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Thioredoxin-Interacting Protein (TXNIP) in Cerebrovascular and Neurodegenerative Diseases: Regulation and Implication

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Abstract

Neurological diseases, including acute attacks (e.g., ischemic stroke) and chronic neurodegenerative diseases (e.g., Alzheimer’s disease), have always been one of the leading cause of morbidity and mortality worldwide. These debilitating diseases represent an enormous disease burden, not only in terms of health suffering but also in economic costs. Although the clinical presentations differ for these diseases, a growing body of evidence suggests that oxidative stress and inflammatory responses in brain tissue significantly contribute to their pathology. However, therapies attempting to prevent oxidative damage or inhibiting inflammation have shown little success. Identification and targeting endogenous “upstream” mediators that normalize such processes will lead to improve therapeutic strategy of these diseases. Thioredoxin-interacting protein (TXNIP) is an endogenous inhibitor of the thioredoxin (TRX) system, a major cellular thiol-reducing and antioxidant system. TXNIP regulating redox/glucose-induced stress and inflammation, now is known to get upregulated in stroke and other brain diseases, and represents a promising therapeutic target. In particular, there is growing evidence that glucose strongly induces TXNIP in multiple cell types, suggesting possible physiological roles of TXNIP in glucose metabolism. Recently, a significant body of literature has supported an essential role of TXNIP in the activation of the NOD-like receptor protein (NLRP3)-inflammasome, a well-established multi-molecular protein complex and a pivotal mediator of sterile inflammation. Accordingly, TXNIP has been postulated to reside centrally in detecting cellular damage and mediating inflammatory responses to tissue injury. The majority of recent studies have shown that pharmacological inhibition or genetic deletion of TXNIP is neuroprotective and able to reduce detrimental aspects of pathology following cerebrovascular and neurodegenerative diseases. Conspicuously, the mainstream of the emerging evidences is highlighting TXNIP link to damaging signals in endothelial cells. Thereby, here, we keep the trend to present the accumulative data on CNS diseases dealing with vascular integrity. This review aims to summarize evidence supporting the significant contribution of regulatory mechanisms of TXNIP with the development of brain diseases, explore pharmacological strategies of targeting TXNIP, and outline obstacles to be considered for efficient clinical translation.

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Abbreviations

AD:

Alzheimer’s disease

AIM2:

Absence in melanoma

AMPK:

AMP-activated protein kinase

ASC:

Apoptosis-associated speck-like

ASK-1:

Apoptosis signal-regulating kinase

BBB:

Blood-brain barrier

Cyt-c:

Cytochrome C

ChREBP:

Carbohydrate response element-binding protein

DAMP:

Damage-associated molecular patterns

DSS:

Disturbed shear stress

ECs:

Endothelial cells

ER:

Endoplasmic reticulum

eMCAO:

Embolic MCAO

FOXO:

Forkhead box transcription factor, class O

GFAP:

Glial fibrillary acidic protein

GLUT:

Glucose transporter

HFD:

High-fat diet

HGD:

High-glucose diet

HUVECs:

Human umbilical vein endothelial cells

HRE:

Human retinal endothelial cells

ICH:

Intracerebral hemorrhage

IL-1β:

Interleukin-1-beta

IRE1α:

Serine/threonine-protein kinase/endoribonuclease

JNK:

c-Jun-N-terminal kinase

KO:

Knockout

KLF-2:

Kruppel-like factor 2

LPS:

Lipopolysaccharide

LRR:

Leucine-rich repeat domain

MAP:

Mitogen-activated protein

MCAO:

Middle cerebral artery occlusion

MI:

Myocardial infarction

MAPK:

Mitogen-activated protein kinase

miRNA:

Microribonucleic acid

MMP-9:

Matrix metalloproteinase 9

MyD-88:

Myeloid differentiation primary response 88

NADPH:

Nicotinamide adenine dinucleotide phosphate-oxidase

NAD:

Nicotinamide adenine dinucleotide phosphate

NADH:

Nicotinamide adenine dinucleotide phosphate

NBD:

Nucleotide-binding domain

NF-κB:

Nuclear factor kappa-B

NLR:

Nucleotide-binding oligomerization domain-like receptor

NLRP:

NOD-like receptor proteins

NMDA:

N-Methyl-D-aspartate

NOD:

Nucleotide-binding oligomerization domain

NOX:

Nicotinamide adenine dinucleotide phosphate oxidase

OGD:

Oxygen glucose deprivation

PAMP:

Pathogen-associated molecular patterns

PERK:

Protein kinase R-like ER kinase

PRR:

Pattern recognition receptor

PTP:

Phospho-tyrosine phosphatases

pVHL:

von Hippel–Lindau protein

RAGE:

Advanced glycation end-products

stz:

Streptozotocin

SAH:

Subarachnoid hemorrhage

SUR1:

Sulfonylurea receptor 1

TLR:

Toll-like receptor

tMCAO:

Transient MCAO

TNF-α:

Tumor necrotizing factor-α

TRX:

Thioredoxin

TXNIP:

Thioredoxin-interacting protein

UPR:

Unfolded protein response

VDUP1:

Vitamin D3 upregulated protein 1

VCAM:

Vascular cell adhesion protein

VEGF:

Vascular endothelial growth factor

WT:

Wild type

ZDF:

Zucker diabetic fatty

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Acknowledgements

Authors would like to thank Ms. Colby Polonsky, Augusta University, Augusta, Georgia, for her assistance with Fig. 1.

Funding

This work was supported by the National Institute of Health [R01-NS097800 (TI)].

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Author notes

  1. Sanaz Nasoohi and Saifudeen Ismael contributed equally to this work.

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee Health Science Center, 855 Monroe Avenue, Wittenborg Bldg, Room-231, Memphis, TN, 38163, USA

    Sanaz Nasoohi, Saifudeen Ismael & Tauheed Ishrat

  2. Neuroscience Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Sanaz Nasoohi & Tauheed Ishrat

  3. Neuroscience Institute, The University of Tennessee Health Science Center, Memphis, TN, USA

    Tauheed Ishrat

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  1. Sanaz Nasoohi
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Nasoohi, S., Ismael, S. & Ishrat, T. Thioredoxin-Interacting Protein (TXNIP) in Cerebrovascular and Neurodegenerative Diseases: Regulation and Implication. Mol Neurobiol 55, 7900–7920 (2018). https://doi.org/10.1007/s12035-018-0917-z

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