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Global Analysis of Tyrosine Nitration

Protein tyrosine nitration alters the bioactivity of a protein and plays important roles in multiple cellular, physiological, and pathological processes [62-64]. Clarification of endogenous tyrosine nitration at the proteome level under different pathophysiological conditions would elucidate the biological functions and roles of tyrosine nitration in pathology. The global proteomic methods for the identification of nitrated proteins (Table 5.1) mainly include

Table 5.1 Identification of in vivo nitrotyrosine-containing proteins in different pathological conditions.

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

(i) Inflammation-related disease

Ghosh et al. [65]

Lung tissues from allergen- induced murine model of asthma

2D western blot and LC-ESI-MS/MS

Twenty-seven putative nitrated proteins were identified

Inflammation- related disease. No nitrotyrosine sites were identified

Lanone

et al. [66]

Rectus abdominis muscle from the same contro and septic patients

Western blot, MALDI- TOF-PMF, and molecular modeling l

Inducible nitric oxide synthase (iNOS) was nitrated at Tyr299, Tyr336, Tyr446, and Tyr698

Analysis coupled with iNOS threedimensional crystal model

Chatterjee

et al. [67]

Spleens from

LPS-induced

systemic

inflammation

model of

C57BL6/

J mice

1D western blot and LC-ESI-MS/MS

Carboxypeptide B1 (CPB1) was nitrated at specific tyrosine sites

Inflammation- related disease

Dhiman

et al. [68]

Plasma from patients with Chagas' disease

1D and 2D western blot, MALDI-PMF, and LC-ESI-MS/MS

Fifty differentially expressed/ nitrated proteins were identified

Inflammation- related disease. No nitrotyrosine sites were identified

Ghesquiere et al. [48]

Serum proteome from a C57BL6/J mouse with septic shock

COFRADIC and ESI-MS

a2-Macroglobulin, apolipoprotein A-I, haptoglobin, and vitamin D-binding protein were nitrated at 6 specific tyrosine sites

Inflammation- related disease. Nitrotyrosine sites were identified

Table 5.1 (Continued)

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

(ii) Aging and aging-related diseases

Sharov

et al. [69]

Skeletal muscle from 6-month-old and 34-month- old Fisher 344/Brown Norway F1 hybrid rats

1D western blot and HPLC-ESI-MS/MS

Phosphorylase b was found in the accumulation of 3-nitrotyrosine on Tyr113, Tyr161, and Tyr573. Nitration on Tyr 113 was detected in 6- and 34-month-old rat; nitration on Tyr161 and Tyr573 was detected only in 34-month-old rat

Endogenous. Nitration is accumulated with aging

L

Kanski, Hong, and Schoneich

[70]

Skeletal

muscle from

34-month-old

Fisher

344/Brown

Norway

F1 rats

IEF, 1D western blot, and ESI-MS/MS

Eleven

nitroproteins and 12 nitrotyrosine sites were identified

Endogenous

Marshall et al. [71]

Liver from young(19-22 weeks) and old (24 months) C57/BL6 male mice

1D western blot and LC-ESI-MS/MS

Six putative nitrated proteins were identified

Nitration is associated with aging. No nitrotyrosine site was identified

Kanski

et al. [72]

Heart from 5- and 26- month-old Fisher 344/BN F1 hybrid rats

1D and 2D western blot, ESI-MS/MS

Forty-eight putative nitrated proteins. Nitration at Tyr105 of the electron transfer flavoprotein was identified

Endogenous. Heart homogenate and heart

mitochondria. Nitration is the effect of biological aging. Not every protein was identified in its nitrotyrosine site

(iii) Tumor

Nakagawa et al.[73]

C6 rat glioma cell line

HPLC, MALDI-PMF

Cytochrome c was nitrated at Tyr 48, Tyr67, and Tyr74

In vitro nitrated with peroxynitrite

(Continued )

Table 5.1 (Continued)

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

Fiore

et al. [74]

Human glioma tissues

Immunohistochemistry,

1DE-MALDI-PMF

Tubulin was nitrated at Tyr224 in glioma grade IV but not in grade I and noncancerous brain tissue

Endogenous.

Laser-induced

decomposition

Zhan and Desiderio [1]

Human

pituitary

postmortem

tissue

2D western blot and vMALDI-MS/MS

Four nitroproteins and 4 nitrotyrosine sites were identified

Endogenous.

Laser-induced

decomposition

Zhan and Desiderio

[75]

Human

pituitary

postmortem

tissue

2D western blot and vMALDI-MS/MS

Four

nitroproteins

and

4 nitrotyrosine sites were identified

Endogenous.

Laser-induced

decomposition

Zhan and Desiderio

[2]

Human

nonfunctional

pituitary

adenoma

tissue

NTAC-

vMALDI-MS/MS

Nine nitroproteins, 10 nitrotyrosine sites, and 3 nitroprotein- interacting proteins were identified

Endogenous.

Laser-induced

decomposition

(iv) Neurodegenerative diseases

Sacksteder

et al. [76]

Brain from

C57BL/6J

mice

SCX-LC-ESI-MS/MS

Twenty-nine nitroproteins and 31 nitrotyrosine sites

Endogenous.

Links to

neurodegenerative

disease

Zhang et al. [78]

Brain from C57BL/6J mice

LC-ESI-MS/MS

Endogenous

Danielson

et al. [79]

Dox-inducible MAO-B PC12 cells

LC-ESI-MS/MS

a-synuclein was nitrated at Tyr39

Model of

Parkinson's

disease

Casoni et al. [80]

Spinal cord from Tg SOD1 G93A mice and Tg SOD1 WT mice

2D western blot and MALDI-PMF

Thirty-two nitroproteins and 16 nitrotyrosine sites

Endogenous.

Laser-induced

decomposition.

Familial

amyotrophic lateral sclerosis

Yoon et al. [81]

Mouse hippocampal cell line HT22

2D western blot and MALDI-PMF

Thirteen nitroproteins were detected

Glutamate- treated HT22 cells

Table 5.1 (Continued)

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

(v) Cardiovascular system and related diseases

Liu

et al. [82]

Male

C57BL/6 mice

myocardial

ischemia-

reperfusion

injury

(I/R) model

1D or 2D western blot, LC-ESI-MS/MS

Twenty-three nitroproteins were identified. Ten of them were from mitochondria

Endogenous. No nitrotyrosine sites were identified

Chen et al. [84]

Sprague Dawley rat in vivo myocardial regional ischemia- reperfusion model

1DE-LC-ESI-MS/MS

Flavin subunit is nitrated at Tyr56 and Tyr142

Endogenous. Mitochondrial complex II in the postischemic myocardium

Ai et al. [85

] Endothelial cell of human coronary arteries

LC-ESI-MS/MS

LDL was nitrated

(vi) The neurovisual system

Justilien

et al. [86]

Mouse

posterior

eyecups

NTAC, SDS-PAGE, LC-ESI-MS/MS

Eight nitroproteins and nine nitrotyrosine sites

Endogenous. SOD2 knockdown mouse model of early AMD

Murdaugh

et al. [87]

Human

Bruch's

membrane

HPLC, ESI-MS/MS

A2E was nitrated

Endogenous. Nitro-A2E is a specific biomarker of nitrosative stress in Bruch's membrane and its concentration is directly related to tissue age

Palamalai et al. [88]

Photoreceptor rod outer segments of cyclic light- reared rats treated or not with the antioxidant

2D western blot and LC-ESI-MS/MS

Ten putative nitroproteins were identified

Endogenous. No nitrotyrosine sites were identified

(Continued )

Table 5.1 (Continued)

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

(vii) Diabetes

Kato et al.[90]

Healthy and diabetic human urine

LC-ESI-MS/MS

Urine

nitrotyrosine

Endogenous

(viii) Kidney disease

Piroddi

et al. [92]

Plasma from kidney disease patients

2DE and LC- ESI-MS/MS

Fourteen tentative nitroproteins and 7 nitrotyrosine sites were identified

Endogenous

(ix) Plant diseases

Chaki et al. [93]

Sunflower

hypocotyls

2D western blot and LC-ESI-MS/MS

Twenty-one putative nitroproteins were identified

No nitrotyrosine sites were identified

(x) Others

Aslan

et al. [95]

Liver and kidney from sickle cell disease mouse

Western blot and precipitation, MALDI- PMF, LC-ESI-MS/MS

Actin was nitrated at Tyr91, Tyr198, and Tyr240

Endogenous

Lee

et al. [35]

Hippocampus from smoke inhalation rat model

2D western blot and MALDI-PMF or MALDI-MS/MS

Five nitroproteins of mitochondrial proteins were identified

Endogenous. No nitrotyrosine sites were identified

Reed et al. [96]

Traumatic brain- injured rats

2D western blot and MALDI-PMF

Several nitroprotein such as GSH were identified

Ulrich et al. [98]

Human lung tissues and blood samples, animal granule protein preparation

Western blot and MALDI-PMF

Six nitroproteins and nitrotyrosine sites at Tyr349 in eosinophil peroxidase (EPO) and Tyr33 in bother eosinophil cationic protein (ECP) and eosinophil-derived neurotoxin (EDN)

Endogenous

Webster,

Brockman,

and

Myatt [97]

Human

placenta

1D western blot and MALDI-PMF

p38 MAPK was nitrated

No nitrotyrosine sites were identified

Table 5.1 (Continued)

References

Specimen

Methods

Nitroprotein and

nitrotyrosine

sites

Remark

Casanovas et al. [99]

Lipoprotein lipase of bovine and rat

2D western blot and LC-ESI-MS/MS

Lipoprotein lipase was nitrated at Tyr95, Tyr164,

Tyr 316

Endogenous

Hamilton et al. [101]

Human

plasma

LC-ESI-MS/MS

Low-density lipoprotein (LDL) was nitrated at Tyr276, Tyr666, and Tyr720 of LDL-a1, Tyr2524 of LDL-a2, Tyr4141 of LDL-a3, Tyr3139, Tyr3205, and Tyr3489 of LDL-P2

Sharov et al. [102]

Rabbit muscle

LC-ESI-MS/MS

Glycogen phosphorylase b was nitrated at 28 nitrotyrosine sites

Zhu et al. [103]

Liver from SOD1-/- and WT

C57BL/6 mice

1DE, LC-ESI-MS/MS

Ten candidate nitrated proteins were identified

No nitrotyrosine sites were identified

Chen and Chen [104]

Human blood samples from smokers and nonsmokers

LC-ESI-MS/MS under the selected reaction monitoring (SRM) mode

Hemoglobin was nitrated at Tyr24 and Tyr 42 (a-globin), Tyr130 (в-globin)

Nitration of human hemoglobin is associated with cigarette smoking

Sekar et al. [105]

Mast cells

2D western blot and LC-ESI-MS/MS

Aldolase was nitrated

No nitrotyrosine sites were identified

Ohma

and

Brautigan

[106]

Human

peripheral

blood

mononuclear

cells

LC-ESI-MS/MS

Protein

phosphatase 2A was nitrated at Tyr284

Redondo- Horcajo et al.

[107]

Endothelial cells from bovine aortas and mouse lung

LC-ESI-MS/MS

Manganese superoxide dismutase (MnSOD) was nitrated at Tyr34

In vitro nitrated with

cyclosporine A

Note: Reproduced from Zhan et al. [38], with permission from Wiley-VCH, copyright 2015.

one-/two-dimensional (1D/2D) western blot coupled with MALDI peptide mass fingerprint (PMF) or LC-ESI-MS/MS, nitrotyrosine affinity column (NTAC)- MS/MS, iTRAQ-strong ion exchange (SCX)-LC-ESI-MS/MS, selected reaction monitoring (SRM), and COFRADIC coupled with ESI-MS.

Endogenous nitroproteins and nitration sites have been identified in multiple different pathophysiological conditions with proteomics (Table 5.1). Tyrosine nitration is involved in inflammation-related diseases. Nitroproteins were identified in bronchial epithelial cells and bronchoalveolar lavage with asthma [65], a septic patient's rectus abdominis muscle [66], experimental sepsis [67], Chagas' disease [68], and a serum sample of a C57BL6/J mouse model with septic shock [48]. Tyrosine nitration is involved in aging and aging-related diseases. Nitroproteins were discovered in aging rat skeletal muscle [69, 70], mouse liver [71], and rat heart [72]. Tyrosine nitration is clearly involved in tumorigenesis. Nitroproteins were identified in rat glioma cell lines [73] and human gliomas [74]. Eight nitroproteins were identified from human pituitary control tissue [1, 75], and nine nitroproteins, three nitroprotein-interacted proteins, and ten nitrotyrosine sites were identified from a pituitary adenoma [2] (Table 5.2). Tyrosine nitration is involved in neurodegenerative diseases. Nitroproteins were identified in mouse brain [76-78], Parkinson's disease [79], spinal cords of a mouse model of familial amyotrophic lateral sclerosis [80], and HT22 hippocampal cells [81]. Tyrosine nitration is involved in the cardiovascular system and related diseases. Nitroproteins have been identified in ischemia-reperfusion injury [82-84], vascular [85], and mouse heart [77, 78]. Tyrosine nitration is involved in the neurovisual system. Nitroproteins were identified in SOD2 knockdown mouse eyecup [86], human Bruch's membrane [87], and photoreceptor rod outer segments [88]. Tyrosine nitration is involved in diabetes. Nitroproteins have been discovered in diabetic rats [89], a diabetic patient's urine [90], and diabetic mellitus patients [91]. Tyrosine nitration is also involved in kidney disease, where nitroproteins have been identified in a kidney disease patient's plasma [92], diseases in plants [93, 94], and in sickle cell disease [95]; rat hippocampus after acute inhalation of combustion smoke [35]; traumatic brain-injured rats [96]; placenta/preeclampsia [97]; eosinophil granule toxins [98]; hypertriglyceridemia [99]; human plasma [100, 101]; rabbit muscle [102]; murine liver [103]; human hemoglobin associated with cigarette smoking [104]; mast cells [105]; human peripheral blood mononuclear cells [106]; and endothelial cells [107].

 
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