miR-135b: An emerging player in cardio-cerebrovascular diseases

Yingchun Shao; Jiazhen Xu; Wujun Chen; Minglu Hao; Xinlin Liu; Renshuai Zhang; Yanhong Wang; Yinying Dong

doi:10.1016/j.jpha.2024.100997

Volume 14 Issue 10

Oct. 2024

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Yingchun Shao, Jiazhen Xu, Wujun Chen, Minglu Hao, Xinlin Liu, Renshuai Zhang, Yanhong Wang, Yinying Dong. miR-135b: An emerging player in cardio-cerebrovascular diseases[J]. Journal of Pharmaceutical Analysis, 2024, 14(10): 100997. doi: 10.1016/j.jpha.2024.100997

Citation:

Yingchun Shao, Jiazhen Xu, Wujun Chen, Minglu Hao, Xinlin Liu, Renshuai Zhang, Yanhong Wang, Yinying Dong. miR-135b: An emerging player in cardio-cerebrovascular diseases[J]. Journal of Pharmaceutical Analysis, 2024, 14(10): 100997. doi: 10.1016/j.jpha.2024.100997

Citation:

Yingchun Shao, Jiazhen Xu, Wujun Chen, Minglu Hao, Xinlin Liu, Renshuai Zhang, Yanhong Wang, Yinying Dong. miR-135b: An emerging player in cardio-cerebrovascular diseases[J]. Journal of Pharmaceutical Analysis, 2024, 14(10): 100997. doi: 10.1016/j.jpha.2024.100997

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miR-135b: An emerging player in cardio-cerebrovascular diseases

doi: 10.1016/j.jpha.2024.100997

a. The Affiliated Hospital of Qingdao University, Qingdao University, Qingdao Cancer Institute, Qingdao, 266071, China;
b. Department of Radiation Oncology, The Affiliated Hospital of Qingdao University, Qingdao, 266071, China

Funds:

This work was supported by the Natural Science Foundation of Shandong Province, China (Grant No.: ZR2023QH007), the Natural Science Foundation of QingdaoMunicipality, China (Grant No.: 23-2-1-135-zyyd-jch), the Shandong Postdoctoral Science Foundation, China (Grant No.: SDBX2023049), and the China Postdoctoral Science Foundation (Grant No.: 2023M731852).

Received Date: Dec. 03, 2023
Accepted Date: May 03, 2024
Rev Recd Date: Apr. 20, 2024
Publish Date: May 08, 2024

Abstract

Abstract

miR-135 is a highly conserved miRNA in mammals and includes miR-135a and miR-135b. Recent studies have shown that miR-135b is a key regulatory factor in cardio-cerebrovascular diseases. It is involved in regulating the pathological process of myocardial infarction, myocardial ischemia/reperfusion injury, cardiac hypertrophy, atrial fibrillation, diabetic cardiomyopathy, atherosclerosis, pulmonary hypertension, cerebral ischemia/reperfusion injury, Parkinson's disease, and Alzheimer's disease. Obviously, miR-135b is an emerging player in cardio-cerebrovascular diseases and is expected to be an important target for the treatment of cardio-cerebrovascular diseases. However, the crucial role of miR-135b in cardio-cerebrovascular diseases and its underlying mechanism of action has not been reviewed. Therefore, in this review, we aimed to comprehensively summarize the role of miR-135b and the signaling pathway mediated by miR-135b in cardio-cerebrovascular diseases. Drugs targeting miR-135b for the treatment of diseases and related patents, highlighting the importance of this target and its utility as a therapeutic target for cardio-cerebrovascular diseases, have been discussed.
- miR-135b,
- Myocardial injury,
- Brain injury,
- Cardiovascular diseases,
- Cerebrovascular diseases

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References(95)

References

[1]	S. Barangi, A.W. Hayes, G. Karimi, The role of lncRNAs/miRNAs/Sirt1 axis in myocardial and cerebral injury, Cell Cycle 22 (2023) 1062-1073.
[2]	V. Ambros, microRNA pathways in flies and worms: Growth, death, fat, stress, and timing, Cell 113 (2003) 673-676.
[3]	A.P. Ferragut Cardoso, M. Banerjee, A.N. Nail, et al., miRNA dysregulation is an emerging modulator of genomic instability, Semin. Cancer Biol. 76 (2021) 120-131.
[4]	T.X. Lu, M.E. Rothenberg, MicroRNA, J. Allergy Clin. Immunol. 141 (2018) 1202-1207.
[5]	R. Khatri, S. Subramanian, microRNA-135b and its circuitry networks as potential therapeutic targets in colon cancer, Front. Oncol. 3 (2013), 268.
[6]	J.M.F. Vieira, L.N. Zamproni, C.H.C. Wendt, et al., Overexpression of mir-135b and mir-210 in mesenchymal stromal cells for the enrichment of extracellular vesicles with angiogenic factors, PLoS One 17 (2022), e0272962.
[7]	Z. Xiang, J. Yang, The therapeutic potential of miR-135b in myocardial infarction: Anti-inflammatory trials may be enlightening, Int. J. Cardiol. 312 (2020), 99.
[8]	Z. Cao, J. Qiu, G. Yang, et al., miR-135a biogenesis and regulation in malignancy: A new hope for cancer research and therapy, Cancer Biol. Med. 17 (2020) 569-582.
[9]	S. Kadkhoda, S. Eslami, B. Mahmud Hussen, et al., A review on the importance of miRNA-135 in human diseases, Front. Genet. 13 (2022), 973585.
[10]	A. Li, Y. Yu, X. Ding, et al., miR-135b protects cardiomyocytes from infarction through restraining the NLRP3/caspase-1/IL-1β pathway, Int. J. Cardiol. 307 (2020) 137-145.
[11]	W. Sun, R. Shi, J. Guo, et al., miR-135b-3p promotes cardiomyocyte ferroptosis by targeting GPX4 and aggravates myocardial ischemia/reperfusion injury, Front. Cardiovasc. Med. 8 (2021), 663832.
[12]	Q. Chu, A. Li, X. Chen, et al., Overexpression of miR-135b attenuates pathological cardiac hypertrophy by targeting CACNA1C, Int. J. Cardiol. 269 (2018) 235-241.
[13]	Z. Xu, Y. Han, J. Liu, et al., miR-135b-5p and miR-499a-3p promote cell proliferation and migration in atherosclerosis by directly targeting MEF2C, Sci. Rep. 5 (2015), 12276.
[14]	B. Wu, Y. Liu, M. Wu, et al., Downregulation of microRNA-135b promotes atherosclerotic plaque stabilization in atherosclerotic mice by upregulating erythropoietin receptor, IUBMB Life 72 (2020) 198-213.
[15]	Q. Duan, W. Sun, H. Yuan, et al., microRNA-135b-5p prevents oxygen-glucose deprivation and reoxygenation-induced neuronal injury through regulation of the GSK-3β/Nrf2/ARE signaling pathway, Arch. Med. Sci. 14 (2018) 735-744.
[16]	L. Wen, J. Sun, X. Chen, et al., miR-135b-dependent downregulation of S100B promotes neural stem cell differentiation in a hypoxia/ischemia-induced cerebral palsy rat model, Am. J. Physiol. Cell Physiol. 319 (2020) C955-C966.
[17]	R. Zeng, D. Luo, H. Li, et al., microRNA-135b alleviates MPP⁺-mediated Parkinson’s disease in in vitro model through suppressing FoxO1-induced NLRP3 inflammasome and pyroptosis, J. Clin. Neurosci. 65 (2019) 125-133.
[18]	Y. Zhang, H. Xing, S. Guo, et al., microRNA-135b has a neuroprotective role via targeting of β-site APP-cleaving enzyme 1, Exp. Ther. Med. 12 (2016) 809-814.
[19]	Y. Huang, Y. Wang, Y. Ouyang, Elevated microRNA-135b-5p relieves neuronal injury and inflammation in post-stroke cognitive impairment by targeting NR3C2, Int. J. Neurosci. 132 (2022) 58-66.
[20]	X. Zhang, X. Zhang, microRNA-135b-5p regulates trophoblast cell function by targeting phosphoinositide-3-kinase regulatory subunit 2 in preeclampsia, Bioengineered 13 (2022) 12338-12349.
[21]	L. Liu, H. Xu, H. Zhao, et al., microRNA-135b-5p promotes endothelial cell proliferation and angiogenesis in diabetic retinopathy mice by inhibiting Von Hipp-el-Lindau and elevating hypoxia inducible factor α expression, J. Drug Target. 29 (2021) 300-309.
[22]	X. Yuan, Y. Wu, L. Lu, et al., Long noncoding RNA SNHG14 knockdown exerts a neuroprotective role in MPP⁺-induced Parkinson’s disease cell model through mediating miR-135b-5p/KPNA4 axis, Metab. Brain Dis. 37 (2022) 2363-2373.
[23]	K. Lv, Y. Liu, Y. Zheng, et al., Long non-coding RNA MALAT1 regulates cell proliferation and apoptosis via miR-135b-5p/GPNMB axis in Parkinson’s disease cell model, Biol. Res. 54 (2021), 10.
[24]	C. Zhao, Y. Jiao, Y. Zhang, et al., Lnc SMAD5-AS1 as ceRNA inhibit proliferation of diffuse large B cell lymphoma via Wnt/β-catenin pathway by sponging miR-135b-5p to elevate expression of APC, Cell Death Dis. 10 (2019), 252.
[25]	S. Wang, X. Yang, W. Xie, et al., LncRNA GAPLINC promotes renal cell cancer tumorigenesis by targeting the miR-135b-5p/CSF1 axis, Front. Oncol. 11 (2021), 718532.
[26]	L. Wu, L. Xia, H. Jiang, et al., Long non-coding RNA DANCR represses the viability, migration and invasion of multiple myeloma cells by sponging miR-135b-5p to target KLF9, Mol. Med. Rep. 24 (2021), 649.
[27]	X. Zhang, H. Mao, S. Zhang, et al., lncRNA PCAT18 inhibits proliferation, migration and invasion of gastric cancer cells through miR-135b suppression to promote CLDN11 expression, Life Sci. 249 (2020), 117478.
[28]	Z. Chen, F. Chen, L. Li, LncRNA GAS5 aggravates pathological cardiac hypertrophy by targeting miR-135b to mediate apoptosis, Int. J. Cardiol. 294 (2019), 56.
[29]	S. Yu, M. Yu, J. Chen, et al., Circ_0000471 suppresses the progression of ovarian cancer through mediating mir-135b-5p/dusp5 axis, Am. J. Reprod. Immunol. 89 (2023), e13651.
[30]	S. Chen, Z. Luo, X. Chen, Hsa_circ_0044235 regulates the pyroptosis of rheumatoid arthritis via miR-135b-5p-SIRT1 axis, Cell Cycle 20 (2021) 1107-1121.
[31]	J. Hao, Y. Chen, Y. Yu, Circular RNA circ_0008360 inhibits the proliferation, migration, and inflammation and promotes apoptosis of Fibroblast-like synoviocytes by regulating miR-135b-5p/HDAC4 axis in rheumatoid arthritis, Inflammation 45 (2022) 196-211.
[32]	Y. Zhang, Z. Zhang, Y. Yi, et al., CircNOL10 Acts as a Sponge of miR-135a/b-5p in Suppressing Colorectal Cancer Progression via Regulating KLF9, Onco. Targets Ther. 13 (2020) 5165-5176.
[33]	X. Zhang, J. Lu, Q. Zhang, et al., CircRNA RSF1 regulated ox-LDL induced vascular endothelial cells proliferation, apoptosis and inflammation through modulating miR-135b-5p/HDAC1 axis in atherosclerosis, Biol. Res. 54 (2021), 11.
[34]	H. Chen, M. Mao, J. Jiang, et al., Circular RNA CDR1as acts as a sponge of miR-135b-5p to suppress ovarian cancer progression, Onco. Targets Ther. 12 (2019) 3869-3879.
[35]	Z. Mao, G. Liu, G. Xiao, et al., CircCDR1as suppresses bone microvascular endothelial cell activity and angiogenesis through targeting miR-135b/FIH-1 axis, Orthop. Surg. 13 (2021) 573-582.
[36]	H. Lu, Q. Guo, G. Mao, et al., CircLARP4 suppresses cell proliferation, invasion and glycolysis and promotes apoptosis in non-small cell lung cancer by targeting miR-135b, Onco. Targets Ther. 13 (2020) 3717-3728.
[37]	F. Zhao, Y. Guo, Z. Shi, et al., hsa_circ_001946 elevates HOXA10 expression and promotes the development of endometrial receptivity via sponging miR-135b, Diagn. Pathol. 16 (2021), 44.
[38]	Y. Wang, Z. Wang, C. Shao, et al., Melatonin may suppress lung adenocarcinoma progression via regulation of the circular noncoding RNA hsa_circ_0017109/miR-135b-3p/TOX3 axis, J. Pineal Res. 73 (2022), e12813.
[39]	W. Wang, D. He, J. Chen, et al., Circular RNA Plek promotes fibrogenic activation by regulating the miR-135b-5p/TGF-βR1 axis after spinal cord injury, Aging 13 (2021) 13211-13224.
[40]	C. Chen, H. Shen, Q. Huang, et al., The circular RNA CDR1as regulates the proliferation and apoptosis of human cardiomyocytes through the miR-135a/HMOX1 and miR-135b/HMOX1 axes, Genet. Test. Mol. Biomarkers 24 (2020) 537-548.
[41]	S. Yang, J. Yin, X. Hou, Inhibition of miR-135b by SP-1 promotes hypoxia-induced vascular endothelial cell injury via HIF-1α, Exp. Cell Res. 370 (2018) 31-38.
[42]	A. Bhinge, J. Poschmann, S.C. Namboori, et al., miR-135b is a direct PAX6 target and specifies human neuroectoderm by inhibiting TGF-β/BMP signaling, EMBO J. 33 (2014) 1271-1283.
[43]	J. Zhao, X. Wang, Z. Mi, et al., STAT3/miR-135b/NF-κB axis confers aggressiveness and unfavorable prognosis in non-small-cell lung cancer, Cell Death Dis. 12 (2021), 493.
[44]	N. Ji, Z. Yu, IL-6/Stat3 suppresses osteogenic differentiation in ossification of the posterior longitudinal ligament via miR-135b-mediated BMPER reduction, Cell Tissue Res. 391 (2023) 145-157.
[45]	T.S. Han, D.C. Voon, H. Oshima, et al., Interleukin 1 up-regulates microRNA 135b to promote inflammation-associated gastric carcinogenesis in mice, Gastroenterology 156 (2019) 1140-1155.e4.
[46]	L. Dong, J. Deng, Z. Sun, et al., Interference with the β-catenin gene in gastric cancer induces changes to the miRNA expression profile, Tumour Biol. 36 (2015) 6973-6983.
[47]	Y. Wu, G. Hu, R. Wu, et al., High expression of miR-135b predicts malignant transformation and poor prognosis of gastric cancer, Life Sci. 257 (2020), 118133.
[48]	H. Wang, X. Wang, H. Zhang, et al., The HSF1/miR-135b-5p axis induces protective autophagy to promote oxaliplatin resistance through the MUL1/ULK1 pathway in colorectal cancer, Oncogene 40 (2021) 4695-4708.
[49]	Y. Xin, X. Yang, J. Xiao, et al., miR-135b promotes HCC tumorigenesis through a positive-feedback loop, Biochem. Biophys. Res. Commun. 530 (2020) 259-265.
[50]	J. Pei, L. Cai, F. Wang, et al., LPA₂ contributes to vascular endothelium homeostasis and cardiac remodeling after myocardial infarction, Circ. Res. 131 (2022) 388-403.
[51]	L.S. Tombor, D. John, S.F. Glaser, et al., Single cell sequencing reveals endothelial plasticity with transient mesenchymal activation after myocardial infarction, Nat. Commun. 12 (2021), 681.
[52]	Z. Li, E.G. Solomonidis, M. Meloni, et al., Single-cell transcriptome analyses reveal novel targets modulating cardiac neovascularization by resident endothelial cells following myocardial infarction, Eur. Heart J. 40 (2019) 2507-2520.
[53]	H. Hu, S. Gao, J. Pan, miR-135b might be a potential therapeutic target in the treatment of myocardial infarction, Int. J. Cardiol. 322 (2021), 250.
[54]	S. Mao, X. Luo, W. Zeng, GAS5/MiR-135b axis is a potential target for myocardial infarction, Int. J. Cardiol. 311 (2020), 21.
[55]	Y. Bai, Y. Jiang, A. Li, et al., Reply to the letter “GAS5/MiR-135b axis is a potential target for myocardial infarction”, Int. J. Cardiol. 311 (2020), 20.
[56]	M. Algoet, S. Janssens, U. Himmelreich, et al., Myocardial ischemia-reperfusion injury and the influence of inflammation, Trends Cardiovasc. Med. 33 (2023) 357-366.
[57]	Y. Liu, L. Li, Z. Wang, et al., Myocardial ischemia-reperfusion injury; Molecular mechanisms and prevention, Microvasc. Res. 149 (2023), 104565.
[58]	K. Wang, Y. Li, T. Qiang, et al., Role of epigenetic regulation in myocardial ischemia/reperfusion injury, Pharmacol. Res. 170 (2021), 105743.
[59]	M. Nakamura, J. Sadoshima, Mechanisms of physiological and pathological cardiac hypertrophy, Nat. Rev. Cardiol. 15 (2018) 387-407.
[60]	I. Shimizu, T. Minamino, Physiological and pathological cardiac hypertrophy, J. Mol. Cell. Cardiol. 97 (2016) 245-262.
[61]	Y.K. Tham, B.C. Bernardo, J.Y. Ooi, et al., Pathophysiology of cardiac hypertrophy and heart failure: Signaling pathways and novel therapeutic targets, Arch. Toxicol. 89 (2015) 1401-1438.
[62]	S. Johnson, N. Sommer, K. Cox-Flaherty, et al., Pulmonary hypertension: A contemporary review, Am. J. Respir. Crit. Care Med. 208 (2023) 528-548.
[63]	D. Poch, J. Mandel, Pulmonary hypertension, Ann. Intern. Med. 174 (2021) ITC49-ITC64.
[64]	J. Adler, F. Gerhardt, M. Wissmuller, et al., Pulmonary hypertension associated with left-sided heart failure, Curr. Opin. Cardiol. 35 (2020) 610-619.
[65]	K.M. Olsson, T.J. Corte, J.C. Kamp, et al., Pulmonary hypertension associated with lung disease: New insights into pathomechanisms, diagnosis, and management, Lancet Respir. Med. 11 (2023) 820-835.
[66]	P. Hu, Y. Xu, Y. Jiang, et al., The mechanism of the imbalance between proliferation and ferroptosis in pulmonary artery smooth muscle cells based on the activation of SLC7A11, Eur. J. Pharmacol. 928 (2022), 175093.
[67]	Y. Zhang, M. Hernandez, J. Gower, et al., JAGGED-NOTCH3 signaling in vascular remodeling in pulmonary arterial hypertension, Sci. Transl. Med. 14 (2022), eabl5471.
[68]	J. Wang, X. Yan, W. Feng, et al., S1P induces proliferation of pulmonary artery smooth muscle cells by promoting YAP-induced Notch3 expression and activation, J. Biol. Chem. 296 (2021), 100599.
[69]	P. Zimetbaum, Atrial fibrillation, Ann. Intern. Med. 166 (2017) ITC33-ITC48.
[70]	A. Alonso, Z. Almuwaqqat, A. Chamberlain, Mortality in atrial fibrillation. Is it changing? Trends Cardiovasc. Med. 31 (2021) 469-473.
[71]	B.J.J.M. Brundel, X. Ai, M.T. Hills, et al., Atrial fibrillation, Nat. Rev. Dis. Primers 8 (2022), 21.
[72]	H. Wang, W. Jiang, Y. Hu, et al., Quercetin improves atrial fibrillation through inhibiting TGF-β/Smads pathway via promoting miR-135b expression, Phytomed. Int. J. Phytother. Phytopharm. 93 (2021), 153774.
[73]	Y. Shao, M. Li, Q. Yu, et al., CircRNA CDR1as promotes cardiomyocyte apoptosis through activating hippo signaling pathway in diabetic cardiomyopathy, Eur. J. Pharmacol. 922 (2022), 174915.
[74]	Y. Shao, M. Li, Y. Wang, et al., GDF11 mitigates high glucose-induced cardiomyocytes apoptosis by inhibiting the ALKBH5-FOXO3-CDR1as/Hippo signaling pathway, Biochim. Biophys. Acta Mol. Cell Res. 1871 (2024), 119656.
[75]	W.H. Dillmann, Diabetic cardiomyopathy, Circ. Res. 124 (2019) 1160-1162.
[76]	L. Ren, X. Chen, B. Nie, et al., Ranolazine inhibits pyroptosis via regulation of miR-135b in the treatment of diabetic cardiac fibrosis, Front. Mol. Biosci. 9 (2022), 806966.
[77]	P. Libby, The changing landscape of atherosclerosis, Nature 592 (2021) 524-533.
[78]	E. Falk, Pathogenesis of atherosclerosis, J. Am. Coll. Cardiol. 47 (2006) C7-C12.
[79]	W. Herrington, B. Lacey, P. Sherliker, et al., Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease, Circ. Res. 118 (2016) 535-546.
[80]	K. Kobiyama, K. Ley, Atherosclerosis, Circ. Res. 123 (2018) 1118-1120.
[81]	A. Tedgui, Z. Mallat, Cytokines in atherosclerosis: Pathogenic and regulatory pathways, Physiol. Rev. 86 (2006) 515-581.
[82]	M. Iida, S. Harada, T. Takebayashi, Application of metabolomics to epidemiological studies of atherosclerosis and cardiovascular disease, J. Atheroscler. Thromb. 26 (2019) 747-757.
[83]	A. Bersano, J. Engele, M.K.E. Schafer, Neuroinflammation and brain disease, BMC Neurol. 23 (2023), 227.
[84]	M.W. Salter, B. Stevens, Microglia emerge as central players in brain disease, Nat. Med. 23 (2017) 1018-1027.
[85]	C.G. Ardanaz, M.J. Ramirez, M. Solas, Brain metabolic alterations in Alzheimer’s disease, Int. J. Mol. Sci. 23 (2022), 3785.
[86]	J. Zhang, W. Liu, Y. Wang, et al., miR-135b plays a neuroprotective role by targeting GSK3β in MPP⁺-intoxicated SH-SY5Y cells, Dis. Markers 2017 (2017), 5806146.
[87]	J. Taubel, W. Hauke, S. Rump, et al., Novel antisense therapy targeting microRNA-132 in patients with heart failure: Results of a first-in-human Phase 1b randomized, double-blind, placebo-controlled study, Eur. Heart J. 42 (2021) 178-188.
[88]	S.P. Nana-Sinkam, C.M. Croce, Clinical applications for microRNAs in cancer, Clin. Pharmacol. Ther. 93 (2013) 98-104.
[89]	T. Catela Ivkovic, G. Voss, H. Cornella, et al., microRNAs as cancer therapeutics: A step closer to clinical application, Cancer Lett. 407 (2017) 113-122.
[90]	M. Zhong, L. Che, M. Du, et al., Desflurane protects against liver ischemia/reperfusion injury via regulating miR-135b-5p, J. Chin. Med. Assoc. 84 (2021) 38-45.
[91]	D. Yao, H. Cui, S. Zhou, et al., Morin inhibited lung cancer cells viability, growth, and migration by suppressing miR-135b and inducing its target CCNG2, Tumour Biol. 39 (2017), 1010428317712443.
[92]	L. Zhang, X. Wang, S. He, et al., Gypenosides suppress fibrosis of the renal NRK-49F cells by targeting miR-378a-5p through the PI3K/AKT signaling pathway, J. Ethnopharmacol. 311 (2023), 116466.
[93]	Y. He, J. Sheng, X. Ling, et al., Estradiol regulates miR-135b and mismatch repair gene expressions via estrogen receptor-β in colorectal cells, Exp. Mol. Med. 44 (2012) 723-732.
[94]	J. Zhou, Q. Chen, Poor expression of microRNA-135b results in the inhibition of cisplatin resistance and proliferation and induces the apoptosis of gastric cancer cells through MST1-mediated MAPK signaling pathway, FASEB J. 33 (2019) 3420-3436.
[95]	J. Wang, R. Zhang, B. Zhang, et al., miR-135b improves proliferation and regulates chemotherapy resistance in ovarian cancer, J. Mol. Histol. 53 (2022) 699-712.