Molecular insights on cytochrome c and nucleotide regulation of apoptosome function and its implication in cancer

Yadav, Neelu; Gogada, Raghu; O'Malley, Jordan; Gundampati, Ravi Kumar; Jayanthi, Srinivas; Hashmi, Sana; Lella, Ravi; Zhang, Dianmu; Wang, Jianmin; Kumar, Rahul; Suresh Kumar, Thallapuranam Krishnaswamy; Chandra, Dhyan

doi:10.1016/j.bbamcr.2019.118573

Title: Molecular insights on cytochrome c and nucleotide regulation of apoptosome function and its implication in cancer

Journal Article · 31 December 2019 · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

DOI: https://doi.org/10.1016/j.bbamcr.2019.118573 · OSTI ID:1755277

Yadav, Neelu; Gogada, Raghu; O'Malley, Jordan; Gundampati, Ravi Kumar; Jayanthi, Srinivas; Hashmi, Sana; Lella, Ravi; Zhang, Dianmu; Wang, Jianmin; Kumar, Rahul; Suresh Kumar, Thallapuranam Krishnaswamy; Chandra, Dhyan

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Research Organization:: Univ. of Arkansas, Fayetteville, AR (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: FG02-01ER15161

OSTI ID:: 1755277

Journal Information:: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Journal Name: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research Journal Issue: 1 Vol. 1867; ISSN 0167-4889

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (72)

Proapoptotic activity of cytochrome c in living cells: effect of K72 substitutions and species differences Chertkova, Rita V.; Sharonov, George V.; Feofanov, Alexei V. Molecular and Cellular Biochemistry, Vol. 314, Issue 1-2 https://doi.org/10.1007/s11010-008-9768-7	journal	April 2008
Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9 Complex Initiates an Apoptotic Protease Cascade Li, Peng; Nijhawan, Deepak; Budihardjo, Imawati Cell, Vol. 91, Issue 4 https://doi.org/10.1016/S0092-8674(00)80434-1	journal	November 1997
Apaf-1, a Human Protein Homologous to C. elegans CED-4, Participates in Cytochrome c–Dependent Activation of Caspase-3 Zou, Hua; Henzel, William J.; Liu, Xuesong Cell, Vol. 90, Issue 3 https://doi.org/10.1016/S0092-8674(00)80501-2	journal	August 1997
The ribonucleotide reductase large subunit (RRM1) as a predictive factor in patients with cancer Jordheim, Lars Petter; Sève, Pascal; Trédan, Olivier The Lancet Oncology, Vol. 12, Issue 7 https://doi.org/10.1016/S1470-2045(10)70244-8	journal	July 2011
Regulation of apoptosis by the redox state of cytochrome c Brown, Guy C.; Borutaite, Vilmante Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 7-8 https://doi.org/10.1016/j.bbabio.2008.03.024	journal	July 2008
Nitration of tyrosine 74 prevents human cytochrome c to play a key role in apoptosis signaling by blocking caspase-9 activation García-Heredia, José M.; Díaz-Moreno, Irene; Nieto, Pedro M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 6-7 https://doi.org/10.1016/j.bbabio.2010.03.009	journal	June 2010
Stability and apoptotic activity of recombinant human cytochrome c Olteanu, Alina; Patel, Chetan N.; Dedmon, Matthew M. Biochemical and Biophysical Research Communications, Vol. 312, Issue 3 https://doi.org/10.1016/j.bbrc.2003.10.182	journal	December 2003
Apo cytochrome c inhibits caspases by preventing apoptosome formation Martin, Angel. G.; Nguyen, Jack; Wells, James A. Biochemical and Biophysical Research Communications, Vol. 319, Issue 3 https://doi.org/10.1016/j.bbrc.2004.05.084	journal	July 2004
Specific Ablation of the Apoptotic Functions of Cytochrome c Reveals a Differential Requirement for Cytochrome c and Apaf-1 in Apoptosis Hao, Zhenyue; Duncan, Gordon S.; Chang, Chia-Che Cell, Vol. 121, Issue 4 https://doi.org/10.1016/j.cell.2005.03.016	journal	May 2005
Intracellular Nucleotides Act as Critical Prosurvival Factors by Binding to Cytochrome C and Inhibiting Apoptosome Chandra, Dhyan; Bratton, Shawn B.; Person, Maria D. Cell, Vol. 125, Issue 7 https://doi.org/10.1016/j.cell.2006.05.026	journal	June 2006
Could drugs inhibiting the mevalonate pathway also target cancer stem cells? Likus, Wirginia; Siemianowicz, Krzysztof; Bieńk, Konrad Drug Resistance Updates, Vol. 25 https://doi.org/10.1016/j.drup.2016.02.001	journal	March 2016
Glioblastoma cancer stem cell biology: Potential theranostic targets Sharifzad, Farzaneh; Ghavami, Saeid; Verdi, Javad Drug Resistance Updates, Vol. 42 https://doi.org/10.1016/j.drup.2018.03.003	journal	January 2019
Secondary necrosis: The natural outcome of the complete apoptotic program Silva, Manuel T. FEBS Letters, Vol. 584, Issue 22 https://doi.org/10.1016/j.febslet.2010.10.046	journal	October 2010
Role of the salt bridge between glutamate 546 and arginine 907 in preservation of autoinhibited form of Apaf-1 Shakeri, Raheleh; Hosseinkhani, Saman; Los, Marek J. International Journal of Biological Macromolecules, Vol. 81 https://doi.org/10.1016/j.ijbiomac.2015.08.027	journal	November 2015
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes van Zundert, G. C. P.; Rodrigues, J. P. G. L. M.; Trellet, M. Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.09.014	journal	February 2016
RRM1 expression and clinical outcome of gemcitabine-containing chemotherapy for advanced non-small-cell lung cancer: A meta-analysis Gong, Weiyi; Zhang, Xinmin; Wu, Jinfeng Lung Cancer, Vol. 75, Issue 3 https://doi.org/10.1016/j.lungcan.2011.08.003	journal	March 2012
Calcium Blocks Formation of Apoptosome by Preventing Nucleotide Exchange in Apaf-1 Bao, Qing; Lu, Wenyun; Rabinowitz, Joshua D. Molecular Cell, Vol. 25, Issue 2 https://doi.org/10.1016/j.molcel.2006.12.013	journal	January 2007
PHAPI, CAS, and Hsp70 Promote Apoptosome Formation by Preventing Apaf-1 Aggregation and Enhancing Nucleotide Exchange on Apaf-1 Kim, Hyun-Eui; Jiang, Xuejun; Du, Fenghe Molecular Cell, Vol. 30, Issue 2 https://doi.org/10.1016/j.molcel.2008.03.014	journal	April 2008
Glioblastoma and chemoresistance to alkylating agents: Involvement of apoptosis, autophagy, and unfolded protein response Hombach-Klonisch, Sabine; Mehrpour, Maryam; Shojaei, Shahla Pharmacology & Therapeutics, Vol. 184 https://doi.org/10.1016/j.pharmthera.2017.10.017	journal	April 2018
Therapy resistance mediated by cancer stem cells Steinbichler, Teresa Bernadette; Dudás, József; Skvortsov, Sergej Seminars in Cancer Biology, Vol. 53 https://doi.org/10.1016/j.semcancer.2018.11.006	journal	December 2018
Wheel of Life, Wheel of Death: A Mechanistic Insight into Signaling by STAND Proteins Danot, Olivier; Marquenet, Emélie; Vidal-Ingigliardi, Dominique Structure, Vol. 17, Issue 2 https://doi.org/10.1016/j.str.2009.01.001	journal	February 2009
Crystal Structure of Full-Length Apaf-1: How the Death Signal Is Relayed in the Mitochondrial Pathway of Apoptosis Reubold, Thomas Frank; Wohlgemuth, Sabine; Eschenburg, Susanne Structure, Vol. 19, Issue 8 https://doi.org/10.1016/j.str.2011.05.013	journal	August 2011
Structural Insights into DD-Fold Assembly and Caspase-9 Activation by the Apaf-1 Apoptosome Su, Tsung-Wei; Yang, Chao-Yu; Kao, Wen-Pin Structure, Vol. 25, Issue 3 https://doi.org/10.1016/j.str.2016.12.019	journal	March 2017
A Nucleotide Binding Site in Caspase-9 Regulates Apoptosome Activation Chereau, David; Zou, Hua; Spada, Alfred P. Biochemistry, Vol. 44, Issue 13 https://doi.org/10.1021/bi047360+	journal	March 2005
Phosphomimetic Substitution of Cytochrome c Tyrosine 48 Decreases Respiration and Binding to Cardiolipin and Abolishes Ability to Trigger Downstream Caspase Activation Pecina, Petr; Borisenko, Grigory G.; Belikova, Natalia A. Biochemistry, Vol. 49, Issue 31 https://doi.org/10.1021/bi100486s	journal	August 2010
ATP Acts as a Regulatory Effector in Modulating Structural Transitions of Cytochrome c : Implications for Apoptotic Activity Patriarca, Antonella; Eliseo, Tommaso; Sinibaldi, Federica Biochemistry, Vol. 48, Issue 15 https://doi.org/10.1021/bi801837e	journal	March 2009
HADDOCK: A Protein−Protein Docking Approach Based on Biochemical or Biophysical Information Dominguez, Cyril; Boelens, Rolf; Bonvin, Alexandre M. J. J. Journal of the American Chemical Society, Vol. 125, Issue 7 https://doi.org/10.1021/ja026939x	journal	February 2003
Stoichiometry, Free Energy, and Kinetic Aspects of Cytochrome c : Apaf-1 Binding in Apoptosis Purring, Cherie; Zou, Hua; Wang, Xiaodong Journal of the American Chemical Society, Vol. 121, Issue 32 https://doi.org/10.1021/ja991235h	journal	July 1999
The Apaf-1•procaspase-9 apoptosome complex functions as a proteolytic-based molecular timer Malladi, Srinivas; Challa-Malladi, Madhavi; Fearnhead, Howard O. The EMBO Journal, Vol. 28, Issue 13 https://doi.org/10.1038/emboj.2009.152	journal	June 2009
Release of chromatin protein HMGB1 by necrotic cells triggers inflammation Scaffidi, Paola; Misteli, Tom; Bianchi, Marco E. Nature, Vol. 418, Issue 6894 https://doi.org/10.1038/nature00858	journal	July 2002
Structure of the apoptotic protease-activating factor 1 bound to ADP Riedl, Stefan J.; Li, Wenyu; Chao, Yang Nature, Vol. 434, Issue 7035 https://doi.org/10.1038/nature03465	journal	April 2005
Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c Vaughn, Allyson E.; Deshmukh, Mohanish Nature Cell Biology, Vol. 10, Issue 12 https://doi.org/10.1038/ncb1807	journal	November 2008
The Apaf-1 apoptosome induces formation of caspase-9 homo- and heterodimers with distinct activities Wu, Chu-Chiao; Lee, Sunhee; Malladi, Srinivas Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13565	journal	November 2016
Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death Rogers, Corey; Fernandes-Alnemri, Teresa; Mayes, Lindsey Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14128	journal	January 2017
Tackling the cancer stem cells — what challenges do they pose? Pattabiraman, Diwakar R.; Weinberg, Robert A. Nature Reviews Drug Discovery, Vol. 13, Issue 7 https://doi.org/10.1038/nrd4253	journal	July 2014
Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes Hill, Michelle M.; Adrain, Colin; Duriez, Patrick J. The EMBO Journal, Vol. 23, Issue 10 https://doi.org/10.1038/sj.emboj.7600210	journal	April 2004
The two Drosophila cytochrome C proteins can function in both respiration and caspase activation Arama, Eli; Bader, Maya; Srivastava, Mayank The EMBO Journal, Vol. 25, Issue 1 https://doi.org/10.1038/sj.emboj.7600920	journal	December 2005
Optimal pathways for the assembly of the Apaf-1·cytochrome c complex into apoptosome Qi, Hong; Jiang, Yu; Yin, Zhiyong Physical Chemistry Chemical Physics, Vol. 20, Issue 3 https://doi.org/10.1039/C7CP06726G	journal	January 2018
Caspase-9 CARD : core domain interactions require a properly formed active site Huber, Kristen L.; Serrano, Banyuhay P.; Hardy, Jeanne A. Biochemical Journal, Vol. 475, Issue 6 https://doi.org/10.1042/BCJ20170913	journal	March 2018
A cytochrome c mutant with high electron transfer and antioxidant activities but devoid of apoptogenic effect Abdullaev, Ziedulla Kh.; Bodrova, Marina E.; Chernyak, Boris V. Biochemical Journal, Vol. 362, Issue 3 https://doi.org/10.1042/bj3620749	journal	March 2002
Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1 Kim, H. -E.; Du, F.; Fang, M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 49 https://doi.org/10.1073/pnas.0507900102	journal	October 2005
Metabolic state of glioma stem cells and nontumorigenic cells Vlashi, E.; Lagadec, C.; Vergnes, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 38 https://doi.org/10.1073/pnas.1106704108	journal	September 2011
Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3 Mao, P.; Joshi, K.; Li, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 21 https://doi.org/10.1073/pnas.1221478110	journal	May 2013
Molecular determinants of caspase-9 activation by the Apaf-1 apoptosome Hu, Qi; Wu, Di; Chen, Wen Proceedings of the National Academy of Sciences, Vol. 111, Issue 46 https://doi.org/10.1073/pnas.1418000111	journal	October 2014
Mechanistic insights into caspase-9 activation by the structure of the apoptosome holoenzyme Li, Yini; Zhou, Mengying; Hu, Qi Proceedings of the National Academy of Sciences, Vol. 114, Issue 7 https://doi.org/10.1073/pnas.1620626114	journal	January 2017
Cytochrome c binding to Apaf-1: The effects of dATP and ionic strength Purring-Koch, C.; McLendon, G. Proceedings of the National Academy of Sciences, Vol. 97, Issue 22 https://doi.org/10.1073/pnas.220416197	journal	October 2000
WD-40 Repeat Region Regulates Apaf-1 Self-association and Procaspase-9 Activation Hu, Yuanming; Ding, Liyun; Spencer, David M. Journal of Biological Chemistry, Vol. 273, Issue 50 https://doi.org/10.1074/jbc.273.50.33489	journal	December 1998
An APAF-1·Cytochrome c Multimeric Complex Is a Functional Apoptosome That Activates Procaspase-9 Zou, Hua; Li, Yuchen; Liu, Xuesong Journal of Biological Chemistry, Vol. 274, Issue 17 https://doi.org/10.1074/jbc.274.17.11549	journal	April 1999
Determinants of Cytochrome c Pro-apoptotic Activity Kluck, Ruth M.; Ellerby, Lisa M.; Ellerby, H. Michael Journal of Biological Chemistry, Vol. 275, Issue 21 https://doi.org/10.1074/jbc.275.21.16127	journal	May 2000
Apaf-1 Oligomerizes into Biologically Active ∼700-kDa and Inactive ∼1.4-MDa Apoptosome Complexes Cain, Kelvin; Bratton, Shawn B.; Langlais, Claudia Journal of Biological Chemistry, Vol. 275, Issue 9 https://doi.org/10.1074/jbc.275.9.6067	journal	March 2000
Cytochrome c Promotes Caspase-9 Activation by Inducing Nucleotide Binding to Apaf-1 Jiang, Xuejun; Wang, Xiaodong Journal of Biological Chemistry, Vol. 275, Issue 40 https://doi.org/10.1074/jbc.C000405200	journal	August 2000
A Mutational Epitope for Cytochrome c Binding to the Apoptosis Protease Activation Factor-1 Yu, Tianning; Wang, Xiaodong; Purring-Koch, Cherie Journal of Biological Chemistry, Vol. 276, Issue 16 https://doi.org/10.1074/jbc.M009773200	journal	April 2001
Physiological Concentrations of K+ Inhibit Cytochrome c-dependent Formation of the Apoptosome Cain, Kelvin; Langlais, Claudia; Sun, Xiao-Ming Journal of Biological Chemistry, Vol. 276, Issue 45 https://doi.org/10.1074/jbc.M107419200	journal	November 2001
A New Model for the Transition of APAF-1 from Inactive Monomer to Caspase-activating Apoptosome Reubold, Thomas F.; Wohlgemuth, Sabine; Eschenburg, Susanne Journal of Biological Chemistry, Vol. 284, Issue 47 https://doi.org/10.1074/jbc.M109.014027	journal	November 2009
Resveratrol Induces p53-independent, X-linked Inhibitor of Apoptosis Protein (XIAP)-mediated Bax Protein Oligomerization on Mitochondria to Initiate Cytochrome c Release and Caspase Activation Gogada, Raghu; Prabhu, Varun; Amadori, Michael Journal of Biological Chemistry, Vol. 286, Issue 33 https://doi.org/10.1074/jbc.M110.202440	journal	August 2011
Bim, a Proapoptotic Protein, Up-regulated via Transcription Factor E2F1-dependent Mechanism, Functions as a Prosurvival Molecule in Cancer Gogada, Raghu; Yadav, Neelu; Liu, Junwei Journal of Biological Chemistry, Vol. 288, Issue 1 https://doi.org/10.1074/jbc.M112.386102	journal	January 2013
Early Mitochondrial Activation and Cytochrome c Up-regulation during Apoptosis Chandra, Dhyan; Liu, Jun-Wei; Tang, Dean G. Journal of Biological Chemistry, Vol. 277, Issue 52 https://doi.org/10.1074/jbc.M207622200	journal	October 2002
Apocytochrome c Blocks Caspase-9 Activation and Bax-induced Apoptosis Martin, Angel G.; Fearnhead, Howard O. Journal of Biological Chemistry, Vol. 277, Issue 52 https://doi.org/10.1074/jbc.M209369200	journal	December 2002
Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis Hu, Y. The EMBO Journal, Vol. 18, Issue 13 https://doi.org/10.1093/emboj/18.13.3586	journal	July 1999
Tissue-specific regulation of cytochrome c by post-translational modifications: respiration, the mitochondrial membrane potential, ROS, and apoptosis Kalpage, Hasini A.; Bazylianska, Viktoriia; Recanati, Maurice A. The FASEB Journal, Vol. 33, Issue 2 https://doi.org/10.1096/fj.201801417R	journal	February 2019
Atomic structure of the apoptosome: mechanism of cytochrome c - and dATP-mediated activation of Apaf-1 Zhou, Mengying; Li, Yini; Hu, Qi Genes & Development, Vol. 29, Issue 22 https://doi.org/10.1101/gad.272278.115	journal	November 2015
Cancer stem cells - important players in tumor therapy resistance Colak, Selcuk; Medema, Jan P. FEBS Journal, Vol. 281, Issue 21 https://doi.org/10.1111/febs.13023	journal	September 2014
Integrative Analysis of Complex Cancer Genomics and Clinical Profiles Using the cBioPortal Gao, J.; Aksoy, B. A.; Dogrusoz, U. Science Signaling, Vol. 6, Issue 269 https://doi.org/10.1126/scisignal.2004088	journal	March 2013
Cytochrome C -Mediated Apoptosis Jiang, Xuejun; Wang, Xiaodong Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.073706	journal	June 2004
Oncogenic Kinase–Induced PKM2 Tyrosine 105 Phosphorylation Converts Nononcogenic PKM2 to a Tumor Promoter and Induces Cancer Stem–like Cells Zhou, Zhifen; Li, Min; Zhang, Lin Cancer Research, Vol. 78, Issue 9 https://doi.org/10.1158/0008-5472.CAN-17-2726	journal	February 2018
Cytochrome c Deficiency Confers Apoptosome and Mitochondrial Dysfunction in African-American Men with Prostate Cancer Kumar, Rahul; Bhat, Tariq A.; Walsh, Elise M. Cancer Research, Vol. 79, Issue 7 https://doi.org/10.1158/0008-5472.CAN-18-2383	journal	February 2019
The cBio Cancer Genomics Portal: An Open Platform for Exploring Multidimensional Cancer Genomics Data: Figure 1. Cerami, Ethan; Gao, Jianjiong; Dogrusoz, Ugur Cancer Discovery, Vol. 2, Issue 5 https://doi.org/10.1158/2159-8290.CD-12-0095	journal	May 2012
Acquisition of the Recurrent Gly101Val Mutation in BCL2 Confers Resistance to Venetoclax in Patients with Progressive Chronic Lymphocytic Leukemia Blombery, Piers; Anderson, Mary Ann; Gong, Jia-nan Cancer Discovery, Vol. 9, Issue 3 https://doi.org/10.1158/2159-8290.CD-18-1119	journal	December 2018
BCL2 mutations are associated with increased risk of transformation and shortened survival in follicular lymphoma Correia, Cristina; Schneider, Paula A.; Dai, Haiming Blood, Vol. 125, Issue 4 https://doi.org/10.1182/blood-2014-04-571786	journal	January 2015
Modeling of interaction between cytochrome c and the WD domains of Apaf-1: bifurcated salt bridges underlying apoptosome assembly Shalaeva, Daria N.; Dibrova, Daria V.; Galperin, Michael Y. Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0059-4	journal	May 2015
Regulation of the Apaf-1–caspase-9 apoptosome Bratton, Shawn B.; Salvesen, Guy S. Journal of Cell Science, Vol. 123, Issue 19 https://doi.org/10.1242/jcs.073643	journal	October 2010
A near atomic structure of the active human apoptosome Cheng, Tat Cheung; Hong, Chuan; Akey, Ildikó V. eLife, Vol. 5 https://doi.org/10.7554/eLife.17755	journal	October 2016

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
apoptosome
caspase activation
cytochrome c
mitochondria
nucleotides
tumorigenesis

Title: Molecular insights on cytochrome c and nucleotide regulation of apoptosome function and its implication in cancer

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