S-Nitrosoglutathione Attenuates Oxidative Stress and Improves Retention Memory Dysfunctions in Intra-Cerebroventricular-Streptozotocin Rat Model of Sporadic Alzheimer’s Disease via Activation of BDNF and Nuclear Factor Erythroid 2-Related Factor-2 Antioxidant Signaling Pathway

3.

Dubey

H

,

Gulati

K

,

Ray

A

.

Recent studies on cellular and molecular mechanisms in Alzheimer’s disease: focus on epigenetic factors and histone deacetylase

.

Rev Neurosci

.

2018

;

29

(

3

):

241

–

60

.

4.

Dubey

H

,

Gulati

K

,

Ray

A

.

Amelioration by nitric oxide (NO) mimetics on neurobehavioral and biochemical changes in experimental model of Alzheimer’s disease in rats

.

Neurotoxicology

.

2018

;

66

:

58

–

65

.

5.

Murphy

KE

,

Park

JJ

.

Can co-activation of Nrf2 and neurotrophic signaling pathway slow Alzheimer’s disease

.

Int J Mol Sci

.

2017

;

18

(

6

):

1168

.

6.

Gan

L

,

Johnson

JA

.

Oxidative damage and the Nrf2-ARE pathway in neurodegenerative diseases

.

Biochim Biophys Acta

.

2014

;

1842

(

8

):

1208

–

18

.

7.

Lu

MC

,

Ji

JA

,

Jiang

YL

,

Chen

ZY

,

Yuan

ZW

,

You

QD

, et al.

An inhibitor of the Keap1-Nrf2 protein-protein interaction protects NCM460 colonic cells and alleviates experimental colitis

.

Sci Rep

.

2016

;

6

:

26585

.

8.

Harvey

CJ

,

Thimmulappa

RK

,

Singh

A

,

Blake

DJ

,

Ling

G

,

Wakabayashi

N

, et al.

Nrf2-regulated glutathione recycling independent of biosynthesis is critical for cell survival during oxidative stress

.

Free Radic Biol Med

.

2009

;

46

(

4

):

443

–

53

.

9.

Gella

A

,

Durany

N

.

Oxidative stress in Alzheimer disease

.

Cell Adh Migr

.

2009

;

3

(

1

):

88

–

93

.

10.

Dubey

H

,

Gulati

K

,

Ray

A

.

Journal of pharmacological reports effects of nitric oxide ( NO ) modulators on cognitive function and brain oxidative stress in experimental model of alzheimer’s disease in rats

.

2017

;

2

(

2

).

11.

Yao

W

,

Zhang

JC

,

Ishima

T

,

Dong

C

,

Yang

C

,

Ren

Q

, et al.

Role of Keap1-Nrf2 signaling in depression and dietary intake of glucoraphanin confers stress resilience in mice

.

Sci Rep

.

2016

;

6

:

30659

.

12.

Nagahara

AH

,

Merrill

DA

,

Coppola

G

,

Tsukada

S

,

Schroeder

BE

,

Shaked

GM

, et al.

Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer’s disease

.

Nat Med

.

2009

;

15

(

3

):

331

–

7

.

13.

Zhang

T

,

Pan

B

,

Zhao

B

,

Zhang

L

,

Huang

YL

,

Sun

FY

.

Exacerbation of poststroke dementia by type 2 diabetes IS associated with synergIStic increases of -secretase activation and -amyloid generation in rat brains

.

NSC

.

2009

;

161

(

4

):

1045

–

56

.

14.

Wang

J

,

Zhao

X

,

He

M

.

Is BDNF biological link between depression and type 2 diabetes mellitus

.

Med Hypotheses

.

2012

;

79

(

2

):

255

–

8

.

15.

Xu

P

,

Wang

K

,

Lu

C

,

Dong

L

,

Gao

L

,

Yan

M

, et al.

The protective effect of lavender essential oil and its main component linalool against the cognitive deficits induced by D-galactose and aluminum trichloride in mice

.

Evid Based Complement Alternat Med

.

2017

;

2017

:

7426538

.

16.

Paul

V

,

Ekambaram

P

.

Involvement of nitric oxide in learning & memory processes

.

Indian J Med Res

.

2011

;

133

(

5

):

471

–

8

.

17.

Huang

CC

,

Lin

TJ

,

Lu

YF

,

Chen

CC

,

Huang

CY

,

Lin

WT

.

Protective effects of L-arginine supplementation against exhaustive exercise-induced oxidative stress in young rat tissues

.

Chin J Physiol

.

2009

;

52

(

5

):

306

–

15

.

18.

Biojone

C

,

Casarotto

P

,

Joca

S

,

Castren

E

.

Interplay between nitric oxide and brain-derived neurotrophic factor in neuronal plasticity

.

CNS Neurol Disord Drug Targets

.

2015

;

14

(

8

):

979

–

87

.

19.

Tian

N

,

Cao

Z

,

Zhang

Y

.

MiR-206 decreases brain-derived neurotrophic factor levels in a transgenic mouse model of Alzheimer’s disease

.

Neurosci Bull

.

2014

;

30

(

2

):

191

–

7

.

20.

Um

HC

,

Jang

JH

,

Kim

DH

,

Lee

C

,

Surh

YJ

.

Nitric oxide activates Nrf2 through S-nitrosylation of Keap1 in PC12 cells

.

Nitric Oxide

.

2011

;

25

(

2

):

161

–

8

.

21.

Calabrese

V

,

Mancuso

C

,

Calvani

M

,

Rizzarelli

E

,

Butterfield

DA

,

Stella

AMG

.

Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity

.

Nat Rev Neurosci

.

2007

;

8

(

10

):

766

–

75

.

22.

Rosas-Vidal

LE

,

Do-Monte

FH

,

Sotres-Bayon

F

,

Quirk

GJ

.

Hippocampal-prefrontal BDNF and memory for fear extinction

.

Neuropsychopharmacology

.

2014

;

39

(

9

):

2161

–

9

.

23.

Heldt

SA

,

Stanek

L

,

Chhatwal

JP

,

Ressler

KJ

.

Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories

.

Mol Psychiatry

.

2007

;

12

(

7

):

656

–

70

.

24.

Herry

C

,

Ferraguti

F

,

Singewald

N

,

Letzkus

JJ

,

Ehrlich

I

,

Lüthi

A

.

Neuronal circuits of fear extinction

.

Eur J Neurosci

.

2010

;

31

(

4

):

599

–

612

.

25.

Lonsdorf

TB

,

Haaker

J

,

Kalisch

R

.

Long-term expression of human contextual fear and extinction memories involves amygdala, hippocampus and ventromedial prefrontal cortex: a reinstatement study in two independent samples

.

Soc Cogn Affect Neurosci

.

2014

;

9

(

12

):

1973

–

83

.

26.

Huff

NC

,

Rudy

JW

.

The amygdala modulates hippocampus-dependent context memory formation and stores cue-shock associations

.

Behav Neurosci

.

2004

;

118

(

1

):

53

–

62

.

27.

Broniowska

KA

,

Diers

AR

,

Hogg

N

.

S-Nitrosoglutathione

.

Biochim Biophys Acta

.

2013

;

1830

(

5

):

3173

–

81

.

28.

Khan

M

,

Sakakima

H

,

Dhammu

TS

,

Shunmugavel

A

,

Im

Y-B

,

Gilg

AG

, et al.

S-Nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats

.

J Neuroinflammation

.

2011

;

8

(

1

):

78

.

29.

Paxinos

G

,

Watson

C

.

The rat brain in stereotaxic coordinates

. 7th ed.

Elsevier Academic Press

;

2014

; p.

170

.

30.

Ozkay

UD

,

Can

OD

,

Ozkay

Y

,

Oztürk

Y

.

Effect of benzothiazole/piperazine derivatives on intracerebroventricular streptozotocin-induced cognitive deficits

.

Pharmacol Rep

.

2012

;

64

(

4

):

834

–

47

.

31.

Ishrat

T

,

Parveen

K

,

Khan

MM

,

Khuwaja

G

,

Khan

MB

,

Yousuf

S

, et al.

Selenium prevents cognitive decline and oxidative damage in rat model of streptozotocin-induced experimental dementia of Alzheimer’s type

.

Brain Res

.

2009

;

1281

:

117

–

27

.

32.

Tiwari

S

,

Singh

S

.

Reciprocal upshot of nitric oxide, endoplasmic reticulum stress, and ubiquitin proteasome system in Parkinson’s disease pathology

.

Neuroscientist

.

2021

;

27

(

4

):

340

–

54

.

33.

Wang

H

,

Wang

H

,

Cheng

H

,

Che

Z

.

Ameliorating effect of luteolin on memory impairment in an Alzheimer’s disease model

.

Mol Med Rep

.

2016

;

13

(

5

):

4215

–

20

.

34.

Won

J-S

,

Kim

J

,

Annamalai

B

,

Shunmugavel

A

,

Singh

I

,

Singh

AK

.

Protective role of S-nitrosoglutathione (GSNO) against cognitive impairment in rat model of chronic cerebral hypoperfusion

.

J Alzheimers Dis

.

2013

;

34

(

3

):

621

–

35

.

35.

Salkovic-Petrisic

M

,

Knezovic

A

,

Hoyer

S

,

Riederer

P

.

What have we learned from the streptozotocin-induced animal model of sporadic Alzheimer’s disease, about the therapeutic strategies in Alzheimer’s research

.

J Neural Transm

.

2013

;

120

(

1

):

233

–

52

.

36.

Morris

R

.

Developments of a water-maze procedure for studying spatial learning in the rat

.

J Neurosci Methods

.

1984

;

11

(

1

):

47

–

60

.

37.

Dubey

H

,

Dubey

A

,

Gulati

K

,

Ray

A

.

Protective effects of L-arginine on cognitive deficits and biochemical parameters in an experimental model of type-2 diabetes mellitus induced Alzheimer’s disease in rats

.

J Physiol Pharmacol

.

2022

;

73

(

1

):

3

–

17

.

38.

Qosa

H

,

Mohamed

LA

,

Batarseh

YS

,

Alqahtani

S

,

Ibrahim

B

,

LeVine

H

3rd, et al.

Extra-virgin olive oil attenuates amyloid-β and tau pathologies in the brains of TgSwDI mice

.

J Nutr Biochem

.

2015

;

26

(

12

):

1479

–

90

. H.

39.

Park

SA

,

Chevallier

N

,

Tejwani

K

,

Hung

MM

,

Maruyama

H

,

Golde

TE

, et al.

Deficiency in either COX-1 or COX-2 genes does not affect amyloid beta protein burden in amyloid precursor protein transgenic mice

.

Biochem Biophys Res Commun

.

2016

;

478

(

1

):

286

–

92

.

40.

Dubey

H

,

Dubey

A

,

Gulati

K

,

Ray

A

.

S-nitrosoglutathione modulates HDAC2 and BDNF levels in the brain and improves cognitive deficits in experimental model of Alzheimer’s disease in rats

;

2022

.

41.

Malinski

T

.

Nitric oxide and nitroxidative stress in Alzheimer’s disease

.

J Alzheimers Dis

.

2007

;

11

(

2

):

207

–

18

.

42.

Dubey

H

,

Gulati

K

,

Ray

A

.

Alzheimer’s disease: a contextual link with nitric oxide synthase

.

Curr Mol Med

.

2020

;

20

(

7

):

505

–

15

.

43.

Tropea

MR

,

Gulisano

W

,

Vacanti

V

,

Arancio

O

,

Puzzo

D

,

Palmeri

A

.

Nitric oxide/cGMP/CREB pathway and amyloid-beta crosstalk: from physiology to Alzheimer’s disease

.

Free Radic Biol Med

.

2022

;

193

(

Pt 2

):

657

–

68

.

44.

Ozkay

UD

,

Can

ÖD

,

Ozkay

Y

,

Oztürk

Y

.

Effect of benzothiazole/piperazine derivatives on intracerebroventricular streptozotocin-induced cognitive deficits

.

Pharmacol Rep

.

2012

;

64

(

4

):

834

–

47

.

45.

Ishrat

T

,

Khan

MB

,

Hoda

MN

,

Yousuf

S

,

Ahmad

M

,

Ansari

MA

, et al.

Coenzyme Q10 modulates cognitive impairment against intracerebroventricular injection of streptozotocin in rats

.

Behav Brain Res

.

2006

;

171

(

1

):

9

–

16

.

46.

Agrawal

R

,

Mishra

B

,

Tyagi

E

,

Nath

C

,

Shukla

R

.

Effect of curcumin on brain insulin receptors and memory functions in STZ (ICV) induced dementia model of rat

.

Pharmacol Res

.

2010

;

61

(

3

):

247

–

52

.

47.

Tota

S

,

Kamat

PK

,

Saxena

G

,

Hanif

K

,

Najmi

AK

,

Nath

C

.

Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats

.

Behav Brain Res

.

2012

;

226

(

1

):

317

–

30

.

48.

Rajasekar

N

,

Dwivedi

S

,

Nath

C

,

Hanif

K

,

Shukla

R

.

Protection of streptozotocin induced insulin receptor dysfunction, neuroinflammation and amyloidogenesis in astrocytes by insulin

.

Neuropharmacology

.

2014

;

86

:

337

–

52

.

49.

Giasson

BI

,

Ischiropoulos

H

,

Lee

VMY

,

Trojanowski

JQ

.

The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer’s and Parkinson’s diseases

.

Free Radic Biol Med

.

2002

;

32

(

12

):

1264

–

75

.

50.

Ju

TC

,

Chen

S

,

Liu

CC

,

Yang

DI

.

Protective effects of S-nitrosoglutathione against amyloid beta-peptide neurotoxicity

.

Free Radic Biol Med

.

2005

;

38

(

7

):

938

–

49

.

51.

Javed

H

,

Khan

MM

,

Khan

A

,

Vaibhav

K

,

Ahmad

A

,

Khuwaja

G

, et al.

S-allyl cysteine attenuates oxidative stress associated cognitive impairment and neurodegeneration in mouse model of streptozotocin-induced experimental dementia of Alzheimer’s type

.

Brain Res

.

2011

;

1389

:

133

–

42

.

52.

Bliss

TVP

,

Collingridge

GL

.

A synaptic model of memory: long-term potentiation in the hippocampus

.

Nature

.

1993

;

361

(

6407

):

31

–

9

.

53.

Takeuchi

T

,

Duszkiewicz

AJ

,

Morris

RGM

.

The synaptic plasticity and memory hypothesis: encoding, storage and persistence

.

Philos Trans R Soc Lond B Biol Sci

.

2014

;

369

(

1633

):

20130288

.

54.

Ying

SW

,

Futter

M

,

Rosenblum

K

,

Webber

MJ

,

Hunt

SP

,

Bliss

TVP

, et al.

Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis

.

J Neurosci

.

2002

;

22

(

5

):

1532

–

40

.

55.

Manabe

T

.

Neurobiology: does BDNF have pre- or postsynaptic targets

.

Science

.

2002

;

2002

;

1651

–

1653

.

56.

Wiltgen

BJ

,

Brown

RAM

,

Talton

LE

,

Silva

AJ

.

New circuits for old memories: the role of the neocortex in consolidation

.

Neuron

.

2004

;

44

(

1

):

101

–

8

.

57.

Yavas

E

,

Gonzalez

S

,

Fanselow

MS

.

Interactions between the hippocampus, prefrontal cortex, and amygdala support complex learning and memory [version 1; peer review: 3 approved]

.

F1000Res

.

2019

;

8

:

F1000 Faculty Rev-1292

.

58.

Kim

JJ

,

Fanselow

MS

.

Modality-specific retrograde amnesia of fear

.

Science

.

1992

;

256

(

5057

):

675

–

7

.

59.

D’Hooge

R

,

De Deyn

PP

.

Applications of the Morris water maze in the study of learning and memory

.

Brain Res Rev

.

2001

;

36

(

1

):

60

–

90

.

60.

Lombroso

PJ

,

Ogren

MP

.

Learning and memory, Part I: brain regions involved in two types of learning and memory

.

J Am Acad Child Adolesc Psychiatry

.

2008

;

47

(

11

):

1228

–

32

.

61.

Cheignon

C

,

Tomas

M

,

Bonnefont-Rousselot

D

,

Faller

P

,

Hureau

C

,

Collin

F

.

Oxidative stress and the amyloid beta peptide in Alzheimer’s disease

.

Redox Biol

.

2018

;

14

:

450

–

64

.

62.

Tamagno

E

,

Guglielmotto

M

,

Vasciaveo

V

,

Tabaton

M

.

Oxidative stress and beta amyloid in alzheimer’s disease. Which comes first: the chicken or the egg

.

Antioxidants

.

2021

;

10

(

9

):

1479

.

63.

Nazem

A

,

Sankowski

R

,

Bacher

M

,

Al-Abed

Y

.

Rodent models of neuroinflammation for Alzheimer’s disease

.

J Neuroinflammation

.

2015

;

12

(

1

):

74

.

64.

Grieb

P

.

Intracerebroventricular streptozotocin injections as a model of Alzheimer???s disease: in search of a relevant mechanism

.

Mol Neurobiol

.

2016

;

53

(

3

):

1741

–

52

.

65.

Rauhala

P

,

Lin

M

,

Chiueh

CC

.

Neuroprotection by S-nitrosoglutathione of brain dopamine neurons from oxidative stress

.

FASEB J

.

1998

;

12

(

2

):

165

–

73

.

66.

Jiao

SS

,

Shen

LL

,

Zhu

C

,

Bu

XL

,

Liu

YH

,

Liu

CH

, et al.

Brain-derived neurotrophic factor protects against tau-related neurodegeneration of Alzheimer’s disease

.

Transl Psychiatry

.

2016

;

6

(

10

):

e907

.

67.

Sutherland

RD

,

Martinez

HE

,

Guynes

WA

,

Miller

L

.

Postoperative chest wound infections in patients requiring coronary bypass

.

J Thorac Cardiovasc Surg

.

1977

;

73

(

6

):

944

–

7

.

68.

Tiwari

V

,

Mishra

A

,

Singh

S

,

Mishra

SK

,

Sahu

KK

,

Parul

, et al.

Protriptyline improves spatial memory and reduces oxidative damage by regulating NFκB-BDNF/CREB signaling axis in streptozotocin-induced rat model of Alzheimer’s disease

.

Brain Res

.

2021

;

1754

:

147261

.

69.

Valvassori

SS

,

Arent

CO

,

Steckert

AV

,

Varela

RB

,

Jornada

LK

,

Tonin

PT

, et al.

Intracerebral administration of BDNF protects rat brain against oxidative stress induced by ouabain in an animal model of mania

.

Mol Neurobiol

.

2015

;

52

(

1

):

353

–

62

.

70.

Airaki

M

,

Sánchez-Moreno

L

,

Leterrier

M

,

Barroso

JB

,

Palma

JM

,

Corpas

FJ

.

Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS

.

Plant Cell Physiol

.

2011

;

52

(

11

):

2006

–

15

.

71.

Khan

M

,

Shunmugavel

A

,

Dhammu

TS

,

Khan

H

,

Singh

I

,

Singh

AK

.

Combined treatment with GSNO and CAPE accelerates functional recovery via additive antioxidant activities in a mouse model of TBI

.

J Neurosci Res

.

2018

;

96

(

12

):

1900

–

13

.

72.

He

T

,

Katusic

ZS

.

Brain-derived neurotrophic factor increases expression of MnSOD in human circulating angiogenic cells

.

Microvasc Res

.

2012

;

83

(

3

):

366

–

71

.

73.

Cheng

A

,

Wang

S

,

Cai

J

,

Rao

MS

,

Mattson

MP

.

Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain

.

Dev Biol

.

2003

;

258

(

2

):

319

–

33

.

74.

Chen

MJ

,

Ivy

AS

,

Russo-Neustadt

AA

.

Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 3′ kinase expression

.

Brain Res Bull

.

2006

;

68

(

4

):

257

–

68

.

75.

Butterfield

DA

,

Swomley

AM

,

Sultana

R

.

Amyloid β-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression

.

Antioxid Redox Signal

.

2013

;

19

(

8

):

823

–

35

.

76.

Wruck

CJ

,

Götz

ME

,

Herdegen

T

,

Varoga

D

,

Brandenburg

LO

,

Pufe

T

.

Kavalactones protect neural cells against amyloid beta peptide-induced neurotoxicity via extracellular signal-regulated kinase 1/2-dependent nuclear factor erythroid 2-related factor 2 activation

.

Mol Pharmacol

.

2008

;

73

(

6

):

1785

–

95

.

77.

Dhakshinamoorthy

S

,

Porter

AG

.

Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells

.

J Biol Chem

.

2004

;

279

(

19

):

20096

–

107

.

78.

Mitre

M

,

Mariga

A

,

Chao

MV

.

Neurotrophin signalling: novel insights into mechanisms and pathophysiology

.

Clin Sci

.

2017

;

131

(

1

):

13

–

23

.

79.

Gupta

VK

,

You

Y

,

Gupta

VB

,

Klistorner

A

,

Graham

SL

.

TrkB receptor signalling: implications in neurodegenerative, psychiatric and proliferative disorders

.

Int J Mol Sci

.

2013

;

14

(

5

):

10122

–

42

.

80.

Bouvier

E

,

Brouillard

F

,

Molet

J

,

Claverie

D

,

Cabungcal

JH

,

Cresto

N

, et al.

Nrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression

.

Mol Psychiatry

.

2017

;

22

(

12

):

1701

–

13

.

81.

Yao

W

,

Lin

S

,

Su

J

,

Cao

Q

,

Chen

Y

,

Chen

J

, et al.

Activation of BDNF by transcription factor Nrf2 contributes to antidepressant-like actions in rodents

.

Transl Psychiatry

.

2021

;

11

(

1

):

140

.

82.

Balez

R

,

Ooi

L

.

Getting to NO Alzheimer’s disease: neuroprotection versus neurotoxicity mediated by nitric oxide

.

Oxid Med Cell Longev

.

2016

;

2016

:

3806157

.