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Protein & Peptide Letters


ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Mini-Review Article

Evolution and Structure of API5 and Its Roles in Anti-Apoptosis

Author(s): Meishan Chen, Weiwei Wu, Dongwu Liu, Yanhua Lv, Hongkuan Deng, Sijia Gao, Yaqi Gu, Mujie Huang, Xiao Guo, Baohua Liu, Bosheng Zhao and Qiuxiang Pang*

Volume 28, Issue 6, 2021

Published on: 11 December, 2020

Page: [612 - 622] Pages: 11

DOI: 10.2174/0929866527999201211195551

Price: $65


Apoptosis, also named programmed cell death, is a highly conserved physiological mechanism. Apoptosis plays crucial roles in many life processes, such as tissue development, organ formation, homeostasis maintenance, resistance against external aggression, and immune responses. Apoptosis is regulated by many genes, among which Apoptosis Inhibitor-5 (API5) is an effective inhibitor, though the structure of API5 is completely different from the other known Inhibitors of Apoptosis Proteins (IAPs). Due to its high expression in many types of tumors, API5 has received extensive attention, and may be an effective target for cancer treatment. In order to comprehensively and systematically understand the biological roles of API5, we summarized the evolution and structure of API5 and its roles in anti-apoptosis in this review.

Keywords: Apoptosis, API5, anti-apoptosis, evolution, structure, functional pathways.

Graphical Abstract
Elmore, S.; Brix, A.; Sanders, J.M.; Travlos, G.S. Apoptosis: a review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
[] [PMID: 17562483]
Rathmell, J.C.; Thompson, C.B. Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell, 2002, 109(2)(Suppl.), S97-S107.
[] [PMID: 11983156]
Tower, J. Programmed cell death in aging. Ageing Res. Rev., 2015, 23(Pt A), 90-100.
[] [PMID: 25862945]
Pistritto, G.; Trisciuoglio, D.; Ceci, C.; Garufi, A.; D’Orazi, G. Apoptosis as anticancer mechanism: function and dysfunction of its modulators and targeted therapeutic strategies. Aging (Albany NY), 2016, 8(4), 603-619.
[] [PMID: 27019364]
Geske, F. J.; Gerschenson, L. E. The biology of apoptosis. Human Pathology, 2001, 32(10), 0-1038.
Bosman, F. T.; Visser, B. C.; Oeveren, J. V. Apoptosis: pathophysiology of programmed cell death. Pathology Research & Practice, 1996, 192(7), 0-683.
Bold, R.J.; Termuhlen, P.M.; McConkey, D.J. Apoptosis, cancer and cancer therapy. Surg. Oncol., 1997, 6(3), 133-142.
[] [PMID: 9576629]
Hockenbery, D. Defining apoptosis. Am. J. Pathol., 1995, 146(1), 16-19.
[PMID: 7856725]
Satchell, P.G.; Gutmann, J.L.; Witherspoon, D.E. Apoptosis: an introduction for the endodontist. Int. Endod. J., 2003, 36(4), 237-245.
[] [PMID: 12702117]
Portt, L.; Norman, G.; Clapp, C.; Greenwood, M.; Greenwood, M.T. Anti-apoptosis and cell survival: a review. Biochim. Biophys. Acta, 2011, 1813(1), 238-259.
[] [PMID: 20969895]
Panzarini, E.; Inguscio, V.; Dini, L. Overview of cell death mechanisms induced by Rose Bengal acetate-photodynamic therapy. Int. J. Photoenergy, 2011, 2011(1)
Majtnerova, P.; Rousar, T. An overview of apoptosis assays detecting DNA fragmentation. Mol. Biol. Rep., 2018, 45, 1469-1478.
KERR, J. Apoptosis. Its significance in cancer and cancer therapy. Cancer, 1994, 73(8), 201326.
McHugh, P.; Turina, M. Apoptosis and necrosis: a review for surgeons. Surg. Infect. (Larchmt.), 2006, 7(1), 53-68.
[] [PMID: 16509786]
Hengartner, M.O. The biochemistry of apoptosis. Nature, 2000, 407(6805), 770-776.
[] [PMID: 11048727]
Strasser, A.; Jost, P.J.; Nagata, S. The many roles of FAS receptor signaling in the immune system. Immunity, 2009, 30(2), 180-192.
[] [PMID: 19239902]
Muñoz-Pinedo, C.; Guío-Carrión, A.; Goldstein, J.C.; Fitzgerald, P.; Newmeyer, D.D.; Green, D.R. Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc. Natl. Acad. Sci. USA, 2006, 103(31), 11573-11578.
[] [PMID: 16864784]
Baud, V.; Karin, M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol., 2001, 11(9), 372-377.
[] [PMID: 11514191]
Shen, H.M.; Pervaiz, S. TNF receptor superfamily-induced cell death: redox-dependent execution. FASEB J., 2006, 20(10), 1589-1598.
[] [PMID: 16873882]
Varfolomeev, E.; Vucic, D. Inhibitor of apoptosis proteins: fascinating biology leads to attractive tumor therapeutic targets. Future Oncol., 2011, 7(5), 633-648.
[] [PMID: 21568679]
Mpakou, V.E.; Nezis, I.P.; Stravopodis, D.J.; Margaritis, L.H.; Papassideri, I.S. Programmed cell death of the ovarian nurse cells during oogenesis of the silkmoth Bombyx mori. Dev. Growth Differ., 2006, 48(7), 419-428.
[] [PMID: 16961589]
Srinivasula, S.M.; Datta, P.; Kobayashi, M.; Wu, J.W.; Fujioka, M.; Hegde, R.; Zhang, Z.; Mukattash, R.; Fernandes-Alnemri, T.; Shi, Y.; Jaynes, J.B.; Alnemri, E.S. sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol., 2002, 12(2), 125-130.
[] [PMID: 11818063]
Wu, G.; Chai, J.; Suber, T.L.; Wu, J.W.; Du, C.; Wang, X.; Shi, Y. Structural basis of IAP recognition by Smac/DIABLO. Nature, 2000, 408(6815), 1008-1012.
[] [PMID: 11140638]
Phillipps, H.R.; Hurst, P.R. XIAP: a potential determinant of ovarian follicular fate. Reproduction, 2012, 144(2), 165-176.
[] [PMID: 22653317]
Fulda, S.; Vucic, D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov., 2012, 11(2), 109-124.
[] [PMID: 22293567]
Ren, K.; Zhang, W.; Shi, Y.; Gong, J. Pim-2 activates API-5 to inhibit the apoptosis of hepatocellular carcinoma cells through NF-kappaB pathway. Pathol. Oncol. Res., 2010, 16(2), 229-237.
[] [PMID: 19821157]
Vucic, D.; Dixit, V.M.; Wertz, I.E. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat. Rev. Mol. Cell Biol., 2011, 12(7), 439-452.
[] [PMID: 21697901]
Tewari, M.; Yu, M.; Ross, B.; Dean, C.; Giordano, A.; Rubin, R. AAC-11, a novel cDNA that inhibits apoptosis after growth factor withdrawal. Cancer Res., 1997, 57(18), 4063-4069.
[PMID: 9307294]
Li, D.; Liu, Y.; Li, H.; Peng, J.J.; Tan, Y.; Zou, Q.; Song, X.F.; Du, M.; Yang, Z.H.; Tan, Y.; Zhou, J.J.; Xu, T.; Fu, Z.Q.; Feng, J.Q.; Cheng, P.; chen, T.; Wei, D.; Su, X.M.; Liu, H.Y.; Qi, Z.C.; Tang, L.J.; Wang, T.; Guo, X.; Hu, Y.H.; Zhang, T. MicroRNA-1 promotes apoptosis of hepatocarcinoma cells by targeting apoptosis inhibitor-5 (API-5). FEBS Lett., 2015, 589(1), 68-76.
[] [PMID: 25433291]
Basset, C.; Bonnet-Magnaval, F.; Navarro, M.G.; Touriol, C.; Courtade, M.; Prats, H.; Garmy-Susini, B.; Lacazette, E. Api5 a new cofactor of estrogen receptor alpha involved in breast cancer outcome. Oncotarget, 2017, 8(32), 52511-52526.
[] [PMID: 28881748]
Rigou, P.; Piddubnyak, V.; Faye, A.; Rain, J.C.; Michel, L.; Calvo, F.; Poyet, J.L. The antiapoptotic protein AAC-11 interacts with and regulates Acinus-mediated DNA fragmentation. EMBO J., 2009, 28(11), 1576-1588.
[] [PMID: 19387494]
Marchler-Bauer, A.; Bo, Y.; Han, L.; He, J.; Lanczycki, C.J.; Lu, S.; Chitsaz, F.; Derbyshire, M.K.; Geer, R.C.; Gonzales, N.R.; Gwadz, M.; Hurwitz, D.I.; Lu, F.; Marchler, G.H.; Song, J.S.; Thanki, N.; Wang, Z.; Yamashita, R.A.; Zhang, D.; Zheng, C.; Geer, L.Y.; Bryant, S.H. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res., 2017, 45(D1), D200-D203.
[] [PMID: 27899674]
Faye, A.; Poyet, J-L. Targeting AAC-11 in cancer therapy. Expert Opin. Ther. Targets, 2010, 14(1), 57-65.
[] [PMID: 20001210]
Han, B.G.; Kim, K.H.; Lee, S.J.; Jeong, K.C.; Cho, J.W.; Noh, K.H.; Kim, T.W.; Kim, S.J.; Yoon, H.J.; Suh, S.W.; Lee, S.; Lee, B.I. Helical repeat structure of apoptosis inhibitor 5 reveals protein-protein interaction modules. J. Biol. Chem., 2012, 287(14), 10727-10737.
[] [PMID: 22334682]
Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M.L.; Rehman, M.; Walther, T.C.; Olsen, J.V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science, 2009, 325, 834-840.
Yang, X.J.; Seto, E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell, 2008, 31(4), 449-461.
[] [PMID: 18722172]
Zeng, L.; Zhou, M.M. Bromodomain: an acetyl-lysine binding domain. FEBS Lett., 2002, 513(1), 124-128.
[] [PMID: 11911891]
Imre, G.; Heering, J.; Takeda, A.N.; Husmann, M.; Thiede, B.; zu Heringdorf, D.M.; Green, D.R.; van der Goot, F.G.; Sinha, B.; Dötsch, V.; Rajalingam, K. Caspase-2 is an initiator caspase responsible for pore-forming toxin-mediated apoptosis. EMBO J., 2012, 31(11), 2615-2628.
[] [PMID: 22531785]
Holmberg, C.; Helin, K.; Sehested, M.; Karlström, O. E2F-1-induced p53-independent apoptosis in transgenic mice. Oncogene, 1998, 17(2), 143-155.
[] [PMID: 9674698]
Song, K.H.; Cho, H.; Kim, S.; Lee, H.J.; Oh, S.J.; Woo, S.R.; Hong, S.O.; Jang, H.S.; Noh, K.H.; Choi, C.H.; Chung, J.Y.; Hewitt, S.M.; Kim, J.H.; Son, M.; Kim, S.H.; Lee, B.I.; Park, H.C.; Bae, Y.K.; Kim, T.W. API5 confers cancer stem cell-like properties through the FGf2-NANOG axis. Oncogenesis, 2017, 6(1), e285.
[] [PMID: 28092370]
Hu, Y.; Yao, J.; Liu, Z.; Liu, X.; Fu, H.; Ye, K. Akt phosphorylates acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J., 2005, 24(20), 3543-3554.
[] [PMID: 16177823]
Hu, S.; Snipas, S.J.; Vincenz, C.; Salvesen, G.; Dixit, V.M. Caspase-14 is a novel developmentally regulated protease. J. Biol. Chem., 1998, 273(45), 29648-29653.
[] [PMID: 9792675]
Lord, C.E.N.; Gunawardena, A.H.L.A.N. Programmed cell death in C. elegans, mammals and plants. Eur. J. Cell Biol., 2012, 91(8), 603-613.
[] [PMID: 22512890]
McIlwain, D.R.; Berger, T.; Mak, T.W. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol., 2013, 5(4), a008656-a008656.
[] [PMID: 23545416]
Julien, O.; Wells, J.A. Caspases and their substrates. Cell Death Differ., 2017, 24(8), 1380-1389.
[] [PMID: 28498362]
Cohen, G.M. Caspases: the executioners of apoptosis. Biochem. J., 1997, 326(Pt 1), 1-16.
[] [PMID: 9337844]
Villa, P.; Kaufmann, S.H.; Earnshaw, W.C. Caspases and caspase inhibitors. Trends Biochem. Sci., 1997, 22(10), 388-393.
[] [PMID: 9357314]
Boatright, K.M.; Salvesen, G.S. Mechanisms of caspase activation. Curr. Opin. Cell Biol., 2003, 15(6), 725-731.
[] [PMID: 14644197]
Park, H.H. Structural features of caspase-activating complexes. Int. J. Mol. Sci., 2012, 13(4), 4807-4818.
[] [PMID: 22606010]
Hofmann, K.; Bucher, P.; Tschopp, J. The CARD domain: a new apoptotic signalling motif. Trends Biochem. Sci., 1997, 22(5), 155-156.
[] [PMID: 9175472]
Krumschnabel, G.; Sohm, B.; Bock, F.; Manzl, C.; Villunger, A. The enigma of caspase-2: the laymen’s view. Cell Death Differ., 2009, 16(2), 195-207.
[] [PMID: 19023332]
Jia, L. T.; Chen, S. Y.; Yang, A. G. Cancer gene therapy targeting cellular apoptosis machinery. Cancer Treatment Reviews, 2012, 38(7), 868-876.
Kumar, S.; Kinoshita, M.; Noda, M.; Copeland, N.G.; Jenkins, N.A. Induction of apoptosis by the mouse NEDD2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene CED-3 and the mammalian IL-1 beta-converting enzyme. Genes Dev., 1994, 8(14), 1613-1626.
[] [PMID: 7958843]
Kumar, S. Caspase 2 in apoptosis, the DNA damage response and tumour suppression: enigma no more? Nat. Rev. Cancer, 2009, 9(12), 897-903.
[] [PMID: 19890334]
Shalini, S.; Dorstyn, L.; Dawar, S.; Kumar, S. Old, new and emerging functions of caspases. Cell Death Differ., 2015, 22(4), 526-539.
[] [PMID: 25526085]
Gergely; Imre; Jean; Berthelet; Jan; Heering; Sebastian; Kehrloesser; Inga; Maria, Apoptosis inhibitor 5 is an endogenous inhibitor of caspase-2. EMBO Rep., 2017, 18, 733-744.
Sahara, S.; Aoto, M.; Eguchi, Y.; Imamoto, N.; Yoneda, Y.; Tsujimoto, Y. Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature, 1999, 401(6749), 168-173.
[] [PMID: 10490026]
Fernandes, H.; Czapinska, H.; Grudziaz, K.; Bujnicki, J. M.; Nowacka, M. Crystal structure of human Acinus RNA recognition motif domain. Peerj, 2018, 6(2), e5163.
Bandara, L.R.; La Thangue, N.B. Adenovirus E1a prevents the retinoblastoma gene product from complexing with a cellular transcription factor. Nature, 1991, 351(6326), 494-497.
[] [PMID: 1710781]
Lee, M.; Rivera-Rivera, Y.; Moreno, C.S.; Saavedra, H.I. The E2F activators control multiple mitotic regulators and maintain genomic integrity through Sgo1 and BubR1. Oncotarget, 2017, 8(44), 77649-77672.
[] [PMID: 29100415]
Fueyo, J.; Gomez-Manzano, C.; Yung, W.K.A.; Liu, T.J.; Alemany, R.; McDonnell, T.J.; Shi, X.; Rao, J.S.; Levin, V.A.; Kyritsis, A.P. Overexpression of E2F-1 in glioma triggers apoptosis and suppresses tumor growth in vitro and in vivo. Nat. Med., 1998, 4(6), 685-690.
[] [PMID: 9623977]
Hunt, K.K.; Deng, J.; Liu, T.J.; Wilson-Heiner, M.; Swisher, S.G.; Clayman, G.; Hung, M.C. Adenovirus-mediated overexpression of the transcription factor E2F-1 induces apoptosis in human breast and ovarian carcinoma cell lines and does not require p53. Cancer Res., 1997, 57(21), 4722-4726.
[PMID: 9354430]
Dong, Y.B.; Yang, H.L.; Elliott, M.J.; Liu, T.J.; Stilwell, A.; Atienza, C.Jr.; McMasters, K.M. Adenovirus-mediated E2F-1 gene transfer efficiently induces apoptosis in melanoma cells. Cancer, 1999, 86(10), 2021-2033.
[<2021::AID-CNCR20>3.0.CO;2-1] [PMID: 10570427]
Field, S.J.; Tsai, F.Y.; Kuo, F.; Zubiaga, A.M.; Kaelin, W.G., Jr; Livingston, D.M.; Orkin, S.H.; Greenberg, M.E. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell, 1996, 85(4), 549-561.
[] [PMID: 8653790]
Yamasaki, L.; Jacks, T.; Bronson, R.; Goillot, E.; Harlow, E.; Dyson, N.J. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell, 1996, 85(4), 537-548.
[] [PMID: 8653789]
Wu, X.; Levine, A.J. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA, 1994, 91(9), 3602-3606.
[] [PMID: 8170954]
Macleod, K.F.; Hu, Y.; Jacks, T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J., 1996, 15(22), 6178-6188.
[] [PMID: 8947040]
Phillips, A.C.; Bates, S.; Ryan, K.M.; Helin, K.; Vousden, K.H. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev., 1997, 11(14), 1853-1863.
[] [PMID: 9242492]
Tsai, K.Y.; Hu, Y.; Macleod, K.F.; Crowley, D.; Yamasaki, L.; Jacks, T. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell, 1998, 2(3), 293-304.
[] [PMID: 9774968]
Guo, Z.; Yikang, S.; Yoshida, H.; Mak, T.W.; Zacksenhaus, E. Inactivation of the retinoblastoma tumor suppressor induces apoptosis protease-activating factor-1 dependent and independent apoptotic pathways during embryogenesis. Cancer Res., 2001, 61(23), 8395-8400.
[PMID: 11731416]
Ho, A.T.; Li, Q.H.; Hakem, R.; Mak, T.W.; Zacksenhaus, E. Coupling of caspase-9 to Apaf1 in response to loss of pRb or cytotoxic drugs is cell-type-specific. EMBO J., 2004, 23(2), 460-472.
[] [PMID: 14713951]
Hallstrom, T.C.; Nevins, J.R. Jab1 is a specificity factor for E2f1-induced apoptosis. Genes Dev., 2006, 20(5), 613-623.
[] [PMID: 16481464]
Morris, E.J.; Michaud, W.A.; Ji, J.Y.; Moon, N.S.; Rocco, J.W.; Dyson, N.J. Functional identification of Api5 as a suppressor of E2F-dependent apoptosis in vivo. PLoS Genet., 2006, 2(11), e196.
[] [PMID: 17112319]
Chlebova, K.; Bryja, V.; Dvorak, P.; Kozubik, A.; Wilcox, W.R.; Krejci, P. High molecular weight FGf2: the biology of a nuclear growth factor. Cell. Mol. Life Sci., 2009, 66(2), 225-235.
[] [PMID: 18850066]
Saucedo, L.; Sobarzo, C.; Brukman, N.G.; Guidobaldi, H.A.; Lustig, L.; Giojalas, L.C.; Buffone, M.G.; Vazquez-Levin, M.H.; Marín-Briggiler, C. Involvement of fibroblast growth factor 2 (FGf2) and its receptors in the regulation of mouse sperm physiology. Reproduction, 2018, 156(2), 163-172.
[] [PMID: 29866768]
Woodbury, M.E.; Ikezu, T. Fibroblast growth factor-2 signaling in neurogenesis and neurodegeneration. J. Neuroimmune Pharmacol., 2014, 9(2), 92-101.
[] [PMID: 24057103]
Wang, C.; Ke, Y.; Liu, S.; Pan, S.; Liu, Z.; Zhang, H.; Fan, Z.; Zhou, C.; Liu, J.; Wang, F. Ectopic fibroblast growth factor receptor 1 promotes inflammation by promoting nuclear factor-κB signaling in prostate cancer cells. J. Biol. Chem., 2018, 293(38), 14839-14849.
[] [PMID: 30093411]
Noh, K.H.; Kim, S.H.; Kim, J.H.; Song, K.H.; Lee, Y.H.; Kang, T.H.; Han, H.D.; Sood, A.K.; Ng, J.; Kim, K.; Sonn, C.H.; Kumar, V.; Yee, C.; Lee, K.M.; Kim, T.W. API5 confers tumoral immune escape through FGf2-dependent cell survival pathway. Cancer Res., 2014, 74(13), 3556-3566.
[] [PMID: 24769442]
Jang, H.S.; Woo, S.R.; Song, K.H.; Cho, H.; Chay, D.B.; Hong, S.O.; Lee, H.J.; Oh, S.J.; Chung, J.Y.; Kim, J.H.; Kim, T.W. API5 induces cisplatin resistance through FGFR signaling in human cancer cells. Exp. Mol. Med., 2017, 49(9), e374.
[] [PMID: 28883546]
Luciano, F.; Jacquel, A.; Colosetti, P.; Herrant, M.; Cagnol, S.; Pages, G.; Auberger, P. Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene, 2003, 22(43), 6785-6793.
[] [PMID: 14555991]
Krejci, P.; Pejchalova, K.; Rosenbloom, B.E.; Rosenfelt, F.P.; Tran, E.L.; Laurell, H.; Wilcox, W.R. The antiapoptotic protein Api5 and its partner, high molecular weight FGf2, are up-regulated in B cell chronic lymphoid leukemia. J. Leukoc. Biol., 2007, 82(6), 1363-1364.
[] [PMID: 17827341]
Kim, Y.S.; Park, H.J.; Park, J.H.; Hong, E.J.; Jang, G.Y.; Jung, I.D.; Han, H.D.; Lee, S.H.; Vo, M.C.; Lee, J.J.; Yang, A.; Farmer, E.; Wu, T.C.; Kang, T.H.; Park, Y.M. A novel function of API5 (apoptosis inhibitor 5), TLR4-dependent activation of antigen presenting cells. OncoImmunology, 2018, 7(10), e1472187.
[] [PMID: 30288341]
Jagot-Lacoussiere, L.; Kotula, E.; Villoutreix, B.O.; Bruzzoni-Giovanelli, H.; Poyet, J.L. A cell penetrating peptide targeting AAC-11 specifically induces cancer cells death. Cancer Res., 2016, 76(18), 5479-5490.
[] [PMID: 27406828]
Zhang, S.; Yao, F.; Jing, T.; Zhang, M.; Zhao, W.; Zou, X.; Sui, L.; Hou, L. Cloning, expression pattern, and potential role of apoptosis inhibitor 5 in the termination of embryonic diapause and early embryo development of Artemia sinica. Gene, 2017, 628, 170-179.
[] [PMID: 28710039]

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