Vitamin A Depletion Causes Oxidative Stress, Mitochondrial Dysfunction, and PARP-1-dependent Energy Deprivation

Overview

Journal FASEB J

Specialties Biology
Physiology

Date 2008 Aug 5

PMID 18676402

Citations 41

Authors

Haw-Jyh Chiu

Donald A Fischman

Ulrich Hammerling

Affiliations

Soon will be listed here.

Abstract

A significant unresolved question is how vitamin A deprivation causes, and why retinoic acid fails to reverse, immunodeficiency. When depleted of vitamin A, T cells undergo programmed cell death (PCD), which is enhanced by the natural competitor of retinol, anhydroretinol. PCD does not happen by apoptosis, despite the occurrence of shared early events, including mitochondrial membrane depolarization, permeability transition pore opening, and cytochrome c release. It also lacks caspase-3 activation, chromatin condensation, and endonuclease-mediated DNA degradation, hallmarks of apoptosis. PCD following vitamin A deprivation exhibits increased production of reactive oxygen species (ROS), drastic reductions in ATP and NAD(+) levels, and activation of poly-(ADP-ribose) polymerase (PARP) -1. These latter steps are causative because neutralizing ROS, imposing hypoxic conditions, or inhibiting PARP-1 by genetic or pharmacologic approaches prevents energy depletion and PCD. The data highlight a novel regulatory role of vitamin A in mitochondrial energy homeostasis.

Citing Articles

Differential proteomic profiles between cognitive frail and robust older adults from the MELoR cohort.

Lim S, Ng Y, Majeed A, Tan M, Khor H, Kamaruzzaman S Geroscience. 2024; .

PMID: 39653973 DOI: 10.1007/s11357-024-01462-z.

ROS Chronicles in HIV Infection: Genesis of Oxidative Stress, Associated Pathologies, and Therapeutic Strategies.

Harshithkumar R, Shah P, Jadaun P, Mukherjee A Curr Issues Mol Biol. 2024; 46(8):8852-8873.

PMID: 39194740 PMC: 11352872. DOI: 10.3390/cimb46080523.

Uncommon opsin's retinal isomer is involved in mammalian sperm thermotaxis.

Brandis A, Roy D, Das I, Sheves M, Eisenbach M Sci Rep. 2024; 14(1):10699.

PMID: 38729974 PMC: 11087470. DOI: 10.1038/s41598-024-61488-3.

NLRX1 Inhibits LPS-Induced Microglial Death via Inducing p62-Dependent HO-1 Expression, Inhibiting MLKL and Activating PARP-1.

Huang Y, Huang D, Klochkov V, Chan C, Chen Y, Lin W Antioxidants (Basel). 2024; 13(4).

PMID: 38671928 PMC: 11047433. DOI: 10.3390/antiox13040481.

Microneedles: A novel clinical technology for evaluating skin characteristics.

Kim S, Kim J, Mi Choi Y, Seo S, Jang E, Lee S Skin Res Technol. 2024; 30(3):e13647.

PMID: 38465749 PMC: 10926177. DOI: 10.1111/srt.13647.

References

Takahashi K, Pieper A, Croul S, Zhang J, Snyder S, Greenberg J . Post-treatment with an inhibitor of poly(ADP-ribose) polymerase attenuates cerebral damage in focal ischemia. Brain Res. 1999; 829(1-2):46-54. DOI: 10.1016/s0006-8993(99)01335-9. View

Ha H, Snyder S . Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A. 1999; 96(24):13978-82. PMC: 24176. DOI: 10.1073/pnas.96.24.13978. View

Buck J, Grun F, Derguini F, Chen Y, Kimura S, Noy N . Anhydroretinol: a naturally occurring inhibitor of lymphocyte physiology. J Exp Med. 1993; 178(2):675-80. PMC: 2191109. DOI: 10.1084/jem.178.2.675. View

Smulson M, Simbulan-Rosenthal C, Boulares A, Yakovlev A, Stoica B, Iyer S . Roles of poly(ADP-ribosyl)ation and PARP in apoptosis, DNA repair, genomic stability and functions of p53 and E2F-1. Adv Enzyme Regul. 2000; 40:183-215. DOI: 10.1016/s0065-2571(99)00024-2. View

Korichneva I, Waka J, Hammerling U . Regulation of the cardiac mitochondrial membrane potential by retinoids. J Pharmacol Exp Ther. 2003; 305(2):426-33. DOI: 10.1124/jpet.103.048900. View

Guzy R, Schumacker P . Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol. 2006; 91(5):807-19. DOI: 10.1113/expphysiol.2006.033506. View

Korichneva I, Hoyos B, Chua R, Levi E, Hammerling U . Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J Biol Chem. 2002; 277(46):44327-31. DOI: 10.1074/jbc.M205634200. View

Kim J, Tchernyshyov I, Semenza G, Dang C . HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006; 3(3):177-85. DOI: 10.1016/j.cmet.2006.02.002. View

Lemasters J, Nieminen A, Qian T, Trost L, Elmore S, Nishimura Y . The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta. 1998; 1366(1-2):177-96. DOI: 10.1016/s0005-2728(98)00112-1. View

10.

Miwa M, Masutani M . PolyADP-ribosylation and cancer. Cancer Sci. 2007; 98(10):1528-35. PMC: 11159171. DOI: 10.1111/j.1349-7006.2007.00567.x. View

11.

Chandel N, Maltepe E, GOLDWASSER E, Mathieu C, Simon M, Schumacker P . Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998; 95(20):11715-20. PMC: 21706. DOI: 10.1073/pnas.95.20.11715. View

12.

Cipriani G, Rapizzi E, Vannacci A, Rizzuto R, Moroni F, Chiarugi A . Nuclear poly(ADP-ribose) polymerase-1 rapidly triggers mitochondrial dysfunction. J Biol Chem. 2005; 280(17):17227-34. DOI: 10.1074/jbc.M414526200. View

13.

Derguini F, Nakanishi K, Hammerling U, Chua R, Eppinger T, Levi E . 13,14-Dihydroxy-retinol, a new bioactive retinol metabolite. J Biol Chem. 1995; 270(32):18875-80. DOI: 10.1074/jbc.270.32.18875. View

14.

Hoyos B, Imam A, Chua R, Swenson C, Tong G, Levi E . The cysteine-rich regions of the regulatory domains of Raf and protein kinase C as retinoid receptors. J Exp Med. 2000; 192(6):835-45. PMC: 2193291. DOI: 10.1084/jem.192.6.835. View

15.

Scaduto Jr R, Grotyohann L . Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J. 1999; 76(1 Pt 1):469-77. PMC: 1302536. DOI: 10.1016/S0006-3495(99)77214-0. View

16.

Nishikawa T, Edelstein D, Du X, Yamagishi S, Matsumura T, Kaneda Y . Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000; 404(6779):787-90. DOI: 10.1038/35008121. View

17.

Liu X, Kim C, Yang J, Jemmerson R, Wang X . Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996; 86(1):147-57. DOI: 10.1016/s0092-8674(00)80085-9. View

18.

De Luca L . Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J. 1991; 5(14):2924-33. View

19.

Pieper A, Walles T, Wei G, Clements E, Verma A, Snyder S . Myocardial postischemic injury is reduced by polyADPripose polymerase-1 gene disruption. Mol Med. 2000; 6(4):271-82. PMC: 1949947. View

20.

Yu S, Wang H, Dawson T, Dawson V . Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol Dis. 2003; 14(3):303-17. DOI: 10.1016/j.nbd.2003.08.008. View