Overexpression of hyaluronan-binding protein 1 (HABP1/p32/gC1qR) in HepG2 cells leads to increased hyaluronan synthesis and cell proliferation by up-regulation of cyclin D1 in AKT-dependent pathway

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19750-19764

  Kaul, Rachna ^a,b   Saha, Paramita ^a   Saradhi, Mallampati ^b   Prasad, Ramachandra L A ^a   Chatterjee, Soumya ^a   Ghosh, Ilora ^a   Tyagi, Rakesh K ^b   Datta, Kasturi ^a  

^a School of Environmental Sciences   (India)

^b JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CABLE STRUCTURE; CELL SURVIVAL; CELL-CELL ADHESION; CELLULAR SIGNALING; CELLULAR STRESS; CYCLIND1; HEPG2 CELLS; HUMAN LIVER CANCER CELLS; HYALURONAN SYNTHESIS; HYALURONAN-BINDING PROTEINS; MAP KINASE; MITOCHONDRIAL DYSFUNCTION; MULTIFUNCTIONAL PROTEIN; MURINE FIBROBLASTS; OVER-EXPRESSION; PHENOTYPIC CHANGES; PROMOTER ACTIVITIES; REACTIVE OXYGEN SPECIES; TUMORIGENICITY; UP-REGULATION;

CABLES; CELL ADHESION; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CHEMICAL ACTIVATION; PROTEINS;

BIOSYNTHESIS;

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN D1; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HERMES ANTIGEN; HYALURONAN BINDING PROTEIN 1; HYALURONIC ACID; HYALURONIC ACID BINDING PROTEIN; HYALURONIC ACID SYNTHASE 2; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SYNTHETASE; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

AKT GENE; APOPTOSIS; ARTICLE; CANCER GROWTH; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CARCINOGENICITY; CELL ADHESION; CELL GROWTH; CELL PROLIFERATION; CELL STIMULATION; CELL STRAIN HEPG2; CELL STRESS; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; CYCLIN D1 GENE; ENZYME ACTIVATION; GENE; GENE ACTIVATION; GENE ACTIVITY; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UPREGULATION;

ANIMALS; ANTIGENS, CD44; CARRIER PROTEINS; CELL ADHESION; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN D1; ENZYME ACTIVATION; GLUCURONOSYLTRANSFERASE; HEP G2 CELLS; HUMANS; HYALURONIC ACID; MITOCHONDRIAL PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RABBITS; UP-REGULATION;

MURINAE;

EID: 84861740638     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.266270     Document Type: Article

References (49)

1. Toole, B. P., Zoltan-Jones, A., Misra, S., and Ghatak, S. (2005) Hyaluronan. Acritical component of epithelial-mesenchymal and epithelial-carcinoma transitions. Cells Tissues Organs 179, 66-72 (Pubitemid 40976290)
2. D'Souza, M., and Datta, K. (1985) Evidence for naturally occurring hyaluronic acid binding protein in rat liver. Biochem. Int. 10, 43-51 (Pubitemid 15164141)
3. Gupta, S., and Datta, K. (1991) Possible role of hyaluronectin on cell adhesion in rat histiocytoma. Exp. Cell Res. 195, 386-394 (Pubitemid 121006338)
4. Krainer, A. R., Mayeda, A., Kozak, D., and Binns, G. (1991) Functional expression of cloned human splicing factor SF2. Homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66, 383-394 (Pubitemid 121001375)
5. Deb, T. B., and Datta, K. (1996) Molecular cloning of human fibroblast hyaluronic acid-binding protein confirms its identity with P-32, a protein co-purified with splicing factor SF2. J. Biol. Chem. 271, 2206-2212
6. Ghebrehiwet, B., Lim, B. L., Peerschke, E. I., Willis, A. C., and Reid, K. B. (1994) Isolation, cDNA cloning, and overexpression of a 33-kDa cell surface glycoprotein that binds to the globular "heads" of C1q. J. Exp. Med. 179, 1809-1821
7. Majumdar, M., and Datta, K. (1998) Assignment of cDNA encoding hyaluronic acid-binding protein 1 to human chromosome 17p12-p13. Genomics 51, 476-477 (Pubitemid 28413218)
8. Honoré, B., Madsen, P., Rasmussen, H. H., Vandekerckhove, J., Celis, J. E., and Leffers, H. (1993) Cloning and expression of a cDNA covering the complete coding region of the P32 subunit of human pre-mRNA splicing factor SF2. Gene 134, 283-287
9. Jiang, J., Zhang, Y., Krainer, A. R., and Xu, R. M. (1999) Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc. Natl. Acad. Sci. U.S.A. 96, 3572-3577 (Pubitemid 29168951)
10. Jha, B. K., Salunke, D. M., and Datta, K. (2003) Structural flexibility of multifunctional HABP1 may be important for regulating its binding to different ligands. J. Biol. Chem. 278, 27464-27472
11. van Leeuwen, H. C., and O'Hare, P. (2001) Retargeting of the mitochondrial protein p32/gC1Qr to a cytoplasmic compartment and the cell surface. J. Cell Sci. 114, 2115-2123
12. Majumdar, M., Meenakshi, J., Goswami, S. K., and Datta, K. (2002) 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 (Pubitemid 34694350)
13. Meenakshi, J., Anupama, Goswami, S. K., and Datta, K. (2003) 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
14. Sengupta, A., Tyagi, R. K., and Datta, K. (2004) Truncated variants of hyaluronan-binding protein 1 bind hyaluronan and induce identical morphological aberrations in COS-1 cells. Biochem. J. 380, 837-844 (Pubitemid 38850526)
15. Chowdhury, A. R., Ghosh, I., and Datta, K. (2008) 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
16. Murakami, C., Hirakawa, Y., Inui, H., Nakano, Y., and Yoshida, H. (2002) Effects of epigallocatechin 3-O-gallate on cellular antioxidative system in HepG2 cells. J. Nutr. Sci. Vitaminol. (Tokyo) 48, 89-94 (Pubitemid 34733438)
17. Kongtawelert, P., and Ghosh, P. (1990) A method for the quantitation of hyaluronan (hyaluronic acid) in biological fluids using a labeled avidinbiotin technique. Anal. Biochem. 185, 313-318 (Pubitemid 20107169)
18. Bhilocha, S., Amin, R., Pandya, M., Yuan, H., Tank, M., LoBello, J., Shytuhina, A., Wang, W., Wisniewski, H. G., de la Motte, C., and Cowman, M. K. (2011) Agarose and polyacrylamide gel electrophoresis methods for molecular mass analysis of 5- to 500-kDa hyaluronan. Anal. Biochem. 417, 41-49
19. Tammi, R., MacCallum, D., Hascall, V. C., Pienimäki, J. P., Hyttinen, M., and Tammi, M. (1998) Hyaluronan bound to CD44 on keratinocytes is displaced by hyaluronan decasaccharides and not hexasaccharides. J. Biol. Chem. 273, 28878-28888 (Pubitemid 28507580)
20. Sironen, R. K., Tammi, M., Tammi, R., Auvinen, P. K., Anttila, M., and Kosma, V. M. (2008) Hyaluronan in human malignancies. Exp. Cell Res. 317, 383-391
21. Itano, N., and Kimata, K. (2008) Altered hyaluronan biosynthesis in cancer progression. Semin. Cancer Biol. 18, 268-274
22. Ponta, H., Sherman, L., and Herrlich, P. A. (2003) CD44. From adhesion molecules to signaling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45 (Pubitemid 36077255)
23. Kothapalli, D., Flowers, J., Xu, T., Puré, E., and Assoian, R. K. (2008) Differential activation of ERK and Rac mediates the proliferative and antiproliferative effects of hyaluronan and CD44. J. Biol. Chem. 283, 31823-31829
24. Serbulea, M., Kakumu, S., Thant, A. A., Miyazaki, K., Machida, K., Senga, T., Ohta, S., Yoshioka, K., Hotta, N., and Hamaguchi, M. (1999) Hyaluronan activates mitogen-activated protein kinase via Ras-signaling pathway. Int. J. Oncol. 14, 733-738
25. Lv, H., Yu, G., Sun, L., Zhang, Z., Zhao, X., and Chai, W. (2007) Elevated level of glycosaminoglycans and altered sulfation pattern of chondroitin sulfate are associated with differentiation status and histological type of human primary hepatic carcinoma. Oncology 72, 347-356 (Pubitemid 351238149)
26. Krasiński, R., Tchórzewski, H., and Lewkowicz, P. (2009) Antioxidant effect of hyaluronan on polymorphonuclear leukocyte-derived reactive oxygen species is dependent on its molecular weight and concentration and mainly involves the extracellular space. Postepy. Hig. Med. Dosw. 63, 205-212
27. Shaw, J. P., and Chou, I. (1986) Elevation of intracellular glutathione content associated with mitogenic stimulation of quiescent fibroblasts. J. Cell. Physiol. 129, 193-198 (Pubitemid 17179562)
28. Hamilos, D. L., Zelarney, P., and Mascali, J. J. (1989) Lymphocyte proliferation in glutathione-depleted lymphocytes. Direct relationship between glutathione availability and the proliferative response. Immunopharmacology 18, 223-235 (Pubitemid 20010029)
29. Misra, S., Hascall, V. C., Berger, F. G., Markwald, R. R., and Ghatak, S. (2008) Hyaluronan, CD44, and cyclooxygenase-2 in colon cancer. Connect. Tissue Res. 49, 219-224
30. Turley, E. A., Noble, P. W., and Bourguignon, L. Y. (2002) Signaling properties of hyaluronan receptors. J. Biol. Chem. 277, 4589-4592 (Pubitemid 34968484)
31. Prehm, P. (2006) Biosynthesis of hyaluronan. Direction of chain elongation. Biochem. J. 398, 469-473
32. Tammi, R. H., Kultti, A., Kosma, V. M., Pirinen, R., Auvinen, P., and Tammi, M. I. (2008) Hyaluronan in human tumors. Pathobiological and prognostic messages from cell-associated and stromal hyaluronan. Semin. Cancer Biol. 18, 288-295
33. Itano, N., and Kimata, K. (2002) Mammalian hyaluronan synthases. IUBMB Life 54, 195-199 (Pubitemid 36008328)
34. Spicer, A. P., and Tien, J. Y. (2004) Hyaluronan and morphogenesis. Birth Defects Res. C Embryo Today 72, 89-108 (Pubitemid 38456573)
35. Koyama, H., Hibi, T., Isogai, Z., Yoneda, M., Fujimori, M., Amano, J., Kawakubo, M., Kannagi, R., Kimata, K., Taniguchi, S., and Itano, N. (2007) Hyperproduction of hyaluronan in neu-induced mammary tumor accelerates angiogenesis through stromal cell recruitment. Possible involvement of versican/PG-M. Am. J. Pathol. 170, 1086-1099 (Pubitemid 47339375)
36. Kosaki, R., Watanabe, K., and Yamaguchi, Y. (1999) Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenicity. Cancer Res. 59, 1141-1145 (Pubitemid 29135978)
37. Itano, N., Sawai, T., Atsumi, F., Miyaishi, O., Taniguchi, S., Kannagi, R., Hamaguchi, M., and Kimata, K. (2004) Selective expression and functional characteristics of three mammalian hyaluronan synthases in oncogenic malignant transformation. J. Biol. Chem. 279, 18679-18687 (Pubitemid 38623291)
38. Simpson, M. A. (2006) Concurrent expression of hyaluronan biosynthetic and processing enzymes promotes growth and vascularization of prostate tumors in mice. Am. J. Pathol. 169, 247-257
39. Bourguignon, L. Y., Zhu, H., Shao, L., and Chen, Y. W. (2000) CD44 interaction with tiam1 promotes Rac1 signaling and hyaluronic acid-mediated breast tumor cell migration. J. Biol. Chem. 275, 1829-1838 (Pubitemid 30060806)
40. Lee, R. J., Albanese, C., Stenger, R. J., Watanabe, G., Inghirami, G., Haines, G. K., 3rd, Webster, M., Muller, W. J., Brugge, J. S., Davis, R. J., and Pestell, R. G. (1999) pp60(v-src) induction of cyclin D1 requires collaborative interactions between the extracellular signal-regulated kinase, p38, and Jun kinase pathways. A role for cAMP response element-binding protein and activating transcription factor-2 in pp60 (v-src) signaling in breast cancer cells. J. Biol. Chem. 274, 7341-7350
41. Nakagawa, H., Wang, T. C., Zukerberg, L., Odze, R., Togawa, K., May, G. H., Wilson, J., and Rustgi, A. K. (1997) The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and stomach. Oncogene 14, 1185-1190 (Pubitemid 27141920)
42. Robles, A. I., Rodriguez-Puebla, M. L., Glick, A. B., Trempus, C., Hansen, L., Sicinski, P., Tennant, R. W., Weinberg, R. A., Yuspa, S. H., and Conti, C. J. (1998) Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev. 12, 2469-2474 (Pubitemid 28406950)
43. Ghosh, I., Chowdhury, A. R., Rajeswari, M. R., and Datta, K. (2004) Differential expression of hyaluronic acid binding protein (HABP1/p32/ C1QBP) during progression of epidermal carcinoma. Mol. Cell. Biochem. 267, 133-139 (Pubitemid 39562393)
44. Rubinstein, D. B., Stortchevoi, A., Boosalis, M., Ashfaq, R., Ghebrehiwet, B., Peerschke, E. I., Calvo, F., and Guillaume, T. (2004) 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 (Pubitemid 38746033)
45. Fogal, V., Zhang, L., Krajewski, S., and Ruoslahti, E. (2008) Mitochondrial/cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res. 68, 7210-7218
46. de La Motte, C. A., Hascall, V. C., Calabro, A., Yen-Lieberman, B., and Strong, S. A. (1999) Mononuclear leukocytes preferentially bind via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(I-C). J. Biol. Chem. 274, 30747-30755
47. Evanko, S. P., Tammi, M. I., Tammi, R. H., and Wight, T. N. (2007) Hyaluronan-dependent pericellular matrix. Adv. Drug. Deliv. Rev. 59, 1351-1365 (Pubitemid 350088257)
48. Ren, J., Hascall, V. C., and Wang, A. (2009) Cyclin D3 mediates synthesis of a hyaluronan matrix that is adhesive for monocytes in mesangial cells stimulated to divide in hyperglycemic medium. J. Biol. Chem. 284, 16621-16632
49. Kobayashi, N., Miyoshi, S., Mikami, T., Koyama, H., Kitazawa, M., Takeoka, M., Sano, K., Amano, J., Isogai, Z., Niida, S., Oguri, K., Okayama, M., McDonald, J. A., Kimata, K., Taniguchi, S., and Itano, N. (2010) Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res. 70, 7073-7083