C1QBP is upregulated in colon cancer and binds to apolipoprotein A-I

  • Authors:
    • Kun Kim
    • Min‑Jeong Kim
    • Kyung‑Hee Kim
    • Sun‑A Ahn
    • Jong Heon Kim
    • Jae Youl Cho
    • Seung‑Gu Yeo
  • View Affiliations

  • Published online on: March 21, 2017     https://doi.org/10.3892/etm.2017.4249
  • Pages: 2493-2500
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Abstract

The present study aimed to investigate the expression of complement component 1, q subcomponent-binding protein (C1QBP) in colon cancer cells, and identify proteins that interact with C1QBP. Total proteins were extracted from both the tumor and normal tissues of 22 patients with colon cancer and analyzed using liquid chromatography-mass spectrometry (LC-MS) to identify proteins that were differentially-expressed in tumor tissues. C1QBP overexpression was induced in 293T cells using a pFLAG‑CMV2 expression vector. Overexpressed FLAG‑tagged C1QBP protein was then immunoprecipitated using anti‑FLAG antibodies and C1QBP‑interacting proteins were screened using LC‑MS analysis of the immunoprecipitates. The C1QBP-interacting proteins were confirmed using reverse‑immunoprecipitation and the differential expression of C1QBP in tissues and cell lines was confirmed using western blot analysis. LC‑MS analysis revealed that C1QBP exhibited a typical tumor expression pattern. Two immune‑reactive signals (33 and 14 kDa) were detected in normal and tumor tissues from 19 patients. Furthermore, 14 kDa C1QBP protein was upregulated in the tumors of 15 patients. In total, 39 proteins were identified as candidate C1QBP‑interacting proteins, and an interaction between C1QBP and apolipoprotein A‑I was confirmed. The present study indicates that C1QBP is involved in colon cancer carcinogenesis, and that the mechanisms underlying the established anti-tumor properties of apolipoprotein A‑I may include interacting with and inhibiting the activity of C1QBP.

Introduction

Complement component 1, q subcomponent binding protein (C1QBP) is a multifunctional protein. Its sequence is identical to that of p32, a protein that co-purifies with splicing factor SF2, and that of hyaluronan-binding protein 1, a member of the hyaladherin family (1). Its terminal α-helices are important in protein-protein interactions and regulate its multifunctional nature. C1QBP is commonly localized in the mitochondrial matrix, although it exhibits differential localization among cell lines under various physiological conditions (1). Moreover, it serves important roles in various biological processes, including inflammation, infection, cell signaling and chemotaxis (24).

However, it remains unclear whether C1QBP exerts anti- or pro-tumorigenic effects during cancer pathogenesis (5). Upregulated expression of C1QBP has been reported in various different types of cancer, including breast, prostate, thyroid, colon, pancreatic, gastric, esophageal and lung cancer (69). This elevated expression has been linked to the metastasis of ovarian cancer (10), poor prognosis or metastasis of breast cancer (7,9) and early relapse following surgery in prostate cancer (11). By contrast, other studies have reported that C1QBP is required for the induction of mitochondria-dependent apoptotic cell death (12,13). The constitutive expression of C1QBP in normal fibroblast cells perturbs its growth characteristics and induces apoptosis (14). In addition, it has been demonstrated that C1QBP is upregulated following the induction of apoptosis in HeLa cells in response to a chemotherapeutic agent (cisplatin), suggesting that C1QBP may be involved in apoptosis (15,16).

Over one million people worldwide develop colorectal cancer annually, and the disease has a mortality rate of ~33% (17). Carcinogenesis and biology of colorectal cancer have been recognized as multistep processes involving various molecular alterations (18). Knowledge of the specific molecular markers or pathways that are responsible for disease progression and poor prognosis may be beneficial in the development of more effective treatment.

The present proteomic study revealed that C1QBP was cleaved in the tumor tissues of patients with colon cancer, and that apolipoprotein A-I (ApoA-I) interacts with C1QBP. Furthermore, the possible role of C1QBP in colon cancer via its interaction with ApoA-I is discussed.

Materials and methods

Tissues from colorectal cancer patients

Fresh tissues (normal colon mucosa and primary colon tumor) were obtained from 22 patients with colon cancer (8 female and 14 male, 61.5±10.5 years old) who were enrolled in the current study between January 2006 and May 2007 at the National Cancer Center, Republic of Korea. Following dissection of necrotic exudates and stromal components, the overall cellularity of the normal epithelium and tumors was >75%. The present study was approved and performed in accordance with the guidelines of the Institutional Review Board of the National Cancer Center (Goyang, Republic of Korea), and informed consent was obtained from all patients.

Human cancer cell lines

The human colon cancer cell lines (SNU-81, SNU-407, SNU-C4, NCI-H498, NCI-H508, CaCo2, DLD-1, HCT-116, LoVo and SW620), a cervical cancer cell line (HeLa) and an embryonic kidney cell line (293T) were all obtained from the Korean Culture Line Bank (Seoul, Korea).

Mass analysis

Mass analysis was performed as described previously (19). The bands of SDS-PAGE corresponding to potential proteins of interest were excised, destained using 50% acetonitrile in 0.1 M ammonium bicarbonate (Thermo Fisher Scientific, Inc., Waltham, MA USA) and dried using a SpeedVac evaporator (Savant SVC-100H, Thermo Fisher Scientific, Inc.). Dried gel pieces were swollen with 30 µl of 25 mM sodium bicarbonate (pH 8.8) (Thermo Fisher Scientific, Inc.) containing 50 ng trypsin (Promega Corporation, Madison, WI, USA) at 37°C overnight. Samples were subsequently desalted using Zip-Tips C18 (EMD Millipore, Billerica, MA, USA) and dissolved in 10 µl of 2% acetonitrile (Thermo Fisher Scientific, Inc.) in 0.1% formic acid (Thermo Fisher Scientific, Inc.). Analyses were performed using a linear trap quadrupole (LTQ) XL linear ion trap mass spectrometer (MS; Thermo Fisher Scientific, Inc.) in the Proteomics Core of the National Cancer Center (Goyang, Republic of Korea). The mass spectrometer was set for nanospray ionization (NSI) in the positive mode. Moreover, a syringe pump was used to introduce the calibration solution for the automatic tuning and calibration of the LTQ in an NSI-positive ion mode. The infusion of trypsin-digested samples into the ionization source of the mass spectrometer was performed following liquid chromatographic separation. The spray voltage was set at +1.1 kV, the temperature of the capillary apparatus was maintained at 200°C, the capillary voltage was set at +20 V and the tube lens voltage was +100 V. Moreover, the auxiliary gas was set to zero. Full scan experiments were performed to linear trap in the m/z range of 150–2,000. Systematic MS/MS experiments were performed by changing the relative collision energy and monitoring the intensities of the fragment ions. All MS/MS samples were analyzed using Sequest (version v.27, rev.11; Thermo Fisher Scientific) to search the uniprot_sprot (http://www.uniprot.org) and IPI human databases (European Bioinformatics Institute, Hinxton, UK; ftp://ftp.ebi.ac.uk/pub/databases/IPI/last_release/current/) assuming digestion with trypsin. Sequest was searched with a fragment ion mass tolerance of 1.00 Da and a parent ion tolerance of 1.2 Da. Methionine oxidation was specified as a variable modification.

Western blot analysis

Western blotting was performed as described previously (20). Briefly, cell homogenates containing equivalent quantities (20 µg) of protein were centrifuged at 4,000 × g (4°C) for 5 min and the supernatant fractions were separated using 4–10% gradient SDS-PAGE. Following electrophoresis, the proteins were transferred to polyvinylidene fluoride membranes (EMD Millipore), blocked for 2 h at 4°C in 1% Tween 20-Tris buffered saline buffer containing 1.5% non-fat dry milk (Bio-Rad Laboratories, Inc., Hercules, CA, USA) and 1 mM MgCl2. The blocked membranes were then incubated for 2 h at room temperature with primary antibodies against C1QBP (dilution 1:1,000, cat no. ab131284, Abcam, Cambridge, MA, USA), ApoA-I (dilution 1:1,000, cat no. ab52945, Abcam) or β-actin (dilution 1:2,000, cat no. 04-1116, Merck Millipore, Darmstadt, Germany). They were then washed three times in blocking solution (1% Tween 20-TBS buffer containing 1.5% non-fat dry milk and 1 mM MgCl2) for 15 min each and incubated with diluted horseradish-peroxidase conjugated secondary antibody (dilution 1:2,000, cat no. 4010-05, Southern Biotech Associates, Inc., Birmingham, AL, USA) for 1 h at room temperature. Membranes were then washed with blocking solution (3×15 min), incubated with WEST-ZOL® plus chemiluminescence reagent (iNtRON Biotechnology, Inc., Gyeonggi, Korea) for 1 min and exposed to film (Kodak Blue XB-1, Kodak, Rochester, NY, USA).

Overexpression of C1QBP in 293T cells and immunoprecipitation

In order to generate a pFLAG-CMV2-C1QBP plasmid containing the full-length coding sequence of human C1QBP, polymerase chain reaction (PCR) was performed from a human brain cDNA library (Clontech Laboratories, Inc., Rochester, NY, USA) with the following oligomers: Sense, 5′-GGAATTCTATGCTGCCTCTGCTGCGCTGC-3′ and antisense, 5′-TAACCCGGGCTACTGGCTCTTGACAAAACTCTTGAGG-3′. The amplified PCR product was digested using EcoRI-XmaI (Clontech Laboratories), then inserted into pFLAG-CMV2 (Merck Millipore). The 293T cells were transfected with control or FLAG-C1QBP plasmids. At 48 h after transfection, cells were harvested and aliquots of the total protein from each sample were analyzed using western blotting, as indicated.

For immunoprecipitation-coupled MS analyses, cells were lysed in immunoprecipitation buffer containing 150 mM NaCl, 25 mM HEPES-KOH (pH 7.5), 10% (v/v) glycerol, 1 mM MgCl2, 2 mM sodium orthovanadate, 2 mM glycerophosphate, 1 mM PMSF, 1 mM DTT, 2 mM EDTA, 0.5% Triton X-100 and 1X protease inhibitor cocktail (Roche Applied Science, Madison, WI, USA). Following a brief sonication and incubation on ice, the lysates were centrifuged at 15,000 × g for 5 min to remove the insoluble materials. The lysates were then incubated with anti-FLAG M2 affinity agarose beads (Sigma-Aldrich; Merck Millipore) for 2 h at 4°C, and the collected beads were washed four times with washing buffer (0.05% Triton X-100 immunoprecipitation buffer without a protease inhibitor cocktail), and boiled in SDS sample buffer for protein immunoprecipitation-coupled MS analysis.

Results

Differential expression of C1QBP in tissues from colon cancer patients

Whole proteins were extracted from both the tumor and normal tissues of three patients and were separated by SDS-PAGE (Fig. 1). Sections of gel containing proteins were then cut according to their molecular weight and subjected to proteomic analysis. Proteins of 19–35-kDa were analyzed using the linear ion trap MS system, which identified C1QBP to be present only in tumor tissues (Fig. 1 and Table I).

Table I.

Proteins identified in the range of molecular weight between 19 to 35 kDa indicated in Fig. 1. Proteins were extracted from the paired tissues (tumor, CRC; normal, N) obtained from three colon cancer patients. ‘O’ indicates successful identification of protein.

Table I.

Proteins identified in the range of molecular weight between 19 to 35 kDa indicated in Fig. 1. Proteins were extracted from the paired tissues (tumor, CRC; normal, N) obtained from three colon cancer patients. ‘O’ indicates successful identification of protein.

Total identification no.CRCNormal



Protein accession number and nameCRCNormalCRC1CRC2CRC3N1N2N3
IPI:IPI00014230.1 C1QBP Complement component 1 Q subcomponent-binding protein, mitochondrial30OOO
IPI:IPI00010204.1 SRSF3 Serine/arginine-rich splicing factor 331OOOO
IPI:IPI00021266.1 SNORD4A;RPL23A 60S ribosomal protein L23a31OOOO
IPI:IPI00215914.5 ARF1 ADP-ribosylation factor 131OOO O
IPI:IPI00219622.3 PSMA2 Proteasome subunit alpha type-231OOOO
IPI:IPI00306332.4 RPL24 60S ribosomal protein L2431OOOO
IPI:IPI00003881.5 HNRNPF Heterogeneous nuclear ribonucleoprotein F20 OO
IPI:IPI00007321.2 LYPLA1 cDNA FLJ60607, highly similar to Acyl-protein thioesterase 120O O
IPI:IPI00010105.1 EIF6 Eukaryotic translation initiation factor 620OO
IPI:IPI00016568.1 AK4 Adenylate kinase isoenzyme 4, mitochondrial20O O
IPI:IPI00031691.1 RPL9 60S ribosomal protein L920OO
IPI:IPI00179964.5 PTBP1 Isoform 1 of Polypyrimidine tract-binding protein 120OO
IPI:IPI00219097.4 HMGB2 High mobility group protein B220OO

[i] CRC, colorectal cancer.

Western blot analysis was then used to confirm the expression of C1QBP in normal and tumor tissues from patients with colon cancer (Fig. 2A). Two immunoreactive signals at 33 and 14 kDa were detected using the anti-C1QBP antibody (Fig. 2A). In contrast to the proteomic analysis, 33 kDa C1QBP exhibited no typical expression pattern in tumor tissues (Fig. 2A). However, among the 19 pairs of tissues analyzed, 15 showed upregulation of 14 kDa C1QBP in tumor compared with normal tissues (Fig. 2A). In human colon cancer cell lines, the expression of 33 kDa C1QBP was variable, whereas the short form was not detected (Fig. 2B).

Candidate C1QBP-interacting proteins

In order to further evaluate the role of C1QBP in colon cancer at the molecular level, C1QBP-interacting proteins were screened for in immunoprecipitates from FLAG-tagged C1QBP-overexpressing 293T cells. Fig. 3 presents the results of immunoprecipitation using FLAG antibodies in whole cell lysates from C1QBP-overexpressing 293T cells (pFLAG_CMV2_C1QBP). FLAG-tagged C1QBP was immunoprecipitated successfully using anti-FLAG antibodies, and was detected as a band at 33 kDa on the SDS-PAGE gel (Fig. 3). As a control, immunoprecipitation was performed using 293T cells overexpressing FLAG alone (pFLAG_CMV2_MOCK_293T). The appropriate bands were excised from the gels as described in Fig. 3 and the proteins therein were subjected to in-gel tryptic digestion and MS. The proteins that co-precipitated with C1QBP are listed in Table II after exclusion of proteins also identified in the control lane. In total 39 proteins, including fibrinogen α-, β- and γ-chains, complement C3, complement C4-A, ApoA-I and ApoA-II, were identified as possible C1QBP-interacting proteins (Table II).

Table II.

Candidate proteins interacting with complement component 1, q subcomponent-binding protein.

Table II.

Candidate proteins interacting with complement component 1, q subcomponent-binding protein.

MS/MS sampleProtein nameAccession numberMolecular weight, DaIdentification probability (%)Total spectra, %Sequence coverage, %
2–01General transcription factor 3C polypeptide 1TF3C1_HUMAN238,860.60100.000.06   1.19
2–01Insulin receptor substrate 4IRS4_HUMAN133,751.30   99.800.06   2.07
2–02Heterogeneous nuclear ribonucleoprotein UHNRPU_HUMAN   90,567.20100.000.23   9.09
2–02General transcription factor 3C polypeptide 2TF3C2_HUMAN100,652.80   99.800.07   1.98
2–02ATP-dependent RNA helicase ADHX9_HUMAN140,902.50100.000.07   2.44
2–02 Ubiquitin-associated protein 2-likeUBP2L_HUMAN116,780.70100.000.13   4.34
2–02Thyroid hormone receptor-associated protein 3TR150_HUMAN108,650.90   99.800.07   1.99
2–03General transcription factor 3C polypeptide 3TF3C3_HUMAN101,258.20100.000.27   6.77
2–03Nucleolar RNA helicase 2DDX21_HUMAN   87,328.00   99.800.11   2.55
2–04 Alpha-1-antitrypsinA1AT_HUMAN   46,719.90100.000.11   8.37
2–04Apolipoprotein A-IAPOA1_HUMAN   30,760.50100.000.1112.40
2–04Protein LAS1 homologLAS1L_HUMAN   83,047.50100.000.14   6.40
2–06Lamin-B receptorLBR_HUMAN   70,688.30   99.800.10   3.09
2–08RNA methyltransferase-like protein 1RMTL1_HUMAN   47,002.50100.000.24   7.62
2–08Keratin, type I cytoskeletal 14K1C14_HUMAN   51,544.50100.000.12   9.11
2–09Interleukin enhancer-binding factor 2ILF2_HUMAN   43,044.70100.000.1711.50
2–10Heterogeneous nuclear ribonucleoproteins C1/C2HNRPC_HUMAN   33,652.50100.000.3722.20
2–10Glutaminyl-peptide cyclotransferase-like proteinQPCTL_HUMAN   42,907.60100.000.12   8.12
2–11rRNA 2′-O-methyltransferase fibrillarinFBRL_HUMAN   33,766.10   99.900.09   7.48
2–11Polymerase delta-interacting protein 2PDIP2_HUMAN   42,015.00100.000.2020.10
2–12THO complex subunit 4THOC4_HUMAN   26,870.70100.000.2621.00
2–13 Alpha-1-antichymotrypsinAACT_HUMAN   47,634.90   99.800.04   4.73
2–13 Alpha-2-macroglobulinA2MG_HUMAN163,271.90100.000.5618.80
2–13Plasma protease C1 inhibitorIC1_HUMAN   55,137.50   99.700.04   5.60
2–13 SerotransferrinTRFE_HUMAN   77,046.20100.000.1613.50
2–13HemopexinHEMO_HUMAN   51,658.50100.000.05   8.23
2–13HaptoglobinHPT_HUMAN   45,186.90100.000.1613.10
2–13Fibrinogen alpha chainFIBA_HUMAN   94,955.40100.000.1814.40
2–13Fibrinogen beta chainFIBB_HUMAN   55,910.60100.000.1521.60
2–13Fibrinogen gamma chainFIBG_HUMAN   51,495.30100.000.1114.10
2–13Ig gamma-1 chain C regionIGHG1_HUMAN   36,087.00100.000.3320.00
2–13Ig kappa chain C regionIGKC_HUMAN   11,590.50   99.800.1830.20
2–13Ig lambda-2 chain C regionsLAC2_HUMAN,   11,275.20   99.800.1332.10
2–13Ig mu chain C regionIGHM_HUMAN   49,287.70100.000.1522.80
2–13Complement C3CO3_HUMAN187,131.10100.000.15   7.76
2–13Complement C4-ACO4A_HUMAN192,754.80100.000.05   2.52
2–13Apolipoprotein A-IIAPOA2_HUMAN   11,202.40   99.800.0721.00
2–1460S ribosomal protein L13RL13_HUMAN   24,244.20   99.800.0811.40
Interaction between C1QBP and ApoA-I

Reverse immunoprecipitation was subsequently used to confirm the interaction between C1QBP and candidate proteins. Among the proteins listed in Table II, ApoA-I was selected for confirmation of its interaction with C1QBP. Human SW620 colon cancer cells were used because they express high levels of C1QBP (Fig. 2B, and mouse IgG or antibodies against C1QBP and ApoA-I were added to SW620 whole-cell lysates. Immunoprecipitation was then performed, followed by western blotting. Immunoreactive signals produced by monoclonal antibodies against ApoA-I were detected in immunoprecipitates prepared using both anti-ApoA-I and -C1QBP antibodies (Fig. 4). In addition, SW620 whole cell lysates were immunoreactive for ApoA-I (Fig. 4).

Discussion

The present study revealed that the cleaved form of C1QBP (14 kDa) is upregulated in colon cancer compared with normal cells, which is consistent with previous reports of the pro-tumorigenic properties of C1QBP (5,6,8). Rubinstein et al (8) compared the C1QBP protein levels among several adenocarcinomas. Immunohistochemical staining of histological tissue sections revealed pronounced differences in the expression in colon adenocarcinoma (as well as thyroid, pancreatic, gastric, esophageal and lung cancer) vs. non-malignant tissues. Dembitzer et al (6) revealed strong C1QBP expression in epithelial breast, prostate, liver, lung, colon and skin tumors. However, increased C1QBP staining was also detected in inflammatory and proliferative lesions of the same cell types, as well as in normal and continuously dividing cells. Moreover, McGee et al (5) reported that C1QBP expression was upregulated in breast, colon and lung cancer compared with normal control tissues. Altogether, these data indicate that C1QBP is important in colon cancer tumorigenicity.

A novel observation of the present study is that C1QBP interacts with ApoA-I. Among the many candidate-binding proteins identified, ApoA-I was selected for confirmation because it has a relatively well-established role in colon cancer. The lipid metabolism is closely associated with cancer (21,22). In particular, it has been speculated that lipids and lipoproteins are associated with neoplastic processes, including inflammation, oxidative stress and insulin resistance (23). Moreover, ApoA-I is a major component of high-density lipoprotein in plasma, which exerts protective anti-inflammatory, anti-oxidant and anti-microbial functions, and it is important in innate immunity (21). ApoA-I is synthesized primarily in the liver (80%) and small intestine (10%) (24), and it is known to be important in reverse cholesterol transport and for promoting cholesterol efflux from tissues by acting as a cofactor for lecithin cholesterol acyltransferase (24). In a study of a cohort of >520,000 participants from 10 European countries, high serum concentrations of HDL and ApoA-I were associated with a decreased risk of colon cancer (23). In addition, HDL mimetics inhibited tumor development in both induced and spontaneous mouse models of colon cancer, possibly by inhibiting angiogenesis (21). Zhang et al (25) analyzed the lipid levels of 206 patients with colorectal cancer, 70 patients with benign colorectal disease, and 300 healthy participants, and revealed that serum ApoA-I and ApoB levels were significantly lower in colorectal cancer patients (25). In addition to colon cancer, ApoA-I inhibited tumor development in a mouse model of ovarian cancer (26). Significantly decreased serum levels of ApoA-I were found in patients with cholangiocarcinoma (27), and increased levels in serum were associated with a favorable prognosis in patients with metastatic nasopharyngeal carcinoma (28). These anti-tumor properties of ApoA-I may be associated with its binding to and subsequent inhibition of C1QBP. As such, HDL has received attention as a promising therapeutic strategy for colon cancer. A novel finding in the present study, that C1QBP binds to ApoA-I, may assist the future development of such therapeutic strategies.

Nevertheless, the physiological role of the interaction between ApoA1 and C1QBP requires further investigation. Furthermore, one contradictory study indicated that the expression of ApoA-I was associated with colon adenocarcinoma progression, and that ApoA-I is a potential marker of tumor aggression (29). However, the novel observations in the present study may facilitate identification of the molecular mechanisms underlying the roles of ApoA-I and C1QBP in colon cancer.

Acknowledgements

The present study was supported by the Soonchunhyang University Research Fund.

References

1 

Chowdhury AR, Ghosh I and Datta K: Excessive reactive oxygen species induces apoptosis in fibroblasts: Role of mitochondrially accumulated hyaluronic acid binding protein 1 (HABP1/p32/gC1qR). Exp Cell Res. 314:651–667. 2008. View Article : Google Scholar : PubMed/NCBI

2 

Majumdar M, Meenakshi J, Goswami SK and Datta K: Hyaluronan binding protein 1 (HABP1)/C1QBP/p32 is an endogenous substrate for MAP kinase and is translocated to the nucleus upon mitogenic stimulation. Biochem Biophys Res Commun. 291:829–837. 2002. View Article : Google Scholar : PubMed/NCBI

3 

Ghebrehiwet B and Peerschke EI: cC1q-R (calreticulin) and gC1q-R/p33: Ubiquitously expressed multi-ligand binding cellular proteins involved in inflammation and infection. Mol Immunol. 41:173–183. 2004. View Article : Google Scholar : PubMed/NCBI

4 

Tahtouh M, Garçon-Bocquet A, Croq F, Vizioli J, Sautière PE, van Camp C, Salzet M, Nagnan-le Meillour P, Pestel J and Lefebvre C: Interaction of HmC1q with leech microglial cells: Involvement of C1qBP-related molecule in the induction of cell chemotaxis. J Neuroinflammation. 9:372012. View Article : Google Scholar : PubMed/NCBI

5 

McGee AM, Douglas DL, Liang Y, Hyder SM and Baines CP: The mitochondrial protein C1qbp promotes cell proliferation, migration and resistance to cell death. Cell Cycle. 10:4119–4127. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Dembitzer FR, Kinoshita Y, Burstein D, Phelps RG, Beasley MB, Garcia R, Harpaz N, Jaffer S, Thung SN, Unger PD, et al: gC1qR expression in normal and pathologic human tissues: Differential expression in tissues of epithelial and mesenchymal origin. J Histochem Cytochem. 60:467–474. 2012. View Article : Google Scholar : PubMed/NCBI

7 

Zhang X, Zhang F, Guo L, Wang Y, Zhang P, Wang R, Zhang N and Chen R: Interactome analysis reveals that C1QBP (complement component 1, q subcomponent binding protein) is associated with cancer cell chemotaxis and metastasis. Mol Cell Proteomics. 12:3199–3209. 2013. View Article : Google Scholar : PubMed/NCBI

8 

Rubinstein DB, Stortchevoi A, Boosalis M, Ashfaq R, Ghebrehiwet B, Peerschke EI, Calvo F and Guillaume T: Receptor for the globular heads of C1q (gC1q-R, p33, hyaluronan-binding protein) is preferentially expressed by adenocarcinoma cells. Int J Cancer. 110:741–750. 2004. View Article : Google Scholar : PubMed/NCBI

9 

Chen YB, Jiang CT, Zhang GQ, Wang JS and Pang D: Increased expression of hyaluronic acid binding protein 1 is correlated with poor prognosis in patients with breast cancer. J Surg Oncol. 100:382–386. 2009. View Article : Google Scholar : PubMed/NCBI

10 

Yu H, Liu Q, Xin T, Xing L, Dong G, Jiang Q, Lv Y, Song X, Teng C, Huang D, et al: Elevated expression of hyaluronic acid binding protein 1 (HABP1)/P32/C1QBP is a novel indicator for lymph node and peritoneal metastasis of epithelial ovarian cancer patients. Tumour Biol. 34:3981–3987. 2013. View Article : Google Scholar : PubMed/NCBI

11 

Amamoto R, Yagi M, Song Y, Oda Y, Tsuneyoshi M, Naito S, Yokomizo A, Kuroiwa K, Tokunaga S, Kato S, et al: Mitochondrial p32/C1QBP is highly expressed in prostate cancer and is associated with shorter prostate-specific antigen relapse time after radical prostatectomy. Cancer Sci. 102:639–647. 2011. View Article : Google Scholar : PubMed/NCBI

12 

Itahana K and Zhang Y: Mitochondrial p32 is a critical mediator of ARF-induced apoptosis. Cancer Cell. 13:542–553. 2008. View Article : Google Scholar : PubMed/NCBI

13 

Sunayama J, Ando Y, Itoh N, Tomiyama A, Sakurada K, Sugiyama A, Kang D, Tashiro F, Gotoh Y, Kuchino Y and Kitanaka C: Physical and functional interaction between BH3-only protein Hrk and mitochondrial pore-forming protein p32. Cell Death Differ. 11:771–781. 2004. View Article : Google Scholar : PubMed/NCBI

14 

Meenakshi J, Goswami SK Anupama and Datta K: Constitutive expression of hyaluronan binding protein 1 (HABP1/p32/gC1qR) in normal fibroblast cells perturbs its growth characteristics and induces apoptosis. Biochem Biophys Res Commun. 300:686–693. 2003. View Article : Google Scholar : PubMed/NCBI

15 

Kamal A and Datta K: Upregulation of hyaluronan binding protein 1 (HABP1/p32/gC1qR) is associated with Cisplatin induced apoptosis. Apoptosis. 11:861–874. 2006. View Article : Google Scholar : PubMed/NCBI

16 

Hosseinimehr SJ, Nobakht R, Ghasemi A and Pourfallah TA: Radioprotective effect of mefenamic acid against radiation-induced genotoxicity in human lymphocytes. Radiat Oncol J. 33:256–260. 2015. View Article : Google Scholar : PubMed/NCBI

17 

Han S, Bui NT, Ho MT, Kim YM, Cho M and Shin DB: Dexamethasone inhibits TGF-β1-induced cell migration by regulating the ERK and AKT pathways in human colon cancer cells via CYR61. Cancer Res Treat. 48:1141–1153. 2016. View Article : Google Scholar : PubMed/NCBI

18 

Kim ST, Park KH, Kim JS, Shin SW and Kim YH: Impact of KRAS mutation status on outcomes in metastatic colon cancer patients without anti-epidermal growth factor receptor therapy. Cancer Res Treat. 45:55–62. 2013. View Article : Google Scholar : PubMed/NCBI

19 

Lee JH, Kim KH, Park JW, Chang HJ, Kim BC, Kim SY, Kim KG, Lee ES, Kim DY, Oh JH, et al: Low-mass-ion discriminant equation: A new concept for colorectal cancer screening. Int J Cancer. 134:1844–1853. 2014. View Article : Google Scholar : PubMed/NCBI

20 

Kim KH, Yeo SG, Kim WK, Kim DY, Yeo HY, Hong JP, Chang HJ, Park JW, Kim SY, Kim BC and Yoo BC: Up-regulated expression of l-caldesmon associated with malignancy of colorectal cancer. BMC Cancer. 12:6012012. View Article : Google Scholar : PubMed/NCBI

21 

Su F, Grijalva V, Navab K, Ganapathy E, Meriwether D, Imaizumi S, Navab M, Fogelman AM, Reddy ST and Farias-Eisner R: HDL mimetics inhibit tumor development in both induced and spontaneous mouse models of colon cancer. Mol Cancer Ther. 11:1311–1319. 2012. View Article : Google Scholar : PubMed/NCBI

22 

Cho O, Hwang HS, Lee BS, Oh YT, Kim CH and Chun M: Met inactivation by S-allylcysteine suppresses the migration and invasion of nasopharyngeal cancer cells induced by hepatocyte growth factor. Radiat Oncol J. 33:328–336. 2015. View Article : Google Scholar : PubMed/NCBI

23 

van Duijnhoven FJ, Bueno-De-Mesquita HB, Calligaro M, Jenab M, Pischon T, Jansen EH, Frohlich J, Ayyobi A, Overvad K, Toft-Petersen AP, et al: Blood lipid and lipoprotein concentrations and colorectal cancer risk in the European prospective investigation into cancer and nutrition. Gut. 60:1094–1102. 2011. View Article : Google Scholar : PubMed/NCBI

24 

Halley P, Kadakkuzha BM, Faghihi MA, Magistri M, Zeier Z, Khorkova O, Coito C, Hsiao J, Lawrence M and Wahlestedt C: Regulation of the apolipoprotein gene cluster by a long noncoding RNA. Cell Rep. 6:222–230. 2014. View Article : Google Scholar : PubMed/NCBI

25 

Zhang X, Zhao XW, Liu DB, Han CZ, Du LL, Jing JX and Wang Y: Lipid levels in serum and cancerous tissues of colorectal cancer patients. World J Gastroenterol. 20:8646–8652. 2014. View Article : Google Scholar : PubMed/NCBI

26 

Su F, Kozak KR, Imaizumi S, Gao F, Amneus MW, Grijalva V, Ng C, Wagner A, Hough G, Farias-Eisner G, et al: Apolipoprotein A-I (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc Natl Acad Sci USA. 107:19997–20002. 2010. View Article : Google Scholar : PubMed/NCBI

27 

Wang X, Dai S, Zhang Z, Liu L, Wang J, Xiao X, He D and Liu B: Characterization of apolipoprotein A-I as a potential biomarker for cholangiocarcinoma. Eur J Cancer Care (Engl). 18:625–635. 2009. View Article : Google Scholar : PubMed/NCBI

28 

Jiang R, Yang ZH, Luo DH, Guo L, Sun R, Chen QY, Huang PY, Qiu F, Zou X, Cao KJ, et al: Elevated apolipoprotein A-I levels are associated with favorable prognosis in metastatic nasopharyngeal carcinoma. Med Oncol. 31:802014. View Article : Google Scholar : PubMed/NCBI

29 

Tachibana M, Ohkura Y, Kobayashi Y, Sakamoto H, Tanaka Y, Watanabe J, Amikura K, Nishimura Y and Akagi K: Expression of apolipoprotein A1 in colonic adenocarcinoma. Anticancer Res. 23:4161–4167. 2003.PubMed/NCBI

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May-2017
Volume 13 Issue 5

Print ISSN: 1792-0981
Online ISSN:1792-1015

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Spandidos Publications style
Kim K, Kim MJ, Kim KH, Ahn SA, Kim JH, Cho JY and Yeo SG: C1QBP is upregulated in colon cancer and binds to apolipoprotein A-I. Exp Ther Med 13: 2493-2500, 2017
APA
Kim, K., Kim, M., Kim, K., Ahn, S., Kim, J.H., Cho, J.Y., & Yeo, S. (2017). C1QBP is upregulated in colon cancer and binds to apolipoprotein A-I. Experimental and Therapeutic Medicine, 13, 2493-2500. https://doi.org/10.3892/etm.2017.4249
MLA
Kim, K., Kim, M., Kim, K., Ahn, S., Kim, J. H., Cho, J. Y., Yeo, S."C1QBP is upregulated in colon cancer and binds to apolipoprotein A-I". Experimental and Therapeutic Medicine 13.5 (2017): 2493-2500.
Chicago
Kim, K., Kim, M., Kim, K., Ahn, S., Kim, J. H., Cho, J. Y., Yeo, S."C1QBP is upregulated in colon cancer and binds to apolipoprotein A-I". Experimental and Therapeutic Medicine 13, no. 5 (2017): 2493-2500. https://doi.org/10.3892/etm.2017.4249