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Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Role of BCL-2 Family Proteins in Apoptosis and its Regulation by Nutrients

Author(s): Chen Zheng*, Ting Liu, Huihui Liu and Jing Wang*

Volume 21, Issue 8, 2020

Page: [799 - 806] Pages: 8

DOI: 10.2174/1389203721666191227122252

Price: $65

Abstract

In the body, millions of cells die and proliferate each day to maintain normal function and cooperation of all tissues, organs, and systems. Thus, programmed cell death, or apoptosis, is critical to sustain growth, development, and body health. The vital role of B-cell leukemia/lymphoma-2 (BCL-2) family proteins in apoptosis has been identified. The BCL-2 family includes both pro- and antiapoptotic proteins, which are structurally and functionally related, containing up to four BCL-2 homology (BH) motifs (BH1-4). There are also some nutritional factors that regulate apoptosis via the BCL-2 family proteins. In this review, the BCL-2 family proteins and their apoptosis-inducing mechanism have been discussed, along with the nutrient factors that regulate apoptosis through the BCL-2 family proteins.

Keywords: BCL-2 family proteins, apoptosis, regulation, nutrients, lymphoma, probiotics.

Graphical Abstract

[1]
Singh, R.; Letai, A.; Sarosiek, K. Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins. Nat. Rev. Mol. Cell Biol., 2019, 20(3), 175-193.
[http://dx.doi.org/10.1038/s41580-018-0089-8] [PMID: 30655609]
[2]
Rathmell, J.C.; Thompson, C.B. Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell, 2002, 109(Suppl.), S97-S107.
[http://dx.doi.org/10.1016/S0092-8674(02)00704-3] [PMID: 11983156]
[3]
Martinou, J.C.; Youle, R.J. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev. Cell, 2011, 21(1), 92-101.
[http://dx.doi.org/10.1016/j.devcel.2011.06.017] [PMID: 21763611]
[4]
Adamkov, M. Logical complexity of Bcl-2 family proteins function in the intrinsic apoptosis. Srp. Arh. Celok. Lek., 2019, 147(1-2), 99-104.
[http://dx.doi.org/10.2298/SARH190124010A]
[5]
Lu, T.; Aron, L.; Zullo, J.; Pan, Y.; Kim, H.; Chen, Y.; Yang, T.H.; Kim, H.M.; Drake, D.; Liu, X.S.; Bennett, D.A.; Colaiácovo, M.P.; Yankner, B.A. REST and stress resistance in ageing and Alzheimer’s disease. Nature, 2014, 507(7493), 448-454.
[http://dx.doi.org/10.1038/nature13163] [PMID: 24670762]
[6]
Rigby, R.J.; Carr, J.; Orgel, K.; King, S.L.; Lund, P.K.; Dekaney, C.M. Intestinal bacteria are necessary for doxorubicin-induced intestinal damage but not for doxorubicin-induced apoptosis. Gut Microbes, 2016, 7(5), 414-423.
[http://dx.doi.org/10.1080/19490976.2016.1215806] [PMID: 27459363]
[7]
Timucin, A.C.; Basaga, H. Pro-apoptotic effects of lipid oxidation products: HNE at the crossroads of NF-κB pathway and anti-apoptotic Bcl-2. Free Radic. Biol. Med., 2017, 111, 209-218.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.11.010] [PMID: 27840321]
[8]
Igney, F.H.; Krammer, P.H. Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer, 2002, 2(4), 277-288.
[http://dx.doi.org/10.1038/nrc776] [PMID: 12001989]
[9]
Locksley, R.M.; Killeen, N.; Lenardo, M.J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell, 2001, 104(4), 487-501.
[http://dx.doi.org/10.1016/S0092-8674(01)00237-9] [PMID: 11239407]
[10]
Min, K.J.; Woo, S.M.; Shahriyar, S.A.; Kwon, T.K. Elucidation for modulation of death receptor (DR) 5 to strengthen apoptotic signals in cancer cells. Arch. Pharm. Res., 2019, 42(1), 88-100.
[http://dx.doi.org/10.1007/s12272-018-01103-y] [PMID: 30632113]
[11]
Mukherjee, P.K.; DeCoster, M.A.; Campbell, F.Z.; Davis, R.J.; Bazan, N.G. Modulation of stress-sensitive MAP kinases and neuronal cell death by glutamate receptor signaling interplay. J. Neurochem., 1999, 72, S75-S75.
[12]
Ashkenazi, A.; Dixit, V.M. Death receptors: signaling and modulation. Science, 1998, 281(5381), 1305-1308.
[http://dx.doi.org/10.1126/science.281.5381.1305] [PMID: 9721089]
[13]
Wajant, H. The Fas signaling pathway: more than a paradigm. Science, 2002, 296(5573), 1635-1636.
[http://dx.doi.org/10.1126/science.1071553] [PMID: 12040174]
[14]
Galluzzi, L.; Bravo-San Pedro, J.M.; Kroemer, G. Organelle-specific initiation of cell death. Nat. Cell Biol., 2014, 16(8), 728-736.
[http://dx.doi.org/10.1038/ncb3005] [PMID: 25082195]
[15]
Pihán, P.; Carreras-Sureda, A.; Hetz, C. BCL-2 family: integrating stress responses at the ER to control cell demise. Cell Death Differ., 2017, 24(9), 1478-1487.
[http://dx.doi.org/10.1038/cdd.2017.82] [PMID: 28622296]
[16]
Joseph, S.K.; Booth, D.M.; Young, M.P.; Hajnóczky, G. Redox regulation of ER and mitochondrial Ca2+ signaling in cell survival and death. Cell Calcium, 2019, 79, 89-97.
[http://dx.doi.org/10.1016/j.ceca.2019.02.006] [PMID: 30889512]
[17]
Tait, S.W.G.; Green, D.R. Mitochondrial regulation of cell death. Cold Spring Harb. Perspect. Biol., 2013, 5(9),a008706.
[http://dx.doi.org/10.1101/cshperspect.a008706] [PMID: 24003207]
[18]
Maas, C.; Verbrugge, I.; de Vries, E.; Savich, G.; van de Kooij, L.W.; Tait, S.W.G.; Borst, J. Smac/DIABLO release from mitochondria and XIAP inhibition are essential to limit clonogenicity of Type I tumor cells after TRAIL receptor stimulation. Cell Death Differ., 2010, 17(10), 1613-1623.
[http://dx.doi.org/10.1038/cdd.2010.39] [PMID: 20395960]
[19]
Jackson, D.N.; Theiss, A.L. Gut bacteria signaling to mitochondria in intestinal inflammation and cancer. Gut Microbes, 2019, 1-20.
[http://dx.doi.org/10.1080/19490976.2019.1592421] [PMID: 30913966]
[20]
Warren, C.F.A.; Wong-Brown, M.W.; Bowden, N.A. BCL-2 family isoforms in apoptosis and cancer. Cell Death Dis., 2019, 10(3), 177.
[http://dx.doi.org/10.1038/s41419-019-1407-6] [PMID: 30792387]
[21]
Adachi, M.; Tsujimoto, Y. Juxtaposition of human bcl-2 and immunoglobulin lambda light chain gene in chronic lymphocytic leukemia is the result of a reciprocal chromosome translocation between chromosome 18 and 22. Oncogene, 1989, 4(9), 1073-1075.
[PMID: 2506501]
[22]
Reed, J.C.; Tsujimoto, Y.; Alpers, J.D.; Croce, C.M.; Nowell, P.C. Regulation of bcl-2 proto-oncogene expression during normal human lymphocyte proliferation. Science, 1987, 236(4806), 1295-1299.
[http://dx.doi.org/10.1126/science.3495884] [PMID: 3495884]
[23]
Tsujimoto, Y.; Cossman, J.; Jaffe, E.; Croce, C.M. Involvement of the bcl-2 gene in human follicular lymphoma. Science, 1985, 228(4706), 1440-1443.
[http://dx.doi.org/10.1126/science.3874430] [PMID: 3874430]
[24]
Tsujimoto, Y.; Finger, L.R.; Yunis, J.; Nowell, P.C.; Croce, C.M. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science, 1984, 226(4678), 1097-1099.
[http://dx.doi.org/10.1126/science.6093263] [PMID: 6093263]
[25]
Leverson, J.D.; Sampath, D.; Souers, A.J.; Rosenberg, S.H.; Fairbrother, W.J.; Amiot, M.; Konopleva, M.; Letai, A. Found in translation: How preclinical research is guiding the clinical development of the BCL2-selective inhibitor venetoclax. Cancer Discov., 2017, 7(12), 1376-1393.
[http://dx.doi.org/10.1158/2159-8290.CD-17-0797] [PMID: 29146569]
[26]
Gross, A.; Katz, S.G. Non-apoptotic functions of BCL-2 family proteins. Cell Death Differ., 2017, 24(8), 1348-1358.
[http://dx.doi.org/10.1038/cdd.2017.22] [PMID: 28234359]
[27]
Timucin, A.C.; Basaga, H.; Kutuk, O. Selective targeting of antiapoptotic BCL-2 proteins in cancer. Med. Res. Rev., 2019, 39(1), 146-175.
[http://dx.doi.org/10.1002/med.21516] [PMID: 29846950]
[28]
Hetz, C.; Glimcher, L. The daily job of night killers: alternative roles of the BCL-2 family in organelle physiology. Trends Cell Biol., 2008, 18(1), 38-44.
[http://dx.doi.org/10.1016/j.tcb.2007.10.003] [PMID: 18077169]
[29]
Chipuk, J.E.; Kuwana, T.; Bouchier-Hayes, L.; Droin, N.M.; Newmeyer, D.D.; Schuler, M.; Green, D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science, 2004, 303(5660), 1010-1014.
[http://dx.doi.org/10.1126/science.1092734] [PMID: 14963330]
[30]
Nechushtan, A.; Smith, C.L.; Lamensdorf, I.; Yoon, S.H.; Youle, R.J. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol., 2001, 153(6), 1265-1276.
[http://dx.doi.org/10.1083/jcb.153.6.1265] [PMID: 11402069]
[31]
Martinou, J.C.; Green, D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol., 2001, 2(1), 63-67.
[http://dx.doi.org/10.1038/35048069] [PMID: 11413467]
[32]
Kale, J.; Osterlund, E.J.; Andrews, D.W. BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ., 2018, 25(1), 65-80.
[http://dx.doi.org/10.1038/cdd.2017.186] [PMID: 29149100]
[33]
McIlwain, D.R.; Berger, T.; Mak, T.W. Caspase ffunctions in cell death and disease (vol 5, a008656, 2013). Cold Spring Harb. Perspect. Biol., 2015, 7(4)
[http://dx.doi.org/10.1101/cshperspect.a026716] [PMID: 25833847]
[34]
Albeck, J.G.; Burke, J.M.; Spencer, S.L.; Lauffenburger, D.A.; Sorger, P.K. Modeling a snap-action, variable-delay switch controlling extrinsic cell death. PLoS Biol., 2008, 6(12), 2831-2852.
[http://dx.doi.org/10.1371/journal.pbio.0060299] [PMID: 19053173]
[35]
Shamas-Din, A.; Kale, J.; Leber, B.; Andrews, D.W. Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb. Perspect. Biol., 2013, 5(4),a008714.
[http://dx.doi.org/10.1101/cshperspect.a008714] [PMID: 23545417]
[36]
Chipuk, J.E.; Moldoveanu, T.; Llambi, F.; Parsons, M.J.; Green, D.R. The BCL-2 family reunion. Mol. Cell, 2010, 37(3), 299-310.
[http://dx.doi.org/10.1016/j.molcel.2010.01.025] [PMID: 20159550]
[37]
Cui, J.; Placzek, W.J. Post-transcriptional regulation of anti-apoptotic BCL2 family members. Int. J. Mol. Sci., 2018, 19(1)E308
[http://dx.doi.org/10.3390/ijms19010308] [PMID: 29361709]
[38]
Vervliet, T.; Parys, J.B.; Bultynck, G. Bcl-2 proteins and calcium signaling: complexity beneath the surface. Oncogene, 2016, 35(39), 5079-5092.
[http://dx.doi.org/10.1038/onc.2016.31] [PMID: 26973249]
[39]
Rong, Y.P.; Bultynck, G.; Aromolaran, A.S.; Zhong, F.; Parys, J.B.; De Smedt, H.; Mignery, G.A.; Roderick, H.L.; Bootman, M.D.; Distelhorst, C.W. The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc. Natl. Acad. Sci. USA, 2009, 106(34), 14397-14402.
[http://dx.doi.org/10.1073/pnas.0907555106] [PMID: 19706527]
[40]
Wang, C. Yang, L.; Hu, Y.H.; Zhu, J.S.; Xia, R.; Yu, Y.Q.; Shen, J.M.; Zhang, Z.; Wang, S.L. Isoliquiritigenin as an antioxidant phytochemical ameliorates the developmental anomalies of zebrafish induced by 2,2 ',4,4 '-tetrabromodiphenyl ether. Sci. Total Environ., 2019, 666, 390-398.
[http://dx.doi.org/10.1016/j.scitotenv.2019.02.272] [PMID: 30802654]
[41]
Chen, X.; Xuan, B.; Xu, D.; Wang, Q.; Cheng, M.; Jin, Y. Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate. Reprod. Domest. Anim., 2019, 54(2), 300-308.
[PMID: 30325531]
[42]
Chen, M.F.; Liou, S.S.; Hong, T.Y.; Kao, S.T.; Liu, I.M. Gigantol has protective effects against high glucose-evoked nephrotoxicity in mouse glomerulus mesangial cells by suppressing ROS/MAPK/NF-kappa B signaling pathways. Molecules, 2019, 24(1)
[http://dx.doi.org/10.3390/molecules24010080] [PMID: 30609798]
[43]
Noh, D.; Choi, J.G.; Huh, E.; Oh, M.S. Tectorigenin, a flavonoid-based compound of leopard lily rhizome, attenuates UV-B-induced apoptosis and collagen degradation by inhibiting oxidative stress in human keratinocytes. Nutrients, 2018, 10(12)E1998
[http://dx.doi.org/10.3390/nu10121998] [PMID: 30562977]
[44]
Melo-Silveira, R.F.; Viana, R.L.S.; Sabry, D.A.; da Silva, R.A.; Machado, D.; Nascimento, A.K.L.; Scortecci, K.C.; Ferreira-Halder, C.V.; Sassaki, G.L.; Rocha, H.A.O. Antiproliferative xylan from corn cobs induces apoptosis in tumor cells. Carbohydr. Polym., 2019, 210, 245-253.
[http://dx.doi.org/10.1016/j.carbpol.2019.01.073] [PMID: 30732760]
[45]
Yan, S.L.; Wang, Z.H.; Mong, M.C.; Yang, Y.C.; Yin, M.C. Combination of carnosine and asiatic acid provided greater anti-inflammatory protection for HUVE cells and diabetic mice than individual treatments of carnosine or asiatic acid alone. Food Chem. Toxicol., 2019, 126, 192-198.
[http://dx.doi.org/10.1016/j.fct.2019.02.027] [PMID: 30802477]
[46]
Bai, M.; Liu, B.; Peng, M.; Jia, J.; Fang, X.; Miao, M. Effect of Sargentodoxa cuneata total phenolic acids on focal cerebral ischemia reperfusion injury rats model. Saudi J. Biol. Sci., 2019, 26(3), 569-576.
[http://dx.doi.org/10.1016/j.sjbs.2018.11.019] [PMID: 30899173]
[47]
Lee, M.R.; Bae, S.J.; Kim, J.E.; Song, B.R.; Choi, J.Y.; Park, J.J.; Park, J.W.; Kang, M.J.; Choi, H.J.; Choi, Y.W.; Kim, K.M.; Hwang, D.Y. Inhibition of endoplasmic reticulum stress in high-fat-diet-induced obese C57BL/6 mice: Efficacy of a novel extract from mulberry (Morus alba) leaves fermented with Cordyceps militaris. Lab. Anim. Res., 2018, 34(4), 288-294.
[http://dx.doi.org/10.5625/lar.2018.34.4.288] [PMID: 30671117]
[48]
Veskovic, M.; Mladenovic, D.; Milenkovic, M.; Tosic, J.; Borozan, S.; Gopcevic, K.; Labudovic-Borovic, M.; Dragutinovic, V.; Vucevic, D.; Jorgacevic, B.; Isakovic, A.; Trajkovic, V.; Radosavljevic, T. Betaine modulates oxidative stress, inflammation, apoptosis, autophagy, and Akt/mTOR signaling in methionine-choline deficiency-induced fatty liver disease. Eur. J. Pharmacol., 2019, 848, 39-48.
[http://dx.doi.org/10.1016/j.ejphar.2019.01.043] [PMID: 30689995]
[49]
Liang, Z.; Yuan, Z.; Li, G.; Fu, F.; Shan, Y. Hypolipidemic, antioxidant, and antiapoptotic effects of polysaccharides extracted from Reishi mushroom, Ganoderma lucidum (Leysser: Fr) karst, in mice fed a high-fat diet. J. Med. Food, 2018, 21(12), 1218-1227.
[http://dx.doi.org/10.1089/jmf.2018.4182] [PMID: 30183494]
[50]
Sharaf, L.K.; Sharma, M.; Chandel, D.; Shukla, G. Prophylactic intervention of probiotics (L.acidophilus, L.rhamnosus GG) and celecoxib modulate Bax-mediated apoptosis in 1,2-dimethylhydrazine-induced experimental colon carcinogenesis. BMC Cancer, 2018, 18(1), 1111.
[http://dx.doi.org/10.1186/s12885-018-4999-9] [PMID: 30424722]
[51]
Zhu, J.; Zhou, M.; Zhao, X.; Mu, M.; Cheng, M. Blueberry, combined with probiotics, alleviates non-alcoholic fatty liver disease via IL-22-mediated JAK1/STAT3/BAX signaling. Food Funct., 2018, 9(12), 6298-6306.
[http://dx.doi.org/10.1039/C8FO01227J] [PMID: 30411754]
[52]
Lin, P.Y.; Li, S.C.; Lin, H.P.; Shih, C.K. Germinated brown rice combined with Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis inhibits colorectal carcinogenesis in rats. Food Sci. Nutr., 2018, 7(1), 216-224.
[http://dx.doi.org/10.1002/fsn3.864] [PMID: 30680175]
[53]
Jiang, Z.; Li, H.; Qiao, J.; Yang, Y.; Wang, Y.; Liu, W.; Han, B. Potential analysis and preparation of chitosan oligosaccharides as oral nutritional supplements of cancer adjuvant therapy. Int. J. Mol. Sci., 2019, 20(4)E920
[http://dx.doi.org/10.3390/ijms20040920] [PMID: 30791594]
[54]
Huang, G.; Mao, J.; Ji, Z.; Ailati, A. Stachyose-induced apoptosis of Caco-2 cells via the caspase-dependent mitochondrial pathway. Food Funct., 2015, 6(3), 765-771.
[http://dx.doi.org/10.1039/C4FO01017E] [PMID: 25578308]
[55]
Wu, B.Y.; Zhu, M.; Ruan, T.; Li, L.J.; Lyu, Y.N.; Wang, H.S. Oxidative stress, apoptosis and abnormal expression of apoptotic protein and gene and cell cycle arrest in the cecal tonsil of broilers induces by dietary methionine deficiency. Res. Vet. Sci., 2018, 121, 65-75.
[http://dx.doi.org/10.1016/j.rvsc.2018.10.009] [PMID: 30359813]
[56]
Fan, X.; Li, S.; Wu, Z.; Dai, Z.; Li, J.; Wang, X.; Wu, G. Glycine supplementation to breast-fed piglets attenuates post-weaning jejunal epithelial apoptosis: a functional role of CHOP signaling. Amino Acids, 2019, 51(3), 463-473.
[http://dx.doi.org/10.1007/s00726-018-2681-9] [PMID: 30483907]
[57]
Zhao, H.M.; Ouyang, H.J.; Liu, L.; Duan, J.Q.; You, J.Y. Effect of glutamine-supplemented enteral nutrition on the apoptosis of colonic mucosal cells in young rats with inflammatory bowl disease., 2019.
[58]
Liu, F.J.; Dong, W.Y.; Zhao, H.; Shi, X.H.; Zhang, Y.L. Effect of molybdenum on reproductive function of male mice treated with busulfan. Theriogenology, 2019, 126, 49-54.
[http://dx.doi.org/10.1016/j.theriogenology.2018.12.002] [PMID: 30530157]
[59]
Aziz, N.M.; Kamel, M.Y.; Mohamed, M.S.; Ahmed, S.M. Antioxidant, anti-inflammatory, and anti-apoptotic effects of zinc supplementation in testes of rats with experimentally induced diabetes. Appl. Physiol. Nutr. Metab., 2018, 43(10), 1010-1018.
[http://dx.doi.org/10.1139/apnm-2018-0070] [PMID: 29726717]
[60]
Padmanabhan, S.; Waly, M.I.; Taranikanti, V.; Guizani, N.; Ali, A.; Rahman, M.S.; Al-Attabi, Z.; Al-Malky, R.N.; Al-Maskari, S.N.M.; Al-Ruqaishi, B.R.S.; Dong, J.; Deth, R.C. Folate/vitamin B12 supplementation combats pxidative stress-associated carcinogenesis in a rat model of colon cancer. Nutr. Cancer, 2019, 71(1), 100-110.
[http://dx.doi.org/10.1080/01635581.2018.1513047] [PMID: 30372163]
[61]
Kavalappa, Y.P.; Rudresh, D.U.; Gopal, S.S.; Shivarudrappa, A.H.; Stephen, N.M.; Rangiah, K.; Ponesakki, G. Beta-carotene isolated from the marine red alga, Gracillaria sp. potently attenuates the growth of human hepatocellular carcinoma (HepG2) cells by modulating multiple molecular pathways. J. Funct. Foods, 2019, 52, 165-176.
[http://dx.doi.org/10.1016/j.jff.2018.11.015]
[62]
Zhang, X.Y.; Xu, Z.P.; Wang, W.; Cao, J.B.; Fu, Q.; Zhao, W.X.; Li, Y.; Huo, X.L.; Zhang, L.M.; Li, Y.F.; Mi, W.D. Vitamin C alleviates LPS-induced cognitive impairment in mice by suppressing neuroinflammation and oxidative stress. Int. Immunopharmacol., 2018, 65, 438-447.
[http://dx.doi.org/10.1016/j.intimp.2018.10.020] [PMID: 30388518]
[63]
Li, Q.; Che, H.X.; Wang, C.C.; Zhang, L.Y.; Ding, L.; Xue, C.H.; Zhang, T.T.; Wang, Y.M. Cerebrosides from sea cucumber improved a beta(1-42)-induced cognitive deficiency in a rat model of Alzheimer’s disease. Mol. Nutr. Food Res., 2019, 63(5)
[64]
Rajput, S.A.; Zhang, C.; Feng, Y.; Wei, X.T.; Khalil, M.M.; Rajput, I.R.; Baloch, D.M.; Shaukat, A.; Rajput, N.; Qamar, H.; Hassan, M.; Qi, D. Proanthocyanidins alleviates AflatoxinB1-induced oxidative stress and apoptosis through mitochondrial pathway in the bursa of Fabricius of broilers. Toxins (Basel), 2019, 11(3)E157
[http://dx.doi.org/10.3390/toxins11030157] [PMID: 30857375]
[65]
Kundu, P.; Patel, S.; Meling, D.D.; Deal, K.; Gao, L.; Helferich, W.G.; Flaws, J.A. The effects of dietary levels of genistein on ovarian follicle number and gene expression. Reprod. Toxicol., 2018, 81, 132-139.
[http://dx.doi.org/10.1016/j.reprotox.2018.07.085] [PMID: 30056207]
[66]
Vera, M.C.; Lorenzetti, F.; Lucci, A.; Comanzo, C.G.; Ceballos, M.P.; Pisani, G.B.; Alvarez, M.L.; Quiroga, A.D.; Carrillo, M.C. Vitamin K2 supplementation blocks the beneficial effects of IFN-α-2b administered on the early stages of liver cancer development in rats. Nutrition, 2019, 59, 170-179.
[http://dx.doi.org/10.1016/j.nut.2018.08.016] [PMID: 30496957]
[67]
Turiello, M.P.; Cristofolini, A.L.; Fiorimanti, M.R.; Diaz, T.; Cavaglieri, L.R.; Merkis, C.I. Effect of prepubertal nutrition on cellular apoptosis and proliferation in at term placenta of Anglo-Nubian goats. Reprod. Domest. Anim., 2019, 54(3), 560-570.
[http://dx.doi.org/10.1111/rda.13395] [PMID: 30575133]
[68]
Gao, Y.; Um, C.Y.; Fedirko, V.; Rutherford, R.E.; Seabrook, M.E.; Barry, E.L.; Baron, J.A.; Bostick, R.M. Effects of supplemental vitamin D and calcium on markers of proliferation, differentiation, and apoptosis in the normal colorectal mucosa of colorectal adenoma patients. PLoS One, 2018, 13(12)e0208762
[http://dx.doi.org/10.1371/journal.pone.0208762] [PMID: 30557404]
[69]
Adams, C.M.; Clark-Garvey, S.; Porcu, P.; Eischen, C.M. Targeting the Bcl-2 family in B cell lymphoma. Front. Oncol., 2019, 8, 636.
[http://dx.doi.org/10.3389/fonc.2018.00636] [PMID: 30671383]
[70]
Opferman, J.T.; Kothari, A. Anti-apoptotic BCL-2 family members in development. Cell Death Differ., 2018, 25(1), 37-45.
[http://dx.doi.org/10.1038/cdd.2017.170] [PMID: 29099482]

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