional distribution of amyloid-Bri deposition and its association with neurofibrillary degeneration in familial British dementia. Am J Pathol 158(2):515–526. https://doi.org/10.1016/s0002-9440(10)63993-4
Hu W, Xia LJ, Chen FH, Wu FR, Tang J, Chen CZ, Jiang S, Chen HH (2012) Recombinant human endostatin inhibits adjuvant arthritis by down-regulating VEGF expression and suppression of TNF-α, IL-1β production. Inflamm Res 61(8):827–835
Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci 5(5):347–360. https://doi.org/10.1038/nrn1387
Im E, Venkatakrishnan A, Kazlauskas A (2005) Cathepsin B regulates the intrinsic angiogenic threshold of endothelial cells. Mol Biol Cell 16(8):3488–3500. https://doi.org/10.1091/mbc.e04-11-1029
Isaacs-Trepanier C, Saleem M, Herrmann N, Swardfager W, Oh PI, Goldstein BI, Mitchell J, Sugamori KS, Lanctôt KL (2020) Endostatin as a mediator between endothelial function and cognitive performance in those at risk for vascular cognitive impairment. J Alzheimers Dis 76(2):601–611
Jellinger KA (2007) The enigma of vascular cognitive disorder and vascular dementia. Acta Neuropathol 113(4):349–388. https://doi.org/10.1007/s00401-006-0185-2
Kalaria RN (2002) Small vessel disease and Alzheimer’s dementia: pathological considerations. Cerebrovasc Dis 13(Suppl. 2):48–52. https://doi.org/10.1159/000049150
Kanai M, Matsubara E, Isoe K, Urakami K, Nakashima K, Arai H, Sasaki H, Abe K, Iwatsubo T, Kosaka T, Watanabe M (1998) Longitudinal study of cerebrospinal fluid levels of tau, Aβ1–40, and Aβ1–42 (43) in Alzheimer’s disease: a study in Japan. Ann Neurol: Off J Am Neurol Assoc Child Neurol Soc 44(1):17–26. https://doi.org/10.1002/ana.410440108
Karumanchi SA, Jha V, Ramchandran R, Karihaloo A, Tsiokas L, Chan B et al (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol Cell 7(4):811–822. https://doi.org/10.1016/s1097-2765(01)00225-8
Kasama T, Shiozawa F, Kobayashi K, Yajima N, Hanyuda M, Takeuchi HT, Mori Y, Negishi M, Ide H, Adachi M (2001) Vascular endothelial growth factor expression by activated synovial leukocytes in rheumatoid arthritis: critical involvement of the interaction with synovial fibroblasts. Arthritis Rheum 44(11):2512–2524. https://doi.org/10.1002/1529-0131(200111)44:11%3C2512::aid-art431%3E3.0.co;2-o
Katzman R (1993 Jan.) Education and the prevalence of dementia and Alzheimer’s disease. Neurology 43:13. https://doi.org/10.1212/wnl.43.1_part_1.13
Kawas CH, Brookmeyer R (2001) Aging and the public health effects of dementia. N Engl J Med 344(15):1160–1161
Kim YM, Jang JW, Lee OH, Yeon J, Choi EY, Kim KW, Lee ST, Kwon YG (2000) Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase 2. Cancer Res 60(19):5410–5413. https://doi.org/10.1016/j.atherosclerosis.2020.02.022
Kivipelto M, Helkala EL, Laakso MP, Hänninen T, Hallikainen M, Alhainen K, Soininen H, Tuomilehto J, Nissinen A (2001) Midlife vascular risk factors and Alzheimer’s disease in later life: longitudinal, population based study. Bmj 322(7300):1447–1451. https://doi.org/10.1212/wnl.56.12.1683
Klagsbrun M, Moses MA (1999) Molecular angiogenesis. Chem Biol 6(8):R217–R224. https://doi.org/10.1016/s1074-5521(99)80081-7
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47(260):583–621. https://doi.org/10.1080/01621459.1952.10483441
Lan HY, Mu W, Ng YY, Nikolic-Paterson DJ, Atkins RC (1996) A simple, reliable, and sensitive method for nonradioactive in situ hybridization: use of microwave heating to improve hybridization efficiency and preserve tissue morphology. J Histochem Cytochem 44(3):281–287. https://doi.org/10.1177/44.3.8648089
Lieu C, Heymach J, Overman M, Tran H, Kopetz S (2011) Beyond VEGF: inhibition of the fibroblast growth factor pathway and antiangiogenesis. Clin Cancer Res 17(19):6130–6139. https://doi.org/10.1158/1078-0432.ccr-11-0659
Lowe J, Mayer RJ, Landon M (1993) Ubiquitin in neurodegenerative diseases. Brain Pathol 3(1):55–65
Lukiw WJ, Carver LA, LeBlanc HJ, Bazan NG (2000) Analysis of 1184 gene transcript levels in Alzheimer CA1 hippocampus: synaptic signaling and transcription factor deficits and upregulation of pro-inflammatory pathways. Alzheimers Rep 3(3):161–167. https://doi.org/10.1016/s0197-4580(00)82895-x
Lyketsos CG, Steele C, Baker L, Galik E, Kopunek S, Steinberg M, Warren A (1997) Major and minor depression in Alzheimer’s disease: prevalence and impact. J Neuropsychiatry Clin Neurosci 9(4):556–561. https://doi.org/10.1176/jnp.9.4.556
Macpherson GR, Ng SS, Forbes SL, Melillo G, Karpova T, McNally J, Conrads TP, Veenstra TD, Martinez A, Cuttitta F, Price DK (2003) Anti-angiogenic activity of human endostatin is HIF-1-independent in vitro and sensitive to timing of treatment in a human saphenous vein assay. Mol Cancer Ther 2(9):845–854
Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 1:50–60. https://doi.org/10.1214/aoms/1177730491
Mendoza L, Valcárcel M, Carrascal T, Egilegor E, Salado C, Sim BK, Vidal-Vanaclocha F (2004) Inhibition of cytokine-induced microvascular arrest of tumor cells by recombinant endostatin prevents experimental hepatic melanoma metastasis. Cancer Res 64(1):304–310. https://doi.org/10.1158/0008-5472.can-03-1829
Messmer-Blust A, An X, Li J (2009) Hypoxia-regulated angiogenic inhibitors. Trends Cardiovasc Med 19(8):252–256. https://doi.org/10.1016/j.tcm.2010.02.006
Miners JS, Palmer JC, Love S (2016) Pathophysiology of hypoperfusion of the precuneus in early Alzheimer’s disease. Brain Pathol 26(4):533–541. https://doi.org/10.1111/bpa.12331
Miosge N, Sasaki T, Timpl R (1999) Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls. FASEB J 13(13):1743–1750. https://doi.org/10.1096/fasebj.13.13.1743
Moeller BJ, Cao Y, Li CY, Dewhirst MW (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5(5):429–441. https://doi.org/10.1016/s1535-6108(04)00115-1
Mohamed WA, Niyazy WH, Mahfouz AA (2011) Angiopoietin-1 and endostatin levels in cord plasma predict the development of bronchopulmonary dysplasia in preterm infants. J Trop Pediatr 57(5):385–388. https://doi.org/10.1093/tropej/fmq112
Moody DM, Brown WR, Challa VR, GHAZI-BIRRY HS, Reboussin DM (1997) Cerebral microvascular alterations in aging, leukoaraiosis, and Alzheimer’s disease. Ann N Y Acad Sci 826(1):103–116. https://doi.org/10.1111/j.1749-6632.1997.tb48464.x
Morisada T, Kubota Y, Urano T, Suda T, Oike Y (2006) Angiopoietins and angiopoietin-like proteins in angiogenesis. Endothelium. 13(2):71–79. https://doi.org/10.1080/10623320600697989
Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J (1999) Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E–deficient mice. Circulation. 99(13):1726–1732. https://doi.org/10.1161/01.cir.99.13.1726
Murakami M, Simons M (2008) Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol 15(3):215–220. https://doi.org/10.1097/moh.0b013e3282f97d98
Noda M, Takii K, Parajuli B, Kawanokuchi J, Sonobe Y, Takeuchi H, Mizuno T, Suzumura A (2014) FGF-2 released from degenerating neurons exerts microglial-induced neuroprotection via FGFR3-ERK signaling pathway. J Neuroinflammation 11(1):1–1. https://doi.org/10.1186/1742-2094-11-76
Oeckl P, Steinacker P, Feneberg E, Otto M (2016) Neurochemical biomarkers in the diagnosis of frontotemporal lobar degeneration: an update. J Neurochem 138:184–192. https://doi.org/10.1111/jnc.13669
Öhlund D, Ardnor B, Öman M, Naredi P, Sund M (2008) Expression pattern and circulating levels of endostatin in patients with pancreas cancer. Int J Cancer 122(12):2805–2810
Oikonomou KA, Kapsoritakis AN, Kapsoritaki AI, Manolakis AC, Tiaka EK, Tsiopoulos FD, Tsiompanidis IA, Potamianos SP (2011) Angiogenin, angiopoietin-1, angiopoietin-2, and endostatin serum levels in inflammatory bowel disease. Inflamm Bowel Dis 17(4):963–970. https://doi.org/10.1002/ibd.21410
Ol O (1994) Canadian study of health and aging: study methods and prevalence of dementia. Can Med Assoc J 150(6):899–913. https://doi.org/10.1017/s0714980800006334
O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88(2):277–285. https://doi.org/10.1016/s0092-8674(00)81848-6
Peng Z, Luo Y, Xiao ZY (2020) Angiopoietin-1 accelerates Alzheimer’s disease via FOXA2/PEN2/APP pathway in APP/PS1 mice. Life Sci 246:117430. https://doi.org/10.1016/j.lfs.2020.117430
Qian S, Li R, Zhang C, Zhang R, Guo D, Bu X, Wang A, Peng H, Chen J, Zhang Y, He J (2020) Plasma endostatin levels at acute phase of ischemic stroke Are associated with post-stroke cognitive impairment. Neurotox Res 8:1–9. https://doi.org/10.1007/s12640-020-00173-5
Quintero-Fabián S, Arreola R, Becerril-Villanueva E, Torres-Romero JC, Arana-Argáez VE, Lara-Riegos J, Ramírez-Camacho MA, Alvarez Sanchez ME (2019) Role of matrix metalloproteinases in angiogenesis and cancer. Front Oncol 9:1370. https://doi.org/10.3389/fonc.2019.01370
Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, Dillehay LE, Madan A, Semenza GL, Bedi A (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev 14(1):34–44
Rezvani HR, Ali N, Nissen LJ, Harfouche G, De Verneuil H, Taïeb A, Mazurier F (2011) HIF-1α in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non-cancer disorders. J Investig Dermatol 131(9):1793–1805. https://doi.org/10.1038/jid.2011.141
Ricard-Blum S, Féraud O, Lortat-Jacob H, Rencurosi A, Fukai N, Dkhissi F, Vittet D, Imberty A, Olsen BR, Van Der Rest M (2004) Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling Role of divalent cations. J Biol Chem 279(4):2927–2936. https://doi.org/10.1074/jbc.m309868200
Rogers MS, D'Amato RJ (2006) The effect of genetic diversity on angiogenesis. Exp Cell Res 312(5):561–574. https://doi.org/10.1016/j.yexcr.2005.10.021
Roses AD (1995) On the metabolism of apolipoprotein E and the Alzheimer diseases. Exp Neurol 132(2):149–156. https://doi.org/10.1016/0014-4886(95)90019-5
Salza R, Oudart JB, Ramont L, Maquart FX, Bakchine S, Thoannès H, Ricard-Blum S (2015) Endostatin level in cerebrospinal fluid of patients with Alzheimer’s disease. J Alzheimers Dis 44(4):1253–1261. https://doi.org/10.3233/jad-142544
Sasaki T, Larsson H, Kreuger J, Salmivirta M, Claesson-Welsh L, Lindahl U, Hohenester E, Timpl R (1999) Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J 18(22):6240–6248. https://doi.org/10.1093/emboj/18.22.6240
Sato Y (2017) Endostatin as a biomarker of basement membrane degradation. J Atheroscler Thromb 24(10):1014–1015. https://doi.org/10.5551/jat.ed077
Schreitmüller B, Leyhe T, Stransky E, Köhler N, Laske C (2012) Elevated angiopoietin-1 serum levels in patients with Alzheimer’s disease. Int J Alzheimers Dis 1:2012–2015. https://doi.org/10.1155/2012/324016
Shi H, Huang Y, Zhou H, Song X, Yuan S, Fu Y, Luo Y (2007) Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood. 110(8):2899–2906. https://doi.org/10.1182/blood-2007-01-064428
Ständker L, Schrader M, Kanse SM, Jürgens M, Forssmann WG, Preissner KT (1997) Isolation and characterization of the circulating form of human endostatin. FEBS Lett 420(2-3):129–133. https://doi.org/10.1016/s0014-5793(97)01503-2
Stetler-Stevenson WG (1999) Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 103(9):1237–1241. https://doi.org/10.1172/jci6870
Stopa EG, Gonzalez AM, Chorsky R, Corona RJ, Alvarez J, Bird ED, Baird A (1990) Basic fibroblast growth factor in Alzheimer’s disease. Biochem Biophys Res Commun 171(2):690–696. https://doi.org/10.1016/0006-291x(90)91201-3
Takashima A, Noguchi K, Sato K, Hoshino T, Imahori K (1993) Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc Natl Acad Sci 90(16):7789–7793. https://doi.org/10.1073/pnas.90.16.7789
Tarkowski E, Issa R, Sjögren M, Wallin A, Blennow K, Tarkowski A, Kumar P (2002) Increased intrathecal levels of the angiogenic factors VEGF and TGF-β in Alzheimer’s disease and vascular dementia. Neurobiol Aging 23(2):237–243. https://doi.org/10.1016/s0197-4580(01)00285-8
Tarkowski E, Andreasen N, Tarkowski A, Blennow K (2003) Intrathecal inflammation precedes development of Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74(9):1200–1205. https://doi.org/10.1136/jnnp.74.9.1200
Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol: Off J Am Neurol Assoc Child Neurol Soc 30(4):572–580. https://doi.org/10.1002/ana.410300410
Thambisetty M, Beason-Held L, An Y, Kraut MA, Resnick SM (2010) APOE ε4 genotype and longitudinal changes in cerebral blood flow in normal aging. Arch Neurol 67(1):93–98. https://doi.org/10.1001/archneurol.2009.913
Turner CA, Eren-Kocak E, Inui EG, Watson SJ, Akil H (2016) Dysregulated fibroblast growth factor (FGF) signaling in neurological and psychiatric disorders. In: Seminars in cell & developmental biology, vol 53. Academic Press, pp 136–143. https://doi.org/10.1016/j.semcdb.2015.10.003
Ujiie M, Dickstein DL, Carlow DA, Jefferies WA (2003) Blood–brain barrier permeability precedes senile plaque formation in an Alzheimer disease model. Microcirculation. 10(6):463–470. https://doi.org/10.1080/mic.10.6.463.470
Vagnucci AH Jr, Li WW (2003) Alzheimer’s disease and angiogenesis. Lancet 361(9357):605–608. https://doi.org/10.1016/s0140-6736(03)12521-4
van Horssen J, Wilhelmus MM, Heljasvaara R, Pihlajaniemi T, Wesseling P, de Waal RM, Verbeek MM (2002) Collagen XVIII: a novel heparan sulfate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer’s disease brains. Brain Pathol 12(4):456–462. https://doi.org/10.1111/j.1750-3639.2002.tb00462.x
Verbeek MM, Otte-Höller I, van den Born J, van den Heuvel LP, David G, Wesseling P, de Waal RM (1999) Agrin is a major heparan sulfate proteoglycan accumulating in Alzheimer’s disease brain. Am J Pathol 155(6):2115–2125. https://doi.org/10.1016/s0002-9440(10)65529-0
Vinters HV (1987) Cerebral amyloid angiopathy. A critical review. Stroke. 18(2):311–324. https://doi.org/10.1161/01.str.18.2.311
Vinters HV, Wang ZZ, Secor DL (1996) Brain parenchymal and microvascular amyloid in Alzheimer’s disease. Brain Pathol 6(2):179–195. https://doi.org/10.1111/j.1750-3639.1996.tb00799.x
Walia A, Yang JF, Huang YH, Rosenblatt MI, Chang JH, Azar DT (2015) Endostatin’s emerging roles in angiogenesis, lymphangiogenesis, disease, and clinical applications. Biochim Biophys Acta (BBA)-Gen Subj 1850(12):2422–2438. https://doi.org/10.1016/j.bbagen.2015.09.007
Wang J, Al-Lamki RS (2013) Tumor necrosis factor receptor 2: its contribution to acute cellular rejection and clear cell renal carcinoma. Biomed Res Int 1:2013. https://doi.org/10.1155/2013/821310
Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE (2000) Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine. 12(8):1232–1235. https://doi.org/10.1006/cyto.2000.0692
Weller J, Budson A (2018) Current understanding of Alzheimer’s disease diagnosis and treatment. F1000Res 7:F1000 Faculty Rev–1161
Wen W, Moses MA, Wiederschain D, Arbiser JL, Folkman J (1999) The generation of endostatin is mediated by elastase. Cancer Res 59(24):6052–6056
Wickström SA, Alitalo K, Keski-Oja J (2004) An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J Biol Chem 279(19):20178–20185. https://doi.org/10.1074/jbc.m312921200
Xu H, Ge W, Jie F, Cao D, Ming P, Luo W, Song J, Li C (2013) Endostar enhances anti-tumor effects of radiation via inhibition of HIF-1α and bFGF in lung adenocarcinoma cell line A549. Chin-Ger J Clin Oncol 12(12):559–563. https://doi.org/10.1007/s10330-013-1255-2
Yamaguchi N, Anand-Apte B, Lee M, Sasaki T, Fukai N, Shapiro R, Que I, Lowik C, Timpl R, Olsen BR (1999) Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J 18(16):4414–4423. https://doi.org/10.1093/emboj/18.16.4414
Yates CM, Butterworth J, Tennant MC, Gordon A (1990) Enzyme activities in relation to pH and lactate in postmortem brain in Alzheimer-type and other dementias. J Neurochem 55(5):1624–1630. https://doi.org/10.1111/j.1471-4159.1990.tb04948.x
Yehya AH, Asif M, Petersen SH, Subramaniam AV, Kono K, Majid AM, Oon CE (2018) Angiogenesis: managing the culprits behind tumorigenesis and metastasis. Medicina. 54(1):8. https://doi.org/10.3390/medicina54010008
Yin G, Liu W, An P, Li P, Ding I, Planelles V, Schwarz EM, Min W (2002) Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis. Mol Ther 5(5):547–554. https://doi.org/10.1006/mthe.2002.0590
Yu Y, Moulton KS, Khan MK, Vineberg S, Boye E, Davis VM, O'Donnell PE, Bischoff J, Milstone DS (2004) E-selectin is required for the antiangiogenic activity of endostatin. Proc Natl Acad Sci 101(21):8005–8010. https://doi.org/10.1073/pnas.0402551101
Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron. 57(2):178–201. https://doi.org/10.1016/j.neuron.2008.01.003
Zorick TS, Mustacchi Z, Bando SY, Zatz M, Moreira-Filho CA, Olsen B, Passos-Bueno MR (2001) High serum endostatin levels in Down syndrome: implications for improved treatment and prevention of solid tumours. Eur J Hum Genet 9(11):811–814. https://doi.org/10.1038/sj.ejhg.5200721
Author information
Authors and Affiliations
Contributions
DK and TB: Conceived the idea and wrote the first draft; SC, AS, SS, and NS: Figure work; VNB, CVDLC, SB, and AAH: Data compilation; AD, LA, and SBU: Proofread
Corresponding author
Ethics declarations
Ethics approval
Not applicable
Consent to participate
Not applicable
Consent for publication
All the authors have approved the manuscript for publication.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kaur, ., Behl, T., Chigurupati, S. et al. Deciphering the focal role of endostatin in Alzheimer’s disease. Environ Sci Pollut Res 28, 61998–62011 (2021). https://doi.org/10.1007/s11356-021-16567-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16567-7