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Frontiers of Medicine

Front. Med.    2017, Vol. 11 Issue (1) : 97-109     DOI: 10.1007/s11684-016-0496-1
iTRAQ-based quantitative proteomic analysis on differentially expressed proteins of rat mandibular condylar cartilage induced by reducing dietary loading
Liting Jiang1,2,Yinyin Xie3,Li Wei4,Qi Zhou4,Ning Li1,Xinquan Jiang2(),Yiming Gao1()
1. Department of Stomatology, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
2. Department of Prosthodontics, Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai Key Laboratory of Stomatology, Shanghai 200011, China
3. State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
4. Shanghai Institute of Traumatology and Orthopedics, Shanghai 200025, China
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As muscle activity during growth is considerably important for mandible quality and morphology, reducing dietary loading directly influences the development and metabolic activity of mandibular condylar cartilage (MCC). However, an overall investigation of changes in the protein composition of MCC has not been fully described in literature. To study the protein expression and putative signaling in vivo, we evaluated the structural changes of MCC and differentially expressed proteins induced by reducing functional loading in rat MCC at developmental stages. Isobaric tag for relative and absolute quantitation-based 2D nano-high performance liquid chromatography (HPLC) and matrix-assisted laser desorption/ionization time-of-flight/ time-of-flight (MALDI-TOF/TOF) technologies were used. Global protein profiling, KEGG and PANTHER pathways, and functional categories were analyzed. Consequently, histological and tartrate-resistant acid phosphatase staining indicated the altered histological structure of condylar cartilage and increased bone remodeling activity in hard-diet group. A total of 805 differentially expressed proteins were then identified. GO analysis revealed a significant number of proteins involved in the metabolic process, cellular process, biological regulation, localization, developmental process, and response to stimulus. KEGG pathway analysis also suggested that these proteins participated in various signaling pathways, including calcium signaling pathway, gap junction, ErbB signaling pathway, and mitogen-activated protein kinase signaling pathway. Collagen types I and II were further validated by immunohistochemical staining and Western blot analysis. Taken together, the present study provides an insight into the molecular mechanism of regulating condylar growth and remodeling induced by reducing dietary loading at the protein level.

Keywords condylar cartilage      mechanical loading      proteomic analysis      iTRAQ      bioinformatics analysis     
Corresponding Authors: Xinquan Jiang,Yiming Gao   
Just Accepted Date: 19 December 2016   Online First Date: 23 January 2017    Issue Date: 20 March 2017
 Cite this article:   
Liting Jiang,Yinyin Xie,Li Wei, et al. iTRAQ-based quantitative proteomic analysis on differentially expressed proteins of rat mandibular condylar cartilage induced by reducing dietary loading[J]. Front. Med., 2017, 11(1): 97-109.
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Liting Jiang
Yinyin Xie
Li Wei
Qi Zhou
Ning Li
Xinquan Jiang
Yiming Gao
Fig.1  Schematic flowchart of experimental procedures.
Fig.2  Sagittal section of the mandibular condyle. (A) Anterior, superior, and posterior regions of condylar cartilage stained with toluidine blue (original magnification, 4×; Bar, 500 μm). (B) Condylar cartilage consisted of four layers: fibrous (F), proliferative (P), maturing (M), and hypertrophic layers (H) (original magnification, 20×). (C) Representative images of superior and anterior regions of condylar cartilage both in soft-diet and hard-diet groups (original magnification, 20×; Bar, 100 mm).
Fig.3  Histologic analysis of the condylar cartilage. (A) Safranin O (original magnification, 20×), tartrate-resistant acid phosphatase (TRAP) staining, and immunostaining for Col I and Col II proteins (original magnification, 40×) and negative controls in the anterior region of condylar cartilage in soft-diet and hard-diet groups. Bars, 100 μm. Immunohistochemical staining-positive cells were indicated by arrows. (B) Comparison of the thickness of the anterior region between soft-diet and hard-diet groups. (C) TRAP-positive cells found in soft-diet and hard-diet groups. (D) Semiquantitative analysis of Col I and Col II-positive areas in soft-diet and hard-diet groups. Bar graph represents the mean±SE of three independent experiments, *P<0.05, **P<0.01, t-test.
Fig.4  PANTHER gene ontology annotation of the differentially expressed proteins identified in rat condylar cartilages. Results were obtained by a web-based browser ( (A) Molecular function distribution of identified proteins. (B) Biological process distribution of identified proteins.
Gene symbol Protein name 116.1/114.1 117.1/114.1
Calcium binding protein (PC00060)
CAB45 5 kDa calcium binding protein precursor 0.53 0.61
PLCE1 Phospholipase C-epsilon-1 0.59 0.53
KPCZ Protein kinase C ζ type 0.57 0.77
CABP1 Ras GTPase-activating protein 1 0.91 1.02
KPCT Protein kinase C ι type 0.61 0.64
PLCG2 Phospholipase C-γ-2 0.70 0.74
CAN9 Calpain-9 0.69 0.73
PLCG1 Phospholipase C-γ-1 0.87 1.01
M2OM Mitochondrial 2-oxoglutarate/malate carrier protein 1.07 1.19
PLCB2 Phospholipase C-β-2 0.76 0.75
PLCB1 Phospholipase C-β-1 0.39 0.51
NUCB1 Nucleobindin-1 precursor 0.48 0.68
PKN2 Protein-kinase C-related kinase 2 2.39 2.96
EFCB3 EF-hand calcium binding domain-containing protein 3 0.69 0.81
CAN10 Calpain-10 1.44 1.22
KPCB Protein kinase C β type 0.60 0.51
KPCG Protein kinase C γ type 1.55 1.61
MAST1 Microtubule-associated serine/threonine-protein kinase 1 0.74 0.75
PKN1 Serine/threonine-protein kinase N1 0.29 0.53
FA10 Coagulation factor X precursor 0.47 0.50
Cytoskeletal protein (PC00085)
ACTN1 α-actinin-1 1.12 1.20
MYH10 Myosin-10 0.60 0.79
FBP1L Formin-binding protein 1-like 0.48 0.53
DREB Drebrin 0.34 0.34
CLIC6 Chloride intracellular channel 6 0.96 1.02
PDLI3 Actinin-associated LIM protein 0.83 0.95
ADDA α-adducin 1.11 0.93
DYN1 Dynamin-1 0.81 0.85
TBA3 Tubulin α-3 chain 0.76 0.81
LMNB1 Lamin-B1 0.64 0.66
K1C14 Keratin, type I cytoskeletal 14 0.53 0.57
SYN3 Synapsin-3 0.58 0.67
DYN2 Dynamin-2 0.29 0.53
NUDC Nuclear migration protein nudC 0.73 0.54
KIF2C Kinesin-like protein KIF2C 0.97 1.08
LHX1 LIM/homeobox protein Lhx1 1.08 1.29
MAP1B Microtubule-associated protein 1B 0.96 0.97
TBB2B Tubulin β-2B chain 1.06 1.06
K2C1B Keratin, type II cytoskeletal 1b 0.45 0.56
CNN1 Calponin-1 0.11 0.21
Extracellular matrix protein (PC00102)
MEGF8 Multiple epidermal growth factor-like domains 8 0.71 0.61
CO5A1 Collagen α-1(V) chain precursor 0.37 0.51
ITB4 Integrin β-4 precursor 1.34 1.40
MEGF6 Multiple epidermal growth factor-like domains 6 precursor 0.66 0.72
R4RL2 Reticulon-4 receptor-like 2 precursor 0.69 0.72
CSPG2 Versican core protein precursor 1.24 1.44
FETUA α-2-HS-glycoprotein precursor 2.39 2.96
CO1A1 Collagen α-1(I) chain precursor 0.61 0.76
CHRD Chordin (Fragment) 0.51 0.65
CO1A2 Collagen α-2(I) chain precursor 0.39 0.44
GAS6 Growth-arrest-specific protein 6 precursor 1.41 1.22
CO2A1 Collagen α-1(II) chain precursor 0.68 0.91
LAMB2 Laminin subunit β-2 precursor 0.59 0.77
AP3M1 AP-3 complex subunitμ-1 1.15 1.50
DSPP Dentin sialophosphoprotein precursor 0.40 0.60
Signaling molecule (PC00207)
CD151 CD151 antigen 1.36 1.41
PLCE1 Phospholipase C-epsilon-1 0.59 0.53
CD53 Cell surface glycoprotein CD53 0.37 0.34
GDF6 Growth/differentiation factor 6 precursor 1.05 1.15
FZD5 Frizzled-5 precursor 0.40 0.60
R4RL2 Reticulon-4 receptor-like 2 precursor 0.69 0.72
PLCG2 Phospholipase C-γ-2 0.70 0.74
CLIC6 Chloride intracellular channel 6 1.03 1.04
PLCG1 Phospholipase C-γ-1 0.87 1.01
SFRP4 Secreted frizzled-related protein 4 precursor 1.39 1.36
A1M α-1-macroglobulin precursor 0.47 0.63
WISP2 WNT1-inducible-signaling pathway protein 2 precursor 1.42 1.69
PLCB1 Phospholipase C-β-1 0.39 0.51
DSPP Dentin sialophosphoprotein precursor 0.40 0.60
RASA1 Ras GTPase-activating protein 1 0.91 1.02
BMP3 Bone morphogenetic protein 3 precursor 1.10 1.03
SYGP1 Ras GTPase-activating protein SynGAP 0.60 0.60
PDGFD Platelet-derived growth factor D precursor 0.94 0.99
VEGFD Vascular endothelial growth factor D precursor 0.44 0.54
FGF5 Fibroblast growth factor 5 precursor 0.49 0.47
CD40L CD40 ligand 0.70 0.64
FA10 Coagulation factor X precursor 0.47 0.50
DAB2P DAB2-interacting protein 0.86 0.98
UBF1 Nucleolar transcription factor 1 0.32 0.33
TNFL4 Tumor necrosis factor ligand superfamily member 4 1.37 1.44
RASA3 Ras GTPase-activating protein 3 1.37 1.43
Transcription factor (PC00218)
MAF Transcription factor Maf 0.63 0.67
ISL2 Insulin gene enhancer protein ISL-2 0.57 0.68
JUN Transcription factor AP-1 1.24 1.15
FOSL1 Fos-related antigen 1 0.92 0.96
1433B 14-3-3 protein β/α 0.44 0.38
Tab.1  List of selected differentially expressed proteins in rat condylar cartilage according to the PANTHER protein class
KEGG Gene symbol P value
rno04020: Calcium signaling pathway PDE1C, VDAC1, ERBB4, CAC1H, KCC2D, NOS1, GNAL, CLTR1, IP3KB, NMDE1, CAC1A, P2RX5, P2RX1, CAC1G, NOS3, ERBB2, KPCG, NMDE3, PLCB2, NMDZ1, CAC1I, PLCB1, TA2R, PLCG1, AT2B1, PLCG2, PLCE1, V1AR, ADCY3, ADRB2, ERBB3, AT2B2, ALEX, AA2AR, KPCB 6.73E-09
rno04540: Gap junction ADCY3, KPCG, PLCB2, GCYA3, PDGFD, ALEX, PLCB1, CXA1, RASN, TBA3, KPCB, TBB2B 0.013
rno04012: ErbB signaling pathway ERBB2, ERBB3, KPCG, NRG2, FRAP, ERBB4, JUN, RASN, KCC2D, KPCB, PLCG1, PLCG2 0.016
rno04010: MAPK signaling pathway FGFR1, JUN, RASA1, ARRB1, CAC1A, CAC1G, RASM, RASN, CAC1H, PA21B, CAC1I, CCG6, DAXX, KPCB, KPCG, DUS6, TGFR1, FGF1, FGF5, FGFR4, GA45A, M3K12 0.035
rno04310: Wnt signaling pathway AXN1, KPCG, SENP2, APC, PLCB2, JUN, KCC2D, PLCB1, FZD5, SMAD2, SFRP4, KPCB, FOSL1, 2AAB, ROCK1 0.075
Tab.2  Identification of differentially expressed proteins by isobaric tag for relative and absolute quantitation (iTRAQ) quantification according to KEGG pathway category
PANTHER Gene symbol P value
P00021: FGF signaling pathway RASA1, KPCG, FGF1, KPCZ, PLCG1, ARAF, PLCG2, PTN6, FGFR4, FGFR1, PP4R1, KPCT, RM38, FGF5, RASN, KPCB, SYGP1, 2AAB, 1433B 0.006
P00027: Heterotrimeric G-protein ?signaling pathway KPCG, DRD3, GPSM1, SI1L1, SSR4, PLCB2, KPCZ, GPSM3, PLCB1, ACM4, ARHGB, RGS3, RGS14, GNRHR, KPCT, IRK9, CAC1A, RGS8, AA2AR, KPCB 0.007
Tab.3  Identification of differentially expressed proteins by iTRAQ quantification according to PANTHER pathway category
Fig.5  Representative results of Western blot. (A) The protein expression levels of Col I and Col II from condylar cartilage in the soft-diet and hard-diet groups analyzed by Western blot. Values were normalized to GAPDH. (B) Quantitation of relative Col I and Col II protein expression (Bar graph represents the mean±SE of three independent experiments, *P<0.05, **P<0.01, t-test).
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