Heat shock protein 47: A novel biomarker of phenotypically altered collagen-producing cells

Acta Histochemica et Cytochemica

Volumn 44, Issue 2, 2011, Pages 35-41

  Taguchi, Takashi ^a   Nazneen, Arifa ^a   Al Shihri, Abdulmonem A ^b   Turkistani, Khadijah A ^b   Razzaque, Mohammed S ^a,b  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Biomarker; Collagen; Fibrosis; HSP47

Indexed keywords

EID: 79955753038     PISSN: 00445991     EISSN: 13475800     Source Type: Journal    
DOI: 10.1267/ahc.11001     Document Type: Review

References (75)

1. Azouz, A., Razzaque, M. S., El-Hallak, M. and Taguchi, T. (2004) Immunoinflammatory responses and fibrogenesis. Med. Electron Microsc. 37; 141-148.
2. Ball, E. H., Jain, N. and Sanwal, B. D. (1997) Colligin, a collagen binding serpin. Adv. Exp. Med. Biol. 425; 239-245.
3. Becker, J. and Craig, E. A. (1994) Heat-shock proteins as molecular chaperones. Eur. J. Biochem. 219; 11-23.
4. Brown, K. E., Broadhurst, K. A., Mathahs, M. M., Brunt, E. M. and Schmidt, W. N. (2005) Expression of HSP47, a collagenspecific chaperone, in normal and diseased human liver. Lab. Invest. 85; 789-797.
5. Cheng, M., Razzaque, M. S., Nazneen, A. and Taguchi, T. (1998) Expression of the heat shock protein 47 in gentamicin-treated rat kidneys. Int. J. Exp. Pathol. 79; 125-132.
6. Endo, T. and Yamano, K. (2009) Multiple pathways for mitochondrial protein traffic. Biol. Chem. 390; 723-730.
7. Grone, H. J., Weber, K., Grone, E., Helmchen, U. and Osborn, M. (1987) Coexpression of keratin and vimentin in damaged and regenerating tubular epithelia of the kidney. Am. J. Pathol. 129; 1-8.
8. Hartl, F. U. and Hayer-Hartl, M. (2009) Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16; 574-581.
9. Hendrick, J. P. and Hartl, F. U. (1993) Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62; 349-384.
10. Hisanaga, Y., Nakashima, K., Tsuruga, E., Nakatomi, Y., Hatakeyama, Y., Ishikawa, H. and Sawa, Y. (2009) Fibulin-5 contributes to microfibril assembly in human periodontal ligament cells. Acta Histochem. Cytochem. 42; 151-157.
11. Kaur, J., Rao, M., Chakravarti, N., Mathur, M., Shukla, N. K., Sanwal, B. D. and Ralhan, R. (2001) Co-expression of colligin and collagen in oral submucous fibrosis: plausible role in pathogenesis. Oral Oncol. 37; 282-287.
12. Kawate, T., Kawamura, R., Uchida, T., Takahashi, K., Hasegawa, T., Futamata, H., Katoh, R. and Takeda, S. (2009) Histochemical analysis of renal dysplasia with ureteral atresia. Acta Histochem. Cytochem. 42; 65-71.
13. Kurkinen, M., Taylor, A., Garrels, J. I. and Hogan, B. L. (1984) Cell surface-associated proteins which bind native type IV collagen or gelatin. J. Biol. Chem. 259; 5915-5922.
14. Kuroda, K. and Tajima, S. (2008) Proliferation of HSP47-positive skin fibroblasts in dermatofibroma. J. Cutan. Pathol. 35; 21-26.
15. Liu, D., Nazneen, A., Taguchi, T. and Razzaque, M. S. (2008) Low-dose local kidney irradiation inhibits progression of experimental crescentic nephritis by promoting apoptosis. Am. J. Nephrol. 28; 555-568.
16. Liu, D., Razzaque, M. S., Cheng, M. and Taguchi, T. (2001) The renal expression of heat shock protein 47 and collagens in acute and chronic experimental diabetes in rats. Histochem. J. 33; 621-628.
17. Liu, D., Razzaque, M. S., Nazneen, A., Naito, T. and Taguchi, T. (2002) Role of heat shock protein 47 on tubulointerstitium in experimental radiation nephropathy. Pathol. Int. 52; 340-347.
18. Mallick, S. (2008) Outcome of patients with idiopathic pulmonary fibrosis (IPF) ventilated in intensive care unit. Respir. Med. 102; 1355-1359.
19. Martelli-Junior, H., Cotrim, P., Graner, E., Sauk, J. J. and Coletta, R. D. (2003) Effect of transforming growth factor-beta1, interleukin-6 and interferon-gamma on the expression of type I collagen, heat shock protein 47, matrix metalloproteinase (MMP)-1 and MMP-2 by fibroblasts from normal gingiva and hereditary gingival fibromatosis. J. Periodontol. 74; 296-306.
20. Masuda, H., Fukumoto, M., Hirayoshi, K. and Nagata, K. (1994) Coexpression of the collagen-binding stress protein HSP47 gene and the alpha 1(I) and alpha 1(III) collagen genes in carbon tetrachloride-induced rat liver fibrosis. J. Clin. Invest. 94; 2481-2488.
21. Nagata, K. (1996) Hsp47: a collagen-specific molecular chaperone. Trends Biochem. Sci. 21; 22-26.
22. Nagata, K. (2003) HSP47 as a collagen-specific molecular chaperone: function and expression in normal mouse development. Semin. Cell Dev. Biol. 14; 275-282.
23. Nagata, K. and Hosokawa, N. (1996) Regulation and function of collagen-specific molecular chaperone, HSP47. Cell Struct. Funct. 21; 425-430.
24. Nagle, R. B., Kneiser, M. R., Bulger, R. E. and Benditt, E. P. (1973) Induction of smooth muscle characteristics in renal interstitial fibroblasts during obstructive nephropathy. Lab. Invest. 29; 422-427.
25. Naitoh, M., Hosokawa, N., Kubota, H., Tanaka, T., Shirane, H., Sawada, M., Nishimura, Y. and Nagata, K. (2001) Upregulation of HSP47 and collagen type III in the dermal fibrotic disease, keloid. Biochem. Biophys. Res. Commun. 280; 1316-1322.
26. Nakai, A., Satoh, M., Hirayoshi, K. and Nagata, K. (1992) Involvement of the stress protein HSP47 in procollagen processing in the endoplasmic reticulum. J. Cell Biol. 117; 903-914.
27. Nakatani, T., Bara, S., Ohnishi, M., Densmore, M. J., Taguchi, T., Goetz, R., Mohammadi, M., Lanske, B. and Razzaque, M. S. (2009) In vivo genetic evidence of klotho-dependent functions of FGF23 in regulation of systemic phosphate homeostasis. FASEB J. 23; 433-441.
28. Nakatani, T., Ohnishi, M. and Razzaque, M. S. (2009) Inactivation of klotho function induces hyperphosphatemia even in presence of high serum fibroblast growth factor 23 levels in a genetically engineered hypophosphatemic (Hyp) mouse model. FASEB J. 23; 3702-3711.
29. Ogawa, Y., Razzaque, M. S., Kameyama, K., Hasegawa, G., Shimmura, S., Kawai, M., Okamoto, S., Ikeda, Y., Tsubota, K., Kawakami, Y. and Kuwana, M. (2007) Role of heat shock protein 47, a collagen-binding chaperone, in lacrimal gland pathology in patients with cGVHD. Invest. Ophthalmol. Vis. Sci. 48; 1079-1086.
30. Ohnishi, M., Nakatani, T., Lanske, B. and Razzaque, M. S. (2009) In vivo genetic evidence for suppressing vascular and soft-tissue calcification through the reduction of serum phosphate levels, even in the presence of high serum calcium and 1,25- Dihydroxyvitamin D levels. Circ. Cardiovasc. Genet. 2; 583-590.
31. Ohnishi, M. and Razzaque, M. S. (2010) Dietary and genetic evidence for phosphate toxicity accelerating mammalian aging. FASEB J. 24; 3562-3571.
32. Razzaque, M. S. (2009) FGF23-mediated regulation of systemic phosphate homeostasis: is Klotho an essential player? Am. J. Physiol. Renal Physiol. 296; F470-476.
33. Razzaque, M. S. (2010) The dualistic role of vitamin D in vascular calcifications. Kidney Int. doi:10.1038/ki.2010.432
34. Razzaque, M. S. and Ahmed, A. R. (2002) Collagens, collagenbinding heat shock protein 47 and transforming growth factorbeta 1 are induced in cicatricial pemphigoid: possible role(s) in dermal fibrosis. Cytokine 17; 311-316.
35. Razzaque, M. S., Ahmed, B. S., Foster, C. S. and Ahmed, A. R. (2003) Effects of IL-4 on conjunctival fibroblasts: possible role in ocular cicatricial pemphigoid. Invest. Ophthalmol. Vis. Sci. 44; 3417-3423.
36. Razzaque, M. S., Azouz, A., Shinagawa, T. and Taguchi, T. (2003) Factors regulating the progression of hypertensive nephrosclerosis. Contrib. Nephrol. 139; 173-186.
37. Razzaque, M. S., Foster, C. S. and Ahmed, A. R. (2003) Role of collagen-binding heat shock protein 47 and transforming growth factor-beta1 in conjunctival scarring in ocular cicatricial pemphigoid. Invest. Ophthalmol. Vis. Sci. 44; 1616-1621.
38. Razzaque, M. S., Foster, C. S. and Ahmed, A. R. (2003) Role of connective tissue growth factor in the pathogenesis of conjunctival scarring in ocular cicatricial pemphigoid. Invest. Ophthalmol. Vis. Sci. 44; 1998-2003.
39. Razzaque, M. S., Hossain, M. A., Kohno, S. and Taguchi, T. (1998) Bleomycin-induced pulmonary fibrosis in rat is associated with increased expression of collagen-binding heat shock protein (HSP) 47. Virchows Arch. 432; 455-460.
40. Razzaque, M. S., Koji, T., Harada, T. and Taguchi, T. (1999) Localization in situ of type VI collagen protein and its mRNA in mesangial proliferative glomerulonephritis using renal biopsy sections. Histochem. Cell Biol. 111; 1-6.
41. Razzaque, M. S., Koji, T., Kawano, H., Harada, T., Nakane, P. K. and Taguchi, T. (1994) Glomerular expression of type III and type IV collagens in benign nephrosclerosis: immunohistochemical and in situ hybridization study. Pathol. Res. Pract. 190; 493-499.
42. Razzaque, M. S., Koji, T., Taguchi, T., Harada, T. and Nakane, P. K. (1994) In situ localization of type III and type IV collagenexpressing cells in human diabetic nephropathy. J. Pathol. 174; 131-138.
43. Razzaque, M. S., Kumari, S., Foster, C. S. and Ahmed, A. R. (2003) Expression profiles of collagens, HSP47, TGF-beta1, MMPs and TIMPs in epidermolysis bullosa acquisita. Cytokine 21; 207-213.
44. Razzaque, M. S., Kumatori, A., Harada, T. and Taguchi, T. (1998) Coexpression of collagens and collagen-binding heat shock protein 47 in human diabetic nephropathy and IgA nephropathy. Nephron 80; 434-443.
45. Razzaque, M. S., Le, V. T. and Taguchi, T. (2005) Heat shock protein 47 and renal fibrogenesis. Contrib. Nephrol. 148; 57-69.
46. Razzaque, M. S., Nazneen, A. and Taguchi, T. (1998) Immunolocalization of collagen and collagen-binding heat shock protein 47 in fibrotic lung diseases. Mod. Pathol. 11; 1183-1188.
47. Razzaque, M. S., Shimokawa, I., Nazneen, A., Higami, Y. and Taguchi, T. (1998) Age-related nephropathy in the Fischer 344 rat is associated with overexpression of collagens and collagenbinding heat shock protein 47. Cell Tissue Res. 293; 471-478.
48. Razzaque, M. S., Shimokawa, I., Nazneen, A., Liu, D., Naito, T., Higami, Y. and Taguchi, T. (1999) Life-long dietary restriction modulates the expression of collagens and collagen-binding heat shock protein 47 in aged Fischer 344 rat kidney. Histochem. J. 31; 123-132.
49. Razzaque, M. S., St-Arnaud, R., Taguchi, T. and Lanske, B. (2005) FGF-23, vitamin D and calcification: the unholy triad. Nephrol. Dial. Transplant. 20; 2032-2035.
50. Razzaque, M. S. and Taguchi, T. (1997) Collagen-binding heat shock protein (HSP) 47 expression in anti-thymocyte serum (ATS)-induced glomerulonephritis. J. Pathol. 183; 24-29.
51. Razzaque, M. S. and Taguchi, T. (1999) The possible role of colligin/HSP47, a collagen-binding protein, in the pathogenesis of human and experimental fibrotic diseases. Histol. Histopathol. 14; 1199-1212.
52. Razzaque, M. S. and Taguchi, T. (1999) Role of glomerular epithelial cell-derived heat shock protein 47 in experimental lipid nephropathy. Kidney Int. Suppl. 71; S256-259.
53. Razzaque, M. S. and Taguchi, T. (2002) Cellular and molecular events leading to renal tubulointerstitial fibrosis. Med. Electron Microsc. 35; 68-80.
54. Razzaque, M. S. and Taguchi, T. (2003) Pulmonary fibrosis: Cellular and molecular events. Pathol. Int. 53; 133-145.
55. Ritossa, F. M. (1962) A new puffing pattern Induced by temperature shock and DNP in Drosophila. Experientia 18; 571-573.
56. Sakamoto, A., Murata, K., Suzuki, H., Yatabe, M. and Kikuchi, M. (2008) Immunohistochemical observation of co-expression of E- and N-cadherins in rat organogenesis. Acta Histochem. Cytochem. 41; 143-147.
57. Satoh, M., Hirayoshi, K., Yokota, S., Hosokawa, N. and Nagata, K. (1996) Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen. J. Cell Biol. 133; 469-483.
58. Sauk, J. J., Nikitakis, N. and Siavash, H. (2005) Hsp47 a novel collagen binding serpin chaperone, autoantigen and therapeutic target. Front. Biosci. 10; 107-118.
59. Sunamoto, M., Kuze, K., Tsuji, H., Ohishi, N., Yagi, K., Nagata, K., Kita, T. and Doi, T. (1998) Antisense oligonucleotides against collagen-binding stress protein HSP47 suppress collagen accumulation in experimental glomerulonephritis. Lab. Invest. 78; 967-972.
60. Taguchi, T., Nazneen, A., Abid, M. R. and Razzaque, M. S. (2005) Cisplatin-associated nephrotoxicity and pathological events. Contrib. Nephrol. 148; 107-121.
61. Taguchi, T. and Razzaque, M. S. (2007) The collagen-specific molecular chaperone HSP47: is there a role in fibrosis? Trends Mol. Med. 13; 45-53.
62. Takeda, K., Kusachi, S., Ohnishi, H., Nakahama, M., Murakami, M., Komatsubara, I., Oka, T., Doi, M., Ninomiya, Y. and Tsuji, T. (2000) Greater than normal expression of the collagen-binding stress protein heat-shock protein-47 in the infarct zone in rats after experimentally-induced myocardial infarction. Coron. Artery Dis. 11; 57-68.
63. Tamaki, K. and Okuda, S. (2003) Role of TGF-beta in the progression of renal fibrosis. Contrib. Nephrol. 139; 44-65.
64. Tasab, M., Batten, M. R. and Bulleid, N. J. (2000) Hsp47: a molecular chaperone that interacts with and stabilizes correctlyfolded procollagen. EMBO J. 19; 2204-2211.
65. Tasab, M., Jenkinson, L. and Bulleid, N. J. (2002) Sequencespecific recognition of collagen triple helices by the collagenspecific molecular chaperone HSP47. J. Biol. Chem. 277; 35007-35012.
66. Walsh, D., Li, Z., Wu, Y. and Nagata, K. (1997) Heat shock and the role of the HSPs during neural plate induction in early mammalian CNS and brain development. Cell. Mol. Life Sci. 53; 198-211.
67. Wells, R. G. (2000) Fibrogenesis. V. TGF-beta signaling pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 279; G845-850.
68. Wells, R. G. (2009) Liver fibrosis: challenges of the new era. Gastroenterology 136; 387-388.
69. Wilson, M. S. and Wynn, T. A. (2009) Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol. 2; 103-121.
70. Yamamura, I., Hirata, H., Hosokawa, N. and Nagata, K. (1998) Transcriptional activation of the mouse HSP47 gene in mouse osteoblast MC3T3-E1 cells by TGF-beta 1. Biochem. Biophys. Res. Commun. 244; 68-74.
71. Yang, S. F., Tsai, C. H. and Chang, Y. C. (2008) The upregulation of heat shock protein 47 expression in human buccal fibroblasts stimulated with arecoline. J. Oral Pathol. Med. 37; 206-210.
72. Zha, Y., Le, V. T., Higami, Y., Shimokawa, I., Taguchi, T. and Razzaque, M. S. (2006) Life-long suppression of growth hormoneinsulin- like growth factor I activity in genetically altered rats could prevent age-related renal damage. Endocrinology 147; 5690-5698.
73. Zha, Y., Taguchi, T., Nazneen, A., Shimokawa, I., Higami, Y. and Razzaque, M. S. (2008) Genetic suppression of GH-IGF-1 activity, combined with lifelong caloric restriction, prevents agerelated renal damage and prolongs the life span in rats. Am. J. Nephrol. 28; 755-764.
74. Zhang, K., Gharaee-Kermani, M., McGarry, B. and Phan, S. H. (1994) In situ hybridization analysis of rat lung alpha 1(I) and alpha 2(I) collagen gene expression in pulmonary fibrosis induced by endotracheal bleomycin injection. Lab. Invest. 70; 192-202.
75. Zhang, K., Rekhter, M. D., Gordon, D. and Phan, S. H. (1994) Myofibroblasts and their role in lung collagen gene expression during pulmonary fibrosis. A combined immunohistochemical and in situ hybridization study. Am. J. Pathol. 145; 114-125.