Involvement of the Stress Protein HSP47 in Procollagen Processing in the Endoplasmic Reticulum

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1992 May 1

PMID 1577863

Citations 54

Authors

A Nakai

M Satoh

K HIRAYOSHI

K Nagata

Affiliations

Soon will be listed here.

Abstract

The 47,000-D collagen-binding glycoprotein, heat shock protein 47 (HSP47), is a stress-inducible protein localized in the ER of collagen-secreting cells. The location and collagen-binding activity of this protein led to speculation that HSP47 might participate in collagen processing. Chemical crosslinking studies were used to test this hypothesis both before and after the perturbation of procollagen processing. The association of procollagen with HSP47 was demonstrated using cleavable bifunctional crosslinking reagents. HSP47 and procollagen were shown to be coprecipitated by the treatment of intact cells with anti-HSP47 or with anticollagen antibodies. Furthermore, several proteins residing in the ER were noted to be crosslinked to and coprecipitated with HSP47, suggesting that these ER-resident proteins may form a large complex in the ER. When cells were heat shocked, or when stable triple-helix formation was inhibited by treatment with alpha,alpha'-dipyridyl, coprecipitation of procollagen with HSP47 was increased. This increase was due to the inhibition of procollagen secretion and to the accumulation of procollagen in the ER. Pulse label and chase experiments revealed that coprecipitated procollagen was detectable as long as procollagen was present in the endoplasmic reticulum of alpha,alpha'-dipyridyl-treated cells. Under normal growth conditions, coprecipitated procollagen was observed to decrease after a chase period of 10-15 min, whereas total procollagen decreased only after 20-25 min. In addition, the intracellular association between HSP47 and procollagen was shown to be disrupted by a change in physiological pH, suggesting that the dissociation of procollagen from HSP47 is pH dependent. These findings support a specific role for HSP47 in the intracellular processing of procollagen, and provide evidence of a new category of "molecular chaperones" in terms of its substrate specificity and the dissociation mechanism.

Citing Articles

High-Temperature Stress Effect on the Red Cusk-Eel () Liver: Transcriptional Modulation and Oxidative Stress Damage.

Dettleff P, Zuloaga R, Fuentes M, Gonzalez P, Aedo J, Estrada J Biology (Basel). 2022; 11(7).

PMID: 36101373 PMC: 9312335. DOI: 10.3390/biology11070990.

Context Matters: Response Heterogeneity to Collagen-Targeting Approaches in Desmoplastic Cancers.

Fuller A, Eisinger-Mathason T Cancers (Basel). 2022; 14(13).

PMID: 35804902 PMC: 9264969. DOI: 10.3390/cancers14133132.

Collagen transport and related pathways in Osteogenesis Imperfecta.

Claeys L, Storoni S, Eekhoff M, Elting M, Wisse L, Pals G Hum Genet. 2021; 140(8):1121-1141.

PMID: 34169326 PMC: 8263409. DOI: 10.1007/s00439-021-02302-2.

Preoperative heat shock protein 47 levels identify colorectal cancer patients with lymph node metastasis and poor prognosis.

Mori K, Toiyama Y, Okugawa Y, Ichikawa T, Nagano Y, Oki S Oncol Lett. 2020; 20(6):333.

PMID: 33123244 PMC: 7583735. DOI: 10.3892/ol.2020.12196.

Exogenous supply of Hsp47 triggers fibrillar collagen deposition in skin cell cultures in vitro.

Khan E, Sankaran S, Llontop L, Del Campo A BMC Mol Cell Biol. 2020; 21(1):22.

PMID: 32228452 PMC: 7106624. DOI: 10.1186/s12860-020-00267-0.

References

Tartakoff A . Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 1983; 32(4):1026-8. DOI: 10.1016/0092-8674(83)90286-6. View

JUVA K, Prockop D, Cooper G, LASH J . Hydroxylation of proline and the intracellular accumulation of a polypeptide precursor of collagen. Science. 1966; 152(3718):92-4. DOI: 10.1126/science.152.3718.92. View

BAINTON D . The discovery of lysosomes. J Cell Biol. 1981; 91(3 Pt 2):66s-76s. PMC: 2112804. DOI: 10.1083/jcb.91.3.66s. View

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

Jimenez S, Yankowski R . Role of molecular conformation on secretion of chick tendon procollagen. J Biol Chem. 1978; 253(5):1420-6. View

Miller E . Isolation and characterization of a collagen from chick cartilage containing three identical alpha chains. Biochemistry. 1971; 10(9):1652-9. DOI: 10.1021/bi00785a024. View

Woods C, Lazarides E . Degradation of unassembled alpha- and beta-spectrin by distinct intracellular pathways: regulation of spectrin topogenesis by beta-spectrin degradation. Cell. 1985; 40(4):959-69. DOI: 10.1016/0092-8674(85)90356-3. View

Roth R, Pierce S . In vivo cross-linking of protein disulfide isomerase to immunoglobulins. Biochemistry. 1987; 26(14):4179-82. DOI: 10.1021/bi00388a001. View

Dorner A, Bole D, Kaufman R . The relationship of N-linked glycosylation and heavy chain-binding protein association with the secretion of glycoproteins. J Cell Biol. 1987; 105(6 Pt 1):2665-74. PMC: 2114744. DOI: 10.1083/jcb.105.6.2665. View

10.

Gething M, McCammon K, Sambrook J . Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 1986; 46(6):939-50. DOI: 10.1016/0092-8674(86)90076-0. View

11.

Kreis T, Lodish H . Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell. 1986; 46(6):929-37. PMC: 7133264. DOI: 10.1016/0092-8674(86)90075-9. View

12.

Nagata K, Yamada K . Phosphorylation and transformation sensitivity of a major collagen-binding protein of fibroblasts. J Biol Chem. 1986; 261(16):7531-6. View

13.

Saga S, Nagata K, Chen W, Yamada K . pH-dependent function, purification, and intracellular location of a major collagen-binding glycoprotein. J Cell Biol. 1987; 105(1):517-27. PMC: 2114926. DOI: 10.1083/jcb.105.1.517. View

14.

Lee W, Conrad D . The murine lymphocyte receptor for IgE. III. Use of chemical cross-linking reagents to further characterize the B lymphocyte Fc epsilon receptor. J Immunol. 1985; 134(1):518-25. View

15.

Kassenbrock C, Garcia P, Walter P, Kelly R . Heavy-chain binding protein recognizes aberrant polypeptides translocated in vitro. Nature. 1988; 333(6168):90-3. DOI: 10.1038/333090a0. View

16.

Bole D, Hendershot L, Kearney J . Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986; 102(5):1558-66. PMC: 2114236. DOI: 10.1083/jcb.102.5.1558. View

17.

Murakami H, Pain D, Blobel G . 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria. J Cell Biol. 1988; 107(6 Pt 1):2051-7. PMC: 2115641. DOI: 10.1083/jcb.107.6.2051. View

18.

Lippincott-Schwartz J, Bonifacino J, Yuan L, Klausner R . Degradation from the endoplasmic reticulum: disposing of newly synthesized proteins. Cell. 1988; 54(2):209-20. DOI: 10.1016/0092-8674(88)90553-3. View

19.

Nakai A, HIRAYOSHI K, Saga S, Yamada K, Nagata K . The transformation-sensitive heat shock protein (hsp47) binds specifically to Fetuin. Biochem Biophys Res Commun. 1989; 164(1):259-64. DOI: 10.1016/0006-291x(89)91711-7. View

20.

Rothman J . Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 1989; 59(4):591-601. DOI: 10.1016/0092-8674(89)90005-6. View