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Angiogenesis

Erschienen in:

24.10.2019 | Review Paper

Role of melatonin in controlling angiogenesis under physiological and pathological conditions

verfasst von: Qiang Ma, Russel J. Reiter, Yundai Chen

Erschienen in: Angiogenesis | Ausgabe 2/2020

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Abstract

Angiogenesis depends on proangiogenic and anti-angiogenic molecules that regulate endothelial cell proliferation and migration. Well-regulated angiogenesis plays a pivotal role in many physiological conditions such as reproduction and embryonic development, while abnormal angiogenesis is also the basis of a variety of pathological processes including tumor metastasis and atherosclerotic plaque formation. Melatonin has a variety of biological effects, including inhibition of tumor metastasis, stabilizing atherosclerotic plaques, and the regulation of seasonal reproductive rhythms, etc. During certain pathophysiological processes, melatonin exerts different functions depending on its ability to regulate angiogenesis. This review reveals that melatonin has different effects on neovascularization under different physiological and pathological conditions. In tumors, in age-related ocular diseases, and in a hypoxic environment, melatonin inhibits neovascularization in tissues, while in gastric ulcers, skin lesions, and some physiologic processes, it promotes angiogenesis. We also speculate that melatonin may inhibit the neovascularization in atherosclerotic plaques, thus preventing the initiation and development of atherosclerosis. Most studies suggest that these effects are related to the role of melatonin in regulating of vascular endothelial growth factor and its receptors, but the specific regulatory mechanisms remain disparate, which may lead to the differential effects of melatonin on angiogenesis under different conditions. In this review, we thus summarize some seemingly contradictory mechanisms by which melatonin controls angiogenesis under different pathological and physiological conditions, and urge that the regulatory mechanisms be further studied.

Folkman J, Shing Y (1992) Angiogenesis. J Biol Chemistry 267(16):10931–10934. https://doi.org/10.1007/978-1-4613-2825-4_42 CrossRefPubMed

Vandekeere S, Dewerchin M, Carmeliet P (2015) Angiogenesis revisited: an overlooked role of endothelial cell metabolism in vessel sprouting. Microcirculation 22(7):509–517. https://doi.org/10.1111/micc.12229 CrossRefPubMed

Alvarez-Garcia V, Gonzalez A, Alonso-Gonzalez C, Martinez-Campa C, Cos S (2013) Antiangiogenic effects of melatonin in endothelial cell cultures. Microvasc Res 87:25–33. https://doi.org/10.1016/j.mvr.2013.02.008 CrossRefPubMed

Rizov M, Andreeva P, Dimova I (2017) Molecular regulation and role of angiogenesis in reproduction. Taiwan J Obstet Gynecol 56(2):127–132. https://doi.org/10.1016/j.tjog.2016.06.019 CrossRefPubMed

Gerbaud P, Murthi P, Guibourdenche J, Guimiot F, Sarazin B, Evain-Brion D, Badet J, Pidoux G (2019) Study of human T21 placenta suggests a potential role of mesenchymal spondin-2 in placental vascular development. Endocrinology 160(3):684–698. https://doi.org/10.1210/en.2018-00826 CrossRefPubMed

DiPietro LA (2016) Angiogenesis and wound repair: when enough is enough. J Leukoc Biol 100(5):979–984. https://doi.org/10.1189/jlb.4MR0316-102R CrossRefPubMedPubMedCentral

Ribatti D, Crivellato E (2012) "Sprouting angiogenesis", a reappraisal. Dev Biol 372(2):157–165. https://doi.org/10.1016/j.ydbio.2012.09.018 CrossRefPubMed

Folkman J, Cotran R (1976) Relation of vascular proliferation to tumor growth. Int Rev Exp Pathol 16:207–248PubMed

Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9(6):653–660. https://doi.org/10.1038/nm0603-653 CrossRefPubMed

10.

McCord CP, Allen FP (1917) Evidences associating pineal gland function with alterations in pigmentation. Journal of experimental zoology 23:207–224. https://doi.org/10.1002/jez.1400230108 CrossRef

11.

Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958) Isolation of melatonin the pineal gland factor that lightens melanocytes. J Am Chem Soc 80(10):2587–2587. https://doi.org/10.1021/ja01543a060 CrossRef

12.

Konturek SJ, Konturek PC, Brzozowska I, Pawlik M, Sliwowski Z, Czesnikiewicz-Guzik M, Kwiecien S, Brzozowski T, Bubenik GA, Pawlik WW (2007) Localization and biological activities of melatonin in intact and diseased gastrointestinal tract (GIT). J Physiol Pharmacol 58(3):381–405PubMed

13.

Reiter RJ, Tan DX, Galano A (2014) Melatonin: exceeding expectations. Physiology (Bethesda) 29(5):325–333. https://doi.org/10.1152/physiol.00011.2014 CrossRef

14.

Claustrat B, Leston J (2015) Melatonin: physiological effects in humans. Neurochirurgie 61(2–3):77–84. https://doi.org/10.1016/j.neuchi.2015.03.002 CrossRefPubMed

15.

Tan DX, Reiter RJ (2019) Mitochondria: the birth place, battle ground and the site of melatonin metabolism in cells. Melatonin Res 2(1):44–66. https://doi.org/10.32794/mr11250011 CrossRef

16.

Reiter RJ, Tan DX, Fuentes-Broto L (2010) Melatonin: a multitasking molecule. Prog Brain Res 181:127–151. https://doi.org/10.1016/S0079-6123(08)81008-4 CrossRefPubMed

17.

Lee HY, Back K (2018) Melatonin plays a pivotal role in conferring tolerance against endoplasmic reticulum stress via mitogen-activated protein kinases and bZIP60 in Arabidopsis thaliana. Melatonin Res 1(1):94–108. https://doi.org/10.32794/mr11250006 CrossRef

18.

Gonzalez AG, Revilla NR, Emilio J (2019) Clinical uses of melatonin: evaluation of human trials on cancer treatment. Melatonin Res 2(2):47–69. https://doi.org/10.32794/mr11250021 CrossRef

19.

Pfeffer M, Korf HW, Wicht H (2018) Synchronizing effects of melatonin on diurnal and circadian rhythms. Gen Comp Endocrinol 258:215–221. https://doi.org/10.1016/j.ygcen.2017.05.013 CrossRefPubMed

20.

Dominguez-Rodriguez A, Abreu-Gonzalez P, Chen Y (2019) Cardioprotection and effects of melatonin administration on cardiac ischemia reperfusion: Insight from clinical studies. Melatonin Res 2(2):100–105. https://doi.org/10.32794/mr11250024 CrossRef

21.

Jardim-Perassi BV, Arbab AS, Ferreira LC, Borin TF, Varma NR, Iskander AS, Shankar A, Ali MM, de Campos Zuccari DA (2014) Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer. PLoS ONE 9(1):e85311. https://doi.org/10.1371/journal.pone.0085311 CrossRefPubMedPubMedCentral

22.

Gonzalez A, Gonzalez-Gonzalez A, Alonso-Gonzalez C, Menendez-Menendez J, Martinez-Campa C, Cos S (2017) Melatonin inhibits angiogenesis in SH-SY5Y human neuroblastoma cells by downregulation of VEGF. Oncol Rep 37(4):2433–2440. https://doi.org/10.3892/or.2017.5446 CrossRefPubMed

23.

Ganguly K, Sharma AV, Reiter RJ, Swarnakar S (2010) Melatonin promotes angiogenesis during protection and healing of indomethacin-induced gastric ulcer: role of matrix metaloproteinase-2. J Pineal Res 49(2):130–140. https://doi.org/10.1111/j.1600-079X.2010.00776.x CrossRefPubMed

24.

Bizzarri M, Proietti S, Cucina A, Reiter RJ (2013) Molecular mechanisms of the pro-apoptotic actions of melatonin in cancer: a review. Expert Opin Ther Targets 17(12):1483–1496. https://doi.org/10.1517/14728222.2013.834890 CrossRefPubMed

25.

Ferrara N, Henzel WJ (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161(2):851–858. https://doi.org/10.1016/0006-291x(89)92678-8 CrossRefPubMed

26.

Cook KM, Figg WD (2010) Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J Clin 60(4):222–243. https://doi.org/10.3322/caac.20075 CrossRefPubMedPubMedCentral

27.

Shulman K, Rosen S, Tognazzi K, Manseau EJ, Brown LF (1996) Expression of vascular permeability factor (VPF/VEGF) is altered in many glomerular diseases. J Am Soc Nephrol 7(5):661–666PubMed

28.

Ourradi K, Blythe T, Jarrett C, Barratt SL, Welsh GI, Millar AB (2017) VEGF isoforms have differential effects on permeability of human pulmonary microvascular endothelial cells. Respir Res 18(1):116. https://doi.org/10.1186/s12931-017-0602-1 CrossRefPubMedPubMedCentral

29.

Shibuya M (2011) Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies. Genes Cancer 2(12):1097–1105. https://doi.org/10.1177/1947601911423031 CrossRefPubMedPubMedCentral

30.

Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med (Berl) 77(7):527–543. https://doi.org/10.1007/s001099900019 CrossRef

31.

Gupta K, Kshirsagar S, Li W, Gui L, Ramakrishnan S, Gupta P, Law PY, Hebbel RP (1999) VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res 247(2):495–504. https://doi.org/10.1006/excr.1998.4359 CrossRefPubMed

32.

Beazley-Long N, Hua J, Jehle T, Hulse RP, Dersch R, Lehrling C, Bevan H, Qiu Y, Lagreze WA, Wynick D, Churchill AJ, Kehoe P, Harper SJ, Bates DO, Donaldson LF (2013) VEGF-A165b is an endogenous neuroprotective splice isoform of vascular endothelial growth factor A in vivo and in vitro. Am J Pathol 183(3):918–929. https://doi.org/10.1016/j.ajpath.2013.05.031 CrossRefPubMedPubMedCentral

33.

Cerezo AB, Hornedo-Ortega R, Alvarez-Fernandez MA, Troncoso AM, Garcia-Parrilla MC (2017) Inhibition of VEGF-induced VEGFR-2 activation and HUVEC migration by melatonin and other bioactive indolic compounds. Nutrients 9(3):249. https://doi.org/10.3390/nu9030249 CrossRefPubMedCentral

34.

Ramirez-Fernandez MP, Calvo-Guirado JL, de-Val JE, Delgado-Ruiz RA, Negri B, Pardo-Zamora G, Penarrocha D, Barona C, Granero JM, Alcaraz-Banos M (2013) Melatonin promotes angiogenesis during repair of bone defects: a radiological and histomorphometric study in rabbit tibiae. Clin Oral Invest 17(1):147–158. https://doi.org/10.1007/s00784-012-0684-6 CrossRef

35.

Emet M, Ozcan H, Ozel L, Yayla M, Halici Z, Hacimuftuoglu A (2016) A review of melatonin, its receptors and drugs. Eurasian J Med 48(2):135–141. https://doi.org/10.5152/eurasianjmed.2015.0267 CrossRefPubMedPubMedCentral

36.

Zonta YR, Martinez M, Camargo IC, Domeniconi RF, Lupi Junior LA, Pinheiro PF, Reiter RJ, Martinez FE, Chuffa LG (2017) Melatonin reduces angiogenesis in serous papillary ovarian carcinoma of ethanol-preferring rats. Int J Mol Sci 18(4):763CrossRefPubMedCentral

37.

Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285(21):1182–1186. https://doi.org/10.1056/NEJM197111182852108 CrossRefPubMed

38.

Reiter RJ, Rosales-Corral SA, Tan DX, Acuna-Castroviejo D, Qin L, Yang SF, Xu K (2017) Melatonin, a Full Service Anti-Cancer Agent: Inhibition of Initiation, Progression and Metastasis. Int J Mol Sci 18(4):843. https://doi.org/10.3390/ijms18040843 CrossRefPubMedCentral

39.

Wang RX, Liu H, Xu L, Zhang H, Zhou RX (2016) Melatonin downregulates nuclear receptor RZR/RORgamma expression causing growth-inhibitory and anti-angiogenesis activity in human gastric cancer cells in vitro and in vivo. Oncol Lett 12(2):897–903. https://doi.org/10.3892/ol.2016.4729 CrossRefPubMedPubMedCentral

40.

Kim KJ, Choi JS, Kang I, Kim KW, Jeong CH, Jeong JW (2013) Melatonin suppresses tumor progression by reducing angiogenesis stimulated by HIF-1 in a mouse tumor model. J Pineal Res 54(3):264–270. https://doi.org/10.1111/j.1600-079X.2012.01030.x CrossRefPubMed

41.

Carbajo-Pescador S, Ordonez R, Benet M, Jover R, Garcia-Palomo A, Mauriz JL, Gonzalez-Gallego J (2013) Inhibition of VEGF expression through blockade of Hif1alpha and STAT3 signalling mediates the anti-angiogenic effect of melatonin in HepG2 liver cancer cells. Br J Cancer 109(1):83–91. https://doi.org/10.1038/bjc.2013.285 CrossRefPubMedPubMedCentral

42.

Goradel NH, Asghari MH, Moloudizargari M, Negahdari B, Haghi-Aminjan H, Abdollahi M (2017) Melatonin as an angiogenesis inhibitor to combat cancer: mechanistic evidence. Toxicol Appl Pharmcol 335:56–63. https://doi.org/10.1016/j.taap.2017.09.022 CrossRef

43.

Alvarez-Garcia V, Gonzalez A, Alonso-Gonzalez C, Martinez-Campa C, Cos S (2013) Regulation of vascular endothelial growth factor by melatonin in human breast cancer cells. J Pineal Res 54(4):373–380. https://doi.org/10.1111/jpi.12007 CrossRefPubMed

44.

Menendez-Menendez J, Martinez-Campa C (2018) Melatonin: an anti-tumor agent in hormone-dependent cancers. Int J Endocrinol 2018:3271948. https://doi.org/10.1155/2018/3271948 CrossRefPubMedPubMedCentral

45.

Calvo-Guirado JL, Ramirez-Fernandez MP, Gomez-Moreno G, Mate-Sanchez JE, Delgado-Ruiz R, Guardia J, Lopez-Mari L, Barone A, Ortiz-Ruiz AJ, Martinez-Gonzalez JM, Bravo LA (2010) Melatonin stimulates the growth of new bone around implants in the tibia of rabbits. J Pineal Res 49(4):356–363. https://doi.org/10.1111/j.1600-079X.2010.00801.x CrossRefPubMed

46.

Shino H, Hasuike A, Arai Y, Honda M, Isokawa K, Sato S (2016) Melatonin enhances vertical bone augmentation in rat calvaria secluded spaces. Med Oral Patol Oral Cir Bucal 21(1):e122–e126. https://doi.org/10.4317/medoral.20904 CrossRefPubMed

47.

Yildirimturk S, Batu S, Alatli C, Olgac V, Firat D, Sirin Y (2016) The effects of supplemental melatonin administration on the healing of bone defects in streptozotocin-induced diabetic rats. J Appl Oral Sci 24(3):239–249. https://doi.org/10.1590/1678-775720150570 CrossRefPubMedPubMedCentral

48.

Soybir G, Topuzlu C, Odabas O, Dolay K, Bilir A, Koksoy F (2003) The effects of melatonin on angiogenesis and wound healing. Surg Today 33(12):896–901. https://doi.org/10.1007/s00595-003-2621-3 CrossRefPubMed

49.

Pugazhenthi K, Kapoor M, Clarkson AN, Hall I, Appleton I (2008) Melatonin accelerates the process of wound repair in full-thickness incisional wounds. J Pineal Res 44(4):387–396. https://doi.org/10.1111/j.1600-079X.2007.00541.x CrossRefPubMed

50.

Mehraein F, Kabir K (2011) The effects of melatonin on open wounds of aged mice skin. Wounds 23(6):166–170PubMed

51.

Abdelraheim SR, Okasha AM, Ghany HM, Ibrahim HM (2015) Ghrelin gene expression in rats with ethanol-induced gastric ulcers: a role of melatonin. Endocr Regul 49(1):3–10CrossRefPubMed

52.

Colucci R, Fornai M, Antonioli L, Ghisu N, Tuccori M, Blandizzi C, Del Tacca M (2009) Characterization of mechanisms underlying the effects of esomeprazole on the impairment of gastric ulcer healing with addition of NSAID treatment. Dig Liver Dis 41(6):395–405. https://doi.org/10.1016/j.dld.2008.10.004 CrossRefPubMed

53.

Celinski K, Konturek SJ, Konturek PC, Brzozowski T, Cichoz-Lach H, Slomka M, Malgorzata P, Bielanski W, Reiter RJ (2011) Melatonin or L-tryptophan accelerates healing of gastroduodenal ulcers in patients treated with omeprazole. J Pineal Res 50(4):389–394. https://doi.org/10.1111/j.1600-079X.2011.00855.x CrossRefPubMed

54.

Konturek PC, Konturek SJ, Celinski K, Slomka M, Cichoz-Lach H, Bielanski W, Reiter RJ (2010) Role of melatonin in mucosal gastroprotection against aspirin-induced gastric lesions in humans. J Pineal Res 48(4):318–323. https://doi.org/10.1111/j.1600-079X.2010.00755.x CrossRefPubMed

55.

Konturek SJ, Konturek PC, Brzozowski T, Bubenik GA (2007) Role of melatonin in upper gastrointestinal tract. J Physiol Pharmacol 58 Suppl 6:23–52PubMed

56.

Ahluwalia A, Brzozowska IM, Hoa N, Jones MK, Tarnawski AS (2018) Melatonin signaling in mitochondria extends beyond neurons and neuroprotection: Implications for angiogenesis and cardio/gastroprotection. Proc Natl Acad Sci USA 115(9):E1942-E1943. https://doi.org/10.1073/pnas.1722131115 CrossRefPubMedPubMedCentral

57.

Ganguly K, Swarnakar S (2012) Chronic gastric ulceration causes matrix metalloproteinases-9 and – 3 augmentation: alleviation by melatonin. Biochimie 94(12):2687–2698. https://doi.org/10.1016/j.biochi.2012.08.004 CrossRefPubMed

58.

Pradeepkumar Singh L, Vivek Sharma A, Swarnakar S (2011) Upregulation of collagenase-1 and – 3 in indomethacin-induced gastric ulcer in diabetic rats: role of melatonin. J Pineal Res 51(1):61–74. https://doi.org/10.1111/j.1600-079X.2010.00845.x CrossRefPubMed

59.

Ganguly K, Swarnakar S (2009) Induction of matrix metalloproteinase-9 and – 3 in nonsteroidal anti-inflammatory drug-induced acute gastric ulcers in mice: regulation by melatonin. J Pineal Res 47(1):43–55. https://doi.org/10.1111/j.1600-079X.2009.00687.x CrossRefPubMed

60.

Rudra DS, Pal U, Maiti NC, Reiter RJ, Swarnakar S (2013) Melatonin inhibits matrix metalloproteinase-9 activity by binding to its active site. J Pineal Res 54(4):398–405. https://doi.org/10.1111/jpi.12034 CrossRefPubMed

61.

Brzozowska I, Strzalka M, Drozdowicz D, Konturek SJ, Brzozowski T (2014) Mechanisms of esophageal protection, gastroprotection and ulcer healing by melatonin. implications for the therapeutic use of melatonin in gastroesophageal reflux disease (GERD) and peptic ulcer disease. Curr Pharm Des 20(30):4807–4815. https://doi.org/10.2174/1381612819666131119110258 CrossRefPubMed

62.

Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294(5545):1337–1340. https://doi.org/10.1126/science.1066373 CrossRefPubMed

63.

Ivan M, Haberberger T, Gervasi DC, Michelson KS, Gunzler V, Kondo K, Yang H, Sorokina I, Conaway RC, Conaway JW, Kaelin WG Jr (2002) Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc Natl Acad Sci USA 99(21):13459–13464. https://doi.org/10.1073/pnas.192342099 CrossRefPubMedPubMedCentral

64.

Jardim-Perassi BV, Lourenco MR, Doho GM, Grigolo IH, Gelaleti GB, Ferreira LC, Borin TF, Moschetta MG, Pires de Campos Zuccari DA (2016) Melatonin regulates angiogenic factors under hypoxia in breast cancer cell line. Anticancer Agents Med Chem 16(3):347–358CrossRefPubMed

65.

Cheng J, Yang HL, Gu CJ, Liu YK, Shao J, Zhu R, He YY, Zhu XY, Li MQ (2019) Melatonin restricts the viability and angiogenesis of vascular endothelial cells by suppressing HIF-1alpha/ROS/VEGF. Int J Mol Med 43(2):945–955. https://doi.org/10.3892/ijmm.2018.4021 CrossRefPubMed

66.

Zhang Y, Liu Q, Wang F, Ling EA, Liu S, Wang L, Yang Y, Yao L, Chen X, Wang F, Shi W, Gao M, Hao A (2013) Melatonin antagonizes hypoxia-mediated glioblastoma cell migration and invasion via inhibition of HIF-1alpha. J Pineal Res 55(2):121–130. https://doi.org/10.1111/jpi.12052 CrossRefPubMed

67.

Sohn EJ, Won G, Lee J, Lee S, Kim SH (2015) Upregulation of miRNA3195 and miRNA374b mediates the anti-angiogenic properties of melatonin in hypoxic PC-3 prostate cancer cells. J Cancer 6(1):19–28. https://doi.org/10.7150/jca.9591 CrossRefPubMedPubMedCentral

68.

Goncalves Ndo N, Rodrigues RV, Jardim-Perassi BV, Moschetta MG, Lopes JR, Colombo J, Zuccari DA (2014) Molecular markers of angiogenesis and metastasis in lines of oral carcinoma after treatment with melatonin. Anticancer Agents Med Chem 14(9):1302–1311CrossRefPubMed

69.

Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1(6):401–408. https://doi.org/10.1016/j.cmet.2005.05.001 CrossRefPubMed

70.

Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91(5):807–819. https://doi.org/10.1113/expphysiol.2006.033506 CrossRefPubMed

71.

Park SY, Jang WJ, Yi EY, Jang JY, Jung Y, Jeong JW, Kim YJ (2010) Melatonin suppresses tumor angiogenesis by inhibiting HIF-1alpha stabilization under hypoxia. J Pineal Res 48(2):178–184. https://doi.org/10.1111/j.1600-079X.2009.00742.x CrossRefPubMed

72.

Cho SY, Lee HJ, Jeong SJ, Lee HJ, Kim HS, Chen CY, Lee EO, Kim SH (2011) Sphingosine kinase 1 pathway is involved in melatonin-induced HIF-1alpha inactivation in hypoxic PC-3 prostate cancer cells. J Pineal Res 51(1):87–93. https://doi.org/10.1111/j.1600-079X.2011.00865.x CrossRefPubMed

73.

Vriend J, Reiter RJ (2016) Melatonin and the von Hippel-Lindau/HIF-1 oxygen sensing mechanism: a review. Biochim Biophys Acta 1865(2):176–183. https://doi.org/10.1016/j.bbcan.2016.02.004 CrossRefPubMed

74.

Dorrell M, Uusitalo-Jarvinen H, Aguilar E, Friedlander M (2007) Ocular neovascularization: basic mechanisms and therapeutic advances. Surv Ophthalmol 52 Suppl 1:S3–S19. https://doi.org/10.1016/j.survophthal.2006.10.017 CrossRefPubMed

75.

Amaral J, Becerra SP (2010) Effects of human recombinant PEDF protein and PEDF-derived peptide 34-mer on choroidal neovascularization. Invest Ophthalmol Vis Sci 51(3):1318–1326. https://doi.org/10.1167/iovs.09-4455 CrossRefPubMedPubMedCentral

76.

Du H, Sun X, Guma M, Luo J, Ouyang H, Zhang X, Zeng J, Quach J, Nguyen DH, Shaw PX, Karin M, Zhang K (2013) JNK inhibition reduces apoptosis and neovascularization in a murine model of age-related macular degeneration. Proc Natl Acad Sci USA 110(6):2377–2382. https://doi.org/10.1073/pnas.1221729110 CrossRefPubMedPubMedCentral

77.

Sakamoto K, Liu C, Tosini G (2004) Circadian rhythms in the retina of rats with photoreceptor degeneration. J Neurochem 90(4):1019–1024. https://doi.org/10.1111/j.1471-4159.2004.02571.x CrossRefPubMed

78.

Crooke A, Huete-Toral F, Colligris B, Pintor J (2017) The role and therapeutic potential of melatonin in age-related ocular diseases. J Pineal Res 63(2):e12430. https://doi.org/10.1111/jpi.12430

79.

Kaur C, Sivakumar V, Yong Z, Lu J, Foulds WS, Ling EA (2007) Blood-retinal barrier disruption and ultrastructural changes in the hypoxic retina in adult rats: the beneficial effect of melatonin administration. J Pathol 212(4):429–439. https://doi.org/10.1002/path.2195 CrossRefPubMed

80.

Lv XD, Liu S, Cao Z, Gong LL, Feng XP, Gao QF, Wang J, Hu L, Cheng XC, Yu CH, Xing YQ (2016) Correlation between serum melatonin and aMT6S level for age-related macular degeneration patients. Eur Rev Med Pharmacol Sci 20(20):4196–4201PubMed

81.

Blasiak J, Reiter RJ, Kaarniranta K (2016) Melatonin in retinal physiology and pathology: the case of age-related macular degeneration. Oxidative Med Cell Long. https://doi.org/10.1155/2016/6819736 CrossRef

82.

Dehdashtian E, Mehrzadi S, Yousefi B, Hosseinzadeh A, Reiter RJ, Safa M, Ghaznavi H, Naseripour M (2018) Diabetic retinopathy pathogenesis and the ameliorating effects of melatonin; involvement of autophagy, inflammation and oxidative stress. Life Sci 193:20–33. https://doi.org/10.1016/j.lfs.2017.12.001 CrossRefPubMed

83.

Arranz-Romera A, Davis BM, Bravo-Osuna I, Esteban-Perez S, Molina-Martinez IT, Shamsher E, Ravindran N, Guo L, Cordeiro MF, Herrero-Vanrell R (2019) Simultaneous co-delivery of neuroprotective drugs from multi-loaded PLGA microspheres for the treatment of glaucoma. J Control Release 297:26–38. https://doi.org/10.1016/j.jconrel.2019.01.012 CrossRefPubMed

84.

Calderon GD, Juarez OH, Hernandez GE, Punzo SM, De la Cruz ZD (2017) Oxidative stress and diabetic retinopathy: development and treatment. Eye 31(8):1122–1130. https://doi.org/10.1038/eye.2017.64 CrossRefPubMedPubMedCentral

85.

Wang J, Xu X, Elliott MH, Zhu M, Le YZ (2010) Muller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage. Diabetes 59(9):2297–2305. https://doi.org/10.2337/db09-1420 CrossRefPubMedPubMedCentral

86.

Wang JJ, Zhu M, Le YZ (2015) Functions of Muller cell-derived vascular endothelial growth factor in diabetic retinopathy. World J Diabetes 6(5):726–733. https://doi.org/10.4239/wjd.v6.i5.726 CrossRefPubMedPubMedCentral

87.

Bai Y, Ma JX, Guo J, Wang J, Zhu M, Chen Y, Le YZ (2009) Muller cell-derived VEGF is a significant contributor to retinal neovascularization. J Pathol 219(4):446–454. https://doi.org/10.1002/path.2611 CrossRefPubMed

88.

Kaur C, Sivakumar V, Foulds WS, Luu CD, Ling EA (2009) Cellular and vascular changes in the retina of neonatal rats after an acute exposure to hypoxia. Invest Ophthalmol Vis Sci 50(11):5364–5374. https://doi.org/10.1167/iovs.09-3552 CrossRefPubMed

89.

Jiang T, Chang Q, Zhao Z, Yan S, Wang L, Cai J, Xu G (2012) Melatonin-mediated cytoprotection against hyperglycemic injury in Muller cells. PLoS ONE 7(12):e50661. https://doi.org/10.1371/journal.pone.0050661 CrossRefPubMedPubMedCentral

90.

Hellings WE, Peeters W, Moll FL, Piers SR, van Setten J, Van der Spek PJ, de Vries JP, Seldenrijk KA, De Bruin PC, Vink A, Velema E, de Kleijn DP, Pasterkamp G (2010) Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation 121(17):1941–1950. https://doi.org/10.1161/CIRCULATIONAHA.109.887497 CrossRefPubMed

91.

Crea F, Libby P (2017) Acute coronary syndromes: the way forward from mechanisms to precision treatment. Circulation 136(12):1155–1166. https://doi.org/10.1161/CIRCULATIONAHA.117.029870 CrossRefPubMedPubMedCentral

92.

Chistiakov DA, Orekhov AN, Bobryshev YV (2015) Contribution of neovascularization and intraplaque haemorrhage to atherosclerotic plaque progression and instability. Acta Physiol (Oxf) 213(3):539–553. https://doi.org/10.1111/apha.12438 CrossRef

93.

Sedding DG, Boyle EC, Demandt JAF, Sluimer JC, Dutzmann J, Haverich A, Bauersachs J (2018) Vasa vasorum angiogenesis: key player in the initiation and progression of atherosclerosis and potential target for the treatment of cardiovascular disease. Front Immunol 9:706. https://doi.org/10.3389/fimmu.2018.00706 CrossRefPubMedPubMedCentral

94.

Jaipersad AS, Lip GY, Silverman S, Shantsila E (2014) The role of monocytes in angiogenesis and atherosclerosis. J Am Coll Cardiol 63(1):1–11. https://doi.org/10.1016/j.jacc.2013.09.019 CrossRefPubMed

95.

Favero G, Rodella LF, Reiter RJ, Rezzani R (2014) Melatonin and its atheroprotective effects: a review. Molecular cellular endocrinology 382(2):926–937. https://doi.org/10.1016/j.mce.2013.11.016 CrossRefPubMed

96.

Zhang Y, Koradia A, Kamato D, Popat A, Little PJ, Ta HT (2019) Treatment of atherosclerotic plaque: perspectives on theranostics. J Pharm Pharmacol 71(7):1029–1043. https://doi.org/10.1111/jphp.13092 CrossRefPubMed

97.

Ding S, Lin N, Sheng X, Zhao Y, Su Y, Xu L, Tong R, Yan Y, Fu Y, He J, Gao Y, Yuan A, Ye L, Reiter RJ, Pu J (2019) Melatonin stabilizes rupture-prone vulnerable plaques via regulating macrophage polarization in a nuclear circadian receptor RORalpha-dependent manner. Journal of pineal research:e12581. https://doi.org/10.1111/jpi.12581 CrossRef

98.

Li H, Li J, Jiang X, Liu S, Liu Y, Chen W, Yang J, Zhang C, Zhang W (2019) Melatonin enhances atherosclerotic plaque stability by inducing prolyl-4-hydroxylase alpha1 expression. J Hypertens 37(5):964–971. https://doi.org/10.1097/HJH.0000000000001979 CrossRefPubMed

99.

Ma S, Chen J, Feng J, Zhang R, Fan M, Han D, Li X, Li C, Ren J, Wang Y, Cao F (2018) Melatonin ameliorates the progression of atherosclerosis via mitophagy activation and NLRP3 inflammasome inhibition. Oxidative Med Cell Long 2018:9286458. https://doi.org/10.1155/2018/9286458

100.

Hussein MR, Ahmed OG, Hassan AF, Ahmed MA (2007) Intake of melatonin is associated with amelioration of physiological changes, both metabolic and morphological pathologies associated with obesity: an animal model. Int J Exp Pathol 88(1):19–29. https://doi.org/10.1111/j.1365-2613.2006.00512.x CrossRefPubMedPubMedCentral

101.

Pita ML, Hoyos M, Martin-Lacave I, Osuna C, Fernandez-Santos JM, Guerrero JM (2002) Long-term melatonin administration increases polyunsaturated fatty acid percentage in plasma lipids of hypercholesterolemic rats. J Pineal Res 32(3):179–186. https://doi.org/10.1034/j.1600-079x.2002.1o851.x CrossRefPubMed

102.

Sartori C, Dessen P, Mathieu C, Monney A, Bloch J, Nicod P, Scherrer U, Duplain H (2009) Melatonin improves glucose homeostasis and endothelial vascular function in high-fat diet-fed insulin-resistant mice. Endocrinology 150(12):5311–5317. https://doi.org/10.1210/en.2009-0425 CrossRefPubMed

103.

Cardinali DP, Cano P, Jimenez-Ortega V, Esquifino AI (2011) Melatonin and the metabolic syndrome: physiopathologic and therapeutical implications. Neuroendocrinology 93(3):133–142. https://doi.org/10.1159/000324699 CrossRefPubMed

104.

Kwon TG, Lerman LO, Lerman A (2015) The vasa vasorum in atherosclerosis: the vessel within the vascular wall. J Am Coll Cardiol 65(23):2478–2480. https://doi.org/10.1016/j.jacc.2015.04.032 CrossRefPubMed

105.

Castle-Miller J, Bates DO, Tortonese DJ (2017) Mechanisms regulating angiogenesis underlie seasonal control of pituitary function. Proc Natl Acad Sci U S A 114(12):E2514–E2523. https://doi.org/10.1073/pnas.1618917114 CrossRefPubMedPubMedCentral

106.

Korf HW (2018) Signaling pathways to and from the hypophysial pars tuberalis, an important center for the control of seasonal rhythms. Gen Comp Endocrinol 258:236–243. https://doi.org/10.1016/j.ygcen.2017.05.011 CrossRefPubMed

107.

Reiter RJ (1980) The pineal and its hormones in the control of reproduction in mammals. Endocr Rev 1(2):109–131. https://doi.org/10.1210/edrv-1-2-109 CrossRefPubMed

108.

Reiter RJ, Tan DX, Kim SJ, Cruz MH (2014) Delivery of pineal melatonin to the brain and SCN: role of canaliculi, cerebrospinal fluid, tanycytes and Virchow-Robin perivascular spaces. Brain Struct Funct 219(6):1873–1887. https://doi.org/10.1007/s00429-014-0719-7 CrossRefPubMed

109.

Reiter RJ (1993) The melatonin rhythm: both a clock and a calendar. Experientia 49(8):654–664. https://doi.org/10.1007/BF01923947 CrossRefPubMed

110.

Basini G, Bussolati S, Ciccimarra R, Grasselli F (2017) Melatonin potentially acts directly on swine ovary by modulating granulosa cell function and angiogenesis. Reprod Fertil Dev 29(12):2305–2312. https://doi.org/10.1071/RD16513 CrossRefPubMed

111.

Kandemir YB, Konuk E, Katirci E, Xxx F, Behram M (2019) Is the effect of melatonin on vascular endothelial growth factor receptor-2 associated with angiogenesis in the rat ovary? Clinics 74:e658. https://doi.org/10.6061/clinics/2019/e658 CrossRefPubMedPubMedCentral

112.

Li Y, Fang L, Yu Y, Shi H, Wang S, Guo Y, Sun Y (2019) Higher melatonin in the follicle fluid and MT2 expression in the granulosa cells contribute to the OHSS occurrence. Reprod Biol Endocrinol 17(1):37. https://doi.org/10.1186/s12958-019-0479-6 CrossRefPubMedPubMedCentral

Titel: Role of melatonin in controlling angiogenesis under physiological and pathological conditions
verfasst von: Qiang Ma
Russel J. Reiter
Yundai Chen
Publikationsdatum: 24.10.2019
Verlag: Springer Netherlands
Erschienen in: Angiogenesis / Ausgabe 2/2020
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI: https://doi.org/10.1007/s10456-019-09689-7

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Role of melatonin in controlling angiogenesis under physiological and pathological conditions

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