Lysyl hydroxylase 3 is secreted from cells by two pathways

Journal of Cellular Physiology

Volumn 227, Issue 2, 2012, Pages 668-675

  Wang, Chunguang ^a   Ristiluoma, Marja Maija ^a   Salo, Antti M ^a   Eskelinen, Sinikka ^b   Myllylä, Raili ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; CHOLESTEROL; GLUCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; LYSYL HYDROXYLASE 3; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; EXTRACELLULAR SPACE; GENE MUTATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALS; BREFELDIN A; CELL LINE; CELL MEMBRANE; CHOLESTEROL; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GOLGI APPARATUS; HUMANS; MUTATION; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; PROTEIN STRUCTURE, TERTIARY;

EID: 82155181728     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22774     Document Type: Article

References (37)

1. Anelli T, Sitia R. 2008. Protein quality control in the early secretory pathway. EMBO J 27: 315-327.
2. Balcarova-Ständer J, Pfeiffer SE, Fuller SD, Simons K. 1984. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J 3: 2687-2694.
3. Baldwin TA, Ostergaard HL. 2002. The protein-tyrosine phosphatase CD45 reaches the cell surface via Golgi-dependent and -independent pathways. J Biol Chem 277: 50333-50340.
4. Fujiwara T, Oda K, Yokata S, Takatsuki A, Ikehara Y. 1988. Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J Biol Chem 263: 18545-19552.
5. Hautala T, Byers MG, Eddy RL, Shows TB, Kivirikko KI, Myllylä R. 1992. Cloning of human lysyl hydroxylase: Complete cDNA-derived amino acid sequence and assignment of the gene (PLOD) to chromosome 1p36.3--p36.2. Genomics 13: 62-69.
6. Heikkinen J, Risteli M, Wang C, Latvala J, Rossi M, Valtavaara M, Myllylä R. 2000. Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J Biol Chem 275: 36158-36163.
7. Heino S, Lusa S, Somerharju P, Ehnholm C, Olkkonen VM, Ikonen E. 2000. Dissecting the role of the Golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. Proc Natl Acad Sci USA 97: 8375-8380.
8. Kellokumpu S, Sormunen R, Heikkinen J, Myllylä R. 1994. Lysyl hydroxylase, a collagen processing enzyme, exemplifies a novel class of luminally-oriented peripheral membrane proteins in the endoplasmic reticulum. J Biol Chem 269: 30524-30529.
9. Kielty CM, Hopkinson I, Grant ME. 1993. Collagen: The collagen family: Structure, assembly, and organization in the extracellular matrix. In: Royce PM, Steinmann PM, editors. Connective tissue and its heritable disorders. New York: Wiley-Liss. pp 103-147.
10. Kivirikko KI, Myllylä R. 1982. Posttranslational enzymes in the biosynthesis of collagen: Intracellular enzymes. Methods Enzymol 82: 245-304.
11. Kivirikko KI, Myllylä R, Pihlajaniemi T. 1992. Hydroxylation of proline and lysine residues in collagens and other animal and plant proteins. In: Harding JJ, Grabbe MJC, editors. Post-translational modifications of proteins. Boca Raton, FL: CRC Press, Inc. pp 1-51.
12. Munro S, Pelham HR. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899-907.
13. Myllylä R, Risteli L, Kivirikko KI. 1975. Assay of collagen-galactosyltransferase and collagen-glucosyltransferase activities and preliminary characterization of enzymic reactions with transferases from chick-embryo cartilage. Eur J Biochem 52: 401-410.
14. Myllylä R, Pihlajaniemi T, Pajunen L, Turpeenniemi T, Kivirikko KI. 1991. Molecular cloning of chick lysyl hydroxylase. Little homology in primary structure to the two types of subunit of prolyl 4-hydroxylase. J Biol Chem 266: 2805-2810.
15. Myllylä R, Wang C, Heikkinen J, Juffer A, Lampela O, Risteli M, Ruotsalainen H, Salo A, Sipilä L. 2007. Expanding the lysyl hydroxylase toolbox: New insights into the localization and activities of lysyl hydroxylase 3 (LH3). J Cell Physiol 212: 323-329.
16. Nickel W, Rabouille C. 2009. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 10: 148-155.
17. Passoja K, Myllyharju J, Pirskanen A, Kivirikko KI. 1998a. Identification of arginine-700 as the residue that binds the C-5 carboxyl group of 2-oxoglutarate in human lysyl hydroxylase 1. FEBS Lett 434: 145-148.
18. Passoja K, Rautavuoma K, Ala-Kokko L, Kosonen T, Kivirikko KI. 1998b. Cloning and characterization of a third human lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95: 10482-10486.
19. Radisky DC, Stallings-Mann M, Hirai Y, Bissell MJ. 2009. Single proteins might have dual but related functions in intracellular and extracellular microenvironments. Nat Rev Mol Cell Biol 10: 228-234.
20. Risteli M, Ruotsalainen H, Salo AM, Sormunen R, Sipilä L, Baker NL, Lamande S, Vimpari-Kauppinen L, Myllylä R. 2009. Reduction of lysyl hydroxylase 3 causes deleterious changes in the deposition and organization of extracellular matrix. J Biol Chem 284: 28204-28211.
21. Ruotsalainen H, Sipilä L, Kerkelä E, Pospiech H, Myllylä R. 1999. Characterization of cDNAs for mouse lysyl hydroxylase 1, 2 and 3, their phylogenetic analysis and tissue-specific expression in the mouse. Matrix Biol 18: 325-329.
22. Ruotsalainen H, Sipilä L, Vapola M, Sormunen R, Salo AM, Uitto L, Mercer DK, Robins SP, Risteli M, Aszodi A, Fässler R, Myllylä R. 2005. Lysyl hydroxylase 3 (LH3) catalyzed glycosylation is essential for basement membranes. J Cell Sci 119: 625-635.
23. Salo AM, Sipilä L, Sormunen R, Ruotsalainen H, Vainio S, Myllylä R. 2006a. The lysyl hydroxylase isoforms are widely expressed during mouse embryogenesis, but obtain tissue- and cell-specific patterns in the adult. Matrix Biol 25: 475-483.
24. Salo AM, Wang C, Sipilä L, Sormunen R, Vapola M, Kervinen P, Ruotsalainen H, Heikkinen J, Myllylä R. 2006b. Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J Cell Physiol 207: 644-653.
25. Salo AM, Cox H, Farndon P, Moss C, Grindulis H, Risteli M, Robins SP, Myllylä R. 2008. A connective tissue disorder caused by mutations of the lysyl hydroxylase 3 gene. Am J Hum Genet 83: 495-503.
26. Sipilä L, Ruotsalainen H, Sormunen R, Baker NL, Lamande SR, Vapola M, Wang C, Sado Y, Aszodi A, Myllylä R. 2007. Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines. J Biol Chem 282: 33381-33388.
27. Suokas M, Myllylä R, Kellokumpu S. 2000. A single C-terminal peptide segment mediates both membrane association and localization of lysyl hydroxylase in the endoplasmic reticulum. J Biol Chem 275: 17863-17868.
28. Suokas M, Lampela O, Juffer AH, Myllylä R, Kellokumpu S. 2003. Retrieval-independent localization of lysyl hydroxylase in the endoplasmic reticulum via a peptide fold in its iron-binding domain. Biochem J 370: 913-920.
29. Tveit H, Akslen LK, Fagereng GL, Tranulis MA, Prydz K. 2009. A secretory Golgi bypass route to the apical surface domain of epithelial MDCK cells. Traffic 10: 1685-1695.
30. Valtavaara M, Papponen H, Pirttila AM, Hiltunen K, Helander H, Myllylä R. 1997. Cloning and characterization of a novel human lysyl hydroxylase isoform highly expressed in pancreas and muscle. J Biol Chem 272: 6831-6834.
31. Valtavaara M, Szpirer C, Szpirer J, Myllylä R. 1998. Primary structure, tissue distribution, and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 273: 12881-12886.
32. van Vliet C, Thomas EC, Merino-Trigo A, Teasdale RD, Gleeson PA. 2003. Intracellular sorting and transport of proteins. Prog Biophys Mol Biol 83: 1-45.
33. Wang C, Valtavaara M, Myllylä R. 2000. Lack of collagen type specificity for lysyl hydroxylase isoforms. DNA Cell Biol 19: 71-77.
34. Wang C, Luosujarvi H, Heikkinen J, Risteli M, Uitto L, Myllylä R. 2002a. The third activity for lysyl hydroxylase 3: Galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21: 559-566.
35. Wang C, Risteli M, Heikkinen J, Hussa AK, Uitto L, Myllylä R. 2002b. Identification of amino acids important for the catalytic activity of the collagen glucosyltransferase associated with the multifunctional lysyl hydroxylase 3 (LH3). J Biol Chem 277: 18568-18573.
36. Wang Y, Lam KS, Yau MH, Xu A. 2008. Post-translational modifications of adiponectin: Mechanisms and functional implications. Biochem J 409: 623-633.
37. Wang C, Kovanen V, Raudasoja P, Eskelinen S, Pospiech H, Myllylä R. 2009. The glycosyltransferase activities of lysyl hydroxylase 3 (LH3) in the extracellular space are important for cell growth and viability. J Cell Mol Med 13: 508-521.