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Juan Carlos Gallardo‐Pérez

Instituto Nacional de Cardiología

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Rafael Moreno‐Sánchez

Universidad Nacional Autónoma de México

Sara Rodríguez‐Enríquez

Autonomous University of Tlaxcala

Álvaro Marín‐Hernández

Instituto Nacional de Cardiología

Emma Saavedra

Instituto Nacional de Cardiología

Silvia Cecilia Pacheco-Velázquez

Oregon Health & Science University

Diana Xochiquetzal Robledo‐Cadena

Universidad Nacional Autónoma de México

Ricardo Jasso‐Chávez

Instituto Nacional de Cardiología

Ileana Hernández‐Reséndiz

University Hospital Regensburg

Rusely Encalada

Instituto Nacional de Cardiología

José S. Rodríguez‐Zavala

Instituto Nacional de Cardiología

Cooperative Institutions

Instituto Nacional de Cardiología

Universidad Nacional Autónoma de México

Instituto Nacional de Cardiologia

Instituto Nacional de Cancerología

Instituto Politécnico Nacional

Instituto Nacional de Neurología y Neurocirugía

Center for Research and Advanced Studies of the National Polytechnic Institute

Institute for Social Security and Services for State Workers

Instituto Nacional de Cancerología

Secretaria de Salud

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Phosphofructokinase type 1 kinetics, isoform expression, and gene polymorphisms in cancer cells

Journal of Cellular Biochemistry (2011)

Rafael Moreno‐Sánchez Álvaro Marín‐Hernández Juan Carlos Gallardo‐Pérez Héctor Quezada Rusely Encalada

Kinetic analysis of PFK-1 from rodent AS-30D, and human HeLa and MCF-7 carcinomas revealed sigmoidal [fructose 6-phosphate, Fru6P]-rate curves with different V(m) values when varying the allosteric activator fructose 2,6 bisphosphate (Fru2,6BP), AMP, Pi, NH(4)(+), or K(+). The rate equation that accurately predicted this behavior was the exclusive ligand binding concerted transition model together with non-essential hyperbolic activation. PFK-1 from rat liver and heart also exhibited the mixed cooperative-hyperbolic kinetic behavior regarding activators. Lowering pH induced decreased affinity for Fru6P, Fru2,6BP, citrate, and ATP (as inhibitor); as well as decreased V(m) and increased content of inactive (T) enzyme forms. High K(+) prompted increased (Fru6P) or decreased (activators) affinities; increased V(m); and increased content of active (R) enzyme forms. mRNA expression analysis and nucleotide sequencing showed that the three PFK-1 isoforms L, M, and C are transcribed in the three carcinomas. However, proteomic analysis indicated the predominant expression of L in liver, of M in heart and MCF-7 cells, of L>M in AS-30D cells, and of C in HeLa cells. PFK-1M showed the highest affinities for F6P and citrate and the lowest for ATP (substrate) and F2,6BP; PFK-1L showed the lowest affinity for F6P and the highest for F2,6BP; and PFK-1C exhibited the highest affinity for ATP (substrate) and the lowest for citrate. Thus, the present work documents the kinetic signature of each PFK-1 isoform, and facilitates the understanding of why this enzyme exerts significant or negligible glycolysis flux-control in normal or cancer cells, respectively, and how it regulates the onset of the Pasteur effect.

HeLa

Phosphofructokinase 1

10.1002/jcb.24039

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Citations (54)

Anti-mitochondrial therapy in human breast multi-cellular spheroids

Biochimica et Biophysica Acta (BBA) - Bioenergetics (2012)

Sara Rodríguez‐Enríquez Juan Carlos Gallardo‐Pérez Edna Ayerim Mandujano-Tinoco Rafael Moreno‐Sánchez

Spheroid

10.1016/j.bbabio.2012.06.329

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GPI/AMF inhibition blocks the development of the metastatic phenotype of mature multi-cellular tumor spheroids

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research (2014)

Juan Carlos Gallardo‐Pérez Nadia Alejandra Rivero-Segura Álvaro Marín‐Hernández Rafael Moreno‐Sánchez Sara Rodríguez‐Enríquez

10.1016/j.bbamcr.2014.01.013

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Citations (29)

Canonical and new generation anticancer drugs also target energy metabolism

Archives of Toxicology (2014)

Sara Rodríguez‐Enríquez Juan Carlos Gallardo‐Pérez Ileana Hernández‐Reséndiz Álvaro Marín‐Hernández Silvia Cecilia Pacheco-Velázquez

10.1007/s00204-014-1246-2

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Acetate Promotes a Differential Energy Metabolic Response in Human HCT 116 and COLO 205 Colon Cancer Cells Impacting Cancer Cell Growth and Invasiveness

Frontiers in Oncology (2021)

Sara Rodríguez‐Enríquez Diana Xochiquetzal Robledo‐Cadena Juan Carlos Gallardo‐Pérez Silvia Cecilia Pacheco-Velázquez Citlali Vázquez

Under dysbiosis, a gut metabolic disorder, short-chain carboxylic acids (SCCAs) are secreted to the lumen, affecting colorectal cancer (CRC) development. Butyrate and propionate act as CRC growth inhibitors, but they might also serve as carbon source. In turn, the roles of acetate as metabolic fuel and protein acetylation promoter have not been clearly elucidated. To assess whether acetate favors CRC growth through active mitochondrial catabolism, a systematic study evaluating acetate thiokinase (AcK), energy metabolism, cell proliferation, and invasiveness was performed in two CRC cell lines incubated with physiological SCCAs concentrations. In COLO 205, acetate (+glucose) increased the cell density (50%), mitochondrial protein content (3–10 times), 2-OGDH acetylation, and oxidative phosphorylation (OxPhos) flux (36%), whereas glycolysis remained unchanged vs. glucose-cultured cells; the acetate-induced OxPhos activation correlated with a high AcK activity, content, and acetylation (1.5–6-fold). In contrast, acetate showed no effect on HCT116 cell growth, OxPhos, AcK activity, protein content, and acetylation. However, a substantial increment in the HIF-1α content, HIF-1α-glycolytic protein targets (1–2.3 times), and glycolytic flux (64%) was observed. Butyrate and propionate decreased the growth of both CRC cells by impairing OxPhos flux through mitophagy and mitochondrial fragmentation activation. It is described, for the first time, the role of acetate as metabolic fuel for ATP supply in CRC COLO 205 cells to sustain proliferation, aside from its well-known role as protein epigenetic regulator. The level of AcK determined in COLO 205 cells was similar to that found in human CRC biopsies, showing its potential role as metabolic marker.

10.3389/fonc.2021.697408

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Regulatory role of acetylation on enzyme activity and fluxes of energy metabolism pathways

Biochimica et Biophysica Acta (BBA) - General Subjects (2021)

Rafael Moreno‐Sánchez Juan Carlos Gallardo‐Pérez Silvia Cecilia Pacheco-Velázquez Diana Xochiquetzal Robledo‐Cadena Sara Rodríguez‐Enríquez

10.1016/j.bbagen.2021.130021

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Non-Steroidal Anti-Inflammatory Drugs Increase Cisplatin, Paclitaxel, and Doxorubicin Efficacy against Human Cervix Cancer Cells

Pharmaceuticals (2020)

Diana Xochiquetzal Robledo‐Cadena Juan Carlos Gallardo‐Pérez Víctor Manuel Dávila‐Borja Silvia Cecilia Pacheco-Velázquez Javier Belmont-Díaz

This study shows that the non-steroidal anti-inflammatory drug (NSAID) celecoxib and its non-cyclooxygenase-2 (COX2) analogue dimethylcelecoxib (DMC) exert a potent inhibitory effect on the growth of human cervix HeLa multi-cellular tumor spheroids (MCTS) when added either at the beginning (“preventive protocol”; IC50 = 1 ± 0.3 nM for celecoxib and 10 ± 2 nM for DMC) or after spheroid formation (“curative protocol”; IC50 = 7.5 ± 2 µM for celecoxib and 32 ± 10 µM for DMC). These NSAID IC50 values were significantly lower than those attained in bidimensional HeLa cells (IC50 = 55 ± 9 µM celecoxib and 48 ± 2 µM DMC) and bidimensional non-cancer cell cultures (3T3 fibroblasts and MCF-10A mammary gland cells with IC50 from 69 to >100 µM, after 24 h). The copper-based drug casiopeina II-gly showed similar potency against HeLa MCTS. Synergism analysis showed that celecoxib, DMC, and casiopeinaII-gly at sub-IC50 doses increased the potency of cisplatin, paclitaxel, and doxorubicin to hinder HeLa cell proliferation through a significant abolishment of oxidative phosphorylation in bidimensional cultures, with no apparent effect on non-cancer cells (therapeutic index >3.6). Similar results were attained with bidimensional human cervix cancer SiHa and human glioblastoma U373 cell cultures. In HeLa MCTS, celecoxib, DMC and casiopeina II-gly increased cisplatin toxicity by 41–85%. These observations indicated that celecoxib and DMC used as adjuvant therapy in combination with canonical anti-cancer drugs may provide more effective alternatives for cancer treatment.

Celecoxib

HeLa

IC50

10.3390/ph13120463

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Citations (38)

Oxidative phosphorylation is impaired by prolonged hypoxia in breast and possibly in cervix carcinoma

The International Journal of Biochemistry & Cell Biology (2010)

Sara Rodríguez‐Enríquez Liliana Carreño‐Fuentes Juan Carlos Gallardo‐Pérez Emma Saavedra Héctor Quezada

Hypoxia

HeLa

10.1016/j.biocel.2010.07.010

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Citations (130)

The nutritional status of Methanosarcina acetivorans regulates glycogen metabolism and gluconeogenesis and glycolysis fluxes

FEBS Journal (2016)

Michel Geovanni Santiago‐Martínez Rusely Encalada Elizabeth Lira‐Silva Erika Pineda Juan Carlos Gallardo‐Pérez

Gluconeogenesis is an essential pathway in methanogens because they are unable to use exogenous hexoses as carbon source for cell growth. With the aim of understanding the regulatory mechanisms of central carbon metabolism in Methanosarcina acetivorans, the present study investigated gene expression, the activities and metabolic regulation of key enzymes, metabolite contents and fluxes of gluconeogenesis, as well as glycolysis and glycogen synthesis/degradation pathways. Cells were grown with methanol as a carbon source. Key enzymes were kinetically characterized at physiological pH/temperature. Active consumption of methanol during exponential cell growth correlated with significant methanogenesis, gluconeogenic flux and steady glycogen synthesis. After methanol exhaustion, cells reached the stationary growth phase, which correlated with the rise in glycogen consumption and glycolytic flux, decreased methanogenesis, negligible acetate production and an absence of gluconeogenesis. Elevated activities of carbon monoxide dehydrogenase/acetyl-CoA synthetase complex and pyruvate: ferredoxin oxidoreductase suggested the generation of acetyl-CoA and pyruvate for glycogen synthesis. In the early stationary growth phase, the transcript contents and activities of pyruvate phosphate dikinase, fructose 1,6-bisphosphatase and glycogen synthase decreased, whereas those of glycogen phosphorylase, ADP-phosphofructokinase and pyruvate kinase increased. Therefore, glycogen and gluconeogenic metabolites were synthesized when an external carbon source was provided. Once such a carbon source became depleted, glycolysis and methanogenesis fed by glycogen degradation provided the ATP supply. Weak inhibition of key enzymes by metabolites suggested that the pathways evaluated were mainly transcriptionally regulated. Because glycogen metabolism and glycolysis/gluconeogenesis are not present in all methanogens, the overall data suggest that glycogen storage might represent an environmental advantage for methanosarcinales when carbon sources are scarce. Also, the understanding of the central carbohydrate metabolism in methanosarcinales may help to optimize methane production.

Gluconeogenesis

10.1111/febs.13717

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NAC partially prevents mitochondrial impairment and oxidative stress in cardiac cells induced by the administration of extracellular vesicles derived from nephrectomy 5/6 rats

Biochimica et Biophysica Acta (BBA) - Bioenergetics (2024)

Omar Emiliano Aparicio‐Trejo Emilo Sanchez-Flores Edilia Tapia Marisol Orozco‐Ibarra Juan Carlos Gallardo‐Pérez

Extracellular Vesicles

10.1016/j.bbabio.2024.149366

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